Regional vulnerability of climate change impacts on Asian rice production and scope for adaptation

Full text

Provided for non-commercial research and educational use only.
Not for reproduction, distribution or commercial use.
This chapter was originally published in the book Advances in Agronomy, Vol 101,
published by Elsevier, and the attached copy is provided by Elsevier for the author's
benefit and for the benefit of the author's institution, for non-commercial research and
educational use including without limitation use in instruction at your institution,
sending it to specific colleagues who know you, and providing a copy to your
institution’s administrator.
All other uses, reproduction and distribution, including without limitation commercial
reprints, selling or licensing copies or access, or posting on open internet sites, your
personal or institution’s website or repository, are prohibited. For exceptions,
permission may be sought for such use through Elsevier's permissions site at:
http://www.elsevier.com/locate/permissionusematerial
From: R. Wassmann, S. V. K. Jagadish, S. Heuer, A. Ismail, E. Redona, R. Serraj,
R. K. Singh, G. Howell, H. Pathak, and K. Sumfleth,
Climate Change Affecting Rice Production: The Physiological and Agronomic
Basis for Possible Adaptation Strategies.
In Donald L. Sparks, editor, Advances in Agronomy, Vol 101.
Burlington: Academic Press, 2009, pp.59-122.
ISBN: 978-0-12-374817-1
© Copyright 2009 Elsevier Inc.
Academic Press.

CHAPTER TWO
Climate Change Affecting Rice
Production: The Physiological
and Agronomic Basis for Possible
Adaptation Strategies
R. Wassmann,*
,†
S. V. K. Jagadish,*S. Heuer,*A. Ismail,*
E. Redona,*R. Serraj,*R. K. Singh,*G. Howell,*H. Pathak,
‡
and K. Sumfleth*
Contents
1. Introduction 60
2. Stress Physiology and Possible Adaptation Mechanisms to Climate
Induced Stresses 63
2.1. High temperature and humidity 63
2.2. Drought 80
2.3. Salinity 93
2.4. Submergence 97
3. Comparative Assessment of Rice Versus Other Crops (In Terms of
Vulnerability and Adaptation Options) 102
3.1. Advantages/disadvantages in warmer climates 102
3.2. Advantages/disadvantages under worsening water stress 106
3.3. Advantages/disadvantages in deteriorating soils 107
3.4. Flexibility for adjusting and coping with climate changes 108
4. Outlook: Current Advances and Future Prospects 109
References 110
Abstract
This review addresses possible adaptation strategies in rice production to
abiotic stresses that will aggravate under climate change: heat (high tempera-
ture and humidity), drought, salinity, and submergence. Each stress is
discussed regarding the current state of knowledge on damage mechanism
for rice plants as well as possible developments in germplasm and crop
Advances in Agronomy, Volume 101 #2009 Elsevier Inc.
ISSN 0065-2113, DOI: 10.1016/S0065-2113(08)00802-X All rights reserved.
*International Rice Research Institute, Metro Manila, Philippines
{
Research Center Karlsruhe (IMK-IFU), Garmisch-Partenkirchen, Germany
{
International Rice Research Institute, New Delhi, India
59
Author's personal copyAuthor's personal copy

management technologies to overcome production losses. Higher temperatures
can adversely affect rice yields through two principal pathways, namely (i) high
maximum temperatures that cause—in combination with high humidity—spikelet
sterility and adversely affect grain quality and (ii) increased nighttime tempera-
tures that may reduce assimilate accumulation. On the other hand, some rice
cultivars are grown inextremely hot environments, so that the development of rice
germplasm with improved heat resistance can capture an enormous genetic pool
for this trait. Likewise, drought is a common phenomenon in many rice growing
environments, and agriculture research has achieved considerable progress in
terms of germplasm improvement and crop management (i.e., water saving
techniques) to cope with the complexity of the drought syndrome. Rice is highly
sensitive to salinity. Salinity often coincides with other stresses in rice production,
namely drought in inland areas or submergence in coastal areas. Submergence
tolerance of rice plants has substantially been improved by introgressing the Sub1
gene into popular rice cultivars in many Asian rice growing areas.
Finally, the review comprises a comparative assessment of the rice versus
other crops related to climate change. The rice crop has many unique features
in terms of susceptibility and adaptation to climate change impacts due to its
semiaquatic phylogenetic origin. The bulk of global rice supply originates from
irrigated systems which are to some extent shielded from immediate drought
effects. The buffer effect of irrigation against climate change impacts, however,
will depend on nature and state of the respective irrigation system. The envi-
saged propagation of irrigation water saving techniques will entail benefits for
the resilience of rice production systems to future droughts. We conclude that
there are considerable risks for rice production stemming from climate change,
but that the development of necessary adaptation options can capitalize on an
enormous variety of rice production systems in very different climates and on
encouraging progress in recent research.
1. Introduction
Rice is consumed by about 3 billion people and is the most common
staple food of a large number of people on earth, in fact it feeds more people
than any other crop (Maclean et al., 2002). Ninety percent of the world’s
rice is produced and consumed in Asia, where irrigated and rainfed rice
ecosystems form the mainstay of food security in many countries (Fig. 1).
Rice production under flooded conditions is highly sustainable and has
apart from emissions of the greenhouse gas methane fewer adverse environ-
mental impacts than other production systems, for example, less soil erosion,
high soil organic matter content, and so on (Bouman et al., 2007). Climate
change, however, could seriously threaten production levels required to
feed future generations in Asia and other continents. Climate change has
many facets, including changes in long term trends in temperature and
60 R. Wassmann et al.
Author's personal copy

rainfall regimes as well as increasing variability in extreme events. The
impacts of these changing conditions on agriculture are already being
seen, yet there are still considerable gaps in our knowledge of how agricul-
tural systems will be affected by both short- and long-term changes in
climate, and what implications these changes will have for rural livelihoods,
particularly among the most vulnerable. Despite some projected increase in
photosynthesis caused by higher concentrations in CO
2
([CO2]), increased
temperature may result in reduced productivity. For some regions and
1 Dot = 10,000 ha
Irrigated rice
1 Dot = 10,000 ha
Rainfed rice
Figure 1 Irrigated and rainfed rice in East, South and Southeast Asia (data source:
Huke and Huke, 1997).
Climate Change Affecting Rice Production 61
Author's personal copy

crops, there will be opportunities for increased production, but all in all,
there is no doubt that net agricultural production will be adversely affected
by climate change (IPCC, 2007a).
Future farming and food systems will have to be better adapted to a range
of abiotic and biotic stresses to cope with the direct and indirect conse-
quences of a progressively changing climate. To this end, intensively man-
aged cropping systems such as rice production offer a variety of entry points
to adjust to projected climate change (Aggarwal and Mall, 2002; Butt et al.,
2005; Easterling et al., 2003; Challinor et al., 2007; Howden et al., 2007;
Travasso et al., 2006). Climate change will aggravate a variety of stresses for
rice plants, namely heat, drought, salinity, and submergence. Improved
tolerance to these abiotic stresses has always been at the heartland of research
institutions, such as the International Rice Research Institute (IRRI),
dealing with agricultural production in unfavorable environments. For
rice production, research on adaptation to climate change can broadly
capitalize on the enormous progress made in disentangling the traits asso-
ciated with tolerance and in developing DNA-based technologies for pre-
cise and speedy breeding of more adapted varieties. The new challenge of
climate change, however, will require stepping up these activities to
unprecedented levels. The resilience of rice production systems has to be
increased in a two-pronged approach, (i) increasing tolerance to individual
stresses and at the same time (ii) achieving multiple stress tolerance.
While we do not see crop technology as the ultimate solution to all
threats posed by climate change, we remain convinced that germplasm
development and improved agronomic practices should be a center piece
of climate change adaptation in agriculture. These approaches have proven
track records in achieving more resilience to climate variability and
extremes. Superimposed on Climate Change effects, agriculture is con-
fronted with other rapid socioeconomic changes resulting in labor
shortages, rising costs of energy, and so on. Competition for water, for
instance, will increase the pressure on rice land and favor the adoption of
cropping systems or practices that consume less irrigation water.
The Green Revolution has improved rice productivity across monsoon
Asia through a combination of new high-yielding varieties with increased
input use, such as stable water supply from new irrigation systems, fertilizer,
and biocide use (Hossain and Fischer, 1995). Because of this increased
productivity, and an increase in cropped area, total rice production over
the last 40 years has more than kept pace with the tremendous growth in
population in Asia and now stands at about 550–600 million tones annually
(Maclean et al., 2002). After a 3-decade long period of low rice prices,
however, rice prices have soared in 2007/2008. The world price of Thai
export grade rice has almost tripled from December 2007 to April 2008 this
year. A major reason for this price increase is the slowing growth in
production, which declined from 2.7% per year in 1970–1990 to 1.2%
62 R. Wassmann et al.
Author's personal copy

per year in 1990–2007. In the foreseeable future, rice will continue to be the
main staple food of Asia (Rosegrant et al., 2001; Sombilla et al., 2002). To
fight poverty and provide food security, rice production must increase
dramatically in spite of climatic change impacts.
2. Stress Physiology and Possible Adaptation
Mechanisms to Climate Induced Stresses
2.1. High temperature and humidity
Rice, like other cultivated crops, has relative variable temperature prefer-
ences over the growing season. Deviation from the stage-dependent opti-
mum temperature will alter the physiological activities or lead to a different
developmental pathway (Downton and Slatyer, 1972). The response of rice
to high temperatures differs according to the developmental stage with high
temperature tolerance at one developmental stage may or may not neces-
sarily lead to tolerance during other stages. Similarly, cold tolerance at the
booting stage was shown to have no relationship to the flowering stage
tolerance in high-yielding rice varieties (Goto et al., 2008). However, an
independent extreme heat episode during vegetative stages was shown to
have no influence on reproductive stage (Porter and Semenov, 2005).
Hence, the effect of high temperature during different developmental stages
has to be partitioned and evaluated separately for assessing, identifying,
characterizing for genetic manipulation of tolerance mechanisms (Wahid
et al., 2007). The crop growth cycle of rice can be broadly divided into three
stages namely vegetative, reproductive, and grain filling or ripening phase
(Fig. 2), and their response to high temperatures with extra emphasis on the
most sensitive reproductive stage is explained in this section.
2.1.1. Heat stress at different ontogenetic stages
2.1.1.1. Vegetative phase During vegetative stage, rice can tolerate rela-
tively high temperatures (35/25 C; expressing day/night temperature
regime). Temperatures beyond this critical level could reduce plant height,
tiller number and total dry weight (Yoshida et al., 1981). In a temperature
gradient chamber study, rice exposed to 3.6 and 7.0 C higher temperature
than ambient, from heading to middle ripening stage, reduced photosyn-
thesis by 11.2–35.6%, respectively (Oh-e et al., 2007). This decline in the
photosynthesis can be attributed to structural changes in the organization
of thylakoids (Karim et al., 1997) and more particularly due to loss of
stacking of grana in the chloroplast or its ability to swell (Wahid et al.,
2007). Moreover, membranes that house these cell organelles are extremely
important as high temperatures increase the kinetic energy, in turn the
molecular movements to loosen the bonds between biological membranes
Climate Change Affecting Rice Production 63
Author's personal copy

(Wahid et al., 2007). Such rapid movements will lead to increase in fluidity
of lipid layer (Savchenko et al., 2002) resulting in increased solute leakage
and membrane instability.
Quantitative electrolyte leakage or cellular membrane thermostability
(CMT) has been used as a measure of heat tolerance during the vegetative
stage in many crops (see Prasad et al., 2006; Tripathy et al., 2000). A positive
association between CMT and heat tolerance at flowering has been found in
cowpea (Vigna unguiculata L.) (Ismail and Hall, 1999). However, a poor
correlation (r= 0.02) between reproductive stage tolerance measured by
spikelet fertility and heat tolerance during vegetative stage measured by
CMT in 14 rice genotypes was observed (Prasad et al., 2006). Accordingly,
in peanuts (Arachis hypogea) a similar relation has been found (Craufurd et al.,
2003; Kakani et al., 2002), indicating different responses to heat at
vegetative and reproductive stages in rice and peanuts.
Spikelet closes
Microgametogenesis
90 DAG
~80 DAG
50–80 min
Microsporogenesis
Anthesis/spikelet opening
Vegetative Grain filling
Reproductive
60 DAG 30 DAG30 DAG
Pollen mother cell formation
Meiosis I (tetrad formation)
Microspore stage
Pollen formation stage (mitosis)
Mature starchy pollen stage
90% heading
Anther dehiscence
Pollination
Pollen germination
Fertilization
Figure 2 Partitioning crop growth cycle of rice variety (120 days) into three major
phases with extra emphasis on heat sensitive stages during the reproductive stage. DAG,
Days after germination.
64 R. Wassmann et al.
Author's personal copy

