Oomycete–plant coevolution

内容需要下载文档才能查看 内容需要下载文档才能查看

Available online at http://wendang.chazidian.com

Oomycete–plantcoevolution:recentadvancesandfutureprospects

MarcoThines1,2andSophienKamoun1

Oomycetesareadiversegroupofeukaryoticorganismsthathavecolonisedmanyecologicalniches;yetmorethan60%oftheknownspeciesareparasiticonplants.ParasitismofplantshasevolvedseveraltimesindependentlyinthreedifferentlineagesoftheOomycota.Here,weprovideanoverviewofthecurrentknowledgeofthediversity,evolutionandlifestylesofplantparasiticoomycetes.Wethenreportonrecentadvancesinmolecularstudiesonoomycete–plantinteractionswithaparticularemphasisonworkwithoomyceteeffectors.Inthefuture,genomesequencingofabroaderspectrumofoomycetespecieswillexpandourknowledgeofpathogenicitymechanismsandwilllikelyrevealnovelstructuralandfunctionalclassesofeffectors.

Addresses1

TheSainsburyLaboratory,NorwichNR47UH,UnitedKingdom2

BiodiversityandClimateResearchCentre(BiK-F),Georg-Voigt-Str.14-16,D-60325Frankfurt,Germany

Correspondingauthors:Kamoun,Sophien(sophien.kamoun@tsl.ac.uk)

andbrownalgaeinthekingdomStraminipila[4,5].Someoomycetesareparasitesthatdevelopwithinasinglehostcell,forexampleadiatom,withtheentirecytoplasmeventuallyrecruitedtoreproduction(holocarpy)[6].Ot-heroomycetescanformdensematsoflong,branchedhyphae,likeinLeptomituslacteus,thesewageoomycete[7].SeveraloomycetegroupshaveevolvedintohighlyadaptedpathogensaffectingorganismsineukaryotickingdomsasdiverseasAlveolata,Animalia,Mycota,StraminipilaandPlantae.Themajorityofoomycetespeciesareparasitesofplants,andsomespecies,suchasthepotatolateblightagentPhytophthorainfestans,causediseasesofgreatimportancetomankind.Unsurprisingly,mostoftheresearchonoomycetesfocusesonplantpathogenicspecies[8??].

Oomyceteevolutionaryhistory:currentstatus

Oomyceteshavemostlikelyevolvedinamarineenviron-ment,asthemostbasallineagesoftheOomycotaarepredominantlymarineparasitesofseaweeds,diatoms,crustaceansandnematodes(Figure1).Despitetheirgreatgeneticdivergence,thesebasallineagesaccountforonlyabout5%ofoomycetespecies,whereasmorethan60%ofthespeciesareplantparasitic.ParasitismofplantshasevolvedatleastthreetimesindependentlyindifferentlineagesoftheOomycota(Figure1).ItemergedonceintheSaprolegnialesinwhichthelegumepathogenApha-nomyceseuteichesisbecominganimportantsubjectofstudy[9–11],andatleasttwiceintheperonosporaleanlineage,whichincludeswidelyknownplantpathogens,suchasdownymildews,Phytophthora,PythiumandAlbugo.Inaddition,evolutionfromapresumablysaprophyticances-torintoobligatebiotrophicpathogenshasoccurredtwiceintheperonosporeleanlineage,leadingtowhiteblisterrusts(Albuginales)anddownymildews(partofthePer-onosporaceae)(Figure1).

TheAlbuginalesareanancientlineagewithseveraltraitsthatunderscoretheirintimateadaptationtoplantpatho-genicity.Suchtraitsincludethelackofnecrotrophyeveninseverelyinfestedplanttissue(Figure2i),andinde-pendencefromatmosphericwaterforsporulation,auniqueoomycetetraitthatisdeterminedbyhighlyregulated,enzymemediatedsporulationandpustuleopeningmechanisms[12].Apparently,thehostimmunesystemisstronglymanipulatedbywhiteblisterrustsresultinginincreasedsusceptibilitytowardsotherpatho-gens[13].Inaddition,contrarytoearlierassumptions,mostspeciesoftheAlbuginaceaewererecentlyshowntobehighlyhostspeci?c[14,15],andaspecialisedspecies,

