Rhizosphere chemical dialogues plant–microbe interactions

根际 环境

Available online at http://www.77cn.com.cn

DayakarVBadri1,TiffanyLWeir1,DanielvanderLelie2andJorgeMVivanco1

Everyorganismonearthreliesonassociationswithits

neighborstosustainlife.Forexample,plantsformassociationswithneighboringplants,micro ora,andmicrofauna,whilehumansmaintainsymbioticassociationswithintestinal

microbial ora,whichisindispensablefornutrientassimilationanddevelopmentoftheinnateimmunesystem.Mostoftheseassociationsarefacilitatedbychemicalcuesexchanged

betweenthehostandthesymbionts.Intherhizosphere,whichincludesplantrootsandthesurroundingareaofsoilin uencedbytheroots,plantsexudechemicalstoeffectively

communicatewiththeirneighboringsoilorganisms.Herewereviewthecurrentliteraturepertainingtothechemicalcommunicationthatexistsbetweenplantsand

microorganismsandthebiologicalprocessestheysustain.

Addresses1

CenterforRhizosphereBiologyandDepartmentofHorticulture&LA,ColoradoStateUniversity,FortCollins,CO80523,USA2

BrookhavenNationalLaboratory,Upton,NY11973,USACorrespondingauthor:Vivanco,JorgeM(j.vivanco@colostate.edu)

Rhizospherechemicaldialogues:plant–microbeinteractions

andparasiticinteractionswithotherplants,pathogenicmicrobesandinvertebrateherbivores.Plantsreleaseenor-mousamountsofchemicalsthroughtheirroots,atasig-ni cantcarboncost,tocombatpathogenicmicroorganismsandattractbene cialones.Rhizosphereinteractionsareaffectedbymanydifferentregulatorysignals,ofwhichonlyafewhavebeenidenti ed,recallingaquotebyLeonardodaVincithat‘Weknowbetterthemechanicsofcelestialbodiesthanthefunctioningofthesoilbelowourfeet’[2].Rhizosphereinteractionsarenotsolelydrivenbyrootsbutarehighlyintegratedwithandin uencedbyresidingorganismsandlocaledaphicfactors.Soil-inhabitingmutualistsandparasites,bothprokaryoticandeukaryotic,areactivelyinvolvedinsignalingwithahost(Figure1).Therefore,rhizosphereinteractionsareverydynamicandcanbealteredbyadditionorlossofanyoftheplayers.Alargebodyofliteratureexistsaboutrhizosphereinter-actions[3–5].Inthisreview,wesummarizethecurrentknowledgeofrhizospherechemicalcommunicationbe-tweenplantrootsandtheirassociatedmicroorganisms.Centraltothisdiscussionistherecentprogressmadeinunderstandingrhizospherechemicaldialoguesbetweenplantsanddifferentcomponentsofthemicrobialcom-munity.Weendwithadiscussionofhowthesechemicaldialoguesmayimproveplant tnessatthecommunitylevelanddiscussthenewchallengesfacedbyresearchers.

CurrentOpinioninBiotechnology2009,20:642–650ThisreviewcomesfromathemedissueonChemicalbiotechnology

EditedbyKazuyaWatanabeandGeorgeBennettAvailableonline28thOctober20090958-1669/$–seefrontmatter

#2009ElsevierLtd.Allrightsreserved.DOI10.1016/j.copbio.2009.09.014

Chemicalsignalingbetweenplantsandmutualists

Plantrootsreleaseawiderangeofcompoundsthatareinvolvedinattractingbene cialorganismsandformingmutualisticassociationsintherhizosphere.Thesecom-poundsincludesugars,polysaccharides,aminoacids,aromaticacids,aliphaticacids,fattyacids,sterols,phe-nolics,enzymes,proteins,plantgrowthregulatorsandsecondarymetabolites.Themostimportantrhizospheremutualismsdescribedarebetweenplantsandmycorrhi-zaeorrhizobacteria.

Mycorrhizalassociationsarepresentinalmostalllandplantsandareessentialbiologicalconstituentsoftherhizo-sphere.Mycorrhizaearegroupedintotwocategories:endomycorrhizae(arbuscular,AM)andectomycorrhizae.TheAMsymbiosisrepresentsthemostwidespreadandancientplantsymbioses,originatingabout450millionyearsago[6].About6000speciesintheGlomeromycotina,AscomycotinaandBasidiomycotinafamilieshavebeenrecordedasmycorrhizalandwithmoresensitivemoleculartechniquesthisnumberisincreasing[7].Similarly,more

