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Diseases of Citrus in Arizona

Item Type text; Pamphlet

Authors Olsen, Mary W.

Publisher College of Agriculture and Life Sciences, University of Arizona(Tucson, AZ)

Download date 16/06/2018 10:44:59

Link to Item http://hdl.handle.net/10150/146963

http://hdl.handle.net/10150/146963

The University of Arizona Cooperative Extension 1

Diseases ofCitrus in Arizona

Cooperative Extension

AZ1154April 2000

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ANT DISEASES

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2 The University of Arizona Cooperative Extension

Contents

INTRODUCTION........................................................................................................................... 4PARASITIC DISEASES ................................................................................................................ 5

FUNGI ...................................................................................................................................... 5PHYTOPHTHORA FOOT ROT ........................................................................................ 5HENDERSONULA BRANCH WILT .................................................................................. 7BROWN HEARTWOOD ROT OF LEMONS .................................................................... 7DRY ROOT ROT ............................................................................................................... 8BLUE AND GREEN FRUIT MOLDS................................................................................. 8ALTERNARIA FRUIT ROT ............................................................................................... 9RIO GRANDE GUMMOSIS ............................................................................................ 10

VIRUS DISEASES ................................................................................................................ 10CITRUS TRISTEZA VIRUS ............................................................................................ 10

VIRUS OR VIRUS-LIKE DISEASES .................................................................................... 11PSOROSIS ...................................................................................................................... 11

MYCOPLASMA DISEASES ........................................................................................................ 11STUBBORN DISEASE ................................................................................................... 11

NEMATODE DISEASES ............................................................................................................. 12THE CITRUS NEMATODE ............................................................................................. 13

NONPARASITIC DISEASES ...................................................................................................... 13MAJOR NUTRIENTS ............................................................................................................ 13ENVIRONMENTAL FACTORS ............................................................................................. 13

This inforamtion has been reviewed by university faculty.


Diseases of Citrus in Arizona

MARY OLSEN

Plant Pathology Specialist

MIKE MATHERON

Research Scientist, Plant Pathology

MIKE MCCLURE

Professor, Plant Pathology

ZHONGGUO XIONG

Associate Professor, Plant Pathology

Based on material originally written by RICHARD HINE, Plant Pathologist (retired),MIKE MATHERON, and LOWELL TRUE, Agricultural Agent (retired).

Photographs by RICHARD HINE.

This information has been reviewed by university faculty.

ag.arizona.edu/pubs/diseases/az1154.pdf

AZ1154April 2000

Cooperative ExtensionCollege of Agriculture and Life Sciences

The University of ArizonaTucson, Arizona 85721

Issued in furtherance of Cooperative Extension work, acts of May 8 and June 30, 1914, in cooperation with the U.S. Department of Agricultureand Life Sciences, James A. Christenson, Director, Cooperative Extension, College of Agriculture, The University of Arizona. The University of Arizona College of Agriculture and Life Sciences is an equal opportunity employer authorized to provide research,educational information, and other services only to individuals and institutions that function without regard to sex, religion, color, nationalorigin, age, Vietnam era Veteran’s status, or handicapping condition.


INTRODUCTION

Citrus, a crop of international importance, is indigenousto areas in southeast Asia. In Arizona, oranges were firstplanted commercially in central Arizona in the late 1800s.Today, commercial production is centered in several warmand low-frost-risk areas of central and southwestern Ari-zona. A great number of citrus varieties also are widelyplanted in home gardens. Many diseases of citrus havebeen described world wide and have colorful and descrip-tive names such as: blue mold, green mold, gray mold, pinkmold, pink nose, brown rot, black spot, black rot, black pit,yellow vein, yellow spot, rubbery wood, lumpy rind, curlyleaf, corky bark, slow decline, spreading decline, andstubborn. Other names are rooted in the many internationallanguages of citrus such as: Italian (impietratura and malsecco), Portuguese (tristeza), or Greek and Latin (cachexia,psorosis, exocortis, xyloporosis, cristacortis, and leprosis).Fortunately, most of the more serious, widespread diseasesdo not occur or are of little importance in Arizona. Thereare, however, a few diseases of sufficient importance todiscuss in this bulletin. They include several diseasescaused by fungi: foot rot gummosis (Phytophthora rootrot) caused by the soil occurring fungi Phytophthoraparasitica and P. citrophthora, Hendersonula branch wilt(caused by the fungus Hendersonula toruloidea), Brownheartwood rot of lemons caused by a species of Antrodiaand Coniophora, and black rot of fruit, caused by Alterna-ria alternata. Catastrophic bacterial diseases that haveplagued more humid and rainy production areas, such asFlorida, do not occur in the desert environments of Arizona.

Of the more than 30 virus and virus-like diseases thathave been described world wide, only Tristeza, Psorosis

and a mycoplasma disease, Stubborn, are presently knownto occur in Arizona. Tristeza and Stubborn disease havebeen extensively studied in Arizona and in other citrusareas of the world. These studies have increased our knowl-edge of the basic biology of these two very differentpathogenic micro-organisms including vector transmis-sion, strains, alternate hosts, effects on host plants and newmethods of diagnosis and detection.

In 1956, research in Arizona identified Tristeza virus inMeyer lemon, and Psorosis, a virus-like disease, in severalold line citrus varieties including Marsh grapefruit,Valencia orange, and Washington navel. These two dis-eases were probably introduced into Arizona in infectedbudwood and planting material prior to 1930. Stubborndisease was first identified in Arizona in 1965.

One of the most important diseases found in citrus inArizona is caused by the citrus nematode (Tylenchulussemipenetrans). This disease has become more widespreadand important because present control options are limited.

