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Critical Reviews in Plant Sciences, 30:1–17, 2011Copyright C© Taylor & Francis Group, LLCISSN: 0735-2689 print / 1549-7836 onlineDOI: 10.1080/07352689.2011.615687

Heat Stress in Wheat during Reproductive and Grain-FillingPhases

Muhammad Farooq,1,2 Helen Bramley,1 Jairo A. Palta,3

and Kadambot H.M. Siddique1

1The UWA Institute of Agriculture, The University of Western Australia, 35 Stirling Highway,Crawley WA 6009, Australia

5

2Department of Agronomy, University of Agriculture, Faisalabad-38040, Pakistan3CSIRO Plant Industry, Private Bag 5, Wembley, WA 6913, Australia

Table of Contents

I. INTRODUCTION .....................................................................................................................................................................................................210

II. IMPACT OF TERMINAL HEAT STRESS ..................................................................................................................................................2A. Photosynthesis .....................................................................................................................................................................................................3

1. Rubisco and Photorespiration ...................................................................................................................................................................32. Photosynthetic Apparatus ...........................................................................................................................................................................3

B. Leaf Senescence ..................................................................................................................................................................................................415C. Water Relations ....................................................................................................................................................................................................5D. Grain Growth and Development ....................................................................................................................................................................5

1. Grain Number and Size ...............................................................................................................................................................................52. Starch Synthesis .............................................................................................................................................................................................73. Grain Filling Rate and Duration ..............................................................................................................................................................7204. Assimilate Translocation ............................................................................................................................................................................7

E. Grain Quality ........................................................................................................................................................................................................9

III. TOLERANCE MECHANISMS OF TERMINAL HEAT STRESS ...................................................................................................9A. Antioxidant Defense System ....................................................................................................................................................................... 10B. Molecular Basis of Heat Tolerance ........................................................................................................................................................... 1025C. Stay-green ........................................................................................................................................................................................................... 10

IV. STRATEGIES TO IMPROVE HEAT STRESS TOLERANCE ....................................................................................................... 10A. Selection and Breeding for Heat Tolerance ............................................................................................................................................ 10B. Genetic Engineering for Heat Tolerance ................................................................................................................................................. 12C. Use of Molecular Markers ............................................................................................................................................................................ 1230

V. MANAGEMENT STRATEGIES .................................................................................................................................................................... 12

VI. CONCLUSION ........................................................................................................................................................................................................ 12

ACKNOWLEDGMENTS ................................................................................................................................................................................................ 13

REFERENCES ..................................................................................................................................................................................................................... 13

35

Referee: Dr. Vincent Vadez, ICRISAT, Patancheru, Andhra Pradesh, India. E-mail: [email protected] correspondence to Kadambot H.M. Siddique, The UWA Institute of Agriculture, The University of Western Australia, 35 Stirling

Highway, Crawley WA 6009, Australia. E-mail: [email protected]

1


2 M. FAROOQ ET AL.

Ambient temperatures have increased since the beginning of thecentury and are predicted to continue rising under climate change.Such increases in temperature can cause heat stress: a severe threatto wheat production in many countries, particularly when it occursduring reproductive and grain-filling phases. Heat stress reduces40plant photosynthetic capacity through metabolic limitations andoxidative damage to chloroplasts, with concomitant reductions indry matter accumulation and grain yield. Genotypes expressingheat shock proteins are better able to withstand heat stress as theyprotect proteins from heat-induced damage. Heat tolerance can be45improved by selecting and developing wheat genotypes with heatresistance. Wheat pre-breeding and breeding may be based onsecondary traits like membrane stability, photosynthetic rate andgrain weight under heat stress. Nonetheless, improvement in grainyield under heat stress implies selecting genotypes for grain size and50rate of grain filling. Integrating physiology and biotechnologicaltools with conventional breeding techniques will help to developwheat varieties with better grain yield under heat stress duringreproductive and grain-filling phases. This review discusses theimpact of heat stress during reproductive and grain-filling stages55of wheat on grain yield and suggests strategies to improve heatstress tolerance in wheat.

Keywords breeding, genetic engineering, grain-filling, photosynthe-sis, stay-green, terminal heat stress

I. INTRODUCTION60

Global climate models predict an increase in mean ambienttemperatures between 1.8 and 5.8◦C by the end of this century(IPCC, 2007). Future climates will also be affected by greatervariability in temperature and increased frequency of hot days(Pittock, 2003). To adapt new crop varieties to the future climate,65we need to understand how crops respond to elevated temper-atures and how tolerance to heat can be improved (Halford,2009).

Plants detect changes in ambient temperature through per-turbations in metabolism, membrane fluidity, protein conforma-70tion and assembly of the cytoskeleton (Ruelland and Zachowski,2010). Such reactions activate adaptive processes like expres-sion of heat shock proteins, until new cellular equilibriums arereached. However, temperatures above the optimum for growthcan be deleterious, causing injury or irreversible damage, which75is generally called ‘heat stress’ (Wahid et al., 2007). Heat stressis a function of the magnitude and rate of temperature increase,as well as the duration of exposure to the raised temperature(Wahid et al., 2007).

In this review, we present the responses of wheat to el-80evated temperatures during the reproductive and grain-fillingstages. We describe common morphological, physiological, andmolecular responses and explore how these responses can beexploited to improve heat tolerance. Wheat (Triticum aestivumL.) is very sensitive to high temperature (Slafer and Satorre,851999) and trends in increasing growing season temperatureshave already been reported for the major wheat-producing re-gions (Gaffen and Ross, 1998; Alexander et al., 2006; Hennessy

et al., 2008). Wheat experiences heat stress to varying degreesat different phenological stages, but heat stress during the repro- 90ductive phase is more harmful than during the vegetative phasedue to the direct effect on grain number and dry weight (Wol-lenweber et al., 2003). End-of-season or ‘terminal’ heat stressis also likely to increase for wheat in the near future (Mitraand Bhatia, 2008; Semenov, 2009). Hence the main focus is 95on responses to elevated temperatures during reproductive andgrain-filling stages and processes that affect grain yield.

