Root biology and genetic improvement for drought avoidance in rice

13 Pages·2011·0.37 MB·English

FieldCropsResearch122(2011)1–13
ContentslistsavailableatScienceDirect
Field Crops Research
journal homepage: www.elsevier.com/locate/fcr
Review
Root biology and genetic improvement for drought avoidance in rice
VeereshR.P.Gowdaa,b,AmeliaHenrya,∗,AkiraYamauchic,H.E.Shashidharb,RachidSerraja,1
aInternationalRiceResearchInstitute,DAPOBox7777,MetroManila,Philippines
bDepartmentofBiotechnology,CollegeofAgriculture,UniversityofAgriculturalSciences,GKVK,Bangalore560065,India
cGraduateSchoolofBioagriculturalSciences,NagoyaUniversity,Chikusa,Nagoya,Japan
a r t i c l e i n f o a b s t r a c t
Articlehistory: Ricerootgrowthencompassesaremarkablegeneticdiversityintermsofgrowthpatterns,architecture,
Received24November2010 andenvironmentaladaptations.Inordertoharnessthisvaluablediversityforimprovingriceresponse
Receivedinrevisedform1March2011 todrought,anunderstandingofkeyroottraitsandeffectivedroughtresponsemechanismsisnecessary.
Accepted1March2011
Atrait-basedapproachwithpreciseunderstandingofthetargetenvironment,includingtemporaland
spatialheterogeneity,isapossiblepathtowardtheuseofrootsanddehydrationavoidancetraitsfor
Keywords: improveddroughtresistanceinrice.Theabilitytogrowdeeprootsiscurrentlythemostacceptedtarget
Drought
traitforimprovingdroughtresistance,butgeneticvariationhasbeenreportedforanumberoftraits
Rice
thatmayaffectdroughtresponse.Here,wereviewvariationinricerootresponsetodroughtfroma
Roots
Breeding physiologicalperspectiveintermsofmorphologyandfunctionwithrespecttothedifferentgrowth
QTL environments(uplandandlowland)commonlyusedbyfarmers.Recentadvancesinlinkingphysiology
Marker-assistedselection andbreedingarealsopresented.
©2011ElsevierB.V.Allrightsreserved.
Contents
1. Introduction............................................................................................................................................ 2
2. Rootstructureandphysiology......................................................................................................................... 2
2.1. Morphologicaltraits............................................................................................................................ 2
2.2. Ricerootanatomyandmechanismsforwateruptake........................................................................................ 3
3. Geneticvariationofriceroottraitsinresponsetodrought........................................................................................... 4
3.1. Geneticvariationformorphologicaltraits..................................................................................................... 4
3.2. Geneticvariationforrootanatomy............................................................................................................ 5
3.3. Heritability..................................................................................................................................... 5
4. Rootsforimprovementofdroughtresistanceinrice................................................................................................. 5
4.1. Uplandrice..................................................................................................................................... 6
4.2. Rainfedlowlandrice............................................................................................................................ 6
4.3. PhenotypingandQTLs.......................................................................................................................... 7
4.4. Geneticimprovementfordroughtavoidance................................................................................................. 8
4.5. Genomicsandproteomics...................................................................................................................... 9
5. Conclusions............................................................................................................................................ 9
5.1. Rootfunctionforwateruptakeunderdrought................................................................................................ 9
5.2. EffectivenessoftheQTLmappingstrategyforroottraits.................................................................................... 10
5.3. Thewayforward.............................................................................................................................. 10
Acknowledgments.................................................................................................................................... 10
References............................................................................................................................................ 10
∗
Correspondingauthorat:CropandEnvironmentalSciencesDivision,IRRI,DAPO
Box7777,MetroManila,Philippines.Tel.:[phone];fax:[phone].
E-mailaddress:[email protected](A.Henry).
1 Presentaddress:ICARDA,Aleppo,Syria.
0378-4290/$–seefrontmatter©2011ElsevierB.V.Allrightsreserved.
doi:10.1016/j.fcr.2011.03.001
2 V.R.P.Gowdaetal./FieldCropsResearch122(2011)1–13
1. Introduction whenitslengthreaches12cm(Hoshikawa,1989).Inthecaseof
rice,thereisonlyoneseminalorembryonicrootanditisusually
Drought is a major abiotic stress, affecting 20% of the total thelongestrootbeforethethird-leafperiod(Zhangetal.,2001).In
rice-growingareainAsia(PandeyandBhandari,2008).Rootsare general,seminalrootshaveapoorconductingcapacity(Haradaand
the principal plant organ for nutrient and water uptake. There- Yamazaki,1993)andtheirroleintheuptakeofwaterandnutrient
fore, improving our understanding of the interactions between islimitedtothevegetativestage(aroundtheseven-leafstage).
rootfunctionanddroughtinricecouldhaveasignificantimpact Mesocotylrootsarethosethatgrowfromthemesocotyl(the
on global food security. This review aims to synthesize previ- axisbetweenthenodeofthecoleoptileandthebaseoftheradi-
ous research on rice root biology for drought and to suggest cal)andtheydeveloponlyunderdeepseedingorwhentheseedis
newdirectionsofresearchinordertoimprovericeproductionin treatedwithcertainchemicals(YoshidaandHasegawa,1982).Usu-
drought-proneregions. ally,theyarenotcoarseandseldomhavelateralorbranchroots.
Plants use different mechanisms to cope with drought stress, Nodal roots are postembryonic roots, which arise from nodes at
namely,droughtescape,droughttolerance,droughtrecovery,and the base of the main stem and tillers. Functionally, nodal roots
droughtavoidance(Levitt,1972;O’TooleandChang,1979).Among elongate deeply into soil, thus constituting a framework for the
thesefourmechanisms,themodeofdroughtresistancewithwhich wholerootsystem.Whenrootlengthexceedsacertainsize,the
rootsaremostlikelyassociatedisdroughtavoidance.Genotypes branchingprocessstartsbyinitiation,emergence,andgrowthof
thathavedeep,coarserootswithahighabilityofbranchingand lateral roots from the root pericycle and epidermis (Morita and
penetration,higherroottoshootratio,elasticityinleafrolling,early Yamazaki,1993).Lateralroots,whichcompriseagreaterpropor-
stomatalclosure,andhighcuticularresistancearereportedascom- tionoftherootsystemintotallengthandnumber(Yamauchietal.,
ponenttraitsofdroughtavoidance(Blumetal.,1989;Samsonetal., 1987a,b;HaradaandYamazaki,1993),areresponsibleforthegreat-
2002;WangandYamauchi,2006). estamountofwaterandnutrientabsorption(Yoshidaetal.,1982).
Achievingdroughtresistanceinricewillbenecessaryformeet- Itisstillunknownhowrootmassormaximumrootlengthrelates
ing the growing water shortage of the world, and it requires tovariationinlateralbranchingorroothairs.Threediscretetypes
a deeper understanding of the mechanisms that could facilitate oflateralrootshavebeenrecognizedinrice:theLtype,whichis
drought resistance (Serraj et al., 2011). Understanding the phys- generally long and coarse (0.2–0.3mm), and capable of branch-
iologyofdroughtresponsecancontributetoplantbreedingefforts ingintohigherorderlaterals;Mtypes,thosethatwerelongand
towarddroughtresistance(FukaiandCooper,1995;Serrajetal., coarsebutwithoutabranch;andStypes,thosethatwereshort,
2009).Roottraitshavebeenclaimedtobecriticalforincreasing fine (0.035–0.1mm), and non-branching but usually numerous.
yieldundersoil-relatedstresses(Lynch,2007;Serrajetal.,2004). Thedifferenttypesoflateralrootsvaryinanatomy,developmen-
Previously,O’TooleandBland(1987)reviewedricerootgrowthat talcharacteristics,carbonandnitrogendynamics,developmental
atimewhengeneticvariationforroottraitswasjustbeginningto responses to various soil environments (Yamauchi et al., 1996),
beexplored.Giventherecentadvancesinphysiologicaltechniques, andgeneticregulationoftheirdevelopment(Wangetal.,2006a).
genetics,andmolecularbiology,thisreviewaimstosynthesizethe Rebouillatetal.(2009)haveprovidedathoroughreviewofriceroot
currentknowledgeofricerootsystemssothatitcanbeusedto development.
