CorrespondencenakazonoagrnagoyauacjpLaboratoryofPlantGeneticsandBreedingGraduateSchoolofBioagriculturalSciencesNagoyaUniversityFurochoChikusaNagoya4648601Japanetalhttpwwwthericejour ID: 183676
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REVIEWOpenAccessMechanismsforcopingwithsubmergenceandwaterlogginginriceShunsakuNishiuchi,TakakiYamauchi,HirokazuTakahashi,LukaszKotulaandMikioNakazonoAbstractRice(OryzasativaL.),unlikeothercereals,cangrowwellinpaddyfieldsandishighlytolerantofexcesswaterstress,fromeithersubmergence(inwhichpartoralloftheplantisunderwater)orwaterlogging(inwhichexcess *Correspondence:nakazono@agr.nagoya-u.ac.jpLaboratoryofPlantGeneticsandBreeding,GraduateSchoolofBioagriculturalSciences,NagoyaUniversity,Furo-cho,Chikusa,Nagoya464-8601,Japanetal ©2012Nishiuchietal;licenseeSpringer.ThisisanOpenAccessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperlycited. totheinternalaerationduringsubmergence,thereby increasingsubmergencetoleranceinrice(Colmerand Pedersen2008b;Pedersenetal.2009;RaskinandKende 1983). Manylowlandricecultivars,despitehavinganability ofinternalaeration,arestill sensitivetocompletesub- mergence.Theirleavesandstemsmoderatelyelongate undercompletesubmergencetoreachtheair-water interface,buttheirelongationgrowthcanexhaust energyreservesandcausedeathwhentheflooding depthisdeepandthefloodingperiodislong(Bailey- Serresetal.2010;JacksonandRam2003).However, somecultivarsusetwodistinctstrategiesofgrowthcon- trolstosurviveundersubmergedconditions.Oneofthe strategiesisaquiescencestrategy[ i.e .,thelow-oxygen quiescencesyndrome(Col merandVoesenek2009)] (Figure1),inwhichshootelongationissuppressedto preservecarbohydratesforalongperiod(10-14days) underflash-floodconditions.Submergence-tolerantcul- tivarscanrestarttheirgrowthduringdesubmergenceby usingpreservedcarbohydrates.Anotherstrategyisan escapestrategy[ i.e .,thelow-oxygenescapesyndrome (Bailey-SerresandVoesenek2008;ColmerandVoese- nek2009)](Figure1),whichinvolvesfastelongationof internodestoriseabovethewaterlevelandisusedby deepwaterricecultivars.Bothstrategiesdependonethy- lene-responsivetranscriptionfactors(Hattorietal.2009; Xuetal.2006). Figure1 Strategiesofadaptationtoexcesswaterstressesintheformofsubmergenceorwaterlogginginriceplants .Ricecanadapt tosubmergencebyinternalaerationandgrowthcontrol.Forinternalaeration,ricedevelopslongitudinallyformingaerenchymaandleafgas films.Ontheotherhand,somericecultivarscansurviveundersubmergencebyusingspecialstrategiesofgrowthcontrol:aquiescencestrategy oranescapestrategy.The Submergence-1A ( SUB1A )geneisresponsibleforthequiescencestrategy,whichisimportantforsurvivalunderflash- floodconditions.The SNORKEL1 ( SK1 )and SNORKEL2 ( SK2 )genesareresponsiblefortheescapestrategy,whichisimportantforsurvivalunder deepwater-floodconditions.RicecanadapttosoilwaterloggingbyformingaerenchymaandabarriertoradialO 2 loss(ROL)intheroots. Nishiuchi etal . Rice 2012, 5 :2 http://www.thericejournal.com/content/5/1/2 Page2of14 Themainadaptationoflowlandricetosoilwaterlog- gingistheformationofaerenchyma,whichpermits relativelyunhinderedtransportofO 2 fromwell-aerated shootstosubmergedroots(Figures1,2;Armstrong 1979;JacksonandArmstrong1999).Longitudinaldiffu- sionofO 2 towardstherootapexcanbefurther enhancedbyinductionofabarriertoradialO 2 loss (ROL)thatminimizeslossofO 2 tothesurrounding environment(Figures1,2).Furthermore,thisbarrier mayimpedethemovementofsoil-derivedtoxins( i.e ., reducedmetalions)andgases( e.g .methane,CO 2 ,and ethylene)intotheroots(Armstrong1979;Colmer 2003a;Greenwayetal.2006).Bothuplandandlowland ricespeciesusethesetraitsunderwaterloggedcondi- tions(Colmer2003b). Somerecentreviewssummarizedthemechanismsof floodingtoleranceinplants(Bailey-SerresandVoesenek 2008;Bailey-Serresetal.2010;ColmerandVoesenek 2009;Hattorietal.2011;Nagaietal.2010).Inthisreview, weincluderecentdiscoveriesthatwerenotcoveredinthe previousreviewsandsummarizewhatisknownaboutthe physiologicalandmolecularmechanismsthatcontribute totoleranceto,oravoidanceof,submergence( i.e .,internal aerationandgrowthcontrols)andalsoadaptationto waterlogging( i.e .,formationsofaerenchymaandabarrier toROL)inriceandothergramineousplants. Internalaerationinsubmergedplants Effectiveinternalaerationinplantsiscrucialtosurvive undersubmergence.Inrice,aerenchymaiswelldeveloped Figure2 DifferencesinlysigenousaerenchymaformationandpatternsofradialO 2 loss(ROL)inricerootsunderdrainedsoil conditionsandwaterloggedsoilconditions .Underdrainedsoilconditions,lysigenousaerenchymaisconstitutivelyformed,butabarrierto ROLisnotformed;thusROLatthebasalpartoftherootdecreasesO 2 diffusiontotheapicalpart.Bycontrast,underwaterloggedsoil conditionslysigenousaerenchymaformationisenhancedandformationofthebarriertoROLisinduced,resultinginthepromotionof longitudinalO 2 diffusiontotherootapex.Underdrainedsoilconditions,lysigenousaerenchymaisconstitutivelyformedatthebasalpartofthe