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Introduction

Prokaryotesandeukaryoteshavecoexistedformillionsofyearsonearth.Itisestimatedthathumanshave1013humancellsand1014bacterialcellsincludingtheendogen-ousbacterial ora[1].Asaresultofthislongassociation,prokaryoteshavedevelopedbothbene cialanddetrimen-talrelationshipswitheukaryotes.Asautotrophicorgan-isms,plantsplayacentralroleinsustainingallotherlifeforms.Unlikemammals,plantsaresessile,thusreleasinganarrayofchemicalsignalstointeractwithotherorgan-isms.Therootsystem,whichwastraditionallythoughttoprovideanchorageanduptakeofnutrientsandwater,isachemicalfactorythatmediatesnumerousundergroundinteractions.Theseincludemutualisticassociationswithbene cialmicrobes,suchasrhizobia,mycorrhizae,endo-phytesandplant-growthpromotingrhizobactertia(PGPR)

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Rhizospherechemicaldialogues:plant–microbeinteractionsBadrietal.643

than200000plantspecieshostmycorrhizalfungi,butarelativelysmallnumberofmycorrhizaltypesareknown[8].Thebiotrophicinterfacesthatareformedbetweenplantrootsandthefungusresultfromrecognitionofexchangedcues.ThereisanextensivelistofplantgenesthatarepredictedtoplayaroleinfacilitatingAMinteractions[9 ,10 ],butcomparativelyfewidenti edinthefungus[11 ,12].Thuslittleknowledgeexistsaboutsignalingprocessesbetweensymbionts,thepathwaysrelatedtosymbiosis-speci cdevelopmentofAMfungiinroottis-sues,ormechanismsofnutrientexchangebetweenthem[12,13,14,15 ].

TheestablishmentofAMsymbiosesbeginswiththecolonizationofacompatiblerootbyhyphaeproducedbyAMfungalsoilpropagules,asexualsporesormycorrhizalroots.Thisisfollowedbyappressoriumformationandentranceintothecortextoformspecializedstructurescalledarbuscles.Beforecolonization,itisassumedthatacontinuousdialogueofsignalsisexchangedbetweenthesymbiontstoestablishcolonization.Sincethissymbiosislackshostspeci cityithasbeensuggestedthateithertheplant-derivedsignalsareconservedthroughouttheplantkingdomorthatabroadrangeofrelatedcompoundsareinvolved.Plant-releasedcompoundslikesugarsandaminoacidsarepotentialfungalstimulibutphenoliccompounds,particularly avonoids,areknownaskeysignalingcom-ponentsinmanyplant–microbeinteractions[16 ].Therearevastquantitiesofdataontheeffectof avonoidsonAMhyphalgrowth,differentiation,androotcolonization[16 ],andspeci ceffectsdependonthechemicalstructureofthecompound[17].Itwasrecentlyfoundthat avonoidsexhibitagenus-speci candspecies-speci ceffectonAMfungi[18].Inaddition,strigolactones,agroupofsesquiterpenelactonesexudedbyLotusjaponicusroots,wereshowntoinducehyphalbranchinginAMfungi,apre-requisiteforsuccessfulrootcolonizationfungi[19 ].Strigalactonespresentintherootexudatesofawiderangeofplantsactdisplayspeci cityassignalsforAMfungibutdidnotaffectotherfungalspeciessuchasTrichoderma,Piriformospora,BotrytiscinereaandCladosporiumsp.[19 ].AfurtherhypothesisisthatstrigolactonesarenotonlyinvolvedininducingAMhyphalbranchingfactorbutalsoacttoattractAMfungitoroots[20].However,morestudiesareneededtoclarifyboththespeci cityandrolesofstrigolactonesinestablishingmycorrhizalassociations.Theproductionandexudationofstrigolactonesarede-pendentonnutrientavailability.Recently,Yoneyamaetal.[21]reportedthatnitrogenandphosphorusde ciencyenhancedthesecretionofastrigolactone,5-deoxysatrigolinsorghumplants.Besidesstrigolactones,somestudiesdemonstratethatcalciumionsareanintracellularmessen-gerduringmycorrhizalsignaling,atleastinapre-contactstage[22 ].

Evenlessunderstoodthanthesignalingbetweenplantsandmycorrhizaeistheinteractionofmycorrhizaewith

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othersoilmicrobes.IthasbeendemonstratedthatAMfungalexudatesdirectlyimpactsoilbacterialcommunitycomposition[23],andsomebacteriaassociatedwithAMcanimprovecolonization,rootbranchingandantifungalproperties[7,24].Futuregoalsshouldincludeidentifyingallplayersofthesesignalingnetworks,particularlythesignalsandreceptorsthatopenthedoortosymbiosisformation.Othermajorchallengesincludeunravelingthesignalingeventsintri-partiteinteractions(plant–AM–bacteria)tobetterunderstandhowsoilbacteriaandAMfungiassociate.Although,somestructuralpropertiesthatregulateinterspeciesinteractionsareknown[25 ]thebacterial–mycorrhizalnetworkstillremainstobeeluci-dated.

