Advances in Drought Resistance of Rice

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Advances in Drought Resistance of RiceMuhammad Farooq a , Abdul Wahid b , Dong-Jin Lee c , Osamu Ito d & Kadambot H. M.Siddique ea Department of Agronomy , University of Agriculture , Faisalabad, 38040, Pakistanb Department of Botany , University of Agriculture , Faisalabad, 38040, Pakistanc Department of Crop Science and Biotechnology , Dankook University , Chungnam, 330-714,Koread Japan International Research Center for Agricultural Sciences , Tsukuba, Japane Institute of Agriculture, Faculty of Natural and Agricultural Sciences, The University ofWestern Australia , Crawley, WA, 6009, AustraliaPublished online: 23 Jun 2009.

To cite this article: Muhammad Farooq , Abdul Wahid , Dong-Jin Lee , Osamu Ito & Kadambot H. M. Siddique (2009) Advancesin Drought Resistance of Rice, Critical Reviews in Plant Sciences, 28:4, 199-217, DOI: 10.1080/07352680902952173

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Critical Reviews in Plant Science, 28:199–217, 2009Copyright © Taylor & Francis Group, LLCISSN: 0735-2689 print / 1549-7836 onlineDOI: 10.1080/07352680902952173

Advances in Drought Resistance of Rice

Muhammad Farooq,1 Abdul Wahid,2 Dong-Jin Lee,3 Osamu Ito,4

and Kadambot H. M. Siddique5

1Department of Agronomy, University of Agriculture, Faisalabad-38040, Pakistan2Department of Botany, University of Agriculture, Faisalabad-38040, Pakistan3Department of Crop Science and Biotechnology, Dankook University, Chungnam-330-714, Korea4Japan International Research Center for Agricultural Sciences, Tsukuba, Japan5Institute of Agriculture, Faculty of Natural and Agricultural Sciences, The University of WesternAustralia, Crawley WA 6009, Australia

Referee: Dr Christine Davies, 42 Langham Street, Nedlands, WA, 6009, Australia

Table of Contents

I. INTRODUCTION ............................................................................................................................................. 200

II. MORPHOLOGICAL, ALLOMETRIC, AND YIELD RESPONSES ................................................................. 200

III. PHYSIOLOGICAL PHENOMENA OF DROUGHT STRESS ........................................................................... 202A. Photosynthetic Properties .............................................................................................................................. 202B. Water Relations ........................................................................................................................................... 203

IV. RESISTANCE MECHANISM AND MANAGEMENT ...................................................................................... 203A. Physiological and Agronomic Implications ..................................................................................................... 203

1. Phenology and Ontogeny ...................................................................................................................... 2042. Antioxidant Defense System ................................................................................................................. 2043. Plant Growth Regulators ....................................................................................................................... 2044. Polyamines .......................................................................................................................................... 2055. Osmotic Adjustment and Compatible Solutes ......................................................................................... 2056. Seed Priming ....................................................................................................................................... 205

B. Silicon Nutrition .......................................................................................................................................... 206

V. CROP IMPROVEMENT ................................................................................................................................... 206A. Breeding for Crop Improvement .................................................................................................................... 206

1. Drought-resistance Traits ...................................................................................................................... 2072. Selection ............................................................................................................................................. 207

B. Molecular and Biotechnological Approaches .................................................................................................. 209

VI. CONCLUSION ................................................................................................................................................. 211

REFERENCES .......................................................................................................................................................... 211

Address correspondence to Kadambot H. M. Siddique, Institute of Agriculture, Faculty of Natural and Agricultural Sciences, The Universityof Western Australia, Crawley, WA 6009, Australia. E-mail: [email protected]

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200 M. FAROOQ ET AL.

Water deficit is a serious environmental stress and the majorconstraint to rice productivity. Losses in rice yield due to watershortage probably exceed losses from all other causes combinedand the extent of the yield loss depends on both the severity andduration of the water stress. Drought affects rice at morphologi-cal, physiological, and molecular levels such as delayed flowering,reduced dry matter accumulation and partitioning, and decreasedphotosynthetic capacity as a result of stomatal closure, metaboliclimitations, and oxidative damage to chloroplasts. Small-staturedrice plants with reduced leaf area and short growth duration arebetter able to tolerate drought stress, although the mechanisms arenot yet fully understood. Increased water uptake by developinglarger and deeper root systems, and the accumulation of osmolytesand osmoprotectants are other important mechanisms for droughtresistance. Drought resistance in rice has been improved by usingplant growth regulators and osmoprotectants. In addition, severalenzymes have been found that act as antioxidants. Silicon has alsoimproved drought resistance in rice by silicification of the rootendodermis and improving water uptake. Seed priming improvesgermination and crop stand establishment under drought. Riceplants expressing HVA1, LEA proteins, MAP kinase, DREB andendo-1, 3-glucanase are better able to withstand drought stress.Polyamines and several enzymes act as antioxidants and reduceadverse effects of drought stress in rice. Drought resistance can bemanaged by developing and selecting drought-tolerant genotypes.Rice breeding and screening may be based on growth duration,root system, photosynthesis traits, stomatal frequency, specific leafweight, leaf water potential, and yield in target environments. Thisreview discusses recent developments in integrated approaches,such as genetics, breeding and resource management to increaserice yield and reduce water demand for rice production.

Keywords grain yield, water relations, drought management, breed-ing and selection, QTLs

I. INTRODUCTIONRice (Oryza sativa L.) is grown in at least 95 countries and

is a staple food for more than half of the world’s population(IRRI, 2002; Coats, 2003). Rice is grown in a wide range ofenvironments including areas where other crops might fail. Dueto population increases, the demand for rice is estimated to be2,000 million metric tons by 2030 (FAO, 2002). Meeting this35% increase in demand requires significant improvements inrice production; a daunting prospect as the climate changes andwater scarcity increases (Bouman et al., 2007). Over 50% ofthe area sown to rice worldwide is rainfed, producing only one-quarter of total rice production (McLean et al., 2002).

Drought is defined as water stress mainly due to lack ofrain. In rainfed ecosystems, drought is the major obstacle forrice production. For example, in the eastern Indian states of Jark-hand, Orissa, and Chhattisgarh, yield losses from severe drought(about 1 year in 5) averaged 40% and were valued at $650 mil-lion (Pandey et al., 2005). Currently, there is no economicallyviable means of increasing rice yield under drought. Develop-ing rice plants resistant to drought is considered a promisingapproach to help satisfy the increasing demand for food in bothdeveloping and underdeveloped countries. This approach re-

quires an understanding of physiological mechanisms and ge-netic controls of contributing traits at different developmentalstages (Manickavelu et al., 2006). There are a number of com-prehensive reviews on drought response in plants (Ingram andBartels, 1996; Holmberg and Bulow, 1998; Farooq et al., 2009a).Specifically, in upland rice, Bernier et al. (2008) and Kamoshitaet al. (2008) reviewed breeding strategies for drought toler-ance and resistance traits, respectively. However, there are nobroad reviews encompassing other aspects of drought resistancein rice. This review presents morphological, physiological andmolecular aspects of drought effects and resistance in rice, anddiscusses strategies and options to improve drought resistancein rice.

