Crop Adaptation to Climate Change (Yadav/Crop Adaptation to Climate Change) || Genetic Adjustment to Changing Climates: Rice

P1: SFK/UKS P2: SFK Color: 1C

BLBS082-12 BLBS082-Yadav July 12, 2011 14:29 Trim: 246mm X 189mm

Chapter 12

Genetic Adjustment to ChangingClimates: RiceTanguy Lafarge, Shaobing Peng, Toshihiro Hasegawa, William P. Quick, S.V. KrishnaJagadish, and Reiner Wassmann

Introduction

Rice is a major staple cereal for nearly halfthe world’s population. Increasing consumptionrates of the burgeoning population requires anincrease in annual production by 0.6–0.9% until2050 (Carriger and Vallee 2007). The irrigatedand rainfed rice systems form the mainstay offood security in Asian and increasingly so insome African countries. Since the Green Revolu-tion, highly productive rice systems have evolvedover decades and are in most cases well suitedto the local climatic conditions: as compared toupland systems, flooded rice fields have feweradverse impacts on the local environment due tolow nitrous oxide production and soil erosion,limited groundwater contamination, and littleuse of herbicide (Bouman et al. 2007). Floodedfields, however, emit relatively high amounts ofgreenhouse gases, namely in the form of methane(Wassmann et al. 2000).

Climate change may threaten productivityand sustainability of rice production systems.General circulation models (GCMs) project cli-matic conditions that will have serious adverseimpacts on rice production and in turn on thesocioeconomic setting of the small and marginal

farmers in tropical and subtropical regions. Theprogressively changing climate comes with arange of aggravating biotic and abiotic stressesof drought, salinity, submergence, and more re-cently heat. Agronomic drought is a result ofinsufficient soil moisture to meet crop and cli-mate requirements, which affects 10 Mha of up-land rice and over 13 Mha of rainfed lowlandrice in Asia alone (Pandey et al. 2007). Droughtis especially consequential in areas with unfa-vorable soils, like 800 Mha of saline/sodic landthroughout the world (FAO 2008) that are ef-fectively rendered unproductive during droughtyears. Drought events shall become even morepronounced in rainfed rice areas where the in-creasing climatic demand due to heat will in-crease the crop demand for water. Reversely,drought increases the probability of heat stressby reducing the cooling system in response tostomatal closure. Flooding can result in sustainedsubmergence of the complete rice canopy, whicheventually causes the death of the rice plants.Flooding is increasingly becoming a major pro-duction constraint affecting about 10–15 Mha ofrice fields in South and Southeast Asia and caus-ing yield losses of up to 1 billion USD every year(Dey and Upadhyaya 1996).

Crop Adaptation to Climate Change, First Edition. Edited by Shyam S. Yadav, Robert J. Redden, Jerry L. Hatfield,Hermann Lotze-Campen and Anthony E. Hall.c© 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

298



GENETIC ADJUSTMENT TO CHANGING CLIMATES: RICE 299

The potentially devastating impacts of tem-perature rise, and its interaction with elevated[CO2], in both tropics and subtropics are oftenoverlooked (Battisti and Naylor 2009), while thestresses of drought and submergence have re-ceived ample attention in rice research over re-cent years. Especially, the food-deficient regionsof the world will need major investments to de-velop crop varieties tolerant to direct and indirectstresses of heat as projected by different GCMs(Battisti and Naylor 2009).

Two comprehensive reviews on climatechange adaptation in rice production have re-cently been published (Wassmann et al. 2009a,2009b). While these reviews focused on (1) phys-iological aspects and agronomic basis, and thepossible adaptations, related to spikelet fertilityas far as heat is concerned and (2) regional vul-nerability of climate change impacts, this newreview on genetic adjustment deals with those as-pects of adaptation that have not received properattention in previous reviews: the physiologicaland morphological processes of plant growth inresponse to (1) elevated [CO2], (2) high night-time temperature, and (3) interaction betweenelevated [CO2] and high temperatures.

Direct effects of elevated CO2

concentration

The current CO2 concentration in the atmosphereis a limiting factor for the CO2 fixation pro-cess of C3 plants, so that rising [CO2] promotesleaf-level photosynthesis and thereby increasesbiomass production and grain yield. However,the increment in [CO2] since the industrial rev-olution has already exceeded 100 ppm (from280 ppm in 1800 to 386 in 2008); [CO2] will fur-ther increase to values of 470–570 ppm by 2050depending on the scenario used (IPCC 2007).These projected changes in [CO2] fall into therange in which rice is highly responsive. On onehand, the CO2 “fertilization” has a distinctivelypositive effect on crop growth, which may evendetermine a positive sign of the overall climatechange impacts on crop production (e.g., Parry

et al. 2004). On the other hand, atmospheric[CO2] fluctuates in a fairly narrow range as com-pared to the highly variable climatic factors, sothat its effect on temporal and spatial variabilityof plant performance is relatively low.

Elevated [CO2] affects plant growth in twomajor physiological pathways: namely (1) in-creasing the photosynthetic rate and (2) decreas-ing stomatal conductance, both of which arerelated to gas exchange between leaf and atmo-sphere. These effects further influence crop car-bon gain, plant growth, nutrient conditions, wateruse, and, ultimately, grain yield. While these ef-fects are common across all crop species withthe C3 photosynthetic pathway, the intensity ofthe effects varies depending on species, growthstage, and environmental conditions (Kimballet al. 2002). The positive response of C3 plantsto elevated [CO2] can be seen as a crucial mech-anism to compensate or even supersede detri-mental effects of future climatic conditions. Theaverage increase in leaf photosynthetic rate at asingle leaf level ranged from 30% to 70% de-pending on rice genotype, growth stage, and en-vironment (Lin et al. 1997). At the canopy level,this increase ranged from 30% to 40%, but theassociated gain in crop biomass and yield rangedonly from 15% to 30% (Lin et al. 1997). Simi-larly, Sakai et al. (2006) reported a greater stim-ulus on photosynthesis at early stage, like 30% atmid-tillering, than during grain filling, with only10% at maturity. The positive effect of elevated[CO2] appeared to be downregulated with cropstage. While shoot biomass, sink size, ratio offilled grains, and seed yield were higher underelevated [CO2] in open top chambers, the frac-tion of biomass partitioned to grain, however,did not exceed that under the ambient conditions(De Costa et al. 2006). The genotypic variationin the response of rice to elevated [CO2] was cor-related with the genotypic variation in the pho-tosynthetic rate to saturated-light conditions (DeCosta et al. 2007). In fact, the capacity of therice plant to accumulate more biomass, and soto develop a larger reproductive sink, under ele-vated [CO2] conditions contributed to the greater



300 CROP ADAPTATION TO CLIMATE CHANGE

yield. Interestingly, the positive effect of elevated[CO2] was more pronounced on hybrid rice thanon conventional japonica varieties, with highernumbers in most morphological parameters, e.g.,(1) maximum tiller number, (2) panicle number,(3) plant height, (4) stem dry weight per tiller, (5)spikelet number per panicle, (6) fertility rate, and(7) grain size (Liu et al. 2008). This better adap-tation of hybrid rice was expected as its betterpartitioning efficiency increases the value of thehigher biomass accumulation (Bueno and La-farge 2009; Lafarge and Bueno 2009). Also, theyield response to elevated [CO2] of an indicagenotype like IR72 was higher than that of ajaponica genotype because of its larger sink for-mation ability and its higher source limitationunder ambient [CO2] (Horie et al. 2000). It ap-pears that a sustained stimulation and growth inresponse to elevated [CO2] requires an increaseof sink organ development to utilize and store ad-ditional photosynthate. Thus, the relative magni-tude of source and sink activities is an importantdeterminant of crop yield under elevated [CO2].