2.1.1.2. Reproductive phase Reproductive stage in rice is more sensitive
to heat than the vegetative stage (Yoshida et al., 1981). Anthesis/flowering,
identified with the appearance of the anthers, is the most sensitive process
during reproductive stage to high temperature (Nakagawa et al., 2002;
Satake and Yoshida, 1978) followed by microgametogenesis (Fig. 3).
Reciprocal studies with manual shedding of pollen from control plants on
to the stigma exposed to high temperature and vice versa showed that the
ability of the pistil to be fertilized remained unaffected even over a period of
5 days at 41 C(Yoshida et al., 1981). Similarly, wheat spikelet fertility was
increased from 30 to 80% by pollinating heat stressed pistil with unstressed
pollen (Saini and Aspinall, 1982). Hence, the male reproductive organ is
mainly responsible for spikelet sterility under high temperature and has been
targeted for increasing tolerance to warmer climates.
Mature male reproductive unit or pollen formation is a result of:
(i) Pollen mother cell formation from diploid sporophytic cells in the
anther
(ii) Formation of haploid unicellular microspores from pollen mother cells
(microsporogenesis)
(iii) Microspores to microgametophytes with gametes and
(microgametogenesis)
(iv) Male gametophytes developing into mature starchy pollen (Fig. 2)
Processes close to the meiotic stage during tetrad formation and young
microspore stage are most sensitive to high temperature during microspo-
rogenesis (Yoshida et al., 1981), similar to drought (Sheoran and Saini,
1996) and cold stress (Imin et al., 2004). A significant reduction in pollen
production at 5 C above ambient air temperature (Prasad et al., 2006) was
Day relative to anthesis
–25 –20 –15 –10 –5 0 5 10
Spikelet fertility (%)
0
20
40
60
80
100
Microsporogenesis
Anthesis
Figure 3 Spikelet fertility of BKN6624–46–2 exposed to high temperature of 35 C
during different stages of panicle development for 5 days (Yoshida et al., 1981; redrawn
by P. Craufurd).
Climate Change Affecting Rice Production 65
Author's personal copy

attributed to impaired cell division of microspore mother cells (Takeoka et al.,
1992). At lower temperature (20 C), wheat spikelets had 93% of viable
pollen in dehisced anther while at a higher temperature of 30 C for 3 days
dehisced anthers had significantly lower percent (59%) of viable pollen
(Saini and Aspinall, 1982). Accordingly, high temperatures (35C) during
microsporogenesis resulted in 34% decline in spikelet fertility (Fig. 3).
Heat stress during anthesis leads to an irreversible effect with stagnation
in panicle dry weight even with subsequent improvement in the environ-
ment (Oh-e et al., 2007). However, rice genotypes can either escape or
avoid high temperatures during anthesis, by heading during the cooler
periods of the season (macroescape), by anthesing during cooler hours of
early morning (microescape, O. glaberrima spp. Yoshida et al., 1981), altered
flowering pattern or by increased transpiration cooling of the canopy.
Advancing peak anthesis toward early hours of the morning (Prasad et al.,
2006), is an efficient strategy to escape high temperatures during later hours
of the day. Significant genotypic variation for early morning peak anthesis
exists in rice germplasm with O. glaberrima (CG14) having the ability to
flower immediately after dawn, potentially escaping high temperatures dur-
ing the later hours of the day (Fig. 4). The early morning flowering advan-
tage of O. glaberrima has been exploited in interspecific crosses between
O. glaberrima and O. sativa to advance peak flowering time of the day by
1h toward early morning (Yoshida et al., 1981). Moreover, rice has the
ability to monitor and control the rate of flowering as an escape mechanism
under high temperature. The concept of spenders and savers with reference
to rate of flowering in rice has been mentioned (Jagadish, 2007, Jagadish
et al., 2007), wherein a 20% increase and 36% decline in the rate of flowering
was seen in cultivars IR64 and Azucena, respectively, at 38 C and 60%
relative humidity over three consecutive days.
Rice plants when exposed to high temperatures during critical stages can
avoid heat by maintaining their microclimate temperature below critical
levels by efficient transpiration cooling. Moreover, the effect of high tem-
perature is closely related to the ambient relative humidity and hence the
level of transpiration cooling is determined by vapor pressure deficit than
temperature per se. Using ultra thin copper constantan thermocouples,
Jagadish et al. (2007) recorded spikelet tissue temperatures of 29.6, 33.7,
and 36.2 C, that is, 0.4, 1.3, and 1.8 C below ambient air temperatures of
30, 35, and 38 C, respectively. Similar differences were observed elsewhere
in rice (Satake, 1995) and in peanut flowers in the same growth cabinets
used by Jagadish et al. (2007) (Vara Prasad et al., 2001). Lower relative
humidity of 60% at 38 C leads to a higher vapor pressure deficit of 2.65
facilitating the plant to exploit its transpiration cooling ability ( Jagadish,
2007; Jagadish et al., 2007). Similarly, Abeysiriwardena et al. (2002)
recorded a 1.5 C increase in spikelet temperature by increasing RH from
55–60% to 85–90% at a constant temperature regime of 35/30 C.
66 R. Wassmann et al.
Author's personal copy

Moreover, Weerakoon et al. (2008) using a combination of high tempera-
tures (32–36 C) with low (60%) and high (85%) RH recorded high spikelet
sterility with simultaneous increase in temperature and RH. Hence it can be
concluded that the reduction in spikelet temperature in relation to RH is
avoidance while the performance of a variety at a given spikelet temperature
to be true tolerance.
On the basis of the interaction between high temperature and relative
humidity, rice cultivation regions in the tropics and sub-tropics can be
classified into hot/dry or hot/humid regions. It can be assumed that
rice cultivation in hot/dry regions where temperatures may exceed 40 C
0
50
100
150
200
250
012345678
012345678
Hours after dawn
Number of spikelets opened
29.6⬚C
36.2⬚C
0
50
100
150
200
250
300
350
Hours after dawn
Number of spikelets opened
29.6⬚C
36.2⬚C
IR64
CG14
Figure 4 Flowering patterns of O. sativa cv. IR64 and O. glaberrima cv.CG14 under
both control and high temperature (bars indicates SE; adapted from Jagadish et al.,
2008).
Climate Change Affecting Rice Production 67
Author's personal copy

(e.g., Pakistan, Iran, India) has been facilitated through unintentional selec-
tion for efficient transpiration cooling under sufficient supply of water.
Furthermore, the effect of transpiration cooling was assessed using a simple
heat budget model for a typical microclimate in paddy fields resulting in a
0.6 C lower canopy temperature at an ambient temperature of 30 C and
RH of 60%. The results showed higher cooling under hot and dry condi-
tion with 2.5 C lower canopy temperature at an ambient temperature of
34 C and 60% RH, 4.6 Cat30C and 20% RH, and 6.9 Cat34C and
20% RH (Matsui et al., 2007). An exceptionally high temperature difference
of 6.8 C between crop canopy and ambient air temperature (34.5 C) was
recorded in Riverina region of New South Wales, Australia which was
primarily due to extremely low humidity of 20% (VPD=4.32), resulting in
strong transpiration cooling mainly driven by high wind velocity of 3.2–
4.2ms
1
(Matsui et al., 2007).
Introduction, acceptance and wide spread cultivation of semidwarf
improved varieties, with better canopy architecture could be one major
reason for adjusting rice to existing temperature changes and could play
an important role in adapting to future extreme temperatures. Moreover,
improved varieties that have panicles surrounded by plant leaf canopy
unlike traditional varieties, are immensely benefited by combined transpi-
ration cooling during the sensitive anthesis period (Fig. 5).
Heat avoiding genotypes thrive well in hot and dry rice cultivation
regions of the world while for hot and humid regions either heat escape
Figure 5 Plant architecture of the rice plant.
68 R. Wassmann et al.
Author's personal copy

or true tolerance is essential to maintain productivity. However, with
predicted increased mean surface air temperature rather than just increased
maximum temperature the rice plant could be exposed to increased day and
night temperatures further indicating the importance of true heat tolerance.
Increased heat tolerance is most needed in O. sativa spp. (IR64; Fig. 4),
compared to O. glaberrima spp., (CG14; Fig. 4) which exhibit peak anthesis
during late morning till midafternoon (Yoshida et al., 1981), exposing the
heat sensitive reproductive organs to high temperatures invariably leading to
increased spikelet sterility ( Jagadish et al., 2008; Prasad et al., 2006). More-
over, O. sativa spp, occupy major rice growing regions of Asia and is
exponentially increasing in the African continent.
High temperatures induce sterility, if the sensitive physiological pro-
cesses (anther dehiscence, pollination, pollen germination on the stigma,
pollen tube growth or the early events of fertilization) are affected. Anthesis
in rice is extremely sensitive to high temperature and spikelets opening on
any flowering day during the flowering period (5–7 days) could be affected
differently depending on the duration of exposure (Fig. 6);
Flowerin
g
time in relation to anthesis (h)
–4 –2 0 2 4
Spikelet fertility (%)
0
20
40
60
80
100
A
CB DE
Figure 6 The extreme sensitivity of high temperature during anthesis leading to
spikelet sterility: (A) high temperature for 4 h, (B) high temperature for 1h,(C)1h
before the onset of high temperature, (D) 1 h immediately after high temperature
exposure, and (E) beyond 1 h of high temperature exposure (modified from Satake and
Yoshida, 1978).
Climate Change Affecting Rice Production 69
Author's personal copy

(i) High temperature exposure for 4 h coinciding with anthesis reduced
spikelet fertility from 90 to <20% (Yoshida et al., 1981; see period ‘‘A’’
in Fig. 6).
(ii) Spikelet tissue temperatures >33.7 C (ambient air temperature of
35 C) for half an hour induced sterility indicating extreme sensitiv-
ity of rice to high temperature at anthesis ( Jagadish, 2007; Jagadish
et al., 2007; see period ‘‘B’’ in Fig. 6).
(iii) Spikelets opening an hour before the onset of high temperature were
unaffected with the subsequent high temperature exposure ( Jagadish,
2007; Jagadish et al., 2007; see period ‘‘C’’ in Fig. 6).
(iv) Spikelets opening within an hour after the high temperature exposure
were partially affected as the function of the pollen sac (anther) itself
would be affected by the preceding high temperatures ( Jagadish, 2007;
Jagadish et al., 2007; Matsui et al., 2000a; see period ‘‘D’’ in Fig. 6).
(v) Spikelets opening beyond 1 h of the high temperature exposure are
unaffected (see period ‘‘E’’ in Fig. 6).
Anther dehiscence is the most susceptible process during anthesis under
high temperature (Matsui et al., 1999b). High temperature results in
increased vapor pressure deficit, enhancing evaporation from the anthers,
thereby depriving the crucial moisture needed for pollen grain swelling
which is inevitable for anther dehiscence. Genotypic differences in anther
characteristics between susceptible and tolerant rice genotypes exist
(Table 1). Artificial spikelet opening triggered rapid pollen swelling, result-
ing in anther dehiscence and subsequent pollen shedding from apical and
basal pores (Matsui et al., 1999a,b). The anther basal pore length is considered
to have a significant contribution toward pollination under high temperature
because of its close proximity to the stigmatic surface (Matsui and Kagata,
2003). The importance of the apical pore under high temperature is not well
understood. Alternatively, in some water stressed anthers of IR64, the basal
pore failed to open while in the other anthers with open pores the pollen
failed to shed from the opened apical pore, which was attributed to increased
pollen stickiness (Liu et al., 2005). A similar mechanism could operate in
anthers of heat sensitive genotypes, which warrants a detailed study.
Dehiscence of the anther leading to pollen deposition on the stigma is
called as pollination. After pollination if takes about 30min for the pollen tube
to reach the embryo sac and fertilization will be completed in 1.5–4 h (Cho,
1956). Ricepollen is extremely sensitive to temperature and relative humidity
(Matsui et al.,1997b) and looses its viability within 10 min of shedding (Song
et al.,2001). Spikelets having >20 germinating pollen on the stigma showed
good agreement with fertility at high temperature of 38C(Matsui et al.,
1997a). The tolerant cultivar Shanyou63 showed significantly slower reduc-
tion in pollen activity, pollen germination and rate of floret fertility compared
to the susceptible cv. Teyou559 at 39 C(Tang et al., 2008). Developmental
70 R. Wassmann et al.
Author's personal copy

processes beyond pollen germination are sensitive to heat and have been
shown in rice (Enomoto et al.,1956;Satake and Yoshida, 1978;Yamada,
1964) and other crops (A. hypogea:Kakani et al., 2002, 2005;Glycine max:
Salem et al.,2007).
The mechanisms of anther dehiscence are well understood (Matsui et al.,
2000a,b) but the physiological and biochemical reasons for reduced pollen
activity and germination are not yet clear. However, endogenous hormones
are known to play an important role in determining male fertility. Tang
et al. (2008) quantified the growth hormones in the anthers and found a
decrease in indole acetic acid (IAA), gibberellic acid (GA
3
), free proline and
soluble proteins but a significant increase in absisic acid (ABA) content.
Table 1 Anther characteristics affecting dehiscence in tolerant and susceptible rice
genotypes (modified from Jagadish et al., 2007)
Anther traits of tolerant
genotypes
Anther traits of
susceptible genotypes Reference
Longer anthers Comparatively shorter
anthers
Matsui et al. (2001)
Two cell layers (degrading
or degraded tapetum and
endothecium cells)
separate the locule from
the lacuna, allowing for
easy anther dehiscence
Three cell layers
(degrading tapetum,
endothecium cells,
and parenchyma cells)
separate the locule
from the lacuna,
hindering anther
dehiscence
Matsui and Omasa
(2002)
Easy and homogeneous
anther dehiscence
Abnormal or no anther
dehiscence
Matsui et al.
(1997b)
Yoshida et al.
(1981)
Satake and Yoshida,
(1978)
Anthers dehisce within the
spikelet on short
filaments, shedding
more pollen on
the stigma
Anther do not dehisce
or they may dehisce
outside the spikelet
on loose sagging
filaments, with less
pollen shed on
the stigma
Satake and Yoshida
(1978)
Longer basal pore length Shorter or no basal pore
opening
Matsui and Kagata
(2003)
Climate Change Affecting Rice Production 71
Author's personal copy

