Adapting plant material to face water stress in vineyards: which physiological targets for an optimal control of plant water status?

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control of plant water status?

Thierry Simonneau, Eric Lebon, Aude Coupel-Ledru, Elisa Marguerit, Landry Rossdeutsch, Nathalie Ollat

To cite this version:

Thierry Simonneau, Eric Lebon, Aude Coupel-Ledru, Elisa Marguerit, Landry Rossdeutsch, et al..

Adapting plant material to face water stress in vineyards: which physiological targets for an optimal control of plant water status?. OENO One, Institut des Sciences de la Vigne et du Vin (Université de Bordeaux), 2017, 51 (2), pp.167. �10.20870/oeno-one.2016.0.0.1870�. �hal-01602544�

Adapting plant material to face water stress in vineyards:

which physiological targets for an optimal control of plant water status?

T. Simonneau^1*,E. Lebon¹,A. Coupel-Ledru²,E. Marguerit³,L. Rossdeutsch³andN.Ollat³

1UMRLEPSE,INRA,2placeViala,F-34060MontpellierCedex1,France

2UMRLEPSE,INRA,MontpellierSupAgro,2placeViala,F-34060MontpellierCedex1,France

3EGFV,BordeauxSciencesAgro,INRA,BordeauxUniversity,210chemindeLeysotte, F-33882Villenaved’Ornon,France

This article is published in cooperation

with the ClimWine international conference held in Bordeaux 11-13 April 2016.

Guest editor: Nathalie Ollat

Aims:Waterscarcity,associatedwithclimatechange,isaparticularthreattothesustainabilityofviticultureinpresentareasof cultivation,usuallypronetodrought.Breedinggrapevineforreducedwateruse,betterwaterextractionandmaintained production(i.e.,highwateruseefficiency)isthereforeofmajorinterest.

Methods and results:Thisrequiresacomprehensiveknowledgeofthephysiologicalimpactsofdroughtonyieldandquality.

Attentionshouldbepaidtothosemechanismsinvolvedintheregulationofwaterstatusinplanttissues,asitistheprimary parameteraffectedbydrought.Transpirationrate,whichhasamajorinfluenceonplantwaterstatus,shouldthereforereceive specialattentioninbreedingprograms.Beyondscions,theroleofrootstocks,whichhavebeenlargelyintroducedinvineyards, shouldbeinvestigatedfurtherasitdetermineswaterextractioncapacityandcouldmodifywaterbalanceingraftedplants.

Conclusion:Herewereviewrecentadvancesinthecharacterizationofgeneticvariabilityinthecontrolofwateruseandwater status,whetherinducedbyrootstockorscion.

Significance and impact of the study:Thisreviewshouldhelpscientistsinchoosingtherelevantphysiologicaltargetsin theirresearchongrapevinetolerancetodrought,whetherforbreedingprospectsornewmanagementpractices.

Keywords:grapevine,drought,wateruse,rootstocks,genetics Abstract

Received 26 July 2016; Accepted 17 octobre 2016 DOI: 10.20870/oeno-one.2016.0.0.1870

Volume 51 > Number 2 > 2017

Introduction

Vineyardsarepredominantlylocatedindrought proneareas.Theycommonlyexperiencemoderate soilwaterdeficit,whichisfavorabletowinequality providedthatitremainsmoderate(Beckerand Zimmerman,1984).Excessofwater,bycontrast,can reducecolorintensityandsugarcontentofberries andproduceunbalanced,flatwine(Matthewset al., 1990;Medranoet al.,2003).Thus,moderatesoil waterdeficitisthebestcompromisetopromotethe expressionofhighenologicalpotentialwithout alteringyield.Thisisusuallyachievedinmost vineyardsbutglobalchangeseriouslythreatensthis fragileequilibrium.Specifically,underthecombined influenceofhighevaporativedemand(dry,warmair) andsoilwaterdeficit,planttissuesstartdehydrating withdetrimentalimpactsonproductionandberry quality(Joneset al.,2005;Delucet al.,2009).

Tofacetransientdroughtorlonger-lastingdry climates,irrigationisdevelopinginproductionareas.

However,pressureonagriculturaluseofwater resourcesisrising.Irrigationofthevineyardoften resultsasverycompetitiveorimpossible.Toprepare forthefuture,viticultureshouldadaptbylimiting water use while maintaining yield. Vineyard establishmentandmanagementpractices,suchas lowerplantationdensity,controlofwaterbalance

throughsoilsurfacemanagement,andthinning,can beconsideredasvaluableshort-termsolutions (GarciadeCortazarAtauri,2006;Duchêneet al., 2010 ;Ripocheet al.,2010).However,these techniquesmightnotalwaysbesufficienttocope withincreasinglydryerconditions(Garciade CortazarAtauri,2006).Additionalstrategiesare needed,includingtheuseofsuitableplantmaterial.