CurrentOpinioninPlantBiology2010,13:427–433

CurrentOpinioninPlantBiology2010,13:427–433ThisreviewcomesfromathemedissueonBioticinteractions

EditedbyJaneE.ParkerandJeffreyG.EllisAvailableonline4thMay2010

1369-5266/$–seefrontmatter

#2010ElsevierLtd.Allrightsreserved.DOI10.1016/j.pbi.2010.04.001

Introductiontotheoomycetes

Oomycetesareadiversegroupofeukaryoticorganismswithaworldwidedistribution.Theycanbefoundinterrestrialmountainsaswellasinopenseaenvironments.TheyhavenotonlycolonisedthedesertsofIran[1],butalsothearcticregionsoftheworld,includingAntarctica[2,3].Nonetheless,theoomycetesremainrelativelypoorlyknowncomparedtothetruefungi,theMycota,towhichtheyareunrelatedphylogenetically.

Acommonfeatureofalloomycetesistheirabilitytodirectlyabsorbnutrients(osmotrophiclifestyle),whichisthemainreasontheyhavelongbeenconfusedwiththefungi,withwhichtheyshareseveralconvergenttraitssuchashyphalgrowthanddispersalbymitoticallyformedspores.However,thetinsel?agellumwithtripartitehairsonthebi?agellatemotilestagesoftheoomycetesrevealedtheirtruephylogeneticaf?nitywithdiatoms

http://wendang.chazidian.com

428Bioticinteractions

Figure

1

http://wendang.chazidian.comsininvertedcommasdenotetaxainneedoftaxonomicrevision.Taxathatarenotyetformallyintroducedaremarkedwithanasterisk.Speciesnumbersareindicatedforthetwolargestoomyceteorders.

Albugolaibachii,wasrecentlyfoundtooccuronthemodelplantArabidopsisthaliana[16????].Albugocandidaistheonlywhiteblisterrustspeciesknownsofarwithabroadhostrangeincludingthreerelatedfamilies,theBrassicaceae,Capparaceae,andCleomaceae[17].Thebasisofthisbroadhostrangeisenigmatic,butispossiblymediatedbyyettobeidenti?edeffectorsthatinterferewithimmunepathwaysthatareconservedamongtheserelatedhostfamilies.

InthePeronosporales,biotrophyhasevolvedgradually,fromopportunisticpathogensamongPythium-likeancestors,tohemibiotrophyinPhytophthoraspecies,which,unliketheobligatebiotrophs,arealsoabletogrowondeadhosttissue(necrotrophy).SomePeronos-poraceaeevolvedahighdegreeofhostspecialisationandaprolongedbiotrophicphaseofinfection,ulti-matelyleadingtoobligatebiotrophywithdecreasingimpactonhost?tness(Figure2a–f).Evolutiontowardsobligatebiotrophywasmostlikelyaccompaniedbytheremarkableexpansionanddiversi?cationineffectorproteins,suchasthehost-translocatedRXLReffectors,whichhavenotbeenidenti?edoutsidethePeronos-porales[18–20].Geneticisolationoftheobligatebiotrophsdrivenbyhostspecialisationispronounced.Thishasledtoextensiveradiationandspeciationinseveraldownymildewgenera,especiallyinHyaloper-onospora,PeronosporaandPlasmopara,resultinginatotalofabout800downymildewspeciesdescribedtodate.Recently,thebasalgraminicolousdowny

CurrentOpinioninPlantBiology2010,13:427–433

mildewlineageswereshowntohaveintermediatecharacteristicsbetweendownymildewsandPhy-tophthorasuggestingstep-by-stepevolutionfromnecro-trophytoobligatebiotrophy[21].