elucidatetheroleofrootsforimprovementsindroughtresistance. Hormone action on the development of root architecture has
been summarized by Osmont et al. (2007). Auxin and abscisic
2. Rootstructureandphysiology acidpromotelateralrootformation,cytokininsuppresseslateral
rootformation,ethylenehasinteractionswithauxinandmayplay
2.1. Morphologicaltraits a role in lateral root formation through cortical cell breakdown,
and gibberellic acid acts with ethylene to promote adventitious
Growthofthericeroot,intermsoftotaldrymatter,maximum root growth in flooded rice. Studies of hormone effects on rice
rootdepth,androotlengthdensity,increasesuntilfloweringstage root growth report that ethylene mediates aerenchyma forma-
and then decreases sharply to maturity (Yoshida and Hasegawa, tionandadventitiousrootgrowthunderfloodedconditionsinrice
1982).KawataandSoejima(1974)indicatedthatrootsproduced (Rzewuski and Sauter, 2008), but is not involved in the forma-
afterfloweringmayplayanimportantroleduringthegrain-filling tion of barriers to radial oxygen loss (Colmer et al., 2006). Use
period.Theshapeoftherootsystemdiffersgreatlywithsoiltexture ofanantisensetransgenicindicatedapositiveroleofcytokinins
(particlesize),soilwaterstatus,andsoilcompaction(Hoshikawa, forricerootdevelopment(Liuetal.,2003).ABAwasobservedto
1989). Rice is characterized by a shallow root system compared playaroleinlateralrootformation,tipswelling,roothairforma-
withothercerealcrops(Angusetal.,1983),havinglimitedwater tion, and water permeability in roots of variety Taichung native
extraction below 60cm (Fukai and Inthapan, 1988). The form of 1 (Chen et al., 2006). Experiments with a mutant for the OsIAA3
thericerootsystemalsovarieswithcultivationmethods(Yoshida geneindicateanimportantroleofauxinforgravitropismandthe
andHasegawa,1982;Tuongetal.,2002).Inuplandconditionswith growthofseminal,nodal,andlateralroots(Nakamuraetal.,2006).
directsowing,therootsystemgenerallydevelopsdeeperthanin Root growth under drought is likely influenced by the interac-
transplantedplantingsinlowlandconditions. tionofplanthormones,asreportedwithethylene,gibberellin,and
The rice root system, a fibrous root system, can be divided abscisicacidforadventitiousrootsindeepwaterrice(Steffensetal.,
into different classes: seminal roots, mesocotyl roots, and nodal 2006).
roots.Lateralrootsemergefromeachoftheseclasses.Thesethree Many studies have restricted their analyses to a set of root
classesdifferinorigin,anatomy,andfunction.Whentheseedger- parametersthatincludesrootdevelopmentwithrespecttotiller
minates,thecoleorhizaemergesfirstandthen,withinashorttime, development,maximumrootdepth,totalrootlength,rootsurface
the first seminal root (radical) breaks through the covering. The area,rootvolume,rootdiameter,rootlengthdensity,rootdistribu-
emergence of the root is the first sign of seed germination. The tionpatterninthesoilcolumn,roottoshootratio,rootbranching,
seedcontainsarelativelylargereserveofstoragecarbohydrateand root hydraulic conductance, root anatomy, root elongation rate,
nutrients(Marschner,1998),whichallowstheembryonicrootto total plant length, and hardpan penetrability, which are of var-
growrapidly.Itgrows3–5cmlongin2–3daysaftergermination. ious functional significance (Table 1; Wang et al., 2006a). It has
Usually,therateofelongationoftheseminalrootwillslowdown beenhypothesizedthatcoarserootshaveadirectroleindrought
V.R.P.Gowdaetal./FieldCropsResearch122(2011)1–13 3
Table1
RoottraitsandtheirfunctionalcharacteristicsthataremostcommonlycharacterizedinrootQTLmappingstudies.
Roottraits Functionalcharacteristics
Maximumrootdepth Potentialforabsorptionofsoilmoistureandnutrientsindeepersoillayer
Roottoshootratio Assimilateallocation
Rootvolume Theabilitytopermeatealargevolumeofsoil
Rootnumber Physicalstrength,potentialforrootsystemarchitecture
Rootdiameter Potentialforpenetrationability,branching,hydraulicconductivity
Deeproottoshootratio Verticalrootgrowth,potentialforabsorptionofsoilmoistureandnutrientindeepersoillayers
Rootlength/weightdensity Rateofwaterandnutrientuptake
Rootbranching Powerofsoilexploration(themajorcontributiontototalrootlength)
Totalrootlength/surfacearea Totalrootsystemsize:thesizeofcontactwithsoil(majordeterminantforwaterandnutrientuptakeasanentirerootsystem)
Specificrootlength Degreeofbranching,densityofrootmaterials,porosityduetoaerenchymadevelopment
Hardpanpenetrationability Abilitytopenetratesubsurfacehardpans
resistance because larger diameter roots are related to penetra- ally toward the aerial parts of the plant. Steudle and Peterson
tion ability (Materechera et al., 1992; Nguyen et al., 1997; Clark (1998) have summarized the “Composite Transport Model” for
etal.,2008)andbranching(Fitter,1991;Ingrametal.,1994),and water uptake and transport in roots, in which apoplastic, sym-
theyhavegreaterxylemvesselradiiandloweraxialresistanceto plastic,andtranscellularpathwayscontributetowateruptakeand
waterflux(Yambaoetal.,1992).Themaximumdepththatroots transport. A combination of pathways can be used, for example,
reachisgeneticallydeterminedanddifferssubstantiallybetween when water moves within the symplast for some distance and
cultivarsgrownunderidenticalconditions,butatthesametime may then cross the plasma membrane to move within the cell
isaffectedbyenvironmentalconditionsinthefield(Yoshidaand wall(Steudle,2000).Exchangebetweenpathwayspossiblyhelps
Hasegawa, 1982). Maximum root depth of a particular genotype rootstoadjusttheirwateruptakeabilityaccordingtotranspiration
isachievedonlywhenrootsdonotencounteraphysicallimitto demandofleaves.
growth.Thequantityofrootlength(orweight)inlayerswithinthe Rice root anatomy characteristically exhibits cortical
soilprofileisusuallyexpressedintermsofrootlength(orweight) aerenchyma, which are associated with gas transport to roots
perunitvolumeofsoil,referredtoasrootlength(orweight)den- growing in anaerobic conditions. The effects of soil moisture on
sity.Sincewaterismostlyabsorbedpassively,rootlengthdensity, aerenchymaformationhavebeendocumented,andthesereports
which reflects the development of lateral roots, can be directly point to aerenchyma formation as prevalent in rice roots from
related to water uptake ability of the plant. As root length den- all types of root growth media. Colmer (2003) studied 12 rice
sity increases, water uptake usually increases, but up to a given varieties, including upland, paddy, and deepwater types, and all
lengthonly,whichistermedcriticalrootlengthdensity.Inrice,like produced aerenchyma in both drained and flooded soil condi-
othercrops,thecriticalrootlengthdensitydependsonsoilcondi- tions,aswellasinaeratedandstagnantsolutionculture.Greater
tions, especially moisture (Siopongco et al., 2005), and roots are aerenchyma formation was observed in the flooded/stagnant
distributedinsuchawaythattheirlengthandmasswilldecrease treatments, but no difference in aerenchyma formation among
exponentially with depth. Root density at depth determines the cultural types was reported. Aerenchyma formation has been
exploitationofwaterpresentatdeeperlevels. observed under drought conditions in both aerobic and lowland
Roottoshootratioisameasureoftheallocationofresources genotypes,althoughtoalesserextentthanunderfloodedcondi-
betweendifferentplantcomponents.Theallocationofresources tions (Suralta and Yamauchi, 2008). Internal gas space may not
toward the root is high at early vegetative stages but decreases reflect aerenchyma formation; rice roots have a root porosity
markedly at flowering and is almost negligible after anthesis of approximately 9% at 20–25mm behind the root tips even
(Gregoryetal.,1996).Aschetal.(2004)reportedthatthepropor- with the absence of aerenchyma (Armstrong, 1971). Parren˜o-de
tionoftotaldrymatterallocatedtorootorshootpartsdependedon Guzman and Zamora (2008) observed that a greater number
therateofsoildry-down,withroot–shootratiosaveraging0.05–0.1 of aerenchyma lacunae were formed under intermittent and
atfloweringinsoil-filledPVCpipes.Geneticvariationinroot–shoot upland water regimes than in flooded conditions. The authors
ratioamongOryzaspecieswasalsoreported,andwasseenamong reported genotypic differences when the roots were observed
subspeciesgroups(Kondoetal.,2003).Japonicaaccessionsrequire at tillering, but not at panicle initiation, which suggests genetic
moreresourceallocationtowardrootsfortheformationofdeep differences in the onset of aerenchyma formation. Although
rootlengththanindicaandausaccessions.Roottoshootratioalso droughthasbeenobservedtoaffectaerenchymaformation,itis
varieswithcultivationsystem.Inuplandconditions,roottoshoot unknownwhetheraerenchymaformationaffectswateruptakein
ratioincreases(BanbaandOokubo,1981;Kondoetal.,2000a;Price rice.
etal.,2002;Singhetal.,2000),comparedwithroottoshootratioin Intheiradaptationtogrowthinfloodedconditions,riceroots
lowlandconditions(Azhiri-Sigarietal.,2000;Ban˜ocetal.,2000a). displayauniqueformationofapoplasticbarrierscomparedwith
This response may be due to mechanical impedance in lowland othercropplants.TheroleofsuberinandtheCasparianbandinlim-
conditions,whichtypicallyfeatureahardpanfromsoilpuddling. itingwateruptakehasreceivedmixedreports.Indrought-stressed
Valuesofdeeproottoshootratiohavealsobeenusedtocharacter- lowlandrice,theimplicationsofapoplasticrootbarrierformation
izetheverticalrootgrowthofrice. are complex since the soil at the start of the season is flooded,
then fluctuates or steadily decreases based on rainfall patterns.
