Table Of Content

PATHOGEN-INDUCEDPLANTCHEMICALDEFENSE:EFFECTONINSECT HERBIVORESANDPARASITOIDS By YASMINJUDITHCARDOZA ADISSERTATIONPRESENTEDTOTHEGRADUATESCHOOL OFTHEUNIVERSITYOFFLORIDAINPARTIALFULFILLMENT OFTHEREQUIREMENTSFORTHEDEGREEOF DOCTOROFPHILOSOPHY • UNIVERSITYOFFLORIDA -''.' 2002 IdedicatethisworktoAlonsb,myhusbandandbestfriend.Ithankhimforbeing mypillarofstrengthandmyendlesssourceofinspiration.Iwouldnothavemadeitthis farwithoutallhisloveandsupport. ACKNOWLEDGMENTS IthankJimTumlinsonforgivingmethefinancialandintellectualfreedomthat madethisworkpossible. IalsowanttothankJimforalwaysbeingtheretoremindme abouttheimportanceofstayingfocused,andforbelievingthereisnosuch thingasan impossibletask,whichmotivatedmetoalwaysreachhigher. Iextendaheartfeltthanks I toHeatherMcAuslane,JoeLewis,JimNation,andRaghavanCharudattanforservingas membersofmysupervisorycommittee. IalsothankJeffreyJonesandTomKucharekfor theirwillingnesstosharetheirpathogenstocksandknowledgewithme.Iamgratefulto HeatherMcAuslane,HansAlbom,NancyEpsky,BarbaraDueben,JuanHuang,Peggy Zelonka,PeggyBrennanandJuliaMeredithforalltheyearsoffriendshipandforallthe specialmomentsthatmadethisamemorablejourney.IalsoextendmygratitudetoPaul Pare,NaokiMori,ConsueloDeMoraes,PeterTeal,DerrickBennett,BaldwynTorto, CameronLait,AmyHowe,JiirgenEngelberth,EricSchmelzandMatthewSammonsfor alltheexperiencesandknowledgeshared. iii TABLEOFCONTENTS Page ACKNOWLEDGMENTS iii ABSTRACT vii CHAPTER , 1 LTTERATUREREVIEWandRESEARCHGOALS 1 Introduction 1 PlantChemicalDefensesagainstInsectsandPathogens 2 PlantVolatileProductionInResponsetoInsectandPathogenAttack 3 BiochemicalPathwaysinPlantDefenseagainstInsectandPathogenPests 4 Insect-andPathogen-DerivedElicitorsofPlantDefenseResponses 8 InteractionsbetweenPhytopathogensandHerbivorousInsects 10 EffectofInducedPlantVolatilesonPathogens,InsectHerbivoresandParasitoids 12 ResearchGoals 14 2 INVIVOVOLATILEEMISSIONSFROMPEANUTPLANTSINDUCEDBY SIMULTANEOUSFUNGALINFECTIONANDINSECTDAMAGE 16 Introduction 16 MaterialsandMethods 17 PlantandInsectMaterial 17 FungalCulture 18 BeetArmywormFeedingonSclerotiumrolfsii-lnfectedPeanuts 19 CollectionofVolatileCompoundsfromFungus-andBeetArmyworm- DamagedPlants 20 CollectionofVolatileCompoundsfromFungalCultures 21 SampleExtractionandAnalysis 21 EffectofSelectedVolatileCompoundsfromS.rolfsii-lnfectedPeanuton RadialGrowthofFungalCultures 22 StatisticalAnalyses 23 Results 23 BeetArmywormFeedingonS.rolfsii-lnfectedPeanuts 23 CollectionofVolatileCompoundsfromFungus-andBAW-DamagedPlants 24 iv CollectionofVolatileCompoundsfromFungalCultures 25 EffectofSelectedVolatileCompoundsfromS.rolfsii-InfectedPeanuton RadialGrowth ofFungalCultures 25 Discussion 26 3 FUNGUS-INDUCEDBIOCHEMICALCHANGESINPEANUTPLANTSAND THEIREFFECTONDEVELOPMENTOFBEETARMYWORM, SPODOPTERAEXIGUAHUBNER(LEPIDOPTERA:NOCTUIDAE)LARVAB5 Introduction 35 MaterialsandMethods 37 PlantandInsectMaterial 37 FungalCulture 38 SclerotiumrolfsiiInfectiononPeanuts 38 BAWPerformanceonHealthyandFungus-InfectedPeanut 38 PlantSamples 39 CarbohydrateAnalysis 39 