Citrus Viruses And Virus-Like Diseases

http://edis.ifas.ufl.edu/ ( Publisher's URL )
MISSING IMAGE

Material Information

Title:
Citrus Viruses And Virus-Like Diseases
Physical Description:
Fact sheet
Creator:
Ferguson, James J.
Publisher:
University of Florida Cooperative Extension Service, Institute of Food and Agriculture Sciences, EDIS
Place of Publication:
Gainesville, Fla.
Publication Date:

Notes

Acquisition:
Collected for University of Florida's Institutional Repository by the UFIR Self-Submittal tool. Submitted by Melanie Mercer.
Publication Status:
Published
General Note:
"Publication date: December 1993.""
General Note:
"Circular 1131"

Record Information

Source Institution:
University of Florida Institutional Repository
Holding Location:
University of Florida
Rights Management:
All rights reserved by the submitter.
System ID:
IR00004645:00001


This item is only available as the following downloads:


Full Text

PAGE 1

Circular1131 TheInstituteofFoodandAgriculturalSciencesisanequalopportunity/affirmativeactionemployerauthorizedtoprovideresearch,educational informationandotherservicesonlytoindividualsandinstitutionsthatfunctionwithoutregardtorace,color,sex,age,handicap,ornational origin.Forinformationonobtainingotherextensionpublications,contactyourcountyCooperativeExtensionServiceoffice. FloridaCooperativeExtensionService/InstituteofFoodandAgriculturalSciences/UniversityofFlorida/ChristineTaylorStephens,DeanDecember1993CitrusVirusesandVirus-LikeDiseases1 J.J.FergusonandS.M.Garnsey2IMPORTANCEVirusandviruslikediseaseshaveamajorimpact oncitrusproductionworld-wideandoftenbecomethe dominantyield-limitingfactoringrovemanagement. Themostobviousimpactofthesediseasesistheir lethaleffectonspecifichosts.Tristezaalonehas destroyedapproximately50milliontreesinthepast 40-50years.Alessobviousbuteconomically importanteffectisthevarietyofnon-lethal,subtle responsesthatreducetreesize,treevigorandfruit yield.Inmanycases,growerssuffersignificantlosses fromvirusdiseaseswithoutrecognizingthenatureof thesediseases.Finally,citrusvirusandvirus-like diseasesmayrestrictthegrower'schoiceofscionsand rootstocksthatcanbegrownprofitablyincertain areas.Forexample,tristeza-sensitivecultivarsmust oftenbeavoidedinareaswheresevereformsofthe virusareprevalent,eventhoughallotherfactors wouldpredictprofitableuseofthesecultivars.NATUREOFVIRUSES StructureVirusesareextremelysmall,infectiousparticles. Plantvirusesarecomposedofanouterprotective sheathofproteinandaninnercoreofnucleicacid, thegeneticmessengermaterialfoundinallliving organisms.Plantvirusesdifferinshapeandsizebut aregenerallyeitherthreadlikeorspherical.They rangeinsizefrom1/12,000to1/1,250,000inchand areconsiderablysmallerthanotherplantpathogens. Althoughvirusesareagentsofdisease,asare bacteria,fungiandnematodes,andcantransmit geneticinformation,theycannotgroworreproduce bythemselvesoutsidethehostplantascanmost livingorganisms.Virusescanreplicateonlyinside suitablehostcellsbyconvertingthereproductive machineryofthehostcelltoreproducethe componentsofthevirus.Viroidsareevensmallerand containonlynucleicacidwithoutanyproteincoat.HostsAmultitudeoflivingorganisms,from single-celledplantsoranimalstolargetreesand mammals,canbeattackedbyviruses.Someviruses attackmanandotheranimalsandcausediseasessuch asinfluenza,polio,rabies,smallpoxandwarts.Other virusescauseplantgalls,flowerbreak,stuntingand decline.Stillothervirusesattackmicroorganismssuch asbacteriaandfungi.Overathousandvirusesare knownandmorethanhalfofthesevirusescause plantdiseases. 1.ThisdocumentisCircular1131,aseriesoftheHorticulturalSciencesDepartment,FloridaCooperativeExtensionService,InstituteofFood andAgriculturalSciences,UniversityofFlorida.Publicationdate:December1993. 2.J.J.Ferguson,AssociateProfessor,CitrusSpecialist,DepartmentofFruitCrops,CooperativeExtensionService,InstituteofFoodand AgriculturalSciences,UniversityofFlorida,Gainesville,FL32611;S.M.Garnsey,CitrusVirologist,USDA,AgriculturalResearchService,2120 CamdenRoad,Orlando,FL32803. Theuseoftradenamesinthispublicationissolelyforthepurposeofprovidingspecificinformation.Itisnotaguaranteeorwarrantyofthe productsnamed,anddoesnotsignifythattheyareapprovedtotheexclusionofothersofsuitablecomposition.