They concluded that low levels of IAA and GA and higher levels of ABA
lead to pollen abortion, a major reason for male sterility. Simultaneous
decline in free proline and soluble proteins in the susceptible cultivar
enhanced stress resulting in floret sterility. Furthermore, accumulation of
compatible osmolytes like sugars, sugaralcohols (Sairam and Tyagi, 2004),
glycine betaine (Sakamoto and Murata, 2002) plays an adaptive role under
extreme temperatures by buffering cellular redox potential (Wahid and
Close, 2007).
Screening for heat tolerant donors Prasad et al. (2006) identified heat
tolerance in both sub spp. of O. sativa and it cannot be generalized that
either indica or japonica sub spp. are more tolerant than the other based on
the place of origin. An aus variety N22 has consistently shown tolerance to
high temperature during anthesis ( Jagadish et al., 2008; Prasad et al., 2006;
Yoshida et al., 1981). However N22 is also known to be highly drought
tolerant with enhanced levels of reactive oxygen scavenging enzymes
resulted in lower H
2
O
2
levels in water stressed panicles of N22 compared
to the susceptible N118. Since, N22 is consistently proved to be truly heat
tolerant under diverse experimental conditions, a similar reactive oxygen
scavenging mechanism could operate leading to heat tolerance, which needs
further experimental evidence for confirmation.
Variable heat tolerance thresholds among rice genotypes during flower-
ing are known (Yoshida et al., 1981). A 3 C difference in critical tempera-
ture causing 50% spikelet sterility between the tolerant genotype (40 C;
Akitakomachi) compared to the susceptible genotype (37 C; Hinohikari) is
recorded (Matsui et al., 2001). Although genotypic difference to critical
heat thresholds in rice is known (Yoshida et al., 1981), experimental
evidence for interaction between high temperature and duration of expo-
sure was recently documented ( Jagadish, 2007; Jagadish et al., 2007). An
interaction between high temperature and duration of exposure in a heat
sensitive genotype (Azucena) but not in a moderately tolerant IR64 was
identified ( Jagadish, 2007; Jagadish et al., 2007), indicating the importance
of temperature and duration interactions in actual field experiments and
inclusion in future crop models. Present crop models have the genotypic
difference in critical temperature thresholds causing sterility incorporated in
them, the possibility of an interaction between temperature and duration of
exposure is assumed to be nonsignificant. Generally, response of rice to high
temperature has been modeled using daily mean temperature (Horie et al.,
1995; Kropff et al., 1995), number of days with maximum temperature
>34 C(Challinor et al., 2007) and more recently using daily minimum and
maximum temperature (Krishnan et al., 2007) but anthesis is extremely
sensitive to hourly time course of temperature. Hence, flowering models
with hourly temperature changes are needed, which can be incorporated
into crop models for better prediction. The interactive effect could be
included into crop models by adopting the cumulative temperature
72 R. Wassmann et al.
Author's personal copy

response above a threshold temperature of 33 C for rice ( Jagadish, 2007;
Jagadish et al., 2007; Nakagawa et al., 2002). A similar response was seen in
ground nut and has been quantified by cumulative temperature approach
(Vara Prasad et al., 1999). Accumulated temperature or thermal time above
a threshold can be calculated by TT = (T33 C) t, where Tis the day
temperature and tis the duration of the treatment (Fig. 7). Furthermore,
quantification of high temperature impact on future crop yields based on
predictions is in its infancy (Challinor et al., 2007) due to less experimental
data available.
2.1.1.3. Ripening phase High temperature affects cellular and develop-
mental processes leading to reduced fertility and grain quality (Barnabas
et al., 2008). Decreased grain weight, reduced grain filling, higher percent-
age of white chalky rice and milky white rice are common effects of high
temperature exposure during ripening stage in rice (Osada et al., 1973;
Yoshida et al., 1981). In addition, increased temperature causes serious
reduction in grain size and amylase content (Yamakawa et al., 2007; Zhu
et al., 2005) further reducing the potential economic benefits farmers can
derive from rice cultivation due to depression in farm-gate and/or milled
grain prices. High temperature during grain-filling period accelerates the
demand for more assimilates to avoid milky white kernels (Kobata and
0 5 10 15 20 25
–5
–4
–3
–2
–1
0
Accumulated hours with temperature >33⬚C
Spikelet fertility (logit %)
Figure 7 Relationbetween spikelet fertility and accumulated hourly temperature >33 C
in Azucena. Key: open symbols ¼33.7 C; closed symbols ¼36.2 C; 2003 (^,e); 2004-
duration:○,1h;□,2h;△,4h;▽, 6h. Fitted line: Y¼6.50 1.67X, r
2
¼0.88. ( Jagadish
et al., 2007).
Climate Change Affecting Rice Production 73
Author's personal copy

Uemuki, 2004). The reduced grain weight under high temperature is
attributed to excessive energy consumption to meet the respiratory demand
of the seeds (Tanaka et al., 1995). Alternatively, the reduction in grain
weight is attributed to higher grain dry matter accumulation rate together
with a shortened grain-filling period (Kobata and Uemuki, 2004). High
temperature during grain-filling period is a critical factor to reduce grain
filling/ripening but this effect could be magnified by lower assimilate supply
(Kobata and Uemuki, 2004). They concluded that the reduction in grain
weight could be overcome if sufficient assimilates were supplied to meet
higher grain dry matter accumulation rate under high temperatures.
Following the work of Kobata and Moriwaki (1990) and Kobata et al.
(2000) the plant density was reduced to half by thinning and found that in
thinned plants significantly more assimilates were produced than required to
meet higher accumulation rates even when the plants were exposed to high
temperatures, mainly due to reduced competition (Kobata and Uemuki,
2004). They recorded >100% increase in grain dry weight even under high
temperature exposure (1–4 C higher than outside temperature) over
2 years. Similarly, by shading or panicle clipping Tsukaguchi and Yusuke
(2008) showed a significant reduction in milky white and white belly
kernels with increased assimilate supply under high temperature during
the initial grain-filling period. Cultivar Koshihikari has been identified to
meet the increased grain dry matter accumulation rates during grain-filling
period and shows reduced percentage of milky white and white belly
kernels with sufficient assimilate supply even under high temperatures
(Kobata and Uemuki, 2004). Hence simple agronomic measures like opti-
mum plant densities, that is, single seedling per hill could be useful in
sufficient assimilate supply during grain filling under high temperature to
overcome a large proportion of chalky grain and reduction in grain weight.
2.1.2. Temperature and CO
2
interaction
Although elevated CO
2
could enhance photosynthesis, especially in C
3
crop like rice, it is a potential component to trap the short wave radiations
from the earth surface only to be redirected back to increase the global
surface mean temperature. Increased biomass production due to elevated CO
2
could potentially increase yield, provided microsporogenesis, flowering, and
grain-filling are not disrupted by environmental stresses such as drought or
high temperature. Biochemically, increase in CO
2
concentration stimulates
increase in RuBisCO and photorespiration is reduced. Hence, increasing
temperature could result in higher net photosynthesis and CO
2
uptake
(Potvin, 1994). Moreover, rice grains are a significant sink for assimilates and
removal or restriction of this carbon sink will fail to exploit the elevated CO
2
due to photosynthetic insensitivity (Stitt, 1991; Webber et al.,1994). Accord-
ingly, Ziska et al. (1996) recorded a significant increase in root/shoot ratio
74 R. Wassmann et al.
Author's personal copy

with elevated CO
2
with increasing temperature and hinted at alternative sinks
becoming active recipients with reduced carbon sink capacity of the grains due
to spikelet sterility from high temperature exposure. Furthermore, Matsui et al.
(1997a) studying the interaction of CO
2
and temperature at reproductive stage
recorded an increase in canopy temperature due to stomata closure at high
CO
2
concentrations. They concluded that the critical air temperature for
spikelet sterility (as determined from the number of germinated pollen grains
on the stigma) was reduced by 1 C at elevated concentrations of carbon
dioxide (ambient +300 ml
1
CO
2
) which could have been due to low transpi-
ration cooling majorly driven my stomata closure. Increasing temperatures
from 28/21 to 37/30 C decreased grain yield from 10.4 to 1.0 Mgha
1
even
under 660 mmolofCO
2
mol
1
of air (Baker et al., 1992). Ziska et al. (1996)
recorded70 and 22% increase in biomass at elevated CO
2
treatment under 29/
21 C and 37/29 C, respectively, while grain yield of 17 contrasting cultivars
recorded <1% filled spikelets. Hence this indicates that increasing CO
2
concentration could limit rice yield if average air temperature increased
simultaneously. Hence interaction of CO
2
and temperature at both vegetative
and reproductive stages has to be further explored to exploit the increasing
CO
2
for increasing yields.
2.1.3. High night temperature
Peng et al. (2004) analyzed weather data at the International Rice Research
Institute farm from 1979 to 2003 to examine the temperature trends and the
relationships between rice yields and temperature. Annual mean maximum
and minimum temperatures increased by 0.35 and 1.13 C, respectively, for
the above period and a close correlation between rice grain yield and mean
minimum temperature was observed. Grain yield declined by 10% for each
1C increase in minimum temperature in the dry season whereas the effect
of maximum temperature was insignificant. Similarly, Pathak et al. (2003)
estimated that the rate of change in the potential yield trend of rice from
1985 to 2000 ranged from 0.12 to 0.05 Mgha
1
yr
1
. Negative yield
trends were observed at six of the nine sites, four of which were statistically
significant (P<0.05). The decrease in radiation and increase in minimum
temperature were identified as the reasons for the yield decline. Although,
high temperature at both day and night reduced the duration of grain
growth, the rate of growth was lower in the early or middle stages of
grain filling, and also reduced cell size midway between the central point
and the surface of endosperm at high night temperature (22/34 C) than
at high day temperature of 34/22 C(Morita et al., 2005). However,
research into the effect of high night temperature is not been understood
well and should be prioritized with much higher mean night temperatures’
predicted.
Climate Change Affecting Rice Production 75
Author's personal copy

2.1.4. Breeding rice for warmer world
The development and adoption of high-yielding and semidwarf rice vari-
eties during the ‘‘Green Revolution’’ period starting in the 1960s more than
doubled the rice production from 256 million (m) tons in 1965 to around
600 mtons in 2007. The new varieties developed were more responsive to
fertilizer inputs, were lodging resistant, had 2–3 times higher yield potential
than traditional varieties, and possessed multiple resistances to biotic and
abiotic stresses leading to stable yields (Khush, 1999). Higher production
achieved through improved varieties led to the lowering of rice prices by
about 40%, thus benefiting the poor population of developing nations who
spend 50–60% of their income on food (Khush, 2001). Moreover, shifting
from traditional to modern varieties increased farmers’ yield by 2.1 tons
ha
1
, on average, and resulted in an annual economic benefit estimated at
US $10.8 billion (Hossain et al., 2002). Evenson and Gollin (1997) esti-
mated that, between 1975 and 1995, widespread adoption of modern
varieties reduced rice importation by 8%, malnutrition by 1.5–2%, and
saved millions of hectares of forests and fragile ecosystems from being
converted into rice areas.
Plant breeding, rice varietal improvement can potentially avert—at least
in part—the negative effects of climate change on rice production.
Although farmers can adapt to climate change by shifting planting dates,
selecting varieties with different growth durations, or changing crop rota-
tions, these coping mechanisms may result in lower yields and with delayed
or changed plantings may slow down rice yield growth. Developing
germplasm with higher tolerance to climate-induced stresses through
breeding is a sound climate change adaptation strategy.
2.1.4.1. Genetic improvement for heat tolerance Breeding rice varieties
tolerant to high temperature has so far received little attention as compared to
other abiotic stresses like drought and salinity. After one comprehensive study
in the early 1980s (Mackill, 1981; Mackill et al., 1982; Mackill and Coffman,
1983), high temperature tolerance of rice has only been treated within region-
specific breeding programs with limited success. In Sindh (Pakistan), IR6 has
been introduced in the year of 1969 and is still the prevalent cultivar, although a
local research institute has released several varieties since 1982 to cope with
high temperatures (Naich and Mari, 2007). Under temperatures that regularly
exceed 36 C during the flowering period, however, IR 6 has outperformed
these new varieties in terms of spikelet sterility (5% for IR6 vs >15% for newer
varieties) and yield (>7tha
1
for IR6 vs<7tha
1
for newer varieties).
Evidence in crops such as tomato, peanut, cotton, and cowpea clearly
indicate that plant breeding can yield varieties adapted to high temperature
stress (Hall, 1992, 2004). Two distinct concepts of breeding can be
explored, that is, (i) breeding rice varieties that can tolerate higher
76 R. Wassmann et al.
Author's personal copy

temperatures per se or (ii) that escape high temperatures either by having
shorter growing seasons or flowering/maturity or by flowering earlier
during the day (Redon
˜aet al., 2007). For the latter, the most promising
approach is to shift the time of flowering from the usual 10 AM to noon
(Yoshida et al., 1981) to an earlier daytime when the temperatures would be
expected to be lower. Wahid et al. (2007) noted that to be successful in
improving agricultural productivity under a stress environment, emphasis
should be put on developing cultivars that can both tolerate environmental
stresses as well as maintain economic yield. Therefore, genes or quantitative
trait loci (QTL) underlying heat tolerance or avoidance need to be identi-
fied and then combined with traits such as high yield, resistance to multiple
stresses, and acceptable grain quality, among others. The breeding process
could be complex and may involve several steps, such as
1. Identification of genetic donors
2. Hybridization and recombination
3. Phenotypic and/or molecular marker-aided selection of desired geno-
types from segregating populations
4. Preliminary evaluation of elite breeding lines in unreplicated trials
5. Extensive multi-environment (both temporal and spatial) testing
6. On-farm trials and participatory varietal selection
7. Varietal release and production of breeder, foundation, registered, and
certified seeds
8. Frontline demonstration and promotion of the newly approved cultivars
The varietal development process requires the active involvement of
multidisciplinary teams comprised of breeders, geneticists, pathologists,
entomologists, physiologists, biotechnologists, agronomists and cereal che-
mists, among others. Recent experience in breeding for biotic and other
abiotic stresses ( Jena and Mackill, 2008) suggests–while the process may be
complex–it should be possible to transfer major QTLs for high temperature
tolerance, once identified, into locally adapted genotypes or new genotype
combinations using either conventional breeding approaches or molecular
maker assisted selection techniques.
2.1.4.2. Genetic donors for heat tolerance and avoidance While heat
tolerance in rice has been determined to be a highly heritable trait as early as
the 1970s (IRRI, 1976), most of the breeding work done so far have
focused on germplasm screening and evaluation (IRRI, 1980; Yoshida
et al., 1981). Genetic variability for high temperature tolerance has been
observed in rice (Mackill et al., 1982; Yoshida et al., 1981). High tempera-
ture tolerant lines were found to have higher pollen shedding under optimal
temperatures than the intolerant lines. Jennings et al. (1979), for example,
found the variety Hoveyzeh from southern Iran to be tolerant at
temperature higher than 45 C when other varieties were already
Climate Change Affecting Rice Production 77
Author's personal copy

