Quiescence
in
rice
submergence
tolerance:
an
evolutionary
hypothesis
Chiara
Pucciariello
and
Pierdomenico
Perata
PlantLab,InstituteofLifeSciences,ScuolaSuperioreSant’Anna,PiazzaMartiridellaLiberta`33,56127Pisa,Italy
Rice(Oryza sativa)varieties differ considerablyintheir tolerancetosubmergence,atraitthathasbeen associ-ated with the SUB1A gene. Recently, this gene was found insome wild rice species and landraces,which along with O. sativa, belong to the AA genome type group.Onthebasisofgeographicalandhistoricaldata, we hypothesize that SUB1A-1 from wild species may have been introgressed into domesticated rice. This introgression probably occurred in the Ganges Basin, with the subsequent spread of the SUB1A-1 to other areasofSouthAsiaduetohumanmigration.Thelackof the SUB1A gene in diploid CC genome type wild rice showingsubmergence-toleranttraitssuggeststhe pres-ence of adifferent survival mechanism inthis genetic group.
Evolutionof submergencetoleranceinrice
Various hydrological regimes characterize natural and anthropic habitats where flood events vary in extent, depth,frequency,andseasonalincidence.Extreme hydro-logicalregimesincluderiverfloodplains,coastalmarshes, theAmazonfloodplain,aswellastheareaswherericeis cultivated,whicharecharacterizedbysubmergenceofthe plantsthatcanreachseveralmetersbutcanalsobeabsent
[1].Flood-proneenvironmentsdeterminethedistribution andabundanceofplantspeciesandexertanevolutionary pressurewhichselectstraitsthatareadvantageousunder theseenvironmental conditions [1].Theadaptability ofa planttowaterloggingorsubmergenceisenhancedbythe developmentofeithermetabolicoranatomical character-istics [1]. These traits act in synergy to promote plant tolerance to water submergence and represent a source ofgeneticvariationsforcropbreeding[2].
Riceisauniquecropduetoitsadaptabilitytodifferent flooding conditions. The number of varieties, landraces, andwildrelativescoveringthelargeareaofproductionis synonymouswith anexceptionalplasticity todiverse hy-drological regimes. Oneofthe manyways thathave en-abledricetoadapttofloodinghasrecentlybeenidentified asa‘quiescencestrategy’[3].Itischaracterizedbyreduced plantelongationduringsubmergence,associatedwith re-growthwhenthewaterrecedes.Theethyleneresponsive factor (ERF) SUBMERGENCE1A(SUB1A), inits allelic form SUB1A-1, is the key determinant of this survival mechanism[4].SUB1A-1isinducedbyethylene,agaseous
planthormonethatbecomesentrappedbywater submer-gence[5].SUB1A-1positivelyregulatesthetranscription ofgenesrelatedtothefermentativemetabolism,whichis requiredunder lowoxygen conditionstosustainenergy production [6].SUB1A-1also repressesgenes relatedto thebreakdownofcarbohydrates,inordertopreservethe sugarsneededtofuelregrowthwhenthewaterrecedes[6]. Remarkably, SUB1A-1 also restricts shoot elongation, thus preventing the excessive use of carbohydrates to sustaingrowth,which wouldin anycase beinsufficient fortheplanttoreachthewatersurface[5].Limitedshoot elongation under submergence is achieved through the positiveactionofSUB1A-1onthegibberellin(GA) signal-ingrepressorsSLENDERRICE-1(SLR1)andSLR1-LIKE (SLRL1)[7].Duringthepost-hypoxicphase,SUB1A-1is involvedinacclimationtodehydration,paradoxically oc-curringas naturalprogression upondesubmergence,by increasingABAresponsivenessandreactiveoxygen spe-cies(ROS)detoxification[8].Somesubmergencetolerance can alsobe conferred bythe intolerant SUB1A-2 allele, whenhighlyexpressed[9].Thisallelediffersintermsof
the absence of the SUB1A-1 MITOGEN-ACTIVATED
PROTEIN KINASE(MAPK)site[4],whichmightaffect theactivationofthe proteinandtheregulationof down-streamgenes.TheintrogressionofSUB1A-1inrice varie-tieswithhighyieldsandgrainqualitytraits,butreduced tolerance to submergence,resultedin the production of new varieties with both a high yield and submergence tolerance[10].
Considerableeffortshavebeenmadetocharacterizethe presence/absenceoftheSUB1AgeneinOryzaspp.[4,9,11– 13].Wesummarizethesefindingsonthebasisof geograph-ical origin anddescription ofthe originalhabitat of the genotypes studied, in order to examine the evolution of SUB1A-1andthusthesubmergencetolerancetrait.