The growth responses in two free-air CO2

enrichment (FACE) studies conducted with riceplants (Kim et al. 2003; Yang et al. 2006), andsummarized by Hasegawa et al. (2007), showedthat the temporal pattern of biomass accumu-lation by the FACE treatment was similar inboth studies. Biomass accumulation was rapid attillering stage and slower at harvest. This stage-dependent response to elevated [CO2] could, inprinciple, be a result of (1) downregulation ofphotosynthesis and/or (2) increased respiration.According to canopy-scale gas exchange mea-surements taken under closed chamber systems,downregulation of photosynthesis was identifiedas the major reason for the decreasing trend incanopy carbon gains within the ontogenetic de-velopment of rice (Sakai et al. 2006). At pro-cess level, the downregulation of photosynthe-sis appears to be caused by declining trends inboth maximum carboxylation rate (Vcmax) andmaximum rate of electron transport (Jmax) (Se-neweera et al. 2002; Chen et al. 2005). Because oflower carboxylation and electron transport rates,the plant cannot take full advantage of elevated

[CO2] at more mature stages. The concurrent de-cline of both Vcmax and Jmax was commonly ob-served for various C3 species exposed to elevated[CO2], but the time-bound decline was more pro-nounced in grass species as compared to legumesand trees (Ainsworth and Rogers 2007). Furtherassessments of species-specific responses—andeventually intraspecific distinctions—are pivotalfor projections of future crop productivity underdifferent [CO2]. In spite of different downregula-tion patterns, FACE experiments conducted withthe three major C3 crops, rice, wheat, and soy-bean, showed similar yield increments (around15%). This is, however, smaller than the incre-ments of other C3 plants that triggers even moreconcern for future food supply given the sig-nificance of these three crops. Plant traits thataccelerate the effects of elevated [CO2] on grainyield need to be identified to tap the full benefitsof increasing [CO2].

Reduction in stomatal conductance is anotherdirect effect of elevated [CO2] and is commonlyobserved across different crops. According to ameta-analysis of published data by Ainsworthand Rogers (2007), the average decrease in stom-atal conductance by the FACE treatment was21%. Interestingly, there was no significant in-terspecific difference between C3 and C4 plantspecies. The response of rice is close to themean response shown in the above meta-analysisreport (Yoshimoto et al. 2005; Shimono et al.2010). In addition to [CO2], light and relativehumidity are also influencing stomatal conduc-tance. The response mechanisms to environ-mental changes are complex, but the Ball-Berrystomatal conductance model, a simple empiri-cal model, could account for the large portion ofchanges in conductance (Shimono et al. 2010).However, the assessment of CO2 effects is stillmarred by methodological inconsistencies be-tween FACE studies on one side and chambermeasurements on the other side. Derived from acomparative analysis of chamber and FACE stud-ies on rice, Ainsworth (2008) concluded that theenhancement of light-saturated assimilation dueto elevated [CO2] in the open-top chambers couldgo even beyond 50% and was about three times as




high as in FACE experiments. Different authorshave tried to untangle this apparent discrepancy.As initial studies pointed toward different pat-terns of downregulation of photosynthetic rates,two FACE experiments conducted in Japan andChina (Seneweera et al. 2002; Chen et al. 2005)indicated that the downregulation of photosyn-thetic rates is independent from the experimentalsetup. An important indirect consequence of thedecrease in stomatal conductance is the reduc-tion in water use. Yoshimoto et al. (2005) stud-ied energy balance of the Shizukuishi rice varietyand found that transpiration of the rice canopydecreased by 8% and water-use efficiency in-creased by 19% under FACE as compared tothe ambient [CO2] conditions. The decrease instomatal conductance, however, implies a reduc-tion of transpirational cooling, which increasesthe canopy temperature and may generate heatstress (Yoshimoto et al. 2005).

High nighttime temperature

Current meteorological observations haveclearly shown that daily minimum tempera-tures are increasing more rapidly than dailymaximum temperatures reflecting distinct evolu-tion for growth rates for nighttime temperatures(NTT) and daytime temperatures (DTT) (Kuklaand Karl 1993; Easterling et al. 1997; Peng et al.2004). A further widening in daily temperatureamplitudes is foreseen, which will have pro-found implications on crop performance. Riceyields of a long-term experiment (1992–2003)at IRRI were strongly and negatively correlatedwith NTT, whereas no correlation was observedwith DTT (Peng et al. 2004). In addition, undercontrolled environments with constant day tem-perature of 33◦C, increasing night temperaturesfrom 25◦C to 29◦C and from 25◦C to 33◦C re-duced grain yield by 34% and 95%, respectively(Ziska and Manalo 1996), and grain dry weightof more than 2 g/plant from 14◦C to 23◦C (Prasadet al. 2008; Fig. 12.1a). Similar conclusions onNTT versus DTT effects were reported from amodeling exercise using historical wheat yields

from Yaqui Valley in Mexico (Lobell and Ortiz-Monasterio 2007). At the crop level, yield de-cline by 0.4 t/ha is predicted with an increase of1◦C in daily average temperature, from 22◦C to23◦C (Seshu and Cady 1984), and by 10% withan increase of 1◦C in minimum average tempera-ture (Peng et al. 2004) (Fig. 12.1b), whereas theeffect of maximum temperature on crop yieldwas insignificant. An increasing number of stud-ies were conducted lately on the response of riceand other crops to higher nighttime temperatures(HNT) at different stages:

� Vegetative stage, i.e., germination to pani-cle initiation (Mohammed and Tarpley 2009a;Kanno et al. 2009; Cheng et al. 2009)

� Reproductive stage, i.e., panicle initiation toflowering (Cheng et al. 2009)

� Ripening stage, i.e., flowering to maturity in-cluding grain quality (Cooper et al. 2006,2008).

Hence, this section aims at reviewing thephysiological responses of rice to HNT and thepossible adaptation measures at different stagesof the crop growth cycle.

At the early developmental stage in cereals,HNT resulted in (1) enhanced leaf emergencerates (Tsunoda 1964; Tamaki et al. 2002; Mc-Master 2005) and (2) higher leaf elongation (Cut-ler et al. 1980; Lafarge et al. 1998; Parent et al.2009), with no effect on the leaf and root dryweights (Cheng et al. 2009). In a hydroponicexperiment encompassing a gradient of differ-ent NTT ranging from 17◦C to 27◦C, greatertotal leaf area and tiller number were reportedwith the growth analysis, indicating an increasein leaf area ratio, leaf weight ratio, and specificleaf area (Kanno et al. 2009). Overall, in plantsexposed to HNT of 27◦C, these authors obtainedhigher plant biomass and attributed it to thehigher relative growth rate caused by an increasein leaf area ratio between 21 and 42 days aftergermination. Contrastingly, at 32◦C nighttimetemperature, Mohammed and Tarpley (2009a,2009b) observed no effect on plant height,




0

2

4

6

8

11

(a)

14 17 20 23

Nighttime temperature

Gra

in d

ry w

eigh

t (g/

plan

t)

10.0

9.5

9.0

8.5

Gra

in y

ield

(to

ns h

a−1 )

8.0

7.5

7.0

6.522.0

(b)

22.5 23.0

Minimum temperature (°C)

23.5 24.0

Fig. 12.1. (a) Impact of nighttime temperature on grain dryweight in wheat Y = −0.25x + 7.96, r2 = 0.94, P < 0.0001,n = 20. (Redrawn with permission from Prasad et al. 2008.)(b) Relationship between grain yield and growing seasonmean minimum temperature, with yield data obtained fromirrigated field experiments 1992–2003 at IRRI during dry sea-son Y = −423.6 + 39.2x − 0.89x2, r2 = 0.77, P < 0.01,n = 11 with each data point representing the yield/year.(Redrawn with permission from Peng et al. 2004.)

stem length, tiller number, and panicle numberper plant.

