Oryza species as source for rice abiotic stress tolerance

15 Pages·2017·0.63 MB·English

GeneticsandMolecularBiology,40,1(suppl),238-252(2017)
Copyright©2017,SociedadeBrasileiradeGenética.PrintedinBrazil
DOI:http://dx.doi.org/10.1590/1678-4685-GMB-2016-0093
ReviewArticle
A walk on the wild side: Oryzaspecies as source for rice abiotic stress
tolerance
PalomaKoprovskiMenguer1,RaulAntonioSperotto2andFelipeKleinRicachenevsky3
1DepartamentodeBotânica,UniversidadeFederaldoRioGrandedoSul(UFRGS),PortoAlegre,RS,
Brazil.
2SetordeGenéticaeBiologiaMoleculardoMuseudeCiênciasNaturais(MCN),CentrodeCiências
BiológicasedaSaúde(CCBS),ProgramadePós-GraduaçãoemBiotecnologia(PPGBiotec),Centro
UniversitárioUNIVATES,Lajeado,RS,Brazil.
3ProgramadePós-GraduaçãoemAgrobiologia,DepartamentodeBiologia,UniversidadeFederaldeSanta
Maria(UFSM),SantaMaria,RS,Brazil.
Abstract
Oryzasativa,thecommoncultivatedrice,isoneofthemostimportantcropsforhumanconsumption,butproduction
isincreasinglythreatenedbyabioticstresses.Althoughmanyeffortshaveresultedinbreedingricecultivarsthatare
relativelytoleranttotheirlocalenvironments,climatechangesandpopulationincreaseareexpectedtosooncallfor
new,fastgenerationofstresstolerantricegermplasm,andcurrentwithin-speciesricediversitymightnotbeenough
toovercomesuchneeds.TheOryzagenuscontainsother23wildspecies,withonlyOryzaglaberrimabeingalsodo-
mesticated.Ricedomesticationwasperformedwithanarrowgeneticdiversity,andtheotherOryzaspeciesareavir-
tuallyuntappedgeneticresourceforricestresstoleranceimprovement.Herewereviewtheoriginofdomesticated
Oryzasativafromwildprogenitors,theecologicalandgenomicdiversityoftheOryzagenus,andthestresstolerance
variationobservedforwildOryzaspecies,includingthegeneticbasisunderlyingthetolerancemechanismsfound.
Thesummaryprovidedhereisimportanttoindicatehowweshouldmoveforwardtounlockthefullpotentialofthese
germplasms for rice improvement.
Keywords:Oryza,rice,wildspecies,abioticstress,domestication.
Received:April06,2016;Accepted:September27,2016.
Introduction increasinglyexposedtoamyriadofabioticstresses(Foley
et al., 2011; Mueller et al., 2012; Sang and Ge, 2013;
Continuous population and consumption growth are
Palmgrenetal.,2014).
placingenormousdemandsonnaturalresourcesandagri-
culture.Today,approximatelyabillionpeoplearechroni- Rice is one of the world’s most important staple
callymalnourishedanditisuncertainwhetherourcurrent crops, feeding more than 2.7 billion people worldwide
agriculturalsystemwillbeabletofeedtheexpectedworld (Muthayyaetal.,2014),andalsoamodelforgenomicre-
population,projectedtoreachninebillionby2050.Theef- searchinmonocots.Itiscultivatedon150millionhectares
ficient use of resources and reduced food waste can save of land, and its annual yield is close to 610 million tons
muchfood,andincreasedcropproductionisfundamental (http://irri.org/). Due to global adverse climate changes,
tomeettheworld’sfuturefoodneeds(Godfrayetal.,2010; ricegrowthandproductivityinrecentyearshasbeenseri-
Foleyetal.,2011;Palmgrenetal.,2014).However,thereis ously affected by abiotic stresses such as cold, drought,
an urgent need to reduce agriculture’s environment foot- heat, flood, and salt (Zhang et al., 2015). Plants have
print, and farming land should not be expanded at the evolved complex but not well understood responses. A
expenseofnaturalecosystems.Wearefacedwiththechal- complicated signaling network is effectively and timely
lenge of increasing food production without degrading initiated,whichultimatelyreprogramstheexpressionofa
land, water and biodiversity in an environment becoming large set of stress-responsive genes (Hong et al., 2016),
leading to a series of morphological, physiological, and
biochemicalchanges(Scafaroetal.,2011;Leietal.,2013).
Send correspondence to Felipe Klein Ricachenevsky. Departa-
The acclimation processes that result from stress percep-
mentodeBiologia,UniversidadeFederaldeSantaMaria(UFSM),
tionaimsatprotectingplantsfromdamagesandincreases
Av.Roraima1000,CEP97105-900,Prédio16,sala3254,Santa
Maria, RS, Brazil. E-mail: [email protected] thechanceofsurvival(HuandXiong,2014).However,itis
Mengueretal. 239
important to highlight that acclimation to stressful condi- damagearelowpercentageanddelayedgermination(Cruz
tionsdoesnotoccurinallplantspecies,anddependingon et al., 2013; Dametto et al., 2015), resulting in yield de-
stress intensity and duration, growth and yield can be se- creasesupto25%ofthefinalyieldandinincreasedweed
verely affected. In nature, there is a wide variability to competition (Fujino et al., 2004). During the vegetative
stress response and tolerance, making worthwhile the stage,itcanseverelyaffectseedlingestablishment,leading
searchfor“tolerancegenes”inwildrelativesofcultivated to yellowing of the leaves, growth retardation, and de-
species. creasedtillering(Cruzetal.,2013).Lowtemperaturesthat
Abioticstressisamajorconcernforriceproduction, occur at critical reproductive stages can adversely affect
and an increasing threat to food security considering cli- grainquality(incompletegrainmaturation)orcauseyield
mate change, population increase and area of arable land reductions(Jenaetal.,2012;Cruzetal.,2013;Zhangetal.,
available. Drought, flooding and extreme temperatures 2014).
should become more frequent according to predictions Availabilityofirrigationwaterisalimitingfactorin
(Wang, 2005; Bita and Gerats, 2013; Hirabayashi et al., attainingthefullpotentialyieldinmanycrops(Singhetal.,
2013), which are likely to increase pressure on grain har- 2015).Droughtisoneofthemostwidespreadanddamag-
vest.Foodsecurityisanissuetothehumanpopulationasa ingenvironmentalstressfactorsinplants(Krannichetal.,
whole, but especially in rural areas of Asia and Africa, 2015), especially in rice, which is sensitive to drought
whichrepresentabout35%ofthetotalriceharvestarea.In stressbecauseitisacclimatedtoeitherrain-fedorfullyirri-
Asia, where 700 million people live in extreme poverty, gatedfields.Theeffectofdroughtmayvarywiththediffer-
30%ofthemareinregionsthatarepronetoabioticstresses ent genotypes, development stages, and degree and dura-
suchasflooding,droughtandexcesssoilsalinity(Ismailet tionofdroughtstress(Wangetal.,2011).Riceplantsare
al.,2013).Thesestressesoftenoccurincombination,and highly sensitive to drought stress during vegetative stage
stressresponsivepathwaysoftenshowextensivecross-talk (resultinginreducedheight,tillernumber,andleafarea),at
(Mittler2006). thepanicleinitiationandbootingstages(Jiangetal.,2004;
Flooding is a widespread environmental stress. The Wang et al., 2011). In China, the average annual drought
rapiddeclineintheoxygen(O )diffusionrateduringflood- affectedareaisupto27millionhectaresandriceproduc-
2
ingisaccompaniedbyareductionincellularO levelsand tion has decreased by 70-80 billion Kg since the 1990s
2
anenergycrisis,whichareparticularlyseverewhenphoto- (Luo,2010).
