Climate Change and Plant Abiotic Stress Tolerance || Drought Stress Responses in Plants, Oxidative Stress, and Antioxidant Defense

9

Drought Stress Responses in Plants, Oxidative Stress,

and Antioxidant Defense

Mirza Hasanuzzaman, Kamrun Nahar, Sarvajeet Singh Gill, and Masayuki Fujita

Abstract

Global climate change is currently viewed as the most devastating threat to theenvironment, and is now gaining considerable attention from farmers, research-ers, and policy makers because of its major influence on agriculture. Thesituation is becoming more serious due to gradual increases in the complexnature of the environment, and due to the unpredictability of environmentalconditions and global climate change. One of the most acute environmentalstresses presently affecting agriculture is drought, which has pronouncedadverse effects on the growth and development of crop plants. The effects ofdrought stress are expected to increase further with increases in climate changeand a growing water crisis. Drought stress usually leads to reductions in cropyield, which can result from many drought-induced morphological, physiologi-cal, and metabolic changes that occur in plants. A key sign of drought stress atthe molecular level is the accelerated production of reactive oxygen species (ROS)such as singlet oxygen (1O2), superoxide (O2

��), hydrogen peroxide (H2O2), andhydroxyl radicals (OH�). The excess production of ROS is common in manyabiotic stresses, including drought stress, and results from impaired electrontransport processes in the chloroplasts and mitochondria. One of the majorcauses of ROS production under drought stress is photorespiration, whichaccounts for more than 70% of the total H2O2 produced. Plants have endogenousmechanisms for adapting to ROS production and are thought to respond todrought stress by strengthening these defense mechanisms. Therefore, enhance-ment of the functions of the naturally occurring antioxidant components(enzymatic and non-enzymatic) may be one strategy for reducing or preventingoxidative damage and improving the drought resistance of plants. In this chapter,we review the most recent reports on drought-induced responses in plants,focusing on the role of oxidative stress as well as on other possible mechanismsand examining how different components of the antioxidant defense system mayconfer tolerance to drought-induced oxidative stress.

209

Climate Change and Plant Abiotic Stress Tolerance, First Edition. Edited by Narendra Tuteja and Sarvajeet S. Gill.� 2014 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2014 by Wiley-VCH Verlag GmbH & Co. KGaA.

9.1

Introduction

The human population continues to increase unabated. It is estimated that therewill be 9 billion people on this planet in 2050 and this will require a doubling offood production. To meet this challenge, we must increase the yield potential of ourfood crops and close the yield gap. The average yield of most crops is about halftheir potential yield; this yield gap is due to losses caused by biotic and abioticstresses [1,2]. Abiotic stresses are the greatest restriction for crop productionworldwide and account for yield reductions of as much as 50% [3,4]. Crop plants, assessile organisms, encounter unavoidable abiotic stresses during their life cycles,including salinity, drought, extreme temperatures, metal toxicity, flooding, UV-Bradiation, ozone, and so on, which all pose a serious challenge to plant growth,metabolism, and productivity [5–15]. Among these abiotic stresses, drought is themost complex and devastating on a global scale [16], and its frequency is expectedto increase as a consequence of climate change [17]. Water shortages are expectedto lead to global crop production losses of up to 30% by 2025, compared to currentyields, according to the Water Initiative report of The World Economic Forum(2009) at Davos [18]. Consequently, drought stress represents a major threat forsustaining food security under current conditions and will be more of a danger inthe future, as climate change is projected to induce more frequent and moreintense higher temperatures and drier conditions in many regions of the world[19–23].Most crop plants show a wide genotypic variability and wide range of crop

damage in response to drought stress [9,24,25]. The primary effect of droughtstress is largely a reduction in plant growth, which depends on cell division, cellenlargement, and differentiation, and involves genetic, physiological, ecological,and morphological events, and their complex interactions. These events areseriously inhibited by drought stress, which adversely affects a variety of vitalphysiological and biochemical processes in plants, including stomatal conduc-tance, membrane electron transport, carbon dioxide (CO2) diffusion, carboxyla-tion efficiency, water-use efficiency (WUE), respiration, transpiration, water loss,photosynthesis, and membrane functions. Disruption of these key functionslimits growth and developmental processes, and leads to reductions in finalcrop yield [26] (Figure 9.1).Drought stress, like other kinds of abiotic stresses, exacerbates the production of

reactive oxygen species (ROS) such as superoxide (O2��), singlet oxygen (1O2),

hydrogen peroxide (H2O2), and hydroxyl radicals (OH�) to levels that are oftenbeyond the plant’s scavenging capacity. This causes oxidative stress that damagescells and cellular components, disrupts the physiological and biochemical lifeprocesses, and even leads to plant death [27–30]. Improvements in tolerance andresistance to drought stress will require intensive studies, and researchers are nowfocusing on oxidative stress as one of the basic damage responses in almost allkinds of stress. In this chapter, we review the effect of drought stress on plantgrowth and physiology. We also review recent reports on drought-induced oxidative

210 9 Drought Stress Responses in Plants, Oxidative Stress, and Antioxidant Defense

stress in plants and examine the antioxidant defense mechanisms that offerprotection against environmental stresses such as drought.

9.2

Plant Response to Drought Stress

9.2.1

Germination

Seed germination is one of the most important phases in the life cycle of aplant, considering the fact that if there is no germination there is no plant, and

Figure 9.1 Possible effects of drought stress

in plants. Reduced water uptake results in a

decrease in tissue water content and

reduction in turgidity due to drought. Under

drought stress conditions, cell elongation in

higher plants is inhibited by reduced turgor

pressure. Drought stress also impair mitosis,

cell elongation, and expansion, which results

in growth reduction. Severe drought

conditions limit photosynthesis due to a

decrease in the enzyme activities required for

photosynthesis. Drought stress disturbs the

balance between the production of ROS and

the antioxidant defense, causing oxidative

stress. The final consequence of drought

stress is a reduction of yield.

9.2 Plant Response to Drought Stress 211

is highly responsive to its existing surrounding environment [31]. Drought isone of the major environmental factors that determines the success or failure ofplant establishment because in order to germinate one of the primerequirements is the presence of water [32]. The study of drought toleranceduring germination, and early and late growth of plants is important fordetermining dry limits at each developmental phase [31]. Drought stressdecreases germination and seedling growth, which lead to a reduction of plantgrowth and yield at later stages [32]. Poly(ethylene glycol) (PEG) density withosmotic potentials of 0, �0.4, �0.8 and �1.2MPa was imposed upon 12 typesof synthetic wheat. Germination rate, germination index, mean emergencetime, final germination percentage, and germination rate index were deter-mined. The results showed that there were significant negative effects ofdrought on the above-mentioned parameters, and there were differences amongdifferent levels of osmotic potentials and genotypes for all the characteristics[33]. Maraghni et al. [34] conducted drought experiments with Ziziphus lotus byapplying PEG-6000. Germination was highest (100%) in deionized watercontrols, while germination percentages declined with a decrease in osmoticpotential and the germination rate decreased with decreasing water potentialfrom 0 to �1.0MPa. Less than 5% of the seeds germinated at �1.0MPa. With areduction of osmotic potential, the number of days to first germination wasdelayed. The mean time to germination was significantly affected by PEG-6000treatment [34]. While studying the medicinal plant Thymus sp., four osmoticpotential levels of drought stress were imposed: PEG-6000 of 0 (control), �3,�6, and �9 bar. All drought stress treatments showed a significant reduction ingermination percentage and germination rate [35]. In tomato, the germinationpercentages were 99%, 90%, 92%, and 90%, and emergence percentages were92%, 78%, 79%, and 81%, respectively, under the treatments of control, earlystress (when the first truss has set the fruits), middle stress (when fruits in thefirst truss were fully matured and started changing color), and late stress (whenfruits on the first truss were ripened fully) [36]. Germination of the sunflower(Helianthus annuus L.) was studied using distilled water as control and underosmotic potentials of �0.3, �0.6, �0.9, and �1.2MPa imposed by PEG-6000.Germination percentage was influenced and inhibited by PEG. The germinationpercentages under �0.3, �0.6, and �0.9MPa PEG treatment were 99%, 96%,and 27%, respectively. None of the seeds was able to germinate at �1.2MPaPEG. The drought stress was not only accompanied by inhibition of germina-tion, but also by an increase of abnormal germination and seedling. With adecrease in osmotic potential, the mean germination time increased, causingdelayed seedling emergence [37]. In fenugreek (Trigonella foenum-graecum L.),PEG-6000 at osmotic levels of 0 (as control), �3, �6, and �9 bar was used, andgermination percentages for these values were 98%, 87%, 77%, and 67%,respectively. The germination velocities were 12%, 8%, 5%, and 4% under thesame conditions. Therefore, the seed germination percentage and velocityreduced with increasing drought [38]. The effect of drought stress was