Diversityofextendedphenotypescausedbyoomycetesonhostplants

Severalplantpathogensalterthemorphologyoftheirhostsinwaysthatimprovecolonisation,survivalanddispersal.Suchextendedphenotypessuggestthathostmanipulationbypathogeneffectorsismorecomplexthanthealterationofhostimmunity[22].Amongthemostdramaticextendedphenotypesofoomycetepathogensarethewitchesbroomphenotypescausedbyseveralgraminicolousdownymildews(Figure2g)[23,24].Inthesecases,systemicinfectionbytheoomyceteleadstothereplacementof?owersbyshoots,whichareoftenheavilyinfectedandwillproducemassiveamountsofbothasexuallyformedsporangiaandsexuallyformedoospores.Witchesbroomsprovidethepathogentheadvantageofbeingexposedtowindandrain,ensuringmoreef?cientdistributionofspores.Thisstrategyhasbeenfurtheroptimisedinthe?oricolousdownymildews,whicharemembersofamonophyleticcladewithinthegenusPeronospora[25].The?oricolousdownymildewsparasitiseAsteranaesensuChase&Reveal[26],andexclusivelysporulateon?oralpartsoftheplantstherebyexploitingpollinatinginsectsfordispersal.Manydownymildewsandwhiteblisterrustscaninfectthegenerativeorgansoftheirhosts(Figure2h–k)anddispersewith

http://wendang.chazidian.com

Oomycete–plantcoevolutionThinesandKamoun429

Figure

2

Diversityofsymptomscausedbyoomycetesontheirhostplants.(a)NecrotrophicgrowthofPhytophthorainfestansontomato.(b)NecrosisofAnemonenemorosaaftersporulationofPlasmovernapygmaea.(c)ChloroticlesioncausedbythesystemicgrowthofPseudoperonosporahumuliinhop.(d)SystemiccolonisationandsporulationofPeronosporasp.onViciatetrasperma,whichhardlyaltersthehostappearanceexceptforslightchlorosis.(e)ProfusesporulationofHyaloperonosporathlaspeos-perfoliationitshost(Microthlaspiperfoliatum)withoutadditionalvisiblesymptoms.(f)DistortionofCardaminehirsutacausedbyHyaloperonosporasp.,withonlylimitedsporulationandnoadverseeffectoninflorescencedevelopment.(g)WitchesbroomofPennisetumglaucumcausedbySclerosporagraminicola(imagecourtesyofSabineTelle).(h)Limitedsporulationof

Hyaloperonosporathlaspeos-arvensisonseedpodsofThlaspiarvense.(i)IntenseinfectionofCardaminepratensisbyAlbugosp.,withsporulation,butwithoutnecrosis.(j)SystemicinfectionandsporulationofHyaloperonosporacrispulaonaseedpodofResedalutea.(k)OpenedseedcapsuleofViciatetraspermasystemicallyinfectedbyPeronosporasp.,withnearlynormalseeddevelopment.

seeds[27–30].Somestudieshavedemonstratedthepre-

senceofoomyceteswithintheseedsoftheirhosts,which

mostlikelyenablespathogensurvivalanddispersal[31–

33](HellerandThines,unpublishedresults).

http://wendang.chazidian.comRecentadvancesinthestudyofoomycete–plantinteractionsLikeotherplantpathogens,oomycetesmanipulatetheirhostsbysecretinganarsenalofproteins,collectivelyCurrentOpinioninPlantBiology2010,13:427–433

430Bioticinteractions

knownaseffectors,whichtargetplantmoleculesandalterplantprocesses[22,34,35].Here,wehighlightsomerecentadvancesinthestudyofoomycete–plantinter-actionswithanemphasisoneffectorbiology

Oomycetegenomics:effectorspopulatedynamicandexpandedgenomeregions

thatenablethesegenome-levelstructuralpolymorphismstoimpactphenotypicvariationremaintobedetermined.

Effectortraf?ckingintoplantcells:How?

ThegenomesofseveraloomyceteshavebeensequencedbutsofaronlythoseofP.sojae,P.ramorumandP.infestanshavebeendescribedinpublications[18,20].Thegen-omeofP.infestansisremarkablebyitslargesize.At240MbpitisthreetofourfoldlargerthanthegenomesofP.sojaeandP.ramorum[18].ThisexpansionwasdrivenbyadramaticincreaseinmobileelementsandotherrepetitiveDNAwhichaccountfor 74%oftheP.infes-tansgenome[18].Mostgenefamiliesarenotexpanded.However,theRXLRandCRNfamiliesofeffectorsareexpandedtwofoldormoreinP.infestansrelativetoP.sojaeandP.ramorum[18].Theseeffectorgenesoccupyregionsofthegenomethatarerichinrepeatsandpooringenes[18].Haasetal.[18]proposedthatthesegenomeregionsaredynamicandaccelerateeffectorevolution,possiblybyenablingnonallelichomologousrecombina-tionandtandemgeneduplication.Genomesequencesofspeciesthatcoverthebroaderphylogeneticspectrumofoomycetepathogenspromiseadditionalinsights.Already,analysesofthetranscriptomesofSaprolegniaparasitica[36],Aphanomyceseuteiches[9]andPythiumulti-mum[37]revealeddistinctrepertoiresofeffectorsandpathogenicitydeterminants,highlightingthevalueofcomparativegenomics.