Many serious and widespread diseases in citrus grown inArizona are nonparasitic in nature. These diseases are notthe result of infection by living microorganisms but arecaused by factors such as: excessive sun and heat, excessesof certain elements including boron or lithium, excess soilsalts, mineral deficiencies, water stress, freeze injury, hail,lightning, and genetic disorders. Two excellent publica-tions that discuss diseases of citrus are: Compendium ofCitrus Diseases and Citrus Health Management, bothpublished by the American Phytopathological Society andIntegrated Pest Management for Citrus, published by theUniversity of California (publication 3303).

Issued in furtherance of Cooperative Extension work, acts of May 8 and June 30, 1914, in cooperation with the U.S. Department of Agriculture,James A. Christenson, Director, Cooperative Extension, College of Agriculture, The University of Arizona.

The University of Arizona College of Agriculture is an equal opportunity employer authorized to provide research, educational informationand other services only to individuals and institutions that function without regard to sex, race, religion, color, national origin, age, Vietnam EraVeteran’s status, or handicapping condition.


Parasitic Diseases

FUNGI

PHYTOPHTHORA FOOT ROT(Phytophthora gummosis)

Phytophthora foot rot or gummosis of citrus in Arizona iscaused by two soil microorganisms, Phytophthoraparasitica and P. citrophthora. This disease is relativelycommon in citrus groves in the Salt River Valley and Yumaareas. Loss of individual trees in home gardens occurs inall of southern Arizona. Disease incidence is especiallyhigh in trees established with the graft union at or belowthe soil surface, exposing susceptible scion tissue to thetwo pathogens. Severe losses also can occur in grovessubjected to flood irrigation if trees are planted on suscep-tible rootstocks.

Symptoms: The most diagnostic symptoms ofPhytophthora foot rot are found at or below the soillevel. Longitudinal cracking of bark, accompanied byprofuse gumming, usually is positive evidence ofinfection. Soil removal around affected trees revealsbark that is watersoaked, slimy, reddish-brown, or inlate stages, black. Diseased bark may be easily re-moved if fungal activity is recent. Advanced stages ofinfection will result in yellow, sparse foliage. Treesmay later collapse and die due to the girdling action ofthe fungal infection.

Fruit infections, although not common in southernArizona, may occur during or shortly after warm rainyperiods during summer and fall. These infections arecaused by motile spores being splashed onto fruit.

This stage of the disease is called brown rot, sincethe diseased areas on the fruit are brown in color.Active growth of trunk lesions occurs during May andJune, declines somewhat during the hot summermonths of July and August, then resumes duringSeptember and October.

Disease cycle: Both P. citrophthora and P. parasitica aresoil-borne fungi. They complete their life cycles in thesoil. In our dry desert conditions infection by thesetwo pathogens occurs, for all practical purposes, onlyon roots and lower bark tissue at the crown of the tree.In humid, wet areas of the world, however, these fungihave the capacity to infect fruit and upper trunk tissue.Recent surveys have determined that P. parasitica isthe more common of the two species in soils in thelower elevation, higher temperature areas of YumaCounty. This may be due to the fact that P. parasiticahas a higher optimum temperature for growth (85°-90° F) than P. citrophthora (75°-80° F). However,both species are commonly found in central Arizona.These species have been recovered from soil andinfected plant tissue in over 85 percent of 60 differentcitrus plantings in Maricopa and Yuma counties. Bothof these fungi produce motile, swimming zoosporeswhen soils are saturated from irrigation or rainfall.These spores are attracted to root tips. After attachmentthey germinate and infect cortical root tissue. Infectedfeeder root cortical tissue becomes rotted and dark inappearance.

Physical removal of this decayed tissue (by rub-bing between your fingers) reveals the whitish, centralroot tissue. This is a simple diagnostic technique thatcan be used in the field. Proof that a Phytophthora sp.is the cause of the decay requires the isolation andidentification of the fungus on Phytophthora specific

Figure 2. Seedling death (damping-off) in a citrus nurserycaused by Phytophthora parasitica. (Weslaco, TX)

Figure 1. Non-specific symptoms in citrus of general treedecline with tip die back and sparse foliage. This conditioncould be caused by several factors includingPhytophthora crown and root rot, citrus nematode, ornutrient deficiencies or excesses. (Yuma, AZ)


media in the laboratory. Both species produce survivalstructures in decayed root tissue that permit indefinitesurvival in soil. Studies in Arizona have shown thatisolates of P. parasitica from noncitrus hosts (tomato,for example) are not pathogenic to citrus. Interestingly,in contrast, isolates of P. parasitica from citrus arehighly pathogenic to tomato.

Control: Most citrus trees are budded on to a rootstock.Most of these rootstocks are more resistant toPhytophthora diseases than the scions (tops), so it isnecessary to keep the bud union at least four to sixinches above the soil line at planting. In general, watershould not be allowed to stand around the crown ofcitrus during irrigation. This is particularly true whenrootstocks susceptible to Phytophthora disease, suchas some selections of rough lemon or sweet orange, are

used. Moderately resistant rootstocks include Citrusmacrophylla, Cleopatra mandarin, and Troyercitrange. Over irrigation that causes soil saturation isdetrimental to normal feeder root development even inthe absence of Phytophthora. It is important to dig aplanting hole as deep as necessary to obtain gooddrainage. Caliche layers, commonly found in our lowrainfall, alkaline soils, should be opened up to allowwater drainage and unrestricted root development.