investigated at water potentials of �0.2 and �0.4MPA (by using PEG-6000) onokra (Hibiscus esculents L.) germination and seedling growth. In this study,percent germination, average time necessary for germination (days), radical andplumule length, and fresh and dry weight of okra seedlings were measured.Data from this investigation showed that germination percent at an osmoticpotential �0.4MPa decreased in comparison to control, but at an osmoticpotential �0.2MPa the result was insignificant. Maximum seed germinationwas dependent to seeds only to �0.4MPa osmotic potential. Compared to thecontrol, drought stress resulted in a reduction of fresh and dry weight andlength of radical and plumule [39].The drought effect on germination also differs depending on genotypes,

although the effect is negative indiscriminately. The effect of drought stress in12 wheat genotypes in levels of 0 as control and –0.5MPa of PEG as water stresswas studied on germination and seedling growth. Results showed that all of themeasured parameters were affected by genotypes and drought treatment as well.Among the 12 genotypes, the highest percentage of germination was observed inSabalan and 4041, which was 96%, and the lowest was in Sissons (55%). Thehighest germination rate was in Gobustan and 4041 with a mean of 0.15, andthe lowest was in Gascogne with average of 0.143. Not only the germination butalso the growth of primary seedlings was also affected by drought. The highestprimary root length (average 8.02 cm) was found in genotype Gobustan and thelowest was in Saratovskaya-29 (average 3.32 cm). The highest and the lowestseedling fresh weights were 1.227 and 1.162 g in the genotypes Gobustan andSissons, respectively. The highest germination index and germination rate indexwere observed in genotype 4041 with averages of 3.947 and 391.67 g,respectively, and the lowest were in the genotype Sissons with an average of53.05 and 127.93 g, respectively [40]. Although sesame (Sesamum indicum L.) is adrought-tolerant oilseed crop, it is sensitive to drought at the germination andseedling stages [41]. Bahrami et al. [31] conducted a study with five sesamecultivars (Oltan, Felestin, Borazjan-5, Safiabad, and Karaj-1) and four levels ofdrought (0, �2.0, �4.5, and �6.6 bar). They responded differently at differentdrought stresses, although the effect was negative (i.e., with the increase ofdrought stress the seedlings of all varieties performed badly). At the highestdrought stress of �6 bar the percent germination was 66%, 43%, 93%, 22%, and82%; the root length was 0.2, 0.5, 1.3, 0.3, and 0.4 cm; the shoot length was 0.3,0.2, 0.6, 0.1, and 0.8 cm; the root dry weight was 2.7, 2.1, 4.3, 2.5, and 2.3mg;and the shoot dry weight was 1.5, 1.2, 5.2, 0.7, and 4.4mg in the varieties ofOltan, Felestin, Borazjan-5, Safiabad, and Karaj-1 respectively [31]. Mensah et al.[42] treated sesame with �0.0 (control), �0.025, �0.125, �0.2500, and�0.5000MPa drought levels, and found that the seed germination was 97, 96.6,97, 74, and 70%, respectively. Drought stress effected a significant reduction ofgermination percentage. Reduction of seedling growth was also observed byHamidi and Safarnejad [43] in alfalfa cultivars, Mostafavi et al. [44] in cornhybrids, and Zaefizadeh et al. [45] on wheat genotypes.


9.2.2

Plant Growth

The cell is the basic structural unit of all living organisms. For cell growth oneof the most basic requirements is water that causes cell expansion, whichfurther results in cell growth, although the cell division process is less affectedby drought as compared to cell expansion [46]. Thus, reduced cell growth due towater scarcity affects growth at the whole-plant level also (Figure 9.2). Droughtcauses growth reduction in multiple ways. Drought inhibits cell expansion, andreduces stomatal opening and carbohydrate supply, ultimately decreasinggrowth and productivity [47,48]. Moreover, drought can reduce the decomposi-tion process and thus nutrient availability [49]. Extreme drought hampers thephotosynthetic pigments and apparatus, and alters biochemical reactions relatedto photosynthesis, and thus leads to reduced productivity [50]. Sometimes it iscommon that drought in combination with heat tends to exacerbate heatresponses by reducing transpirational cooling and therefore increasing leaftemperature [51–53]. So, plants fall in the worst condition in two ways: (i) due tohigh temperature plants need more water for transpiration, which is lackingdue to drought, and (ii) heat enhances the drought condition more rapidly. Thisindirect effect of heat may have a larger impact on plants than heat or droughtstress alone [50,51].While studying with osmotic potentials of �0.3, �0.6, �0.9 and �1.2MPa

(induced by PEG-6000), early seedling growth after germination was inhibited insunflower (H. annuus), which was highly significant. The radicle growth was 11.0,9.6, and 6.4 cm at control, �0.3, and �0.6 treatment; and after that radicle growthstopped with any further decrease of water potential. Shoot length was 10.3 and1.9 cm under control and 0.3MPa, but the shoot growth was inhibited totally underall other treatments. Seedling fresh weight gradually declined with decreasingosmotic potential of solutions. A drought stress-induced increase of abnormalseedlings was observed in this study [37]. Sadeghian and Yavari [54] also reportedthat increasing drought stress resulted in increasing abnormal seedlings in sugar

Figure 9.2 Drought stress-induced growth reduction (a) and wilting (b) in rice (O. sativa) and jute

(Corchorus capsularis) plants.


beet. Drought stress decreased the root length in various plant species like wheatand maize [55]. In medicinal plant Thymus sp. all drought stress treatments (�3,�6, and �9 bar) caused a significant reduction in root length and shoot lengthcompared with control treatment [35]. In rice, drought stress caused a 50–60%reduction in relative water content (RWC) and caused rolling of the flag leaf [25].When Pervez et al. [36] grew tomato plants with four treatments (i.e. control, earlystress (when the first truss has set the fruits), middle stress (when fruits in the firsttruss were fully matured and started changing color), and late stress (when fruitson the first truss were ripened fully)), the well-watered plants produced tallerplants. The plant height under the above-mentioned treatments were 79.2, 73.2,73.5, and 77.5 cm, respectively, where the numbers of leaves per plant were 18.0,16.5, 16.7, and 17.2, respectively. Shoot dry weight per plant were 40.3, 34.9, 34.8,and 36.6 g, respectively. Considering these parameters it can be concluded thatearly-stage drought stress is more harmful [36]. In rice, the reduction of plantheight under drought ranged between 4.3 and 20.9 cm according to the drought-tolerance level of the genotypes [56]. Normal irrigation and drought stress producedwheat plants with 86.27 and 78.77 cm plant height, and 3.66 and 2.50 tillers perplant, respectively [57]. In chickpea (Cicer arietinum L.), the tallest plants wereproduced when they were grown without drought stress [58]. The biodiesel cropJatropha curcas L. is well adapted to arid and semi-arid climate conditions.Seedlings (71-day-old) of J. curcas were subjected to a continuous well-watered(control) or a drought stress period followed by rewatering. Stress was applied byreducing irrigation (10% reduction every 2 days on the weight base) for 28 daysuntil a field capacity reached up to 15% (maximum stress), followed by 1 weekunder well-watered conditions. Plant growth, stem elongation, leaf emergence, andtotal leaf area were found to reduce under drought as compared to control [59].Díaz-L�opez et al. [60] conducted a study where 4-week-old J. curcas seedlings weregrown in growth chambers with five different water regimes corresponding to100%, 75%, 50%, 25%, and 0% field capacity for 4 weeks. Drought treatmentsreduced leaf, stem, and root growth. The decrease in growth was higher in theaerial part of the plant than in the root, which results in increase in the root/shootratio in drought-stressed plants compared to the well-watered plants [60]. Theperformance of two endemic species, Salix paraqplesia and Hippophae rhamnoides,was evaluated under different drought stress treatments, 80%, 40%, and 20% fieldwater capacity, which was performed in the ecotone between the Minjiang dryvalley and mountain forest. Drought stress severely reduced height, basal diameter,leaf number, and biomass production. Drought enhances the increase of below-ground plant parts that renders an increase in the root/shoot ratio. Theaccumulations of C, N, and P of both species were reduced in drought. Comparedwith S. paraqplesia under medium drought stress (40% field capacity), H.rhamnoides showed less change of morphological characteristics [60]. Droughtstress was applied for 12 days in 30-day-old melon plants by decreasing irrigationwater gradually and finally irrigation was completely stopped. At the end of theexperiment shoot dry weight, osmotic potential, leaf water potential, and stomatalconductance were lower in drought-sensitive genotypes (CU 40 and CU 252) than