Copynumbervariationineffectorgenesimpactspathogen?tness

OomyceteRXLReffectorscarryanN-terminaldomainthatenablestranslocationinsidehostcellsandissimilarinsequence,positionandfunctiontothePEXELhosttranslocationsignalofmalariaparasites[41–45].HowtheRXLRdomainenablestranslocationinsidehostcellsisanimportantandchallengingquestion.Douetal.[46]reportedthatRXLReffectorsofP.sojaeenterplantcellsintheabsenceofthepathogen.TheyshowedthattheRXLRmotifofP.sojaeAvr1beffectorisrequiredforcelldeathinductionwhenafull-lengthconstructwiththesignalpeptideisexpressedinsoybeancells,presumablytoenablere-entryoftheproteinfollowingsecretion[46].Inaddition,Douetal.[46]demonstratedthatrecombi-nantfusionproteinsoftheRXLRdomainandthegreen?uorescentproteindirectlypenetratesoybeanrootcells.TheseexperimentssuggestthatRXLReffectorsdonotrequireapathogen-derivedmachinerytotraf?cinsidehostcellsandexclusivelyexploithost-derivedmolecules.Surprisingly,theseresultsmarkedlydifferfromthepre-vailingmodelofhosttranslocationofPEXELeffectorsreportedinPlasmodium,whichinvolvesprocessingofthePEXELmotifbyanendoplasmicreticulum-speci?cpro-teasefollowedbytherecruitmentofthecleavedeffectorsintoaparasite-derivedtranslocon[47–50].

Effectoractivities:desperatelyseekinghosttargets

Segmentalduplicationofnear-identicalcopiesandcopynumbervariation(CNV)arefrequentinRXLReffectorgenesofP.sojaeandP.ramorum[38????].Asigni?cantnumberofpredictedRXLReffectorgenes,rangingfrom17%inP.sojaeto65%inP.ramorum,wereestimatedtobepresentintwoormorecopies[38????].ThreeP.sojaeeffectorgenes,Avr1a,Avr3aandAvr3c,whichconferavirulencetotheircognatesoybeanRpsresistancegenes,occurintandemrepeatsanddisplayCNV[38????,http://wendang.chazidian.comVimpactstranscriptaccumulationofAvr1aandAvr3aandvirulenceonresistantsoybeanplantshighlightinganunusualmechanismofgeneticadaptationtohostresist-ance[38????].AnotherintriguingcaseofCNVinvolvestheP.infestansAvr3b-Avr10-Avr11locus,whichdeterminesavirulencetothreepotatoresistancegenesR3b,R10andR11[40].Acandidateavirulencegene,pi3.4,wasident-i?edinthislocusandfoundtoencodealargeproteinwiththefeaturesofatranscriptionalregulator[40].Inavirulentstrains,theAvr3b-Avr10-Avr11locusdisplayscopynum-bervariationresultinginampli?cationofupto25trun-catedcopiesofpi3.4[40].ThiscasefurtheremphasizestheoccurrenceofCNVinPhytophthoragenesassociatedwithvirulence/avirulence.However,themechanisms