ProteinAnalysis 40 ProteinaseInhibitorAnalysis 41 SolublePhenolicAnalysis 41 JasmonicAcidandSalicylicAcidAnalysis 41 StatisticalAnalyses 43 Results 43 BeetArmywormPerformanceonHealthyandFungus-InfectedPeanut...43 PlantNutritionalAnalysis 44 JasmonicAcidandSalicylicAcidAnalysis 44 Discussion 44 4 EFFECTOFPEANUTPLANTFUNGALINFECTIONONOVIPOSITION PREFERENCEBYSPODOPTERAEXIGUAANDONHOSTSEARCHING BEHAVIORBYCOTESIAMARGINIVENTRIS 51 Introduction 51 MaterialsandMethods 53 PlantandInsectMaterial 53 FungalCulture 54 SclerotiumrolfsiiInfectiononPeanuts 54 BeetArmywormOviposition 55 ResponseofCotesiamarginiventristoHealthyandS.roZ/f/j-Damaged Plants 55 StatisticalAnalyses 58 Results 58 Discussion 59 5 INDUCTIONOFVOLATILECOMPOUNDSANDSIGNALINGHORMONESBY BACTERIALINFECTIONANDINSECTHERBIVOREDAMAGEONPEPPER PLANTS 65 Introduction 65 MaterialsandMethods 67 PlantandInsectMaterial 67 PathogenCultureandPlantInoculation 67 CollectionofVolatileCompoundsfromXanthomonas-andBeet Armyworm-DamagedPeppers 68 ExtractionandAnalysisofVolatileSamples 69 LevelsofJasmonicAcidandSalicylicAcidinPlants 70 StatisticalAnalyses 72 Results 72 Discussion 75 6 SUMMARYANDCONCLUSIONS 83 LISTOFREFERENCES 89 BIOGRAPHICALSKETCH 103 vi AbstractofThesisPresentedtotheGraduateSchool oftheUniversityofFloridainPartialFulfdlmentofthe RequirementsfortheDegreeofDoctorofPhilosophy PATHOGEN-INDUCEDPLANTCHEMICALDEFENSE:EFFECTONINSECT HERBIVORESANDPARASITOIDS By YasminJudithCardoza August2002 Chairperson:JamesH.TumlinsonHI MajorDepartment:EntomologyandNematology Thestudypresentedhereisthefirstinwhichtheproductionofvolatile compoundsbyasinglehost-plantsysteminresponsetobothinsectherbivoresand pathogenshasbeenevaluatedsimultaneously. Additionally,itisthefirststudyonthe effectofpreviouspathogeninfectionontheproductionofplantvolatilesinresponseto insectdamage. Thestudyofplantvolatiledefensesmayimproveourunderstandingof plantresistancemechanismstodiseaseandinsectherbivores. Theidentificationof specificpathogen-andherbivore-inducedplantvolatileswillgreatlycontributetothe development,improvementandimplementationofhost-plantresistanceandothercontrol methodsforinsectandpathogenpests. Inmypeanut-whitemold-beetarmyworm system,beetarmyworm(BAW) feedingandovipositionpreferenceandlarvalperformancewereallenhancedbythe fungal-infectiononpeanutplants. Thismayindicateaninterferenceofthefungal i vii infectionwiththeplant'sdirectchemicaldefensesagainsttheherbivores. Peanutplants releaseaspecificsetofvolatilechemicalinresponsetowhitemoldinfection. This volatileprofilediffersqualitativelyandquantitativelyfromsignalsemittedinresponseto BAWdamage. Previousinfectionontheplantbythewhitemoldfungusdoesnot interferewiththeemissionofvolatilesbytheinfectedplantinresponsetoBAWattack. Thewhitemold-derivedcompound3-octanoneandtheplant-producedvolatilemethyl salicylatewereonlyrecoveredfromplantsinfectedwithS.rolfsii. Thus,thepresenceof thesecompoundscouldpotentiallybeusedinthefutureforthedetectionofwhitemold- infectedplantsinthefield. AlthoughBAWpreferenceandperformancewereenhanced