synthesisislimitedorabsent(Bailey-SerresandVoesenek, Adeclineinriceproductioncausedbyheatstressis
2008). Although rice is considered a flood tolerant crop, one of the biggest concerns resulting from future climate
only limited cultivars display tolerance to prolonged sub- change. Maximum and minimum daily temperatures, and
mergence(Niroulaetal.,2012),withmostdyingwithin14 thenumberofhotdaysandwarmnightsinayear,areesti-
daysofcompletesubmergence. matedtoincreaseovermostlandareas(IPCC,2014).Inad-
Salinityisoneofthemostdevastatingabioticstresses dition, climate variability is predicted to increase, leading
in rice, and the salt-affected soils currently account for to frequent episodes of heat stress, often coinciding with
about20%ofthetotalpaddyriceplantingarea(Zhouetal., keydevelopmentalstagesincrops,suchasflowering(Hira-
2016). Soil salinity has adverse effects on plant germina- bayashietal.,2015).Itispredictedthatriceyieldswould
tion,strength,andyield(MunnsandTester,2008).Onex- bereducedbyupto10%withanaveragedailytemperature
posure to salt stress, the ionic balance (especially Na+/K+ increase of 1 °C (Peng et al., 2004). During early growth
ratio)anddistributionistheultimatemanifestationofsev- stagesofrice,theoccurrenceofheatstressinhibitsseedling
eralphysiologicprocessesinresponsetosaltstress(Chen establishment,leadingtonon-uniformgrowth,andreduced
Yetal.,2013),creatinganimbalanceinthesuppliesofwa- yield. The physiological and genetic basis of the heat re-
ter and other nutrient solutes (Sengupta and Majumder, sponseduringtheseedlingstageispoorlyunderstood(Lei
2010).Mostplantscanadapttolowormoderatesalinities, etal.,2013).Hightemperaturesatanthesiscausespikelet
buttheirgrowthisseverelylimitedabove200mMNaCl. sterilityduetothefailureofantherdehiscenceandthere-
Therefore, plant survival and growth depends on adapta- ductioninthenumberofgerminatingpollengrainsonthe
tions to re-establish ionic homeostasis (Hasegawa et al., stigma,leadingtoreductionsingrainyield(Jagadishetal.,
2000). 2010).
Coldstressisoneofthemajorenvironmentalfactors Therefore, the development of cultivated rice with
limitingthegrowth,productivity,andgeographicaldistri- abioticstresstoleranceisneededtostabilizetheproduction
butionofcrops,mostlyintemperateandhighaltitudeareas, levelofrice.Themethodcurrentlypracticedforimproving
due to the tropical origin of the rice species (Cruz et al., abiotic stress tolerance in rice cultivars is to explore
2013; Zhang et al., 2014). Low temperature can affect germplasmfordesirabletraits(Scafaroetal.,2010).Recent
growthanddevelopmentofriceplantsduringanydevelop- attempts(untilnowlimitedtoO.sativaspecies)havebeen
mentalstage,fromgerminationtograinfilling.Duringger- successful,withbackcrossingofOryzasativassp.japonica
mination,themostcommonsymptomsofcoldtemperature and indica leading to substantial improvements in abiotic
240 Oryzaspeciesandabioticstress
stresstolerance(Chengetal.,2007).Asthereareabout24 DivergenceoftheAgenometookplaceoverthepast
knownspecieswithintheOryzagenus,alargesourceofge- two million years, and the current most divergent species
netic material remains virtually untapped. The search for withinthisgrouparetheperennialO.meridionalis(rhizo-
variabilityintheancestorsofcultivatedrice,whichunder- matous) and O. longistaminata (Zhu and Ge, 2005;
goesalonghistoryofartificialselection,hasgreatpotential Vaughanetal.,2008).O.sativahastwopresumedwildan-
valueforricebreeding.Stresstolerancetraitsarelikelyto cestors(O.rufipogonandO.nivara),whiletheannualO.
befoundinwildricespecies(Tianetal.,2015),whichare barthii is the progenitor of African domesticated rice O.
recognizedasanimportantgeneticresourceforcultivated glaberrima (please see next section). The two cultivated
riceimprovement(SakaiandItoh,2010).Inthisreview,we speciesandtheirrespectiveprogenitorssharedanunknown
focusonthericedomesticationhistory,thediversification ancestralofabout0.86MYA(SarlaandSwamy,2005;Zhu
oftheOryzagenus,themechanismsandunderlyinggenetic etal.,2014).PerennialO.glumaepatulaistheonlyAge-
basisforabioticstresstoleranceinspecieswithintheOryza nome group member with a current distribution in Latin
diversity,whichillustratesthefeasibilityofusingricewild Americaandpresentsastrongrelationbetweengeneticand
relativesasasourceforbreedingstresstolerantO.sativa. geographicdistances(Jacqueminetal.,2013;Vaughanet
al., 2003). The A genome species O. meridionalis, O.
Diversity in theOryzagenus longistaminata, O. glaberrima and O. barthii are consid-
ered candidates for tolerance to heat and drought stresses
RicebelongstothegenusOryza,ofthetribeOryzeae, basedontheirdistributionintemperatureandmoistureex-
subfamily Ehrhartoideae and family Poaceae (Grass Phy- tremes(Atwelletal.,2014).
logenyWorkingGroup,2001).ThetribeOryzeaeincludes
TheCCgenomegroupisformedbyO.officinalis,O.
nineortengeneraandupto70species,andisverylikely
rhizomatis and O. eichingeri. All three species are peren-
monophyletic; in this tribe, Oryza L. and Leersia Sw. are
nial,occurringinshadeorsemi-shadeforestenvironments,
the two largest genera (reviewed by Kellogg, 2009). The
among other habitats. O. officinalis (generally rhizoma-
analysisofbothnuclearandchloroplastgenesrevealedthat
tous)hasahighlevelofgeneticdiversitybetweenpopula-
Oryza and Leersia are sister genera. The divergence of
tions, and O. rhizomatis (rhizomatous) is endemic to Sri
Oryza–Leersia from the other genera occurred approxi-
Lanka(Vaughanetal.,2003;LuandJackson,2004).The
mately 20.5 MYA and the divergence of Oryza from
only member of the diploid BB genome group is O.
