Plant drought stress: effects, mechanisms and management · 2017. 7. 5. · Plant drought stress: eﬀects, mechanisms and management 187 Table I. Economic yield reduction by drought

Plant drought stress effects mechanisms and

management

M Farooq A Wahid N Kobayashi D Fujita SMA Basra

To cite this version

M Farooq A Wahid N Kobayashi D Fujita SMA Basra Plant drought stress effectsmechanisms and management Agronomy for Sustainable Development Springer VerlagEDPSciencesINRA 2009 29 (1) pp185-212

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Agron Sustain Dev 29 (2009) 185ndash212ccopy INRA EDP Sciences 2008DOI 101051agro2008021

Review article

Available online atwwwagronomy-journalorg

for Sustainable Development

Plant drought stress effects mechanisms and management

M Farooq1 3 A Wahid2 N Kobayashi3 D Fujita3 SMA Basra4

1 Department of Agronomy University of Agriculture Faisalabad-38040 Pakistan2 Department of Botany University of Agriculture Faisalabad-38040 Pakistan

3 International Rice Research Institute (IRRI) DAPO Box 7777 Metro Manila Philippines4 Department of Crop Physiology University of Agriculture Faisalabad-38040 Pakistan

(Accepted 3 April 2008)

Abstract ndash Scarcity of water is a severe environmental constraint to plant productivity Drought-induced loss in crop yield probably exceedslosses from all other causes since both the severity and duration of the stress are critical Here we have reviewed the effects of droughtstress on the growth phenology water and nutrient relations photosynthesis assimilate partitioning and respiration in plants This article alsodescribes the mechanism of drought resistance in plants on a morphological physiological and molecular basis Various management strategieshave been proposed to cope with drought stress Drought stress reduces leaf size stem extension and root proliferation disturbs plant waterrelations and reduces water-use efficiency Plants display a variety of physiological and biochemical responses at cellular and whole-organismlevels towards prevailing drought stress thus making it a complex phenomenon CO2 assimilation by leaves is reduced mainly by stomatalclosure membrane damage and disturbed activity of various enzymes especially those of CO2 fixation and adenosine triphosphate synthesisEnhanced metabolite flux through the photorespiratory pathway increases the oxidative load on the tissues as both processes generate reactiveoxygen species Injury caused by reactive oxygen species to biological macromolecules under drought stress is among the major deterrents togrowth Plants display a range of mechanisms to withstand drought stress The major mechanisms include curtailed water loss by increaseddiffusive resistance enhanced water uptake with prolific and deep root systems and its efficient use and smaller and succulent leaves to reducethe transpirational loss Among the nutrients potassium ions help in osmotic adjustment silicon increases root endodermal silicification andimproves the cell water balance Low-molecular-weight osmolytes including glycinebetaine proline and other amino acids organic acids andpolyols are crucial to sustain cellular functions under drought Plant growth substances such as salicylic acid auxins gibberrellins cytokininand abscisic acid modulate the plant responses towards drought Polyamines citrulline and several enzymes act as antioxidants and reduce theadverse effects of water deficit At molecular levels several drought-responsive genes and transcription factors have been identified such as thedehydration-responsive element-binding gene aquaporin late embryogenesis abundant proteins and dehydrins Plant drought tolerance can bemanaged by adopting strategies such as mass screening and breeding marker-assisted selection and exogenous application of hormones andosmoprotectants to seed or growing plants as well as engineering for drought resistance

drought response stomatal oscillation osmoprotectants hormones stress proteins drought management CO2

1 INTRODUCTION

Faced with scarcity of water resources drought is the singlemost critical threat to world food security It was the catalystof the great famines of the past Because the worldrsquos watersupply is limiting future food demand for rapidly increasingpopulation pressures is likely to further aggravate the effectsof drought (Somerville and Briscoe 2001) The severity ofdrought is unpredictable as it depends on many factors such asoccurrence and distribution of rainfall evaporative demandsand moisture storing capacity of soils (Wery et al 1994)

Investigations carried out in the past provide consider-able insights into the mechanism of drought tolerance in

Corresponding author farooqcpgmailcom mfarooqcgiarorg

plants at molecular level (Hasegawa et al 2000) Three mainmechanisms reduce crop yield by soil water deficit (i) re-duced canopy absorption of photosynthetically active radia-tion (ii) decreased radiation-use efficiency and (iii) reducedharvest index (Earl and Davis 2003) The reproducibility ofdrought stress treatments is very cumbersome which signif-icantly impedes research on plant drought tolerance A slowpace in revealing drought tolerance mechanisms has hamperedboth traditional breeding efforts and use of modern genet-ics approaches in the improvement of drought tolerance ofcrop plants (Xiong et al 2006) Although plant responsesto drought are relatively well known plant performance un-der a more complex environment where multiple stresses co-occur is fragmentary That is why the plants have to respond

Article published by EDP Sciences

186 M Farooq et al

simultaneously to multiple stresses eg drought excessivelight and heat which may coincide in the field These kindsof investigations are usually not predictable from single factorstudies (Zhou et al 2007)

It is imperative to improve the drought tolerance of cropsunder the changing circumstances Currently there are no eco-nomically viable technological means to facilitate crop pro-duction under drought However development of crop plantstolerant to drought stress might be a promising approachwhich helps in meeting the food demands Development ofcrops for enhanced drought resistance among other thingsrequires the knowledge of physiological mechanisms and ge-netic control of the contributing traits at different plant de-velopmental stages Valuable work has been done on droughttolerance in plants Ingram and Bartels (1996) more than adecade ago elegantly reviewed those appreciable efforts Morerecent reviews deal with specific aspects of plant drought tol-erance (Penna 2003 Reddy et al 2004 Agarwal et al 2006)This review encompasses an overview of the current work re-ported on some effects and mechanisms of drought tolerancein higher plants and important management strategies to over-come the drought effects mainly on field crops

2 EFFECTS OF DROUGHT ON PLANTS

The effects of drought range from morphological to molec-ular levels and are evident at all phenological stages of plantgrowth at whatever stage the water deficit takes place An ac-count of various drought stress effects and their extent is elab-orated below

21 Crop growth and yield

The first and foremost effect of drought is impaired ger-mination and poor stand establishment (Harris et al 2002)Drought stress has been reported to severely reduce germina-tion and seedling stand (Kaya et al 2006) In a study on peadrought stress impaired the germination and early seedlinggrowth of five cultivars tested (Okcu et al 2005) Moreoverin alfalfa (Medicago sativa) germination potential hypocotyllength and shoot and root fresh and dry weights were reducedby polyethylene glycol-induced water deficit while the rootlength was increased (Zeid and Shedeed 2006) However inrice drought stress during the vegetative stage greatly reducedthe plant growth and development (Fig 1 Tripathy et al2000 Manikavelu et al 2006)

Growth is accomplished through cell division cell enlarge-ment and differentiation and involves genetic physiologicalecological and morphological events and their complex inter-actions The quality and quantity of plant growth depend onthese events which are affected by water deficit (Fig 2) Cellgrowth is one of the most drought-sensitive physiological pro-cesses due to the reduction in turgor pressure (Taiz and Zeiger2006) Under severe water deficiency cell elongation of higherplants can be inhibited by interruption of water flow from thexylem to the surrounding elongating cells (Nonami 1998)

Well-watered Drought-stress

Figure 1 Effect of drought stress on the vegetative growth of rice cvIR64 Both the plants were grown under well-watered conditions upto 20 days following emergence One pot was submitted to progres-sive soil drying (drought stress) The afternoon before the drought allpots were fully watered (to saturation) After draining overnight thepots were enclosed around the stem to prevent direct soil evaporationA small tube was inserted for re-watering pots The decrease in soilmoisture was controlled by partial re-watering of the stressed pots toavoid a quicker imposition of stress and to homogenize the develop-ment of drought stress A well-watered control pot was maintainedat the initial target weight by adding the daily water loss back to thepot This figure shows the plants 20 days after imposition of droughtstress

Drought stress(Reduced water availability)

Loss of turgor Impaired mitosis

Obstructedcell elongation Limited

cell division

Diminished growth

Figure 2 Description of possible mechanisms of growth reductionunder drought stress Under drought stress conditions cell elongationin higher plants is inhibited by reduced turgor pressure Reduced wa-ter uptake results in a decrease in tissue water contents As a resultturgor is lost Likewise drought stress also trims down the photo-assimilation and metabolites required for cell division As a conse-quence impaired mitosis cell elongation and expansion result in re-duced growth

Plant drought stress effects mechanisms and management 187

Table I Economic yield reduction by drought stress in some representative field crops

Crop Growth stage Yield reduction ReferencesBarley Seed filling 49ndash57 Samarah (2005)Maize Grain filling 79ndash81 Monneveux et al (2005)Maize Reproductive 63ndash87 Kamara et al (2003)Maize Reproductive 70ndash47 Chapman and Edmeades (1999)Maize Vegetative 25ndash60 Atteya et al (2003)Maize Reproductive 32ndash92 Atteya et al (2003)Rice Reproductive (mild stress) 53ndash92 Lafitte et al (2007)Rice Reproductive (severe stress) 48ndash94 Lafitte et al (2007)Rice Grain filling (mild stress) 30ndash55 Basnayake et al (2006)Rice Grain filling (severe stress) 60 Basnayake et al (2006)Rice Reproductive 24ndash84 Venuprasad et al (2007)Chickpea Reproductive 45ndash69 Nayyar et al (2006)Pigeonpea Reproductive 40ndash55 Nam et al (2001)Common beans Reproductive 58ndash87 Martiacutenez et al (2007)Soybean Reproductive 46ndash71 Samarah et al (2006)Cowpea Reproductive 60ndash11 Ogbonnaya et al (2003)Sunflower Reproductive 60 Mazahery-Laghab et al (2003)Canola Reproductive 30 Sinaki et al (2007)Potato Flowering 13 Kawakami et al (2006)

Impaired mitosis cell elongation and expansion result in re-duced plant height leaf area and crop growth under drought(Nonami 1998 Kaya et al 2006 Hussain et al 2008)

Many yield-determining physiological processes in plantsrespond to water stress Yield integrates many of these phys-iological processes in a complex way Thus it is difficultto interpret how plants accumulate combine and display theever-changing and indefinite physiological processes over theentire life cycle of crops For water stress severity durationand timing of stress as well as responses of plants after stressremoval and interaction between stress and other factors areextremely important (Plaut 2003) For instance water stressapplied at pre-anthesis reduced time to anthesis while at post-anthesis it shortened the grain-filling period in triticale geno-types (Estrada-Campuzano et al 2008) In barley (Hordeumvulgare) drought stress reduced grain yield by reducing thenumber of tillers spikes and grains per plant and individualgrain weight Post-anthesis drought stress was detrimental tograin yield regardless of the stress severity (Samarah 2005)

Drought-induced yield reduction has been reported in manycrop species which depends upon the severity and duration ofthe stress period (Tab I) In maize water stress reduced yieldby delaying silking thus increasing the anthesis-to-silking in-terval This trait was highly correlated with grain yield specif-ically ear and kernel number per plant (Cattivelli et al 2008)Following heading drought had little effect on the rate ofkernel filling in wheat but its duration (time from fertiliza-tion to maturity) was shortened and dry weight reduced atmaturity (Wardlaw and Willenbrink 2000) Drought stress insoybean reduced total seed yield and the branch seed yield(Frederick et al 2001) In pearl millet (Pennisetum glaucum)co-mapping of the harvest index and panicle harvest indexwith grain yield revealed that greater drought tolerance wasachieved by greater partitioning of dry matter from stover tograins (Yadav et al 2004)

Drought at flowering commonly results in barrenness Amajor cause of this though not the only one was a reductionin assimilate flux to the developing ear below some thresholdlevel necessary to sustain optimal grain growth (Yadav et al2004) Moisture deficit reduced cotton (Gossypium hirsutum)lint yield although the timing duration severity and speedof development undoubtedly had pivotal roles in determininghow the plant responded to moisture deficit Lint yield wasgenerally reduced due to reduced boll production because offewer flowers and greater boll abortions when the stress inten-sity was greater during reproductive growth (Pettigrew 2004)

Grain filling in cereals is a process of starch biosynthesisfrom simple carbohydrates It is believed that four enzymesplay key roles in this process sucrose synthase adenosinediphosphate-glucose-pyrophosphorylase starch synthase andstarch branching enzyme (Taiz and Zeiger 2006) Decline inthe rate of grain growth resulted from reduced sucrose syn-thase activity while cessation of growth resulted from inac-tivation of adenosine diphosphate-glucose-pyrophosphorylasein the water-stressed wheat (Ahmadi and Baker 2001) Wa-ter deficit during pollination increased the frequency of kernelabortion in maize (Zea mays) Under water stress diminishedgrain set and kernel growth in wheat and a decreased rate ofendosperm cell division was associated with elevated levels ofabscisic acid in maize (Morgan 1990 Ober et al 1991) Inpigeonpea drought stress coinciding with the flowering stagereduced seed yield by 40ndash55 (Nam et al 2001) In rice onthe other hand water stress imposed during the grain-fillingperiod enhanced remobilization of pre-stored carbon reservesto grains and accelerated grain filling (Yang et al 2001) Insummary prevailing drought reduces plant growth and devel-opment leading to hampered flower production and grain fill-ing and thus smaller and fewer grains A reduction in grainfilling occurs due to a reduction in the assimilate partitioningand activities of sucrose and starch synthesis enzymes

188 M Farooq et al

22 Water relations

Relative water content leaf water potential stomatal resis-tance rate of transpiration leaf temperature and canopy tem-perature are important characteristics that influence plant wa-ter relations Relative water content of wheat leaves was higherinitially during leaf development and decreased as the dry mat-ter accumulated and leaf matured (Siddique et al 2001) Ob-viously water-stressed wheat and rice plants had lower relativewater content than non-stressed ones Exposure of these plantsto drought stress substantially decreased the leaf water poten-tial relative water content and transpiration rate with a con-comitant increase in leaf temperature (Siddique et al 2001)A conservative influence of decreased stomatal conductancein non-irrigated plants was negated by a leaf-to-air vapor pres-sure difference caused by the associated higher leaf temper-ature Transpiration rates were similar in both treatments andthe lower total water use of the non-irrigated stand resulted en-tirely from a smaller leaf area index (Craufurad et al 2000)

Nerd and Nobel (1991) reported that during drought stresstotal water contents of Opuntia ficus-indica cladode were de-creased by 57 The water-storage parenchyma of the clado-des lost a greater fraction of water than the chlorenchyma andthus showed a lower turgor potential In another study on Hi-biscus rosa-sinensis relative water content turgor potentialtranspiration stomatal conductance and water-use efficiencywere decreased under drought stress (Egilla et al 2005)

The ratio between dry matter produced and water con-sumed is termed as water-use efficiency at the whole-plantlevel (Monclus et al 2005) Abbate et al (2004) concludedthat under limited supply water-use efficiency of wheat wasgreater than in well-watered conditions They correlated thishigher water-use efficiency with stomatal closure to reduce thetranspiration In another study on clover (Trifolium alexan-drinum) water-use efficiency was increased due to loweredwater loss under drought stress primarily by decreased tran-spiration rate and leaf area and relatively lesser reduction inyield (Lazaridou and Koutroubas 2004) Also in Pinus pon-derosa and Artemisia tridentata drought stress did not reducethe water-use efficiency rather it was increased mainly dueto a rapid decrease in stomatal conductance with increasingwater deficit (DeLucia et al 1989) Lazaridou et al (2003)further reported that leucern (Medicago sativa) grown underdrought had greater water-use efficiency than that under irri-gated conditions for the same leaf water potential Howeverin potato early season drought stress significantly minimizedthe water-use efficiency leading to greatly decreased growthand biomass accumulation (Costa et al 1997)

In fact although components of plant water relations are af-fected by reduced availability of water stomatal opening andclosing is more strongly affected Moreover change in leaftemperature may be an important factor in controlling leaf wa-ter status under drought stress Drought-tolerant species main-tain water-use efficiency by reducing the water loss Howeverin the events where plant growth was hindered to a greater ex-tent water-use efficiency was also reduced significantly

23 Nutrient relations

Decreasing water availability under drought generally re-sults in limited total nutrient uptake and their diminished tis-sue concentrations in crop plants An important effect of waterdeficit is on the acquisition of nutrients by the root and theirtransport to shoots Lowered absorption of the inorganic nu-trients can result from interference in nutrient uptake and theunloading mechanism and reduced transpirational flow (Garg2003 McWilliams 2003) However plant species and geno-types of a species may vary in their response to mineral up-take under water stress In general moisture stress induces anincrease in N a definitive decline in P and no definitive effectson K (Garg 2003)

Transpiration is inhibited by drought as shown for beech(Peuke et al 2002) but this may not necessarily affect nutri-ent uptake in a similar manner Influence of drought on plantnutrition may also be related to limited availability of energyfor assimilation of NOminus3 NH+4 PO3minus

4 and SO2minus4 they must be

converted in energy-dependent processes before these ions canbe used for growth and development of plants (Grossman andTakahashi 2001)

As nutrient and water requirements are closely related fer-tilizer application is likely to increase the efficiency of cropsin utilizing available water This indicates a significant inter-action between soil moisture deficits and nutrient acquisitionStudies show a positive response of crops to improved soilfertility under arid and semi-arid conditions Currently it isevident that crop yields can be substantially improved by en-hancing the plant nutrient efficiency under limited moisturesupply (Garg 2003) It was shown that N and K uptake washampered under drought stress in cotton (McWilliams 2003)Likewise P and PO3minus

4 contents in the plant tissues diminishedunder drought possibly because of lowered PO3minus

4 mobility asa result of low moisture availability (Peuke and Rennenberg2004) In drought-treated sunflower the degree of stomatalopening of K+-applied plants initially indicated quicker de-cline However at equally low soil water potential diffusiveresistance in the leaves of K+-applied plants remained lowerthan those receiving no K+ (Lindhauer et al 2007) In sum-mary drought stress reduces the availability uptake translo-cation and metabolism of nutrients A reduced transpirationrate due to water deficit reduces the nutrient absorption andefficiency of their utilization

24 Photosynthesis

A major effect of drought is reduction in photosynthesiswhich arises by a decrease in leaf expansion impaired pho-tosynthetic machinery premature leaf senescence and associ-ated reduction in food production (Wahid and Rasul 2005)When stomatal and non-stomatal limitations to photosynthesisare compared the former can be quite small This implies thatother processes besides CO2 uptake are being damaged Therole of drought-induced stomatal closure which limits CO2uptake by leaves is very important In such events restricted

Stomatal closure

Diminished CO2 influx

ABA-signalling

Limited carboxylation

Lower tissue water potential

Rubisco binding inhibitors

Diminished activities of PEPcaseNADP-ME FBPase PPDK

Lower Rubiscoactivity

Down-regulation of

non-cyclic e-transport Obstructed ATPsynthesis

Declinedphotosynthesis

ROS production

Attack onmembranes

Figure 3 Photosynthesis under drought stress Possible mechanismsin which photosynthesis is reduced under stress Drought stress dis-turbs the balance between the production of reactive oxygen speciesand the antioxidant defense causing accumulation of reactive oxy-gen species which induces oxidative stress Upon reduction in theamount of available water plants close their stomata (plausibly viaABA signaling) which decreases the CO2 influx Reduction in CO2

not only reduces the carboxylation directly but also directs moreelectrons to form reactive oxygen species Severe drought conditionslimit photosynthesis due to a decrease in the activities of ribulose-15-bisphosphate carboxylaseoxygenase (Rubisco) phosphoenolpyru-vate carboxylase (PEPCase) NADP-malic enzyme (NADP-ME)fructose-1 6-bisphosphatase (FBPase) and pyruvate orthophosphatedikinase (PPDK) Reduced tissue water contents also increase the ac-tivity of Rubisco binding inhibitors Moreover non-cyclic electrontransport is down-regulated to match the reduced requirements ofNADPH production and thus reduces the ATP synthesis ROS re-active oxygen species

CO2 availability could possibly lead to increased susceptibilityto photo-damage (Cornic and Massacci 1996)

Drought stress produced changes in photosynthetic pig-ments and components (Anjum et al 2003) damaged pho-tosynthetic apparatus (Fu J and Huang 2001) and diminishedactivities of Calvin cycle enzymes which are important causesof reduced crop yield (Monakhova and Chernyadegravev 2002)Another important effect that inhibits the growth and photo-synthetic abilities of plants is the loss of balance between theproduction of reactive oxygen species and the antioxidant de-fense (Fu J and Huang 2001 Reddy et al 2004) causingaccumulation of reactive oxygen species which induces ox-idative stress in proteins membrane lipids and other cellularcomponents (Fig 3) Some important components of photo-synthesis affected by drought are discussed below