Control of Phytophthora diseases in citrus hasbeen enhanced by the availability of highly active,systemic fungicides specific for control ofPhytophthora. These chemicals are applied to the soiland the crown and trunk areas of affected trees. Studies

Figure 3. Typical gummy lesions caused by Phytophthoraparasitica in citrus bark. (Yuma, AZ)

Figure 4. Bark removed from sample shown in photograph3. Note the dark tissue where P. parasitica is active. (Yuma,AZ)

Figure 5. A close-up of a rootstock susceptible to P.parasitica and a resistant scion. Note the line ofdemarcation between resistant tissue (above) and thesusceptible discolored tissue (below). (Weslaco, TX)

Figure 6. Typical symptoms of an active lesion caused by P.parasitica. Note the dark, discolored infected tissue thatextends into the light-colored disease-free trunk tissue.(Cagayan, Philippines)


in Arizona indicated that isolates of P. parasitica andP. citrophthora pathogenic to citrus do not occurnaturally in Arizona soils. This fact suggests that thesefungi were most likely introduced into Arizona onimported planting material prior to our present inspec-tion and certification programs.

HENDERSONULA BRANCH WILTThis disease, also known as sooty canker or limb wilt, is

caused by the fungus, Hendersonula toruloidea, a woundpathogen that invades citrus bark that has been damaged byfreezing injury, sunburn, or mechanical injury but does notinfect uninjured bark tissue. This fungus has a wide hostrange and causes disease in many plants unrelated to citrus.

Symptoms: The most common symptom of sooty canker isthe sooty, black growth that develops beneath barktissue. This black canker is due to the presence ofmasses of black, fungal spores that appear under thebark and on the surface of the canker. Because thefungus grows into and kills sapwood, the leaves onbranches with cankers wilt, turn brown, and die.Branches die back to the cankered area. Scatteredbranches are usually affected. Most cankers developon unshaded trunks or limbs that face toward the sun.Sunburned trunks and limbs are highly susceptible toinfection.

Biology of the pathogen: In Arizona, the fungus producesonly conidia and thus has a very simple life cycle. Thesmall conidia, produced in black, powdery massesunder bark, are easily wind disseminated. Thesespores, which arise from segmented hyphae, are carried

to damaged bark tissue where they germinate andinitiate infection. The mycelium grows into livingtissue. Infected sapwood is stained gray to black in color.

Control: Sooty canker can be controlled when infectionsare confined to limbs and upper branches. Smallerinfected branches should be removed when symptomsappear. Since sunburned bark is the primary infectionsite, large limbs should be pruned only when trees aredormant.

When removing infected limbs, cut back to atleast one foot below the canker. The cut area andpruning tools should be treated with a solution of onepart household bleach and nine parts water. Pruningwounds should be painted with a copper fungicide toprevent infection. Reapply the copper compound tothe wound each spring to insure adequate protectionagainst infection. Control becomes increasingly diffi-cult as the disease progresses into the scaffoldbranches and is virtually impossible once the maintrunk is infected.

Tree vigor should be maintained through properfertilization and deep watering on a regular schedule.Severe pruning of larger branches and limbs of treesshould be avoided. Whitewash, applied to exposedlower trunk areas, will reduce the possibilities ofinfection by preventing sunburn and reducing barktemperature.

BROWN HEARTWOOD ROT OFLEMONS

Two different wood rot fungi recently have been shownto cause decay and death of branches of lemon trees in theYuma area. The fungi, Antrodia sinuosa and Coniophoraeremophila, initially invade branch tissue though wounds

Figure 7. Symptoms of sooty canker caused byHendersonula toruloidea. (Phoenix, AZ)

Figure 8. A close up of the sooty canker trunk lesion shown inphotograph 7. Note damaged bark on limb above the pruningwounds.


resulting from fractured or partially broken limbs. Thesewounds usually result from tractor damage, heavy fruitload and wind damage. The aerially dispersed spores of thefungi are deposited in these wounds, where subsequentcolonization of wood tissue and development of wooddecay in living heartwood occur. These infections result indeath of branches above the infection site.

Symptoms: The first obvious symptom is death of a lemontree branch. These branches are often partially brokenfrom the tree. The fractured infected wood is lightbrown in color. No evidence of fungal growth isobserved on wood infected with Coniophora, whereaswhite fungal mycelium can be observed within thebrown decayed wood infected with Antrodia. As thewood rot spreads, limbs continue to break from the treeuntil all that remains is a decayed stump.

Biology of the pathogens: Antrodia and Coniophora bothproduce aerially dispersed spores. Coniophora hasnot been found sporulating on infected lemon wood,so infected wood in lemon plantings is not producingspores that could infect other lemon trees. On the otherhand, Antrodia has been observed sporulating onlemon wood, so that additional infections could arisefrom spores produced from decayed lemon wood.

Control: Broken or dying branches should be removed witha flush, clean cut close to the main branch to minimizedevelopment of wood rot at wound sites. If the wood rotdecay is caused by Antrodia, removal of wood debris willeliminate this potential source of spores and minimizethe threat of new infections. Maintaining tree vigor withadequate irrigation and proper fertilization should pro-mote wound healing and minimize development ofwood rot. No fungicides currently available for use oncitrus will control this disease.

DRY ROOT ROTDry root rot of citrus occurs sporadically, attacking trees

that usually are weakened by some other factor. The mostsusceptible rootstocks include citranges, citrumelo, Citrusmacrophylla, rough lemon and Cleopatra mandarin. Thegeneral symptoms of dry root rot resemble those caused byPhytophthora and other pathogens that damage roots orgirdle the trunk, such as reduced vigor, leaves dull green incolor, restricted new growth and twig dieback. If rootdamage is severe, leaves may suddenly wilt and dry on thetree during summer and early autumn.

Symptoms: Examination of infected trees usually reveals adry decay of fibrous roots, larger roots and trunk at orbelow the soil surface. The wood below the bark is notdecayed but may be stained a dark color. A soil-borneplant pathogenic fungus, Fusarium solani, can berecovered from infected root tissue. Dry root rot mayadvance and develop for years with a slight wilt underdry conditions being the only symptom. However,once enough root tissue has been destroyed, leaves oninfected trees may suddenly wilt and turn yellow; atthis stage the tree may die with the leaves still at-tached. In addition to direct destruction of root tissue,the symptoms of Fusarium dry root rot are caused byinhibition of water transport in root tissue and produc-tion of toxins by the pathogen.