Asmentioned, avonoidsplayakeyroleintheearlysignalingeventsoflegume–rhizobiainteractions[26].Thelegumerhizospherechemicallyattractsrhizobiabysecreting avonoidsandrelatedcompounds[27].Sub-sequently,theNodDproteinofrhizobiaperceivesspeci c avonoidsthroughoneortwo-componentregu-latorysystems,initiatingtranscriptionofnodgenesthatencodethebiosyntheticmachineryforabacterialsignal,theNodfactor.Nodfactorsarelipochitooligosaccharidesconsistingofb-1,4-linkedN-acetyl-glucosamineback-boneswithfouror veresidueswithanacylchainatC2inthenon-reducingendanddecoratedwithacetyl,sulfonyl,carbamoyl,fucosylorarabinosylmoietiesatde nedpos-itionsdependingontherhizobialstrain[28].PerceptionoftheNodfactorsbytheplantinducesmultiplesignalingpathwaysthatinitiateroothairinfectionandnoduleformation.Thereareothernon avonoidrelatedcom-poundslikexanthones,vanillinandisovanillinthatinduceNodDgeneexpression,buttheyarerequiredatmuchhigherconcentrationsthan avonoids[29 ],andthustheirimportanceinnaturalenvironmentsisques-tionable.Recently,Caietal.[30 ]reportedthatcanava-nine,acompoundpresentintheseedcoatandrootexudatesofvariouslegumeplants,istoxictomanysoilbacteriabutnottorhizobialstrainsthatpossessspeci ctransportertotransport(detoxify)thiscompound.Theyalsosuggestedthathostlegumessecretecanavanineintotherhizospheretoselectbene cialrhizobia.Furtherstudiesarewarrantedtoidentifyfactorsdetermininghost–rhizobiumspeci city.

Molecularcommunicationbetweenhostandpathogens

Therearefourmaingroupsofplantpathogens[31]butonlytwoofthemaremajorplayersinthesoil;http://www.77cn.com.cnparativelyfewerbacteriaareconsideredtobesoilborneplantpathogens;however,somewell-studiedexceptionsincludeRalstoniasolanacearum(bac-terialwiltoftomato)andAgrobacteriumtumefaciens,thecasualagentofcrowngalldisease[32,33].Fungiandoomycetes,physiologicallyandmorphologicallysimilarbutphylogeneticallydistinctgroupsoforganisms,arethe

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Figure

1

Pictorialillustrationofthechemicalcommunicationthatexistsbetweenplantrootsandotherorganismsinthecomplexrhizosphere.Plantrootssecreteawiderangeofcompounds,amongthosesugarsandaminoacidsareengagedinattracting(chemotaxis)microbes(1),flavonoidsactassignalingmoleculestoinitiateinteractionswithmycorrhiza(AMfungi)(2),rhizobium(3)andpathogenicfungi(oomycetes)(4),aliphaticacids(e.g.malicacid)areinvolvedinrecruitingspecificplantgrowthpromotingrhizobacteria(Bacillussubtilis)(5),nematodessecretegrowthregulators(cytokinins)thatareinvolvedinestablishingfeedingsitesinplantroots(6)andnematodessecreteothercompounds(organicacids,aminoacidsandsugars)involvedinattractingbacteriaandinbacterialquorumsensing(7).Knowledgeoftherolesofothertypesofcompounds,suchasfattyacids(8)andproteins(9),secretedbyrootsintherhizosphereandothermulti-partiteinteractions(10)remainsunknown.

mostpredominantsoilbornepathogens.Likeplant–mutualistassociations,pathogensalsoutilizechemicalsignalsinearlystepsofhostrecognitionandinfection.Beforetheestablishmentofinfection,Phytophthorasojaezoosporesarechemicallyattractedbydaidzeinandgen-isteinsecretedbysoybean[34];however,thenatureoftheiso avonereceptoronthezoosporesremainsunknown.Mostplantsproduceantimicrobialsecondarymetabolites,eitheraspartoftheirnormalprogramofgrowthanddevelopmentorinresponsetopathogen

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attackandthoseantimicrobialcompoundsprotectplantsfromawiderangeofpathogens[35].Preformedanti-fungalcompounds,calledphytoanticipins,occurconsti-tutivelyinhealthyplantsandactaschemicalbarriersforfungalpathogens.Bycontrast,phytoalexinsareantimi-crobialcompoundsinducedinresponsetopathogenattackbutnotnormallypresentinhealthyplants.Thesetwogroupsofcompoundshaveprovenveryeffectiveforawiderangeoffungalpathogens.However,moststudiespertainingtothesecompoundswereconductedinleaves,