241 Stomatal oscillations

The first response of virtually all plants to acute waterdeficit is the closure of their stomata to prevent the tran-spirational water loss (Mansfield and Atkinson 1990) This

may result in response to either a decrease in leaf turgorandor water potential (Ludlow and Muchow 1990) or to alow-humidity atmosphere (Maroco et al 1997) The debateas to whether drought mainly limits photosynthesis throughstomatal closure or metabolic impairment has continued fora long time (Sharkey 1990 Tezara et al 1999) During thelast decade stomatal closure was generally accepted to be themain determinant for decreased photosynthesis under mild tomoderate drought (Cornic and Massacci 1996 Yokota et al2002)

When the amount of available soil water is moderately orseverely limiting the first option for plants is to close stomata(Cornic and Massacci 1996) This decreases the inflow of CO2

into the leaves and spares more electrons for the formation ofactive oxygen species (Fig 3) As the rate of transpiration de-creases the amount of heat that can be dissipated increases(Yokota et al 2002) Various experiments have shown thatstomatal responses are often more closely linked to soil mois-ture content than to leaf water status This suggested that stom-ata respond to chemical signals eg abcissic acid produced bydehydrating roots (Fig 3) whilst leaf water status is kept con-stant (Morgan 1990 Taylor 1991 Turner et al 2001) En-vironmental conditions that enhance the rate of transpirationalso increase the pH of leaf sap which can promote abscisicacid accumulation and concomitantly diminish stomatal con-ductance Increased cytokinin concentration in the xylem sappromotes stomatal opening directly and affects the sensitiv-ity of stomata towards abscisic acid (Wilkinson and Davies2002)

Comparing results from different studies is complex due tointerspecific differences in the response of stomatal conduc-tance and photosynthesis to leaf water potential andor relativewater content the parameters most often used to assess the de-gree of drought (Cornic and Massacci 1996) It is clear thatstomata close progressively as drought progresses followedby a parallel decline in net photosynthesis However stomatalconductance is not controlled by soil water availability alonebut by a complex interaction of intrinsic and extrinsic factors

242 Photosynthetic enzymes

Very severe drought conditions limit photosynthesis due toa decline in Rubisco activity (Bota et al 2004) The activityof the photosynthetic electron transport chain is finely tuned tothe availability of CO2 in the chloroplast and change in photo-system II under drought conditions (Loreto et al 1995) De-hydration results in cell shrinkage and consequently a declinein cellular volume This makes cellular contents more viscousTherefore an increase in the probability of protein-protein in-teraction leads to their aggregation and denaturation (Hoekstraet al 2001) Increased concentration of solutes leading to in-creased viscosity of the cytoplasm may become toxic and maybe deleterious to the functioning of enzymes including thoseof the photosynthetic machinery (Hoekstra et al 2001)

The level of Rubisco in leaves is controlled by the rateof synthesis and degradation Even under drought stress theRubisco holoenzyme is relatively stable with a half-life of

190 M Farooq et al

several days (Hoekstra et al 2001) However drought stressshowed a rapid diminution in the abundance of Rubisco smallsubunit transcripts which indicated its decreased synthesis(Vu et al 1999) Rubisco activity is modulated in vivo eitherby reaction with CO2 and Mg2+ to carbamylate a lysine residuein the catalytic site or by binding inhibitors within the cat-alytic site (Fig 3) Such a binding either blocks activity or thecarbamylation of the lysine residue which is essential for ac-tivity At night 2-carboxyarabinitol-1-phosphate is formed inmany species which binds tightly to Rubisco inhibiting cat-alytic activity It is reported that tight-binding inhibitors candecrease Rubisco activity in the light In tobacco (Nicotianatabacum) decrease in Rubisco activity under drought stresswas not a primary result of changes in activation by CO2 andMg2+ and was rather due to the presence of tight-binding in-hibitors (Parry et al 2002) A rapid decline in photosynthesisunder drought was accompanied by decreased maximum ve-locity of ribulose-1 5-bisphosphate carboxylation by Rubiscospeed of ribulose-1 5-bisphosphate regeneration Rubisco andstromal fructose bis-phosphatase activities and the quantumefficiency of photosystem II in higher plants (Reddy et al2004 Zhou et al 2007) Moreover under severe drought car-boxylation efficiency by Rubisco was greatly declined and itacted more as oxygenase than carboxylase (Fig 3)

During water stress activities of the phosphoenolpyruvatecarboxylase nicotinamide adenine dinucleotide phosphate-malic enzyme Rubisco fructose-1 6-bisphosphatase andpyruvate orthophosphate dikinase decreased linearly with low-ered leaf water potential (Fig 3) Pyruvate orthophosphatedikinase activities were decreased 91 times during waterstress a much greater reduction than other enzymes whichwere from 2 to 4 times suggesting that pyruvate orthophos-phate dikinase is very likely to be the limiting enzyme to pho-tosynthesis under water stress (Du et al 1996)

243 Adenosine triphosphate synthesis

There is a long-standing controversy as to whether droughtmainly limits photosynthesis through stomatal closure (Cornicand Massacci 1996) or by metabolic impairment (Tezaraet al 1999) Evidence that impaired adenosine triphosphatesynthesis is the main factor limiting photosynthesis even un-der mild drought has further stimulated the debate (Lawlor andCornic 2002) It is reported that impaired photophosphoryla-tion and adenosine triphosphate synthesis are the main factorslimiting photosynthesis even under mild drought (Tezara et al1999)

Under drought stress production of limited nicotinamideadenine dinucleotide phosphate maintains the continuation ofelectron transport although the status of the reductant may behigh even when the fluxes are small leading to a more in-creased demand than supply Under drought stress non-cyclicelectron transport is down-regulated to match the require-ments of decreased nicotinamide adenine dinucleotide phos-phate production and cyclic electron transport is activatedThis generates a proton gradient that induces the protectiveprocess of high-energy-state quenching (Golding and Johnson

2003) Support for this model came from the isolation of a mu-tant deficient in high-energy-state quenching that lacked cyclicelectron transport (Munekage et al 2002) Support for cyclicelectron transport under drought also came from non-steady-state measurements (Cornic et al 2000)

Dissipation mechanisms of excess photon energy underwater stress were studied in ndhB-inactivated tobacco (cvXanthi) mutants impaired in reduced nicotinamide adeninedinucleotide phosphate dehydrogenase-dependent cyclic elec-tron flow around photosystem I The relative water contentand net CO2 assimilation was reduced to 30 and almostzero after an 11-day water stress regime in the mutant andwild-type plants respectively A decline in photosystem II ac-tivity (sim75) and an increase in malondialdehyde (sim45)an estimate of lipid peroxidation were found in both theplant groups when subjected to water stress Thus a defi-ciency in reduced nicotinamide adenine dinucleotide phos-phate dehydrogenase-dependent cyclic electron flow aroundphotosystem I did not lead to oxidative damage because themutant compensated for this deficiency by activating alterna-tive dissipating routes of excess photon energy such as up-regulation of ferredoxin-dependentcyclic electron flow aroundphotosystem I and enhanced accumulation of α-tocopherol(α-toc) quinine (Munneacute-Bosch et al 2005)

In fact the activities of the enzymes of carbon assimilationand those involved in adenosine triphosphate synthesis are re-tarded and sometimes inhibited depending upon the extent ofavailable moisture Of these Rubisco which shows dual func-tions acts as oxygenase under water-limiting conditions andtherefore limited CO2 fixation is noticed

25 Assimilate partitioning

Assimilate translocation to reproductive sinks is vital forseed development Seed set and filling can be limited byavailability or utilization ie assimilate source or sink lim-itation respectively (Asch et al 2005) Drought stress fre-quently enhances allocation of dry matter to the roots whichcan enhance water uptake (Leport et al 2006) De Souza andDa Silv (1987) while analyzing the partitioning and distribu-tion of photo-assimilates in annual and perennial cotton underdrought stress reported that the root-to-shoot dry matter ratiowas high in perennial cotton thereby showing a preferentialaccumulation of starch and dry matter in roots as an adaptationto drought Thus perennial cotton apparently owed its droughtresistance to the partitioning of assimilates that favored starchaccumulation and growth of the root system The export rateof sucrose from source to sink organs depends upon the cur-rent photosynthetic rate and the concentration of sucrose in theleaves (Komor 2000) Drought stress decreases the photosyn-thetic rate and disrupts the carbohydrate metabolism and levelof sucrose in leaves that spills over to a decreased export rateThis is presumably due to drought stress-induced increased ac-tivity of acid invertase (Kim et al 2000) Limited photosyn-thesis and sucrose accumulation in the leaves may hamper therate of sucrose export to the sink organs and ultimately affectthe reproductive development

Apart from source limitation the capacity of the repro-ductive sinks to utilize the incoming assimilates is also af-fected under drought stress and may also play a role inregulating reproductive abortion (Zinselmeier et al 1999)Drought-induced carbohydrate deprivation enhanced endoge-nous abscisic acid concentration and an impaired ability toutilize the incoming sucrose by the reproductive sinks arepotential factors contributing to seed abortion in grain crops(Setter et al 2001) A reduced acid invertase activity can ar-rest the development of reproductive tissues due to improperphloem unloading (Goetz et al 2001) In addition droughtstress may inhibit important functions of vacuolar invertase-mediated sucrose hydrolysis and osmotic potential modula-tion In drought-stressed maize a low invertase activity in theyoung ovaries lowers the ratio of hexoses to sucrose This mayinhibit cell division in the developing embryoendosperm re-sulting in weak sink intensity and may ultimately lead to fruitabortion (Andersen et al 2002)

In summary drought stress not only limits the size of thesource and sink tissues but the phloem loading assimilatetranslocation and dry matter portioning are also impairedHowever the extent of effects varies with the plant speciesstage duration and severity of drought

26 Respiration

Drought tolerance is a cost-intensive phenomenon as a con-siderable quantity of energy is spent to cope with it The frac-tion of carbohydrate that is lost through respiration determinesthe overall metabolic efficiency of the plant (Davidson et al2000) The root is a major consumer of carbon fixed in pho-tosynthesis and uses it for growth and maintenance as wellas dry matter production (Lambers et al 1996) Plant growthand developmental processes as well as environmental condi-tions affect the size of this fraction (ie utilized in respiration)However the rate of photosynthesis often limits plant growthwhen soil water availability is reduced (Huang and Fu 2000)A negative carbon balance can occur as a result of diminishedphotosynthetic capacity during drought unless simultaneousand proportionate reductions in growth and carbon consump-tion take place

In wheat depending on the growth stage cultivar and nu-tritional status more than 50 of the daily accumulated pho-tosynthates were transported to the root and around 60 ofthis fraction was respired (Lambers et al 1996) Drought-sensitive spring wheat (Longchun 8139ndash2) used a relativelygreater amount of glucose to absorb water especially in se-vere drought stress (Liu et al 2004) Severe drought reducedthe shoot and root biomass photosynthesis and root respira-tion rate Limited root respiration and root biomass under se-vere soil drying can improve growth and physiological activ-ity of drought-tolerant wheat which is advantageous over adrought-sensitive cultivar in arid regions (Liu and Li 2005)

There are two mitochondrial electron transport pathwaysfrom ubiquinone to oxygen in plants The alternative pathwaybranches from the cytochrome pathway and donates electronsto oxygen directly by alternative oxidase (Moore and Siedow

O2-e- e-

O23- O-

H2OWater

2H+ H+

OHHydroxylradical

e-3O2 O2-

H2OWater

Oxide ion

Oxeneion

Peroxideion

Superoxideradical ionDioxygen

Hydrogen peroxide

H2OPerhydroxylradical

Singlet oxygen

Figure 4 Generation of reactive oxygen species by energy transferor sequential univalent reduction of ground state triplet oxygen (Apeland Hirt 2004 reproduced with permission)

1991) The alternative pathway is not coupled with adenosinetriphosphate synthesis but can be induced in response to stressor inhibition of the main electron transfer pathway (Wagnerand Moore 1997) When plants are exposed to drought stressthey produce reactive oxygen species which damage mem-brane components (Blokhina et al 2003) In this regard al-ternative oxidase activity could be useful in maintaining nor-mal levels of metabolites and reduce reactive oxygen speciesproduction during stress Oxygen uptake by sugar beet wascharacterized by a high rate distinct cytochrome oxidase-dependent terminal oxidation and up to 80 inhibition of res-piration in the presence of 05 mM potassium cyanide At anearly drought stage (10 days) a decrease in the activity of thecytochrome-mediated oxidation pathway was largely counter-balanced by the activation of mitochondrial alternative oxi-dase whereas long-term dehydration of plants was accompa-nied by activation of additional oxidative systems insensitiveto both potassium cyanide and salicylhydroxamate (Shugaevaet al 2007) In summary water deficit in the rhizosphere leadsto an increased rate of root respiration leading to an imbal-ance in the utilization of carbon resources reduced productionof adenosine triphosphate and enhanced generation of reactiveoxygen species

27 Oxidative damage

Exposure of plants to certain environmental stresses quiteoften leads to the generation of reactive oxygen species in-cluding superoxide anion radicals (Ominus2 ) hydroxyl radicals(OH) hydrogen peroxide (H2O2) alkoxy radicals (RO) andsinglet oxygen (O1

2) (Munneacute-Bosch and Penuelas 2003) Re-active oxygen species may react with proteins lipids and de-oxyribonucleic acid causing oxidative damage and impairingthe normal functions of cells (Foyer and Fletcher 2001) Manycell compartments produce reactive oxygen species of thesechloroplasts are a potentially important source because excitedpigments in thylakoid membranes may interact with O2 toform strong oxidants such as Ominus2 or O1

2 (Niyogi 1999 Reddyet al 2004) Further downstream reactions produce other reac-tive oxygen species such as H2O2 and OHminus (Fig 4) The inter-action of O2 with reduced components of the electron transportchain in mitochondria can lead to reactive oxygen species for-mation (Moumlller 2001) and peroxisomes produce H2O2 when

192 M Farooq et al

glycolate is oxidized into glyoxylic acid during photorespira-tion (Fazeli et al 2007)

Mechanisms for the generation of reactive oxygen speciesin biological systems are represented by both non-enzymaticand enzymatic reactions The partition between these twopathways under oxygen deprivation stress can be regulatedby the oxygen concentration in the system In non-enzymaticreactions electron O2 reduction can occur at higher oxygenconcentrations (Apel and Hirt 2004) At very low O2 concen-trations plant terminal oxidases and the formation of reactiveoxygen species via the mitochondrial electron transport chainstill remain functional Among enzymatic sources of reactiveoxygen species xanthine oxidase an enzyme responsible forthe initial activation of O2 should be mentioned The elec-tron donor xanthine oxidase can use xanthine hypoxanthineor acetaldehyde while the latter has been shown to accumu-late under oxygen deprivation (Pfister-Sieber and Braendle1994 Apel and Hirt 2004) This can represent a possiblesource for hypoxia-stimulated reactive oxygen species produc-tion (Fig 4) The next enzymatic step is the dismutation ofthe superoxide anion by superoxide dismutase to yield H2O2(Lamb and Dixon 1997) Peroxidases and catalases also playan important role in the fine regulation of reactive oxygenspecies in the cell through activation and deactivation of H2O2(Sairam et al 2005) Several apoplastic enzymes may alsogenerate reactive oxygen species under normal and stressfulconditions Other oxidases responsible for the two-electrontransfer to dioxygen (amino acid oxidases and glucose oxi-dase) can contribute to H2O2 accumulation (Apel and Hirt2004)

Reactive oxygen species are formed as by-products in theelectron transport chains of chloroplasts (Apel and Hirt 2004)mitochondria and the plasma membrane (Sairam et al 2005)The plant mitochondrial electron transport chain with itsredox-active electron carriers is considered as the most prob-able candidate for intracellular reactive oxygen species for-mation Mitochondria can produce reactive oxygen speciesdue to the electron leakage at the ubiquinone site ndash theubiquinonecytochrome b region (Gille and Nohl 2001) ndashand at the matrix side of complex I (NADH dehydrogenase)(Moumlller 2001)

Superoxide radical and its reduction product H2O2 arepotentially toxic compounds and can also combine by theHaber-Weiss reaction to form the highly toxic OHminus (Sairamet al 1998) Many reports show the deleterious effects of re-active oxygen species whose production is stimulated underwater stress (Blokhina et al 2003) Reactive oxygen speciescause lipid peroxidation and consequently membrane injuriesprotein degradation and enzyme inactivation (Sairam et al2005) Oxidative stress may also cause protein oxidationwith a loss of enzyme activity and the formation of protease-resistant cross-linked aggregates (Berlett and Stadtman 1997)Oxidatively-damaged proteins accumulate in pea leaves sub-jected to moderate water stress (Moran et al 1994)

Overall the production of reactive oxygen species is lin-ear with the severity of drought stress which leads to en-hanced peroxidation of membrane lipids and degradation ofnucleic acids and both structural and functional proteins

Various organelles including chloroplasts mitochondria andperoxisomes are the seats as well as first target of reactive oxy-gen species produced under drought stress

3 DROUGHT RESISTANCE MECHANISMS

Plants respond and adapt to and survive under droughtstress by the induction of various morphological biochemi-cal and physiological responses Drought tolerance is definedas the ability to grow flower and display economic yield un-der suboptimal water supply Drought stress affects the waterrelations of plants at cellular tissue and organ levels causingspecific as well as unspecific reactions damage and adaptationreactions (Beck et al 2007) To cope with the drought tol-erant plants initiate defense mechanisms against water deficit(Chaves and Oliveira 2004) which need to be investigated infurther detail (Zhou et al 2007) In the following sectionsmechanisms of drought tolerance at different levels are pre-sented

31 Morphological mechanisms

Plant drought tolerance involves changes at whole-planttissue physiological and molecular levels Manifestation of asingle or a combination of inherent changes determines theability of the plant to sustain itself under limited moisture sup-ply An account of various morphological mechanisms opera-tive under drought conditions is given below

311 Escape

Escape from drought is attained through a shortened life cy-cle or growing season allowing plants to reproduce before theenvironment becomes dry Flowering time is an important traitrelated to drought adaptation where a short life cycle can leadto drought escape (Araus et al 2002) Crop duration is inter-actively determined by genotype and the environment and de-termines the ability of the crop to escape from climatic stressesincluding drought (Dingkuhn and Asch Dingkuhn) Matchinggrowth duration of plants to soil moisture availability is criti-cal to realize high seed yield (Siddique et al 2003) Droughtescape occurs when phenological development is successfullymatched with periods of soil moisture availability where thegrowing season is shorter and terminal drought stress predom-inates (Araus et al 2002) In field-grown clones of robustacoffee leaf shedding in response to drought stress occurredsequentially from older to younger leaves suggesting that themore drought-sensitive the clone the greater the extent of leafshedding (DaMatta 2004)

Time of flowering is a major trait of a crop adaptation tothe environment particularly when the growing season is re-stricted by terminal drought and high temperatures Develop-ing short-duration varieties has been an effective strategy forminimizing yield loss from terminal drought as early maturityhelps the crop to avoid the period of stress (Kumar and Abbo

2001) However yield is generally correlated with the lengthof crop duration under favorable growing conditions and anydecline in crop duration below the optimum would tax yield(Turner et al 2001)

312 Avoidance

Drought avoidance consists of mechanisms that reduce wa-ter loss from plants due to stomatal control of transpirationand also maintain water uptake through an extensive and pro-lific root system (Turner et al 2001 Kavar et al 2007) Theroot characters such as biomass length density and depth arethe main drought avoidance traits that contribute to final yieldunder terminal drought environments (Subbarao et al 1995Turner et al 2001) A deep and thick root system is helpfulfor extracting water from considerable depths (Kavar et al2007)

Glaucousness or waxy bloom on leaves helps with mainte-nance of high tissue water potential and is therefore consid-ered as a desirable trait for drought tolerance (Richards et al1986 Ludlow and Muchow 1990) Varying degrees of glau-cousness in wheat led to increased water-use efficiency but didnot affect total water use or harvest index Determination ofleaf temperature indicated that compared with non-glaucousleaves glaucous leaves were 07 C cooler and had a lowerrate of leaf senescence (Richards et al 1986) These authorssuggested that a 05 C reduction in leaf temperature for sixhours per day was sufficient to extend the grain-filling periodby more than three days However yield advantages are likelyto be small as many varieties already show some degree ofglaucousness

313 Phenotypic flexibility

Plant growth is greatly affected by water deficit At a mor-phological level the shoot and root are the most affected andboth are the key components of plant adaptation to droughtPlants generally limit the number and area of leaves in re-sponse to drought stress just to cut down the water budget atthe cost of yield loss (Schuppler et al 1998) Since roots arethe only source to acquire water from soil the root growth itsdensity proliferation and size are key responses of plants todrought stress (Kavar et al 2007)