completely sterile. Moradi and Gilani, (2007) reported the local Iranian
landraces Anbori and Hoveaze (probably the same as or a variant of Hovey-
zeh), to be also tolerant to high temperatures. Yoshida et al. (1981) reported
that varieties such as Agbede, Carreon, Dular, N22, OS4, P1215936, and
Sintiane Diofor have fertility percentages ranging from 84 to 90% even at
high temperatures. Some other promising heat tolerant and avoidance
entries identified are documented ( Jagadish et al., 2008; Mackill, 1981;
Matsui and Omasa, 2002; Matsui et al., 2001, 2007; Redon
˜aet al., 2007;
Yoshida et al., 1981). Genetic variation for time of day flowering (TDF) has
also been reported in rice. Yoshida et al. (1981) noted that O. glaberrima
flowers early in the morning and proposed that this trait be incorporated
into O. sativa through breeding. Furthermore, they reported that derivatives
from O. glaberrima and O. sativa crosses flowered earlier than O. sativa.
Sheehy et al. (2005) also found O. glaberrima accessions to have early TDF
while noting that Chhalangpa had the earliest TDF of 0915 h among
selected O. sativa cultivars. Prasad et al. (2006) confirmed the observations
of Yoshida et al. (1981) that cultivars of O. glaberrima (CG-14 and CG-17)
and interspecific hybridization derivative lines (WAB-12 and WAB-16)
flowered early (0700 and 0830 h). However, despite early flowering, it
was noted that the spikelet fertilities of CG-14, CG-17, WAB-12, and
WAB-16 were decreased by high temperature suggesting different genetic
control for the heat tolerance and early TDF traits. Among O. sativa
cultivars that flowered earlier than 1000h were IR-8, IR-72, and N-22.
2.1.4.3. Selection indexes for heat tolerance and avoidance Proper
screening techniques and procedures under the right environments are
crucial for determining the true value of a given genotype to be used for
both genetics and plant breeding applications. The choice of a field screen-
ing environment, for example, can influence the reliable detection of
morphological and agronomic characters conferring high temperature tol-
erance (Hall, 1992). Several parameters have been proposed as selection
indexes in breeding for heat tolerance and avoidance in rice. Some
important selection indexes used for heat tolerance and avoidance are
(i) Early morning flowering to escape heat damage and screening for high
temperature tolerant lines done at 38 C while 35 C can be used to
eliminate heat susceptible materials (Satake and Yoshida, 1978)
(ii) High pollen shedding (i.e., expressed as pollen number on the stigma)
(Mackill and Coffman, 1983; Prasad et al., 2006)
(iii) Pollen production in the anthers and high spikelet fertility for heat
tolerance during the reproductive phase (Prasad et al., 2006).
(iv) Grain weight heat susceptibility index [GWHSI=(grain weight at
optimum temperature-grain weight at high temperature)/grain weight
78 R. Wassmann et al.
Author's personal copy

at optimum temperature 100] to evaluate tolerance of rice to heat
stress (Zhu et al., 2005)
(v) Six hour high temperature exposure encompassing the peak anthesis
period for the flowering day to reduce the possibility of escape
(Jagadish et al., 2008)
(vi) Length of basal dehiscence could be used as morphological marker for
selecting high temperature tolerant genotypes (Matsui et al., 2005,
2007). They found out that the length of basal dehiscence was highly
correlated with the pollination viability under hot conditions. Further-
more, they observed that long basal dehiscence helps the pollen
grains to fall from theca into stigma, thereby increasing reliability of
pollination under hot and normal environmental conditions.
2.1.4.4. Genetics of heat tolerance Heat tolerance is controlled by not
only one major gene but several genes (Mackill, 1981; Maestri et al., 2002).
Mackill and Coffman (1983) reported that the genetic control of high pollen
shedding in rice is recessive and influenced by different genes. In contrast,
Yoshida et al. (1981) observed that most of the genetic variation for pollen
shedding is additive. Their results showed significant broad sense and
narrow sense heritabilities of 76 and 71%, respectively, while finding a
high correlation between spikelet fertility and pollen shedding.
QTL analysis, correlation and co-segregation approaches, and the use of
genetic stocks were most applicable in studying the genetic basis of heat
tolerance in cereals (Maestri et al., 2002). In rice, QTL mapping for heat
tolerance at grain-filling stage revealed three QTLs controlling the trait
(Zhu et al., 2005). These QTLs were detected on chromosomes 1, 4, and 7
with LOD scores of 8.16, 11.08, and 12.86, respectively (LOD stands for
logarithm of the odds, for example, LOD score of three means the odds are
10
3
/1 in favor of genetic linkage), and correspondingly explaining 8.9, 17.3,
and 13.5%, of the phenotypic variance. The QTL in chromosome 4 showed
no interaction with environment and epistatic effect, suggesting stable
expression over different environments and genetic backgrounds. The
QTLs on chromosomes 1 and 7, on the other hand, had significant GE
interactions. Moreover, eight pairs of QTLs with epistatic effects were
detected. Other QTL mapping studies designed to identify major QTLs
from known donors such as N22 into popular indica varieties are currently
underway at IRRI.
Traditional breeding methods comprise pedigree and bulk selection
based on morphological markers such as percent fertility. These approaches
have been successfully used in breeding for heat tolerance in other
crops (Hall, 1992) whereas IRRI breeding programs have focused on
other traits than heat tolerance. However, as the molecular genetic basis
of heat tolerance in rice is elucidated and QTLs are identified and suitable
markers developed, molecular breeding approaches are expected to be
Climate Change Affecting Rice Production 79
Author's personal copy

utilized for developing superior heat tolerant varieties more precisely and
expeditiously. A shuttle-breeding strategy was successfully used in develop-
ing rainfed lowland rice varieties in Eastern India while also facilitating the
exchange of breeding materials of diverse origin (Mallik et al., 2002). This
type of program is envisioned for validating the field performance of
promising breeding lines in hotspot areas while shortening the breeding
cycle. In field screening, the confounding effects of relative humidity on
heat-induced spikelet sterility (Weerakoon et al., 2008) also need to be
accounted for. Thus, it may be necessary to stratify the target breeding
environments into hot and humid versus hot and dry zones and tailor the
selection protocols accordingly. Also, incorporation of a heat tolerance
breeding objective into ideotype as well as intersubspecific heterosis breed-
ing programs for raising yield potential (Peng et al., 2008) could be adopted
as a strategy for increasing rice productivity and breaking the yield ceiling,
even under various climate change scenarios.
2.2. Drought
The recent IPCC Technical Paper on Climate Change and Water stated
with high confidence that ‘‘the negative impacts of future climate change on
freshwater systems are expected to outweigh the benefits’’ (Bates et al.,
2008). As compared to the current situation, we will see much more land
where the water stress will aggravate and only a small portion of the land
where the water stress situation will be alleviated. In spite of an increased
total water supply, the effects of increased precipitation variability and
seasonal runoff shifts, water quality, and flood risks are likely to prevail in
their impact on food production.
It has been shown that the production of rice, maize, and wheat has
declined in many parts of Asia in the past few decades, due to increasing
water stress, arising partly from increasing temperatures, increasing fre-
quency of El Nin
˜o events and reductions in the number of rainy days
(Aggarwal et al., 2000; Fischer et al., 2002; Tao et al., 2004). In turn, this
will decrease food security and increase vulnerability of poor rural farmers,
especially in the arid and semiarid tropics (Bates et al., 2008).
Because of its semiaquatic phylogenetic origin and the diversity of rice
ecosystems and growing conditions, current rice production systems rely on
ample water supply and thus, are more vulnerable to drought stress than
other cropping systems (O’Toole, 2004). Drought stress is the largest
constraint to rice production in the rainfed systems, affecting 10 million
ha of upland rice and over 13 million ha of rainfed lowland rice in Asia alone
(Pandey et al., 2007). At the whole plant level, soil water deficit is an
important environmental constraint influencing all the physiological pro-
cesses involved in plant growth and development. Drought is conceptually
80 R. Wassmann et al.
Author's personal copy

defined in terms of rainfall shortage compared to a normal average value in
the target region. However, drought occurrence and effects on rice pro-
ductivity depend more on rainfall distribution than on the total seasonal
rainfall. A typical example was given in a recent screening experiment
at IRRI during the wet season 2006, when seasonal rainfall exceeded
1000 mm, including a major typhoon (International name: Xangsane)
with around 320 mm rainfall in a single day. Yet, a short dry spell that
coincided with the flowering stage resulted in a dramatic decrease of grain
yield and harvest index, compared to the irrigated control (Serraj et al.,
2008). Beyond the search for global solutions to a generic ‘‘drought,’’ the
precise characterization of droughts in the target population of environ-
ments (TPEs) is a prerequisite for better understanding their consequences
on crop production (Heinemann et al., 2008).
2.2.1. The present situation of catastrophic, chronic,
and inherent droughts
Drought definitions depend on the disciplinary outlook, including meteo-
rological, hydrological, and agricultural perspectives. Agricultural drought
occurs when soil moisture is insufficient to meet crop water requirements,
resulting in yield losses. Depending on timing, duration, and severity, this
can result in catastrophic, chronic, or inherent drought stress, which would
require different coping mechanisms, adaptation strategies and breeding
objectives.
The 2002 drought in India could be described as a catastrophic event, as it
affected 55% of the country’s area and 300 million people. Rice production
declined by 20% from the inter-annual baseline trend (Pandey et al., 2007).
Similarly, the 2004 drought in Thailand affected over 8 million people in
almost all provinces. Severe droughts generally result in starvation and
impoverishment of the affected population, resulting in production losses
during years of complete crop failure, with dramatic socioeconomic conse-
quences on human populations (Pandey et al.,2007). Production losses to
drought of milder intensity, although not so alarming, can be substantial. The
average rice yield in rainfed eastern India during ‘‘normal’’ years still varies
between 2.0 and 2.5 tha
1
, far below achievable yield potentials. Chronic dry
spells of relatively short duration, can often result in substantial yield losses,
especially if they occur around flowering stage. In addition, drought risk
reduces productivity even during favorable years in drought-prone areas,
because farmers avoid investing in inputs when they fear crop loss. Inherent
drought is associated with the increasing problem of water scarcity, even in
traditionally irrigated areas, due to rising demand and competition for water
uses. This is, for instance the case in China, where the increasing shortage of
Climate Change Affecting Rice Production 81
Author's personal copy

water for rice production is a major concern, although rice production is
mostly irrigated (Pandey et al.,2007).
Increasing rice productivity in the drought-prone rainfed areas requires
adapted solutions and strategies in response to the different types of
droughts, based on precise characterization of the TPEs. With milder
chronic droughts being generally more frequent than the catastrophic
ones, overall crop productivity in rainfed areas would probably benefit
more from breeding for enhanced water productivity and resistance to the
chronic type of water deficits.
2.2.2. Interaction of drought and CO
2
on crop yield and
physiological responses
The potential impacts of increasing [CO
2
] on photosynthesis have been
well documented for many crops (e.g., Allen et al., 1994). Because soil water
availability is the most limiting environmental factor for crop growth
(Boyer, 1982), it is crucial to analyze the possible interactions of water
deficits and [CO
2
] upon major crops such as rice. If there is a fundamental
change in plant responses to soil water content, then plant growth under
climate changes associated with less precipitation might be either aggravated
or lessened as compared to what is expected using response functions
developed for current CO
2
levels.
Most of the carbon stored in the mature rice grains originates from CO
2
assimilation during the grain-filling period, with the flag leaf as the most
photosynthetically active, factors that lower the photosynthesis rate of the
flag leaf during this period could potentially limit grain yield. Baker et al.
(1997a) analyzed the growth and grain yield responses of rice to drought
stress under carbon dioxide concentration [CO
2
] enrichment. Rice (cv.
IR-72) was grown to maturity in plant growth chambers under naturally
sunlit, in atmospheric [CO
2
] of 350 and elevated (700 mmol CO
2
mol
1
air). The [CO
2
] enrichment increased plant growth, number of panicles per
plant and grain yield. Drought accelerated leaf senescence, reduced leaf area
and above-ground biomass and delayed crop ontogeny. The [CO
2
] enrich-
ment allowed 1–2 days more growth during drought-stress cycles. It was
concluded that in the absence of air temperature increases, future global
increases in [CO
2
] should promote rice growth and yield while providing a
modest reduction of near 10% in water use and so increase drought avoid-
ance (Baker et al., 1997a). Similarly, a recent study in wheat (Manderscheid
and Weigel, 2007) showed that CO
2
enrichment enhanced final biomass
and grain yield by less than 10% under well-watered conditions and by more
than 44% under drought-stress conditions, respectively. This indicated that
the increase in atmospheric CO
2
concentration will be likely to attenuate
the effects of drought stress on wheat grain yield.
The analysis of potential acclimation of rice photosynthesis to long-term
[CO
2
] growth treatments, by comparison of canopy photosynthesis rates
82 R. Wassmann et al.
Author's personal copy

across a wide range of short-term [CO
2
] showed essentially no acclimation
response (Baker et al., 1997b). Photosynthetic rate was found to be a
function of current short-term [CO
2
] rather than long-term [CO
2
] growth
treatment. Carbon dioxide enrichment significantly increased both canopy
net photosynthetic rate and water-use efficiency while reducing evapotrans-
piration by about 10%. This water saving under [CO
2
] enrichment allowed
photosynthesis to continue for about 1–2 days longer during drought in the
enriched compared with the ambient [CO
2
] control treatments (Baker et al.,
1997b). Widodo et al. (2003) have confirmed that elevated CO
2
delays the
effects of drought stress and accelerates recovery of rice leaf photosynthesis.
At elevated [CO
2
], midday leaf photosynthetic and concentrations of chlo-
rophyll (Chl) were increased, whereas total soluble protein (TSP) decreased,
compared with plants at ambient [CO
2
]. Furthermore, elevated [CO
2
]
increased midday leaf sucrose-phosphate synthase (SPS) activity and
enhanced midday leaf sucrose and starch accumulation during early repro-
ductive phases, but not during later reproductive phases. Water deficit
caused substantial decreases in midday photosynthesis and concentrations
of Chl and TSP, with concomitant reductions in photosynthetic primary
products and SPS activity. However, these drought-induced effects were
more severe for plants grown at ambient than at elevated [CO
2
], as the latter
ones were able to maintain leaf photosynthesis longer into the drought
period than plants grown at ambient [CO
2
]. In addition, leaf photosynthesis
recovered from water deficit more rapidly in the elevated [CO
2
] treatment.
It was concluded that in the absence of other potential climate stresses, rice
grown under future increases in atmospheric [CO
2
] may be better able to
tolerate drought situations (Widodo et al., 2003).
Similarly in wheat, Manderscheid and Weigel (2007) reported that CO
2
enrichment stimulated the green area index under drought stress and the
seasonal radiation absorption was only decreased by 16%. Radiation use
efficiency was reduced by drought and increased by CO
2
elevation and
the CO
2
effect was higher under drought (+60%) than under well-watered
conditions (+32%). Robredo et al. (2007) analyzed the impact of elevated
[CO
2
] on water relations, water use efficiency (WUE) and photosynthetic
gas exchange in barley (Hordeum vulgare L.) under wet and drying soil
conditions. They concluded that the improved water status of drought-
stressed plants grown at elevated CO
2
was the result of stomatal control
rather than of osmotic adjustment. Photosynthesis under drought was
maintained at higher rates for longer with elevated [CO
2
]. The reduction
of stomatal conductance and transpiration, and the enhancement of carbon
assimilation by elevated [CO
2
], increased instantaneous and whole plant
WUE in both irrigated and drought-stressed plants. Thus, the metabolism
of barley plants grown under elevated [CO
2
] and moderate or mild water
deficit conditions was benefited by increased photosynthesis and lower
transpiration (Robredo et al., 2007). Previous studies in soybean showed
Climate Change Affecting Rice Production 83
Author's personal copy

