REVIEWARTICLE

Integrated management of damping-off diseases A review

Jay Ram Lamichhane1 amp Carolyne Duumlrr2 amp Andreacute A Schwanck3ampMarie-Heacutelegravene Robin4

amp

Jean-Pierre Sarthou5amp Vincent Cellier6 amp Antoine Messeacutean1

amp Jean-Noeumll Aubertot3

Accepted 8 February 2017 Published online 16 March 2017 INRA and Springer-Verlag France 2017

Abstract Damping-off is a disease that leads to the decay ofgerminating seeds and young seedlings which represents forfarmers one of the most important yield constraints both innurseries and fields As for other biotic stresses conventionalfungicides are widely used to manage this disease with twomajor consequences On the one hand fungicide overusethreatens the human health and causes ecological concernsOn the other hand this practice has led to the emergence ofpesticide-resistant microorganisms in the environment Thusthere are increasing concerns to develop sustainable and du-rable damping-off management strategies that are less relianton conventional pesticides Achieving such a goal requires abetter knowledge of pathogen biology and disease epidemiol-ogy in order to facilitate the decision-making process It alsodemands using all available non-chemical tools that can beadapted to regional and specific production situations

However this still is not the case and major knowledge gapsmust be filled Here we review up to 300 articles of thedamping-off literature in order to highlight major knowledgegaps and identify future research priorities Themajor findingsare (i) damping-off is an emerging disease worldwide whichaffects all agricultural and forestry crops both in nurseries andfields (ii) over a dozen of soil-borne fungi and fungus-likeorganisms are a cause of damping-off but only a few of themare frequently associated with the disease (iii) damping-offmay affect from 5 to 80 of the seedlings thereby inducingheavy economic consequences for farmers (iv) a lot of re-search efforts have been made in recent years to develop bio-control solutions for damping-off and there are interestingfuture perspectives and (v) damping-off management re-quires an integrated pest management (IPM) approach com-bining both preventive and curative tactics and strategiesGiven the complex nature of damping-off and the numerousfactors involved in its occurrence we recommend further re-search on critical niches of complexity such as seeds seed-bed associated microbes and their interfaces using novel androbust experimental and modeling approaches based on fiveresearch priorities described in this paper

Keywords Abiotic stresses Best management practices

Economic losses Integrated pestmanagement Interactions

Seed germination Seedling decay Soil-borne pathogens

Contents1 Introduction2 Symptoms of damping-off

21 Pre-emergence symptoms22 Post-emergence symptoms23 Occurrence of damping-off symptoms

Jay Ram Lamichhanejayramlamichhanegmailcom Jay-RamLamichhaneinrafr

1 INRA Eco-Innov Research Unit Avenue Lucien BreacutetigniegraveresF-78850 Thiverval-Grignon France

2 INRA IRHS 1345 42 rue George MorelF-49071 Beaucouzeacute France

3 INRA UMR AGIR 1248 24 chemin de BorderougendashAuzevilleF-31320 Castanet-Tolosan France

4 Universiteacute de Toulouse INPT EI-Purpan UMR AGIR 1248 24chemin de BorderougendashAuzevilleF-31320 Castanet-Tolosan France

5 Universiteacute de Toulouse INPT ENSAT UMR AGIR 1248 24chemin de BorderougendashAuzevilleF-31320 Castanet-Tolosan France

6 INRA Domaine expeacuterimental drsquoEpoisses UE 0115F-21110 Breteniegravere France

Agron Sustain Dev (2017) 37 10DOI 101007s13593-017-0417-y

3 Integrated management of damping-off31 Seed treatment to enhance germination and seed-

ling vigor32 Deployment of host-plant resistance andor toler-

ance33 Adoption of best cropping practices34 Timely treatment interventions of seedlings with

effective products341 Biological control342 Chemical control

4 Key challenges and future priorities for damping-offmanagement

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anasto-mosis groups

42 Determination of potential interactions within andor between damping-off pathogens and other liv-ing organisms

43 A better knowledge of the role of abiotic factorsthat predispose seeds and seedlings to damping-offdiseases

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

45 Modeling to help design integrated managementstrategies of damping-off diseases

5 Conclusions and perspectivesAcknowledgementsReferences

1 Introduction

Damping-off is a historical term coined during the early nine-teenth century and represents one of the oldest worldwidenursery problems as discussed in detail in the classic nurserymanual (Hartley and Pierce 1917 Tillotson 1917 Hartley1921) Damping-off was considered ldquothe most serious prob-lem encountered in raising nursery seedlingsrdquo and conse-quently was one of the most focused research subject sincethe beginning of its description (Hartley and Pierce 1917) Thedefinition of damping-off is not straightforward in the litera-ture Many authors refer to damping-off as a ldquodiseaserdquo(McNew 1960 Horst 2013) while others refer to damping-off as a ldquosymptomatic conditionrdquo (Agrios 2005 Kemerait andVidhyasekaran 2006) In the former case damping-off is usu-ally associated to soil-borne pathogens while in the latter caseseed-borne pathogens can promote damping-off Nevertheless both interpretations comprehend that damping-off involves non-germination prevention of seedling emer-gence after germination or the rotting and collapse of seed-lings at the soil level

Overall damping-off can be caused by a number of bioticor abiotic stressesfactors which prevent seeds to germinate orseedlings to emerge including those caused by plant-pathogenic bacteria or insect pests notably those living in soilsuch as Delia spp Agriotes spp or Melolontha spp (Fig 1)As a consequence the symptoms associated with damping-offwidely vary depending on the type of stress associated with itand time of its occurrence In general many fungi and fungi-like species (Table 1) have been reported as the most impor-tant biotic stress weakening or destroying seeds and seedlingsof almost all species including fruit vegetable field ornamen-tal and forestry crops (Filer and Peterson 1975 Kraft et al2000) However this paper will focus on damping-off causedby Fusarium spp Rhizoctonia spp Pythium spp andPhytophthora spp since these pathogens are the most fre-quently associated with damping-off and are considered themost important causal agents of this problem in the literature(Table 1) Furthermore the role of abiotic stresses will be alsodiscussed as they indirectly affect damping-off occurrenceFavorable abiotic conditions for damping-off problems gener-ally involve excessive soil moisture and excessive overheadmisting lower soil temperatures before emergence higher soiltemperatures after emergence and overcrowded flats or seed-beds (Wright 1957 Papavizas and Davey 1961 Duniway1983a James 2012a Starkey and Enebak 2012)

In recent years numerous soil-borne fungi belonging toover a dozen of genera and oomycetes (Pythium andPhytophthora) and some seed-borne fungi have been report-ed to cause damping-off on a large number of crops (Table 1)Most of these pathogens are common in agricultural soils andcan be spread via non-anthropic and anthropic activities in-cluding water run-off through irrigation or rain (Zappia et al2014) soil contamination by improperly sanitized tools intro-duction of infected plants (mainly in case of seed-borne path-ogens) improperly sanitized greenhouse and the use of con-taminated irrigation water (Papavizas and Davey 1961Duniway 1983b Schmitthenner and Canaday 1983 Huangand Kuhlman 1990 James 2012a Starkey and Enebak2012) Once established damping-off pathogens are able tosurvive for many years in the soil even in the absence of hostplants either as saprophytes or as living resting structures thatare capable of enduring adverse conditions (Menzies 1963)Their wide host range also aids in the longevity of these fungiand fungus-like organisms

Despite a long history behind and a number of researchworks conducted on damping-off it still represents one ofthe most difficult problems to be managed both in the nurser-ies and fields There is no country or geographic area withoutdamping-off problems on a number of economically impor-tant crops Indeed since only the beginning of the twenty-firstcentury almost 50 new reports of damping-off diseases havebeen noticed on over 30 crops and from over 20 countries(Table 1) This clearly suggests that damping-off problem is

10 Page 2 of 25 Agron Sustain Dev (2017) 37 10

multifaceted and requires more research efforts to generatefurther knowledge needed for a durable and sustainable man-agement of damping-off

Overall the economic losses due to damping-off arerepresented by a direct cost due to damages of seed orseedlings (Fig 2) and an indirect cost which consistsof an additional cost of replanting and the consequentlower yields due to the later planting dates (Babadoostand Islam 2003 Bacharis et al 2010 Horst 2013)Although there is no detailed and precise estimationabout the real economic impact of damping-off at theglobal level in monetary terms a previous study report-ed that 40 million extra seedlings are planted each yearonly in Georgia (the USA) to counterbalance losses dueto non-viable seeds and damping-off of seedlings(Huang and Kuhlman 1990) Likewise in 2016 inBrittany (France) the grass or cereal fly Geomyzatripunctata damaged thousands of hectares of maizecrops with significant economic losses in the region(BSV 2016) An extensive literature research showedthat the incidence of damping-off may vary from 5 to80 (Table 1)

In addition to a significant economic importance there is aconsiderable environmental impact due to the widespread useof fungicides to manage this frequently occurring problemFor example the methyl bromide seed treatment and fumiga-tion a practice forbidden in the European Union (Mouttetet al 2014) still represents one of the major practices adoptedelsewhere including in the USA to manage damping-off dis-eases (Weiland et al 2013) However following the MontrealProtocol (UNEP 2006) this practice tends to decline and re-strictions for soil fumigation have been increased (Weiland

et al 2013) Nevertheless other conventional fungicides playan increasingly important role in mitigating seed and seedlingdamage caused by damping-off pathogens The frequent useof these fungicides has led to the development of fungicide-resistant isolates with additional challenges for farmers tomanage damping-off (Taylor et al 2002 Moorman et al2002 Lamichhane et al 2016)

In light of the high economic impact of damping-off andnegative environmental effects generated by conventionalfungicide-based control strategies there is a need to developalternative and sustainable solutions to manage damping-offIntegrated pest management (IPM) exemplifies a sustainableapproach to this aim as it combines preventive measures (egenhancement of seed health which represents the core of re-silient agroecosystems) as well as best agronomic and culturalpractices first and pesticide-based tactics as the last optionTherefore the objectives of this work were to (i) highlightthe major features of damping-off diseases especially thosecaused by Fusarium spp Rhizoctonia spp Pythium spp andPhytophthora spp (ii) report and discuss currently used dis-ease management strategies and knowledge gaps and (iii)suggest key challenges and future priorities for a sustainablemanagement of damping-off diseases

2 Symptoms of damping-off

Damping-off symptoms can be observed from seeding untilthe fourth to sixth week post-sowing (Horst 2013) The dis-ease symptoms can be divided in two phases based on the timeof its appearance

Fig 1 Damping-off is either adisease of germinating seeds (pre-emergencemdashA) or youngseedlings (post-emergencemdashB)The latter also comprisescotyledon blight While damping-off is usually refereed to diseasescaused by soil-borne fungi oroomycetes a number of abioticstresses may contribute todamping-off symptoms (C)(adapted from Landis (2013)

Agron Sustain Dev (2017) 37 10 Page 3 of 25 10

Tab

le1

Anon-exhaustiv

elisto

fstudieshighlig

htingfirstreportsof

damping-offworldwidesince2001

Con

tinent

Cou

ntry

Occurrence

Typ

eHost

Patho

gen

Incidence(

)Reference

Asia

China

2015

Post-emergence

Oat

Rhizoctonia

solani

AG2ndash1

19(Zhang

etal2015)

2013

Post-emergence

Foxtailm

illet

Rhizoctonia

AG-A

30(O

uet

al2015)

2010

Post-emergence

Sugarbeet

Rhizoctonia

AG-A

20(W

angandWu2012)

2011

Post-emergence

Chinese

cabbage

Alternaria

japonica

ND

(Ren

etal2012)

2010

Post-emergence

Rhodiolasachalinensis

Rhizoctoniasolani

AG-4

HG-II

60(Baiet

al2011)

2003

Post-emergence

Swisschard

Rhizoctonia

solani

AG-4

HGAG-A

80(Yanget

al2007)

2014

Post-emergence

Schisandra

chinensis

Rhizoctonia

solani

AG-4

HG-I

10(O

uet

al2015)

India

2011

Post-emergence

Mexican

marigold

Ceratobasidiumsp

15(Saroj

etal2

013)

Iran

2000

Post-emergence

Sugarbeet

Pythium

spp

ND

(Babai-A

hary

etal2004)

Iraq

2012

Post-emergence

Okra

Phytophthoranicotia

nae

ND

(Matny

2012)

Japan

2005

Pre-em

ergence

Okra

Pythium

ultim

umvarultim

um25

(Kidaet

al2007)

2007

Post-emergence

broccoli

Rhizoctonia

solani

AG-2-2

IVND

(Misaw

aet

al2015)

Malaysia

2010

Post-emergence

Coconut

Marasmielluspalmivorus

ND

(Alm

alikyet

al2012)

Oman

2004ndash2005

Post-emergence

Cucum

ber

Pythium

spp

ND

(Al-Sarsquodietal2007)

Turkey

2009

Post-emergence

Wheat

Rhizoctonia

solani

AG8

ND

(Uumlnaland

Sara

Dolar

2012)

Africa

Algeria

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumequiseti

64ndash77

(Lazreget

al2013a)

2008ndash2010

Pre-

andpost-emergence

Aleppopine

Globisporangium

ultim

umND

(Lazreget

al2013b)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumchlamydosporum

64ndash77

(Lazreget

al2013c)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumredolens

64ndash77

(Lazreget

al2013d)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumacum

inatum

64ndash77

(Lazreget

al2013e)

Benin

2001ndash2002

Post-emergence

Cow

pea

Phomaspand

otherfungal

species

ND

(Adandonon

etal2004)

Egypt

2000

Pre-

andpost-emergence

Wheat

Pythium

diclinum

ND

(Abdelzaher2004)

Europe

Greece

2007

Post-emergence

Cottonandtobacco

Rhizoctonia

spp

ND

(Bachariset

al2010)

Italy

2007

Post-emergence

Bottlebrush

Cylindrocladium

scoparium

30ndash70

(Polizziet

al2007)

2006

Pre-

andpost-emergence

Oak

Cylindrocladiella

parva

65(Scattolin

andMontecchio2007)

2004

Pre-

andpost-emergence

Beech

Fusariumavenaceum

70(M

ontecchio2005)

2010

Post-emergence

Leafbeet

Pythium

aphaniderm

atum

20(G

aribaldi

etal2013)

2011

Post-emergence

strawberrytree

Colletotrichumacutatum

simmondsii

ND

(Polizziet

al2011)

2010

Post-emergence

Pink

ipecirc

Rhizoctonia

solani

AG-4

5(Polizziet

al2010)

2009

Post-emergence

Fanpalm

Rhizoctonia

solani

AG-4

20(Polizziet

al2009)

2007

Post-emergence

African

daisy

Rhizoctonia

solani

AG-4

30(A

iello

etal2008a)

2008

Post-emergence

Lagunariapatersonii

Rhizoctonia

solani

AG-4

20(A

iello

etal2008b)

Netherlands

2005

Post-emergence

Fennel

Alternaria

petroselini

6ndash10

(Pryor

andAsm

a2007)

Spain

2011

Post-emergence

Swisschard

Rhizoctonia

solani

20(Palmeroet

al2012)

2009

Post-emergence

Pinus

radiata

Cylindrocarponpauciseptatum

ND

(Agustiacute-Brisach

etal2011)

NorthCentralAmerica

Canada

2005

Post-emergence

Durum

wheat

Arthriniumsacchari

ND

(Mavragani

etal2007)

Mexico

2014

Post-emergence

Habaneropepper

Phytophthoracapsici

ND

(Saacutenchez-Borgeset

al2015)

USA

2003

Post-emergence

Canola

Rhizoctonia

solani

AG2ndash1

ND

(Paulitzet

al2006)

2007ndash2009

Post-emergence

Soybean

Fusariumcommune

ND

(Elliset

al2012)

2011

Post-emergence

Indian

spinach

Rhizoctonia

solani

10(Liaoet

al2011)

2009

Post-emergence

Pea

Pythium

spp

ND

(Alcalaet

al2016)

1994

Post-emergence

Wild

rice

Pythium

torulosum

ND

(Marcum

andDavis2006)

SouthAmerica

Brazil

2014

Post-emergence

Casuarina

equisetifolia

Fusariumlacertarum

80(Poletto

etal2

015)

Brazil

2008ndash2011

Pre-em

ergence

Rice

Bipolarisoryzae

ND

(Schwanck

etal2015)

Oceania

Australia

1998ndash1999

Post-emergence

Carrot

Alternaria

radicina

47(Coles

andWicks

2003)

10 Page 4 of 25 Agron Sustain Dev (2017) 37 10

21 Pre-emergence symptoms

They occur when seeds decay prior to emergence This canoccur (i) before seed germination or when (ii) the germinatingseeds are killed by biotic stresses while shoot tissues are stillbelow ground (Fig 3 Filer and Peterson 1975 Crous 2002Horst 2013) In the first case seeds become soft rotten andfail to germinate In the second case stems of germinatingseeds are affected with characteristic water-soaked lesionsformed at or below the soil line (Cram 2003 Landis 2013)With the progression of the disease these lesions may darkento reddish-brown brown or black Expanding lesions quicklygirdle young and tender stems Seedlings may wilt and diesoon before emergence In general random pockets of poorseedling emergence are an indication of pre-emergencedamping-off

Abiotic stresses can be divided into two categories chem-ical and physical stress The first notably involves limiting (i)concentrations in carbon dioxide or ethylene (Negm andSmith 1978) (ii) potential of hydrogen (Foy 1984) (iii) os-motic potential (Romo and Haferkamp 1987) and (iv) phyto-toxicity (Wang et al 2001) The second includes (i) extremetemperatures (high or low) (Khan 1977 Wen 2015) extremeseedbed humidity (high or low) (Maraghni et al 2010 Wen2015) and (iii) mechanical stresses such as seedbed clods(Duumlrr and Aubertot 2000) or crusting at the soil surface(Aubertot et al 2002) Other mechanical events such as re-moval of mulch or soil by wind and rain may also contribute

to non-uniform seeding of containers or beds poor seed de-velopment and seed rot and decay (Landis 2013)

a

b

Fig 2 An overview of soybean(a) and pea (b) fields affected bydamping-off diseases due toPythium spp The presence ofempty space along the rowindicates seed or seedlingsaffected by pre- and post-emergence damping-off diseaseswhich killed plants Theeconomic losses in such asituation are severe owing to adirect cost due to damages of seedor seedlings and an indirect costrelated to an additional cost ofreplanting and the consequentlower yields due to the laterplanting dates (Fig 1A is photocourtesy of Martin Chilvers whileFig 1B is photo courtesy ofLindsey J du Toit)

Fig 3 Characteristic symptoms of pre-emergence damping-off of pea(Pisum sativum L) caused by Pythium spp Despite the same sowingdate only the first three seeds on the left have emerged Note non-emerged seeds with or without root development Soft rotten anddecayed seeds prior to germinating or the germinating seeds killed bybiotic stresses while shoot tissues are still below ground arecharacteristic symptoms of pre-emergence damping-off The sixth seedfrom the left had germinated but the stem of germinating seeds wasaffected by the disease with characteristic water-soaked lesions belowthe soil line This led to wilting of the seedling soon after emergence(Photo courtesy of Lindsey J du Toit)

Agron Sustain Dev (2017) 37 10 Page 5 of 25 10

Because biotic and abiotic stresses interact among them itis important to distinguish which of them are associated withthe disease symptoms

22 Post-emergence symptoms

Post-emergence damping-off symptoms occur when seedlingsdecay wilt and die after emergence (Fig 4 Boyce 1961Horst 2013) In most cases all symptoms result in the collapseand death of at least some seedlings in any given seedlingpopulation In the case of soil-borne pathogen there couldbe the death of seedlings in groups in roughly circular patchesand the seedlings may have stem lesions at ground levelSeedling stems can become thin and tough (commonly knownas ldquowirestemrdquo) which often leads to reduced seedling vigorThese symptoms can be also accompanied by leaf spottingand a complete root rot may occur Overall the symptomson the stem of the seedlings include water-soaked sunkenlesion at or slightly below the ground level and sometime alsobelow ground line (ie on the roots) causing the plant to fallover (Wright 1944 Filer and Peterson 1975) Surviving plantsare stunted and affected areas often show uneven growth

Abiotic stresses such as superficial soil heat can also leadto post-emergence seedling symptoms such as whitish lesionswhich are often located only on one side of the stem in theearly growth stage of seedlings (Hartley 1918) Such symp-toms can be distinguished from those caused by biotic stresses

because the damage owing to heat lesions is generallyscattered throughout nurseriesseedbeds which mainly de-pend on patterns of shade and heat buildup (Hartley 1921)while that caused by biotic stresses often occurs in expandingpatches Soil crusting is another important abiotic stress thatoften hinders seedling emergence or leads to stunted seedlinggrowth (Fig 5) Phytotoxicity caused by chemical fungicidesis another abiotic stress The symptoms of phytotoxicity how-ever may vary based on the type of chemical used includingmarginal necrosis chlorotic patches or spots and malformedflowers buds and young leaves (Dole andWilkins 2004) Forexample fungicides based with benzimidazole can cause re-duced plant growth and visual damage in bedding plants(Iersel and Bugbee 1996)

23 Occurrence of damping-off symptoms

Most damping-off diseases present a single sort of symptom(pre- or post-emergence) However both sorts of symptomsare also reported to some extent (Table 1) although the under-lying factors leading to the occurrence of each sort of symp-tom are poorly discussed in the literature The complexity ofdamping-off symptoms result from interactions betweencropping practices and the production situation (Aubertotand Robin 2013) This may explain the relevant lack of infor-mation This complexity involves synergism among damping-off pathogens (Al-Hazmi and Al-Nadary 2015) variation of

Fig 4 Characteristic symptoms of post-emergence damping-off ofsoybean (a and b) and corn (c and d) The succulent tissue of sproutswith aboveground shoots collapsed leading to wilting of some seedlingpopulations Soybean seedlings with stem lesions at ground level and the

death of seedlings in groups (a and b) The presence of an empty spacealong the row between corn seedlings indicates the lack of emergedseedlings due to damping-off disease (c and d) (Photo courtesy ofMartin Chilvers)

10 Page 6 of 25 Agron Sustain Dev (2017) 37 10

symptoms according to environmental conduciveness(Schwanck et al 2015) direct effect of plant density(Burdon and Chilvers 1975) and many other factors whichare very specific for each damping-off symptom For instancethe disease cycle components of damping-off are seldomdiscussed in a broader sense in the literature by comparingdifferent diseases Some factors related to the timemoment ofdisease occurrence and timing of disease cycle componentscould determine whether pre- or post-emergence symptomswill occur In this sense it is possible that for both pre- andpost-emergence damping-off the infection occurs during seedgermination but a longer or shorter incubation period mayimplicate in pre- or post-emergence damping-off In additionthe effect of individual factors involved on the disease pro-cesses from the disease cycle and the host cycle (eg seedgermination) for damping-off symptom development is rare-ly discussed in the literature Taken together several studiesvirtually explore the effect of a given factor (eg temperature)on damping-off diseases intensity (Ben-Yephet and Nelson1999) without specifying whether the factor plays a specificrole on the pathogen (eg organism metabolism) or on thehost (eg slow germination process increases time exposureunderground) Further knowledge on disease cycle featuresand processes would help better understand damping-offsymptom occurrence Although it was out of the focus of thiswork it is worth to mention that from the extensive literaturereview we did not perceive any pattern on the sort ofdamping-off symptom (pre- or post-) according to the regionthe pathogen genus or crop species affected Therefore ameta-analytical approach to test hypotheses associated withdamping-off diseases would be highly valuable to better ex-plain the factors involved in damping-off symptoms

occurrence To this aim the list of damping-off diseases weprovide in Table 1 constitutes a potential starting point

3 Integrated management of damping-off

An effective management of damping-off requires the deploy-ment of a number of strategies which can be classified into thefollowing four major groups (i) seed treatment to enhancegermination and seedling vigor (ii) deployment of resistantor tolerant cultivars to damping-off diseases (iii) adoption ofbest cropping practices and (iv) timely treatment interven-tions of seedlings with effective products (conventional pesti-cides as well as biopesticides andor biocontrol agents) Noneof these strategies is effective in managing damping-off dis-ease when applied individually and thus it requires that all ofthem are combined within the frame of IPM

31 Seed treatment to enhance germination and seedlingvigor

While the use of completely healthy seeds is the most effectivemeans to prevent andor contain damping-off diseases seedsmight not be always free from pathogens and thus wouldbenefit from treatments Even when there is no risk of con-taminated seeds from seed-borne pathogens seed treatmentscan be an effective means to increase seedling emergenceparticularly when done on seeds of low vigor and when theseed coat has been damaged (Mancini and Romanazzi 2014)

Chemical seed treatments still represent a major practice inagriculture to manage damping-off diseases (Rhodes andMyers 1989 Babadoost and Islam 2003 Howell 2007

Fig 5 Lack of sugar beet (Beta vulgaris L) seedlings emergence due tosoil crusting followed by drought The formation of soil crusts on the soilsurface represents a strong mechanical barrier which impedes seedlingsfrom being emerged Overall lack of seed germination and emergence in

such a field is characteristic of abiotic stresses including stunted growth ofseedlings without any necrosis of leaves or stems (Photo courtesy ofCarolyne Duumlrr)

Agron Sustain Dev (2017) 37 10 Page 7 of 25 10

Bradley 2007 Leisso et al 2009 Dorrance et al 2009Rothrock et al 2012 Kandel et al 2016) Several chemicalsincluding bleach hydrogen peroxide ethanol and fungicidescan be applied to remove pathogen inoculum from seed coats(Dumroese and James 2005 Mancini and Romanazzi 2014)Generally chemical treatments are effective but they can alsonegatively affect seed germination and cause phytotoxicity(Axelrood et al 1995 du Toit 2004) besides negative impactsto human health and the environment (Lamichhane et al2016) In addition to chemical treatments physical seed treat-ment can be applied including hot water hot air and electrontreatments (Mancini and Romanazzi 2014) Finally a numberof biological seed treatment methods are being developed andused in recent years with a satisfactory level of damping-offdisease suppression (Table 2)

Because seed germination and emergence are ofteninfluenced by site-specific soil and climate conditionsan in-depth knowledge of a specific site in question is aprerequisite for an effective decision-making process forseed treatments An experiment on pesticide-freeagroecosystems conducted in 2014 across eight experi-mental sites in France with non-treated seeds showedthat the percentage of emergence rates markedly differsfor the same seeds across the sites (Fig 3) In particu-lar while the rate of emergence of soft wheat was100 in the Le Rheu and Grignon sites it was loweracross other sites ranging from 43 in Auzeville to75 in Lusignan (Fig 6) This means that while seedtreatments may result essential across some sites due tounfavorable soil and climatic conditions which are con-ducive to disease development it may not be the casein other areas

32 Deployment of host-plant resistance andor tolerance

Overall host-plant resistance as a management tactic is com-posed of the following two strategies (i) deployment of resis-tant andor tolerant plant varieties which support lower path-ogen populations or better tolerate injury caused by them and(ii) the integration of such varieties with other managementtactics within the frame of IPM Unfortunately for many plantpathogens including those causing damping-off diseases noplant cultivar with measurable resistance is available(Babadoost and Islam 2003) Therefore the only way to betteruse the available crop varieties with tolerance to pathogens isthrough their adequate integration with other disease manage-ment measures Nevertheless insufficient focus has been paidto date to the integration of plant resistance with other IPMtactics and to quantifying the benefits of plant resistance inmulti-tactic IPM programs (Stout and Davis 2009)

On the other hand the breeding approach used to date todevelop resistant andor tolerant crop varieties should berevisited if we want to focus on sustainable crop protectionbased on IPM This is particularly true taking into account thefact that most if not all crop varieties bred to date are basedon a market-driven approach focused on high-yielding andmost profitable crop varieties This trend has boosted adoptionof short rotations or monoculture practices on one hand andignored the potential that minor crops may have for IPM onthe other (Messeacutean et al 2016) The limited range of availableminor crop varieties has been reported as one of the majorobstacles to crop diversification thereby confining certainbeneficial practices such as multiple cropping or intercropping(Enjalbert et al 2016 Messeacutean et al 2016) Therefore breed-ing for IPM should be based on a different approach than the