roots(a),butitisnotusuallyformedattheapicalpartoftheroots(b).Underwaterloggedsoilconditions,lysigenousaerenchymaisinducedat thebasalpart(c)andtheapicalpart(d)oftheroots.Lysigenousaerenchymaismorehighlydevelopedatthebasalpartoftheroots(a,c)than attheapicalpart(b,d).ArrowthicknessreflectstheamountofO 2 available.Ep,epidermis;Ex,exodermis;Sc,sclerenchyma;Co,cortex;En, endodermis. Nishiuchi etal . Rice 2012, 5 :2 http://www.thericejournal.com/content/5/1/2 Page3of14 inroots,internodes,sheaths,andthemid-ribofleaves(ColmerandPedersen2008a;Matsukuraetal.2000;Steffensetal.2011)andcontributestotheeffectiveinter-nalaerationbetweenshootsandroots(Colmer2003a;ColmerandPedersen2008a).SubmergedleaveshavegasfilmsthataidOandCOexchangebetweenleavesandthesurroundingwater,andthusincreaseunderwaternetphotosynthesisbysupplyingCOduringtheday(underlightconditions)andpromoteOuptakeforrespirationatnight(ColmerandPedersen2008b;Pedersenetal.2009;RaskinandKende1983).Asaresult,leafgasfilmscontri-butetoleafsugarproductionbyphotosynthesiswhenunderwater,andinturnshootandrootdrymass(Pedersenetal.2009).RemovalofleafgasfilmscausedadecreaseofOpartialpressure(pO)inrootswhenshootswereindarkness,suggestingthatleafgasfilmspartiallycontributetoOtransportfromshoottoroot(Pedersenetal.2009;Winkeletal.2011).Takentogether,thesefind-ingsindicatethatleafgasfilmsareimportantforsubmer-gencetoleranceinrice(Pedersenetal.2009;RaskinandKende1983).Strategiesofadaptationtoflash-floodconditionsCatling(1992)definedsubmergencetoleranceasabilityofariceplanttosurvive10-14daysofcompletesubmergenceandrenewitsgrowthwhenthewatersub-sides;thereisnostemelongationduringsubmergence.Underthisdefinition,submergencetoleranceindicatesflash-floodtolerance.Generally,theseedlingsofmanylowlandricecultivarselongatetheirleavestogetoxygenatthewaterssurfaceundersubmergedconditions.However,becausethisshootelongationrequireslargeamountsofenergy,mostricecultivars(.,flash-flood-intolerantcultivars)havepoorabilitytorecoverfullyafterthewaterrecedesandeventuallysustainseveredamageordie(JacksonandRam2003).Bycontrast,theflash-flood-tolerantEastIndianricecultivarFR13Ashowsrestrictedshootelongationandreducedenergyconsumptionundersubmergence(SetterandLaureles1996).TheenergyinFR13Aplantsispreservedduringsubmergence,andupondesubmergencetheirgrowthcanberestartedbyusingthisenergy(Fukaoetal.2006;Singhetal.2001).Thereisthereforeanegativecorrela-tionbetweenshootelongationandsurvivalrateundercompletesubmergence(SetterandLaureles1996).FR13AhastheSubmergence-1SUB1)locusonchro-mosome9(XuandMackill1996).Xuetal.(2006)dis-coveredthatthelocuscontainsSUB1BSUB1C,allofwhichencodeethyleneresponsefac-torsandareupregulatedundersubmergence,butonlySUB1Aisresponsiblefortheflash-floodtolerance.Thenear-isogeniclineM202(SUB1),whichwasgeneratedbyintrogressionoftheSUB1regionfromFR13Aintotheflash-flood-intolerantcultivarM202,showsrestrictedshootelongationundersubmergence,asdoesFR13A(Bailey-Serresetal.2010;Fukaoetal.2006;Xuetal.2006).Topreserveenergyandcarbohydrates,M202(SUB1)suppressestheexpressionofgenesencod--amylaseandsucrosesynthase,whichareinvolvedinstarchandsucrosemetabolism(Fukaoetal.2006).Inaddition,positivelyregulatesthegenesinvolvedinalcoholfermentationandthuspromotesacclimationofplantstoflash-floodconditions(Fukaoetal.2006).FukaoandBailey-Serres(2008)reportedthatalsoenhancestheexpressionofgenesencodingSLEN-DERRICE-1(SLR1)andSLR1like1(SLRL1),whicharekeyrepressorsofgibberellin(GA)signalinginrice;italsonegativelyregulatestheGAresponseinordertorestrictshootelongationundersubmergence.Recently,itwasshownthatSUB1Aexpressionisalsoinducedbydroughtandoxidativestressupondesubmergence(Fukaoetal.2011).SUB1ApositivelyregulatestheexpressionsofgenesinvolvedinABA-mediatedacclima-tiontodroughtconditions.Moreover,underoxidativestress,SUB1Apromotestheexpressionofgenesrelatedtothedetoxificationofreactiveoxygenspecies(ROS)andreducestheaccumulationofROS.Asaresult,M202()hasahigherdroughtandoxidativetoler-ancethanM202(Fukaoetal.2011).Inrain-fedricefields,inadequatewatermanagementispronetocausefloodinganddrought.Thus,assubmergenceanddroughtstressescancauseseveredecreasesinricepro-ductioninrain-fedricefields,introgressionofthegeneintoricecultivarsintolerantofsubmer-genceanddroughtisapromisingwayofincreasingriceproductivityinthesefields(Fukaoetal.2011).Strategiesforadaptationtodeepwater-floodconditionsDeepwaterfloodinglastsforseveralmonths,andOdeficiencycausesenergydepletioninplants.Tosurviveunderdeepwater-floodconditions,riceplantsmustescapefromtheflooding.Auniquetraitofdeepwaterriceisthatitsinternodesrapidlyandsubstantiallyelon-gatetoavoiddeepwaterflooding.Remarkably,somedeepwaterricecultivarscanincreasetheirheightby25cm/day(Vergaraetal.1976).Thisrapidelongationallowstheleaftipstoextendabovethewatersurfaceandenablesthericeplantstoefficientlyphotosynthesizeandexchangegasesforrespiration(Bailey-SerresandVoesenek2008).Duringinternodeelongation,ethylenebiosynthesisisactivatedandtheaccumulatedethyleneregulatestheincreasesinGAcontentanddecreaseinABAcontent.AsinternodeelongationispromotedbyGAorrepressedbyABA,theincreasedGA/ABAratiocontributestotheelongation(Kendeetal.1998;Sauter2000).Indeed,GAactivatestheexpressionofcelldivi-sion-relatedgenes(Sauteretal.1995;vanderKnaapetal.1997),andthusactivecelldivisionisobservedatetalhttp://www.thericejournal.com/content/5/1/2Page4of14 