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Rhizospherechemicaldialogues:plant–microbeinteractionsBadrietal.645

notintherootsorintherhizosphere.Recently,Bednareketal.[36]reportedthatArabidopsisrootsandleavesdiffergreatlyintheaccumulationofindolicandphenylpropa-noidcompoundsuponinfectionwithPythiumsylvaticum.Onthebasisofthisreport,onecanhypothesizethattheliteraturepertainingtothephytoalexinandphytoantici-pinresponsesafterleafinfectionswilldifferfromrootinfectionstudies.Followingthisobservation,Badrietal.[37]reportedthatdifferentialgenome-wideexpressionpro lesinrootsupontheindependentadditionofthreeimportantplantsignalingmolecules(SA,MeJAandNO)totherootsandthatthesepro lesweredifferentthanthosefromleavestreatedwiththesamesignalingmol-eculesdescribedintheliterature.Thereisaneedtobetterunderstandhowphytoalexins,phytoanticipinsandothersecondarymetabolitesacttoinhibitrootfungalpathogens.Thedevelopmentofarice–Magnaporthegrisea(causalagentofblastdisease)pathosystemwouldbeparticularlyusefulasthisfungalpathogeniscapableofinfectingbothleavesandrootsofriceplants[38 ].Inaddition,thissystemwouldallowustoidentifyiftheroleofphytoalexinsorphytoanticipinsinvolvedinplantdefenseagainstthisfungalpathogenontheleavesisthesameasinroots.Furtherresearchiswarrantedonsoilbornefungalpathogensbecausetheycauseacon-siderableyieldlosstocropscomparedwithfoliarpatho-gens[39 ].

Nematodesarecomplex,worm-likeeukaryoticinvert-ebratesthatrankamongthemostnumerousanimalsontheplanet[40].Mostnematodesinsoilarefreeliving,andconsumebacteria,fungiandothernematodes,butsomecanparasitizeplants.Themajorityofcropdamageiscausedbybothroot-knotnematodes(RKN)andcystnematodes[41].Itisgenerallythoughtthatnematodesperceivetheirenvironmentthroughchemosensoryper-ception.Typically,RKNmustlocateandpenetratearoot,migrateintothevascularcylinderandestablishaperma-nentfeedingsite.Theseeventsareaccompaniedbyextensivesignalingbetweenthenematodeandthehost,andarewelldescribedatthelevelofidentifyingproteinsthataresecretedbynematodesduringthemigratoryphase[41,42].However,theidenti cationofinitialsig-nalingmolecules(non-proteinsignalingcompounds)releasedfromthehosttoattractnematodesisstillataprimitivestage.Nematodeswithawidehostrangerespondtoroot-releasedcompounds/diffusatesfromawiderangeofhosts,whereasspecieswitharestrictedhostrangehatchonlywhenpresentedwithsignalsfromthathost[43].Recently,Horiuchietal.[44 ]reportedthatMedicagorootsreleasedavolatile(dimethylsul de)thatattractednematodes(C.elegans),whichactedasvectorsforrhizobiaandeffectivelyenhancednodulation.How-ever,detailedinformationaboutthereciprocalinitialsignalexchangebetweennematodesandhostislackingwiththeexceptionoftheroleofcytokininsinhost–nematoderelationships[45 ].Thenematodessecrete

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cytokininsthatplayaroleincellcycleactivationandinestablishingthefeedingsiteasanutrientsinkinthehostroots.Anotherrecentstudydemonstratedthathownematodesecretions(non-proteinaceouscompounds)interactwithsoil-inhabitingbacteria[46 ]byusingthemodelnematodeCaenorhabditiselegans.Thisstudywillopenanewavenueofresearchtostudythechemicalinteractionsofotherparasiticnematodeswiththeirhosts.

Quorumsensing(QS)andrhizospherecommunication

TheexquisitelycoordinatedgeneexpressionthatresultedinproductionofbioluminescentproteinsbythemarinebacteriaVibrio scheriiwasonceconsideredaninterestingnovelty,anditwasseveralyearsbeforethescienti cimportanceofthisdiscoverywasrealized.Ithasnowbeendeterminedthatcoordinatedactivityamongmicrobialcellsusingdiffusiblechemicalsignalsisawide-spreadphenomenon,called‘quorumsensing’or‘cell-tocellcommunication’.AlthoughthechemicalsignalsandmechanismsofQSsystemsvary,themostprevalentformofQSsignalsusedbyplant-associatedbacteriaareacylhomoserinelactones(AHLs),whichvaryinthelength,oxidationstate,anddegreeofsaturationoftheiracylsidechainstoprovideadegreeofspeciesspeci city.Atthresholdconcentrations,theseAHLsformcomplexeswiththeircognatereceptors,whichbindtoDNAandacttoregulateexpressionofspeci cgenes,effectivelyallow-ingpopulationsofindividualcellstoactasacollectiveunit.Thisisasimpli edexplanationasincreasingevi-dencesuggeststhatsignalconcentrationalonedoesnotdictatetheactivationorrepressionofQS-controlledgenes,butthatlocalenvironmentandspatialdistributionofcellsarealsoimportantcontributingfactors[47,48 ].Thebehaviorsthatarein uencedbyQSareextremelyvariedbutfromabroaderecologicalperspectivetheyfacilitatenutrientornicheacquisition,modulatecollec-tivedefenseagainstcompetitors,andpermitcommunityescapeinthefaceofpopulationdestruction[49].Inplant-associatedbacteria,QSisofteninvolvedinestablishingsuccessfulassociations,whethertheyaresymbioticorpathogenic.TheroleofQSinthepathogenesisofErwiniacarotovoraandAgrobacteriumtumefaciensontheirrespect-iveplanthostsarewellcharacterized.TheentericphytopathogenE.carotovraproducesanumberofQS-regulatedvirulencefactors,suchaspectinases,cellu-lasesandproteasesandsomestrainsproduceab-lactamantibioticthatisthoughttoprovidenicheprotectiontoE.carotovoraonceithasestablishedaninfection[50].However,whetherplantfactorsareinvolvedinestablish-ingorinhibitingQStodeterminehostspeci cityofE.carotovoraisunknown.