PAGE 2

CitrusVirusesandVirus-LikeDiseases Page2SymptomsPlantvirusescancauseavarietyofdisease symptoms,mostofwhichresultfromsystemic infection(infectionspreadthroughouttheplant). Stuntingandreductioninyieldareprobablythemost commoneffectsofviraldiseasesofplantsbutspecific foliage,fruit,woodandbarksymptomsalsooccur. Thesesymptomsincludemosaics,yellowingand ringspots.Amosaicpatternconsistsoflight-green, yelloworwhiteareasmixedwiththenormalgreen colorofleaves.Dependingontheintensityof infectionortheparticularpatternofdiscoloration, mosaicscanbedescribedasmottling,streaking,vein clearing,veinbanding,chlorosisandspotting. Yellowingreferstoauniformdiscolorationor chlorosisoffoliagewithoutanyspottingpatterns. Ringspotisadistinctivepatternofabrown, red-brownoryellowbordersurroundingagreen center.TransmissionPlantvirusescanbespreadinvariousways, includingpropagation(buddingandgrafting), contaminatedplantsap,seedorpollen,insects,mites, nematodes,certainfungiandparasiticplants (dodder).Theprincipalmeansoftransmissionof citrusvirusesareinfectedpropagativematerial, insectsandcontaminatedtools. Theprimarypurposeofbudwoodcertification programshasbeentopreventthespreadofvirusesby infectedbudwoodandcontaminatedseed.Despite variousquarantinesagainstthemovementof potentiallydiseasedplantmaterial,including budwood,manhasfrequentlymovedcitrusviruses longdistancesandestablishedtheminnew productionareas.Seedtransmissionofpsorosishas beenobservedinTroyercitrange,Carrizocitrange andtrifoliateorange.Noothercitrusvirusesare knowntobetransmittedthroughseed.Pollen transmissionofcitrusviruseshasnotbeen demonstrated. Inoculationofhealthyplantswithsapfrom infectedplants(mechanicaltransmission)isimportant inthefieldspreadofpathogens,suchascitrus exocortisviroidwhichcanbeeasilyspreadasa contaminantonpruningandcuttingtools.Theuseof virus-freebudwoodandbudwoodcertification programsarehighlyeffectiveforcontrollingviruses spreadmainlybypropagationsuchasmuchofthe psorosiscomplex,exocortisandxyloporosis. Insectsaresignificantvectorsofseveralimportant virusandvirus-likepathogensofcitrus.Although tristezaisspreadbyseveralspeciesofaphids,the mosteffectiveaphidvectoroftristeza, Toxoptera citricida,thebrowncitrusaphid,hasnotyetoccurred inFlorida,buthasbeenrecentlydiscovered throughouttheCaribbean.Threemajorvirus-like diseases(stubborn,greeningandcitrusvariegated chlorosis)arecausedbyspecializedtypesofbacteria andarespreadbyseveraldifferentleafhoppersand2 speciesofcitruspsyllids(insectsthesizeof planthoppers).IDENTIFICATIONANDDETECTIONTheclassicmeansofidentifyingvirusandviruslikeinfectionsincitrusisbasedonidentificationof symptomsinthefieldorbyinoculatingcitrus indicatorplants(herbaceousandwoodyplantsthat aresensitivetoaparticularvirus).Herbaceous indicatorplantshavebeenused1)toidentifysome mechanicallytransmittedvirusesand2)todetect unsuspectedlatentinfections(infectionwithoutthe developmentofvisiblesymptoms)notrevealedby testsusingcitrusindicatorplants.Reliableherbaceous indicatorplantshavebeenfoundforexocortis,but notfortristeza,xyloporosisandmostformsof psorosis. Althoughimprovementintheuseofcitrus indicatorplantshasbeenmade,plantproceduresstill requireextensiveperiodsoftime,goodplantmaterial andfacilities,andskilledpersonnel.Interpretationof resultsformildstrains(virusstrainsthatcauseonly mildsymptoms)andformixedinfections(infectionof aplantbymorethanonevirusatthesametime)may dependontemperature,plantvigorandthe experienceoftheobserver. Considerableprogresshasbeenmadein developingserologicaldetectionproceduresforcitrus viruses.Serologyreferstotheuseofaportionof animalblood,theserum,inproceduresthatareused toidentifyviruses.Thefirststepintheserology procedureistoinoculateanimals,usuallyrabbitsor mice,withpurifiedvirus.Thevirusactsasanantigen orforeignsubstancethatstimulatestheimmune systemoftheanimaltoproducespecificantibodies thatreactonlywiththevirusinjected.These antibodiesarecollectedfromtheserumportionofthe animal'sbloodandareusedinvariouslaboratory