2.2. Ricerootanatomyandmechanismsforwateruptake Hose et al. (2001) concluded that the extent and rate of Caspar-
ianbandandsuberinlamellaformationdependonenvironmental
Before water reaches transpiring leaves, it must penetrate conditions(drought,hypoxia,salt,heavymetal,andnutrientavail-
throughaseriesofconcentriccelllayers.Inrice,theselayersinclude ability).Typically,agreaterdegreeofCasparianbandandsuberin
therootepidermis,hypodermis(exodermis),schlerenchymalayer, lamella development resulted in less water permeability of the
several layers of cortex cells, endodermis, pericycle, and xylem root. Formation of an exodermis in rice was induced by growth
vessels.Oncewaterhasreachedthexylemvessels,itmovesaxi- instagnantsolution,andresultedinaneffectivebarriertoradial
4 V.R.P.Gowdaetal./FieldCropsResearch122(2011)1–13
oxygenlossinrice(Colmeretal.,1998).Componentsofrootbarri- proteins(TIPs),Nod26-likeintrinsicproteins(NIPs),andsmalland
ersincludealignifiedschlerenchymalayer,asuberizedexodermis basicintrinsicproteins(SIPs);Sakuraietal.,2005).Inrice,expres-
(hypodermis),andarhizodermis(acelllayeroutsideoftheexo- sionofeachaquaporingeneinrootsvarieswithroottissue,but
dermis). isgenerallymoreabundantattheroottipthaninotherpartsof
The effects of apoplastic barriers on water uptake and trans- the root (Sakurai et al., 2008). This is due to the prevalence of
portinriceareunclearsincegenotypesofricecanbeadaptedto aerenchymaalongthelengthofriceroots,asthereducedexpres-
floodedornon-floodedconditions.Kondoetal.(2000a)reported sionawayfromthetipdiffersfromthatofothercrops(e.g.,maize;
thatmaizereducedsoilwaterpotentialtolowerlevelsthanrice Hachezetal.,2006).
underdroughtconditions,andthat,inadditiontohavingasmaller MostresearchinriceonaquaporinsanddroughtfocusesonPIPs.
rootlengththanmaize,ricehadalowerabilitytotakeupwater Studiescomparingdrought-stresseduplandandlowlandricegen-
perunitrootlength.Wateruptakeinricedeclinedmarkedlyunder erallyreportagreaterresponseinaquaporingeneexpressionfrom
severedroughtstresscomparedwithmildstress,whereaswater upland rice. To date, all aquaporin studies in rice that included
uptakeinmaizewassimilaratthetwostresslevels,possiblydue a drought treatment did so using polyethylene glycol (PEG) in
tothedeeperrootgrowththatwasobservedinmaize.Consistent solution culture. Lian et al. (2004) observed an up-regulation of
withtheseresults,Miyamotoetal.(2001)reportedamuchlower the PIP RCW3 in upland rice under drought, but not in lowland
hydraulicconductivityofricerootscomparedwiththoseofother rice. When the RCW3 was inserted into the same lowland rice
species, but with no visible differences in endodermis, exoder- background,however,greaterosmoticroothydraulicconductance,
mis,oraerenchymaformationbetweenlowland(IR64)andupland leafwaterpotential,andtranspirationwereobserved.Lianetal.
(Azucena)varietiesgrowninsolutionculture.However,theroot (2006)examinedtheexpressionofallricePIPs,andreporteddif-
hydraulicconductivityofIR64wassignificantlylowerthanthatof ferentialexpressionbetweenuplandandlowlandrice,rootsand
Azucenainaeroponicallygrownroots,whichisanexpectedtrend shoots,well-wateredanddroughtconditions,andnotablybetween
giventheenvironmenttowhichthesevarietiesareadapted.This droughtandABAtreatments.Interestingly,somePIPsweredown-
pointstotheimportanceofrootgrowthenvironmentforstudying regulatedunderdrought.Inawhole-genomecomparisonofgene
hydraulicconductivity. expressionunderdroughtandwell-wateredconditions,allgenes
Roothydraulicconductivityhasbeenfurthercharacterizedin showingincreasedexpressioninuplandricealsoexistedinlowland
IR64(lowland)andAzucena(upland)rice,withemphasisonsepa- rice(Wangetal.,2007).Sinceuplandriceistypicallyunderstoodto
ratingtheindividualrootcomponentsaffectingwatermovement. bemoredrought-resistantthanlowlandrice,thisledtheauthorsto
Inbothstudiesdescribedbelow,nodifferencesbetweenvarieties suggestthatover-expressionofsomeofthesegenesmayimprove
werereported.Ranathungeetal.(2003)observedhydrauliccon- thedroughtresistanceoflowlandvarieties.
ductivityoftheouterpartofthericeroot(cortexandexodermis)
to be 30 times that of the endodermis and stele. Subsequently,
Ranathungeetal.(2004)usedinktoblocktheapoplastandHgCl to 3. Geneticvariationofriceroottraitsinresponseto
2
closeaquaporins,andconcludedthatwatermovementispredomi- drought
nantlythroughtheapoplastsincetheinkhadabiggereffectonroot
hydraulicconductivity.Theauthorsnotedalowresistanceofthe 3.1. Geneticvariationformorphologicaltraits
exodermis,butdidnotnoticeanypatchinessofCasparianbands,
whichmayhaveincreasedtheirpermeability.Thesestudieswere Significant genetic variation exists among different rice culti-
laterquestionedforusingaeratedsolutionasagrowthmedium, varsforrootmorphologicaltraits(O’TooleandBland,1987)suchas
whichlikelydidnotinducetheformationofatightbarrierinthe rootdiameter(Armenta-Sotoetal.,1983),rootdepth(Nicouetal.,
outerpartoftheroot(Garthwaiteetal.,2006). 1970;ReyniersandBinh,1978;Yadavetal.,1997;Mambaniand
Hydraulicconductanceofwholerootsystemsinricehasbeen Lal,1983a;Nemotoetal.,1998;Katoetal.,2006),rootpullingforce
recently reported in rice roots from both solution and soil cul- (O’Toole and Bland, 1987; Ekanayake et al., 1985a), deep root to
ture (Matsuo et al., 2008). In solution culture, root hydraulic shootratio(YoshidaandHasegawa,1982),rootnumber(Armenta-
conductance was greater in a lowland japonica variety (Koshi- Soto et al., 1983), root growth plasticity (O’Toole, 1982; Ingram
hikari; previously classified as drought-susceptible) than in an etal.,1994;Priceetal.,2002),androotpenetrationability(Babu
upland variety (Sensho; mildly drought-resistant). In soil, the etal.,2001;Clarketal.,2008,2000;Alietal.,2000).