Conversely,ithasbeenestablishedthatchemicalsfromtheplanthostcontributetoinfectionbythetumor-inducingbacteriaA.tumefaciens.Thesignal-receptorpair

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(TraI/TraR)responsibleforregulationofQSinA.tume-faciensoccursontheTi(ortumor-inducing)plasmid,whichisrequiredforgallformationinhostplants.Aninfectionoccurswhenasegmentofthisplasmidisinte-gratedintothenucleusofhostplantcells,resultingintheproductionofopinesthatcanthenbeutilizedasanovelsourceofnitrogenandcarbon[51].Thepresenceofopines,whichareonlyfoundintheplanttumor,thenupregulateexpressionofthebacterialTraRgene.Thus,theQSsystem,whichallowsforconjugationandreplica-tionoftheTiplasmid,isonlyeffectivelyactivatedafterinfection,resultinginaquestionableroleforQSinA.tumefacienspathogenicity[52].Tocomplicatematters,A.tumefaciensalsoproducesaproteinBlcC(formerlyAttM)thathaslactonaseactivity,whichitwassuggestedmaynegativelyregulateQSthroughsignaldegradation[53,54],aphenomenoncalled‘quorumquenching’.Anotherstudyshowedthatthepresenceoftheplantdefensemetabolitesalicylicacidresultedinincreasedexpressionofthislactonaseandinhibitionofvirulence(vir)genescarriedontheTiplasmid[55].However,thebiologicalsigni canceofthisplant-inducedlactonasetoactasaquorumquencherwasnotsubstantiatedbyinplantadataandappearstohaveonlyatransienteffect[56 ].

Quorumsensinghasalsobeenimplicatedasanimportantfactorinthesymbioticassociationbetweenlegumesandrhizobia,althoughmanydetailsofitsinvolvementarestillemerging.ManyrhizobiadisplayingmutationsoftheirQSsystemshavereducedabilitytoinfectroothairsand/orformnodules[57–59].Additionally,severallegumeshavebeenshowntosecretecompoundsthatcaninterferewithbacterialQS[60,61,62 ],andMedicagotruncatularespondeddifferentiallywithregardstorootexudationandproteinexpressiontoAHLsproducedbyitssymbiontSinorhizobiummelilotiandanopportunisticpathogenPseu-domonasaeruginosa[63].However,amongtheplant-pro-ducedQSagonistsandantagoniststhatmayplayaroleinlegume/rhizobiainteractions,theonlyonethathaschemicallyidenti edisL-Canavanine,anarginineanalog[62 ];thus,ithasbeenpredictedthattheobservedQSinhibitionmaybeanindirecteffectpotentiallycausedbyproteinmisfoldingoftranscriptionregulators[59].

seemtobequitepromiscuouswhenitcomestohostplantcolonizationandplantbene cialeffects,suchastheBurkholderiacepaciaBu72,whichwasisolatedfromyellowlupine[68]butalsosigni cantlyimprovedbiomasspro-ductionofpoplarDN-34[67,69].Therefore,beforeapplyingplantgrowthpromotingendophyticbacteriapreliminarystudiestocon rmtheplantgrowthpromot-ingsynergyoftheselectedendophytesandtheplantspeciesarerequired.

Acloserelationshipexistsbetweenendophyticandrhizo-spherebacteriaandmanyfacultativeendophyticbacteriacanalsosurviveintherhizosphere,wheretheycanentertheirhostplantviatheroots.Rootcolonizationbyrhizo-spherebacteriainvolvesseveralstages[70]andendophy-ticbacteriaarehypothesizedtofollowasimilarprocess.Intheinitialstage,bacteriamovetotheplantrootseitherpassivelyviasoilwater uxesoractivelyviaspeci cinductionof agellaractivitybyplant-releasedcom-pounds.Inasecondstep,non-speci cadsorptionofbacteriatotherootstakesplace,followedbyanchoring(thirdstep),andresultinginthe rmattachmentofbacteriatotherootsurface.Speci corcomplexinter-actionsbetweenthebacteriumandthehostplant,in-cludingthesecretionofrootexudates,mayarisethatcanresultintheinductionofbacterialgeneexpression(fourthstep).Endophyticbacteriacansubsequently( fthstep)entertheirhostplantatsitesoftissuedamage,whichnaturallyariseastheresultofplantgrowth(lateralrootformation),orthroughroothairsandatepidermalcon-junctions[71].Inaddition,plantexudatesleakingthroughthesewoundsprovideanutrientsourceforthecolonizingbacteria.