SUB1Ageneispresentinwildandcultivatedrice The genusOryzaL. consistsofapproximately 23species harboringseveraldistinctgenomegroups[14].TheOryza spp.that belongstothe AA genometype includesOryza sativaandOryzaglaberrimacultivatedriceandwild spe-cies (i.e., Oryza rufipogon, Oryza nivara, Oryza barthii, Oryzalongistaminata,Oryzameridionalis,andOryza glu-maepatula)[15],whichcanexchange geneticinformation whensympatricandfloweringatthesametime[16].After being originallyassociated with theO.sativa small sub-group of indicavarieties [4], including the aus landrace FloodingResistant13A(FR13A),SUB1Aalleleshavealso been described in other genotypes including some wild
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Correspondingauthor:Perata,P. (p.perata@sssup.it)
group,O.rufipogonandO.nivaraareconsideredtobethe mostlikely ancestors from whichO.sativawas domesti-cated[17].
Figure1showsamapofwildandlandracerice
acces-sionsbelongingtotheAAgenometypeinvestigatedtodate forthepresence/absenceofSUB1Aandwiththe Interna-tional RiceGermplasm Collection (IRGC) number ofthe International Rice Research Institute (IRRI). The map showsthepresenceofvariouswildricespeciesharboring theSUB1A-1 allelearoundthebasinsoftheGangesand Brahmaputra rivers,whichinclude areasofNorthIndia, Nepal,andBangladesh.Onewasoriginallyreportedtobea hybridswarm,thusprobablyanaturalpopulationofwild andcultivatedriceinterspecifichybrids.Most archeologi-calevidenceindicatestheYangtzeValleyinChinaasthe original area of rice cultivation by humans [18–21]. In addition,geneticevidencesuggeststhattheGangesValley inIndiawasasecondsiteofpotentialricedomestication
[22].Aphylogeographicstudyalsoshowedthatthe south-ernHimalayaswasthedomesticationregionoftheindica group from the O. rufipogon progenitor [23]. Migrants could havedisseminatedthe seedsof submergence-toler-antplantsfromthisareatootherpartsofAsia,asshownby the presenceof landraceswith theSUB1A-1 gene inSri Lanka,Vietnam,andThailand(Figure1).
Interestingly, the presence of the intolerant allele SUB1A-2 hasalsobeenidentifiedin O.sativagenotypes fromChina,Cuba,Nigeria,andGuinea–Bissau.Theonly accession of the African cultivated rice O. glaberrima investigatedshowstheabsenceofSUB1Aandwas collect-edinSenegal[13].Todate,onlyafewAAriceaccessions from Africa have been analyzed, making it difficult to formulateahypothesisastohowSUB1Aintrogressedin thisarea.
PrevioussurveysofAAricegenotypesrevealedthatthe SUB1A gene was sometimes, butnot always,present in O. nivara, O. rufipogon, and O. sativa [9,11–13]. This supportsthetheorythatsubmergencetolerancewas intro-gressed fromdivergent populationsofwild relativesinto cultivatedO.sativa[13].Wildricespeciesbelongingtothe AAgenomegroupevolvedinareascharacterizedby differ-entwaterregimes,withO.nivaraoccurringinseasonally dry habitats, andO. rufipogonin permanentlywet ones
[14].However,insomeplacesO.nivaraandO.rufipogon, whicharecross-compatible,aresympatricinareasofrice cultivation.Despitetheirecologicaldistinction,O.nivara andO.rufipogonhavesimilarmorphological characteris-tics and a relatively low genetic differentiation, thus O.nivaraisalsoconsideredasasubspeciesoranecotype ofO.rufipogon [14,24].Onehypothesisisthat O.nivara evolvedfromanO.rufipogonancestorafterahabitatshift
[17].ThetransferoftheSUB1Agenemaythushavebeen successfulinenvironmentswhereflashfloodingoccursat thericeseedlingstage[25].
Gene flows from AA genome type wild rice species toward nearby O. sativa could have occurred with the introgression ofkeydomestication alleles[26].However, geneflowsfromcultivatedricecouldalsohavecontributed
populationsgrowingadjacenttocultivatedricefieldsthan thosefoundsomedistanceaway,thusindicatingthatgene flowsoccurfromcultivatedtowildrice[27,28].Theabsence ofwildriceharboringSUB1AinSriLanka,where SUB1A-containingO.sativalandracesarepresent,suggeststhat either they have only been recently introduced in Sri Lanka or that SUB1A was introgressed from wild rice species to O. sativa during domestication in the Indian Basin,andthentransferredtoSriLanka.
