42SteeringSoilMicrobiomestoSuppressAbovegrou

OpinionSteeringSoilMicrobiomestoSuppressAbovegroundInsectPestsAnaPineda,1,*,@IanKaplan,2andT.MartijnBezemer1,3Soil-bornemicrobesaffectabovegroundherbivorousinsectsthroughacas-cadeofmolecularandchemicalchangesintheplant,butknowledgeofthesemicrobe–plant–insectinteractionsismostlylimitedtooneorafewmicrobialstrains.Yet,thesoilmicrobialcommunitycomprisesthousandsofuniquetaxainteractingincomplexnetworks,theso-called‘microbiome’,whichprovidesplantswithmultiplebeneficialfunctions.Therehasbeenlittleexplorationoftheroleandmanagementofwholemicrobiomesinplant–insectinteractions,call-ingfortheintegrationofthiscomplexityinaboveground–belowgroundresearch.Here,weproposeholisticapproachestoselectsoilmicrobiomesthatcanbeusedtoprotectplantsfromabovegroundattackers.MicrobesConferringImmunityinthePhytobiomeThelateentomologist,ThomasEisner,oncefamouslystated,‘BugsarenotgoingtoinherittheEarth.Theyownitnow’[1].However,inlightofon-goingdiscoveriesinmicrobialtaxonomyandecology,wecanprobablyaffirmthatinfact‘MicrobesowntheEarth’.Thecomplexnetworkofmicroorganismsinhabitinganarea(e.g.,soil,plant,oranimal),referredtoasthemicrobiome(seeGlossary),impartscrucialfunctionstoalllivingorganisms.Forinstance,thechemicaldefencesthatwerepreviouslyconsideredaninnategeneticfeatureofmanyanimalsandplantsareinfactproducedbymicrobialsymbionts[2,3]andweexpectmoreexamplestoberevealedinthenearfuture.Inhumans,immunityandevenbehaviorareinfluencedbytheintestinalmicrobiome[4,5].Interestingly,therhizosphere,athininterfacebetweenrootsandsoil,canbeconsideredtheplantequivalenttothehumanintestinaltract[6].Soilisthemajorsourceofmicrobes,whichdeterminetheplant-associatedmicrobiome[7].Soilmicrobesarenotonlycrucialforenhancingplantsurvival,growth,andtolerancetoabioticstress,butalsoinducesystemicresistanceagainstpathogensandinsectsbothaboveground[8–11]andbelowground[12].Thus,thesoilmicrobiomehasemergedasakeycomponentofplantimmunity[8,9,13],andshapeshowplantsinteractwiththeirabioticandbioticenvironments,intheso-called‘phytobiome’[14,15].Mostoftheworkonabovegroundplantdefence,sofar,focusesontheimpactofindividualmicrobialspeciesorstrains.ThisisincontrasttoDNA-sequencingtechniquesthatarerevealinganastonishingtaxonomicdiversityinsoils,notonlyintherhizosphere,butalsotheplantitself[7,16,17].Giventhatthebeneficialeffectsfortheplantareoftenprovidedbyaconsortiumofmicrobes[18],thereisanurgentneedforapproachesthatincorporatethewiderdiversitythatexistsinnatureintomicrobe-mediatedplantprotectionstrategies[19].ImpactofSoilMicrobiomesonAbovegroundHerbivoresEvidenceforhowbelowgroundmicrobialcommunities,asawhole,impactabovegroundinsectsisscarce;however,giventhetypicallystrongresponsestoonlyoneortwoTrendsSoilmicrobesareamajorsourceoftheplantmicrobiomeandrecentadvancesshowthattheyarekeycom-ponentsofplantresistanceagainstabovegroundattackers.However,mostofourknowledgeofhowbelowgroundmicrobesaffectabovegroundpestsislimitedtosinglestraineffects,callingforresearchthatincorporatesthefullpotentialoftheentiresoilmicrobiome.Soilmicrobiomescanbemanipulated,ashasbeendoneforcenturiesthroughagriculturalpracticessuchascroprotationortheuseofamend-ments.Conditionedsoilscanalsobetransplantedtorestoreecologicalfunctionsinotherecosystems.Theroleoftheplantinshapingsoilmicrobiomes[259_TD$DIFF]andinhowplantsrespondtothosemicrobiomescanbemaximizedbutweneedtoincreaseourmechanisticunderstandingatthegenetic,physiological,andecologicallevels.1DepartmentofTerrestrialEcology,NIOO-KNAW,Postbus50,6700ABWageningen,TheNetherlands2DepartmentofEntomology,PurdueUniversity,901W.StateStreet,WestLafayette,IN47907,USA3InstituteofBiology,SectionPlantEcologyandPhytochemistry,LeidenUniversity,POBox9505,2300,RALeiden,TheNetherlands@Twitter:@ana_pineda_*Correspondence:[e-mail](A.Pineda).TRPLSC1575No.ofPages9TrendsinPlantScience,MonthYear,Vol.xx,No.yy©2017ElsevierLtd.Allrightsreserved.TRPLSC1575No.ofPages9experimentallyaugmentedmicrobes,weanticipatethatthecommunity-wideeffectsaresubstantial.Soilmicrobiomescanimpactabovegroundinsectsindirectlythroughplant-medi-atedmechanisms,ordirectlythroughpathogenicormutualisticinteractions.Arecentstudyshowedthatincreasesinthepopulationofthespecialistfoliar-feedingaphidAphisjacobaeadependedonthecompositionofmicrobialcommunitiesinhabitingthesoilusedbyitshostplantragwort(Seneciojacobaea).Thesoilsmaintaineddifferentfungalcommunitiesthatinfluencedtheconcentrationofaminoacidsinthephloemsap,whichtheauthorsproposedinfluenced,inturn,theaphids[20].Similarly,inoculationofdistinctmicrobiomescollectedfromsoilswithdifferentplantspeciesalteredtheleafmetabolomeofarabidopsis(Arabidopsisthaliana)andresistanceoftheplanttothecaterpillarTrichoplusiani[21].Viaremovalofthemajorityofmicroorganismsusingafilterof0.45mm,thisstudyfurtherconfirmedthecontributionofthemicrobialcomponentofthesoil(insteadofthepresenceofchemicalcompoundsthatcouldpassthefilter)toplantperformance.Thesestudiesillustratethatexposuretoparticularmicrobiomesalterstheresistanceofplantstoabovegroundinsects