Table 2 Examples of literature reports highlighting the efficacy of non-chemical seed treatments to suppress damping-off diseases The testedformulations are most often reported to suppress both pre- and post-emergence damping-off although their effectiveness may vary in terms of diseasesuppressiveness

Crop Pathogen Formulationproduct Reference

Alfalfa Pythium spp Mineral seed coating (Samac et al 2014)Canola Pythium spp Rhizosphere bacteria (Bardin et al 2003)Corn Pythium and Fusarium spp Several biocontrol agents (Mao et al 1997 Mao et al 1998)Cotton Pythium spp Enterobacter cloacae and

Erwinia herbicola(Nelson 1988)

Cotton Pythium spp Rhizopus oryzae Trichoderma spp (Howell 2007)Cucumber Pythium ultimum Ethanol extracts of Serratia

marcescens and Trichoderma spp(Roberts et al 2016)

Cucumber Pythium spp Phosphonate (Abbasi and Lazarovits 2005 Abbasi andLazarovits 2006)

Sunflower Rhizoctonia solani Spermine (El-Metwally and Sakr 2010)Lentil pea

sugar beetPythium spp Rhizobium leguminosarum (Bardin et al 2004b Huang and Erickson 2007)

Pea Pythium spp Rhizosphere bacteria (Bardin et al 2003)Safflower Pythium spp Rhizosphere bacteria (Bardin et al 2003)Sesame Soil-borne pathogens Paenibacillus polymyxa (Ryu et al 2006)Sugar beet Pythium spp Rhizosphere bacteria crop straw powders (Bardin et al 2003 Bardin et al 2004a)Tomato and hot pepper Pythium spp Fluorescent Pseudomonads (Ramamoorthy et al 2002)

10 Page 8 of 25 Agron Sustain Dev (2017) 37 10

traditional one given the strategic role of breeding in the com-petitiveness of crops and their adaptation to more diversifiedcropping systems (Enjalbert et al 2016)

33 Adoption of best cropping practices

Once the causal agent of damping-off has been identifiedall available cropping practices could be adapted to dis-courage the development of the pathogen Indeed anytechnique that allows to reduce the time between seedgermination and emergence helps reduce effects of bioticstresses on seedlings Overall many pathogens involvedin damping-off are relatively weak pathogens which re-quire favorable environmental conditions for infection tooccur (Table 1) In addition to the susceptibility of hostand aggressiveness of pathogen populations the severityof damping-off is highly dependent on some critical fac-tors including seedbed preparation soil pH managementseeding date and rate growing density nutrition

irrigation growing environment crop sequence andintercropping cover crops soil residue management soilsolarization and tillage (Table 3) Therefore understand-ing combined effects of abiotic and biotic stresses andfactors influencing them are a prerequisite towards effec-tive IPM strategies of damping-off Once these criticalfactors have been identified which might differ fromone region to another best cropping practices should beput in place and adopted

One of the most important practices that allow to thebest management of damping-off and root diseases is fer-tilization Adequate availability of nutrients in the soil canensure higher vigor with earlier emergence that limit theperiod of time where pathogens can infect seeds and seed-lings during the autotrophic stage In particular the ad-vantages of fertilizer placement on seed germination andseedling emergence have been previously demonstrated(Cook et al 2000) The placement of fertilizers directlyunder or slightly to one side of the seed at the time ofplanting or sowing results in an increased level of seedgermination and emergence (Fig 7) This is because rel-atively immobile nutrients such as phosphorus are notreadily available for plants especially for those specieshaving no or a few lateral roots Therefore field fertiliza-tion where damping-off diseases are important requiresthat the nutrients be made easily accessible to the roots toincrease growth rate Although these nutrients do not al-ways reduce seedling infection they often enhance seedgermination and seedling vigor (Smiley et al 1990Patterson et al 1998) Indeed higher seedling vigor al-lows seedlings to rapidly escape from the soil surfaceeven in the presence of a high soil population density ofthe pathogen(s)

34 Timely treatment interventions of seedlingswith effective products

The strategies described above are mainly of preventive natureas they can be developed and adopted before the occurrence ofdamping-off diseases Once the infection occurs on seedlingsand there is a high risk of epidemic development growershave to attempt for an effective control of the diseaseOverall there are two key measures available for damping-off control as described below

341 Biological control

Because of their adverse effects on human health and theenvironment the use of conventional pesticides includingfungicides has come under increasing public scrutiny inmany countries especially in the European Union(Bourguet and Guillemaud 2016 Lamichhane et al2016) In addition increasing reports of pest resistance

Fig 6 Percentage of seed emergence (non-treated seeds) observed acrossdifferent experimental sites managed under the ldquoRes0Pestrdquo network inFrance in 2014 Res0Pest is a ldquopesticide-freerdquo trial network launched in2011 by the INRACIRAD IPM network to address objectives of theFrench National Action Plan Ecophyto to develop and demonstrate thefeasibility of pesticide-free cropping systems (Deytieux et al 2014) Eightexperimental sites comprised of five arable cropping systems (in brown)and three mixed crophusbandry systems (in green) are ongoing acrossthe sites DW durum wheat SW soft wheat MSW mixed of soft wheatvarieties SB spring barley Different percentages of emergence across theexperimental sites highlight how soil and climate and cropping practicesaffect seed germination and the seedling emergence process throughbiotic and abiotic stress Low percentages of emerged seedlings arehighlighted in red

Agron Sustain Dev (2017) 37 10 Page 9 of 25 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

multifaceted and requires more research efforts to generatefurther knowledge needed for a durable and sustainable man-agement of damping-off

Overall the economic losses due to damping-off arerepresented by a direct cost due to damages of seed orseedlings (Fig 2) and an indirect cost which consistsof an additional cost of replanting and the consequentlower yields due to the later planting dates (Babadoostand Islam 2003 Bacharis et al 2010 Horst 2013)Although there is no detailed and precise estimationabout the real economic impact of damping-off at theglobal level in monetary terms a previous study report-ed that 40 million extra seedlings are planted each yearonly in Georgia (the USA) to counterbalance losses dueto non-viable seeds and damping-off of seedlings(Huang and Kuhlman 1990) Likewise in 2016 inBrittany (France) the grass or cereal fly Geomyzatripunctata damaged thousands of hectares of maizecrops with significant economic losses in the region(BSV 2016) An extensive literature research showedthat the incidence of damping-off may vary from 5 to80 (Table 1)

In addition to a significant economic importance there is aconsiderable environmental impact due to the widespread useof fungicides to manage this frequently occurring problemFor example the methyl bromide seed treatment and fumiga-tion a practice forbidden in the European Union (Mouttetet al 2014) still represents one of the major practices adoptedelsewhere including in the USA to manage damping-off dis-eases (Weiland et al 2013) However following the MontrealProtocol (UNEP 2006) this practice tends to decline and re-strictions for soil fumigation have been increased (Weiland

et al 2013) Nevertheless other conventional fungicides playan increasingly important role in mitigating seed and seedlingdamage caused by damping-off pathogens The frequent useof these fungicides has led to the development of fungicide-resistant isolates with additional challenges for farmers tomanage damping-off (Taylor et al 2002 Moorman et al2002 Lamichhane et al 2016)

In light of the high economic impact of damping-off andnegative environmental effects generated by conventionalfungicide-based control strategies there is a need to developalternative and sustainable solutions to manage damping-offIntegrated pest management (IPM) exemplifies a sustainableapproach to this aim as it combines preventive measures (egenhancement of seed health which represents the core of re-silient agroecosystems) as well as best agronomic and culturalpractices first and pesticide-based tactics as the last optionTherefore the objectives of this work were to (i) highlightthe major features of damping-off diseases especially thosecaused by Fusarium spp Rhizoctonia spp Pythium spp andPhytophthora spp (ii) report and discuss currently used dis-ease management strategies and knowledge gaps and (iii)suggest key challenges and future priorities for a sustainablemanagement of damping-off diseases

2 Symptoms of damping-off

Damping-off symptoms can be observed from seeding untilthe fourth to sixth week post-sowing (Horst 2013) The dis-ease symptoms can be divided in two phases based on the timeof its appearance

Fig 1 Damping-off is either adisease of germinating seeds (pre-emergencemdashA) or youngseedlings (post-emergencemdashB)The latter also comprisescotyledon blight While damping-off is usually refereed to diseasescaused by soil-borne fungi oroomycetes a number of abioticstresses may contribute todamping-off symptoms (C)(adapted from Landis (2013)

Agron Sustain Dev (2017) 37 10 Page 3 of 25 10

Tab

le1

Anon-exhaustiv

elisto

fstudieshighlig

htingfirstreportsof

damping-offworldwidesince2001

Con

tinent

Cou

ntry

Occurrence

Typ

eHost

Patho

gen

Incidence(

)Reference

Asia

China

2015

Post-emergence

Oat

Rhizoctonia

solani

AG2ndash1

19(Zhang

etal2015)

2013

Post-emergence

Foxtailm

illet

Rhizoctonia

AG-A

30(O

uet

al2015)

2010

Post-emergence

Sugarbeet

Rhizoctonia

AG-A

20(W

angandWu2012)

2011

Post-emergence

Chinese

cabbage

Alternaria

japonica

ND

(Ren

etal2012)

2010

Post-emergence

Rhodiolasachalinensis

Rhizoctoniasolani

AG-4

HG-II

60(Baiet

al2011)

2003

Post-emergence

Swisschard

Rhizoctonia

solani

AG-4

HGAG-A

80(Yanget

al2007)

2014

Post-emergence

Schisandra

chinensis

Rhizoctonia

solani

AG-4

HG-I

10(O

uet

al2015)

India

2011

Post-emergence

Mexican

marigold

Ceratobasidiumsp

15(Saroj

etal2

013)

Iran

2000

Post-emergence

Sugarbeet

Pythium

spp

ND

(Babai-A

hary

etal2004)

Iraq

2012

Post-emergence

Okra

Phytophthoranicotia

nae

ND

(Matny

2012)

Japan

2005

Pre-em

ergence

Okra

Pythium

ultim

umvarultim

um25

(Kidaet

al2007)

2007

Post-emergence

broccoli

Rhizoctonia

solani

AG-2-2

IVND

(Misaw

aet

al2015)

Malaysia

2010

Post-emergence

Coconut

Marasmielluspalmivorus

ND

(Alm

alikyet

al2012)

Oman

2004ndash2005

Post-emergence

Cucum

ber

Pythium

spp

ND

(Al-Sarsquodietal2007)

Turkey

2009

Post-emergence

Wheat

Rhizoctonia

solani

AG8

ND

(Uumlnaland

Sara

Dolar

2012)

Africa

Algeria

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumequiseti

64ndash77

(Lazreget

al2013a)

2008ndash2010

Pre-

andpost-emergence

Aleppopine

Globisporangium

ultim

umND

(Lazreget

al2013b)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumchlamydosporum

64ndash77

(Lazreget

al2013c)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumredolens

64ndash77

(Lazreget

al2013d)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumacum

inatum

64ndash77

(Lazreget

al2013e)

Benin

2001ndash2002

Post-emergence

Cow

pea

Phomaspand

otherfungal

species

ND

(Adandonon

etal2004)

Egypt

2000

Pre-

andpost-emergence

Wheat

Pythium

diclinum

ND

(Abdelzaher2004)

Europe

Greece

2007

Post-emergence

Cottonandtobacco

Rhizoctonia

spp

ND

(Bachariset

al2010)

Italy

2007

Post-emergence

Bottlebrush

Cylindrocladium

scoparium

30ndash70

(Polizziet

al2007)

2006

Pre-

andpost-emergence

Oak

Cylindrocladiella

parva

65(Scattolin

andMontecchio2007)

2004

Pre-

andpost-emergence

Beech

Fusariumavenaceum

70(M

ontecchio2005)

2010

Post-emergence

Leafbeet

Pythium

aphaniderm

atum

20(G

aribaldi

etal2013)

2011

Post-emergence

strawberrytree

Colletotrichumacutatum

simmondsii

ND

(Polizziet

al2011)

2010

Post-emergence

Pink

ipecirc

Rhizoctonia

solani

AG-4

5(Polizziet

al2010)

2009

Post-emergence

Fanpalm

Rhizoctonia

solani

AG-4

20(Polizziet

al2009)

2007

Post-emergence

African

daisy

Rhizoctonia

solani

AG-4

30(A

iello

etal2008a)

2008

Post-emergence

Lagunariapatersonii

Rhizoctonia

solani

AG-4

20(A

iello

etal2008b)

Netherlands

2005

Post-emergence

Fennel

Alternaria

petroselini

6ndash10

(Pryor

andAsm

a2007)

Spain

2011

Post-emergence

Swisschard

Rhizoctonia

solani

20(Palmeroet

al2012)

2009

Post-emergence

Pinus

radiata

Cylindrocarponpauciseptatum

ND

(Agustiacute-Brisach

etal2011)

NorthCentralAmerica

Canada

2005

Post-emergence

Durum

wheat

Arthriniumsacchari

ND

(Mavragani

etal2007)

Mexico

2014

Post-emergence

Habaneropepper

Phytophthoracapsici

ND

(Saacutenchez-Borgeset

al2015)

USA

2003

Post-emergence

Canola

Rhizoctonia

solani

AG2ndash1

ND

(Paulitzet

al2006)

2007ndash2009

Post-emergence

Soybean

Fusariumcommune

ND

(Elliset

al2012)

2011

Post-emergence

Indian

spinach

Rhizoctonia

solani

10(Liaoet

al2011)

2009

Post-emergence

Pea

Pythium

spp

ND

(Alcalaet

al2016)

1994

Post-emergence

Wild

rice

Pythium

torulosum

ND

(Marcum

andDavis2006)

SouthAmerica

Brazil

2014

Post-emergence

Casuarina

equisetifolia

Fusariumlacertarum

80(Poletto

etal2

015)

Brazil

2008ndash2011

Pre-em

ergence

Rice

Bipolarisoryzae

ND

(Schwanck

etal2015)

Oceania

Australia

1998ndash1999

Post-emergence

Carrot

Alternaria

radicina

47(Coles

andWicks

2003)

10 Page 4 of 25 Agron Sustain Dev (2017) 37 10

21 Pre-emergence symptoms

They occur when seeds decay prior to emergence This canoccur (i) before seed germination or when (ii) the germinatingseeds are killed by biotic stresses while shoot tissues are stillbelow ground (Fig 3 Filer and Peterson 1975 Crous 2002Horst 2013) In the first case seeds become soft rotten andfail to germinate In the second case stems of germinatingseeds are affected with characteristic water-soaked lesionsformed at or below the soil line (Cram 2003 Landis 2013)With the progression of the disease these lesions may darkento reddish-brown brown or black Expanding lesions quicklygirdle young and tender stems Seedlings may wilt and diesoon before emergence In general random pockets of poorseedling emergence are an indication of pre-emergencedamping-off

Abiotic stresses can be divided into two categories chem-ical and physical stress The first notably involves limiting (i)concentrations in carbon dioxide or ethylene (Negm andSmith 1978) (ii) potential of hydrogen (Foy 1984) (iii) os-motic potential (Romo and Haferkamp 1987) and (iv) phyto-toxicity (Wang et al 2001) The second includes (i) extremetemperatures (high or low) (Khan 1977 Wen 2015) extremeseedbed humidity (high or low) (Maraghni et al 2010 Wen2015) and (iii) mechanical stresses such as seedbed clods(Duumlrr and Aubertot 2000) or crusting at the soil surface(Aubertot et al 2002) Other mechanical events such as re-moval of mulch or soil by wind and rain may also contribute

to non-uniform seeding of containers or beds poor seed de-velopment and seed rot and decay (Landis 2013)

a

b

Fig 2 An overview of soybean(a) and pea (b) fields affected bydamping-off diseases due toPythium spp The presence ofempty space along the rowindicates seed or seedlingsaffected by pre- and post-emergence damping-off diseaseswhich killed plants Theeconomic losses in such asituation are severe owing to adirect cost due to damages of seedor seedlings and an indirect costrelated to an additional cost ofreplanting and the consequentlower yields due to the laterplanting dates (Fig 1A is photocourtesy of Martin Chilvers whileFig 1B is photo courtesy ofLindsey J du Toit)

Fig 3 Characteristic symptoms of pre-emergence damping-off of pea(Pisum sativum L) caused by Pythium spp Despite the same sowingdate only the first three seeds on the left have emerged Note non-emerged seeds with or without root development Soft rotten anddecayed seeds prior to germinating or the germinating seeds killed bybiotic stresses while shoot tissues are still below ground arecharacteristic symptoms of pre-emergence damping-off The sixth seedfrom the left had germinated but the stem of germinating seeds wasaffected by the disease with characteristic water-soaked lesions belowthe soil line This led to wilting of the seedling soon after emergence(Photo courtesy of Lindsey J du Toit)

Agron Sustain Dev (2017) 37 10 Page 5 of 25 10

Because biotic and abiotic stresses interact among them itis important to distinguish which of them are associated withthe disease symptoms

22 Post-emergence symptoms

Post-emergence damping-off symptoms occur when seedlingsdecay wilt and die after emergence (Fig 4 Boyce 1961Horst 2013) In most cases all symptoms result in the collapseand death of at least some seedlings in any given seedlingpopulation In the case of soil-borne pathogen there couldbe the death of seedlings in groups in roughly circular patchesand the seedlings may have stem lesions at ground levelSeedling stems can become thin and tough (commonly knownas ldquowirestemrdquo) which often leads to reduced seedling vigorThese symptoms can be also accompanied by leaf spottingand a complete root rot may occur Overall the symptomson the stem of the seedlings include water-soaked sunkenlesion at or slightly below the ground level and sometime alsobelow ground line (ie on the roots) causing the plant to fallover (Wright 1944 Filer and Peterson 1975) Surviving plantsare stunted and affected areas often show uneven growth

Abiotic stresses such as superficial soil heat can also leadto post-emergence seedling symptoms such as whitish lesionswhich are often located only on one side of the stem in theearly growth stage of seedlings (Hartley 1918) Such symp-toms can be distinguished from those caused by biotic stresses

because the damage owing to heat lesions is generallyscattered throughout nurseriesseedbeds which mainly de-pend on patterns of shade and heat buildup (Hartley 1921)while that caused by biotic stresses often occurs in expandingpatches Soil crusting is another important abiotic stress thatoften hinders seedling emergence or leads to stunted seedlinggrowth (Fig 5) Phytotoxicity caused by chemical fungicidesis another abiotic stress The symptoms of phytotoxicity how-ever may vary based on the type of chemical used includingmarginal necrosis chlorotic patches or spots and malformedflowers buds and young leaves (Dole andWilkins 2004) Forexample fungicides based with benzimidazole can cause re-duced plant growth and visual damage in bedding plants(Iersel and Bugbee 1996)

23 Occurrence of damping-off symptoms

Most damping-off diseases present a single sort of symptom(pre- or post-emergence) However both sorts of symptomsare also reported to some extent (Table 1) although the under-lying factors leading to the occurrence of each sort of symp-tom are poorly discussed in the literature The complexity ofdamping-off symptoms result from interactions betweencropping practices and the production situation (Aubertotand Robin 2013) This may explain the relevant lack of infor-mation This complexity involves synergism among damping-off pathogens (Al-Hazmi and Al-Nadary 2015) variation of

Fig 4 Characteristic symptoms of post-emergence damping-off ofsoybean (a and b) and corn (c and d) The succulent tissue of sproutswith aboveground shoots collapsed leading to wilting of some seedlingpopulations Soybean seedlings with stem lesions at ground level and the

death of seedlings in groups (a and b) The presence of an empty spacealong the row between corn seedlings indicates the lack of emergedseedlings due to damping-off disease (c and d) (Photo courtesy ofMartin Chilvers)

10 Page 6 of 25 Agron Sustain Dev (2017) 37 10

symptoms according to environmental conduciveness(Schwanck et al 2015) direct effect of plant density(Burdon and Chilvers 1975) and many other factors whichare very specific for each damping-off symptom For instancethe disease cycle components of damping-off are seldomdiscussed in a broader sense in the literature by comparingdifferent diseases Some factors related to the timemoment ofdisease occurrence and timing of disease cycle componentscould determine whether pre- or post-emergence symptomswill occur In this sense it is possible that for both pre- andpost-emergence damping-off the infection occurs during seedgermination but a longer or shorter incubation period mayimplicate in pre- or post-emergence damping-off In additionthe effect of individual factors involved on the disease pro-cesses from the disease cycle and the host cycle (eg seedgermination) for damping-off symptom development is rare-ly discussed in the literature Taken together several studiesvirtually explore the effect of a given factor (eg temperature)on damping-off diseases intensity (Ben-Yephet and Nelson1999) without specifying whether the factor plays a specificrole on the pathogen (eg organism metabolism) or on thehost (eg slow germination process increases time exposureunderground) Further knowledge on disease cycle featuresand processes would help better understand damping-offsymptom occurrence Although it was out of the focus of thiswork it is worth to mention that from the extensive literaturereview we did not perceive any pattern on the sort ofdamping-off symptom (pre- or post-) according to the regionthe pathogen genus or crop species affected Therefore ameta-analytical approach to test hypotheses associated withdamping-off diseases would be highly valuable to better ex-plain the factors involved in damping-off symptoms

occurrence To this aim the list of damping-off diseases weprovide in Table 1 constitutes a potential starting point

3 Integrated management of damping-off

An effective management of damping-off requires the deploy-ment of a number of strategies which can be classified into thefollowing four major groups (i) seed treatment to enhancegermination and seedling vigor (ii) deployment of resistantor tolerant cultivars to damping-off diseases (iii) adoption ofbest cropping practices and (iv) timely treatment interven-tions of seedlings with effective products (conventional pesti-cides as well as biopesticides andor biocontrol agents) Noneof these strategies is effective in managing damping-off dis-ease when applied individually and thus it requires that all ofthem are combined within the frame of IPM

31 Seed treatment to enhance germination and seedlingvigor

While the use of completely healthy seeds is the most effectivemeans to prevent andor contain damping-off diseases seedsmight not be always free from pathogens and thus wouldbenefit from treatments Even when there is no risk of con-taminated seeds from seed-borne pathogens seed treatmentscan be an effective means to increase seedling emergenceparticularly when done on seeds of low vigor and when theseed coat has been damaged (Mancini and Romanazzi 2014)

Chemical seed treatments still represent a major practice inagriculture to manage damping-off diseases (Rhodes andMyers 1989 Babadoost and Islam 2003 Howell 2007

Fig 5 Lack of sugar beet (Beta vulgaris L) seedlings emergence due tosoil crusting followed by drought The formation of soil crusts on the soilsurface represents a strong mechanical barrier which impedes seedlingsfrom being emerged Overall lack of seed germination and emergence in

such a field is characteristic of abiotic stresses including stunted growth ofseedlings without any necrosis of leaves or stems (Photo courtesy ofCarolyne Duumlrr)

Agron Sustain Dev (2017) 37 10 Page 7 of 25 10

Bradley 2007 Leisso et al 2009 Dorrance et al 2009Rothrock et al 2012 Kandel et al 2016) Several chemicalsincluding bleach hydrogen peroxide ethanol and fungicidescan be applied to remove pathogen inoculum from seed coats(Dumroese and James 2005 Mancini and Romanazzi 2014)Generally chemical treatments are effective but they can alsonegatively affect seed germination and cause phytotoxicity(Axelrood et al 1995 du Toit 2004) besides negative impactsto human health and the environment (Lamichhane et al2016) In addition to chemical treatments physical seed treat-ment can be applied including hot water hot air and electrontreatments (Mancini and Romanazzi 2014) Finally a numberof biological seed treatment methods are being developed andused in recent years with a satisfactory level of damping-offdisease suppression (Table 2)

Because seed germination and emergence are ofteninfluenced by site-specific soil and climate conditionsan in-depth knowledge of a specific site in question is aprerequisite for an effective decision-making process forseed treatments An experiment on pesticide-freeagroecosystems conducted in 2014 across eight experi-mental sites in France with non-treated seeds showedthat the percentage of emergence rates markedly differsfor the same seeds across the sites (Fig 3) In particu-lar while the rate of emergence of soft wheat was100 in the Le Rheu and Grignon sites it was loweracross other sites ranging from 43 in Auzeville to75 in Lusignan (Fig 6) This means that while seedtreatments may result essential across some sites due tounfavorable soil and climatic conditions which are con-ducive to disease development it may not be the casein other areas

32 Deployment of host-plant resistance andor tolerance

Overall host-plant resistance as a management tactic is com-posed of the following two strategies (i) deployment of resis-tant andor tolerant plant varieties which support lower path-ogen populations or better tolerate injury caused by them and(ii) the integration of such varieties with other managementtactics within the frame of IPM Unfortunately for many plantpathogens including those causing damping-off diseases noplant cultivar with measurable resistance is available(Babadoost and Islam 2003) Therefore the only way to betteruse the available crop varieties with tolerance to pathogens isthrough their adequate integration with other disease manage-ment measures Nevertheless insufficient focus has been paidto date to the integration of plant resistance with other IPMtactics and to quantifying the benefits of plant resistance inmulti-tactic IPM programs (Stout and Davis 2009)

On the other hand the breeding approach used to date todevelop resistant andor tolerant crop varieties should berevisited if we want to focus on sustainable crop protectionbased on IPM This is particularly true taking into account thefact that most if not all crop varieties bred to date are basedon a market-driven approach focused on high-yielding andmost profitable crop varieties This trend has boosted adoptionof short rotations or monoculture practices on one hand andignored the potential that minor crops may have for IPM onthe other (Messeacutean et al 2016) The limited range of availableminor crop varieties has been reported as one of the majorobstacles to crop diversification thereby confining certainbeneficial practices such as multiple cropping or intercropping(Enjalbert et al 2016 Messeacutean et al 2016) Therefore breed-ing for IPM should be based on a different approach than the

Table 2 Examples of literature reports highlighting the efficacy of non-chemical seed treatments to suppress damping-off diseases The testedformulations are most often reported to suppress both pre- and post-emergence damping-off although their effectiveness may vary in terms of diseasesuppressiveness

Crop Pathogen Formulationproduct Reference

Alfalfa Pythium spp Mineral seed coating (Samac et al 2014)Canola Pythium spp Rhizosphere bacteria (Bardin et al 2003)Corn Pythium and Fusarium spp Several biocontrol agents (Mao et al 1997 Mao et al 1998)Cotton Pythium spp Enterobacter cloacae and

Erwinia herbicola(Nelson 1988)

Cotton Pythium spp Rhizopus oryzae Trichoderma spp (Howell 2007)Cucumber Pythium ultimum Ethanol extracts of Serratia

marcescens and Trichoderma spp(Roberts et al 2016)

Cucumber Pythium spp Phosphonate (Abbasi and Lazarovits 2005 Abbasi andLazarovits 2006)

Sunflower Rhizoctonia solani Spermine (El-Metwally and Sakr 2010)Lentil pea

sugar beetPythium spp Rhizobium leguminosarum (Bardin et al 2004b Huang and Erickson 2007)

Pea Pythium spp Rhizosphere bacteria (Bardin et al 2003)Safflower Pythium spp Rhizosphere bacteria (Bardin et al 2003)Sesame Soil-borne pathogens Paenibacillus polymyxa (Ryu et al 2006)Sugar beet Pythium spp Rhizosphere bacteria crop straw powders (Bardin et al 2003 Bardin et al 2004a)Tomato and hot pepper Pythium spp Fluorescent Pseudomonads (Ramamoorthy et al 2002)

10 Page 8 of 25 Agron Sustain Dev (2017) 37 10

traditional one given the strategic role of breeding in the com-petitiveness of crops and their adaptation to more diversifiedcropping systems (Enjalbert et al 2016)