the resistant genotypes (CU 159 and CU 196). At the end of 12 days, dry weight wasreduced by 63.99% in sensitive genotype CU 252 under drought stress and it wasdecreased by 26% in resistant genotype CU 196. The osmotic potential decreased to562% in sensitive genotypes CU 40 and CU 252, and it decreased to 118% inresistant genotypes CU 159 and CU 196. On average, the leaf water potentialdecreased by 50% under drought stress [62]. Leaf area expansion is often reducedunder drought and in that case the transpiration surface is drastically decreased.Leaf expansion is one of the most sensitive growth processes limited by drought.Due to mild drought, a reduction in leaf numbers, rate of expansion, and final leafsize are most common. Under severe stress, a decrease in rate of leaf elongationand leaf growth is common, which may also stop under severe conditions. Droughtalso reduces total leaf area and hampers the initiation of new leaves [46]. Thameuret al. [63] examined two barley varieties under normal water (100% field capacity)and drought stress (50% field capacity). Under water-deficit stress, due to acombination of leaf growth reduction and abscission, leaf area was sharplyreduced. Among the two varieties of barley (Tlalit and Switir) the RWC in well-watered plants ranged from 89% to 91%; however, the leaf area was highest inSwitir (8 cm2). Leaf area and RWC are both positively correlated under well-wateredconditions. Leaf area was higher in control treatment as compared to the drought-stressed ones. Leaf area ratio was higher in Tlalit under non-stressed conditions(3 leaf day�1 plant�1) than Switir (2 leaf day�1 plant�1). The decreases in the RWCwere about 74 and 78%, respectively, in the tillering stage in Switir and Tlalit underdrought, but at anthesis RWC decreased to reach 68% and 73% in the respectivevarieties. Due to drought the decreased leaf area ratio in Switir was 7%, while Tlalitshowed a higher reduction of about 31% [63]. However, the reduction in leaf areaunder water deficit in plants can result in a survival strategy in order to reduce thearea available for transpiration. Continued drought stress can hasten leafsenescence [64]. Death of leaf tissue and leaf drop, particularly of old and matureleaves, may occur, which is more prominent in post-flowering or gain-filling stages;these are considered as drought-avoiding mechanisms also [46]. In peanut (Arachishypogaea L.), a 34–67% reduction in biomass production was observed due todrought by Haro et al. [65]. Under drought stress plants tend to increase root lengthin order to obtain more water from the deeper soil levels. Increased below-groundbiomass is a common response to drought as reported by many researchers [47,66],but under the same conditions decreased shoot biomass is an unavoidablephenomenon [66], which ultimately results a lower total biomass [50].

9.2.3

Plant---Water Relations

Drought stress has a great impact on plant–water relations. The major attributesthat are effected by drought are RWC, leaf water potential, osmotic potential,pressure potential, and transpiration rate [67]. Water potential, broadly, connotesreducing water loss through evaporation through the roots. Water potentialsignificantly declined in roots, leaves, and pods under drought in general; however,


root water potential dropped much earlier than in leaves and pods [68]. Thereduction of water potential is also greatly dependent on crop species, varieties, andlevel of stress. This is due to differences of their tolerance to drought. For instance,drought-tolerant genotypes maintained a higher leaf water potential for longer andwilted later than sensitive genotypes upon exposure to drought [69]. Tissue watercontents decreased linearly with increased severity of drought [70]. WUE is alsogreatly affected by drought, but this effect is dependent on the crop species andvarieties. In potato (Solanum tuberosum L.), early-season drought substantiallyreduced WUE [71]. However, Abbate et al. [72] and Subramanian et al. [73] reportedhigher WUE in wheat and tomato under drought than well-watered controls, whichwas mainly due to the reduced transpiration rates under drought. Crop stage is alsoimportant in defining the effect of drought on WUE. For instance, drought stressdecreased WUE in sunflower; however, the extent of the reduction was significantlyhigher when stress was imposed at flowering than at budding [74].

9.2.4

Stomatal Conductance and Gas Exchange

Stomatal closure is one of the earliest plant responses under drought concomitantwith the reduced water potential and turgor associated with even a small decreasein RWC [75]. Stomatal conductance is important considering the fact that it has aclose association with many physiological parameters, such as electron transportrate, carboxylation efficiency, WUE, respiration, transpiration, limited watertransportation, and CO2 diffusion. As studied by many researchers, stomatalconductance is affected by drought [75,76]. Drought-sensitive and drought-tolerantplant shows different stomatal movements in response to water-deficit conditions.Stomatal conductance and carbon assimilation are maintained in drought-sensitivecrops after the water potential falls [77], whereas in drought-adapted plants thestomata may be closed in dry and hot environments in the presence of a high tissuewater content [78]. Both hydraulic and chemical signals sent from drying roots tothe shoot are involved in the regulation of stomatal closure and decreased growthduring soil drying [79]. According to Medrano et al. [80], stomatal conductance isdependent on some factors that are also altered by drought; among which areexternal factors such as soil water availability, vapor pressure deficit, and so on, andinternal factors such as abscisic acid (ABA), xylem conductivity, leaf water status,and so on. Under drought a chemical signal is produced by ABA in plant roots,which is synthesized in the roots in response to soil drying. This signal istransported from the root to leaf through the xylem by the transpiration stream;this is thought to induce stomatal closure [80,81]. Some other factors likeprecursors of ABA or cytokinins, mineral composition, and pH of the xylem have arole in stomatal movement [82]. A decrease in pH of the xylem causes ABAHtransportation into alkaline components of the leaf cell symplast, which is awayfrom the sites of action of ABA on the stomata. On the other hand, the rate ofionized ABA transportation in the xylem sap increases under increased pH [83].Thus, the acidic and alkaline pH determines the stomatal movement to a great


extent [84]. It was also revealed that drought-induced xylem sap pH of herbaceousspecies is more responsible for stomatal movement as compared to woodyperennials [84].Stomatal closure has a strong interaction with photosynthesis. In addition,

due to the presence of the stomatal pores on plant leaf surfaces, waterevaporates through the stomatal openings causing plants to lose water. Over95% of water loss from plants can occur by evaporation (transpiration) throughthe stomatal pores. Therefore, it is important for plants to be able to balance theamount of CO2 being brought into the plant with the amount of water escapingas a result of the open stomatal pores [85,86]. Stomata close progressively asdrought progresses, followed by parallel decreases of net photosynthesis. AsCO2 availability in the chloroplasts depends on stomatal conductance, it hasbeen frequently assumed that drought decreases photosynthesis simply byclosing stomata and limiting CO2 availability. However, stomatal conductance iscontrolled not only by soil water availability, but a complex interaction of factorsinternal and external to the leaf [87] (Figure 9.3). It was reported that leaf waterstatus and, in particular, the hydrostatic pressure or turgor strongly interactedwith stomatal conductance and transpiration. Although a strong correlation isobserved between leaf water potential and stomatal conductance, the preciserelationship is mostly dependent on species or cultivars, drought duration, plantarchitecture, environmental conditions, and so on [88].There are many examples related to stomatal movement under water-deficit

conditions. A study was conducted by Mafakheri et al. [58] with three chickpea(C. arietinum) varieties: Bivaniej (kabuli), ILC482 (kabuli), and Pirouz (desi).

Figure 9.3 Regulation of stomatal aperture by drought and other environmental factors. PAR,

photosynthetically active radiation.


Stomatal conductance and transpiration decreased in all the varieties subjected todrought stress. It was concluded that as one of the first responses of plants todrought is stomatal closure, this causes a restriction of gas exchange between theatmosphere and the inside of the leaf. Stomatal conductance has a relation withcrop yield. In this experiment, Pirouz showed the lowest stomatal conductance andseed yield under drought stress, and Bivaniej showed the best performanceconsidering those factors [57]. Naithani et al. [76] reported that atmosphericdrought regulates stomatal closure, whereas the combination of atmospheric andsurface drought controls leaf transpiration. Although drought-induced stomatalclosure is a limitation for photosynthesis, it is considered a effective mechanism forpreventing water loss. Quinoa (Chenopodium quinoa Willd.) plants have a sensitivestomatal closure, by which the plants are able to maintain leaf water potential andphotosynthesis, and increase WUE. At drought stress, root-originated ABA plays asignificant role in stomata movement of quinoa; here, ABA plays a regulatory rolein drought-induced decrease of turgor of stomata guard cells and its closure [89]. Inthe Mediterranean environment different varieties of durum wheat (Triticumdurum Desf.) were evaluated under rainfed-induced drought and artificiallyirrigated conditions. Although genotypic variation was observed in differentparameters, the overall effect was that compared to the irrigation treatment due todrought, stomatal conductance was reduced, which might be the cause of thereduction in the CO2 exchange rate and the ratio of internal CO2 concentration toambient CO2 concentration, and these ultimately reduced the grain number atmaturity, grain yield, and biomass production [90].Under drought a reduction in the activity of Hþ-pumping ATPases associated

with the root xylem is responsible for increased alkalinity of the xylem sap, which isalso seen in plant responses to other stresses [91]. This event has a role in bufferadjustment to a stressful pH of between 6.4 and 7.0 that renders stomatal closureand reduces leaf growth [82]. However, this response may change according to theplant type and extent of stress. In soybean, no significant difference in pH betweendrought-stressed and fully watered plants was seen [92]. As described by manyauthors, drought directly affects the internal transport of CO2 and enzyme activity,which become more prominent in relation to stomatal limitation [93]. Stomatalclosure and a reduction in mesophyll conductance due to water stress result in areduction of CO2 to the carboxylation site and thus photosynthesis is affected[78,94].