roothydraulicconductanceofanuplandindicavariety(Beodien; Studies on genetic variation for root traits in rice have been
drought-tolerant)wasgreaterthanthatofKoshihikari.Theauthors ongoing for decades. In 1970, Nicou et al. reported significant
concludedthatroothydraulicconductivitymaybemoreaffectedby geneticvariationforroottraitsamongbothuplandandlowland
waterchannelsthanbyrootanatomy.Rootwateruptakeabilityand cultivarsofAsia,Africa,andSouthAmerica.Asianlowlandvarieties
hydraulicconductancehavebeenevaluatedaccordingtorootpres- had finer and more highly branched roots, whereas African and
sure,determinedbyrootsystemxylemsapfluxthroughcutstems South American cultivars had larger diameter and less branched
(or“bleedingrate”).XylemsapfluxoflowlandvarietyKoshihikari roots.Changetal.(1972)comparedroottraitsofseveralupland
decreasedwithdecreasingwateravailabilityinawater-savingtrial, andlowlandvarietiesandfoundthatdroughtresistancewasasso-
but did not change in two upland varieties (Beodin and Shen- ciatedwithcoarse,longroots,adenserootsystem,andahighroot
sho;MatsuoandMochizuki,2009b).Rootpressurehasalsobeen toshootratio.YoshidaandHasegawa(1982)alsoreportedgenetic
attributedtorecoveryfromxylemcavitationinresponsetodrought variationinrootdepth,withatendencyforuplandricecultivarsto
(Stilleretal.,2003).Beforebreederscanberecommendedtobreed havedeeperrootsthanlowlandricecultivars.Ingrametal.(1994)
cultivarswithhighwateruptakeability,itisnecessarytoconfirm used cultivars belonging to different types of rice for root stud-
the role of high root hydraulic conductivity in maximizing plant iesandfoundtropicaljaponicatypestohavelargerrootsystems
growthandyieldunderdrought. than indica types. In another study, Lafitte et al. (2001) investi-
Aquaporin expression has been reported to correlate directly gated the genotypic variation for root traits in different types of
with root hydraulic conductance (e.g., Javot et al., 2003 in Ara- riceandreportedthatindicaricetypeshadfine,highlybranched
bidopsis and Sakurai et al., 2005 in rice). Thirty-three aquaporin superficialrootswithnarrowxylemvesselsandlowroottoshoot
genes have been identified in rice from all four major subfami- ratio, whereas japonica types had coarse roots with wider ves-
lies(plasmamembraneintrinsicproteins(PIPs),tonoplastintrinsic sels,lessbranchedlongroots,andalargeroottoshootratio.Aus
V.R.P.Gowdaetal./FieldCropsResearch122(2011)1–13 5
types were reported to have intermediate root diameter, with a instancesthisvariationhasbeenlinkedwithabilitytoextractsoil
rootdistributionprofilesimilartothatofjaponicatypesbutwith water.Additivegeneeffectswereimportantintheexpressionof
finerroots.Othercomparisonsamongricevarieties(Thanhetal., rootxylemvesselareasothatsuchtraitscouldbestudiedefficiently
1999; Azhiri-Sigari et al., 2000; Kondo et al., 2003; Matsuo and inanearly-segregatinggeneration(Bashar,1987).Rootresistance
Mochizuki, 2009a; Uga et al., 2009; Henry et al., 2011) further towaterflowcanbeconsideredintermsoftwocomponents:radial
reflectthegeneticdiversityforroottraitsinrice.Yuetal.(1995) resistance and axial resistance (Landsberg and Fowkes, 1978). It
reportedgenotypicvariationforrootpenetrationabilityofricecul- iscurrentlythoughtthatradialwaterflowismorelimitingthan
tivarsbyusingthewaxlayermethod,inwhichdifferentparaffin axialwaterflow(SteudleandPeterson,1998),butseveralstudies
waxesweremixedtoachieveaknownmechanicalimpedanceand havepromotedtheideaofselectinglargerxylemvesselsforbreed-
includedintheroot-growthmedium.Usingthesamemethod,Babu ingdroughtresistance.Harajima(1936)reportedthattherewere
etal.(2001)foundthatjaponicaaccessionshaveahigherrootpen- fewerprimaryxylemelementsinseminalrootsofuplandjaponica
etration index (number of roots penetrating the wax layer/total varietiesthaninthoseoflowlandjaponicavarieties.Inexperiments
numberofnodalandseminalroots)thanindicatypesinlinesused withbothsolutioncultureandlowlandfieldconditions,Kondoetal.
todevelopdoubledhaploidmappingpopulations(CT9993/IR62266 (2000b) studied root anatomical traits, including stele diameter,
andIR58821/IR52561)formappingandtaggingroottraits. metaxylemnumber,andmetaxylemdiameterinbothuplandand
Many wild species in the genus Oryza may offer genetic lowlandricecultivars,andfoundthattraditionaluplandjaponica
resources for drought resistance research since they have more cultivarshadthelargeststeleandmetaxylemdiameter.
novelallelesthancultivatedrice(Zhangetal.,2006).Inanexperi- In another study by Yambao et al. (1992), root diameter was
mentunderscreenhouseconditions,wildspeciesofOryza(mostly demonstratedtobeaneffectiveselectionindexforxylemsizein
belongingtotheprimarygenepool)werecomparedforrootand roots with diameters up to about 1.2mm. The authors hypothe-
otherdrought-adaptivetraits(Liuetal.,2004).Thatstudyrevealed sized that coarse roots would confer drought resistance because
thatsomewildspecieshavesuperiorrootgrowthunderdrought theyhavegreaterxylemvesselradiiandloweraxialresistanceto
stress.Oryzalongistaminataaccessionsandsomejaponicacultivars water flux, but it was concluded that this would not effectively
showedeitheranincreaseintotalrootmassoranincreaseinthe contributetoimprovingdroughtresistance.
proportionofrootmassinthedeepersoillayersunderdrought,
whereas indica cultivars and Oryza rufipogon accessions did not
3.3. Heritability
showanydifference.
Evaluation of mutants for root traits can provide important
Informationonheritabilityandgeneactionofaplanttraitisa
insightsintorootgrowthanddevelopment.Inrice,somemutants
prerequisiteforasuccessfulbreedingprogram.Suchstudiesrely
withoutseminalrootsorwithoutlateralrootshavebeenidentified.
heavilyuponarelativelylargenumberofplantstoarriveatsta-
Sofar,tengeneshavebeenidentifiedinricerelatingtorootgrowth,
tistically significant results, thus making root traits difficult to
outofwhichmutantsofsixgenes,rm1andrm2(IchiiandIshikawa,
incorporate.Assuch,informationonheritabilityandgeneaction
1997),rrl1andrrl2(Inukaietal.,2001a),srt5(Yaoetal.,2002),and
ofriceroottraitsisstillverylimited.Earlierstudies(Changetal.,
srt6(Yaoetal.,2003),areinvolvedinareductioninseminalroot
1982; Armenta-Soto et al., 1983; Chang et al., 1986) using aero-
elongation.Mutantsoftwogenes,crl1andcrl2(Inukaietal.,2001b),
ponicsystemsfoundthatdominantgenescontrolrootnumber,root
areinvolvedinareductioninnumberofnodalroots,one(rm109;
depth,androotmass,whereasrootdiameteriscontrolledbyboth
HaoandIchii,1999)isinvolvedinblockinglateralrootinitiation,
dominantandrecessivegenes.Armenta-Sotoetal.(1983)reported
andone(rh2;Ichiietal.,2000)isinvolvedinreducingroothairs.
highernarrow-senseheritabilityestimatesforrootdiameter(62%),
Othermutantsincludecrl4(Kitomietal.,2008),lrt1(lateralroot-
rootlength(60%),androotnumber(44%).
lessphenotype;Chhunetal.,2003a),arm1andarm2(lateralroot
Ekanayakeetal.(1985a),usingF ,F ,andF populationsfrom
numberdecreases;Chhunetal.,2003b),andlrt2(lateralrootless 1 2 3
acrossbetweenIR20(shallow,finerootsystem)andMGL-2(deep,
phenotype;Wangetal.,2006b).Mostofthesegeneshavenotbeen
coarserootsystem),reportedthatrootdiameter,rootdryweight,
identifiedexceptforcrl1(Inukaietal.,2008).
androotlengtharepolygenictraitswithsubstantialproportions
Roothairsareextensionsofepidermiscellsofrootsthatarecon-
ofadditivevariationandwithnarrow-senseheritabilitiesgreater
sideredtobeanimportantstructurefornutrientuptakeasthey
than50%.Theysuggestedthatselectionfortheseroottraitsbased
coveralmost77%ofthesurfaceareaoftherootinanycrop(Jills
on individual plant performance could be successful in early-
etal.,2000).Experimentswiththeroothairlessmutantrh2indi-
segregatinggenerations.Inanotherstudy,Ekanayakeetal.(1985b)
catedthatroothairsdonothaveaprimaryroleinwateruptake
observed low inheritance in lowland rice for root pulling force,
at the seedling stage under drought and even their contribution
whichistheverticalforcerequiredtoremoveoneplantfromthe
tonutrientuptakediffersbyelementandculturemethod(Suzuki
soil. Low heritability for some root traits is a common breeding
etal.,2003).Moreresearchatdifferentstagesanddifferentdrought
concern,buttheissuecanberesolvedbydevelopingsuitableselec-
levelsisnecessarytoassessthepotentialroleforroothairsinwater
tionmethodsthattakefulladvantageofgeneticvariabilityandalso
uptakeunderdrought.Inaddition,lateralrootsgenerallyhavea
makepossiblerapidselection,byincreasingbothheritabilityand
largeeffectonoverallplantarchitecture(Yamauchietal.,1987a,b)
selectionresponse(RichardsandPassioura,1981).
andplaykeyrolesinwateruptake(Varneyetal.,1993),particularly
underdroughtconditions(Ban˜ocetal.,2000b;Wangetal.,2009).