PAGE 3

CitrusVirusesandVirus-LikeDiseases Page3teststoidentifyviruses.Onesuchassayreferredtoas ELISA(EnzymeLinkedImmunosorbantAssay),has beenusedaroundtheworldtotestmillionsofcitrus treesfortristeza.Serologyproceduresareavailable forthreecitrusviruseswhichoccurinFlorida (tristeza,citrusvariegation,andcitrusleafrugose viruses).CONTROLControlstrategiesforplantvirusesinclude1) avoidanceorexclusionofthedisease,2)theuseof certifiedbudwood,3)eradicationorsuppression,4) theuseoftolerantorresistantcultivars,5)cross protection,and6)culturalpracticesthatreduce infection.Thesuccessofeachofthesecontrol strategiesdependsonanumberoffactors,including knowledgeofthecausalagentofthedisease, symptomsandmodeofdissemination.MAJORVIRUSESANDVIRUS-LIKE DISEASES Tristeza SignificanceCitrustristezavirus(CTV),themostdestructive virusdiseaseofcitrus,hascauseddisastrouslossesin manycitrus-producingareasworldwide."Tristeza," whichmeanssadnessormelancholyinSpanish, actuallyreferstoseveraldiseasesymptoms,manyof whichoccurinFlorida.Strainsoftristezaexistwhich differinthesymptomstheyproduce. ThetristezasymptommostfamiliartoFlorida growersisaquickdeclineoforange,grapefruitand mandarintreesonsourorangerootstock.CTVcan alsocausestempittinginlimes,somesweetoranges, grapefruitandinsomerootstockslike Citrus macrophylla.Severestempitting,whichcanbevery damaging,ispresentinmajorcitrusgrowingareas suchasBrazil,SouthAfrica,AustraliaandAsia. Severestempittingduetotristezaisnotpresentin Floridabutwouldcausesevereproblemsinthefuture ifintroduced.Severestrainsoftristezamaycause seedlingyellows,aleafchlorosisandstuntingofsour orange,lemon,grapefruit,andcitronseedlings.The leavesonaffectedplantsaresmallandyellowand growthusuallyceasesafterthefirstfewleavesare formed.Seedlingyellowsisanexperimentalreaction thatoccursinlaboratoryindicatorplantsandis usuallynotencounteredinthefield.Thesignificance ofseedlingyellowsisthatitindicatesthepresenceof severestrainsoftristeza.Symptoms DeclineFielddiagnosisoftristezacanbebasedon observationofthefollowingsymptoms:1)tristeza decline,associatedprimarilywithtreesonsourorange or Citrusmacrophylla rootstocks,2)affectedtreeslack feederrootsanddonotmaintainnormalamountsof starchinroots,3)decliningtreesfrequently,butnot always,showhoneycombingandthickeningofthe innerbarkjustbelowthebudunion. Treedeclineusuallyresultsfromreductionofthe feederrootsystemornecrosisofthephloemtissue nearthebudunion.Declinesymptomscanbe associatedwithanumberofdiseasesincludingfoot rotandrootrot,nematodediseaseslikespreading declineandslowdecline,blight,anumberofviruses, androotweevilandwaterdamage.Intristezadecline, thephloem(conductingtissuelocatedinsidethebark throughwhichsugarsproducedintheleavesby photosynthesisaremovedtoroots)isaffected,thus girdlingthetree.Thisgirdlingisassociatedwithleaf chlorosisandwilting,heavyfruitset,starchdepletion intherootsystemanddestructionoffeederroots. Withoutfeederrootsthetreewilts,producingquick declinesymptoms. Treesdecliningfromtristezausuallyhavereduced starchlevelsintheirrootsystems.Starchcanbe detectedbydippingcutendsofrootsinaniodine potassiumiodidemixture.Rootsturnblue-blackwhen starchisabundantbuttherootsofatristeza-affected sourorangetreeusuallydonotstain.However,since decliningtreesaffectedbyotherdiseaseslikeblight oftenhavelowrootstarchlevels,thisprocedureisnot aninfallibletestfortristeza. Treeswith"quickdecline"maydierapidly,with theprogressionofsymptomsfromleafwiltingtotree deathoccurringwithinseveralweeks.Suchtreesmay alsofruitheavilybecauseofstarchaccumulation abovethebudunion.Ayelloworbrownstainmay occurontheinnerfaceofthebark,justbelowthe budunion. InFlorida,treescommonlydeclineoveraperiod ofseveralyears.Treesthatdeclineslowlyusually develophoneycombingsymptoms(amassingof numeroussmallpinholesontheinsideofthebark

PAGE 4

CitrusVirusesandVirus-LikeDiseases Page4justbelowthebudunion).Inaddition,theinnerbark ofaffectedtreesonsourorangerootstockoften thickensjustbelowthebudunion.Whenbudwood infectedwithsevereisolatesofcitrustristezavirusis propagatedonsourorangerootstock,youngtrees growweakly,oftensetfruitprematurely,arechlorotic andmayremainstuntedandunthrifty.StemPittingStempitting,aconditionassociatedwithtristeza andseveralothercitrusvirusdiseases,consistsof depressionsintheouterwoodwithcorresponding pegsorprojectionsontheinnerfaceofthebark.This pittingcanbeseenbypeelingthebarkoffsmall twigs.Tristeza-inducedstempittingcanvary accordingtovirusstrainandhost. Inseverecasesofstempitting,thetrunkand scaffoldlimbshaveagnarledorropelikein appearance. Citrusmacrophylla seedlingsfrequently showmoderatestempittingfromFloridastrainsof tristeza.Severestrainsoftristezamaycausestem pittinginsweetorangecultivarsregardlessof rootstock. Affectedtreesareusuallystuntedorhaveamore compactgrowthhabitthannormaltrees.Sweet orangestempittingstrainsoftristezaoccurinBrazil, Peru,JapanandCalifornia.However,noseverestem pittingstrainshavebeenreportedinFlorida.PlantsAffectedWithfewexceptions,mostcitruscultivarscan becomeinfectedwithcitrustristezavirus(CTV),but many(mandarins,sweetoranges,roughlemonand Rangpurlime)oftendonotshowobvioussymptoms). Others(lime,lemon,grapefruit,citronand Citrus macrophylla)showsymptomsofvaryingintensity. Trifoliateorangeandsometrifoliateorangehybrids suchasCarrizocitrangeareresistanttotristeza infection.Thatis,thevirusdoesnotmultiplyinthese plantsevenwhentheyaregraftedwithCTV-infected scionmaterial.TransmissionTristezaisspreadinFloridabypropagationand byaphids.By1968,extensivenaturalspreadof tristezabyaphidsforcedtheBudwoodRegistration ProgramtoabandonhopesofmaintainingtheCitrus BudwoodFoundationGroveasvirus-free.Valuable scionsourcescouldnotbemaintainedfreeoftristeza inthefieldandnewlypropagatednurserytreeswould becomeinfectedeventuallyinanycase. A1980surveyindicatedthatabout90%ofthe registeredbudwoodsourcesofsweetorange propagatedonsourorangewereinfectedwith tristeza.Manyofthesetreespresumablycarrymild strains,butsincemostnurserieshavepropagatedtheir budwoodsourcesontristeza-tolerantrootstocksthe severityorvirulenceofthestraincannotbe determinedfromtheconditionofthetreefromwhich thebudwoodwastaken. Recentobservationsclearlyshowthatsome budwoodsourcetreesare,infact,infectedwithsevere strainsthatproducestuntedtreesonsourorange rootstock.Budwoodfromtreesinfectedwithsevere strainsproducevigorous,normaltreeson tristeza-tolerantstocks.However,thesetreesonly servetoincreasethereservoirofseveretristeza strainsthatcanbespreadbyaphidstoadjacent plantingsoftreesonsourorangerootstock. Threespeciesofaphids(Toxopteraaurantii,the blackcitrusaphid, Aphisgossypii ,themelonaphid, and Aphisspiraecola,thespireaaphid)canvector tristezainFlorida.Fortunately,themosteffective vector, Toxopteracitricida,thebrowncitrusaphid,is notyetpresent. Differentstrainsoftristezacanbespreadby differentaphidsatdifferentrates.Aphidspreadof citrustristezavirusisalsoaffectedbyenvironmental conditionsandbythehostitself.Somehostcultivars apparentlyarebettertristezasourcesandsomeare betterreceptorplantsthanothers.Ingeneralnatural spreadismorerapidinorangeandgrapefruitthanin othercitrus.Control TristezaResistantRootstocksSeveralconditionsaffectcontrolstrategiesfor citrustristezavirus(CTV)inFlorida:1)thevirusis alreadywidespreadandmostbudwoodsourcesare infected,2)CTVisnaturallyspreadbyaphidsfrom thelargeinoculumsourcealreadypresent.The growerisfacedwiththechoiceofeitheracceptingthe risksoftristezaandplantingtreesonsourorange rootstockorofchoosinganotherrootstockwithother inherentdiseasesusceptibilitiesandhorticultural characteristics.