9.2.5

Photosynthesis

Like other physiological processes, photosynthesis is also influenced by environ-mental factors, of which limited water or drought is a major stress. Drought affectsphotosynthesis in multidimensional ways. It has an adverse effect on thephotosynthetic apparatus, and the membrane, enzymes, and absorption processes[95]. Drought-induced modification of organelle movement also affects photosynth-esis to a great extent. Upon imposition of drought one of the prime responses of


plants is closing or little movement of stomata to reduce water loss by transpiration,which is more prominent in plant species from drought-prone areas [78,96].Drought stress affects photosynthesis by reducing leaf area, enhancing stomatalclosure, decreasing water status in the leaf tissues, reducing the rate of CO2

assimilation, causing ultrastructural changes in chloroplasts, affecting electrontransport and CO2 assimilation reactions impairing ATP synthesis and ribulosebisphosphate (RuBP) generation, and altering the level of photosynthates in thetissues [97] (Figure 9.4). Water stress causes an imbalance in the hormone level inplants. Due to alteration in the hormonal balance, concentrations of many of thekey enzymes of photosynthesis decline in water-stressed plants (Figure 9.4).Drought stress causes a decrease in RWC and water potential of leaves,progressively decreasing stomatal conductance, leading to a decline in CO2 molarfraction in chloroplasts, decreased CO2 assimilation, and reduced rate ofphotosynthesis [98]. Stomatal closure is among the earliest responses of plantssubjected to water stress and it is generally assumed to be the main cause of thedrought-induced decrease in photosynthesis because stomatal closure leads to adecrease in CO2 intake by mesophyll cells, and thereby decreased CO2 assimilationand net photosynthesis [99].The mesophyll tissues are the most important leaf tissues where photosynth-

esis occurs. Mesophyll conductance is also impaired by drought [100], whichalso limits photosynthesis, although the degree of limitation caused by it is stillunder debate [93,101]. Due to limitation of mesophyll conductance solubility ofCO2, surface areas of the apoplastic and symplastic routes of CO2 are

Figure 9.4 Possible reasons for the decline in photosynthesis in plants under drought stress.


obstructed. Both stomatal conductance and mesophyll conductance are limitedby soil water deficit, but stomatal conductance is more sensitive [100,101]. Ifexcess light energy is received by the plant photosystem with limited CO2

supply under drought, sequences of unusual and unwanted phenomena canoccur. On the one hand, due to the limited CO2 supply there is a lack ofelectron acceptors in the chloroplast. On the other hand, if excess light energy isreceived by chloroplast, ferredoxin remains in the over-reduced condition, theregeneration of NADPþ is reduced, the electron transport chain is reduced, andimpaired ATP production and impaired RuBP regeneration due lower RuBisCOactivity occur. In such a condition, through the Mehler reaction, a number ofROS like O2

��, OH�, and so on, are produced when electrons having a highstate of energy are transferred from Photosystem I to molecular oxygen[102,103]. If the protection of ROS is beyond the plant-scavenging capacity, amore severe condition is generated as those ROS damage the membrane,photosynthetic pigment, other organelles related to photosynthesis, and othercell organelles [78]. More emphatically, drought-induced ROS impairs thephotosystem and reaction center of the photosynthetic apparatus and lightharvesting complex II [104], and ROS can react with proteins, lipids, andpigments [105]. Photosystem II is more susceptible to drought as compared toPhotosystem I [106].Numerous plant studies revealed that photosynthesis is limited by stomatal and

non-stomatal factors. Plant responses to photosynthesis are different. In Populusnigra L. leaf the net photosynthetic rate fell to almost zero at the lowest soilmoisture (fraction of available soil water¼ 25%) at 35 days after starting droughttreatment [107]. Xu et al. [108] reported that severe and extreme drought causedsignificant drops in the light-saturated net photosynthetic rate of 22% and 75%,respectively, compared to the control treatment of ample moisture. The leaf netphotosynthetic rate and stomatal conductance in summer drought-stressedPhillyrea angustifolia plants were decreased by about 90%. At that time leaf RWCwas low (50%). However, no effect was seen for maximum efficiency ofPhotosystem II photochemistry (Fv/Fm) under the same drought condition. It wasconcluded that photosynthesis downregulation may mainly derive from stomatallimitation for this species [109]. A similar result was found by Xu et al. [108].Photosynthesis and growth both are negatively affected by water deficit. Thecommon feature in all plant species is that carbon demand (growth) always decaysbefore carbon supply (photosynthesis) is affected by water deficit and so growth ismore sensitive than photosynthesis [110]. It was mention in several studies thatstomatal movement and RuBisCO activity are important, although RuBisCOactivity is maintained even when leaf RWC drops to 50% while stomata are already75% closed [111,112]. Seedlings (71 days old) of J. curcas were subjected tocontinuous well-watered (control) or to a drought stress period followed byrewatering. Stress was applied by reducing irrigation (10% reduction every 2 dayson the weight base), for 28 days, until the field capacity reached up to 15%(maximum stress). Net photosynthesis was not affected by mild to moderate stress,but it abruptly dropped at severe stress. This was due to reduced stomatal


conductance, which showed an earlier decline than net photosynthesis. Droughtstress did not reduce chlorophyll contents, but led to a reduced chlorophyll a/bratio [58].Dias and Bruggemann [113] reported that as compared to control, drought-stressed

plants had more heat dissipation, decline of the photochemical chlorophyllfluorescence quenching, Photosystem II quantum yield reduction, and diminishedelectron transport rate. Several reports supported that drought stress reducedphotosynthesis or caused photoinhibition; photorespiration is also the cause ofreduced CO2 assimilation. Reduced photosynthesis or photoinhibition are accompa-nied by harvesting complexes, involving the xanthophyll cycle and lutein cycle, whichcontrol thermal dissipation [114,115]. Water stress caused a decline in chlorophyll andcarotenoid contents. This is another reason for hampering the photosynthesisprocess. The reduction in chlorophyll a accumulation was from 34.66% to 27.13% indifferent Avena species [116]. Wheat (Triticum aestivum) plants grown in soil after 3, 6,and 9 days of withholding water showed a 45%, 55%, and 59% reduction inchlorophyll content, but the change in carotenoid was insignificant [117]. After 7 daysof drought treatment the total chlorophyll content in cotton (Gossypium hirsutum L.)decreased by 21% and 23%; the carotenoid content was decreased by 31 and 33% inGM090304 and Ca/H 631 genotypes, respectively, as compared to the control. Thechlorophyll a/b ratio of drought-stressed plants decreased significantly in both thegenotypes. Similar results were investigated in Brassica napus [118], Albizia lebbeck[119], Cassia siamea seedlings [119], Vigna mungo [120], Pistacia vera [121], Pistiastratiotes [122], and Phaseolus vulgaris [123]. In our study, we observed that chlorophyllcontent in rapeseed leaves significantly decreased when exposed to PEG-induceddrought stress (Figure 9.5). Thameur et al. [63] reported that a decline in net CO2

assimilation rate was duemainly to stomatal closure. A high net CO2 assimilation rateunder water deficit was associated with a high RWC. In chickpea (C. arietinum),imposing drought stress during vegetative growth or anthesis significantly decreasedchlorophyll a, chlorophyll b, and total chlorophyll content. Differences betweenvarieties in chlorophyll b and total chlorophyll content at flowering were notsignificant [57]. The major reason for reduced rates of leaf photosynthesis under mildor moderate drought stress was stomatal closure, causing reduced leaf internal CO2

concentration [57,124]. In transgenic cultivar Lumianyan28 of cotton (G. hirsutum L.)drought stress negatively effected growth, RWC, and photosynthesis [125].Field-grown cotton plants in a semi-arid environment showed diminished net

CO2 assimilation rates and stomatal conductance, and a rise in leaf temperatures inwater-limited compared to well-watered plants of all cultivars. The activation stateof RuBisCO was reduced in water-limited than well-watered plants; at the sametime RuBisCO is also inhibited due to a temperature rise in dry-hot conditions ofsemi-arid environments. CO2 limitation and RuBisCO deactivation both accountfor the limitation of photosynthesis [126]. According to Yu et al. [127], non-stomatallimitation of grapevine is the cause of the reduced carboxylation efficiency or to theinhibited functional activity of Photosystem II, and a decrease in photosynthesismight be due to leaf-to-air vapor pressure deficit and the depression of effectivequantum yield of Photosystem II photochemistry. Dias and Br€uggemann [128] also


stated that under moderate and severe drought the photosynthetic capacity andquantum yield were reduced due to a reduction in Calvin cycle enzyme activity andphotochemistry. A significant decrease in photosynthesis in amur grape (Vitisamurensis Rupr.) was associated with increasing intercellular CO2 concentration[95]. Intercellular CO2 remained constant when photosynthesis decreased; again,intercellular CO2 showed a decrease in low drought stress and increase inmoderate and severe drought stresses [113]. The decrease in photosynthesis mightbe due to photodamage by environmental stresses like drought or temperature[129]. These studies also support that the reduction in photosynthesis is caused bynon-stomatal limitation. Drought is responsible for reduced photosyntheticassimilation rates that reduce ultimately the growth and yield. Without this,drought causes a small leaf area index that also reduces overall photosynthesis andproductivity [93].