II. MORPHOLOGICAL, ALLOMETRIC, AND YIELDRESPONSES

Rice adapts to drought stress by the induction of vari-ous morphological, physiological, and biochemical responses.Many yield-determining physiological processes respond to wa-ter stress, and most are dynamic, fluctuating with time accordingto internal and external factors. The severity, duration, and tim-ing of drought stress as well as responses, which may take placeafter stress removal, and interaction between stress and otherfactors may be highly variable (Table 1; Plaut, 2003).

Leaf and root growth and development can be severely af-fected by water stress (Fig. 1). Since plants acquire water fromthe soil, root growth, density, proliferation, and size are keyfactors in drought stress resistance (Yoshida and Hasegawa,1982). O’Toole and Chang (1979) found that rice varieties withlonger, thicker roots were more drought-resistant than thosewith shorter, thinner roots; and fulfilled water requirements forgrowth during drought. In another study, rice cultivars withdeeper root systems were better adapted to relatively drier con-ditions (Boyer, 1996). Deep root development is largely affectedby soil conditions and significant genotype × environment inter-actions (Kondo et al., 2000, 2003; Cairns et al., 2004) (Fig. 2).Azhiri-Sigari et al. (2000) characterized deep root systems us-ing the following three root traits: 1) root-to-shoot ratio; 2) deeproot ratio (ratio of deep root mass below 30 cm depth to totalroot mass); and 3) specific root length (root length per unit rootweight); the first two being important for deep root developmentin rainfed lowland rice.

When rice was water stressed at 80% of transpirable watersoil moisture deficit for 20 days in the vegetative phase, leaf ex-pansion rate declined compared to well-watered plants (Farooqet al., 2009h). Other responses included reductions in height,leaf area and biomass production, tiller abortion, and changesin root dry matter and rooting depth. In a series of recent stud-ies, drought stress significantly decreased seedling fresh anddry weights (Farooq et al., 2008; 2009b–g). Due to the irriga-tion technique used, vertical soil moisture distribution variedlittle, but roots grew deeper under drought stress (Asch et al.,2005).

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DROUGHT RESISTANCE OF RICE 201

TABLE 1Economic Yield Reduction by Drought Stress in Rice

Growth stage Stress type Yield reduction Reference

Reproductive Mild stress 53.92% Lafitte et al. (2007)Reproductive Severe stress 94.48% Lafitte et al. (2007)Grain filling Mild stress 30–55% Basnayake et al. (2006)Grain filling Severe stress 60% Basnayake et al. (2006)Reproductive — 24–84% Venuprasad et al. (2007)— Severe stress 45–50% Jongdee et al. (2006)— Mild stress 15–20% Jongdee et al. (2006)— Severe stress 87–75% Kumar et al. (2008)— Very severe stress 95% Kumar et al. (2008)— Mild stress 35–56% Kumar et al. (2008)— Mild stress 15–54% Jian-Chang et al. (2008)— Mild stress 10–38% Atlin et al. (2006)— Severe stress 56–76% Atlin et al. (2006)Heading — 23% Lafitte et al. (2006)Grain filling Mild stress 19% Lanceras et al. (2004)Flowering Short severe stress 54% Lanceras et al. (2004)Flowering and grain filling Prolonged severe stress 84% Lanceras et al. (2004)Flowering and grain filling Prolonged mild stress 52% Lanceras et al. (2004)

FIG. 1. Effect of drought stress on vegetative growth of rice (cv. IR64). Bothplants were grown under well-watered conditions for 20 days following emer-gence. One pot (on right) was submitted to progressive soil drying (droughtstress) for 20 days. The decrease in soil moisture was controlled by partialrewatering of stressed pots to avoid a quicker imposition of stress and to ho-mogenize development of drought stress. Well-watered control pot (on left) wasmaintained at initial target weight by adding daily water loss back to the pot.

Rice plants respond to drought by decreasing numbers ofnew tillers and leaves, reducing leaf elongation, rolling existingleaves, and promoting leaf death (Cutler et al., 1980; Hsiao et al.,1984; Turner et al., 1986) all of which reduce interception ofphotosynthetically active radiation (PAR) (Inthapan and Fukai,1988). Stomata are particularly sensitive to drought. Leaf con-ductance decreased sharply with decreases in leaf water poten-tial (O’Toole et al., 1984), which reduced the rate of photosyn-thesis and radiation-use efficiency (Inthapan and Fukai, 1988).These responses reduced dry matter production and eventuallygrain yield.

Rice yield, in response to drought, depends on the timing ofthe drought event in relation to plant growth stage. For example,stress at 12 days prior to anthesis adversely affected spikelet fer-tility with severe reductions in grain yield (Cruz and O’Toole,1984; Ekanayake et al., 1989). Yield components are sensitiveto water stress at different stages of plant growth, such as an-ther dehiscence (Ekanayake et al., 1989) and panicle exsertion(O’Toole and Namuco, 1983). Limited data are available onthe relationship between yield reduction under water stress andplant water status of a broad range of adapted cultivars. Dataare confounded by differences in flowering date of materialstested (Ingram et al., 1990). Yield reduction due to water deficitdepends strongly on timing of the stress (Garrity and O’Toole,1994). Vegetative drought score, which is associated with ge-netic differences in leaf water potential and water extractionby roots, was not a reliable indicator of the ability to toler-ate stress at flowering (Puckridge and O’Toole, 1981). Yield

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FIG. 2. Root growth and proliferation under well-watered and drought stress conditions in various rice genotypes grown in root box. Rice genotypes Nip, sl 13,sl 34, sl 45 and sl 50 were grown under well-watered and drought stress (15% soil moisture contents) and harvested 38 days after seeding (courtesy Ms. ManaKano).

differences between plants which were transiently stressed inthe early vegetative phase and well-watered plants were notsignificant, even though flowering and maturity were delayed.Severe drought in the reproductive phase resulted in large yieldreductions, mainly due to increased numbers of unfilled grainsand grain weight (Wopereis et al., 1996). Productivity of ricein rainfed lowlands depends not only on the accumulation ofdry matter, but also on its effective partitioning to grain. Withlate-season drought, an enhanced capacity to allocate dry matterto grain under water-deficit conditions should be advantageous(Passioura, 1982). Field studies on dry matter partitioning un-der drought were conducted at eight locations in Chattisgarh,India, between 1995 and 1998, using five genetically diverserice cultivars. Dry matter accumulation at flowering and ma-turity was significantly reduced at drought-affected sites. Vari-ation between cultivars in dry matter partitioning to grain un-der both favorable and water-stressed conditions was observed.Drought stress at the reproductive stage significantly increaseddry matter partitioning from leaves and stems to grains in allcultivars (Kumar et al., 2006). Under drought stress, dry matterpartitioning into green leaves varied among cultivars. NSG-19 partitioned the least dry matter to green leaves at matu-rity which was associated with higher remobilization of assimi-lates to fill grains. Delayed flowering due to drought stress wasnegatively associated with grain yield, and seemed to be gov-erned by a lower plant water status. The contribution of drymatter partitioning from stems and leaves to grain filling in-creased with the severity of drought stress, particularly in culti-vars with an enhanced capacity for leaf senescence during grain

filling, which stabilized grain yields under drought (Kumar et al.,2006).

III. PHYSIOLOGICAL PHENOMENA OF DROUGHTSTRESS

The effect of drought is heightened in arid and semi-arid areas(Boyer, 1982) inducing many physiological, biochemical, andmolecular responses, with photosynthesis being one of the pri-mary physiological targets (Chaves, 1991; Lawlor, 1995; Becket al., 2007). In addition, drought stress hampers plant waterrelations and disrupts membrane function (Farooq et al., 2008,2009b–f). Some physiological phenomena affected by droughtin rice are described below.