II. IMPACT OF TERMINAL HEAT STRESSThe optimum temperature for wheat anthesis and grain fill- 100

ing ranges from 12 to 22◦C (Table 1). Exposure to temperaturesabove this can significantly reduce grain yield (McDonald etal., 1983; Macas et al., 1999, 2000; Mullarkey and Jones, 2000;Tewolde et al., 2006). Heat stress during anthesis increases flo-ret abortion (Wardlaw and Wrigley, 1994). Heat stress during 105the reproductive phase can cause pollen sterility, tissue dehy-dration, lower CO2 assimilation and increased photorespiration.Although high temperatures accelerate growth (Fischer, 1980;Kase and Catsky, 1984), they also reduce the phenology, which isnot compensated for by the increased growth rate (Wardlaw and 110Moncur, 1995; Zahedi and Jenner, 2003). However, tempera-tures �30◦C, during floret formation, may cause complete steril- Q1

ity (Saini and Aspinal, 1982). Therefore, when temperatures areelevated between anthesis to grain maturity, grain yield is re-duced because of the reduced time to capture resources (Fig. 1). 115

TABLE 1Base (Tmin), optimum (Topt) and maximum (Tmax)

temperatures for various reproductive phases in wheat

Stage TemperatureMean temperature

(◦C)Number of

papers

Terminalspikelet

Tmin 1.8 ± 0.25 14

Topt 11.7 ± 1.61 11Tmax > 21.4 ± 2.33 8

Anthesis Tmin 9.7 ± 0.43 7Topt 23.0 ± 1.15 9Tmax 32.0 ± 1.74 6

Grain filling Tmin 9.6 ± 0.75 11Topt 21.3 ± 1.27 12Tmax 34.3 ± 2.66 9

Note: Data taken from Al-Khatib and Paulsen (1984); Amani et al.(1996); Anjum et al. (2008); Anwar et al. (2007); Asseng et al. (2010);Barnabas et al. (2008); Blum et al. (2001); Calderini et al. (1999);Ferris et al. (1998); Fischer (1980, 1985); Fokar et al. (1998); Gibsonand Paulsen (1999); Guedira et al. (2002); Pushpalatha et al. (2008);Rahman et al. (1977); Samra and Singh (2005); Shewry (2009); Spiertzet al. (2006); Stone and Nicolas (1994, 1995a, b); Stone et al. (1995);van Herwaarden et al. (1998); Wardlaw (1994); Wollenweber et al.(2003); Yang et al. (2002); Zhao et al. (2007, 2008).


HEAT STRESS IN WHEAT 3

FIG. 1. Influence of mean temperatures from anthesis to harvest maturity on(a) grain yield and (b) number of grains per ear in winter wheat (data fromWheeler et al., 1996a, b).

From 1950 to 1993, the increase in global daily minimumtemperatures was more than double the increase in daily max-imum temperatures (Easterling et al., 1997). Increased dailyminimum temperature appears to have greater impact on wheatproduction as grain yield is more strongly negatively correlated120with increasing minimum temperatures than maximum temper-atures (Lobell et al., 2005). For instance, in Mexico, wheatyield decreased by 10% for every 1◦C increase in night-timetemperature, but the same increase in day-time temperature hadno significant effect (Lobell et al., 2005). Night temperatures125>20◦C can reduce spikelet fertility with a concomitant reduc-tion in grain number and size (Prasad et al., 2008a). Increasednight temperatures also linearly decrease the duration of grainfilling. For example, Prasad et al. (2008a) found that night tem-peratures of 20 and 23◦C reduced the grain-filling period by 3130and 7 d, respectively.

A. PhotosynthesisPhotosynthesis is the most sensitive physiological process

to elevated temperature (Wahid et al., 2007) and any reduc-tion in photosynthesis affects growth and grain yield of wheat135(Al-Khatib and Paulsen, 1990, 1999). Heat stress reduces pho-tosynthesis through disruptions in the structure and function ofchloroplasts, and reductions in chlorophyll content (Xu et al.,1995). The inactivation of chloroplast enzymes, mainly induced

by oxidative stress, may also reduce the rate of leaf photosyn- 140thesis. Oxidative stress may induce lipid peroxidation leading toprotein degradation, membrane rupture and enzyme inactivation(Sairam et al., 2000).

1. Rubisco and PhotorespirationRibulose-1,5-bisphosphate carboxylase/oxygenase (Ru- 145

bisco) is a key enzyme that regulates carboxylation during pho-tosynthesis (Ogren, 1984). The inhibition of photosynthesis dueto high temperature is often attributed to increases in the rateof photorespiration. This is because the solubility of CO2 andO2, and the kinetics of Rubisco are affected under high tem- 150peratures (Fig. 2; Ogren, 1984; Long et al., 2004). However,reductions in net photosynthetic rate due to high temperatureare also attributed to non-photorespiratory processes (Fig. 2;Crafts-Brandner and Salvucci, 2000; Pushpalatha et al., 2007).

Rubisco activase (RCA), a cytosol-synthesized chloroplast 155protein, facilitates the removal of inhibitory sugar phosphatesfrom Rubisco-active sites and thus regulates the Rubisco activity(Salvucci and Ogren, 1996). This RCA-mediated step is vital asit frees the Rubisco active site for carboxylation (Salvucci andOgren, 1996; Spreitzer and Salvucci, 2002). Upon exposure to 160high temperature, Rubisco is deactivated because of faster rateof end product formation or slower reactivation by RCA, resul-tantly Rubisco activase looses its ability in keeping the Rubiscoactive and efficient (Salvucci and Crafts-Brandner, 2004a, b).Demirevska-Kepova et al. (2005) observed changes in the abun- 165dance of Rubisco large and small subunits and RCA in wheatleaves upon exposure to heat stress (40◦C) in darkness or inlight. Heat stress for 24 h in darkness irreversibly decreased theRubisco subunits and RCA.