Biology of the pathogen: Fusarium solani is a commonsoil and root-inhabiting fungus which is associatedwith the roots, stem and bark of healthy as well asdiseased citrus trees. The transformation of the fungusinto a pathogen is correlated with stress factors, such asroot damage caused by Phytophthora, over-water-ing, under-watering, poor soil drainage, excess fertil-izer, heat stress and root injury due to plowing, herbi-cides or nematodes.

Control: Since stress factors like those listed above cantrigger disease development, prevention of these stressfactors can minimize the occurrence and severity of dryroot rot. To date, control of Fusarium dry root rot withfungicides has not been successful.

BLUE AND GREEN FRUIT MOLDSBlue and green mold are common postharvest diseases of

citrus. All types of citrus fruit are susceptible to these twomold diseases.

Symptoms: The initial symptom of blue and green mold isthe appearance of a soft, watery and slightly discoloredspot from 1/4 to 1/2 inch in diameter. This spotenlarges to 1 to 2 inches in diameter after 1 to 1.5 daysat 75° F. White mycelium appears on the surface, andwhen the growing fungus is about 1 inch in diameter,

Figure 9. A Broken branch in lemon caused byinfection by a wood decay fungus, Coniophora. (Yuma,AZ)


blue or olive green spores are produced. The entirefruit surface is rapidly covered with the blue or olivegreen spores, which are easily spread if the fruit ishandled or exposed to air currents.

Biology of the pathogens: The fungus that causes bluemold is Penicillium italicum, whereas the pathogencausing green mold is Penicillium digitatum. Sporesof the fungi are produced in chains in massive quantitieson infected fruit. The fungi survive in the orchard asspores. Infection occurs by airborne spores enteringthe fruit rind through injuries. The infection andsporulation cycle can occur many times during theseason in the packinghouse. Blue and green molddevelop most rapidly at around 75° F; on the otherhand, rot is virtually stopped at a temperature of 34° F.

Control: Careful picking, handling, packing and storage offruit minimizes injuries to thefruit rind and the risk ofblue or green mold development. Sanitary packing-house practices, including the use of disinfectantssuch as chlorine or other materials, help reduce theconcentration of fungal spores capable of causinginfection. Post-harvest application of selected fungi-cides can help delay the development of blue andgreen mold, especially in combination with immedi-ate cooling of fruit after packing.

ALTERNARIA FRUIT ROTAlternaria fruit rot, also called Black rot, is a fungal

disease caused by Alternaria alternata. The disease oc-curs occasionally in lemons and navel oranges in Arizona.It was first described in the late 1890s from California. Thefungus occurs throughout the citrus growing areas of theworld. Alternaria attacks only citrus fruit. Alternaria rot isprimarily a problem in storage, but it sometimes occurs in

the orchard where it can cause premature fruit drop. In otherparts of the world the disease has been reported on citrusfruit other than navels and lemons. Alternaria fruit rot ismost important in areas where citrus is processed for juicebecause of juice contamination by masses of black fungalmycelium found in the interior of the infected fruit.

Symptoms: Fruit infected with Alternaria may turn light incolor several weeks before the color break in healthyfruits. Some infected fruit may prematurely drop whileothers may remain on the tree.

Infected fruit may appear normal. The simplemethod of diagnosis is to cut the fruit in half, exposingthe stylar or “blossom” end and the central cavity.Diseased fruit have a brown to blackish discolorationat the “blossom” end . The discoloration and decaymay be restricted to the “blossom” end or it mayextend deep into the central cavity. Observations ofinfected tissue in the laboratory reveals the presence ofAlternaria. Fungal spores are unique in appearance.There may be little or no external evidence of infec-tion. In lemons the disease is most common duringstorage. In Arizona, splitting, caused by environmentalfactors, often predisposes navel oranges to infectionby Alternaria. Large navel fruit may split and drop inthe fall during hot, dry weather. The incidence ofsplitting is higher in sunburned fruit, and in treesstressed by drought and frost injury.

Biology: Alternaria alternata is an active saprophyte.The fungus grows on dead citrus tissue during wetweather. Airborne conidia are produced during theseperiods. These spores germinate and the fungus estab-lishes itself in the button or stylar end of the fruit.

Entrance into the fruit is facilitated when splits orgrowth cracks occur. The fungus grows into thecentral core of the fruit and causes a black decay.

Figure 10. A tear stain, caused by drops of watercarrying spores of Alternaria alternata. (Phoenix,AZ)

Figure 11. Mummy-like, black fruit infected withAlternaria alternata. (Phoenix, AZ)


Alternaria produces large numbers of conidia ininfected fruit. The fruit may dry and become black andmummy-like in appearance . This fruit becomes one ofthe survival mechanisms for the fungus.

Control: Proper fertilization and irrigation will reduce theincidence of this disease. There are no chemicals thatare presently recommended for control.

RIO GRANDE GUMMOSISThis name has been given to a gumming disease of

mature citrus, particularly grapefruit, thought to be causedby several fungi, but no particular pathogen has beenidentified.

Symptoms: Symptoms begin as narrow cracks in the bark oflimbs and trunk in which a yellow, water solubleexudate accumulates. Gum formation on the trunk orbranches and gum exudation from blisters on the trunkcontinues and forms gum pockets under the bark. Theadvancing margin of infection is orange to pink. Oncesapwood is exposed, wood decay may begin. In laterstages of disease, heart rot may also be prevalent.