Thisrequiresacomprehensiveknowledgeofthe physiologicalimpactsofdroughtonyieldandquality.

In the following, we review the primary consequences of water deficit on grapevine.

Specifically,geneticvariabilityinthemechanisms involvedinthecontrolofplantwaterstatusis examined.

Physiological responses to water deficit 1. Drop in plant water potential as a primary consequence of water deficit

Waterpotentialcharacterizeswateravailabilityfrom athermodynamicpointofview.DenotedΨ,itisat thebasisofwatermovementsfromthesoiltothe plantorgansandultimatelytotheatmosphere.

Conventionally,freewateratsealevelhasapotential of zero, corresponding to the maximal water availabilityinasaturatedsoil.Soildryingresultsina

A

R

Figure 1. Physiological responses associated with a drop in plant water potential. Simplified representation adapted from Chaves et al.(2010) and Marguerit (2010).

Theleftdiagramillustratesthedropofwaterpotentialoccurringatdifferentintensitiesdependingonthesoilwaterpotential (dryerfromrighttoleft)andoftheevaporativedemand(higherfromrighttoleft).Duringthenight,waterpotential equilibrates(verticalline).Inthedaytime,underhighevaporativedemand,plantwaterpotentialsbecomemorenegative (dashedlines)andfurtherdeclineindrysoil(dottedline).Arrowsindicatetheinfluenceofthephysiologicaladaptations (limitationofwaterlosses,maintenanceofhydraulicconductanceandenhancedwateruptake)onwaterpotentials,highlighting

thefavorable(filled,blackarrows)andtheunfavorablesituations(dotted,greyarrows).Therightdiagramoutlinesthemain physiologicaladaptationsfavoringthemaintenanceofplantwaterstatus.Thenegativeconsequencesofadecreaseinleafwater

potentialoncarbonassimilationarealsohighlighted.

decreaseofsoilwaterpotential(Ψbecomesmore negative as water binds to soil particles and concentratingsolutes).Undernontranspiring conditions,waterpotentialsinplantsequilibratewith themosthumidlayerexploredbytherootsystem (Améglioet al.,1999).Astranspirationrateincreases inthedaytime,plantwaterpotentialdecreases.This dropinwaterpotentialismoreseverewhenhydraulic conductanceislimitingwatertransportonthepath from the soil through the plant to the leaves (Figure 1).Becauseexcessivedropsinwater potentialmaybedisastrousforplants,theyhave developeddiverseadaptationstopreventthem.

2. Cavitation threatens hydraulic integrity of xylem conduits

Inatranspiringplant,sapwaterascendstowardsthe leavesusingthenon-living,heavilythickenedand lignifiedxylemvesselsandtracheids.Waterflow followsagradientofincreasinglynegativepressure withinacontinuouswatercolumn.Anybreakinthis columnwoulddisruptthewholewaterflow.

Whensoildryingcombineswithhighevaporative demand,hightensilestrengthdevelopsinthexylem, therebyfavoringcavitation,whichistheapparitionof gaseousbubbles(caveats)inthexylemsapdueto waterevaporation,aggregationofdissolvedgasesor airentrythroughpitmembranes.Onceinitiatedthe bubblethenrapidlyexpandstooverrunthevessel (Brodersenet al.,2013).Thisgaseousembolismmay resultintheruptureofthewatercolumninthexylem, beingamajorthreatfortheplant.

Vessel embolism decreases stem hydraulic conductance,whichinturndecreasesleafwater potentialitself,favoringfurtherembolism.Inthe absenceofstomatalclosureorreductioninleafarea, thiscyclecanresultinfunctionalitylossofallthe conductingtissue.Thisresultsindramatically amplifiedeffectsofwaterdeficitonthedropinleaf waterpotentialalongthewaterpath(Brodribband Cochard, 2009 ; Zuffereyet al., 2011) with catastrophicconsequencesonplantdehydrationand evendeath(McDowellet al.,2008).Vesselsize partlydeterminesplantvulnerabilitytocavitation, small-diameterconduitsbeinglessvulnerable(Tyree, 2003)butlessefficienttotransportwater.Thus,plant adaptationtodryenvironmentsdependsonatrade- offbetweenefficientconduitsandlowvulnerability tocavitation.Ingrapevine,whichdisplayslong vessels(acommonfeatureamonglianaspecies), vesselsizesaredependentonthecultivar(Chouzouri andSchultz,2005;Tramontiniet al.,2013a),leaving roomforgeneticvariationindroughtresponse.

Thresholdwaterpotentialforcavitationalsovaries withspecies,cultivarsandgrowthconditions.As comparedtootherspecies,grapevinehascommonly beendescribedasvulnerabletocavitationoccurring athigh(lessnegative)waterpotentialthreshold (SchultzandMatthews,1988 ;McElroneet al., 2012).Upto70%lossofconductivityhasbeen reportedwithmoderatetensionsinstemsaround -0.75MPa(Tibbetts&Ewers,2000).Nevertheless, anefficientcontrolofwaterlossesthroughstomata oftenprotectsgrapevinefromcavitation(Zuffereyet al.,2011).

Recentstudiesreportthattransportcapacitycouldbe largelyrestoredbytheendofthedayorduringthe night,whentranspirationratedecreases.Thishas beenassignedtowaterrefillingofembolizedxylem vessels. Although mechanistically debated, restorationofwatertransportcapacityhasbeen observedinanumberofspecies,whetherinroots (Domecet al.,2006;Lovisoloet al.,2008a),shoots (ZwienieckiandHolbrook,1998)orleaves(Johnson et al.,2009).Plantcapacitytorestorehydraulic integrityovernightunderdryconditionswould largelydependonsoilexplorationbyroots(Zufferey et al., 2011). Carbohydrates stored in cells neighboringtheconductingvessels,togetherwith aquaporins (e.g. membrane channel proteins facilitatingwatertransport),alsoappearaspossible, importantactorsofthisrestoration(Salleoet al., 2009).

3. Limitation of transpiration releases hydraulic tension and saves water

Oneofthemostobviousandimmediateeffectsof waterdeficitisareductioninshootgrowth(Chaves, 1991),withcellexpansionbeingparticularly sensitivetowatershortage(Hsiao,1973).Branches aremoresensitivethanfirstorderaxes(Lebonet al., 2006),andobservationofgrowthcessationatthe shootapicesisapowerfultooltoearlydetect incipientwaterdeficit(Pellegrinoet al.,2006).

Limitedvigorunderdroughtresultsinadecreaseof evaporativeareas,therebyloweringtranspirationand releasingwatertensioninthexylem.Leaffoldingor wiltingareotheradaptationshavingsimilar,although reversible,effectsonwatersavingbyincreasing boundarylayerresistanceandreducingintercepted light,henceloweringsurfacetemperatureand evaporativedemand.

Additionally,plantsdynamicallymodulatethe apertureofstomata,thosemicroporeslocatedatthe leafsurfacethatmakepossiblewatervaporandCO2

exchanges.Arapidstomatalclosureisgenerally

observedunderwaterdeficit(Damouret al.,2010), which efficiently lowers water flow density.

However,thiswayofsavingwaterhasaheavycost fortheplantbecausestomatalclosureunavoidably lowersCO₂ uptakeanddecreasesphotosynthesis, althoughtovariableextentdependingonspeciesand varieties(TardieuandSimonneau,1998).Plantsthus faceadilemma,andadaptivestrategiesarenecessary toreachatrade-offensuringCO₂ uptakewhile limitingwaterlosses.

Otheradaptationsmayparticipateinminimizing transpirationrate,includingchangesinthicknessand compositionofthewaxycuticlethatwaterproofsthe leafsurfaceandforceswatertoleavetheplant through stomata. Relation between cuticle componentsandtheirefficacytolimitwaterlosses remainstobeunderstood(RiedererandSchreiber, 2001).

4. High root water extraction capacity postpones the negative impact of water deficit

Rootdevelopmentishighlyplastic,withtypical shifts in the allocation of plant’s resources (carbohydrates)towardsrootgrowthattheexpense oftheshootsindryconditions.Thisallowstheplant toincreasesoilexplorationforwateruptakewhile reducingtranspiration(SharpandDavies,1985 ; Crameret al.,2013).Themaintenanceofrootgrowth capacitiesduringwaterdeficit,togetherwithsome plasticityinroothydraulicarchitectureunder fluctuatingconditions,dependonthespeciesand,in grapevine,isvariableamongrootstocks(Bauerleet al.,2008).

5. Osmotic adjustment helps maintaining water into the cells

Plantsevolvedindifferentwaystomaintain physiologicalactivitywhilewaterpotentialdeclines.

Amajorresponseisosmoticadjustment,which allowsthecellstomaintaintheirwatercontentand turgorevenwhenwaterpotentialdecreasesintheir vicinity.Osmoticadjustmentinacellconsistsof trappingorgeneratingsolutestoincreasetheir concentration,leadingtointeractionsofwaterwith solutesinsidethecell.Thisdecreasestheosmotic potential,acomponentofthetotalwaterpotential, whileturgor,theothercomponentincells,canbe maintainedevenwhenagivendropintotalwater potential is transmitted to the cell from its environment.