that elevated [CO
2
] decreased water loss rate and increased leaf area devel-
opment and photosynthetic rate under both well-watered and drought-
stressed conditions (Serraj et al., 1999). There was, however, no significant
effect of CO
2
concentration in the response relative to soil water content of
normalized leaf gas exchange and leaf area. This study also demonstrated
that drought response based on soil water content for transpiration, leaf area,
and photosynthesis provides an effective method for describing
the responses of the physiological processes to the available soil water,
independent of CO
2
concentration (Serraj et al., 1999).
2.2.3. Genetic basis of grain formation failure under drought
Although drought affects all stages of rice growth and development, water
stress during the flowering stage depresses grain formation much more than
drought at other reproductive stages (Boonjung and Fukai, 1996). There-
fore, screening for tolerance near flowering stage has been considered to be
more useful in breeding for improved drought resistance. The strong effects
of drought on grain yield are largely due to the reduction of spikelet fertility
and panicle exsertion. Several studies have found that reproductive devel-
opment from meiosis in the spore mother cells to fertilization and early seed
establishment was extremely sensitive to various stresses, including drought.
These stresses cause various structural and functional disruptions in repro-
ductive organs, leading to failure of fertilization or premature abortion of
the seed (Saini, 1997; Saini and Westgate, 2000). Drought can inhibit the
development of reproductive organs, such as the ovary (Saini et al., 1983)
and the pollen at meiosis stage (Saini, 1997); but it can also inhibit processes
such as anther dehiscence, pollen shedding, pollen germination, and fertili-
zation (Ekanayake et al., 1990;Satake and Yoshida, 1978).
The drought-induced inhibition of panicle exsertion has been identified
as a consequence of a decrease in peduncle elongation, which can usually
account for 70–75% spikelet sterility under water deficit (O’Toole and
Namuco, 1983). Drought stress slows down the peduncle elongation, and
re-watering can only partially restore elongation. Recent studies at IRRI
found that drought significantly delayed the peduncle elongation, trapped a
significant fraction of panicle within the flag leaf sheath due to the repression
of the expression of cell-wall invertase genes ( Ji et al., 2005). The spikelets
left inside the leaf sheath are usually sterile, resulting in a poor yield, which
indicates that peduncle elongation may play a major role in panicle exser-
tion and spikelet fertility under stress. Mutant studies showed that the cause
of spikelet sterility can be of two types: inhibition of starch accumulation in
pollen grains and failure of anther dehiscence and/or synchronization with
anthesis due to suspension of septum degradation and stomium breakage
(Zhu et al., 2004). If drought stress occurs during these processes, the
reproductive organs will be abnormal and damaged and then grain set will
be sterile. Liu et al. (2005) reported a significant difference in number of
84 R. Wassmann et al.
Author's personal copy

pollen grains between IR64 and Moroberekan in the four top rachis under
drought conditions. The variation in spikelet fertility between the geno-
types was mainly due to the difference in locule wall structure, and then to
variation of the number of pollen grains on stigma (Liu et al., 2005).
2.2.4. Genetic enhancement of drought-stress resistance
The success in breeding for improved drought resistance depends essentially
on the choice of parents, selection criteria and robustness of the managed
screening protocols. Successful breeding programs must have clear objec-
tives, namely to produce a cultivar that is superior to farmers’ varieties in a
particular TPE. The objectives of a screening system are to focus on the
TPEs and adaptation to major stress occurrence scenarios, and to minimize
field variability for detecting heritable differences in drought resistance.
Comparing several drought screening protocols in the upland or in drained
lowland paddies, Lafitte and Courtois (2002) found that intermittent stress,
imposed by withholding irrigation during the period bracketing the entire
flowering and grain-filling stages, is generally reliable for ranking cultivars’
performance under drought, similarly to stress targeted precisely at the
flowering period of individual cultivars.
Recent research findings at IRRI have demonstrated the feasibility of
direct selection for yield under drought (Kumar et al., 2008). Since yield
under stress is a function of yield potential, escape, and drought response, the
use of the Drought Resistance Index (DRI) can help to distinguish drought
resistance from escape and yield potential (Ouk et al., 2006) and therefore
further enhance the precision and reproducibility of drought screening.
While breeding for upland and aerobic rice has recently made significant
progress in developing new rice cultivars for water-short environments
(Bernier et al., 2008), the progress in rainfed lowlands has been relatively
slow. Most improved cultivars grown in drought-prone rainfed lowlands
were originally bred for irrigated conditions and were never selected for
drought tolerance (Kumar et al., 2008). Drought escape has been exploited
in the drought-prone areas of eastern India and Bangladesh, through short-
duration varieties, mainly of the aus germplasm group. But most of these
varieties are not necessarily drought resistant. The slow progress in the
genetic improvement of grain yield in the rainfed lowland was explained
by two major factors: the complexity of the target genotype environment
system and the insufficiency of genetic resources available to the breeding
programs (Cooper et al., 1999).
Large genetic variation exists within rice and its wild Oryza relatives for
performance under drought stress, but progress in developing improved
cultivars has been relatively slow. Many parental lines and donors have been
identified for drought resistance in upland (Atlin et al., 2006), but only a few
have been reported for the more extensive rainfed lowland system. The
identification of parental materials and development of new populations was
Climate Change Affecting Rice Production 85
Author's personal copy

a major target for the IRRI rainfed lowland breeding program in the 1990s,
focusing on the major target environments in eastern India and northeast
Thailand (Sarkarung and Pantuwan, 1999). Breeding populations were
developed in the backgrounds of Mahsuri, Safri17, and Sabita for eastern
India and KDML105 for northeast Thailand. An extensive G E study in
rainfed lowland by Wade et al. (1999) analyzed the interactions of 37 geno-
types across 36 environments in India, Bangladesh, Thailand, Indonesia, and
the Philippines from 1994 to 1997. Only a small group of genotypes were
stable across environments. The cultivar NSG19 was found to be adapted to
environments with rapid-onset late drought, whereas Sabita and KDML105
showed adaptation to environments with late maturity or recovery after
drought.
Stress-sensitive mega varieties are still widespread across South and
Southeast Asian rainfed rice production systems, including Swarna, Sambha
Mahsuri, IR36, IR64, BR11, and MTU 1010. These varieties are generally
preferred by farmers for their yield potential and quality traits are not
tolerant to drought. As they were bred for the irrigated ecosystem, these
varieties provide high yield in non-drought years, but they show a high-
yield reduction in mild to moderate drought years and collapse completely
in severe drought-stress years (Kumar et al., 2008).
In field experiments conducted at IRRI during the dry seasons of 2006–
2008, large scale field-managed drought screening has been focusing on the
confirmation of drought-resistant breeding lines and identification of new
potential donors of drought resistance within gene bank germplasm collec-
tions, molecular breeding lines, Oryza glaberrima introgression lines, hybrids,
and their parental lines (Serraj et al., 2008), in addition to mutants and
transgenic lines (Herve and Serraj, 2009).
2.2.5. Agronomic approaches to cope with less water
The cultivation of rice in flooded fields requires about 2500–3000 m
3
water
to produce 1 ton of rice grain versus around 1000 m
3
to produce 1 ton of
wheat grain. In Asia, more than 80% of the developed freshwater resources
are used for irrigation purposes, mostly for rice production. Thus, even small
savings of water due to a change in current practices will translate into a
significant bearing on reducing the total consumption of fresh water for rice
farming. By 2025, 15–20 million hectares of irrigated rice will experience
some degree of water scarcity (Bouman et al., 2007). Many rainfed areas are
already drought-prone under present climatic conditions and are likely to
experience more intense and more frequent drought events in the future.
Thus, water saving techniques are absolutely essential for sustaining—
and possibly increasing—future rice production under climate change. The
potentials and constraints of different water-saving approaches have recently
been discussed in detail within a review published in this journal (Bouman
86 R. Wassmann et al.
Author's personal copy

et al., 2007), so that this presentation here provides only a brief overview of
the available approaches and highlights a few aspects with specific relevance
to climate change adaptation.
The period of land preparation encompasses various options to save
water, namely lining of field channels, land leveling, improved tillage, and
bund preparation. Likewise, crop establishment can be optimized under
water scarcity by direct seeding which reduces turnaround time between
crops and may tap rainfall. Finally, the crop growth period offers essentially
three alternative management practices to save irrigation water: saturated
soil culture (SSC), alternate wetting and drying (AWD), and aerobic rice.
In SSC, the soil is kept as close to saturation as possible, thereby
decreasing seepage and percolation losses. A meta-analysis of field experi-
ments showed that water input decreased on average by 23% (range:
5–50%) as compared to continuously flooded check, with a nonsignificant
yield reduction of 6% on average (Bouman and Tuong, 2001). Figure 8
provides three examples from the Philippines indicating higher WUE
through SSC.
In AWD, irrigation water is applied in certain intervals leading to
episodes of non-flooded soil conditions in the fields. The intervals of non-
flooded periods can vary from 1 day to more than 10 days depending on the
specific management regime and soil/climate conditions. In almost all field
experiments, AWD resulted in slightly lower yields (see Fig. 8). However,
AWD is consistently increasing WUE, that is, the amount of grain produced
per unit of water input. The efficiency of AWD also depends on the soil
type. AWD is a mature technology for lowland rice areas with heavy soils
and shallow groundwater tables has been widely adopted in those areas in
China (Li and Baker, 2004). In loamy and sandy soils with deeper ground-
water(e.g., in Northern India) water inputs can be even reduced up to 50%,
but yield losses are generally high (more than 20%) as compared to flooding
(Sharma et al., 2002; Singh et al., 2002; Tabbal et al., 2002). AWD is also an
integral part of the System of Rice Intensification (SRI), an approach
developed in Madagascar and now intensively advocated in many
rice-growing countries (Uphoff, 2007).
Aerobic rice is a very distinct way of growing rice as compared to paddy
fields; in fact, it is grown like other cereals, such as wheat, in non-flooded,
non-saturated (aerobic) soil with supplementary irrigation. Growing aero-
bic rice eliminates the water losses that are typical for flooded rice (seepage,
percolation, and evaporation from the standing water layer). On the other
hand, it requires various adjustments to obtain high yields under non-
flooded conditions, namely special input-responsive rice cultivars adapted
to aerobic soils and new management practices. Field experiments at IRRI
indicated a wide range of yield losses (Fig. 8). Peng et al. (2006) attributed
these differences to cultivar effects and their specific performance in the dry
and wet seasons, but also indicated that the range of yield losses was higher
Climate Change Affecting Rice Production 87
Author's personal copy

when aerobic rice was grown over several consecutive seasons. In spite of
some encouraging evidence, e.g., aerobic varieties in Brazil with a yield
potential of up to 6 tons ha
1
(Pinheiro et al., 2006), the implementation of
aerobic rice in farmers’ fields still has to overcome several obstacles. Irre-
spective of the existing problems, research until now has synthesized
opportunities for further development of aerobic rice.
0
2
4
6
8
10
Flooded
AWD
Flooded
Flooded
AWD
Flooded
AWD
Flooded
AWD
AWD
Flooded
AWD
AWD
Flooded
AWD
AWD
Flooded
Flooded
Yield (t/ha)
0
1000
2000
3000
4000
Total water input (mm)
Yield
Total water input
<============Philippines=========><===China===><===India===>
(b)
0
2
4
6
8
10
Flooded
SSC
SSC
Flooded
SSC
Flooded
Flooded
aerobic
Flooded
aerobic
Flooded
aerobic
Flooded
aerobic
Flooded
aerobic
Yield (t/ha)
0
1000
2000
3000
4000
Total water input (mm)
Yield
Total water input
<=================Philippines================><====China===>
A
B
Figure 8 Yields and total water inputs under flooded conditions and water saving
techniques; (A) for saturated soil culture (data from Tabbal et al.,2002) and aerobic rice
(data from Bouman et al., 2005 and Yang et al., 2005); (B) for alternate wetting-drying
(data from Belder et al., 2004; Mishra et al., 1990; Tabbal et al., 2002).
88 R. Wassmann et al.
Author's personal copy

Irrigation can be perceived as a buffer against drought effects and thus, as
rendering some degree of resilience to irrigated rice production under
climate change. Between the 1960s and the turn of the century the irrigated
area in Asia doubled, but this development encompassed very different
irrigation systems (Table 2). Historically irrigation has developed in four
distinct but overlapping phases: (A) community irrigation, (B) river diver-
sion schemes, (C) storage dams, and (D) pumps for access and control of
surface and ground water (Barker and Molle, 2004). Community and
pumping systems can be found throughout Asia whereas the other types
are confined to specific hydrological conditions, that is, high water dis-
charge from large rivers and man made reservoirs for irrigation. One of the
decisive features to determine the buffer effect by a given irrigation type is
the respective size. Community systems typically have small catchments
and water storage capacities, so that rainfall deficits can hardly be attenuated
through these systems. In contrast, river diversion schemes have an
inherently larger catchment area, especially in the mega deltas, that will
compensate for local rainfall anomalies within a broader area. The buffer
effect of storage dams and pumping systems can be assessed as being
intermediate between community systems and river diversion schemes
(see details in Table 2).
Apart from size, the effectiveness of irrigation schemes to ensure water
supply under drought also depends on the current state of infrastructure.
Most community systems and storage dams are rather old and are often
dilapidated entailing high water losses in the canal/tube systems. The use of
pumps is becoming more and more popular in many rice-growing regions.
Pumps are nowadays affordable for many farmers and their use is extremely
flexible, but the scope of irrigation is only patchy due to limited capacity of
individual pumping units. Insofar, they may provide only limited cushion
against severe dry spells. As compared to other irrigation types, irrigation
schemes that divert water from large rivers, namely in deltaic regions,
represent the best cushion against droughts. Apart from having large and
heterogeneous catchments, many of these irrigation systems have extensive
canal systems with good accessibility throughout the delta as well as a
reliable hydro-technological infrastructure (e.g., sluices) to optimize water
supply. Rice production in the deltas of Mekong, Red River, Irrawaddy,
and Ganges–Brahmaputra is of outstanding importance for food security in
Vietnam, Myanmar and Bangladesh, respectively; the Mekong Delta is also
a major source of rice traded internationally. On the other hand, the deltaic
areas are exposed to high risks associated with climate change. Rice pro-
duction in the deltaic regions will directly be affected by sea level rise that
increase the risk of inundation (Wassmann et al., 2004). Insofar, the future
challenge for irrigation systems in deltaic regions may be primarily about the
prevention of salinity intrusion (see Section 2.3) and excessive flooding (see
Section 2.4) as opposed to compensating for dry spells.
Climate Change Affecting Rice Production 89
Author's personal copy

