Plant responses to flooding stress

Plant

responses

to

flooding

stress

Elena

Loreti

1

,

Hans

van

Veen

2

and

Pierdomenico

Perata

2

Mostplantspeciescannotsurviveprolongedsubmergenceor

soilwaterlogging.Cropsareparticularlyintoleranttothelackof

oxygenarisingfromsubmergence.Ricecaninsteadgerminate

andgrowevenifsubmerged.Themolecularbasisforrice

tolerancewasrecentlyunveiledandwillcontributetothe

developmentofbetterricevarieties,welladaptedtoflooding.

Theoxygensensingmechanismwasalsorecentlydiscovered.

Thissystemlikelyoperatesinallplantspeciesandreliesonthe

oxygen-dependentdestabilizationofthegroupVIIethylene

responsefactors(ERFVIIs),aclusterofethyleneresponsive

transcriptionfactors.Anhomeostaticmechanismthatcontrols

geneexpressioninplantssubjectedtohypoxiaprevents

excessiveactivationoftheanaerobicmetabolismthatcouldbe

detrimentaltosurvivingthestress.

Addresses

1_{InstituteofAgriculturalBiologyandBiotechnology,CNR,Pisa,Italy} 2

PlantLab,InstituteofLifeSciences,ScuolaSuperioreSant’Anna, 56124Pisa,Italy

Correspondingauthor:Perata,Pierdomenico(p.perata@sssup.it)

CurrentOpinioninPlantBiology2016,33:64–71

ThisreviewcomesfromathemedissueonCellsignallingandgene regulation

EditedbyKimberleySnowdenandDirkInze´

http://dx.doi.org/10.1016/j.pbi.2016.06.005

1369-5266/#2016ElsevierLtd.Allrightsreserved.

Introduction

Althoughplantsproduceoxygenthroughphotosynthesis, thelackofanefficientsystemtotransportoxygento non-photosynthetic organs implies that these organs canbe deprivedof oxygeniftheiranatomylimits oxygen diffu-sionfrom outside [1,2]. Additionally, complete submer-genceoftheplantbyfloodingeventsmayalsoleadto low-oxygenavailabilityintheabovegroundorgans,especially when water turbidity limits photosynthesis [3]. When oxygenbecomeslimitingforrespirationplantsexperience hypoxia,whilstthecompleteabsenceofoxygen(anoxia)is evenmoredetrimentaltoplantsurvival.Bothhypoxiaand anoxia trigger extensivereprogramming of gene expres-sion, with induction of the fermentative metabolism, allowingtheplant to use glycolysis for ATPproduction [1].Climatechangeswillleadtoextremesinwater avail-abilitythatwillcauseseveredroughtinsomeareas,while

floodingdue to extremerainfall eventswill affect other geographicalareas[4].Unlessnew cropvarietiesable to withstandabioticstressesaredeveloped,productivitywill begravelyaffected.Untiladecadeagolittlewasknown aboutthegenesthatconfertolerancetosubmergence,and itisonlyduringrecent yearsthatlighthasbeenshedon the molecular mechanisms behind oxygen sensing and signallinginplants[2].Inthisreviewwewillhighlightthe mostrecentfindingsinthefieldofplantanaerobiosis,from ecophysiologyofplantsgrowinginwetlandstothe trans-lationofdiscoveriesmadeinArabidopsistocrops.

Flooding

in

the

wild

Floodingisanaturaloccurrenceinmany ecosystemsand thereforemanywildspeciesaresuperblyadaptedtowatery conditions.Hereimprovedgasexchangewiththe environ-mentisessentialtoavoidhypoxiawithintheplant.Tothis end,plantscaninduceand/orconstitutivelydevelop aeren-chyma,longitudinalconnectedgasspaces,whichprovidea rapid means of aerial gas exchange over long distances withintheplant[5].Thisisusuallycombinedwithachange inrootarchitecturetominimizethedistance(andtherefore diffusive resistance) between the aerial surface and the flooded root tips [6], for instance via adventitious roots, whichcan createa collection of air conducting snorkels originatingfromthehypocotylorstemintotheanaerobic substrate.Oftenaerenchymaarecombinedwithabarrier thatpreventsoxygenleakageintothesurrounding anaero-bicsoil,whichdrasticallyimprovesfloodingtolerance[7]. An extensiveaerenchyma system is extremely effective underwaterloggedconditionswheretheshootremainsin aerialcontact and can thus funnel airdown to the root. Duringcompletesubmergence,however,the shootdoes not make aerial contact oxygen, their effectiveness in funnelling air towards the roots is greatlycompromised. Insuchcases,somewetlandplantspecies,inanattempt toregainaerialshootcontact,displayrapidvertical elonga-tion of leaves, internodes or petioles to snorkel for air. This escape strategy is observed in some rice varieties (seebelow), aswellas in severalotherplantspecies[8]. Inanalternativestrategytheplantaimstoenterastateof inactivity (quiescence), to be revived once the flood recedes[9,10].Thisisalsoadifficulttacticasenergyand carbonutilisationshouldbekepttoaminimumtomake reserveslastalongtime,whilsttheyshouldsimultaneously besufficienttomaintaincellularintegrity(Figure1a).