Thiswidespreadresponsetowaterstressoccursin leaves,rootsandreproductiveorgansofmany species(TurnerandJones,1980;Morgan,1984)and

isundergeneticcontrol(e.g.Teulatet al.,2001).In grapevine,osmoticadjustmenthasbeenevidenced underwaterdeficitinleaves(Rodrigueset al.,1993) androots(DuringandDry,1995).Itmightbea majorstrategytoavoidtissuedehydrationand maintaingrapevineproductionindryconditions (Hareet al.,1998;PatakasandNoitsakis,1999).The mostinterestingsolutesarethosethat,besidestheir roleinosmoticadjustment,playaroleinnutrientor energystorage,membraneprotectionordetoxifying activities(Szabadoset al.,2011).

6. Primary traits for a drought tolerant grapevine ideotype

Plantresponsestodroughtarepluralandinvolvea range of morphological and physiological adaptationsofbothaerialandundergroundorgans.

Theprimaryfeaturesofinterestforgrapevine encompassatightcontrolofwaterlossesthrough stomatalregulation,osmoregulation,togetherwith photosynthesismaintenancetothebenefitofberry developmentandrootgrowth.Thetightcoupling betweenphotosynthesisandtranspiration,whichare bothcontrolledbystomataandleafarea,doesnot maketrivialtodecreasetranspirationwithoutaltering photosynthesis.However,theratioofphotosynthesis totranspirationratesvariestosomeextentwith environmentalconditionsandgenotypes(Tomaset al.,2014;Medranoet al.,2015).Anadequatecontrol ofstomatalapertureallowstheplanttotake advantageoftheenvironmentalconditionsby loweringthewatercostofgasexchange.

Physiological control of leaf water potential in a drying soil

1. The stomatal control of transpiration

Transpirationalwaterlosses,which,incombination withsoildrying,areresponsiblefordrawingdown waterpotentialinplants,mainlyoccurthroughthe stomata.Stomataformmicroscopicporesmainly locatedontheabaxial(inferior)epidermisofthe leavesingrapevine,aspeciesthereforequalifiedas hypostomatous.Apairofadjacentguardcells controlstheporeaperturethroughrapidmodification incellvolumeassociatedwithturgorchanges.

Changesinturgorresulteitherfromvariationsin totalwaterpotentialdrivenbysoilorairdrying (hydraulicresponse),orfromactivechangesin osmoticpotentialcausedbysolutemovements(into oroutoftheguardcells),themselvesgeneratedby chemicalsignalsthatmodifyiontransporteractivity (biochemicalresponse).Moreover,stomataldensity displaysahighinter-specificandintra-specific variability,asexemplifiedforgrapevine(Bosoet al.,

2011).However,variabilityinstomataldensitywas notfoundtoexplainmuchofthedifferencesin transpirationrate(Hopperet al.,2014).

Stomatalclosureinresponsetowaterdeficitis controlledbyabscisicacid(ABA),aplanthormone havinglongbeenrecognizedasakeyplayerinplant abioticstressresponses(Loveys,1984;Wilkinson andDavies,2002 ;Yamaguchi-Shinozakiand Shinozaki,2006).ABAbiosynthesis,metabolism, andtransfertowardsguardcellsmodulatestomatal sensitivitytowaterdeficit(Stollet al.,2000;Cramer et al.,2007).ABAsynthesisinrootswasfirst proposedasthepivotofplantresponsetodrought.

Soildryingissensedbytherootsastheirwater potentialdecreases,resultinginanincreasedABA biosynthesisbythiscompartment(Simonneauet al., 1998).ABAisthenconveyedtotheleavesthrough thexylemvessels(TardieuandSimonneau,1998).

ABA biosynthesis also occurs in the leaves (Holbrooket al.,2002 ;Christmannet al.,2005 ; Christmannet al.,2007;Ikegamiet al.,2009)where hydraulicandchemicalsignalstriggerfoliarABA synthesisinresponsetowaterdeficit(Christmannet al.,2013;Mittler&Blumwald,2015),althoughthe precisesignaltransductionstillremainstobe deciphered.SeveralkeyenzymesoftheABA biosyntheticpathway,namelyABA2,AAO3,and NCED3,areexpressedinspecificareasofvascular tissuesinresponsetowaterdeficit(Endoet al., 2008).Importantly,VvNCED1 codingfor9-cis- epoxycarotenoïddioxygenaseNCED,anenzyme catalyzing the first committed step in ABA biosynthesis,hasbeenidentifiedasdecisiveforABA accumulationunderwatershortageingrapevine (Speirset al.,2013 ;Rossdeutschet al.,2016).