Table 2 Typology of irrigation systems (after Barker and Molle, 2004) and their potential role under climate change
(A) Community
systems
(B) River diversion
schemes (C) Large storage dams
(D) Pumps for access
and control of water
Historical
development
In most cases old
irrigation systems
(some several
centuries old); in
many cases
deteriorating
Old origin, but have
continuously been
upgraded over recent
decades
Most dams were
constructed from 1950s
to 1980s (with a peak in
the 1970s); recent
constructions in China
In semiarid regions
since the 1960s; now
increasingly popular
throughout
monsoon Asia
Geographic
distribution
Pervasive throughout
Asia
In major river deltas (e.g.,
Mekong, Chao Phraya,
and so on)
Scattered in effectively
every Asian country; in
many cases with
deteriorated water
transport systems
Pervasive throughout
Asia
Scale of
catchment/
irrigation
Typically small
catchment and
irrigation schemes
(<1000ha)
Very large catchment and
irrigation area
Varying in size; catchment
in upland areas and
irrigation in lowland
areas
Very small irrigation
(<1 ha) by
individual unit, but
frequently used
Buffer effect to
local/short-
term droughts
(plus and
minus)
LOW:
– Small catchments
– Low water storage
capacities
– Poor infrastructure
discriminates ‘‘end
of the pipe’’ farmers
in drought situations
HIGH:
+ Large and
heterogeneous
catchment
+ Extensive canal systems
with good accessibility
+ Hydro-technological
infrastructure
(e.g., sluices) to
optimize water supply
MODERATE:
+ Potential water storage
from wet to dry
season/year
+ Uplands often with high
heterogeneity in rainfall
– In most cases only
medium sized catchment
– Poor infrastructure
discriminates ‘‘end of the
MODERATE:
+ Very flexible use in
time and space
+ Pumping of
groundwater if
needed
+ Independent from
(delayed) policy
reaction to CC
90
Author's personal copy

– Risks for delta regions
due to sea level rise and
vulnerability to climate
extremes
pipe’’ farmers in drought
situations
– Only patchy
amelioration of
drought in landscape
– Constrains for poor
farmers due to
purchasing and
operating costs
Possible
Improvement
to cope
Climate
Change
impact
* Reduction of water
losses/canal lining
* Water diversion/
conjunctive use
* Temporary use of
groundwater
* Water pricing
* Greater equity
among water
recipients
* Micro-irrigation
* Innovative water
harvesting
* New sluices to reduce
salinity affects
* Micro-irrigation/
improved varieties/
crop rotations
* Basin-wide frameworks
for water allocation
* Reduction of water
losses/canal lining
* New reservoirs
* Trans basin diversion
* Improved dam
management
* Sectoral
re-allocation prioritizing
agriculture at drought
events
* Micro-irrigation/
improved varieties/crop
rotations
* Innovative water
harvesting
* Collective use of
groundwater by
several farmers
* Micro-irrigation
* Subsidies for
pumping in drought
situations
* Innovative water
harvesting
91
Author's personal copy

2.2.6. An integrated research strategy for drought resistance
improvement under climate change scenarios
The need for precise characterization of the drought-prone TPE has long
been emphasized, but this effort is yet to be done systematically, across the
drought-prone rice environments in South and Southeast Asia and Sub-
Saharan Africa taking into account the dynamics and risks of climate change.
Under future scenarios of climate change, simulation models can play a role
both in the characterization and in enhancing the precision and integration
of phenotyping either by linking model coefficients directly to or more
heuristically to guide integrated phenotyping approaches. Increased crop
yield and water productivity require the optimization of the physiological
processes involved in the initial critical stages of plant response to soil
drying, WUE and dehydration avoidance mechanisms (Serraj et al., 2008).
Overall, it is now well accepted that the complexity of the drought syn-
drome can only be tackled with a holistic approach integrating plant
breeding with physiological dissection of the resistance traits and molecular
genetic tools together with agronomical practices that lead to better conser-
vation and utilization of soil moisture and matching crop genotypes with
the environment. Some of the steps involved in this multidisciplinary
approach are described below:
(i) Define the target drought-prone environment(s), and identify the
predominant type(s) of drought stress and the rice varieties preferred
by farmers. Define the phenological, and morphological traits that
contribute substantially toward adaptation to drought stress(es) in
the target environment(s). A critical research aspect is dissecting the
interactions between drought, CO
2
and temperature.
(ii) Use simulation modeling and systems analysis to evaluate crop response
to the major drought patterns under variable CO
2
and temperature
scenarios, and assess the value of candidate physiological traits in the
target environment.
(iii) Develop and refine appropriate screening methodologies for charac-
terizing genetic stocks that could serve as donor parents for the traits of
interest.
(iv) Identify the genetic stocks for various putative, constitutive and induc-
ible traits in the germplasm and establish genetic correlations between
the traits of interest and the degree of adaptation to the targeted
drought stress.
(v) Harness functional genomics, transgenics and reverse genetics tools to
understand the genetic control of the relevant traits.
(vi) Use mapping populations and/or linkage disequilibrium mapping to
identify genetic markers and QTLs for traits that are critical for stress
resistance.
92 R. Wassmann et al.
Author's personal copy

(vii) Incorporate some of the components of relevant physiological traits
into various agronomic genetic backgrounds to provide a range of
materials with specific traits of interest for improving adaptation to
drought and abiotic stresses in locally adapted varieties.
2.3. Salinity
Increasing threat of salinity has become an essential issue linked to the
consequences of climate change. Increased CO
2
concentration per se may
not have the detrimental effects on crop growth but the indirect effect of
increased temperature on sea level rise, much larger areas of coastal wetlands
may be affected by flooding and salinity in the next 50–100 years (Allen
et al., 1996). A rise of 1000 mm sea level due to thermal expansion is
estimated for 3.58 C increase in temperature. This excludes the additional
expected increase in sea level due to melted ice leading to increased coastal
salinity and further yield reduction, even in previously favorable areas
(Manabe and Stouffer, 1994; Wassmann et al., 2004). Furthermore, greater
than half (55%) of total ground water is naturally saline (Ghassemi et al.,
1995). Secondary salinization, specifically due to the injudicious use of
water and fertilizers in irrigated agriculture could increase the percentage
of brackish ground water. The ground water table, if it rises and is brackish
in nature, becomes ruinous to most of the vegetation. Higher temperature
aggravates the situation by excessive deposition of salt on surface due to
capillary action which is extremely difficult to leach below the rooting zone.
The increased temperature will also disrupt weather patterns, leading to
more frequent occurrence of problems associated with floods, drought, and
salinity.
Rice can be categorized as a moderately salt sensitive crop with a
threshold electrical conductivity of 3 dS m
1
(Maas and Hoffman, 1977).
Recently, many new rice varieties have been developed worldwide with
enhanced level of tolerance both for saline and sodic soils. Rice is usually
monocropped in tropic and subtropic coastal areas during wet seasons due
to its adaptation to waterlogged environments while tolerating salinity up to
a certain extent. Soil sodicity is a different kind of problem soil, as a result of
high salt concentration and low infiltration rate and poor hydraulic con-
ductivity. This forces water stagnation on the soil surface which in turn do
not allow any crop except rice to survive. Hence, rice is recommended as
the first crop to be planted during reclamation of sodic soils. The high
adaptability of rice under salt-affected areas makes it the most preferred crop
for growing in these unfavorable environments.
At elevated CO
2
concentration, there is greater WUE, improved plant
water status and more rapid leaf production in the vegetative growth phase
Climate Change Affecting Rice Production 93
Author's personal copy

provided there is non-limiting supply of the nutrients (Ackerly et al., 1992;
Grashoff et al., 1995). In saline conditions, increased WUE potentially could
reduce the salt uptake by plant. Partial stomatal closure under such future
environmental conditions could be an ideal mechanism for salt tolerance
(Bowman and Strain, 1987; Rozema et al., 1991). Alternatively, high
temperature at the plant canopy level will increase transpiration by changing
the vapour pressure deficit at the leaf surface, accelerate ageing of the
foliage, and also shorten the growing season or grain-filling period which
is very critical for the grain yield (Kenny et al., 1993). Rising temperature
will accelerate the crop development for most of the cultivars that may lead
to a reduced water use over the shortened growth period, but also to a loss
of potential yield. Further studies related to shortening of growth duration
and amount of water transpired during high temperature with reference to
salt uptake is needed.
2.3.1. Mechanisms of salinity stress
There are several mechanisms operating for salt tolerance in crop plants of
which major ones are
Ionic balance: Ionic balance is a major contributor for the tolerance mech-
anism. Rice on exposure to salt stress in the soil, ions of the soluble salts,
specially Na
+
,K
+
, and Cl

, are generally taken up along with the water
uptake through transpirational stream. For normal functioning of the
cells, high K
+
/Na
+
ratio is essential which is usually the case under
non-salt stress conditions. However under salt stress environment, rice
intakes excessive amount of Na
+
as cheap cation at the cost of energy
consuming uptake of K
+
and Ca
2+
. Higher passive uptake and increased
load of Na
+
in the xylem ultimately enters in the tissues/cells to disrupt
the physiological and biochemical activities. This accumulation leads to
disturbed Na
+
/K
+
ratio with toxic levels of Na
+
in the plant cells which
also impairs the enzymatic activity inside the cell leading to the ultimate
death of cell, tissue or the organ (Flowers and Yeo, 1981; Yeo and
Flowers, 1983; Yeo et al., 1990). Rice can tolerate 50–100 mM Na
+
in
cytosol, beyond which either the cell has to further sequester the Na
+
to
tonoplast or cell membrane through antiporters otherwise the cell suc-
cumbs to high salt concentration. Therefore, different mechanisms of
ionic control through partitioning are seen. Mainly two mechanisms are
known for Na
+
entry into the root cell cytosol. Either, it may be through
cation channels or transporters. It has been shown in different systems that
high affinity K
+
transporters (HKT) act as low affinity Na
+
transporters
facilitating the entry of Na
+
into the root cells under high salinity stress.
Further, Na
+
may also enter root xylem stream through apoplastic path-
ways as shown in rice by Yadav et al. (1996).
94 R. Wassmann et al.
Author's personal copy

Compartmentation: Many studies have documented the beneficial effects of
sodium compartmentation in the cells, tissues, or organs in the plant
system. In order to adapt to the changing environment and to minimize
the deteriorating effects, precise regulation of ion transport system in the
plant at cell, tissue, or whole plant level is critical for salt tolerance. Some
of the mechanisms occurring in the plants to maintain desirable K
+
/Na
+
ratios in the cytosol include (i) regulation of K
+
uptake and/or prevention
of Na
+
entry (ii) efflux of Na
+
from the cell, and (iii) utilization of Na
+
for
osmotic adjustment. Osmotic regulation is maintained either by Na
+
compartmentation into the vacuole or by the biosynthesis and accumula-
tion of compatible solutes (Sharma and Singh, 2008). This is called cell
level compartmentation. However, specific plant tissue or organ is aimed
to store the toxic ions that can be sacrificed by active metabolic activity.
Plants usually deposit the excess toxic ions like Na
+
in their old leaves and
leaf sheaths because they are easy to sacrifice after rendering them inactive
(Yeo and Flowers, 1983; Yeo et al., 1990).
Organic compatible osmolytes: Besides accumulation of ions for osmotic
adjustment plants also synthesize organic osmolytes to help in maintaining
water uptake and cell turgor under osmotic stress situations. These
osmolytes are localized in cytoplasm, and the inorganic ions such as
Na
+
and Cl

are preferentially sequestered into vacuole, thus leading to
the turgor maintenance for the cell under osmotic stress (Bohnert et al.,
1995; Flowers et al., 1977). A range of osmotic solutes namely proline,
betaine, polyols, sugar alcohols, and soluble sugars has been reported in
different plants upon their exposure to salt and water stress conditions.
Glycine betaine and trehalose act as osmoprotectants by stabilizing qua-
ternary structures of proteins and highly ordered states of membranes.
Mannitol serves as free radicle scavenger. Proline serves as a storage sink
for carbon and nitrogen and a free radicle scavenger. Due to their proper-
ties, these organic osmolytes are known a osmoprotectants (Bohnert and
Jensen, 1996; Chen and Murata, 2000).
Oxidative stress management: Under salinity stress, the accumulation of
reactive oxygen species (ROS) including superoxide radicals, H
2
O
2
,
and hydroxyl radicals has been termed as an important cause of damage
to the plant cell (Apse et al., 2003). Alleviation of these oxidative stresses
reduces the cell level damage and enhances the level of salt tolerance. The
tolerant plants produce more antioxidants like ascorbic acid and reduce
glutathione and various reactive oxygen scavenging enzymes than the
sensitive plants. Production of stress proteins as well as the accumulation
of compatible osmolytes has been reported which probably detoxify the
plants by scavenging reactive oxygen specien or preventing them from
damaging cellular structures (Apse et al., 2003;Ismail et al., 2007; Moradi
and Ismail, 2007). Plants with high activity of such detoxifying enzymes
will be naturally selected for future climates.
Climate Change Affecting Rice Production 95
Author's personal copy