PAGE 5

CitrusVirusesandVirus-LikeDiseases Page5Tristeza-tolerantorresistantrootstocksare available,andtristezadeclinecanbeavoidedbyusing roughlemon,Volkamerlemon,Rangpurlime, Cleopatramandarin,Carrizocitrange,trifoliate orange,sweetorangeorSwinglecitrumelo(seeTable 1).Thesealternativesgenerallyhaveotherdrawbacks suchassusceptibilitytoblight,footrotorcold.New hybridrootstocksarebeingdevelopedcontinuously, buttheirvaluecannotbedeterminedwithoutyearsof fieldtesting.Forthemoment,thegrowermust evaluateallriskscarefullyandchoosetherootstock thatposesthefewestrisksforhisownsituation. ThetristezasituationinFloridawillnotimprove andgrowersshouldnotusesourorangewithout consideringthelongtermrisks.Ifsourorange rootstockisused,itshouldnotbepropagatedwith budwoodcontainingasevereisolateofCTV.At presentthiscanbestbedonebyascertainingthatthe budwoodsourcehaspreviouslyperformedwellon sourorangeandbyobservingthattheyoungbudlings growoffwellinthenurseryandinyoungplantings. Bewareofbudwoodsourcesthatperformmarkedly lesswellonsourorangethanonCleopatramandarin orCarrizocitrangerootstock.ScreeningTheBudwoodRegistrationProgramisscreening someofthemostheavilyusedregisteredsciontrees andinformationonthespecificcitrustristezavirus (CTV)contentofindividualsourcetreesshouldsoon beavailable.Sincebiologicalscreeningtestsareslow anddifficulttoconductonalargescale,meansto rapidlyscreentreesforstrainseverityremainsahigh researchpriority. Itisimportanttoallgrowersthatthereservoirof severeCTVisolatesnotbeincreasedneedlesslyby propagation.Yetwiththecurrentproductionofover 14millionbuddednurserytreesperyear,the potentialisobvious. Growerswhochoosetristezatolerantorresistant stocksarelesslikelytobeconcernedthanthosewho choosesourorange. Quarantineeffortsshouldbemaintainedand increasedtoprevententryofmoresevereCTVstrains fromoverseasandfromothercitrusproducingareas andtoprevententryofthebrowncitrusaphidwhich isthemostefficientvector.Smugglingofprize newhorticulturalselectionsfromoverseasisalwaysa temptationandcannotbeentirelypreventedby regulations.Growersshouldthereforestrongly supportagriculturalquarantinesandinspectionsat portsofentry.MildStrainCrossProtectionMildstraincrossprotection,wherebythemild strainisdeliberatelyintroducedintoatreeand preventsthesubsequentexpressionofseverestrains whichareinoculatedlater,hasbeenproposedasa controlstrategyfortristeza.Healthy-lookingtreeson sourorangecarryingmildstrainsoftristezamay,in fact,haveanaturalcrossprotectionalready.The protectiveabilityofnaturallyoccurringmildstrainsin Floridahasnotbeenprovenalthoughmanytestsare inprogress.Preliminaryexperimentaldatasuggest cautioninthatsomemildisolatesdonotprotectwell againstaphidreinfectionwithseverequick-decline isolates.Mildstraincrossprotectionisusedona commercialbasisinBraziltoprotectagainstthestem pittingeffectsofcitrustristezavirus(CTV)inPera orangegraftedonCTV-tolerantrootstocks,primarily Rangpurlime.Onlyverylimitedfielddataforcross protectionintreesonsourorangerootstockare availablefromFlorida,CaliforniaandAustralia.Mild straincrossprotectionmayeventuallybeusedtohelp deterCTVdeclineeffectsonsourorangebutitwill notbeacompletelongtermsolution.LongTermApproachesAlongtermapproachtotristezacontrolisto developresistantscioncultivarsandcitrustristeza virus(CTV)tolerantsourorangetypes.The resistancefoundintrifoliateorangecanbe transferredbyhybridizationandpreliminaryresults suggestthatdevelopmentofCTVresistantscion cultivarswithacceptablefruitqualityispossible. Unfortunately,incorporatingtheneededhorticultural propertieswillbemoredifficultthanincorporating CTVresistance. Anotherapproachistoreducenaturalspreadby aphidvectors,eitherbydirectcontrolofthevectorat criticalperiodsorbydevelopingcultivarsthatare repellenttoaphids.