VariationsofpHbetweentissues,togetherwiththe actionofglucosidasesorglucosylesterases,modify theconcentrationoffreeABAreachingthestomata (NambaraandMarion-Poll,2005).DepletionofABA mayalsoparticipateintheregulationofABA balance.Aspecificgroupofenzymes,includingthe ABA8’-hydroxylases,regulatesABAdegradationto inactivecompounds(Speirset al.,2013).Astrong allelicdiversityforgenesinvolvedineitherABA biosynthesisordegradationcouldexplaingenetic variationsinABAaccumulationunderwaterdeficit (NambaraandMarion-Poll,2005;Riahiet al.,2013).

Ingrapevine,variabilityinABAaccumulationhas beenobservedamongrootstocks(Peccoux,2011)as wellasscions(Soaret al.,2004).

Additionally to ABA accumulation, stomatal sensitivitytothehormoneisalsohighlyvariable (TardieuandSimonneau,1998;Rossdeutschet al., 2016).Itdependsonnumerousmolecularstepsatthe

guardcelllevel.PerceptionofABAcorrespondsto bindingtothePYR/PYL/RCARproteins(Brandtet al.,2012).Thisleadstoconformationalchangeinthe receptorenablingABAinteractionwithPP2Cs phosphatase,whichinturnreleasesSnRK2skinases.

SnRK2sactivatetranscriptionfactors,ABA- responsiveelementBindingFactors(ABFs),which resultsinABA-responsivegeneexpression(Klingler et al.,2010 ;Bonehet al.,2012).Thiscascade modulatestheactivityofionchannelsintheguard cells,whichtranslatesinosmoticandturgorchanges, andultimatelyregulatesstomatalclosure(Joshi-Saha et al.,2011).Manyotheractorsinvolvedinthose responseshavebeenidentified,includingvariations ininternalCa²⁺concentrationandaccumulationof nitrousoxideinguardcells.

Howchemicalcontrolofstomatalapertureinteracts withhydraulicsisstillamatterofdebate.Ithas recentlybeenproposedthatABAmightaffectleaf hydraulicconductancethroughadecreaseinwater permeabilitywithinleafvasculartissues.ABAwould thuspromotestomatalclosureinadualwayvia effectsonhydraulicsupstreamstomataandadirect biochemicaleffectontheguardcells(Pantinet al., 2013).VariabilityintheroleofABAonhydraulic conductanceremainstobeexploredasapossible causeofthelargediversityofstomatalsensitivitiesto ABAobservedamongspeciesandwithingrapevine cultivars.

2. Isohydric genotypes are able to maintain leaf water potential in drying soils

Soildryinginevitablyresultsinadecreaseofwater potentialinplantsincludingleaves.However, contrastingcontrolsofleafwaterpotentialhavebeen observedacrossspecieswhensubmittedtosimilar soilwaterdeficitconditions(TardieuandSimonneau, 1998).So-calledisohydricspecies,suchasmaize, efficientlymaintainhighleafwaterpotentialinthe daytime (ΨM) when the soil dries, whereas anisohydricspecies,suchassunflower,exhibit substantialdecreaseofΨM(Tardieuet al.,1996).In severalspeciesincludingtheoverall,roughly isohydricgrapevine(Prietoet al.,2010),avariable efficacytomaintainhighΨ_Mhasbeenobserved acrossgenotypes.Twowidespreadcultivars,namely Grenache and Syrah, have been consistently describedwithdifferentresponsestosoilwater deficit.Grenachewasshowntobenear-isohydric, compared with Syrah, which exhibited more anisohydricbehavior(Schultz,2003;Soaret al., 2006b).

The classical view relates the contrasted (an)isohydricbehaviorstothemoreorlessefficient controloftranspirationratebystomatalclosure (Buckley,2005).Stomatalconductancewasshownto decreaseearlierduringthecourseofasoildrying episodeinisohydricspecies,thusreducingthedrop ofleafwaterpotentialinthedaytimeascomparedto anisohydricspecies(TardieuandSimonneau,1998).

