Genomics of biotrophy in fungi and oomycetes — emerging patterns

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Genomicsofbiotrophyinfungiandoomycetes—emergingpatterns

¨rgKa¨mper2PietroSpanu1andJo

Weareonthevergeofa?oodofnewgenomedatafroma

plethoraofplantpathogens.Althoughthedataarejustbeginningtobeanalysedsystematicallyandtobepublished,thereareemergingpatternsassociatedwithpathogenicityandbiotrophy.Theexpansionofproteinfamilieswithfunctionsrequiredforhostinfectionisfoundinmostpathogens;inaddition,weseespeci?cadaptationsofthebiotrophs,asthereductionofproteinsinvolvedinplantcell-walldegradation,oraspecializationincarbonutilizationthatavoidsplantresponses.Theexpansionofgenomesbyrepeatedelementsandtheresultinggenomedynamicsarethoughttobeoneofthedrivingforcesforthefastevolutionofpathogenicityfactors,resultinginan

adaptiveadvantagetothechanginghostileenvironmentoftheplanthost.

Addresses1

DepartmentofLifeSciences,ImperialCollegeofScience,TechnologyandMedicine,ImperialCollegeRoad,LondonSW72AZ,UnitedKingdom2

KarlsruheInstituteofTechnology,InstituteofAppliedBiosciences,DepartmentofGenetics,Hertzstrasse16,76187Karlsruhe,Germany¨mper,Correspondingauthor:Spanu,Pietro(p.spanu@ic.ac.uk)andKa

¨rg(joerg.kaemper@kit.edu)Jo

Inbothfungiandoomycetestheabilitytoinfectplants

andbiotrophyisapolyphyletictrait.Thisraisesthequestionofwhetherbiotrophyisancestraltonecrotrophy,orviceversa.Theintermediatestatusoffacultativebiotrophy(hemibiotrophy)iscommonamongplantpathogens.Manybona-?denecrotophshavestagesofinfectionwhichresemblebiotrophy;hemibiotrophymaythereforerepresentanevolutionary‘‘?exible’’status.Incontrastobligatebiotrophyseemstobeanevolutionary‘dead-end’specialization:onceenteredinto,itisatroughfromwhichitisimpossibletoescape.

Exploitingthegenome:repertoireofbiotrophicfungi

Genomicsimpactsourunderstandingofboththemolecu-largeneticbasisforbiotrophyanditsevolutioninmicrobialpathogensandmutualisticsymbionts.The?oodofnewdatafromalargecohortofmicrobialgenomesenablesarapidandsystematicminingforgeneidenti?cation,classi?cationandfunctionalanalysis(http://wendang.chazidian.com/annotation/fungi/;http://www.jgi.doe.gov/gen-ome-projects/).Theadventofcomparativegenomicswillaffectthewayweunderstandtheseorganisms,possiblyakintotheimpactthatcomparativeanatomyhadinthe18thand19thcenturies.

Adaptationandspecializationofbiotrophicpathogenstotheirhostplantrequiresspeci?csetsofgenes.Theexpansionofindividualproteinfamiliessuggeststheyplayaspeci?croleinplantpathogeninteractions.Themostobviousfamilyexpansionfoundinhemibiotrophicandbiotrophicfungiandoomycetesaresecretedproteinswithpotentialeffectorfunction[1,2????];thistopichasreceivedhugeattentioninrecentyearsandisthesubjectofnumerousauthoritativereviews[3–5].Inthehemibio-trophsMagnaportheoryzae(syn.M.grisea)andFusariumgraminearum,G-protein-coupledreceptorsarehighlyabundant,with84GPCRsinF.graminearumand61inM.grisea[6,7],whichmayemphasizethenecessityforthesepathogenstorespondtoenvironmentalcues.How-ever,otherspecies,suchasthesmutfungusUstilagomaydis,haveobviouslydevelopedalternativestrategies:asidefromthepheromonereceptor,U.maydisharboursonlytwoadditionalpotentialGPCR,bothofwhicharedispensableforpathogenicdevelopment(GWeinzierl,J¨mper,unpublishedresults).Ka