CurrentOpinioninPlantBiology2010,13:427–433

Onecriticalquestioninthestudyofoomyceteeffectorsistheidenti?cationoftheirbiochemicalactivitiesandmodeofactiononhostcells.The?rststeptowardsthisobjec-tiveistoidentifythehosttargetmoleculesoftheeffec-tors.Sofar,thehosttargetsofRXLReffectorshavenotbeendescribedintheliteraturealthoughitisobviousfromconferenceproceedingsthatsomeprogresshasbeenmade[51].Incontrast,thetargetproteinsofseveraloomyceteapoplasticeffectors,manyofwhichfunctionashydrolaseinhibitors,havebeendetermined[35,52–54].Interestingly,theP.infestanscysteineproteaseinhibitorsEPIC1andEPIC2BbindandinhibitthetomatodefenseproteaseRcr3[55].TheysharethisactivitywithAvr2,anapoplasticeffectorsecretedbythefungusCladosporiumfulvum[56].The?ndingthatunrelatedpathogensevolvedeffectorstoinhibitthesamehosttarget,suggeststhattheinhibitedprotease,Rcr3,isanimportantcom-ponentofplantdefense[55].Inthefuture,additionalstudiesonoomyceteeffectorsandtheirhosttargetswillundoubtedlyhelptodiscoveranddissectnovelplantimmunepathways.

3Dstructuresofsecretedtoxin-likeproteins

Thestructuresoftwosecretedoomyceteproteinswithtoxinactivitieshavebeenreportedrecently[57,58].Sev-eralspeciesofbacteria,fungiandoomycetessecreteNep1-likeproteins(NLPs),conservedproteinsthathave

http://wendang.chazidian.com

Oomycete–plantcoevolutionThinesandKamoun431

evolvedorhavebeenacquiredbylargelyunrelatedorganismsandelicitnecrosisandimmuneresponsesintheleavesofdicotyledonousplants[59,60].InP.infestansandP.sojae,someNLPgenesareupregulatedduringtransitionfrombiotrophictonecrotrophicgrowth[18,61,62].ThecrystalstructureofanNLPfromtheoomycetePythiumaphanidermatumrevealedstructuralsimilaritytoactinoporins,cytolytictoxinsproducedbymarineorganisms[57].MutantanalysesrevealedthatthesamestructuralfeaturesarerequiredforNLPcytolysisandmembranepermeabilizationofplantcells,aswellascomplementationtofullvirulenceofanNLPmutantofthephytopathogenicbacteriumPectobacteriumcarotovorum[57].TheseresultsstrengthentheviewthatNLPsarevirulencefactorsthatfacilitatePythiumandPhytophthoranutrientacquisitionandtherebycolonisationofhostplantsduringthenecrotrophicphaseofinfection[61,62].PcFisasecreted52-amino-acidpeptideofPhytophthoracactorumthatcontainssix6cysteinesanda4-hydroxypro-lineatresidue49[63,64].PcFtriggersnecrosisintomatoandstrawberry,aneconomicallyimportanthostforP.cactorum[64].PcFisthoughttofunctionasatoxinandhasmultiplehomologsinseveralPhytophthoraspecies[18,20,65,66].Nuclearmagneticresonance(NMR)solutionstructureofPcFrevealedahelix–loop–helixmotiffoldwithsimilaritytoOlee6,amajorallergenfromolivetreepollensuggestingthatPcFmaymimicplantproteins[58].However,theexactmodeofactionofPcFfamilyproteinsremainsunclear.

structuralandfunctionalclassesofeffectors.Inparticular,itwillbeinterestingtodeterminetheextenttowhichtheknowledgegeneratedonPhytophthoraeffectorswillapplytoother,morespecialisedandmorebiotrophicoomycetepathogens.

Acknowledgements

MTissupportedbyafellowshipfromtheMaxPlanckSociety,theElite

¨rttemberg,andtheProgramforPostdocsoftheLandesstiftungBaden-Wu

GermanSciencefoundation(DFG);SKisfundedbytheGatsbyCharitableFoundation,theBiotechnologyandBiologicalSciencesResearchCouncil(BBSRC),andBASFPlantSciences.

Referencesandrecommendedreading

Papersofparticularinterest,publishedwithintheperiodofreview,havebeenhighlightedas:??ofspecialinterest

????ofoutstandinginterest1.

Mirzaee,AbbasiM,MohammadiM:AlbugocandidacausingwhiterustonErysimumcrassicauleinIran.AustralasPlantDisNotes2009,4:124-125.

BridgePD,NewshamKK,DentonGJ:SnowmouldcausedbyaPythiumsp.:apotentialvascularplantpathogeninthemaritimeAntarctic.PlantPathol2008,57:1066-1072.

HughesKA,LawleyB,NewshamKK:SolarUV-Bradiation

inhibitsthegrowthofAntarcticterrestrialfungi.ApplEnvironMicrobiol2003,69:1488-1491.