It has long been established that plants bearing smallleaves are typical of xeric environments Such plants withstanddrought very well albeit their growth rate and biomass arerelatively low (Ball et al 1994) Leaf pubescence is a xero-morphic trait that helps protect the leaves from excessive heatload Hairy leaves have reduced leaf temperatures and tran-spiration (Sandquist and Ehleringer 2003) whilst inter- andintra-specific variation exists for the presence of this trait Un-der high temperature and radiation stress hairiness increasesthe light reflectance and minimizes water loss by increasingthe boundary layer resistance to water vapor movement awayfrom the leaf surface Although drought stress also induces the

production of trichomes on both sides of wheat leaves theyhad no significant influence on boundary layer resistance

The water content in drought-treated mature stems declinedby 4 and water potential by ndash025 MPa It is shown thatactive phloem supply of assimilates and associated water re-serves from mature stems was the mechanism that alloweddeveloping stems of Hylocereus undatus to maintain growthunder drought conditions (Nerd and Neumann 2004) More-over girdling the phloem of growing stems rapidly inhibitedstem elongation but secretion of sucrose-containing nectarwas maintained during drought The water potential gradientwas in the wrong direction for xylem transport from matureto young growing stems and axial hydraulic conductivity waslow to negligible (Nerd and Neumann 2004)

Roots are the key plant organ for adaptation to drought Iftolerance is defined as the ability to maintain leaf area andgrowth under prolonged vegetative stage stress the main basisof variation appears to be constitutive root system architecturethat allows the maintenance of more favorable plant water sta-tus (Nguyen et al 1997) The possession of a deep and thickroot system allowed access to water deep in the soil whichwas considered important in determining drought resistance inupland rice (Kavar et al 2007) Evidence suggests that it isquality ie the distribution and structure and not quantity ofroots that determines the most efficient strategy for extractingwater during the crop-growing season (Fig 5) The droughttolerance of tea onion and cotton was increased by improvedroot growth and root functioning Selection for a deep and ex-tensive root system has been advocated to increase productiv-ity of food legumes under moisture-deficit conditions as it canoptimize the capacity to acquire water (Subbarao et al 1995)

Studies carried out on the effects of alleles of the wheatshoot dwarfing genes on root-shoot dry matter partitioningand drought resistance revealed that cultivars possessing thereduced height gene 1 and reduced height gene 2 gibberellin-insensitive dwarfing genes were more susceptible to droughtstress than reduced height gene 1 and reduced height gene2 tall cultivars (Miralles et al 1997) The semi-dwarfing genesreduced height gene 1 and reduced height gene 2 resulted ingreater root biomass at anthesis due to increased thickeningof existing roots using surplus assimilates arising from the re-stricted stem growth Thus the benefit of greater assimilatesavailable for root growth was not expressed as more extensiveor deeper root growth Differences have also been observed inthe adaptive response of root distribution to soil drying (Liuet al 2004)

To summarize plants may escape drought stress by cuttingshort their growth duration and avoid the stress with the main-tenance of high tissue water potential either by reducing wa-ter loss from plants or improved water uptake or both Someplants may reduce their surface area either by leaf shedding orproduction of smaller leaves

32 Physiological mechanisms

Osmotic adjustment osmoprotection antioxidation and ascavenging defense system have been the most important

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Nip sl 13 sl 34 sl 45 sl 50

Well-watered

Drought stress

Figure 5 Root growth and proliferation under well-watered and drought stress conditions in various rice genotypes Different rice genotypes(Nip sl 13 sl 34 sl 45 sl 50) were grown under continuous flooded conditions (well-watered) and 15 soil moisture contents (drought stress)The study was conducted in root boxes The figure shows root proliferation 38 days after seeding (courtesy Ms Mana Kano)

bases responsible for drought tolerance The physiological ba-sis of genetic variation in drought response is not clear inpart because more intricate mechanisms have been suggestedSome of these mechanisms are described below

321 Cell and tissue water conservation

Under drought stress sensitive pea genotypes were more af-fected by a decline in relative water content than tolerant ones(Upreti et al 2000) In faba bean determination of leaf waterpotential was useful for describing the drought effect but wasnot suitable for discriminating tolerant from sensitive geno-types This suggested that water potential was not the definingfeature of the tolerance (Riccardi et al 2001) Neverthelessother studies opined that determination of leaf water status inthe morning and water content in leaves in the afternoon werepotentially useful for screening drought tolerance in chickpea(Pannu et al 1993)

Osmotic adjustment allows the cell to decrease osmotic po-tential and as a consequence increases the gradient for waterinflux and maintenance of turgor Improved tissue water statusmay be achieved through osmotic adjustment andor changesin cell wall elasticity This is essential for maintaining physi-ological activity for extended periods of drought (Kramer andBoyer 1995) Wild melon plant survived drought by main-taining its water content without wilting of leaves even un-der severe drought Drought stress in combination with strong

light led to an accumulation of high concentrations of cit-rulline glutamate and arginine in leaves of wild watermelonThe accumulation of citrulline and arginine may be related tothe induction of dopamine receptor interacting protein gene 1a homologue of the acetylornithine deacetylase gene in Es-cherichia coli where it functions to incorporate the carbonskeleton of glutamate into the urea cycle (Yokota et al 2002)

It has been identified that among various mechanisms os-motic adjustment abscisic acid and induction of dehydrinsmay confer tolerance against drought injuries by maintaininghigh tissue water potential (Turner et al 2001) With the ac-cumulation of solutes the osmotic potential of the cell is low-ered which attracts water into the cell and helps with turgormaintenance The maintenance of turgor despite a decrease inleaf water volume is consistent with other studies of specieswith elastic cell walls Osmotic adjustment helps to maintainthe cell water balance with the active accumulation of solutesin the cytoplasm thereby minimizing the harmful effects ofdrought (Morgan 1990) Osmotic adjustment is an importanttrait in delaying dehydrative damage in water-limited environ-ments by continued maintenance of cell turgor and physiologi-cal processes (Taiz and Zeiger 2006) The osmotic adjustmentalso facilitates a better translocation of pre-anthesis carbohy-drate partitioning during grain filling (Subbarao et al 2000)while high turgor maintenance leads to higher photosyntheticrate and growth (Ludlow and Muchow 1990 Subbarao et al2000)

Abiotic stresses(Drought salinity heat chilling)

Proteins Lipids DNA

ROS production(1O2 H2O O2

2- H2O2)

CAT SODAPX

PODGR AA

Figure 6 Role of antioxidant enzymes in the ROS scavenging mecha-nism Exposure to abiotic stresses (including drought chilling salin-ity etc) leads to the generation of ROS including singlet oxygen(1O2) perhydroxyl radical (H2Omiddot) hydroxyl radicals (O2minus

2 ) hydro-gen peroxide (H2O2) and alkoxy radical (RO) The ROS may reactwith proteins lipids and DNA causing oxidative damage and im-pairing the normal functions of cells The antioxidant defense sys-tem in the plant cell includes both enzymatic and non-enzymaticconstituents Amongst the enzymatic components are superoxide dis-mutase catalase peroxidase ascorbate peroxidase and glutathionereductase Upon exposure to abiotic stresses tolerant cells activatetheir enzymatic antioxidant system which then starts quenching theROS and protecting the cell ROS reactive oxygen species

322 Antioxidant defense

The antioxidant defense system in the plant cell consti-tutes both enzymatic and non-enzymatic components En-zymatic components include superoxide dismutase catalaseperoxidase ascorbate peroxidase and glutathione reductaseNon-enzymatic components contain cystein reduced glu-tathione and ascorbic acid (Gong et al 2005) In environmen-tal stress tolerance such as drought high activities of antioxi-dant enzymes and high contents of non-enzymatic constituentsare important

The reactive oxygen species in plants are removed by a va-riety of antioxidant enzymes andor lipid-soluble and water-soluble scavenging molecules (Hasegawa et al 2000) theantioxidant enzymes being the most efficient mechanismsagainst oxidative stress (Farooq et al 2008) Apart from cata-lase various peroxidases and peroxiredoxins four enzymesare involved in the ascorbate-glutathione cycle a pathwaythat allows the scavenging of superoxide radicals and H2O2(Fig 6) These include ascorbate peroxidase dehydroascor-bate reductase monodehydroascorbate reductase and glu-tathione reductase (Fazeli et al 2007) Most of the ascorbate-glutathione cycle enzymes are located in the cytosol stroma ofchloroplasts mitochondria and peroxisomes (Jimeacutenez et al1998) Ascorbate peroxidase is a key antioxidant enzyme in

plants (Orvar and Ellis 1997) whilst glutathione reductasehas a central role in maintaining the reduced glutathione poolduring stress (Pastori et al 2000) Two glutathione reduc-tase complementary deoxyribonucleic acids have been iso-lated one type encoding the cytosolic isoforms (Stevens et al2000) and the other encoding glutathione reductase proteinsdual-targeted to both chloroplasts and mitochondria in differ-ent plants (Chew et al 2003)

Among enzymatic mechanisms superoxide dismutaseplays an important role and catalyzes the dismutation of twomolecules of superoxide into O2 and H2O2 the first step in re-active oxygen species scavenging systems Lima et al (2002)from a study utilizing two rapidly drought-stressed clones ofCoffea canephora proposed that drought tolerance might orat least in part be associated with enhanced activity of antiox-idant enzymes In contrast Pinheiro et al (2004) did not finda link between protection against oxidative stress and droughttolerance when four clones of C canephora were subjected tolong-term drought

Carotenoids and other compounds such as abietane diter-penes have received little attention despite their capacity toscavenge singlet oxygen and lipid peroxy-radicals as well asto inhibit lipid peroxidation and superoxide generation un-der dehydrative forces (Deltoro et al 1998) The transcript ofsome of the antioxidant genes such as glutathione reductase orascorbate peroxidase was higher during recovery from a waterdeficit period and appeared to play a role in the protection ofcellular machinery against damage by reactive oxygen species(Ratnayaka et al 2003) A superoxide radical has a half-life ofless than 1 sec and is rapidly dismutated by superoxide dismu-tase into H2O2 a product that is relatively stable and can bedetoxified by catalase and peroxidase (Apel and Hirt 2004)These metalloenzymes constitute an important primary line ofdefense of cells against superoxide free radicals generated un-der stress conditions Therefore increased superoxide dismu-tase activity is known to confer oxidative stress tolerance (Panet al 2006)

Oxidative damage in the plant tissue is alleviated by aconcerted action of both enzymatic and non-enzymatic an-tioxidant systems These include β-carotenes ascorbic acidα-tocopherol reduced glutathione and enzymes including su-peroxide dismutase peroxidase ascorbate peroxidase cata-lase polyphenol oxidase and glutathione reductase (Hasegawaet al 2000 Prochazkova et al 2001) Carotenes form a keypart of the plant antioxidant defense system (Havaux 1998Wahid 2007) but they are very susceptible to oxidative de-struction The β-carotene present in the chloroplasts of allgreen plants is exclusively bound to the core complexes ofphotosystem I and photosystem II Protection against damag-ing effects of reactive oxygen species at this site is essentialfor chloroplast functioning Here β-carotene in addition tofunctioning as an accessory pigment acts as an effective an-tioxidant and plays a unique role in protecting photochemi-cal processes and sustaining them (Havaux 1998) A majorprotective role of β-carotene in photosynthetic tissue may bethrough direct quenching of triplet chlorophyll which pre-vents the generation of singlet oxygen and protects from ox-idative damage

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323 Cell membrane stability

Biological membranes are the first target of many abioticstresses It is generally accepted that the maintenance of in-tegrity and stability of membranes under water stress is amajor component of drought tolerance in plants (Bajji et al2002) Cell membrane stability reciprocal to cell membraneinjury is a physiological index widely used for the evalua-tion of drought tolerance (Premachandra et al 1991) More-over it is a genetically related phenomenon since quantita-tive trait loci for this have been mapped in drought-stressedrice at different growth stages (Tripathy et al 2000) Dhandaet al (2004) showed that membrane stability of the leaf seg-ment was the most important trait to screen the germplasm fordrought tolerance

Cell membrane stability declined rapidly in Kentucky blue-grass exposed to drought and heat stress simultaneously(Wang and Huang 2004) In a study on maize K nutri-tion improved the drought tolerance mainly due to improvedcell membrane stability (Gnanasiri et al 1991) Tolerance todrought evaluated as increase in cell membrane stability underwater deficit conditions was differentiated between cultivarsand correlated well with a reduction in relative growth rateunder stress (Premachandra et al 1991) In holm oak (Quer-cus ilex) seedlings hardening increased drought tolerance pri-marily by reducing osmotic potential and stomatal regulationimproved new root growth capacity and enhanced cell mem-brane stability Among treated seedlings the greatest responseoccurred in seedlings subjected to moderate hardening Vari-ation in cell membrane stability stomatal regulation and rootgrowth capacity was negatively related to osmotic adjustment(Villar-Salvador et al 2004)

The causes of membrane disruption are unknown notwith-standing a decrease in cellular volume causes crowding andincreases the viscosity of cytoplasmic components This in-creases the chances of molecular interactions that can causeprotein denaturation and membrane fusion For model mem-brane and protein systems a broad range of compounds havebeen identified that can prevent such adverse molecular inter-actions Some of these are proline glutamate glycinebetainecarnitine mannitol sorbitol fructans polyols trehalose su-crose and oligosaccharides (Folkert et al 2001) Another pos-sibility of ion leakage from the cell may be due to thermal-induced inhibition of membrane-bound enzymes responsiblefor maintaining chemical gradients in the cell (Reynolds et al2001) Arabidopsis leaf membranes appeared to be very resis-tant to water deficit as shown by their capacity to maintainpolar lipid contents and the stability of their composition un-der severe drought (Gigon et al 2004)

324 Plant growth regulators

Plant growth regulators when applied externally and phy-tohormones when produced internally are substances that in-fluence physiological processes of plants at very low concen-trations (Morgan 1990) Both these terms have been used

interchangeably particularly when referring to auxins gib-berellins cytokinins ethylene and abscisic acid (Taiz andZeiger 2006) Under drought endogenous contents of auxinsgibberellins and cytokinin usually decrease while those of ab-scisic acid and ethylene increase (Nilsen and Orcutte 1996)Nevertheless phytohormones play vital roles in drought toler-ance of plants

Auxins induce new root formation by breaking root api-cal dominance induced by cytokinins As a prolific root sys-tem is vital for drought tolerance auxins have an indirectbut key role in this regard Drought stress limits the pro-duction of endogenous auxins usually when contents of ab-scisic acid and ethylene increase (Nilsen and Orcutte 1996)Nevertheless exogenous application of indole-3-yl-acetic acidenhanced net photosynthesis and stomatal conductance in cot-ton (Kumar et al 2001) Indole-3-butyric acid is a naturallyoccurring auxin Drought stress and abscisic acid applicationenhance indole-3-butyric acid synthesis in maize Recentlyit was revealed that Indole-3-butyric acid synthetase fromArabidopsis is also drought-inducible (Ludwig-Muumlller 2007)Experiments with indole-3-yl-acetic acid and ethylene glycoltetra-acetic acid suggested that calcium and auxin participatein signaling mechanisms of drought-induced proline accumu-lation (Sadiqov et al 2002)

Drought rhizogenesis is an adaptive strategy that occursduring progressive drought stress and is reported from Bras-sicaceae and related families by the formation of short tuber-ized hairless roots These roots are capable of withstandinga prolonged drought period and give rise to a new functionalroot system upon rehydration The drought rhizogenesis washighly increased in the gibberrelic acid biosynthetic mutantga5 suggesting that some gibberrelic acids might also partic-ipate in this process (Vartanian et al 1994)

Abscisic acid is a growth inhibitor and produced under awide variety of environmental stresses including drought Allplants respond to drought and many other stresses by accumu-lating abscisic acid Abscisic acid is ubiquitous in all floweringplants and is generally recognized as a stress hormone that reg-ulates gene expression and acts as a signal for the initiation ofprocesses involved in adaptation to drought and other environ-mental stresses (Fig 7) It has been proposed that abscisic acidand cytokinin have opposite roles in drought stress Increasein abscisic acid and decline in cytokinins levels favor stomatalclosure and limit water loss through transpiration under waterstress (Morgan 1990) When plants wilt abscisic acid levelstypically rise as a result of increased synthesis (Taylor 1991)Increased abscisic acid concentration leads to many changesin development physiology and growth Abscisic acid altersthe relative growth rates of various plant parts such as increasein the root-to-shoot dry weight ratio inhibition of leaf area de-velopment and production of prolific and deeper roots (Sharpet al 1994) It triggers the occurrence of a complex seriesof events leading to stomatal closure which is an importantwater-conservation response (Turner et al 2001) In a studyon genetic variation for abscisic acid accumulation in ricea consistent negative relationship between the ability of de-tached and partially dehydrated leaves to accumulate abscisicacid and leaf weight was established (Ball et al 1994) By its

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

MitochondriaChloroplast

Changes in gene expression protein

enzyme abundance and regulation

Antioxidant activationde novo synthesis

Proline Glycinebetaine

accumulation

Stomatal closure

Transcription factors

Drought tolerance

Figure 7 Proposed cellular events and signaling cascades in a plantcell responding to drought stress Drought stress is perceived by anunknown mechanism which then activates the signaling cascadesplausibly by abcissic acid (ABA) hydrogen peroxide (H2O2) and cal-cium (Ca+2) These cascades then activate the synthesis of specificprotein kinases which activate more downstream responses such aschanges in gene expression The response to these signaling cascadesalso results in changes in plant metabolism including activation andsynthesis of antioxidants synthesis and accumulation of osmoprotec-tants and solutes and stomatal closure under acute drought stress

effect in closing stomata abscisic acid can control the rateof transpiration and to some extent may be involved in themechanism conferring drought tolerance in plants

Abscisic acid induces expression of various water stress-related genes In a recent study Zhang et al (2005) reporteda regulatory role of telomeric repeat binding factor gene 1 inabscisic acid sensitivity and drought response during seedlingdevelopment Bray (1997) suggested the existence of abscisicacid-dependent and abscisic acid-independent transductioncascades and pathways to act as a signal of drought stress andthe expression of specific water stress-induced genes Abscisicacid produces such changes that confer an ability to maintaincellular turgor to withstand dehydrative forces (Fig 7)

Ethylene has long been considered a growth inhibitoryhormone although it is involved in environmentally drivengrowth inhibition and stimulation (Taiz and Zeiger 2006) Theresponse of cereals to drought includes loss of leaf functionand premature onset of senescence in older leaves Ethylenemay serve to regulate leaf performance throughout its lifespanas well as to determine the onset of natural senescence and me-diate drought-induced senescence (Young et al 2004) Recentstudies suggest that growth promotion is a common feature inethylene responses To escape this adversity plants can opti-mize growth and tolerate abiotic stresses such as drought andthis response also involves ethylene synthesis (Pierik et al2007)

Among the other endogenously produced growth regulatingfactors the role of salicylic acid in the induction of toleranceagainst several abiotic stresses has been emphasized recentlyIn the case of drought tolerance the role of endogenously

produced salicylic acid is still enigmatic Salicylic acid po-tentiates the generation of reactive oxygen species in photo-synthetic tissues of Arabidopsis thaliana during osmotic stress(Borsani et al 2001)

Polyamines are known to have profound influence on plantgrowth and development Being cationic polyamines can as-sociate with anionic components of the membrane such asphospholipids thereby protecting the lipid bilayer from dete-riorating effects of stress (Bouchereau et al 1999) There hasbeen a growing interest in the study of polyamine participationin the defense reaction of plants against environmental stressesand extensive research efforts have been made in the last twodecades (Bouchereau et al 1999 Kasukabe et al 2004)Many genes for enzymes involved in polyamine metabolismhave been cloned from several species and their expressionunder several stress conditions has been analyzed For exam-ple the apple spermidine synthase gene when overexpressedencodes high levels of spermidine synthase which substan-tially improves abiotic stress tolerance including drought (Wenet al 2007)

Among various polyamines a rise in the putrescence levelis generally due to an enhanced arginine decarboxylase activ-ity (Bouchereau et al 1999) Compared with sensitive plantsstress-tolerant plants generally have a greater capacity to syn-thesize polyamines in response to stress resulting in a two-to three fold rise in endogenous polyamine levels over theunstressed ones (Kasukabe et al 2004) Recent studies sug-gested that rice has a great capacity to enhance polyaminebiosynthesis particularly spermidine and spermine in freeform and putrescence in insoluble-conjugated form in leavesearlier in response to drought stress This was considered as animportant physiological trait of drought tolerance in rice (Yanget al 2007)

325 Compatible solutes and osmotic adjustment

One of the most common stress tolerance strategies inplants is the overproduction of different types of compatibleorganic solutes (Serraj and Sinclair 2002) Compatible solutesare low-molecular-weight highly soluble compounds that areusually nontoxic even at high cytosolic concentrations Gen-erally they protect plants from stress through different meanssuch as contribution towards osmotic adjustment detoxifica-tion of reactive oxygen species stabilization of membranesand native structures of enzymes and proteins (Fig 8)

