chemical control of plant diseases - researchmap

REVIEW FOR THE 100TH ANNIVERSARY

Chemical control of plant diseases

Takashi Hirooka • Hideo Ishii

Received: 6 January 2013 / Accepted: 5 May 2013 / Published online: 6 August 2013

� The Phytopathological Society of Japan and Springer Japan 2013

Abstract As the world population increases, we also

need to increase food production. Chemical control has

been critical in preventing losses due to plant diseases,

especially with the development of numerous specific-

action fungicides since the 1960s. In Japan, a host-

defense inducer has been used to control rice blast since

the 1970s without any problems with resistance devel-

opment in the pathogen. Leaf blast has been controlled

using a labor-saving method such as the one-shot

application of a granular mixture of fungicide and

insecticide to nursery boxes, which became mainstream

in the 2000s. However, the need for many choices of

fungicides that have several modes of action was

demonstrated by the development of resistance to cyt-

alone dehydratase inhibitors. In Europe, many pathogens

have threatened cereals since the great increase in cereal

production in 1970s, creating a large market for broad-

spectrum fungicides. In Brazil, Phakopsora pachyrhizi

was distributed to large soybean acreages during 2000s,

and the outbreak of soybean rust resulted in a large

increase in fungicide use. While the importance of

chemical control is recognized, fungicide resistance is

an avoidable problem; published guidelines on counter-

measure and manuals on testing sensitivity to fungicides

are available. Since chemical regulations have become

stricter, new fungicides are less likely to be developed.

Our task is to maintain the effectiveness and diversity

of the present modes of action for fungicides and

implement countermeasures against the development of

fungicide resistance.

Keywords Fungicide � Mode of action � Fungicide

resistance � Chemical control � Rice blast �Host-defense inducer

Introduction

For plant disease control, chemicals are a critical element

in effective integrated pest management (IPM) programs.

Chemical control began with the introduction of lime sulfur

and Bordeaux mixture in the mid-1800s, and fungicides

that have multiple sites of action with protective and

contact properties against several target sites in fungal

metabolism played a leading role in the first half of the

1900s. Fungicides that inhibit a specific target site were

introduced in the 1960s. Many specific fungicides have

protective and curative properties with systemic action,

giving users flexible application windows and became a

mainstay until recently (Knight et al. 1997; Morton and

Staub 2008).

After the research and development process for a

fungicide is finalized by a company, the product must

then be registered in each country before it can be used

by growers. The present review describes the trends in

chemical controls from the last five decades and dis-

cusses (1) fungicide markets, (2) fungicide groups by

mode of action, (3) practical examples of chemical

controls, which include rice blast and issues surrounding

chemical control in Japan, cereal diseases in Europe, and

soybean diseases in Brazil, and (4) fungicide resistance

and countermeasures in Japan.

T. Hirooka (&)

Nihon Nohyaku Co., Ltd, Kyobashi 1-19-8, Chuo-Ku,

Tokyo 104-8386, Japan

e-mail: [email protected]

H. Ishii

National Institute for Agro-Environmental Sciences (NIAES),

Kannondai 3-1-3, Tsukuba, Ibaraki 305-8604, Japan

123

J Gen Plant Pathol (2013) 79:390–401

DOI 10.1007/s10327-013-0470-6

Fungicide market

World sales of fungicides for crop use totaled US$9.91

billion in 2010 and have increased by 6.5 % annually since

1999. Major targeted crops include pome fruits (24 %),

cereals (23 %), soybean (12 %), vine (10 %), rice (8 %),

potato (7 %), maize (4 %), and rape (3 %) (Phillips

McDougall 2000, 2011). Fungicide sales in every region in

2010 increased over 1999 sales (Fig. 1). In Latin America,

use tripled because of an outbreak of soybean rust in

Brazil. Sales in Asia in 2010 were the same as those in

Latin America. Fungicide sales increased in Asia, China

and India and in developing countries in Southeast Asia.

The Japanese fungicide market, occupying half of the

Asian market, comprised solo products and mixtures with

insecticides. Sales of solo products for fruits, vegetables

and upland crops in Japan reached 74 billion yen in 2010

but declined gradually as agriculture waned with the aging

of farmers, decreases in the workforce, and increases in

agricultural imports. Sales of mixtures with insecticides

used mainly in paddy rice fields totaled 33 billion yen and

have remained constant over the past 10 years (Japan Plant

Protection Association 2012).

Fungicide groups classified by mode of action

Commercial fungicides are summarized based on mode of

action, percentage of sales, market-entry time, and spectrum

of efficacy in Table 1. The international Fungicide Resis-

tance Action Committee (FRAC) has grouped fungicides

according to target site, and FRAC codes assist farmers in

managing fungicide resistance (FRAC Code List 2013). The

classification in Table 1 uses the FRAC criteria for reference.

