土传病原体特异性-原生区vs非原生区的对比研究

生态学/植物病理土传病原体特异性：原生区vs非原生区的对比研究（生物入侵/植物生态）作者：K.O.Reinhart、W.H.vanderPutten、T.O.G.Tytgat、K.Clay许可：CCBY4.0(CreativeCommonsAttribution)【内容简介】研究植物原生区与非原生区土传病原体的感染特异性差异，发表于Hindawi《国际生态学杂志》，CC-BY开放获取。（学术资料，仅供参考）【关键词】土传病原体、植物生态学、原生分布区、非原生分布区、病原体特异性、生物入侵【分类】科技>医药卫生>生物学——————————————————————————————Variationinspecificityofsoil-bornepathogensfromaplant'snativerangeversusitsnonnativerangeReinhart,K.O.;Putten,W.H.vander;Tytgat,T.O.G.;Clay,K.2011,Article/Lettertoeditor(InternationalJournalofEcology,(2011))Doilinktopublisher:/10.1155/2011/737298Versionofthefollowingfulltext:Publisher’sversionDownloadedfrom:/2066/93607Downloaddate:2026-03-16Note:Tocitethispublicationpleaseusethefinalpublishedversion(ifapplicable).HindawiPublishingCorporationInternationalJournalofEcologyVolume2011,ArticleID737298,6pagesdoi:10.1155/2011/737298ResearchArticleVariationinSpecificityofSoil-BornePathogensfromaPlant’sNativeRangeversusItsNonnativeRangeKurtO.Reinhart,1WimH.VanderPutten,2,3TomTytgat,4andKeithClay51UnitedStatesDepartmentofAgriculture-AgriculturalResearchService,FortKeoghLivestock&RangeResearchLaboratory,243FortKeoghRoad,MilesCity,MT,59301-4016,USA2NetherlandsInstituteofEcology,CentreforTerrestrialEcology,DepartmentofMultitrophicInteractions,Boterhoeksestraat48,6666GAHeteren,TheNetherlands3LaboratoryofNematology,WageningenUniversity,Binnenhaven5,6709PDWageningen,TheNetherlands4DepartmentofEcogenomics,InstituteforWaterandWetlandResearchRadboud,UniversityNijmegenHuygens,buildingHeyendaalseweg135,6525AJNijmegen,TheNetherlands5DepartmentofBiology,IndianaUniversity,Bloomington,IN,47405-3700,USACorrespondenceshouldbeaddressedtoKurtO.Reinhart,kurt.reinhart@Received1November2010;Accepted1February2011AcademicEditor:BradfordHawkinsCopyright©2011KurtO.Reinhartetal.ThisisanopenaccessarticledistributedundertheCreativeCommonsAttributionLicense,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperlycited.Existingtheoryforinvasivenonnativespeciesemphasizestheroleofescapingspecialistenemies.Ausefulapproachistoreciprocallytransplantenemiesinacontrolledandcommonexperimenttoquantifytheinteractionspecificityofenemiesfromplant’snativeandnonnativeranges.Quantitativemeasuresofinteractionspecificity,fromtwoexperimentswiththreehostgenotypes(Belgium,Louisiana,andPennsylvania)and37Pythiumisolates(10Europeand27USA),revealedthatPythiumpathogensfrompopulationsofPrunusserotinainitsnativerangewerenothostgenotypespecificwhilePythiumpathogensfromitsnonnativerangevarywithhostgenotype.ThisstudyprovidesempiricalevidencesuggestingthatPythiumfromthenonnativerangeareeitherpreadaptedtoorareactivelyadaptingtothishost.Althoughonlyforasinglepathosystem,thisstudyillustratestheimportanceofunderstandingenemyimpactandhost-specificitytoassesswhetheraninvaderhasescapeditsnaturalenemies.1.IntroductionPathogensdrivebothgenetic(e.g.,[1])andspeciesdiversity(e.g.,[2])byasharedmechanism—negativefrequency-dependentdiseasedynamicswhichcausesmorenegativeeffectsonthefitnessofcommonspeciesandgenotypesthanrareforms(reviewedin[1]).Naturalenemiesalsoaffectbiologicalinvasions.TheprominentEnemyReleaseHypothesis(ERH)hasthreecentralunderpinningsrelatedtospecializationbyenemies[3]:“(1)thespecialistenemiesofthestudyspecies(initsnativerange)willbeabsentfromthenew[invaded]region;(2)hostswitchingbyspecialistenemiesofnativecongenerswillberare;and(3)generalistswillhaveagreaterimpactonthenativecompetitors.”Todate,moststudiesrelatedtoERHhavefocusedonspecies-levelspecializationbyenemies(e.g.,[4]),buttheneedexiststobetterunderstandformsofgenotypicspecialization(e.g.,[5–7]).Biologicalcontrolpractitionershavelongacknowledgedtheimportanceofgenotypicformsofspecializationandtheneedforcontrolagentstoaffectallweedgenotypes(e.g.,[8]).Furthermore,apositivecorrelationhasbeendetectedbetweenthenumberofassociatedpathogensandtheout-crossingrateofthehost[9].Theseexamplesofgenotypespecificityhelptoexplainwhyoutcrossingweedsarehardertocontrolwithinsectbiocontrolsthanselfingplants[10].Thoughvariationinpathogenimpactsislikelyanimportantfactorexplainingbiologicalinvasions[11],littleisactuallyknownaboutthevariationinplant-pathogeninteractionsandtheirspecializationatabiogeographicscale2InternationalJournalofEcology(nativeversusnonnativeranges).Onerecentstudyrevealedthatsomeenemiesarebroadlydistributedmakingacom-pleteescapeunlikelybutavoidanceofvirulenttaxaappearedimportant[12].Thisstudywasnovelbecauseitperformedareciprocaltransplantexperimentofpathogens(Pythiumspp.)fromplant’s(Prunusserotina)nativeversusnonnativerangesinapathogenicityexperimentconductedinacon-trolledenvironment.Thedatacanbefurtherusedtotestforgeneticeffectsofthehostondiseaseexpressionbythedifferentpoolsofpathogensfromthenativeversusnonnativerangesbecausethestudycontrolledgenetic×environmentinteractionswhichisuncommonrelativetootherrelatedbiogeographicstudies.Theprimarythemeoftheoriginalpaperwasonbiogeographicvariationinpathogenvirulenceindependentofhostgenotype[12].HerewereanalyzethedatatohelpidentifywhetherquantitativemeasuresofenemyimpactcausedbypoolsofPythiumfromeitherthenativeornonnativerangesvarieddependingonhostgenotype.Unlikepatternsofassociationalspecificitybetweenhostandpathogenthatdonotexplicitlycharacterizeenemyimpactanddonotcontrolforenvironmentaleffects,thisstudydescribesinteractionspecificitywhichreferstohowmeasuresofenemyimpactvarybyhostgenotypewhileenvi-ronmentalfactorsareheldconstant.Relativetotheoriginalstudy,wetestnewhypothesesontheinteractionspecificityofPythiumisolatesassociatedwithPrunusinitsnativeandnonnativerangestodetermine(1)ifhostgenotypeaffectsdiseaseexpressionand(2)iftheresponsivenesstohostgenotype(i.e.,interactionspecificity)isgreaterforPythiumfromthehost’snativethannonnativeranges,anextensionofERH.2.MaterialsandMethodsHerewereanalyzedatafromapreviousstudy[12].Theyper-formedtwopathogenicityexperimentsusingPythiumiso-lates,acommonsoil-bornepathogen,associatedwithPrunusserotinainitsnativeandnonnativeranges.Bothexperimentswereconductedinthesamelaboratoryundersimilarcontrolledconditions,utilizedidenticalgrowthfacilities,andsimilarexperimentaldesigns.Althougheachexperimentusedonlytwohostgenotypes,theexperimentsincludedhostgenotypesfromthenonnative(Belgium)andnativeranges(LouisianaandPennsylvania).Incorporatingmoregenotypeswouldbeidealbutthestudyprovidesamini-mumnumberofgenotypestoidentifywhetherinteractionspecificitybypoolsofPythiumisolatesvariesinresponsetohostgenotype.SincethePythiumisolatesarefromwidelydistributedP.serotinapopulationsinthenativeandnonnativeranges,thestudydoesnotattempttospecificallycomparelocalpathogenswithlocalhostgenotypes.Thefocusofthestudyisinsteadongeneralcomparisonsofthepoolsofpathogenswheninteractingwithdivergenthostgenotypes.2.1.PathogenicityExperiment1.Experiment1wascon-ductedintwopartstestingtheeffectofPythiumoriginonperformanceofP.serotinaseedlings.Thefirstpartused100806040200Seedlingsurvival(%)(Louisianaseed)020406080100Seedlingsurvival(%)(Belgiumseed)(a)100806040200Rootrot(%)(Louisianaseed)020406080100Rootrot(%)(Belgiumseed)(b)Figure1:PositivecorrelationofPrunusserotinaseedoriginatingfromitsnative(x-axis,Louisiana,USA)andnonnativeranges(y-axis,Belgium)for%seedlingmortalityand%rootrotresults.Apositivecorrelationsuggeststhatthepathogenicactivityoftheisolatesdoesnotdependonhostgenotype.Eachsymbolrepresentstheaverageresponseofexperimentalunits(n=3vesselsperisolate)toagivenisolatewhileinteractingwithseedlingsfromeitherthenativerange(x-axis)ornonnativerange(y-axis).Somedatapointsoverlap(n=10).AllisolateswerefromthenativerangeandrepresentadifferentpoolofisolatesthanshowninFigure2.seedoriginatingfromthenativerange(Louisiana,USA)andsecondpartusedseedfromthenonnativerange(Belgium).Thetwopartsdifferedintheirtimingandthevesselsizes.ThefirstpartusedseedfromLouisiana,USA,andwasstartedonMay5,2006,andthesecondpartusedseedfromBelgiumandwasstartedonJune23,2006.ThepartusingseedfromLouisianawasalsoconductedinsmallerexperimentalvessels(65versus100mmdiametervessels).Experiment1usedPythiumfromthenativeandnonna-tiveranges(n=10isolatesfromthenativerangeandn=3isolatesfromthenonnativerange)butonlydataforthelargerpoolofPythiumfromthenativerangeareusedhere.ThepathogenicityexperimentusedindividualisolatestoInternationalJournalofEcology3100806040200Seedlingsurvival(%)(Pennsylvaniaseed)020406080100Seedlingsurvival(%)(Louisianaseed)(a)100806040200Rootrot(%)(Pennsylvaniaseed)020406080100Rootrot(%)(Louisianaseed)(b)0.060.050.040.030.020.010Stembiomass(g)(Pennsylvaniaseed)00.010.020.030.040.050.06Stembiomass(g)(Louisianaseed)OriginofPythiumisolatesNativerange(USA)Non-nativerange(Europe)(c)Figure2:EffectofisolatesofPythiumspp.,associatedwithPrunusserotinatreesintheirnative(∇:17isolatesfromUSA)andnonnativeranges(•:10isolatesfromwesternEurope),onthesurvival,rootrot,andstembiomassofP.serotinaseedlingsfromtwoportionsofitsnativerange,LouisianaandPennsylvania,USA.EachsymbolrepresentstheaverageresponseofexperimentalunitstoagivenisolatewhileinteractingwithseedlingsfromeitherPennsylvaniaseed(n=2vesselsperisolate)orLouisianaseed(n=3vesselsperisolate).Bestfitregressionlinesareshownandthehatchedlinescorrespondwithdataforisolatesfromthenativerange.Eachexperimentalvesselcontainedonlyoneisolateandseedlingsfromonlyasingleseedsource.Somedatapointsoverlap.inoculateindependentvesselscontainingsevenseedlingsofPrunusserotinaderivedfromeachseedsource.Experimentalunitswerereplicatedthreetimesperisolateandseedcombination.Seedlingsurvivalandrootrotwerequantifiedforseedlingsatca.25days.Forourreanalysis,weassumethatthetwopartsofexperiment1arefunctionallyequivalentandthatvirulencetrendswillnotbeaffectedbythesubtlevariationsbetweenparts(i.e.,starttimeandvesselsize)sinceotherfactorswerecontrolled.2.2.PathogenicityExperiment2.Similartoexperiment1,thevirulenceof17Pythiumisolatesfrom13populationsinthe4InternationalJournalofEcologynativerangeand10isolatesfromsixpopulationsintheinvadedEuropeanrangewascomparedusingacontrolledpathogenicityexperimentconductedinthelaboratory[12].Experiment2testedtheeffectofPythiumisolatesfromdifferentoriginsonPrunusserotinaderivedfromseedorigi-