PAGE 6

CitrusVirusesandVirus-LikeDiseases Page6 Table1. SusceptibilitytoTristezaDecline. Rootstock Susceptibility CarrizoCitrange notsusceptible Citrusmacrophylla moresusceptible Citrusvolkameriana notsusceptible CleopatraMandarin notsusceptible Milam notsusceptible RangpurLime notsusceptible RoughLemon notsusceptible SourOrange verysusceptible SweetOrange notsusceptible SwingleCitrumelo notsusceptible TrifoliateOrange notsusceptiblePsorosis SignificancePsorosis,acomplexofdiseasesthatisdistributed worldwide,canaffectmostcitruscultivars.Thecausal agentofpsorosishasnotyetbeenidentified,butitis assumedtobeavirusoragroupofviruses.The formsofpsorosisthatoccurinFloridaarepsorosisA, psorosisB,blindpocketandconcavegum.Thereis someevidencethatthepsorosisBstrainmaybe identicaltosomestrainsofcitrusringspotvirus. PsorosishadbeenwellcontrolledbytheBudwood RegistrationProgrambutcanstillbefoundinolder plantingsinmanyareas. Recently,interestinpsorosisBorringspothas increasedbecausenaturalspreadoccursbyunknown meansinArgentina,Texas,and,inonecase,in Florida.Treedeclinefromnaturalpsorosisinfections iscurrentlyamajorprobleminArgentinaandis regardedasapotentialthreatinFloridaandTexas.LeafandFruitSymptomsAllformsofpsorosiscancausefleckingsymptoms inyoungleavesbutthesesymptomsnormallyareseen onlyinearlyspringinthefieldandeventhenonlyon someleaves.Leafsymptomscharacteristicofpsorosis Aconsistofafleckingpatternarrangedinfaintbands 1/4-1mmwide(1/101-1/25inch)alongtheleaf veins.Leaffleckingarrangedinanoakleafpattern centeredonthemidribisassociatedwithconcave gumformofpsorosis.Leafpatternsfadeasleaves matureandusuallyarenotvisibleinfullymature leaves. PsorosisBleafsymptomsconsistoffleckingand chloroticblotchpatterns,oftenwithsomeringspot patternsthatcanpersistinmatureleaves.Fruitmay showpartialorcompleteringsofsunkentissueonthe rind.Theundersurfaceofmatureleavesmayalso showbrownswellingsthatresemblegreasyspot.Since meticulousinspectionisrequiredtofindleaf symptomsevenonknowninfectedtrees,leafflecking isgenerallynotconsideredtobeagoodfield diagnosticsymptom.BarkSymptomsInFlorida,psorosisAbarkscalingusually developsapproximately6yearsaftertheappearance ofleafsymptoms.Scalingbeginsinisolatedareasof thetrunkormainlimbsandconsistsoftheseparation fromthebarkofsmall,dryirregularflakes0.2-0.3 mm(1/127-1/84inch)thick.Scalinginvolvesmoreand moreofthebarkuntiltheaffectedareaencirclesthe entiretrunk,severelyaffectingtreehealth,yieldand susceptibilitytofreezeinjury.Scalesremainattached attheedgeofthelesionandcurloutwardlikea shingle.Conductingtissuejustinsidethebark becomesimpregnatedwithbrowngum.Whenlesions becomeadvanced,normaltransferofnutrientsis impededbythegumformationandtheportionofthe treeabovethelesiondeclines.Thecurlingofthebark toproduceanawning-likeeffectandtheexudationof minorquantitiesofgumhelptodistinguishpsorosis Afromscalinginducedbyothercauses.InpsorosisB, scalingandwoodsymptomsaresimilartopsorosisA exceptthattheydevelopmoreextensively. Blindpocketpsorosisischaracterizedby steep-sided,narrow,channel-likeparalleldepressions runninglengthwiseinthetrunk.Aformknownas eruptiveblindpocketpsorosisisfurthercharacterized byscalingofthebarkandtheflowofgum.Neither typeofpsorosisoccursfrequentlyinFlorida,butthey arementionedherebecauseblindpocketpsorosisis sometimesconfusedwithfoldsthatnormallyoccurin cultivarssuchastangerine,tangeloandtrifoliate orange.Concavegumpsorosiscausessomewhat similarsymptoms,butthedepressionsarelesssevere. Limbsmaybeflattenedsomewhattocreatean "ax-handle"effect.Incontrasttonormaldepressions,