Continuedresearchwithroottraitmutantscouldopenthewayto 4. Rootsforimprovementofdroughtresistanceinrice
morethoroughgeneticandmolecularanalysisandcouldsupport
molecularbreedersinbreedingcropswithimprovedrootarchitec- Therelationshipsbetweenrootgrowthandgrainyieldunder
tureoncethephenotypesofthesetraitsarebetterunderstood. drought are complex. Positive associations between root length
andgrainyieldhavebeendocumentedinrice(MambaniandLal,
3.2. Geneticvariationforrootanatomy 1983a; Lilley and Fukai, 1994). In contrast, Ingram et al. (1994)
foundnosignificantassociationbetweenthetwotraits.Itmaybe
In addition to root morphological features, considerable vari- thatasimplecorrelationbetweenrootgrowthandyieldcouldbe
ation is also documented for root anatomical traits among rice expectedonlyinwell-definedtargetenvironments(Mambaniand
varieties(Terashimaetal.,1987;Kondoetal.,2000b)andinsome Lal,1983a;Ekanayakeetal.,1985a).Venuprasadetal.(2002),in
6 V.R.P.Gowdaetal./FieldCropsResearch122(2011)1–13
a study involving simultaneous evaluation of root character and 4.2. Rainfedlowlandrice
grain yield, concluded that genotypes with a deep rooting habit
had an advantage in stress conditions and that those genotypes Droughtresistancemechanismsthatareappropriateforupland
thathadproduceddeeprootspriortotheonsetofstressshowed systemsmaynotbesuitableforrainfedlowlandconditionsandvice
improvedproductivitycomparedwithagenotypethatdidnothave versa(Mackilletal.,1996),mainlybecauseoftheuniquehydrol-
thecapacitytoproducerootspriortotheonsetofstress.Thestudy ogyofrainfedlowlandsinwhichsoiltransitionsfromfloodedand
alsosuggested,basedonQTLmapping,thatthelociforproductivity anaerobictodroughtandaerobic(Wadeetal.,1999).Inadditionto
traitswerenotcongruentwiththoserelatedtorootmorphology, thedifferencesinwaterstatusbetweenuplandandlowlandcon-
exceptatonelocus.Subsequently,Toorchietal.(2006)andKanbar ditions,theeffectofcultivationonsoilpropertiesisamajorfactor
et al. (2009), based on canonical correlation studies conducted determiningdifferencesinrootgrowthanddroughtadaptability
undercontrastingmoistureregimes,suggestedthatmaximumroot betweenuplandandlowlandrice.
depth,root–shootratio,androotdryweightconferredanadvan- Puddling,themechanicalbreakdownofsurfacesoilaggregates,
tagetograinyieldunderstress. isthemostcommonlandpreparationmethodforlowlandricein
Ricecultivationhastwomajorlandmanagementsystems,com- South and Southeast Asia. Hardpans that develop from puddling
monlyreferredtoasuplandandlowland.Thesetwosystemsdiffer improvesoilwaterretentioncapacity(SharmaandDeDatta,1985)
greatlyintheiryieldpotentialsbecauseofsoilcharacteristicsthat buthinderrootpenetrationtoreachmoistureindeeperzonesof
affectrootgrowthandplantresponsetodrought,andaretherefore soilafterdryingoccurs(Ghildyal,1978;Hasegawaetal.,1985;Yu
consideredinseparatesectionsinthisreview. et al., 1995; Clark et al., 2000, 2002; Babu et al., 2001; Samson
et al., 2002). In a survey conducted in 35 rice-growing locations
ofSouthandSoutheastAsiabySharmaetal.(1994),resistanceto
penetrationinthesurface10cmaveraged0.64MPaunderflooded
4.1. Uplandrice conditionsand1.7MPainpuddledfieldswithoutstandingwater.
Elsewhere, root penetration declined (>50%) at soil strengths of
Ricecultivarsadaptedexclusivelytouplandconditionsaretyp- 0.5–2MPa(O’Toole,1982)anddeclinedevenmoreat3MPaand
icallycharacterizedbyadeepandcoarserootsystem,tallstature, above(BengoughandMullins,1990).Acrossspecies,morpholog-
thickerstems,andfewertillers(Ge,1992;Lingetal.,2002),whereas ical and physiological changes in plant growth due to effects of
lowlandricecultivarshaveshallowandfinerroots,alargenumber hardpansonrootsincludeareductionintranspirationrateandleaf
ofroots,andmanytillers(Langetal.,2003).Inuplandfieldsdur- areaexpansion,andultimatelyadecreaseindrymatteraccumu-
ingstress,themajorsourcesofwaterforgrowthanddevelopment lation (Masle and Passioura, 1987; Ludlow et al., 1989; Assaeed
arerainthatisretainedbythesoilandgroundwater.Acoarseand etal.,1990;Masle,1992).Theseeffectsmaybeduetodirectconse-
deeprootsystem,forsoilpenetrationandaccesstowaterreserves quencesofreducedrootaccesstowaterandnutrients.Thepresence
deepinthesoil,isconsideredvaluableforimproveddroughtresis- ofahardpaninshallowsoillayersmayfurtherpromoteuneven
tanceunderuplandconditions(O’TooleandChang,1979;Lingetal., moisturedistributioninthesoilprofile,sothatarootsystemtends
2002).Ricerootsystemsandtheirrelationshiptodroughtresis- tobepartiallyexposedtodrysoil,causingstomatestoclosewhile
tancewerepreviouslyreviewedbyYoshidaandHasegawa(1982). therestoftherootsystemcanaccesswater(Siopongcoetal.,2008,
Theauthorsnoticedlargevariationamonguplandricecultivarsfor 2009).Inadditiontothepresenceofahardpanandgreaterstratifi-
rootlengthdensitybelow30cmandsuggestedthattheeffectof cationofsoilcharacteristicsduetopuddling,rainfedlowlandsoils
droughtstressdependsontheabilityofplantstodevelopadeep differfromuplandsoilsinthatseveresoilcrackingoccursuponsoil
rootsystem.Changetal.(1986)alsofoundthatricewithadeeproot drying.Soilcracking,whichcanpenetratehardpans,stronglyinflu-
systemavoideddroughtbetterthanricewithashallowrootsystem. encesrainfallinfiltrationandwaterevaporationprocesses(Tuong
Advantagesconferredbyadeeprootsystemdependonthree etal.,1996).Sanchez(1973)reportedthatsoilcrackingimpeded
majorfactors:durationofthedroughtperiod,availabilityofwater rootdevelopmentbasedonvisualobservations;otherwiseverylit-
atdepth,andrateofwateruptake.Ifwaterisnotlimitedinupper tleisknownoftheeffectsofsoilcrackingongrowthofriceroot
layers of the soil, the plant may not benefit from the formation systems.
ofdeeproots.Inuplandconditions,PuckridgeandO’Toole(1981) Resultsofseverallowlandexperiments(Hasegawaetal.,1985;
foundthatdeep-rootedcultivarKinandangPatongextractedmore Sharma et al., 1987; Mambani et al., 1989; Nabheerong, 1993;
wateratadepthof40–70cmthanshallow-rootedcultivars(IR20 Pantuwanetal.,1996;Samsonetal.,1995)indicatethat69–94%
and IR36). Similar results were also obtained by Mambani and ofrootsarelocatedinthetop10cmofthesoilandveryfewroots
Lal(1983b),LilleyandFukai(1994),andKatoetal.(2007).Such arefoundbelow30cm.Verticaldeeprootpenetrationwouldhelp
comparisonsofwateruptakearedifficulttoestimateinlowland rice to avoid drought stress; however, root penetration is often
conditionsduetothecomplexinteractionsofdeepdrainageand restricted by the presence of a hardpan. Genotypic variation in
lateralwatermovementinthesubsoil. theabilityofricetopenetratecompactedsoillayersandsimulated
A range of trends have been reported regarding root growth compactlayershasbeenshowntoexist(O’Toole,1982;Yuetal.,
response to drought stress in upland rice, including both root 1995;Rayetal.,1996;Alietal.,2000;Priceetal.,2000;Zhengetal.,
growth inhibition and root growth promotion in drought stress 2000;Babuetal.,2001;Clarketal.,2002;Samsonetal.,2002).Rice
treatments.Katoetal.(2006)havereviewedtheeffectsofvarious showslesssoilpenetrationabilitythanotherspecies.Iijimaetal.