¨berdieGeisselstrukturderVlkW:U

¨rmer.Archivfu¨rProtistenkunde1939,Saprolegniaceenschwa

92:157-160.

DickMW:StraminipilousFungi:Systematicsofthe

PeronosporomycetesIncludingAccountsoftheMarineStraminipilousProtists,thePlasmodiophoridsandSimilarOrganismsDordrecht/Boston/London:KluwerAcademicPublishers;2001.

¨berdieEntwicklungdesmarinenSchnepfE,DrebesG:U

parasitischenPhycomycetenLagenismacoscinodisci

¨nderwissenschaftliche(Lagenidiales).Helgola

Meeresuntersuchungen1977,29:291-301.

¨llerA,Gru¨ndelA,LangerE:TheseasonaloccurrenceofRiethmu

thesewagefungusLeptomituslacteus(Roth)C.Agardhinstagnantandrunningwaterbodiesofdifferentwater

chemistryofHesseandThuringia,Germany.ActaHydrochimHydrobiol2006,34:58-66.

2.

3.

4.

5.

Futureprospects

Thestudyofoomycetesandtheireffectorsisahighlydynamicandexpandingareaofresearch.However,mostoftheworkfocusesonafewspecies,particularlyP.infestans,P.sojaeandH.arabidopsidis.Littleisknownabouttheeffectorsofotherplantparasiticoomycetes,someofwhichhaveevolvedremarkableadaptationstotheirparasiticlifestyle(Figure2).Indeed,theinteractionsbetweenoomyceteparasitesandplantscanbemorecomplexthancolonisationofleaforroottissueandsomespeciestriggerstrikingsymptoms,suchaswitchesbrooms(Figure2g),orspecialiseonparticularplantorgansasinthe?oricolousdownymildews.Theseobservationspromptanumberofintriguingquestionsgiventhatnaturalselectionwouldfavoureffectorsthatmediateanytypeofphenotypicexpressionaslongastheyimprovepathogen?tness.Arethereoomyceteeffectorsthatactbeyondalteringhostimmunity?Arethereeffectorsthatalterplantdevelopmenttofacilitatepathogensurvivalanddispersal?Arethereeffectorsthatareexpressedonlyinparticularplantorgans?Forinstance,downymildewsandwhiteblisterruststhatareseedtransmittedmayhaveevolvedeffectorsthataffectseedsurvivalandgermina-tion.Undoubtedly,genomesequencingofabroaderspectrumofoomycetespecieswillexpandourknowledgeofpathogenicitymechanismsandlikelyrevealnovel

http://wendang.chazidian.com

6.

7.

8.??

LamourK,KamounS(Eds):OomyceteGeneticsandGenomics:Diversity,InteractionsandResearchTools.Hoboken,NJ:Wiley–Blackwell;2009.

Thisbookprovidesacomprehensivetreatmentofgeneticsandgenomicsofoomycetesandisausefulresourcetonewcomerstothe?eld.9.

GaulinE,MadouiMA,BottinA,JacquetC,MatheC,CoulouxA,WinckerP,DumasB:TranscriptomeofAphanomyces

euteiches:newoomyceteputativepathogenicityfactorsandmetabolicpathways.PLoSOne2008,3:e1723.

10.HamonC,BarangerA,MiteulH,LecointeR,LeGoffI,DeniotG,

OnfroyC,MoussartA,ProsperiJM,TivoliBetal.:Acomplexgeneticnetworkinvolvingabroad-spectrumlocusandstrain-speci?clocicontrolsresistancetodifferentpathotypesofAphanomyceseuteichesinMedicagotruncatula.TheorApplGenet2010,120:955-970.´guez-UribeondoJ,Garc?´E,´aMA,CereniusL,Kozub?´kova11.Die

¨derha¨llK,BallesterosI,WindelsC,WeilandJ,KatorH,So

´nMP:PhylogeneticrelationshipsamongplantandanimalMart?

parasites,andsaprotrophsinAphanomyces(Oomycetes).FungalGenetBiol2009,46:365-376.12.HellerA,ThinesM:Evidencefortheimportanceofenzymatic

digestionofepidermalwallsduringsubepidermalsporulation

CurrentOpinioninPlantBiology2010,13:427–433