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molecules
Article
SignalingintheTomatoImmunityagainstFusariumoxysporum
FranciscoHernández-Aparicio,PuriflcaciónLisón,IsmaelRodrigo,JoséMaríaBellésand
ópez-Gresa*
InstitutodeBiologíaMolecularyCelulardePlantas,UniversitatPolitècnicadeValència—ConsejoSuperiorde
InvestigacionesCientíflcas,46022Valencia,Spain;Francisco-Jorge.******@(.-A.);
******@(.);******@(.);******@(.)
*Correspondence:******@
Abstract:Newstrategiesofcontrolneedtobedevelopedwiththeaimofeconomicandenvironmental
-
standingthecomplexplant–pathogeninteractionsandunravelingnewchemicalcontrolstrategies.
GC-MS-basedmetabolomics,alongwithaphytohormoneanalysisofacompatibleandincompatible
,revealedthespeciflc

plantswerecharacterizedbytheover-emissionofmethyl-andethyl-salicylateaswellassomefatty
acidderivatives,,
terpenoids,benzenoids,and2-ethylhexanoicacidweredifferentiallyemittedbyplantsundergoing
anincompatibleinteraction,togetherwiththeactivationofthejasmonicacid(JA)
accordancewiththisresponse,ahigherexpressionofseveralgenesparticipatinginthebiosynthesis

ofthesevolatiles,suchasMTS1,TomloxC,TomloxD,andAOS,aswellasJAZ7,aJAmarkergene,was
Citation:Hernández-Aparicio,F.;
Lisón,P.;Rodrigo,I.;Bellés,.;immunetomatoplantscouldleadtothedevelopmentofnewresistanceinducersagainstFusarium
López-Gresa,.
TomatoImmunityagainstFusarium
,26,:Fusarium;tomato;naturalproducts;volatiles;bioticinteraction;metabolomics;GC-MS
/
molecules26071818
AcademicEditor:Marí
AmparoBlázquezTomatoes(Solanumlycopersicum)areanimportantcrop,whosecultivationandcon-
sumptionarebothconstantlyincreasing,reachingaworldwideproductionofmorethan
Received:[1].Inaddi-
Accepted:20March2021
tion,thetomatoisanexcellentmodelplantforstudyingplant–pathogeninteractions,and
Published:24March2021
theresultsofsuchresearchcanbescaled-
worldwide,thecontrolofmainpestsordiseasesbecomesessentialtopreventyieldand
Publisher’sNote:MDPIstaysneutral
,thereare
withregardtojurisdictionalclaimsin
publishedmapsandinstitutionalaffll-thosecausedbybacteriasuchasPseudomonassyringae,virusesliketomatomosaicvirus
iations.(ToMV),andpathogenicfungisuchasBotrytiscinerea,Phytophthorainfestans,andFusarium
,(Fol)istheformaspecialisthataffects
tomatoplants[2]andrepresentstheflfthmostimportantplantpathogenicfungusaround
theworldresponsibleforeconomiclossesaround14%intomatocrops[3].
Folhashemibiotrophicbehavior,livinginsoilduringlongperiodsbeforeinfectinga
Copyright:©2021bytheauthors.

LicenseeMDPI,Basel,Switzerland.
centripetalintracellulargrowthbydigestionofthecellwall,mainlyviaintercellular
Thisarticleisanopenaccessarticle
distributedunderthetermsandprogress[4].OnceFolreachesthexylem,itsgrowthwithinthexylemvesselsgoesthrough