33 Adoption of best cropping practices

Once the causal agent of damping-off has been identifiedall available cropping practices could be adapted to dis-courage the development of the pathogen Indeed anytechnique that allows to reduce the time between seedgermination and emergence helps reduce effects of bioticstresses on seedlings Overall many pathogens involvedin damping-off are relatively weak pathogens which re-quire favorable environmental conditions for infection tooccur (Table 1) In addition to the susceptibility of hostand aggressiveness of pathogen populations the severityof damping-off is highly dependent on some critical fac-tors including seedbed preparation soil pH managementseeding date and rate growing density nutrition

irrigation growing environment crop sequence andintercropping cover crops soil residue management soilsolarization and tillage (Table 3) Therefore understand-ing combined effects of abiotic and biotic stresses andfactors influencing them are a prerequisite towards effec-tive IPM strategies of damping-off Once these criticalfactors have been identified which might differ fromone region to another best cropping practices should beput in place and adopted

One of the most important practices that allow to thebest management of damping-off and root diseases is fer-tilization Adequate availability of nutrients in the soil canensure higher vigor with earlier emergence that limit theperiod of time where pathogens can infect seeds and seed-lings during the autotrophic stage In particular the ad-vantages of fertilizer placement on seed germination andseedling emergence have been previously demonstrated(Cook et al 2000) The placement of fertilizers directlyunder or slightly to one side of the seed at the time ofplanting or sowing results in an increased level of seedgermination and emergence (Fig 7) This is because rel-atively immobile nutrients such as phosphorus are notreadily available for plants especially for those specieshaving no or a few lateral roots Therefore field fertiliza-tion where damping-off diseases are important requiresthat the nutrients be made easily accessible to the roots toincrease growth rate Although these nutrients do not al-ways reduce seedling infection they often enhance seedgermination and seedling vigor (Smiley et al 1990Patterson et al 1998) Indeed higher seedling vigor al-lows seedlings to rapidly escape from the soil surfaceeven in the presence of a high soil population density ofthe pathogen(s)

34 Timely treatment interventions of seedlingswith effective products

The strategies described above are mainly of preventive natureas they can be developed and adopted before the occurrence ofdamping-off diseases Once the infection occurs on seedlingsand there is a high risk of epidemic development growershave to attempt for an effective control of the diseaseOverall there are two key measures available for damping-off control as described below

341 Biological control

Because of their adverse effects on human health and theenvironment the use of conventional pesticides includingfungicides has come under increasing public scrutiny inmany countries especially in the European Union(Bourguet and Guillemaud 2016 Lamichhane et al2016) In addition increasing reports of pest resistance

Fig 6 Percentage of seed emergence (non-treated seeds) observed acrossdifferent experimental sites managed under the ldquoRes0Pestrdquo network inFrance in 2014 Res0Pest is a ldquopesticide-freerdquo trial network launched in2011 by the INRACIRAD IPM network to address objectives of theFrench National Action Plan Ecophyto to develop and demonstrate thefeasibility of pesticide-free cropping systems (Deytieux et al 2014) Eightexperimental sites comprised of five arable cropping systems (in brown)and three mixed crophusbandry systems (in green) are ongoing acrossthe sites DW durum wheat SW soft wheat MSW mixed of soft wheatvarieties SB spring barley Different percentages of emergence across theexperimental sites highlight how soil and climate and cropping practicesaffect seed germination and the seedling emergence process throughbiotic and abiotic stress Low percentages of emerged seedlings arehighlighted in red

Agron Sustain Dev (2017) 37 10 Page 9 of 25 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

Tab

le1

Anon-exhaustiv

elisto

fstudieshighlig

htingfirstreportsof

damping-offworldwidesince2001

Con

tinent

Cou

ntry

Occurrence

Typ

eHost

Patho

gen

Incidence(

)Reference

Asia

China

2015

Post-emergence

Oat

Rhizoctonia

solani

AG2ndash1

19(Zhang

etal2015)

2013

Post-emergence

Foxtailm

illet

Rhizoctonia

AG-A

30(O

uet

al2015)

2010

Post-emergence

Sugarbeet

Rhizoctonia

AG-A

20(W

angandWu2012)

2011

Post-emergence

Chinese

cabbage

Alternaria

japonica

ND

(Ren

etal2012)

2010

Post-emergence

Rhodiolasachalinensis

Rhizoctoniasolani

AG-4

HG-II

60(Baiet

al2011)

2003

Post-emergence

Swisschard

Rhizoctonia

solani

AG-4

HGAG-A

80(Yanget

al2007)

2014

Post-emergence

Schisandra

chinensis

Rhizoctonia

solani

AG-4

HG-I

10(O

uet

al2015)

India

2011

Post-emergence

Mexican

marigold

Ceratobasidiumsp

15(Saroj

etal2

013)

Iran

2000

Post-emergence

Sugarbeet

Pythium

spp

ND

(Babai-A

hary

etal2004)

Iraq

2012

Post-emergence

Okra

Phytophthoranicotia

nae

ND

(Matny

2012)

Japan

2005

Pre-em

ergence

Okra

Pythium

ultim

umvarultim

um25

(Kidaet

al2007)

2007

Post-emergence

broccoli

Rhizoctonia

solani

AG-2-2

IVND

(Misaw

aet

al2015)

Malaysia

2010

Post-emergence

Coconut

Marasmielluspalmivorus

ND

(Alm

alikyet

al2012)

Oman

2004ndash2005

Post-emergence

Cucum

ber

Pythium

spp

ND

(Al-Sarsquodietal2007)

Turkey

2009

Post-emergence

Wheat

Rhizoctonia

solani

AG8

ND

(Uumlnaland

Sara

Dolar

2012)

Africa

Algeria

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumequiseti

64ndash77

(Lazreget

al2013a)

2008ndash2010

Pre-

andpost-emergence

Aleppopine

Globisporangium

ultim

umND

(Lazreget

al2013b)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumchlamydosporum

64ndash77

(Lazreget

al2013c)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumredolens

64ndash77

(Lazreget

al2013d)

2008ndash2009

Pre-

andpost-emergence

Aleppopine

Fusariumacum

inatum

64ndash77

(Lazreget

al2013e)

Benin

2001ndash2002

Post-emergence

Cow

pea

Phomaspand

otherfungal

species

ND

(Adandonon

etal2004)

Egypt

2000

Pre-

andpost-emergence

Wheat

Pythium

diclinum

ND

(Abdelzaher2004)

Europe

Greece

2007

Post-emergence

Cottonandtobacco

Rhizoctonia

spp

ND

(Bachariset

al2010)

Italy

2007

Post-emergence

Bottlebrush

Cylindrocladium

scoparium

30ndash70

(Polizziet

al2007)

2006

Pre-

andpost-emergence

Oak

Cylindrocladiella

parva

65(Scattolin

andMontecchio2007)

2004

Pre-

andpost-emergence

Beech

Fusariumavenaceum

70(M

ontecchio2005)

2010

Post-emergence

Leafbeet

Pythium

aphaniderm

atum

20(G

aribaldi

etal2013)

2011

Post-emergence

strawberrytree

Colletotrichumacutatum

simmondsii

ND

(Polizziet

al2011)

2010

Post-emergence

Pink

ipecirc

Rhizoctonia

solani

AG-4

5(Polizziet

al2010)

2009

Post-emergence

Fanpalm

Rhizoctonia

solani

AG-4

20(Polizziet

al2009)

2007

Post-emergence

African

daisy

Rhizoctonia

solani

AG-4

30(A

iello

etal2008a)

2008

Post-emergence

Lagunariapatersonii

Rhizoctonia

solani

AG-4

20(A

iello

etal2008b)

Netherlands

2005

Post-emergence

Fennel

Alternaria

petroselini

6ndash10

(Pryor

andAsm

a2007)

Spain

2011

Post-emergence

Swisschard

Rhizoctonia

solani

20(Palmeroet

al2012)

2009

Post-emergence

Pinus

radiata

Cylindrocarponpauciseptatum

ND

(Agustiacute-Brisach

etal2011)

NorthCentralAmerica

Canada

2005

Post-emergence

Durum

wheat

Arthriniumsacchari

ND

(Mavragani

etal2007)

Mexico

2014

Post-emergence

Habaneropepper

Phytophthoracapsici

ND

(Saacutenchez-Borgeset

al2015)

USA

2003

Post-emergence

Canola

Rhizoctonia

solani

AG2ndash1

ND

(Paulitzet

al2006)

2007ndash2009

Post-emergence

Soybean

Fusariumcommune

ND

(Elliset

al2012)

2011

Post-emergence

Indian

spinach

Rhizoctonia

solani

10(Liaoet

al2011)

2009

Post-emergence

Pea

Pythium

spp

ND

(Alcalaet

al2016)

1994

Post-emergence

Wild

rice

Pythium

torulosum

ND

(Marcum

andDavis2006)

SouthAmerica

Brazil

2014

Post-emergence

Casuarina

equisetifolia

Fusariumlacertarum

80(Poletto

etal2

015)

Brazil

2008ndash2011

Pre-em

ergence

Rice

Bipolarisoryzae

ND

(Schwanck

etal2015)

Oceania

Australia

1998ndash1999

Post-emergence

Carrot

Alternaria

radicina

47(Coles

andWicks

2003)

10 Page 4 of 25 Agron Sustain Dev (2017) 37 10

21 Pre-emergence symptoms

They occur when seeds decay prior to emergence This canoccur (i) before seed germination or when (ii) the germinatingseeds are killed by biotic stresses while shoot tissues are stillbelow ground (Fig 3 Filer and Peterson 1975 Crous 2002Horst 2013) In the first case seeds become soft rotten andfail to germinate In the second case stems of germinatingseeds are affected with characteristic water-soaked lesionsformed at or below the soil line (Cram 2003 Landis 2013)With the progression of the disease these lesions may darkento reddish-brown brown or black Expanding lesions quicklygirdle young and tender stems Seedlings may wilt and diesoon before emergence In general random pockets of poorseedling emergence are an indication of pre-emergencedamping-off

Abiotic stresses can be divided into two categories chem-ical and physical stress The first notably involves limiting (i)concentrations in carbon dioxide or ethylene (Negm andSmith 1978) (ii) potential of hydrogen (Foy 1984) (iii) os-motic potential (Romo and Haferkamp 1987) and (iv) phyto-toxicity (Wang et al 2001) The second includes (i) extremetemperatures (high or low) (Khan 1977 Wen 2015) extremeseedbed humidity (high or low) (Maraghni et al 2010 Wen2015) and (iii) mechanical stresses such as seedbed clods(Duumlrr and Aubertot 2000) or crusting at the soil surface(Aubertot et al 2002) Other mechanical events such as re-moval of mulch or soil by wind and rain may also contribute

to non-uniform seeding of containers or beds poor seed de-velopment and seed rot and decay (Landis 2013)

a

b

Fig 2 An overview of soybean(a) and pea (b) fields affected bydamping-off diseases due toPythium spp The presence ofempty space along the rowindicates seed or seedlingsaffected by pre- and post-emergence damping-off diseaseswhich killed plants Theeconomic losses in such asituation are severe owing to adirect cost due to damages of seedor seedlings and an indirect costrelated to an additional cost ofreplanting and the consequentlower yields due to the laterplanting dates (Fig 1A is photocourtesy of Martin Chilvers whileFig 1B is photo courtesy ofLindsey J du Toit)

Fig 3 Characteristic symptoms of pre-emergence damping-off of pea(Pisum sativum L) caused by Pythium spp Despite the same sowingdate only the first three seeds on the left have emerged Note non-emerged seeds with or without root development Soft rotten anddecayed seeds prior to germinating or the germinating seeds killed bybiotic stresses while shoot tissues are still below ground arecharacteristic symptoms of pre-emergence damping-off The sixth seedfrom the left had germinated but the stem of germinating seeds wasaffected by the disease with characteristic water-soaked lesions belowthe soil line This led to wilting of the seedling soon after emergence(Photo courtesy of Lindsey J du Toit)

Agron Sustain Dev (2017) 37 10 Page 5 of 25 10

Because biotic and abiotic stresses interact among them itis important to distinguish which of them are associated withthe disease symptoms

22 Post-emergence symptoms

Post-emergence damping-off symptoms occur when seedlingsdecay wilt and die after emergence (Fig 4 Boyce 1961Horst 2013) In most cases all symptoms result in the collapseand death of at least some seedlings in any given seedlingpopulation In the case of soil-borne pathogen there couldbe the death of seedlings in groups in roughly circular patchesand the seedlings may have stem lesions at ground levelSeedling stems can become thin and tough (commonly knownas ldquowirestemrdquo) which often leads to reduced seedling vigorThese symptoms can be also accompanied by leaf spottingand a complete root rot may occur Overall the symptomson the stem of the seedlings include water-soaked sunkenlesion at or slightly below the ground level and sometime alsobelow ground line (ie on the roots) causing the plant to fallover (Wright 1944 Filer and Peterson 1975) Surviving plantsare stunted and affected areas often show uneven growth

Abiotic stresses such as superficial soil heat can also leadto post-emergence seedling symptoms such as whitish lesionswhich are often located only on one side of the stem in theearly growth stage of seedlings (Hartley 1918) Such symp-toms can be distinguished from those caused by biotic stresses

because the damage owing to heat lesions is generallyscattered throughout nurseriesseedbeds which mainly de-pend on patterns of shade and heat buildup (Hartley 1921)while that caused by biotic stresses often occurs in expandingpatches Soil crusting is another important abiotic stress thatoften hinders seedling emergence or leads to stunted seedlinggrowth (Fig 5) Phytotoxicity caused by chemical fungicidesis another abiotic stress The symptoms of phytotoxicity how-ever may vary based on the type of chemical used includingmarginal necrosis chlorotic patches or spots and malformedflowers buds and young leaves (Dole andWilkins 2004) Forexample fungicides based with benzimidazole can cause re-duced plant growth and visual damage in bedding plants(Iersel and Bugbee 1996)

23 Occurrence of damping-off symptoms

Most damping-off diseases present a single sort of symptom(pre- or post-emergence) However both sorts of symptomsare also reported to some extent (Table 1) although the under-lying factors leading to the occurrence of each sort of symp-tom are poorly discussed in the literature The complexity ofdamping-off symptoms result from interactions betweencropping practices and the production situation (Aubertotand Robin 2013) This may explain the relevant lack of infor-mation This complexity involves synergism among damping-off pathogens (Al-Hazmi and Al-Nadary 2015) variation of

Fig 4 Characteristic symptoms of post-emergence damping-off ofsoybean (a and b) and corn (c and d) The succulent tissue of sproutswith aboveground shoots collapsed leading to wilting of some seedlingpopulations Soybean seedlings with stem lesions at ground level and the

death of seedlings in groups (a and b) The presence of an empty spacealong the row between corn seedlings indicates the lack of emergedseedlings due to damping-off disease (c and d) (Photo courtesy ofMartin Chilvers)

10 Page 6 of 25 Agron Sustain Dev (2017) 37 10

symptoms according to environmental conduciveness(Schwanck et al 2015) direct effect of plant density(Burdon and Chilvers 1975) and many other factors whichare very specific for each damping-off symptom For instancethe disease cycle components of damping-off are seldomdiscussed in a broader sense in the literature by comparingdifferent diseases Some factors related to the timemoment ofdisease occurrence and timing of disease cycle componentscould determine whether pre- or post-emergence symptomswill occur In this sense it is possible that for both pre- andpost-emergence damping-off the infection occurs during seedgermination but a longer or shorter incubation period mayimplicate in pre- or post-emergence damping-off In additionthe effect of individual factors involved on the disease pro-cesses from the disease cycle and the host cycle (eg seedgermination) for damping-off symptom development is rare-ly discussed in the literature Taken together several studiesvirtually explore the effect of a given factor (eg temperature)on damping-off diseases intensity (Ben-Yephet and Nelson1999) without specifying whether the factor plays a specificrole on the pathogen (eg organism metabolism) or on thehost (eg slow germination process increases time exposureunderground) Further knowledge on disease cycle featuresand processes would help better understand damping-offsymptom occurrence Although it was out of the focus of thiswork it is worth to mention that from the extensive literaturereview we did not perceive any pattern on the sort ofdamping-off symptom (pre- or post-) according to the regionthe pathogen genus or crop species affected Therefore ameta-analytical approach to test hypotheses associated withdamping-off diseases would be highly valuable to better ex-plain the factors involved in damping-off symptoms

occurrence To this aim the list of damping-off diseases weprovide in Table 1 constitutes a potential starting point

3 Integrated management of damping-off

An effective management of damping-off requires the deploy-ment of a number of strategies which can be classified into thefollowing four major groups (i) seed treatment to enhancegermination and seedling vigor (ii) deployment of resistantor tolerant cultivars to damping-off diseases (iii) adoption ofbest cropping practices and (iv) timely treatment interven-tions of seedlings with effective products (conventional pesti-cides as well as biopesticides andor biocontrol agents) Noneof these strategies is effective in managing damping-off dis-ease when applied individually and thus it requires that all ofthem are combined within the frame of IPM

31 Seed treatment to enhance germination and seedlingvigor

While the use of completely healthy seeds is the most effectivemeans to prevent andor contain damping-off diseases seedsmight not be always free from pathogens and thus wouldbenefit from treatments Even when there is no risk of con-taminated seeds from seed-borne pathogens seed treatmentscan be an effective means to increase seedling emergenceparticularly when done on seeds of low vigor and when theseed coat has been damaged (Mancini and Romanazzi 2014)

Chemical seed treatments still represent a major practice inagriculture to manage damping-off diseases (Rhodes andMyers 1989 Babadoost and Islam 2003 Howell 2007

Fig 5 Lack of sugar beet (Beta vulgaris L) seedlings emergence due tosoil crusting followed by drought The formation of soil crusts on the soilsurface represents a strong mechanical barrier which impedes seedlingsfrom being emerged Overall lack of seed germination and emergence in

such a field is characteristic of abiotic stresses including stunted growth ofseedlings without any necrosis of leaves or stems (Photo courtesy ofCarolyne Duumlrr)

Agron Sustain Dev (2017) 37 10 Page 7 of 25 10

Bradley 2007 Leisso et al 2009 Dorrance et al 2009Rothrock et al 2012 Kandel et al 2016) Several chemicalsincluding bleach hydrogen peroxide ethanol and fungicidescan be applied to remove pathogen inoculum from seed coats(Dumroese and James 2005 Mancini and Romanazzi 2014)Generally chemical treatments are effective but they can alsonegatively affect seed germination and cause phytotoxicity(Axelrood et al 1995 du Toit 2004) besides negative impactsto human health and the environment (Lamichhane et al2016) In addition to chemical treatments physical seed treat-ment can be applied including hot water hot air and electrontreatments (Mancini and Romanazzi 2014) Finally a numberof biological seed treatment methods are being developed andused in recent years with a satisfactory level of damping-offdisease suppression (Table 2)

Because seed germination and emergence are ofteninfluenced by site-specific soil and climate conditionsan in-depth knowledge of a specific site in question is aprerequisite for an effective decision-making process forseed treatments An experiment on pesticide-freeagroecosystems conducted in 2014 across eight experi-mental sites in France with non-treated seeds showedthat the percentage of emergence rates markedly differsfor the same seeds across the sites (Fig 3) In particu-lar while the rate of emergence of soft wheat was100 in the Le Rheu and Grignon sites it was loweracross other sites ranging from 43 in Auzeville to75 in Lusignan (Fig 6) This means that while seedtreatments may result essential across some sites due tounfavorable soil and climatic conditions which are con-ducive to disease development it may not be the casein other areas

32 Deployment of host-plant resistance andor tolerance

Overall host-plant resistance as a management tactic is com-posed of the following two strategies (i) deployment of resis-tant andor tolerant plant varieties which support lower path-ogen populations or better tolerate injury caused by them and(ii) the integration of such varieties with other managementtactics within the frame of IPM Unfortunately for many plantpathogens including those causing damping-off diseases noplant cultivar with measurable resistance is available(Babadoost and Islam 2003) Therefore the only way to betteruse the available crop varieties with tolerance to pathogens isthrough their adequate integration with other disease manage-ment measures Nevertheless insufficient focus has been paidto date to the integration of plant resistance with other IPMtactics and to quantifying the benefits of plant resistance inmulti-tactic IPM programs (Stout and Davis 2009)

On the other hand the breeding approach used to date todevelop resistant andor tolerant crop varieties should berevisited if we want to focus on sustainable crop protectionbased on IPM This is particularly true taking into account thefact that most if not all crop varieties bred to date are basedon a market-driven approach focused on high-yielding andmost profitable crop varieties This trend has boosted adoptionof short rotations or monoculture practices on one hand andignored the potential that minor crops may have for IPM onthe other (Messeacutean et al 2016) The limited range of availableminor crop varieties has been reported as one of the majorobstacles to crop diversification thereby confining certainbeneficial practices such as multiple cropping or intercropping(Enjalbert et al 2016 Messeacutean et al 2016) Therefore breed-ing for IPM should be based on a different approach than the

Table 2 Examples of literature reports highlighting the efficacy of non-chemical seed treatments to suppress damping-off diseases The testedformulations are most often reported to suppress both pre- and post-emergence damping-off although their effectiveness may vary in terms of diseasesuppressiveness

Crop Pathogen Formulationproduct Reference

Alfalfa Pythium spp Mineral seed coating (Samac et al 2014)Canola Pythium spp Rhizosphere bacteria (Bardin et al 2003)Corn Pythium and Fusarium spp Several biocontrol agents (Mao et al 1997 Mao et al 1998)Cotton Pythium spp Enterobacter cloacae and

Erwinia herbicola(Nelson 1988)

Cotton Pythium spp Rhizopus oryzae Trichoderma spp (Howell 2007)Cucumber Pythium ultimum Ethanol extracts of Serratia

marcescens and Trichoderma spp(Roberts et al 2016)

Cucumber Pythium spp Phosphonate (Abbasi and Lazarovits 2005 Abbasi andLazarovits 2006)

Sunflower Rhizoctonia solani Spermine (El-Metwally and Sakr 2010)Lentil pea

sugar beetPythium spp Rhizobium leguminosarum (Bardin et al 2004b Huang and Erickson 2007)

Pea Pythium spp Rhizosphere bacteria (Bardin et al 2003)Safflower Pythium spp Rhizosphere bacteria (Bardin et al 2003)Sesame Soil-borne pathogens Paenibacillus polymyxa (Ryu et al 2006)Sugar beet Pythium spp Rhizosphere bacteria crop straw powders (Bardin et al 2003 Bardin et al 2004a)Tomato and hot pepper Pythium spp Fluorescent Pseudomonads (Ramamoorthy et al 2002)

10 Page 8 of 25 Agron Sustain Dev (2017) 37 10

traditional one given the strategic role of breeding in the com-petitiveness of crops and their adaptation to more diversifiedcropping systems (Enjalbert et al 2016)

33 Adoption of best cropping practices

Once the causal agent of damping-off has been identifiedall available cropping practices could be adapted to dis-courage the development of the pathogen Indeed anytechnique that allows to reduce the time between seedgermination and emergence helps reduce effects of bioticstresses on seedlings Overall many pathogens involvedin damping-off are relatively weak pathogens which re-quire favorable environmental conditions for infection tooccur (Table 1) In addition to the susceptibility of hostand aggressiveness of pathogen populations the severityof damping-off is highly dependent on some critical fac-tors including seedbed preparation soil pH managementseeding date and rate growing density nutrition

irrigation growing environment crop sequence andintercropping cover crops soil residue management soilsolarization and tillage (Table 3) Therefore understand-ing combined effects of abiotic and biotic stresses andfactors influencing them are a prerequisite towards effec-tive IPM strategies of damping-off Once these criticalfactors have been identified which might differ fromone region to another best cropping practices should beput in place and adopted

One of the most important practices that allow to thebest management of damping-off and root diseases is fer-tilization Adequate availability of nutrients in the soil canensure higher vigor with earlier emergence that limit theperiod of time where pathogens can infect seeds and seed-lings during the autotrophic stage In particular the ad-vantages of fertilizer placement on seed germination andseedling emergence have been previously demonstrated(Cook et al 2000) The placement of fertilizers directlyunder or slightly to one side of the seed at the time ofplanting or sowing results in an increased level of seedgermination and emergence (Fig 7) This is because rel-atively immobile nutrients such as phosphorus are notreadily available for plants especially for those specieshaving no or a few lateral roots Therefore field fertiliza-tion where damping-off diseases are important requiresthat the nutrients be made easily accessible to the roots toincrease growth rate Although these nutrients do not al-ways reduce seedling infection they often enhance seedgermination and seedling vigor (Smiley et al 1990Patterson et al 1998) Indeed higher seedling vigor al-lows seedlings to rapidly escape from the soil surfaceeven in the presence of a high soil population density ofthe pathogen(s)

34 Timely treatment interventions of seedlingswith effective products

The strategies described above are mainly of preventive natureas they can be developed and adopted before the occurrence ofdamping-off diseases Once the infection occurs on seedlingsand there is a high risk of epidemic development growershave to attempt for an effective control of the diseaseOverall there are two key measures available for damping-off control as described below

341 Biological control

Because of their adverse effects on human health and theenvironment the use of conventional pesticides includingfungicides has come under increasing public scrutiny inmany countries especially in the European Union(Bourguet and Guillemaud 2016 Lamichhane et al2016) In addition increasing reports of pest resistance

Fig 6 Percentage of seed emergence (non-treated seeds) observed acrossdifferent experimental sites managed under the ldquoRes0Pestrdquo network inFrance in 2014 Res0Pest is a ldquopesticide-freerdquo trial network launched in2011 by the INRACIRAD IPM network to address objectives of theFrench National Action Plan Ecophyto to develop and demonstrate thefeasibility of pesticide-free cropping systems (Deytieux et al 2014) Eightexperimental sites comprised of five arable cropping systems (in brown)and three mixed crophusbandry systems (in green) are ongoing acrossthe sites DW durum wheat SW soft wheat MSW mixed of soft wheatvarieties SB spring barley Different percentages of emergence across theexperimental sites highlight how soil and climate and cropping practicesaffect seed germination and the seedling emergence process throughbiotic and abiotic stress Low percentages of emerged seedlings arehighlighted in red

Agron Sustain Dev (2017) 37 10 Page 9 of 25 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

21 Pre-emergence symptoms

They occur when seeds decay prior to emergence This canoccur (i) before seed germination or when (ii) the germinatingseeds are killed by biotic stresses while shoot tissues are stillbelow ground (Fig 3 Filer and Peterson 1975 Crous 2002Horst 2013) In the first case seeds become soft rotten andfail to germinate In the second case stems of germinatingseeds are affected with characteristic water-soaked lesionsformed at or below the soil line (Cram 2003 Landis 2013)With the progression of the disease these lesions may darkento reddish-brown brown or black Expanding lesions quicklygirdle young and tender stems Seedlings may wilt and diesoon before emergence In general random pockets of poorseedling emergence are an indication of pre-emergencedamping-off

Abiotic stresses can be divided into two categories chem-ical and physical stress The first notably involves limiting (i)concentrations in carbon dioxide or ethylene (Negm andSmith 1978) (ii) potential of hydrogen (Foy 1984) (iii) os-motic potential (Romo and Haferkamp 1987) and (iv) phyto-toxicity (Wang et al 2001) The second includes (i) extremetemperatures (high or low) (Khan 1977 Wen 2015) extremeseedbed humidity (high or low) (Maraghni et al 2010 Wen2015) and (iii) mechanical stresses such as seedbed clods(Duumlrr and Aubertot 2000) or crusting at the soil surface(Aubertot et al 2002) Other mechanical events such as re-moval of mulch or soil by wind and rain may also contribute

to non-uniform seeding of containers or beds poor seed de-velopment and seed rot and decay (Landis 2013)

a

b

Fig 2 An overview of soybean(a) and pea (b) fields affected bydamping-off diseases due toPythium spp The presence ofempty space along the rowindicates seed or seedlingsaffected by pre- and post-emergence damping-off diseaseswhich killed plants Theeconomic losses in such asituation are severe owing to adirect cost due to damages of seedor seedlings and an indirect costrelated to an additional cost ofreplanting and the consequentlower yields due to the laterplanting dates (Fig 1A is photocourtesy of Martin Chilvers whileFig 1B is photo courtesy ofLindsey J du Toit)