Although fungicides are classified roughly in terms of

specific-target fungicides and conventional multi-site fungi-

cides, the sterol demethylation inhibitors (DMIs) and quinone

outside inhibitors (QoI) are representative of specific fungi-

cides and account for approximately half of the total fungi-

cide sales. Meanwhile, multi-site fungicides, including

dithiocarbamates (mancozeb), inorganic (copper and sulfur

formulations), phthalimides (captan) and chloronitriles

(chlorothalonil) account for roughly one-fifth of fungicide

sales and are still on the increase. To control many plant

pathogens, multi-site fungicides are necessary, and special

efforts are engaged to maintain the registration in many

countries based on safety. In addition, specific fungicides

with new modes of action are greatly desired to maintain

diversity in the mode of action, which is critical for managing

the development of fungicide-resistance pathogens.

Sterol biosynthesis inhibitors (SBIs)

SBIs are classified into FRAC mode of action groups G1, G2,

G3 and G4 according to different target sites within the sterol

biosynthesis pathway. Those in G1, G2 (amines including

spiroxamine) and G3 (hydroxyanilides) are used as agro-

chemicals. Those in G4 are used only as pharmaceuticals.

Since the target site of fungicides in G1 is sterol C14

demethylase, they are named demethylation inhibitors

(DMIs). DMIs account for almost 90 % of the SBIs, and most

belong to one chemical class, the triazoles, which in include

the top three compounds in sales, tebuconazole, epoxico-

nazole and prothioconazole, followed by the next three in

sales, difenoconazole, propiconazole and cyproconazole. In

addition, metconazole (Sampson et al. 1992) is one of the

major fungicides for the control of Sclerotinia rot on rape and

Fusarium head blight (FHB) on cereals in Europe. Aside from

the triazoles, there are four chemical classes: imidazoles

(triflumizole), pyrimidines, pyridines and piperazines. SBIs

have a broad spectrum of efficacy, protective and curative

properties, systemic action, long-lasting activity, and field

resistance is relatively slow to develop (Kuck et al. 2012b).

In Japan, DMIs are used on fruits, vegetables, tea plants,

cereals and ornamentals and as seed treatments. Repre-

sentative DMIs include triflumizole (Hashimoto et al.

1986), tebuconazole and difenoconazole. Other products

discovered by Japanese companies, include pefurazoate

(Wada et al. 1991) and ipconazole (Tateishi et al. 1998),

used as rice seed treatments and imibenconazole (Ogawa

1995), oxpoconazole fumarate (Morita and Nishimura

2001) and simeconazole (Tsuda et al. 2000) used primarily

on fruits and vegetables.

QoIs

QoIs, known as strobilurins, started to be used in the 1990s

and have become the most important fungicides after the

Fig. 1 Fungicide market for crop use by region in 1999 and 2010

(Phillips McDougall 2000, 2011). NAFTA includes the US, Canada

and Mexico

J Gen Plant Pathol (2013) 79:390–401 391

123

SBIs in the last 20 years. They act by inhibiting the oxi-

dation of ubiquinol at the Quinone outside (Qo) binding

site on the cytochrome bc1 complex, which is located in

the inner mitochondrial membrane of fungi (Knight et al.

1997). Features common to QoIs are: (1) They are derived

from natural products. (2) They have been chemically

optimized to overcome instability in light and toxicity to

mammals. (3) They are broad spectrum, (4) with protective

and curative properties and (5) systemic action. (6) Field

resistance can develop quickly. (7) They delay senescence

(Sauter 2012).

Azoxystrobin and kresoxim-methyl were introduced to

the market in the 1990s. Currently, azoxystrobin, pyrac-

lostrobin, which replaced kresoxim-methyl, and trifloxyst-

robin are the top three QoIs, followed by fluoxastrobin,

picoxystrobin and dimoxystrobin. In Japan, azoxystrobin

and kresoxim-methyl account for 70 % of the QoI market,

followed by trifloxystrobin and pyraclostrobin. They are

used on fruits, vegetables, tea plants, cereals and orna-

mentals. On Japanese rice, azoxystrobin, metominostrobin

(Masuko et al. 2001) and orysastrobin (Stammler et al.

2007) are used. The newest QoI fungicide, pyribencarb

(Kataoka et al. 2010), launched in 2012, has a binding site

that is assumed to differ slightly from that of the other

QoIs.