9.2.6

Reproductive Development and Seed Formation

Drought directly affects the reproduction process of plants. Early reproductivestages, micro- and megasporogenesis, are the most sensitive among thesubphases. Pollen viability, germination, pollen tube growth, stigma viability

Figure 9.5 Phenotypic appearance of rapeseed

(B. napus L.) seedlings under drought stress

conditions. Hydroponically grown rapeseed

(12-day-old) seedlingswere exposed to drought

stress (inducedbyPEG) for48 h. (a)Control, (b)

PEG10%,and (c)PEG20%.Drought stresswas

imposed for 48 h.


and receptivity, anthesis, pollination, fertilization, and embryo development areseverely vulnerable to drought stress. Lack of any of these processes causesembryo abortion that ultimately affects the yield. There are various reasons fordrought-induced damage of reproductive stages, including alteration of carbonand nitrogen mobilization or metabolism, or direct damage to those events dueto drought. Decreased water potentials in the floral tissues, including pollen,female gametophyte, and stigma, and decreased carbohydrate or nitrogensupply, are common in drought stress. Another phenomenon can occur, whichis that drought-induced hormonal changes may cause sterility. Drought stressafter fertilization decreases seed size rather than seed number. Seed size is thefinal component of yield. Seed size is largely dependent on the availability ofphotosynthetic reserves, which are either currently available or can be movedfrom other parts into the grains. Seed size is mainly decreased by the reductionin assimilate and nitrogen supplies either through decreased photosyntheticrates or because of a decrease in photosynthetic leaf area observed underdrought stress [46]. Thus, drought stress at different phases of the reproductivestage is the reason for reducing yield by quantity and quality by altering orhindering different physiological processes.The physiological effects of drought stress on the reproductive development of

rice have long been recognized and extensively reviewed [130–132]. Droughtstress inhibits the processes of pollen development at meiosis, causing antherdehiscence and pollen shedding, pollen germination, and fertilization [133].Several studies suggested that drought at anther meiosis can induce pollensterility, which is often considered as the most sensitive stage [134,135].According to Kato et al. [135], even mild water deficit at the meiosis stage causedhigh rates of pre-flowering abortion of secondary branches and caused a 40–45%reduction in the number of spikelets per panicle. There is a relationship betweenthe water status of the leaf and spikelet sterility. This decrease was attributed to areduction of plant water status as measured by leaf water potential, which wassignificantly associated with spikelet fertility [136]. In the rice variety IR64, 66%spikelet fertility was recorded with 50–60% RWC in the studies of Rang et al. [25],while the same genotype had 33% fertility when exposed to 40–50% flag leafRWC as studied by Liu et al. [137]. In rice, spikelet fertility was reduced by 64.6%and peduncle length by 20.9% compared to the control. The average peduncleelongation rate ranged from 3.16 to 4.97 and 1.56 to 4.11 cmday�1 in theirrigated and drought-stressed treatments, respectively. The application ofreproductive-stage drought stress near heading reduced severely grain yield,which was only about 21% of that achieved under well-watered conditions [136].Drought in combination with heat stress causes more severe damage ofreproductive parts. Five rice genotypes were studied under drought stress anddrought stress in combination with heat stress in order to observe theirreproductive responses. The later stress treatment caused more harm to thereproductive behavior. The flowering period was significantly extended in both ofthe stresses. Compared with the control, the average peduncle length wasreduced by 24% and 27%, the number of pollen on the stigma was reduced by


31%, and 71%, the number of germinated pollen on the stigma decreased by59%, and 84%, and the panicle exsertion was reduced by 48% and 56% due todrought and drought combined with heat stress, respectively, in all genotypes[25]. Drought had a significant effect on the number of pods of C. arietinum.Plants had the highest number of pods when they were grown without droughtstress. Among the three varieties Bivaniej (kabuli), ILC482 (kabuli) and Pirouz(desi), Pirouz showed the highest pod number, but it had the lowest yield,probably due to a decrease in percentage of filled pod and 1000 grain weight [57].That the decrease in yield of grain legumes grown under drought conditions islargely due to the reduction in the number of pods per plant was also supportedin several other studies [138,139]. In peanut (A. hypogaea), drought stress causeda reduction in yield by various ways, like reducing the pod set, pod number, andinhibiting process peg penetration to the soil surface due to hard soil surfaceresulting from desiccation by drought; reduced pod numbers and individual seedweight were larger in magnitude when the intensity of the stress increased [65].In Bambara groundnut (Vigna subterranea), pod number per plant was the mostsensitive yield component and was reduced by 43% due to drought. The reasonfor this reduction is abortion of some flowers and restriction of the number ofpods to fill in order to maintain a source–sink balance. The size of pods wasreduced in this experiment. Unfilled pods were also found on plants from thedrought treatments, which may be because of restriction of fertilization duringdrought stress [140]. Drought stress during the reproductive phase may affect thereproductive sink strength (i.e., capacity to establish a new sink) of common bean(P. vulgaris) genotypes. The effect of drought on the availability and subsequentmetabolism of assimilates in the reproductive sink organs determines the yield,although these varied according to the genotypic differences. Seed sucroseconcentrations of the common bean variety BrSp decreased by 29% to 47% underdrought, whereas stress resulted in an increase (up to 43%) in concentration ofthe seed carbohydrate in the variety SEA 15 [141]. As stated by many authors,flowers can be aborted if the stress is imposed before and at anthesis. Thisphenomenon was found to decrease the seed numbers in peanut [142], wheat[143], and rice [144]. In legumes, most of the abortion occurs during the earlystages of embryo development. Drought-induced ABA production is anothercommon occurrence that is also responsible for the shedding of leaves orreproductive organs. Sometimes it may also happen that drought-inducedinhibition of photosynthesis reduces or inhibits the mobilization of assimilatefrom the source to the sink (i.e., reproductive parts) and causes the sterility [46].Failure of reproductive development is a major cause of yield reduction in fababean and quinoa exposed to drought [145]. This is also a common phenomenonfor many other crops. The reason was mentioned that reproductive developmentis extremely vulnerable to drought stress. Early seed development like meiosis ofpollen development and the following later phases of seed development are mostsensitive. Ovary abortion and pollen sterility under drought in maize and in othersmall grains, which reduced the grain number; this was also supported by manyfindings [145,146].


9.2.7

Yield Attributes and Yield

Drought is one of the most important limiting factors for agricultural cropproduction all around the world. Drought stress both during vegetative andearly reproductive growth reduces yield. The assimilation of vegetative partscontributes to yield and that is why vegetative-stage drought is important; moreemphatically, drought in the reproductive stage diminishes the yield directly byhampering the reproductive parts or developmental stages, which are verysusceptible to all kinds of stress, including drought. Drought hampers the yieldby obstructing the panicle, peduncle, rachis, tiller growth, and development;reducing the number of seeds, seed size, and seed quality. Reductions of finalyield were measured in different crop plants under drought stress conditions asshown in Table 9.1.The complex nature of the morphological, physiological, and phenological

traits of plant genotypes are influenced by the soil moisture, which determinesthe yield. Effects of drought on crop plants also depend on their develop-mental stages. Although the pattern of damage may differ, the result is thesame (i.e., reduction of yield). Yield and yield components of 13 advancedwinter and intermediate wheat genotypes were evaluated under normalirrigation and drought stress conditions, and the results showed significantdifferences in their grain yield. Due to drought stress, the average grain yieldof genotypes was reduced by 50%. However, this reduction also varied amonggenotypes. The authors concluded that there is a positive correlation betweenthe yield components and yield of wheat [57]. The response of rice varieties todrought has been extensively studied. Drought is considered as one of themajor constraints on rice cultivation, which significantly reduces grain yield[162]. Drought adversely affects more than half of the rice production areaworldwide [163]. Drought stress shortens the grain-filling period and enhancesearly senescence by redirecting remobilization of assimilates from thevegetative parts to the grains [164]. Drought stress during each of the ricegrowth stages (vegetative growth, flowering, and terminal stage) causes spikeletsterility that leads to unfilled grains [165], which is one of main reasons forreduced yield or even crop loss due to drought stress. The severity of droughtstress is also well considered for determining the yield. Yield reduction in ricemay be significant even under a moderate stress [147], but high-yield-potentialvarieties have an advantage over varieties with lower yield potential under thesame stress conditions [166]. In rice genotypes, mean yield ranges wereobserved from 3.9 to 5.0 t ha�1 under non-stress, from 1.78 to 3.40 t ha�1

under moderate stress, and from 0.45 to 2.19 t ha�1 under severe stress [166].To assess the effect of drought stress on seed yield, seed quality, and growth oftomato, an experiment was conducted in the greenhouse by using tomato cv.“Moneymaker” as a test crop. Among the four treatments of the experiment,the first one was the control or non-stress condition, the second one was earlystress (when the first truss has set the fruits), the third one was the middle


Table 9.1 Drought-induced reduction in yield in different crop species.