Fig 3 Characteristic symptoms of pre-emergence damping-off of pea(Pisum sativum L) caused by Pythium spp Despite the same sowingdate only the first three seeds on the left have emerged Note non-emerged seeds with or without root development Soft rotten anddecayed seeds prior to germinating or the germinating seeds killed bybiotic stresses while shoot tissues are still below ground arecharacteristic symptoms of pre-emergence damping-off The sixth seedfrom the left had germinated but the stem of germinating seeds wasaffected by the disease with characteristic water-soaked lesions belowthe soil line This led to wilting of the seedling soon after emergence(Photo courtesy of Lindsey J du Toit)

Agron Sustain Dev (2017) 37 10 Page 5 of 25 10

Because biotic and abiotic stresses interact among them itis important to distinguish which of them are associated withthe disease symptoms

22 Post-emergence symptoms

Post-emergence damping-off symptoms occur when seedlingsdecay wilt and die after emergence (Fig 4 Boyce 1961Horst 2013) In most cases all symptoms result in the collapseand death of at least some seedlings in any given seedlingpopulation In the case of soil-borne pathogen there couldbe the death of seedlings in groups in roughly circular patchesand the seedlings may have stem lesions at ground levelSeedling stems can become thin and tough (commonly knownas ldquowirestemrdquo) which often leads to reduced seedling vigorThese symptoms can be also accompanied by leaf spottingand a complete root rot may occur Overall the symptomson the stem of the seedlings include water-soaked sunkenlesion at or slightly below the ground level and sometime alsobelow ground line (ie on the roots) causing the plant to fallover (Wright 1944 Filer and Peterson 1975) Surviving plantsare stunted and affected areas often show uneven growth

Abiotic stresses such as superficial soil heat can also leadto post-emergence seedling symptoms such as whitish lesionswhich are often located only on one side of the stem in theearly growth stage of seedlings (Hartley 1918) Such symp-toms can be distinguished from those caused by biotic stresses

because the damage owing to heat lesions is generallyscattered throughout nurseriesseedbeds which mainly de-pend on patterns of shade and heat buildup (Hartley 1921)while that caused by biotic stresses often occurs in expandingpatches Soil crusting is another important abiotic stress thatoften hinders seedling emergence or leads to stunted seedlinggrowth (Fig 5) Phytotoxicity caused by chemical fungicidesis another abiotic stress The symptoms of phytotoxicity how-ever may vary based on the type of chemical used includingmarginal necrosis chlorotic patches or spots and malformedflowers buds and young leaves (Dole andWilkins 2004) Forexample fungicides based with benzimidazole can cause re-duced plant growth and visual damage in bedding plants(Iersel and Bugbee 1996)

23 Occurrence of damping-off symptoms

Most damping-off diseases present a single sort of symptom(pre- or post-emergence) However both sorts of symptomsare also reported to some extent (Table 1) although the under-lying factors leading to the occurrence of each sort of symp-tom are poorly discussed in the literature The complexity ofdamping-off symptoms result from interactions betweencropping practices and the production situation (Aubertotand Robin 2013) This may explain the relevant lack of infor-mation This complexity involves synergism among damping-off pathogens (Al-Hazmi and Al-Nadary 2015) variation of

Fig 4 Characteristic symptoms of post-emergence damping-off ofsoybean (a and b) and corn (c and d) The succulent tissue of sproutswith aboveground shoots collapsed leading to wilting of some seedlingpopulations Soybean seedlings with stem lesions at ground level and the

death of seedlings in groups (a and b) The presence of an empty spacealong the row between corn seedlings indicates the lack of emergedseedlings due to damping-off disease (c and d) (Photo courtesy ofMartin Chilvers)

10 Page 6 of 25 Agron Sustain Dev (2017) 37 10

symptoms according to environmental conduciveness(Schwanck et al 2015) direct effect of plant density(Burdon and Chilvers 1975) and many other factors whichare very specific for each damping-off symptom For instancethe disease cycle components of damping-off are seldomdiscussed in a broader sense in the literature by comparingdifferent diseases Some factors related to the timemoment ofdisease occurrence and timing of disease cycle componentscould determine whether pre- or post-emergence symptomswill occur In this sense it is possible that for both pre- andpost-emergence damping-off the infection occurs during seedgermination but a longer or shorter incubation period mayimplicate in pre- or post-emergence damping-off In additionthe effect of individual factors involved on the disease pro-cesses from the disease cycle and the host cycle (eg seedgermination) for damping-off symptom development is rare-ly discussed in the literature Taken together several studiesvirtually explore the effect of a given factor (eg temperature)on damping-off diseases intensity (Ben-Yephet and Nelson1999) without specifying whether the factor plays a specificrole on the pathogen (eg organism metabolism) or on thehost (eg slow germination process increases time exposureunderground) Further knowledge on disease cycle featuresand processes would help better understand damping-offsymptom occurrence Although it was out of the focus of thiswork it is worth to mention that from the extensive literaturereview we did not perceive any pattern on the sort ofdamping-off symptom (pre- or post-) according to the regionthe pathogen genus or crop species affected Therefore ameta-analytical approach to test hypotheses associated withdamping-off diseases would be highly valuable to better ex-plain the factors involved in damping-off symptoms

occurrence To this aim the list of damping-off diseases weprovide in Table 1 constitutes a potential starting point

3 Integrated management of damping-off

An effective management of damping-off requires the deploy-ment of a number of strategies which can be classified into thefollowing four major groups (i) seed treatment to enhancegermination and seedling vigor (ii) deployment of resistantor tolerant cultivars to damping-off diseases (iii) adoption ofbest cropping practices and (iv) timely treatment interven-tions of seedlings with effective products (conventional pesti-cides as well as biopesticides andor biocontrol agents) Noneof these strategies is effective in managing damping-off dis-ease when applied individually and thus it requires that all ofthem are combined within the frame of IPM

31 Seed treatment to enhance germination and seedlingvigor

While the use of completely healthy seeds is the most effectivemeans to prevent andor contain damping-off diseases seedsmight not be always free from pathogens and thus wouldbenefit from treatments Even when there is no risk of con-taminated seeds from seed-borne pathogens seed treatmentscan be an effective means to increase seedling emergenceparticularly when done on seeds of low vigor and when theseed coat has been damaged (Mancini and Romanazzi 2014)

Chemical seed treatments still represent a major practice inagriculture to manage damping-off diseases (Rhodes andMyers 1989 Babadoost and Islam 2003 Howell 2007

Fig 5 Lack of sugar beet (Beta vulgaris L) seedlings emergence due tosoil crusting followed by drought The formation of soil crusts on the soilsurface represents a strong mechanical barrier which impedes seedlingsfrom being emerged Overall lack of seed germination and emergence in

such a field is characteristic of abiotic stresses including stunted growth ofseedlings without any necrosis of leaves or stems (Photo courtesy ofCarolyne Duumlrr)

Agron Sustain Dev (2017) 37 10 Page 7 of 25 10

Bradley 2007 Leisso et al 2009 Dorrance et al 2009Rothrock et al 2012 Kandel et al 2016) Several chemicalsincluding bleach hydrogen peroxide ethanol and fungicidescan be applied to remove pathogen inoculum from seed coats(Dumroese and James 2005 Mancini and Romanazzi 2014)Generally chemical treatments are effective but they can alsonegatively affect seed germination and cause phytotoxicity(Axelrood et al 1995 du Toit 2004) besides negative impactsto human health and the environment (Lamichhane et al2016) In addition to chemical treatments physical seed treat-ment can be applied including hot water hot air and electrontreatments (Mancini and Romanazzi 2014) Finally a numberof biological seed treatment methods are being developed andused in recent years with a satisfactory level of damping-offdisease suppression (Table 2)

Because seed germination and emergence are ofteninfluenced by site-specific soil and climate conditionsan in-depth knowledge of a specific site in question is aprerequisite for an effective decision-making process forseed treatments An experiment on pesticide-freeagroecosystems conducted in 2014 across eight experi-mental sites in France with non-treated seeds showedthat the percentage of emergence rates markedly differsfor the same seeds across the sites (Fig 3) In particu-lar while the rate of emergence of soft wheat was100 in the Le Rheu and Grignon sites it was loweracross other sites ranging from 43 in Auzeville to75 in Lusignan (Fig 6) This means that while seedtreatments may result essential across some sites due tounfavorable soil and climatic conditions which are con-ducive to disease development it may not be the casein other areas

32 Deployment of host-plant resistance andor tolerance

Overall host-plant resistance as a management tactic is com-posed of the following two strategies (i) deployment of resis-tant andor tolerant plant varieties which support lower path-ogen populations or better tolerate injury caused by them and(ii) the integration of such varieties with other managementtactics within the frame of IPM Unfortunately for many plantpathogens including those causing damping-off diseases noplant cultivar with measurable resistance is available(Babadoost and Islam 2003) Therefore the only way to betteruse the available crop varieties with tolerance to pathogens isthrough their adequate integration with other disease manage-ment measures Nevertheless insufficient focus has been paidto date to the integration of plant resistance with other IPMtactics and to quantifying the benefits of plant resistance inmulti-tactic IPM programs (Stout and Davis 2009)

On the other hand the breeding approach used to date todevelop resistant andor tolerant crop varieties should berevisited if we want to focus on sustainable crop protectionbased on IPM This is particularly true taking into account thefact that most if not all crop varieties bred to date are basedon a market-driven approach focused on high-yielding andmost profitable crop varieties This trend has boosted adoptionof short rotations or monoculture practices on one hand andignored the potential that minor crops may have for IPM onthe other (Messeacutean et al 2016) The limited range of availableminor crop varieties has been reported as one of the majorobstacles to crop diversification thereby confining certainbeneficial practices such as multiple cropping or intercropping(Enjalbert et al 2016 Messeacutean et al 2016) Therefore breed-ing for IPM should be based on a different approach than the

Table 2 Examples of literature reports highlighting the efficacy of non-chemical seed treatments to suppress damping-off diseases The testedformulations are most often reported to suppress both pre- and post-emergence damping-off although their effectiveness may vary in terms of diseasesuppressiveness

Crop Pathogen Formulationproduct Reference

Alfalfa Pythium spp Mineral seed coating (Samac et al 2014)Canola Pythium spp Rhizosphere bacteria (Bardin et al 2003)Corn Pythium and Fusarium spp Several biocontrol agents (Mao et al 1997 Mao et al 1998)Cotton Pythium spp Enterobacter cloacae and

Erwinia herbicola(Nelson 1988)

Cotton Pythium spp Rhizopus oryzae Trichoderma spp (Howell 2007)Cucumber Pythium ultimum Ethanol extracts of Serratia

marcescens and Trichoderma spp(Roberts et al 2016)

Cucumber Pythium spp Phosphonate (Abbasi and Lazarovits 2005 Abbasi andLazarovits 2006)

Sunflower Rhizoctonia solani Spermine (El-Metwally and Sakr 2010)Lentil pea

sugar beetPythium spp Rhizobium leguminosarum (Bardin et al 2004b Huang and Erickson 2007)

Pea Pythium spp Rhizosphere bacteria (Bardin et al 2003)Safflower Pythium spp Rhizosphere bacteria (Bardin et al 2003)Sesame Soil-borne pathogens Paenibacillus polymyxa (Ryu et al 2006)Sugar beet Pythium spp Rhizosphere bacteria crop straw powders (Bardin et al 2003 Bardin et al 2004a)Tomato and hot pepper Pythium spp Fluorescent Pseudomonads (Ramamoorthy et al 2002)

10 Page 8 of 25 Agron Sustain Dev (2017) 37 10

traditional one given the strategic role of breeding in the com-petitiveness of crops and their adaptation to more diversifiedcropping systems (Enjalbert et al 2016)

33 Adoption of best cropping practices

Once the causal agent of damping-off has been identifiedall available cropping practices could be adapted to dis-courage the development of the pathogen Indeed anytechnique that allows to reduce the time between seedgermination and emergence helps reduce effects of bioticstresses on seedlings Overall many pathogens involvedin damping-off are relatively weak pathogens which re-quire favorable environmental conditions for infection tooccur (Table 1) In addition to the susceptibility of hostand aggressiveness of pathogen populations the severityof damping-off is highly dependent on some critical fac-tors including seedbed preparation soil pH managementseeding date and rate growing density nutrition

irrigation growing environment crop sequence andintercropping cover crops soil residue management soilsolarization and tillage (Table 3) Therefore understand-ing combined effects of abiotic and biotic stresses andfactors influencing them are a prerequisite towards effec-tive IPM strategies of damping-off Once these criticalfactors have been identified which might differ fromone region to another best cropping practices should beput in place and adopted

One of the most important practices that allow to thebest management of damping-off and root diseases is fer-tilization Adequate availability of nutrients in the soil canensure higher vigor with earlier emergence that limit theperiod of time where pathogens can infect seeds and seed-lings during the autotrophic stage In particular the ad-vantages of fertilizer placement on seed germination andseedling emergence have been previously demonstrated(Cook et al 2000) The placement of fertilizers directlyunder or slightly to one side of the seed at the time ofplanting or sowing results in an increased level of seedgermination and emergence (Fig 7) This is because rel-atively immobile nutrients such as phosphorus are notreadily available for plants especially for those specieshaving no or a few lateral roots Therefore field fertiliza-tion where damping-off diseases are important requiresthat the nutrients be made easily accessible to the roots toincrease growth rate Although these nutrients do not al-ways reduce seedling infection they often enhance seedgermination and seedling vigor (Smiley et al 1990Patterson et al 1998) Indeed higher seedling vigor al-lows seedlings to rapidly escape from the soil surfaceeven in the presence of a high soil population density ofthe pathogen(s)

34 Timely treatment interventions of seedlingswith effective products

The strategies described above are mainly of preventive natureas they can be developed and adopted before the occurrence ofdamping-off diseases Once the infection occurs on seedlingsand there is a high risk of epidemic development growershave to attempt for an effective control of the diseaseOverall there are two key measures available for damping-off control as described below

341 Biological control

Because of their adverse effects on human health and theenvironment the use of conventional pesticides includingfungicides has come under increasing public scrutiny inmany countries especially in the European Union(Bourguet and Guillemaud 2016 Lamichhane et al2016) In addition increasing reports of pest resistance

Fig 6 Percentage of seed emergence (non-treated seeds) observed acrossdifferent experimental sites managed under the ldquoRes0Pestrdquo network inFrance in 2014 Res0Pest is a ldquopesticide-freerdquo trial network launched in2011 by the INRACIRAD IPM network to address objectives of theFrench National Action Plan Ecophyto to develop and demonstrate thefeasibility of pesticide-free cropping systems (Deytieux et al 2014) Eightexperimental sites comprised of five arable cropping systems (in brown)and three mixed crophusbandry systems (in green) are ongoing acrossthe sites DW durum wheat SW soft wheat MSW mixed of soft wheatvarieties SB spring barley Different percentages of emergence across theexperimental sites highlight how soil and climate and cropping practicesaffect seed germination and the seedling emergence process throughbiotic and abiotic stress Low percentages of emerged seedlings arehighlighted in red

Agron Sustain Dev (2017) 37 10 Page 9 of 25 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

Because biotic and abiotic stresses interact among them itis important to distinguish which of them are associated withthe disease symptoms

22 Post-emergence symptoms

Post-emergence damping-off symptoms occur when seedlingsdecay wilt and die after emergence (Fig 4 Boyce 1961Horst 2013) In most cases all symptoms result in the collapseand death of at least some seedlings in any given seedlingpopulation In the case of soil-borne pathogen there couldbe the death of seedlings in groups in roughly circular patchesand the seedlings may have stem lesions at ground levelSeedling stems can become thin and tough (commonly knownas ldquowirestemrdquo) which often leads to reduced seedling vigorThese symptoms can be also accompanied by leaf spottingand a complete root rot may occur Overall the symptomson the stem of the seedlings include water-soaked sunkenlesion at or slightly below the ground level and sometime alsobelow ground line (ie on the roots) causing the plant to fallover (Wright 1944 Filer and Peterson 1975) Surviving plantsare stunted and affected areas often show uneven growth

Abiotic stresses such as superficial soil heat can also leadto post-emergence seedling symptoms such as whitish lesionswhich are often located only on one side of the stem in theearly growth stage of seedlings (Hartley 1918) Such symp-toms can be distinguished from those caused by biotic stresses

because the damage owing to heat lesions is generallyscattered throughout nurseriesseedbeds which mainly de-pend on patterns of shade and heat buildup (Hartley 1921)while that caused by biotic stresses often occurs in expandingpatches Soil crusting is another important abiotic stress thatoften hinders seedling emergence or leads to stunted seedlinggrowth (Fig 5) Phytotoxicity caused by chemical fungicidesis another abiotic stress The symptoms of phytotoxicity how-ever may vary based on the type of chemical used includingmarginal necrosis chlorotic patches or spots and malformedflowers buds and young leaves (Dole andWilkins 2004) Forexample fungicides based with benzimidazole can cause re-duced plant growth and visual damage in bedding plants(Iersel and Bugbee 1996)

23 Occurrence of damping-off symptoms

Most damping-off diseases present a single sort of symptom(pre- or post-emergence) However both sorts of symptomsare also reported to some extent (Table 1) although the under-lying factors leading to the occurrence of each sort of symp-tom are poorly discussed in the literature The complexity ofdamping-off symptoms result from interactions betweencropping practices and the production situation (Aubertotand Robin 2013) This may explain the relevant lack of infor-mation This complexity involves synergism among damping-off pathogens (Al-Hazmi and Al-Nadary 2015) variation of

Fig 4 Characteristic symptoms of post-emergence damping-off ofsoybean (a and b) and corn (c and d) The succulent tissue of sproutswith aboveground shoots collapsed leading to wilting of some seedlingpopulations Soybean seedlings with stem lesions at ground level and the

death of seedlings in groups (a and b) The presence of an empty spacealong the row between corn seedlings indicates the lack of emergedseedlings due to damping-off disease (c and d) (Photo courtesy ofMartin Chilvers)

10 Page 6 of 25 Agron Sustain Dev (2017) 37 10

symptoms according to environmental conduciveness(Schwanck et al 2015) direct effect of plant density(Burdon and Chilvers 1975) and many other factors whichare very specific for each damping-off symptom For instancethe disease cycle components of damping-off are seldomdiscussed in a broader sense in the literature by comparingdifferent diseases Some factors related to the timemoment ofdisease occurrence and timing of disease cycle componentscould determine whether pre- or post-emergence symptomswill occur In this sense it is possible that for both pre- andpost-emergence damping-off the infection occurs during seedgermination but a longer or shorter incubation period mayimplicate in pre- or post-emergence damping-off In additionthe effect of individual factors involved on the disease pro-cesses from the disease cycle and the host cycle (eg seedgermination) for damping-off symptom development is rare-ly discussed in the literature Taken together several studiesvirtually explore the effect of a given factor (eg temperature)on damping-off diseases intensity (Ben-Yephet and Nelson1999) without specifying whether the factor plays a specificrole on the pathogen (eg organism metabolism) or on thehost (eg slow germination process increases time exposureunderground) Further knowledge on disease cycle featuresand processes would help better understand damping-offsymptom occurrence Although it was out of the focus of thiswork it is worth to mention that from the extensive literaturereview we did not perceive any pattern on the sort ofdamping-off symptom (pre- or post-) according to the regionthe pathogen genus or crop species affected Therefore ameta-analytical approach to test hypotheses associated withdamping-off diseases would be highly valuable to better ex-plain the factors involved in damping-off symptoms

occurrence To this aim the list of damping-off diseases weprovide in Table 1 constitutes a potential starting point

3 Integrated management of damping-off

An effective management of damping-off requires the deploy-ment of a number of strategies which can be classified into thefollowing four major groups (i) seed treatment to enhancegermination and seedling vigor (ii) deployment of resistantor tolerant cultivars to damping-off diseases (iii) adoption ofbest cropping practices and (iv) timely treatment interven-tions of seedlings with effective products (conventional pesti-cides as well as biopesticides andor biocontrol agents) Noneof these strategies is effective in managing damping-off dis-ease when applied individually and thus it requires that all ofthem are combined within the frame of IPM

31 Seed treatment to enhance germination and seedlingvigor

While the use of completely healthy seeds is the most effectivemeans to prevent andor contain damping-off diseases seedsmight not be always free from pathogens and thus wouldbenefit from treatments Even when there is no risk of con-taminated seeds from seed-borne pathogens seed treatmentscan be an effective means to increase seedling emergenceparticularly when done on seeds of low vigor and when theseed coat has been damaged (Mancini and Romanazzi 2014)

Chemical seed treatments still represent a major practice inagriculture to manage damping-off diseases (Rhodes andMyers 1989 Babadoost and Islam 2003 Howell 2007

Fig 5 Lack of sugar beet (Beta vulgaris L) seedlings emergence due tosoil crusting followed by drought The formation of soil crusts on the soilsurface represents a strong mechanical barrier which impedes seedlingsfrom being emerged Overall lack of seed germination and emergence in

such a field is characteristic of abiotic stresses including stunted growth ofseedlings without any necrosis of leaves or stems (Photo courtesy ofCarolyne Duumlrr)

Agron Sustain Dev (2017) 37 10 Page 7 of 25 10

Bradley 2007 Leisso et al 2009 Dorrance et al 2009Rothrock et al 2012 Kandel et al 2016) Several chemicalsincluding bleach hydrogen peroxide ethanol and fungicidescan be applied to remove pathogen inoculum from seed coats(Dumroese and James 2005 Mancini and Romanazzi 2014)Generally chemical treatments are effective but they can alsonegatively affect seed germination and cause phytotoxicity(Axelrood et al 1995 du Toit 2004) besides negative impactsto human health and the environment (Lamichhane et al2016) In addition to chemical treatments physical seed treat-ment can be applied including hot water hot air and electrontreatments (Mancini and Romanazzi 2014) Finally a numberof biological seed treatment methods are being developed andused in recent years with a satisfactory level of damping-offdisease suppression (Table 2)

Because seed germination and emergence are ofteninfluenced by site-specific soil and climate conditionsan in-depth knowledge of a specific site in question is aprerequisite for an effective decision-making process forseed treatments An experiment on pesticide-freeagroecosystems conducted in 2014 across eight experi-mental sites in France with non-treated seeds showedthat the percentage of emergence rates markedly differsfor the same seeds across the sites (Fig 3) In particu-lar while the rate of emergence of soft wheat was100 in the Le Rheu and Grignon sites it was loweracross other sites ranging from 43 in Auzeville to75 in Lusignan (Fig 6) This means that while seedtreatments may result essential across some sites due tounfavorable soil and climatic conditions which are con-ducive to disease development it may not be the casein other areas

32 Deployment of host-plant resistance andor tolerance

Overall host-plant resistance as a management tactic is com-posed of the following two strategies (i) deployment of resis-tant andor tolerant plant varieties which support lower path-ogen populations or better tolerate injury caused by them and(ii) the integration of such varieties with other managementtactics within the frame of IPM Unfortunately for many plantpathogens including those causing damping-off diseases noplant cultivar with measurable resistance is available(Babadoost and Islam 2003) Therefore the only way to betteruse the available crop varieties with tolerance to pathogens isthrough their adequate integration with other disease manage-ment measures Nevertheless insufficient focus has been paidto date to the integration of plant resistance with other IPMtactics and to quantifying the benefits of plant resistance inmulti-tactic IPM programs (Stout and Davis 2009)

On the other hand the breeding approach used to date todevelop resistant andor tolerant crop varieties should berevisited if we want to focus on sustainable crop protectionbased on IPM This is particularly true taking into account thefact that most if not all crop varieties bred to date are basedon a market-driven approach focused on high-yielding andmost profitable crop varieties This trend has boosted adoptionof short rotations or monoculture practices on one hand andignored the potential that minor crops may have for IPM onthe other (Messeacutean et al 2016) The limited range of availableminor crop varieties has been reported as one of the majorobstacles to crop diversification thereby confining certainbeneficial practices such as multiple cropping or intercropping(Enjalbert et al 2016 Messeacutean et al 2016) Therefore breed-ing for IPM should be based on a different approach than the

Table 2 Examples of literature reports highlighting the efficacy of non-chemical seed treatments to suppress damping-off diseases The testedformulations are most often reported to suppress both pre- and post-emergence damping-off although their effectiveness may vary in terms of diseasesuppressiveness

Crop Pathogen Formulationproduct Reference

Alfalfa Pythium spp Mineral seed coating (Samac et al 2014)Canola Pythium spp Rhizosphere bacteria (Bardin et al 2003)Corn Pythium and Fusarium spp Several biocontrol agents (Mao et al 1997 Mao et al 1998)Cotton Pythium spp Enterobacter cloacae and

Erwinia herbicola(Nelson 1988)

Cotton Pythium spp Rhizopus oryzae Trichoderma spp (Howell 2007)Cucumber Pythium ultimum Ethanol extracts of Serratia

marcescens and Trichoderma spp(Roberts et al 2016)

Cucumber Pythium spp Phosphonate (Abbasi and Lazarovits 2005 Abbasi andLazarovits 2006)

Sunflower Rhizoctonia solani Spermine (El-Metwally and Sakr 2010)Lentil pea

sugar beetPythium spp Rhizobium leguminosarum (Bardin et al 2004b Huang and Erickson 2007)

Pea Pythium spp Rhizosphere bacteria (Bardin et al 2003)Safflower Pythium spp Rhizosphere bacteria (Bardin et al 2003)Sesame Soil-borne pathogens Paenibacillus polymyxa (Ryu et al 2006)Sugar beet Pythium spp Rhizosphere bacteria crop straw powders (Bardin et al 2003 Bardin et al 2004a)Tomato and hot pepper Pythium spp Fluorescent Pseudomonads (Ramamoorthy et al 2002)

10 Page 8 of 25 Agron Sustain Dev (2017) 37 10

traditional one given the strategic role of breeding in the com-petitiveness of crops and their adaptation to more diversifiedcropping systems (Enjalbert et al 2016)

33 Adoption of best cropping practices

Once the causal agent of damping-off has been identifiedall available cropping practices could be adapted to dis-courage the development of the pathogen Indeed anytechnique that allows to reduce the time between seedgermination and emergence helps reduce effects of bioticstresses on seedlings Overall many pathogens involvedin damping-off are relatively weak pathogens which re-quire favorable environmental conditions for infection tooccur (Table 1) In addition to the susceptibility of hostand aggressiveness of pathogen populations the severityof damping-off is highly dependent on some critical fac-tors including seedbed preparation soil pH managementseeding date and rate growing density nutrition

irrigation growing environment crop sequence andintercropping cover crops soil residue management soilsolarization and tillage (Table 3) Therefore understand-ing combined effects of abiotic and biotic stresses andfactors influencing them are a prerequisite towards effec-tive IPM strategies of damping-off Once these criticalfactors have been identified which might differ fromone region to another best cropping practices should beput in place and adopted

One of the most important practices that allow to thebest management of damping-off and root diseases is fer-tilization Adequate availability of nutrients in the soil canensure higher vigor with earlier emergence that limit theperiod of time where pathogens can infect seeds and seed-lings during the autotrophic stage In particular the ad-vantages of fertilizer placement on seed germination andseedling emergence have been previously demonstrated(Cook et al 2000) The placement of fertilizers directlyunder or slightly to one side of the seed at the time ofplanting or sowing results in an increased level of seedgermination and emergence (Fig 7) This is because rel-atively immobile nutrients such as phosphorus are notreadily available for plants especially for those specieshaving no or a few lateral roots Therefore field fertiliza-tion where damping-off diseases are important requiresthat the nutrients be made easily accessible to the roots toincrease growth rate Although these nutrients do not al-ways reduce seedling infection they often enhance seedgermination and seedling vigor (Smiley et al 1990Patterson et al 1998) Indeed higher seedling vigor al-lows seedlings to rapidly escape from the soil surfaceeven in the presence of a high soil population density ofthe pathogen(s)