Thereductionofspeci?cgene/proteinfamiliesisequallyinformative.Forexample,U.maydislacksvariouspatho-genicitysignaturesthatareassociatedwithpathogenswithanecrotrophicstage:M.oryzae,F.graminearum

CurrentOpinioninPlantBiology2010,13:409–414

CurrentOpinioninPlantBiology2010,13:409–414ThisreviewcomesfromathemedissueonBioticinteractions

EditedbyJaneE.ParkerandJeffreyG.EllisAvailableonline27thApril2010

1369-5266/$–seefrontmatter

#2010ElsevierLtd.Allrightsreserved.DOI10.1016/j.pbi.2010.03.004

Introduction

Biotrophyisanecologicalnicheoccupiedbyalargeanddiversegroupofmicrobeswhichinteractwithplants.Ingeneral,biotrophsarecapableofinfectingandfeedingoffaplanthostwithoutkillingit.Thiscontrastswithnecrotrophy,wherethemicrobescausecelldeathandfeedoffthedeadtissues.Manybiotrophshavenoknownsaprophyticexistenceinnature,cannotbesimplycultured,relycompletelyontheirlivinghostsandarethusclassi?edasobligate.Inthisarticlewewilldiscussideasonthegeneticandevolutionarybasisofbiotrophy,whichareemergingfromgenomicandcom-parativegenomicanalysisoffungalandoomycetepathogensofplants.

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410Bioticinteractions

andCochliobolusheterostrophusharbourupto25polyketidesynthasesinvolvedintheproductionofsecondarymetab-olitessuchasantibioticsortoxins,U.maydispossessesonlythree[1].Similarly,thesetofproteinsrequiredforthedegradationofplantcellwalls,aspolysaccharidehydrolases,polysaccharidelyasesandpectinesterases,issmallwhencomparedtothatofhemibiotrophicfungithatusetheseenzymestodegradetheplanttissueduringtheirnecrotrophicstage[8].Thisreductionofcell-walldegradingenzymesisevenmorestrikingwhenthegen-omesoftheobligatebiotrophsarecomparedtocloserelativeswhicharenon-obligatepathogens.Thepaucityofplantcell-walldegradingenzymesisinlinewiththebiotrophiclifestyle;theenzymesarelikelyusedtosoftenorweakentheplantcellwallstofacilitatethecelltocellpassageofhyphae,rathertofacilitatetheutilizationofcell-wallderivedcarbohydrates;inaddition,thereleaseofcell-wallderivedelicitorsthattriggeraplantresponseisavoided.Incontrast,thecell-wall-degradingenzymesdevotedtotheremodellingofthepathogen’sowncellwallsareretainedasintheirnon-biotrophiccounterparts(JMcDowelletal.,abstract,XVIIPlantandAnimalGenomeConference,SanDiego,USA,January2010;PSpanuetal.,abstract,9thInternationalMycologicalCon-gress,Edinburgh,UK,August2010).

Inadditiontogenefamilyexpansionandgenefamilyloss,thekeytounderstandingbiotrophymayalsoinvolvethespeci?cregulationofgeneexpression:theskillofthecraftsmandependsonthetimelyandspatialuseofgiventools,asmuchasonthesetoftoolsitself.Inearlyresearchintranscriptomics,weusedEST-basedarraysfortheobligatebiotrophBlumeriagraministocomparedevelop-mentalstagesbeforeandafterpenetrationofthehostplant.Themain?ndingswerestrikingpatternsofcoor-dinateexpressionofgenesencodingprimarymetabolicpathwaysand,separately,ofgenesencodingvirulencedeterminants[9,10].Morerecentcomparisonoftranscrip-tomedynamicsduringdevelopmentonhost,non-hostandarti?cialsurfacesindicatesthatingeneraltheresponsetoaspeci?chostsurfacesetsinmotionahighlycomplexnetworkofgene-regulationevenbeforepenetra-tionoftheplantcells(PSpanu,unpublished).InU.maydis,genome-basedarrayshavebeenusedtoanalysedifferentaspectsofpathogenicdevelopment,suchastheresponsetonutrientstarvation,ironuptakeandtheresponsetoH2O2[11–13];inaddition,monitoringofthegeneexpressionpro?leduringinplantagrowthhasidenti?edclusteredgenesforsecretedeffectorsas‘plantinduced’[1].InU.maydis,theonsetofthebiotrophicstageiscontrolledviathebE/bWtranscriptionfactorencodedbytheb-matingtypelocus,whichallowedtheassessmentofexpressionattheswitchfromsaprophytictobiotrophicgrowth(KHeimeletal.,unpublished).b-Regulatedgenesareinvolvedincell-wallremodelling,encodepotentialsecretedeffectors,andalsofunctionincellcyclecontrol:bE/bWinducesaG2cellcyclearrest