The

submerged

plant:

low

oxygen

and

high

ethylene

Because of its gaseous nature ethylene hardly leaves the plant under flooded conditions and thus rapidly

accumulates inside the plant. It is therefore a highly reliable andrapid cueforplants todetecttheir predica-ment[11].Anothersignalistheoxygenavailability.The internal level of these gases is abalance between con-sumption,productionanddiffusiveresistance.Therefore active,heterotrophicorcompacttissue,suchasmeristems androots,willrapidlyexperiencelowoxygenupon flood-ing. Inphotosynthetic tissue theconsumption and pro-ductionofoxygenisdependentonlightconditions,and thus alsotheoxygenavailability.

Ethylene is the primary signal for most adaptations to flooding.EthylenemodulatesahormonalcascadeofABA, GAandultimatelyauxintoinduceadventitiousrootingin tomato,Solanumdulcamarum,andrice,and[12–14]. How-ever,rootemergencealsorequiresethyleneinduceROS formationintheepidermalcells,leadingtotheircelldeath toallowrootpenetration[15].Similarly,lysigenous aeren-chymaformation,whichisformedbyapoptosisofspecific cellsinthecortex,involvesanethylenedependentdropin antioxidant activity. The subsequent increase in ROS leads to the required cell death [16–18]. Interestingly, theimportantsuberinbasedoxygenbarrierisnotaffected byethylene,butlikelycausalgenesinvolvedinits forma-tion have been identified [19]. The escape strategy to reachthewatersurfaceisalsoethylenedriven.However, downstreamsignallingisconsidereddivergentintheplant kingdom,asitwasfoundtoactviagroupVIIERFsinrice (see below), but via genes typical of low light induced elongationinRumexpalustris[20–22].Remarkably, ethyl-ene pre-treatment induced anoxia tolerance of Rumex palustris was associated with enhanced hypoxia related gene expression.A behaviour thatwas absent in Rumex acetosa, a species that experience fewer flooding events and employsaquiescence insteadof an escapestrategy [20]. This highlights the importance of a link between ethyleneandhypoxicsignallingpathways.

The high levels of ethylene associated with flooding inhibit root elongation, but through the formation of aerenchyma the excessive ethylene is easily removed. However,speciesthatareineffectiveinproducing aeren-chymathereforeexperiencestrongrootgrowthreduction under flooded conditions[23]. The strong dose depen-dencyofethylenesignalling[24]mightplayanimportant roleinitscontrastingdevelopmentalrolesduringflooding

(Figure 2).Toavoiddetrimentaleffectsassociatedwith

highlevelsofethylene,someofthespeciesthat continu-ously occupy aquaticor flood-prone environments have Figure1 (a) flooding ethylene entrapment adventitious root formation root elongation Iysigenous aerenchyma ↑ ROS localized cell death in root cortex photosynthesis

escape_quiescence escapequiescence short term long term

reserve mobilisation glycolytic flux shoot elongation carbon starvation adv. roots/ aerenchyma O₂ levels ↑ NADPH-oxidase ↓ metallothionein ↓ ABA ↑GA, IAA

↑ epidermal ROS

(b)