Endophyticbacteriacanimproveplantgrowthandde-velopmentinadirectorindirectway.Directplantgrowthpromotingmechanismsofendophyticbacteriamayinvolvenitrogen xation[65,72],theproductionofplantgrowthregulatorssuchasauxins,cytokininsandgibber-ellins[73–75],suppressionoftheproductionofstressethyleneby1-aminocyclopropane-1-carboxylate(ACC)deaminaseactivity[76,77],andalterationofsugarsensingmechanismsinplants[78].Forinstance,alterationofbiosynthesisand/ormetabolismoftrehaloseinplantahavebeenshowntoincreasetolerancetodrought,saltandcold[79].Itisthereforenoteworthythatseveralendophyticbacteriafrom,forexample,poplarwereabletoef cientlymetabolizetrehalose[67].Endophyticbac-teriacanalsoindirectlybene tplantgrowthbyprevent-ingthegrowthoractivityofplantpathogensthroughcompetitionforspaceandnutrients[80],antibiosis[81],productionofhydrolyticenzymes[82],inhibitionofpathogen-producedenzymesortoxins[83]andthroughinductionofplantdefensemechanisms[84].

Asystemsbiologyapproachtobetterunderstandthesynergisticinteractionsbetweenplantsandtheirbene cial

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Endophytesaschemicalfactories

Inadditiontointeractingwithmicroorganismsintherhizosphere,plantsareinternallycolonizedbyendophyticbacteriaandfungi.Endophyticbacteriacanbede nedasbacteriathatresidewithinlivingplanttissuewithoutcausingsubstantiveharmtotheirhost.Diversearraysofbacterialgenerahavebeenreportedtobeendophytic[64,65].Thecommunitystructureofendophyticbacteriawasshowntobestronglyaffectedbytheplantspecies,uptothelevelofthecultivar[66],pointingtospecies-speci cassociationsbetweenendophytesandtheirplanthost[67].Onthecontrary,someendophyticbacteria

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endophyticbacteriarepresentsanimportant eldofresearch,whichisfacilitatedbytherecentsequencingofthegenomesofseveralplantspeciesandseveralendo-phyticbacteria.Forinstance,thegenomecomparisonbetweenthepoplarendophyteS.maltophiliaR551-3andtheopportunisticpathogenK279apointedtotheexistenceofinsertionhotspotsinthecoregenomeofthisspecies[85].ThemechanismsresponsibleforcolonizingplantsandforantagonisticactivityofS.maltophiliastrainsagainstplantpathogensseemsimilartothoseresponsibleforcoloniza-tionofhumantissuesandforpathogenicity.Furthermore,antibioticresistanceandsynthesiswasfoundtobepartofthecoregenome.Therefore,theapplicationofrhizo-sphericandendophyticbacteria,suchasS.maltophiliaorB.cepacia,tocontrolplantpathogensorpromoteplanthealthshouldbeverycarefullyconsidered,astheymayhavepotentialasopportunisticpathogens.FB17butnototherBacillussp.Thissuggeststhateachbene cialrhizobacterianeedsaspeci csignaltocolonizethehost.AllPGPRshaveindirectpositiveeffectsonplanthealthbyinhibitingsoilbornepathogensbymeansofcompetitionandantibiosis[39].PGPRsalsohavedirectpositiveeffectsonplanthealthbyinducingsystemicresistance(ISR)inordertopreparetheplantsfrompathogenattackorbyexposingtheplantstoPGPR-releasedcompoundssuchas2,3-butanediol,pyoverdine,andlipopeptidesurfactants[39 ].However,mostexper-imentsexaminingthemechanismsofPGPRsdealwithonlyasinglehost–singlePGPRinteraction.Innature,therhizospherecontainsmillionsofmicrobesincludingPGPR,pathogensandmicrofauna.Furtherstudiesareneededtounravelthesemultiplexinteractionsatamol-ecularleveltoenhancetheirutilizationforagriculturalbene ts.

