39OrganicAmendmentsBeneficialMicrobesandSo

PY56CH01_LoritoARI30April201813:2AnnualReviewofPhytopathologyOrganicAmendments,BeneficialMicrobes,andSoilMicrobiota:TowardaUnifiedFrameworkforDiseaseSuppressionGiulianoBonanomi,1MatteoLorito,1,2FrancescoVinale,1,2andSheridanL.Woo2,31DepartmentofAgriculturalSciences,UniversityofNaplesFedericoII,80055Portici(NA),Italy;email:[e-mail]2InstituteforSustainablePlantProtection,NationalResearchCouncil(IPSP-CNR),80055Portici(NA),Italy3DepartmentofPharmacy,UniversityofNaplesFedericoII,80131NapoliAnnu.Rev.Phytopathol.2018.56:1.1–1.20TheAnnualReviewofPhytopathologyisonlineatphyto.annualreviews.org2018byAnnualReviews.AllrightsreservedKeywordssoilmicrobiota,beneficialmicrobes,biocontrol,soilbornepathogens,13C-CPMASNMRAbstractOrganicamendments(OAs)andsoilbornebiocontrolagentsorbeneficialmicrobes(BMs)havebeenextensivelystudiedandappliedworldwideinmostagriculturallyimportantplantspecies.However,poorintegrationofresearchandtechnicalapproacheshaslimitedthedevelopmentofeffectivediseasemanagementpracticesbasedonthecombinationofthesetwobio-basedstrategies.Insightsintotheimportanceoftheplant-associatedmicrobiomeforcropproductivity,whichcanbemodifiedormodulatedbyintroducingOAsand/orBMs,areprovidingnovelopportunitiestoachievethegoaloflong-termdiseasecontrol.ThisreviewdiscussesnovelwaysoffunctionallycharacterizingOAsandhowtheymaybeusedtopromotetheeffectofaddedbiocontrolagentsand/orbeneficialsoilmicrobiotatosupportnaturalsuppressivenessofplantpathogens.1.1ReviewinAdvancefirstpostedonMay16,2018.(Changesmaystilloccurbeforefinalpublication.)Annu.Rev.Phytopathol.2018.56.Downloadedfrom:2INTRODUCTIONIncreasingpublicawarenessaboutsustainablecropandvegetableproductionhaspromptedre-searchintolow-inputagriculturalmanagementpractices.However,considerablelossesarestillcausedbysoilborneplantpathogens,whicharedifficulttocontrolwithsyntheticchemicalpes-ticides.Theglobalbanofmethylbromide,whichisassociatedwithrestrictionsontheuseofalternativesoilfumigants(74),hasfurtherincreasedtheneedformethodsprovidingacceptablelevelsofdiseasecontrolbutlimitedsideeffectsontheenvironment.Inthiscontext,theuseoforganicamendments(OAs),possiblyintegratedwithapplicationsthatintroduceorpromotetheactivityofbeneficialmicrobes(BMs),hasbeenproposedbutitspotentialisnotyetfullyexplored.Controlofsoilbornepathogenshasbeenobtainedbyusinggreenandanimalmanure(61),organicwastesfromagro-industry(28),compost(40),and,morerecently,biochar(31).Thelistofaffectedpathogensincludesbacteria(e.g.,Ralstoniasolanacearum),oomycetes(e.g.,Phytophthoraspp.andPythiumspp.),andfungi(e.g.,Fusariumspp.,Rhizoctoniasolani,Sclerotiniaspp.,Sclerotiumspp.,andVerticilliumdahliae)(11).InthecaseofBMs,theirusefulnessisillustratedbythelargenumberofproductsavailableworldwide(69).DespitetherecognizedpotentialvalueofOAsandBMs,lackofpredictabilityandconsistencystilllimittheiradoptionincommercialagriculture.IthasbeenreportedthatOAsarenoteffectivefordiseasecontrolandinquiteafewcasesmayenhanceplantdiseaseintensity(77,103,121).Un-desiredsideeffectsofBMsseemtobelessfrequent,buttheirefficacycanvarygreatlywhenappliedtodifferentcultivationsystemsandsoiltypesorindiverseclimaticconditions(114).Therefore,animprovedunderstandingofthemechanismsthatregulateOA-basedsuppressiveness,aswellaspathogenicandantagonisticmicrobeinteractions,willhelptodevelopnew,more-reliableproductapplications.ThisreviewexplorestheopportunityprovidedbypowerfulchemicalandgenetictoolstostudyOAnature,application,andmechanismsofactioninrelationtothecurrentunderstandingofmicrobialecologyinthesoil.ThetwotopicsarelinkedbyaddressingtheissueofthenutritionalroleofOAsandtheeffectonthevirulenceandaggressivenessofsoilborneplantpathogens,BMs,andnativemicrobiota.Finally,wediscusstheprinciplesforapplyingeffectivecombinationsofdifferentOAtypesandBMs.HISTORICALOVERVIEWOrganicAmendmentfortheControlofSoilbornePathogensInthepast70years,hundredsofpapers,basedonthousandsofexperiments,havereportedthesuppressiveeffectofdifferentOAtypeson78plantpathogenspecies(Figure1).Earlyscientificevidencedatesbacktothe1940sand1950s,whencropresiduesandN-richorganicwasteswerefoundcapableofcontrollingR.solani,Fusariumoxysporum,andVerticilliumalbo-atrum(97,116).Inthe1960s,theresearcheffortledbyG.C.PapavizasstudiedtheeffectofcropresiduesonFusariumspecies,R.solani,andThielaviopsisbasicola,amongotherpathogens(1,86).WiththeexceptionofafewpaperslinkingOAstosoilfungistasis(67),interestinthebiocontrolpropertiesofOAsdeclinedinthe1970s.ItrecoveredinthenexttwodecadesthankstotheworkoftheHoitinkgrouponthesuppressivenessofsomepeat-basedpottingmixesandcompost(26,70).Accordingtoameta-analysisofthistopicbasedon2,423experiments,OAswereindeedsuppressivein45%ofcasesandhadanonsignificanteffectin35%ofcases,althoughtherewasasignificantincreaseindiseaseincidencein20%ofthetests(11).CompostremainsthemostwidelystudiedOAtype,withmorethan1,000relatedpapers,