PAGE 7

CitrusVirusesandVirus-LikeDiseases Page7gumimpregnationsarefoundinthewoodwith concavegumandblindpocketformsofpsorosis.PlantsAffectedMostcultivarsdevelopleafsymptoms,butbark scalingandtreedeclineoccurprimarilyonsweet orange,grapefruitandsomemandarins.Even cultivarswhichdonotexpressdistinctsymptoms generallycanbeinfectedbythevirus.Budunion effectshavenotbeendescribed,butdifferent reactionscanbeseenreadilyinsomescion-rootstock combinations(seeTable2).Forexample,whensweet orangescionsaregraftedonsourorangerootstock, barkscalingisconfinedtosweetorange.TransmissionAllstrainsofpsorosisaretransmittedbyinfected budwood.Novectorsareknownbuttheyare suspectedinsomelocations.Experimental, mechanicaltransmissionofsomestrainshasbeen demonstrated,butmechanicalspreadinthefieldhas notbeenreported.Seedtransmissionofpsorosis occursinCarrizoandTroyercitrangesandin trifoliateorange. Table2. SusceptibilitytoPsorosis. Rootstock Susceptibility CarrizoCitrange notsusceptible Citrusmacrophylla notsusceptible Citrusvolkameriana notsusceptible CleopatraMandarin notsusceptible Milam notsusceptible RangpurLime notsusceptible RoughLemon notsusceptible SourOrange notsusceptible SweetOrange susceptible SwingleCitrumelo notsusceptible TrifoliateOrange notsusceptibleControlFloridagrowerswhopurchaseregisteredtrees shouldhavenopsorosisproblems.Theobservationof naturalspreadofaformofpsorosis(ringspot)in Argentinaand,toalesserextent,inTexas,is triggeringsomeadditionalresearchonpsorosis.At leastonecaseofnaturalspreadhasbeenobserved experimentallyinFloridabutitapparentlyremains uncommon.Growerswhoarereplantinginareas heavilyinfestedwithpsorosisshouldwatchfor evidenceofnaturalinfectioninyoungtreesand contacttheirExtensionofficeimmediatelyif symptomsareobserved.Exocortis SignificanceCitrusexocortiswasoriginallyconsideredtobe causedbyavirus,butisnowknowntobecausedby aviroid;asmall,infectious,self-replicatingnucleic acidmoleculewithoutacoatprotein.Viroidsare extremelysmalland,evenwhenhighlymagnifiedwith specialtechniques,aredifficulttovisualizewithan electronmicroscope.Sincetheviroidmoleculehasa specialconfiguration,itisstabletoheatandtoother treatmentswhichinactivateviruses. Theprimaryeconomiceffectofcitrusexocortis viroid(CEV)isdwarfingoftreesgraftedon susceptiblerootstock.Scalingoftherootstockbark mayalsooccur.Theeffectsarerarelylethalandthe degreeofstuntingvarieswiththestrainofCEV. Majordamagefromexocortishasnotoccurredin Floridabecauseexocortis-freebudwoodsourceswere developedbeforeexocortis-sensitiverootstockswere usedextensively,andthepossibilitiesforspreadon contaminatedtoolswererecognized. Strainsofexocortisvarygreatlyinseverity.Mild formsofexocortishavebeenusedtoproducedwarfed citrustreesforhigh-densityplantings.Whilethis approachtotreedwarfingispromising,itmayhave limitedapplicationinFloridawhere exocortis-sensitivestocks(trifoliateorange,Carrizo citrange,Rangpurlimeandsweetlime)arealso susceptibletoblight.

PAGE 8

CitrusVirusesandVirus-LikeDiseases Page8SymptomsThemostobviousfieldsymptomsofexocortisare barkscalingontherootstockandgeneralstuntingof thetree.Barkscalingusuallybeginswhentreesare fromthreetoeightyearsold.Infectionbysevere strainsbecomesapparentmorequicklythaninfection bymildones.Thefirstsymptomsareshallow, longitudinalsplitsinthebarkbelowthebudunion.In time,splittingoccursovertheentirerootstockand stripsofbarkbegintoscaleoff.Incontrasttosome otherdiseases,thebarktissueunderneaththescales remainsalive. Severestrainsofexocortiscanstunttreesbadly, especiallythoseontrifoliateorangerootstock.Fruit qualityisnormallynotaffected.Yieldreductionis generallyassociatedwithreducedcanopysize.Arapid indexingmethodisavailableforexocortiswhich utilizestheviroid-stimulatedleafdistortionand stuntingofEtrogcitronandseveralherbaceous plants.Anotherrapidindexingprocedurewhich involvespurifyingcitrusexocorticviroidfrominfected tissueandsubjectingittolaboratoryanalysishas recentlybeendeveloped.PlantsAffectedTrifoliateorange,CarrizoandTroyercitrangeand Rangpurandsweetlimeareimportantcommercial rootstockssusceptibletoscaling;however,cultivars whichdonotexpressdistinctsymptomsgenerally allowreplicationoftheviroid.Budunioneffectshave notbeendescribed,butdifferenthostreactionscan beseenreadilyinsomescion-rootstockcombinations. Forexample,whensweetorangescionsaregraftedon trifoliateorangerootstockbarkscalingisconfinedto thetrifoliateorangetissueofthetrunk.TransmissionExocortiscanbespreadbybuddingandgrafting andasacontaminantonpruningequipment.The BudwoodRegistrationProgramhaslargelyeliminated thespreadofexocortisthroughtheuseofregistered nurserystock,butexocortis-infectedcitrusisstill producedfromnonregisteredsourcesinFlorida. Treeswithtolerantscion-rootstockcombinationswill notshowanyobvioussymptoms(seeTable3). Hedgingequipmentcanprobablyspreadtheviroid, buttheextentofthespreaddependsuponthe numberoftreesthatareinfected,thecultivarsthat areinfectedandthecultivarsthatwillbeinoculated. Tangelosandgrapefruitarelesssusceptibleto mechanicalinoculationthansweetorange.Ifatreeis largeenoughtohedgeandtop,thenexocortis infectionshouldnotbeaproblemeventotreeson sensitiverootstocks.Someeventualreductionin growthcouldoccurifmaturetreeswereinfectedbut thesetreesshouldcontinuetobeproductive. Accidentalcontaminationofbudwoodsource trees,nurserytreesoryoungtreeplantingsvia buddingorpruningequipmentcanbeaveryserious problemandmustbeavoided.Growersshould purchasetreespropagatedfromexocortis-free budwoodandshouldprotectyoungtreesagainst contamination. Forexample,Carrizocitrangehasbeenfrequently usedasareplantrootstockinmaturegrovesitesand caneasilybecontaminatedduringnormalgrove operations.DiseaseControlSinceexocortiscanbespreadthrough propagationofinfectedbudwoodandvia contaminatedbuddingorpruningtools,budwood certificationcoupledwithdecontaminationofcutting toolsconstitutestheprimarycontrolstrategy.Two disinfectantsthathavebeenfoundeffectiveagainst theviroidareanaqueoussolutioncontaining2% sodiumhydroxideplus2%formalinorafreshlymade 5-10%solutionofcommonhouseholdbleach.