Control: Several factors have been identified as contribut-ing to disease including freeze damage, poor drainage,and salt accumulation. Weakened and injured treesseem to be predisposed to the disease. There is nocontrol other than cultural practices that keep trees invigorous condition. Good pruning practices thatremove freeze damaged wood and encourage fasthealing are the best way to prevent disease.

VIRUS DISEASES

CITRUS TRISTEZA VIRUSCitrus Tristeza Virus (CTV) is one of the most

destructive of the many viruses that affect citrus. Thevirus pathogen has been responsible for the death anddebilitation of millions of citrus trees in Argentina,Brazil, South Africa, and other areas. Observations inthe late 1800s and early 1900s of declining sweetorange trees on sour orange rootstocks led scientists toconclude that tree failure was due to an incompatibilitybetween certain scion varieties and sour orange roots.In 1946, American and Brazilian plant pathologistsreported that tree failure was caused by a virus disease.The Brazilians demonstrated that an aphid, Toxopteracitricidus, was a vector of the virus. The Braziliansnamed the disease “tristeza,” a Portuguese word mean-ing sadness, an appropriate name for a virus diseasethat had killed 18 million trees in Argentina and 10million trees in Brazil. The virus was identified inCalifornia in the late 1940s. Severe losses occurred inSouthern California in a number of citrus varieties that

were budded to sour orange rootstocks. Studies inCalifornia demonstrated the existence of several vari-ants or strains of CTV. These strains varied in severity,vector specificity, and host range. It was proven thatseveral distinct diseases (Tristeza, Stem-pitting, Seed-ing-yellows, and Lime dieback) were caused by strainsof CTV. In Arizona, CTV was first identified in 1956 inMeyer lemon. Later surveys discovered the virus inmature trees of Clementine mandarin, Dancy tanger-ine, and Marsh white grapefruit at both the Yuma andTempe University of Arizona Citrus Experiment Sta-tions.

Symptoms: Symptoms of CTV in citrus are extremelyvariable and depend on the isolate of the virus, host,environment, and scion/rootstock relationships.Common symptoms include reduced fruit size, leafvein-clearing, yellowing and cupping of leaves, andstem pitting. Infection of sweet orange, mandarin, orgrapefruit trees on sour orange rootstock causes ne-crosis in the phloem of the sour orange rootstock justbelow the bud union. This girdling causes eventualdecline and death of the infected tree.

Present Situation in Arizona: To understand the presentsituation of CTV in Arizona, it is necessary to discusscertain biological properties of this virus. CTV is nottransmissible by seed or mechanical means. The virusis disseminated only in infected bud wood, plantingmaterial and by several species of aphids. The mostefficient vector, Toxoptera citricidus (the black citrusaphid) does not occur in Arizona but does occur inFlorida. This species, prevalent in South America,played a key role in the early epidemics of CTV. Thecotton aphid, Aphis gossypii, is a vector of certainstrains of CTV in California, but not in Arizona. Thereis no evidence that aphids are involved in the spread of

Figure 12. Advanced sympoms caused by the CitrusTristeza Virus in sweet orange on sour orangerootstock. (Riverside, CA)


CTV in Arizona. The introduction of T. citricidus intoArizona or California, however, would present a perilto trees on sour orange rootstock. CTV has not beendetected in citrus commercially grown in the SaltRiver Valley of Central Arizona even though citrus inthis area is grown predominately on sour orange root-stock. All citrus trees in the certification program havebeen tested for the presence of CTV by use of an ELISAserological test. The results were 100 percent negativeon mother block trees at the Yuma station. The factthat CTV is not presently a factor in commercialplantings of citrus on sour orange roots is due to anumber of factors: the Arizona Citrus CertificationProgram, initiated over 25 years ago, has been effec-tive in preventing the introduction of diseased budwood and planting material into Arizona; the cottonaphid (A. gossypii), which occasionally feeds on citrusin Arizona, apparently does not transmit the strains ofCTV that occur in Arizona; old line citrus varietiescarrying the virus have been eradicated; and quarantineregulations on imported citrus have been effective.

VIRUS OR VIRUS-LIKE DISEASES

PSOROSISPsorosis is an occasional problem in old citrus plantings

in Arizona. The disease, which occurs primarily in orangeand grapefruit trees, is characterized primarily by thescaling and flaking of the bark on the scion cultivar.Because of these symptoms, the disease is sometimesreferred to as scaly bark. Symptoms do not occur until thetree is usually over ten years in age. First symptoms of scalybark consist of small flecks of gum on the trunk and mainbranches. These areas become dry and scaly. As theyenlarge, the tree becomes stressed and less productive.Twig and limb death may occur.

Causal agent: The cause of bark scaling in citrus hasfrustrated plant pathologists since symptoms were firstobserved in Florida and California in the late 1890s.Initially, in the 1930s, bark scaling in citrus was namedPsorosis. In the late 1970s, a number of graft-transmit-table diseases that caused bark scaling were lumpedtogether and referred to as Psorosis. They includedPsorosis A, Psorosis B, citrus ringspot, concave gum,cristacortis, and impietratura. The causal agent ofthese diseases was listed as virus or virus-like. The firstof these diseases to be identified as caused by a viruswas the citrus ringspot disease. The causal virus wasnamed the Citrus Ringspot Virus (CRV).

In the 1990s plant pathologists from Argentina,South Africa, Spain, and the U.S. identified a virus,Citrus-psorosis-associated Virus (CPsAV) as a probablecause of certain strains of Psorosis. All of the Psorosisdiseases, including the two caused by viruses, aredisseminated only by infected bud wood. No vectorsof these diseases have been identified. The strains ofPsorosis that occur in Arizona have not been studied.

Control: These diseases have been controlled by eradicationand effective citrus certification programs in Arizonaand California. The disease is not common in Arizona.