Rhizoremediation

Plant-assistedbioremediationorphytoremediationholdspromiseforinsitutreatmentofpollutedsoils.Thegeneralsubjectofphytoremediationhasbeenreviewedbynumerousjournalarticlesandbookchapters,andaspectsspeci ctotherhizosphereareincluded.ArecentreviewarticlebyWenzel[86]comprehensivelycoverstherhi-zopshereprocessesandmanagementinplant-assistedbioremediationofsoils;therefore,anextensivediscussionisnotwarrantedhere.However,itisveryclearthattheunderstandingoftheplant–microbialconsortiaintherhizospherewillenhanceourabilitytoengineerplantsforphytoremediationpurposesveryeffectivelyasdescribedbyDzantor[87]andRyanetal.[88].Furtheremphasisshouldbeputonevaluatingresultsobtainedfromsimpli edlabexperimentstoheterogenousnaturalconditionsundersuchascomplexrhizosphereenviron-ments(multipleplants–multiplemicrobes).

Noveltritrophicinteractions

Rootsecretedcompoundsarealsobeingstudiedfortheirinvolvementintritropicinteractions(plant–microbe–nematode)intherhizosphere.Onlyafewexamplesarewelldocumentedinthislineofresearch[3],suchasplant–AMF–parasiticweedinteractions[92],legume–nematode–rhizobiumassociations[44],andtheattractionofentomopathogenicnematodestoinsectdamagedroots[93].Alltheseinteractionsarestudiedatlaboratorylevelsbyusingsimpli edmodelsystemsbuttheknowledgeabouthowtheseinteractionsmightoccureffectivelyinthecomplexrhizosphereundernaturalconditionsstillremainsscarce.

Canproteinsintheexudatesbechemicalsignals?

Whilethereisabundantinformationontheroleofrootsecretedsecondarymetabolitesinrhizosphereplant–microbeinteractions,theroleofexudedproteinsispoorlystudied.Recentevidencedemonstratesthatmicrobescanmodulaterootexudationofproteinsandthatplantscandothesameinsoilbacteria[94].Thesereportscon rmthatthecompositionofproteinsexudedbyplantrootsisdynamicallyeffectedbytheorganismsintheirsurround-ings.ArecentreviewbyMathesius[95 ]discussedtheuseofproteomicstostudyroot–microbeinteractions.Mostoftheconclusionsreachedtodatearebasedonresultsobtainedfromsimplelaboratoryexperimentalmodels.Someofthesecretedproteinsarestartingtobeidenti edbutnothing(almost)isknownabouthowthesesecretedproteinsfromdifferentorganismsinteractatinterspecies/inter-genericlevelsorwhateffecttheyhaveonotherorganismsintherhizosphere.Mostimportantly,researchneedstobeconductedtodetermineiftheproteinsretaintheirenzymaticactivitiesintherhizosphere.

PGPRsinteractionwithplantroots

Therhizosphereistheplaygroundandinfectioncourtforsoilbornepathogensandalsoabattle eld,wherebothmicro oraandmicrofaunainteractwithsoilbornepatho-gensandin uencetheoutcomeofpathogeninfection[39].However,severalbene cialmicroorganismsthatresideintherhizospherecaninhibitthegrowthandactivityofsoilbornepathogens.Theactivityandeffectsofbene cialrhizospheremicroorganismsonplantgrowthandhealtharewelldocumentedforbacterialikePseudo-monas,BurkholderiaandfungilikeTrichodermaandGliocladium.Similartotheinvolvementof avonoidsinlegume–rhizobiasignaling,root-secretedcompounds(both avonoidsandothersecretedcompounds)modu-latetheinteractionbetweenplantsandPGPRsandtheseinteractionsarereviewedbyseveralarticles[3,5,89,90].But,thespeci croot-releasedsignalinrecruitingspeci cbacteriaspeciesispoorlyunderstood.Recentevidence[91]demonstratedthatL-malicacidsecretedfromplantrootsisinvolvedinspeci callyrecruitingBacillussubitilis

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Futurechallenges

Rhizospherechemicaldialoguesarethelanguageofcommunicationbetweenplantrootsandmicrobesin

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648Chemicalbiotechnology

theareawherethesoilandrootsareincloseproximity.Severallinesofevidenceimplicateroot-secretedexu-datesassignalingagentsthatplayakeyroleintheseinteractions.Researchershavealreadyidenti edsomeofthefactorsinitiatingthedialoguesintherhizospherethatdrivetheseinteractions.However,therearestillnumer-ousotherfactors/determinantsyettobeidenti edtobetterunderstandtheseinteractionsatanecologicallevel.Therhizosphereisconsideredtobecommongroundforecologists,molecularbiologistsandplantbiologiststofurtherexplorethesenovelinteractionsoccurringinthiscomplexzone.Recenttechnologyde-velopmentintheareasof‘omics’suchasproteomics,metabolomics,transcriptomicsandsecretomicsallowustofurtherunderpintheseinteractionsef cientlyforagriculturalbene t.Acombinationofdataanalysesobtainedfromthese‘omics’studieswillfurtherstrengthenourcapabilitytovisualizeacompletepictureofthesecomplexmulti-speciesinteractions.

DetailedgeneexpressionanalysisofAMinfectedrootsduringthedevelopmentoftheprepenetrationapparatus.