Current Opinion in Plant Biology

Ethyleneisapivotalregulatorgrowthsurvivalstrategies(a)androot development(b)duringsubmergenceandwaterlogging.During completesubmergence,ethyleneinducedgrowthstrategiesare paramounttosurvival(a),butbothhavedifferentshorttermandlong termeffectsonplantperformance,especiallysinceunderlongterm submergenceescapingplantswillhaveregainedaerialcontact. Naturally,photosynthesisisseverelyreducedbyflooding,butthrough anescapestrategysomephotosynthesiscanberecoveredthrough there-establishmentofaerialcontact.Thissubsequentlyreducesthe needforreservemobilisationandlimitsoxygenshortagevia aerenchyma.Initially,escapingplantswillhavelowinternalO2levels, duetotheirhighmetabolicactivitywhichisfuelledbyastrong glycolyticfluxandreservemobilisation.Thesehighdemands, generallymeanescapingplantssufferstronglyfromcarbonstarvation. Thoughalltheseeffectsareamelioratedonceaerialcontactismade. Becausequiescentplantshavelowactivity,theirrequirementson reservesandenergyarelimited.Subsequently,internalO2levels wouldbeatahighersteadystateandcarbonshortagewouldbe considerablelower.However,quiescentplantsstillrelyonreserve mobilisationtosustaincellularfunctions,bothduringshorttermand longtermflooding.Rootdevelopmentisalsoessentialtosurvive floodedconditions.Theaqueousenvironmentpreventsethyleneto readilyleavetheplanttissuesthroughgasdiffusion.Thisethylene entrapmentstartsacascadethatleadsachangeinrootarchitecture (b),throughforinstancetheformationofadventitiousroots.This includesahormonalcascadeandROSinducedepidermalcelldeath.

Simultaneously,highlevelsofethyleneinsubmergedroots,inhibitroot elongation.However,ethylenealsoleadstoadropintheantioxidant metallothioneinandanincreaseNADPHoxidase,whichtogetherleads toanaccumulationofROS.ROSactsasasignalforprogrammedcell deathofspecificcortexcells,eventuallyleadingtotheformationof lysigenousaerenchyma.Asaresult,theimprovedgasdiffusioncan removehighethylenelevelsandthusreleasestheinhibitiononroot elongation.

lostorreducedtheircapacitytoeitherproduce,senseor respondto ethylene[24,25].

Darkness,atypicalcomponentoffloodinginmurkywater, is responsible for a large portion of the transcriptomic changes observed during complete submergence in the darkinArabidopsis[26].Thisindicatesthatacclimationto flooding,atleastindarkconditions,predominatelyoccurs viasugarandenergysignalling,asalsowasshowninrice [27].Wherethecontributionofhypoxiainregulatinggene expressionindarksubmergenceacclimationcanbeminor, hypoxia regulated gene expression is correlated, either positivelyor negatively,to floodingtolerance in natural variationofArabidopsis,RumexandRorippa,whichmakes itanimportantareaof study[20,26,28].

Flooding

in

the

field:

rice

Rice is remarkably well adapted to submergence

(Figure 2) and can even germinate in the complete

absence of oxygen [29]. This anaerobic germination (AG)includesalengtheningofthecoleoptile,that, anal-ogoustotheescapestrategy,aimstomakeaerialcontact butconsiderablevariationexistsamongricegenotypesin coleoptileextensionduringanoxia[29].Differentlyfrom other cereal seeds that fail to induce the a-amylase enzymes required for starch degradation under anoxia, ricecaryopsesproducethisenzyme,whichallowsstarch degradationcoupledtothefermentativemetabolismand subsequentgermination[30–32].Therapiddepletionof solublecarbohydratesoccurringduringthefirsthoursof germinationunderanoxia,togetherwithapossible low-oxygen dependent change in calcium levels, leads to a signalling cascade that finally leads to a-amylase Figure2 (a) O₂ O₂ Gibberellin α-Amylase α-Amylase Starch Germination Sugar starvation T6P Trehalose Sucrose Glucose Anaerobic metabolism Germination Air Submergence Ethylene Gibberellin Elongation Growth SK1, SK2 SUB1A Starch CIPK15 OsTPP7 Glucose Aerobic Respiration (b) (c)