Benzimidazoles and thiophanates

This group of specific fungicides, introduced about 1970,

includes thiophanate-methyl, carbendazim and benomyl as

representatives. They inhibit b-tubulin assembly during

mitosis and were first used to control gray mold and apple

Table 1 Mode of action (Fungicide Resistance Action Committee 2013; Kuck et al. 2012a; Phillips McDougall 2010), market share in 2009,

year introduced and spectrum of efficacy of major fungicide groups

Fungicide group Mode of action Market share Year introduced Spectrum of efficacy

Target site code FRAC code (% of total) 2009

Demethylation inhibitors (DMIs) G1 3 29.2 1970s A, B, D

Quinone outside inhibitors (QoIs) C3 11 22.1 1990s A, B, D, O

Dithiocarbamates Multi-site M3 6.8 *1950s A, B, D, O

Inorganic Multi-site M1, M2 4.7 *1950s A, B, D, O

Phthalimides Multi-site M4 4.2 *1950s A, B, D, O

Benzimidazoles and thiophanates B1 1 4.1 1960s A, B, D

Succinate dehydrogenase inhibitors

(SDHIs) 1st generation

C2 7 3.5 1960s Ba

SDHIs 2nd generation 1980s Ba

SDHIs 3rd generation 2000s A, B, D

Chloronitriles Multi-site M5 3.2 *1950s A, B, D, O

Phenylamides A1 4 2.9 1970s O

Amines G2 5 2.9 1980s A, B, D

Carboxylic acid amides (CAAs) H5 40 2.1 1980s O

Dicarboximides E3 2 1.9 1970s A

Anilinopyrimidines D1 9 1.9 1990s A

Others (cymoxanil) Unknown 27 10.5 1970s O

Others (fosetyl-aluminium) Unknown 33 1970s O

Others (fluazinam) C5 29 1990s O, A, D

Others (host defense inducers) P1, P2, P3 P 1970s Magnaporthe

Others (melanin biosynthesis

inhibitors [MBIs])

I1, I2 16.1, 16.2 1980s Magnaporthe

Others (uncouplers, phosphonate,

other Multi-site, cyanoacetamide oximes, etc.)

A1 RNA polymerase I, B1 b-tubulin assembly in mitosis, C2 complex II: succinate-dehydrogenase, C3 complex III: cytochrome bc1 (ubiquinol

oxidase) at Qo site, C5 uncouplers of oxidative phosphorylation, D1 methionine biosynthesis, E3 MAP/histidine-kinase in osmotic signal

transduction, G1C14-demethylase in sterol biosynthesis, G2 D14-reductase and D8 ? D7-isomerase in sterol biosynthesis, H5 cellulose synthase,

I1 reductase in melanin biosynthesis (MBI-R), I2 dehydratase in melanin biosynthesis (MBI-D), P1 salicylic acid pathway, P2 unknown, P3

unknown, Multi-site multi-site contact activity, A ascomycetes, B basidiomycetes, D deuteromycetes, O oomycetesa Notably Rhizoctonia spp.

392 J Gen Plant Pathol (2013) 79:390–401

123

scab, but the pathogens rapidly developed field resistance,

and they are now widely used in their relative crop seg-

ments because of their broad spectrum. Though benomyl

sales have decreased since registration was cancelled in the

European Union and the US (Phillips McDougall 2011),

thiophanate-methyl meets the strict criteria for registration

in Japan, the European Union and the US, and its use has

been increasing to control Sclerotinia rot of soybean in

Brazil and deoxynivalenol (DON) levels on cereal grains in

the European Union (Hamamura 2012).

Succinate dehydrogenase inhibitors (SDHIs)

This group inhibits succinate dehydrogenase in complex II

of the mitochondrial respiratory chain. Development of

SDHIs can be tracing back to three generations. The first

generation (e.g., carboxin) was developed in the 1960s and

used as a seed treatment against Rhizoctonia spp. Repre-

sentative of the second generation, mepronil (Kawada et al.

1985) and flutolanil (Araki and Yabutani 1981; Hirooka

et al. 1989) were introduced in the 1980s, followed by

furametpyr (Oguri 1997) and thifluzamide (O’Reilly et al.

1992) in 1990s. They are also active against basidiomy-

cetes, notably Rhizoctonia spp. and are used to control rice

sheath blight, another important disease of rice in Japan.

Flutolanil is used to control potato black scurf in Europe

and Rhizoctonia disease of peanuts, potato, and turf in the

US.

The leading products of the third generation of SDHIs

are boscalid and penthiopyrad (Yanase et al. 2007). Their

chemical structures are closely related to the older com-

pounds, but their spectrum of efficacy has broadened to

include ascomycetes. Since these findings, several com-

panies have intensified their research and development on

this group, and new active ingredients such as isopyrazam,

bixafen, penflufen, sedaxane, fluxapyroxad, benzovindi-

flupyr and fluopyram are reportedly ready to be launched.