Crops Drought stress level Duration and

growth stage

Yield

reduction

References

Rice Severe drought stress(crop was fully irrigatedfor 1 month after trans-planting and thendrained out)

Until 50% flowering Grain yield:74%

[147]

Rice Soil moisture tensionreached �30 kPa at20 cm depth

Reproductive stage Grain yield:49%

[148]

Rice Withholding the irriga-tion at 51 d after sowing

Reproductive stage Grain yield:93%

[149]

Rice Soil water tensionreached about �70 kPa at15 cm and �40 kPa at30 cm soil depth

7 wk after sowinguntil harvest

Grain yield:97%

[150]

Wheat Irrigation was cut offafter the heading stage

After anthesis Grain yield:25%

[151]

Wheat Water withdrawn afterstem elongation stage

Stem elongationstage

Grain yield:46%

[152]

Wheat Withholding irrigationafter anthesis

Anthesis to harvest Seed yield:93%

[153]

Barley No irrigation after grainfilling stage

Grain-filling stage Grain yield:52%

[154]

Mungbean Withholding water for10 d

6 wk after planting Seed yield:82%

[155]

Chickpea Withholding irrigation Vegetative andanthesis phases

Seed yield:61%

[58]

Lentil No irrigation aftervegetative stage

Vegetative stage Seed yield:57%

[156]

Cowpea Withholding water Vegetative and repro-ductive stages

Grain yield:69%

[157]

Cowpea Termination of irrigationat 50% flowering period

Flowering stage Grain yield:45%; harvestindex: 28%

[158]

Canola 30% available water Flowering stage Seed yield:62%

[159]

Soybean 70% soil water depletion Vegetative to harvest Seed yield:14%

[160]

Tomato Drought stress imposedby withholding water

Vegetative stage Fruit weight:8%

[36]

Okra 3.8m3 water per season --- Total yield:44%

[161]


stress (when fruits in the first truss were fully matured and started changingcolor), and the forth one was late stress (when fruits on the first truss wereripened fully). Late stress exerts no significant effects on fruit production andproduced a little higher fruits per plant (15.2) as compared to control (14.7).Plants were more affected from middle stress than early stress, although boththese stresses have less effect. Control plants had more fruits than early andmiddle stress. As compared to the control (700 g), a significant reduction infruit weight in early (642 g) and middle stressed plants (613 g) was observed,and late stress showed no effect on fruit weight, producing large sized andheavier fruits. Considering the seed characteristics, middle and late stresstreatments produced seeds with higher seed number and higher seed weightcompared to the control, and the early stress caused more of a decline innumbers of seed per plant than the control treatment [36]. During the researchcarried out with three chickpea (C. arietinum) varieties (Bivaniej (kabuli),ILC482 (kabuli), and Pirouz (desi) in response to drought, 10% higher seedyield was obtained under drought stress at the anthesis stage than that ofdrought treatment at vegetative stage. The highest yield was obtained fromBivaniej both under non-stressed and drought stress conditions. The losses inyield in response to drought treatment were 61% for Bivaniej, 45% for ILC482,and 66% for Pirouz [58]. Similar results related to drought stress were alsofound in several other studies. Water stress during vegetative or earlyreproductive growth usually reduces yield by reducing the number of seeds insoybean [167] and canola [168]. Drought was also found to create adverse effecton yield components and the yield of several other cereal, oil seed, pulse, andvegetable crops in several studies, including corn [169], soybean [169], maize[170], bean [171], chickpea [172], and groundnut [173]. Drought stress affectsmany traits including, morphological, physiological, and metabolic events ofplants simultaneously; the combined result is decreased grain yield and quality[46,174]. If drought stress occurred at the grain-filling period it decreased thenet photosynthetic rate of the flag leaf of barley, but the grain-filling rate wasnot effected significantly [174]. Drought stress at the middle to late growthstages accelerates leaf senescence, shortening the grain-filling period. It alsoreduces grain weight and grain yield of barley [174]. Under drought stress of50% field capacity the reduction in yield was highest in the barley varietySwitir (40%) and lowest in Tlalit (34%) compared with the adequately irrigatedcontrol (100% field capacity). Drought resulted in a reduction of total grainproduced per plant, from 3 and 2 to 6 and 4 g, respectively, for Switir andTlalit [63]. Yield components (pod number m�2, seed number m�2, andindividual seed weight) were negatively affected in peanut (A. hypogaea) due todrought, which causes a decline in seed yield up to 73% [65]. Greven et al.[175] found that in olive, fruit size from the dry trees was about 40% of thatfrom the irrigated trees, the irrigated trees yielded over 10.0 kg of fruit per treewhile the dry trees yielded only 6.1 kg per tree; the average weight ofindividual fruit was reduced from 4.0 to 2.4 g. They also found that droughtnot only reduced the yield, but also diminished the quality of olive oils. Water


stress at the vegetative stage alone can reduce yield more than 36% and waterstress at the reproductive stage can reduce yield more than 55% [176].

9.3

Drought and Oxidative Stress

Most abiotic stresses result in increased ROS production [9]. Among the abioticstresses, drought-induced ROS production had been documented in a numberof plant species growing under different conditions [177–179]. Under normal ornon-stressed conditions most cellular compartments of plants maintain areducing environment and maintain a steady homeostatic condition. Uponimposition of stress, generally an increased ROS level is prominent. ROSproduction beyond the plant’s quenching capability is often defined as adisruption of redox signaling and redox control [180], which can cause oxidativestress by damaging membrane lipids, proteins, photosynthetic pigments, andnucleic acids through oxidation process, and these are considerably amplifiedunder drought stress [27,29,30,181]. Drought stress impairs the photosynthesisprocess in various ways, resulting in the production of dangerous ROS likeO2

��, H2O2,1O2, and OH� beyond the plant’s scavenging capacity and causing

oxidative stress [27,30,181]. Drought alters and damages the photosyntheticpigments and photosynthetic apparatus [55]. Water deficit makes the cellularcontent more viscous, for which the protein denatures, thus the membrane ofthe photosynthetic apparatus as well as the cell membrane denatures, and at thesame time the enzymes of the Calvin cycle are inactivated, the efficiency ofcarboxylation reaction and CO2 fixation by RuBisCO is reduced, and this resultsin increased photorespiration, which is one of the major reasons of ROSproduction [182]. It has been reported that more than 70% of total H2O2 isproduced due to drought-induced photorespiration [183]. Drought-inducedstomatal closure is another common phenomenon that reduces the CO2

availability in the fixation site of the Calvin cycle. The rate of regeneration ofNADPþ is also reduced under drought, thus the electrons of the electrontransport chain cannot be accepted properly, and finally excess reduction of theelectron transport chain causes leakage of electrons to O2 and the production ofROS (O2

��, 1O2, H2O2, and OH�) [103]. Additionally, under stressful conditionschloroplasts receive excessive excitation energy beyond their capacity to bind itand ferredoxin remains in the over-reduced condition during photosyntheticelectron transfer; the electrons having a high state of energy are transferredfrom Photosystem I to molecular oxygen. During this transfer the superoxideanion radical O2

�� is generated through the Mehler reaction and this super-oxide radical leads to the production of more harmful oxygen radicals like OH�

[103,184,185]. Several studies also agreed about the fact that under droughtstress the imbalance between light capture and its utilization [186] inPhotosystem II changes the photochemistry of chloroplasts, which causesexcess production of highly reactive ROS species [187]. In his review, de

9.3 Drought and Oxidative Stress 229

Carvalho [185] proposed that the drought stress response occurs in threesuccessive phases. In plant, the normal ROS steady-state level is disturbed bydrought stress where initially the enhancement of ROS production due tostomatal closure shifts the equilibrium upwards and this triggers defense signaltransduction pathways. However, prolonged drought stress results in exacer-bated ROS production that cannot be counterbalanced by the antioxidantsystem, leading to deleterious oxidative events that ultimately result in celldeath (Figure 9.6).Lipid peroxidation is thought to be the most common and obvious damaging

process for all living organisms, including animals and plants [188]. Lipidperoxidation not only affects normal cellular functioning, but simultaneouslythe lipid-derived radicals accelerate oxidative stress [189]. Enhanced electrolyteleakage under drought stress was observed due to oxidative stress, andsubsequent lipid peroxidation and plasmalemma injury in rice [190], maize[191], and rapeseed [29]. Drought stress produces ROS that subsequently impairthe photosystem and reaction center of the photosynthetic apparatus. Singletoxygen damages light harvesting complex II [104]. Trebst [105] reported that thehighly reactive 1O2 can react with proteins, lipids, and pigments. Lu and Zhang[106] reported that Photosystem II is more susceptible to drought as comparedto Photosystem I, and a decline in D1 and D2 proteins causes the destruction ofPhotosystem II. Again, due to differences in the antioxidative capacity, oxidativedamage was not found to be uniform in the different cells or tissues in C4plants [192,193]. Oxidative stress caused more damage to bundle sheath tissueas compared to the mesophyll tissue [194]. The imposition of drought for 12days in two apple species, Malus prunifolia and Malus hupehensis, resulted insignificant malondialdehyde (MDA) accumulations, and increased the O2