The introgression of SUB1A in cultivated rice could havebeenarelativelyrecentevent.TogetherwithSUB1A (whosepresenceinricecultivarsisvariable),othergenes encodingERFsareinvariablypresentintheSUB1region, namelySUB1BandSUB1C[6].Phylogeneticanalysishas providedevidencethatSUB1AandSUB1Bdivergedfrom SUB1CduringthedifferentiationbetweentheAAandCC genomecomplexes[13],andthatSUB1Aresultedfromthe duplicationofSUB1B[11].TherecentevolutionofSUB1A isalsosuggestedbytheoccurrence ofsmallallelic varia-tionsinthisgene(SUB1A-1andSUB1A-2only)compared withthehighlypolymorphicSUB1BandSUB1C(nineand sevenalleles,respectively)[4].
SUB1Aisabsentinsubmergence-tolerantwildrice belongingtotheCCgenomegroup
Todate,theSUB1Agenehasnotbeenfoundindiploidwild relatives belonging tothe CC type genome group Oryza officinalis,Oryzarhizomatis,andOryzaeichingeriwhich, however,havebeenshowntosurvivefloodingbyreducing growthundersubmergence [13].Only SUB1C-like genes havebeenfoundinthesegenotypes,suggestingthatthis ERFmaybemoreprimitivethanotherSUB1genes[13]. WildricebelongingtothediploidCCgenometypeand not harboring the SUB1A gene haveshown a disjointed distributioninAfricaandAsia(Figure2).Arecent hypoth-esis suggested that O. eichingeri from Africa may have beenintroducedtoSriLankaaverylongtimeago,because theaccessionsfromthetwolocationsarehighlygenetically divergent[24].Thisspeciesshowsmorphologicaland ge-neticvariationsinrelationtogeographicalderivationand habitat, thus exhibiting a high degree of intraspecific variation[14].InSouthAsia,wildCC andAAgenotypes have been found in the same geographical region [24]. ManyoftheCCgenotypesinvestigatedtodatehavebeen collectedinSriLankawhereO.sativalandracesharboring SUB1Aarealsopresent(Figures1and2).However,trials ofbreeding programswith O.eichingeri have reported a very low level of success in crosses with O. sativa [15]. Moreover, in Sri Lanka the habitat of O. rhizomatis is confinedtoseasonallydryzones[24],makingthegenetic exchangebetweenAAandCCricerelativelydifficult.
OnegeneticanalysisdeterminedthattheSUB1Callele, which is present in O. officinalis, O. rhizomatis, and O.eichingeri,doesnotcontributetosubmergencetolerance inrice[29].Moreover,theheterologousectopicexpression ofriceSUB1C inArabidopsis thalianashowed alimited contribution of this gene to the submergence stress re-sponse[30].Overall,thissupportstheideaofamolecular
11 Hs IRGC-103828 (1A-1)
22 On IRGC-93300 (1A-1) 13 Or IRGC-81882 (1A-1) 14 Or IRGC-82982 (1A-2) 15 On IRGC-80507 (1A-1) Wild rice without Sub1A
1 On IRGC-103418 2 On IRGC-81927 3 On IRGC-93275 4 On IRGC-105702 5 Or IRGC-93219 6 Or IRGC-99547 7 Or IRGC-104599
Wild rice with Sub1A
8 On IRGC-80695 On IRGC-80717 Or IRGC-105905
11 On IRGC-105725
Landraces with Sub1A
12 On IRGC-80506
13 On IRGC-80470
14 On IRGC-106355
16 Or IRGC-105960 (1A-2) Os IRGC-25913 (1A-2) Os IRGC-37497 (1A-1) Os IRGC-108921 (1A-1) Os IRGC-19064 (1A-2) Os IRGC-97470 (1A-2) Os IRGC-97614 (1A-2) Os IRGC-58975 (1A-1) Os IRGC-15430 (1A-2) Os IRGC-36437 (1A-1) Os IRGC-15294 (1A-2) Os IRGC-36253 (1A-1) Os IRGC-15379 (1A-1) Os IRGC-15314 (1A-1) Os IRGC-15337 (1A-2) Os IRGC-15464 (1A-2) Os IRGC-8948 (1A-1) Os IRGC-24224 (1A-2) Os IRGC-64535 (1A-2) Os IRGC-40242 (1A-2) Os IRGC-29858 (1A-1) Os IRGC-96206 (1A-2) 1 1 2 2 3 4 5 6 7 9 10 8 11 12 13 14 15 16 17 19 20 18 21 Landraces without Sub1A
Os IRGC-26449 Os IRGC-18387 Os IRGC-59211 Os IRGC-26921 Os IRGC-15238 Os IRGC-15602 Os IRGC-15433 Os IRGC-15478 Os IRGC-73193 1 1 2 3 4 5 6 8 9 7 9 10 17 Or IRGC-80433 (1A-1) 18 Or IRGC-80592 (1A-2) Sri Lanka Bhutan 4 1 3 4 6 7 9 10 Myanmar Laos Cambodia 11 Malaysia Vietnam Indonesia Philippines Thailand Brunei Singapore 5 13 14 6 2 3 4 5 6 7 8 9 4 5 6 7 8 9 101112 13 14 15 16 17 18 19 20 21 12 3 7 India 8 5 8 Os IRGC-26907 10 Os IRGC-74847 11 Os IRGC-75040 12 Os IRGC-20281 (1A-2) 22 Os IRGC-20829 (1A-1) 23 Os IRGC-28539 (1A-2) 24 Os IRGC-84242 (1A-1) 25 Os IRGC-84239 (1A-2) 26 10 11 12 24 25 26 2 23 22 2 1 1 Brahmaputra 27 28 Os IRGC-15419 (1A-1) Os IRGC-15449 (1A-1) 28 27 Nepal Ganges 2 3 1 Bangladesh