Only fluopyram is a pyridinyl-ethyl benzamide, as opposed

to the other third generation compounds, which are car-

boxamides. For boscalid synthesis, a palladium-catalyzed

coupling reaction was the first use of a coupling reaction in

large-scale agrochemical synthesis (Rheinheimer et al.

2012). This contribution to the agricultural chemical

industries was one of the achievements recognized when

the Nobel Prize in Chemistry was awarded to Ei-ichi

Negishi and Akira Suzuki in Japan and Richard F. Heck in

the US in 2010.

Other groups

The broad-spectrum fungicides dicarboximides, including

procymidone (Oguri and Takayama 2003), iprodione and

vinclozolin, and the benzimidazoles were used to control of

Botrytis on vines, fruits and vegetables in the 1980s. After

resistance to them developed, the anilinopyrimidines,

including cyprodinil, mepanipyrim (Maeno et al. 1990) and

pyrimethanil, were introduced in the 1990s and have been

used to control strains with multiple resistances to dicarb-

oximides and benzimidazoles (Gisi and Muller 2012).

Specific fungicides to control oomycete plant diseases

include the phenylamides such as metalaxyl-M (Muller and

Gisi 2012), Quinone inside inhibitor (QiI) fungicides such

as cyazofamid (Mitani et al. 1998) and amisulbrom (Honda

et al. 2007), and carboxylic acid amides (CAA) (Gisi et al.

2012) such as dimethomorph, benthiavalicarb-isopropyl

(Miyake et al. 2005) and mandipropamid. There are also

fungicides with unknown modes of action: cymoxanil and

fosetyl-aluminum. Last, a relatively broad-spectrum fun-

gicide, fluazinam (Komyoji et al. 1995), is classified as

medium risk for resistance and is thus used globally to

control potato late blight, downy mildews and gray mold.

In Japan and Korea, host defense inducers and melanin

biosynthesis inhibitors (MBIs) have become widely used as

major countermeasures against rice blast. They have pro-

tective activity against the rice blast pathogen, Magna-

porthe oryzae, without directly inhibiting fungal growth

in vitro. Host defense inducers prevent rice plants from

infection by M. oryzae by inducing a resistance reaction in

the plants (Hirooka and Umetani 2004; Iwata 2001). They

are defined by FRAC as follows: code P1, acibenzolar-

S-methyl; code P2, probenazole (Iwata 2001); and code P3,

tiadinil (Hirooka and Umetani 2004) and isotianil (Toquin

et al. 2012) (Table 1). Although details of their modes of

action have been reviewed elsewhere (Toquin et al. 2012;

Yamaguchi and Fujimura 2005), a point to highlight is that

the leading compound among the host defense inducers,

probenazole, because of its unique mode of action was

discovered in Japan and has been in practical use in Jap-

anese rice culture since the mid-1970s.

MBIs inhibit appressorial penetration of rice by M. ory-

zae by inhibiting pigmentation of the appressoria (Yam-

aguchi and Fujimura 2005). They are divided into two

groups: polyhydroxynaphthalene reductase inhibitors

(MBI-R) such as tricyclazole, pyroquilon and phthalide

(Chida and Sisler 1987) and scytalone dehydratase inhibi-

tors (MBI-D) such as carpropamid (Kurahashi et al. 1999),

diclocymet (Manabe et al. 2002) and fenoxanil (Sieverding

et al. 1998).

Practical examples of chemical control

Chemical control of rice blast in Japan

Rice blast is the most economically important disease in

Japanese rice culture and occurs in large outbreaks once to


123

twice in every 10 years (Fig. 2). Because chemical control

of rice blast has been the most pertinent task for rice cul-

ture in Japan, many fungicides have been developed and

introduced (Yamaguchi and Fujimura 2005). Until 1990,

systematic, protective applications for rice blast control

were established as follows: (1) foliar spray with dust,

suspension concentrate or emulsifiable concentrate formu-

lations of fungicides such as kasugamycin, fthalide, tri-

cyclazole, ferimzone (Matsuura et al. 1994), (2) into-water

application of granular formulations of fungicides such as

probenazole, isoprothiolane (Hirooka et al. 1982), whose

target site is phospholipid biosynthesis, or pyroquilon to

the paddy water, or (3) an appropriate combination of the

foliar spray and into-water application.

Around 1990, blast-susceptible rice varieties were

widely grown because consumers preferred them; thus,

chemical control became even more important as blast-

resistant rice varieties fell out of favor. In 1993, Japan had

so many rainy days that there were fewer opportunities to

apply foliar sprays, and the incidence of rice blast

increased explosively. Under such circumstances, the into-

water applications of probenazole granules to paddy water

were less affected by the weather and had excellent pro-

tective efficacy. After 1993, foliar sprays were substan-

tially replaced by the into-water application of granules to

control rice leaf blast.