MYCOPLASMA DISEASES

STUBBORN DISEASEStubborn disease is a major disease of citrus in North

Africa and in the middle-eastern and Mediterranean citrusareas including Israel, Egypt, and Turkey. In North Americathe disease is known to occur only in the hot, dry citrusareas of Arizona and California. For unknown reasons, thedisease has not been found in citrus in Florida or Texas.Prior to the 1970s, it was thought the disease was caused bya virus. In the early 1970s, however, research in severalareas determined the disease was caused by a uniquemycoplasma-like organism that was named Spiroplasmacitri. Presently, Stubborn is an important disease in Ari-zona and California. In Arizona, Stubborn disease is espe-cially prevalent in Washington Navel trees but may occurin Valencias, Sweets, and Grapefruit.

Symptoms: The disease may appear at any time during thelife of the tree, and severity and symptoms vary fromyear to year. Symptoms consist of stunted growth;misshapen, flat-topped trees; proliferation of shootdevelopment resulting in witches’-brooms; twig die-back; small, stiff, upright foliage showing marked Znor Mn deficiency-like symptoms; occasional diffuseyellow and green mottling of leaves; small leavessharply pointed, cupped, and having marginal chlorosis;fruit malformed, “acorn shaped” with rind thick atstem end and thin at stylar end; many aborted seeds

Figure 13. Symptoms of Stubborn disease in citrus fruit.Note the small malformed fruit (right) taken from a diseasedtree in comparison with a healthy fruit (left). (Yuma, AZ)


found in seedy varieties; progressively decreasingyields of small fruits having insipid flavor; “off-sea-son” bloom. In some instances, only part of the treeshows these described symptoms. Stubborn diseasedoes not normally cause death in citrus. Stunting ismost common in trees that are infected when young.Symptoms are accentuated during hot weather.

Field diagnosis of Stubborn is difficult becausemany of the variable symptoms caused by stubbornmay also be the result of freezing damage, insectinfestations, wind, and improper irrigation or nutri-tional factors. Several laboratory tests are currentlyavailable for diagnosis. They include serologicaltechniques (including ELISA) and indexing.

Situation in Arizona: The causal organism of Stubborn,Spiroplasma citri, has been isolated from ten differentcultivars of citrus in Arizona. Some naturally infectedplants other than citrus include: wild turnip, Brassicasp; London rocket, Sisymbrium irio; Zinnia sp.; Mari-gold, Tagetes spp.; Viola sp.; periwinkle, Vinca rosa;onion, Allium cepa; squash, Cucurbita pepo; plan-tago and Malva sp. Two leafhoppers, Circulifertenellus and Scaphytopius nitridus are vectors of thedisease in the southwestern United States. Recentstudies demonstrated that Spiroplasma citri repro-duces in the sugarbeet leafhopper C. tenellus. Thecells of Spiroplasma citri are injected into plants viasalivary secretion during leafhopper feeding.

Causal agent: Spiroplasma citri is one of the few myco-plasma-like organisms that can be grown in laboratorymedia. The cells of the organism are wall-free, fila-mentous, motile or spiral-shaped. The organism can becultured from infected tissue. Isolates from infectedcitrus in Arizona have been obtained by passing thesap of leaves, bark, and seed through small microbio-logical filters into specific media. Amazingly, S. citri,which was though to be restricted to the southwesternUnited States, was identified in the early 1980s as thecause of brittle root of horseradish in Illinois andMaryland. This fact has prompted a reevaluation of thepotential threat of this organism to non-citrus crops inareas far removed from the southwestern United States.

Control: Nursery trees should be propagated fromStubborn-free budwood. Infected trees should beremoved from the orchard and replaced withhealthy replants.

NEMATODE DISEASES

THE CITRUS NEMATODEMore than 40 nematode species have been described

worldwide on citrus. In Arizona, however, only one spe-cies, the citrus nematode, Tylenchulus semipenetrans, isimportant and damaging. This nematode has become ofincreasing importance since the withdrawal of the soilfumigant, DBCP, which was previously used as a post plantfumigant for control. The citrus nematode was first foundinfecting citrus in California in 1912. The nematode wasdescribed from Arizona in 1926. Today, the citrus nema-tode has been reported in all citrus producing regions of theworld. Surveys made in the United States indicate thatinfestations of citrus areas range from approximately 50 to60 percent in California and Florida to 90 percent in Texasand Arizona.

Symptoms: Symptom development depends on overall treevigor. Infected trees growing under optimum condi-tions may appear healthy for many years. For thisreason, the disease is often referred to as “slow-de-cline.” Heavily infected root systems eventually causea reduction in yield and quality of fruit. Trees in earlystages of decline, however, may have relatively vigor-ous root systems. Above ground symptoms of nema-tode damage are non-specific. Root feeding and sub-sequent damage reduces the overall vigor of infectedtrees. Symptoms include leaf yellowing, sparse foli-age, small, non-uniform fruit, and defoliated up-per branches. Dieback is particularly noticeable in theupper portion of trees. Affected trees appear similar tostress conditions caused by Phytophthora root rot,poor nutrition, and inadequate irrigation. Tree de-cline, which depends upon care of the grove and

Figure 14. A photomicrograph showing typical filamentousgrowth in Spiroplasm citri on a laboratory medium.


overall tree vigor, may not occur for three to five yearsafter heavy infection. Infected roots may appear coarseand dirty. Female nematodes are found in small groupson the root surface. Soil adheres to the gelatinousmatrix in which eggs are embedded. Positive identifi-cation requires the extraction of the nematodes fromsoil samples taken in the feeder root zone between thetrunk and the drip line of the tree. The nematodes mayalso be identified microscopically on infected roots inthe laboratory.

