Genomics of biotrophy in fungi and oomycetes — emerging patterns
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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
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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
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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.
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