Osmotic adjustment is a mechanism to maintain water re-lations under osmotic stress It involves the accumulation of arange of osmotically active moleculesions including solublesugars sugar alcohols proline glycinebetaine organic acidscalcium potassium chloride ions etc Under water deficit andas a result of solute accumulation the osmotic potential of thecell is lowered which attracts water into the cell and helpswith the maintenance of turgor By means of osmotic adjust-ment the organelles and cytoplasmic activities take place atabout a normal pace and help plants to perform better in termsof growth photosynthesis and assimilate partitioning to grainfilling (Ludlow and Muchow 1990 Subbarao et al 2000) As

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

Destabilising molecule

Figure 8 Role of compatible solutes in drought tolerance In the hy-drated state the presence of water reduces the interaction of desta-bilizing molecules (a) in tolerant cells the synthesis of compatiblesolutes preferentially excludes the binding of destabilizing moleculesand stabilizes native protein conformation (b) and in sensitive cellsthe lack of compatible solutes results in the preferential binding ofdestabilizing molecules to the protein surface leading to degradation(c) (Adapted from Hoekstra et al 2001)

a mechanism osmotic adjustment has been suggested as animportant trait in postponing the dehydration stress in water-scarce environments (Morgan 1990) Variation in osmotic ad-justment among chickpea cultivars in response to soil droughthas been observed and seed yield of chickpea was corre-lated with the degree of osmotic adjustment when grown un-der a line-source irrigation system in the field (Moinuddin andKhannu-Chopra 2004) Contrarily Serraj and Sinclair (2002)found no yield advantage from osmotic adjustment in anycrop Nevertheless further investigations are imperative to es-tablish this controversy

As mentioned above osmotic adjustment is accomplishedwith the accumulation of compatible solutes Of these prolineis one amongst the most important cytosolutes and its free ac-cumulation is a widespread response of higher plants algaeanimals and bacteria to low water potential (Zhu 2002 Wahidand Close 2007) Its synthesis in leaves at low water potentialis caused by a combination of increased biosynthesis and slowoxidation in mitochondria Despite some controversy manyphysiological roles have been assigned to free proline includ-ing stabilization of macromolecules a sink for excess reduc-tant and a store of carbon and nitrogen for use after reliefof water deficit (Zhu 2002) Proline contents were increasedunder drought stress in pea cultivars (Alexieva et al 2001)Drought-tolerant petunia (Petunia hybrida) varieties were re-ported to accumulate free proline under drought that actedas an osmoprotectant and induced drought tolerance (Yamadaet al 2005)

Glycinebetaine (N N N-trimethyl glycine) is one of themost extensively studied quaternary ammonium compoundsand compatible solutes in plants animals and bacteria (Wahidet al 2007) Many studies demonstrate that glycinebetaineplays an important role in enhancing plant tolerance under a

range of abiotic stresses including drought (Quan et al 2004)The introduction of genes synthesizing glycinebetaine intonon-accumulators of glycinebetaine proved to be effective inincreasing tolerance to various abiotic stresses (Sakamoto andMurata 2002) Naidu et al (1998) reported that cotton cul-tivars adapted to water stress conditions accumulated higherglycinebetaine than the non-adapted ones under drought Inaddition to direct protective roles of glycinebetaine eitherthrough positive effects on enzyme and membrane integrityor as an osmoprotectant glycinebetaine may also protect cellsfrom environmental stresses indirectly by participating in sig-nal transduction pathways (Subbarao et al 2000)

Citrulline named after Citrullus a Latin name of water-melon from which it was isolated is an amino acid Althoughnot built into proteins during their synthesis and not encodedby a nuclear gene several proteins are known to contain cit-rulline (Kawasaki et al 2000) Wild watermelon (Citrulluslanatus) has the ability to adapt to severe drought stress despitecarrying out normal C3-type photosynthesis which seem to becorrelated with citrulline accumulation (Akashi et al 2001)Wild watermelon primarily accumulated citrulline followed byglutamate and arginine in place of proline and glycinebetaine(Kawasaki et al 2000) Yokota et al (2002) reported a highercitrulline accumulation in the wild watermelon leaves assum-ing that citrulline is located only in the cytosol and constitutes5 of the total volume of the mesophyll cells Citrulline is anovel and the most effective OHminus scavenger among compati-ble solutes examined so far Moreover it can effectively pro-tect DNA and enzymes from oxidative injuries (Akashi et al2001 Bektasoglu et al 2006)

Rapid accumulation of the non-protein amino acidγ-aminobutyric acid was identified in plant tissues upon ex-posure to stress many years ago γ-aminobutyric acid acts asa zwitterion exists in free form and has a flexible moleculethat can assume several conformations in solution includinga cyclic structure that is similar to proline At physiologicalpH γ-aminobutyric acid is highly water-soluble (Shelp et al1999) and may function as a signaling molecule in higherplants under stress (Serraj et al 1998) The physiological rolesof γ-aminobutyric acid in drought tolerance entail osmotic reg-ulation (Shelp et al 1999) detoxication of reactive oxygenradicals conversion of putrescine into proline and intracellu-lar signal transduction (Kinnersley and Turano 2000)

Drought stress initiates a signal transduction pathway inwhich increased cytosolic Ca2+ activates Ca2+calmodulin-dependent glutamate decarboxylase activity leading toγ-aminobutyric acid synthesis (Shelp et al 1999) ElevatedH+ and substrate levels can also stimulate glutamate decar-boxylase activity leading primarily to γ-aminobutyric acidaccumulation Experimental evidence supports the involve-ment of γ-aminobutyric acid in pH regulation nitrogen stor-age plant development and defense as well as a compatibleosmolyte and an alternative pathway for glutamate utiliza-tion (Shelp et al 1999 Wahid et al 2007) After droughtstress the content of proline was more than 50 and at theend of recovery the γ-aminobutyric acid content reached 27(Simon-sarkadi et al 2006)

Trehalose is a non-reducing disaccharide of glucose thatfunctions as a compatible solute in the stabilization of bio-logical structures under abiotic stress (Goddijn et al 1997) Innature trehalose is biosynthesized as a stress response by a va-riety of organisms including bacteria fungi algae insects in-vertebrates and lower plants (Wingler 2002) Capacity to pro-duce trehalose earlier thought to be absent from higher plantshas now been reported to accumulate in high amounts in somedrought-tolerant ferns the resurrection plant Selaginella lep-idophylla (Penna 2003) and desiccation-tolerant angiospermMyrothamnus flabellifolia (Drennan et al 1993) The pres-ence of low amounts of trehalose was demonstrated even in to-bacco (Goddijn et al 1997) and many higher plants (Kosmaset al 2006) Its metabolism may be channelized to enhancedrought tolerance in plants (Pilon-Smits et al 1998 Penna2003) Physiological roles of trehalose include efficient stabi-lization of dehydrated enzymes proteins and lipid membranesas well as protection of biological structures under desicca-tion stress (Wingler 2002) rather than regulating water poten-tial (Lee et al 2004) Karim et al (2007) reported that en-hanced drought tolerance by trehalose depends on improvedwater status and expression of heterologous trehalose biosyn-thesis genes during Arabidopsis root development

At a molecular level exogenously applied trehalose maytrigger the abscisic acid-insensitive 4 gene expression butdecrease sucrose induction providing a possible molecularmechanism for the trehalose effect on plant gene expressionand growth (Ramon et al 2007) Trehalose-accumulatingorganisms produce this sugar in a two-step process by theaction of the enzymes trehalose-6-phosphate synthase andtrehalose-6-phosphate phosphatase when exposed to stressImproved drought tolerance has been reported in the trans-genic plants overproducing trehalose-6-phosphate synthase inspite of minute accumulation of trehalose (Karim et al 2007)

In fact plants can withstand drought stress by conservingcell and tissue water principally by osmatic adjustment main-tenance of the antioxidant defense system for the scaveng-ing of reactive oxygen species and keeping the cell mem-branes stabilized Plant growth regulators and polyaminesγ-aminobutyric acid free amino acids and sugars also play avital role in drought tolerance by scavenging the reactive oxy-gen species stomatal regulation and protection of vital macro-molecules and maintenance of the cell water balance

33 Molecular mechanisms

Plant cellular water deficit may occur under conditions ofreduced soil water content Under these conditions changes ingene expression (up- and down-regulation) take place Variousgenes are induced in response to drought at the transcriptionallevel and these gene products are thought to function in toler-ance to drought (Kavar et al 2007) Gene expression may betriggered directly by the stress conditions or result from sec-ondary stresses andor injury responses Nonetheless it is wellestablished that drought tolerance is a complex phenomenoninvolving the concerted action of many genes (Agarwal et al2006 Cattivelli et al 2008)

331 Aquaporins

Aquaporins have the ability to facilitate and regulate pas-sive exchange of water across membranes They belong to ahighly conserved family of major intrinsic membrane proteins(Tyerman et al 2002) In plants aquaporins are present abun-dantly in the plasma membrane and in the vacuolar membraneThe structural analysis of aquaporins has revealed the gen-eral mechanism of protein-mediated membrane water trans-port Although the discovery of aquaporins in plants has re-sulted in a prototype shift in the understanding of plant waterrelations (Maurel and Chrispeels 2001) the relation betweenaquaporins and plant drought resistance is still elusive (Aharonet al 2003) Nevertheless it is believed that they can regu-late the hydraulic conductivity of membranes and potentiate aten- to twenty-fold increase in water permeability (Maurel andChrispeels 2001)

Studies on aquaporins and plant water relations have beencarried out for many years Mercury is a potential inhibitorof aquaporins This was evident from a number of reports onmercury-induced decline in root hydraulic conductivity whichsubstantiated that aquaporins play a major role in overall rootwater uptake (Javot and Maurel 2002) and play a role incellular osmoregulation of highly compartmented root cells(Maurel et al 2002 Javot et al 2003) Reverse genetics pro-vides an elegant approach to explore aquaporin roles in plantwater relations (Kaldenhoff et al 1998) The overexpressionof the plasma membrane aquaporin in transgenic tobacco pro-gressively improved plant vigor under favorable growth condi-tions but the prolactin-inducible protein 1b gene overexpres-sion had retrogressive influence under salinity and caused fastwilting under water stress (Aharon et al 2003) Phosphory-lation (Johansson et al 1998) calcium and pH (Tournaire-Roux et al 2003) are important factors modulating aquaporinactivity

Recently efforts have been concentrated on investigatingthe function and regulation of plasma membrane intrinsic pro-tein aquaporins The aquaporins play a specific role in con-trolling transcellular water transport For instance they areabundantly expressed in roots where they mediate soil wateruptake (Javot and Maurel 2002) and transgenic plants down-regulating one or more prolactin-inducible protein genes hadlower root water uptake capacity (Javot et al 2003)

332 Stress proteins

Synthesis of stress proteins is a ubiquitous response to copewith prevailing stressful conditions including water deficitMost of the stress proteins are soluble in water and thereforecontribute towards the stress tolerance phenomena by hydra-tion of cellular structures (Wahid et al 2007) Synthesis ofa variety of transcription factors and stress proteins is exclu-sively implicated in drought tolerance (Taiz and Zeiger 2006)

Dehydration-responsive element-binding genes belongto the v-ets erythroblastosis virus repressor factor genefamily of transcription factors consisting of three sub-classes dehydration-responsive element-binding gene1 and

200 M Farooq et al

dehydration-responsive element-binding gene2 which are in-duced by cold and dehydration respectively (Choi et al2002) The dehydration-responsive element-binding genes areinvolved in the abiotic stress signaling pathway It was pos-sible to engineer stress tolerance in transgenic plants by ma-nipulating the expression of dehydration-responsive element-binding genes (Agarwal et al 2006) Introduction of anovel dehydration-responsive element-binding gene transcrip-tional factor effectively improved the drought tolerance abil-ity of groundnut (Mathur et al 2004) and rice (Yamaguchi-Shinozaki and Shinozaki 2004) After successful cloningof dehydration-responsive element-binding gene1 (Liu et al1998) many capsella bursa-pastoris-like genes have been re-ported to be synthesized in response to drought stress in var-ious plant species including rye and tomato (Jaglo et al2001) rice (Dubouzet et al 2003) wheat (Shen et al 2003)cotton (Huang and Liu 2006) brassica (Zhao et al 2006)and soybean (Chen et al 2007) Introduction of dehydration-responsive element-binding gene1A genes in transgenic tallfescue (Festuca arundinacea) showed increased drought re-sistance with the accumulation of a high level of proline Thisindicated the ability of capsella bursa-pastoris 3 to inducedrought tolerance (Zhao et al 2007) Drought stress causesmany changes in the expression levels of late embryogenesisabundantdehydrin-type genes and molecular chaperones thatprotect the cellular proteins from denaturation (Mahajan andTuteja 2005)

Heat shock proteins belong to a larger group of moleculescalled chaperones They have a role in stabilizing other pro-teinsrsquo structure Low-molecular-weight heat shock proteinsare generally produced only in response to environmentalstress particularly high temperature (Wahid et al 2007)But many heat shock proteins have been found to be in-duced by different stresses such as drought anaerobic con-ditions and low temperatures (Coca et al 1994) They arereported to serve as molecular chaperones that participate inadenosine triphosphate-dependent protein unfolding or assem-blydisassembly reactions and prevent protein denaturationduring stress (Gorantla et al 2006)

Membrane-stabilizing proteins and late embryogenic abun-dant proteins are another important protein group responsiblefor conferring drought tolerance These increase the water-binding capacity by creating a protective environment forother proteins or structures referred to as dehydrins They alsoplay a major role in the sequestration of ions that are con-centrated during cellular dehydration (Gorantla et al 2006)These proteins help to protect the partner protein from degra-dation and proteinases that function to remove denatured anddamaged proteins Dehydrins also known as a group of lateembryogenesis abundant proteins accumulate in response toboth dehydration and low temperature (Close 1997) In addi-tion to their synthesis at the desiccating stage of seed they alsoaccumulate during periods of water deficit in vegetative tis-sues These proteins are easily identifiable from their particu-lar structural features such as the highly conserved Lysine-richdomain predicted to be involved in hydrophobic interactionsleading to macromolecule stabilization (Svensson et al 2002)

333 Signaling and drought stress tolerance

General responses to stress involve signaling stress detec-tion via the redox system checkpoints arresting the cell cy-cle and deoxyribonucleic acid repair processes stimulated inresponse to deoxyribonucleic acid damage The complexityof signaling events associated with the sensing of stress andthe activation of defense and acclimation pathways is be-lieved to involve reactive oxygen species calcium calcium-regulated proteins mitogen-activated protein kinase cascadesand cross-talk between different transcription factors (Kovtunet al 2000 Chen et al 2002)

Chemical signals eg reactive oxygen species calciumand plant hormones are involved in inducing stress toler-ance by acting via transduction cascades and activate ge-nomic re-programing (Fig 7 Joyce et al 2003) Mitogen-activated protein kinases are important mediators in signaltransmission connecting the perception of external stimuli tocellular responses Mitogen-activated protein kinase cascadesare involved in signaling various stresses including drought(Wrzaczek and Hirt 2001) Calcium has been established as aubiquitous intracellular second messenger in plants Calcium-based signaling systems comprise a receptor a system for gen-erating the increase in cytosolic calcium downstream com-ponents that are capable of reacting to increased cytosoliccalcium and other cellular systems responsible for return-ing cytosolic calcium to its pre-stimulus level (Alistair andBrownlee 2004) More recently it is reported that calcium canimprove water stress tolerance in Catharanthus roseus by in-creasing γ-glutamyl kinase and reducing the proline oxidaseactivities (Abdul Jaleel et al 2007)

The calcium-dependent protein kinases in higher plant cellsare an important group of calcium sensors that decode calciumion signals in plant cells (Cheng et al 2002) As a family ofunique serinethreonine kinases in higher plants they performdiverse and important functions in plant signal transduction(Mori et al 2006) Drought stress increases the cytoplasmiccalcium level in living plant cells (Knight 2000) A num-ber of potential calcium sensors such as salt overly-sensitive3-like proteins (Zhu 2002) or Casitas B-lineage Lymphoma(Luan et al 2002) and calcium-dependent protein kinasesmay further transduce stress-induced calcium signals (Harmonet al 2000) Mishra et al (2006) also reported that signal-ing for cell division and stress responses in plants is mediatedthrough monoammonium phosphate kinases and even auxinsalso utilize a monoammonium phosphate kinase pathway forits action

A number of phospholipid systems are activated by os-motic stress generating an array of messenger moleculessome of which may function upstream of the osmotic stress-activated protein kinases Abscisic acid biosynthesis is regu-lated by osmotic stress at multiple steps Both abscisic acid-dependent and - independent osmotic stress signaling firstmodify constitutively expressed transcription factors leadingto the expression of early response transcriptional activatorswhich then activate downstream stress tolerance effector genes(Zhu 2002) Recently Wan et al (2007) reported that amongstthe 29 calcium-dependent protein kinase genes identified so

far all contained multiple stress-responsive cis-elements up-stream in the promoter region (1 kb) Sucrose non-fermenting1-related protein kinase 2 has also been reported to be capableof mediating signals initiated during drought stress resultingin appropriate gene expression (Umezawa et al 2005)

In fact various chemical signals transduced under droughtstress activate an array of genes leading to the synthesis ofproteins and metabolites conferring drought tolerance in anumber of plant species

4 MANAGING DROUGHT STRESS

Drought stress effects can be managed by production of themost appropriate plant genotypes together with adjustment ofagronomic practices (sowing time plant density and soil man-agement) This is done to ensure that sensitive crop stages oc-cur at the time when likelihood of drought is minimal Var-ious strategies of paramount importance to accomplish thisobjective may entail production of appropriate plant varietiesand improvement of the existing high-yielding varieties Ef-forts have been made to produce drought-tolerant genotypesusing the knowledge of responses of plants to drought stressand mechanisms involved as elaborated above The two mostimportant strategies may include (a) selecting the desired ma-terials as in traditional breeding using molecular and biotech-nological means including production of genetically modifiedor transgenic plants (Fig 9) and (b) inducing drought toler-ance in otherwise susceptible plants by priming and hormonalapplication An account of these efforts is elaborated below

41 Selection and breeding strategies

Conventional breeding has been based on empirical selec-tion for yield (Atlin and Lafitte 2002) However this approachis far from being optimal since yield is a quantitative traitand characterized by a low heritability and a high genotypetimes environment interaction (Babu et al 2003) It is stronglybelieved that understanding of a physiological and molecularbasis may help target the key traits that limit yield Such anapproach may complement conventional breeding programsand hasten yield improvement (Cattivelli et al 2008) More-over even the power of molecular biology for locating impor-tant gene sequences and introgressing quantitative trait loci oreven for selecting or genetically transforming important quan-titative trait loci strongly depends upon our understanding ofyield-determining physiological processes (Araus et al 2002Kirigwi et al 2007)

Screening under natural drought stress conditions in the tar-get environments is difficult because of the irregular and er-ratic drought response But screening under controlled stressenvironments and rain-out shelters is more manageable Selec-tion response in the target population of environments undernatural stress can be considered a correlated response to se-lection in the managed stress environment (Venuprasad et al2007) On the other hand classical breeding is a good ap-proach for developing drought tolerance which relies upon

Screening genotypes for drought tolerance

Developing materials for analysis

QTL analysis andGene mapping

Transgenic plants for drought tolerance

Marker-assisted selection (MAS)Gene cloning

Developing materials carrying QTL

Gene pyramiding for drought tolerance

Developing materials carrying multiple gene

Development of materials for drought tolerance

Figure 9 Developing materials for drought tolerance Under droughtstress conditions the genotypes showing drought tolerance are se-lected To analyze the genotypes for drought tolerance the materi-als for analysis are developed Using developed materials QTL anal-ysis and gene mapping are conducted For gene cloning identifiedgenes or major QTL are analyzed in detail using a large size popula-tion A cloned gene for drought tolerance is transferred into widelyadapted varieties To develop the materials carrying the gene or QTLfor drought tolerance DNA markers which linked to the gene or QTLare used for marker-assisted selection Similarly marker-assisted se-lection is used for developing the materials of gene pyramiding Genecloning marker-assisted selection and gene pyramiding are usefulfor developing the materials for drought tolerance QTL quantitativetrait locus

multi-location testing of progenies in environments represent-ing a random selection of the variation in drought stress in thetarget environment (Babu et al 2003) A modification to thisstrategy involves selection for putative drought-adaptive sec-ondary traits (Ludlow and Muchow 1990) either alone or aspart of a selection index Selection for low-transpiration typesat unchanged water-use efficiency would result in lower yieldsunder optimum conditions