The efficiency of plants to use photosynthateswas also affected under HNT. Lower starchand sucrose accumulation in leaf blades andleaf sheaths were observed (Kanno et al. 2009),which might be due to the preferential use of car-

bohydrates for plant growth. Skinner and Nelson(1995) reported that the meristematic cell zoneconstitutes a major sink for carbohydrates,with an increase in leaf cell production duringthe night in tomato (Lycopersicun esculentum;Hussey 1965). Considering that metabolic activ-ity was higher with plants growing under HNTthan under low night temperature, carbohydratedemand from growing zone of elongating organswas also higher (Kanno et al. 2009). Further-more, analysis of gas exchange indicated that thegross CO2 uptake per unit leaf area was also en-hanced under HNT, suggesting increase in photo-synthetic capacity and leaf area, with both beingco-determinants of the overall biomass accumu-lation under HNT. The effects on photosynthesisare, however, still unclear. While HNT (32◦C)was reported to have no immediate effect onleaf photosynthetic rates of rice (Mohammed andTarpley 2009a), it may cause damage to photo-system II (Havaux and Tardy 1996) and/or causeoxidative damage to membranes (Larkindale andKnight 2002). In wheat, leaf photosynthetic ratesand chlorophyll content were strongly reducedunder NTT higher than 20◦C, with an increasein the O/P ratio of chlorophyll indicating greaterdamage to thylakoid membranes (Prasad et al.2008). Previous studies reported premature lossof chlorophyll (Reynolds et al. 1994), which waslinked to lower net photosynthesis (Pn) underhigh temperatures (Guo et al. 2006). Contrast-ingly, Turnbull et al. (2002) stated that Pn ofthe succeeding daytime can be increased underHNT, whereas Mohammed and Tarpley (2009a)found no such relationship. In addition, the per-centage of reduction in yield under HNT wasmuch higher than the percentage of increase inrespiration rates, indicating that crop response totemperature is a complex system that impliesintegrating several plant processes apart fromrespiration (Mohammed and Tarpley 2009a).Similarly, the rate of maintenance respiration in-creased with increasing night temperature, butthe reported yield reductions in maize, wheat,and soybean could not be explained solely bychanges in respiration (Peters et al. 1971). Hence,




further detailed studies are essential to get a bet-ter understanding of these processes, and currentcrop growth models should account for differen-tial effects of maximum and minimum tempera-ture on respiration, photosynthesis, phenologicaldevelopment, sink regulation, and morphologi-cal traits to simulate accurately crop responseunder climate change scenarios.

Earlier panicle emergence by two days wasnoted in rice under HNT by Mohammed andTarpley (2009). Similarly, in wheat, duration toanthesis, to seed set, and to physiological matu-rity was reduced by 1, 2, and 4 days, respectively,with an increase in night temperature from 14◦Cto 20◦C, and by 2, 4, and 10 days, respectively,with an increase of the night temperature to 23◦C(Prasad et al. 2008). Percent pollen germinationwas reduced under HNT because of the reduc-tion of the number of reproductive sinks, ap-parently leading to an increase in biomass par-titioning to vegetative structures (Kanno et al.2009). A yield decline of 90% was observed un-der HNT of 32◦C mainly due to detrimental ef-fects on pollen germination and spikelet fertility,but not on photosynthesis (Mohammed and Tarp-ley 2009a, 2009b). Lower panicle dry weight andfertility rate were reported under HNT of 32◦C,while no difference in the number of spikeletsper panicle was observed (Cheng et al. 2009).

The duration of grain filling in wheat wasreduced by 3 and 7 days when night tempera-ture increased from 14◦C to 20◦C and to 23◦C,respectively, but no effect was observed on therate of grain filling (Prasad et al. 2008). This re-sulted in smaller grain size as grain-filling ratedid not compensate for loss of duration (Tashiroand Wardlaw 1991). In rice, grain growth rateat early or middle stage of grain filling andcell size midway between the central point andsurface of the endosperm were reduced un-der HNT (22◦C daytime/34◦C nighttime) com-pared to high daytime temperature (HDT, 34◦Cdaytime/22◦C nighttime) resulted in the reduc-tion of the final grain weight (Morita et al. 2005).

Changes in amylopectin content indicatedthat head rice yield is related to starch-filling en-

zymes, starch structure, and sink strength of thespikelet (Counce et al. 2005). Similarly, roughrice 200 spikelets dry weight and grain lengthwere not affected under HNT, but brown ricegrain width was reduced (Cooper et al. 2008).The total protein content and brown rice lipidcontent at maturity did not vary significantlyfor long-grain and medium-grain cultivars, butthe lipid content significantly increased in longgrain hybrids, namely XL8 and XP710. Usingsix different rice cultivars exposed to night tem-peratures of 22◦C, 26◦C, and 30◦C throughoutgrain development, two cultivars with constantrice yields, Cypress and Bengal, were indiffer-ent to HNT (Cooper et al. 2008). Moreover, nosignificant difference in the number of chalkygrains at any of the night temperatures was ob-served with Cypress (Cooper et al. 2008), indi-cating the presence of genetic diversity in ricegermplasm capable of withstanding HNT withsustained grain filling and quality, which couldbe further exploited in future breeding programs.

The vegetative stage generally benefits fromincreasing HNT, while the reproductive and earlygrain-filling stages are adversely affected. How-ever, the current knowledge on crop responseto HNT effects is still premature as comparedto HDT effects. At this point, the most plau-sible hypothesis for explaining the HNT effectis the loss of carbohydrates through respiration(De Costa et al. 2007) and its increase with cropstage, which is now addressed in studies to in-vestigate the impact mechanism for yield lossesunder high night temperature (Laza et al., per-sonal communication).

Interaction of CO2 concentrationand temperature

While doubling [CO2] with a concomitant tem-perature rise of more than 2◦C will significantlyincrease rice yield in cool temperate areas, itwill drastically reduce the yield in warm tem-perate areas and for dry-season rice in the trop-ics (Horie et al. 2000). Elevated [CO2] levelsmay further aggravate this problem because of




increased stomatal closure and reduced transpi-rational cooling due to high photosynthates feed-back on photosynthesis. In open-top chamber ex-periments at IRRI, the positive effect of elevated[CO2] on yield was overcome by the increase indaily temperature (Ziska et al. 1997): in the wetseason, yield in open-top chambers increased by0.9 Mg/ha under elevated [CO2] (+ 300 ppm)compared to that under control conditions, butdecreased by 0.7 Mg/ha if the associated temper-ature was higher than the ambient temperature by4◦C. This feature was commonly observed in en-vironments where temperature at time of anthesisis already approaching the critical threshold foranthesis, 35◦C, and where spikelet sterility is anissue (Lin et al. 1997; Jagadish et al. 2008). Ele-vated [CO2] even increased spikelet susceptibil-ity to high temperature damage by decreasing thecritical threshold temperature (Kim et al. 1996b),with the reduction in sink strength due to spikeletsterility further reducing the positive effect of el-evated [CO2] (Matsui et al. 1997). In contrast,no interaction on spikelet sterility was reportedbetween high night temperature and [CO2]. Theoverall issue of spikelet sterility under globalwarming addressing processes at microsporoge-nesis and anthesis time and highly dependenton local temperature (Matsui et al. 2005) hasbeen extensively developed in a previous review(Wassmann et al. 2009a) and will not be furtherdiscussed here.

The combination of elevated [CO2] with highnight temperature of 32◦C triggered the reduc-tion in panicle dry weight while it increased un-der elevated [CO2] alone. In contrast, shoot andstem biomass increased under elevated [CO2]and HNT (Cheng et al. 2009). The principaleffect of elevated [CO2] was higher grain dryweight, whereas the principal effect of HNTwas the reduction of filled grain number. Over-all, rice yield in controlled-environment cham-bers increased with elevated [CO2] but was re-duced with interaction between elevated [CO2]and HNT (Cheng et al. 2009).

The combination of elevated [CO2] with HDTlower than 31.5◦C triggered a cooperative en-

hancement of carbon assimilation observed attillering stage (Lin et al. 1997). The photo-synthetic rate was higher under elevated [CO2]for two temperature regimes (day/night temper-atures of 31◦C/24 and 35◦C/28◦C); however, itwas reduced with high temperatures irrespectiveof [CO2] levels (Sujatha et al. 2008). Activityof sucrose-P synthase and accumulation of solu-ble sugars and starch were also enhanced underboth temperature regimes (Sujatha et al. 2008).Radiation-use efficiency was also higher underelevated [CO2] and high thermal conditions, con-sidering an average temperature of 32◦C be-tween 10 am and 4 pm in open-top chambers(De Costa et al. 2006). However, under highertemperatures, because of detrimental effect oftemperature above the optimum value, whichhas been determined around 30◦C for rice (Yinet al. 1996), growth processes are affected, sinkstrength is reduced, and this may contribute to thedownregulation of photosynthesis. At later stage,the stimulation of the photosynthetic rate underelevated [CO2] was reduced under high temper-ature with the reduction of Rubisco activity (Linet al. 1997). In fact, under high temperature andelevated [CO2], the activation state of Rubiscoin leaves is reduced since photosynthesis wasconstrained by the activity of Rubisco activase(Crafts-Brandner and Salvucci 2000). Rubiscoappears as the major limitation to CO2 fixation,under elevated [CO2], high temperature, andoptimal light (Jensen 2000).