Meanwhile, environmentally friendly agriculture with

fewer applications of chemicals was strongly promoted,

and the development of labor-saving control methods was

also requested. In 1998, a granular formulation of car-

propamid mixed with insecticides for nursery box appli-

cation was launched and provided long-lasting efficacy

against leaf blast and a variety of pests with a one-shot

application at transplanting. A new granular formulation of

probenazole with sufficient crop tolerance was developed

for nursery box about the same time, then tricyclazole,

diclocymet, tiadinil, pyroquilon, orysastrobin and finally

isotianil came into the market during the 2000s. The one-

shot application of granules with long-lasting efficacy at or

before transplanting became the mainstream for the control

of leaf blast. At present, new slow-releasing granular for-

mulations of fungicides mixed with insecticide that have

been developed are safe for nursery box application even at

sowing (Fig. 2). Panicle blast, however, is very difficult to

control with a nursery box application, so foliar sprays and/

or into-water applications of granules are still required to

control panicle blast.

Although the one-shot application in nursery boxes

became the mainstream in 2000s, there was a great change

in the type of fungicides used (Fig. 3). In 2001, field

resistance to MBI-Ds was reported when the use of MBI-

Ds had expanded to around 250,000 ha, (estimated from

Fig. 2 Symptoms of rice leaf blast, nursery box application of

granular formulation of mixtures of a fungicide and an insecticide at

sowing. a, b Rice leaf blast in paddy fields (Hirooka and Umetani

2004). c Apparatus for granule application in nursery box at sowing.

d Granule application on bed soil from the hopper of the apparatus.

e Nursery box with granules applied at sowing before covering with

soil. f Rice seedlings after granule application at sowing


123

the shipping volume). MBI-Ds, rated by FRAC as having a

medium risk for resistance development (Brent and Holl-

omon 2007), have been mostly replaced with host resis-

tance inducers (probenazole and tiadinil) and MBI-Rs

(tricyclazole, pyroquilon), which are rated as low risk

based on their long-term use without any resistance prob-

lems. Since QoIs is rated as high fungicide risk and Mag-

naporthe is also rated as high pathogen risk, the use of

orysastrobin, which has excellent efficacy against rice blast

and sheath blight, then became prevalent. Details about

countermeasures are described later. But reduced perfor-

mance of orysastrobin was first reported in 2012 when the

use of QoIs had expanded to about 200,000 ha, a pre-

sumable threshold for resistance development based on the

fungicide resistance risk in M. oryzae.

Several issues surrounding chemical control in Japan

As mentioned earlier, fungicides with different modes of

action are used to control the many important diseases such

as scab, powdery mildews, gray mold of fruits and vege-

tables in Japan. Although many fungicides have been

introduced to agricultural fields, farmers need effective

control methods and appropriate implementation. The

Research Committee of Evidence-Based Control (EBC) of

the Phytopathological Society of Japan was established to

use experimental evidence to develop a theory on disease

control, and they hold workshops to extend the practice to a

wider circle of people.

The control of FHB in wheat and barley is extremely

important because the fungus reduces grain quality and

produces mycotoxins (Nakajima 2004). Thiophanate-

methyl has been an effective fungicide to control FHB and

mycotoxin accumulation (Nakajima 2004; Ueda and

Yoshizawa 1988). Recently, optimal timings for the use of

thiophanate-methyl on wheat and barley have been detailed

(Yoshida and Nakajima 2012).

When agricultural emissions of methyl bromide (MBr),

an effective broad-spectrum fumigant against soilborne

pathogens and pests, were implicated as a potentially sig-

nificant contributor to stratospheric ozone depletion,

developed countries mandated a complete ban of its use by

2005 as a precautionary measure and have needed to

develop safe, effective alternative methods. In Japan, MBr

was allowed in special cases for some vegetables, but that

use was phased out by 2012. Alternatives to MBr developed

by the National Agriculture and Food Research Organiza-

tion in Japan as chemicals such as chloropicrin, physical

control using solar heat, improved cultural management,

and the introduction of resistant varieties (Nishi 2006).

Regarding the regulations, a positive list system was

implemented in 2006 to improve regulations to limit

residual agricultural chemicals in foods. After implemen-

tation of the system, food import violations increased,

greatly impacting countries that exported agricultural

products to Japan (Tanaka and Uchimi 2007). Within

Japan, farmers continued to comply with usage standards

for agricultural chemicals and paid closer attention to

preventing chemical drift during applications (Watanabe

2007).