theintercalarymeristemintheinternodeundersubmer-gence(MétrauxandKende1984).Moreover,highlevelsofexpressionofgenesencodingexpansin,whichisinvolvedincell-wallloosening(ChoandKende1997a,b,c;LeeandKende2001),andchangesintheorienta-tionofcellulosemicrofibrilsareobservedintheinter-nodeduringinternodeelongation(Sauteretal.1993).Aerenchymaformationoccursintheinternodessimul-taneouslywiththeirelongation,andisenhancedbyethylene(Steffensetal.2011).Growthofadventitiousroots,whichisprecededbydeathofepidermalcellsthatcovertherootprimordia(MergemannandSauter2000;SteffensandSauter2005),isalsopromotedbyethylene(Steffensetal.2006).Recently,Hattorietal.(2009)identifiedtheKEL1SK1)andSNORKEL2SK2)genesresponsibleforinternodeelongationindeepwaterrice.Non-deepwaterrice(.,lowlandrice)intowhichSK1SK2hadbeenintroducedshowedinternodeelongationinthesamewayasdeepwaterrice,indicatingthatthegenesarekeyfactorsfortheescapestrategyofdeepwaterriceunderdeepwater-floodconditions.Becauseofspaceconsiderations,detailsofthefunctionofgeneshavenotbeenincludedinthisreview,buttheyhavebeensummarizedbyNagaietal.(2010)andHattorietal.Strategiesofadaptationtowaterlogging:(1)aerenchymaFormationofaerenchymaisessentialtothesurvivalandfunctioningofplantssubjectedtowaterlogging.Theaer-enchymacontributestoOsupplyfromshootstorootsandtotheventilationofgases(.COandmethane)fromrootstoshoots(Colmer2003a;Evans2003).Theventilationofgasesinaerenchymaismainlycausedbygasdiffusioninrice,butinsomewetlandspecieswiththrough-flowpathwayse.g.alongrhizomes),gasflowscanalsooccurbyhumidity-andVenturi-inducedpres-sureflows(e.gPhragmitesaustralis;Armstrongetal.1996).TheaerenchymamayprovideaphotosyntheticbenefitbyconcentratingCOfromrootrespirationandtransportingittotheleafintercellularspacesinsomewetlandplantspecies(ConstableandLongstreth1994).Ingeneral,aerenchymacanbeclassifiedintotwotypes:(i)schizogenousaerenchyma,whichdevelopsbycellseparationanddifferentialcellexpansionthatcre-atesspacesbetweencells,inRumexpalustris;and(ii)lysigenousaerenchyma,formedbythedeathandsubsequentlysisofsomecells,e.g.,inrice(Jacksonetal1985a),maize(Drewetal1981),wheat(TroughtandDrew1980),andbarley(ArikadoandAdachi1955).Intheroots,lysigenousaerenchymaformsinthecortex(Figure2),whereasinthestemsitcanforminthecor-texandpithcavity(Armstrong1979).Insomewetlandplantspeciessuchasrice,rootlysi-genousaerenchymaisconstitutivelyformedunderdrainedsoilconditions(.,aerobicconditions;Jacksonetal.1985a),anditsformationcanbefurtherenhancedduringsoilwaterlogging(Figure2;Colmeretal2006;JustinandArmstrong1991;Shionoetal.2011;VisserandBögemann2006).Inrice,aerenchymaformationisinitiatedattheapicalpartsoftherootsandgraduallyexpandstothebasalpartsoftheroots(Figure2;Ranathungeetal.2003).Fullydevelopedaerenchyma,whichisobservedonthebasalpartsofroots,separatestheinnerstelefromtheoutercelllayers(.,sclerench-yma,hypodermis/exodermis,andepidermis)oftheroots(Figure2;ArmstrongandArmstrong1994;KozelaandRegan2003;Ranathungeetal.2003).Strandsofremain-ingcellsandcellwallsseparategasspacesinthecortex,formingradialbridges,whichareimportantforthestructuralintegrityoftherootandforbothapoplasticandsymplastictransportofnutrients(Figure2;DrewandFourcy1986).Duringaerenchymaformationinriceroot,celldeathbeginsatthecellsinthemid-cortexandthenspreadsoutradiallytothesurroundingcorticalcells(Kawaietal.1998).Theepidermis,hypodermis/exodermis,endodermis,andsteleareunaffected,indicat-ingthatlysigenousaerenchymaformationoccursbyclo-selycontrolledmechanisms(Yamauchietal.2011).Bycontrast,innon-wetlandplantspeciessuchasmaize,wheat,andbarley,rootlysigenousaerenchymadoesnotformunderwell-drainedsoilconditions,butitmaybeinducedbypooraeration(McDonaldetal.2001;McPherson1939;TroughtandDrew1980).Gen-erally,inductionofaerenchymaformationtakes24-72hoursafterthestartofanaerobictreatment(Haqueetal.2010;Maliketal.2003;Rajhietal.2011).Inaddition,aerenchymaformationislessextensiveinnon-wetlandplantspeciesthaninwetlandplantspecies(Armstrong1979;ColmerandVoesenek2009).Thus,non-wetlandplantsarelesstoleranttowaterloggingthanwetlandplants,suchasrice.SignalingoflysigenousaerenchymaformationInriceandmaize,ethyleneisimplicatedintheinduc-tionoflysigenousaerenchymaformation(Drewetal.2000;JacksonandArmstrong1999;JustinandArm-strong1991;Konings1982;Shionoetal.2008).Ricerootsformlysigenousaerenchymaconstitutivelyevenunderwell-aeratedconditions(Jacksonetal.1985a;Jus-tinandArmstrong1991;Shionoetal.2011).Lysigenousaerenchymaformationinricerootscanbefurtherincreasedbyethylenetreatmentunderaeratedcondi-tionsanddecreasedbytreatmentwithanethyleneper-ceptioninhibitor(e.g.silverions)understagnant(0.1%agar)deoxygenatedconditions(whichmimicshypoxic/anoxicconditionsinwaterloggedsoils;Wiengweeraetal.1997),althoughcultivars(e.g.Norin36andRB3)etalhttp://www.thericejournal.com/content/5/1/2Page5of14 