Sink regulation appears as a key componentof studies on the interactive effects of elevated[CO2] and high temperature conditions on plantperformance, particularly during the reproduc-tive and grain-filling stages when high tempera-ture has much more negative impact than at earlydevelopmental stage. Under elevated [CO2], theplant capacity to adjust to growing conditionsand to develop a greater sink (number of spikeletsper unit area) contributed to greater yield (DeCosta et al. 2007): in particular, under these con-ditions, an increase in allocation to root biomass(Ziska et al. 1996) and to tiller production (Bakeret al. 1990), but a decrease in leaf area per tiller




(Kim et al. 1996a) and a minor effect on leafarea development (Nakagawa et al. 1993; Ziskaet al. 1997) have been reported. In contrast, underhigh temperature, a negative effect on biomassaccumulation has been highlighted (Ziska andManalo 1996). Ito et al. (2009) reported, un-der daytime temperature of 38◦C, a reductionin starch synthesis during grain filling and an ac-cumulation of sucrose in plant vegetative organs,probably due to suboptimal sink regulation. Thismay be the reason for altered grain quality withreduced amylose content at high temperature(Tanaka et al. 2009). These effects should be clar-ified by carefully assessing temperature responsecurves of growth and physiological processes,their relevance, and their genetic variability. Inthis way, Parent et al. (2010) reported that growthand developmental processes do not express thesame response curve to temperature as carbonmetabolism for three different species in a rangeof temperature conditions. They introduced theconcept of temperature-compensated rates of de-velopmental processes and reported stable rateswhen these rates were calculated per unit equiv-alent time at 20◦C. The main activities in futureresearch addressing interaction between elevated[CO2] and high temperature should deal with therole of respiration and of internal sink formationand strength in the regulation of carbohydratespartitioning: association of these processes withnitrogen and CO2 uptake through root and stom-atal activities in response to sink strength shouldbe addressed. In the tropics, considering the ex-pected detrimental effect of increasing temper-ature despite elevated [CO2], it will be crucialto develop cultivars with improved sink regula-tion, as it has been emphasized by Bueno et al.(2010) also for high yield targets in comparisonto temperate and subtropical environments.

The combination of elevated [CO2] with otherfactors like soil nitrogen availability, climatic de-mand, and ozone concentration needs also to beconsidered. (1) The response of rice to [CO2] hasbeen reported as nitrogen dependent (Ziska et al.1996; Kim et al. 2001), with the canopy photo-synthesis increasing per unit of N content (Sakai

et al. 2006). (2) Evaporative demand has beendecreasing over recent decades (Peterson et al.1995; Roderick and Farquhar 2002) and watervapor pressure is expected to increase in paral-lel with global warming. This will even reduceplant cooling ability and increase spikelet tem-perature, which could become detrimental underhigh temperature conditions. (3) A reduction inyield of 14% was observed under 62 ppb O3

(Ainsworth 2008). Many yield components, likephotosynthesis, biomass, leaf area index, grainnumber, and grain dry weight, were reduced un-der elevated [O3] and this would also probablydownsize the positive effects registered underelevated [CO2].

Opportunities for geneticimprovement for tolerance

Most of the current research related to quanti-tative trait locus (QTL) mapping and candidategenes discovery for abiotic stress tolerance inrice concern drought, salinity, and submergence(Cooper et al. 1999; Xu et al. 2000; Fukudaet al. 2004; Fukao et al. 2006; Xu et al. 2006;Herve and Serraj 2009). In the case of the con-trol of heat tolerance, several genes are known tobe involved (Mackill 1981; Maestri et al. 2002;Zhu et al. 2005). Some studies aiming at map-ping the genetic control of heat tolerance havestarted recently, but they target the spikelet steril-ity issue only by focusing on the processes ofanther dehiscence, pollination, pollen germina-tion, and/or pollen tube growth: genotypic dif-ferences in anther characteristics between sus-ceptible and tolerant rice genotypes exist (Wass-mann et al. 2009a), and slower reduction at 39◦Cwas observed in pollen activity, pollen germi-nation, and rate of floret fertility with a toler-ant genotype (Tang et al. 2008). In search fordonors for heat tolerance, no clear difference wasreported between indica and japonica (Prasadet al. (2006), but an aus variety N22 (Prasadet al. 2006; Jagadish et al. 2008) and local Ira-nian landraces (Moradi and Gilani 2007) have




consistently shown tolerance to high tempera-ture at anthesis under diverse experimental con-ditions. This cultivar N22 and other promisinggenotypes are currently used in breeding pro-grams at IRRI as donors for tolerance to heat-induced sterility (Redona et al. 2007); mappingpopulations are being established for QTL iden-tification; shuttle breeding with F4 lines is con-ducted in high temperature environments (Pak-istan, Iran, India, and Bangladesh); and promis-ing entries are dispatched in 15 countries forscreening (INGER network, Edilberto Redona,personal communication). The characterizationof the genetic polymorphism for heat toleranceis underway through a proteomic approach foridentifying candidate genes and the develop-ment of gene-based markers for marker assistedbreeding.

Research for heat tolerance also concernsgrain quality. Biochemical analyses of starchshowed that the high temperature-ripened grainscontained decreased levels of amylose and longchain-enriched amylopectin, which might be at-tributed to the repressed expression of granule-bound starch synthase I and branching enzymes,especially BEIIb (Yamakawa et al. 2007). Thisresulted in the occurrence of grains with vari-ous degrees of chalky appearance and suggestedthat alterations of amylopectin structure mightbe involved in grain chalkiness (Yamakawa et al.2007). Mapping populations for QTL identifi-cation for tolerance to heat-induced chalkinessis underway using single sequence repeat (SSR)markers (Melissa Fitzgerald, personal communi-cation).

Opportunities to improve germplasm toler-ance of assimilation and growth processes to ele-vated [CO2], high night temperature, and interac-tions between elevated [CO2] and HNT, the focusof this paper, can be cited from the literature, al-though no current research is directly addressingthis issue. These opportunities include researchfor improving (1) yield potential, including thedevelopment of C4 rice, (2) tolerance to drought,considering it may be in fact the expression of atolerance to heat with the reduction of the plant

cooling ability through stomatal closure, and(3) tolerance to biotic stresses by introgressinggenes from wild species.

1. Some QTL mapping and gene discovery ad-dressed the control of expression of traitsacting on yield potential, like phenology,photosynthetic rate, crop architecture, andsink regulation. As examples, under favorableconditions, partial genetic control of headingdate by the Ghd7 QTL (Xue et al. 2008),of sink regulation by the rg5 QTL (Ishimaruet al. 2005), of tillering dynamics by theMOC1 gene (Li et al. 2003) and the OsNAC2gene (Mao et al. 2007), and of characteristicsof flag leaf by delimited regions of chromo-somes 3 and 4 (Yue et al. 2006) have beenreported. Incidentally, these traits are also in-volved in the crop tolerance to changing cli-mates as already shown in this chapter and byDe Costa et al. (2007).

2. The introduction of a C4-like pathway intoC3 rice plants offers the potential to enhancephotosynthetic rates and reduce photorespi-ratory losses. Theoretical justification for thisapproach is well summarized by Mitchelland Sheehy (2007). It shows (1) increasedradiation-use efficiency due to reduced ratesof photorespiration, (2) increased water-useefficiency due to reduced requirement forhigh stomatal conductance, and (3) improvednitrogen-use efficiency due to reduced invest-ment in photosynthetic proteins. All of thesecomponents could enhance C3 crop yields byup to 50%. Some studies have shown, how-ever, that considerable regulatory feedbackmechanisms exist in C4 plants that down-regulate photosynthetic gene expression tomatch sink demand (Sheen 1999). Indeed,yield potential of such plants is not realizedat field level (Sinclair et al. 2004), which hasalso been observed in FACE experiments.A potential benefit of C4 like photosynthe-sis in C3 rice plants is the increased toler-ance to high temperature conditions such asin the tropics. At current [CO2] and [O2], the




oxygenation reaction of Rubisco representsabout 30% of its activity, requiring consid-erable expenditure of energy to recycle car-bon via the photorespiration pathway, whichcan reduce photosynthesis by as much as40% (Sharkey 1988). This is further compli-cated by the sensitivity of photorespiration totemperature that is considerably increased astemperature rises due to increased affinity ofRubisco for O2 relative to CO2 and increasedsolubility of O2 in water at higher temper-atures. The C4 plants are able, however, toreduce the sensitivity of photosynthesis totemperature by minimizing photorespiratorylosses: they have evolved a CO2 concentrationmechanism that confers significant advan-tages especially in environments with highlight intensity and high temperatures. In ad-dition, the higher photosynthetic rates of theC4 plants can better supply the higher demandfrom respiration and sinks due to high nighttemperature. Also, higher tolerance to hightemperature can also widen the geographicalgrowth range of the rice crop. In drought-prone environments, increased water-use ef-ficiency when water supply is sufficient shallincrease the water availability of C4 plantsduring grain filling.