Leersia14.2MYA(Geetal.,2002;GuoandGe,2005).
punctata, which also exists in the allotetraploid form
TheOryzagenusconsistsof24speciesspreadworld-
BBCC.BothBBandBBCCpopulationsaredistributedin
wide (Table 1) (Kellogg, 2009; Jacquemin et al., 2013).
Africa but occupying distinct niches. The diploid form is
ThephylogenyoftheOryzagenusspansapproximately15
foundinopenhabitats,whiletheallotetraploidinshadeor
millionyears(MY)ofevolutionaryhistory,aprocessthat
semi-shade environments (Vaughan et al., 2003). Both
created diverse ecological adaptations (Vaughan et al.,
formsofO.punctataarepotentialgeneticreservoirsfortol-
2003;Ammirajuetal.,2010).TheOryzaspecieshave11
erancetodroughtstressifconsideringtheirplasticityover
differentgenometypes(AA,BB,CC,BBCC,CCDD,EE,
moistureextremes(Atwelletal.,2014).O.eichingeriisbe-
FF,GG,KKLL,HHJJ,andHHKK),anda3.6-genomesize
lievedtobetheCCgenomedonortotheallotetraploidO.
variation(Luetal.,2009;Jacqueminetal.,2013;Atwellet
punctata,whilethediploidO.punctataistheBBgenome
al.,2014).
donortotheotherallotetraploidBBCCspeciesO.minuta
A phylogenomic study sampled and sequenced 142 and O. malampuzhaensis (rhizomatous). Perennial O.
single-copy genes to clarify the relationships among all minutaandO.malampuzhaensisseemtohavearisenfrom
diploidgenometypesofthericegenus(Zouetal.,2008). different polyploidy events if considering their distinct
The analysis identified two episodes of rapid speciation morphology,distributionandgeneticdiversity(Jacquemin
thatoccurredapproximatelyfiveandtenmillionyearsago etal.,2013;Vaughanetal.,2003).O.minutadiploidpro-
(MYA) and gave rise to almost the entire diversity of the genitors are O. punctata (BB), as already mentioned, and
genus. The first event occurred approximately ten MYA O. officinalis (CC), and its recent polyploidization is be-
(GuoandGe,2005)andledtoarapiddiversificationofthe lievedtohaveoccurredwithinthelast400,000years(Luet
Ggenome,Fgenomeandalineagethatsubsequentlydiver- al., 2009). O. malampuzhaensis, endemic to the Nalla-
sifiedintotherestofthericegenomes.Additionally,theH, malaisofEasternGhats(India),isunderseverethreatcon-
J and K genomes that are now only present in tetraploid sidering its narrow distribution over a small geographical
speciesalsodivergedaroundthistime(Geetal.,1999;Guo area,whichleadstovulnerabilitytohabitatdestructionand
andGe,2005).Thesecondeventledtothediversification fragmentation (Elangovan et al., 2012). The CCDD ge-
oftheA,B,andCgenomesapproximatelyfiveMYA,con- nomespeciesO.latifolia,O.altaandO.grandiglumisare
firmingthattheAandBgenomespeciesaresistersandthe verycloselyrelated,withcurrentdistributioninLatinAme-
Cgenomecladeissistertothat(Zouetal.,2008,Kellogg, rica.Infact,somestudiessuggestthatCCDDgroupmem-
2009). bersareonecomplexspecieswithdifferentecotypes(Vau-
Mengueretal. 241
es
n
o
si
s
e 3
Acc 27 52 405 36 f6 37 907 76 16 29 86 6 309 12 65 25
dUsualhabitat Savannaandsometimesinwoodland;wetsites;open UndulatingplainsofEucalyptusandLeptochloaorboxwoodland;wetsites;open Mopaneorsavannawoodland,savannaorfadama;deepwater;open Flatironstonerocks,granite/lateriticoutcrops;waterupto0.5mdeep,butmoreofteninshallowwater;open Saltmarshecosystems;inundated(twiceaday)withsalineriverorseawater;open Undisturbedforest,galleryorevergreenforest,orforestmargins;damporfloodedsites;shadeorsemi-shade Uplandtodeepwater;open Swampsandmarshes;usuallydeepwater;open Savannaorwoodland;wateratriver’sedgesorwetsites;openorshade Forestfloor;dampsites;shade Lowforest,rainforest,secondarygrowthforest,openwoodland,undulatingsavanna,pasture,cultivatedfields,openswamp,hillslopes,highridges,coastalbelts;wetordampsites;openorsemi-shade Forestareas;seasonallywet;shadeorsemi-shade Savannaoropeningsinrainorgalleryforests;deepwater;open Forestpools;seasonallydry;shade Edgesofseasonallyfreshwaterlagoons,temporarypools,andswamps;seasonallywet;open Forestareas;dampsites;shade
metypes,lifespan,geographicaldistributions,habitatsandavailableaccessions. cDistribution Belize,Brazil,Colombia,GuyanaandParaguay NorthernAustralia Benin,Botswana,BurkinaFaso,Cameroon,CentralAfricaRepublic,Chad,Côted’Ivoire,Ethiopia,TheGambia,Ghana,Guinea,Mali,Maurita-nia,Namibia,Niger,Nigeria,Senegal,SierraLeone,Sudan,Tanzania,andZam-bia BurkinaFaso,Cameroon,CentralAfricanRepublic,Chad,DemocraticRepublicofCongo,Guinea,Mali,Niger,Senegal,SierraLeone,Sudan,Tanzania,andZambia India,SriLanka,BangladeshandMyanmar CentralAfricaRepublic,Côted’IvoireDemocraticRepublicofCongo,Ke-nya,Rwanda,SriLanka,Tanzania,andUganda WestAfrica Bolivia,Brazil,Colombia,CostaRica,Cuba,DominicanRepublic,FrenchGui-ana,Guyana,Honduras,Mexico,Panama,Surinam,andVenezuela Argentina,Bolivia,Brazil,Colombia,Ecuador,FrenchGuiana,Paraguay,andPeru India,Cambodian,Vietnam,Thailand,southernChina,Malaysia,Philippine,Ne-palandSriLanka Argentina,Belize,Bolivia,Brazil,Colombia,CostaRica,Cuba,DominicanRe-public,Ecuador,ElSalvador,FrenchGuiana,Guatemala,Guyana,Haiti,Honduras,Mexico,Nicaragua,Panama,Paraguay,Peru,PuertoRico,Suri-nam,TrinidadandVenezuela IndonesiaandPapuaNewGuinea Angola,Benin,Botswana,BurkinaFaso,Burundi,Cameroon,CentralAfricaRe-public,Chad,Congo,Côted’Ivoire,DemocraticRepublicofCongo,Ethio-pia,Gabon,TheGambia,Ghana,Kenya,Madagascar,Malawi,Mali,Martinique,Mozambique,Namibia,Niger,Nigeria,Rwanda,Senegal,Sey-chelles,SierraLeone,Somalia,SouthAfrica,Sudan,Tanzania,Uganda,Zambia,andZimbabwe WesternGhatsofSouthIndia Australia,Indonesia,andPapuaNewGuinea Indonesia,Malaysia,Philippines,andThailand
o
includingtheirgen a/Genome bLifehistory CCDD/Perennial EE/Perennial AA/Annual FF/Annual KKLL/Perennial CC/Perennial AA/Annual AA/Perennial CCDD/Perennial GG/Perennial CCDD/Perennial HHJJ/Perennial AA/Perennial BBCC/Perennial AA/Annual GG/Perennial
s,
Table1-Oryzaspecie Species Oryzaalta Oryzaaustraliensis Oryzabarthii Oryzabrachyantha Oryzacoarctata Oryzaeichingeri Oryzaglaberrima Oryzaglumaepatula Oryzagrandiglumis Oryzagranulata Oryzalatifolia Oryzalongiglumis Oryzalongistaminata Oryzamalampuzhaensis Oryzameridionalis Oryzameyeriana
242 Oryzaspeciesandabioticstress
es
n
o
ssi 82
e 4 7 9
Acc 86 206 317 g98 g98 21 21 161 212 3
dUsualhabitat Lowlandareasbesidestreamsandriverbanks;seasonallywet;shadeorsemi-shade Swampyareas;seasonallywetandshallowwater;open Edgeoforinforests,openvegetation,inabandonedculti-vatedricefields,inSoutheastAsianearthecoast;wetsites;openorsemi-shade Seasonallyswampareas,aroundwaterholesandpools,onriverbanksinareasthatfloodto1mdepth;open Forestareas;wetsites;shade Tropicalforestandopen,tallscrubwithgrassyopenings;swampyorperiodicallyfloodedareas;openorsemi-shade Marshesornearstreamsidesinforest;seasonallywet;shade Swampsandmarshes;seasonallydeepwaterandwetyearround;open Uplandtodeepwater;open Forestareas;wetsites;shadeorsemi-shade
cDistribution PhilippinesandPapuaNewGuinea Bangladesh,Cambodia,China,India,Laos,Malaysia,Myanmar,Nepal,SriLanka,Thailand,andVietnam Australia,Bangladesh;Brunei,Cambodia,China,India,Indonesia,Laos,Malay-sia,Myanmar,Nepal,PapuaNewGuinea,Philippines,Thailand,andVietnam Angola,Benin,Cameroon,CentralAfricaRepublic,Chad,Congo,Côted’Ivoi-re,DemocraticRepublicofCongo,Ethiopia,Ghana,Kenya,Madagascar,Ma-lawi,Mozambique,Nigeria,Sudan,Swaziland,Tanzania,Uganda,Zambia,andZimbabwe Angola,Benin,Cameroon,CentralAfricaRepublic,Chad,Congo,Côted’Ivoi-re,DemocraticRepublicofCongo,Ethiopia,Ghana,Kenya,Madagascar,Ma-lawi,Mozambique,Nigeria,Sudan,Swaziland,Tanzania,Uganda,Zambia,andZimbabwe SriLanka Cambodia,Indonesia,Laos,Malaysia,Myanmar,PapuaNewGuinea,andThai-land Australia,Bangladesh,China,India,Indonesia,Laos,Malaysia,Myanmar,Ne-pal,PapuaNewGuinea,Philippines,SriLanka,Thailand,andVietnam SoutheastAsia IndonesiaandPapuaNewGuinea a,b,c,da,c,duandJackson2004,SenguptaandMajumder2010,Vaughanetal.,2003heGenesysDatabase(http://www.genesys-pgr.org/).eresiacoarctata.erennialO.punctata.
Table1(cont.) aSpeciesGenome/ bLifehistory OryzaminutaBBCC/Perennial OryzanivaraAA/Annual OryzaofficinalisCC/Perennial OryzapunctataBB/Annual OryzapunctataBBCC/Perennial OryzarhizomatisCC/Perennial OryzaridleyiHHJJ/Perennial OryzarufipogonAA/Perennial OryzasativaAA/Annual OryzaschlechteriHHKK/Perennial aa,b,c,dAccordingtoJacqueminetal.,2013,LeNumberofaccessionentriesperspeciesintfIncludesaccessionsregisteredasOryza/PortgIncludesaccessionsfrombothannualandp
Mengueretal. 243
ghanetal.,2003).O.altapolyploidizationwasestimatedto ica was introduced and hybridized with indica, around
have happened less than 1.6 MYA. Additionally, O. 4,000yearsago(Fulleretal.,2009,2011;GrossandZhao,
grandiglumisandO.latifoliaareconsideredcandidatesfor 2014).BothO.rufipogonanditsannualderivedO.nivara
tolerancetofloodingstress(Luetal.,2009;Atwelletal., arenativetoIndiatoday.Inmostofthephysiologicaland
2014). morphologicaltraits,O.nivaraisrathersimilartotheculti-
The GG genome species O. granulata and O. vated rice than O. rufipogon. Thus, O. nivara could have
meyeriana are found in forest shade environments. O. served as the indica progenitor, and domestication would
granulataoccupiesthemostbasalpositionintheOryzage- have required fewer genetic modifications or mating sys-
nusphylogeny,presentsahighlevelofgeneticdiversitybe- temtransitions(Lietal.,2006;SangandGe,2013).Ifthis
tween populations, and is a potential genetic resource for hypothesis is correct, selection would have been less in-
tolerancetocoldstress(Aggarwaletal.,1997;Vaughanet tense for indica because O. nivara already presented sev-
al., 2003; Atwell et al., 2014). The F genome species O. eral cultivated rice traits. Thus, key domestication alleles
brachyantha has a compact genome (the smallest in the had more chance to arise during japonica domestication
Oryza genus) and is distributed in West and East Africa fromO.rufipogon,andsemi-domesticatedindicabecame
(ChenJetal.,2013).Limitedinformationisavailablefor theprimaryrecipientofthedomesticationalleleswhenja-
O. coarctata (KKLL), O. longiglumis (HHJJ), O. ridleyi ponica was brought to India (Vaughan et al., 2008; Sang
(HHJJ)andO.schlechteri(HHKK)(Vaughanetal.,2003; andGe,2013).
Jacquemin et al., 2013). Regarding abiotic stresses, O.