differintheirsensitivitytoethylene(JustinandArm-strong1991).JustinandArmstrong(1991)alsopointedoutthatconsiderationofthelengthsoftherootssampledwasimportantforcomparisonofaerenchymaformationsbetweentreatments.Morerecently,ethylenehasbeenshowntoincreaserootaerenchymaformationinanotherricecultivar,Calrose(Colmeretal.2006).Inmaizeroots,ethylenebiosynthesisisstimulatedbyenhancingtheactivityof1-aminocyclopropene-1-car-boxylicacid(ACC)synthaseandACCoxidaseatthebeginningofaerenchymaformation(Heetal.1996a).Thus,treatmentofmaizerootswithinhibitorsofethy-lenebiosynthesis(.aminoethoxyvinylglycine,ami-nooxyaceticacid(AOA),andcobaltchloride)oractione.g.silverions)effectivelyblocksaerenchymaformationunderhypoxicconditions(Drewetal.1981;Jacksonetal.1985b;Konings1982).Theseobservationsindicatethatethyleneworksasatriggerfortheinductionofaer-enchymaformationinriceandmaize.Ontheotherhand,intherootsofanotherwetlandspecies(),lysigenousaerenchymaformationisnotaffectedbytreatmentwithethyleneortheethyleneperceptioninhibitor1-methylcyclopropene(1-MCP;VisserandBögemann2006).Todeterminewhetherethyleneis(orisnot)acommonfactorinregulationoftheinductionoflysigenousaerenchymaformationintherootsofwet-landspecies,theeffectofethyleneonaerenchymafor-mationshouldbestudiedbytreatmentofawiderrangeofwetlandspecieswhileconsideringthepossibleinflu-encesofrootlengthandtissueagealongtherootaxes(JustinandArmstrong1991;VisserandBögemannEthylene-responsivelysigenousaerenchymaformationisaffectedbychemicalinhibitorsorstimulatorsofpro-grammedcelldeath(PCD)andothersignalingpathways.HeterotrimericG-protein-,phospholipaseC(PLC)-,ino-sitol1,4,5-trisphosphate(IP3)-,orCa-dependentsig-nalingpathwaysareinvolvedintheprocessoflysigenousaerenchymaformationinmaizeroots(Drewetal.2000;Heetal.1996b).Ithasbeenproposedthat,underoxygendeprivation,Caisreleasedfrommitochondriaintothecytosol(Subbaiahetal.1994);theelevatedcytosolicCamayprovokesubsequentactivationofkinasesandphos-phatasesduringaerenchymaformation(SubbaiahandSachs2003).Lysigenousaerenchymaformationisalsoinducedbyokadaicacid,aninhibitorofproteinphospha-tases,andisrepressedbyK252a,aninhibitorofproteinkinases(Drewetal.2000;Heetal.1996b).Thesecal-cium-dependentsignalingsmayresultinactivationofexpressionofthegenesresponsibleforaerenchymafor-mation(Drewetal.2000;SubbaiahandSachs2003).PCDisatightlyregulatedpathwaythataccompaniestheactivationofspecificbiochemicalpathways(Greenberg1996).PCDisdistinguishedfromnecrosis,whichoccursbyuncontrolled,accidentalcelldeathwithoutactivationofsignalingpathways(Drewetal.2000;Gunawardenaetal.2001a).Celldeathduringlysigenousaerenchymaformationissimilartoapoptosisinanimalcells,whichincludesDNAfragmentation,nuclearcondensation,andnuclearandplasmamembraneblebbing(Drewetal.Oneofthefinalstepsinlysigenousaerenchymafor-mationisdegradationofthecellwall,whichismediatedbycell-wallmodificationordegradationenzymes.Changesinesterifiedandde-esterifiedpectinsinthecellwallofthemaizecortexareobservedduringcelldeath(Gunawardenaetal.2001b).Subsequently,thecellwallisdegradedbythecombinedactionofpectolytic,xyla-nolytic,andcellulosolyticenzymes(Evans2003;JacksonandArmstrong1999).Theactivityofcellulase(CEL)isincreasedbytreatmentwithethylene,okadaicacids,andreagentsthatincreaseintracellularCalevels,whereasCELactivityisdecreasedbytreatmentwithK252aandinhibitorsofCaincrease(Heetal.1996b).Inmaizeroots,expressionofageneencodingxyloglucanendo-transglycosylase(XET)isinducedbywaterlogging,anditsinductionisinhibitedbytreatmentwiththeethylenebiosynthesisinhibitorAOA(SaabandSachs1996).TreatmentwithAOApreventstheformationoflysigen-ousaerenchyma,suggestingthatinductionofXETpro-ductioninresponsetoethyleneisinvolvedinaerenchymaformationthroughcell-wallmodification(SaabandSachs1996).Onthebasisofthisevidence,Evans(2003)proposedthatcelldeathintherootcortexduringlysigenousaer-enchymaformationcanbeclassifiedintofivesteps:(1)perceptionofhypoxiaandinitiationofethylenebio-synthesis;(2)perceptionofethylenesignalingbycellsofthemid-cortex;(3)initiationofcelldeathwithlossofionstothesurroundingenvironment,plasmamembraneinvagination,andformationofsmallvesicles;(4)chro-matincondensation,increasedactivityofcell-wallhydrolyticenzymes,andthesurroundingoforganellesbymembranes;and(5)cell-walldegradation,celllysis,andabsorptionofthecellcontentsandwaterbythesurroundingcells.GenesassociatedwithlysigenousaerenchymaformationSofar,studiesoflysigenousaerenchymaformationhavebeendonemainlyfromaphysiologicalperspective.However,thegenesinvolvedinlysigenousaerenchymaformationintheroothavenotbeenidentified.Recently,Rajhietal.