Rubisco is more sensitive to increased temperatures than the 170rest of the enzymes involved in carboxylation. For example, sig-nificantly higher phosphoenolpyruvate (PEP) carboxylase ac-tivities and lower Rubisco activities were observed in each ofthe non-leaf photosynthetic organs (e.g., awn, glume, lemma,peduncle, and sheath) compared with the flag leaf blade (Xu 175et al., 2004). Heat stress (34/17◦C) for 12 d rapidly decreasedRubisco activity, whereas the activity of PEP carboxylase in-creased initially but later declined in all organs. Higher PEP car-boxylase/Rubisco ratios were maintained, particularly in non-leaf organs, which had higher PEP carboxylase/Rubisco ratios 180than the flag leaf at all times (Xu et al., 2004).

Although Rubisco catalytic activity increases with tempera-ture, its low affinity for CO2 and ability to act as an oxygenaselimit the chance of increasing net photosynthesis with temper-ature (Salvucci and Crafts-Brandner, 2004a). At high tempera- 185tures, the solubility of oxygen decreases to a lesser extent thanCO2, resulting in increased photorespiration and lower photo-synthesis (Lea and Leegood, 1999).

2. Photosynthetic ApparatusThrough effects on photosystem II (PSII)- and photosystem 190

I (PSI)-mediated electron transfer, and Calvin cycle activity,


4 M. FAROOQ ET AL.

Heat stress

Limited carboxylation

Lower CO2 solubility

Increasedphotorespiration

Down-regulation of

non-cyclic e-transport

Obstructed ATPsynthesis

Declinedphotosynthesis

ROS production

Attack onmembranes

Leaf senescence

Diminished activities of PEPcase, NADP-ME, FBPase, PPDK, Rubisco

4C/Art

FIG. 2. Possible mechanism in which photosynthesis is reduced under heat stress. Heat stress disturbs the balance between production of reactive oxygenspecies (ROS) and antioxidant defence causing accumulation of ROS, which induces oxidative stress. With increases in ambient temperature, CO2 solubility inwater decreases, which not only reduces carboxylation directly but also directs more electrons to form ROS and promotes photorespiration. Severe heat stresslimits photosynthesis due to a decline in activities of ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco), phosphoenolpyruvate carboxylase (PEPCase),NADP-malic enzyme (NADP-ME), fructose-1, 6-bisphosphatase (FBPase) and pyruvate orthophosphate dikinase (PPDK). Heat stress increases leaf senescenceand thus limits photosynthetic area. Moreover, non-cyclic electron transport is down-regulated to match the reduced requirements of NADPH production and thusreduces ATP synthesis. (Color figure available online).

exposure to heat stress (40◦C) damages the photosynthetic ap-paratus (Baker, 1991; Sharkey, 2005). However, under moderateheat stress (<40◦C), no inhibition of PSII has been observed,even though there was a substantial reduction in carbon assim-195ilation (Law and Crafts-Brandner, 1999; Sharkey, 2005). PSIIappears to be influenced by temperatures above 45◦C (Sharkey,2005) but is not severely affected by moderately high temper-atures (<40◦C) (Allakhverdiev et al., 2008). Nonetheless, PSIIrepair is impeded due to reactive oxygen species induced dam-200age on the protein de novo synthesis system, thus reducing car-bon fixation and oxygen evolution, and disrupting linear electronflow.

Prasad et al. (2008b) reported that the most important rea-sons for PSII sensitivity to high temperature are heat-induced205increase in thylakoid membrane fluidity and electron-transport-dependent integrity of PSII. The inhibition of PSII electrontransport under heat stress is often indicated by a sharp increasein the basal level of chlorophyll fluorescence that correspondsto photosynthetic inhibition (Ristic et al., 2007). Heat-stress-210induced damage and disruption of the integrity of thylakoidmembranes also causes the photophosphorylation to cease (Diasand Lidon, 2009).

Heat stress and excessive light may damage PSII-active sites.Heat stress may also separate the light harvesting complex-II 215(LHCII) from the PSII core complex physically (Schreiber andBerry, 1977). Despite increased thylakoid membrane leakiness,cyclic electron transport around PSI, stimulated by high tem-perature, may help in maintenance of high ATP contents andincrease in pH-related non-photochemical quenching (Bukhov 220et al., 1999).

B. Leaf SenescenceLeaf senescence is the progressive loss of green leaf area

that occurs during reproductive development of a crop (Nooden,1988). As plants use the resources to cope with the stress, limited 225assimilates remain available for reproductive development. Heatstress further triggers the senescence-related metabolic changesin wheat (Al-Khatib and Paulsen, 1984; Paulsen, 1994). In ad-dition, chlorophyll biosynthesis is inhibited under exposure toheat stress (42◦C; Tewari and Tripathy, 1998), which hastens leaf 230senescence. The breakdown of thylakoid components is also ac-celerated by heat stress, leading to leaf senescence (Hardinget al., 1990).



Diurnal temperature differences are also important in thisregard; for instance, larger diurnal fluctuations promoted senes-235cence of flag leaves under high-temperature conditions (Zhaoet al., 2007).

C. Water RelationsLeaf relative water contents (LRWC), leaf water potential,

stomatal conductance and rate of transpiration are influenced240by leaf and canopy temperature (Farooq et al., 2009a, b). Indry environments, higher temperatures lead to higher vapourpressure deficits, which drive higher evapotranspiration. As soilwater is depleted, LRWC and leaf water potential decrease.However, evaporation from the leaf surface enhances leaf and245canopy cooling, so overheating may be ameliorated by higherrates of transpiration.

Although trade-offs exist between heat balance, stomatal reg-ulation and depletion rate of limited soil water, there is a ten-dency for most species to conserve water over temperature reg-250ulation, particularly when ambient temperatures exceed 30◦C(Martınez-Ballesta, 2009). There is limited information on thedynamics of water and heat balance for wheat during reproduc-tive and grain-filling stages, but an example of the dynamicsin seedlings occurred in the study by Machado and Paulsen255(2001). LRWC and leaf water potential were not affected byheat stress when soil water content was close to field capacity,but relative water contents were slightly affected by day/nighttemperatures of 40/35◦C. When water was withheld under thehighest temperature, relative water content and leaf water po-260tential decreased as soil water content decreased to 18%, andleaves ultimately senesced and plants died. Transpiration ratesalso decreased with increasing temperature (from 15/10◦C to40/35◦C) and plant growth decreased (Machado and Paulsen,2001). However, soil water content decreased more rapidly when265the temperature imposed was 25◦C or above, which was prob-ably due to greater soil evaporation, which was not controlled.Root temperature, however, was not controlled in their study or,as is the case in most heat stress studies, since root function-ing in water and nutrient uptake is particularly sensitive to heat270(reviewed by Martınez-Ballesta, 2009), elevated root tempera-tures may confound results. In another study, high temperatures(35/25◦C) after tillering significantly reduced water potential intwo wheat genotypes at anthesis and 7 and 15 d after anthe-sis, with a greater reduction in the genotype more susceptible275to temperature stress (Almeselman et al., 2009). Sairam et al.(2000) also reported that relative water contents were substan-tially reduced by increased temperature.