11.SeddasPMA,AriasCM,ArnouldC,vanTuinenD,GodfroyO, BenhassouHA,GouzyJ,MorandiD,DessaintF,Gianinazzi-PearsonV:Symbiosis-relatedplantgenesmodulatemolecular

responsesinanarbuscularmycorrhizalfungusduringearlyrootinteractions.MolPlant–MicrobeInteract2009,22:341-351.StudyexplainshowthesymbiosisrelatedplantgenesmodulateAMfungigeneexpressionpro lesinearlyrootinteractions.

12.BalestriniR,LanfrancoL:Fungalandplantgeneexpression

inarbuscularmycorrhzalsymbiosis.Mycorrhiza2006,16:509-524.13.Gianinazzi-PearsonV,Sejalon-DelmasN,GenreA,JeandrozS,

BonfanteP:Plantsandarbuscularmycorrhizalfungi:cuesandcommunicationintheearlystepsofsymbioticinteractions.AdvBotRes2007,46:181-219.14.KrajinskiF,FrenzelA:TowardstheelucidationofAM-speci c

transcriptioninMedicagotruncatula.Phytochemistry2007,68:75-81.15.RequenaN,SerranoE,OconA,BreuningerM:Plantsignalsand fungalperceptionduringarbuscularmycorrhiza

establishment.Phytochemistry2007,68:33-40.

Comprehensivereviewabouthowtheplantroot-secretedcompoundsareinvolvedinAMfungalinitiationandestablishment.

16.SteinkellnerS,LendzemoV,LangerI,SchweigerP,KhaosaadT, ToussaintJ-P,VierheiligH:Flavonoidsandstrigolactonesin

rootexudatesassignalsinsymbioticandpathogenicplant–fungusinteractions.Molecules2007,12:1290-1306.

Comprehensivereviewabouttheroleof avonoidsandstrigolactonesassignalmoleculesforsymbioticandpathogenicinteractions.

17.ScervinoJM,PonceMA,Erra-BasselsR,VierheiligH,OcampoJA,

GodeasA:GlycosidationofapigeninresultsinalossofactivityondifferentgrowthparametersofarbuscularmycorrhizalfungifromthegenusGlomusandGigaspora.SoilBiolBiochem2006,38:2919-2922.18.ScervinoJM,PonceMA,Erra-BasselsR,VierheiligH,OcampoJA,

GodeasA:Flavonoidsexhibitfungalspeciesandgenus

speci ceffectsonthepresymbioticgrowthofGigasporaandGlomus.MycolRes2005,109:789-794.19.AkiyamaK,MatsuzakiK,HayashiY:Plantsesquiterpenes inducehyphalbranchinginarbuscularmycorrhizalfungi.

Nature2005,435:824-827.

FirststudydemonstratedexperimentallythatstrigolactonesinducehyphalbranchinginAMfungi.

20.SbranaCM,GiovannettiM:Chemotropisminthearbuscular

mycorrhizalfungusGlomusmosseae.Mycorrhiza2005,15:539-545.21.YoneyamaK,XieX,KusumotoD,SekimotoH,SugimotoY,

TakeuchiY,YoneyamaK:Nitrogende ciencywewellasphophorusde ciencyinsorghumpromotestheproductionandexudationof5-deoxystrigol,thehostrecognitionsignalforarbuscularmycorrhizalfungiandrootparasites.Planta2007,227:125-132.22.NavazioL,MoscatielloR,GenreA,NoveroM,BaldanB, BonfanteP,MarianiP:Adiffusiblesignalfromarbuscular

mycorrhizalfungielicitsatransientcytosoliccalcium

elevationinhostplantcells.PlantPhysiol2007,144:673-681.Provides rstexperimentalproofthatcytosoliccalciumelevationinthehostcellsbydiffusibleAMfactors.

23.TolijanderJF,LindahlBD,PaulLR,ElfstrandM,FinlayRD:

In uenceofarbuscularmycorrhizalmycelialexudatesonsoilbacterialgrowthandcommunitystructure.FEMSMicrobiolEcol2007,61:295-304.24.HartmannA,SchmidM,vanTuinenD,BergG:Plant-driven

selectionofmicrobes.PlantSoil2009,321:235-257.25.LittleAE,RobinsonCJ,PetersonCB,RaffaKF,HandelsmannJ: Rulesofengagement:interspeciesinteractionsthatregulate

microbialcommunities.AnnuRevMicrobiol2008,62:375-401.Discussesworkingde nitionsofcentralecologicalthemesandalsoreviewsthestatusattheinterfacebetweenevolutionaryandecologicalstudy.

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Acknowledgements

TheworkinJMVlaboratorywassupportedbytheNationalSciencefoundation(MCB-0542642)andUSdepartmentofDefenseSERDP(SI1388)http://www.77cn.com.cnstly,weapologizetothoseauthorswhoseworkcouldnotbediscussedbecauseofspacelimitations.

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