In recent studies on unselected populations of doubled-haploid lines broad-sense heritability of grain yield underreproductive-stage drought stress was comparable with thatof grain yield estimated in non-stressed conditions (Atlin andLafitte 2002 Babu et al 2003 Venuprasad et al 2007) Con-siderable efforts have been targeted at the genetic analysisof secondary traits such as root system architecture leaf wa-ter potential panicle water potential osmotic adjustment andrelative water content (Jongdee et al 2002) A suitable sec-ondary trait is (1) genetically associated with grain yield un-der drought (2) highly heritable (3) stable and feasible tomeasure and (4) not associated with yield loss under idealgrowing conditions (Edmeades et al 2001) However suchtraits rarely have high broad-sense heritability like yield underdrought stress and are often not highly correlated with it (Atlinand Lafitte 2002)

202 M Farooq et al

Hampered water-use efficiency is an initial and themost common plant response to drought stress and plantspeciesvarieties show great variations for this trait Thus it isa genetically linked trait Available reports show that drought-tolerant species reduce the water loss either by reducing theleaf area or restricting stomatal opening or both (Lazaridouet al 2003 Abbate et al 2004 Lazaridou and Koutroubas2004) simultaneously with with less effect on the biomass pro-duction (Lazaridou et al 2003 Abbate et al 2004 Lazaridouand Koutroubas 2004) In the genotypes which are either un-able to adjust their organ size and reduce water loss or sustainthe biomass production under water-limited conditions water-use efficiency is substantially reduced (Costa et al 1997)Condon et al (2004) described three key processes in breed-ing to improve water-use efficiency in crop plants These in-clude (1) increasing the uptake of available water (2) im-proving biomass production per unit transpired water and(3) partitioning of produced biomass towards the harvestedproduct

42 Molecular and functional genomics approaches

For more than two decades molecular and biochemicalstudies have identified many of the abscisic acid- and stress-responsive genes and a few of the transcription factors re-sponsible for their induction in crop plants (Buchanan et al2005 Poroyko et al 2005) The products of certain stress-responsive genes could function in alleviating stress damagethrough still elusive mechanisms (Shinozaki et al 2003)

Many laboratory and field studies have shown that trans-genic expression of some of the stress-regulated genes resultsin increased tolerance to drought and other stresses Thesetransgenic approaches are currently the mainstream method tobioengineer drought tolerance in crop plants (Bahieldina et al2005) However enhanced expression of these genes is fre-quently associated with retarded growth and thus may limitits practical applications Arising from breeding or bioengi-neering the next generation of drought-tolerant crop plants re-quires better understanding of the molecular and genetic basisof drought resistance (Xiong et al 2006) In this regard rice asubmerged plant offers an excellent model for the precise un-derstanding of drought tolerance phenomena An increasingnumber of studies witnesses that rice displays early morpho-logical changes upon exposure to drought at various growthstages (Manikavelu et al 2006) Since drought tolerance isa genetically controlled phenomenon many quantitative traitloci for membrane stability and other functionally related phe-nomena genes have been characterized using bioinformaticstools (Tripathy et al 2000 Fu et al 2007)

To identify the less obvious genetic networks that respondto stress more straightforward and sensitive methods are nec-essary The advent of whole genomics and related technologiesis providing the necessary tools to identify key genes that re-spond to drought stress and relating their regulation to adaptiveevents occurring during stress (Bruce et al 2002) Differen-tial display was one of the earliest methods of parallel screen-ing for differences in the levels of complementary DNA frag-

ments generated from messenger RNA isolated from samplesbetween experimental treatments (Liang and Pardee 1992)

The progressive cloning of many stress-related genesand responsive elements and the proof of their associationwith stress-tolerant quantitative trait loci suggests that thesegenes may represent the molecular basis of stress tolerance(Cattivelli et al 2002 2008) On the other hand the identifica-tion of quantitative trait loci associated with drought toleranceis also an important tool for marker-assisted selection of desir-able plants (Fig 9) In a recent study mapping of quantitativetrait loci for grain yield and its components using a simple se-quence repeatexpressed sequence tag marker map explainedconsiderable variation in chromosome 4A of wheat (Kirigwiet al 2007) It makes clear that the combination of traditionaland molecular breeding marker-assisted selection and geneticengineering may allow a more rapid way to improve abioticstress tolerance in crops (Chaves and Oliveira 2004)

In summary to be able to prove that a transgenic plant ismore resistant to water stress than the wild type one wouldneed a rigorous evaluation of the physiological performanceas well as water status of transformed plants This will avoidambiguous interpretations of the genetic effects on drought re-sistance of plants (Chaves and Oliveira 2004)

43 Induction of drought resistance

Drought resistance can be induced by adopting variousstrategies Of these exogenous use of various growth regu-lating and other chemicals has proven worthwhile in produc-ing drought resistance at various growth stages in a number ofplants An account of these strategies is given below

431 Seed priming

One of the short-term and most pragmatic approaches toovercome the drought stress effects is seed priming Seedpriming is a technique by which seeds are partially hy-drated to a point where germination-related metabolic pro-cesses begin but radicle emergence does not occur (Farooqet al 2006) Primed seeds usually exhibit increased germi-nation rate greater germination uniformity and sometimesgreater total germination percentage (Kaya et al 2006 Farooqet al 2007) This approach has been applied to overcome thedrought stress effects in a range of crop species

Improvement of rice and other crops for growing in water-scant areas is of current interest In the newly introduced aero-bic rice culture the frequency and intensity of drought may in-crease manifold Du and Tuong (2002) while testing the effec-tiveness of different osmotica to improve the performance ofdirect-seeded rice noted that osmopriming with 4 KCl solu-tion and saturated CaHPO4 solution was successful in improv-ing the seedling emergence crop stand establishment and yieldunder stress In drought-prone areas primed rice seeds germi-nated well and seedlings emerged faster and more uniformlyleading to increased yield (Harris et al 2002) A germinationtrial of 11 varieties of upland rice under limited soil moisture

conditions revealed early and synchronized emergence owingto seed priming (Harris and Jones 1997)

Seed priming improved performance of wheat seeds underdrought stress in terms of germination and water-use efficiencyof drought-stressed plants by 44 compared with unprimedseeds (Ajouri et al 2004) The beneficial effects of primingincluded faster emergence of crop seedlings early floweringand higher grain yield even under drought stress (Kaur et al2005) In sunflower osmopriming with KNO3 and hydroprim-ing improved the germination and stand establishment understress conditions (Kaya et al 2006)

432 Use of plant growth regulators

Foliar application of plant growth regulators both naturaland synthetic has proven worthwhile for improving growthagainst a variety of abiotic stresses Drought stress alone in-hibited increases in length and fresh weight of the hypocotylwhile applied levels of gibberrelic acid reversed this effect Inthis case gibberrelic acid partially increased the water statusof the seedlings and partially sustained protein synthesis (Taizand Zeiger 2006) Exogenous application of gibberellic acidincreased the net photosynthetic rate stomatal conductanceand transpiration rate in cotton (Kumar et al 2001) and stim-ulated pollen and seed cone production in Sitka spruce (Piceasitchensis) under drought stress (Philipson 2003)

Among other hormones exogenous application of1-aminocyclopropane-1-carboxylic acid also improvesdrought tolerance by delaying senescence (Todd et al 2004)In another study exogenously applied uniconazole brassino-lide and abscisic acid increased soybean yields both underwell-watered and water deficit conditions Under water stressconditions plant growth regulator treatments significantlyincreased water potential and improved chlorophyll content(Zhang et al 2004) Jasmonates including jasmonic acidand its related compounds are a group of naturally occurringgrowth regulators rather recently discovered in higher plants(Creelman and Mullet 1995) Jasmonates play an essentialrole in the signaling pathway triggering the expression ofplant defense genes in response to various stresses (Koda1997) Exogenously applied jasmonic acid induced droughttolerance by increasing the betaine level in pear (Gao et al2004) Exogenous application of brassinolide uniconazoleand methyl jasmonate in maize improved drought toleranceowing to increased activities of superoxide dismutase catalaseand ascorbate peroxidase abscisic acid and total carotenoidcontents (Li et al 1998) Benzyladenine is an active cy-tokinin which can increase the drought resistance of differentplants (Shang 2000)

Salicylic acid can also effectively improve plant growthunder drought conditions (Senaratna et al 2000) In a re-cent study exogenous application of salicylic acid improvedthe drought tolerance of winter wheat which was correlatedwith an increased catalase activity (Horvaacuteth et al 2007) Bothsalicylic acid and acetyl-salicylic acid (a derivative of sal-icylic acid) applied at various concentrations through seedsoaking or foliar spray protected muskmelon (Cucumis melo)

seedlings subjected to drought stress However the best pro-tection was obtained from seedlings pretreated with lower con-centrations of salicylic acid (Korkmaz et al 2007)

The fact that seed imbibition with salicylic acid or acetyl-salicylic acid confers stress tolerance in plants is more con-sistent with signaling for gene expression rather than theirdirect effects (Senaratna et al 2000) The endogenous sali-cylic acid content was increased in drought-stressed Phillyreaangustifolia (Munneacute-Bosch and Penuela 2003) suggestingthat salicylic acid might have a role in the drought stress re-sponse In wheat salicylic acid was shown to increase theabscisic acid content leading to the accumulation of proline(Shakirova et al 2003) Pretreatment with 05 mM salicylicacid for 1 day limited the drought tolerance of 2-week-oldmaize plants by increasing their polyamine content (Neacutemethet al 2002) However soaking grains in acetyl-salicylic acidimproved the drought tolerance of wheat

433 Use of osmoprotectants

Osmoprotectants are involved in signaling and regulat-ing plant responses to multiple stresses including reducedgrowth that may be part of the plantrsquos adaptation against stress(Fig 7) In plants the common osmoprotectants are prolinetrehalose fructan mannitol glycinebetaine and others (Zhu2002) They play adaptive roles in mediating osmotic adjust-ment and protecting subcellular structures in stressed plants(Fig 8) However not all plants accumulate these compoundsin sufficient amounts to avert adverse effects of drought stress(Penna 2003) Ashraf and Foolad (2007) outlined three ap-proaches to increase the concentrations of these compounds inplants grown under stress conditions to increase their stresstolerance (1) use of traditional protocols of plant geneticsand breeding to develop cultivars with natural abilities to pro-duce high levels of these compounds under stress conditions(2) engineering genetically modified plants capable of produc-ing sufficient amounts of these compounds in response to en-vironmental stresses and (3) as a short-cut method exogenoususe of these osmolytes on plants to enhance their stress toler-ance ability

Exogenously applied glycinebetaine improves the growthand production of some plants under stress (Naidu et al 1998Chen et al 2000 Hussain et al 2008) In many crop plantsthe natural accumulation of glycinebetaine is lower than suf-ficient to ameliorate the adverse effects of dehydration causedby various environmental stresses (Subbarao et al 2000) Ex-ogenous application of glycinebetaine has been reported to im-prove drought tolerance in this regard (Hussain et al 2008)Foliar-applied glycinebetaine improved the growth of plantssubjected to water deficit by the maintenance of leaf wa-ter status due to improved osmotic adjustment and enhancedphotosynthesis primarily due to a greater stomatal conduc-tance and carboxylation efficiency of Rubisco (Sakamoto andMurata 2002) Exogenous application of glycinebetaine effec-tively diminished the drought effects in terms of greater num-ber of achenes per capitulum in sunflower (Azam et al 2005)However pre-soaking of seeds with glycinebetaine was not

204 M Farooq et al

effective in preventing the adverse effects of water stress onyield components Glycinebetaine application at the vegetativestage was more effective in ameliorating the adverse effectsof drought (Azam et al 2005) Glycinebetaine also increasedanti-oxidative enzyme activities under water deficit (Ma et al2007) Exogenously applied proline enhanced the endogenousaccumulation of free proline and improved the drought toler-ance in petunia (Yamada et al 2005)

Inhibitors of polyamine biosynthetic enzymes limit stresstolerance of wheat but the concomitant exogenous applicationof polyamines restores it (Liu et al 2004) Exogenous sper-midine application before the drought stress significantly im-proved the stress tolerance in barley (Kubis 2003) In a recentreview Liu et al (2007) concluded that though there was vari-ation in effects between polyamines and plant species exoge-nous polyamine application to stressed cells or tissues couldlead to injury alleviation and growth promotion Yang et al(2007) suggested that for rice to perform well under droughtstress it should have higher levels of free spermidinefree sper-mine and insoluble-conjugate putrescine

434 Silicon

Silicon is the second most abundant element in soils anda mineral substrate for most of the worldrsquos plant life Ampleevidence is available indicating that when silicon is readilyavailable to plants it plays a significant role in their growthmineral nutrition mechanical strength and resistance to sev-eral stresses (Epstein 1994) It has not been considered an es-sential element for higher plants yet partly because its rolein plant biology is less well understood (Gong et al 2003)Nevertheless numerous studies demonstrate that silicon is animportant element and plays an important role in tolerance ofplants to environmental stresses (Savant et al 1999)

With respect to drought stress relevant work is limited onsilicon Sorghum (Sorghum bicolor) plants grown in pots inthe presence of silicon had higher relative water content anddry materials by improving shoot water uptake (Hattori et al2001 2005) Wheat plants applied with silicon could maintainbetter water status and higher content of dry materials com-pared with non-silicon treatment under drought (Gong et al2003) Exogenously applied silicon lowered the shoot to rootratio indicating the facilitation of root growth and mainte-nance of a higher photosynthetic rate and stomatal conduc-tance compared with plants grown without silicon applicationunder drought stress (Hattori et al 2005) In another studyGong et al (2005) opined that the silicon-triggered improve-ment in drought tolerance of wheat plants was associated withan increase in antioxidant defense thereby alleviating oxida-tive stress on functional molecules of cells Silicification en-dodermal tissue was found to play an important role in watertransport across the root of rice (Lux et al 1999) and sorghum(Lux et al 2002) These data together with the rate of siliconuptake and deposition by sorghum roots (Lux et al 2003) andthe effects of losing root cell walls in sorghum (Hattori et al2003) suggested an important role of silicon in water transportand maintenance of root growth under drought stress

5 CONCLUSION

Water deficit reduces plant growth and development lead-ing to the production of smaller organs and hampered flowerproduction and grain filling A diminution in grain filling oc-curs due to a decrease in the accumulation of sucrose andstarch synthesis enzymes Timing duration severity and speedof development undoubtedly have pivotal roles in determin-ing how a plant responds to water deficit Following droughtstomata close progressively with a parallel decline in net pho-tosynthesis and water-use efficiency Stomatal conductance isnot controlled by soil water availability alone but by a com-plex interaction of intrinsic and extrinsic factors Dependingupon the availability of moisture activities of the enzymes ofcarbon assimilation and those involved in adenosine triphos-phate synthesis are decreased and sometimes inhibited Oneof the major factors responsible for impaired plant growth andproductivity under drought stress is the production of reac-tive oxygen species in organelles including chloroplasts mito-chondria and peroxisomes The reactive oxygen species targetthe peroxidation of cellular membrane lipids and degradationof enzyme proteins and nucleic acids

Being very complex the drought tolerance mechanism in-volves a number of physiological and biochemical processesat cell tissue organ and whole-plant levels when activatedat different stages of plant development Examples of thesemechanisms are reduction in water loss by increasing stom-atal resistance increased water uptake by developing large anddeep root systems accumulation of osmolytes and osmopro-tectant synthesis Amongst plant growth substances salicylicacid cytokinin and abscisic acid have been reported to playan important role in drought tolerance Scavenging of reactiveoxygen species by enzymatic and non-enzymatic systems cellmembrane stability expression of aquaporins and stress pro-teins are also vital mechanisms of drought tolerance Droughtstress effects can be managed by production of most appropri-ate plant genotypes seed priming plant growth regulators useof osmoprotectants silicon and some other strategies

Although physiological mechanisms of drought toleranceare relatively well understood further studies are essentialto determine the physiological basis of assimilate partition-ing from source to sink plant phenotypic flexibility whichleads to drought tolerance and factors that modulate plantdrought-stress response Like most other abiotic stresses fo-liar plant parts are more directly impinged upon by droughtthan roots However an understanding of root responses todrought stress most likely involving root-shoot signaling is apreferred area of research Investigations that seek to improvecrop performance by increasing osmotic adjustment need tofocus on meristematic regions of roots For effective applica-tion and commercial use of exogenous glycinebetaine prolineand other compatible solutes as inducers of drought tolerancetheir mechanisms of action the most optimal concentrationsand appropriate plant developmental stages must be carefullydetermined The role of H2O2 as a signaling molecule as wellas the identification of regulatory components in the path-way that leads to plant responses to drought stress are fun-damental clues for future research Applications of genomics

proteomics and trascriptomic approaches to a better under-standing of the molecular basis of plant drought tolerance andimproved water-use efficiency under drought are also impera-tive Mutants or transgenic plants exhibiting differential capa-bilities for reactive oxygen species formation and eliminationcould be useful to elucidate this fundamental point Molecu-lar knowledge of response and tolerance mechanisms is likelyto pave the way for engineering plants that can withstand andgive satisfactory economic yield under drought stress

REFERENCES

Abbate PE Dardanellib JL Cantareroc MG Maturanoc MMelchiorid RJM Sueroa EE (2004) Climatic and water avail-ability effects on water-use efficiency in wheat Crop Sci 44 474ndash483

Abdul Jaleel C Manivannan P Sankar B Kishorekumar A Gopi RSomasundaram R Panneerselvam R (2007) Water deficit stressmitigation by calcium chloride in Catharanthus roseus Effects onoxidative stress proline metabolism and indole alkaloid accumula-tion Colloid Surf B 60 110ndash116

Agarwal PK Agarwal P Reddy MK Sopory SK (2006) Role ofDREB transcription factors in abiotic and biotic stress tolerance inplants Plant Cell Rep 25 1263ndash1274

Aharon R Shahak Y Wininger S Bendov R Kapulnik Y Galili G(2003) Overexpression of a plasma membrane aquaporins in trans-genic tobacco improves plant vigour under favourable growth con-ditions but not under drought or salt stress Plant Cell 15 439ndash447

Ahmadi A Baker DA (2001) The effect of water stress on the activi-ties of key regulatory enzymes of the sucrose to starch pathway inwheat Plant Growth Regul 35 81ndash91

Ajouri A Asgedom H Becker M (2004) Seed priming enhances ger-mination and seedling growth of barley under conditions of P andZn deficiency J Plant Nutr Soil Sc 167 630ndash636

Akashi K Miyake C Yokota A (2001) Citrulline a novel compatiblesolute in drought-tolerant wild watermelon leaves is an efficienthydroxyl radical scavenger FEBS Lett 508 438ndash442

Alexieva V Sergiev I Mapelli S Karanov E (2001) The effect ofdrought and ultraviolet radiation on growth and stress markers inpea and wheat Plant Cell Environ 24 1337ndash1344

Alistair MH Brownlee C (2004) The generation of Ca2+ signals inplants Annu Rev Plant Biol 55 401ndash27

Andersen MN Asch F Wu Y Jensen CR Naeligsted H Mogensen VOKoch KE (2002) Soluble invertase expression is an early target ofdrought stress during the critical abortionndashsensitive phase of youngovary development in maize Plant Physiol 130 591ndash604

Anjum F Yaseen M Rasul E Wahid A Anjum S (2003) Water stressin barley (Hordeum vulgare L) I Effect on chemical compositionand chlorophyll contents Pakistan J Agr Sci 40 45ndash49

Apel K Hirt H (2004) Reactive oxygen species metabolism oxidativestress and signal transduction Annu Rev Plant Biol 55 373ndash99

Araus JL Slafer GA Reynolds MP Royo C (2002) Plant breedingand drought in C3 cereals what should we breed for Ann Bot 89925ndash940

Asch F Dingkuhnb M Sow A Audebert A (2005) Drought-inducedchanges in rooting patterns and assimilate partitioning between rootand shoot in upland rice Field Crop Res 93 223ndash236

Ashraf M Foolad MR (2007) Roles of glycinebetaine and proline inimproving plant abiotic stress resistance Environ Exp Bot 59206ndash216

Atlin GN Lafitte HR (2002) Marker-assisted breeding versus directselection for drought tolerance in rice in Saxena NP OrsquoTooleJC (Eds) Field screening for drought tolerance in crop plantswith emphasis on rice Proc Int Workshop on Field Screeningfor Drought Tolerance in Rice Patancheru India 11-14 Dec 2000ICRISAT Patancheru India and The Rockefeller Foundation NewYork p 208

Atteya AM (2003) Alteration of water relations and yield of corn geno-types in response to drought stress Bulg J Plant Physiol 29 63ndash76

Azam F Ashraf M Ashraf MY Iqbal N (2005) Effect of exogenousapplication of glycinebetaine on capitulum size and achene numberof sunflower under water stress Int J Biol Biotechnol 2 765ndash771

Babu RC Nguyen BD Chamarerk VP Shanmugasundaram PChezhian P Jeyaprakash SK Ganesh A Palchamy S SadasivamS Sarkarung S Wade LJ Nguyen HT (2003) Genetic analysisof drought resistance in rice by molecular markers Crop Sci 431457ndash1469