A. Photosynthetic PropertiesPhotosynthesis is one of the main metabolic processes de-

termining crop production, and is directly affected by drought.When available water is decreased or severely limited underdrought stress, plants tend to close their stomata (Cornic andMassacci, 1996; Hu et al., 2004; Farooq et al., 2009a), decreas-ing the inflow of CO2 into leaves and directing more electronsto form active oxygen species (Fig. 3). As transpiration ratedecreases, the amount of heat dissipated declines. Under theseconditions, plants suffer from multiple constraints includinginjury of cell components by active oxygen and increasing tem-perature (Parry et al., 2002; Farooq et al., 2008). In a numberof studies, applied drought stress substantially decreased the

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FIG. 3. Under moderate water deficits, intercellular CO2 (Ci) decreases dueto stomatal closure, while photosynthetic capacity is maintained. This decreasein Ci may induce reversible inhibition of some enzymes. At the same time,starch content decreases and reducing sugars are maintained or even increase.This change in carbohydrate status can lead to alterations of gene expression(redrawn from Chaves and Oliveira, 2004).

net rate of photosynthesis in rice by 20–30% (Farooq et al.,2009b–f).

Several studies have investigated the demand for photoas-similates (sink strength) in regulating photosynthesis throughchanges in carbohydrate partitioning and accumulation understressful conditions (Sharkey 1990; Tezara et al., 1999; Pauland Foyer, 2001; von Caemmerer, 2003; Zhou et al., 2007).Sink strength limits photosynthesis under several stresses. Indrought-stressed rice, photosynthetic capacity decreased as aresult of stomatal closure as an early and effective response towater deficit (Chaves et al., 2002; Lawlor and Cornic, 2002),thereby reducing assimilation rate and yield (Araus et al., 2002).Assimilate partitioning between shoots and roots, as determinedby changes in dry matter, was not affected by drought whenplants were gradually stressed; however, additional biomass waspartitioned to roots. Dry matter partitioning to roots ceased un-der severe stress.

In rice, as in other C3 cereals, grain is a well-defined sinkwhere 60–90% of the carbon for grain development comes fromphotosynthetic activity of the flag leaf (Yoshida, 1981). Main-tenance of assimilate export during drought from source leavesand storage organs such as stems may sustain grain develop-ment under unfavorable conditions for growth and may helpto stabilize yields in changing environments. Severe droughtconditions resulted in limited photosynthesis due to a declinein Rubisco activity (Bota et al., 2004). Dehydration causes cellshrinkage and a subsequent decline in cellular volume. Thisresults in viscous cellular contents, increasing the probabilityof protein–protein interactions, their aggregation and denatu-ration. Increased concentrations of solutes may become toxic,thereby affecting the functioning of some enzymes, includingthose required for photosynthetic machinery (Hoekstra et al.,2001).

Both light and dark reactions of photosynthesis are crucialin the production of reducing powers such as NADPH and ATP,and biomass yield. In a study using two rice varieties (A4 andF2000), drought stress decreased quantum yield of PS II (�PSII), maximum efficiency of PS II (F ′

V /F ′M ) and photosynthetic

fluorescence quenching (qP), and increased non-photosyntheticfluorescence quenching (qN). F2000 had larger values of �PSII and F ′

V /F ′M at lower relative water contents (RWC) than A4.

With the onset of drought, A4 increased the xanthophyll cyclepool; F2000 remained constant throughout the drought cycle.In both varieties, drought increased the de-epoxidation state(DEPS) by 40% but at a higher RWC in A4 than in F2000(Pieters and Souki, 2005). Zhou et al. (2007) reported a substan-tial inhibition of stomatal conductance and net photosynthesisowing to drought stress, mainly due to metabolic limitations andoxidative damage to the chloroplast.

B. Water RelationsRelative water content (RWC), leaf water potential (ψL),

stomatal conductance (gs), rate of transpiration (Tr), leaf temper-ature, and canopy temperature are important characteristics in-fluencing plant water relations (Cabuslay et al., 2002). Droughtstress affects water relations of rice at both the cellular andwhole plant level causing specific and nonspecific reactions,damage and adaptation reactions (Beck et al., 2007). Leaf waterpotential of rice under water stress was lower than controls, withdifferences increasing after midday (Hu et al., 2004). Pre-dawnψL of rice decreased significantly when soil water content orsoil water potential reached a threshold, resulting in reducedsingle leaf net photosynthetic rate (Hu et al., 2004). In anotherreport, both panicle and leaf water potential of upland varietiesstarted to decline later in the day than in the lowland variety,thereby maintaining a higher level of both panicle and leaf waterpotential and recovering more quickly (Liu et al., 2007).

Siopongco et al. (2008) provided evidence for root signalsduring progressive soil drying, where gs and Tr decreased be-fore ψL started to decline. Increases in leaf ABA concentrationunder field drought, and its strong association with soil moisturetension and gs, suggest its involvement in mediating stomatalresponses during early drought in rice. The recovery in ψL afterseverely droughted roots in the greenhouse was attributed toincreased hydraulic conductance. A significant decrease in ψL,solute potential, turgor pressure, and RWC of rice was notedunder drought stress conditions (Farooq et al., 2008; 2009b–f).

IV. RESISTANCE MECHANISM AND MANAGEMENTThe mechanisms underlying genetic variation in both consti-

tutive and adaptive root distribution may be sensitive to signals,particularly auxin, that influence root elongation and branching(Ge et al., 2004).

A. Physiological and Agronomic ImplicationsUnder mild stress conditions, osmotic adjustment allows for

the maintenance of turgor and therefore can impair stomatal

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function, expansive growth and other turgor-dependent process(Farooq et al., 2009a). Osmotic adjustment, osmoprotection, an-tioxidation, and scavenging defense systems are important fac-tors to consider in the resistance in rice and other plant speciesto drought (Farooq et al., 2009a). The physiological basis ofgenetic variation in the response of rice to drought is not clearpartly because many different measures of resistance have beenreported. If tolerance is defined as the ability to maintain leafarea and growth under prolonged vegetative stress, the main ba-sis of variation appears to be constitutive root system architec-ture and its associated tillering habit that allows for maintenanceof more favorable plant water status (Nguyen et al., 1997). Inthe field, the impact of the root system is easily confounded byplant size effects (Mitchell et al., 1998). Differences have alsobeen reported in adaptive response of root distribution to soildrying (Azhiri-Sigari et al., 2000).

1. Phenology and OntogenyPlant size, usually expressed as single plant leaf area or leaf

area index, plays a major role in water use. Small-statured riceplants with reduced leaf area are generally less productive,but use less water. Botanists have long recognized that smallplants bearing small leaves are typical ecotypes of xeric environ-ments (Blum, 2007). While such plants withstand drought verywell, their growth rates and biomass are relatively low (Hensen,1985).

In drought-prone upland areas of eastern India andBangladesh, drought escape is an important mechanism thatallows rice to produce grain despite limited water availabil-ity (Haque et al., 1992; Khush et al., 1997). Short-durationvarieties are commonly used in upland fields in this region(Haque et al., 1992); some of which reach maturity in as lit-tle as 80 days (Khush et al., 1997). Such varieties usually es-cape terminal drought, but they are not necessarily drought-resistant. Some are short duration (Bangladeshi types) varieties,adapted to the entire range of rice ecosystems and irrigated indrought-prone upland fields, also have drought-resistant char-acteristics (Glaszmann, 1987). Short-duration varieties are alsofound within the tropical japonica germplasm group. These va-rieties are particularly important in rice-producing areas in WestAfrica, and include drought-avoiding varieties such as WAB56-140, which has been used as a recurrent parent to produce somenew rice for Africa (NERICA) varieties (Asch et al., 2005; Nd-jiondjop et al., 2006).