34 Timely treatment interventions of seedlingswith effective products

The strategies described above are mainly of preventive natureas they can be developed and adopted before the occurrence ofdamping-off diseases Once the infection occurs on seedlingsand there is a high risk of epidemic development growershave to attempt for an effective control of the diseaseOverall there are two key measures available for damping-off control as described below

341 Biological control

Because of their adverse effects on human health and theenvironment the use of conventional pesticides includingfungicides has come under increasing public scrutiny inmany countries especially in the European Union(Bourguet and Guillemaud 2016 Lamichhane et al2016) In addition increasing reports of pest resistance

Fig 6 Percentage of seed emergence (non-treated seeds) observed acrossdifferent experimental sites managed under the ldquoRes0Pestrdquo network inFrance in 2014 Res0Pest is a ldquopesticide-freerdquo trial network launched in2011 by the INRACIRAD IPM network to address objectives of theFrench National Action Plan Ecophyto to develop and demonstrate thefeasibility of pesticide-free cropping systems (Deytieux et al 2014) Eightexperimental sites comprised of five arable cropping systems (in brown)and three mixed crophusbandry systems (in green) are ongoing acrossthe sites DW durum wheat SW soft wheat MSW mixed of soft wheatvarieties SB spring barley Different percentages of emergence across theexperimental sites highlight how soil and climate and cropping practicesaffect seed germination and the seedling emergence process throughbiotic and abiotic stress Low percentages of emerged seedlings arehighlighted in red

Agron Sustain Dev (2017) 37 10 Page 9 of 25 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

symptoms according to environmental conduciveness(Schwanck et al 2015) direct effect of plant density(Burdon and Chilvers 1975) and many other factors whichare very specific for each damping-off symptom For instancethe disease cycle components of damping-off are seldomdiscussed in a broader sense in the literature by comparingdifferent diseases Some factors related to the timemoment ofdisease occurrence and timing of disease cycle componentscould determine whether pre- or post-emergence symptomswill occur In this sense it is possible that for both pre- andpost-emergence damping-off the infection occurs during seedgermination but a longer or shorter incubation period mayimplicate in pre- or post-emergence damping-off In additionthe effect of individual factors involved on the disease pro-cesses from the disease cycle and the host cycle (eg seedgermination) for damping-off symptom development is rare-ly discussed in the literature Taken together several studiesvirtually explore the effect of a given factor (eg temperature)on damping-off diseases intensity (Ben-Yephet and Nelson1999) without specifying whether the factor plays a specificrole on the pathogen (eg organism metabolism) or on thehost (eg slow germination process increases time exposureunderground) Further knowledge on disease cycle featuresand processes would help better understand damping-offsymptom occurrence Although it was out of the focus of thiswork it is worth to mention that from the extensive literaturereview we did not perceive any pattern on the sort ofdamping-off symptom (pre- or post-) according to the regionthe pathogen genus or crop species affected Therefore ameta-analytical approach to test hypotheses associated withdamping-off diseases would be highly valuable to better ex-plain the factors involved in damping-off symptoms

occurrence To this aim the list of damping-off diseases weprovide in Table 1 constitutes a potential starting point

3 Integrated management of damping-off

An effective management of damping-off requires the deploy-ment of a number of strategies which can be classified into thefollowing four major groups (i) seed treatment to enhancegermination and seedling vigor (ii) deployment of resistantor tolerant cultivars to damping-off diseases (iii) adoption ofbest cropping practices and (iv) timely treatment interven-tions of seedlings with effective products (conventional pesti-cides as well as biopesticides andor biocontrol agents) Noneof these strategies is effective in managing damping-off dis-ease when applied individually and thus it requires that all ofthem are combined within the frame of IPM

31 Seed treatment to enhance germination and seedlingvigor

While the use of completely healthy seeds is the most effectivemeans to prevent andor contain damping-off diseases seedsmight not be always free from pathogens and thus wouldbenefit from treatments Even when there is no risk of con-taminated seeds from seed-borne pathogens seed treatmentscan be an effective means to increase seedling emergenceparticularly when done on seeds of low vigor and when theseed coat has been damaged (Mancini and Romanazzi 2014)

Chemical seed treatments still represent a major practice inagriculture to manage damping-off diseases (Rhodes andMyers 1989 Babadoost and Islam 2003 Howell 2007

Fig 5 Lack of sugar beet (Beta vulgaris L) seedlings emergence due tosoil crusting followed by drought The formation of soil crusts on the soilsurface represents a strong mechanical barrier which impedes seedlingsfrom being emerged Overall lack of seed germination and emergence in

such a field is characteristic of abiotic stresses including stunted growth ofseedlings without any necrosis of leaves or stems (Photo courtesy ofCarolyne Duumlrr)

Agron Sustain Dev (2017) 37 10 Page 7 of 25 10

Bradley 2007 Leisso et al 2009 Dorrance et al 2009Rothrock et al 2012 Kandel et al 2016) Several chemicalsincluding bleach hydrogen peroxide ethanol and fungicidescan be applied to remove pathogen inoculum from seed coats(Dumroese and James 2005 Mancini and Romanazzi 2014)Generally chemical treatments are effective but they can alsonegatively affect seed germination and cause phytotoxicity(Axelrood et al 1995 du Toit 2004) besides negative impactsto human health and the environment (Lamichhane et al2016) In addition to chemical treatments physical seed treat-ment can be applied including hot water hot air and electrontreatments (Mancini and Romanazzi 2014) Finally a numberof biological seed treatment methods are being developed andused in recent years with a satisfactory level of damping-offdisease suppression (Table 2)

Because seed germination and emergence are ofteninfluenced by site-specific soil and climate conditionsan in-depth knowledge of a specific site in question is aprerequisite for an effective decision-making process forseed treatments An experiment on pesticide-freeagroecosystems conducted in 2014 across eight experi-mental sites in France with non-treated seeds showedthat the percentage of emergence rates markedly differsfor the same seeds across the sites (Fig 3) In particu-lar while the rate of emergence of soft wheat was100 in the Le Rheu and Grignon sites it was loweracross other sites ranging from 43 in Auzeville to75 in Lusignan (Fig 6) This means that while seedtreatments may result essential across some sites due tounfavorable soil and climatic conditions which are con-ducive to disease development it may not be the casein other areas

32 Deployment of host-plant resistance andor tolerance

Overall host-plant resistance as a management tactic is com-posed of the following two strategies (i) deployment of resis-tant andor tolerant plant varieties which support lower path-ogen populations or better tolerate injury caused by them and(ii) the integration of such varieties with other managementtactics within the frame of IPM Unfortunately for many plantpathogens including those causing damping-off diseases noplant cultivar with measurable resistance is available(Babadoost and Islam 2003) Therefore the only way to betteruse the available crop varieties with tolerance to pathogens isthrough their adequate integration with other disease manage-ment measures Nevertheless insufficient focus has been paidto date to the integration of plant resistance with other IPMtactics and to quantifying the benefits of plant resistance inmulti-tactic IPM programs (Stout and Davis 2009)

On the other hand the breeding approach used to date todevelop resistant andor tolerant crop varieties should berevisited if we want to focus on sustainable crop protectionbased on IPM This is particularly true taking into account thefact that most if not all crop varieties bred to date are basedon a market-driven approach focused on high-yielding andmost profitable crop varieties This trend has boosted adoptionof short rotations or monoculture practices on one hand andignored the potential that minor crops may have for IPM onthe other (Messeacutean et al 2016) The limited range of availableminor crop varieties has been reported as one of the majorobstacles to crop diversification thereby confining certainbeneficial practices such as multiple cropping or intercropping(Enjalbert et al 2016 Messeacutean et al 2016) Therefore breed-ing for IPM should be based on a different approach than the

Table 2 Examples of literature reports highlighting the efficacy of non-chemical seed treatments to suppress damping-off diseases The testedformulations are most often reported to suppress both pre- and post-emergence damping-off although their effectiveness may vary in terms of diseasesuppressiveness

Crop Pathogen Formulationproduct Reference

Alfalfa Pythium spp Mineral seed coating (Samac et al 2014)Canola Pythium spp Rhizosphere bacteria (Bardin et al 2003)Corn Pythium and Fusarium spp Several biocontrol agents (Mao et al 1997 Mao et al 1998)Cotton Pythium spp Enterobacter cloacae and

Erwinia herbicola(Nelson 1988)

Cotton Pythium spp Rhizopus oryzae Trichoderma spp (Howell 2007)Cucumber Pythium ultimum Ethanol extracts of Serratia

marcescens and Trichoderma spp(Roberts et al 2016)

Cucumber Pythium spp Phosphonate (Abbasi and Lazarovits 2005 Abbasi andLazarovits 2006)

Sunflower Rhizoctonia solani Spermine (El-Metwally and Sakr 2010)Lentil pea

sugar beetPythium spp Rhizobium leguminosarum (Bardin et al 2004b Huang and Erickson 2007)

Pea Pythium spp Rhizosphere bacteria (Bardin et al 2003)Safflower Pythium spp Rhizosphere bacteria (Bardin et al 2003)Sesame Soil-borne pathogens Paenibacillus polymyxa (Ryu et al 2006)Sugar beet Pythium spp Rhizosphere bacteria crop straw powders (Bardin et al 2003 Bardin et al 2004a)Tomato and hot pepper Pythium spp Fluorescent Pseudomonads (Ramamoorthy et al 2002)

10 Page 8 of 25 Agron Sustain Dev (2017) 37 10

traditional one given the strategic role of breeding in the com-petitiveness of crops and their adaptation to more diversifiedcropping systems (Enjalbert et al 2016)

33 Adoption of best cropping practices

Once the causal agent of damping-off has been identifiedall available cropping practices could be adapted to dis-courage the development of the pathogen Indeed anytechnique that allows to reduce the time between seedgermination and emergence helps reduce effects of bioticstresses on seedlings Overall many pathogens involvedin damping-off are relatively weak pathogens which re-quire favorable environmental conditions for infection tooccur (Table 1) In addition to the susceptibility of hostand aggressiveness of pathogen populations the severityof damping-off is highly dependent on some critical fac-tors including seedbed preparation soil pH managementseeding date and rate growing density nutrition

irrigation growing environment crop sequence andintercropping cover crops soil residue management soilsolarization and tillage (Table 3) Therefore understand-ing combined effects of abiotic and biotic stresses andfactors influencing them are a prerequisite towards effec-tive IPM strategies of damping-off Once these criticalfactors have been identified which might differ fromone region to another best cropping practices should beput in place and adopted

One of the most important practices that allow to thebest management of damping-off and root diseases is fer-tilization Adequate availability of nutrients in the soil canensure higher vigor with earlier emergence that limit theperiod of time where pathogens can infect seeds and seed-lings during the autotrophic stage In particular the ad-vantages of fertilizer placement on seed germination andseedling emergence have been previously demonstrated(Cook et al 2000) The placement of fertilizers directlyunder or slightly to one side of the seed at the time ofplanting or sowing results in an increased level of seedgermination and emergence (Fig 7) This is because rel-atively immobile nutrients such as phosphorus are notreadily available for plants especially for those specieshaving no or a few lateral roots Therefore field fertiliza-tion where damping-off diseases are important requiresthat the nutrients be made easily accessible to the roots toincrease growth rate Although these nutrients do not al-ways reduce seedling infection they often enhance seedgermination and seedling vigor (Smiley et al 1990Patterson et al 1998) Indeed higher seedling vigor al-lows seedlings to rapidly escape from the soil surfaceeven in the presence of a high soil population density ofthe pathogen(s)

34 Timely treatment interventions of seedlingswith effective products

The strategies described above are mainly of preventive natureas they can be developed and adopted before the occurrence ofdamping-off diseases Once the infection occurs on seedlingsand there is a high risk of epidemic development growershave to attempt for an effective control of the diseaseOverall there are two key measures available for damping-off control as described below

341 Biological control

Because of their adverse effects on human health and theenvironment the use of conventional pesticides includingfungicides has come under increasing public scrutiny inmany countries especially in the European Union(Bourguet and Guillemaud 2016 Lamichhane et al2016) In addition increasing reports of pest resistance

Fig 6 Percentage of seed emergence (non-treated seeds) observed acrossdifferent experimental sites managed under the ldquoRes0Pestrdquo network inFrance in 2014 Res0Pest is a ldquopesticide-freerdquo trial network launched in2011 by the INRACIRAD IPM network to address objectives of theFrench National Action Plan Ecophyto to develop and demonstrate thefeasibility of pesticide-free cropping systems (Deytieux et al 2014) Eightexperimental sites comprised of five arable cropping systems (in brown)and three mixed crophusbandry systems (in green) are ongoing acrossthe sites DW durum wheat SW soft wheat MSW mixed of soft wheatvarieties SB spring barley Different percentages of emergence across theexperimental sites highlight how soil and climate and cropping practicesaffect seed germination and the seedling emergence process throughbiotic and abiotic stress Low percentages of emerged seedlings arehighlighted in red

Agron Sustain Dev (2017) 37 10 Page 9 of 25 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

Bradley 2007 Leisso et al 2009 Dorrance et al 2009Rothrock et al 2012 Kandel et al 2016) Several chemicalsincluding bleach hydrogen peroxide ethanol and fungicidescan be applied to remove pathogen inoculum from seed coats(Dumroese and James 2005 Mancini and Romanazzi 2014)Generally chemical treatments are effective but they can alsonegatively affect seed germination and cause phytotoxicity(Axelrood et al 1995 du Toit 2004) besides negative impactsto human health and the environment (Lamichhane et al2016) In addition to chemical treatments physical seed treat-ment can be applied including hot water hot air and electrontreatments (Mancini and Romanazzi 2014) Finally a numberof biological seed treatment methods are being developed andused in recent years with a satisfactory level of damping-offdisease suppression (Table 2)

Because seed germination and emergence are ofteninfluenced by site-specific soil and climate conditionsan in-depth knowledge of a specific site in question is aprerequisite for an effective decision-making process forseed treatments An experiment on pesticide-freeagroecosystems conducted in 2014 across eight experi-mental sites in France with non-treated seeds showedthat the percentage of emergence rates markedly differsfor the same seeds across the sites (Fig 3) In particu-lar while the rate of emergence of soft wheat was100 in the Le Rheu and Grignon sites it was loweracross other sites ranging from 43 in Auzeville to75 in Lusignan (Fig 6) This means that while seedtreatments may result essential across some sites due tounfavorable soil and climatic conditions which are con-ducive to disease development it may not be the casein other areas

32 Deployment of host-plant resistance andor tolerance

Overall host-plant resistance as a management tactic is com-posed of the following two strategies (i) deployment of resis-tant andor tolerant plant varieties which support lower path-ogen populations or better tolerate injury caused by them and(ii) the integration of such varieties with other managementtactics within the frame of IPM Unfortunately for many plantpathogens including those causing damping-off diseases noplant cultivar with measurable resistance is available(Babadoost and Islam 2003) Therefore the only way to betteruse the available crop varieties with tolerance to pathogens isthrough their adequate integration with other disease manage-ment measures Nevertheless insufficient focus has been paidto date to the integration of plant resistance with other IPMtactics and to quantifying the benefits of plant resistance inmulti-tactic IPM programs (Stout and Davis 2009)

On the other hand the breeding approach used to date todevelop resistant andor tolerant crop varieties should berevisited if we want to focus on sustainable crop protectionbased on IPM This is particularly true taking into account thefact that most if not all crop varieties bred to date are basedon a market-driven approach focused on high-yielding andmost profitable crop varieties This trend has boosted adoptionof short rotations or monoculture practices on one hand andignored the potential that minor crops may have for IPM onthe other (Messeacutean et al 2016) The limited range of availableminor crop varieties has been reported as one of the majorobstacles to crop diversification thereby confining certainbeneficial practices such as multiple cropping or intercropping(Enjalbert et al 2016 Messeacutean et al 2016) Therefore breed-ing for IPM should be based on a different approach than the

Table 2 Examples of literature reports highlighting the efficacy of non-chemical seed treatments to suppress damping-off diseases The testedformulations are most often reported to suppress both pre- and post-emergence damping-off although their effectiveness may vary in terms of diseasesuppressiveness

Crop Pathogen Formulationproduct Reference

Alfalfa Pythium spp Mineral seed coating (Samac et al 2014)Canola Pythium spp Rhizosphere bacteria (Bardin et al 2003)Corn Pythium and Fusarium spp Several biocontrol agents (Mao et al 1997 Mao et al 1998)Cotton Pythium spp Enterobacter cloacae and

Erwinia herbicola(Nelson 1988)

Cotton Pythium spp Rhizopus oryzae Trichoderma spp (Howell 2007)Cucumber Pythium ultimum Ethanol extracts of Serratia

marcescens and Trichoderma spp(Roberts et al 2016)

Cucumber Pythium spp Phosphonate (Abbasi and Lazarovits 2005 Abbasi andLazarovits 2006)

Sunflower Rhizoctonia solani Spermine (El-Metwally and Sakr 2010)Lentil pea

sugar beetPythium spp Rhizobium leguminosarum (Bardin et al 2004b Huang and Erickson 2007)

Pea Pythium spp Rhizosphere bacteria (Bardin et al 2003)Safflower Pythium spp Rhizosphere bacteria (Bardin et al 2003)Sesame Soil-borne pathogens Paenibacillus polymyxa (Ryu et al 2006)Sugar beet Pythium spp Rhizosphere bacteria crop straw powders (Bardin et al 2003 Bardin et al 2004a)Tomato and hot pepper Pythium spp Fluorescent Pseudomonads (Ramamoorthy et al 2002)

10 Page 8 of 25 Agron Sustain Dev (2017) 37 10

traditional one given the strategic role of breeding in the com-petitiveness of crops and their adaptation to more diversifiedcropping systems (Enjalbert et al 2016)

33 Adoption of best cropping practices

Once the causal agent of damping-off has been identifiedall available cropping practices could be adapted to dis-courage the development of the pathogen Indeed anytechnique that allows to reduce the time between seedgermination and emergence helps reduce effects of bioticstresses on seedlings Overall many pathogens involvedin damping-off are relatively weak pathogens which re-quire favorable environmental conditions for infection tooccur (Table 1) In addition to the susceptibility of hostand aggressiveness of pathogen populations the severityof damping-off is highly dependent on some critical fac-tors including seedbed preparation soil pH managementseeding date and rate growing density nutrition

irrigation growing environment crop sequence andintercropping cover crops soil residue management soilsolarization and tillage (Table 3) Therefore understand-ing combined effects of abiotic and biotic stresses andfactors influencing them are a prerequisite towards effec-tive IPM strategies of damping-off Once these criticalfactors have been identified which might differ fromone region to another best cropping practices should beput in place and adopted

One of the most important practices that allow to thebest management of damping-off and root diseases is fer-tilization Adequate availability of nutrients in the soil canensure higher vigor with earlier emergence that limit theperiod of time where pathogens can infect seeds and seed-lings during the autotrophic stage In particular the ad-vantages of fertilizer placement on seed germination andseedling emergence have been previously demonstrated(Cook et al 2000) The placement of fertilizers directlyunder or slightly to one side of the seed at the time ofplanting or sowing results in an increased level of seedgermination and emergence (Fig 7) This is because rel-atively immobile nutrients such as phosphorus are notreadily available for plants especially for those specieshaving no or a few lateral roots Therefore field fertiliza-tion where damping-off diseases are important requiresthat the nutrients be made easily accessible to the roots toincrease growth rate Although these nutrients do not al-ways reduce seedling infection they often enhance seedgermination and seedling vigor (Smiley et al 1990Patterson et al 1998) Indeed higher seedling vigor al-lows seedlings to rapidly escape from the soil surfaceeven in the presence of a high soil population density ofthe pathogen(s)

34 Timely treatment interventions of seedlingswith effective products

The strategies described above are mainly of preventive natureas they can be developed and adopted before the occurrence ofdamping-off diseases Once the infection occurs on seedlingsand there is a high risk of epidemic development growershave to attempt for an effective control of the diseaseOverall there are two key measures available for damping-off control as described below

341 Biological control

Because of their adverse effects on human health and theenvironment the use of conventional pesticides includingfungicides has come under increasing public scrutiny inmany countries especially in the European Union(Bourguet and Guillemaud 2016 Lamichhane et al2016) In addition increasing reports of pest resistance

Fig 6 Percentage of seed emergence (non-treated seeds) observed acrossdifferent experimental sites managed under the ldquoRes0Pestrdquo network inFrance in 2014 Res0Pest is a ldquopesticide-freerdquo trial network launched in2011 by the INRACIRAD IPM network to address objectives of theFrench National Action Plan Ecophyto to develop and demonstrate thefeasibility of pesticide-free cropping systems (Deytieux et al 2014) Eightexperimental sites comprised of five arable cropping systems (in brown)and three mixed crophusbandry systems (in green) are ongoing acrossthe sites DW durum wheat SW soft wheat MSW mixed of soft wheatvarieties SB spring barley Different percentages of emergence across theexperimental sites highlight how soil and climate and cropping practicesaffect seed germination and the seedling emergence process throughbiotic and abiotic stress Low percentages of emerged seedlings arehighlighted in red

Agron Sustain Dev (2017) 37 10 Page 9 of 25 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

traditional one given the strategic role of breeding in the com-petitiveness of crops and their adaptation to more diversifiedcropping systems (Enjalbert et al 2016)

33 Adoption of best cropping practices

Once the causal agent of damping-off has been identifiedall available cropping practices could be adapted to dis-courage the development of the pathogen Indeed anytechnique that allows to reduce the time between seedgermination and emergence helps reduce effects of bioticstresses on seedlings Overall many pathogens involvedin damping-off are relatively weak pathogens which re-quire favorable environmental conditions for infection tooccur (Table 1) In addition to the susceptibility of hostand aggressiveness of pathogen populations the severityof damping-off is highly dependent on some critical fac-tors including seedbed preparation soil pH managementseeding date and rate growing density nutrition

irrigation growing environment crop sequence andintercropping cover crops soil residue management soilsolarization and tillage (Table 3) Therefore understand-ing combined effects of abiotic and biotic stresses andfactors influencing them are a prerequisite towards effec-tive IPM strategies of damping-off Once these criticalfactors have been identified which might differ fromone region to another best cropping practices should beput in place and adopted

One of the most important practices that allow to thebest management of damping-off and root diseases is fer-tilization Adequate availability of nutrients in the soil canensure higher vigor with earlier emergence that limit theperiod of time where pathogens can infect seeds and seed-lings during the autotrophic stage In particular the ad-vantages of fertilizer placement on seed germination andseedling emergence have been previously demonstrated(Cook et al 2000) The placement of fertilizers directlyunder or slightly to one side of the seed at the time ofplanting or sowing results in an increased level of seedgermination and emergence (Fig 7) This is because rel-atively immobile nutrients such as phosphorus are notreadily available for plants especially for those specieshaving no or a few lateral roots Therefore field fertiliza-tion where damping-off diseases are important requiresthat the nutrients be made easily accessible to the roots toincrease growth rate Although these nutrients do not al-ways reduce seedling infection they often enhance seedgermination and seedling vigor (Smiley et al 1990Patterson et al 1998) Indeed higher seedling vigor al-lows seedlings to rapidly escape from the soil surfaceeven in the presence of a high soil population density ofthe pathogen(s)

34 Timely treatment interventions of seedlingswith effective products

The strategies described above are mainly of preventive natureas they can be developed and adopted before the occurrence ofdamping-off diseases Once the infection occurs on seedlingsand there is a high risk of epidemic development growershave to attempt for an effective control of the diseaseOverall there are two key measures available for damping-off control as described below

341 Biological control

Because of their adverse effects on human health and theenvironment the use of conventional pesticides includingfungicides has come under increasing public scrutiny inmany countries especially in the European Union(Bourguet and Guillemaud 2016 Lamichhane et al2016) In addition increasing reports of pest resistance

Fig 6 Percentage of seed emergence (non-treated seeds) observed acrossdifferent experimental sites managed under the ldquoRes0Pestrdquo network inFrance in 2014 Res0Pest is a ldquopesticide-freerdquo trial network launched in2011 by the INRACIRAD IPM network to address objectives of theFrench National Action Plan Ecophyto to develop and demonstrate thefeasibility of pesticide-free cropping systems (Deytieux et al 2014) Eightexperimental sites comprised of five arable cropping systems (in brown)and three mixed crophusbandry systems (in green) are ongoing acrossthe sites DW durum wheat SW soft wheat MSW mixed of soft wheatvarieties SB spring barley Different percentages of emergence across theexperimental sites highlight how soil and climate and cropping practicesaffect seed germination and the seedling emergence process throughbiotic and abiotic stress Low percentages of emerged seedlings arehighlighted in red

Agron Sustain Dev (2017) 37 10 Page 9 of 25 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

development to pesticides have become an issue therebyincreasing risks of pest management failure with potentialthreats of economic losses for farmers (Onstad 2013Bourguet and Guillemaud 2016 Lamichhane et al2016) Chemical fungicides can also cause phytotoxicityon crops and foliage plants which is another drawback oftheir use (Dias 2012)

The application of biocontrol agentsformulations isan important substitute to conventional fungicides withlower negative impacts Often biocontrol is widelypracticed as an alternative disease management strategyto conventional fungicides especially when the latter arenot effective or cause secondary problems such as seedphytotoxicity from fungicides (Burns and Benson 2000)Individual beneficial organisms used as biocontrolagents can prevent damping-off pathogens through fivemechanisms (Table 4) There are dozens of biocontrol

products to control damping-off worldwide and most ofthem are based on antagonist fungi includingTrichoderma spp and Gliocladium spp or bacteria suchas Pseudomonas spp and Bacillus spp (Table 5)However not all of them are registered and marketedas biocontrol agents nor they are used as plant growthpromoters plant strengtheners (or biostimulants) or soilconditioners (Paulitz and Beacutelanger 2001) Numerousstudies conducted on biocontrol research in the last15 years clearly suggest the increasing concern of thescientific community to generate knowledge on an alter-native to chemical solutions (Table 5) Most of thesestudies have also demonstrated a good effectiveness ofb iocon t ro l produc ts in managing the disease Accordingly the biocontrol industry has become verydynamic in recent years especially in terms of usingthe available scientific knowledge to develop and

Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development

Critical factors Best cropping practices References

Seed quality Use of clean healthy and sterile seeds treatments withnon-chemical products including beneficial microbes toenhance seed health and resilience and to promote rapidgermination and emergence and control pre-emergencedamping-off and chemical treatment to controlpost-emergence damping-off

(Mao et al 1998 Babadoost and Islam 2003 Jensenet al 2004 Abbasi and Lazarovits 2006 Howell2007 Gwinn et al 2010 Mastouri et al 2010Samac et al 2014 Roberts et al 2016)

Seedbed preparation Utilize pest-free soil or growing medium through incorporation ofcompost plant residues or microbial amendments into soil orgrowing medium which suppress soil-borne pathogensperform soil solarization bio-fumigation adopt mixture ofparticle sizes and good porosity to avoid soil crusting improvesoil drainage by subsoiling crowning the beds installingdrainage tiles and incorporating composted organic matter toimprove soil texture water-holding capacity nutrientavailability and cation exchange capacity

(Kassaby 1985 Ben-Yephet and Nelson 1999 Duumlrr andAubertot 2000 Diab et al 2003 Deadman et al2006 Njoroge et al 2008 Pane et al 2011 He et al2011 Landis 2013 Bahramisharif et al 2013aVitale et al 2013)

Adjustment of soil pH Use relatively acidic soils with a low pH (45ndash60) increase soilpH with organic amendments with applications of aluminumsulfate sulfur or acid peat

(Russell 1990 Davey 1996 Cram 2003)

Seeding date Perform sowing neither too early nor too late avoid warm or wetweather for sowing well irrigate soils to the depth of thegrowing roots without flooding the soil

(Hwang et al 2000 Cram 2003)

Growing density Avoid over-sowing or excessive plant densities use crop varietieswith asynchronous germination