Duringtheprocessofcropdomesticationmanyofthe
coarctatashowsconsiderableadaptationtosalinity,andO.
inherited traits involved in biotic and abiotic stress resis-
ridleyiandO.schlechteriareconsideredgoodgeneticres-
tancemayhavebeenweakenedorlost,sinceitisestimated
ervoirsfortolerancetoflooding(Luetal.,2009;Sengupta
thatonly10-20%ofwildspeciesdiversityispresentincul-
andMajumder,2010;Atwelletal.,2014).Asummaryof
tivatedrice(Zhuetal.,2007;Palmgrenetal.,2014).Oneof
allOryzaspeciescitedinthisreview,includingtheirgeno-
themostimportantresourcesforimprovementofcultivated
types,lifespan,geographicaldistributionsandhabitats,is
riceisthegeneticreservoirhiddeninwildricespeciesdis-
presentedinTable1.
tributedacrossseveralbiomesworldwide.Itisalsoimpor-
tant to underline that isolated populations within species
The origin of Asian cultivated rice
may also contain critical genes (Jacquemin et al., 2013;
TherearetwodistinctgroupsofAsiancultivatedrice, Atwelletal.,2014).Ricegenebanksaroundtheworldex-
namely O. sativa ssp. japonica and indica, which can be hibitanextensiveseedcollection,coveringthegeneticdi-
differentiated by morphological and physiological traits, versity present in farmers’ cultivars, landraces and Oryza
additionallytoanincompletesterilitybarrier(SangandGe, species. The two largest gene banks are the International
2013).Theoriginandevolutionofthejaponicaandindica RiceResearchInstituteinthePhilippines(4,370wildspe-
subspeciesisunderconsiderabledebateoverthepastsev- cies and hybrids accessions at IRRI, http://irri.org), and
eralyears.Twomodelsofinteractivedomesticationscenar- Oryzabase in Japan (1,703 entries,
ios were proposed. The ‘snowballing model’ suggests a http://www.shigen.nig.ac.jp) (Jacquemin et al., 2013).
single domestication event that created an early cultivar Moreover, the Genesys database
withasetofdomesticationtraits.Thisearlycultivar,when (http://www.genesys-pgr.or) allows searching accessions
hybridized with different wild rice populations, japonica- formanyspeciesinseveralseedbanks,beingavaluablere-
like and indica-like, would have enabled the fixation of sourceforgermplasmdistribution(seetotalnumberofac-
critical domestication alleles in each one of them sepa- cessions available for each Oryza species in Table 1). A
rately.Alternatively,inthe‘combinationmodel’,bothsub- genus-wide comparative genome platform is essential to
species were domesticated independently from diverse understand the genetic differences associated with abiotic
wild rice ecotypes with subsequent hybridization, leading factors. The sequencing of 16 Oryza genomes is either
to the introgression and fixation of domestication alleles complete or underway with “gold standard” reference se-
(SangandGe,2007). quences available for the cultivated species O. sativa ssp.
Consideringarcheologicalandgeneticstudiesavail- japonica and O. glaberrima, and for the wild species O.
able to date, the ‘combination model’ is suggested as the barthii and O. brachyantha (Jacquemin et al., 2013). The
closestscenariofromwhathadhappenedduringAsianrice introgression of desirable traits via conventional breeding
domestication(GrossandZhao,2014).Briefly,thejapon- intocultivatedriceshouldbemorefeasiblefromcloserela-
ica subspecies was originated from O. rufipogon in the tives(althoughaviablehybridO.coarctataXO.sativahas
YangtzeRiverValleyinChina,wherericecultivationpos- been reported – see below). Among the AA genome spe-
siblystartedaround8,000yearsago.Meanwhile,indicaor cies,introgressionlinescanbeobtainedbybackcrossingF1
proto-indica independent origin of cultivation probably hybridsthatarepartiallysterile,andvariouslevelsofpost-
took place in the Ganges plains in India, but proto-indica zygotic barriers are known (Doi et al., 2008). The gene
domesticationwasonlycompleteafterdomesticatedjapon- groups that cause these incompatibilities were genetically
244 Oryzaspeciesandabioticstress
identified,butfurtherstudiesareneededtobreaktherepro-
ductiveisolation(Jietal.,2005;Qiuetal.,2005).WhenO.
sativa is crossed to non-AA genome species, viable but
highlysterileF1hybridscanbeobtainedusingembryocul-
ture.However,theaberrantchromosomepairinginmeiosis
makes it difficult to introgress genetic information from
thesespeciesintocultivatedrice(Doietal.,2008).Trans-
genicapproacheswillbeeventuallyneededforgenesfrom
taxonomicallydistantspecies(Vaughanetal.,2003;Palm-
gren et al., 2014). Therefore, it is of great significance to
understandthegeneticdiversitywithinthewildrelativesof
Oryzainthecontextoftheirnaturalenvironmentoforigin, Figure1-SubmergencetoleranceandgeneticarchitectureofSUB1locus
inordertoidentifythegeneticbasisofphenotypicvariation incultivatedandwildOryzaspecies.GenotypesfromAAgenomespecies
Oryzasativa,OryzarufipogonandOryzanivaraaretolerantorsensitive
betweenandwithin-species.Thisknowledgeisanimpor-
to submergence depending on the presence of SUB1A-1 allele of the
tant resource to improve rice production under abiotic
SUB1A gene. Genotypes that either have SUB1A-2 allele or lack a
stresses(SangandGe,2013;GrossandZhao,2014;Palm- SUB1A,carryingonlySUB1BandSUB1Cgenes,aresensitive.Geno-
grenetal.,2014). typesfromCCgenomespeciesOryzaeichingeri,Oryzarhizomatisand
theCCDDtetraploidspeciesOryzagrandiglumiswereshowntobetoler-
anttosubmergencewhilecarryingaSUB1Agene-lackingSUB1locus,
Abiotic stress tolerance in wild relatives: indicatingthelocusdoesnotcontributetothestresstoleranceinthesespe-
cies.
submergence
Riceiscommonlygrowninfloodedsoilcontaininga
whereasathirdgene,SUB1A,ispresentonlyinasubsetof
thin water layer. Although rice roots are well adapted to
them.Interestingly,tolerancetosubmergenceislinkedtoa
hypoxicconditions,mostricecultivarsdierapidlyiftheir
specificalleleoftheSUB1Agene,namedSUB1A-1(Xuet
shoots are submerged (Mackill et al., 2012). Several
al.,2006).AccessionsthatlackSUB1Agene,orcarrythe
rainfed rice areas are at risk of flooding, a stress that de-
SUB1A-2 allele, are sensitive to submergence (Figure 1).
creases yield substantially (Ismail et al., 2013). Submer-
IntrogressionoffunctionalcopiesofSUB1A-1insensitive
gence inhibits aerobic metabolism and photosynthesis,
genotypesissufficienttogeneratetolerantplants(Xuetal.,
leading to carbohydrate depletion and, depending on the
2006).