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thatisreleasedonlyafterplantpenetration.ThuswhilstbE/bWregulatesthegenesthatarerequiredforinplantagrowth,italsocausestherequirementtoinfecttheplantbymeansofacellcycleblock,i.e.itleadstotheinitiationof‘obligatebiotrophy’.ThebE/bWheterodimerorches-tratesaregulatorycascadeofdifferenttranscriptionfac-tors:Rbf1,asamasterregulator,isrequiredfortheexpressionofmostb-regulatedgenes,includingthetran-scriptionfactorsHdp2andBiz1.Rbf1,Biz1andHdp2areallindependentlyrequiredforpathogenicdevelopment(KHeimeletal.,http://wendang.chazidian.com1controlstheexpres-sionofgenesspeci?callyinducedattheveryearlyin-¨mper,unpublished),whichfectionstage(MVranes,JKa

canexplaintherequirementofBiz1forappressoriade-velopment[14].Theadvantageofsuchcomplexregulat-orypathwaysisthedynamicintegrationofdifferentsignalsthatallowtheabove-mentionedtemporalandspatialcontrolofdevelopmentaldecisions,as,forexample,theadaptationtospeci?ctissues.ThesecretedeffectorPep1,forexample,isinducedinpenetratinghyphae,consistentwiththerequirementoftheproteinduringthisstage[15].Transcriptpro?lingofdifferentmaizeorgansduringinteractionwithU.maydisrevealedthatinparticulargenesforsecretedeffectorsshowahighleveloforganspeci?cresponses.Mostinterestingly,thetissuespeci?cregulationwaslinkedtoafunctionofdifferenteffectorsinorgan-speci?ctumourformation(DSkibbeetal.,unpublished).

Evolutionofvirulencegenes/effectors

ComparativeanalysisofthethreesequencedoomycetegenomesfromPhytophthorasojae,P.ramorumandP.infestansrevealedrapidexpansionsanddiversi?cationsofproteinfamiliesassociatedwithplantinfection,ashydrolases,ABCtransporters,toxinsandsecretedeffec-tors[2????,16].Inparticular,theeffectorsshowedarapidturnoverandextensiveexpansionofmulti-genefamilies[17,18??].ThegenesarelocalizedtohighlydynamicgenomicregionsrichinrepetitiveDNA,whichmaybecrucialfortherapidadaptationofthepathogen.Althoughcomparablein-depthanalyseshavenotbeenpublishedyetforbiotrophicfungi,itisconceivablethatthefastevolutionofvirulencegenesisageneralfeatureofpathogenicorganisms.Inthe?axrustMelampsoraliniextensivesequencevariationwasfoundindifferentiso-latesattwoeffectorloci,AvrP123andAvrP4[19].InN.haematococcaandLeptosphaeriamaculans(causingtheblacklegdiseaseonBrassica),thegenesforpotentialeffectorsareclusteredingenomicregionsinterspersedwithtransposableelementsandtransposonderivedrepeats[20,21];likewise,theAvr-PitagenesofM.oryzaeareassociatedwithtelomeresand?ankedbyrepetitiveelements[22].ThefastevolutionofgeneswithinsuchregionswasdemonstratedinL.maculans:withina?eldpopulationduringasingleyeartheAvrLm6genewasinactivatedbymultiplepatternsofmutationcausedbydeletionsand,frequently,byrepeatinducedpoint