During reproductive and grain-filling phases, water is neededfor stem and peduncle elongation to raise the ear up through the280unfolding leaf to the top of the canopy; cell expansion andgrowth of all parts of the ear; facets of flowering, such as pollenripening, rapid extension of stamen filaments and fertilization;grain growth and filling. Water flow for many of these processesinvolves crossing membranes, possibly facilitated by aquapor-285ins. Elevated temperature tends to increase hydraulic conduc-

tivity of membranes and plant tissues due to increased aqua-porin activity, membrane fluidity and permeability (Martınez-Ballesta, 2009) and, to a greater degree, reduced water viscositywith increasing temperature (Cochard et al., 2007). Increasing 290hydraulic conductivity may be beneficial in leaves and roots,minimizing changes in leaf water potential, so stomata can stayopen for longer. Alternatively, increased permeability of mem-branes may cause flowers and grains to dehydrate, particularly ifgradients driving water flow into flowers or grains are disrupted 295by heat stress.

D. Grain Growth and DevelopmentGrain development is impacted by heat stress because assim-

ilate translocation and grain-filling duration and rate are influ-enced directly by changes in ambient temperature. The extent 300of heat-driven damage is dependent on the level of heat stress.

1. Grain Number and SizeBoth grain number and weight are sensitive to elevated tem-

perature (Ferris et al., 1998). Influence of temperature on eachof these components of grain yield depends on the developmen- 305tal phase at which the elevated temperature occurs. For instance,between spike initiation and anthesis, temperatures above 20◦Cmay substantially reduce grain number per spike (Saini andAspinall, 1982). Several events during this phenostage that in-fluence grain number include spikelet initiation, floral organ 310differentiation, male and female sporogenesis, pollination andfertilization. Heat stress speeds up development of the spike(Porter and Gawith, 1999) reducing spikelet number and thus,the number of grains per spike (Saini and Aspinall, 1982). How-ever, the period between spike initiation and anthesis is not the 315most sensitive period to heat stress. The most sensitive periodis between the appearance of double ridges on the shoot apexand flag leaf. An inverse relationship between duration of heatstress and grain number per spike has been observed during thistime (Rawson and Bagga, 1979). The reason for this sensitivity 320is because spikelets begin to form in the spike from ridges oftissue between ridges of undifferentiated leaf primordia, calledthe double ridge stage. Each spikelet meristem then starts toproduce florets (McMaster, 1997). The reduction in the dura-tion of emergence to double ridge and double ridge to anthesis 325reduces spikelet number per spike and grain number per spikelet(McMaster, 1997).

Although high temperature (>30◦C) during floret develop-ment may cause complete sterility (Saini and Aspinall, 1982),variation among wheat genotypes has also been observed (Table 3302; Gibson and Paulsen, 1999; Anjum et al., 2008; Zhao et al.,2008). Heat stress around floral initiation has severe effects ongrain number. For instance, grain number per spike decreased by4% for every 1◦C (from 15–22◦C) increase in the 30 d preced-ing anthesis (Fischer, 1985). The availability of carbohydrates 335for floret development is one factor determining grain num-ber (Abbate et al., 1995; Demotes-Mainard and Jeuffroy, 2004)because inadequate availability of assimilates may cause floret


TAB

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2In

fluen

ceof

tem

pera

ture

onw

heat

grai

nw

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t(m

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indi

ffer

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Tem

pera

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(◦ C)

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-79

Atti

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V21

83

1430

3115

5150

35.5

42.5

47.8

1837

3820

2755

5022

3232

31.6

27.9

33.1

2525

2326

2929

2839

4032

3410

4236

2926

.123

.930

.235

3831

3827

3139

4448

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son

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.(20

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Mea

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6



death (Kirby, 1988). Wheat plants exposed to 30◦C for 3 consec-utive days, when pollen mother cells were dividing, substantially340reduced grain set and therefore grain yield (Saini and Aspinall,1982). Reduction in grain set was also observed when plantswere exposed for 1 day to 30◦C, or for 3 days to day/night tem-peratures of 30/20◦C (Saini and Aspinall, 1982). Reductions ingrain yield due to reduced grain set are not compensated for by345increases in grain weight (Saini and Aspinall, 1982). Heat stressalso impairs viability of anthers and pollen, resulting in poorfertilization (Saini and Aspinall, 1982; Ferris et al., 1998). Thesensitivity of pollen to heat stress is associated with the inabilityof pollen to synthesize heat shock proteins (HSPs; Mascaren-350has and Crone, 1996). Heat stress effects during pre-anthesis,particularly during meiosis and growth of the ovaries whichmay impose an upper limit for potential grain weight, are alsoassociated with reduced grain numbers (Calderini et al., 1999).

Elevated temperatures reduce the duration between anthesis355and physiological maturity (Warrington et al., 1977), which isassociated with a reduction in grain weight (Warrington et al.,1977; Shpiler and Blum, 1986). Reduced grain weight (∼1.5mg per day) can occur for every 1◦C above 15–20◦C (Streck,2005).360

Variability in terms of high temperature effects on wheatgrain number and size appears to be related to genotypic dif-ferences in heat tolerance (Viswanathan and Khanna-Chopra,2001; Tahir and Nakata, 2005). For instance, Castro et al. (2007)observed smaller grains in 14 spring wheat genotypes regardless365of duration and timing of the high temperature event. Whereasincrease in temperature (from 30 to 38◦C), during reproductivephase, reduced the main stem grain weight by 20 to 44% (Tahirand Nakata, 2005).