PAGE 9

CitrusVirusesandVirus-LikeDiseases Page9 Table3. SusceptibilitytoExocortisViroid. Rootstock Susceptibility CarrizoCitrange moresusceptible Citrusmacrophylla notsusceptible Citrusvolkameriana notsusceptible CleopatraMandarin notsusceptible Milam notsusceptible RangpurLime moresusceptible RoughLemon notsusceptible SourOrange notsusceptible SweetOrange notsusceptible SwingleCitrumelo notsusceptible TrifoliateOrange verysusceptibleXyloporosis/Cachexia SignificanceXyloporosis/Cachexiahasgenerallybeen consideredavirusdiseasebutrecentevidence suggestsitiscausedbyaviroid.Xyloporosisis commoninold-linetreesandisacontinuingproblem wheregrowershavetopworkedold-linetreeswith cultivarssuchasmandarinhybridsthataresensitive toxyloporosis.Xyloporosis-freebudwoodfornearly allcultivarsisavailable,butinanattempttocutcosts, growerssometimespaydearlyforusingunregistered budwood.SymptomsXyloporosiswasoriginallydescribedinsweetlime andcachexiawasdescribedinOrlandotangelo,but thediseasesareapparentlyidentical.Foveaisa similardiseaseinMurcotts.Xyloporosiscancause stunting,chloroticfoliageanddeclinesymptomsthat canbesimilartothosecausedbyotheragents.The definitivesymptomsofxyloporosisarestempitting andgumimpregnationofthebarkinsensitive cultivars.Pittingandgumdevelopmentusuallybegin nearthebudunion,butmayspreadtothe xyloporosis-sensitiveportionofthetree.Thepitsand correspondingpegsarenotasangularasthosefound intristeza-affectedtreesandmayresultinagenerally bumpysurfaceonbothwoodandbarkfaces.Pegson thebarkfaceusuallycontaingum.Oncethese symptomsbecomewelldeveloped,aflatcutabout halfwayintothebarkwillrevealgumpocketsof varyingsize.Symptomsusuallytake18-48monthsto developinhighlysusceptiblecultivarssuchasOrlando tangeloandCitrusmacrophyllaandlongerinless sensitivecultivars.Satsumasmaynotshowsymptoms for8yearsormore.Indexingisusuallydoneby inoculatinganindicatorsidegraftofParson'sSpecial mandarinonavigorousrootstocksuchasrough lemon,orbygraftingthetestplantonOrlando tangeloorEllendalemandarinseedlings.PlantsAffectedXyloporosiscanaffectmosttangelos,some mandarins,manymandarinhybrids,sweetlimeand Citrusmacrophylla.Roughlemonmayalsoshowmild symptoms.Itisespeciallysevereon Citrusmacrophylla andOrlandotangelo.Oranges,grapefruit,lemons, acidlimes,somemandarins,trifoliateorangeandits hybridsareamongthosehostswhichcanbeinfected, butusuallydon'tshowobvioussymptoms(seeTable 4).TransmissionLikeexocortis,xyloporosiscanbetransmittedby infectedbudwoodandcontaminatedcuttingtools.A surplusofwhitegrapefruithasledsomegrowersto topworkold-linetreeswithothercultivarsthatarein greaterdemand.Topworkinginvolvesgraftingor buddinganewscioncultivarontoanexisting rootstock-scioncombination.Thenewscionmaterial issetinthemainscaffoldbranchesafterthetreehas beenprunedseverelyorissetdirectlyinthetrunk followingremovaloftheentiretopofthetree.When mandarinhybridsarepropagatedthisway,theycan becomeinfectedbythexyloporosispathogenthatwas presentbutnotexpressedinthewhitegrapefruit scion.Conversely,ifOrlandotangelosaretopworked, theymayalsobecomeinfectedunlessvirus-free budwoodisusedfortopworking.ControlControlofxyloporosiscanbeachievedbyusing registeredbudwoodandbydecontaminationof cuttingtools.Twodisinfectantsthathavebeenfound effectiveareanaqueoussolutioncontaining2% sodiumhydroxideplus2%formalinorafreshlymade 5-10%solutionofhouseholdbleach.Top-working sensitivecultivarsshouldbeavoidedwhenxyloporosis couldbepresentintherootstockorscion.