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¨mper411GenomicsofbiotrophyinfungiandoomycetesSpanuandKa

mutations(RIP)[23??].Itisanemergingpicturethatmany

ofthebiotrophs,andparticularlytheobligatebiotrophs,havesurprisinglyhighnumbersoftransposableelementsintheirgenomesasawhole.Thesearemostlyretro-transposonswhichcauseaconsequentincreaseinthesizeofwholegenomes(PSpanuetal.,abstract,10thEuropeanFungalGeneticConference,Leiden,March2010).Itistemptingtospeculatethatthisistheresultsofanadaptiveadvantageconferredbyahighlydynamicgenome,andthatthisisparticularlythecaseforpathogenswhosesolenicheisanotherorganismwhichisitselfevolvingandadaptingtoresistharmfulinfections:theRedQueen[24]goesinoverdrive.

Itmustbenoted,however,thatthefastadaptationviadynamicregionswithingenomesisnotauniversalphenomenon.U.maydis,forexample,harboursonlyfewremnantsoftransposableelements(andnootherrepetitiveelements)[1],andthegenesforsecretedeffectorsarenotlocatedwithinunstablechromosomallocations.Nevertheless,theeffectorgeneshaveafastevolutionary‘pace’.InbothU.maydisaswellasintherelatedsmutSporisoriumreilianum,alsoinfectingmaize,

Figure

1

theeffectorgenesarearrangedinseveralclusters.Althoughthegenomesofbothfungishowingeneralahighsyntheny,theeffectorgenesoftendifferinnumbersanddisplaymuchlowersequenceconservationthantheremaininggenome(JSchirawski,RKahmann,unpub-lished).Whilstinotherfungitheoccurrenceofclustersmaybeexplainedbytheirvicinityto‘dynamic’regions,inU.maydistheclusteringmaybeexplainedthroughtheirregulationviachromatinstructure.WehaveobservedthatthedeletionofeitherthehistonedeacetylaseHda1[25]orofthepotentialhistonedemethylaseRum1[26]leadstothederepressionofvariousclusteredgenes(MTreu-¨mper,unpublishedresults).Thus,indifferenttlein,JKa

fungi,diversemechanismshaveshapedtheclusteringofgenes.

Metabolicreprogramming

Biotrophicfungineedtoacquirenutrientsfromlivingtissueandcauseaslittledamagetothehostaspossible.Inpathogensthatbreachthecellwall(intracellularparasites)theinterfacebetweenthehyphaeandtheensheathingplasmamembraneisconsideredthemainsiteofsignalandnutrientexchange;inseveralbiotrophs

Intracellularhyphaeofbiotrophicfungiareensheathedbyaplantmembranecontinuouswiththeplasmalemma.(a)Anisolatedhaustorium(feedingstructure)ofBlumeriagraminisstainedwithWGA-Alexa488;theplantderivedperihaustorialmembraneisseenhere(*)asitpartiallydetachesfromthehaustoriumbecauseofosmoticimbalancesintheisolatingmedium(PSpanu,unpublished).Thehaustorialdigits(**)increasetheoverallsurfacearea,presumablytofacilitateexchangesbetweeninteractionpartners.(b)Ustilagomaydishyphaetraversingplantcells(*)andarecloselyencasedbythehostplasmamembrane(**).HyphaearelabelledwithacytoplasmaticallylocalizedRFP,theplantplasmamembraneisvisualizedviaaPIN1–YFPfusionproteinexpressedbythemaizeplant(CourtesyofGDoehlemann,MPIforTerrestrialMicrobiology,Marburg).(Scalebars:10mm)http://wendang.chazidian.com