bywhitemoldinfectiononpeanutplants,itdoesnotappearthatpreviousinfectionofthe planthasanynegativeeffectonthehostsearchingabilityofitsparasitoid,Cotesia marginiventris. Parasitoidswereactuallyobservedlandingmorefrequentlyon,andwere significantlymoreresponsivetovolatilesfrominfected,ratherthanhealthypeanutplants. Thismaybearesponsetohigheramountsofvolatilesbeingreleasedbyinfectedplants eithercausedbytheplant'sincreasedsensitivitytoBAWfeedingduetothefungal infectionortoincreasedfeedingbytheBAWonleavesfrominfectedplants. Finally, Ifoundthatpepperplantsundersimultaneousattackbyleafspotbacteria, Xanthomonascampestrispv.vesicatoria(pepperrace3)(XCVP3)andBAWwereable toproduceavolatileprofilequalitativelysimilarto,butquantitativelygreaterthan,that producedbyplantsunderinsectdamagealoneduringthe4daysafterbacterial inoculation. However,after4daysfrombacterialinoculation,theamountofvolatiles emittedbyXCVP3-infectedplantsinresponsetoBAWinfestationwassignificantly lowerthanthatproducedbyhealthyplantsinresponsetoBAWdamage. Analysesofthe viii levelsofsignalinghormonesjasmonicacid(JA)andsalicylicacid(SA)intheseplants revealedthatthereductioninvolatileproductioninresponsetoinsectdamagewas precededbyasignificantincreaseinconjugatedSA,andconsequentreleaseofmethyl salicylatebyplantsunderthecombinedbacterial/insectattack. Also,thecumulativeJA increaseinXCVP3/BAWplantswassignificantlyhigherthanthatofcontrolplants,but didnotdiffersignificantlyfromthoseofplantsdamagedbyeitherorganismalone. Overall,thedatapresentedhereinsupporttheideaofanorchestratedinteractionbetween thelevelsofJAandSAtoregulatetheinductionandemissionofvolatileorganic compoundsbypepperplantsunderbacterialandinsectherbivoreattack. ix CHAPTER1 LITERATUREREVffiW Introduction Herbivorousinsectsandplantdiseasesareseriousthreatsfortheagricultural environmentbecausetheyreduceyieldandqualityofcrops. Inparticular,plantdiseases (causedbyinfectiousviruses,bacteria,phytoplasmas,fungi,andnematodes)cause seriouslossesinagriculturalcommodities. Theseproblemsincludereducedyields,lower productshelf-life,anddecreasedaestheticandnutritionalvalue. Inadditiontothedirect damagetotheplant,somepathogenstrainsandinsectspeciesalsoresultinthe ^ productionandaccumulationofsecondarymetabolitesandtoxinsthatcancausehealth problemsinhumansandanimals. Controlofplantdiseasesandpestsisvitalfor providinganadequatesupplyoffood,feed,andfibertocopewiththeincreasinghuman populationanditsdemands. InFloridaalone,morethanadozenplantdiseaseepidemics occurredfrom1970-1990(Kucharek1990). Growerscurrentlyspendlargesumsof moneytocontrolpathogensandinsectsthatattacktheircrops. Nevertheless,cropand commoditylossesbecauseofdiseasesandherbivoredamagecostbillionsofdollarseach year. IntheUnitedStates,itisestimatedthattheyearlyeconomiclossesare approximately9.1billiondollarsforplantdiseases,andapproximately7.7billiondollars forinsectdamage,allthisaftertheapplicationofcontrolmeasurespracticedunder modemagriculture(Agrios1997). Thus,informationabouthowinsectandpathogen 1

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