PAGE 10

CitrusVirusesandVirus-LikeDiseases Page10 Table4. SusceptibilitytoXyloporosis. Rootstock Susceptibility CarrizoCitrange notsusceptible Citrusmacropyylla verysusceptible Citrusvolkameriana notsusceptible CleopatraMandarin notsusceptible Milam notsusceptible RangpurLime susceptible RoughLemon susceptible SourOrange notsusceptible SweetOrange notsusceptible SwingleCitrumelo notsusceptible TrifoliateOrange notsusceptibleMINORVIRUSDISEASESThecurrentabsenceofextensivenaturalspread andtheuseofdiseasefreeregisterednurserystock currentlyseemseffectiveincontainingthefollowing diseases.Severalofthesediseasescouldbeextremely damagingiftheybecomewidespread.Growersshould beawareofthesediseasesandtheirdestructive potential.CitrusVariegationVirusCitrusvariegationvirus(CVV)hasbeenfoundin allmajorcitrusproducingregions,includingFlorida. Onceconsideredaformofpsorosis,CVVandthe closelyrelatedcrinklyleafvirusarenowknowntobe distinctpathogens.CVVcanbereadilytransmitted mechanicallytonon-citrushosts. SeveraldifferentisolatesofCVVhavebeenfound indifferentlocationsinFlorida.CVVcanproduce variegatedleafsymptomsincitrons,lemonsand grapefruit,andmildersymptomsinmanyotherhosts, includingsweetorange.Strikingleafandfruit symptomsoftenappearingrapefruitafterasevere winter,butthetreesmaysubsequentlygrownormally withfewvisiblesymptoms. Normally,CVVcanbedetectedinEtrogcitron indicatorplantswhileindexingforexocortis,buta recentlydiscoveredmildisolateproducedveryweak symptomsinthisindicatorplant.Fortunately,good serologicaltechniquesareavailableandtheEnzyme LinkedImmunoSorbantAssayprocedurecanbeused forrapiddetectionofCVV.Useofregistered budwoodshouldpreventproblemswithCVVinnew plantings.CitrusLeafRugoseVirusCitrusleafrugosevirus(CLRV)isrelatedto citrusvariegationvirus.CLRVwasdiscoveredby chanceinanoldvarietyplantingnearEustis,Florida andisthoughttobespreadnaturally,possibly throughpollen.Subsequentindexingshowedittobe presentinanumberofcultivars,includingearly introductionsfromCaliforniaandseveralseedlings trees.Serologicaltechniquesarenowavailableforthe detectionofCLRV. CLRVcausesminorleaffleckinginlemons,some puckeringinleavesofMexicanlimeandasevere stuntinginyounggrapefruitseedlings.Itinfectsa largenumberofothercultivarswithoutproducing obvioussymptoms.Thisdiseaseisnotyetwidespread andhasnotbeenfoundinregisteredbudwood sources.Aswithcitrusvariegationvirus,thebest controlstrategyforCLRVistoavoidthediseaseby usingonlyregisteredbudwoodsources.CitrusRingspotVirusThespreadofcitrusringspotvirus(CRSV) presentsaclassicillustrationoftheimportationand spreadofavirusdiseaseoninfectednurserystock. CRSVwasfirstisolatedinFloridafromayoungStar Rubygrapefruittreethathadbeensmuggledfrom TexasintoFlorida.Budwoodcutfrominfectedtrees wasusedinacommercialnursery,furtherspreading thedisease. Althoughsomenaturalspreadofringspothas occurredinTexas,thereisnogoodevidenceof naturalspreadinFlorida.TheTexasstrainofCRSV andsubsequentlydiscoveredFloridastrainsproduce similarsymptomsbuttheviruseshavenotyetbeen fullycharacterized.Therelationshipofthenaturally spreadformofpsorosisinArgentinatoCRSVstrains inFloridaalsoneedsclarification.Thepersistent observationsofnaturalspreadofthisdiseaseare ominousbecauseCSRVstrainsappearcapableof causingseveredamagetomaturetrees.Atpresent, thebestcontrolpolicyistouseregisteredbudwood andtobevigilantagainstnaturalspreadofthe disease.

PAGE 11

CitrusVirusesandVirus-LikeDiseases Page11StrainsofpsorosisBcommonlyproduce symptomssimilartothoseproducedbyCRSV.These psorosisstrainsaremechanicallytransmissibleto herbaceousindicatorplants,producingleaflesionsin theseherbaceousplantsandtypicalleafringspot symptomsingrapefruitseedlings.Numeroussources ofthepsorosisBstrainhavebeenfoundinoldtrees inFloridathatexhibitbark-scalingsymptoms.Tatterleaf-CitrangeStuntVirusInJapanandtheUnitedStates,tatterleaf-citrange stuntvirus(TL-CSV)hasbeenrecoveredfromcitrus originallyimportedfromChina.Althoughitisof limiteddistributionandnaturalspreadhasnotbeen reportedintheUSorJapan,itisofinterestbecause ofthedevastatingscion-rootstockincompatibilityit causesininoculatedmandarinandsweetorangetrees ontrifoliateorangeorcitrangerootstocks.Thevirus iswidespreadinMeyerlemontreesinFlorida.Meyer lemonaswellasorange,mandarinandgrapefruitcan besymptomlesscarriers.Theviruscanbedetectedby graftinoculationtoRuskcitrangeorCitrusexcelsa plants,orbymechanicalinoculationtobeans. Thebestcontrolstrategyistoreducethenumber ofTL-CSVinfectedtrees.AllnewplantingsofMeyer lemonshouldbefromvirus-freesources.Other cultivarsshouldneverbegraftedonold-lineMeyer lemonoronMeyerlemongraftedtoothercultivars.AlgerianNavelOrangeVirusThisviruswasdiscoveredinanavelorange cultivarimportedmanyyearsagofromAlgeriawhen thatcultivarwasscreenedforvirusdiseasesusing herbaceousindicatorplants.Thisvirusproduces symptomsinseveralherbaceousindicatorplantsbut ithasnotyetproducedsymptomsinanyofthe seedlingcitruscultivarstestedthusfar.Hostrange testsongraftedtreeshaveyettobedone. Atthispointthereisnoindicationofadisease problemassociatedwiththisvirusbutitspresence indicatesthatallthevirusesaffectingcitrushavenot yetbeendiscovered.Someofthesevirusesmaynot becomeapparentuntilasensitivehostisinfected.

PAGE 12

CitrusVirusesandVirus-LikeDiseases Page12MilamStemPittingInthemid-1970's,aseverestempittingcondition wasobservedinsomeMilamlemonseed-sourcetrees. Definitebutlessseverepittingwasalsoobservedin severalmandarinhybrids,includingRobinson,Lee andPage.Thesymptomswereverysimilartothose causedbytristeza,buttristezawasnotfoundinallof thepittedtrees.Milamtreeswithstem-pittingwere topworkedtodifferentcultivarstodetermineifit wouldseverelyaffectothercultivars.Nostriking symptomsoccurredinanyoftheeightcultivars tested,includingValenciaorangeandMarsh grapefruit.Transmissiontestshavebeeninconclusive. Pittinghasnotbeenproducedonsmall,container grownplantsintheglasshouseorscreenhouse.Pitting isgenerallyconfinedtothetrunkandmajorscaffold limbsonaffectedtreesinthefieldanddoesnot extendbelowgroundonMilamseedlings.Thispitting doesnotappeartoaffecttreevigorandhasnotyet becomeaproblem.Growers,however,shouldbe awareofthissituationandpropagateMilam,Page, LeeandRobinsonfromsourcesfreeofobvious stem-pitting.