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412Bioticinteractions

specialstructures,thehaustoria,leadtoanexpansionoftheinterface,bythatimprovingtheexchange(Figure1).Forfoliarpathogenstheconsequenceofnutrientuptakeisashiftfromsourcetosinkininfectedplanttissues.Thisreprogrammingofthehostmetabolismmaybetheresultfromthelocalutilizationofacarbonsource,assucrose,bythepathogen,bythatinducingasink.However,metabo-lomeandtranscriptomeanalysesrevealedforM.oryzaeandU.maydisthatthereprogrammingoccursinpre-sympto-matictissueswhenthepathogenisstillintheprocessofpenetratingindividualepidermalcells[27,28].Thus,itappearsmorelikelythatthepathogenin?uencesthecarbon?owinthehostviaactivesignalling,possiblybytheactionofsecretedeffectors.Sincethebiotrophicfungistudiedtodateappeartorelyontheprovisionofhexosesasacarbonsource,theydependoninvertaseactivityintheapoplasttoaccessthesucrosepool[29].Inaccordancewiththis,asystematicevaluationofinvertasegenesinfungalgenomesrevealedthattheirnumberwaspositivelycorre-latedwithbiotrophy,whilstmostgenomesofmycorrhizaltaxalackinvertasegenes[30??].ExceptionsofthisrulearefoundinU.maydisandB.graminis.InU.maydisthesingleclassicalinvertaseisdispensableforpathogenicdevelop-¨mper,unpublished),evenwhendeletedment(SGoos,JKa

incombinationwiththegeneforasucrose-6P-hydrolasethatwasshowntoberequiredforsucrosecleavageinAspergillusniger[31].InB.graminis,nohomologuesofextracellularinvertasesorsucrose-6P-hydrolaseatallhavebeenfound(PSpanu,unpublished).Bothfungiuseprob-ablystrategiesforcarbonacquisitionthatdonotrequiretheactionofsecretedinvertases.Thesystematicdeletionanalysisofall19hexosetransporterspresentinthegenomeofU.maydishasledtotheidenti?cationofanoveltypeofsucrosetransporter,Srt1,asavirulencefactor[32????].Srt1isexpressedonlywithintheplant,andhasahigheraf?nitytosucrosethantheknownplanttransporters,andallowsthedirectutilizationofsucroseattheplant/fungalinterfacewithoutextracellularhydrolysisand,thus,withouttheproductionofextracellularmonosaccharidesknowntoelicitplantimmuneresponses[32????].B.graminisharbourstwosucrosetransporterswithsimilaritiestoSrt1(PSpanu,unpublished),whichmayarguethatthedirectuptakeofsucroseischaracteristicforthebiotrophiclifestyle.Ofcourse,themostinterestingquestioniswhetherthegenomeofobligatebiotrophicfungiallowsanyconclusionwhatismissinginthesefungitomakethemdependentontheirhosts.Anevidentexplanationwouldbethatessentialmetabolicpathwaysaremissing:butatpresentthisdoesnotappeartobethecaseforthetrueobligatebiotrophB.graminis[9].Amorelikelyalternativeisthatintheregulationofmetabolismdependsontheplant-derivedcues[33]:tocontinuewiththecraftsmanmeta-phor:itisnotthatthetoolsaremissing,buttheycannotbeusedwithoutperceptionofhostsignals.Infactwemayseethishappeninginthenon-obligatebiotrophU.maydis.DuringitssaprophyticstageU.maydisgrowsonminimal

CurrentOpinioninPlantBiology2010,13:409–414

mediawithoutrequirementofanysupplements.How-ever,oncethebiotrophicstageisentered,thefungusdependsentirelyontheplant:itbehaveslikeanobligate[34].Itmaybesaidthatthepriceforanadvancedandhighlyintegratecompatibleinteractionsystemmaybethethelossoffreedom.

Conclusions

Atpresentweareonthevergeofa?oodofgenomedatafromamyriadoffungiandoomycetes.Currentlythedataareonlyjustbeginningtobepublished,tobecomefreelyavailableandanalysedsystematically,indepthandacrosstaxa.Theemergingpatternsinbiotrophyhinttoremark-ableconvergencesintheevolutionaryspace:?rstly,limitationorlossofwholeswathesofplantcell-wall-degradingenzymes;secondly,expansionanddiversi?ca-tionofproteineffectorsfamiliesclusteredincoordinatelyexpressedgenomicregionsorsometimesassociatedwiththedynamicandunstableelements;thirdly,theadaptiveadvantagethatresultsfromthisassociationdrivesanexpansionofgenomicparasites(transposableelements)andoverallexpansionofgenomesize.