stress intensity, plant death (Fukao and Bailey-Serres,
ThetolerantSUB1A-1alleleisderivedfromtheaus
2004). However, rice plants are able to tolerate submer-
subgroupofindicarice(Xuetal.,2006).Wildspeciesfrom
genceusingdifferentstrategies.Inthelowoxygenescape
theOryzagenuscommonlygrowinconstantlyorseason-
syndrome(or“escapestrategy”)shootelongationisstimu-
allywethabitats(Vaughanetal.,2003),andthussubmer-
lated by progressive flooding, keeping leaves in contact
gencetolerancecouldbefoundinotherspecies.Niroulaet
with the air and escaping the increasing levels of water
al.(2012)tested109accessionsofriceandwildrelatives,
(Bailey-SerresandVoesenek,2008).Inthe“quiescentstra-
including12species,forsubmergencetolerance,andfound
tegy”,hypoxiareduceselongation,repressescarbohydrate
O.rufipogonandO.nivara(AAgenome;Table2)tolerant
degradation and stimulates anaerobic metabolism. When
accessions that carry the SUB1A-1 allele, showing that
water recedes, plants resume growth. While the escape
SUB1 locus architecture determines submergence toler-
strategy only results in submergence tolerance if flooding
anceinthesespecies,asinO.sativa(Figure1;Niroulaet
occursprogressively,ricegenotypesthatusethequiescent
al., 2012). Strikingly, accessions of O. rhizomatis and O.
strategyareabletosurviveupto14daysofcompletesub-
eichingeri(CCgenome;Table2)werealsofoundtobesub-
mergence(Bailey-SerresandVoesenek,2008).Bothstrate-
mergencetolerant,butSUB1Asequenceswereabsentfrom
gies were elucidated at the molecular level: the quiescent
genomes of tested accessions, indicating that a novel,
strategyislinkedtotheSUB1locus,whiletheescapestrat-
SUB1A-independent mechanism is responsible for sub-
egyisdependentontheSNORKEL(SK)locus(forreviews
mergencetolerance,atleastinthesetwoCCgenomespe-
see Bailey-Serres and Voesenek, 2008; Mickelbart et al.,
cies(Figure1;Niroulaetal.,2012).
2015).
Oryza grandiglumis is a tetraploid species with
SUB1isthemajorQTLassociatedwithsubmergence CCDD genome (Table 2) that grows in Amazonian
tolerance in rice cultivars that use the quiescent strategy floodplains,wherewaterlevelscanreachupto10meters,
(Fukaoetal.,2009).TheSUB1locuswasmappedtochro- andthusitwasexpectedtoshowsomedegreeofsubmer-
mosome 9, and is composed of a cluster of ethylene re- gencetolerance(Okishioetal.,2014,2015).Dependingon
sponse factors (ERF) genes located in tandem, named the flooding conditions, O. grandiglumis showed distinct
SUB1A,SUB1BandSUB1C(Figure1).Differentricege- responses: when progressively submerged, the internodes
notypeshavetwogenesinthecluster,SUB1BandSUB1C, elongated, resembling the escape strategy of O. sativa;
Mengueretal. 245
Table2-TolerancetoabioticstressesfoundinaccessionsofOryzaspeciesandreferences.
Species TolerancecomparedtoO.sativa Reference
Oryzacoarctata Salt SenguptaandMajumder,2009
Oryzaeichingeri Submergence Niroulaetal.,2012
Oryzaglaberrima Salt,Drought Ndjiondjopetal.,2010,Plattenetal.,2013
Oryzaglumaepatula Submergence Hattorietal.,2009
Oryzagrandiglumis Submergence Okishioetal.,2014,2015
Oryzameridionalis Heat Scafaroetal.,2010
Oryzanivara Drought Singhetal.,2015
Oryzaofficinalis Drought,Heat(EarlyMorningFlowering) Ishimaruetal.,2010,Fengetal.,2012
Oryzarhizomatis Submergence Niroulaetal.,2012
Oryzarufipogon Salinity,Cold,Drought,Submergence Hattorietal.,2009,Tianetal.,2011,Xiaoetal.,2014
however,whenplantswerecompletelysubmerged,growth Thegeneticbasisoftolerancetoionicstressismuch
was reduced, as in the quiescent strategy (Okishio et al., betterunderstoodthantoosmoticstress(Royetal.,2014).
2014).Interestingly,SUB1AisabsentinO.grandiglumis, ArangeoftransportersinvolvedinreducingNa+accumula-
indicatingthataSUB1A-independentmechanismforaqui- tioninshootsandinsubcellularcompartmentalizationwas
escentstrategyispresent,asobservedforO.rhizomatisand described, such as the high affinity potassium transporter
O.eichingeri(Figure1).GenessimilartoSNORKEL1and (HKT),saltoverlysensitive(SOS)andNa+/H+exchanger
SNORKEL2, responsible for the escape strategy in deep- (NHX)genefamilies(Mickelbartetal.,2015).HKTmem-
water-adapted O. sativa, as well as O. rufipogon and O. bersarecrucialdeterminantsoftissueconcentrationofNa+.
glumeapatula (AA genome; Table 2), are absent in O. OsHKT1;5isthecausativegeneofSaltol,themajorquanti-
grandiglumis (Hattori et al., 2009, Okishio et al., 2015). tative trait locus (QTL) for salt accumulation in O. sativa
These results indicate that O. grandiglumis is tolerant to genotypes(Renetal.,2005).OsHKT1;5isaplasmamem-
both gradual and full submergence by unknown mecha- branetransporterthatregulatespartitioningofNa+between
nisms (Okishio et al., 2014), indicating that CC genome rootsandshootsbyeffluxofNa+fromthexylemtoadja-
Oryzaspeciesmightprovidenewmolecularmechanismsto cent parenchyma cells (Hauser and Horie, 2010). Four
improvecultivatedrice. aminoacidchangesinOsHKT1;5resultedinincreasedNa+
efflux activity in salt tolerant indica cultivar Nona Bokra
comparedtothesaltsensitivecultivarKoshihikari(Renet
Salinity
al.,2005).AlthoughotherQTLsweredescribed(Negrãoet
al.,2011),Saltolistheonlyonethathasbeenclonedsofar.
Soilsalinizationisaworldwideproblemforagricul-
InalargescreeningeffortwhichincludedseveralO.
ture.Itaffects6%oftotalEarth’sland,asaresultofnatural
sativacultivars,landracesandO.glaberrima(AAgenome,
accumulation over long periods of time (Rengasamy,
Table2)genotypes,itwasshownthatsalinitysensitivityis
2002). However, agricultural activity contributes to sec-
correlated with Na+ concentration in leaf blades.
ondary salinization: 2% of all dry land is becoming
OsHKT1;5genotypewasshowntobeamajordeterminant
salinized,andmorethan20%ofirrigatedsoilsareaffected,
fortolerance:themoreactivetheeffluxtransporter,which
mostly because of irrigation water containing small
directstheNa+exclusionfromthetranspirationstream,the
amountsofsodiumchloride(TesterandDavenport,2003).
lessNa+istranslocatedtoleaves(Plattenetal.,2013).In-
Plantsvaryintheirsensitivitytosaltstress,andriceis terestingly,theseauthorsfoundtolerantO.glaberrimaac-
themostsensitiveamongcereals.Salinityreducesgrowth cessionswithlowNa+concentrationinleaves,butcarrying
rate,includingcellularandleafexpansion,numberoftillers OsHKT1;5 alleles that are associated with salt sensitivity
andphotosynthesis,andcanleadtoprematuresenescence and Na+ accumulation in leaves of O. sativa genotypes.