3. Plants better tolerant to water scarcity be-cause of better root hair proliferation andelongation, and cell wall permeability, shallalso have increased tolerance to high tem-perature and high water demand because ofenhanced soil water accessibility. Such traitsare related to candidate genes identified inthe QTL region of DTY12.1 (Narciso et al.2010) on chromosome 12 in the Vandana/WayRarem population and explained about 51%of the genetic variance for yield under drought(Bernier et al. 2007). To date, this QTL ex-hibits the largest effect for grain yield un-der drought in several genetic backgroundsincluding IR64 and showed large and con-sistent effect in a wide range of moderate tosevere drought stress situations (Bernier et al.2009).

4. Broadening gene pool of rice through intro-gression of genes from diverse sources shallalso contribute to overcome global climatechange, especially higher temperatures. Thewild species of Oryza, to which cultivatedrice belongs to, and one of the cultivatedAfrican rice species (O. glaberrima), are areservoir of useful genes for tolerance toabiotic stresses. With the advances in tissueculture techniques, molecular markers, andgenomics, the scope for utilization of wildspecies in developing improved germplasmand rice varieties less vulnerable to high tem-perature seems promising (Darshan Brar, per-sonal communication).

Conclusion and outlook

Some main issues of rice crop performance re-lated to elevated [CO2], HNT, and interactionbetween elevated [CO2] and high temperatureare still unsolved:

� How the overall sink regulation (tillering dy-namics, internode and panicle dimensioningand growth, priority between organs/sinks, or-gan senescence), carbohydrates remobiliza-tion, and respiration are modified

� Whether the reduced stomata conductance atmid-afternoon is due to high climatic demand,poor soil exploration, high photorespiration,or assimilate overload (poor sink activity)

� Whether the nitrogen uptake is modified atlate stages in relation to root activities andsenescence.

Such studies and assessments require (1)proper experimental setups where the respectiveeffects of environmental components can be an-alyzed and (2) integration of data into appro-priate crop models to address the response ofthe genotypic variability to the interaction be-tween components. So far, many studies havebeen conducted in growth chambers where ra-diation, temperature, humidity, and [CO2] canbe monitored independently (Allen et al. 1995;




Crafts-Brandner and Salvucci 2000; Sujathaet al. 2008; Cheng et al. 2009). To be closerto field conditions, other studies have been con-ducted in open-top chambers or temperature gra-dient chambers with natural radiation (Ziskaet al. 1997; Nakagawa and Horie 2000; De Costaet al. 2006) where plants can be grown in soiltanks or small field areas but where the con-trol of growing conditions is less accurate. Thevalidity of the conclusions from such studieshas been questioned recently (Long et al. 2006),stating that yield increase under elevated [CO2]was significantly higher in enclosures than inFACE systems and that conditions inside enclo-sures did not reflect the real environment. Thepotential of the FACE rings is, however, lim-ited since their actual size (octagonal plot ofabout 20 m of diameter) enables studies withcontrasted genotypes (Kim et al. 2001; Sene-weera et al. 2002; Hasegawa et al. 2007; Shi-mono et al. 2010) but should be significantly in-creased to characterize the genotype variabilityand conduct phenotyping activities. Larger ringsshould then be designed, established in tropicalconditions where global warming is a strong is-sue (Ainsworth et al. 2008), and equipped withsmaller rings of infra-red heaters (Kimball et al.2008) or heating cables placed inside the water(as in the case of the FACE system in Japan)to modify the temperature locally and evalu-ate in situ the interaction between temperatureand [CO2]. This debate, however, needs to dis-criminate studies with respect to the type, size,and internal conditions of enclosures and thetime when each study was conducted (Ziskaand Bunce 2007; Tubiello et al. 2007). As anexample, ambient [CO2] is actually 380 ppm,appreciably higher than 320 ppm, which wasthe rate 15–20 years ago. Also, most stud-ies inside enclosures considered double [CO2](700 ppm) as a treatment while [CO2] inside fer-tilized FACE rings is generally 550 ppm only,i.e., 200 ppm higher than that of the ambient(Ziska and Bunce 2007). In addition, tissue tem-perature, which is the key thermal parameterto consider in order to assessing the effect on

growth processes (Lafarge et al. 1998), is notlinearly related to air temperature, but is alsodependent on the overall climatic and soil condi-tions, and the characteristics of the genotype un-der study. It is then critical to measure tissue tem-perature, and, in case of controlled conditions, toconsider air temperature measured at relevant lo-cations. Overall, the best opportunity to addressthe interaction between high temperature and el-evated [CO2] is probably to combine differentexperimental setups associated with a system-atic and rigorous characterization of the growingconditions including microclimate.

Addressing the interactions between compo-nents of the environment, namely [CO2] and tem-perature, but also humidity and soil nitrogen con-tent, requires an integrative modeling approachwhere the effects of component traits of inter-est governing the phenotypic plasticity of yieldformation are accounted separately and for con-trasted conditions. Stressing events may occurat various times, in various extents, and simul-taneously during crop growth. It is therefore es-sential that the morpho-physiological responseof plants/crops to such combined stresses is in-tegrated in a dynamic way, enabling capture andevaluation of the relevant genotypic and envi-ronmental control of yield formation processes.The EcoMeristem model, a whole plant modelsimulating environmental impact on genotype-dependent regulation of morphogenesis (with re-gards to competition for carbohydrates and wa-ter availability within the plant) is the type ofmodel adapted to this purpose (Luquet et al.2006, 2008). In the near future, this model shallbe connected with (1) a GECROS-type modelthat accounts for the response of stomatal con-ductance and photosynthesis to abiotic condi-tions potentially at the organ level (Yin and vanLaar 2005), (2) a physical model able to simu-late organ temperature (meristem, panicle) withrespect to local energy balance (Yoshimoto et al.2005), and (3) a 3D modeling approach that pro-vides the framework to simulate the local energybalance (Pradal et al. 2008). Such technical de-velopment will allow simulating the integration




of potential changes triggered by genetic en-hancement. Also, it should highlight how thestructural (plant architecture regulated by plantgrowth and affecting the local environment ofthe plant)–functional (metabolism and morpho-genesis response to the environment) interactioncan govern organ microclimate conditions andinfluence final plant performance.

Acknowledgments

The authors want to thank Drs Delphine Luquet,Darshan Brar, and Ajay Kohli for their usefulcontributions to the manuscript.

References

Ainsworth EA (2008) Rice production in a changing climate:A meta-analysis of responses to elevated carbon dioxideand elevated ozone concentration. Global Change Biol-ogy 14: 1642–1650.

Ainsworth EA, Rogers A (2007) The response of photosyn-thesis and stomatal conductance to rising [CO2]: Mech-anism and environmental interactions. Plant, Cell andEnvironment 30: 258–270.

Ainsworth EA, Beier C, Calfapietra C, Ceulemans R,Durand-Tardif M, Farquhar GD, Godbold DL, HendreyGR, Hickler T, Kaduk J, Karnosky DF, Kimball BA, Ko-rner C, Koornneef M, Lafarge T, Leakey ADB, LewinKF, Long SP, Manderscheid R, McNeil DL, Mies TA,Miglietta F, Morgan JA, Nagy J, Norby RJ, Norton RM,Percy KE, Rogers A, Soussana JF, Stitt M, Weigel HJ,White JW (2008) Next generation of elevated [CO2]experiments with crops: A critical investment for feed-ing the future world. Plant, Cell and Environment 31:1317–1324.