water regimes on deep root growth and biomass partitioning to (1991)indicatedthatmaizerootswerebetterabletopenetratehard
rootsinuplandrice.Theauthorsconcludedthatwhilemanystud- soilthanriceroots.Ingeneral,rootsofdicotyledonousplantshave
iesreportanincreaseinroot:shootratioanddeeprootgrowthin ahigherpenetrationratethanmonocotroots(Materecheraetal.,
responsetodrought,conditionsastimingofthedroughtatseedling 1992), and upland rice cultivars have greater penetration ability
stage,veryseveredroughtstress,andpresenceofhardpanshave thanlowlandcultivars(Yuetal.,1995).Changesinsoilconditions
reducedresourcepartitioningtoroots.Conclusionsaboutdrought can greatly alter root distribution patterns. However, the mech-
effectsonrootgrowthmayalsodifferbecauserootmassandroot anismbywhichrootspenetratecompactedsoillayersisnotwell
length can show opposite trends, especially when root diameter understood.Itremainstobedemonstratedwhetherthepenetrated
decreasesbecauseofdrought,resultingingreaterlengthbutless rootmasshasanyroleintheuptakeofmoistureandincreasing
mass. grainyieldinlowlandconditions.
V.R.P.Gowdaetal./FieldCropsResearch122(2011)1–13 7
Somestudiesclaimthatrootplasticitymightbeanimportant androottoshootratio,whereastheenvironmentaleffectofnitro-
physiologicaltraitingenotypicadaptationfordroughtstressunder gen treatment was relatively high for total dry weight and deep
lowland conditions (Ingram et al., 1994; Yamauchi et al., 1996). rootlengthratio(lengthofrootsatdepth/totalrootlengthmea-
Rootplasticitycanbedefinedastheabilityofagenotypetoadjust sured).Theseresultsemphasizetheimportanceofcharacterizing
itsrootgrowthphenotypeaccordingtoenvironmentalconstraints experimentalconditionsforrootstudies.
(O’TooleandBland,1987).Thetimingofrootgrowthinresponseto Root traits are generally controlled by many genes through
theresupplyofwaterfollowingaperiodofdroughtstressisavital quantitativetraitloci(QTL).SincethefirststudybyChampouxetal.
featureofrootgrowthplasticity(e.g.,Ban˜ocetal.,2000a).Genetic (1995)tolocategenescontrollingriceroottraitswithmolecular
variation has been observed in rice for plasticity in several root markers,manyQTLsrelatedtoroottraitshavebeenidentifiedin
traits,includingtheabilityoflateralrootstodevelopinresponse riceusing12differentmappingpopulations(Table2),withQTLs,
to rewatering after soil drying (Ban˜oc et al., 2000b), and also in identifiedandanalyzedinriceformorethan30rootmorphological
responsetosoildryingafterflooding(Suraltaetal.,2010).Genetic parameters.ThemoststudiedroottraitsinallQTLmappingstudies
differenceshavealsobeenobservedintheabilityofseminalroots aremaximumrootdepth,rootdiameter,androottoshootratio.
tocontinueelongationandformaerenchymaunderfloodedcon- ThemostnotablecontrastamongricerootQTLstudiesisthe
ditionsafterdrought(SuraltaandYamauchi,2008;Suraltaetal., vastarrayofgrowthmediaandobservationmethodsused.Since
2008a,b, 2010). Another definition of root plasticity is the abil- the G×E effect on root growth is particularly important for rice
itytoadjustrootarchitecture,suchastheratiooffinetocoarse underdroughtconditions,withlowlandsoilsbeingacomplexlay-
rootsortheangleofrootgrowth.Underprogressivedrought(not eringofde-aggregatedsoiloverahardpanandrangingfromflooded
intermittentdrought;Katoetal.,2006),thistypeofplasticitymay paddiestodrycrackedsoilsoverthesameseason,understanding
be valuable for improved rice growth under drought by allocat- how growth and observation methods affect root QTL studies is
ingresourcestoincreasedrootgrowthonlywhenneeded.These keyforusingourknowledgeofQTLstoimprovedroughtresistance
abilities are quite important for rainfed lowland rice due to the inrice.MostoftheaboveQTLstudieshavemeasuredroottraits
uniquesoilenvironmentasmentionedearlier,andthusthedesir- incontainersundercontrolledconditions,althoughithasyettobe
ablerootstraitsarenotassimpleasthoseforuplandricesuchas provenwhethertheseresultsreflecttruegeneticdifferences(Steele
deeporcoarseroots.Differentgenotypeshaveexhibiteddifferent etal.,2007).Althoughtherearemanycomprehensivereviewsof
responsesinplasticitydependingontypeofdroughtstress(Kano methodsforrootstudythatdescribemethodscommonlyused(e.g.,
et al., 2011); this points to the importance of understanding the soil cores, monolith, minirhizotrons, pots, and solution culture;
targetenvironmentforexploitingvariousdroughtresistancedonor Gregory,2006;Smitetal.,2000;Böhm,1979),somemethodshave
germplasm. beenparticularlyusedforriceandareoutlinedhere.
Other than the minirhizotron method, in which transparent
tubesareinsertedintothesoilatanangleandaportablemicro-
4.3. PhenotypingandQTLs
cameraisinsertedtovisualizetheroots,rootsaretypicallyassessed
in the field using destructive methods, including soil cores and
Many studies across crops have indicated considerable geno-
type×environment (G×E) interactions for root traits, which is monoliths.Inlowlandricefieldswherefloodingcanimpedethe
collectionofknownsoilvolumes,rootpullingforce,theforcethat
expectedgiventhenumberofenvironmentalfactors(i.e.,soilphys-
is required to uproot rice plants, has been used as a means of
ical,chemical,andbiological)thataffectrootgrowth.Inrice,Kondo
etal.(2003)investigatedG×Einteractionsbyusingbothupland evaluating the relative size and depth of root systems (O’Toole
andSoemartono,1981).Inthismethod,plantsareliftedfromthe
andlowlandvarietiesatthreeuplandsitesinthePhilippines,where
soil using a device that clamps to the base of the plant and is
both site and nitrogen treatments contributed to environmental
attachedtoaforcemeter.Rootpullingforceisdependentonroot
variation. In that study, genotype accounted for the largest pro-
length density of the portion of the root system that remains in
portion of variation for specific root weight, nodal root number,
Table2
QTLsrelatedtorootcharacteristicsinrice.
Geneticbackground Parenttype NumberofQTLs Screeningmethodsandtreatments Reference
(rangeof
phenotypic
variation(R2))
CO39×Moroberekan(RILs) I×TJ 56(6.0–33.0%) PVCcylinders;wellwateredanddroughtstress Champouxetal.(1995)
29(6.0–19.0%) Wax-petrolatumlayersystem;wellwatered Rayetal.(1996)
IR64×Azucena(DH) I×TJ 39(4.0–22.3%) PVCcylinders;aerobic Yadavetal.(1997)
12(4.0–35.0%) Wax-petrolatumlayersystem;wellwatered Zhengetal.(2000)
3(12.9–30.7%) PVCcylinders;wellwateredanddroughtstress Venuprasadetal.(2002)
29(11.9–26.7%) PVCcylinders;droughtstress Hemamalinietal.(2000)
CT9993×IR62266(DH) TJ×I 36(8.0–37.0%) Wax-petrolatumlayersystemandfield;aerobic Zhangetal.(2001)
38(3.6–51.8%) PVCcylinders;droughtstress Kamoshitaetal.(2002b)
Bala×Azucena(F2) I×J 21(5.0–38.0%) Solutionculture PriceandTomos(1997)
Bala×Azucena(RILs) I×TJ 17(5.0–18.0%) Waxlayersystem;wellwatered Priceetal.(2000)
25(5.4–28.0) Glass-sidedchambers;droughtstress Priceetal.(2002)
28(5.4–13.5%) Soilboxmethod;well-wateredanddroughtstress MacMillanetal.(2006)
IR1552×Azucena(RILs) I×TJ 23(11.4–20.0%) Potculture,well-wateredanddroughtstress Zhengetal.(2003)
IR58821×IR52561(RILs) I×I 28(6.0–27.0%) Waxpetroleumlayersystem;wellwatered Alietal.(2000)
20(5.7–29.9%) PVCcylinders;droughtstress Kamoshitaetal.(2002a)
IAC165×Co39(RILs) TJ×I 29(6.3–24.4%) PVCcylinders;aerobic Courtoisetal.(2003)
Akihikari×IRAT109(BIL) TJ×TJ 5(8–24%) Solutionculture Horiietal.(2006)
IRAT109×Yuefu(DH) TJ×TJ 51(1.1–25.6%) PVCcylinders,lowlandfield;wellwateredanddrought Lietal.(2005)
Zhenshan97×IRAT109(RILs) I×TJ 53(2.6–29.8%) LowlandfieldandPVCcylinders;well-wateredanddroughtstress Yueetal.(2008)
Otomemochi×Yumenohatamochi J×J 20(7.0–31.2%) Lowlandfield;well-wateredanddroughtstress Ikedaetal.(2007)
IR64×KinandangPatong(RILs) I×TJ 10(8.7–23.9%) Uplandfield;wellwatered Ugaetal.(2008)
8 V.R.P.Gowdaetal./FieldCropsResearch122(2011)1–13
thesoil(Ekanayakeetal.,1986).Itwasreportedthatahighpulling inimprovedvarieties(Cattivellietal.,2008).Thisexplainstheneed
forceisassociatedwiththeplant’sabilitytodevelopdeeperand forinter-specificcrossestoexplorenovelalleles,andreflectsthe
largerdiameterrootswithgreatpenetrationability.However,her- backgrounddependencyofQTLs.