Current Opinion in Plant Biology

Ricegerminationandgrowthunderaerial(a)andsubmerged(b) conditionsisregulatedatdifferentlevels,dependingonthegenotype aswellasthegrowth-stage.Ricegerminationunderanoxiaisvery peculiar,withrapidcoleoptileelongation(a,b).Onlyoncethewater surfaceisreachedandthecoleoptilecanactasasnorkeldotheroot andprimaryleafdevelop.Germinationunderanoxiaisextremely challengingbecauseATPcanonlybeproducedthroughtheactivityof glycolysiscoupledwithethanolicfermentation,whichyieldsonlya fractionoftheATPproducedbymitochondrialrespiration,ready accesstostarchreservesisthusessential.Underanoxiaorhypoxia starchdegradationthroughthegibberellin-induceda-amylasepathway

cannotoccurbecauseoxygenisrequiredforgibberellinsynthesis(a) andalsobecausericefailstorespondtogibberellinsunder low-oxygenconditions.Inanaerobicallygerminatingricevarietiesthe low-oxygenconditions(b)requirestarchdegradationthroughtheactionof a-amylases,someofwhichareinducedbysugarstarvation,rather thangibberellin,andinafeed-backmannerisrepressedbyincreased availabilityofsugars.Thisfeedbackloopbetweensugarstarvation anda-amylaseactsviaapathwayrequiringCIPK15.Viableanaerobic germinationrequiresOsTPP7toreducetheperceptionofsugarsso thatsugarinducedinhibitiona-amylaseisprevented,resultingina strongfluxsugarsreleasedviastarchdegradation.Thisallowsriceto feedtheanaerobicmetabolismwithsugarsandobtainenoughATPto supportgermination.Inadultriceplants(c)differentstrategiesare observedthatallowthericeplanttosurvivesubmergence.

Submergenceresultsinethyleneaccumulation,thatinducesSUB1Ain genotypespossessingthisgene.SUB1Arepressesgrowthof submergedplants,thusallowingtheplanttopreservecarbon reserves,whichinturnwillallowre-growthoftheplantwhenthewater recedes.InsteadindeepwaterricevarietiesethyleneinducestheSK genes,whichinducefaststemelongation.Thisresultsinan‘escape’ strategythatallowstheplanttokeepitsleavesabovethewater surface,thusallowingoxygentobetransportedtothesubmerged partsoftheplantthroughtheaerenchyma.Ricevarietiesthatdonot possesseitherSUB1AorSKgenesdisplayanintermediate phenotype,withslowstemelongationthatdepletestheplantfrom carbonresourceswithoutallowingtogainaerialcontact.

production. Thisprocessbegins withtheactivationof a Calcineurin B-like (CBL), whichtargets theprotein ki-naseCIPK15,whichinturntriggerstheSnRK1Apathway that induces the MYBS1transcriptionfactor which acti-vates the starvation-inducible a-amylase gene RAmy3D [27].Thereisconsiderablevariationamongstricevarieties in their ability to successfully germinate and establish when submerged in the field, though most activate RAmy3D during this anaerobicgermination. AG of rice allowsdirectsowinginsteadof transplanting,whichisof great importance as it makes rice cultivationmore eco-nomically sustainable[33]. A QTL analysis identified OsTPP7asthelocusresponsibleforefficientAG.OsTPP7 encodes a trehalose-6-P-phosphate (T6P) phosphatase, which is non-functionalin ricevarieties thatare unable toestablishundersubmergedconditions[33].The pres-enceoftheOsTPP7inriceaccessionswascorrelatedwith increasedsinkstrengthofelongatingcoleoptiles,resulting in prolonged tolerance to complete submergence. High sucrose results in high T6P levels and consequentlyin repression of SnrK1 and downregulation of a-amylases. DuringanaerobicgerminationOsTPP7misleadsthe seed-lingabout itssugarstatus byconvertingT6Pinto treha-lose. Subsequently the rice seedling can maintain a relativehighsugaravailabilitybutlowT6Plevels,which, ifhigh,wouldrepressa-amylases(Figure2b).The subse-quent intenseflux ofglucose fromstarchdegradation is essential for fuelling glycolysis and lengthening of the coleoptile.Ricegerminationunderanoxiaisthereforethe consequence of clever sugar management, that allows adept accesstostarchreserves[34].Tothisaimthefine tuningofsugarsensingbykeepinglowerT6Plevelsfora givensucroseconcentrationbythelow-oxygeninducible OsTPP7appearsto beessential[33].

In some areas of Asiasubmergence occursvery rapidly and lasts for months, here rice varieties named ‘deep-water rice’ are grown. The adult plant continues to snorkel for air and keeps up with the increasing water level. This trait relies on two group VII ERF genes: SNORKEL1andSNORKEL2(SK1,SK2)[22].Only pres-entindeepwaterricevarieties,theyactivatea gibberel-lin-dependentinternodeelongation,upto25cmperday, sufficienttomaintainanaerialcontactwithsomeofthe leaveswhichallowairtransfertothesubmergedpartsof theplant viaaerenchyma (Figure 2c).