� andH2O2 in the leaves from both species compared with their controls, althoughthe effects were severe in the latter species. Drought led to considerable damage

Figure 9.6 Different phases of drought stress in terms of oxidative stress and antioxidant

defense in plants.


in the cellular membranes in both species [195]. Higher leakage of electrons toO2 occurred during photosynthesis under drought stress and as compared tounstressed wheat seedlings the drought stress caused approximately 50% higherleakage of photosynthetic electrons through the Mehler reaction [196,197]. Asimilar result was also found in sunflower [198]. The production of hydroxylradicals in thylakoids under drought was considered as a great threat because oftheir oxidizing potential to react with almost all biological molecules [199].Their accumulation leads to a chain of deleterious reactions, and exerts harmfuleffects by damaging thylakoidal membranes and the photosynthetic apparatus;several reports state that no enzymatic reactions were found to remove orreduce the highly reactive hydroxyl radicals [200]. Reactive nitrogenous specieswere also found to increase under drought. Increased nitric oxide (NO) levels ofwater-stressed grapevine leaves was observed by Patakas et al. [201]. Incucumber roots, a higher level of NO was mentioned by Arasimowicz-Jeloneket al. [202] during water stress. The physiology and cellular status of root andleaf tissues of Medicago truncatula were observed under 11 days of droughtstress. Cellular damage, membrane damage, enhanced levels of reactive oxygenand nitrogen species, and reduced stomatal conductance were key features ofthat stress, and rewatering resulted in partial or complete alleviation of thestress-induced damage [203].Drought stress responses towards the production of H2O2 and lipid peroxidation

differ by genotype, and sometimes with variety of genotypes, and here the durationof water stress and the age of the plant are also important factors. Uzilday et al.[103] compared the effects of drought among two C3 and C4 plants. Cleome spinosawas considered for C3 and Cleome gynandra was considered for C4, and they wereexposed to drought stress for 5 and 10 days. Lipid peroxidation as represented byMDA and H2O2 contents remarkably increased in C. spinosa as compared to C.gynandra under drought stress, which proved the higher sensitivity of the first planttowards drought stress. H2O2 and lipid peroxidation were found to rise inT. aestivum (20 days old and 9–11 days water stress) [177], Populus przewalskii(water stress at 2 months old) [204], and Pinus densata, Pinus tabulaformis, andPinus yunnanensis (water stress for 1 month in 1-year-old plants) [205]. H2O2 wasalso found to increase in Prunus hybrids (70 days of water stress in 1-year-oldplants) [206], P. przewalskii (water stress at 2 months aged plants) [207],Oryza sativa(3 weeks of water stress in 2.5 months aged seedling) [208], Poa pratensis (waterstress for 5 days) [209], T. durum (35 days of water stress on 30-day-old seedlings)[210], and T. aestivum (197 days of water stress in 3-month-old plants) the decreaseof H2O2 and increase of lipid peroxidation [211] with increasing water stress.It is well established that as a result of drought stress the generated harmful ROS

damage the cell structures, proteins, lipids, carbohydrates, and nucleic acids, anddisrupt cellular homeostasis, in severe cases leading to cell death. However, in spiteof the detrimental effects of ROS, they also play major physiological roles inintracellular signaling, cellular regulation, and as secondary messengers, whichhave been studied in several reports [188,212]. The role of ROS as signals for geneexpression has been confirmed by several authors [213,214].

9.3 Drought and Oxidative Stress 231

9.4

Antioxidant Defense System in Plants Under Drought Stress

Plants acquire well-organized enzymatic and non-enzymatic defense systemsthat function together to control the flow of uncontrolled oxidation undervarious stress conditions and protect plant cells from oxidative damage byscavenging ROS. The well-documented antioxidant enzymes in plants aresuperoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX),glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), dehy-droascorbate reductase (DHAR), glutathione peroxidase (GPX), guaicol perox-idase (GOPX), glutathione-S-transferase (GST), and so on. Among the non-enzymatic antioxidant components, ascorbic acid, glutathione (GSH), phenoliccompounds, alkaloids, non-protein amino acids, and a-tocopherols are com-monly found in plants [188] (Figure 9.7). The improvement of the antioxidantdefense system is considered to be effective in the development of resistanceand adaptive features in plants against drought stress. It has been supported bymany research findings that the enhanced activities of components of theantioxidant system like antioxidant enzymes and non-enzymatic compoundsdecrease oxidative damage, and develop and improve the drought tolerance andresistance of plants [185,215].

Figure 9.7 Antioxidant defense system in plants under drought stress-induced oxidative stress.


9.4.1

Non-Enzymatic Components

The important non-enzymatic antioxidants, including ascorbate, GSH, carotenoid,tocopherols, thioredoxin, vitamin E, and so on, play a vital role to alleviate ROSinduced damages during drought stress [215].Under drought stress ascorbate is considered as one of the strongest non-

enzymatic antioxidants [216], whereas the protective action of the GSH systemagainst oxidation of proteins is also established. Selote and Khanna-Chopra [217]reported that under drought stress the tolerant variety of rice N22 had significantlyhigher GSH and ascorbate content, which resulted in a higher level of RWC, turgorpotential, and lower H2O2 in N22 compared to the susceptible N118 rice variety. Intolerant rice varieties Xiangzhongxian No. 2 and IR50, ascorbic acid and GSH wereenhanced by up to 3 days of drought stress and at that time a relatively stablemembrane structure, reduced electrolyte leakage, and lower H2O2 production werefound compared to the sensitive control. However, when similar stress conditionscontinued for 5 days, an inverted result was observed, which indicates that controlof ROS-induced damage depends not only upon the capacity to produce the non-enzymatic antioxidant components, but also upon the duration of drought [190].The GSH pool and the GSH/GSSG ratio were highly reduced in leaves of non-acclimated wheat seedlings compared to acclimated seedlings under water stress[177], and the reason might be due to the enhanced activities of ascorbate–GSHcycle enzymes of acclimated plants. While studying rapeseed seedlings (B. napuscv. BINA sharisha 3) under drought stress, exogenous Se significantly increasedascorbate, GSH and GSSG content, although the intensity of increase wasdependent upon the severity of stress [29]. Larger increases in the levels ofascorbate and GSH were found in tolerant apple species of M. prunifolia than insusceptible M. hupehensis when water was withheld for 12 days, which ensured astronger protective mechanism and maintained cell structural integrity [195]. Apartfrom its involvement in the regeneration of the ascorbate pool, ascorbate playsanother vital role of protecting or rejuvenation oxidized carotenoid or tocopherols,which are well documented for enhancing stress tolerance [218].Not only ascorbate and GSH, but also b-carotene and a-tocopherol enhanced

stress tolerance, including against drought [219]. According to Krieger-Liszkay[220], antioxidant metabolites like b-carotene and a-tocopherol act as the first lineof defense against ROS. They are very efficient in quenching 1O2; three chlorophyllmolecules can be quenched by carotenoid in the antenna system [221], thus theyprevent the production of singlet oxygen. Among the tocopherols, both a- andc-tocopherols perform as scavengers of 1O2. They help in the protection ofPhotosystem II organization and function, especially during photoinhibition. Theyalso play important roles in D1 protein turnover that helps to protect PhotosystemII during stress [222]. However, carotenoid seems to be susceptible to oxidativedestruction [223] and that is why it has been considered as a less importantantioxidant by many researchers despite its ROS-scavenging capabilities [224].Xanthophyll pigments, zeaxanthin and antheraxanthin (at their increased levels),

9.4 Antioxidant Defense System in Plants Under Drought Stress 233

were also found to reduce ROS production by the xanthophyll cycle, which oftenhelps in dissipating excess energy [193]. Falvonoids was also considered asantioxidant scavengers like a-tocopherol, although there is still a debate regardingunderlying mechanism [225].