Theideaspresentedherewillneedtobetestedrigorouslyandsystematically,particularlythroughanalysisofcloselyrelatedorganismswhichadoptverydivergentlifestyles.Wearebutatthedawnofcomparativegenomics,andasthesunrisesoverthepathogenomiclandscapesnewandperhapsunexpecteddiscoverieswillbemade.Excitingtimeslieahead.

Acknowledgements

WewouldliketothankRKahmann,JSchirawski,GDoehlemann(MPIforterrestrialMicrobiology,Marburg,Germany)andVWalbot(StanfordUniversity,USA)forkindlyprovidingtheirunpublisheddata.

Referencesandrecommendedreading

Papersofparticularinterest,publishedwithintheperiodofreview,havebeenhighlightedas:??ofspecialinterest

????ofoutstandinginterest1.

¨mperJ,KahmannR,Bo¨lkerM,MaLJ,BrefortT,SavilleBJ,Ka

¨llerOetal.:InsightsfromBanuettF,KronstadJW,GoldSE,Mu

thegenomeofthebiotrophicfungalplantpathogenUstilagomaydis.Nature2006,444:97-101.

2.????

HaasBJ,KamounS,ZodyMC,JiangRH,HandsakerRE,

CanoLM,GrabherrM,KodiraCD,RaffaeleS,Torto-AlaliboTetal.:GenomesequenceandanalysisoftheIrishpotatofaminepathogenPhytophthorainfestans.Nature2009,461:393-398.Indepthanalysisofthe240MbP.infestansgenomeincomparisonwiththegenomesoftworelatedPhytophthoraspecies,P.sojae(95Mb)andP.ramorum(65Mb).TheexpansionoftheP.infestansgenomeresultsfromtheproliferationofrepetitiveDNA.Thecomparativeanalysisshowsarapidturnoverandextensiveexpansionofspeci?cfamiliesofsecreteddiseaseeffectorproteins,manyofwhichareinducedduringinfection.Thereportshowsconclusivelythatvirulence-associatedgenesareloca-lizedtothedynamicandexpandedregionsoftheP.infestansgenome,reasoningtherapidadaptabilityofthepathogen.3.

StergiopoulosI,DeKockMJ,LindhoutP,DeWitPJ:AllelicvariationintheeffectorgenesofthetomatopathogenCladosporiumfulvumrevealsdifferentmodesofadaptiveevolution.MolPlantMicrobeInteract2007,20:1271-1283.

http://wendang.chazidian.com

¨mper413GenomicsofbiotrophyinfungiandoomycetesSpanuandKa

4.

EllisJG,Ra?qiM,GanP,ChakrabartiA,DoddsPN:Recent

progressindiscoveryandfunctionalanalysisofeffectorproteinsoffungalandoomyceteplantpathogens.CurrOpinPlantBiol2009,12:399-405.

HogenhoutSA,VanderHoornRA,TerauchiR,KamounS:Emergingconceptsineffectorbiologyofplant-associatedorganisms.MolPlantMicrobeInteract2009,22:115-122.

DeanRA,TalbotNJ,EbboleDJ,FarmanML,MitchellTK,

OrbachMJ,ThonM,KulkarniR,XuJR,PanHetal.:ThegenomesequenceofthericeblastfungusMagnaporthegrisea.Nature2005,434:980-986.

CuomoCA,GuldenerU,XuJR,TrailF,TurgeonBG,DiPietroA,WaltonJD,MaLJ,BakerSE,RepMetal.:TheFusariumgraminearumgenomerevealsalinkbetweenlocalizedpolymorphismandpathogenspecialization.Science2007,317:1400-1402.