Roots are key components of rice adaptation to drought en-vironments. Root depth and extension into deep soil is crucialfor its performance under limited water supply if moisture isavailable at depth. Since rice plants obtain water and mineralrequirements from roots and the availability of these resources islimited, it is difficult to overstate the importance of roots to plantproductivity. A deep and prolific root system allows access towater deep in the soil profile, and is considered crucially impor-tant in determining drought resistance in upland rice, and sub-stantial genetic variation exists for this (O’Toole, 1982; Yoshida

and Hasegawa, 1982; Ekanayake et al., 1985; Fukai and Cooper,1995). The potential for deep roots is expressed constitutivelyand can be phenotyped under nonstress conditions.

Deep-rooting cultivars are more resistant to drought thanshallow-rooting ones (Nemoto et al., 1998; Farooq et al., 2009i),as they are better able to exploit water retained in deep soillayers (Kondo et al., 2003). The size of the root system variessubstantially between different ecotypes of rice (Price et al.,1997). For example, tropical japonica types are reported to havelarger root systems than indica types (Ingram et al., 1994; Farooqet al., 2009i). Not only is the size of the root system important fordrought resistance, but so too is the distribution of root biomassand root length (Kondo et al., 2003).

2. Antioxidant Defense SystemThe antioxidant defense system in rice includes both en-

zymatic and nonenzymatic constituents. In the ascorbate–glutathione cycle, ascorbate peroxidise (APX) reduces H2O2

using ascorbate as an electron donor. Oxidized ascorbate is thenreduced by reduced glutathione (GSH) generated from oxidizedglutathione (GSSG) catalyzed by glutathione reductase (GR) atthe expense of NADPH (Lin and Kao, 2000).

Nonenzymatic constituents protect plant cells by combininganion- and cation-binding properties involving a radical scav-enging function (Bors et al., 1989). Spermine, spermidine (Spd)and putrescine (Put) reduce levels of superoxide radicals gen-erated by senescing plant cells (Drolet et al., 1986). Alterna-tively, polyamine (PA) catabolism produces H2O2, a signalingmolecule that enters the stress-signal-transduction-chain pro-moting an activation of antioxidative defense response, but canalso act as a pro-oxidant agent (Wang et al., 2005).

3. Plant Growth RegulatorsPlant growth regulators (PGRs) are either naturally occur-

ring or synthetic and, when applied exogenously, can increaseyields of a target plant. They act as chemical messengers reg-ulating the normal progression of developmental changes aswell as responses to environmental signals (Morgan, 1990). Theterm PGR and phytohormones has been used interchangeably,particularly when referring to auxins, gibberellins, cytokinins,ethylene, and abcissic acid (Taiz and Zeiger, 2006).

Rice plants respond to drought by accumulating abscisic acid(ABA). Applications of ABA are known to affect plant growthand development, mimicking the effects of water stress, therebyhelping plants to better survive stress conditions (Davies andJones, 1991). In a study on genetic variation in ABA accumula-tion in rice, a consistent negative relationship between the abilityof detached and partially dehydrated leaves to accumulate ABAand leaf weight was found (Henson, 1985).

Cytokinins play a role in stomatal regulation under waterstress. Water stress lowers cytokinin activity, and rewatering ofdrought-stressed plants restores it (Reid and Wample, 1985).An increase in ABA and decrease in cytokinin under waterstress favors stomatal closure and reduces water loss through

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transpiration (Morgan, 1990). Although stomatal closure isthought to be an adaptive strategy of plants to water stress,it interferes with gas exchange and results in oxidative stress inplant cells, especially under high light (Demmig et al., 1988,Smirnoff and Stewart, 1995).

To investigate the effects of formulated fertilizer synergistson drought resistance in rice, a pot experiment was conductedto analyze photosynthetic characteristics and accumulation ofABA and proline in a mid-season rice variety. The synergistsimproved net photosynthetic rate and coordination between wa-ter loss and CO2 absorption, and reduced harmful effects onphotosynthesis. Under drought, ABA accumulated in roots andleaves, more so in the roots. This suggests that the synergistincreases ABA accumulation, but reduces proline accumulationin rice under drought (Wang et al., 2007).

4. PolyaminesPolyamines (PAs) are known to influence plant growth and

development (Walden et al., 1997; Scholten, 1998; Bais et al.,1999). In rice, PAs accumulate under various environmentalstresses (Bouchereau et al., 1999). The stress sensitivity of adc2-1 was recovered by the addition of exogenous putrescine (Put).When an oat arginine decarboxylase (ADC) gene was overex-pressed in rice, Capell et al. (1998) observed improved droughtresistance in terms of chlorophyll loss.

Rice had a greater capacity than other cereals for PA biosyn-thesis in leaves in response to water stress but the extent variedwith PA forms and stress stages (Capell et al., 1998; Bouchereauet al., 1999; Yang et al., 2007). Yang et al. (2007) suggestedhigher levels of free spermidine (Spd)/free spermine (Spm) andinsoluble-conjugated Put, as well as early accumulation of freePAs would be beneficial in the adaptation of rice to drought.Yang et al. (2007) found six rice cultivars, differing in droughtresistance and subjected to well-watered and water-stressedtreatments during the reproductive stage, increased activity ofarginine decarboxylase, S-adenosyl-L-methionine decarboxy-lase and Spd synthase in leaves. The accompanied increasesin free Spd, free Spm and insoluble-conjugated Put were sig-nificantly correlated with the yield maintenance ratio (ratio ofgrain yield under water-stressed conditions to grain yield underwell-watered conditions) (Yang et al., 2007).

5. Osmotic Adjustment and Compatible SolutesOsmotic adjustment (OA) is a specific response to maintain

water relations (turgor) under osmotic stress by accumulatingorganic solutes such as sugar alcohols, proline, quaternary am-monium and/or tertiary sulphonium compounds in response toosmotic stress (Serraj and Sinclair, 2002). Compatible solutescan protect enzymes and membranes against deleterious effectsof destabilizing ions (Yancey et al., 1982) (Fig. 4). In a recentreview, Serraj and Sinclair (2002) concluded that yield advan-tages from OA only occur at very low and uneconomic yields.However, further investigations are required to confirm this.The introduction of genes synthesizing glycinebetaine (GB) into

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DdedargePnoitcetor

Protein

Compatible solute

Destabilising molecule

Watermolecule

FIG. 4. Role of compatible solutes in drought resistance; (a) in the hydratedstate, the presence of water reduces the interaction of destabilizing molecules,(b) in resistant cells the synthesis of compatible solutes preferentially excludesbinding of destabilizing molecules and stabilizes native protein conformation,and (c) in sensitive cells lacking compatible solutes result in preferential bind-ing of destabilizing molecules to the protein surface, leading to degradation.(conceived from Hoekstra et al. 2001).

nonaccumulators of GB proved effective in increasing resistanceto various abiotic stresses (Sakamoto and Murata, 2002; Chenand Murata, 2002; Kumar et al., 2004). Rice does not produceGB under stress or non-stress conditions (Rhodes and Hanson,1993). Hence, transgenic plants over-expressing GB synthesiz-ing genes increased production of GB and resistance to droughtstress (Rhodes and Hanson, 1993).