The anisohydric behavior would thus favor photosynthesismaintenanceunderwaterdeficit.This hasbeenconfirmedingrapevine(Lovisoloet al., 2010)whereanisohydriccultivarsalsoexhibithigher vigorinconditionsofwaterdeficit(Pouet al.,2012), aslongassoildryingdoesnotinduceanyserious decreaseofplantwaterpotential.Anisohydricplants mightalsobemoreresistanttocavitationthan isohydricones(Schultz,2003;Alsinaet al.,2007) andmighteasilyrecoverfrompartialcavitation events,thusexhibitingahighertolerancetomoderate waterdeficitevents.However,beyondacertain thresholdinsoildrying,theanisohydricbehavior mightnotremainfavorablebecausehighlevelsof dehydrationleadtoseriousdamages.Thishasbeen exemplifiedforgrapevinecultivarssuchasSyrahand Chardonnay(Alsinaet al.,2007).Bycontrast,the isohydriccultivarCabernet-Sauvignondisplaysa reducedphotosynthesisbutispreservedagainst damagessuchasphotoinhibition,whichisthe alterationofphotosynthesisduetohighlightintensity (Hochberget al.,2013).Hence,oneofthese behaviorscanbemoreinterestingdependingonthe water deficit scenario (duration, intensity, combinationwithevaporativedemand).While anisohydriccultivarsmayberecommendedinthe caseofshortperiodsofmoderatewaterdeficit becausetheysustainproduction,theisohydricones appearasmoresuitabletofacelonglastingperiods ofseveredrought.Specificitiesoftheclimatic scenariosshouldbeconsideredtodefinethemore advantageoustypeofcultivarfromanagronomic pointofview.

3. Reconsidering the origin of the variation in (an)isohydric behaviors

Theclassicalviewof(an)isohydrywasrecently questionedinseveralstudies.Itwasproposedthat changesinhydraulicconductancemaycontribute, concurrentlywithstomatalregulation,tothecontrol ofΨ_Munderadverseconditions(Frankset al.,2007;

Pantinet al.,2013).Additionally,(an)isohydrywould notbeagenotype-constitutivefeature(Lovisoloet al.,2010)butcouldvaryinasameplantfollowing seasonanddevelopment(Poniet al.,1993;Chaveset al.,2010).Somestudiesconcludedtovariable ranking of (an)isohydric behaviors between

grapevinecultivars,notablyGrenacheandSyrah (Pouet al.,2012).Thegeneticoriginof(an)isohydry wasthuschallenged.

Geneticvariationin(an)isohydrywasextensively studiedingrapevineusingamappingpopulation obtainedfromacrossbetweenSyrahandGrenache (Coupel-Ledruet al.,2014).Significantgenetic controlofΨ_Mundermoderatedroughtwasobserved undercontrolledconditionsusingpottedplantsina phenotypingplatform.Severalgenomicregions (QTLs)wereidentifiedasunderlyingthegenetic variationofΨM.Further,themaintenanceofΨM

underwaterdeficitconditionswasnotsimply controlledbytranspirationresponsetosoildrought.

SomeoftheQTLsdetectedforgeneticvariationin Ψ_Mresponsetomoderatewaterdeficitcollocated withQTLsfortranspirationresponse,butothers collocatedwithQTLsdetectedforplanthydraulic conductance(Coupel-Ledruet al.,2014).Overall, geneticvariationofΨMunderwaterdeficitconditions correlated with variation in plant hydraulic conductance(Coupel-Ledru,2015).Itwasthus proposedthatwholeplanthydraulicconductance underwaterdeficitmightcombinewithstomatal controloftranspirationtodetermine(an)isohydry.

Specifically,variationin(an)isohydrymayresult fromslightdeviationinthebalancebetween transpirationrateandhydraulicconductance.

ThegeneticanalysisoftheSyrah×Grenache offspring(Coupel-Ledruet al.,2014)alsoevidenced thattranspirationrateandsoil-to-leafhydraulic conductancemostlycorrelated.Thismayexplain why grapevine can be considered as roughly isohydric by contrast with other species like sunflowerwheremoreseveredropsinΨM rapidly occurasthesoildries(Tardieuet al.,1996).In grapevine,thisbalancemaybetheresultofmultiple coordinationbetweenstomatalresponseandvariation inspecifichydraulicconductanceinleaves(Pouet al.,2012),petioles(Schultz,2003)androotswhere correlationwithexpressionsofwaterchannel proteinsinrootshasbeenevidenced(Vandeleuret al.,2009).Identificationofgenesspecifically associated with QTLs detected for hydraulic conductance and control of ΨM but not for transpirationresponse(andviceversa)wouldbeof particularinteresttolookfororiginsofpossible imbalancebetweentranspirationandwatertransport capacityandtoprogressonthedeterminismof (an)isohydry.

Rootstocks: the hidden half

Whilethechoiceofscionvarietiesisoftenregulated bytheirperformanceinspecificclimaticconditions ormarketingpurposes(vanLeeuwenandSeguin, 2006),rootstocksoffermoreflexiblesolutionsfor adaptingthegraftedplanttodrought.Alarge variabilityinrootstockresponsetowaterdeficithas beenreportedbyseveralauthors(Carbonneau,1985;

Ollatet al.,2016 ;Zhanget al.,2016),although underlyingmechanismsstillneedtobeenlightened.