TRENDS in Plant Science
Figure1.LocationoftheoriginalcollectionsitesofAAgenometypewildgenotypes(squaresymbols)andlandraces(circlesymbols),withorwithoutSUB1Agenes[9,11– 13].WildgenotypesandlandraceswithouteitherSUB1A-1orSUB1A-2arerepresentedbybluesymbols.GenotypeswiththetolerantalleleSUB1A-1areindicatedas‘1A-1’ inthekeyandyellowsquaresorcirclesymbolsinthemap,whilethoseharboringtheintolerantalleleSUB1A-2areindicatedwith‘1A-2’inthekeyandorangesquaresor circlesinthemap.Theaccessionsshownrepresentthoseinvestigatedtodateforthepresence/absenceofSUB1AandwiththeInternationalRiceGermplasmCollection (IRGC)numberoftheInternationalRiceResearchInstitute(IRRI).ThesourcecountryandcollectionsiteoftheAAgenometypewildriceaccessionswerestudiedusingthe originalcollectionformsoftheInternationalRiceInformationSystem(IRIS)fromtheIRRI(http://www.irri.org),whereaslandraceswereinvestigatedwithinformation obtainedbytheSystem-wideInformationNetworkforGeneticResources(SINGER),nowpartofthePlantGeneticResourceGateway(GENESYS, http://www.genesys-pgr.org).Thepassportdataofeachaccessionwascheckedtolocatethesitewherethesamplewasoriginallycollectedbeforebeingsenttotheseedbank.Thecollection siteincludedawildzoneorafieldborderforthewildspeciesandthegermplasmlocationbeforebeingsenttothegenebankforlandraces.Ricespecieswithunspecifiedor otherstatuses(e.g.,improvedcultivarandcrosses)werenotincludedintheanalysis,andneitherwerethewildaccessionslackingtheoriginalIRRIcollectionform.The dottedarrowsrepresentthedirectionsinwhichdomesticatedricemayhavespread.
mechanismofsubmergencetolerancewhichmaybeunique totheCCtypegenomegroupandwhichstillneeds tobe found.ThericevarietiesMadabaruandIR72haverecently beenshowntoharbornovelsubmergencetolerance quan-titative trait loci (QTLs), which are independent of the ethylene-mediatedSUB1Apathway[31].
Concludingremarks
Various studies have highlighted that the presence of SUB1Aallelesishighlyvariableinseveralwildand land-raceaccessionsofricebelongingtotheAAgenomegroup. Analysisofthegeographicaldistributionofwildriceand landracedata,togetherwiththemolecularanalysisforthe presenceofSUB1genes,suggeststhattheintrogressionof SUB1A-1fromwildintocultivatedriceoriginatedaround theGanges Basin.ThepresenceofSUB1A-1inO.sativa landraces present in other Asian regions suggests that early settlers may have brought with them the seeds of submergence-tolerantplants.
Submergence-toleranttraitshavealsobeenshowntobe presentinsomediploidCCtypewildriceaccessionswhich, however,lackSUB1A.OnlySUB1C-likegeneshavebeen foundinthesegenotypes;therefore,itispossiblethatthey
harboradistinctivemolecularmechanismofsubmergence tolerance, which is still unknown. In South Asia, these genotypesarefoundinthesamegeographicregionwhere AA rice species grow; however, success in intergenomic crossesisvery low.
Novel QTLs associated with submergence-tolerant traitsmightbeusefulinenhancing thelevelofsurvival. Indeed,thehybridizationofwildandcultivatedricewith theintrogressionofaliengenescangiverisetonew inter-estingvariations,duetothehighlevelofgeneticdiversity. Ricebreedingprogramsthatcouldovercometheproblemof cross-compatibility barriers would be a breakthrough in riceenhancement.
Acknowledgments
We would like to thank Julia Bailey-Serres for helpful discussions, ClaudioPugliesiforreadingthemanuscript,andSandroParlantiforhis assistanceinpreparingthemanuscript.
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