Allen LH Jr, Baker JT, Albrecht SL, Boote KJ, Pan D,Vu JVC (1995) Carbon dioxide and temperature effecton rice. In: S Peng, KT Ingram, H-U Neue, and LH Ziska(eds) Climate Change and Rice, pp. 258–277. Springer-Verlag, Berlin.

Baker JT, Allen LH Jr, Boote KJ (1990) Growth and yield re-sponses of rice to carbon dioxide concentration. Journalof Agricultural Science of Cambridge 115: 313–320.

Battisti DS, Naylor RL (2009) Historical warnings of fu-ture food insecurity with unprecedented seasonal heat.Science 323: 240–244.

Bernier J, Kumar A, Venuprasad R, Spaner D, Atlin G (2007)A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice. Crop Science 47:507–516.

Bernier J, Kumar A, Venuprasad R, Spaner D, Verulkar S,Mandal NP, Sinha PK, Peeraju P, Dongre PR, MahtoRN, Atlin GN (2009) Characterization of the effect of a

QTL for drought resistance in rice, qtl12.1, over a rangeof environments in the Philippines and eastern India.Euphytica 166: 207–217.

Bouman BAM, Humphreys E, Tuong TP, Barker R (2007)Rice and water. Advances in Agronomy 92: 187–237.

Bueno C, Lafarge T (2009) Higher performance of rice hy-brids than of elite inbreds in the tropics: 1. Hybrids ac-cumulate more biomass during each phenological phase.Field Crops Research 112: 229–237.

Bueno C, Pasuquin E, Tubana B, Lafarge T (2010) Improv-ing sink regulation, and searching for promising traitsassociated with hybrids, as a key avenue to increase yieldpotential of the rice crop in the tropics. Field Crops Re-search 118: 199–207.

Carriger S, Vallee D (2007) More crop per drop. Rice Today6: 10–13.

Chen GY, Yong ZH, Liao Y, Zhang DY, Chen Y, Zhang HB,Chen J, Zhu JG, Xu DQ (2005) Photosynthetic acclima-tion in rice leaves to free-air CO2 enrichment related toboth ribulose-1, 5-bisphosphate carboxylation limitationand ribulose-1, 5-bisphosphate regeneration limitation.Plant Cell Physiology 46: 1036–1045.

Cheng W, Sakai H, Yagi K, Hasegawa T (2009) Interac-tions of elevated [CO2] and night temperature on ricegrowth and yield. Agricultural and Forest Meteorology149: 51–58.

Cooper M, Fukai S, Wade LJ (1999) How can breeding con-tribute to more productive and sustainable rainfed low-land rice systems? Field Crops Research 64: 199–209.

Cooper NTW, Siebenmorgen TJ, Counce PA, Meullenet JFC(2006) Explaining rice milling quality variation usinghistorical weather data analysis. Cereal Chemistry 83:447–450.

Cooper NTW, Siebenmorgen TJ, Counce A (2008) Effectsof nighttime temperature during kernel development onrice physicochemical properties. Cereal Chemistry 85:276–282.

Counce PA, Bryant RJ, Bergman CJ, Bautista RC, Wang YA,Siebenmorgen TJ, Moldenhauer KAK, Meullenet JFC(2005) Rice milling quality, grain dimensions, and starchbranching as affected by high nighttime temperatures.Cereal Chemistry 82: 645–648.

Crafts-Brandner SJ, Salvucci ME (2000) Rubisco acti-vase constrains the photosynthetic potential of leaves athigh temperature and CO2. Proceedings of the NationalAcademy of Sciences 97: 13430–13435.

Cutler JM, Steponkus PL, Wach MJ, Shahan KW (1980)Dynamic aspects and enhancement of leaf elongation inrice. Plant Physiology 66: 147–152.

De Costa WAJM, Weerakoon WMW, Chinthaka KGR,Herath HMLK, Abeywardena RMI (2007) Genotypicvariation in the response of rice (Oryza sativa L.) toincreased atmospheric carbon dioxide and its physiolog-ical basis. Journal of Agronomy and Crop Science 193:117–130.

De Costa WAJM, Weerakoon WMW, Herath HMLK, Ama-ratunga KSP, Abeywardena RMI (2006) Physiology of




yield determination of rice under elevated carbon diox-ide at high temperature in a sub-humid tropical climate.Field Crops Research 96: 336–347.

Dey MM, Upadhyaya HK (1996) Yield loss due to drought,cold and submergence in Asia. In: RE Evenson, RWHerdt, and M Hossain (eds) Rice Research in Asia:Progress and Priorities, pp. 291–303. CAB Internationaland IRRI, Wallingford, Oxon, UK.

Easterling DR, Horton B, Jones PD, Peterson TC, KarlTR, Parker DE, Salinger MJ, Razuvayev V, PlummerN, Jamason P, Folland CK (1997) Maximum and min-imum temperature trends for the globe. Science 277:364–367.

FAO (2008) FAO land and plant nutrition manage-ment service. Available from: http://www.fao.org/ag/agl/agll/spush. Accessed in 2011.

Fukao T, Xu KN, Ronald PC, Bailey-Serres J (2006) Avariable cluster of ethylene response factor-like genesregulates metabolic and developmental acclimation re-sponses to submergence in rice. The Plant Cell 18:2021–2034.

Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hi-rochika H, Tanaka Y (2004) Function, intracellular local-ization and the importance in salt tolerance of a vacuolarNa+/H +antiporter from rice. Plant Cell Physiology 45:146–159.

Guo YP, Zhou HF, Zhang LC (2006) Photosynthetic char-acteristics and productive mechanism against photo-oxidation during high temperature stress in two citrusspecies. Science Horticulture 108: 260–267.

Hasegawa T, Shimono H, Yang L, Kim HY, Kobayashi T,Sakai H, Yoshimoto M, Lieffering M, Ishiguro K, WangYL, Zhu JG, Kobayashi K, Okada M (2007) Responseof rice to increasing CO2 and temperature: Recent find-ings from large-scale free-air CO2 enrichment (FACE)experiments. In: PK Aggarwal, JK Lahda, RK Singh,C Dewakumar, and B Hardy (eds) Science, Technology,and Trade for Peace and Prosperity, pp. 439–447. Inter-national Rice Research Institute, Los Banos, Philippines.Proceedings of the 2nd International Rice Congress, Oc-tober 9–12, 2006, New Delhi, India, 782pp.

Havaux M, Tardy F (1996) Temperature-dependent adjust-ment of the thermal stability of photosystem 2 in vivo:Possible involvement of xanthophylls-cycle pigments.Planta 198: 324–333.

Herve P, Serraj R (2009) Gene technology and drought: Asimple solution for a complex trait? African Journal ofBiotechnology 8: 1740–1749.

Horie T, Baker JT, Nakagawa H (2000) Crop ecosystemresponse to climatic change: Rice. In: KR Reddy andHF Hodges (eds) Climate Change and Global CropProductivity, pp. 81–106. CAB Publishing International,Wallingford, Oxon, UK.

IPCC (Intergovernmental Panel on Climate Change) (2007)Summary for policy makers. In: Climate Change 2007.The Physical Science Basis. Cambridge University Press,Cambridge, UK, and New York, NY.

Ishimaru K, Kashiwagi T, Hirotsu N, Madoka Y (2005) Iden-tification and physiological analyses of a locus for riceyield potential across the genetic background. Journal ofExperimental Botany 56: 2745–2753.

Ito S, Hara T, Kawanami Y, Watanabe T, Thiraporn K,Ohtake N, Sueyoshi K, Mitsui T, Fukuyama T, Taka-hashi Y, Sato T, Sato A, Ohyama T (2009) Carbon andnitrogen transport during grain filling in rice under hightemperature conditions. Journal of Agronomy and CropScience 195: 368–376.

Jagadish SVK, Craufurd PQ, Wheeler TR (2008) Pheno-typing parents of mapping populations of rice for heattolerance during anthesis. Crop Science 48: 1140–1146.

Jensen RG (2000) Activation of Rubisco regulates photosyn-thesis at high temperature and CO2. Proceedings of theNational Academy of Sciences 97: 12937–12938.

Kanno K, Mae T, Makino A (2009) High night tempera-ture stimulates photosynthesis, biomass production andgrowth during the vegetative stage of rice plants. SoilScience and Plant Nutrition 55: 124–131.