(Burdon and Chilvers 1975 Neher et al 1987 Landis2013)

Nutrition Apply well-balanced fertilization especially microelements(phosphorus potassium and calcium)

(Gladstone and Moorman 1989 James 1997El-Metwally and Sakr 2010 Landis 2013)

Growing environment Maintain moderate humidity escape application of high watervolume to avoid waterlogging and adopt frequent and lightapplications maintain adequate light and optimal temperatures

(Beech 1949 Duniway 1983b Wong et al 1984Yitbarek et al 1988 Hwang et al 2000 Schmidtet al 2004 Kiyumi 2009 Landis 2013 Li et al2014)

Crop sequence andintercropping

Avoid monoculture and adopt long rotation schemes to lowerdown pathogen populations introduce Brassica crops as theirroot exudates contain soil-borne pathogen populations

(Hwang et al 2008 Abdel-Monaim and Abo-Elyousr2012)

Cover crops and soil residuemanagement

While cover crops are overall useful to produce organic mattersand protect the soil from erosion and leaching their benefit canvary with the type of species selected Certain leguminouscover crops even favor greater populations of damping-offpathogens than graminaceous plants

(Hansen et al 1990 Russell 1990 Davey 1996 Baileyand Lazarovits 2003)

Tillage Perform tillage to incorporate plant residues into the soil to reducesoil-borne pathogen populations although the effect of tillagemay differ from the type of pathogen to be managed

(Tachibana 1983 Workneh et al 1998 Bailey andLazarovits 2003)

10 Page 10 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

commercialize formulations However most of theseformulations are based on individual biocontrol agentsand they specifically target a specific pathogen

342 Chemical control

While alternative tactics to chemical control are the priorityfor IPM to manage damping-off diseases such measuresavailable on the market are not always effective in controllingdamping-off diseases andor their effectiveness is variableTherefore a judicious use of fungicides maybe needed tocombine with other IPM tactics especially when the diseaseinfection has already occurred (Harman 2000)

Chemical control of damping-off as foliar applicationhowever is restricted to a few active ingredients due to thehigh cost of fungicides and the small number of productsregistered for some crops including those for ornamental use(Garzoacuten et al 2011) Among the most frequently used fungi-cides there are etridiazole and metalaxyl active againstPhytopthora and Pythium spp benomyl and thiophanatemethyl active against Fusarium and Rhizoctonia sppmancozeb and maneb active against Fusarium andPhythium spp and captan active against commondamping-off pathogens A rapid decrease in market availabil-ity of many previously available fungicides further limits ac-cess to chemical treatments inmany countries especially in theEuropean Union (Lamichhane et al 2016) On the other handresistance to commonly used fungicides developed by severalstrains of pathogens has challenged the long-term sustainabil-ity of chemical control (Taylor et al 2002 Allain-Bouleacute et al2004 Moorman and Kim 2004 Reeleder et al 2007 Weilandet al 2014) All these new scenarios clearly highlight that non-chemical measures will be increasingly developed and used

for the management of damping-off particularly for post-emergence ones This trend is clear also in the literature wheremost recent research efforts are on the development of biocon-trol solutions rather than focusing on the chemical ones(Tables 2 and 5) This happens due to the general concernswith regards to conventional pesticides but also because pri-vate and public sectors can design new solutions for the so-called ldquobiocontrol marketrdquo However even with biocontrolsolutions diagnosis of the involved pathogens along withthe analysis of treatment opportunity is still required

4 Key challenges and future prioritiesfor damping-off management

In order to tackle the complex and multifaceted nature ofdamping-off diseases and a range of factors that affect theiroccurrence and development we propose five research prior-ities which are essential towards a better understanding andmanagement of damping-off diseases

41 Correct identification of damping-off pathogensincluding non-secondary colonizers and anastomosisgroups

An accurate identification of the causal agent(s) associatedwith damping-off is imperative for understanding the etiologyof damping-off outbreaks and thus represents a cornerstonefor the decision-making process to IPM This involvesconfirming the pest learning how it spreads and then identi-fying critical points for its management including develop-ment of preventive measures based on adapted cropping prac-tices Most often the specific pathogen causing damping-off

Fig 7 Effect of fertilizer placement on germination and emergence ofoilseed rape While the placement of micronutrients (zinc andphosphorous) at the time of sowing allowed seeds to readily germinateand emerge (the three lateral sides of the plot) the lack of nutrientplacement has resulted in markedly reduced seed germination and

emergence (the middle of the plot) The same field practices wereapplied in the field including the same date of sowing and cultivar Inaddition to oilseed rape the cultivated field presents annual weed Poaannua and Vulpia myuros (light green color) (Photo courtesy of Jean-Pierre Sarthou)

Agron Sustain Dev (2017) 37 10 Page 11 of 25 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

cannot be determined based on the visual inspections of symp-toms Therefore their correct identification is essential It isgenerally performed using both culture-based and culture-independent methods However both of these techniqueshave their advantages and drawbacks and hence are comple-mentary to each other For example culture-based techniquesallow for the characterization of important traits such as viru-lence or fungicide resistance Not only are they time consum-ing but they also underestimate the true diversity of species

present within a sample (Zinger et al 2012 James 2012b Biket al 2016) Culture-independent methods such as next gen-eration sequencing on the other hand allow to identify theoverall species diversity present in a given sample but theirlimit is that they do not allow to determine the virulence andfungicide resistance of the microbes associated with the dis-ease (Lamichhane and Venturi 2015)

Although many modern PCR techniques allow a rapid de-tection and identification of one or more specific pathogens

Table 4 Key mechanisms involved in biocontrol activities and list of selected references

Mechanism Description References

Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one ormore pathogens

(Shang et al 1999 Wright et al 2001 Koumoutsi et al 2004Kloepper et al 2004 Islam et al 2005 Leclere et al 2005Pal and McSpadden 2006 Gerbore et al 2014)

Parasitism A biocontrol organism parasitizes one or more pathogens This is a typicalexample of Trichoderma spp which winds around the hyphae ofsoil-borne fungi and oomycetes by puncturing their cell wall

(Benhamou and Chet 1997 Kiss 2003 Milgroom and Cortesi2004 Pal and McSpadden 2006 Gerbore et al 2014)

Competition for nutrients A biocontrol organism produces and releases many substances that havesuppressive effects towards pathogens This help a biocontrol agent toeffectively colonize plant environments

(van Dijk and Nelson 2000 Kageyama and Nelson 2003 Paland McSpadden 2006 Liu et al 2013 Gerbore et al 2014)

Production of lytic enzymes or otherchemical signals

A biocontrol organism produces metabolites that can interfere withpathogen growth andor activities via degradation of essentialcompounds needed for soil-borne pathogens to develop and start theinfection process

(Bull et al 2002 Kilic-Ekici and Yuen 2003 Benhamou 2004Palumbo et al 2005 de los Santos-Villalobos et al 2013Gerbore et al 2014)

Induced systemic resistance (ISR) A beneficial organism stimulates the plantrsquos immune system therebyprotecting plants from pathogens ISR is a different mechanism fromsystemic acquired resistance (SAR) The latter occurs following anexposition of a plant to a low level of a specific pathogen which allowsplants to acquire resistance to that specific pathogen in the future

(Chen et al 2000 Hammond-Kosack and Jones 2000Bargabus et al 2002 Bargabus et al 2004 Ongena et al2004 Kloepper et al 2004 Meziane et al 2005 Pal andMcSpadden 2006 Gerbore et al 2014 Pieterse et al 2014)

Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since2001 These biological control agents were either applied to seedlings or to soil to achieve disease suppression

Pathogen(s) Host Biological control agent(s) References

Pythium spp Tomato Different bacteria (Gravel et al 2005)

Pythium aphanidermatum Cucumber Paenibacillus spp with organic compoundsStreptomyces griseoviridis Trichoderma sppGliocladium catenulatum

(Punja and Yip 2003 Li et al 2011)

Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al 2006)

Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al 2002 Carisseet al 2003)

Pythium ultimum andRhizoctonia solani

Bedding plants Gliocladium catenulatum (Mcquilken et al 2001)

Rhizoctonia spp Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al 2015)

Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43 Glomus mosseae andplant growth-promoting fungi Paenibacillusillinoisensis

(Jung et al 2003 Chandanie et al2009 Huang et al 2012)

Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al 2008)

Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al 2008)

Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002)

Rhizoctonia solani Different crops Trichoderma spp (Lewis and Lumsden 2001)

Rhizoctonia solani andFusarium solani

Tomato Olive mill waste water and its indigenous bacteria (Yangui et al 2008)

Rhizoctonia spp Cotton Nonpathogenic Binucleate Rhizoctonia spp (Jabaji-Hare and Neate 2005)

Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al 2005)

10 Page 12 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

including those reported to cause damping-off diseases(Weiland and Sundsbak 2000 Lievens et al 2006 Ishiguroet al 2013) the timely identification of the overall speciesdiversity involved in the disease occurrence process stillremains a challenge In addition such techniques re-quire DNA purification the availability of more expen-sive and sophisticated equipment and more highlytrained technical personnel to perform the test(Schroeder et al 2012) which is a strong limit to theirwider adoption Therefore we still need to developtechniques which could simplify the detection on onehand and be economically sustainable on the other

All four soil-borne pathogens dealt in this paper are char-acterized by a complex of genetically distinct species with awide host range or virulence preference for certain hosts Forexample Rhizoctonia solani species Kuumlhn (teleomorphThanatephorus cucumeris A B Frank Donk) is a multinu-cleate species that has been divided into 14 anastomosisgroups (AGs AG1 to AG13 and AG B1 (Sneh et al 1991Carling and Summer 1992 Carling et al 2002) BinucleateRhizoctonia spp (teleomorph Ceratobasidium) are dividedinto 19 AGs (AG A to AG S) Finally R oryzae and R zeaeare multinucleate with the teleomorphs Waitea circinata varcircinata and W circinata var zeae respectively (Sneh et al1991) Given its variable nature within- and between-AG var-iation in virulence and host range a correct and timely iden-tification of the specific genetic lines associated withdamping-off diseases is still a challenge which calls for fur-ther research efforts

Fusarium spp are characterized by a wide genetic diversityand their taxonomy has been afflicted by changing speciesconcepts with as few as 9 to over 1000 species being recog-nized by different taxonomists during the past 100 years(Summerell et al 2003) Indeed the complexity and the rec-ognized difficulty of rapidly identifying cultures to specieshave been reported as the major reason hindering effectivedisease management (Summerell et al 2003) The challengewithin the Fusarium species complex is also to determine thespecific role of secondary colonizers in occurrence and devel-opment of damping-off diseases since they are characterizedby a high variability and complexity in terms of host range andvirulence

Similar problems exist also for Pythium species with mostplant-pathogenic lines having a wide host range For examplePythium ultimum is reported to attack over 719 host plants(Farr and Rossman 2012) Other species such as Pythiumgraminicola and Pythium arrhenomanes are restricted onlyto Poaceae family (Schroeder et al 2012) Traditional baitingor other culture-based techniques are still widely used for theidentification of Pythium species although culture-independent methods such as cytochrome oxidase subunit 1pyrosequencing are also used (Coffua et al 2016) The chal-lenge is that methodological biases inherent to culture-

independent methods may often lead to inconsistencies in di-versity estimates of Pythium species associated with damping-off diseases Nevertheless culture-based techniques are theonly means to demonstrate for example the presence of po-tential pathogens even in fields with no previous history ofdamping-off diseases Indeed based on culture-based tech-niques several studies have isolated Pythium species fromsymptomatic and asymptomatic plants and demonstrated theirpathogenicity on a large number of plant species(Bahramisharif et al 2013b Coffua et al 2016) Furtherculture-based methods and morphological observations may stillresult essential in confirming the presence of novel or unexpectedspecies within a sampling location and thus have to be consid-ered for identification purposes (Zitnick-Anderson and Nelson2014)

The complexity in terms of taxonomy is even more accen-tuated for the genus Phytophthora with many studies overrecent years recognizing different Phytophthora as a speciescomplex Often the taxonomic status of the related species isalso a matter of controversy or the presence of several distinctlineages perhaps representing as yet undescribed species(Safaiefarahani et al 2015) Many new species ofPhytophthora are constantly proposed and the taxonomy ofthis genus has been evolving very dynamically (Henricot et al2014) Consequently development of rapid and reliable diag-nostic methods is a challenging task for this genus too

Because most damping-off pathogens are either soil-or water-borne instead of airborne adoption of goodphytosanitary practices generally allows to managedamping-off diseases This is especially the case if aproper detection of the causal agent(s) is timely madeThis helps understand also critical management pointsthat allow pathogens to enter into the field andor nurs-ery The mode of transmission maybe different for eachpathogen although spread in infected soil or growingmedium is common to all species (Table 6) Becausemost of these pathogens are common in agriculturalsoils they can be spread via contaminated soil introduc-tion of infected plants (mainly in case of seed-bornepathogens) improperly sanitized equipment and green-house and the use of contaminated irrigation water(Zappia et al 2014) In particular Pythium spp andPhytophthora spp have motile zoospores which aremost commonly spread by water leading to epidemicdevelopments (Hong and Moorman 2005 Zappia et al2014) Therefore the potential presence of these patho-gens in irrigation water should be timely determinedusing appropriate bioassays such as in-situ baiting(Ghimire et al 2009) or PCR techniques (Martin et al2012 Schroeder et al 2012) Appropriate treatments ofthe water should be implemented if their presence isconfirmed in irrigation water Detection and managementapproaches of plant pathogens in irrigation water have

Agron Sustain Dev (2017) 37 10 Page 13 of 25 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

been previously described (Hong and Moorman 2005Stewart-Wade 2011 Zappia et al 2014)

42 Determination of potential interactions within andorbetween damping-off pathogens and other livingorganisms

Plant disease occurrence and development are deter-mined by numerous interactions between host pathogenand prevailing environmental conditions especially bio-cenosis under the influence of cropping practices Thisis especially the case of soilborne pathogens for whichthere are many possibilities for potential interactionswith other microorganismsagents occupying the sameecological niche A number of recent studies reportedsignificant interactions within andor between severaldamping-off pathogens and other pathogenic organisms(Table 7) Such studies have emphasized that co-inoculation of two or more pathogens consistently causemore detrimental effects on root development than ei-ther pathogen alone These findings will guide futureresearch on damping-off diseases including studies ofthe genetic diversity within species epidemiologicaland ecological features of the disease and host-pathogen interactions and ultimately help to developdurable and sustainable damping-off managementpractices

Although our understanding about individual geneticlines of microbes causing damping-off has increasedover the years there is a severe knowledge gap abouthow synergistic interactions between two or more genet-ic lines belonging to the same or different fungalgenerapathogenic agents can lead to the occurrenceand spread of damping-off diseases Therefore a focusto understanding such interactions would be another

direction for future research which is pivotal for thedevelopment of effective disease management strategies(Lamichhane and Venturi 2015)

43 A better knowledge of the role of abiotic factors thatpredispose seeds and seedlings to damping-off diseases

Overall while there is good knowledge in the literatureconcerning the role of individual abiotic factors on damping-off (especially soil moisture and temperature) little is knownabout how interactions between abiotic and biotic factors leadto the occurrence of such diseases Few works performed onabiotic stresses have highlighted that a number of abiotic fac-tors predispose seed or seedlings to damping-off pathogensand increase the severity of infection This is mainly due tocertain soil and climate factors which restrict normal seed androot growth and development (Burke et al 1972a b) In par-ticular wet (eg due to poor drainage or overwatering) andcool soils cool to moderate air temperatures are particularlyfavorable for the development of key damping-off pathogens(Table 3) Key predisposing factors which trigger the devel-opment of Fusarium Rhizoctonia Pythium andPhytophthora species are reported in Table 6

Soil characteristics including soil aggregate size and tex-ture markedly affect seedling emergence Aggregate size in-fluences the way the soil water content changes with time andthe seed-soil contact the path of the seedling to the soil sur-face and the rate of soil surface degradation by rainfallGreater soil aggregates size also represents mechanical obsta-cles for seedlings (Duumlrr and Aubertot 2000) Soil compactionis another factor causing stress in plants especially wheremechanized crop production is practiced resulting in reducedroot development (Allmaras et al 1988 Harveson et al 2005)Excessive soil compaction decreases porosity degrades soil

Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development Any IPMapproach should consist in the adoption of cropping practices including cultivar choice and chemical control which could discourage factors favoringdamping-off

Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References

Pythium spp Irrigation water soil High soil moisture pH gt58 the effect of temperatureis variable based on the type of damping-off Whilepre-emergence damping-off may occur at lowtemperatures (12 degC) the post-emergence oneis favored by relatively high temperature (18 to 30 degC)

(Roth and Riker 1943 Leach 1947Wright 1957)

Phytophthoraspp

Irrigation water infected soil Water-saturated soils and higher soil pH levels(lt8) variable effects of temperature and nitrogen

(Lambert 1936 Duniway 1983bSchmitthenner and Canaday 1983)

Fusarium spp Contaminated seeds(in soil or growing mediaand on used containers)airborne spores

Higher soil pH and with increased N levels variableeffects of temperature often depending on the pathogenof the isolates

(Tint 1945 Huang and Kuhlman 1990James 2012a)

Rhizoctoniaspp

Seeds airborne sporesinfected soil

High soil temperatures and increasing dryness(reduced moisture) No particular effect of pH low CN ratio

(Jackson 1940 Roth and Riker 1943Papavizas and Davey 1961 Starkeyand Enebak 2012)

10 Page 14 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

structure and can impede water movement and root growththereby predisposing seeds or seedlings to biotic stresses

Higher salinity levels have been reported to triggerdamping-off diseases A recent study found an evidence abouta synergistic interaction between salinity stress of seed orseedlings and salinity-tolerant Pythium species (Al-Sadiet al 2010) Other studies showed an enhanced level of dis-ease development on a number of crops due to higher salinitylevels (Rasmussen and Stanghellini 1988 Sanogo 2004Triky-Dotan et al 2005) Likewise heat developed just abovethe ground line can lead to seedling stresses or damages(Helgerson 1989)

44 Development of disease-suppressive seedbed soilswith or without conservation agriculture

Suppressive soils provide an environment in which plant dis-ease development is reduced even in the presence of a path-ogen and a susceptible host (Hadar and Papadopoulou 2012)Although several studies have reported the potentiality ofdisease-suppressive soils their practical application is stilllimited The reason behind is the lack of reliable predictionand quality control tools for assessing the level and specificityof the suppression effect This is especially true taking intoaccount the very complex soil environment with a high levelof dynamic complexity and interactions occurring among mi-crobes plants and the environment (Lemanceau et al 2015)More specifically to damping-off the development of a spe-cific means that suppresses the development of a givendamping-off pathogen may not provide a satisfactory suppres-sion of another pathogen thereby questioning the durability ofthis approach Indeed a suppressive soil to one pathogen may

not necessarily be suppressive to another due to specificity inthe soil-plant-microbe interactions (Whipps 2001) Thereforethe creation of disease-suppressive seedbed environments thatdiscourage the development of most damping-off pathogens isa challenging task for research A previous study (Bonanomiet al 2007) reported variable suppressive effects of organicamendments although in most cases such materials providedan effective disease suppressiveness Another concern is thatthe suppressive effects of certain amendments such as com-posts are relatively lower and more variable when they areapplied in the field compared to container media (Noble andCoventry 2005)

The difficulties in evaluating the level and specificity of thesuppression effect can however be addressed at least to someextent using modernmethods of analyzing microbial commu-nity structures including metagenomics The latter allowidentification of both culturable and non-culturable microor-ganisms and thus provide important insights to help define thekey organisms or groups of organisms that allow to exercisenatural suppression of damping-off pathogens However toguide research inmicrobial ecology in complex environmentssuch as soil there is a lack of ecological theory which hindershypothesis-driven research and interpretation of metadata es-pecially while dealing with compost and compost-amendedenvironments (Prosser et al 2007 Hadar and Papadopoulou2012) In particular our knowledge is still poor concerningwhy there are numerous cases of compost-mediated diseasesuppression but no or rare cases of suppressive soils at locallevels (ie under field conditions) To respond to this ques-tion a recent study identified common traits that have beenregarded as potential indicators of suppression (Hadar andPapadopoulou 2012) A better understanding of these

Table 7 Selection of synergisticinteractions within andorbetween damping-off pathogensand other pathogenic organismsreported since 2000

Host Interactions between References

Cassava Fusarium spp (Bandyopadhyay et al 2006)Cereals Fusarium spp (Del Ponte et al 2014)Chile pepper Rhizoctonia solani andMeloidogyne incognita (Al-Hammouri et al 2013)Clover Root-infecting fungi and parasitic nematodes (You et al 2000)Coffee Meloidogyne arabicida and Fusarium oxysporum (Bertrand et al 2000)Ginger Pythium spp (Le et al 2014)Green beans Meloidogyne incognita and Rhizoctonia solani (Al-Hazmi and Al-Nadary 2015)Lentil Fusarium oxysporum fsp lentis andMeloidogyne

javanica(De et al 2001)

Maize Pythium and Fusarium spp (Harvey et al 2008 Lamprecht et al2011)

Parsnip andparsley

Pythium spp (Petkowski et al 2013)

Soybean Fusarium spp (Barros et al 2014)Soybean Rhizoctonia spp and other microbes and nematode

communities(Liu et al 2016)

Soybean Phytophthora sojae and Heterodera glycines (Kaitany et al 2000)Potato Rhizoctonia solani and plant parasitic nematodes (Back et al 2000 Karlsson 2006 Bjoumlrsell

2015)Tomato Rhizoctonia solani andMeloidogyne incognita (Kumar and Haseeb 2009 Vidya Sagar

et al 2012)

Agron Sustain Dev (2017) 37 10 Page 15 of 25 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

indicators may surely help develop disease-suppressive soilsthereby contributing to damping-off management

Because suppressive soil to one pathogen may not alwaysbe suppressive to another there is a need for individual eval-uation of compost products for specific pathosystems and thedevelopment of standardized compost production and storageprotocols At the same time there needs a better focus towardsa development of suppressive soils under field conditions byoptimizing already existing compost-based amendments orcombining every single tool andor strategy that allows toenhance a disease-suppressive soil environment This includesmanipulation of the physiochemical and microbiological en-vironment via best management practices and biological con-trol using organisms such as Trichoderma spp (Tables 2 3and 4)

Overall there is a paucity of information in the literatureconcerning how conservation agriculture may affect damping-off diseases although prediction can be made from traditionalepidemiological knowledge Because the major damping-offpathogens discussed in this paper have a broad host range theretention of crop residues on soil surface maybe a nutrient(food) source for the pathogens after harvest as well the pres-ence of cover crops may act as a potential reservoir of thesepathogens (intermediate hosts (Bockus and Shroyer 1998Cook 2001) For example in areas with infected crop resi-dues infected seeds contribute to a rather small part of theinoculum as seeds and seedlings can be infected during theirdevelopment In addition no-till fields maintain more surfaceresidues than conventional-till fields at least early in the sea-son (Lindstrom andOnstad 1984 Govaerts et al 2007) whichmeans more moisture (Belvins et al 1971 Power et al 1986)a condition that favors development of damping-off pathogens(Schmitthenner and Van Doran 1985) Further while the pres-ence of crop residues may act as a physical barrier and preventpathogens from being spread through soil movement by windwater or agricultural equipment such effects may not be ap-plied to damping-off pathogens given their soil-borne nature

The little information available in the literature showsthat conservation agriculture may have variable effectson damping-off pathogens For instance a reduction oftillage has been reported to have both negative (Dickand Van Doran 1985 Schmitthenner and Van Doran1985 Adandonon et al 2004) and positive (Tachibana1983 Rovira 1986 Cook and Haglund 1991 Paulitzet al 2002 Govaerts et al 2007) effects on damping-off pathogens development A previous study (Worknehet al 1998) demonstrated the recovery of Phytophthorasojae in greater frequency near the soil surface in no-tillfields than in conventional-till fields This suggests thatthe potential development of damping-off diseases maybe greater in no-till fields than in conventional-till onesHowever Schillinger et al (2010) demonstrated thatwhen no-till regime was included in a conservation ag-riculture approach (ie together with a more complexrotation and a permanent soil coverage) the incidenceof Gaeumannomyces graminis var tritici was decreasedin comparison to continuous annual winter wheat inde-pendently of the soil management As for R solani nograin yield loss was observed in any kind of treatmentapplied although it was more pronounced in the no-tilltreatments Very similar results were obtained by otherauthors while dealing with several cereal pathogens(Matusinsky et al 2009 Paulitz et al 2009)

However it is worth to highlight that most of these studieswere based on short-term experiments and we do not know howdirect seeding affects damping-off disease over longer periods oftime Moreover most of the results come from researches onpartially-applied conservation agriculture systems whereas it iswell known that full benefits of conservation agriculture are de-livered when its three principles are applied for several years(Farooq and Siddique 2015) Hence more research efforts basedon long-term experiments are needed to better elucidate the ef-fects of conservation agriculture on these pathogens which maydiffer case by case

Fig 8 Generic conceptual modelthat represents the impact ofcropping practices and weather onbiotic and abiotic stressesaffecting seed germination andseedling emergence

10 Page 16 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

45 Modeling to help design integrated managementstrategies of damping-off diseases

Despite several benefits they provide simulation studies wererarely performed to understand seed germination and seedlingemergence However a model called SIMPLE (SIMulation ofPlant Emergence) was previously developed and used to pre-dict the effects of the main physical factors within the seedbedincluding soil temperature and water potential as well as me-chanical obstacles to germination and emergence (Duumlrr et al2001) A few subsequent studies attempted to evaluate the ef-fects of sowing conditions using the samemodel including sow-ing date sowing depth and seedbed preparation or of seed lotcharacteristics (Dorsainvil et al 2005 Moreau-Valancogne et al2008 Constantin et al 2015) This SIMPLE model was alsoused to analyze the extent of the effects of plant genetic diversityon seed emergence rates under a wide range of environmentalconditions (Brunel-Muguet et al 2011 Duumlrr et al 2016)

Little efforts towards the modeling of damping-off diseaseshave been undertaken so far Early epidemiological modelingapproaches were conducted in order to mathematically de-scribe soil-borne diseases as a function of inoculum density(Baker 1971 Grogan et al 1980) These approaches alwaysrelied on data sets obtained by experiments where one or morerarely several factors would vary For instance Burdon andChilvers (1975) analyzed and modeled the impact of clumpedplanting patterns on epidemics of damping-off disease(Pythium irregulare) in cress seedling as a function of numberof clumps per unit area Furthermore similar modeling ap-proaches permitted to model soil suppressiveness toR solani (Wijetunga and Baker 1979) Often these ap-proaches linked observed data to simple theoretical epidemi-ological models that were fitted to describe disease epidemicsGilligan (1983) proposed a typology of the early modelingapproaches in the field of soil-borne epidemiology modelsfor primary infection (rhizosphere models surface densitymodels probability models) models for secondary infections(for three types of pathogens unspecialized pathogens such asdamping-off and non-ectotrophic root rotting fungi special-ized ectotrophic pathogens specialized systemic pathogens)models for disease progress (growth curve analysis non-linear models such as the ones proposed by van der Plank(1963) epidemiological models embedding host growth mul-tivariate methods and computer simulations) Otten et al(2003) proposed a simple compartmental model S-I(susceptible-infected) to model transmission rates for soil-borneepidemics as a function of primary inoculum density (R solani)and the number of contacts of plants It was later extended to takeinto account soil suppressiveness (Otten et al 2004)More recentworks allowed to model the impact of crop sequence on attacksof Fusarium oxysporum fsp cepae (Leoni et al 2013) or theimpact of climate change on six soil-borne fungal plant patho-gens using a generic model associated to data on the impact of

temperature obtained in controlled chambers and a soil humiditymodel (Manici et al 2014)