2.3.2. Adaptive mechanisms for salinity tolerance
With the projected increase in high temperature, the rice genotypes in salt-
affected soils will have to adapt to avoid yield losses. Salinity tolerance is
important both at seedling and reproductive stage under high temperature
regimes. High evapotranspirational demands due to increased temperature
will favor the plants which can withstand the higher accumulation of salt
under salt-stress environment. This would be relevant to the tropical and
subtropical areas but more so to salt-stressed arid and subarid regions where
RH is lower than usual. Pyramiding genes/QTLs for salinity tolerance and
heat tolerance using marker-assisted breeding would be the ideal choice.
There are existing landraces which can withstand very high level of salt
tolerance and could be a good candidate for high temperature and salt
affected regions but inherently they are poor yielder. Although salinity
tolerant genotypes are available in the improved background considering
the future climate projections, salinity tolerance has to be further enhanced.
This could be achieved by pyramiding of the component mechanisms for
salinity tolerance like development of good excluder with better tissue
tolerance. For example, Na
+
entry in cytosol is restricted or minimized
through root cells, it will reduce transportation of toxic ions to shoots from
the roots, thereby lowering the salt load on to the plant system. Tissue
tolerance reflects the capacity of the genotype to withhold salt load and
maintaining its high photosynthetic activity (Flowers et al., 1985; Yeo and
Flowers, 1983, 1986; Yeo et al., 1990). Developing genotypes with different
sodium transporters that could provide the needed ion homeostasis during
salt stress opens the possibility of engineering crop plants with improved salt
tolerance. This is possible by enhanced vacuolar H
+
-pumping to provide
additional driving force for vacuolar sodium accumulation via the vacuolar
Na
+
/H
+
antiporter. This has been demonstrated in transgenic tomato plants
by overexpressing AtNHX1, the A. thaliana vacuolar Na
+
/H
+
antiporter
(Zhang and Blumwald, 2001; Zhang et al., 2001) and also in rice using the
rice homolog OsNHX1 (Fukuda et al., 2004).
Coastal rice ecosystems usually receive heavy rainfall during the wet
season. This may coincide with strong sea disturbances, inundating the
coasts because of high tides. Due to combined high rainfall and high tide,
the rice crop in the coastal areas experiences submergence with moderately
saline water, specifically during early crop growth. With the projected
seawater rise, such saline water inundation in the coastal areas would be
more frequent in the future. Therefore, initial 5–6 weeks are more crucial
for the survival of the plants. To cope with this companion stress problem—
salinity and submergence, rice plants need to have tolerance to both stresses.
The major QTL for the submergence tolerance in rice has already been
identified (Xu and Mackill, 1996; Xu et al., 2000) and the technique for
transferring the gene for submergence tolerance (Sub1) in different rice
96 R. Wassmann et al.
Author's personal copy

varieties through MAS has already been tested successfully (Neeraja et al.,
2007). Therefore it seems possible to develop salinity and submergence—
dual tolerant rice varieties. Ideally, a rice variety for salt stressed environ-
ments should have heat, salinity, and submergence tolerance to perform
sustainability in future changing climates.
2.4. Submergence
Submergence is an important abiotic stress affecting about 10–15 million ha
of rice fields in South and South East Asia causing yield losses estimated to
US $1B every year (Dey and Upadhyaya, 1996). This number is anticipated
to increase considerably in the future given the increase in seawater level, as
well as an increase in frequencies and intensities of flooding caused by
extreme weather events (Bates et al., 2008).
Although a semiaquatic plant, rice is generally intolerant of complete
submergence and plants die within few days when completely submerged.
This is also the case for deep water rice that escapes complete submergence
by rapid internode elongation that pushes the plants above the water surface
where it has access to oxygen and light to resume the mitochondrial
oxidative pathway and photosynthesis. There are, however, few varieties
that are tolerant to complete submergence capable of surviving under water
for about 14 days and to recover after the water recedes (Fig. 9). Tolerant
rice varieties have been identified already in the 1970s (Vergara and
Mazaredo, 1975) and have been used as donors of tolerance by breeders,
and studies on the tolerance mechanisms ever since. The most widely used
variety is FR13A, a tall, photoperiod-sensitive variety of the aus-type rice
from India. Other tolerant varieties are Kurkarrupan and Goda Heenati
from Sri Lanka. The chromosomal region conferring most of the tolerance
in FR13A, designated submergence 1 (Sub1), has been mapped to Chr. 9 by
independent groups (Nandi et al., 1997; Toojinda et al., 2003; Xu and
Mackill, 1996), and the Sub1 locus has recently been fine mapped and
sequenced in an FR13A-derived tolerant line (Xu et al., 2006). The infor-
mation on the genes located in the Sub1 locus now facilitates in-depth
analyses of the molecular and physiological tolerance mechanisms, and,
more importantly, triggered a breakthrough in marker-assisted breeding of
submergence tolerant rice varieties (for a time lapse series video visit http://
www.irri.org/timelapse.asp).
2.4.1. Physiology and molecular biology of submergence tolerance
The hormonal control and physiological basis of submergence tolerance and
submergence escape (deep water rice) have been studied in detail and
the data have recently been summarized in several excellent reviews
Climate Change Affecting Rice Production 97
Author's personal copy

(Bailey-Serres and Voesenek, 2008; Fukao and Bailey-Serres, 2008; Sarkar
et al., 2006). The major difference between the two responses to submer-
gence is that internode elongation is induced in deep water rice, whereas
cell elongation is suppressed in submergence tolerant rice. Of central
importance to both, submergence escape and tolerance, is therefore the
regulation of energy providing processes. Under submergence, plants are
exposed to low oxygen conditions and the final electron acceptor O
2
in the
electron transport chain in mitochondria is limited. Plants therefore need to
recycle NADH via an alternative pathway to maintain glycolysis. This is
mainly achieved by ethanolic fermentation converting pyruvate to ethanol
which regenerates one molecule of NAD
+
. This is transiently preceded by
conversion of pyruvate to lactate leading to a drop in cellular pH and
regeneration of one NAD
+
molecule. Whereas ethanol is benign since it
can diffuse out of the cell, the formation of acetaldehyde as a toxic interme-
diate is problematic. Detoxification of acetaldehyde, probably by the mito-
chondrial aldehyde dehydrogenase OsAdh2 (Nakazono et al., 2000), is
therefore important to avoid cell death under prolonged submergence.
Several other cellular processes are altered under low oxygen conditions
and the interested reader might be referred to the reviews cited above for
further details.
Given the poor energy (ATP) production of the anaerobic pathways
(2–4 mol ATP versus 30–36 mol ATP under aerobic conditions), starch
reserves are rapidly depleted. Physiological studies of a submergence toler-
ant near isogenic Sub1 line (M202-Sub1) showed that tolerance is associated
with a significantly higher transcript level and in vitro activity of key enzymes
of the ethanolic fermentation pathway (pyruvate decarboxylase, PDC, and
alcohol dehydrogenase, ADH), in conjunction with delayed starch degra-
dation and maintenance of a higher level of soluble sugars until 14 days of
submergence (Fukao et al., 2006). At the same time, submergence tolerant
plants show less elongation under submergence and therefore require less
energy. Suppression of cell elongation has been associated with a lower
expression of cell wall loosening expansion genes in the Sub1 near isogenic
lines (Fukao et al., 2006). In summary, these data suggest that Sub1 confers
tolerance via an optimized maintenance metabolism and suppression of the
energy consuming escape response. This enables plants to survive under
water for about 14 days and to retain sufficient carbohydrate CH reserves for
regeneration of growth once the water recedes (Fig. 9).
The above outlined processes are mainly controlled by the phytohor-
mone ethylene and a fine balance of the antagonistic hormones, that is
gibberellic acid (GA) and abscisic acid (ABA). Both, ethylene and GA
stimulate cell division and cell elongation, whereas ABA acts in an antago-
nistic way and is rapidly degraded under submergence (Das et al., 2005; Ella
et al., 2003; Saika et al., 2007; for review see Fukao and Bailey-Serres, 2008).
Sequencing of the Sub1 locus on Chr. 9 recently revealed the presence of
98 R. Wassmann et al.
Author's personal copy

three ethylene-responsive transcription factor (ERF) genes (Sub1A,Sub1B,
and Sub1C) and the Sub1A-1 allele has been identified as the major deter-
minant of tolerance (Xu et al., 2006). Interestingly, the Sub1A gene is absent
from all analyzed japonica varieties, including the Nipponbare reference
genome, and located on ‘‘chromosome unknown’’ in the indica reference
genome of 93–11. This finding shows the limitations of the current refer-
ence genomes and the importance of sequencing major QTLs in the
respective donor parent even when obvious candidate genes are present in
the syntenic region in Nipponbare. Detailed sequence and expression
analyses of the three ERF genes revealed tolerant-specific alleles and expres-
sion pattern for Sub1A and Sub1C, but not for Sub1B. In general, high
Sub1A and low Sub1C expression is observed in tolerant varieties, whereas
low Sub1A and high Sub1C expression is detected in intolerant varieties
(Xu et al., 2006). In addition, both genes carry characteristic single nucleo-
tide polymorphism (SNPs) that created a putative kinase phosphorylation
site in Sub1A-1 and mutated a putative phosphorylation site in Sub1C-1.
These SNPs are now being targeted by allele specific markers used for
molecular breeding (see below). Although the function of the tolerant
specific Sub1C-1 allele remains to be finally clarified by transgenic
approaches, gene expression analyses in a range of different tolerant and
intolerant rice varieties suggest that this gene is not a major determinant of
tolerance (Septiningsih et al., 2008; Dang et al., manuscript in preparation).
In contrast, it was shown that over expression of Sub1A-1 in an intolerant
variety (Liaogeng) that naturally lacks the Sub1A genes, confers tolerance by
suppressing elongation growth under submergence (Xu et al., 2006). It was
further shown that Sub1A is induced by ethylene, but not by GA treatment.
Samba-Sub1
Samba
Samba-Sub1
IR64-Sub1
IR49830 (Sub1 )
IR64
IR42
IR64
IR64-Sub1
Samba-Sub1
IR49830 (Sub1)
Samba
IR64
IR64-Sub1 IR49830 (Sub1)
IR42
IR64-Sub1
IR64
IR49830 (Sub1)
IR49830 (Sub1)
IR42
Samba
IR42
Samba
Figure 9 New Sub1 lines after 17 days submergence in field at IRRI.
Climate Change Affecting Rice Production 99
Author's personal copy

In summary, these data suggest that Sub1A is an upstream regulator that acts
as a suppressor of the ethylene induced escape response.
2.4.2. Molecular breeding of submergence tolerant rice varieties
Sub1 is an exceptionally strong QTL that shows a large effect in diverse
genetic backgrounds and environments. This indicates that Sub1 acts far
upstream in the stress response pathway and that the factors interacting with
Sub1 are highly conserved in all target varieties. However, slight differences
in tolerance levels are observed between Sub1-introgression lines
(Septiningsih et al., 2008) suggesting the existence of modifying factors or
additional tolerance genes (QTLs) with small effects.
Although submergence tolerant breeding lines were developed already
in the 1980s they were never adopted by farmers since they were not locally
adapted and did not meet farmers’ and consumers’ expectations on grain
quality (Mackill, 2006). A novel marker-assisted backcrossing (MAB)
approach was therefore developed that facilitate introgression of Sub1 into
the background of widely grown rice varieties, so-called mega varieties. On
the basis of the Sub1 sequence information, PCR-based allele specific
Sub1A and Sub1C markers (foreground markers) were developed that
facilitate the distinction of the tolerant and intolerant Sub1 haplotype
(Neeraja et al., 2007; Septiningsih et al., 2008; Dang et al., manuscript in
preparation). These markers are now routinely being used in conjunction
with Sub1 flanking and background markers. Background markers are being
used to restore, as much as possible, the genetic background of the recipient
parent and to remove undesirable additional introgressions from the Sub1
donor. Flanking markers are used to select for double cross over plants
upstream and downstream of Sub1 thereby minimizing the size of the Sub1
introgression (Fig. 10). Flanking and background markers, both, need to be
developed for each individual cross whereas Sub1 foreground markers can
be used for most crosses. With this new technique, submergence tolerant
plants can be developed by two to three backcrosses (BC
2
F
3
or BC
3
F
2
)to
the recipient mega variety (Septiningsih et al., 2008). The resulting Sub1
varieties are indistinguishable from the original intolerant variety with
respect to yield, grain quality and other desirable agronomic traits.
The main advantage of using mega varieties as recipient parent is that
farmers’ and consumers’ preferred traits present in these varieties are pre-
served, and the risk of introducing undesirable traits is considerably reduced.
Indeed it is being discussed if Sub1 versions of mega varieties can enter into
an accelerated national release pipeline to speed up out-scaling for the
benefit of farmers in submergence-prone areas. Sub1 versions of six impor-
tant rice varieties (IR64, Swarna, BR11, TDK1, Samba Mahsuri, and
CR1009; Septiningsih et al., 2008) have been developed, and Swarna-Sub1
has already been tested by national institutes in more than seven Asian
countries. In parallel, management options and fertilizer recommendations
100 R. Wassmann et al.
Author's personal copy

are being developed and tested in collaboration with national agricultural
institutes (Ella and Ismail, 2006). So far, Sub1 varieties performed well in
almost all trials and data from field experiments in 2007 in India with natural
flooding events between 10 and 30 days showed a 36% average yield advan-
tage of Swarna-Sub1 over the intolerant original Swarna variety (IRRI,
unpublished data).
2.4.3. Moving beyond Sub1
A germplasm screening has been conducted at IRRI to identify novel
sources of submergence tolerance distinct from Sub1. The Sub1 haplotype
and submergence tolerance level of over 200 rice accessions has been
determined revealing few tolerant accessions with the intolerant Sub1
haplotype (Sub1A-2,Sub1C-2). However, subsequent gene expression
analyses revealed unexpectedly high expression of Sub1A-2 in tolerant
1 2 3 4 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12
Progeny plant with target QTLs and
background introgressions from donor
Local variety with pyramided QTLs
and restored genetic background
F1 generation
X
1 2 3 4 5 6 7 8 9 10 11 12
1
2
Backcross (BC) to local variety and
marker selection starting in BC1F1
Tolerant donor Intolerant local variety
1 2 3 4 5 6 7 8 9 10 11 12
1
2
2nd (and 3rd) BC to local variety,
marker selection, 1–2 x selfing
1
2
Chr.
Final product
Figure 10 Pyramiding of stress tolerance QTL(s) by marker-assisted backcrossing.
A tolerant donor variety carrying one or two hypothetical target QTLs (black squares
with white numbers) located on a given rice chromosome (grey bars) is crossed to an
intolerant recipient parent, e.g., a locally adapted rice cultivar. Three types of molecular
markers are applied earliest in the first back cross (BC) generation to select for plants
carrying the target QTLs in the genetic background of the recipient parent: QTL-specific
foreground markers (black arrows), flanking markers to select for plants with double cross
over (grey arrows), and background markers on all chromosomes with ~5 Mb spacing
(triangles) to select against the genetic background of the donor parent. BC
2
F
3
or BC
3
F
2
progenies are almost identical to the original recipient variety but are tolerant.
Climate Change Affecting Rice Production 101
Author's personal copy