Biology: The citrus nematode, an obligate parasite, repro-duces only on living roots of host plants. Early re-searchers in Arizona proved that populations of nema-todes in roots were highest in the early stages of treedecline and lowest in roots of declining trees. Theyfound that nematode populations and root systemswere almost in equilibrium. Low nematode popula-tions in dead or dying root systems allowed new rootdevelopment. New root development resulted inincreased nematode populations. This repeatingcycle, however, eventually resulted in tree decline.Four races or biotypes of the citrus nematode havebeen described worldwide. A “citrus” biotype hasbeen described from populations of the nematode fromArizona. This biotype reproduces on Citrus spp. andon the hybrids “Carrizo” and “Troyer” citrange as wellas on grape, olive, and persimmon.

Control: No chemicals are presently recommended forpost-plant control of the citrus nematode.

Nonparasitic Diseases

MAJOR NUTRIENTSIn general, citrus trees do not have to be fertilized

heavily, but regular applications of nitrogen in one form oranother are needed. Usually nitrogen is the only majornutrient required. Potassium and phosphorous generallyare adequate in central Arizona soils, but all soils requirenitrogen. On the Yuma Mesa, citrus has responded tophosphate applications.

Nitrogen deficiency, showing up as yellow-green leaves,normally develops over a period of two or four years onunfertilized trees but can be quickly corrected with properfertilization.

Pale green leaves are normal in two situations. A heavydrop of old leaves normally occurs in March and April.Before leaf drop, nitrogen is removed from these leaves andmigrates to new leaves, leaving old leaves pale green.Leaves on shoots produced on grapefruit during the sum-mer and fall normally turn yellow in the winter, but regaintheir green color in the spring.

In southern Arizona, a mature grapefruit tree in good,healthy condition will need an annual application of onepound of actual nitrogen each year. Oranges and othermature citrus will require two pounds. Apply half of this inFebruary and the remainder as a split application in May/August. Manure may be applied periodically in the fall, butshould be supplemented with commercial fertilizer in thespring. On the sandy Yuma Mesa soils, an annual applica-tion of two to three pounds of actual nitrogen is needed formature trees.

Nitrogen can be supplied to the soil in the form of animalmanures, commercially prepared chemical fertilizers or acombination of the two. Commercial fertilizers are gener-ally preferred because research indicates that excessive useof animal manure may induce iron chlorosis in citrus andincrease salts.

Micronutrient deficiencies: The most common micro-nu-trients that are deficient for normal citrus growth inArizona are iron, zinc, and manganese. These elementsare normally not needed before trees are three to fiveyears old. Diagnosis of specific micro-nutrient defi-ciencies is dependant on the location of the symptomson the tree, the pattern of leaf discoloration, and tissueanalysis.

Iron: Iron chlorosis (yellow-white leaves with green veins)is common in Arizona because iron is less available forroot uptake in our alkaline soils. Symptoms normallyappear on young, rapidly growing leaves. Mild symp-toms may disappear with aging of leaves. The entireyoung leaf appears yellow-green with exception of thetissue surrounding leaf veins which remain green.

Leaves may turn almost white with green tissueremaining only around the leaf veins. Lime inducediron chlorosis is a common nonparasitic disease inmany plants grown in Arizona, including citrus. Thedisease is more common in home plantings than incommercial groves because ornamentals and lawns areoften planted near citrus in back yard plantings. Thesenearby plants need frequent irrigation. Iron chlorosisin citrus is exacerbated by overwatering. Shallow-rooted ornamentals that require frequent wateringshould not be planted in tree basins. Grapefruit treesnormally turn yellow during the winter months but re-green as new leaves appear in the spring. Do not applyiron to correct this “winter chlorosis” condition.

To correct iron chlorosis chemically, treat treeswith iron sulfate or an iron chelate compound. Placeiron sulfate in a shallow circular trench around the treetrunk or broadcast it around the entire tree basin fromthe trunk to outside the drip line, and apply four to sixinches of water. An average-size tree requires 20 to 30pounds of iron sulfate. When using iron chelate, applyaccording to label directions to the tree basin area and


irrigate thoroughly.Trees do not respond to chelate applications in

winter but will respond well from April through Sep-tember.

Zinc: Zinc is a common deficiency in Arizona. The symp-toms appear, as with iron deficiency, on recently ex-panded, young leaves. A “mottle-leaf” pattern oc-curs in leaf tissue. Yellowing develops in areas be-tween the leaf veins. Severe deficiency causes smallleaves and short internodes. Defoliation and diebackmay occur in stressed trees. Zinc deficiency is more ofa problem on sandy soils or where manure has beenfrequently applied. Optimum leaf concentration is25-100 ppm (parts per million) Zinc. Deficiencies maybe corrected by foliar or soil applications of zinc saltsor zinc chelates.

Manganese: Deficiency symptoms also occur on youngleaves. Symptoms overlap with those of iron defi-ciency. If leaf tissue concentration of manganeseis below 25 ppm a foliar application of manganesesulfate may be helpful. Soil applications of manganesesulfate in our alkaline soils are less effective than foliarapplications.

ENVIRONMENTAL FACTORSWater stress: Water use in citrus is highest during June,

July, and August and lowest from November throughMarch. In central Arizona research on water consumptionin mature citrus indicates that daily moisture use is lessthan 0.1 inch per day from November through March butincreases to a peak of 0.23 inches per day in July. It was alsodetermined in these studies that approximately 85 percentof the water used in mature navel oranges in central Arizonawas from the upper three feet of the soil profile. Thus, waterloss from the soil under a large mature tree 16 to 20 feet tallis about six inches in July and one inch in January. Averagesandy-loam soils that hold about four inches of waterrequire irrigation at about 20-day intervals in July. Coarsersoils (sandy) require more frequent irrigation. Time eachirrigation by the condition of the tree or trees rather than bythe calendar. A slight wilting of leaves indicates that a treedoes not have enough water and irrigation is needed. Newleaves show the first sign of water stress.