Clearlythesuccess ofriceinfloodedhabitatsisdueto its abilitytorapidlyregainaerialcontact[35]. Interest-ingly, only a few rice varieties can survive complete submergence for an extended period of time, a phe-nomena that regularly occurs in so-called flash-floods. These varieties survive thanks to the group VII ERF gene SUB1A [36], whose product positively regulates the fermentation capacity, but represses plant growth by restrictinggibberellin-signalling [37,38]. Therefore, rice varieties that survive complete submergence

activate, through SUB1A, a quiescence strategy that allows them to reduce carbohydrate use to the mini-mumrequiredforkeepingtheplantalive,whileitwaits for water to recede, to continue aerial growth [39]

(Figure 2c).

Flooding

in

the

lab:

Arabidopsis

and

the

N-end

rule

pathway

for

oxygen

sensing

Arabidopsis is nothighly tolerant to submergence [40], neverthelessitmadethediscoveryofoxygensensingand signallingmechanismspossible[41].Besidestheclassical anaerobic genes, several HYPOXIA-RESPONSIVE UN-KNOWN PROTEIN (HUP) genes were identified [42], representingpossiblyinterestingelementsinthe anaero-bicresponsepathway.Furthermore,anatlasof hypoxic-dependent gene expression in specific cell types was producedand revealed aset ofapproximately 50genes that were activated regardless of their cellular identity [43].Thisprovidesanenormous amountof information thatcouldbeexploitedto elucidatethesignalling path-waybehindtheresponseofplantstolowoxygen.Therole of group VII ERFs in rice prompted research on this gene-familyinArabidopsis,inwhichthegroupVIIERFs are five[44],with theinitialidentificationof two HYP-OXIA-RESPONSIVE ERFs (HRE1andHRE2) which contribute to hypoxia tolerance and signalling [45]. RAP2.12, another group VII ERF, is not induced by hypoxia,but neverthelessactivates ADH[46].RAP2.12 isregulatedbyoxygenattheproteinlevel,withoxygen provokingitsdegradation[47,48].Onlyunderlowoxygen areRAP2.12 andtheothertwoconstitutivelyexpressed groupVIIERFs,RAP2.2andRAP2.3,stableand redun-dantlyactivatethecoreanaerobicresponse[49,50].This oxygensensingmechanismreliesonthe oxygen-depen-dentoxidationofthegroupVIIERFN-terminalcysteine (Cys),mediatedbythePLANTCYSTEINEOXIDASE (PCO)enzymes[51].TheoxidisedCystargetsRAP2.12 to the proteasome through an N-end-rule pathway of ubiquitinmediatedproteolysis(Figure3).Interestingly, also nitricoxide(NO) isabletoinduce groupVIIERF degradation, indicating thatthis pathway might also be involvedin otherprocessesincludingseedgermination, stomatal closure, and hypocotyl elongation [52]. Re-markably,oxygensensing throughgroupVIIERFswas showntocoordinatephotomorphogenesisduringseedling development[53].Itispresentlyunknownwhetherand how group VII ERF cysteine oxidation requires both PCOs andNO.

The RAP2.12 dependent activationof thedownstream genesisessentialtosurvivesubmergence,butalsoneeds to be finely tuned. The HYPOXIA-RESPONSE AT-TENUATOR1 (HRA1)is atrihelixtranscription factor thatrepressestheactionofRAP2.12.HRA1gene expres-sion is itself activated by RAP2.12 stabilization under hypoxia, indicating the existence of an homeostatic mechanism for regulating theanaerobic response, such

thatitdoesnotharmfullyexceedtheneedsoftheplant [54].Interestingly, alsohydrogenperoxideproduction underanoxiaoccursduringtheearlyphasesofthestress [55]. Recently, a protein interconnecting the oxygen-sensingmachinerywithROSproductionwasidentified.

HYPOXIA-RESPONSIVE UNIVERSAL STRESS

PROTEIN1(HRU1)isinducedbythe oxygen-respon-sive N-end-rule pathway and affects ROS production, possibly throughan interaction witha membrane-local-izedNADPH-oxidase(RBOHD)anditsregulatorROP2 [56].Overalltheserecentfindingssuggestthat hypoxia-dependent signalling is tightly controlled via various signals and proteins in a highly connected network. It istemptingtospeculatethatexcessiveactivationofthe fermentativepathwaybyRAP2.12maydepletesugarsto a level that induces severe starvation, hampering long termsurvivalandrecoveryfromhypoxia.Ahighly coor-dinated network, including HRA1 and HRU1, could preventsuchadetrimentalscenario.