of older leaves (Munns and Tester, 2008, Sirault et al., TheseresultsindicatethatO.glaberrimagenotypescould
2009).Thedeleteriouseffectsofsaltinplantscanbeare- exclude Na+ from shoots using a mechanism independent
sultofosmoticstress(causedbysaltinthesoil),orofionic ofOsHKT1;5(Plattenetal.,2013).
stress (toxic effect of Na+ accumulation in plant tissues; OtherspeciesfromthegenusOryzawereexploredfor
Munns and Tester, 2008). The tolerance to ionic stress is salttolerancegenes.O.rufipogonwasshowntobesalttol-
dealt with by Na+ exclusion from xylem vessels to avoid erantwhencomparedtoricesensitivecultivars(Zhouetal.,
shootaccumulation,orbytissuetolerance,whenNa+levels 2016).IntrogressionlinesderivedfromO.rufipogonXO.
reachtoxiclevelsandplantleafcellscompartmentalizesalt sativacrossrevealed15QTLsforsalinitytolerance,13of
toreducedamage(Royetal.,2014). them derived from the O. rufipogon parent (Tian et al.,
246 Oryzaspeciesandabioticstress
2011). Over-expression of bHLH transcription factors regulated during the day, presumably reflecting the circa-
OrbHLH001andOrbHLH2fromO.rufipogonresultedin dianvariationintideexperiencedbytheplant,andisalso
Arabidopsis and O. sativa salt tolerant lines (Zhou et al., rapidly induced by NaCl treatment, compartmentalizing
2009;Lietal.,2010;ChenYetal.,2013).Theseauthors Na+ into vacuoles (Kizhakkedath et al., 2015). Thus, O.
showedthatOrbHLH001isabletopositivelyregulatethe coarctataisadaptedtohighsalinityenvironmentsbyusing
K+ transporter OsAKT1, suggesting that salt tolerance re- multiplemechanismstocopewithsaltstress,includingde-
sultsfrommaintenanceofK+homeostasisunderhighNa+ creasedroot-to-shoottranslocationandincreasedcompart-
conditions(ChenYetal.,2013).Basedonheterologousex- mentalizationinthevacuoleandsecretioninsalthairs.
pressioninArabidopsis,OrbHLH2wassuggestedtoposi-
Proteomic analyses identified up-regulated proteins
tivelyregulategenesfromtheCBF/DREBpathway(Zhou by Na+ treatment in O. coarctata, including transcription
et al., 2009). Indeed, transcriptomic studies of the O.
factors of the CBF/DREB pathway of abiotic stress re-
rufipogonresponsetohighsalinityshowedthattranscrip-
sponse(ShinozakiandYamaguchi-Shinozaki,2000);acel-
tionfactorsareamongthetopup-regulatedgenes(Zhouet
lulose synthase-like, which could help maintaining cellu-
al.,2016).
losesynthesisduringsaltstress(Endleretal.,2015);andan
L-myo-inositol 1-phosphate synthase, important for ino-
Oryza coarctata, a promising source of salinity sitol synthesis. Inositol metabolism is, in fact, one of the
and submergence genes for rice moststudiedaspectsofO.coarctatasalttolerance.Itsde-
rivative,pinitol,isaknownosmoprotectantinmanyplant
Oryza coarctata (also known as Porteresia species,andaccumulatesinO.coarctataunderhighsalin-
coarctata, Lu and Ge, 2003) is an allotetraploid wild rice ity(Senguptaetal.,2008;SenguptaandMajumder,2010).
withextremesaltandsubmergencetolerance.Itisunique Strikingly, cloning and characterization of O. coarctata
amongwildricespecies,sinceithasaKKLLgenome(Ta- L-myo-inositol 1-phosphate synthase (INO1) showed that
ble1;Luetal.,2009).O.coarctatagrowsincoastalregion enzyme activity is maintained properly even in high salt
of India and Bangladesh, where it experiences lunar tides concentrations,andthatitsexpressioninplantsandbacte-
and is submerged with saline seawater every 12 hours riaconfershigh,albeitvariable,salttolerancetotheseor-
(SenguptaandMajumder,2010,Gargetal.,2014).Ithas ganisms (Majee et al., 2004; Das-Chatterjee et al., 2006;
alsobeenestablishedasanimportantresourceforprospect- SenguptaandMajumder,2010).Thishighlightsthepoten-
inggenestoimprovecultivatedrice(Gargetal.,2014).A tialofwildspeciestoprovideusefulproteinsforrice(and
hybrid derived from a cross between O. sativa and O. other crops) improvement. Moreover, inositol methyl
coarctatahasbeenreported(Jena,1994),andsalttolerant transferase(IMT1),whichmethylatesinositolintopinitol,
rice cultivars with introgressed O. coarctata traits for salt is up-regulated in the same conditions as INO1 in O.
tolerance are currently under development in the Interna- coarctata,indicatingthatinositolsynthesisandconversion
tional Rice Research Institute (IRRI; www.irri.org). Still, to pinitol are key steps for salt tolerance in this species
little is known about the physiological and molecular de- (Senguptaetal.,2008).
tailsofthiswildriceadaptationtohighsalinityconditions.
Morerecently,astudyevaluatedO.coarctatatrans-
O.coarctatagrowth,relativewatercontentandpho- criptomic changes under salt and submergence stresses
tosynthesis are unaffected by high concentrations (400 (alone or combined, compared to control conditions), and
mM) of NaCl, conditions in which O. sativa salt tolerant found several transcription factors up-regulated in leaves
cultivars do not develop properly (Sengupta and Majum- understressconditions,suchasNAC,WRKYandMYBgene
der,2009).LeavesofO.coarctatacontain“salthairs”,out- familymembers,indicatingextensivetranscriptionalregu-
growthsoftheepidermisthatincreasetheirnumberunder lationinstressresponses(Gargetal.,2014).GeneOntol-
highsalinityandsecreteexcessivesalt.Whensaltconcen- ogyanalysesshowedenrichmentofABA-responsivegenes
trationinthegrowthmediaishigh(300-400mM),thesalt undersalinitystress,andofcarbohydratemetabolismand
hairs in the abaxial surface collapse and fall off from the anaerobic respiration genes under submergence stress. In
leaf surface (Sengupta and Majumder, 2009). Still, total plantsundersubmergencestress,genesrelatedtoethylene
Na+ concentration in leaves of O. coarctata does not in- andgibberellinresponseswerealsoidentified,alongwith
creaseundersaltstress,indicatingthatO.coarctataavoids Alcohol Dehydrogenase, a marker for anoxia stress, indi-
Na+toxicityinmesophyllcellsbycompartmentalizationof catingthataSUB1A-relatedresponsemightbepresentin
salt in epidermal hairs, a mechanism similar to what is O.coarctata(Gargetal.,2014;seeabovefordiscussionon
knownforotherhalophytegrasses(SenguptaandMajum- submergencestressmechanisms).However,demonstration
der,2009,2010).Thesecretedsaltisasignificantpropor- of the presence of SUB1A-like ERF transcription factors
tionoftheNa+reachingleaves,andimportanttomaintaina andoftheirroleinsubmergenceresponseinO.coarctatais
low Na:K ratio (Sengupta and Majumder, 2010). A lacking.Moreover,suberinandcellulosesynthesis-related
tonoplast-localizedtransporterfromtheNHXfamilyofO. transcriptswereidentifiedasup-regulatedinbothstresses,
coarctata was recently cloned. PcNHX1 transcription is indicatingthattheseprocessesmightbekeyforstresstoler-
Mengueretal. 247
ance,asobservedinotherspecies(Gargetal.,2014;Endler sequencefoundintolerantjaponicacultivarsrepresentsan
etal.,2015;Barberonetal.,2016). ancient allele from O. rufipogon that was selected during
domestication(Maetal.,2015).However,itisimportantto
Cold notethattheSNPinCOLD1explainsonlypartofthecold
toleranceinrice,atraitforwhichmanyminoreffectQTLs
The japonica cultivars of O. sativa are usually
are expected to contribute (Cruz et al., 2013; Ma et al.,
adaptedtotemperateclimates,aprocessthatwasdrivenby
2015;Maoetal.,2015).Thus,otherQTLsshouldbechar-
domestication,whileindicacultivarsaregenerallytropical
acterized and used in combination in order to develop
(Kovachetal.,2007;Maetal.,2015).Thus,temperateja-
highlytolerantlines,andnewlyidentifiedgenesfromwild
ponicacultivarsaremoretoleranttolowtemperaturesthan
speciesmightalsobeuseful.