Symptoms of inadequate soil moisture depend on theperiod of stress. Early symptoms consist of leaf rolling.Long droughts may cause defoliation and dieback. InArizona, hot dry winds may accentuate moisture stress andcause leaves to dry up on the tree. In young leaves,chlorosis may occur on the leaf blade between the midriband the leaf margins. These chlorotic (yellowish) areas maylater turn gray to light brown. This condition is referred toas “mesophyll collapse.” Damage to surface roots bydisking or ploughing during water stress situations mayaccentuate this symptom. High daytime temperatures

and dry winds may cause heavy leaf drying in October andNovember. Grapefruit trees seem most susceptible to thistype of injury. In severe cases, small twigs may crack, gumand die. Adequate water during these hot windy periods isthe only practical method of reducing injury.

Freezing damage: Freezing can damage both tree andfruit of all citrus varieties, but some are more sensitive thanothers. Limes and lemons are the most tender, oranges andgrapefruit are of intermediate hardiness, and mandarins arethe most hardy. Older orange and grapefruit trees are quitetolerant to cold and seldom need to be protected. The fruitis usually damaged when temperatures fall below 26° F forseveral hours.

In the desert areas of Arizona, nighttime temperatures candrop below freezing from mid-November to late March,most often in January. In most areas of southern Arizonawhere citrus is grown, some type of frost protection isnecessary from November through March during the firsttwo or three years. Palm fronds give effective protection,but corn stalks also work well. Protect the trunk and mainbranches of young trees, leaving one-third of the leafy areaexposed to sunlight and air, by placing and tying four to sixfronds or 12 to 15 corn or sorghum stalks around the tree.

Young trees can be successfully protected from frost byrunning water under the tree during below-freezing hours,covering them with a large cardboard box, placing a burlapbag over the tree, or covering with cloth. Do not use plasticunless you build a frame to keep the plastic away from treefoliage. Plastic does not hold in much heat compared toother materials. Remove heavy cloth coverings after eachfrost period. Burlap may be left in place for the entirewinter. Hanging a light bulb in the branches on cold nightsprovides additional heat.

Figure 17. Frost damage in lemon. (Yuma, AZ)


If a tree is frozen, do not prune frozen parts until newgrowth emerges in spring. After new growth begins, theexact portions killed by frost can be more clearly seen andpruned off.

Sunburn: Temperatures above 110 degrees F usually burnsome leaves and fruit and may damage any exposedbark on young or old trees. Protect any exposed barkareas with tree wraps or white, water-base paint.

When lower branches or tops of old trees have beenpruned, exposed bark usually is sunburned andmay be killed. Fungus infection may follow and de-stroy larger areas. Such trees must be protected bypainting trunks and scaffold limbs with whitewashor any white, water-base paint. Heavy paper tree pro-tectors or cardboard should be applied to young treesafter painting.

Leaf and Fruit Drop: Two conditions, leaf drop and fruitdrop, are poorly understood problems in citrus. Leafdrop appears to be a normal phenomenon. Citrus, anevergreen tree, sheds leaves gradually throughout theyear. Replacement of leaves occurs naturally. Leafdrop is heaviest during the spring months but occurs tosome extent all year. Fruit drop may also be a normalphysiological event.

Only a small percentage of the blossoms on a treedevelop into fruit. Although most of these drop soonafter petal fall, some fruit will drop in later May andJune.

In most years, this June drop allows crop thinning.If it did not happen, the tree would break down underthe load and fruit would be small and inferior.

The amount of June drop depends on variety. Seed-less oranges have greater drop than ones with manyseeds; tangerines with many seeds have a smallamount of drop. Cross-pollination of Tangelo and

Tangerine varieties causes many more seeds todevelop and thus reduces the drop.

With Valencia oranges and grapefruit, a heavy cropof mature fruit reduces the food supply to the youngfruit and this increases the drop.

In some years, high temperatures in May help in-duce heavy drop. Maintaining an even wateringschedule and adequate nutrient level for tree use willminimize small fruit drop in most varieties.

Toxicity of salts: Salinity is measured and reportedin terms of EC (electrical conductivity) of a soil-saturation extract (ECe) or water (ECw). Citrus ismoderately salt tolerant provided that levels of boronor lithium are not toxic.

The units of ECe measurement are mhos per centime-ter (mhos/cm). A soil analysis report will usuallycontain a column for ECe x 103, the electrical conduc-tivity of a saturation extract of the soil multiplied by1000 and reported as mmhos/cm. The soil sampleshould be taken in the root zone. Water analysis willreport ECw x 103. It is interesting to compare thesensitivity of citrus to some of the major crops grown inArizona. Citrus is sensitive to soil salinity at ECe valuesin excess of 1.8. This sensitivity is similar to other cropsgrown in Arizona such as potatoes, corn, peppers,lettuce, grapes, almonds, and plums.

The threshold for salt damage in citrus is an ECe of 1.8(approximately 1152 ppm total salts). At ECe 3.0 (approxi-mately 1920 ppm salts) there is approximately a 20 percentreduction in yield. Symptoms of salt injury consist ofirregular brown necrotic (dead) areas along the leaf marginsand near the leaf tip. Defoliation, dieback, and fruit dropand yield reductions occur in acute cases. Excessive fertili-zation may cause these symptoms. Heavy irrigation mayreduce salt concentrations. Most commonly these prob-lems occur in backyard situations where frequent, lightirrigations and soil water evaporation move salts into theupper root zone.

Figure 18. Sunburn damage on citrus fruit. (Phoenix, AZ)

AZ1154

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