6. Seed PrimingSeed priming involves partial hydration of seeds where

germination-related metabolic processes begin but radicle emer-gence does not (Bradford, 1986). This results in an extension ofPhase II, essentially restricting the seed within the lag phase(Taylor et al., 1998). In rice, primed seeds usually exhibitincreased germination rates, germination uniformity, and to-tal germination percentages (Farooq et al., 2006a–f, 2009h)which have been attributed to metabolic repair during imbibi-tion (Farooq et al., 2006a), a buildup of germination-promotingmetabolites (Farooq et al., 2006a, 2009h) and osmotic adjust-ment (Bradford, 1986). However, for seeds that are not redriedafter treatment, a simple reduction in the lag time of imbibitionoccurs (Taylor et al., 1998; McDonald, 2000).

In the newly introduced aerobic rice culture, the frequencyand intensity of drought may increase substantially. For instance,rice seeds osmoprimed with 4% KCl solution and saturatedCaHPO4 solution and sown directly improved seedling emer-gence, stand establishment, and yield under water-deficit con-ditions (Du and Toung, 2002). Harris et al. (2002) reported thatin drought-prone areas, primed rice seeds germinated well andseedlings emerged faster and more uniformly, leading to in-creased yields. In a germination trial of 11 varieties of uplandrice under limited water conditions, seed priming resulted in

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earlier and synchronized emergence (Harris and Jones, 1997).Seed priming with GB, SA, and polyamines improved droughtresistance in rice by maintaining tissue water potential and en-hancing the capacity to express antioxidant systems, which im-proved the integrity of cellular membranes and enabled plantsto maintain high photosynthesis, soluble sugars, and α-amylaseactivity (Farooq et al., 2008, 2009b, e). Foliar treatments weremore effective than seed treatments while, in the GB treat-ment, foliar application with 100 mg L−1 was the most effective(Farooq et al., 2008).

B. Silicon NutritionSilicon (Si) is the second most abundant element in soil

and a mineral substrate for most of the world’s plant life. It isreadily absorbed such that terrestrial plants contain appreciableconcentrations ranging from a fraction of 1% of dry matter to10% or even higher (Epstein, 1994). Its uptake and transport inrice, a typical Si-accumulator, is an active process (Lewin andReimann, 1969; Epstein, 1994; Ma et al., 2006). Rapid progresshas recently been made in characterizing Si uptake and transportin rice by using rice mutants (Ma et al., 2002; Tamai and Ma,2003). Lateral roots of rice play an important role in Si uptakewhereas root hairs do not (Ma et al., 2001). Si uptake by riceis a specific transporter-mediated process and the transportercontaining Cys, not Lys residues, is not inducible and has alow affinity for Si (Tamai and Ma, 2003). Furthermore, a generesponsible for xylem loading of Si has recently been mappedto chromosome 2 of rice using the Lsi1 mutant (formerly GR1mutant) and is localized on the plasma membrane of the distalside of both exodermis and endodermis cells and constitutivelyexpressed in the roots (Ma et al., 2006). The Si gene, Lsi1 ispredicted to encode a membrane protein similar to aquaporins(Ma et al., 2006).

Studies show that Si is not inert, but acts as a physical ormechanical barrier in plants. It is not only deposited in cell walls,but is also actively involved in metabolic and/or physiologicalactivities, especially in plants subjected to multiple stresses (Maand Yamaji, 2008). With respect to drought stress, studies onSi involvement are limited. Si may decrease transpiration rateand membrane permeability of rice under water deficit inducedby polyethylene glycerol. Silicon application may also enhancedrought resistance of plants. Under water stress, such as soildrying and high water demand from the atmosphere, silicon-applied rice has been shown to retain a higher leaf water potentialthan crops grown without Si application (Yoshida, 1965; Matohet al., 1991; Agarie et al., 1998). The active reaction of stomatato atmospheric humidity in rice has been suggested to inhibit leafwater deficit (Agarie et al., 1998; Lux et al., 1999). Endodermaltissue, which plays an important role in water transport acrossthe root, accumulates large amounts of Si in mature drought-tolerant rice cultivars (Lux et al., 1999).

Of the two recently reported genes (Lsi1 and Lsi2) encodingSi transporters have been identified from rice. Lsi1 (low silicon

1) belongs to a Nod26-like major intrinsic protein subfamily inaquaporin, while Lsi2 encodes a putative anion transporter. Lsi1is localized on the distal side of both exodermis and endodermisin rice roots, while Lsi2 is localized on the proximal side of thesame cells. Lsi1 shows influx transport activity for Si, while Lsi2shows efflux transport activity. Therefore, Lsi1 is responsible fortransport of Si from the external solution to root cells, whereasLsi2 is an efflux transporter responsible for transport of Si fromroot cells to apoplast. Coupling of Lsi1 with Lsi2 is required forefficient uptake of Si in rice (Ma and Yamaji, 2008).

V. CROP IMPROVEMENTGenetic improvement for drought resistance has been ad-

dressed using a conventional approach by selecting for yieldand secondary traits (Farooq et al., 2009a). The effectivenessof selection for secondary traits to improve yield under water-limiting conditions has been demonstrated in maize (Chapmanand Edmeades, 1999) and wheat (Richards et al., 2000). Manystudies have investigated genetic variation in traits, which areexpected to influence the response of rice to drought stress.These include deeper and thicker roots (Yadav et al., 1997), rootpulling resistance (Pantuwan et al., 2002a), greater root pene-tration (Fukai and Cooper, 1995; Ali et al., 2000; Clark et al.,2000), osmotic adjustment (Lilley and Ludlow, 1996) and mem-brane stability (Tripathy et al., 2000). The power of molecularbiology for locating important gene sequences and introgressingQTL, or even selecting genetically important QTL to developdrought tolerant genotypes strongly depends on our understand-ing of yield-determining physiological processes (Kirigwi et al.,2007).

In the following sections, different selection and breedingstrategies, functional genomic approaches, and biotechnologicaltools to develop suitable protocols to enhance drought resistancein rice are presented.

A. Breeding for Crop ImprovementConventional breeding is often based on empirical selection

for yield (Atlin and Lafitte, 2002), which is far from optimal,since yield is a quantitative trait and characterized by low her-itability and high genotype × environment (G × E) interac-tions (Babu et al., 2003). Understanding the physiological andmolecular basis may help target key yield-limiting traits. Suchan approach may complement conventional breeding programsand hasten yield improvement (Cattivelli et al., 2008).