Rootstocksparticipateintheregulationofplantwater balance through their own uptake capacities associatedwithrootgrowthandwatertransport (Carbonneau,1985;Bauerleet al.,2008;Alsinaet al.,2011;Peccoux,2011;Zhanget al.,2016)orvia theireffectsonstomatalregulation(Lovisoloet al., 2010 ;Margueritet al.,2012)andaboveground development (Jones, 2012). Water extraction capacitiesbyrootsarereportedtobevariable betweenrootstocksandgeneticallycontrolled (Carbonneau,1985;Soaret al.,2006a;Margueritet al.,2012),eventhoughthephysiologicalmechanisms underlyingthistraitarestillunknown.Inaddition, rootstocksareknowntoaffectscionphenology, vegetativegrowth,yieldandfruitquality(Tandonnet et al.,2010).

1. Root development

to better explore soil water resources

Adeepanddenserootsystemfavorswateruptaketo compensateforwaterlossesbytranspiration.

Grapevineisknownforitsabilitytogrowdeeproots.

Rootdistributionandrootsystemarchitectureare moreaffectedbysoiltypeandtrainingsystemthan byrootstockgenotype(Smartet al.,2006).In addition,interactionswithsciongenotypeshavea strongeffectonrootsystemdevelopment(Tandonnet et al.,2010).Bycontrast,rootstockgenotypehas moreimpactonrootdensityexpressedasbiomass- orrootnumberbyvolumeofsoil-(Southeyand Archer,1988;Peccoux,2011),orontheratiooffine rootstototalroots(VanZyl,1988).Inthevineyard, somehighlydroughttolerantrootstockssuchas 140Ruaremoreabletogrowrootsindeepsoillayers (SoutheyandArcher,1988).Furthermore,the maintenanceofrootgrowthunderdryconditionsas wellastherootsystemplasticitywithsoilwater statusmaydifferentiaterootstockgenotypes(Bauerle et al.,2008)accordingtotheirstrategytocopewith drought(Comaset al.,2010).Furtherinvestigations ofrootgrowthpropertiesfordifferentrootstocks wouldbeprofitableforthefuture.

2. The control of water transport to shoot

Therootsystemcontributesinanon-negligibleway tothewholeplantresistancetowaterflow(Steudle, 2000).Thereisalargevariabilityamongrootstocks inrootvascularanatomy(vesseldiameterandlength, percentageofconductingtissues ;Pongracz&

Beukman,1970;Alsinaet al.,2011;Peccoux,2011).

Thesedifferencescanaffectrootabilitytoconvey watertothecanopy(i.e.hydraulicconductance),and rootvulnerabilitytocavitation.Differencesbetween rootstocksforroothydraulicconductancehavebeen reported(deHerraldeet al.,2006;Peccoux,2011;

Tramontiniet al.,2013b),butmaybemorerelatedto whole root system size than individual root properties(Alsinaet al.,2011).Inaddition,drought effectonroothydraulicconductivitymaydiffer betweenrootstocks.Barrios-Masiaset al. (2015) observedalowerdecreaseofrootconductivityfor thedroughttolerantrootstock110R,incomparisonto thedroughtsensitive101-14MGt.Differencesare relatedtothedevelopmentofsuberizedapoplastic barriersintheroottipsatthebeginningofthe maturationzone.Ingrapevine,rootstogetherwith leavesaremoresensitivetoembolismthantheother plantcompartments(Tramontini&Lovisolo,2016).

Besides,itwasrecentlyshownthatwildVitisspecies stemsdifferfortheirsensitivitytocavitationunder water stress and their ability to repair after rehydration,parallelingcontrastingresponsesofroot pressuretore-wateringassociatedtoosmotic regulation(Knipferet al.,2015).

Withoutanydoubt,thesefactshavespecific, molecularoriginsinthecontextofgraftedplants.

Transcriptomicanalysesintheroottissuesofvarious rootstock-scioncombinationssubmittedtolongterm waterdeficitsupporttheinvolvementofcellwalland osmoticmetabolismsinthevariabilityofresponses amongrootstocks(Peccoux,2011).

3. Aquaporins as key actors in transmembrane water transport

Theabilitytodrivewaterfromroottipstostomata doesnotonlydependonvascularpathways.Water alsofollowsinter-andintracellularpathwaysthatare under the control of water channel proteins embeddedincellmembranes,namedaquaporins (Maurelet al.,2015).Thegenesencodingforsuch proteinshavebeenidentifiedforgrapevine(Fouquet et al.,2008;Sheldenet al.,2009).Theirexpression hasbeenreportedindifferentplantcompartments, variousgenotypesandunderdroughtconditions (Galmeset al.,2007 ;Gambettaet al.,2012 ; Rossdeutsch,2015).Someofthesegenesaremore

expressedinroottipsthaninmorematuresuberized zonesoftherootswheretheradialhydraulic conductivityislower(Gambettaet al.,2013).