itabilityofrootpullingforcewasrelativelylow(Ekanayakeetal.,
1985b)sincemanyothersoilfactorsinadditiontorootdepthaffect 4.4. Geneticimprovementfordroughtavoidance
rootpullingforce.Incontrolledenvironments,containersincluding
largePVCcylinders,rhizotrons,andpotshavebeenusedforQTL Traditionalaccessionscanberesistanttodroughtbecauseofa
studies.ThePVCcylindersystem(typically>15cmdiameterand longhistoryofnaturalselectioninthetargetenvironments.Trans-
1mheight)isconsideredanimprovementoverpotculturesince fer of primary or secondary traits, such as those associated with
rootdepthislessrestricted,andsoilmoisturewithdepthandsoil root growth, to desirable backgrounds to enhance grain yield is
dryingaremorerepresentativeoffieldconditions(Upchurchand complicated by a lack of clear understanding of the genetics of
Taylor,1990).Somecontainerstudiesincludeawaxlayerforthe componenttraitsandtheirinteractions,andalackoftightlylinked
assessmentofrootpenetrationability.Thewaxlayersystemwas markers.Recently,Ugaetal.(2011)andObaraetal.(2010)reported
first applied for screening root penetration ability by Taylor and amajorQTLforrootingdepth(Dro1)androotlength(qRL6.1)using
Gardner(1960).Waxlayersconsistedof60%waxand40%petrola- basket and solution culture (hydroponic) methods, respectively.
tumwhitewitharesistanceof1.4MPaat27◦C.Later,thissystem DespitethelargenumberofminorandmajorQTLsidentified,only
was used to simulate the hardpan present in lowland fields (Yu twoattemptshavebeenmadeinricetointrogressarootQTLinto
et al., 1995; Ray et al., 1996; Ali et al., 2000; Babu et al., 2001; anotherbackground.BasedontheQTLinvestigationofYadavetal.
Clarketal.,2002,2008).However,Clarketal.(2002)foundthat (1997),Shenetal.(2001)conductedastudyforintrogressingaroot
cultivarswithgoodpenetrationunderthewaxlayerscreendidnot depthQTLfromadeep-rootedvariety,Azucena,intoIR64inthree
consistentlyshowsuperiorperformanceinthefield.Growthofroot cyclesofmarker-assistedbackcrosses.However,fewlineswitha
systemsinbasketshasbeenusedtopredictrootingdepthindirectly significantlyimprovedphenotype(deeperroots)resultedfromthat
accordingtogrowthangle(Oyanagietal.,1993).Usingthebasket effort.Inanotherstudy,Steeleetal.(2006)introgressedfourQTLs
method,Katoetal.(2006)demonstratedtherelationshipbetween relatedtorootlengthanddiameterandoneQTLrelatedtoaroma
highrootgrowthangleandrootdepthinrice,andUgaetal.(2009) intoanIndianuplandvariety,KalingaIII,ina6-yearmarker-aided
observedvariationinrootgrowthangleinriceaccessionsunder backcrossprogram.Onetargetsegment(RM242–RM201)onchro-
uplandfieldconditions.Containerstudieshaveincludedtheinjec- mosome9significantlyincreasedrootlengthunderbothirrigated
tionofherbicideatdepthtoscreenfordeeprootgrowth(Robertson anddroughtstresstreatments,confirmingthatthisrootlengthQTL
etal.,1985).AeroponicandsolutionculturewithPEGstudieshave fromAzucenafunctionsinanovelgeneticbackground.
also been conducted to assess root growth over time. Although Tightly linked markers for each root QTL are necessary for
this wide range of phenotyping environments/systems used for improving root traits through marker-assisted selection. Sharma
QTLstudiesmaycontributetoinconsistencyinthelociidentified, etal.(2002)identifiedtightlylinkedmarkersforroottraitsadopt-
relatively large differences in root production among genotypes ing bulked segregant analysis and found two markers (OPBH14
canbeconsistentlyobservedregardlessofroot-zonecontainersize andRM201)tobecosegregatingwithmaximumrootdepthinthe
(Shashidhar,personalcommunication). IR64/Azucenamappingpopulationandthesewerevalidatedacross
ThetypeofprogenyusedforricerootQTLstudieshasincluded differentgermplasm(Chaitraetal.,2006).Vinodetal.(2006)iden-
F (Price and Tomos, 1997; Price et al., 1997), backcross inbred tified candidate genes for root traits related to morphology and
2
lines(Katoetal.,2008),doubledhaploidlines(Yadavetal.,1997; physiology.ThesewerevalidatedintheCT9993/IR62266mapping
Zhengetal.,2000;Hemamalinietal.,2000;Venuprasadetal.,2002; population,whichwasevaluatedforroottraitsundercontrasting
Toorchietal.,2002;Babuetal.,2003;Kamoshitaetal.,2002a;Zhang moistureregimes.Prabuddhaetal.(2008)identifiednear-isogenic
etal.,2001),andmostlyrecombinantinbredlines(Champouxetal., linesforseveralroottraits,andcandidategenesthatwerefoundto
1995; Ray et al., 1996; Price et al., 2000, 2002; Ali et al., 2000; beassociatedwithaparticularroottraitwerealsovalidatedwith
Kamoshitaetal.,2002b;Courtoisetal.,2003;Zhengetal.,2003). thenear-isogeniclines.
The number of progeny has ranged from 56 (Hemamalini et al., Problems associated with these studies were: (1) QTLs
2000)to220(Kamoshitaetal.,2002a).ThenumberofQTLsiden- introgressed were not fine-mapped with appropriate selectable
tified for root traits has ranged from 1 to 19 and the amount of markers, so the desired gene might have been lost in the selec-
phenotypicvariabilityexplainedamongtheprogenyexaminedby tionprocess;and(2)theQTLsidentifiedhadasmalleffectonthe
anyoneQTLrangedfromabout4%toasmuchas66.6%(Ugaetal., phenotypeitself.Thus,thechallengeformolecularbreedersisto
2011).ItisalsoimportanttonotethatthenumberofQTLsidentified discoverheritablystablemajorQTLsthatfunctionindependentlyof
dependsonthethresholdvaluespecified.Inmostofthestudies,all geneticbackground,andtodevelopaneffectivebreedingmethod
QTLsshowingapositiveeffectonroottraitswerederivedfroma fortheapplicationofsuchQTLs.OnceamajorQTLisidentifiedand
drought-resistantparent. validated,positionalcloningistheapproachmostcommonlyused
MostoftheQTLmappingstudiesforriceroottraitsconferring toclosethegenotype-phenotypegap(SalviandTuberosa,2005).
droughttolerancehavebeenconductedusingprogeniesderivedby Inspiteofsuchgreateffort,noQTLcloninghasbeenachievedso
crossingvarietiesbelongingtoadifferentsubspeciesgroup(japon- far in rice for root traits. In QTL mapping, the main factor limit-
ica×indica;asreviewedinKamoshitaetal.,2008)ratherthanby ing the precision of QTL localization is the number of progenies
usingprogeniesderivedbycrossingvarietiesbelongingtothesame usedinthestudy,moresothanotherfactorssuchasusingmore
subspecies group, that is, indica×indica or japonica×japonica. molecularmarkersorusingbetterstatisticaltechniques(Kearsey
Often,theseparentallinesexhibitslightmorphologicaldifferences, andFarquhar,1998).Associationmappingisapromisingmethod
buttheirprogenyexhibitconsiderablegeneticvariabilityformany for complex trait dissection and it focuses on association within
roottraits(transgressivesegregation).ObtainingvaluableQTLsor populationsofunrelatedindividuals.Usingassociationmapping,it
genesforbreedingbasicallydependsontraitdiversitybetweenthe ispossibletolocateQTLswithbetterprecisionthanusingamap-
donorandtherecurrentparents.Allthesegregatingpopulationsof pingpopulation(Courtoisetal.,2009).Linkingourknowledgeof
theaboveQTLstudieshaveonemodern(improved)andonetra- QTLmappingwithprecisionphenotypingthatisrepresentativeof
ditionalvariety.Undersuchcircumstances,mostlypositivealleles the target drought environment is critical for future progress in
arederivedfromthemoderncultivarandtheyarealreadypresent droughtresistanceforrice.