Kim HY, Horie T, Nakagawa H, Wada K (1996a) Effectsof elevated CO2 concentration and high temperature ongrowth and yield of rice. I. The effect on development, drymatter production and some growth characters. JapaneseJournal of Crop Science 65: 634–643.

Kim HY, Horie T, Nakagawa H, Wada K (1996b) Effectsof elevated CO2 concentration and high temperature ongrowth and yield of rice. II. The effect on yield and itscomponent of Akihikari rice. Japanese Journal of CropScience 65: 644–651.

Kim HY, Lieffering M, Miura S, Kobayashi K, OkadaM (2001) Growth and nitrogen uptake of CO2 en-riched rice under field conditions. New Phytologist 150:223–229.

Kim HY, Lieffering M, Kobayashi K, Okada M, Miura S(2003) Seasonal changes in the effects of elevated CO2

on rice at three levels of nitrogen supply: A free-air CO2

enrichment (FACE) experiment. Global Change Biology9: 826–837.

Kimball BA, Kobayashi K, Bindi M (2002) Responses ofagricultural crops to free-air CO2 enrichment. Advancesin Agronomy 77: 293–368.

Kimball BA, Conley MM, Wang S, Lin X, Luo C, Mor-gan J, Smith D (2008) Infrared heater arrays for warm-ing ecosystem field plots. Global Change Biology 14:309–320.

Kukla G, Karl TR (1993) Nighttime warming and the green-house effect. Environmental Sciences Technology 27:1468–1474.

Lafarge T, Bueno C (2009) Higher crop performance of ricehybrids than of elite inbreds in the tropics: 2. Does sinkregulation, rather than sink size, play a major role? FieldCrops Research 114: 434–440.

Lafarge T, de Raıssac M, Tardieu F (1998). Elongation rate ofsorghum leaves has a common response to meristem tem-perature in diverse African and European environmentalconditions. Field Crops Research 58: 69–79.




Larkindale J, Knight MR (2002) Protection against heatstress-induced oxidative damage in Arabidopsis involvescalcium, abscisic acid, ethylene, and salicylic acid. PlantPhysiology 128: 682–695.

Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X,Liu X, Teng S, Hirishi F, Yuan M, Luo D, Han B, Li J(2003) Control of tillering in rice. Nature 422: 618–621.

Liu H, Yang L, Wang Y, Huang J (2008) Yield formationof CO2-enriched hybrid rice cultivar Shanyou 63 underfully open-air field conditions. Field Crops Research 108:93–100.

Lin W, Ziska LH, Namuco OS (1997) The interaction ofhigh temperature and elevated CO2 on photosyntheticacclimation of single leaves of rice in situ. PhysiologiaPlantarum 99: 178–184.

Lobell DB, Ortiz-Monasterio IJ (2007) Impact of day versusnight temperature on spring wheat yields: A compari-son of empirical and CERES model predictions in threelocations. Agronomy Journal 99: 469–477.

Long SP, Ainsworth EA, Leakey ADB (2006) Foodfor thought: Lower-than-expected crop yield stimu-lation with rising CO2 concentrations. Science 312:1918–1921.

Luquet D, Dingkuhn M, Clement-Vidal A (2008) Modelingdrought effects on rice with EcoMeristem: feedbacks ofwater and carbohydrate relations on phenotypic plastic-ity. In: Delphine Luquet (ed.) Whole Plant PhysiologyModeling Project, CIRAD, Montpellier. Proceedings ofthe Final Meeting, February 4–7, Johnston, IA.

Luquet D, Dingkuhn M, Kim HK, Tambour L, Clement-VidalA (2006) EcoMeristem, a model of morphogenesis andcompetition among sinks in rice. 1. Concept, validationand sensitivity analysis. Functional Plant Biology 33:309–323.

Mackill DJ (1981) Studies on the Mechanism and Genetics ofHigh Temperature Tolerance in Rice. PhD Dissertation,University of California Davis, CA.

Maestri E, Klueva N, Perrotta C, Gulli M, Nguyen HT,Marmiroli N (2002) Molecular genetics of heat toler-ance and heat shock proteins in cereals. Plant MolecularBiology 48: 667–681.

Mao C, Ding W, Wu Y, Yu J, He X, Shou H, Wu P(2007) Over-expression of a NAC-domain protein pro-motes shoot branching in rice. New Phytologist 176:288–298.

Matsui T, Kobayasi K, Kagata H, Horie T (2005) Correla-tion between viability of pollination and length of basaldehiscence of the theca in rice under a hot-and-humidcondition. Plant Production Science 8: 109–114.

Matsui T, Namuco OS, Ziska LH, Horie T (1997) Effectsof high temperature and CO2 concentration on spikeletsterility in indica rice. Field Crops Research 51: 213–219.

McMaster GS (2005) Phytomers, phyllochrons, phenologyand temperate cereal development. Journal of Agricul-tural Science 143: 137–150.

Mitchell PL, Sheehy JE (2007) Surveying the possible path-ways to C4 rice. In: JE Sheehy, PL Mitchell, and B Hardy

(eds) Charting New Pathways to C4 Rice. World Scien-tific Publishing, pp. 399–412. Proceedings of the Inter-national Workshop on Supercharging the Rice Engine,July 17–21, 2006, IRRI Headquaters, Los Banos, ThePhilippines, 422pp.

Mohammed AR, Tarpley L (2009a) Impact of high nighttimetemperature on respiration, membrane stability, antioxi-dant capacity and yield of rice plants. Crop Science 49:313–322.

Mohammed AR, Tarpley L (2009b) High nighttime tem-peratures affect rice productivity through altered pollengermination and spikelet fertility. Agricultural and ForestMeteorology 149: 999–1008.

Moradi F, Gilani A (2007) Impact of global warming andhigh temperature stress on Iranian rice cultivars: Anoverview. International Workshop on Cool Rice for aWarmer World, March 26–30, Huazhong AgriculturalUniversity, Wuhan, Hubei, China.

Morita S, Jun-Ichi Y, Jun-Ichi T (2005) Growth and en-dosperm cell size under high night temperatures in rice(Oryza sativa L.). Annals of Botany 95: 695–701.

Nakagawa H, Horie T (2000) Rice responses to elevatedCO2 and temperature. Global Environmental Research3: 101–113.

Nakagawa H, Horie T, Nakano J, Kim HY, Wada K,Kobayashi M (1993) Effect of elevated CO2 concen-tration and high temperature on growth and develop-ment of rice. Journal of Agricultural meteorology 48:799–802.

Narciso J, Oane RH, Popluechai S, Gowda VRP, EnriquezBA, Kumar A, Kohli A (2010) Cellulose synthase as amajor candidate gene in the large effect QTL for rice yieldunder drought stress. The 40th Crop Science Society ofthe Philippines Scientific Conference and Anniversary,March 15–20, Davao City, The Philippines.

Pandey S, Bhandari H, Hardy B (2007) Economic Costsof Drought and Rice Farmers Coping Mechanisms: ACross-country Comparative Analysis, 203pp. Interna-tional Rice Research Institute, Manila.

Parent B, Conejero G, Tardieu F (2009). Spatial and temporalanalysis of non-steady elongation of rice leaves. Plant,Cell and Environment 32: 1561–1572.

Parent B, Turc O, Gibon Y, Stitt M, Tardieu F (2010)Modelling temperature-compensated physiological rates,based on the coordination of responses to temperatureof developmental processes. Annals of Botany 61(8):2057–2069.

Parry ML, Rosenzweig C, Iglesias W, Livermore M, Fis-cher G (2004) Effects of climate change on globalfood production under SRES emissions and socio-economic scenarios. Global Environmental Change 14:53–67.

Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, ZhongX, Centeno GS, Khush GS, Cassmann KG (2004) Riceyields decline with higher night temperature from globalwarning. Proceedings of the National Academy of Sci-ences 101: 9971–9975.




Peters DB, Pendleton JW, Hageman RH, Brown CM (1971)Effect of night air temperature on grain yield of corn,wheat, and soybeans. Agronomy Journal 63: 809.

Peterson TC, Golubev VS, Groisman PY (1995) Evaporationloosing its strength. Nature 377: 687–688.

Pradal C, Dufour-Kowalski S, Boudon F, Fournier C, GodinC (2008) OpenAlea: A visual programming and compo-nent base software platform for plant modeling. Func-tional Plant Biology 35: 751–760.