¨mperJ,DoehlemannG,WahlR,VranesM,deVriesRP,Ka

KahmannR:Establishmentofcompatibilityinthe

Ustilagomaydis/maizepathosystem.JPlantPhysiol2008,165:29-40.

BothM,CsukaiM,StumpfMP,SpanuPD:Geneexpressionpro?lesofBlumeriagraminisindicatedynamic

changestoprimarymetabolismduringdevelopmentofanobligatebiotrophicpathogen.PlantCell2005,17:2107-2122.

19.BarrettLG,ThrallPH,DoddsPN,vanderMerweM,LindeCC,

LawrenceGJ,BurdonJJ:DiversityandevolutionofeffectorlociinnaturalpopulationsoftheplantpathogenMelampsoralini.MolBiolEvol2009,26:2499-2513.20.FudalI,RossS,GoutL,BlaiseF,KuhnML,EckertMR,CattolicoL,

Bernard-SamainS,BalesdentMH,RouxelT:Heterochromatin-likeregionsasecologicalnichesforavirulencegenesintheLeptosphaeriamaculansgenome:map-basedcloningofAvrLm6.MolPlantMicrobeInteract2007,20:459-470.21.GoutL,FudalI,KuhnML,BlaiseF,EckertM,CattolicoL,

BalesdentMH,RouxelT:Lostinthemiddleofnowhere:theAvrLm1avirulencegeneoftheDothideomyceteLeptosphaeriamaculans.MolMicrobiol2006,60:67-80.22.KhangCH,ParkSY,LeeYH,ValentB,KangS:Genome

organizationandevolutionoftheAVR-PitaavirulencegenefamilyintheMagnaporthegriseaspeciescomplex.MolPlantMicrobeInteract2008,21:658-670.23.FudalI,RossS,BrunH,BesnardAL,ErmelM,KuhnML,??BalesdentMH,RouxelT:Repeat-inducedpointmutation(RIP)

asanalternativemechanismofevolutiontowardvirulenceinLeptosphaeriamaculans.MolPlantMicrobeInteract2009,22:932-941.

Thestudyrevealsthefateofpathogenicity-relatedgenesresidinginnon-coding,heterochromatin-likeregionsinfungi:withina?eldpopulationduringasingleyeartheAvrLm6genewasinactivatedbymultipleindependentmutationevents,asdeletionsand,frequently,byrepeatinducedpointmutations(RIP).

24.VanValenL:Anewevolutionarylaw.EvolutTheory1973,1:1-30.25.ReichmannM,JamnischekA,WeinzierlG,LadendorfO,HuberS,

¨mperJ:ThehistonedeacetylaseHda1fromKahmannR,Ka

Ustilagomaydisisessentialforteliosporedevelopment.MolMicrobiol2002,46:1169-1182.¨mperJ:26.Quadbeck-SeegerC,WannerG,HuberS,KahmannR,Ka

Aproteinwithsimilaritytothehumanretinoblastomabindingprotein2actsspeci?callyasarepressorforgenesregulatedbythebmatingtypelocusinUstilagomaydis.MolMicrobiol2000,38:154-166.27.CaldoRA,NettletonD,PengJ,WiseRP:Stage-speci?c

suppressionofbasaldefensediscriminatesbarleyplantscontainingfast-anddelayed-actingMlapowderymildewresistancealleles.MolPlantMicrobeInteract2006,19:939-947.28.DoehlemannG,WahlR,HorstRJ,VollLM,UsadelB,PoreeF,

¨hnemannJ,SonnewaldU,KahmannRetal.:StittM,Pons-Ku

Reprogrammingamaizeplant:transcriptionalandmetabolicchangesinducedbythefungalbiotrophUstilagomaydis.PlantJ2008,56:181-195.29.VoegeleRT,WirselS,MollU,LechnerM,MendgenK:Cloningand

characterizationofanovelinvertasefromtheobligate

biotrophUromycesfabaeandanalysisofexpressionpatternsofhostandpathogeninvertasesinthecourseofinfection.MolPlantMicrobeInteract2006,19:625-634.30.ParrentJL,JamesTY,VasaitisR,TaylorAF:Friendor??foe?Evolutionaryhistoryofglycosidehydrolasefamily32

genesencodingforsucrolyticactivityinfungiandits

implicationsforplant–fungalsymbioses.BMCEvolBiol2009,9:148.