Chemical control of cereal diseases in Europe

The great increase in cropping intensity in European cereal

production in the 1960s and 1970s created a major market

where practically none had existed. The remarkable ability

0

1,000

2,000

3,000

4,000

5,000

6,000

7,000

8,000

9,000

10,000

2001 2002 2003 2004 2005 2006 2007 2008 2009 2010

Host defense inducer

MBI-D

MBI-R

Phospholipid

QoI

Year

Ship

ping

vol

ume

(t)

Fig. 3 Shipping volume of

fungicides, according to mode

of action, used for rice in Japan

during the 2000s. MBI-D:

melanin biosynthesis inhibitors-

dehydratase, MBI-R: melanin

biosynthesis inhibitors-

reductase, QoI: Quinone outside

inhibitors. (Data source: Japan

Plant Protection Association)


123

of new pathogens to adapt to intensively cultivated cereals

has led to a large list of pathogens that can threaten these

crops (Morton and Staub 2008). In Europe, cereals are

classified as a high value crop, and chemical use is wide-

spread, amounting to US$1.013 billion on cereals (Phillips

McDougall 2011). Because a number of diseases have to be

controlled at the same time on European cereals, the fun-

gicides must have broad-spectrum of efficacy. Disease

control on cereals begins with seed treatments.

Seed treatments, used to control diseases such as bunt

and smut caused by seed- and soil-borne pathogens, is fully

consistent with integrated pest management (IPM), since

fungicides provide control at extremely low rates and

treatment of the seed restricts activity to a limited area

around the seed (Allison 2002). DMIs and QoIs with strong

systemic properties have been commercialized, but sys-

temic activity is low when applied to seeds at recom-

mended dose rates, thus strongly reducing the risk that

fungal resistance will develop because air-borne pathogens

are not targeted or pressurized (Suty-Heinze et al. 2004).

Foliar sprays are applied generally two to three times

per crop from just before jointing of plants to flowering.

DMIs are intensively used, and mixed with fungicides

having other modes of action such as QoIs to decrease the

risk of resistance development and enhance the spectrum of

efficacy (Dutzmann and Suty-Heinze 2004). The use of

QoIs declined after field resistance developed in S. tritici,

but has recently increased as part of a mixture with DMIs

or new SDHIs, especially because of their greening effect

that maximizes yield (Phillips McDougall 2011). FHB is a

problem on wheat and barley in Europe also (Pirgozliev

et al. 2003) and must also be factored into the chemical

control strategy.

Chemical control of soybean diseases in Brazil

The area cropped with soybean in Brazil enlarged from

13 M ha in 1999 to 23.5 M ha in 2010, and fungicide sales

increased from US$37 M in 1999 to US$900 M in 2010,

presumably contributing to a yield increase from 2.4 to 2.9

t/ha (Phillips McDougall 2000, 2011). The good rainfall

and high temperature is conducive to numerous fungal

pathogens, which, if not controlled, may cause significant

losses to a variety of crops including soybeans (Calegaro

2003). When an outbreak of Asian rust (Phakopsora

pachyrhizi) reached the large soybean acreages in Brazil

during 2000, fungicide use greatly increased. The broad-

spectrum fungicides, DMIs, QoIs, new SDHIs and thi-

ophanates, are used to control soybean diseases.

Fungicide resistance and countermeasures in Japan

History and recent outbreak of fungicide resistance

in Japan

Fungicide resistance was first found in the field in 1971

when the efficacy of two antibiotics, polyoxin and kasu-

gamycin, decreased respectively against black spot disease

on Japanese pear (pathogen: Alternaria alternata Japanese

pear pathotype) and blast disease on rice (M. oryzae)

(Miura 1984; Nishimura et al. 1973).

Since then, fungicide resistance has continued to cause

problems, repeatedly decreasing fungicide efficacy on

various crops (Table 2). Fungal strains resistant to benz-

imidazoles, which were common in the 1970s, are still

widespread in Japan. Resistance to dicarboximides,

Table 2 Field occurrence of

fungicide resistance in Japan

(major cases)

Fungicide Pathogen

Polyoxin Alternaria alternata Japanese pear pathotype

Kasugamycin Magnaporthe oryzae

Benzimidazoles Botrytis cinerea, Venturia nashicola, Monilinia fructicola,

Gibberella fujikuroi, Cercospora kikuchii, Colletotrichum

gloeosporioides

Dicarboximides B. cinerea, A. alternata Japanese pear pathotype

Phenylamides Pseudoperonospora cubensis, Phytophthora infestans

Demethylation inhibitors (DMIs) Podosphaera xanthii, Sphaerotheca aphanis var. aphanis,

Mycovellosiella nattrasii, V. nashicola

Fluazinum B. cinerea

Quinone outside inhibitors (QoIs) P. xanthii, P. cubensis, M. nattrasii, Corynespora cassiicola,

B. cinerea, C. gloeosporioides, Passalora fulva,

Pestalotiopsis longiseta, Plasmopara viticola, M. oryzae

Cyfulfenamid P. xanthii

Scytalone dehydratase inhibitors

(MBI-Ds)

M. oryzae

Succinate dehydrogenase inhibitors

(SDHIs)

C. cassiicola, P. xanthii, B. cinerea, M. nattrasii


123

phenylamides, and DMI fungicides is also common. More

recently, resistance to QoI, MBI-D and SDHI fungicides

has been found as described next.