Prasad PVV, Boote KJ, Allen LH, Sheehy JE, ThomasJMG (2006) Species, ecotype and cultivar differences inspikelet fertility and harvest index of rice in responseto high temperature stress. Field Crops Research 95:398–411.

Prasad PVV, Pisipati SR, Ristic Z, Bukovnik U, Fritz AK(2008) Impact of nighttime temperature on physiologyand growth of spring wheat. Crop Science 48: 2372–2380.

Redona ED, Laza MA, Manigbas NL (2007) Breeding ricefor adaptation and tolerance to high temperatures. Pro-ceedings of the International Workshop on Cool Rice fora Warmer World, March 26–30, Huazhong AgriculturalUniversity, Wuhan, Hubei, China.

Reynolds MP, Balota M, Delgado MIB, Amani I, FisherRA (1994) Physiological and morphological traits as-sociated with spring wheat yield under hot irrigatedconditions. Australian Journal of Plant Physiology 21:717–730.

Roderick ML, Farquhar GD (2002) The cause of decreasedpan evaporation over the last 50 years. Science 298:1410–1411.

Sakai H, Hasegawa T, Kobayashi K (2006) Enhancementof rice canopy carbon gain by elevated CO2 is sensitiveto growth stage and leaf nitrogen concentration. NewPhytologist 170: 321–332.

Seneweera SP, Conroy JP, Ishimaru K, Ghannoum O, OkadaM, Lieffering M, Han Yong K, Kobayashi K (2002)Changes in source-sink relations during developmentinfluence photosynthetic acclimation of rice to free-airCO2 enrichment (FACE). Functional Plant Biology 29:945–953.

Seshu DV, Cady FB (1984) Response of rice to solar radiationand temperature estimated from international yield trials.Crop Science 24: 649–654.

Sharkey TD (1988) Estimating the rate of photorespirationin leaves. Physiologia Plantarum 73: 147–152.

Sheen J (1999) C4 gene expression. Annual Review ofPlant Physiology and Plant Molecular Biology 50:187–217.

Shimono H, Okada M, Inoue M, Nakamura H, KobayashiK, Hasegawa T (2010) Diurnal and seasonal variationsin stomatal conductance of rice at elevated atmosphericCO2 under fully open-air conditions. Plant, Cell and En-vironment 33: 322–331.

Sinclair TR, Purcell LC, Sneller CH (2004) Crop transforma-tion and the challenge to increase yield potential. Trendsin Plant Science 9: 70–75.

Skinner RH, Nelson CJ (1995) Elongation of the grass leafand its relationship to the Phyllochron. Crop Science 35:4–10.

Sujatha KB, Uprety DC, Nageswara Rao D, Raghuveer RaoP, Dwivedi N (2008) Up-regulation of photosynthesis andsucrose-P synthase in rice under elevated carbon dioxideand temperature conditions. Plant Soil Environment 4:155–162.

Tamaki M, Kondo S, Itani T, Goto Y (2002) Temperatureresponses of leaf emergence and leaf growth in barley.Journal of Agricultural Science 138: 17–20.

Tanaka K, Onishi R, Miyazaki M, Ishibashi Y, YuasaT, Iwaya-Inoue M (2009) Changes of NMR relax-ation of rice grains, kernel quality and physicochemicalproperties in response to a high temperature after flower-ing in heat-tolerant and heat-sensitive rice cultivars. PlantProduction Science 12: 185–192.

Tang RS, Zheng JC, Jin ZQ, Zhang D, Huang H, Chen LG(2008) Possible correlation between high temperature-induced floret sterility and endogenous levels of IAA,GAs and ABA in rice (Oryza sativa L.). Plant GrowthRegulations 54: 37–43.

Tashiro T, Wardlaw I (1991) The effect of high temperatureon kernel dimensions and the type and occurrence ofkernel damage in rice. Australian Journal AgriculturalResearch 22: 485–496.

Tsunoda K (1964) Studies on the effect of water-temperatureon the growth and yield in rice plants. Bulletin NationalInstitute Agricultural Science Series W 11: 75–174.

Tubiello FN, Amthor JS, Boote KJ, Donatelli M, EasterlingW, Fischer G, Gifford RM, Howden M, Reilly J, Rosen-zweig C (2007) Crop response to elevated CO2 and worldfood supply. A comment on “Food for thought. . .” byLong et al., Science 312: 1918–1921, 2006. EuropeanJournal of Agronomy 26: 215–223.

Turnbull MH, Murthy R, Griffin KL (2002) The relativeimpacts of daytime and night-time warming on photo-synthetic capacity in Populus detoides. Plant Cell Envi-ronment 25: 1729–1737.

Wassmann R, Jagadish SVK, Heuer S, Ismail A, Redona E,Serraj R, Singh RK, Howell G, Pathak H, Sumfleth K(2009a) Climate change affecting rice production: Thephysiological and agronomic basis for possible adapta-tion strategies. Advances in Agronomy 101: 59–122.

Wassmann R, Jagadish SVK, Heuer S, Ismail A, RedonaE, Serraj R, Singh RK, Howell G, Pathak H, SumflethK (2009b) Regional vulnerability of rice production inAsia to climate change impacts and scope for adaptation.Advances in Agronomy 102: 91–133.

Wassmann R, Neue HU, Lantin RS (2000) Characterizationof methane emissions from rice fields in Asia. 1. Compar-ison among field sites in five countries. Nutrient CyclingAgroecosystems 58: 1–12.

Xu K, Xu X, Ronald PC, Mackill DJ (2000) A high-resolutionlinkage map of the vicinity of the rice submergence toler-ance locus Sub1. Molecular and General Genetics 263:681–689.




Xu K, Xu X, Fukao P, Canlas R, Maghirang-Rodriguez R,Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, MackillDJ (2006) Sub1A is an ethylene-response-factor-like genethat confers submergence tolerance to rice. Nature 442:705–708.

Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, ZhouH, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation inGhd7 is an important regulator of heading date and yieldpotential in rice. Nature Genetics 40: 761–767.

Yamakawa H, Hirose T, Kuroda M, Yamaguchi T (2007)Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA mi-croarray. Plant Physiology, 144, 258–277.

Yang LX, Huang JY, Yang HJ, Dong GC, Liu G, Zhu JG,Wang YL (2006) Seasonal changes in the effects of free-air CO2 enrichment (FACE) on dry matter productionand distribution of rice (Oryza sativa L.). Field CropsResearch 98: 12–19.

Yin X, Kropff MJ, Goudriaan J (1996) Differential effects ofday and night temperature on development to floweringin rice. Annals of Botany 77: 203–213.

Yin X, van Laar HH (2005) Crop Systems Dynamics: An Eco-physiological Model for Genotype-by-Environment Inter-actions. Wageningen Academic Publishers, Wageningen,The Netherlands, 168pp. ISBN 9076998558.

Yoshimoto M, Oue H, Kobayashi K (2005) Energy balanceand water use efficiency of rice canopies under free-airCO2 enrichment. Agricultural and Forest Meteorology133: 226–246.

Yue B, Xue W-Y, Luo L-J, Xing Y-Z (2006) QTL analysisfor flag leaf characteristics and their relationships withyield and yield traits in rice. Acta Genetica Sinica 33:824–832.

Zhu C, Xiao Y, Wang C, Jiang L, Zhai H, Wan J (2005)Mapping QTL for heat-tolerance at grain filling stage inrice. Rice Science 12: 33–38.

Ziska LH, Bunce JA (2007) Predicting the impact of chang-ing CO2 on crop yields: Some thoughts on food. NewPhytologist 175: 607–618.

Ziska LH, Manalo PA (1996) Increasing night temperaturecan reduce seed set and potential yield of tropical rice.Australian Journal of Plant Physiology 23: 791–794.

Ziska LH, Namuco O, Moya T, Quilang J (1997) Growth andyield response of field-grown tropical rice to increasingcarbon dioxide and air temperature. Agronomy Journal89: 45–53.

Ziska LH, Weerakoon W, Namuco OS, Plamplona R (1996)The influence of nitrogen on the elevated CO2 responseon field growth. Australian Journal of Plant Physiology23: 45–52.

Documents

Crop Adaptation to Climate Change (Yadav/Crop Adaptation to Climate Change) || Genetic Adjustment to Changing Climates: Rice