Because there is a lack of tools to help design integratedmanagement strategies of damping-off diseases frameworksderived from the conceptual model as presented in Fig 8would be very useful Such models should integrate the im-pact of cropping practices and weather on the physical andchemical components of seedbed along with their impact ondamping-off disease primary inocula frommultiple pathogensand antagonistic microorganisms As reported in Fig 8 inter-actions between cropping practices and production situationsare numerous and such models should integrate mechanismsas parsimoniously as possible For instance theabovementioned SIMPLE model could be used as a basis todevelop such models since it already integrates the major abi-otic stresses (thermal hydric and mechanical stress)

Future research combining experimental and modeling ap-proaches should focus on a better understanding of the role ofabiotic stresses in damping-off diseases In addition diagno-ses of commercial fields with various levels of damping-offsymptoms could also help analyze the effects of interactionsbetween cropping practices and production situations on thebiotic and abiotic drivers of damping-off The developedmodels would thus significantly improve our understandingof the critical interactions between biotic and abiotic factorsthat affect damping-off diseases and would help design inte-grated management strategies of dumping-off diseases

5 Conclusions and perspectives

The great economic importance of damping-off diseases andincreasing concerns in finding sustainable solutions to thisproblem imply that opportunities exist to develop IPM strate-gies Achieving this outcome will require a greater under-standing of the ecology genetics and pathogenicity of themicrobes associated with the disease Research should focuson critical niches of complexity such as seed seedbed asso-ciated microbes and their interfaces for which innovative androbust experimental and modeling approaches are needed Inparticular development and validation of new simulationmodels or improvement of those already existing ones mayresult useful

Legislative pressure fueled by public concern over the useof conventional pesticides in agriculture requires that alterna-tive to conventional pesticides be developed and applied for adurable and sustainable disease management Neverthelessmanagement of damping-off appears to be less straightfor-ward than one might expect Given that several pathogenicorganisms interact and cause damping-off it is fundamentalto have prior knowledge of the interaction concerned as evena very low population density of soil-borne pathogens canlead to severe epidemic development Consequently the

Agron Sustain Dev (2017) 37 10 Page 17 of 25 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

prevention or containment of one pathogen may not resolvethe problem of the interaction Therefore there is a remarkableneed for a better understanding of the interactions betweenplants the environment and natural resident microbialagentscommunities under the influence of cropping prac-tices The information reported in this paper underlines thenecessity of understanding such a complex relationshipwhich is essential for an effective decision-making processon damping-off disease management

Acknowledgements We are grateful to Prof Lindsey J du ToitWashington State University USA and Dr Martin Chilvers MichiganState University USA for providing high-quality photos of damping-offdisease symptoms We also thank the participants of the Reacutes0Pest IPMnetwork (DEPHY EXPE ECOPHYTO) coordinated by theINRACIRAD who provided the data shown in Fig 6 and in particularGuillaume Audebert Alain Berthier Caroline Colnenne SeacutebastienDarras Violaine Deytieux Andreacute Gavaland Philippe Le Roy andAntoine Savoie

References

Abbasi PA Lazarovits G (2005) Effects of AG3 phosphonate formula-tions on incidence and severity of Pythium damping-off of cucum-ber seedlings under growth room microplot and field conditionsCan J Plant Pathol 27420ndash429 doi10108007060660509507241

Abbasi PA Lazarovits G (2006) Seed treatment with phosphonate (AG3)suppresses Pythium damping-off of cucumber seedlings Plant Dis90459ndash464 doi101094PD-90-0459

Abdel-Monaim MF Abo-Elyousr KAM (2012) Effect of preceding andintercropping crops on suppression of lentil damping-off and root rotdisease in New Valley ndash Egypt Crop Prot 3241ndash46 doi101016jcropro201110011

Abdelzaher HMA (2004) Occurrence of damping-off of wheat caused byPythium diclinum tokunaga in El-Minia Egypt and its possible con-trol by Gliocladium roseum and Trichoderma harzianum ArchPhy t op a t h o l P l a n t P r o t 3 7 147ndash159 d o i 10 1 0800323540042000205893

Adandonon A Aveling TAS Tamo M (2004) Occurrence and distribu-tion of cowpea damping-off and stem rot and associated fungi inBenin J Agric Sci 142561ndash566 doi101017S0021859604004629

Agrios GN (2005) Plant pathology Academic Press New York NYAgustiacute-Brisach C Peacuterez-Sierra A Garciacutea-Figueres F et al (2011) First

report of damping-off caused by Cylindrocarpon pauciseptatumon Pinus radiata in Spain Plant Dis 95874 doi101094PDIS-02-11-0125

Aiello D Castello I Vitale A et al (2008a) First report of damping-off onAfrican daisy caused by Rhizoctonia solani AG-4 in Italy Plant Dis921367 doi101094PDIS-92-9-1367B

Aiello D Parlavecchio G Vitale A et al (2008b) First report of damping-off caused by Rhizoctonia solani AG-4 on Lagunaria patersonii inItaly Plant Dis 92836 doi101094PDIS-92-5-0836A

Alcala AVC Paulitz TC Schroeder KL et al (2016) Pythium speciesassociated with damping-off of pea in certified organic fields inthe Columbia basin of Central Washington Plant Dis 100916ndash925 doi101094PDIS-07-15-0774-RE

Al-Hammouri A Lindemann W Sanogo S et al (2013) Interaction be-tween Rhizoctonia solani andMeloidogyne incognita on Chile pep-per in soil infested simultaneously with both plant pathogens Can JPlant Sci 9367ndash69 doi104141cjps2012-037

Al-Hazmi AS Al-Nadary SN (2015) Interaction between Meloidogyneincognita and Rhizoctonia solani on green beans Saudi J Biol Sci22570ndash574 doi101016jsjbs201504008

Allain-Bouleacute N Leacutevesque CA Martinez C et al (2004) Identification ofPythium species associated with cavity-spot lesions on carrots ineastern Quebec Can J Plant Pathol 26365ndash370 doi10108007060660409507154

Allmaras RR Kraft JM Miller DE (1988) Effects of soil compaction andincorporated crop residue on root health Annu Rev Phytopathol 26219ndash243

Almaliky BSA Abidin MAZ Kader J Wong MY (2012) First report ofMarasmiellus palmivorus causing post-emergence damping off oncoconut seedlings inMalaysia Plant Dis 97143 doi101094PDIS-07-12-0627-PDN

Al-Sarsquodi AM Drenth A Deadman ML et al (2007) Molecular character-ization and pathogenicity of Pythium species associated withdamping-off in greenhouse cucumber (Cucumis sativus) in OmanPlant Pathol 56140ndash149 doi101111j1365-3059200601501x

Al-Sadi AM Al-Masoudi RS Al-Habsi N et al (2010) Effect of salinityon pythium damping-off of cucumber and on the tolerance ofPythium aphanidermatum Plant Pathol 59112ndash120 doi101111j1365-3059200902176x

Aubertot J-N Robin M-H (2013) Injury profile SIMulator a qualitativeaggregative modelling framework to predict crop injury profile as afunction of cropping practices and the abiotic and biotic environ-ment I Conceptual bases PLoS One 8(9)e73202 doi101371journalpone0073202

Aubertot J-N Duumlrr C Richard G et al (2002) Are penetrometer measure-ments useful in predicting emergence of sugar beet (Beta vulgarisL) seedlings through a crust Plant Soil 241177ndash186 doi101023A1016170329919

Axelrood PE NeumannM Trotter D et al (1995) Seedborne Fusarium onDouglas-fir pathogenicity and seed stratification method to de-crease Fusarium contamination New For 935ndash51 doi101007BF00028924

Babadoost M Islam SZ (2003) Fungicide seed treatment effects on seed-ling damping-off of pumpkin caused by Phytophthora capsici PlantDis 8763ndash68 doi101094PDIS200387163

Babai-Ahary A Abrinnia M Heravan IM (2004) Identification and path-ogenicity of Pythium species causing damping-off in sugarbeet inNorthwest Iran Australas Plant Pathol 33343ndash347 doi101071AP04038

Bacharis C Gouziotis A Kalogeropoulou P et al (2010) Characterizationof Rhizoctonia spp isolates associated with damping-off disease incotton and tobacco seedlings in Greece Plant Dis 941314ndash1322doi101094PDIS-12-09-0847

Back MA Jenkinson P Haydock PPJ (2000) The interaction betweenpotato cyst nematodes and Rhizoctonia solani diseases in potatoesProc Bright Crop Prot Conf Pests Dis British Crop ProtectionCouncil Farnham UK pp 503ndash506

Bahramisharif A Lamprecht SC Calitz F McLeod A (2013a)Suppression of pythium and Phytophthora damping-off of rooibosby compost and a combination of compost and nonpathogenicPythium taxa Plant Dis 971605ndash1610 doi101094PDIS-04-13-0360-RE

Bahramisharif A Lamprecht SC Spies CFJ et al (2013b) Pythium sppassociated with rooibos seedlings and their pathogenicity towardrooibos lupin and oat Plant Dis 98223ndash232 doi101094PDIS-05-13-0467-RE

Bai Q Xie YWangX et al (2011) First report of damping-off ofRhodiolasachalinensis caused by Rhizoctonia solani AG-4 HG-II in ChinaPlant Dis 96142 doi101094PDIS-07-11-0559

Bailey KL Lazarovits G (2003) Suppressing soil-borne diseases withresidue management and organic amendments Soil Tillage Res72169ndash180 doi101016S0167-1987(03)00086-2

10 Page 18 of 25 Agron Sustain Dev (2017) 37 10

Baker R (1971) Analyses involving inoculum density of soil-borne plantpathogens in epidemiology Phytopathology 611280ndash1292

Bandyopadhyay R Mwangi M Aigbe SO Leslie JF (2006) Fusariumspecies from the cassava root rot complex in West AfricaPhytopathology 96673ndash676 doi101094PHYTO-96-0673

Bardin SD Huang HC Liu L Yanke LJ (2003) Control by microbialseed treatment of dampingoff caused by Pythium sp on canolasafflower dry pea and sugar beet Can J Plant Pathol 25268ndash275doi10108007060660309507079

Bardin SD Huang HC Moyer JR (2004a) Control of pythium damping-off of sugar beet by seed treatment with crop straw powders and abiocontrol agent Biol Control 29453ndash460 doi101016jbiocontrol200309001

Bardin SD Huang HC Pinto J et al (2004b) Biological control ofpythium damping-off of pea and sugar beet by Rhizobiumleguminosarum bv viceae Can J Bot 82291ndash296

Bargabus RL Zidack NK Sherwood JE Jacobsen BJ (2002)Characterisation of systemic resistance in sugar beet elicited by anon-pathogenic phyllosphere-colonizing Bacillus mycoides bio-logical control agent Physiol Mol Plant Pathol 61289ndash298doi101006pmpp20030443

Bargabus RL Zidack NK Sherwood JE Jacobsen BJ (2004) Screeningfor the identification of potential biological control agents that in-duce systemic acquired resistance in sugar beet Biol Control 30342ndash350 doi101016jbiocontrol200311005

Barros GG Zanon MSA Chiotta ML et al (2014) Pathogenicity of phy-logenetic species in the Fusarium graminearum complex on soy-bean seedlings in Argentina Eur J Plant Pathol 138215ndash222doi101007s10658-013-0332-2

BeechWS (1949) The effects of excess solutes temperature andmoistureupon damping-off Pennsylvania Agric Exp Stn Bull 50929

Belvins RL Cook D Phillips SH Phillips RE (1971) Influence of no-tillage on soil moisture Agron J 63593ndash596

Benhamou N (2004) Potential of the mycoparasite Verticilliumlecanii to protect citrus fruit against Penicillium digitatumthe causal agent of green mold a comparison with the effectof chitosan Phytopathology 94693ndash705 doi101094PHYTO2004947693

BenhamouN Chet I (1997) Cellular andmolecular mechanisms involvedin the interaction between Trichoderma harzianum and Pythiumultimum Appl Environ Microbiol 632095ndash2099

Ben-Yephet Y Nelson EB (1999) Differential suppression of damping-offcaused by Pythium aphanidermatum P irregulare andP myriotylum in composts at different temperatures Plant Dis 83356ndash360 doi101094PDIS1999834356

Bertrand B Nunez C Sarah JL (2000) Disease complex in coffee involv-ing Meloidogyne arabicida and Fusarium oxysporum Plant Pathol49383ndash388 doi101046j1365-3059

Bik HM Porazinska DL Creer S et al (2016) Sequencing our way to-wards understanding global eukaryotic biodiversity Trends EcolEvol 27233ndash243 doi101016jtree201111010

Bjoumlrsell P (2015) Interactions between some plantparasitic nematodesand Rhizoctonia solani in potato fields The Swedish University ofAgricultural Sciences

Bockus WW Shroyer JP (1998) The impact of reduced tillage on soil-borne plant pathogens Annu Rev Phytopathol 36485ndash500doi101146annurevphyto361485

Bonanomi G Antignani V Pane C Scala F (2007) Suppression of soil-borne fungal diseases with organic amendments J Plant Pathol 89311ndash324

Bourguet D Guillemaud T (2016) The hidden and external costs of pes-ticide use In Lichtfouse E (ed) Sustain Agric Rev Vol vol 19Springer International Publishing Cham pp 35ndash120 doi101007978-3-319-26777-7_2

Boyce JS (1961) Forest pathology third McGrawHill USA New York

Bradley CA (2007) Effect of fungicide seed treatments on stand estab-lishment seedling disease and yield of soybean in North DakotaPlant Dis 92120ndash125 doi101094PDIS-92-1-0120

Brunel-Muguet S Aubertot J-N Durr C (2011) Simulating the impact ofgenetic diversity ofMedicago truncatula on germination and emer-gence using a crop emergence model for ideotype breeding AnnBot doi101093aobmcr071

Bull CT Shetty KG Subbarao KV (2002) Interactions betweenmyxobacteria plant pathogenic fungi and biocontrol agents PlantDis 86889ndash896 doi101094PDIS2002868889

Bulletin de Santeacute Vegetal (BSV) (2016) Reacutesultats de lrsquoenquecircte deacutegacircts demouche (geacuteomyze) sur maiumls en Bretagne Technical report p 9 (InFrench)

Burdon JJ Chilvers GA (1975) Epidemiology of damping-off disease(Pythium irregulare) in relation to density of Lepidium sativumseedlings Ann Appl Biol 81135ndash143 doi101111j1744-73481975tb00530x

Burke DW Holmes LD Barker AW (1972a) Distribution of Fusariumsolani f Sp phaseoli and bean roots in relation to tillage and soilcompaction Phytopathology 62550ndash554

Burke DW Miller DE Holmes LD Barker AW (1972b) Counteractingbean root rot by loosening the soil Phytopathology 62306ndash309

Burns JR Benson DM (2000) Biocontrol of damping-off ofCatharanthus roseus caused by Pythium ultimum withTrichoderma virens and Binucleate Rhizoctonia fungi Plant Dis84644ndash648 doi101094PDIS2000846644

Carisse O Bernier J Benhamou N (2003) Selection of biological agentsfrom composts for control of damping-off of cucumber caused byPythium ultimum Can J Plant Pathol 25258ndash267 doi10108007060660309507078

Carling DE Summer DR (1992) Rhizoctonia In Singleton L Mihail JDRush CM (eds) Methods res Soilborne Phytopathogenic fungiAmerican Phytopathological Society St Paul MN the USA pp157ndash165

Carling DE Baird RE Gitaitis RD et al (2002) Characterization of AG-13 a newly reported anastomosis Group of Rhizoctonia solaniPhytopathology 92893ndash899 doi101094PHYTO2002928893

Chandanie WA Kubota M Hyakumachi M (2009) Interactions betweenthe arbuscular mycorrhizal fungus Glomus mosseae and plantgrowth-promoting fungi and their significance for enhancing plantgrowth and suppressing damping-off of cucumber (Cucumis sativusL) Appl Soil Ecol 41336ndash341 doi101016japsoil200812006

Chen CQ Belanger RR Benhamou N Paulitz TC (2000) Defense en-zymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatumPhysiol Mol Plant Pathol 5613ndash23 doi101006pmpp19990243

Coffua LS Veterano ST Clipman SJ et al (2016) Characterization ofPythium spp associated with asymptomatic soybean in southeasternPennsylvania Plant Dis doi101094PDIS-11-15-1355-RE

Coles RB Wicks TJ (2003) The incidence of Alternaria radicina oncarrot seeds seedlings and roots in South Australia AustralasPlant Pathol 3299ndash104 doi101071AP02069

Constantin J Duumlrr C Tribouillois H Justes E (2015) Catch crop emer-gence success depends on weather and soil seedbed conditions ininteraction with sowing date a simulation study using the SIMPLEemergence model F Crop Res 17622ndash33 doi101016jfcr201502017

Cook RJ (2001) Management of wheat and barley root diseases in mod-ern farming systems Australas Plant Pathol 30119ndash126doi101071AP01010

Cook JR Haglund WA (1991) Wheat yield depression associated withconservation tillage caused by root rot pathogens not phytotoxinsfrom the straw Soil Biol Biochem 231125ndash1132

Cook RJ Ownley BH Zhang H Vakoch D (2000) Influence of paired-row spacing and fertilizer placement on yield and root diseases ofdirect-seeded wheat Crop Sci 401079ndash1087

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Cram MM (2003) Damping-Off Tree Plant Notes 501ndash5Crous PW (2002) Damping-off In Crous PW (ed) Taxonomy and pa-

thology of Cylindrocladium (Calonectria) and allied genera TheAmerican Phytopathological Society St Paul MN pp 15ndash17

Davey CB (1996) Nursery soil management-organic amendments InLandis TD South DB (eds) Natl Proceedings For Conserv NursAssoc Portland (OR) p 6ndash18

de los Santos-Villalobos S Guzmaacuten-Ortiz DA Goacutemez-Lim MA et al(2013) Potential use of Trichoderma asperellum (SamuelsLiechfeldt et Nirenberg) T8a as a biological control agent againstanthracnose in mango (Mangifera indica L) Biol Control 6437ndash44doi101016jbiocontrol201210006

De RK Ali SS Dwivedi RP (2001) Effect of interaction betweenFusarium oxysporum fsp lentis and Meloidogyne javanica on len-til Indian J Pulses Res 1471ndash73

Deadman M Al Hasani H Al Sadi A (2006) Solarization andbiofumigation reduce Pythium aphanidermatum induced damping-off and enhance vegetative growth of greenhouse cucumber inOman J Plant Pathol 88335ndash337

Del Ponte EM Spolti P Ward TJ et al (2014) Regional and field-specificfactors affect the composition of Fusarium head blight pathogens insubtropical no-till wheat agroecosystem of Brazil Phytopathologydoi101094PHYTO-04-14-0102-R

Deytieux V Bernicot MH Cellier V et al (2014) An experimental net-work to study pesticide free cropping systems in arable crops InSzilvaacutessy Z (ed) 13th Congr Eur Soc Agron Debrecen Hungary p339ndash340

Diab HG Hu S Benson DM (2003) Suppression of Rhizoctonia solanion impatiens by enhanced microbial activity in composted swinewaste-amended potting mixes Phytopathology 931115ndash1123doi101094PHYTO20039391115

Dias MC (2012) Phytotoxicity an overview of the physiological re-sponses of plants exposed to fungicides J Bot doi1011552012135479

Dick WA Van Doran DM (1985) Continuous tillage and rotation combi-nations effects on corn soybean and oat yields Agron J 77459ndash465

Dole JM Wilkins HF (2004) Floriculture principles and species PrenticeHall Englewood Cliffs New Jersey

Dorrance AE Robertson AE Cianzo S et al (2009) Integrated manage-ment strategies for Phytophthora sojae combining host resistanceand seed treatments Plant Dis 93875ndash882 doi101094PDIS-93-9-0875

Dorsainvil F Durr C Justes E Carrera A (2005) Characterisation andmodelling of white mustard (Sinapis alba L) emergence under sev-eral sowing conditions Eur J Agron 23146ndash158 doi101016jeja200411002

du Toit LJ (2004)Management of diseases in seed crops in Encyclopediaof Plant and Crop Science In Dekker GRM (ed) Encycl Plant CropSci New York p 675ndash677

Dumroese RK James RL (2005) Root diseases in bareroot and containernurseries of the Pacific Northwest epidemiology management andeffects on outplanting performance New For 30185ndash202doi101007s11056-005-4422-7

Duniway JM (1983a) Role of physical factors in the develop-ment ofPhytophthora diseases In Erwin DC Bartnicki-Garcia S Tsao PH(eds) Phytophthora its Biol Taxon Ecol Pathol AmericanPhytopathological Society Saint Paul MN pp 175ndash187

Duniway JM (1983b) Role of physical factors in the develop-ment ofPhytophthora diseases In Erwin DC Bartnicki-Garcia S Tsao PH(eds) Phytophthora its Biol Taxon Ecol Pathol AmericanPhytopathological Society St Paul Minn USA pp 175ndash187

Duumlrr C Aubertot J-N (2000) Emergence of seedlings of sugar beet (Betavulgaris L) as affected by the size roughness and position of ag-gregates in the seedbed Plant Soil 219211ndash220 doi101023A1004723901989

Duumlrr C Aubertot JN Richard G et al (2001) SIMPLE a model forSIMulation of PLant Emergence predicting the effects of soil tillageand sowing operations Soil Sci Soc Am J 65414ndash442 doi102136sssaj2001652414x

Duumlrr C Constantin J Wagner M-H Navier H Demilly D Goumlertz S NesiN (2016) Virtual modeling based on deep phenotyping providescomplementary data to field experiments to predict plant emergencein oilseed rape genotypes Eur J Agron 7990ndash99 doi101016jeja201606001

Ellis ML Arias MMD Jimenez DRC et al (2012) First report ofFusarium commune causing damping-off seed rot and seedlingroot rot on soybean (Glycine max) in the United States Plant Dis97284 doi101094PDIS-07-12-0644-PDN

El-Metwally MA Sakr MT (2010) A novel strategy for controllingdamping-off and charcoal rot diseases of sunflower plants grownunder calcareous-saline soil using spermine potassium and zincPlant Pathol J 91ndash13

Enjalbert J Borg J Forst E et al (2016) New challenges for breedingvarieties adapted to mixed cropping systems In Lamichhane JRArseniuk E Messeacutean A (eds) Breed IPM Sustain low-input AgricSyst Radzikoacutew p 30

Farooq M Siddique MKH (2015) Conservation agriculture conceptsbrief history and impacts on agricultural systems In Farooq MSiddique MKH (eds) Conserv Agric Springer InternationalPublishing Cham pp 3ndash17

Farr DF Rossman AY (2012) Fungal nomenclature database systematicmycology and microbiology laboratory ARS USDA httpntars-gringovfungaldatabasesfungushostFungusHostcfm

Filer THJ Peterson GW (1975) Damping-off In Peterson GW Smith RS(eds) For Nurs Dis United States USDA Forest ServiceAgriculture Handbook No 470 Washington DC pp 6ndash8

Foy CD (1984) Physiological effects of hydrogen aluminium and man-ganese toxicities in acid soil In Pearson RW Adams F (eds) Soilacidity liming 2nd Editio American Society of AgronomyWisconsin pp 57ndash97

Garibaldi A Gilardi G Ortu G Gullino ML (2013) First report ofdamping-off caused by Pythium aphanidermatum on leaf beet(Beta vulgaris subsp vulgaris) in Italy Plant Dis 97292doi101094PDIS-08-12-0746-PDN

Garzoacuten CD Molineros JE Yaacutenez JM et al (2011) Sublethal doses ofMefenoxam enhance Pythium damping-off of geranium Plant Dis951233ndash1238 doi101094PDIS-09-10-0693

Georgakopoulos DG Fiddaman P Leifert C Malathrakis NE (2002)Biological control of cucumber and sugar beet damping-off causedby Pythium ultimum with bacterial and fungal antagonists J ApplMicrobiol 921078ndash1086

Gerbore J Benhamou N Vallance J et al (2014) Biological control ofplant pathogens advantages and limitations seen through the casestudy of Pythium oligandrum Environ Sci Pollut Res 214847ndash4860 doi101007s11356-013-1807-6

Ghimire SR Richardson PA Moorman GW et al (2009) An in-situbaiting bioassay for detecting Phytophthora species in irrigationrunoff containment basins Plant Pathol 58577ndash583 doi101111j1365-3059200802016x

Gilligan CA (1983) Modeling of soilborne pathogens Annu RevPhytopathol 2145ndash64 doi101146annurevpy21090183000401

Gladstone LA Moorman GW (1989) Pythium root rot of seedling gera-niums associated with various concentrations of nitrogen phospho-rous and soidium chloride Plant Dis 73733ndash736

Govaerts B Fuentes MMezzalamaM et al (2007) Infiltration soil mois-ture root rot and nematode populations after 12 years of differenttillage residue and crop rotation managements Soil Tillage Res 94209ndash219 doi101016jstill200607013

Gravel V Martinez C Antoun H Tweddell RJ (2005) Antagonist micro-organisms with the ability to control Pythium damping-off of tomato

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seeds in rockwool BioControl 50771ndash786 doi101007s10526-005-1312-z

Grogan RG Sall MA Punja ZK (1980) Concepts for modelling rootinfection by soilborne fungi Phytopathology 70361ndash363

Gwinn KD Ownley BH Greene SE et al (2010) Role of essential oils incontrol of Rhizoctonia damping-off in tomato with bioactive monar-da herbage Phytopathology 100493ndash501 doi101094PHYTO-100-5-0493

Hadar Y Papadopoulou KK (2012) Suppressive composts microbialecology links between abiotic environments and healthy plantsAnnu Rev Phytopathol 50133ndash153 doi101146annurev-phyto-081211-172914

Hammond-Kosack K Jones JDG (2000) Responses to plant pathogensbiochemistry and molecular biology of plants Rockville

Hansen EM Myrold DD Hamm PB (1990) Effects of soil fumigationand cover crops on potential pathogens microbial activity nitrogenavailability and seedling quality in conifer nurseriesPhytopathology 80698ndash704

Harman GE (2000) Myths and dogmas of biocontrolmdashchanges in per-ceptions derived from research on Trichoderma harzianum T-22Plant Dis 84377ndash393

Hartley C (1918) Stem lesions caused by excessive heat J Agric Res 14595ndash604

Hartley C (1921) Damping-off in forest nurseries USDABureau of PlantIndustry Washington (DC) Bulletin 99

Hartley C Pierce RG (1917) The control of damping-off of coniferousseedlings USDA Bull 45332

Harveson RM Smith JA Stroup WW (2005) Improving root health andyield of dry beans in the Nebraska Panhandle with a new techniquefor reducing soil compaction Plant Dis 89279ndash284 doi101094PD-89-0279

Harvey PR Warren RA Wakelin S (2008) The PythiumndashFusarium rootdisease complexmdashan emerging constraint to irrigated maize insouthern New South Wales Aust J Exp Agric 48367ndash374

He M Tian G Semenov AM van Bruggen AHC (2011) Short-term fluctuations of sugar beet damping-off by Pythiumultimum in relation to changes in bacterial communities afterorganic amendments to two soils Phytopathology 102413ndash420 doi101094PHYTO-07-11-0189

Helgerson OT (1989) Heat damage in tree seedlings and its preventionNew For 3333ndash358 doi101007BF00030044

Henricot B Peacuterez Sierra A Jung T (2014) Phytophthora pachypleura spnov a new species causing root rot of Aucuba japonica and otherornamentals in the United Kingdom Plant Pathol 631095ndash1109doi101111ppa12194

Hong CX Moorman GW (2005) Plant pathogens in irrigation waterchallenges and opportunities Crit Rev Plant Sci 24189ndash208doi10108007352680591005838

Horst RK (2013) Damping-off Westcottrsquos plant disease handbookSpringer Netherlands Dordrecht p 177

Howell CR (2007) Effect of seed quality and combination fungicide-Trichoderma spp seed treatments on pre- and postemergencedamping-off in cotton Phytopathology 9766ndash71 doi101094PHYTO-97-0066

Huang HC Erickson RS (2007) Effect of seed treatment with Rhizobiumleguminosarum on Pythium damping-off seedling height root nod-ulation root biomass shoot biomass and seed yield of pea andlent i l J Phytopathol 15531ndash37 doi 101111 j 1439-0434200601189x