QoI fungicide resistance

It is well known that QoI fungicides are at very high risk

for resistance to develop in the target pathogens. In fact,

resistance in strains of fungal or oomycete pathogens to

QoI fungicides caused a decrease in QoI performance in

the field. Resistant strains have so far been detected in

about 60 pathogen species worldwide including 22 species

within Japan. A point mutation in the cytochrome b gene,

causing the substitution of alanine for glycine at amino acid

position 143, which is presumably involved in fungicide-

binding affinity, is thought to be the major cause of high

QoI resistance (Ishii 2012c). Most recently, however,

another point mutation, leading to the substitution of

phenylalanine for leucine, has been found at position 129

in two fungi, Passalora fulva (Watanabe 2011) and Pes-

talotiopsis longiseta (Yamada and Sonoda 2012).

DNA-based molecular techniques such as PCR–RFLP

(Ishii et al. 2007) and real-time PCR (Banno et al. 2009)

have been developed to identify QoI resistance rapidly.

Although PCR–RFLP is used frequently to diagnose

resistance, the dynamics of the multi-copy mitochondrial

cytochrome b gene, with the concomitant presence of

mutated and wild-type genes in various ratios within the

cells often causes difficulties in interpreting the results

(Ishii 2009).

Of major concern has been whether M. oryzae develops

resistance to QoI fungicides in paddy fields, and molecular

methods have been developed to diagnose such resistance

(Wei et al. 2009). Intensive monitoring for resistance is

ongoing because fungal isolates that are less sensitive to

QoIs have already been detected (Nakamura et al. 2011). In

2012, field resistance was found in some areas in western

Japan (Miyagawa and Fuji 2013).

MBI-D fungicide resistance

Nursery box treatments with the MBI-D fungicides car-

propamid and diclocymet became a common cultural

practice in many rice-growing areas because their efficacy

in controlling rice blast had been long-lasting. However, in

2001, the efficacy of carpropamid against leaf blast was

suddenly lost in Saga Prefecture, Kyushu (Yamaguchi

2003). Results from extensive studies indicated that resis-

tant strains played a significant role in the decrease in

efficacy (Sawada et al. 2004; Takagaki et al. 2004). It is

very likely that the long-lasting efficacy, based on the

persistent properties of the fungicide, has acted as a strong

selection pressure against resistant strains, and they rapidly

increased in fungal populations. As of 2011, resistant

strains have been detected from 36 of 47 prefectures in

Japan although the impact of resistance largely differs

depending on the areas (Ishii 2012b).

Molecular techniques such as PIRA-PCR (Kaku et al.

2003) and PCR-Luminex (Ishii et al. 2008) have been

developed to identify resistant strains rapidly. Use of car-

propamid and other MBI-D fungicides is stopped whenever

wide range of distribution of resistant strains confirmed in

an area. Results from monitoring tests suggest that resistant

strains seem to be less fit to the environment once the

selection pressure from the MBI-D fungicides is removed

(Kimura 2006).

SDHI fungicide resistance

Many SDHIs are being developed around the world.

However, resistance is developing against them also. For

example, boscalid-resistant isolates of Corynespora cas-

siicola rapidly appeared (Miyamoto et al. 2009), and iso-

lates resistant to penthiopyrad, which belongs to the same

cross-resistance group as boscalid, have also been detected

in the cucumber powdery mildew fungus (Miyamoto et al.

2010b). More recently, boscalid resistance has been found

in Botrytis cinerea on strawberry (Suzuki et al. 2012) and

Mycovellosiella nattrassii on eggplant (Okada et al. 2012).

The molecular mechanism underlying boscalid resis-

tance has been studied, and a point mutation in the sdhB

gene in C. cassiicola is associated with both a very high

and a high resistance to boscalid (Miyamoto et al. 2010a).

The same mutation has also been detected from boscalid-

resistant isolates of P. xanthii and B. cinerea (Ishii et al.