For a breeder, individual or combinations of traits that aredirectly or indirectly associated with enhanced plant survivalare likely to improve economic yield (with or without stability),which may constitute potential target(s) for study and selection(Kirigwi et al., 2007). The following six difficulties inherent toselecting drought-resistant rice for rainfed lowlands were iden-tified by Fukai et al. (1999): 1) coupling of photosynthesis andtranspiration processes when water is limited, hence difficultyin increasing dry matter production and yield; 2) interaction

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Screening genotypes for drought resistance

Developing materials for analysis

QTL analysis andGene mapping

Transgenic plants for drought resistance

Marker-assisted selection (MAS)

Gene cloning

Developing materials carrying QTL

Gene pyramiding for drought resistance

Developing materials carrying multiple gene

Development of materials for drought resistance

FIG. 5. Developing materials for drought resistance. Genotypes are screenedfor drought resistance, which are used for the development of genetic materialsfor QTL analysis and gene mapping. For gene cloning, identified gene or majorQTL are analyzed in detail using large populations. Cloned gene for droughtresistance is transferred into widely adapted varieties. To develop materials car-rying gene or QTL for drought resistance, DNA markers having link to gene orQTL are used for marker-assisted selection. Likewise, marker-assisted selectionis used for developing materials of gene pyramiding. The gene cloning, marker-assisted selection and gene pyramiding are useful for developing materials fordrought resistance.

between nutrient availability and water stress, even with mildsoil water deficits reducing availability; 3) incomplete under-standing of mechanisms of drought resistance; 4) importance ofphenology and potential yield as components of yield under lim-ited water that override the effectiveness of drought-resistancecharacteristics; 5) large G × E interactions for yield, causing in-consistency in yield performance in different environments, andhence necessitating more testing in different locations and years;and 6) different types of drought and different traits that maybe required for each drought type. The protocol for developingmaterials for drought resistance is outlined in Figure 5.

1. Drought-resistance TraitsTo enable scientists of different disciplines to better under-

stand plant responses to water deficits and link this understand-ing with breeding of improved cultivars, drought-resistancetraits may be divided into primary, secondary, integrative, phe-nological, and plant-type traits. Primary traits are further dividedinto constitutive traits (i.e., no drought stress, such as rootingdepth, root thickness, branching angle, and root distributionpattern; Lafitte et al., 2001; Kato et al., 2006) and inducedtraits (e.g., hardpan penetration and osmotic adjustment). Con-stitutive root traits, interacted with drought intensity, have alarge effect on extractable soil water during drought (e.g., Lilleyand Fukai, 1994). This influences expression of both inducedand secondary traits, such as maintenance of plant water sta-tus, canopy temperature, leaf rolling score, and leaf death score.

These secondary traits may then reduce spikelet fertility andyield components (i.e., integrative traits) and, ultimately, yield(Kobata et al., 1994). Plant-type traits such as tiller number andplant height modify the expression of secondary and integra-tive traits by affecting transpirational demand. Genotypes withgreater plant height are often larger in overall plant size, inter-cept more light and use water faster by transpiration, leading tolower plant water status (Kamoshita et al., 2004), higher leafdeath scores and more spikelet sterility (Pantuwan et al., 2002c;Kato et al., 2007). Phenology, interacted with timing of drought,has a large effect on yield through integrative traits.

Plant-type traits (e.g., plant height) and phenology (e.g., flow-ering time) are usually highly heritable and used extensively intraditional plant breeding (Cooper et al., 1999a, b). Leaf rollingand canopy temperature (i.e., secondary traits) are also usefulfor quickly screening hundreds of lines (Lafitte et al., 2004a;Hirayama et al., 2006). Although yields under stress generallyhave a higher phenotypic correlation with some yield compo-nents (e.g., grain number and fertile spikelets; integrative traits)than they do with primary traits, primary traits are likely tobe controlled by fewer underlying genes or QTLs. Therefore,molecular characterization of primary traits (e.g., QTL analysisor candidate gene approaches) will presumably be more promis-ing than the study of yield components. Trait type classificationsare to some extent arbitrary. Thus, we classify flowering delayas an integrative trait.

The root system of rice is poorly adapted to water-limitedconditions. A deeper root system has been shown to allow up-land rice to extract more water from soil, resulting in a higheryield potential under drought. Varieties with a high deep-rootweight to shoot weight ratio exhibit enhanced drought resistancein upland rice (Fukai and Cooper, 1995). A deeper root systemin rice is thought to be a promising way of increasing wateruptake, and ultimately grain yield under drought-stress condi-tions (Mambani and Lal, 1983; Fukai and Cooper, 1995; Kondoet al., 2003). Other root characteristics, such as increased xylemvessel size and root thickness may also improve water uptake(Yambao et al., 1992).

2. SelectionDespite drought being a major constraint to rice production,

little effort has been devoted to developing drought-resistantcultivars. Most of the improved cultivars grown in drought-prone areas were originally bred for irrigated conditions, andwere not selected for drought resistance.

Several studies have reported low selection efficiency forgrain yield under drought stress (Rosielle and Hamblin, 1981;Blum, 1988; Edmeades et al., 1989). Hence, initial efforts toimprove grain yield under drought were focused on improvingsecondary traits such as root architecture, leaf water potential,panicle water potential, osmotic adjustment, and relative watercontent (Fukai et al., 1999; Price and Courtois, 1999; Jongdeeet al., 2002; Pantuwan et al., 2002a; Toorchi et al., 2003). Re-cent studies have shown that these traits are unlikely to have

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TABLE 2Selection Criteria to Develop Cultivars for Each Target Population of Environments in the

Rainfed Lowland Rice Breeding Program

Target domain Cultivar requirement Selection strategy

Upper (drought) Early maturity Select for yield at test locationWeak photoperiod sensitivity at test locationLess delay in floweringLow spikelet sterilityMaintenance of leaf water potential

Middle (drought-prone) Intermediate maturity Select for yield at test locationPhotoperiod sensitivityIntermediate heightLess delay in floweringLow spikelet sterilityMaintenance of leaf water potential

Middle (favorable) High grain yield Select for potential grain yieldIntermediate height

Lower (flooded) Late maturity Select for yield at test locationPhotoperiod sensitivity at test locationSubmergence tolerance

Source: Jongdee et al. (2006).

higher broad-sense heritability than grain yield under droughtstress and are often not highly correlated with grain yield (Atlinand Lafitte, 2002; Bernier et al., 2008). Moreover, yield gainsfrom secondary trait selections have not been clearly demon-strated, although a few rice studies have identified the responseof yield under drought stress in rice (Cooper et al., 1999b;Lafitte et al., 2004a, b; Venuprasad et al., 2007, 2008; Bernieret al., 2008; Kumar et al., 2008). Thus there is a need to selectyield-enhancing traits in rice (Jongdee et al. 2006) (Table 2).

Three morphological traits—stomatal frequency, specificleaf weight and leaf chlorophyll content—are known to be as-sociated with net photosynthetic rate, stomatal conductance andtranspiration rate and are supposedly less affected by samplingenvironments. Stomatal frequency influences stomatal conduc-tance and thus net photosynthetic rate in rice (Ishimaru et al.,2001). Genotypes with higher specific leaf weight tend to havehigher photosynthesitic rates (Nelson, 1988) which may allowplants to better adapt to water stress. High specific leaf weightsalso enable greater carbon gain by reducing transpiration lossesunder drought (Chaves et al., 2002).

Leaf water potential (ψL) is a major physiological trait as-sociated with drought resistance, which can be used as a se-lection criterion to improve drought resistance in rice (Jongdeeet al., 2002). Maintenance of high ψL may resist drought (Levitt,1980). Rice cultivars that maintained higher ψL grew betterunder water-limited conditions (Jongdee et al., 2002). Plantbreeders, therefore, rely on direct selection for grain yield in tar-get environments as the main criterion for selection. However,genotypes that produce high yields in a breeding experiment ex-

posed to drought conditions do not necessarily possess traits fordrought resistance. Such genotypes may produce high yields un-der nonlimiting water conditions, or may reach maturity beforethe drought event.