Elevated temperatures can also cause grain shrinkage through370ultrastructural changes in the aleurone layer and endospermcells (Fig. 3), as observed by Dias et al. (2008) when day/nighttemperatures increased from 25/14◦C to 31/20◦C. In the absenceof heat stress, the aleurone layer of a wheat grain has large cells(Fig. 2) surrounding a starchy endosperm. Under heat stress,375the endosperm’s cellular structure is denser, packed with starchgranules embedded in the protein matrix (Fig. 3; Pyler, 1988).

2. Starch SynthesisStarch accounts for ∼70% of wheat grain dry weight, and

reduced starch deposition is the main reason of reductions in380grain weight (Bhullar and Jenner, 1985). As the enzymes in-volved in starch biosynthesis, in developing kernels of wheat,are sensitive to high temperature, the process is sensitive to heatstress (Denyer et al., 1994; Jenner, 1994). As temperatures riseabove 18–22◦C, the duration of starch biosynthesis and depo-385sition to grain is reduced (Spiertz et al., 2006). Reductions instarch content account for most of the reduction in grain drymatter at temperatures above 18–22◦C (Spiertz et al., 2006).

Sucrose synthase, soluble starch synthase (SSS) and granule-bound starch synthase are the three enzymes which rate limit390starch biosynthesis in wheat (Hawker and Jenner, 1993). Sucrose

synthase is likely to be important in determining the rate ofstarch synthesis (Hawker and Jenner, 1993; Keeling et al., 1993),whereas granule-bound starch synthase controls the amylosebiosynthesis of (Morell et al., 2001). SSS regulates the synthesis 395of starch and is sensitive to heat stress (Rijven, 1986; Keelinget al., 1993, 1994). Heat stress decreases the activity of SSS inwheat, reducing grain growth and starch accumulation (Prakashet al., 2003, 2004). Even short periods of episodic temperatureover 30◦C slows starch accumulation principally due to heat- 400induced denaturation of SSS (Jenner, 1994).

3. Grain Filling Rate and DurationHeat stress accelerates the rate of grain filling whereas grain

filling duration is shortened (Dias and Lidon, 2009). For in-stance, 5◦C increases in temperature above 20◦C increased the 405rate of grain filling and reduced the grain filling duration by 12days in wheat (Yin et al., 2009). Under these conditions, the sup-ply of photoassimilates may be limited (Calderini et al., 2006).It is estimated that for every 1◦C above the optimal growingtemperature of 15–20◦C, the duration of grain-filling is reduced 410by 2.8 d (Streck, 2005).

The rate of grain growth increases as temperature increases,but this apparently depends on whether the number of grains perspike is reduced (Sofield et al., 1977). In spikes where the num-ber of grains is less affected by elevated temperature, spikelets 415reduce the rate of grain growth (Sofield et al., 1977). Therefore,we would expect that an increase in the grain filling rate couldcompensate for the shorter grain-filling period; however, thisdid not occur at temperatures above 30◦C (Sofield et al., 1977).Other studies have also reported that the duration of grain filling 420under heat stress was not compensated by greater grain-fillingrates (Wardlaw et al., 1980; Stone et al., 1995). Furthermore,Viswanathan and Khanna-Chopra (2001) showed that both du-ration and rate of grain growth were reduced by heat stress ingenotypes differing in grain weight stability. 425

4. Assimilate TranslocationDuring grain filling, assimilates are transferred from either

current assimilation or from pre-anthesis stored stem reserves(Palta et al., 1994; Blum, 1998). Under ideal conditions, 90to 95% of carbon required for grain filling is transferred from 430current carbon assimilation (Kobata et al., 1992). Under waterand heat stress, the relative contribution of pre-anthesis storedreserves and current assimilation changes substantially (Evanset al., 1975; Palta et al., 1994). When the photosynthetic sourceof assimilates is reduced by heat stress, the alternative source for 435grain filling is remobilized stem reserves. The demand for stemreserves under heat stress dramatically increases, ranging from6 to 100% depending on the heat-induced reduction in photo-synthesis (Blum, 1998). However, under heat stress genotypicvariation exists for the contribution of stem reserves for grain 440filling (Yang et al., 2002). For instance, current photosynthe-sis can provide 63 and 65% of assimilates to grain at 20/15◦Cand 30/25◦C day/night temperatures, respectively (Blum et al.,


8 M. FAROOQ ET AL.

FIG. 3. Scanning electron microscopy of grains of wheat cultivars (a) Golia and (b) Sever under optimal and heat stressed conditions (reproduced from Diaset al. 2008; with permission from The Brazilian Journal of Plant Physiology).

1994). Tolerance to heat stress is associated with genotypes withstable photosynthesis, but also those with high capacity to store445stem reserves (Blum et al., 1994).

At high temperatures, assimilate translocation which occursthrough both symplastic and apoplastic pathways, is substan-

tially reduced. Assimilate transport from flag leaf to grain issubstantially reduced by temperatures above 30◦C but there is 450no influence of temperature (from 1 to 50◦C) on translocationfrom the stem (Wardlaw, 1974). This indicates that, in wheat,the effect of heat stress on assimilate translocation is indirect



even though heat stress reduces the rate of assimilate transportfrom vegetative organs to grain (Plaut et al., 2004).455

E. Grain QualityGrain protein content and grain size are the most important

characteristics determining grain quality in wheat (Coles et al.,1997). Heat stress during grain-filling phase affects the grainprotein contents (Wardlaw et al., 2002; Gooding et al., 2003)460through reductions in starch deposition, which influences pro-tein concentration by allowing more nitrogen per unit of starch(Stone and Nicolas, 1998). Although the daily flow of carbonand nitrogen into grain increases with increasing temperature,carbon flow decreases per degree-day (Wardlaw et al., 1980;465Daniel and Triboi, 2000). As a result, grain size is more affectedby temperature than quantity of grain nitrogen (Uhlen et al.,1998; Daniel and Triboi, 2000).