Differenceshavebeenreportedamongrootstock genotypesfortheexpressionofthesegenesunder well-wateredanddroughtconditions,orforthe proportionofconductanceunderthecontrolof aquaporins(Lovisoloet al.,2008b;Gambettaet al., 2012;Rossdeutsch,2015).Althoughtheexpression ofsomeaquaporingeneslikeVvPIP1 ;1inroots appearstocorrelatewithhydraulicconductanceand planttranspiration(Vandeleuret al.,2009),the situationinagraftedplantismuchmorecomplex andscioneffectshavetobeconsideredaswell (Tramontiniet al.,2013b ;Rossdeutsch,2015).

Rootstocksalsopresentcontrastingabilitiesto produceABAunderdroughtconditions(Rossdeutsch et al.,2016)andtheinteractionsofchemicaland hydraulicsignalsofsoilwaterstatusfromrootstock toscionshouldbetakenintoaccount.Theroleof ABAinthecontroloftheexpressionandactivityof aquaporinsisnowclearlyestablished(Finkelstein, 2013;Grondinet al.,2015).

4. Genetic architecture for transpiration and growth as controlled by rootstock

Thegeneticarchitectureforwaterdeficitresponses inducedbyrootstockremainspoorlystudied (Marguerit, 2010 ; Margueritet al., 2012).

Specifically,itcanbequestionedtowhatextent transpiration,growthandwateruseefficiencyare geneticallycontrolledbytherootstock.Thisquestion hasbeenaddressedina3-yearexperimentusinga pedigreepopulationissuedfromthecrossbetweenV.

viniferaCabernetSauvignon×V. riparia Gloirede Montpellier made up of 138 individuals.

Transpirationrate,d¹³C(aproxyforwateruse efficiency),transpirationefficiency(ratioofbiomass producedtowatertranspired),waterextraction capacityandtheresponseoftranspirationtowater deficitwerecharacterized.Broadsenseheritability wasabove0.3formosttraits,althoughwith significantyeareffectshighlightingthestrongimpact oftheenvironment.Fewsignificantcorrelationswere foundbetweentraits.Asmentionedaboveforscions, traitsrelatedtogeneticvariabilityinrootstock exhibitedapolygeniccontrolasrevealedbythe detectionofmultipleQTLs.OneQTLforwater extractioncapacitywasidentifiedinthethreeyears onlinkagegroup3,confirmingthehypothesis proposedbyCarbonneau(1985)andSoaret al.

(2006a)thatthistraitwasgeneticallycontrolledat therootstocklevel.Ageneticarchitectureof transpirationplasticitytowaterdeficitwasevidenced whichwaspartiallyindependentfromthegenetic

architectureoftranspirationrate,suggestingan independentselectionprocessforthesetwotraits.

RipariaGloiredeMontpellier,reputedassensitiveto waterdeficit,earlyreduceditssciontranspirationas thesoilwasdrying.Thegeneticarchitecturesofd¹³C and transpiration efficiency were partially independent,underliningthecomplexityofselecting plantmaterialforwateruseefficiency(Condonet al., 2004).Transpirationefficiencyappearedtobeless influencedbyclimatic(year)effectandsoilwater conditions,andcouldthereforebemoreeasilyused forbreeding.TheQTLsdetectedintheoffspring includedgenesthathavebeencharacterizedas potentiallyinvolvedinwaterdeficitresponses (Margueritet al.,2012).Candidategenesrelatedto hormone(notablyABA)andhydraulic(aquaporins) signalingbetweentherootstockandthescionare particularlyinterestingastheyplayamajorrolein waterdeficitresponses(Soaret al.,2006a;Vandeleur et al.,2009).

Thisreviewandotherdatacollectedonrootstocks showthatdroughttolerancemayprobablybe acquiredthroughdifferentmechanisms(Serraet al., 2014 ;Rossdeutschet al.,2016).Thisdiversity shouldbetakenintoaccounttoadaptplantmaterial todifferentsituationsandlevelsofwaterdeficit.

Conclusions

Grapevineresponsetowaterlimitationiscomplex andinvolvesmanyphysiologicalmechanisms.

Geneticvariabilityhasbeendescribedforseveral traitsrelatedtothesemechanismsandmany associatedgenomicregionshavealreadybeen identifiedatthescionandrootstocklevels.Better knowledgeontheroleoffavorableallelesinthese regionswillhelpdesigningadequateplantmaterialto dealwiththeincreasedriskofdroughteventsinthe contextofclimatechange.

Acknowledgments:Thisworkwassupportedby fundingfromtheprojectLong-TermAdaptationto Climate Change in Viticulture and Enology (LACCAVE)oftheFrenchNationalInstitutefor AgriculturalResearch(INRA).

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