Lack of effective selection criteria is considered a majorimpediment to breeding improved rice cultivars for drought-prone environments (Ouk et al., 2006; Venuprasad et al., 2007).Earlier breeding efforts to improve drought resistance in riceconcentrated mainly on secondary traits such as root systemarchitecture, leaf water potential, panicle water potential, os-motic adjustment, and relative water content (Fukai et al., 1999;Price and Courtois, 1999; Jongdee et al., 2002; Pantuwan et al.,2002b; Toorchi et al., 2003). Direct selection for grain yieldunder stress was considered inefficient because heritability ofgrain yield under drought stress was thought to be low rel-ative to yield in nonstress environments (Rosielle and Ham-blin, 1981; Blum, 1988; Edmeades et al., 1989; Fukai andCooper, 1995). However, several recent studies using segre-gating generations and fixed lines from mapping populationsand varieties did not find heritability of grain yield underdrought stress to be consistently lower than that under nonstressconditions (Blum et al., 1999; Atlin and Lafitte, 2002; Babuet al., 2003; Lanceras et al., 2004; Bernier et al., 2007;Venuprasad et al., 2007; Kumar et al., 2007, 2008). It can beconcluded that in well-managed stress trials, direct selection foryield under drought stress is likely to be effective. There is littleevidence that secondary traits are highly correlated with grainyield under stress (Atlin and Lafitte, 2002). There is also noclear evidence that selection for secondary traits results in yield

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gains under drought stress in rice. At present, direct selectionfor grain yield in managed stress trials appears to be the mostpromising route to improved drought resistance in rice (Atlinet al., 2004; Venuprasad et al., 2007).

The use of managed environments and targeted multi-location testing has facilitated progress in breeding drought-resistant rice (Fischer et al., 2003). Classical studies havegenerated significant information regarding physiological traitsrelated to drought resistance in plants. Of these, photosynthesis-related traits are among the most important factors influencingbiomass and yield in rice and are known to have high heritabil-ity (Cook and Evans, 1983). Identification of QTL conditioningnet photosynthetic rate, stomatal conductance, and transpira-tion rate is a logical step to facilitate marker-assisted selection(MAS) for improving yield of rice under drought stress. Unfor-tunately, few studies have been conducted in this regard, partlybecause measuring these traits under field conditions is influ-enced by sampling environments and requires many replicationsto obtain accurate data. This creates a major problem in pheno-typing a typical mapping population of 200 individuals or linesfor these physiological traits (Zhao et al., 2008).

Direct selection in managed stress trials during dry seasonshad an average gain of 25%, relative to indirect selection in non-stress conditions, under naturally occurring wet season stress.In addition, direct selection under stress in uplands had an aver-age gain of 16% and 45% over non-stress-selected and randomlines, respectively, under stress in lowlands. The yield advan-tage of the stress-selected lines appeared to result mainly frommaintenance of higher harvest indices. These results show thatdirect selection for grain yield under stress is effective and doesnot reduce yield potential in rice (Venuprasad et al., 2008).

B. Molecular and Biotechnological ApproachesUnder water stress, changes in gene expression occur, which

may result directly from the stress conditions or indirectly fromsecondary stresses and/or injury responses (Hanson and Hitz,1982). Such changes are induced by a complex series of sig-nal transduction events that have not been clearly delineated.Certain genes and proteins associated with drought toleranceare expressed in rice; some genes for aquaporins or putativeaquaporins, such as rice rTip1, are upregulated under droughtstress (Liu et al., 1994). However, the simple accumulation ofaquaporin does not equate with adaptive function. Aquaporinactivity can be influenced by phosphorylation (Johansson et al.,1998), Ca2+ (Gerbeau et al., 2002) and pH (Gerbeau et al.,2002; Tournaire-Roux et al., 2003).

Molecular approaches to drought resistance have been widelystudied in rice. The rice genetic map is well covered by mi-crosatellite markers (McCouch et al., 2003), and rice researchersworldwide have developed diverse mapping populations and re-lated databases (Ware et al., 2002). Mapping studies have beensuccessful in identifying genetic regions associated with highlyheritable traits such as plant height and flowering date, and in

some cases it has been possible to identify the specific geneunderlying a QTL (Ishimaru et al., 2004). QTLs have also beenidentified for some secondary traits that are expected to be asso-ciated with drought response such as rooting depth, membranestability, and osmotic adjustment (Lafitte et al., 2004a; c). Tol-erance is measured as yield under drought; however, few strongand repeatable QTLs have been identified. As more studies arepublished using realistic stress levels and adequate documen-tation of the dynamics of drought development, it should bepossible to focus on some key QTLs that appear to be impor-tant across environments or populations. To date, it has notbeen possible to identify sufficiently large and discrete QTLsfor performance under drought to justify MAS. Instead, resultsof QTL studies are likely to be useful in locating promisinggenetic regions for identifying candidate genes. Nonetheless,modifications to QTL mapping strategies may be useful for cul-tivar improvement. These include linkage disequilibrium studiesand the advanced-backcross QTL approach that combines se-lection and QTL identification in closely related backcross lines(Lafitte et al., 2004c).

Rice plants expressing the barley group 3 late embryogen-esis abundant (LEA) gene HVA1 in leaves and roots showedimproved osmotic stress tolerance and recovery after droughtstress (Xu et al., 1996; Sivamani et al., 2000). With one or morecopies of a putative amphipathic α-helix-forming domain (theK-segment), dehydrins are the best-studied LEA proteins. Theyare considered to have a surfactant role, preventing coagulationof numerous macromolecules (Close, 1997).

Many studies report changes in the expression of individualgenes when rice is challenged by drought stress that frequentlyrespond to other abiotic and biotic stresses. These include mi-togen activated protein kinase (MAPK) (Agrawal et al., 2003),drought regulatory element binding (DREB) genes (Dubouzetet al., 2003), an endo-1, 3-glucanase (Akiyama and Pillai, 2001),a translation elongation factor (Li Zi and Chen Shou, 1999),and glutathione reductase (Kaminaka et al., 1998). For rice, mi-croarray analysis has identified differences in gene regulationin panicles of tolerant and susceptible varieties grown understress in field conditions (Kathiresan et al., 2004). In additionto direct effects of drought on gene expression, changes in post-translational modifications such as protein phosphorylation alsooccur. Advances in proteomics and metabolomics provide op-portunities to follow these changes (Koller et al., 2002). DREBgenes under the control of rd29A are being tested on tropicalrice (Datta, 2002). Dehydrins, group 2 LEA proteins, accumu-late in response to both dehydration and low temperature (Close,1997).