Grain protein content is inversely related to grain size(Guttieri et al., 2000; Erekul and Kohn, 2006). Whilst grain470protein content increases under heat stress, the functionalityof protein significantly decreases (Corbellini et al., 1997), af-fecting end-use quality. Total grain protein content of the cropdecreases under heat stress because heat stress decreases grainyield (Stone and Nicolas, 1998; Castro et al., 2007). Heat stress475also decreases the duration, but not rate, of protein deposition

in the grain (Castro et al., 2007). The greatest increase in grainprotein content in wheat occurs when heat stress is imposedearly in grain filling (Castro et al., 2007). However, exposure toheat stress decreases synthesis of glutenin, while synthesis of 480gliadins remains stable or increases (Majoul et al., 2003). Heatstress also decreases the sedimentation index as an effect associ-ated with increased protein content in grain, but with decreasedlevels of essential amino acids (Dias et al., 2008).

III. TOLERANCE MECHANISMS OF TERMINAL HEAT 485STRESS

Plants tend to reduce heat-induced damage by leaf rolling,leaf shedding, reducing leaf size, thickening leaves, reducinggrowth duration, transpirational cooling and other adjustmentsin morphology and ontogeny (Wahid et al., 2007). Plant re- 490sponses to heat stress are mediated by an intrinsic capacity toendure basal thermotolerance and, after acclimation, the abilityto gain thermotolerance. The capability of crop plants to sur-vive and produce good grain yield under heat stress is generallyregarded as heat tolerance (Wahid et al., 2007). Changes and 495mechanisms that enable the plants to cope with heat stress aregiven in Fig. 4.

Heat stress

Receptor

H2O2

ABA

Ca+2

NO}

SA

Mitochondria/Chloroplast

Cytoplasm

Protein Kinases

Transcription factors

Nucleus

Changes in gene expression,

protein/enzyme abundance

and regulation

Antioxidant activation /de novo synthesis

Proline, GB, GABA

accumulation

Reduced

senescence

HSPs

Heat resistance

4C/Art

FIG. 4. Proposed cellular events and signalling cascades in a plant cell responding to heat stress. Heat stress is perceived by perturbation to cellular equilibrium,which then activates signals possibly by hydrogen peroxide (H2O2), abscisic acid (ABA), calcium (Ca+2) and nitric oxide (NO). These signals then induce synthesisof specific protein kinases, which activate more downstream responses such as changes in gene expression. The response to these signalling cascades also resultsin changes in plant metabolism, activation and synthesis of antioxidants, synthesis of heat shock proteins, and accumulation of osmoprotectants and solutes, andreduces senescence under heat stress. (Color figure available online).


10 M. FAROOQ ET AL.

A. Antioxidant Defense SystemReactive oxygen species (ROS),—superoxide radicals, hy-

droxyl radicals, and hydrogen peroxide—are produced in the500cells in a natural fashion, but overproduction of these com-pounds can be harmful (Esfandiari et al., 2007). Heat stresstriggers the production and accumulation of ROS (Sairamet al., 2000; Mittler, 2002; Almeselmani et al., 2009). Hencetheir detoxification by antioxidant systems is important for pro-505tecting plants against heat stress (Asada, 2006; Suzuki and Mit-tler, 2006).

The antioxidant defense system in plants involves both en-zymatic and non-enzymatic antioxidant systems. The enzy-matic antioxidant system includes ascorbate peroxidase, dehy-510droascorbate reductase, glutathione S-transferase, superoxidedismutase, catalase, guaiacol peroxidase, and glutathione re-ductase (Noctor and Foyer, 1998). Non-enzymic antioxidantsinclude glutathione, ascorbate and tocopherols.

Superoxide dismutase converts O−2 to hydrogen peroxide,515

whereas catalase and peroxidases breakdown hydrogen perox-ide. Catalase eliminates hydrogen peroxide by catalyzing itsdecomposition to H2O and O2. Both guaiacol peroxidase andascorbate peroxidase can detoxify hydrogen peroxide, but bothenzymes need hydrogen peroxide to be scavenged by reducing520agents. Ascorbate helps scavenge OH, O−

2 and hydrogen per-oxide for the ascorbate-peroxidase-mediated reactions, whileguaiacol scavenges ROS for guaiacol peroxidise–mediated re-actions (Goyal and Asthir, 2010).

Balla et al. (2009) demonstrated that upon exposure to heat525stress, during the reproductive phase, activities of enzymaticantioxidants were substantially increased in heat-tolerant geno-types of wheat. The activities of catalase and superoxide dismu-tase have been correlated with heat stress (34/22◦C) during thereproductive phase (Zhao et al., 2007), as well as the capacity530to acquire thermotolerance (Almeselmani et al., 2009). Like-wise, protection of wheat plants from heat-induced oxidativedamage during the reproductive phase has also been correlatedwith non-enzymic antioxidants, such as ascorbate (Sairam et al.,2000).535

B. Molecular Basis of Heat ToleranceExpression of heat shock proteins (HSPs) is the most studied

molecular response under heat stress. HSPs save proteins fromheat-induced aggregation and thus during the recovery period,facilitates their re-folding (Hendrick and Hartl, 1993; Schoffl540et al., 1998; Feder and Hofmann, 1999; Maestri et al., 2002).Expression of HSP genes is a fundamental response to heatstress (Rampino et al., 2009). When exposed to high temperature(>35◦C), normal protein synthesis in wheat is reduced, but HSPsare produced (Blumenthal et al., 1994).545

In wheat genotypes grown at 32 to 35◦C, Nguyen et al.(1994) detected messenger RNAs encoding a major class of lowmolecular weight HSPs—HSP 16.9. In another study, whereseveral wheat varieties were exposed to 3.2 to 3.6◦C higherthan normal, HSP 18 accumulated in developing grains of heat-550

tolerant varieties more than susceptible types (Sharma-Natuet al., 2010). Sumesh et al. (2008) also observed higher HSP 100content at elevated temperature in a relatively tolerant variety.

Dehydrin proteins belong to Group 2 late embryogenesisabundant proteins (LEA). Dehydrins help to stabilize macro- 555molecules against heat-induced damage (Brini et al., 2010). Inwheat, for instance, DHN-5 protein helped protect and stabilizekey enzymes to start metabolism (Brini et al., 2010).