Anextensivephylogeneticanalysisoffungalglucosidehydrolases(e.g.invertases)whichcombinestheuseofgenomicdataandexperi-mental(PCR-based)detectionofthesegenes.Thestudyrevealsageneraltrendtowardslossofinvertasesinanimalpathogenicfungiandanexpansionanddiversi?cationofinvertasefamiliesinmostplantpathogenicfungi.Interestinglythemycorrhizalfungiappeartolose/nothavethehydrolaseswhichleadstheauthorstoaskthemselveswhetherplantsmayusepresenceofinvertasesto‘todifferentiateantagonisticfrommutualisticbiotrophicsymbionts’.Itwouldbeintri-guingtospeculatethatsomehighlyspecializedpathogens,suchasB.graminismayadoptlossofextracellularinvertasesasaformofmolecularmimicry.

31.GoosenC,YuanXL,vanMunsterJM,RamAF,vanderMaarelMJ,

DijkhuizenL:Molecularandbiochemicalcharacterizationofa

CurrentOpinioninPlantBiology2010,13:409–414

5.

6.

7.

8.

9.

10.BothM,EckertSE,CsukaiM,MullerE,DimopoulosG,SpanuPD:

Transcriptpro?lesofBlumeriagraminisdevelopment

duringinfectionrevealaclusterofgenesthatarepotentialvirulencedeterminants.MolPlantMicrobeInteract2005,18:125-133.¨mperJ,Bo¨lkerM:11.HewaldS,LinneU,SchererM,MarahielMA,Ka

Identi?cationofageneclusterforbiosynthesisof

mannosylerythritollipidsinthebasidiomycetousfungusUstilagomaydis.ApplEnvironMicrobiol2006,72:5469-5477.¨mperJ,12.EichhornH,LessingF,WinterbergB,SchirawskiJ,Ka

¨llerP,KahmannR:Aferroxidation/permeationironuptakeMu

systemisrequiredforvirulenceinUstilagomaydis.PlantCell2006,18:3332-3345.13.MolinaL,KahmannR:AnUstilagomaydisgeneinvolvedinH2O2

detoxi?cationisrequiredforvirulence.PlantCell2007,19:2293-2309.¨mperJ,Perez-MartinJ:Biz1,azinc14.Flor-ParraI,VranesM,Ka

?ngerproteinrequiredforplantinvasionbyUstilago

maydis,regulatesthelevelsofamitoticcyclin.PlantCell2006,18:2369-2387.15.DoehlemannG,vanderLindeK,AssmannD,SchwammbachD,

HofA,MohantyA,JacksonD,KahmannR:Pep1,a

secretedeffectorproteinofUstilagomaydis,isrequiredforsuccessfulinvasionofplantcells.PLoSPathog2009,5:e1000290.16.TylerBM,TripathyS,ZhangX,DehalP,JiangRH,AertsA,

ArredondoFD,BaxterL,BensassonD,BeynonJLetal.:Phytophthoragenomesequencesuncoverevolutionaryoriginsandmechanismsofpathogenesis.Science2006,313:1261-1266.17.QutobD,Tedman-JonesJ,DongS,Ku?uK,PhamH,WangY,

DouD,KaleSD,ArredondoFD,TylerBMetal.:CopynumbervariationandtranscriptionalpolymorphismsofPhytophthorasojaeRXLReffectorgenesAvr1aandAvr3a.PLoSOne2009,4:e5066.18.JiangRH,TripathyS,GoversF,TylerBM:RXLReffector??reservoirintwoPhytophthoraspeciesisdominatedbya

singlerapidlyevolvingsuperfamilywithmorethan700members.ProcNatlAcadSciUSA2008,105:4874-4879.

Therapidexpansionanddiversi?cationofthe‘effectome’:http://wendang.chazidian.com