indica,andintrogressionofcoldtolerancetraitsfromtem-
perate into tropical genotypes is desirable (Cruz et al.,
Drought
2013;Damettoetal.,2015).However,littleisknownabout
the molecular basis for low temperature tolerance in O. Droughttoleranceisacomplextrait,withmanygenes
sativa,andevenlessaboutthevariationofcoldtolerance andprocessesinvolved(Singhetal.,2015).Riceinparticu-
amongitswildrelatives. lar demands great amounts of water for proper develop-
The Oryza genus has a pan-tropical distribution, ment, owing to its shallow roots compared to other crops
growinginregionswithanaveragelowtemperatureof15 (Kondo et al., 2000). QTLs for drought tolerance were
°Coraboveduringthegrowthseason,withonlyafewex- identifiedwithinO.sativavariability,andcausativegenes
ceptions (Atwell et al., 2014). Hence, it is possible that have been cloned (Vikram et al., 2011; Uga et al., 2013).
other species of Oryza might be better adapted to lower DRO1 (DEEPER ROOTING 1), a previously unknown
temperatures,beingabletoprovideallelestoimprovecold protein,isresponsiblefordownwardgrowthofriceroots,
tolerance.Atwelletal.(2014)usedthedistributionofeach and introgression of DRO1 in otherwise shallow root rice
speciesindifferentclimatestoestimatethebestcandidates genotypesincreasesrootangleanddroughttolerance(Uga
forstresstolerance,andO.granulataissuggestedasapos- et al., 2013). Still, wild rice species might be a source of
siblesourceforcoldtolerance.O.eichingeri(CCgenome, stronger drought tolerance genes and mechanisms, since
Table2)alsogrowsinlowtemperatureenvironments,and theyareadaptedtoamuchwiderspectrumofenvironments
couldbeconsideredagoodcandidate(Atwelletal.,2014). (Vaughanetal.,2003;Atwelletal.,2014).
However,screeningsofcoldtolerancearestilllackingfor Speciesthatarepresentinlowmoistureregionswere
mostOryzaspecies. suggestedasmorelikelycandidatesfordroughttolerance,
One genotype of O. rufipogon, named Dongxiang namely: O. barthii, O. australiensis, O. glaberrima, O.
wild rice, is able to withstand overwintering in its natural longistaminata and O. punctata (Atwell et al., 2014). At
habitatandtemperatureaslowas3°Cforthreedaysinlab- least three of these (O. australiensis, glaberrima and
oratory conditions (Xiao et al., 2014; Mao et al., 2015). longistaminata),plusO.meridionalis,presentthickleaves
UsinganexperimentalpopulationderivedfromDongxiang andhighmesophyllconductancetoCO diffusion,indicat-
2
wildriceXNanjing11(acoldsensitivecultivar)crosses,a ing that they might be drought tolerant, since these traits
CBF3/DREB1Ggenewasfoundtoco-localizetoaprevi- canbeassociatedwithahigherwateruseefficiency(Sca-
ously identified cold-related QTL (Xiao et al., 2014). faroetal.,2011;Giulianietal.,2013).Indeed,fieldevalua-
CBF/DREBsareknownregulatorsofcoldandotherabiotic tion of O. glaberrima showed that some accessions could
stress responses (Mao and Chen, 2012; Mickelbart et al., beusedasdonorsincrossingwithO.sativafordroughttol-
2015). Interestingly, CBF3/DREB1G is up-regulated as erancebreeding(Ndjiondjopetal.,2010).
earlyasthreehoursaftercoldtreatmentinbothDongxiang TheO.rufipogongenotypeDongxiangwasalsoused
wildrice,butonlyafter12hoursinthesensitiveone.Genes tobreeddroughttoleranceinO.sativa.Anintrogressedline
known to be downstream of CBF/DREB1 in the cold re- was shown to be more tolerant when compared to the O.
sponseareup-regulatedaccordinglyinbothtolerantgeno- sativa recurrent parent, with higher survival rate, along
types(Xiaoetal.,2014).OtherQTLsuniquetoDongxiang withhigherprolineandsolublesugaraccumulation(Zhang
wildriceweredescribed(Maoetal.,2015). et al., 2014). However, it is clear that the trait is geno-
Recently,aSNPassociatedwithtemperatejaponica type-specific, since different O. rufipogon accessions can
cold tolerance was described. COLD1 (chilling-tolerance havewidelydifferentsensitivitylevels.Fengetal.(2012)
divergence)isaplasmamembrane-andendoplasmicretic- testedtoleranceofeightaccessionsofO.rufipogonandone
ulum-localizedregulatorofGproteinthatactivatesCa2+in- ofO.officinalis,andobservedthataccessionsfromtropical
fluxduringcoldsensing.OneSNPthatresultsinanamino origin are more tolerant. Interestingly, the single O.
acidchangewasfoundtoberesponsibleforthedifference officinalis(CCgenome;Table2)accessionperformedeven
incoldtolerance.TheSNPfoundinjaponicaissharedwith betterunderdroughtconditions(Fengetal.,2012).
accessions of O. rufipogon, but not with O. nivara or O. Anotherstudyanalyzedleafrollingscoreandrelative
barthii (AA genome; Ma et al., 2015). Thus, the COLD1 water content in several O. sativa, O. rufipogon and O.