Little progress has been made in characterizing geneticdeterminants of drought resistance because it is a complexphenomenon comprising physio-biochemical processes at bothcellular and organismic levels at different stages of plant devel-opment (Tripathy et al., 2000). Attempts by several groups to useconventional hybridization to get C3-C4 hybrids include Su andWu (2004) and Matsuoka (2001). Ku et al. (1999) introduced

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TABLE 3Transgenic Rice Plants Reporting Effects under Drought Stress

Gene Effect Reference

p5cr Faster shoot and root growth observed in transgenic seedlings than controlsunder drought stress. Stress-inducible expression of p5cs transgene hadgreatest effect

Su and Wu (2004)

Coda Majority of transgenics survived an episode of acute drought stress. Undercycles of drought/recovery, transgenics had higher biomass and were tallerthan controls

Sawahel (2003)

otsA and otsB Transgenic lines showed more sustained plant growth, less photo-oxidativedamage and more favourable mineral balance under drought stress thancontrols

Garg et al. (2002)

otsA and otsB Sustained plant growth, less photo-oxidative damage, favorable mineralbalance under drought stress and more trehalose. Increased droughttolerance

Garg et al. (2002)

OsCDPK7 Overexpression of OsCDPK7 had less wilting than controls Saijo et al. (2000)HVA1 Transgenic plants maintained higher growth rates than controls under

droughtXu et al. (1996)

HVA1 Higher leaf RWC and tolerance to water stress by protecting cell membrane Babu et al. (2004)HVA1 After drought stress, transgenic lines showed increased stress tolerance (cell

integrity and growth) compared to controlsRohila et al. (2002)

PMA80 andPMA1959

Accumulation of either PMA80 or PMA1959 correlated with increaseddrought tolerance

Cheng et al. (2002)

Shsp17.7 Transgenic plants with higher expression levels of sHSP17.7 proteinrecovered upon rewatering after stress

Sato and Yokoya (2007)

SWPA2 Transgenic plants exhibited less membrane injuries than controls Wang et al. (2005)nhaA Germination rate, growth and average yield per plant of transgenic lines

were better than those of control lines under salt or drought stress.Moreover, sodium and proline content of transgenic lines under droughtstress was also higher than in controls

Wu et al. (2005)

p5cs Transgenic plants had faster shoot and root growth and higher prolineaccumulation compared with non-transformed plants under drought stress

Su and Wu (2004)

HRDY Enhanced root system and improved water use efficiency in transgenic plants Karaba et al. (2007)COX Increased GB synthesis improved plant growth response under stress in

transgenics compared with controlsSu et al. (2006)

SNAC1 Transgenic plants had higher seed setting and yield under stress conditionsthan controls

Hu et al. (2006)

Adc Increased endogenous putrescine level improved drought tolerance intransgenic plants

Capell et al. (2004)

OsCIPK23 Improved pollination and seed set in transgenic rice than controls underdrought stress

Yang et al. (2008)

TPS and TPP Better growth performance and photosynthetic capacity in transgenic plantsthan controls under stress

Jang et al. (2003)

TPSP Sustained plant growth, reduced photo-oxidative damage and photosyntheticactivity under drought stress

Garg et al. (2002)

OsDREB1A,OsDREB1B,OsDREB1C,OsDREB1D, andOsDREB2A

Improved growth and photosynthetic capacity in transgenic plants thancontrols under drought stress

Dubouzet et al. (2003)

OsCDPK7 Improved glycine rich and LEA proteins under drought stress in transgenicplants than controls

Saijo et al. (2000)

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phosphoenolpyruvate carboxylase (PEPC) from maize in rice toachieve a high-level expression of PEPC protein (1–3-fold thatof maize leaves). Although no significant effects were observedin the rates of photosynthesis, transformed rice plants exhib-ited reduced O2 inhibition of photosynthesis characteristic ofC3 plants and attained 40% of potential photosynthesis.

Genetic engineering techniques hold promise for develop-ing rice with drought tolerance (Table 3). Garg et al. (2002)introduced otsA and otsB genes for trehalose biosynthesis fromEscherichia coli into rice and transgenic rice accumulated tre-halose at 3–10 times the rate of nontransgenic controls. Tre-halose is a nonreducing disaccharide of glucose that functionsas a compatible solute in the stabilization of biological structuresunder abiotic stress. Transgenic rice containing genes for upreg-ulation of DREB and trehalose biosynthetic genes (Garg et al.,2002) have been developed and are expected to be tested in fieldsin the near future. Stress-inducible promoters such as OsDREB1have induced strong expression of stress-responsive genes intransgenic rice, resulting in increased resistance to drought,salt and freezing stresses (Yamaguchi-Shinozaki and Shinozaki,2005). In rice, searches of genome-wide conserved sequenceshave shown that several DREB genes exist, e.g. OsDREB1A, Os-DREB1B, OsDREB1C, OsDREB1D, OsDREB1F, OsDREB2A,OsDREB4-1 andOsDREB4-2 (Dubouzet et al., 2003; Tian et al.,2005; Wang et al., 2008).

The major focus should be to improve crop yield by in-creasing carbon gain during the crop cycle under drought. It istherefore necessary to target genes that increase water-use ef-ficiency without yield penalties. This may be difficult becauseimproving water-use efficiency is usually accompanied by de-creased photosynthesis (Flexas et al., 2004) and yield (Condonet al., 2004).

VI. CONCLUSIONDrought stress reduces rice growth and development result-

ing in hampered flower production and grain filling. This de-pends on the timing, duration, severity and intensity of thestress. Following drought stress, stomata close progressivelywith a parallel decline in net photosynthesis. The drought re-sistance mechanism is complex, involving physiological andbiochemical processes at cell, tissue, organ and whole-plantlevels, depending on the stage of plant development. For exam-ple, plants reduce water loss by increasing stomatal resistance,and increase water uptake by developing large and deep rootsystems, and accumulating osmolytes and osmoprotectants. Sil-icon plays an important role in rice drought resistance mainly byincreasing root endodermal silicification thereby improving wa-ter uptake. A cDNA microarray analysis revealed several genesthat were more abundantly transcribed in transgenics than inwild types under drought stress. These genes included thosefor stress-responsive transcription factors such as DREB andstress-protective proteins like rd29A.

The effects of drought stress can be managed by plant im-provement and selection, seed priming, plant growth regulators,

and the use of osmoprotectants, among others. For exogenousglycinebetaine, proline, and other compatible solutes to be effec-tive inducers of drought resistance; their mechanisms of action,optimal concentrations, and appropriate plant developmentalstages need to be understood. The role of H2O2 as a signallingmolecule as well as identifying regulatory components in thepathway that leads to plant responses to drought stress in riceare fundamental clues for future research.

Although physiological mechanisms of drought resistance inrice are relatively well understood, further studies to determinethe physiological basis of assimilate partitioning from sourceto sink, plant phenotypic flexibility, which leads to drought re-sistance, and factors that modulate drought-stress response inrice are needed. Like most other abiotic stresses, foliar plantparts are more directly affected by drought than roots in rice.However, understanding root responses to drought stress, mostlikely involving root-shoot signalling, would be a preferred areaof research. Investigations seeking to improve crop performanceby increasing osmotic adjustment need to focus on meristem-atic regions of roots. Mutants or transgenic plants exhibitingdifferential capabilities for reactive oxygen species (ROS) for-mation and elimination may be useful. Molecular knowledgeof response and resistance mechanisms sustaianble economicyields. Furthermore, applications of functional genomics ap-proaches will help to understand the molecular basis of theresponse of rice to drought stress as well as drought resistance.

An integrated systems approach is essential in the study ofcomplex quantitative traits like yield stability under droughtstress in plants. Research must use the latest genomics resourcescombining new technologies in quantitative genetics, genomicsand bioinformatics with an ecophysiological understanding ofthe interactions between crop plant genotypes and the growingenvironment and thus better inform crop improvement.

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Agrawal, G. K., Tamogami, S., Iwahashi, H., Agrawal, V. P., and Rakwal, R.2003. Transient regulation of jasmonic acid-inducible rice MAP kinase gene(OsBWMK1) by diverse biotic and abiotic stresses. Plant Physiol. Biochem.41: 355–361.

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Documents

Advances in Drought Resistance of Rice