Huang JW Kuhlman EG (1990) Fungi associated with damping-off ofslash pine seedlings in Georgia Plant Dis 7427ndash30

Huang X Zhang N Yong X et al (2012) Biocontrol of Rhizoctonia solanidamping-off disease in cucumber with Bacillus pumilus SQR-N43Microbiol Res 167135ndash143 doi101016jmicres201106002

Hwang SF Gossen BD Turnbull GD et al (2000) Seeding date temper-ature and seed treatment affect Pythium seedling blight of field peaCan J Plant Pathol 22392ndash399 doi10108007060660009500458

Hwang SF Ahmed H Turnbull GD (2008) Effect of crop rotation oncanola seedling blight and soil pathogen population dynamicsCan J Plant Pathol 30369

Iersel MW Bugbee B (1996) Phytotoxic effects of benzimidazole fungi-cides on bedding plants J Amer Soc Hort Sci 1211095ndash1102

Ishiguro Y Asano T Otsubo K et al (2013) Simultaneous detec-tion by multiplex PCR of the high-temperature-growingPythium species P aphanidermatum P helicoides andP myriotylum J Gen Plant Pathol 79350ndash358 doi101007s10327-013-0466-2

Islam MT Hashidoko Y Deora A et al (2005) Suppression of damping-off disease in host plants by the rhizoplane bacterium Lysobacter spstrain SB-K88 is linked to plant colonization and antibiosis againstsoilborne Peronosporomycetes Appl Environ Microbiol 713786ndash3796 doi101128AEM7173786-37962005

Jabaji-Hare S Neate SM (2005) Nonpathogenic binucleate Rhizoctoniaspp and benzothiadiazole protect cotton seedlings againstRhizoctonia damping-off and alternaria leaf spot in cottonPhytopathology 951030ndash1036 doi101094PHYTO-95-1030

Jackson LW (1940) Effects of H-ion and Al-ion concentrations ondamping-off of conifers and certain causat ive fungi Phytopathology 30563ndash579

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James RL (2012b) Damping-off In CramMM FrankMSMallams KM(eds) For Nurs Pests Agric Handb vol 680 USDAForest ServiceWashington DC pp 115ndash116

Jayaraj J Radhakrishnan NV Velazhahan R (2006) Development of for-mulations of Trichoderma harzianumstrain M1 for control ofdamping-off of tomato caused by Pythium aphanidermatum ArchPhytopathol Plant Prot 391ndash8 doi10108003235400500094720

Jensen B Knudsen IMB Madsen M Jensen DF (2004) Biopriming of

infected carrot seed with an antagonistClonostachys rosea selectedfor control of seedborne Alternaria spp Phytopathology 94551ndash

560 doi101094PHYTO2004946551Jiang J-H Tam S-L Toda T Chen L-C (2015) Controlling Rhizoctonia

damping-off of Chinese mustard by using endomycorrhizalRhizoctonia spp isolated from orchid mycorrhizae Plant Dis 10085ndash91 doi101094PDIS-06-14-0597-RE

Jung WJ An KN Jin YL et al (2003) Biological control of damping-offcaused by Rhizoctonia solani using chitinase-producingPaenibacillus illinoisensis KJA-424 Soil Biol Biochem 351261ndash1264 doi101016S0038-0717(03)00187-1

Kageyama K Nelson EB (2003) Differential inactiviation of seed exu-dates stimulation of Pythium ultimum sporangium germination byEnterobacter cloacae influences biological control efficacy on dif-ferent plant species Appl Environ Microbiol 691114ndash1120doi101128AEM6921114-11202003

Kaitany R Melakeberhan H Bird GW Safir G (2000) Association ofPhytophthora sojae with Heterodera glycines and nutrient stressedsoybeans Nematropica 30193ndash199

Kandel YR Wise KA Bradley CA et al (2016) Fungicide and cultivareffects on sudden death syndrome and yield of soybean Plant Dis1001339ndash1350 doi101094PDIS-11-15-1263-RE

Karlsson A (2006) Possible interactions between Rhizoctonia solani andplant parasitic nematodes (PPN) in Swedish potato fields TheSwedish University of Agricultural Sciences

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Kassaby FY (1985) Solar-heating soil for control of damping-off dis-eases Soil Biol Biochem 17429ndash434 doi1010160038-0717(85)90004-5

Kemerait RC Vidhyasekaran P (2006) Agricultural systems ConciseEncycl plant Pathol120ndash122

Khan RA (1977) Effect of high-temperature stress on the growth and seedcharacteristics of barley and cotton In Aksel R von Borstel RC(eds) Muhammed a Genet Divers Plants Springer US BostonMA pp 319ndash324

KidaK TojoMYanoK Kotani S (2007) First report ofPythium ultimumvar ultimum causing damping-off on okra in Japan Plant Pathol 561042 doi101111j1365-3059200701634x

Kilic-Ekici O Yuen GY (2003) Induced resistance as a mechanism ofbiological control by Lysobacter enzymogenes strain C3Phytopathology 931103ndash1110 doi101094PHYTO20039391103

Kiss L (2003) A review of fungal antagonists of powdery mildews andtheir potential as biocontrol agents Pest Manag Sci 59475ndash483doi101002ps689

Kiyumi KSM (2009) Greenhouse cucumber production systems inOman a study on the effect of cultivation practices on crop diseasesand crop yields University of Reading

Kloepper JW Ryu C-M Zhang S (2004) Induced systemic resistance andpromotion of plant growth by Bacillus spp Phytopathology 941259ndash1266 doi101094PHYTO200494111259

Koumoutsi A Chen XH Henne A et al (2004) Structural and functionalcharacterization of gene clusters directing nonribosomal synthesis ofbioactive lipopeptides in Bacillus amyloliquefaciens strain FZB42 JBacteriol 1861084ndash1096 doi101128JB18641084-10962004

Kraft JM Haware MP Halila H et al (2000) Soilborne diseases and theircontrol In Knight R (ed) Link Res Mark Oppor Pulses 21stCentury Kluwer Academic Publishers Dordrecht pp 457ndash466

Kumar V Haseeb A (2009) Interactive effect of Meloidogyne incognitaand Rhizoctonia solani on the growth and yield of tomato Indian JNematol 39387ndash388

Lambert EB (1936) A seedling wilt of black locust caused byPhytophthora parasitica J Agric Res 467ndash476

Lamichhane JR Venturi V (2015) Synergisms between microbial patho-gens in plant disease complexes a growing trend Front Plant Sci 6doi103389fpls201500385

Lamichhane JR Dachbrodt-Saaydeh S Kudsk P Messeacutean A (2016)Toward a reduced reliance on conventional pesticides in Europeanagriculture Plant Dis 10010ndash24 doi101094PDIS-05-15-0574-FE

Lamprecht SC Tewoldemedhin YT Botha WJ Calitz FJ (2011) Speciescomplex associated with maize crowns and roots in the KwaZulu-Natal province of South Africa Plant Dis 951153ndash1158doi101094PDIS-02-11-0083

Landis TD (2013) Forest nursery pests damping-off For Nurs Notes 225ndash32

Lazreg F Belabid L Sanchez J et al (2013a) First report of Fusariumequiseti causing damping-off disease on Aleppo pine in AlgeriaPlant Dis 981268 doi101094PDIS-02-13-0194-PDN

Lazreg F Belabid L Sanchez J et al (2013b) First report ofGlobisporangium ultimum causing Pythium damping-off onAleppo pine in Algeria Africa and the Mediterranean regionPlant Dis 971111 doi101094PDIS-07-12-0625-PDN

Lazreg F Belabid L Sanchez J et al (2013c) First report of Fusariumchlamydosporum causing damping-off disease on Aleppo pine inAlgeria Plant Dis 971506 doi101094PDIS-02-13-0208-PDN

Lazreg F Belabid L Sanchez J et al (2013d) First report of Fusariumredolens as a causal agent of Aleppo pine damping-off in AlgeriaPlant Dis 97997 doi101094PDIS-12-12-1169-PDN

Lazreg F Belabid L Sanchez J et al (2013e) First report of Fusariumacuminatum causing damping-off disease on Aleppo pine inAlgeria Plant Dis 97557 doi101094PDIS-06-12-0608-PDN

LeDP SmithM Hudler GW Aitken E (2014) Pythium soft rot of gingerdetection and identification of the causal pathogens and their con-trol Crop Prot 65153ndash167 doi101016jcropro201407021

Leach LD (1947) Growth rates of host and pathogen as factors determin-ing the severity of preemergence damping-off J Agric Res 75161ndash179

Leclere V Bechet M Adam A et al (2005) Mycosubtilin overproductionby Bacillus subtilis BBG100 enhances the organismrsquos antagonisticand biocontrol activities Appl Environ Microbiol 714577ndash4584doi101128AEM7184577-45842005

Lee TO Khan Z Kim SG Kim YH (2008) Amendment withpeony root bark improves the biocontrol efficacy ofTrichoderma harzianum against Rhizoctonia solani JMicrobiol Biotechnol 181537ndash1543

Leisso RS Miller PR Burrows ME (2009) The influence of biologicaland fungicidal seed treatments on chickpea (Cicer arietinum)damping off Can J Plant Pathol 3138ndash46 doi10108007060660909507570

Lemanceau P Maron P-A Mazurier S et al (2015) Understanding andmanaging soil biodiversity a major challenge in agroecologyAgron Sustain Dev 3567ndash81 doi101007s13593-014-0247-0

Leoni C de Vries M ter Braak CJF et al (2013) Fusarium oxysporumfsp cepae dynamics in-plant multiplication and crop sequencesimulations Eur J Plant Pathol 137545ndash561 doi101007s10658-013-0268-6

Lewis JA Lumsden RD (2001) Biocontrol of damping-off ofgreenhouse-grown crops caused by Rhizoctonia solani with a for-mulation of Trichoderma spp Crop Prot 2049ndash56 doi101016S0261-2194(00)00052-1

Li B Ravnskov S Xie G Larsen J (2011) Differential effects of organiccompounds on cucumber damping-off and biocontrol ofanatagonistic bacteria J Plant Pathol 9343ndash50 doi104454jppv93i1272

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Liao X Fu Y Zhang S Duan YP (2011) First report of damping-off onBasella rubra caused by Rhizoctonia solani anastomosis group 4 inFlorida Plant Dis 96288 doi101094PDIS-08-11-0639

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Lindstrom MA Onstad CA (1984) Influence of tillage systems on soilphysical parameters and infiltration after planting J Soil WaterConserv 39149ndash152

Liu P Luo L LongC (2013) Characterization of competition for nutrientsin the biocontrol of Penicillium italicum by Kloeckera apiculataBiol Control 67157ndash162 doi101016jbiocontrol201307011

Liu B Shen W Wei H et al (2016) Rhizoctonia communities in soybeanfields and their relation with other microbes and nematode commu-nities Eur J Plant Pathol 144671ndash686 doi101007s10658-015-0805-6

Mancini V Romanazzi G (2014) Seed treatments to control seedbornefungal pathogens of vegetable crops Pest Manag Sci 70860ndash868doi101002ps3693

Manici LM Bregaglio S Fumagalli D Donatelli M (2014) Modellingsoil borne fungal pathogens of arable crops under climate changeInt J Biometeorol 582071ndash2083 doi101007s00484-014-0808-6

MaoW Lewis JA Hebbar PK Lumsden RD (1997) Seed treatment witha fungal or a bacterial antagonist for reducing corn damping-offcaused by species of Pythium and Fusarium Plant Dis 81450ndash454 doi101094PDIS1997815450

Mao W Lumsden RD Lewis JA Hebbar PK (1998) Seed treatmentusing pre-infiltration and biocontrol agents to reduce damping-off

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of corn caused by species of Pythium and Fusarium Plant Dis 82294ndash299 doi101094PDIS1998823294

Maraghni M Gorai M Neffati M (2010) Seed germination at differenttemperatures and water stress levels and seedling emergence fromdifferent depths of Ziziphus lotus South African J Bot 76453ndash459doi101016jsajb201002092

MarcumDB Davis RM (2006) First report of damping-off of wild rice inCalifornia caused by Pythium torulosum Plant Dis 90523doi101094PD-90-0523B

Martin FN Abad ZG Balci Y Ivors K (2012a) Identification and detec-tion of Phytophthora reviewing our progress identifying our needsPlant Dis 961080ndash1103 doi101094PDIS-12-11-1036-FE

Mastouri F Bjoumlrkman T Harman GE (2010) Seed treatment withTrichoderma harzianum alleviates biotic abiotic and physiologicalstresses in germinating seeds and seedlings Phytopathology 1001213ndash1221 doi101094PHYTO-03-10-0091

Matny ON (2012) First report of damping-off of okra caused byPhytophthora nicotianae in Iraq Plant Dis 97558 doi101094PDIS-08-12-0735-PDN

Matusinsky PMikolasova R KlemK Spitzer T (2009) Eyespot infectionrisks on wheat with respect to climatic conditions and soil manage-ment J Plant Pathol 9193ndash101

Mavragani DC Abdellatif L McConkey B et al (2007) First report ofdamping-off of durum wheat caused by Arthrinium sacchari in thesemi-arid Saskatchewan fields Plant Dis 91469 doi101094PDIS-91-4-0469A

McNew GL (1960) The nature origin and evolution of parasitism InHorsfall JG Dimond AE (eds) Plant Pathol An Adv TreatiseAcademic Press New York pp 19ndash69

Mcquilken MP Gemmell J Lahdenperauml ML (2001) Gliocladiumcatenulatum as a potential biological control agent of damping-offin bedding plants J Phytopathol 149171ndash178 doi101046j1439-0434200100602x

Menzies JD (1963) Survival of microbial plant pathogens in soil Bot Rev2979ndash122

Messeacutean A Lamichhane JR Menard J-M (2016) Role of crop diversifi-cation to boost IPM and implications for breeding In LamichhaneJR Arseniuk E Messeacutean A (eds) Breed IPM Sustain low-inputAgric Syst Radzikoacutew p 6

Meziane H Van Der Sluis I Van Loon LC et al (2005) Determinants ofPseudomonas putidaWCS358 involved in inducing systemic resis-tance in plants Mol Plant Pathol 6177ndash185 doi101111j1364-3703200500276x

Milgroom MG Cortesi P (2004) Biological control of chestnut blightwith hypovirulence a critical analysis Annu Rev Phytopathol 42311ndash338 doi101146annurevphyto42040803140325

Misawa T KubotaM Sasaki J Kuninaga S (2015) First report of broccolifoot rot caused by Rhizoctonia solani AG-2-2 IVand pathogenicitycomparison of the pathogen with related pathogens J Gen PlantPathol 8115ndash23 doi101007s10327-014-0551-1

Montecchio L (2005) Damping-off of beech seedlings caused byFusarium avenaceum in Italy Plant Dis 891014 doi101094PD-89-1014A

Moorman GW Kim SH (2004) Species of Pythium from greenhouses inPennsylvania exhibit resistance to Propamocarb and MefenoxamPlant Dis 88630ndash632 doi101094PDIS2004886630

Moorman GW Kang S Geiser DM Kim SH (2002) Identification andcharacterization of Pythium species associated with greenhouse flo-ral crops in Pennsylvania Plant Dis 861227ndash1231 doi101094PDIS200286111227

Moreau-Valancogne P Coste F Crozat Y Duumlrr C (2008) Assessing emer-gence of bean (Phaseolus vulgaris L) seed lots in France fieldobservations and simulations Eur J Agron 28309ndash320doi101016jeja200709003

Mouttet R Escobar-Gutieacuterrez A Esquibet M et al (2014) Banning ofmethyl bromide for seed treatment could Ditylenchus dipsaci again

become a major threat to alfalfa production in Europe Pest ManagSci 701017ndash1022 doi101002ps3745

NegmFB SmithOE (1978) Effects of ethylene and carbon dioxide on thegermination of osmotically inhibited lettuce seed Plant Physiol 62473ndash376

Neher DA Augspurger CKWilkinson HT (1987) Influence of age struc-ture of plant populations on damping-off epidemics Oecologia 74419ndash424 doi101007BF00378939

Nelson EB (1988) Biological control of Pythium seed rot andpreemergence damping-off with Enterobacter cloacae andErwinia herbicola applied as seed treatments Plant Dis 72140ndash142

Njoroge SMC Riley MB Keinath AP (2008) Effect of incorporation ofBrassica spp residues on population densities of soilborne micro-organisms and on damping-off and Fusarium wilt of watermelonPlant Dis 92287ndash294 doi101094PDIS-92-2-0287

Noble R Coventry E (2005) Suppression of soil-borne plant diseaseswith composts a review Biocontrol Sci Tech 153ndash20doi10108009583150400015904

Ongena M Duby F Rossignol F et al (2004) Stimulation of thelipoxygenase pathway is associated with systemic resistance in-duced in bean by a nonpathogenic Pseudomonas strain Mol Plant-M i c r o b e I n t e r a c t 1 7 1 0 0 9 ndash 1 0 1 8 d o i 1 0 1 0 9 4MPMI20041791009

Onstad DW (2013) Insect resistance management biology economicsand prediction Academic Press p 560

Otten W Filipe JAN Bailey DJ Gilligan CA (2003) Quantification andanalysis of transmission rates for soilborne epidemics Ecology 843232ndash3239 doi10189002-0564

Otten W Filipe JAN Gilligan CA (2004) An empirical method to esti-mate the effect of soil on the rate for transmission of damping-offdisease New Phytol 162231ndash238 doi101111j1469-8137200401011x

Ou SQ Ji C Sun FL et al (2015) Rhizoctonia solani AG-4 HG-I causingseedling damping-off of Schisandra chinensis in Jilin provinceChina Plant Dis 1001017 doi101094PDIS-05-15-0557-PDN

Pal KK McSpadden B (2006) Biological control of plant pathogensPlant Health Instr doi101094PHI-A-2006-1117-02

Palmero D Gaacutelvez L Gil-Serna J Benito S (2012) Rhizoctonia solani ascausal agent of damping off of Swiss chard in Spain Spanish J AgricRes 101117ndash1120

Palumbo JD Yuen GY Jochum CC et al (2005) Mutagenesis of β-13-Glucanase genes in Lysobacter enzymogenes strain C3 results inreduced biological control activity toward Bipolaris leaf spot of tallfescue and Pythium damping-off of sugar beet Phytopathology 95701ndash707 doi101094PHYTO-95-0701

Pane C Spaccini R Piccolo A et al (2011) Compost amendments en-hance peat suppressiveness to Pythium ultimum Rhizoctonia solaniand Sclerotinia minor Biol Control 56115ndash124 doi101016jbiocontrol201010002

Papavizas CG Davey CB (1961) Saprophytic behavior of Rhizoctonia insoil Phytopathology 51693ndash699

Patterson L-M Smiley RW Alderman SM (1998) Effect of seed treat-ment fungicides and starter fertilizer on root diseases and yield ofspring wheat Fungic Nematic Tests 53425

Paulitz TC Beacutelanger RR (2001) Biological control in greenhouse sys-tems Annu Rev Phytopathol 39103ndash133 doi101146annurevphyto391103

Paulitz TC Smiley RW Cook RJ (2002) Insights into the prevalence andmanagement of soilborne cereal pathogens under direct seeding inthe Pacific Northwest USA Can J Plant Pathol 24416ndash428doi10108007060660209507029

Paulitz TC Okubara PA Schillinger WF (2006) First report of damping-off of canola caused by Rhizoctonia solani AG 2-1 in Washingtonstate Plant Dis 90829 doi101094PD-90-0829B

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Paulitz TC Schroeder KL SchillingerWF (2009) Soilborne pathogens ofcereals in an irrigated cropping system effects of tillage residuemanagement and crop rotation Plant Dis 9461ndash68 doi101094PDIS-94-1-0061

Petkowski JE de Boer RF Norng S et al (2013) Pythium species associ-ated with root rot complex in winter-grown parsnip and parsleycrops in south eastern Australia Australas Plant Pathol 42403ndash411 doi101007s13313-013-0211-5

Pieterse CMJ Zamioudis C Berendsen RL et al (2014) Induced systemicresistance by beneficial microbes Annu Rev Phytopathol 52347ndash375 doi101146annurev-phyto-082712-102340

Poletto T Maciel CG Muniz MFB et al (2015) First report ofFusarium lacertarum causing damping-off in Casuarinaequisetifolia in Brazil Plant Dis 991040 doi101094PDIS-12-14-1272-PDN

Polizzi G Vitale A Aiello D et al (2007) First report of damping-off andleaf spot caused by Cylindrocladium scoparium on different acces-sions of bottlebrush cuttings in Italy Plant Dis 91769 doi101094PDIS-91-6-0769B

Polizzi G Aiello D Castello I et al (2009) First report of damping-offcaused by Rhizoctonia solani AG-4 on Mediterranean fan palm inItaly Plant Dis 94125 doi101094PDIS-94-1-0125A

Polizzi G Aiello D Vitale A et al (2010) First report of damping-offcaused by Rhizoctonia solani AG-4 on pink ipecirc (Tabebuiaimpetiginosa) in Italy Plant Dis 9578 doi101094PDIS-10-10-0748

Polizzi G Aiello D Guarnaccia Vet al (2011) First report of damping-offon strawberry tree caused by Colletotrichum acutatum andC simmondsii in Italy Plant Dis 951588 doi101094PDIS-07-11-0567

Power JF Wilhelm WW Doran JW (1986) Crop residue effects on soilenvironment and dryland maize and soybean production SoilTillage Res 8101ndash111

Prosser JI Bohannan BJM Curtis TP et al (2007) The role of ecologicaltheory in microbial ecology Nat Rev Microbiol 5384ndash392doi101038nrmicro1643

Pryor BM AsmaM (2007) First report of seedling damping-off of fennelcaused by Alternaria petroselini in the Netherlands Plant Dis 911688 doi101094PDIS-91-12-1688A

Punja ZK Yip R (2003) Biological control of damping-off and root rotcaused by Pythium aphanidermatum on greenhouse cucumbersCan J Plant Pathol 25411ndash417 doi10108007060660309507098

Rajkumar M Lee KJ Freitas H (2008) Effects of chitin and salicylic acidon biological control activity of Pseudomonas spp against dampingoff of pepper South African J Bot 74268ndash273 doi101016jsajb200711014

Ramamoorthy V Samiyappan T Raguchander R (2002) Enhancing re-sistance of tomato and hot pepper to Pythium diseases by seed treat-ment with fluorescent pseudomonads Eur J Plant Pathol 108429ndash441 doi101023A1016062702102

Rasmussen SL Stanghellini ME (1988) Effect of salinity stress on devel-opment of pythium blight in Agrostis palustris Phytopathology 781495ndash1497

Reeleder RD Miller J Capell B Schooley J (2007) Mefenoxam sensi-tivity and the impact of fumigation on Pythium species andPhytophthora cactorum in ginseng soils Can J Plant Pathol 29427ndash436 doi10108007060660709507489

Ren XX Zhang GZ Dai WA (2012) First report of damping-off causedby Alternaria japonica on Chinese cabbage seedlings in ChinaPlant Dis 961378 doi101094PDIS-04-12-0328-PDN

Rhodes LH Myers DK (1989) Effect of seed treatment with metalaxyl orpyroxyfur on damping-off of alfalfa caused by Phytophthoramegasperma fsp medicaginis Crop Prot 8369ndash372 doi1010160261-2194(89)90057-4

Roberts DP Lohrke SM Meyer SLF et al (2005) Biocontrol agents ap-plied individually and in combination for suppression of soilborne

diseases of cucumber Crop Prot 24141ndash155 doi101016jcropro200407004

Roberts DP Lakshman DK McKenna LF et al (2016) Seed treatmentwith ethanol extract of Serratia marcescens is compatible withTrichoderma isolates for control of damping-off of cucumber causedby Pythium ultimum Plant Dis 1001278ndash1287 doi101094PDIS-09-15-1039-RE

Romo JT Haferkamp MR (1987) Effects of osmotic potential potassiumchloride and sodium chloride on germination of greasewood(Sarcobatus vermiculatus) West North Am Nat 47110ndash116

Roth LF Riker AJ (1943) Influence of temperature moisture and soilreaction on the damping-off of red pine seedlings by Pythium andRhizoctonia J Agric Res 67273ndash293

Rothrock CSWinters SAMiller PK et al (2012) Importance of fungicideseed treatment and environment on seedling diseases of cotton PlantDis 961805ndash1817 doi101094PDIS-01-12-0031-SR

Rovira AD (1986) Influence of crop rotation and tillage on Rhizoctoniabare patch of wheat Phytopathology 76669ndash673

Russell K (1990) Damping-off In Hamm PB Campbell SJ Hansen EM(eds) Grow Heal seedlings Identif Manag pests Northwest Fornurseries Forest Research Laboratory Oregon State UniversitySpecial publication Corvallis (OR) p 2ndash5

Ryu C-M Kim J Choi O et al (2006) Improvement of biological controlcapacity of Paenibacillus polymyxa E681 by seed pelleting onse s ame B i o l Con t r o l 39 282ndash289 do i 10 1016 j biocontrol200604014

Sabaratnam S Traquair JA (2002) Formulation of a streptomyces biocon-trol agent for the suppression of Rhizoctonia damping-off in tomatotransplants Biol Control 23245ndash253 doi101006bcon20011014

Safaiefarahani B Mostowfizadeh-Ghalamfarsa R Hardy GESJ BurgessTI (2015) Re-evaluation of the Phytophthora cryptogea speciescomplex and the description of a new species Phytophthorapseudocryptogea sp nov Mycol Prog 141ndash12 doi101007s11557-015-1129-9

Samac DA Schraber S Barclay S (2014) A mineral seed coating forcontrol of seedling diseases of alfalfa suitable for organic productionsystems Plant Dis 99614ndash620 doi101094PDIS-03-14-0240-RE

Saacutenchez-Borges CA Souza-Perera RA Zuacutentildeiga-Aguilar JJ et al (2015)First report of Phytophthora capsici causing damping-off ofCapsicum chinense in the Yucatan peninsula Plant Dis 1001247doi101094PDIS-09-15-1047-PDN

Sanogo S (2004) Response of chile pepper to Phytophthora capsici inrelation to soil salinity Plant Dis 88205ndash209

Saroj A Kumar A Saeed ST et al (2013) First report of Tagetes erectadamping-off caused byCeratobasidium sp from India Plant Dis 971251 doi101094PDIS-02-13-0145-PDN

Scattolin L Montecchio L (2007) First report of damping-off of commonoak plantlets caused by Cylindrocladiella parva in Italy Plant Dis91771 doi101094PDIS-91-6-0771B

Schillinger WF Young DL Kennedy AC Paulitz TC (2010) Diverse no-till irrigated crop rotations instead of burning and plowing continu-ous wheat F Crop Res 11539ndash49 doi101016jfcr200910001

Schmidt CS Agostini F Leifert C et al (2004) Influence of soil temper-ature and matric potential on sugar beet seedling colonization andsuppression of Pythium damping-off by the antagonistic bacteriaPseudomonas fluorescens and Bacillus subtilis Phytopathology94351ndash363 doi101094PHYTO2004944351

Schmitthenner AF Canaday CH (1983) Role of chemical factors in de-velopment of Phytophthora diseases In Erwin DC Bartnicki-Garcia S Tsao PH (eds) Phytoplithora its Biol Taxon EcolPathol American Phytopathological Society St Paul pp 175ndash187

Schmitthenner AF VanDoran DM (1985) Integrated control of root rot ofsoybean caused by Phytophthora megasperma f sp glycinea InParker CA Rovira AD Moore KJ et al (eds) Ecol ManagSoilborne plant Pathog American Phytopathological Society StPaul pp 263ndash266

10 Page 24 of 25 Agron Sustain Dev (2017) 37 10

Schroeder KL Martin FN de Cock AWAM et al (2012b) Moleculardetection and quantification of Pythium species evolving taxonomynew tools and challenges Plant Dis 974ndash20 doi101094PDIS-03-12-0243-FE

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