natingfromtworegionsinthenativerange(Louisiana(n=3replicatevesselsperisolate)versusPennsylvania(n=2replicatevesselsperisolate)).PhylogeneticresearchhasrevealedthatpopulationsinthenonnativerangewerelikelyestablishedfromplantmaterialfromPennsylvania,thecenterofP.serotinageneticdiversity[13].Unlikeexperiment1,experiment2wasnotbrokenintopartsandwasinsteadperformedasonelargeexperiment.Inaddition,experiment2utilizedonlythreeseedlingspervessel.Seedlingsurvival,rootrot,andstembiomasswerequantifiedforseedlingsat25days.Furtherdetailsoftheexperimentaldesignareprovidedintheoriginalstudy[12].2.3.Analyses.Multiplecorrelationsfordifferentresponsevariables(i.e.,seedlingsurvival,rootrot,andstembiomass)weremadebetweenexperimentalportionsassociatedwithdifferentseedgenotypesinteractingwithacommonpoolofPythiumisolates.Separatecomparisonsweremadeforexper-iments1and2.Usingdatafromexperiment1,weperformedmultiplecorrelationstodetermineifthepoolofisolatesinteractedsimilarly(positivecorrelation)ordifferentlywiththetwoseedsources(LouisianaandBelgium).Thiswasrepeatedfordatafromexperiment2usingseedfromtwosources(LouisianaandPennsylvania).Positivecorrelationsindicatethatthepathogenicactivityoftheisolatesdoesnotdependuponhostgenotype.NonpositivecorrelationssuggestthatpathogenicactivityoftheisolatesdependsonhostgenotypeandthatdiseasesymptomsassociatedwithapoolofPythiumarehost-genotypespecific.Forexperiment2,weassessedwhetherPythiumfromnativeversusnonnativerangesdifferedintheirspecificityforspecifichost-genotypesbycomparingtheresponsevariablesforseedlingsfromPennsylvaniaandLouisianawithpoolsofPythiumisolatesfromeitherthenativeornonnativeranges.ThiswasaccomplishedbycomparingtheslopesoftheregressionsforisolatesfromthenativeversusnonnativerangesusingmultipleANCOVAanalyzesinProcGLMinSASversion9.13(SASInstituteInc.,CaryNC,USA).Theresponsevariableforoneofthegenotypeswasincludedasthecovariate.Asignificantinteractionbetweenthetreatmentandcovariaterevealedthattheslopesdifferedbetweenisolatepools.Measuresofpathogenicactivityforthetwopoolsofisolatesoverlappedbuttheirrangelimitsdidnotmirroroneanother.Thisisnotidealforacomparisonofslopes.However,theanalyseswerestillperformedsinceportionsofthetwodatarangesineachcomparisonoverlappedandthisvariationinrangesistheresultofmeaningfulecologicaldifferencesthatcannotbecontrolled.3.Results3.1.SpecificityofPythiumfromtheNativeRange.InExperi-ment1,thepathogenicactivityofindividualPythiumisolateswassimilarregardlessofwhethertheyinteractedwithseedfromthenativeversusnonnativeranges(experiment1;survival,r=0.86,androtroot,r=0.78,Figure1).Inportionofexperiment2,measuresofpathogenicactivitywerealsounresponsivetooriginofhostmaterial(LouisianaversusPennsylvania)(survival,r=0.87;rootrot,r=0.52;andstembiomass,r=0.73,Figure2).3.2.BiogeographicVariationinHostSpecificity.Contrarytothepositivecorrelationsdescribedabove,Pythiumfromthenonnativerange(experiment2)respondeddifferentlytodifferenthostgenotypes(survival,r=−0.45;rootrot,r=−0.17;andstembiomass,r=−0.04,Figure2).Moreover,asignificantdifferencebetweentheslopesofthesurvivaldataandbiomassdatawasdetected(Figure2,ANCOVA,P=.014andP=.015,resp.)betweenthePythiumisolatesfromthenativeversusnonnativeranges.Weobservedasimilaralbeitmarginallysignificantdifferencebetweentheslopesfortherootrotportionofthedata(P=.075).Overall,theseresultsindicatebiogeographicalvariationininteractionspecializationbypoolsofPythiumfromthenativeversusnonnativerangeofP.serotina.4.DiscussionTheEnemyReleaseHypothesis(ERH)hasemphasizedtheimportanceofescapinghost-specificenemies[3]andimplicitwiththisistheassumptionthathost-specificenemiesregulatetheabundanceofindividualsandescapingtheireffectspromotespopulationgrowthandinvasion.Thecontributionofpathogenswithgeneralisttendencies,likePythium[14],islesscleartoERH.HereweshowthatapoolofPythiumisolatesfromthenonnativerangeofaninvasivetree(P.serotina)isactuallymorehost-genotypespecificthantwopoolsfromitsnativerange.Specifically,poolsofPythium(n=10or17isolatesperexperiment)fromP.serotina’snativerangerespondedpredictablytovaryinghostgenotypes(LouisianaversusBelgiumandLouisianaversusPennsylvania,resp.)suggestingalackofinteractionspecificitybythepathogenstodifferenthostgenotypes.AsecondexperimentcomparedtheinteractionspecificityofapoolofPythiumfromthenative(n=17)versusnonnativeranges(n=10)andincludedhostmaterialfromtwogeographicallydistinctregionsinthehost’snativerange(LouisianaandPennsylvania).Althoughcomparisonswithmorehostgenotypesmightyielddifferentresults,thefindingsreportedhereareprovocativeandsuggestalackofinteractionspecificitybypoolsofPythiumisolatesfromthenativerangewhilethepoolofPythiumisolatesfromthenonnativerangeisconsiderablymorehost-genotypespecific.ThevariationininteractionspecificitybygroupsofrelatedpathogensfromnativeversusnonnativerangesreportedhereseeminglycontradictsamajorassumptionofERH—successfulinvadershavelefttheirvirulentspecialistenemiesbehind[3].TheinvadingP.serotinaappeartohaveescapedfromthemostvirulentPythiumtaxa[12];however,thepoolofPythiumfromitsnonnativerangehadpathogeniceffectsthatdependedmoreonhost-genotypethanthosefromitsInternationalJournalofEcology5nativerange.Thus,PythiumspeciesfromthenonnativerangeostensiblyhavegreaterinteractionspecificityandareeitherpreadaptedtoP.serotinaoradaptingtoP.serotina.Acriticalassumptionforhowpathogensmaintaingeneticandspeciesdiversityisthatdiseasedynamicsarehostfrequencydependentandcycleovertimeinresponsetohostfrequency[15].WepositthatP.serotinapopulationsinthenativerangeareinadifferentstageofthedynamicthanconspecificsininvadedEuropeanforests.Forexample,initsnativerange,P.serotinaisprimarilyasubordinatespeciesbutinitsnonnativerangeitislocallyabundantandcandominateEuropeanforests[12,16].Iftheenemiesarepoordispersers(i.e.,spatiallyvariable(e.g.,[17]))andthehostsarerare(and/orgeneticallydiverse),thenthepathogenmaybeforcedtopreyonmorethanonespecies/genotypetomaximizeitsfitness.Inordertoutilizemorethanonehost/genotype,thepathogenmustbelesshost-specificthantightlycoevolvedhost-pathogensystems.Incontrast,invadedEuropeanforestshavehigherfre-quenciesofP.serotina,basedondensityanddominancedata[12].Theorybasedonnegativefrequency-dependentdiseasedynamicspredictsthatenemieswillevolvespecificityforaprevalentnovelhostspecies[1,18,19].Also,invadersoftenexperiencefoundereffectsandhavelessgeneticdiversitythanintheirnativerange[20]increasingthelikelihoodforspecializationtodevelop.Aspredicted,invadingpopulationsofP.serotinahavelowergeneticdiversityandallelicrichnessrelativetopopulationsintheirnativerangecorrespondingwithlossesingeneticdiversityfromafoundereffect[13].Sinceexperiment2usedhostmaterialfromLouisianaandPennsylvania(estimatedtobethesourcematerialforthehostpopulationsinwesternEurope[13]),variationinpathogenicactivitybythepoolofPythiumfromwesternEuropeanmayhavebeenbecausethecomparisonincludedhostmaterialthattheregionalpoolwasgenerallyfamiliarversusothersources.ThisformofinteractionspecificitymaybethetracesignatureofthedevelopmentofamorespecializedpathosystembetweenPrunus-Pythiumthanistypicalinitsnativerange.Alternatively,theobservedhost-specificitymaybeanartifactofresidentPythiumfrominvadedforestsinwesternEuropebeingpreadaptedtoP.serotina.Evidenceisaccumulatingontheimportanceofgeneralistpathogens(e.g.,[14,21])andherbivores[22–24].Invasivesuccessmaydependmoreonescapingone’sgeneralistenemiesthaniscurrentlyacknowledgedbyERHpredictions.Exploringthedynamicsofhost/parasitecyclingmayhelptounderstandthedevelopmentofnascentpathosystemsandtheimpendingcollapseofinvasivepopulations[25].Weshouldconsiderutilizationofresidentenemiestomanagethemostproblematicinvasivespecies(e.g.,[7,26]).Anunder-standingofresidentenemiesisofpracticalsignificanceinevaluatingtheefficacyoftraditionalbiologicalcontrolsanddeterminingthepotentialofresidentenemiesasbiologicalcontrols(e.g.,[7]).Incorporatingresidentenemiesintoanintegratedpestmanagementplanforinvasiveplantsisapromisingformofbiocontrolthatcouldreducetheasso-ciatedcosts,improvesuccessofestablishmentbyutilizingenemiespreadaptedtotheenvironment,avoidtheassociatedconstraintsofconductingefficacytrialswithrestrictivequarantinerequirements,andreduceenvironmentalrisksofimporting“exotic”peststocontroltheinvader.However,invasivespeciesare“movingtargets”thatarelikelytoeventuallyacquirenaturalenemiesthatwillregulatetheirpopulations[27].AcknowledgmentsTheresearchofK.O.ReinhartwassupportedbyUSDA-NRI(2003-02047)andNationalParksEcologicalResearchFellowshipProgram,fundedthroughagrantfromtheAndrewW.MellonFoundationhelpingformapartnershipbetweentheNationalParkService,theEcologicalSocietyofAmerica,andtheNationalParkFoundation.TheauthorsappreciateMarkWestforassistancewithstatisticalanalysisandJenniferRudgersandJenniferKoslowforcommentsonanearlierdraftofthemanuscript.References[1]K.Clay,K.Reinhart,J.Rudgers,T.Tintjer,J.Koslow,andS.L.Flory,“Redqueencommunities,”inEcologyofInfectiousDiseases:InteractionsbetweenDiseasesandEcosystems,V.Eviner,F.Keesing,andR.Ostfeld,Eds.,pp.148–178,PrincetonUniversityPress,Princeton,NJ,USA,2008.[2]J.B.S.Haldane,“Diseaseandevolution,”CurrentScience,vol.63,no.9,pp.599–604,1992.[3]R.M.KeaneandM.J.Crawley,“Exoticplantinvasionsandtheenemyreleasehypothesis,”TrendsinEcologyandEvolution,vol.17,no.4,pp.164–170,2002.[4]L.M.Wolfe,“Whyalieninvaderssucceed:supportfortheescape-from-enemyhypothesis,”AmericanNaturalist,vol.160,no.6,pp.705–711,2002.[5]E.SiemannandW.E.Rogers,“Increasedcompetitiveabilityofaninvasivetreemaybelimitedbyaninvasivebeetle,”EcologicalApplications,vol.13,no.6,pp.1503–1507,2003.[6]D.Garcia-Rossi,N.Rank,andD.R.Strong,“Potentialforself-defeatingbiologicalcontrol?VariationinherbivorevulnerabilityamonginvasiveSpartinagenotypes,”EcologicalApplications,vol.13,no.6,pp.1640–1649,2003.[7]G.S.GilbertandI.M.Parker,“Rapidevolutioninaplant-pathogeninteractionandtheconsequencesforintroducedhostspecies,”EvolutionaryApplications,vol.3,no.2,pp.144–156,2010.[8]R.CharudattanandA.Dinoor,“Biologicalcontrolofweedsusingplantpathogens:accomplishmentsandlimitations,”CropProtec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