C. Stay-greenLeaf senescence starts early in response to heat stress, par- 560

ticularly when these stresses occur during post-flowering stagesof grain filling. Therefore, maintenance of leaf chlorophyll andphotosynthetic capacity, called ‘stay-green,’ is considered an in-dicator of heat tolerance (Fokar et al., 1998). Because the lossof chlorophyll is associated with less assimilation of current 565carbon into grains (see above), stay-green genotypes should bebetter able to maintain grain filling under elevated temperatures.

Certain stay-green sorghum genotypes have been found tocontain higher specific leaf nitrogen contents, indicating thatthis trait is correlated with shoot nitrogen content (Borrell 570et al., 2001). The stay-green trait has been evaluated in sev-eral crops (Harris et al., 2007; Kumari et al., 2007), but breed-ing for this trait has been limited in wheat. Although threecomponents—chlorophyll content at anthesis, duration of senes-cence, and rate of senescence—determine the stay-green fea- 575ture during heat stress, the rate of senescence, not the start ofsenescence, is important component of stay-green (Harris et al.,2007).

IV. STRATEGIES TO IMPROVE HEAT STRESSTOLERANCE 580

Development and selection of crop varieties is, most often,aimed at improving yield under existing climatic conditions.With the changing climate, in particular episodes of high tem-perature during the reproductive phase, ideotypes with physi-ological, morphological, and molecular traits unique for heat 585tolerance are required (Semenov and Halford, 2009). Strategiesto improve heat stress tolerance in wheat include crop improve-ment through breeding and molecular tools, and agronomic andother management practices.

A. Selection and Breeding for Heat Tolerance 590

Expansion of genetic variability in the wheat gene pool is im-portant for breeding programs aimed to improve heat toleranceduring reproductive and grain-filling stages. Although severalreports indicate the existence of genetic diversity for heat tol-erance in conventional wheat varieties (Wardlaw, 1994; Fokar 595et al., 1998; Calderini et al., 1999; Gibson and Paulsen, 1999;Spiertz et al., 2006; Anjum et al., 2008; Zhao et al., 2008), newsources of genetic diversity must be explored. One option is tocross-breed wheat (Triticum aestivum) with its key ancestors,Aegilops tauchii and Triticum durum. 600



TABLE 3QTLs identified for heat tolerance in wheat during the

reproductive phase

Trait Chromosome Reference

Rate of senescence 2A Vijayalakshmiet al. (2010)

6A6B

Greenness at maximumsenescence

4B

5D3A6B

SPAD chlorophyllcontent

7B

Fv/Fm chlorophyllfluorescence

7A

Yield 4ACanopy temperature 4A Pinto et al.

(2010)Number of grains 1A, 2A, 3B, 4A, 5BGrain weight 1B, 2B, 3B, 5A, 6DDays to flowering 2D, 7D Mason et al.

(2010)Stay-green 1A, 3B, 7D Kumar et al.

(2010)

Through conventional breeding, genetic variability for heattolerance amongst breeding lines/varieties can be identified.Breeding and pre-breeding involves selection and genotypescreening. Selecting genotypes for high yield under heat stress is

the most important strategy; it is, however, expensive due to the 605high cost associated with conducting yield trials in controlledenvironments. Selection and screening can be based on char-acteristics associated with better yields under heat stress. Thecharacters used as selection criteria for heat tolerance shouldbe: (1) strongly correlated with grain yield under heat stress; (2) 610rapid, stable, and easy to measure; and (3) highly heritable (Ed-meades et al., 2001). Potential traits for screening heat tolerancein wheat are shown in Table 4. Q2

Genotype screening based on electrolyte leakage, an indexof membrane stability, from leaves subjected to extreme tem- 615peratures, is one of the rapid screening methods (Blum, 1988;Shanahan et al., 1990). Electrolytes are collected from stressedtissue soaked in deionized water and quantified by measuringelectrical conductivity (Ibrahim and Quick, 2001). Correlationbetween membrane stability and grain yield under heat stress 620has been found (Blum et al., 2001).

Reduction of tetrazolium triphenyl chloride in mitochondriamay also be used as an indicator of heat tolerance. Here, tetra-zolium triphenyl chloride solution is vacuum-infiltrated into leaftissues exposed to high temperature. Cell viability is quantified 625by the relative level of tetrazolium triphenyl chloride reductionto formazan, which is detected by spectrophotometer (Towilland Mazur, 1974).

Genotypes may also be screened for depression of canopytemperature, flag-leaf stomatal conductance and photosynthetic 630rate, which are highly correlated with field performance andgrain yield under heat stress (Reynolds et al., 1994, 1998; Amaniet al., 1996).

Landraces are varieties adapted to their native environment.Most of today’s wheat varieties have been derived from lan- 635draces (Trethowan and Mujeeb-Kazi, 2008). Significant vari-ability for heat tolerance exists amongst landraces. For instance,

TABLE 4Potential traits/characters for screening wheat for heat tolerance

S. No. Trait/character Correlated with yield Reference

1 Inhibition of meiosis No Saini et al. (1983); Zeng et al. (1985)2 Photosynthesis rate Yes Reynolds et al. (1994)3 Leaf chlorophyll content Yes Reynolds et al. (1994)4 Canopy temperature depression Yes Shanahan et al. (1990); Reynolds et al. (1994,

1998); Amani et al. (1996); Blum et al. (2001);5 Membrane stability Yes6 Flag-leaf stomatal conductance Yes Reynolds et al. (1994)7 Grain weight No clear evidence Tyagi et al. (2003); Singha et al. (2006); Dias and

Lidon (2009);8 Tetrazolium triphenyl chloride

reductionNo clear evidence Towill and Mazur (1974)

9 Early heading No clear evidence Tewolde et al. (2006)10 High temperature index No clear evidence Rane and Nagarajan (2004)11 Stay-green No Reynolds et al. (2001); Xu et al. (2000)


12 M. FAROOQ ET AL.

heat-tolerant landraces tend to have higher leaf chlorophyll con-tents (Hede et al., 1999) and higher stomatal conductance. Thesematerials may be used in breeding programs aimed to induce640heat tolerance in wheat.