Translating

lab

research

into

better

crops

The identification of SUB1A as the determinant for submergence tolerance in rice allowed the breeding of flood-tolerant rice varieties, often called ‘scuba rice’

[4,57,58]. These varieties showed the same yield and

qualitytraitsastheirnon-Sub1counterpartswhengrown undernon-floodedconditions,butdisplayedyield advan-tagesof 1to morethan3tha 1after complete submer-genceforvariousdurations[59].Thisisagreatexampleof rapidtranslationofascientificdiscoveryintoagricultural improvementsinlessthantenyearssincethediscoveryof SUB1Ain2006[35].Experimentalevidenceshowingthat SUB1A also contributes to drought tolerance in rice suggeststhatthistraitwillcontributetothedevelopment of ricevarieties better adaptedto climatechanges[60]. Incorporatingfloodingtoleranceintocropsotherthanrice willbeverychallenging,giventhelackofaccessionswith flooding tolerance traits. However,the discoveryof the oxygen sensing mechanism in Arabidopsis could show Figure3

Anaerobic Gene Expression

O₂ O₂ Sucrose Starch Glucose Hypoxia NAD Glycolysis NAD NAD NADH ATP ATP Pyruvate Ethanol Acetaldehyde ADP ADP Aerobic respiration NADH H₂O₂ RAP2.12 SuSy RAP2.12 RAP2.12 PROTEASOME PCO NO HRA1 PDC ADH HRU1 RBOHD ROS Gene Expression

Current Opinion in Plant Biology

Anaerobicsignalling(left)andmetabolism(right)inArabidopsis.Underconditionsofhypoxiaoranoxiarespirationinthemitochondriaisseverely impaired.NADHregenerationtoNAD,requiredtoallowglycolysistoproceed,thusoccursthroughtheactivationofPDCandADH.Starch metabolismandsucrosemetabolismthroughsucrosesynthase(SuSy)providethecarbonunitsrequiredforglycolysis.SuSy,PDC,ADHare examplesofenzymesencodedbyanaerobicgenes,whoseactivationistriggeredbyhypoxia.OxygensensingoccursthroughERF-VIIgenessuch asRAP2.12andRAP2.2(thelatternotshowninfigure)thatareunstableunderaerobicconditions,becausePCOenzymesoxidisetheN-terminal Cysresidue,resultingindegradationofRAP2.12bytheproteasome.Nitricoxide(NO)alsoinducesdegradationofERF-VIIproteins.RAP2.12 inducestheexpressionofanaerobicgenes,amongwhichisalsoHRU1,whichcontrolshydrogenperoxideproductionbyRBOHD.Theinteraction ofRAP2.12withHRA1dampenstheactionofRAP2.12.

great promise for crop improvements. However, both strong and weak hypoxic signalling, that is very large versusmoderateinductionofgroupVIIERFtargets,has beenconnectedtofloodingtolerance[20,26,28,47,48,61]. Nevertheless,barley withreducedexpression ofthe N-end-rule pathway E3 ligase PROTEOLYSIS6 (PRT6) showsincreasedtolerance towaterlogging[62]. Incorporating traits from the superblyadapted wetland specieswillinvariablybechallenging,butcouldprovide bigleapsinfloodingtolerance.Aerenchymaformationisa developmentally complextraitand sofarwehavebeen unable to import this trait into a species that did not possessitalready.Moreover,maizedevelopsaerenchyma uponwaterlogging,butdespitethisabilityitstillsuffers stronglyfromsoilflooding.Otherchangesinroot devel-opment,suchasenhancedadventitiousrooting,mightbe morepromisingandpliabletoourcrops,asthesetraitsare often alreadypresent tosomeextent.

Tolerancetosubmergenceincludesthedelicatebalance between theinductionof the fermentative mechanism, that represents a requirement for basal tolerance, and othermechanismspreventingcarbonstarvationand oxi-dativestress.Onlyafterwehaveacompletepictureofthe manytolerancetraitswillthedevelopmentofcrop varie-tiestoleranttowaterloggingorsubmergencebefeasible.

Acknowledgement

ThisworkwassupportedbyScuolaSuperioreSant’Anna,Pisa,Italy.

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and

recommended

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