V.R.P.Gowdaetal./FieldCropsResearch122(2011)1–13 9
Anothernecessaryapproachforprogressindroughtresistance have been reported across crops that are responsible for the
throughriceroottraitsisanintegrationoftheknowledgegenerated regulation of signal transduction and the expression of stress-
thusfar.Kamoshitaetal.(2008)havesummarizedthelargenumber related genes that impart stress resistance to plants. Transgenic
ofstudiesinricefordroughtresistanceinQTLmappingstudiesofat rice with the transcription factor AtDREB1A or its orthologue
least15differentpopulations.RicerootQTLsfordroughthavebeen OsDREB1A(Dehydration-ResponsiveElementBindinggene)tested
compiledusingQTLmeta-analysisinmultiplepopulations(Norton inpotsdemonstratedimprovedresistancetosimulateddrought,
etal.,2008;Courtoisetal.,2009).MultipleQTLstudiesfromasingle highsalt,andlow-temperaturestresses(Yamaguchi-Shinozakiand
population(Bala×Azucena:Khowajaetal.,2009)havealsobeen Shinozaki,2004).TransgeniclinescarryingtheOsNAC045transcrip-
conductedthatidentifiedseveraldenseclustersofrootQTLs.This tion factor, whose functions include a role in the development
integrativeapproachacrossalargenumberofstudiesconducted of lateral roots, were reported to have a greater survival rate in
inmultipleenvironments/phenotypingsystemsismorelikelyto rice after drought and salt treatments (Zheng et al., 2009) and
identifyimportantareasofthegenomeforricerootresponseto OsNAC10lineswitharoot-specificpromotedshowedgreateryield
droughtthananysingleQTLstudyalone. thanthewildtypeunderdroughtinthefield(Jeongetal.,2010).
Asabreedingstrategy,incorporatingdroughtresistancefora Improvedperformanceunderdroughtwasobservedintransgenic
particularstageofdevelopment(i.e.,vegetativeorfloweringstage) plantsofthegeneOsMT1a(metallothionein)thatispredominantly
wouldbecounter-productiveshouldstressoccuratanon-targeted expressed in roots and is induced by dehydration (Yang et al.,
stage. When the stage of occurrence, duration, and intensity of 2009).RootgrowthwasenhancedintransgenicsofBRX(BREVIS
stressisunpredictable,breedingfordroughtresistanceirrespec- RADIX-like homologous genes; Liu et al., 2010a) and OsVP1 (H+
tiveofgrowthstageislikelytobemosteffective.Roottraitsthat pyrophosphataseintonoplasts)andOsNHX1(Na+/H+exchangers;
resultinimprovedplantwaterstatusthroughastress-pronegrow- Liuetal.,2010b)thatwerereportedtoconferdroughttolerance.
ingseasoncouldconfernon-stage-specificdroughtresistance.For ExceptfortheOsNAC10studybyJeongetal.(2010),root-related
example,conventionalbreedingforroot-relateddroughtresistance droughtresistanceintermsofgrainyieldinricetransgenicsinfield
in rice was conducted using farmer-participatory plant breeding studieshavenotbeenreported.
approaches(Shashidhar,2008).Bycrossingatraditionaldrought- Proteomicsisalsoadvancingasatoolforidentifyingdrought-
tolerant accession (Budda) with IR64 and forwarding the filial tolerancecharacters,yetitspotentialisnotexploitedfullyinplant
generationssimultaneouslyunderseverestressandwell-watered research,especiallycomparedwithotherorganismssuchasyeast
conditions,severaladvancedlineswereobtained.Waterreceived andhumans(Jorrinetal.,2007).Anumberofproteomicstudies
by each segregating line was budgeted. Screening for root mor- on drought have been conducted on rice leaves (Salekdeh et al.,
phology using large container studies was adopted in advanced 2002a,b; Ali and Komatsu, 2006; Ke et al., 2009), but less work
generations.Theadvancedlines(ARBseries)werenominatedfor hasbeenconductedonroots.Aproteomicevaluationofriceunder
trials along with the accession from other breeders in India and saltstressbySalekdehetal.(2002b)revealedalargenumberof
materialfromIRRI.TrialswereconductedacrossIndiaunderthree differences in root proteins between salt-tolerant and sensitive
hydrologiesateachsiteandrepeatedoverthreeyears,andselected varieties,includingproteinswithantioxidantpropertiesandpro-
linesperformedwellacrossthreeyearsinseverestress(Verulkar teinsinvolvedinlignification.Rabelloetal.(2008)comparedgene
et al., 2010). The lines have been released for cultivation in the expressionandproteomeprofilesinrootsofdrought-tolerantand
drought-pronedistrictsofKarnatakainIndia. drought-sensitiveuplandricevarieties,andreportedthetolerant
varietytohaveincreasedexpressionofgenesorproteinsinvolved
4.5. Genomicsandproteomics inturgor,cellintegrity,andoxidativestress.Coupledwithphysio-
logicallyrelevantdroughtstresstreatments,thefunctionalinsights
Somegenesandsignalingpathwaysinvolvedintheanatomical fromproteomicsarepromisingforimprovingourunderstandingof
and morphological development of rice roots have been identi- ricerootphysiologyunderdrought.
fied(seereviewsbyCoudertetal.,2010;Rebouillatetal.,2009),
particularly for crown root initiation. Although advancements in
understandingthegeneticbasisofricerootattributeshavebeen 5. Conclusions
made,itisstillunclearexactlyhowtheseattributesaffectwater
uptakeunderdrought.Geneexpressionanalysishelpsinidentify- 5.1. Rootfunctionforwateruptakeunderdrought
ingthefunctionallyimportantgenesandpathwaysinvolvedinroot
architectureunderwater-deficitconditions(Breyneetal.,2003). Oryza sativa L. includes large genetic diversity for root archi-
Yangetal.(2004)conductedatissue-specificgeneexpressionstudy tecture, but the environmental response of root growth among
indrought-stressedriceroots,inwhich66transcriptswereidenti- genotypesisjustasdiverse.Thishighlightstheimportanceofchar-
fiedandclonedinrootsofAzucena.Fourtranscriptsweremapped acterizing the growing environment in all rice root studies. To
within an interval containing QTLs for root growth under water improve our understanding of the role of roots in rice response
deficitintheAzucena/IR1552population.Inanotherstudy,Wang todrought,itisnecessarytorethinkcarefullysomeofthecom-
et al. (2007) observed that the majority of genes expressed in monparadigmsaboutricerootbiology.Earlyreportsondrought
uplandriceandlowlandricearealmostidenticalandthat13%of and rice roots generalized the idea that rice has shallow root
alltheexpressedsequencetags(ESTs)detectedinleavesand7%of growth (maximum root depth of 30cm), and that improvement
thoseinrootswereexpresseddifferentiallyintranscriptsbetween fordroughtshouldemphasizedeep,coarserootgrowth.Wenow
thetwocultivartypes.Combiningourknowledgeofgenesinvolved knowthatmanyricegenotypeshavethepotentialfordeeproot
inrootdevelopmentwiththosethataredifferentiallyexpressed growth(comparedwithotherricegenotypes;notcomparedwith
underdroughtcouldhelpidentifyimportanttargettraitsormech- otherdeep-rootedspecies),butthisisstronglycontrolledbythe
anismsfordroughtresistance. environment (i.e., presence of hardpans, severity of the drought
Recent studies have indicated that, apart from conventional stress). Coarse nodal roots may be critical for penetrating hard-
andmarker-assistedselection,potentialexistsforthetransgenic pans,butnotalldroughtenvironmentscontaindistincthardpans.
approachtoenhancedroughtresistanceinplantsbyincorporat- Furthermore, fine roots present a large percentage of total root
ing genes that are involved in stress tolerance (Agarwal et al., length in almost all conditions and thus are strongly expected
2006; Hervé and Serraj, 2009). Numerous transcription factors to contribute greatly to water uptake by the entire root system,
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