Bahieldina A Mahfouz HT Eissa HF Saleh OM Ramadan AMAhmed IA Dyer WE El-Itriby HA Madkour MA (2005)Field evaluation of transgenic wheat plants stably expressing theHVA1 gene for drought tolerance Physiol Plant 123 421ndash427

Bajji M Kinet J Lutts S (2002) The use of the electrolyte leakagemethod for assessing cell membrane stability as a water stress tol-erance test in durum wheat Plant Growth Regul 36 61ndash70

Ball RA Oosterhuis DM Mauromoustakos A (1994) Growth dynam-ics of the cotton plant during water-deficit stress Agron J 86 788ndash795

Basnayake J Fukai S Ouk M (2006) Contribution of potential yielddrought tolerance and escape to adaptation of 15 rice varietiesin rainfed lowlands in Cambodia Proceedings of the AustralianAgronomy Conference Australian Society of Agronomy BirsbaneAustralia

Beck EH Fettig S Knake C Hartig K Bhattarai T (2007) Specificand unspecific responses of plants to cold and drought stress JBiosci 32 501ndash510

Bektasoglu B Esin CS Ozyuumlrek Mustafa O Kubilay G Resat A(2006) Novel hydroxyl radical scavenging antioxidant activity as-say for water-soluble antioxidants using a modified CUPRACmethod Biochem Bioph Res Co 345 1194ndash2000

Berlett BS Stadtman ER (1997) Protein oxidation in aging diseaseand oxidative stress J Biol Chem 272 20313ndash20316

Blokhina O Virolainen E Fagerstedt KV (2003) Antioxidants oxida-tive damage and oxygen deprivation stress a review Ann Bot 91179ndash194

Borsani O Valpuesta V Botella MA (2001) Evidence for a role of sal-icylic acid in the oxidative damage generated by NaCl and osmoticstress in Arabidopsis seedlings Plant Physiol 126 1024ndash1030

Bota J Flexas J Medrano H (2004) Is photosynthesis limited by de-creased Rubisco activity and RuBP content under progressive waterstress New Phytol 162 671ndash681

Bouchereau A Aziz A Larher F Tanguy M (1999) Polyamines andenvironmental challenges Rec Develop Plant Sci 140 103ndash125

Bray EA (1997) Plant responses to water deficit Trends Plant Sci 248ndash54

Bruce WB Edmeades GO Barker TC (2002) Molecular and physio-logical approaches to maize improvement for drought tolerance JExp Bot 53 13ndash25

Buchanan CD Lim S Salzman RA Kagiampakis I Morishige DTWeers BD Klein RR Pratt LH Cordonnier-Pratt MM KleinP Mullet J (2005) Sorghum bicolorrsquos transcriptome response todehydration high salinity and ABA Plant Mol Biol 58 699ndash720

Cattivelli L Baldi P Crosetti C Di Fonzo N Faccioli P Grassi MMastrangelo AM Pecchioni N Stanca AM (2002) Chromosomeregions ans stress-related sequences involved in resistance to abioticstress in triticeae Plant Mol Biol 48 649ndash665

206 M Farooq et al

Cattivelli L Rizza F Badeck FW Mazzucotelli E Mastrangelo AMFrancia E Mare C Tondelli A Stanca AM (2008) Drought tol-erance improvement in crop plants An integrative view from breed-ing to genomics Field Crop Res 105 1ndash14

Chapman SC Edmeades GO (1999) Selection improves drought tol-erance in tropical maize populations II Direct and correlated re-sponses among secondary traits Crop Sci 39 1315ndash1

Chaves MM Oliveira MM (2004) Mechanisms underlying plant re-silience to water deficits prospects for water-saving agriculture JExp Bot 55 2365ndash2384

Chen M Wang QY Cheng XG Xu ZS Li LC Ye XG Xia LQMa YZ (2007) GmDREB2 a soybean DRE-binding transcrip-tion factor conferred drought and high-salt tolerance in transgenicplants Biochem Bioph Res Co 353 299ndash305

Chen W Provart NJ Glazebrook J Katagiri F Chang HS EulgemT Mauch F Luan S Zou G Whitham SA Budworth PR TaoY Xie Z Chen X Lam S Kreps JA Harper JF Si-Ammour AMauch-Mani B Heinlein M Kobayashi K Hohn T Dangl JLWang X Zhu T (2002) Expression profile matrix of Arabidopsistranscription factor genes suggests their putative functions in re-sponse to environmental stresses Plant Cell 14 559ndash574

Chen WP Li PH Chen THH (2000) Glycinebetaine increases chill-ing tolerance and reduces chilling-induced lipid peroxidation in Zeamays L Plant Cell Environ 23 609ndash618

Cheng SH Willmann MR Chen H Sheen J (2002) Calcium signalingthrough protein kinases the Arabidopsis calcium-dependent pro-tein kinase gene family Plant Physiol 129 469ndash485

Chew O Whelan J Miller AH (2003) Molecular definition of theascorbate-glutathione cycle in Arabidopsis mitochondria revealsdual targeting of antioxidant defences in plants J Biol Chem 27846869ndash46877

Choi DW Rodriguez EM Close TJ (2002) Barley Cbf3 Gene identi-fication expression pattern and map location Plant Physiol 1291781ndash1787

Close TJ (1997) Dehydrins a commonality in the response of plants todehydration and low temperature Physiol Plant 100 291ndash296

Coca MA Almoguera C Jordano J (1994) Expression of sunflowerlow molecular weight heat shock proteins during embryogenesisand persistence after germination localization and possible func-tional implications Plant Mol Biol 25 479ndash492

Condon AG Richards RA Rebetzke GJ Farquhar GD (2004)Breeding for high water-use efficiency J Exp Bot 55 2447ndash2460

Cornic G Bukhov NG Wiese C Bligny R Heber U (2000) Flexiblecoupling between light-dependent electron and vectorial protontransport in illuminated leaves of C-3 plants Role of photosystemI-dependent proton pumping Planta 210 468ndash477

Cornic G Massacci A (1996) Leaf photosynthesis under drought stressin Baker NR (Ed) Photosynthesis and the Environment KluwerAcademic Publishers The Netherlands

Costa LD Vedove GD Gianquinto G Giovanardi R Peressotti A(1997) Yield water use efficiency and nitrogen uptake in potatoinfluence of drought stress Potato Res 40 19ndash34

Craufurad PQ Wheeler TR Ellis RH Summerfield RJ Prasad PVV(2000) Escape and tolerance to high temperature at flowering ingroundnut J Agr Sci 135 371ndash378

Creelman RA Mullet JE (1995) Jasmonic acid distribution and actionin plants regulation during development and response to biotic andabiotic stress Proc Natl Acad Sci (USA) 92 4114ndash4119

DaMatta FM (2004) Exploring drought tolerance in coffee a physiolog-ical approach with some insights for plant breeding Braz J PlantPhysiol 16 1ndash6

Davidson EA Verchot LV Cattanio JH Ackerman IL CarvalhoHM (2000) Effects of soil water content on soil respiration inforests and cattle pastures of eastern Amazonian Biogeochemistry48 53ndash69

Deltoro VI Calatayud A Gimeno C AbadotildeAcirca A Barreno E (1998)Changes in chlorophyll a fuorescence photosynthetic CO2 assimi-lation and xanthophyll cycle interconversions during dehydration indesiccation-tolerant and intolerant liverworts Planta 207 224ndash228=31pt

DeLucia EH Heckathorn SA (1989) The effect of soil drought onwater-use efficiency in a contrasting Great Basin desert and Sierranmontane species Plant Cell Environ 12 935ndash940

De Souza JG Da Silv JV (1987) Partitioning of carbohydrates in an-nual and perennial cotton (Gossypium hirsutum L) J Exp Bot 381211ndash1218

Dhanda SS Sethi GS Behl RK (2004) Indices of drought tolerancein wheat genotypes at early stages of plant growth J Agron CropSci 190 6ndash12

Dingkuhn M Asch F (1999) Phenological responses of Oryza sativaO glaberrima and inter-specific rice cultivars on a toposquence inWest Africa Euphytica 110 109ndash126

Drennan PM Smith MT Goldsworthy D van Staden J (1993) Theoccurrence of trehalose in the leaves of the desiccation-tolerant an-giosperm Myrothamnus flabellifolius Welw J Plant Physiol 142493ndash496

Du LV Tuong TP (2002) Enhancing the performance of dry-seededrice effects of seed priming seedling rate and time of seedling inPandey S Mortimer M Wade L Tuong TP Lopes K HardyB (Eds) Direct seeding Research strategies and opportunitiesInternational Research Institute Manila Philippines pp 241ndash256

Du YC Kawamitsu Y Nose A Hiyane S Murayama S Wasano KUchida Y (1996) Effects of water stress on carbon exchange rateand activities of photosynthetic enzymes in leaves of sugarcane(Saccharum Sp) Aust J Plant Physiol 23 719ndash726

Dubouzet JG Sakuma Y Ito Y Kasuga M Dubouzet EG Miura SSeki M Shinozaki K Yamaguchi-Shinozaki K (2003) OsDREBgenes in rice Oryza sativa L encode transcription activators thatfunction in drought- high-salt- and cold-responsive gene expres-sion Plant J 33 751ndash763

Earl H Davis RF (2003) Effect of drought stress on leaf and wholecanopy radiation use efficiency and yield of maize Agron J 95688ndash696

Edmeades GO Cooper M Lafitte R Zinselmeier C Ribaut JMHabben JE Loumlffler C Baumlnziger M (2001) Abiotic stresses andstaple crops Proceedings of the Third International Crop ScienceCongress August 18ndash23 2000 Hamburg Germany CABI

Egilla JN Davies Jr FT Boutton TW (2005) Drought stress in-fluences leaf water content photosynthesis and water-use effi-ciency of Hibiscus rosa-sinensis at three potassium concentrationsPhotosynthetica 43 135ndash140

Epstein E (1994) The anomaly of silicon in plant biology Proc NatlAcad Sci (USA) 91 11ndash17

Estrada-Campuzano G Miralles DJ Slafer GA (2008) Genotypic vari-ability and response to water stress of pre- and post-anthesis phasesin triticale Eur J Agron 28 171ndash177

Farooq M Basra SMA Wahid A (2006) Priming of field-sown riceseed enhances germination seedling establishment allometry andyield Plant Growth Regul 49 285ndash294

Farooq M Basra SMA Ahmad N (2007) Improving the performanceof transplanted rice by seed priming Plant Growth Regul 51 129ndash137

Farooq M Aziz T Basra SMA Cheema MA Rehamn H (2008)Chilling tolerance in hybrid maize induced by seed priming withsalicylic acid J Agron Crop Sci 194 161ndash168

Fazeli F Ghorbanli M Niknam V (2007) Effect of drought on biomassprotein content lipid peroxidation and antioxidant enzymes in twosesame cultivars Biol Plant 51 98ndash103

Folkert AH Elena AG Buitink J (2001) Mechanisms of plant desic-cation tolerance Trends Plant Sci 6 431ndash438

Foyer CH Fletcher JM (2001) Plant antioxidants colour me healthyBiologist 48 115ndash120

Frederick JR Camp CR Bauer PJ (2001) Drought-stress effects onbranch and main stem seed yield and yield components of determi-nate soybean Crop Sci 41 759ndash763

Fu BY Xiong JH Zhu LH Zhao XQ Xu HX Gao YM Li YSXu JL Li ZK (2007) Identification of functional candidate genesfor drought tolerance in rice Mol Genet Genom 278 599ndash609

Fu J Huang B (2001) Involvement of antioxidants and lipid perox-idation in the adaptation of two cool-season grasses to localizeddrought stress Environ Exp Bot 45 105ndash114

Gao XP Wang XF Lu YF Zhang LY Shen YY Liang Z ZhangDP (2004) Jasmonic acid is involved in the water-stress-inducedbetaine accumulation in pear leaves Plant Cell Environ 27 497ndash507

Garg BK (2003) Nutrient uptake and management under droughtnutrient-moisture interaction Curr Agric 27 1ndash8

Gigon A Matos A Laffray D Zuily-fodil Y Pham-Thi A (2004)Effect of drought stress on lipid metabolism in the leaves ofArabidopsis thaliana (Ecotype Columbia) Ann Bot 94 345ndash351

Gille L Nohl H (2001) The ubiquinolbc1 redox couple regulates mito-chondrial oxygen radical formation Arch Biochem Biophys 38834ndash38

Gnanasiri SP Saneoka H Ogata S (1991) Cell membrane stability andleaf water relations as affected by potassium nutrition of water-stressed maize J Exp Bot 42 739ndash745

Goddijn OJM Verwoerd TC Voogd E Krutwagen PWHH DegraafPTHM Poels J Vandun K Ponstein AS Damm B Pen J(1997) Inhibition of trehalase activity enhances trehalose accumu-lation in transgenic plants Plant Physiol 113 181ndash190

Goetz M Godt DE Guivarcrsquoh A Kahmann U Chriqui D Roitsch T(2001) Induction of male sterility in plants by metabolic engineer-ing of the carbohydrate supply Proc Natl Acad Sci (USA) 986522ndash6527

Golding AJ Johnson GN (2003) Down-regulation of linear and acti-vation of cyclic electron transport during drought Planta 218 107ndash114

Gong H Chen K Chen G Wang S Zhang C (2003) Effects of siliconon growth of wheat under drought J Plant Nutr 26 1055ndash1063

Gong H Zhu X Chen K Wang S Zhang C (2005) Silicon alleviatesoxidative damage of wheat plants in pots under drought Plant Sci169 313ndash321

Gorantla M Babu PR Lachagari VBR Reddy AMM WusirikaR Bennetzen JL Reddy AR (2006) Identification of stress-responsive genes in an indica rice (Oryza sativa L) using ESTsgenerated from drought-stressed seedlings J Exp Bot 58 253ndash265

Grossman A Takahashi H (2001) Macronutrient utilization by photo-synthetic eukaryotes and the fabric of interactions Annu Rev PlantPhys 52 163ndash210

Halliwell B Gutteridge JMC (1999) Free radicals in biology andmedicine 3rd ed Oxford University Press New York NY

Harmon AC Gribskov M Harper JF (2000) CDPKs a kinase for everyCa2+ signal Trends Plant Sci 5 154ndash159

Harris D Jones M (1997) On-farm seed priming to accelerate germina-tion in rainfed dry-seeded rice Int Rice Res Notes 22 30

Harris D Tripathi RS Joshi A (2002) On-farm seed priming to im-prove crop establishment and yield in dry direct-seeded rice inPandey S Mortimer M Wade L Tuong TP Lopes K HardyB (Eds) Direct seeding Research Strategies and OpportunitiesInternational Research Institute Manila Philippines pp 231ndash240

Hasegawa PM Bressan RA Zhu JK Bohnert HJ (2000) Plant cellu-lar and molecular responses to high salinity Annu Rev Plant Phys51 463ndash499

Hattori T Lux A Tanimoto E Luxova M Sugimoto Y InanagaS (2001) The effect of silicon on the growth of sorghum underdrought in Proceedings of the 6th Symposium of the InternationalSociety of Root Research Nagoya Japan 2001 pp 348ndash349

Hattori T Inanaga S Tanimoto E Lux A Luxovarsquo M SugimotoY (2003) Silicon-induced changes in viscoelastic properties ofsorghum root cell walls Plant Cell Physiol 44 743ndash749

Hattori T Inanaga S Hideki A Ping A Shigenori M Miroslava LLux A (2005) Application of silicon enhanced drought tolerance inSorghum bicolor Physiol Plant 123 459ndash466

Havaux M (1998) Carotenoids as membrane stabilizers in chloroplastsTrends in Plant Sci 3 147ndash151

Hoekstra FA Golovina EA Buitink J (2001) Mechanisms of plantdesiccation tolerance Trends Plant Sci 6 431ndash438

Horvaacuteth E Paacutel M Szalai G Paacuteldi E Janda T (2007) Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants Biol Plant 51480ndash487

Huang B Liu JY (2006) Cloning and functional analysis of the novelgene GhDBP3 encoding a DRE-binding transcription factor fromGossypium hirsutum Biochim Biophys Acta 1759 263ndash269

Huang BR Fu J (2000) Photosynthesis respiration and carbon alloca-tion of two cool-season perennial grasses in response to surface soildrying Plant Soil 227 17ndash26

Hussain M Malik MA Farooq M Ashraf MY Cheema MA (2008)Improving Drought tolerance by exogenous application of glycine-betaine and salicylic acid in sunflower J Agron Crop Sci 194193ndash199

Ingram J Bartels D (1996) The molecular basis of dehydration tolerancein plants Annu Rev Plant Phys Plant Mol Biol 47 377ndash403

Jaglo KR Kleff S Amundsen KL Zhang X Haake V Zhang JZDeits T Thomashow MF (2001) Components of the ArabidopsisC-repeatdehydration-responsive element binding factor cold re-sponse pathway are conserved in Brassica napus and other plantspecies Plant Physiol 127 910ndash917

Javot H Maurel C (2002) The role of aquaporins in root water uptakeAnn Bot 90 301ndash313

Javot H Lauvergeat V Santoni V Martin-Laurent F Guclu J VinhJ Heyes J Franck KI Schaffner AR Bouchez D Maurel C(2003) Role of a single aquaporin isoform in root water uptakePlant Cell 15 509ndash522

Jimeacutenez A Hernandez JA Ros Barcelo A Sandalio LM del RioLA Sevilla F (1998) Mitochondrial and peroxisomal ascorbateperoxidase of pea leaves Physiol Plant 104 687ndash692

Johansson I Karlsson M Shukla VK Chrispeels MJ Larsson CKjellbom P (1998) Water transport activity of the plasma mem-brane aquaporin PM28A is regulated by phosphorylation Plant Cell10 451ndash459

Jongdee B Fukai S Cooper M (2002) Leaf water potential and osmoticadjustment as physiological traits to improve drought tolerance inrice Field Crop Res 76 153ndash163

Joyce SM Cassells AC Mohan JS (2003) Stress and aberrant pheno-types in vitro culture Plant Cell Tiss Orga 74 103ndash121

Kaldenhoff R Grote K Zhu JJ Zimmermann U (1998) Significanceof plasmalemma aquaporins for water-transport in Arabidopsisthaliana Plant J 14 121ndash128

Kamara AY Menkir A BadundashApraku B Ibikunle O (2003) The in-fluence of drought stress on growth yield and yield components ofselected maize genotypes J Agr Sci 141 43ndash50

Karim S Aronsson H Ericson H Pirhonen M Leyman B Welin BMaumlntylauml E Palva ET Dijck PV Holmstroumlm K (2007) Improveddrought tolerance without undesired side effects in transgenic plantsproducing trehalose Plant Mol Biol 64 371ndash386

208 M Farooq et al

Kasukabe Y He L Nada K Misawa S Ihara I Tachibana S (2004)Overexpression of spermidine synthase enhances tolerance to mul-tiple environmental stresses and up-regulates the expression of vari-ous stress-regulated genes in transgenic Arabidopsis thaliana PlantCell Physiol 45 712ndash722

Kaur S Gupta AK Kaur N (2005) Seed priming increases crop yieldpossibly by modulating enzymes of sucrose metabolism in chick-pea J Agron Crop Sci 191 81ndash87

Kavar T Maras M Kidric M Sustar-Vozlic J Meglic V (2007)Identification of genes involved in the response of leaves ofPhaseolus vulgaris to drought stress Mol Breed 21 159ndash172

Kawakami J Iwama K Jitsuyama Y (2006) Soil water stress and thegrowth and yield of potato plants grown from microtubers and con-ventional seed tubers Field Crop Res 95 89ndash96

Kawasaki S Miyake C Kouchi T Yokota A (2000) Responses of wildwatermelon to drought stress accumulation of an ArgE homologueand citrulline in leaves during water deficit Plant Cell Phys 41864ndash873

Kaya MD Okccedilub G Ataka M Ccedilıkılıc Y Kolsarıcıa Ouml (2006) Seedtreatments to overcome salt and drought stress during germinationin sunflower (Helianthus annuus L) Eur J Agron 24 291ndash295

Kim JY Maheacute A Brangeon J Prioul JL (2000) A maize vacuolurinvertase IVR2 is induced by water stress Organtissue specificityand diurnal modulation of expression Plant Physiol 124 71ndash84

Kinnersley AM Turano FJ (2000) Gama aminobutyric acid (GABA)and plant responses to stress Crit Rev Plant Sci 19 479ndash509

Kirigwi FM Van Ginkel M Brown-Guedira G Gill BS PaulsenGM Fritz AK (2007) Markers associated with a QTL for grainyield in wheat under drought Mol Breed 20 401ndash413

Knight H (2000) Calcium signaling during abiotic stress in plants IntRev Cytol 195 269ndash325