(2011)identifiedgenesassociatedwithlysi-genousaerenchymaformationinmaizerootsbyusingamicroarrayanalysiscombinedwithlasermicrodissec-tion.TheyfoundthatCasignaling-relatedgenesencodingCalcineurinB-likeproteinandCalmodulin-likeproteinwereupregulatedunderwaterloggedcondi-tions,andtheirexpressionlevelswerehigherintheetalhttp://www.thericejournal.com/content/5/1/2Page6of14 corticalcellsthaninthestelarcells.Waterloggingalso inducestheexpressionofcell-wallmodification-related genes( e.g . XET and CEL ).Inductionoftheexpressions ofcalciumsignaling-andcellwallmodification-related genesissuppressedbytreatmentwith1-MCP.These resultssupportthepreviouslyproposedmechanismof ethylene-mediatedlysigenousaerenchymaformation (JacksonandArmstrong1999;Drewetal.2000;Evans 2003). Ageneencodingrespiratoryburstoxidasehomolog (RBOH;aplanthomologofgp91 phox inmammalian NADPHoxidase),whichhasaroleinROSgeneration (TorresandDangl2005),isupregulatedstronglyinthe corticalcellsandslightlyles sstronglyinthestelarcells andtheoutercelllayersofmaizeroots(Figure3;Rajhi etal.2011;Yamauchietal.2011).Ontheotherhand,a geneencodingmetallothionein(MT),whichhasarole inROSscavenging(Wongetal.2004,Xueetal.2009), isconstitutivelyexpressedinallofthecorticalcells,the stelarcells,andtheoutercelllayersofmaizeroots underaerobicconditions.Bycontrast,underwater- loggedconditionsthe MT geneishardlyexpressedatall inthecorticalcellsbutisst illhighlyexpressedinthe stelarcellsandtheoutercelllayers(Figure3;Rajhi etal.2011;Yamauchietal.2011).Theseresultssuggest thatH 2 O 2 andotherROSarescavengedbytheconsti- tutivelyexpressedMTinstelarcellsandtheoutercell layers,whereasinthecorticalcellsdecreased MT expressionpreventsROSscavenging,therebyleadingto greaterROSaccumulation,w hichactivatesthesubse- quentprocessesofPCD( i.e .,lysigenousaerenchymafor- mation)inmaizeroots(Figure3).Interestingly, upregulationof RBOH anddownregulationof MT also occurinricerootsduringinducibleaerenchymaforma- tionunderanaerobicconditions(YamauchiandNaka- zono,unpublished).Simila rly,ethylene-promoted Figure3 Modeloflysigenousaerenchymaformation .Waterloggingpromotesbiosynthesisandaccumulationofethylene,followedby inductionof RBOH expression.RBOHactivityleadstoproductionandaccumulationofO 2 ·- attheapoplast.TheO 2 ·- isspontaneouslyor enzymaticallyconvertedtoH 2 O 2 ,whichcaneasilydiffuseintothecytosolthroughtheplasmamembrane.Underwaterloggedconditions,inthe cytosolofstelarcellsandcellsintheoutercelllayers,H 2 O 2 andotherROSarescavengedbyconstitutively-expressedMT.Bycontrast,inthe corticalcells,thedecreased MT expressionpreventsROSscavenging,therebyleadingtogreaterROSaccumulation,whichactivatesthe subsequentprocessesofprogrammedcelldeathandlysisofthecorticalcells( i.e .,lysigenousaerenchymaformation).Underaerobicconditions, the RBOH geneisexpressedatlowlevelandthe MT geneisconstitutivelyexpressedinthecorticalcells.WL,waterloggedconditions;Aer, aerobicconditions;OCL,outercelllayers;ap,apoplast;cs,cytosol. Nishiuchi etal . Rice 2012, 5 :2 http://www.thericejournal.com/content/5/1/2 Page7of14 downregulationofexpressionofageneencodingMT2benhancestheaccumulationofHproducedbyNADPHoxidaseandthusinducesepidermalcelldeathinrice(SteffensandSauter2009)oraerenchymaforma-tioninriceinternodes(Steffensetal.2011).Theseresultssuggestthatdownregulationofgenesplaysanimportantroleintissue-specificorcelltype-specificPCDinriceandmaize.Strategiesofadaptationtowaterlogging:(2)formationofabarriertoROLOxygenmoleculesdiffusinglongitudinallythroughaer-enchymatowardtheroottipsmaybeeitherconsumedbyrespirationordiffusedradiallytotherhizosphere(Armstrong1979;Colmer2003a).ROL,thefluxofOfromtheaerenchymatothesoil,isdeterminedbytheconcentrationgradient,thephysicalresistancetoOfusioninaradialdirection,andconsumptionofOcellsalongthisradialdiffusionpath(Armstrong1979;Colmer2003a).ROLaeratestherhizosphereandisthereforeconsideredtobeofadaptivesignificanceinplantsgrowinginwaterloggedsoil(Armstrong1979;Blossfeldetal.2011;Colmer2003a;Neubaueretal.2007).However,ROLreducesthesupplyofOtotherootapexandtherebycausesadecreaseinrootlengthinanaerobicsoil(Armstrong1979;Colmer2003a;Colmeretal.1998;JacksonandArmstrong1999).Therootsofmanywetlandspecies,includingrice,havetheabilitytopreventROLtotherhizospherebyformingabarrierintherootperipheralcelllayersexter-iortotheaerenchyma(Figure2;McDonaldetal.2002;Visseretal.2000).Thisadaptivetraitenhanceslongitu-dinalOdiffusionthroughtheaerenchymatowardstherootapexbydiminishinglossesofOtotherhizo-sphere,therebyenablingtherootstoelongateintoanae-robicsubstrates(Armstrong1979).TherootsofsomewetlandspecieshaveconstitutivelypresentbarrierstoROL(e.gJ.effusus;Visseretal.2000),whereasinotherspeciessuchasriceandHordeummari-thebarriertoROLisinducedduringgrowthunderanaerobicconditions(Colmer2003b;Colmeretal.1998;Garthwaiteetal.2003;Kotulaetal.2009a;Shionoetal.2011).AnalysisofthespatialpatternsofROLalongricerootshasrevealedthatOleakagefromthebasalregionsofthelongrootsunderstagnantconditionsisquitelow(Figure4),buttherearelargeamountsofOfluxfromtherootapexes(Figure4)andnumerousshortlateralrootsthatappearnearthebaseofthemainaxes(Armstrong1971a;Armstrongetal.1996,Colmer2003b).ThebarriertoROL,togetherwithreoxidationoftherhizospherearoundtheroottipsandlateralroots,enableselongationoftherootsintotheanoxicenviron-mentandrestrictstheentryoftoxiccompoundsfromhighlyreducedsoils(Armstrong1979;Armstrongetal.1996;ColmerandVoesenek2009).DespitetheimportanceofthebarriertoROL,therearefewdataavailableontheOpermeabilitycoeffi-cientacrossthecelllayersexteriortotheaerenchyma.Recently,KotulaandSteudle(2009)developedagasperfusiontechniquetomeasuretheOpermeabilityoftheoutercelllayersoftherootsandappliedthetech-niquetoricegrownundereitheraeratedorstagnantdeoxygenatedconditions.Plantsgrowninthestagnant-deficientconditionsoftheexternalgrowthmediumshowedmuchlowerOpermeabilitythanplantsgrowninanaeratedsolution.ThevariationinOmeability,eitherbyblockingapoplasticporesorkillinglivingtissues,indicatedthatphysicalresistanceisthedominatingfactorimpedingOlossfromriceroots,althoughrespiratoryOconsumptionmaycontributetolowratesofROL(Kotulaetal.2009b).Strongphy-sicalimpedancetoradialOdiffusioninricerootshasalreadybeenshownbyArmstrong(1971b).Inthisstudy,abarriertoROLwasevidentintheadventitiousrootsofrice,evenwhenrespirationwasinhibitedbycoolingtherootmediumto3°C.SimilarfindingshavebeenreportedbyArmstrongetal.(2000)andGarthwaiteetal.(2008)intherootsofP.australisH.marinum,respectively.InH.marinumthephysicalbarrierappearedtoaccountfor84%ofthereductioninOlossandrespiratoryactivityfor16%(Garthwaiteetal.2008).AnatomicalandchemicalnatureofthebarriertoROLItseemsthatsuberizationand/orlignificationofthecellwallsintherootlayersexteriortotheaerenchymaisimplicatedinthedevelopmentofatightbarriertoROL(Figure5;Armstrongetal.2000;Garthwaiteetal.2008;Kotulaetal.2009a;Soukupetal.2007).Inarecentstudyinrice,ratesofROLfromtherootsofplantsgrownunderaeratedordeoxygenatedcondi-tionswerequantified,andtheresultswerecombinedwithparallelhistochemistryandanalyticalchemistry(Kotulaetal.2009a).DeoxygenatedconditionsinducedtheearlydevelopmentofCasparianbandsandsuberinlamellaeintheexodermisandofligninindenselypacked,uniseriatesclerenchymalcellslocatedinteriortotheexodermis(Figure5).Inagreementwiththeresultsofthehistochemicalanalyses,quantitativeana-lysesusinggaschromatographyandmassspectrometryhaveshownthatthelevelsofsuberin(botharomaticandaliphaticdomains),aswellaslignin,releasedfromtheouterrootsleevesareseveraltimesgreaterinplantsgrowninoxygen-deprivedmediacomparedwithplantsgrowninaeratedsolution(Kotulaetal.2009a;Ranathungeetal.2011).Independentofthegrowthconditions,thetotalamountsofsuberinandligninetalhttp://www.thericejournal.com/content/5/1/2Page8of14 Figure4 RatesofROLalongintactadventitiousrootsofricegrownunderaeratedorstagnantdeoxygenatedconditions .The experimentwasconductedfollowingthemethodsofColmeretal.(1998)withminormodifications.Rice(cv.Nipponbare)wasgrownina28°C, continuallylitgrowthchamber.Nine-day-oldplantsweregrowninaeratednutrientsolution(Aeratedconditions)orstagnantdeoxygenatedagar solution(Stagnantconditions)for14or15daysbeforemeasurementsweretakenalongadventitiousroots(80-130mmlong).ROL measurementswereperformedat27-29°Cunderlightconditionsusingcylindricalroot-sleevingO 2 electrode.Valuesaremeans( n =3)±SD. Figure5 Stainingforsuberinandligninintheoutercelllayersofricerootsgrownunderaeratedorstagnantdeoxygenated conditions .Nine-day-oldriceplantsweregrowninaeratednutrientsolution(Aeratedconditions;a,c)orstagnantdeoxygenatedagarsolution (Stagnantconditions;b,d)for14days.Basalparts(10-20mmregionsfromtheroot-shootjunction)oftheadventitiousrootswereslicedinto 80- m-thicksections,andwereincubatedinlacticacidsaturatedwithchloralhydrateat70°Cfor1hforclearing.Forsuberinstaining,sections werestainedwithFluorolYellow088atroomtemperaturefor1handobservedunderUV-lightwithepifluorescencemicroscopy(a,b).For ligninstaining,sectionswerestainedfor5minwithphloroglucinol/hydrochlorideatroomtemperaturetovisualizeligninwithcinnamyl aldehydegroups(c,d).Whitearrowindicatesyellow-greenfluorescenceofsuberinathypodermis/exodermisandblackarrowindicatesorange- redpigmentationofstainedligninatthesclerenchyma.Ep,epidermis;Ex,exodermis;Sc,sclerenchyma;Co,cortex.Scalebars=50 m. Nishiuchi etal . Rice 2012, 5 :2 http://www.thericejournal.com/content/5/1/2 Page9of14 increasealongtherootstowardsthebasalzones(Kotulaetal.2009a;Ranathungeetal.2011).AlthoughthesestudieshaveshownadirectrelationshipbetweenchangesinOpermeabilityandtheformationofapo-plasticbarriers,theprecisenatureoftheROLbarrierremainsunclear.Namely,therelativecontributionsofsuberinandlignininlimitingROLarenotwellknown;potentially,oneofthetwomightnotbeneededforformationofthebarrier(Kotulaetal.2009a).FunctionoflignininpreventingROLmaynotbeappliedtoallplantspecies.InAmazoniantreespecies(DeSimoneetal.2003),aswellasinP.australis(Soukupetal.2007),resistancetoROLiscorrelatedonlywiththedepositionofsuberin,butnotlignin.HistochemicalsolutepenetrationstudiesusingperiodicacidhavefurtherconfirmedthatintherootsofP.australissuberizedexodermisnotthelignifiedsclerenchyma,whichiseasilypenetratedbyperiodicacidistheradialpermeationbarrier(Soukupetal.2007).Shionoetal.