Attribution(CCBY)license(https://bringaboutaprogressiveobstructionofthevesselsandtheconsecutivecollapseofthe
,Folcausesayellowingandwitheringofthe
/).upperleaves,browningofthehypocotylvessels,anddeathinlongterminfection[5].
Molecules2021,26,:///molecules26071818:.
Molecules2021,26,18182of17
Theuseoffungicidesagainstfusariumwiltduringcroppingisineffective,andthere-
,duetoitspersistenceinsoilanditseasydissemination
throughseedsandwind,fusariumwiltisdifflculttocontrol,withthepossibilityofscaling
,themosteffectivemeansofcontrolis
theuseofresistantcultivars,buttheco-evolutionofresistantgenesanddifferentformae
specialesmakesthisinteractionverycomplex[6].Thereareelevencandidatesforeffec-
torsoravirulencegenesinFol,denominatedSIX(secretedinxylem),whichcontributeto
thepathogenvirulence[7].Amongthem,Avr1,Avr2,andAvr3arewidelydescribed[8].
TomatoplantscontainingtheI(immunity)resistancegenes(I,I2,I3andI7)becomeresis-
tanttofungalinfectionafterthecorrespondingAvrrecognition,thereforeactivatingthe
effector-triggeredimmunity(ETI),whichischaracterizedbythedevelopmentoftheso-
calledsystemicacquiredresistance(SAR),andresultinginanincompatibleinteraction[9].
ThecomplexityofthisinteractionlaysonthesuppressionbyAvr1ofI2andI3mediated
resistanceintomatoplants[8].Besides,thereisnofurtherknowledgeaboutthepathogenic
actionoftheotherSIXeffectors[10].Incontrast,tomatoplantsdeflcientintheIresistance
genesaresusceptibletofungalinfectionbyalackof“geneforgene”recognition,resulting
inacompatibleinteraction.
Differentphytohormonessuchassalicylicacid(SA),jasmonicacid(JA),abscisicacid
(ABA),andethylene(ET)havebeeninvolvedintomatoplantresponseagainstdifferent
pathogens[11,12].However,thecontributionofthesesignalmoleculesinbothcompatible
andincompatibletomato–Folinteractionhasnotyetbeenexplored.
Metabolomicshasemergedasapowerfulplatformforbothunderstandingthecom-
plexplant–-
targetedmetabolomicsapproachesbasedonnuclearmagneticresonance(NMR)ormass
spectrometry(MS)havebeenappliedtoproviderapidandaccurateinformationaboutthe
defensemetabolitesimplicatedindifferentpathogen–tomatointeractionssuchastomato–
citrusexocortisviroid(CEVd)[13],tomato–Pseudomonassyringae[14],tomato–ToMV[15],
ortomato–Phytophtorainfestans[16].Speciflcally,theapplicationofMStechniquescoupled
withgas(GC)orliquidchromatography(LC)haveallowedfortheidentiflcationofdif-
ferentiallyemittedvolatileorganiccompounds(VOCs)oraccumulatedmetabolitesinthe
resistanttomatocultivarstocreatenewchemicalcontrolstrategies.
Inthepresentarticle,anuntargetedGC-MSmetabolomicsstudyofthecompatible
andincompatibleinteractionbetweentheFolrace1andisogeniclinesoftomatoplants,
eithercontainingornotcontainingthecorrespondingIresistancegene,wascarriedout
toidentifythechemicalcompositionofthearomaemittedbytheresistanttomatoplants.
Moreover,theinductionofsomegenesinvolvedintheVOCbiosynthesispathwaysandthe
activationofthemainsignalingdefensiveroutesalongwiththelevelsofSA,JAandABA

phytohormonesandVOCsinvolvedintheimmunetomatoresponseagainstFol.


