52Legacyoflandusehistorydeterminesreprogram

TheISMEJournal●AlexandreJousset3●WietsedeBoer2,4●VíctorJ.Carrión2●TaolinZhang1●XingxiangWang1,5●EikoE.Kuramae2Received:2April2018/Revised:25August2018/Accepted:4October2018©TheAuthor(s)2018.ThisarticleispublishedwithopenaccessAbstractMicroorganismsassociatedwithrootsarethoughttobepartoftheso-calledextendedplantphenotypeswithrolesintheacquisitionofnutrients,productionofgrowthhormones,anddefenseagainstdiseases.Sincethecropsselectivelyenrichmostrhizospheremicrobesoutofthebulksoil,wehypothesizedthatchangesinthecompositionofbulksoilcommunitiescausedbyagriculturalmanagementaffecttheextendedplantphenotype.Inthecurrentstudy,weperformedshotgunmetagenomesequencingoftherhizospheremicrobiomeofthepeanut(Arachishypogaea)andmetatranscriptomeanalysisoftherootsofpeanutplantsgrowninthesoilwithdifferentmanagementhistories,peanutmonocroppingandcroprotation.Wefoundthatthepastplantingrecordhadasignificanteffectontheassemblyofthemicrobialcommunityinthepeanutrhizosphere,indicatingasoilmemoryeffect.Monocroppingresultedinareductionoftherhizospheremicrobialdiversity,anenrichmentofseveralrarespecies,andareducedrepresentationoftraitsrelatedtoplantperformance,suchasnutrientsmetabolismandphytohormonebiosynthesis.Furthermore,peanutplantsinmonocroppedsoilexhibitedasignificantreductioningrowthcoincidingwithadown-regulationofgenesrelatedtohormoneproduction,mainlyauxinandcytokinin,andup-regulationofgenesrelatedtotheabscisicacid,salicylicacid,jasmonicacid,andethylenepathways.Thesefindingssuggestthatlandusehistoryaffectscroprhizospheremicrobiomesandplantphysiology.IntroductionSoilmicrobialcommunitiesarekeycontributorstohostnutri-tion,development,andimmunity[1–3].However,agriculturalpracticescandrivethecompositionofplant-associatedmicro-biomestoadapttheplanttobioticandabioticstresses[4].Ithasbeenshownthatapplicationofherbicides,pesticides,andtillagepracticescanleadtoshiftsintherhizospheremicrobialcommunitycompositions[5–9],withpossibleconsequencesforcropperformance[4,10,11].Inacomparisonofplantsgrowninmonoculturesandmixtures,itwasfoundthattheformerhadthelowestmicrobialdiversity[12].Yet,theeffectofcontinuousmonocroppingisnotnecessarilynegative,asnotexclusivelypathogensbutalsoantagonistsofpathogensmaybecomeenriched[13].However,ourunderstandingofhowfarmingpracticesaffecttherhizospherecommunityassemblyremainslimited.Therefore,itisessentialtohaveabetterunderstandingoftheroleofrhizospheremicrobiomesinthefunctioningofcrops[14,15].Plantsexude5–21%oftheirphotosyntheticallyfixedcarbonthroughtheroots[16].Therefore,therhizosphereisahotspotofmicrobialactivity,whereasthesurrounding*[e-mail]@issas.ac.cn1CASKeyLaboratoryofSoilEnvironmentandPollutionRemediation,InstituteofSoilScience,ChineseAcademyofSciences,Nanjing210008,China2DepartmentofMicrobialEcology,NetherlandsInstituteofEcology,NIOO-KNAW,Wageningen6708PB,TheNetherlands3InstituteforEnvironmentalBiology,Ecology&Biodiversity,UtrechtUniversity,Utrecht3584CH,TheNetherlands4SoilBiologyGroup,WageningenUniversity,Wageningen6708PB,TheNetherlands5ExperimentalStationofRedSoil,ChineseAcademyofSciences,Yingtan335211,ChinaElectronicsupplementarymaterialTheonlineversionofthisarticle()containssupplementarymaterial,whichisavailabletoauthorizedusers.1234567890();,:1234567890();,:bulksoilisdepletedineasilydegradableorganicmatter[17–20].Differentplantsspeciesselectfordifferentrhizo-spheremicrobialcommunitiesandthisislargelydeterminedbythecompositionofrhizodeposits[21,22].Forexample,theadditionofp-coumaricacid(arootexudatecomponent)tothesoilchangestheorganizationandcompositionofthebacterialrhizospherecommunitiesofcucumberseedlings[23].Inaddition,stableisotopeprobingstudiesindicatethatcarbonfixedbytheplantviaphotosynthesisisdirectlyincorporatedbyspecificbacterialtaxaintherhizosphere[24].Therefore,wehypothesizedthatrepeatedplantingofthesamecropinafieldwouldleadtoagradualenrichmentofaspeciessubsetinthecroprhizosphere.Theperformanceoftherhizospherecommunity,e.g.,nutrientacquisition,growthhormoneproductions,anddefenseagainstdiseases,isamajordeterminantoftheplantphenotype[25,26].Detailedinvestigationsoftheinterac-tionsbetweenplantsandmicroorganismshaverevealedthatplantscanrespondtorhizospheremicrobesindifferentways[27–31].Accordingtoarecentstudy,rootexudate-mediatedchangesintherhizospherecommunityofpeanut(Arachishypogaea)seedlingsstronglyinfluencethephy-siologyandfurtherdevelopmentofpeanutplants[32].Inthepresentstudy,weaimedtodecipherandlinktheimpactofthecroppinghistoryonthepeanutrhizospherecom-munityandtheresultingcropphenotype.Peanutplantsweregrowninsoilswithdifferentcroppinghistory(monocroppedorcroprotation).Themicrobiomeofthepeanutrhizospherewasthenassessedbyshotgunmeta-genomeanalysis,andplantresponseswereevaluatedbytranscriptomics.MaterialsandmethodsFieldtrialandtreatmentsFieldexperimentswereperformedatafieldstationoftheChineseAcad