2012; Miyamoto et al. 2010b). Interestingly, a novel SDHI

fungicide fluopyram showed strong inhibitory activities not

only against boscalid-sensitive but also highly boscalid-

resistant isolates, indicating that a slightly different site of

action is involved for fluopyram than for boscalid and

penthiopyrad (Ishii et al. 2011, 2012).

DMI fungicide resistance

DMIs have the biggest share of the world fungicide market.

They have been used to control a variety of diseases on

cereals, vegetables, fruit crops and others since the mid-

1980s in Japan. A decrease in fungal sensitivity to DMIs in

general developed gradually. But now the efficacy of DMIs

such as fenarimol and hexaconazole against scab, the most

important disease of Japanese pear caused by Venturia

nashicola, is inadequate (Ishii and Kikuhara 2007). When

incomplete cross-resistance among DMIs exists, then

difenoconazole should be mixed with other effective fun-

gicides to control this disease.


123

Countermeasures

Successive applications of fungicides that possess the same

mode of action are well known to increase the likelihood

that resistance will develop (Dekker 1982). Based on this

theory and field experiences, alternative or mixed appli-

cations with one in a different group have been recom-

mended. However, we already know that these

conventional countermeasures cannot always stop the

occurrence of fungicide resistance.

After orysastrobin, a QoI fungicide, was marketed for

rice, the Research Committee on Fungicide Resistance of

the Phytopathological Society of Japan (PSJ Research

Committee on Fungicide Resistance) prepared guidelines

on how to use orysastrobin and other QoI fungicides that

had already been on the market; only one application a per

year is recommended, if necessary, and QoIs should be

used as a nursery box treatment in alternation with other

unrelated fungicides such as MBI-R fungicides or host

defense inducers, e.g. probenazole every 2–3 years (So and

Yamaguchi 2008). The same strategy is also recommended

for MBI-D fungicides, if they are still effective. Unfortu-

nately, however, QoI-resistant isolates of rice blast fungus

have been detected recently from paddy fields where seeds

had received the nursery box treatment with orysastrobin

successively for the last several years.

Guidelines on the use of QoIs and SDHIs in vegetables,

fruit, and tea have also been released from PSJ Research

Committee on Fungicide Resistance (Ishii 2012a). In 2009,

the Committee issued a supplemental version of the labo-

ratory manual (PSJ Research Committee on Fungicide

Resistance 2009), which will be quite useful when testing

fungicide sensitivity because the manual contains the

majority of pathogens and fungicides with known prob-

lems. A database of literature relating to fungicide resis-

tance reported in Japan accompanies the manual.

Future subjects

Disease management still relies largely on chemical con-

trol, but the occurrence of fungicide resistance may

increase in the future because the choice of fungicides is

often difficult when effective alternatives are lacking.

Development and integration of disease management tools

need to be accelerated not only to resolve the problem of

fungicide resistance but also to alleviate public concerns

about agricultural chemicals.

Conclusions

A re-registration process requires that agricultural chemi-

cals satisfy the demand of regulatory authorities regarding

low toxicity to humans and wildlife, low environmental

impact, low residues in food and so on. The public and

farmers also demand compatibility with IPM programs.

These demands are the main criteria of agricultural

chemical companies for deciding which fungicide to

develop and commercialize, and the probability of dis-

covery becomes lower. This change will then limit farmers’

choices for products (Knight et al. 1997). By contrast, the

struggle against pathogens that limit food production, as

shown in practical examples, will continue in the future.

Our task is to maintain the available diversity in the mode

of action groups of fungicides and implement counter-

measures against fungicide resistance based on our cumu-

lative knowledge.

Acknowledgments The contributions of Japanese agricultural

chemical companies to the discovery of fungicides referred in this

review are listed alphabetically as follows: Kumiai (mepronil),

Kumiai-Ihara (mepanipyrim, benthiavalicarb-isopropyl, pyribencarb),

Kureha (fthalide, ipconazole, metconazole), Hokko (kasugamycin,

imibenconazole), Ishihara (cyazofamid, fluazinam), Meiji Seika

(probenazole), Mitsui (penthiopyrad), Nihon Bayer Agrochem/now

Bayer CropScience (carpropamid), Nihon Nohyaku (isoprothiolane,

flutolanil, fenoxanil, tiadinil), Nippon Soda (triflumizole, thiophanate-

methyl), Nissan (amisulbrom), Sankyo/now Mitsui (simeconazole),

Shionogi/now Bayer CropScience (metominostrobin), Sumitomo

(procymidone, furametpyr, diclocymet), Takeda/now Sumitomo

(ferimzone), Ube-Hokko (pefurazoate), Ube-Otsuka (oxpoconazole

fumarate).

Credits: H. Ishii wrote ‘‘Fungicide resistance and countermeasures

in Japan’’, and T. Hirooka wrote the rest.

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