(2011)foundthatsuberinincreasedpriortochangesinlignininrice,suggestingthatdepositionofsuberinismoreimportantfortheROLbarrierformationthanlignin.However,thesuberinandlignindepositswerenotevidentintherootswithinthefirst2daysofstag-nanttreatment,duringwhichtimebarrierinductionwasalreadycomplete.Inlongadventitiousroots(105-130mminlength),barriertoROLwaswellformedwithin24hoursunderstagnantdeoxygenatedcondi-tionsanddarkgranulesofhigh-densitymaterialwereobservedbytransmissionelectronmicroscopyinthespacesbetweentheexodermalcellsandalsobetweenthesclerenchymacellsinrootsat48hoursafterthestagnanttreatment(Shionoetal.2011).Thisresultsuggeststhatthesemicrostructuralchangesalsocon-tributetothediminutionofROLinthericeroot.TheprecisenatureofthebarriertoROLstillneedstobemoreclearlyelucidated(seebelow).ThebarriertoROLvs.nutrientandwateruptakeAlthoughthebarriertoROLhelpswetlandplantstotoleratewaterlogging,itmayalsoreducewaterandnutrientuptake(Armstrong1979;Koncalová1990).Forexample,theratesofNHandNOnetuptakeinthebasalregionofricerootswereabout30%ofthoseinmaize,evenwhentheplantsweregrowninaeratedsolution(ColmerandBloom1998)andthepermeabilityofrootstowaterissubstantiallysmallerinricethaninmaize(Hoseetal.2001;Miyamotoetal.2001).How-ever,arecentstudydemonstratedthattheearlyforma-tionofapoplasticbarriersintheendodermisandexodermisofricerootsinstagnantsolutionsdoesnotsignificantlyaffecthydraulicconductivity(Ranathungeetal.2011).Thisisinagreementwiththeearlierfind-ingsofGarthwaiteetal.(2006)instagnantlygrownH.marinum,inwhichinductionofthebarriertoROLdidnotimpedethewaterpermeabilityoftheroots.Incontrasttowaterflow,stagnantgrowthconditionsmarkedlyreducethepermeabilityofthericerootstooxygenandtoionssuchasFe,Cu,andNaCl(Arm-strongandArmstrong2005;Kotulaetal.2009b;Krish-namurthyetal.2009;Ranathungeetal.2011).Theextrasuberinandlignindepositedintherootsinstagnantsolutionsmayeffectivelyclogthewallpores,makingabarriersufficienttoblockthepassageofoxygenandions,butnotwater,whichismainlybulkandviscousinnature(Kotulaetal.2009b;Ranathungeetal.2004,2011).Itappearsthatricerootslivinginanaerobicmediacanretainoxygenintheaerenchymawhiletakingupsufficientwater(Kotulaetal.2009b;Ranathungeetal.2011).Thisisachievedbecauseofdifferencesinthetransportmechanismsofoxygenandwater.Whenmeasuredwithheavywater,thediffusionalwaterperme-abilityoftheouterpartofthericerootwasanorderofmagnitudesmallerthanthatofoxygen(Ranathungeetal.2004;Kotulaetal.2009b;KotulaandSteudle2009).However,diffusionalwaterpermeabilitywassmallerthanthebulkwaterpermeabilitybyafactorof600-1400.Thelatterparameteristheonethatisimportantduringwateruptake(SteudleandPeterson1998).ThissuggeststhatricehasevolvedanoptimumbalancebetweenwateruptakeandOloss.Watermovespredo-minantlythroughtheporousapoplasticpathwaybyusingahydrostaticpressuregradient(Ranathungeetal.2004),whereasthemovementofOoughttobeappre-ciableoverthewholeinter-cellinterfaceandisdiffu-sionalinnature(Kotulaetal.2009b;Ranathungeetal.FormationofthebarriertoROLTherearemajoruncertaintiesregardingthesignalsinvolvedintheformationofaninduciblebarriertoROL.Colmeretal.(2006)showedthatethylene,whichpromotestheinductionoflysigenousaerenchymafor-mation(JustinandArmstrong,1991),didnotinduceatightbarriertoROLinriceroots,indicatingthatthesetworootaerationtraits,whichareconsideredtoactsynergisticallytoenhanceOdiffusiontotherootapex,appeartobedifferentiallyregulated.Bycontrast,asig-nificantdeclineinROL,whichiscorrelatedwithsuberi-zationandlignificationoftheoutercelllayers,isobservedaftertheexposureofricerootstocarboxylicacids(.aceticacid,propanoicacid,butyricacid,andcaproicacid;ArmstrongandArmstrong2001)andsulfide(intheformofphytotoxinsproducedbymicro-organismsinwaterloggedsoils;ArmstrongandArm-strong2005).SimilareffectsarefoundwhencarboxylicacidsareappliedtotherootsofH.marinumColmer,andNakazono,unpublished).However,thereductioninROLfromtherootsofriceandH.mari-exposedtotoxiclevelsofcarboxylicacidsandetalhttp://www.thericejournal.com/content/5/1/2Page10of14 sulfidewasassociatedwithinjury,ratherthanwithaspecificsignalforinductionofthebarriertoROL(Arm-strongandArmstrong2001;Colmer2003a).Recently,Flecketal.(2011)showedthatSinutritionincreasedsuberizationandlignificationofriceroots,whichwasaccompaniedbysilicicacid-triggeredtran-scriptionofgenesassociatedwithsuberinandligninbiosynthesis.Asaconsequenceofsuberizationandlig-nificationoftheouterrootcelllayers,theoxidationpowerofthericerootswasreduced.Althoughitissug-gestedbyFlecketal.