TocharacterizetheestablishmentoftheETI,asymptomatologyanalysisofFol-
inoculatedMovione(MOV)tomatoplantscarryingtheIresistancegenewasperformed.
Concurrently,Momor(MOM)tomatoplantslackingtheIresistancegenewereusedto
,evidentdifferencesinsymptom
severitywereobservedbetweenbothisogeniclinesat14dayspost-inoculation(dpi).:.
MoleculesMolecules20212021,,2626,1818,xFORPEERREVIEW3of173of17
(MOM)andMovione(MOV)tomatoplantsat14dpiafterFusariumoxysporum
(MOM)andMovione(MOV)tomatoplantsat14dpiafterFusariumox-
(Fol)(Fol)-
ceptibleMOM(MOM(B)comparedtomock-inoculated(B)comparedtomock-inoculated(A),andinfection-resistantMOV(A),andinfection-resistantMOV(D),ascomparedtotheircorrespondingmock-D),ascomparedtotheircorresponding
mock-inoculated(inoculated(C).C).
AsFigures1C,Dshow,MOVdisplayednoAsFigure1C,Dshow,MOVdisplayednophenotypicaldifferencesbetweenmock-andphenotypicaldifferencesbetweenmock-
Fol-inoculatedplants,,Fol-infected
andFol-inoculatedplants,,Fol-in-
MOMplantswerecharacterizedbyaheightandweightreduction,yellowingofthe
fectedMOMplantswerecharacterizedbyaheightandweightreduction,yellowingofthe
leaves,browningofthexylemvessels,andevenatotalcollapseofmostplants,therefore
leaves,browningofthexylemvessels,andevenatotalcollapseofmostplants,therefore
conflrmingtheirsusceptibilitytoFol(Figure1B).Finally,nodifferencesbetweenboth
confirmingtheirsusceptibilitytoFol(Figure1B).Finally,nodifferencesbetweenbothnon-
non-inoculatedisogeniclineswereobserved(Figure1A,C).
inoculatedisogeniclineswereobserved(Figure1A,C).
TobetterquantifythedifferencesbetweeninfectedMOVandMOMplants,several
TobetterquantifythedifferencesbetweeninfectedMOVandMOMplants,several
morphologicalparametersweremeasuredsuchasheight,weight,theratiobetweenthe
morphologicalparametersweremeasuredsuchhypocotyllengthandtheepicotyllengthinreferencetotheheight,aswellasthewaterasheight,weight,theratiobetweenthe
hypocotyllengthandtheepicotyllengthinreconsumptionperplant(TableS1,SupplementaryMaterials).Infectedtomatoplantswereferencetotheheight,aswellasthewater
consumptionperplant(TableS1,Supplementaryclassifledaccordingtotheirdiseaseindex[17]asamediumvalueoutofthescoreoftheMaterials).Infectedtomatoplantswere
classifiedaccordingtotheirdiseaseindex[17]asamediumvalueoutofthescoreofthesymptomsfrommild(1)toverysevere(4)alongtheinfection(seeMaterialsandMethods).
symptomsfrommild(1)toverysevere(4)alongtheinfection(seeMaterialsandMeth-Asexpected,astatisticallysigniflcantreductionofheight,weight,hypocotylelon-
ods).gation,andsymptomseveritywasobservedbetweenbothisogeniclines,conflrmingthe
resistanceofMOVtomatoplantstoAsexpected,astatisticallysignificantreductionofheight,weight,hypocotylelonga-Folinfection.
tion,andsymptomseveritywasobservedbetweenTostudythepossiblerelationshipbetweentheobservedsymptomsandthepresencebothisogeniclines,confirmingthere-
sistanceofMOVtomatoplantstoofthepathogen,FollevelswereanalyzedinthehypocotylofbothinfectedisogeniclinesatFolinfection.
7and14dpibyqPCR,beingstatisticallyhigherinMOMthaninMOVplantsatanytimeTostudythepossiblerelationshipbetweentheobservedsymptomsandthepresence
ofthepathogen,(FigureS1),
at7and14dpibyqPCR,beingstatisticallyhigherinMOMthaninMOVplantsatany
time(FigureS1),-andABA-MediatedDefenseResponseafterthesymptomsobservedinFigure1.
FolInfection
,theactivationofthemainyJA-andABA-MediatedDefenseResponseafter

correspondingtothepathwaysmediatedbySA,JA,ET,orABA,whicharethemostTobettercharacterizetheinfectioninbothisogeniclines,theactivationofthemain
,wereanalyzedbyusingRT-qPCRpressionlevelsofdifferentmarkergenes
correspondingtothepathwaysmediatedbySA,JA,ET,orABA,whicharethemostim-(Figure2)bothinsusceptibleMomor(MOM)andresistantMovione(MOV)tomatoplants
portantphytohormonesinvolvedinplantdefense,wereanalyzedbyusingRT-qPCR(Fig-after3,7,and