Maintaining grain weight under heat stress during grain fill-ing is a measure of heat tolerance (Tyagi et al., 2003; Singhaet al., 2006). In this regard, Dias and Lidon (2009) proposedthat high grain-filling rate and high potential grain weight can645be useful selection criteria for improving heat tolerance.

Tewolde et al. (2006) reported that early-heading varietiesperformed better than later-heading varieties because they (1)produced fewer leaves per tiller and retained more green leaves,(2) had longer grain-filling periods, and (3) completed grain650filling earlier in the season when air temperatures were lower.

Mass screening of wheat genotypes for heat tolerance mayalso be done for the stay-green character (Reynolds et al., 2001).A visual rating of stay-green is quick and easy way for the plantbreeders to screen on mass scale (Xu et al., 2000). Nonetheless,655this trait may be a disadvantage as it is associated with thetendency to retain the stem reserves (Blum, 1998).

B. Genetic Engineering for Heat ToleranceGenetic engineering involves the introduction of individual

genes, of interest, into the candidate genotypes help in im-660proving tolerance against heat stress (Barnabas et al., 2008).However, wheat’s complex genome has hampered research ongenetic modification compared with other plant species.

Protein synthesis elongation factor in chloroplast (EF-Tu) hasbeen related to heat tolerance in several crops. In wheat, cultivars665that accumulated more EF-Tu at maturity tolerated heat stressbetter than those with less EF-Tu (Ristic et al., 2008). Fu et al.(2008) expressed a maize gene coding for plastidal EF-Tu intransgenic wheat. Transgenic wheat plants had less aggregationof leaf proteins and damage to thylakoids, and higher rate of CO2670fixation compared with non-transgenic plants under heat stress.The study demonstrated that genes, other than HSP genes, maybe used to improve heat tolerance in wheat.

C. Use of Molecular MarkersMost of the traits related with the yield and heat tolerance675

are controlled by several genes each with minor individual butsignificant effects when acting together. In wheat, the quantita-tive trait loci (QTLs) analysis has, partly, been hindered by largegenome size (Bennett et al., 1982). The polyploid nature of thegenome also makes molecular analysis complicated (Barnabas680et al., 2008) due to repetitions of DNA sequences.

Natural genetic variation may be used through direct selec-tion under heat stress during the reproductive phase or throughQTL mapping and subsequent marker-assisted selection. QTLmapping allows assessment of numbers, locations, magnitude685of phenotypic effects, and patterns of gene action (Vinh andPaterson, 2005).

Recently, several QTLs have been identified in wheat for heattolerance during the reproductive phase (Table 3). For instance,

Kumar et al. (2010) identified three QTLs for the stay-green 690character. Likewise, Vijayalakshmi et al. (2010) identified QTLsfor senescence-related traits. Pinto et al. (2010) identified a QTLon chromosome 4A-a for canopy temperature under heat.

In addition to QTLs for senescence/stay-green traits, severalhave been mapped for wheat yield and its related traits under 695heat stress (Table 3). For example, under heat stress a QTL atthe same location as the QTL for canopy temperature accountedfor 17% of yield variation (Pinto et al., 2010). Likewise, Masonet al. (2010) identified 15 and 12 QTLs associated with yield andits associated traits in 2005 and 2006, respectively. The results 700suggest that for heat tolerance main spike should be used for theidentification of QTLs genomic regions Mason et al., 2010).

V. MANAGEMENT STRATEGIESAgronomic strategies for mediating future increases in am-

bient temperature include practices that conserve water (e.g., no 705tillage and stubble retention), fertilization during critical growthstages and timing of sowing. For example, continuous watersupply to heat-stressed wheat helped sustain grain-filling rate,duration and size (Dupont et al., 2006). Of course, this is notpossible in rainfed wheat growing regions if it doesn’t rain. 710

Application of nitrogen, phosphorus and potassium improveplant growth under moderate heat stress (Dupont et al., 2006).When nitrogen, phosphorous and potassium are applied post-anthesis, more protein accumulates in the grain at day/nighttemperatures of 24/17◦C, but not at 37/28◦C. Application of 715some micronutrients such as zinc, can also improve heat toler-ance in wheat (Graham and McDonald, 2001). The timing ofnutrient application to coincide with key developmental stagesis already regularly practiced, such as nitrogen application whenthe spike is 1 cm in length. 720

Time of sowing is another important management strategyin some regions. Although periods of elevated temperature mayoccur during the growing season, grain filling usually occurswhen seasonal temperatures are increasing. Early planting mayavoid terminal heat stress so that grain filling occurs during 725cooler temperatures (Loss and Siddique, 1994).

Other management strategies for improving heat tolerance,such as application of exogenous signalling compounds, os-molytes and certain inorganic salts, are less likely to have asignificant impact on broadacre agriculture, and are therefore 730not discussed here.

VI. CONCLUSIONHigh temperatures causing heat stress in wheat are expected

to increase in frequency across the globe. Heat stress substan-tially affects grain setting, duration and rate, and ultimately 735grain yield. Nonetheless the timing, duration and intensity ofheat stress determine its impact on grain yield. The adversitiesof heat stress can be minimized by developing tolerant geno-types and agronomic strategies.



Even though in wheat, mechanisms of heat tolerance on a740physiological basis are relatively well-understood, research intoassimilate partitioning and phenotypic flexibility are needed.

Molecular knowledge of response and tolerance mechanismsto harvest higher grain yields on a sustainable basis must beexplored. Likewise, use of functional genomics approaches will745be helpful in understanding the molecular basis of the responseof wheat to heat tolerance.

Identifying allelic sources for heat tolerance and their in-trogression into elite lines through conventional breeding andmodern biotechnological and molecular tools (Ortiz et al., 2008)750are an important area for future research. The latest genomics re-sources combined with ecophysiological research may be help-ful to understand the genotypes and the environment interac-tions. An integrated system approach should be designed tostudy the complex quantitative traits like yield stability under755heat stress.

ACKNOWLEDGMENTSM. Farooq thanks The University of Agriculture, Faisalabad,

Pakistan, The Australian Endeavour Research Fellowship, TheUniversity of Western Australia and CSIRO Plant Industry for760support that made his visit to Western Australia possible.

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