(2011)thatalteredlevelsofsilicicacidplayaroleinpromotingthebiosynthesisofsuberinandlignin,thesignalinvolvedininducibleROLbarrierformationremainsunclear.Althoughgreatprogresshasbeenmadeinourunder-standingofthemechanismsinvolvedinadaptationtosubmergenceorwaterlogging,therearestillgapsinourknowledge,mainlyinregardtothesignalingpathwaysandmolecularprocesses.ThegeneticregulationoftheformationoflysigenousaerenchymaandthebarriertoROLremainstobedetermined.Recently,Nakazonoandhiscolleagues(Rajhietal.2011;Shiono,Yamazaki,andNakazono,unpublished)havebeeninvestigatingtheexpressionsofgenesassociatedwiththeformationofinduciblelysigenousaerenchymaandthebarriertoROLbyusinglasermicrodissection-mediatedmicroarrayana-lysisofthecortexinmaizerootsandtheoutercelllayersinriceroots,respectively,underanaerobiccondi-tions.Thisapproachshouldhelptoidentifyimportantgenesinvolvedintheformationofthesetwostructures.FurtherinsightsintothenatureofthebarriertoROLandthemolecularmechanismofinduciblebarrierfor-mationcouldbeachievedfromthecharacterizationofsuberinorligninformation-affectedricemutantsincomparisonwiththerespectivewildtypes(Ranathungeetal.2011).ConclusionsThisreviewsummarizeswhatisknownaboutthephy-siologicalandmolecularmechanismsusedbyricetocopewithsubmergenceandwaterlogging.Forsubmer-gence,themechanismsincludeinternalaerationandgrowthcontrols(.,aquiescencestrategyoranescapestrategy).Forwaterlogging,themechanismsincludeformationofaerenchymaandabarriertoROL.Theseadaptivetraitsenablericeplantstohavehightolerancetosubmergenceorwaterloggingcom-paredwithotherdrylandcrops.Anadvantageofriceisthatitsgenomehasbeenfullysequencedandmanytoolsforstudyingitsmolecularbiologyandgeneticse.g.oligomicroarrays,mutantcollections,anddata-bases)havebeendeveloped.TheseresourcesshouldaccelerateourunderstandingofthemechanismsinvolvedinadaptationofricetoexcesswaterstressandshouldleadtotheirintroductionintodrylandAcknowledgementsTheauthorsthankDrs.T.D.ColmerandK.Shionoforstimulatingdiscussions.ThisworkwassupportedpartlybyagrantfromtheBio-orientedTechnologyResearchAdvancementInstitution(PromotionofBasicResearchActivitiesforInnovativeBiosciences),agrantfromtheMinistryofAgriculture,Forestry,andFisheriesofJapan(GenomicsforAgriculturalInnovation,IPG-0012),andgrants-in-aidfromtheMinistryofEducation,Culture,Sports,Science,andTechnologyofJapan.LKisgratefultotheJapaneseSocietyforthePromotionofScienceforthepostdoctoralfellowship.Alloftheauthorscontributedequallytothedraftingandrevisingofthispaperandhavereadandapprovedthefinalmanuscript.CompetinginterestsTheauthorsdeclarethattheyhavenocompetinginterests.Received:21November2011Published:27February2012ArikadoH,AdachiY(1955)Anatomicalandecologicalresponsesofbarleyandsomeforagecropstothefloodingtreatment.BulletinFacultyAgriculture,MieUniversityTsuMie11:1ArmstrongJ,ArmstrongW(1994)Chlorophylldevelopmentinmaturelysigenousandschizogenousrootaerenchymaprovidesevidenceofcontinuingcorticalcellviability.NewPhytologist126:493ArmstrongJ,ArmstrongW(2001)Riceand:effectsoforganicacidsongrowth,rootpermeability,andradialoxygenlosstotherhizosphere.AmericanJournalofBotany88:1359ArmstrongJ,ArmstrongW(2005)Rice:sulfide-inducedbarrierstorootradialoxygenloss,Feandwateruptake,andlateralrootemergence.AnnalsofBotany96:625ArmstrongJ,ArmstrongW,BeckettPM,HalderJE,LytheS,HoltR,SinclairA(1996)Pathwaysofaerationandthemechanismsandbeneficialeffectsofhumidity-andVenturi-inducedconvectionsinPhragmitesaustralis(Cav.)TrinexSteud.AquaticBotany54:177ArmstrongW(1971a)Radialoxygenlossesfromintactricerootsasaffectedbydistancefromtheapex,respirationandwaterlogging.PhysiologiaPlantarumArmstrongW(1971b)Oxygendiffusionfromtherootsofricegrownundernon-waterloggedconditions.PhysiologiaPlantarum24:242ArmstrongW(1979)Aerationinhigherplants.AdvancesinBotanicalResearchArmstrongW,CousinsD,ArmstrongJ,TurnerDW,BeckettPM(2000)Oxygendistributioninwetlandplantrootsandpermeabilitybarrierstogas-exchangewiththerhizosphere:amicroelectrodeandmodellingstudywith.AnnalsofBotany86:687ArmstrongW,DrewMC(2002)Rootgrowthandmetabolismunderoxygendeficiency.In:WaiselYetal(ed)PlantRoots:TheHiddenHalf,3rdedn.NewYork&Baselpp729Bailey-SerresJ,FukaoT,RonaldP,IsmailA,HeuerS,MackillD(2010)Submergencetolerantrice:sjourneyfromlandracetomoderncultivar.Rice3:138Bailey-SerresJ,VoesenekLACJ(2008)Floodingstress:acclimationsandgeneticdiversity.AnnualReviewofPlantBiology59:313BlossfeldS,GansertD,ThieleB,KuhnAJ,LöschR(2011)Thedynamicsofoxygenconcentration,pHvalue,andorganicacidsintherhizosphereofSoilBiologyandBiochemistry43:1186CatlingD(1992)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Submit your manuscript to a t from:Convenient online submissionRigorous peer reviewImmediate publication on acceptanceOpen access: articles freely available onlineHigh visibility within the Þ eldRetaining the copyright to your articleSubmit your next manuscript at springeropen.com etalhttp://www.thericejournal.com/content/5/1/2Page14of14