Koda Y (1997) Possible involvement of jasmonates in various mor-phogenic events Physiol Plant 100 639ndash646

Komor E (2000) Source physiology and assimilate transport the inter-action of sucrose metabolism starch storage and phloem export insource leaves and the effects on sugar status in phloem Aust JPlant Physiol 27 497ndash505

Korkmaz A Uzunlu M Demirkiran AR (2007) Treatment with acetylsalicylic acid protects muskmelon seedlings against drought stressActa Physiol Plant 29 503ndash508

Kosmas SA Argyrokastritis A Loukas MG Eliopoulos E TsakasS Kaltsikes PJ (2006) Isolation and characterization of droughtrelated trehalose 6-phosphate-synthase gene from cultivated cotton(Gossypium hirsutum L) Planta 223 329ndash339

Kovtun Y Chiu WL Tena G Sheen J (2000) Functional analysis ofoxidative stress-activated mitogen-activated protein kinase cascadein plants Proc Natl Acad Sci (USA) 97 2940ndash2945

Kramer PJ Boyer JS (1995) Water relations of Plants and SoilsAcademic Press San Diego

Kubis J (2003) Polyamines and scavenging system influence of ex-ogenous spermidine on catalase and guaiacol peroxidase activitiesand free polyamine level in barley leaves under water deficit ActaPhysiol Plant 25 337ndash343

Kumar B Pandey DM Goswami CL Jain S (2001) Effect of growthregulators on photosynthesis transpiration and related parametersin water stressed cotton Biol Plant 44 475ndash478

Kumar J Abbo S (2001) Genetics of flowering time in chickpea and itsbearing on productivity in the semi-arid environments Adv Agron72 107ndash138

Lafitte HR Yongsheng G Yan S Li1 ZK (2007) Whole plant re-sponses key processes and adaptation to drought stress the caseof rice J Exp Bot 58 169ndash175

Lamb C Dixon RA (1997) The oxidative burst in plant disease resis-tance Annu Rev Plant Phys 48 251ndash275

Lambers H Atkin OK Scheureater I (1996) Respiratory patterns inroots in relation to their function in Waisel Y (Ed) Plant RootsThe Hidden Half Marcel Dekker NewYork

Lawlor DW Cornic G (2002) Photosynthetic carbon assimilation andassociated metabolism in relation to water deficits in higher plantsPlant Cell Environ 25 275ndash294

Lazaridou M Koutroubas SD (2004) Drought effect on water use ef-ficiency of berseem clover at various growth stages New direc-tions for a diverse planet Proceedings of the 4th International CropScience Congress Brisbane Australia 26 Septndash1 Oct 2004

Lazaridou M Kirilov A Noitsakis B Todorov N Katerov I (2003)The effect of water deficit on yield and water use efficiency oflucerne Optimal forage systems for animal production and the en-vironment Proceedings of the 12th Symposium of the EuropeanGrassland Federation Pleven Bulgaria 26ndash28 May 2003

Lee SB Kwon HB Kwon SJ Park SC Jeong MJ Han SE ByunMO Daniell H (2004) Accumulation of trehalose within trans-genic chloroplasts confers drought tolerance Mol Breed 11 1ndash13

Leport L Turner NC French RJ Barr MD Duda R Davies SL(2006) Physiological responses of chickpea genotypes to terminaldrought in a Mediterranean-type environment Eur J Agron 11279ndash291

Li L Van Staden J Jager AK (1998) Effects of plant growth regula-tors on the antioxidant system in seedlings of two maize cultivarssubjected to water stress Plant Growth Regul 25 81ndash87

Liang P Pardee AB (1992) Differential display of eukaryotic messengerRNA by means of the polymerase chain reaction Science 257 967ndash971

Lima ALS DaMatta FM Pinheiro HA Totola MR Loureiro ME(2002) Photochemical responses and oxidative stress in two clonesof Coffea canephora under water deficit conditions Environ ExpBot 47 239ndash247

Lindhauer MG (2007) Influence of K nutrition and drought on wa-ter relations and growth of sunflower (Helianthus annuus L) ZPflanzenernaumlhr Bodenk 148 654ndash669

Liu HP Dong BH Zhang YY Liu ZP Liu YL (2004) Relationshipbetween osmotic stress and the levels of free soluble conjugatedand insoluble-conjugated polyamines in leaves of wheat seedlingsPlant Sci 166 1261ndash1267

Liu HS Li FM (2005) Root respiration photosynthesis and grain yieldof two spring wheat in response to soil drying Plant Growth Regul46 233ndash240

Liu HS Li FM Xu H (2004) Deficiency of water can enhance rootrespiration rate of droughtndashsensitive but not drought-tolerant springwheat Agr Water Manage 64 41ndash48

Liu JH Kitashiba H Wang J Ban Y Moriguch T (2007) Polyaminesand their ability to provide environmental stress tolerance to plantsPlant Biotechnol 24 117ndash126

Liu Q Kasuga M Sakuma Y Abe H Miura S Yamaguchi-Shinozaki K Shinozaki K (1998) Two transcription factorsDREB1 and DREB2 with an EREBPAP2 DNA binding domainseparate two cellular signal transduction pathways in drought-and low temperature-responsive gene expression respectively inArabidopsis Plant Cell 10 1391ndash1406

Loreto F Tricoli D Di Marco G (1995) On the relationship betweenelectron transport rate and photosynthesis in leaves of the C4 plantSorghum bicolor exposed to water stress temperature changes andcarbon metabolism inhibition Aust J Plant Physiol 22 885ndash892

Luan S Kudla J Rodriguez-Concepcion M Yalovsky S Gruissem W(2002) Calmodulins and calcineurin B-like proteins calcium sen-sors for specific signal response coupling in plants Plant Cell 14S389ndashS400

Ludlow MM Muchow RC (1990) A critical evaluation of traits forimproving crop yields in water-limited environments Adv Agron43 107ndash153

Ludwig-Muumlller J (2007) Indole-3-butyric acid synthesis in ecotypes andmutants of Arabidopsis thaliana under different growth conditionsJ Plant Physiol 164 47ndash59

Lux A Luxovaacute M Morita S Abe J Inanaga S (1999) Endodermal sili-cification in developing seminal roots of lowland and upland culti-vars of rice (Oryza sativa L) Can J Bot 77 955ndash960

Lux A Luxovaacute M Hattori T Inanaga S Sugimoto Y (2002)Silicification in sorghum (Sorghum bicolor) cultivars with differentdrought tolerance Physiol Plant 115 87ndash92

Lux A Luxovaacute M Abe J Tanimoto E Hattori T Inanaga S (2003)The dynamics of silicon deposition in the sorghum root endodermisNew Phytol 158 437ndash441

Ma XL Wang YJ Xie SL Wang C Wang W (2007) Glycinebetaineapplication ameliorates negative effects of drought stress in to-bacco Russ J Plant Physiol 54 472ndash479

Mahajan S Tuteja N (2005) Cold salinity and drought stresses anoverview Arch Biochem Biophys 444 139ndash158

Manikavelu A Nadarajan N Ganesh SK Gnanamalar RP Babu RC(2006) Drought tolerance in rice morphological and molecular ge-netic consideration Plant Growth Regul 50 121ndash138

Mansfield TJ Atkinson CJ (1990) Stomatal behaviour in water stressedplants in Alscher RG Cumming JR (Eds) Stress Responses inPlants Adaptation and Acclimation Mechanisms Wiley-Liss NewYork pp 241ndash264

Maroco JP Pereira JS Chaves MM (1997) Stomatal responses toleaf-to-air vapour pressure deficit in Sahelian species Aust J PlantPhysiol 24 381ndash387

Martiacutenez JP Silva H Ledent JF Pinto M (2007) Effect of droughtstress on the osmotic adjustment cell wall elasticity and cell vol-ume of six cultivars of common beans (Phaseolus vulgaris L) EurJ Agron 26 30ndash38

Mathur PB Devi MJ Serraj R Yamaguchi-Shinozaki K Vadez VSharma KK (2004) Evaluation of transgenic groundnut lines un-der water limited conditions Int Archis Newslett 24 33ndash34

Maurel C Chrispeels MJ (2001) Aquaporins a molecular entry intoplant water relations Plant Physiol 125 135ndash138

Maurel C Javot H Lauvergeat V Gerbeau P Tournaire C Santoni VHeyes J (2002) Molecular physiology of aquaporins in plants IntRev Cytol 215 105ndash148

Mazahery-Laghab H Nouri F Abianeh HZ (2003) Effects of the re-duction of drought stress using supplementary irrigation for sun-flower (Helianthus annuus) in dry farming conditions Pajouhesh-va-Sazandegi Agron Hort 59 81ndash86

McWilliams D (2003) Drought Strategies for Cotton CooperativeExtension Service Circular 582 College of Agriculture and HomeEconomics New Mexico State University USA

Miralles DL Slafer GA Lynch V (1997) Rooting patterns in near-isogenic lines of spring wheat for dwarfism Plant Soil 197 79ndash86

Mishra NS Tuteja R Tuteja N (2006) Signaling through MAP kinasenetworks in plants Arch Biochem Biophys 452 55ndash68

Moinuddin KHM Khannu-Chopra R (2004) Osmotic adjustment inchickpea in relation to seed yield and yield parameters Crop Sci44 449ndash455

Moumlller IM (2001) Plant mitochondria and oxidative stress electrontransport NADPH turnover and metabolism of reactive oxygenspecies Annu Rev Plant Phys 52 561ndash591

Monakhova OF Chernyadegravev II (2002) Protective role of kartolin-4 inwheat plants exposed to soil drought Appl Biochem Micro+ 38373ndash380

Monclus R Dreyer E Villar M Delmotte FM Delay D Petit JMBarbaroux C Thiec DL Breacutechet C Brignolas F (2006) Impact

of drought on productivity and water use efficiency in 29 genotypesof Populus deltoids times Populus nigra New Phytol 169 765ndash777

Monneveux P Saacutenchez C Beck D Edmeades GO (2006) Drought tol-erance improvement in tropical maize source populations evidenceof progress Crop Sci 46 180ndash191

Moore AL Siedow JN (1991) The regulation and nature of the cyanide-resistant oxidase of plant mitochondria Biochim Biophys Acta1059 121ndash140

Moran JF Becana M Iturbe-Ormaetxe I Frechilla S Klucas RVAparicio-Trejo P (1994) Drought induces oxidative stress in peaplants Planta 194 346ndash352

Morgan PW (1990) Effects of abiotic stresses on plant hormone systemsin Stress Responses in plants adaptation and acclimation mecha-nisms Wiley-Liss Inc pp 113ndash146

Mori IC Murata Y Yang Y Munemasa S Wang YF AndreoliS Tiriac H Alonso JM Harper JF Ecker JR Kwak JMSchroeder JI (2006) CDPKs CPK6 and CPK3 function in ABAregulation of guard cell S-type anion- and Ca2+-permeable chan-nels and stomatal closure PLoS Biol 4 1749ndash1762

Munekage Y Hojo M Meurer J Endo T Tasaka M Shikanai T (2002)PGR5 is involved in cyclic electron flow around photosystem I andis essential for photoprotection in Arabidopsis Cell 110 361ndash371

Munneacute-Bosch S Penuelas J (2003) Photo and antioxidative protectionand a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants Planta 217 758ndash766

Munneacute-Bosch S Shikanai T Asada K (2005) Enhanced ferredoxin-dependent cyclic electron flow around photosystem I andα-tocopherol quinone accumulation in water-stressed ndhB-inactivated tobacco mutants Planta 222 502ndash511

Naidu BP Cameron DF Konduri SV (1998) Improving drought tol-erance of cotton by glycinebetaine application and selection inProceedings of the 9th Australian agronomy conference WaggaWagga

Nam NH Chauhan YS Johansen C (2001) Effect of timing of droughtstress on growth and grain yield of extra-short-duration pigeonpealines J Agr Sci 136 179ndash189

Nayyar H Kaur S Singh S Upadhyaya HD (2006) Differential sen-sitivity of Desi (small-seeded) and Kabuli (large-seeded) chickpeagenotypes to water stress during seed filling effects on accumula-tion of seed reserves and yield J Sci Food Agr 86 2076ndash2082

Neacutemeth M Janda T Horvaacuteth E Paacuteldi E Szalai G (2002) Exogenoussalicylic acid increases polyamine content but may decreasedrought tolerance in maize Plant Sci 162 569ndash574

Nerd A Neumann PM (2004) Phloem water transport maintains stemgrowth in a drought-stressed crop cactus (Hylocereus undatus) JAm Soc Hortic Sci 129 486ndash490

Nerd A Nobel PS (1991) Effects of drought on water relations andnonstructural carbohydrates in cladodes of Opuntia ficus-indicaPhysiol Plant 81 495ndash500

Nguyen HT Babu RC Blum A (1997) Breeding for drought resistancein rice Physilogy and molecular genetics considerations Crop Sci37 1426ndash1434

Nilsen ET Orcutte DM (1996) Phytohormones and plant responses tostress in Nilsen ET Orcutte DM (Eds) Physiology of Plantunder Stress Abiotic Factors John Wiley and Sons New Yorkpp 183ndash198

Niyogi KK (1999) Photoprotection revisited genetic and molecular ap-proaches Annu Rev Plant Phys 50 333ndash359

Nonami H (1998) Plant water relations and control of cell elongation atlow water potentials J Plant Res 111 373ndash382

Ober ES Setter TL Madison JT Thompson JF Shapiro PS(1991) Influence of water deficit on maize endosperm development

210 M Farooq et al

enzyme activities and RNA transcripts of starch and zein synthesisabscisic acid and cell division Plant Physiol 97 154ndash164

Ogbonnaya CI Sarr B Brou C Diouf O Diop NN Roy-MacauleyH (2003) Selection of cowpea genotypes in hydroponics pots andfield for drought tolerance Crop Sci 43 1114ndash1120

Okcu G Kaya MD Atak M (2005) Effects of salt and drought stresseson germination and seedling growth of pea (Pisum sativum L)Turk J Agr For 29 237ndash242

Orvar BL Ellis BE (1997) Transgenic tobacco plants expressing anti-sense RNA for cytosolic ascorbate peroxidase show increased sus-ceptibility to ozone injury Plant J 11 1297ndash1305

Pan Y Wu LJ Yu ZL (2006) Effect of salt and drought stress onantioxidant enzymes activities and SOD isoenzymes of liquorice(Glycyrrhiza uralensis Fisch) Plant Growth Regul 49 157ndash165

Pannu RK Singh DP Singh P Chaudhary BD Singh VP (1993)Evaluation of various plant water indices for screening the geno-types of chickpea under limited water environment Haryana JAgron 9 16ndash22

Parry MAJ Andralojc PJ Khan S Lea PJ Keys AJ (2002) Rubiscoactivity effects of drought stress Ann Bot 89 833ndash839

Pastori G Foyer CH Mullineaux P (2000) Low temperature-inducedchanges in the distribution of H2O2 and antioxidants between thebundle sheath and mesophyll cells of maize leaves J Exp Bot 51107ndash113

Penna S (2003) Building stress tolerance through overproducing tre-halose in transgenic plants Trends Plant Sci 8 355ndash357

Pettigrew WT (2004) Physiological consequences of moisture deficitstress in cotton Crop Sci 44 1265ndash1272

Peuke AD Rennenberg H (2004) Carbon nitrogen phosphorus andsulphur concentration and partitioning in beech ecotypes (Fagussylvatica L) phosphorus most affected by drought Trees 18 639ndash648

Peuke AD Hartung W Schraml C Rennenberg H (2002)Identification of drought sensitive beech ecotypes by physiologicalparameters New Phytol 154 373ndash388

Pfister-Sieber M Braendle R (1994) Aspects of plant behavior underanoxia and post-anoxia Proc R Soc Edinburgh 102B 313ndash324

Philipson JJ (2003) Optimal conditions for inducing coning ofcontainer-grown Picea sitchensis grafts effects of applying differ-ent quantities of GA47 timing and duration of heat and droughttreatment and girdling Forest Ecol Manag 53 39ndash52

Pierik R Sasidharan R Voesenek LACJ (2007) Growth control byethylene adjusting phenotypes to the environment J Plant GrowthRegul 26 188ndash200

Pilon-Smits EAH Terry N Sears T Kim H Zayed A Hwang SBVan Dun K Voogd E Verwoerd TC Krutwagen RWHHGoddijn OJM (1998) Trehalose-producing transgenic tobaccoplants show improved growth performance under drought stress JPlant Physiol 152 525ndash532

Pinheiro HA DaMatta FM Chaves ARM Fontes EPB LoureiroME (2004) Drought tolerance in relation to protection against ox-idative stress in clones of Coffea canephora subjected to long-termdrought Plant Sci 167 1307ndash1314

Plaut Z (2003) Plant exposure to water stress during specific growthstages Encyclopedia of Water Science Taylor amp Francis pp 673ndash675

Poroyko V Hejlek LG Spollen WG Springer GK Nguyen HTSharp RE Bohnert HJ (2005) The maize root transcriptome byserial analysis of gene expression Plant Physiol 138 1700ndash1710

Premachandra GS Saneoka H Kanaya M Ogata S (1991) Cell mem-brane stability and leaf surface wax content as affected by increas-ing water deficits in maize J Exp Bot 42 167ndash171

Prochazkova D Sairam RK Srivastava GC Singh DV (2001)Oxidative stress and antioxidant activity as the basis of senescencein maize leaves Plant Sci 161 765ndash771

Quan RD Shang M Zhang H Zhang J (2004) Improved chilling tol-erance by transformation with betA gene for the enhancement ofglycinebetaine synthesis in maize Plant Sci 166 141ndash149

Ramon M Rollan F Thevelein J Dijck P Leyman B (2007) ABI4mediates the effects of exogenous trehalose on Arabidopsis growthand starch breakdown Plant Mol Biol 63 195ndash206

Ratnayaka HH Molin WT Sterling TM (2003) Physiological and an-tioxidant responses of cotton and spurred anoda under interferenceand mild drought J Exp Bot 54 2293ndash2305

Reddy AR Chaitanya KV Vivekanandan M (2004) Drought-inducedresponses of photosynthesis and antioxidant metabolism in higherplants J Plant Physiol 161 1189ndash1202

Reynolds MP Oritz-Monasterio JI Mc Nab A (2001) Application ofphysiology in wheat breeding CIMMYT Mexico

Riccardi L Polignano GB de Giovanni C (2001) Genotypic responseof faba bean to water stress Euphytica 118 39ndash46

Richards RA Rawson HM Johnson DA (1986) Glaucousness inwheat its development and effect on water-use efficiency gasexchange and photosynthetic tissue temperatures Aust J PlantPhysiol 13 465ndash473

Sadiqov ST Akbulut M Ehmedov V (2002) Role of Ca2+ in droughtstress signaling in wheat seedlings Biochemistry-Moscow+ 67491ndash497

Sairam RK Deshmukh PS Saxena DC (1998) Role of antioxidantsystems in wheat genotypes tolerance to water stress Biol Plant41 387ndash394

Sairam RK Srivastava GC Agarwal S Meena RC (2005)Differences in antioxidant activity in response to salinity stress intolerant and susceptible wheat genotypes Biol Plant 49 85ndash91

Sakamoto A Murata N (2002) The role of glycinebetaine in the protec-tion of plants from stress clues from transgenic plants Plant CellEnviron 25 163ndash171

Samarah NH (2005) Effects of drought stress on growth and yield ofbarley Agron Sustain Dev 25 145ndash149

Samarah NH Mullen RE Cianzio SR Scott P (2006) Dehydrin-likeproteins in soybean seeds in response to drought stress during seedfilling Crop Sci 46 2141ndash2150

Sandquist DR Ehleringer JR (2003) Population- and family-level vari-ation of brittlebush (Encelia farinosa Asteraceae) pubescence itsrelation to drought and implications for selection in variable envi-ronments Am J Bot 90 1481ndash1486

Savant NK Korndoumlrfer GH Datnoff LE Snyder GH (1999) Siliconnutrition and sugarcane production a review J Plant Nutr 221853ndash1903

Schuppler U He PH John PCL Munns R (1998) Effects of waterstress on cell division and cell-division-cycle-2-like cell-cycle ki-nase activity in wheat leaves Plant Physiol 117 667ndash678

Senaratna T Touchell D Bunn E Dixon K (2000) Acetyl salicylic acid(aspirin) and salicylic acid induce multiple stress tolerance in beanand tomato plants Plant Growth Regul 30 157ndash161

Serraj R Sinclair TR (2002) Osmolyte accumulation can it really helpincrease crop yield under drought conditions Plant Cell Environ25 333ndash341

Serraj R Barry JS Sinclair TR (1998) Accumulation of γ-aminobutyric acid in nodulated soybean in response to droughtstress Physiol Plant 102 79ndash86

Setter TL Flannigan BA Melkonian J (2001) Loss of kernel set dueto water deficit and shade in maize carbohydrate supplies abscisicacid and cytokinins Crop Sci 41 1530ndash1540