9.4.2

Enzymatic Components

Plants have different antioxidant enzymes that are compartment-specific andpresent in various cell organelles, like chloroplasts, mitochondria, peroxisomes,cytosol, and stroma, by which ROS production remains under control via highlyefficient scavenging mechanisms [215,226]. The major oxidative enzymes are SOD,CAT, APX, GPX, GR, MDHAR, DHAR, GPX, POD, and GST.SOD has been recognized as the first line of defense in response to ROS by

converting them to H2O2 [227]. CAT and APX detoxify H2O2 through the AsA–GSH cycle [228]. Here, the reducing agent of the ascorbate and GSH regenerationsystem plays a major role. APX of the AsA–GSH cycle converts H2O2 to H2O byoxidizing ascorbate into monodehydroascorbate (MDHA). Then in the presence ofNAD(P)H, the enzyme MDHAR converts MDHA to ascorbate [215,229]. Pan et al.[230] also mention that there is a strong correlation between SOD activity anddrought-induced oxidative stress tolerance. Further, it was supported by manyauthors that the involvement of the ascorbate–GSH cycle, including APX, DHAR,MDHAR, and glutathione reductase, allows scavenging of superoxide radicals andH2O2 [223,231]. Selote and Khanna-Chopra [217] reported that due to significantlyhigher SOD and APX activities in drought-stressed panicles of rice, there was ahigher level of RWC, turgor potential, and lower H2O2, and here the tolerant varietyN22 showed better performance than the susceptible N118. Xiangzhongxian No. 2and IR50, two drought-tolerant rice entries produced enhanced antioxidantenzymes of SOD, CAT, and APX, which resulted in lower levels of electrolyteleakage, stable membrane organization, and less H2O2 production under 3 days ofdrought stress [190]. Exogenous Se in drought-stressed rapeseed seedlings (B.napus cv. BINA sharisha 3) upregulated the antioxidant enzyme activities [29].Under both mild and severe drought stress the activities of DHAR, GST, and GPXsignificantly increased, and CAT activity decreased. MDHAR and glutathionereductase activities were enhanced only by mild stress. Moreover, the Se-pretreated(25 mM Na2SeO4, 48 h) seedlings exposed to drought stress showed amplifiedactivities of APX, DHAR, MDHAR, glutathione reductase, GST, GPX, and CATenzymes, and lower levels of H2O2 and MDA. Thus the evidence of protection ofdrought-induced rapeseed seedlings by increased levels of antioxidant enzymesunder drought stress is confirmed [29]. Seedlings of 10 oilseed rape (B. napus)cultivars were grown under three irrigation regimes (field capacity, 60% fieldcapacity, and 30% field capacity) in a greenhouse to asses antioxidant enzymeactivities. Drought stress improved the activities of SOD and POD, while CATactivity diminished. In this experiment, Licord was proved as the most tolerantcultivar by showing the highest level of enzyme activities, and the varieties Hyola


308 and Okapy were considered as drought sensitive as they showed the lowestlevels of enzyme activities. Further, native polyacrylamide gel electrophoresisanalysis identified eight SOD isozymes. Three isoforms of Mn-SOD and fiveisoforms of Cu/Zn-SOD were identified in the examined leaves. Mn-SODexpression was enhanced by drought stress. Five POD isoforms were detected.POD-4 and �5 intensities were elevated under drought stress. These isoforms areimportant to differentiate drought-tolerant cultivars under drought stress [232].Increase in the activities of various antioxidant defense enzymes like SOD, APX,GR, and CATneutralized the oxidative stress-induced damage that occurred due todrought in rice plants [233]. The reproductive stage is extremely sensitive todrought stress [137,234]. During the meiosis stage of anther development in rice,drought stress resulted in suppression of ROS-scavenging enzymes CAT, APX, andDHAR, and hampered the developmental process. Under such conditions, Nguyenet al. [235] mentioned the need for the improved efficiency of ROS-scavengingmechanisms and enzymes and non-enzymatic components to overcome stress andset seed. Drought stress was imposed by applying 40% PEG upon two Zea mays L.var. 704 (drought tolerant) and var. 301 (drought sensitive) varieties, and theactivities of GPX, APX, and CAT in the roots and shoots were measured. Theenzyme activities were higher in 704 as compared to that of 301, which conferreddrought tolerance in that tolerant variety [236]. A mild water stress (50% fieldcapacity) condition was continued for 22 days and some tomato cultivars (L.esculentum) were grown. The contents of H2O2 and MDA were significantlyincreased in all the cultivars except in the cultivar Zarina. Appropriate induction ofantioxidant enzymes APX, DHAR, MDHAR, and glutathione reductase allowedcultivar Zarina to be tolerant to drought-induced oxidative stress [237]. In somestudies, CAT has been recognized to have a primary role in H2O2 detoxification inMedicago plants [203]. On the contrary, some studies suggested that CAT may beless important than APX in scavenging H2O2 in roots in long-term stress [238]. C.spinosa (C3) and C. gynandra (C4) were exposed to drought stress for 5 and 10 days,and their drought tolerance compared on the basis of relative shoot growth rate,RWC, osmotic potential, H2O2 content, lipid peroxidation content, and activities ofantioxidant enzymes SOD, CAT, POX, APX, and GR. Drought stress caused anincrease in POX, CAT, APX, and glutathione reductase in both species. SODactivity was somewhat decreased in C. gynandra and it remained unaffected in C.spinosa. MDA, which is a measure of lipid peroxidation, and H2O2 content werealso markedly increased in C. spinosa in contrast to C. gynandra upon imposition ofdrought stress. C. gynandra showed positive results in other parameters also. Theseresults suggest that in C. spinosa, the antioxidant defense system was insufficient tosuppress the increasing ROS production under stress conditions, which is higherin C. gynandra and rendered a lower level of MDA and H2O2 production [103].Well-synchronized induction of the ROS detoxification system was observed indrought acclimated wheat seedlings [239]. Drought stress generated excessiveaccumulation of H2O2 and elevated lipid peroxidation levels owing to the reducedresponse of antioxidant enzymes APX, MDHAR, DHAR, and glutathionereductase. A reverse result was demonstrated in drought-acclimated wheat roots

9.4 Antioxidant Defense System in Plants Under Drought Stress 235

during severe water stress. Enhanced upregulation of SOD, APX, CAT, POX, andAsA–GSH cycle components was prominent at both the whole-cell level andmitochondria. At the same time, higher RWC and lower levels of H2O2 wereproduced in acclimated seedlings [239]. Two apple species, one tolerant (M.prunifolia) and one susceptible (M. hupehensis), were subjected to 12 days ofdrought stress and their performances were compared with the well-wateredcondition. Under the well-watered condition, lipid peroxidation and antioxidantparameters did not differ significantly. However, under drought stress M.hupehensis was more susceptible as it produced increased levels of H2O2, O2

��, andMDA as compared to M. prunifolia. After analyzing the antioxidant enzymes it wasobserved that in contrast to M. hupehensis, SOD, POD, APX, GR, and DHARactivities were enhanced to a greater extent in M. prunifolia, but CAT and MDHARdid not change significantly. At the same time it maintained better ultrastructuralorganelles, and lower H2O2, O2

��, and MDA. These results show the role ofantioxidative enzymes to alleviate drought-induced damage inM. prunifolia [195].

9.5

Conclusion and Future Perspectives

Drought stress is a complex phenomenon and plants undergo several morphologi-cal, anatomical, and biochemical adaptations at the cellular and organellar levels tocope with this stress. A better understanding of the effects of drought on plants istherefore vital in order to establish improved management practices and breedingefforts in agriculture, and to allow prediction of the fate of natural vegetation underclimate change. Coordinated approaches involving traditional plant breeding, alongwith molecular approaches, should be followed to identify and cultivate drought-tolerant varieties. Recently, different exogenous protectants, such as osmoprotec-tants (proline, glycine betaine, trehalose, etc.), plant hormones (gibberellic acids,jasmonic acid, brassinosteroids, salicylic acid, etc.), antioxidants (ascorbic acid,GSH, tocopherols, etc.), signaling molecules (NO, H2O2, etc.), polyamines(spermidine, spermine, putrescine, etc.), and trace elements (Se, Si, etc.) have beenfound effective in mitigating drought-induced damage in plants. Crop plants thatare tailored to have improved capacity for biosynthesis or bioaccumulation of theseprotectants might show enhanced stress tolerance.The responses and the tolerance of plants to drought stress are still unclear, and

require further critical physiological and molecular studies to reveal the underlyingmechanisms. In addition, discovering which signaling cascades are induced totrigger the profound changes seen in the expression of specific genes is also vitalfor understanding stress adaptation. Molecular knowledge that reveals tolerancemechanisms will ultimately lead the way to the manufacture of stress-tolerantplants, thereby forming the basis for improved crop production and increases ineconomic yield in plants growing under suboptimal environmental conditions.Many efforts are presently aimed at building drought tolerance into plants, butmany challenges still remain. Technological advances such as proteomics,


transcriptomics, and metabolomics provide powerful synergistic tools for enhan-cing gene information, and revealing gene function and regulatory networks.Progressive studies have shown that a combination of metabolic fluxes andphysiological changes in plants can provide accurate predictions about possiblemechanisms required for adaptation to drought stress.

Acknowledgments

We wish to thank Md. Mahabub Alam, Laboratory of Plant Stress Responses,Faculty of Agriculture, Kagawa University, Japan for providing several supportingarticles and suggestions for improving the chapter. We are also highly thankful toAnisur Rahman and Md. Hasanuzzaman, Department of Agronomy, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh for their critical reading of thechapter.

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Climate Change and Plant Abiotic Stress Tolerance || Drought Stress Responses in Plants, Oxidative Stress, and Antioxidant Defense