Shakirova FM Sakhabutdinova AR Bezrukova MV FatkhutdinovaRA Fatkhutdinova DR (2003) Changes in the hormonal statusof wheat seedlings induced by salicylic acid and salinity Plant Sci164 317ndash322

Shang Z (2000) Effect of 6-BA and KT on photophosphorylation activityin wheat flag leaves under water stress Acta Agr Boreali-Sinica 1534ndash38

Sharkey TD (1990) Water stress effects on photosynthesisPhotosynthetica 24 651ndash661

Sharp RE Wu Y Voetberg GS Soab IN LeNoble ME (1994)Confirmation that abscisic acid accumulation is required for maizeprimary root elongation at low water potentials J Exp Bot 451743ndash1751

Shelp BL Bown AW McLean MD (1999) Metabolism and functionsof gammaaminobutyric acid Trends Plant Sci 11 446ndash452

Shen YG Zhang WK He SJ Zhang JS Liu Q Chen SY (2003) AnEREBPAP2-type protein in Triticum aestivum was a DRE-bindingtranscription factor induced by cold dehydration and ABA stressTheor Appl Genet 106 923ndash930

Shinozaki K Yamaguchi-Shinozaki K Seki M (2003) Regulatory net-work of gene expression in the drought and cold stress responsesCurr Opin Plant Biol 6 410ndash417

Shugaeva N Vyskrebentseva E Orekhova S Shugaev A (2007) Effectof water deficit on respiration of conducting bundles in leaf petiolesof sugar beet Russ J Plant Physiol 54 329ndash335

Siddique KHM Loss SP Thomson BD (2003) Cool seasongrain legumes in dryland Mediterranean environments of WesternAustralia Significance of early flowering in Saxena NP (Ed)Management of Agricultural Drought Science Publishers Enfield(NH) USA pp 151ndash161

Siddique MRB Hamid A Islam MS (2001) Drought stress effects onwater relations of wheat Bot Bull Acad Sinica 41 35ndash39

Simon-sarkadi L Kocsy G Vaacuterhegyi Aacute Galiba G De Ronde JA2006 Stress-induced changes in the free amino acid compositionin transgenic soybean plants having increased proline content BiolPlant 50 793ndash796

Sinaki JM Heravan EM Rad AHS Noormohammadi G Zarei G(2007) The effects of water deficit during growth stages of canola(Brassica napus L) AmndashEuras J Agri Environ Sci 2 417ndash422

Somerville C Briscoe J (2001) Genetic engineering and water Science292 2217

Stevens RG Creissen GP Mullineaux PM (2000) Characterization ofpea cytosolic glutathione reductase expressed in transgenic tobaccoPlanta 211 537ndash545

Subbarao GV Johansen C Slinkard AE Rao RCN Saxena NPChauhan YS (1995) Strategies and scope for improving droughtresistance in grain legumes Crit Rev Plant Sci 14 469ndash523

Subbarao GV Nam NH Chauhan YS Johansen C (2000) Osmoticadjustment water relations and carbohydrate remobilization in pi-geonpea under water deficits J Plant Physiol 157 651ndash659

Svensson J Ismail AM Palva ET Close TJ (2002) Dehydrins inStorey KB Storey JM (Eds) Cell and Molecular Responses tostress Vol 3 Sensing Signalling and Cell Adaptation ElsevierScience Amsterdam pp 155ndash171

Taiz L Zeiger E (2006) Plant Physiology 4th Ed Sinauer AssociatesInc Publishers Massachusetts

Taylor IB (1991) Genetics of ABA synthesis in Davies WJ HGJones (Eds) Abscisic acid Physiology and Biochemistry BiosScientific Publishers Ltd UK pp 23ndash38

Tezara W Mitchell VJ Driscoll SD Lawlor DW (1999) Water stressinhibits plant photosynthesis by decreasing coupling factor andATP Nature 401 914ndash917

Todd EY Robert BM Daniel RG (2004) ACC synthase expressionregulates leaf performance and drought tolerance in maize plant J40 813ndash825

Tournaire-Roux C Sutka M Javot H Gout E Gerbeau P Luu D-T Bligny R Maurel C (2003) Cytosolic pH regulates root watertransport during anoxic stress through gating of aquaporins Nature425 393ndash397

Tripathy JN Zhang J Robin S Nguyen TT Nguyen HT (2000)QTLs for cell-membrane stability mapped in rice (Oryza sativa L)under drought stress Theor Appl Genet 100 1197ndash1202

Turner NC Wright GC Siddique KHM (2001) Adaptation of grainlegumes (pulses) to water-limited environments Adv Agron 71123ndash231

Tyerman SD Niemietz CM Brameley H (2002) Plant aquaporinsmultifunctional water and solute channels with expanding rolesPlant Cell Environ 25 173ndash194

Umezawa T Yoshida R Maruyama K Yamaguchi-Shinozaki KShinozaki K (2005) SRK2C a SNF1-related protein kinase 2 im-proves drought tolerance by controlling stressresponsive gene ex-pression in Arabidopsis thaliana Proc Natl Acad Sci (USA) 10117306ndash17311

Upreti KK Murti GSR Bhatt RM (2000) Response of pea culti-vars to water stress changes in morpho-physiological charactersendogenous hormones and yield Veg Sci 27 57ndash61

Vartanian N Marcotte L Ciraudat J (1994) Drought Rhizogenesis inArabidopsis thaliana differential responses of hormonal mutantsPlant Physiol 104 761ndash767

Venuprasad R Lafitte HR Atlin GN (2007) Response to direct se-lection for grain yield under drought stress in rice Crop Sci 47285ndash293

Villar-Salvador P Planelles R Oliet J Pentildeuelas-Rubira JL JacobsDF Gonzaacutelez M (2004) Drought tolerance and transplanting per-formance of holm oak (Quercus ilex) seedlings after drought hard-ening in the nursery Tree Physiol 24 1147ndash1155

Vu JCV Gesch RW Allen LH Boote KJ Bowes G (1999) CO2 en-richment delays a rapid drought-induced decrease in Rubisco smallsubunit transcript abundance J Plant Physiol 155 139ndash142

Wagner AB Moore AL (1997) Structure and function of the plant alter-native oxidase its putative role in the oxygen defence mechanismBioscience Rep 17 319ndash333

Wahid A (2007) Physiological implications of metabolites biosynthe-sis in net assimilation and heat stress tolerance of sugarcane(Saccharum officinarum) sprouts J Plant Res 120 219ndash228

Wahid A Close TJ (2007) Expression of dehydrins under heat stressand their relationship with water relations of sugarcane leaves BiolPlantarum 51 104ndash109

Wahid A Rasul E (2005) Photosynthesis in leaf stem flower and fruitin Pessarakli M (Ed) Handbook of Photosynthesis 2nd ed CRCPress Florida pp 479ndash497

Wahid A Gelani S Ashraf M Foolad MR (2007) Heat tolerance inplants an overview Environ Exp Bot 61 199ndash223

Wan B Lin Y Mou T (2007) Expression of rice Ca(2+)-dependent pro-tein kinases (CDPKs) genes under different environmental stressesFEBS Lett 581 1179ndash1189

Wang Z Huang B (2004) Physiological Recovery of Kentucky bluegrassfrom simultaneous drought and heat stress Crop Sci 44 1729ndash1736

Wardlaw IF Willenbrink J (2000) Mobilization of fructan reserves andchanges in enzyme activities in wheat stems correlate with waterstress during kernel filling New Phytol 148 413ndash422

Wen XP Pang XM Matsuda N Kita M Inoue H Hao YJ HondaC Moriguchi T (2007) Over-expression of the apple spermidine

212 M Farooq et al

synthase gene in pear confers multiple abiotic stress tolerance byaltering polyamine titers Transgenic Res 17 251ndash263

Wery J Silim SN Knights EJ Malhotra RS Cousin R (1994)Screening techniques and sources and tolerance to extremesof moisture and air temperature in cool season food legumesEuphytica 73 73ndash83

Wilkinson S Davies WJ (2002) ABA-based chemical signalling thecoordination of responses to stress in plants Plant Cell Environ25 195ndash210

Wingler A (2002) The function of trehalose biosynthesis in plantsPhytochemistry 60 437ndash 440

Wrzaczek M Hirt H (2001) Plant MAP kinase pathways how many andwhat for Biol Cell 93 81ndash87

Xiong L Wang R Mao G Koczan JM (2006) Identification of droughttolerance determinants by genetic analysis of root response todrought stress and abscisic acid Plant Physiol 142 1065ndash1074

Yadav RS Hash CT Bidinger FR Devos KM Howarth CJ (2004)Genomic regions associated with grain yield and aspects of post-flowering drought tolerance in pearl millet across environments andtester background Euphytica 136 265ndash277

Yamada M Morishita H Urano K Shiozaki N Yamaguchi-ShinozakiK Shinozaki K Yoshiba Y (2005) Effects of free proline accumu-lation in petunias under drought stress J Exp Bot 56 1975ndash1981

Yamaguchi-Shinozaki K Shinozaki K (2004) Improving drought andcold stress tolerance in transgenic rice Proceedings of World RiceResearch Conference Tsukuba Japan 5ndash7 November 2004

Yang J Zhang J Wang Z Zhu Q Wang W (2001) Remobilization ofcarbon reserves in response to water deficit during grain filling ofrice Field Crop Res 71 47ndash55

Yang J Zhang J Liu K Wang Z Liu L (2007) Involvement ofpolyamines in the drought resistance of rice J Exp Bot 58 1545ndash1555

Yokota A Kawasaki S Iwano M Nakamura C Miyake C AkashiK (2002) Citrulline and DRIP-1 Protein (ArgE Homologue) inDrought Tolerance of Wild Watermelon Ann Bot 89 825ndash832

Young TE Meeley RB Gallie DR (2004) ACC synthase expressionregulates leaf performance and drought tolerance in maize Plant J40 813ndash825

Zeid IM Shedeed ZA (2006) Response of alfalfa to putrescine treat-ment under drought stress Biol Plant 50 635ndash640

Zhang M Duan L Zhai Z Li J Tian X Wang B He Z Li Z (2004)Effects of plant growth regulators on water deficit-induced yieldloss in soybean Proceedings of the 4th International Crop ScienceCongress Brisbane Australia

Zhang X Zhang Z Chen J Chen Q Wang X Huang R (2005)Expressing TERF1 in tobacco enhances drought tolerance and ab-scisic acid sensitivity during seedling development Planta 222494ndash501

Zhao J Ren W Zhi D Wang L Xia G (2007) ArabidopsisDREB1ACBF3 bestowed transgenic tall fescue increased toler-ance to drought stress Plant Cell Rep 26 1521ndash1528

Zhao TJ Sun S Liu Y Liu JM Liu Q Yan YB Zhou HM (2006)Regulating the drought-responsive element (DRE)-mediated sig-naling pathway by synergic functions of trans-active and trans-inactive DRE binding factors in Brassica napus J Biol Chem 28110752ndash10759

Zhou Y Lam HM Zhang J (2007) Inhibition of photosynthesis andenergy dissipation induced by water and high light stresses in riceJ Exp Bot 58 1207ndash1217

Zhu JK (2002) Salt and drought stress signal transduction in plantsAnnu Rev Plant Biol 53 247ndash273

Zinselmeier C Jeong B-R Boyer JS (1999) Starch and the control ofkernel number in Maize at low water potentials Plant Physiol 12125ndash35

Introduction

Effects of drought on plants

Crop growth and yield

Water relations

Nutrient relations

Photosynthesis

Stomatal oscillations

Photosynthetic enzymes

Adenosine triphosphate synthesis

Assimilate partitioning

Respiration

Oxidative damage

Drought resistance mechanisms

Morphological mechanisms

Escape

Avoidance

Phenotypic flexibility

Physiological mechanisms

Cell and tissue water conservation

Antioxidant defense

Cell membrane stability

Plant growth regulators

Compatible solutes and osmotic adjustment

Molecular mechanisms

Aquaporins

Stress proteins

Signaling and drought stress tolerance

Managing drought stress

Selection and breeding strategies

Molecular and functional genomics approaches

Induction of drought resistance

Seed priming

Use of plant growth regulators

Use of osmoprotectants

Silicon

Conclusion

References

Agron Sustain Dev 29 (2009) 185ndash212ccopy INRA EDP Sciences 2008DOI 101051agro2008021

Review article

Available online atwwwagronomy-journalorg

for Sustainable Development

Plant drought stress effects mechanisms and management

M Farooq1 3 A Wahid2 N Kobayashi3 D Fujita3 SMA Basra4

1 Department of Agronomy University of Agriculture Faisalabad-38040 Pakistan2 Department of Botany University of Agriculture Faisalabad-38040 Pakistan

3 International Rice Research Institute (IRRI) DAPO Box 7777 Metro Manila Philippines4 Department of Crop Physiology University of Agriculture Faisalabad-38040 Pakistan

(Accepted 3 April 2008)

Abstract ndash Scarcity of water is a severe environmental constraint to plant productivity Drought-induced loss in crop yield probably exceedslosses from all other causes since both the severity and duration of the stress are critical Here we have reviewed the effects of droughtstress on the growth phenology water and nutrient relations photosynthesis assimilate partitioning and respiration in plants This article alsodescribes the mechanism of drought resistance in plants on a morphological physiological and molecular basis Various management strategieshave been proposed to cope with drought stress Drought stress reduces leaf size stem extension and root proliferation disturbs plant waterrelations and reduces water-use efficiency Plants display a variety of physiological and biochemical responses at cellular and whole-organismlevels towards prevailing drought stress thus making it a complex phenomenon CO2 assimilation by leaves is reduced mainly by stomatalclosure membrane damage and disturbed activity of various enzymes especially those of CO2 fixation and adenosine triphosphate synthesisEnhanced metabolite flux through the photorespiratory pathway increases the oxidative load on the tissues as both processes generate reactiveoxygen species Injury caused by reactive oxygen species to biological macromolecules under drought stress is among the major deterrents togrowth Plants display a range of mechanisms to withstand drought stress The major mechanisms include curtailed water loss by increaseddiffusive resistance enhanced water uptake with prolific and deep root systems and its efficient use and smaller and succulent leaves to reducethe transpirational loss Among the nutrients potassium ions help in osmotic adjustment silicon increases root endodermal silicification andimproves the cell water balance Low-molecular-weight osmolytes including glycinebetaine proline and other amino acids organic acids andpolyols are crucial to sustain cellular functions under drought Plant growth substances such as salicylic acid auxins gibberrellins cytokininand abscisic acid modulate the plant responses towards drought Polyamines citrulline and several enzymes act as antioxidants and reduce theadverse effects of water deficit At molecular levels several drought-responsive genes and transcription factors have been identified such as thedehydration-responsive element-binding gene aquaporin late embryogenesis abundant proteins and dehydrins Plant drought tolerance can bemanaged by adopting strategies such as mass screening and breeding marker-assisted selection and exogenous application of hormones andosmoprotectants to seed or growing plants as well as engineering for drought resistance

drought response stomatal oscillation osmoprotectants hormones stress proteins drought management CO2

1 INTRODUCTION

Faced with scarcity of water resources drought is the singlemost critical threat to world food security It was the catalystof the great famines of the past Because the worldrsquos watersupply is limiting future food demand for rapidly increasingpopulation pressures is likely to further aggravate the effectsof drought (Somerville and Briscoe 2001) The severity ofdrought is unpredictable as it depends on many factors such asoccurrence and distribution of rainfall evaporative demandsand moisture storing capacity of soils (Wery et al 1994)

Investigations carried out in the past provide consider-able insights into the mechanism of drought tolerance in

Corresponding author farooqcpgmailcom mfarooqcgiarorg

plants at molecular level (Hasegawa et al 2000) Three mainmechanisms reduce crop yield by soil water deficit (i) re-duced canopy absorption of photosynthetically active radia-tion (ii) decreased radiation-use efficiency and (iii) reducedharvest index (Earl and Davis 2003) The reproducibility ofdrought stress treatments is very cumbersome which signif-icantly impedes research on plant drought tolerance A slowpace in revealing drought tolerance mechanisms has hamperedboth traditional breeding efforts and use of modern genet-ics approaches in the improvement of drought tolerance ofcrop plants (Xiong et al 2006) Although plant responsesto drought are relatively well known plant performance un-der a more complex environment where multiple stresses co-occur is fragmentary That is why the plants have to respond

Article published by EDP Sciences

186 M Farooq et al

cell division

Diminished growth

188 M Farooq et al

22 Water relations

24 Photosynthesis

Stomatal closure

ABA-signalling

Down-regulation of

ROS production

Attack onmembranes

190 M Farooq et al

26 Respiration

O2-e- e-

O23- O-

H2OWater

2H+ H+

OHHydroxylradical

e-3O2 O2-

H2OWater

Oxide ion

Oxeneion

Peroxideion

Hydrogen peroxide

Singlet oxygen

27 Oxidative damage

192 M Farooq et al

311 Escape

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

186 M Farooq et al

cell division

Diminished growth

188 M Farooq et al

22 Water relations

24 Photosynthesis

Stomatal closure

ABA-signalling

Down-regulation of

ROS production

Attack onmembranes

190 M Farooq et al

26 Respiration

O2-e- e-

O23- O-

H2OWater

2H+ H+

OHHydroxylradical

e-3O2 O2-

H2OWater

Oxide ion

Oxeneion

Peroxideion

Hydrogen peroxide

Singlet oxygen

27 Oxidative damage

192 M Farooq et al

311 Escape

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

188 M Farooq et al

22 Water relations

24 Photosynthesis

Stomatal closure

ABA-signalling

Down-regulation of

ROS production

Attack onmembranes

190 M Farooq et al

26 Respiration

O2-e- e-

O23- O-

H2OWater

2H+ H+

OHHydroxylradical

e-3O2 O2-

H2OWater

Oxide ion

Oxeneion

Peroxideion

Hydrogen peroxide

Singlet oxygen

27 Oxidative damage

192 M Farooq et al

311 Escape

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

188 M Farooq et al

22 Water relations

24 Photosynthesis

Stomatal closure

ABA-signalling

Down-regulation of

ROS production

Attack onmembranes

190 M Farooq et al

26 Respiration

O2-e- e-

O23- O-

H2OWater

2H+ H+

OHHydroxylradical

e-3O2 O2-

H2OWater

Oxide ion

Oxeneion

Peroxideion

Hydrogen peroxide

Singlet oxygen

27 Oxidative damage

192 M Farooq et al

311 Escape

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

Stomatal closure

ABA-signalling

Down-regulation of

ROS production

Attack onmembranes

190 M Farooq et al

26 Respiration

O2-e- e-

O23- O-

H2OWater

2H+ H+

OHHydroxylradical

e-3O2 O2-

H2OWater

Oxide ion

Oxeneion

Peroxideion

Hydrogen peroxide

Singlet oxygen

27 Oxidative damage

192 M Farooq et al

311 Escape

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

190 M Farooq et al

26 Respiration

O2-e- e-

O23- O-

H2OWater

2H+ H+

OHHydroxylradical

e-3O2 O2-

H2OWater

Oxide ion

Oxeneion

Peroxideion

Hydrogen peroxide

Singlet oxygen

27 Oxidative damage

192 M Farooq et al

311 Escape

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

26 Respiration

O2-e- e-

O23- O-

H2OWater

2H+ H+

OHHydroxylradical

e-3O2 O2-

H2OWater

Oxide ion

Oxeneion

Peroxideion

Hydrogen peroxide

Singlet oxygen

27 Oxidative damage

192 M Farooq et al

311 Escape

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

192 M Farooq et al

311 Escape

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

312 Avoidance

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

194 M Farooq et al

Well-watered

Drought stress

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

Proteins Lipids DNA

2- H2O2)

CAT SODAPX

PODGR AA

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

196 M Farooq et al

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

Drought stress

ReceptorH2O2

ABACa+2

Protein Kinases

Salicylic acid

accumulation

Stomatal closure

Drought tolerance

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

198 M Farooq et al

Hydrated

De-hydrated

(c)(b)

Protection Degraded

Protein

Compatible solute

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

331 Aquaporins

332 Stress proteins

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

200 M Farooq et al

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

202 M Farooq et al

431 Seed priming

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

204 M Farooq et al

434 Silicon

5 CONCLUSION

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

REFERENCES

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

206 M Farooq et al

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

208 M Farooq et al

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

210 M Farooq et al

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

212 M Farooq et al

Introduction


Water relations

Nutrient relations

Photosynthesis





Respiration

Oxidative damage



Escape

Avoidance




Antioxidant defense





Aquaporins

Stress proteins






Seed priming



Silicon

Conclusion

References

Documents

Plant drought stress: effects, mechanisms and management · 2017. 7. 5. · Plant drought stress: eﬀects, mechanisms and management 187 Table I. Economic yield reduction by drought