accessions, in contrast to low Sub1A-2 expression in intolerant accessions
(Dang et al., manuscript in preparation). These data suggest that high
expression of Sub1A, regardless of the specific allele, is sufficient to confer
at least some level of tolerance. In-depth analyses of the Sub1A-1 and
Sub1A-2 promoter regions are now ongoing and will reveal the regulatory
factors acting upstream of Sub1A (N. Singh, IRRI, unpublished data).
3. Comparative Assessment of Rice Versus
Other Crops (In Terms of Vulnerability
and Adaptation Options)
Rice is a C
3
grass that evolved in semiaquatic, low-radiation habitats
and is currently grown in wider range of environments from humid tropics
to arid and semiarid conditions and even to temperate zones. As such, it
carries a peculiar range of adaptations to existing and changing environ-
ments compared with other crop species. This broader adaptation will make
rice more amenable for manipulation to adjust to climate changes as a
consequence of global warming. However, to cope with these changes,
adjustments will be necessary both in breeding strategies to develop suitable
and more robust varieties, as well as in management strategies.
3.1. Advantages/disadvantages in warmer climates
As discussed in Section 2.1, especially rice is sensitive to heat stress during
reproductive development. Consequently, the currently available varieties
are not fitting for future climates, particularly in areas where striking shifts in
either or both night and day temperatures are expected. These conditions
could endure substantial reduction and alternation in rice growth and
development. Accelerated development during reproductive stage for
example, will shorten the duration of grain filling, reducing grain yield in
some cases, as observed for other crop species (Hall et al., 1997). Besides,
rice is grown under climatic and socioeconomic conditions that differ from
other major crop species such as maize and wheat. The unique feature of
growing rice in flooded soils (ca. 90%), and mostly being confined to lower
latitudes (30 N and 30 S), may suggest that rice will probably be subjected
to different challenges as a consequent of global warming. However, the
overall effects of heat stress on rice could be of lesser impacts under certain
circumstances, (1) in areas where sufficient good quality water is available,
(2) in drier environments where aerial humidity is low to promote evapo-
rative cooling, and (3) given that new high-yielding varieties were devel-
oped that can maintain high stomatal and hydraulic conductance to
maintain transpiration in hotter climates to cool sensitive tissues and organs.
102 R. Wassmann et al.
Author's personal copy

The degree of high temperature damage depends to a large extent on the
crop species and stage of development. Generally, high soil temperatures
can reduce the required time for emergence and crop establishment, but
with large variation in the maximum threshed between warm-season and
cool-season annuals. For example, the threshold maximum seed zone
temperature for cowpea is about 37 C, but only 25–33 C for lettuce.
High temperature damage during crop establishment in rice could be
avoided by transplanting in standing water in hotter climates to mitigate
the effects of hotter dry soil in the root zone experienced with dry land
crops. Under such conditions, transplanting will be a better option than
direct seeding. However, for direct seeding systems, varieties that germinate
under water (Ismail et al., 2008) may be useful in areas where surface soils
become hot during crop establishment, as a shallow water film or even
water logging will mitigate this heat effect during germination.
During the vegetative stage, high day temperatures can damage the com-
ponents of leaf photosynthesis, particularly those of photosystem II, as well as
membrane properties (Ismail and Hall, 1999). Studies comparing responses to
heat in contrasting species indicated that photosystem II of wheat, a cool season
species, is more sensitive to heat stress than photosystem II of rice and pearl
millet, which are adapted to higher temperatures (Al-Khatib and Paulsen,
1999). In extreme cases, heat stress can cause mortality, but with large variation
depending on species. For instance, temperatures above 35 C for sufficient
duration are lethal to pea, whereas cowpea can produce substantial biomass
when grown in one of the hottest crop production environments (maximum
shelter temperature of 50 C), although its vegetative development may
exhibit some abnormalities. The strong ability of some rice genotypes to
undergo evaporative cooling will be advantageous under such conditions,
provided that sufficient high quality irrigation water is available with sufficient
vapor pressure deficit between the canopy and air to drive the transpiration
process and enhance cooling of the canopy.
Reproductive development of many crops is more sensitive to heat stress
than vegetative growth (Hall, 1992, 1993). Here we will briefly review the
current understanding of the responses to heat stress in cowpea, one of the
most hardy crop species adapted to dry and hot environments, since ample
information is available that might have some implications for other systems
such as in rice. High temperature seems to cause relatively less damage to
cowpea during vegetative growth, but more so during reproductive devel-
opment, and the damage is greater when stress occurs during the night than
during the day, which is similar to the observations made on rice (Peng et al.,
2004). Being mostly indeterminate, the effects also vary with the stage of
development of specific reproductive structures in cowpea. Heat stress can
negatively impact floral bud development, flower development, pod set, grain
filling and even grain quality, and these responses will be reviewed in brief.
Climate Change Affecting Rice Production 103
Author's personal copy

Floral bud development is greatly suppressed or completely hindered by
heat stress, with consequent inhibition of flower production. Two weeks or
more of consecutive or interrupted hot nights during the first month after
germination can cause this damage (Ahmed and Hall, 1993). This suppres-
sion occurs under long days but not under short days in the field, and is
dependent on light quality. Floral buds were not suppressed in long-day
high night temperature conditions when light with high red/far-red ratio of
about 1.9 was used in growth chambers, but pod set was low. However,
when growth chambers were used with lighting systems with a red/far-red
ratio of 1.3–1.6, floral bud suppression was similar to what seen under long-
day high night temperatures in the field, where sunlight has a red/far-red
ratio of about 1.2. These findings caution against the use of controlled
conditions with artificial lighting systems, as it can result in either artifacts
or methodological advantages when studying responses to heat stress.
Extreme prudence should be taken when setting these conditions. In view
of these effects, further studies are needed to elucidate the interactive effects
of light quality and duration with high temperature during the early stages of
panicle development in rice. However, these effects might be of lesser
significance if the developing rice panicles were kept closer to floodwater
in paddy fields during early development.
Flower development in cowpea is also sensitive to high temperature,
with the sensitive stage occurring at about 9–7 days before anthesis (Ahmed
et al., 1992; Warrag and Hall, 1984), which is after meiosis and coincides
with the release of pollen microspores from the tetrads. High night temper-
ature at this stage causes premature degeneration of the tapetal layer that
provides nutrients to developing pollen, resulting in infertile pollen and
even hinders anther dehiscence in some cowpea genotypes. These damages
also inhibit transport of proline from the tapetal layer to developing pollen
grains (Mutters et al., 1989a). The association between genetic differences in
sensitivity to heat stress and rapid leakage of electrolytes from tissues sub-
jected to high temperature observed in cowpea (Ismail and Hall, 1999) may
suggest that, this heat-induced malfunction of cellular membranes could
impact other processes such as pollen development.
Subjecting cowpea shoot to moderately high night temperature can
damage pod set (Warrag and Hall, 1984), however, much hotter day
temperatures did not, and reciprocal artificial pollinations between plants
grown under high and optimal night temperatures indicated the low pod set
was caused by male sterility while the pistils did not appear to be affected,
which is similar to observations made on cereals, as wheat (Saini and
Aspinall, 1982) and rice (Yoshida et al., 1981). This effect was also demon-
strated in the field using enclosure systems (Nielsen and Hall, 1985). The
injury was later demonstrated to occur during the last 6h of the night, where
plants subjected to high temperature during this period exhibited substantial
increase in pollen sterility; but not when plants were subjected to high
104 R. Wassmann et al.
Author's personal copy

temperature during the first 6h of the night (Mutters and Hall, 1992),
suggesting that specific heat sensitive processes during pollen development
occur in the late night period or at predawn when temperatures are the
coolest and are probably under circadian control. These effects were also
found to be more severe under longer days and are perhaps phytochrome-
mediated (Mutters et al., 1989b). These findings might have some relevance
to rice, where cultivars that flower earlier in the morning (Sheehy et al.,
2005; Yoshida et al., 1981) are expected to be more tolerant to heat stress,
possibly by completing these sensitive processes earlier, during the cooler
predawn period. Heat stress also causes embryo abortion resulting in fewer
seeds per pod. High day and high night temperatures as well as other stresses,
such as drought, reduce the number of ovules that produce seeds resulting in
fewer seeds per pod. Grains produced under high temperature also can have
asymmetrically twisted cotyledons (Warrag and Hall, 1984) with brown
seed coat discoloration in some cultivars, which reduces the grain market
value. Whether similar effects on grain quality could be experienced in rice
remain to be seen.
The accelerated reproductive development under night-time heat stress
may negatively influence productivity. Under the cool nights of subtropical
California (min. temperatures of 16 C), individual pods of cowpea took
21 days from anthesis to mature dry pod, but only 14 days when the same
cultivar was grown under higher night temperatures of the tropics (min.
temperatures of 26 C). This rapid pod development may increase the
extent of embryo abortion and result in smaller grains. The more rapid
development of individual grains also shortens the overall reproductive
period, causing lower grain yields of cowpea cultivars grown with optimal
management in tropics than in the subtropics (Hall et al., 1997). Apart from
the effect of solar radiation, low night temperatures might partially explain
why the maximum grain yield of warm season crops, such as rice, is usually
higher in the subtropics and middle latitudes. In cowpea, evidence for heat-
induced yield reduction was demonstrated under natural farmers’ fields
using a set of cultivars with similar genetic backgrounds, evaluated under
optimal management over eight environments contrasting in temperature
regimes, but with similar high levels of solar radiation (Ismail and Hall,
1998), to provide a more realistic evaluation of heat stress effects. Grain
yield was negatively correlated with mean minimum night temperatures
during the 3-week period beginning 1 week before first flowering. For
minimum night temperatures greater than 16.5 C grain yield decreased by
14% per C, associated with a similar decrease (12% per C) in number of
pods per peduncle, but only a small decrease (6% per C) in shoot biomass
production. This confirms the earlier observations that effects of heat stress
are more detrimental on reproductive development in cowpea, as was also
observed in rice (Yoshida et al., 1981). In fact, sensitive varieties that showed
complete suppression of reproductive development were very vigorous
Climate Change Affecting Rice Production 105
Author's personal copy

under field conditions, and a system was proposed involving the use of
sensitive cowpea varieties as cover crops in hot environments. In rice,
enhanced male sterility will be useful for hybrid seed production.
Whether incorporating heat tolerance into crop plants will have any
negative consequences on agronomic or quality traits should also be con-
sidered carefully. For example, incorporating heat tolerance in cowpea
resulted in more compact genotypes, and this becomes more apparent
with increasing temperature during the growing season. This may require
new management strategies to avoid reduction in yield under field condi-
tions, such as adjusting the planting density (Ismail and Hall, 2000), as was
also reported in rice (Baloch et al., 2006). Apparently, heat stress could have
variable consequences during different developmental stages of crop plants,
with strong interaction in some cases, with other factors such as photope-
riod and light quality. Whether similar responses are experienced by rice
awaits further studies.
3.2. Advantages/disadvantages under worsening
water stress
Global warming is expected to impact the extent and severity of other
environmental stresses such as drought, salinity, and frequency of storms
and floods. Varieties that withstand the consequent high temperatures may
also need to encompass tolerances of other stresses relevant to particular
areas or ecosystems. Besides, traits associated with tolerance to some of these
stresses may also help mitigate the effects of high temperatures. For instance,
mechanisms of tolerance of drought and salinity that result in higher water
uptake and maintenance of stomatal function under stress will bear a
consequent cooling effect. Certain protective mechanisms such as ability
to upregulate the antioxidant pathways to scavenge reactive oxygen species
generated during stress are useful under most abiotic stresses and substantial
genetic variability in these traits were reported in rice as well as in other
crops (Moradi and Ismail, 2007). Roles of compatible solutes in reducing
tissue desiccation and protecting macromolecules and cellular membranes
under stress are becoming more apparent, and our understanding of their
physiological and molecular basis is progressing fast (Svensson et al., 2002).
More severe water shortages as well as increased wetness are anticipated
in different regions with global warming, and both conditions will have
substantial consequences on productivity of food crops, particularly rice.
Implications of water shortage as well as rice responses to such conditions
were thoroughly reviewed in Section 2.2. Given the high sensitivity to
water stress in rice, significant changes in either the farming systems and/or
cropping sequences will become necessary, including measures like shifting
from paddy production to aerobic rice systems (Bouman et al., 2002), and the
adjustment of cropping calendar to escape the hotter periods during the year.
106 R. Wassmann et al.
Author's personal copy

In some cases with severe incidences of water shortage, shifting from rice
to other crops that are less demanding for water might be necessary; particu-
larly during the dry season or in areas that are predominantly irrigated.
Substantial efforts are needed to develop such future varieties to suit these
evolving systems.
3.3. Advantages/disadvantages in deteriorating soils
The upshot of climate change in worsening soil problems, particularly salt
stress, is becoming obvious with the rising sea level; increasing storm
incidences and reliance on water resources of poor quality as fresh water
become more precious. Salt-affected soils in both coastal and inland areas
already have low productivity and provide fewer options for food security
and livelihood for local farmers. Salinity in coastal areas is more difficult to
handle through reclamation or long-term infrastructure investments
because of its dynamic nature and the complex relations between users at
this fresh-saline water interface, particularly for agriculture versus aquacul-
ture uses. In inlands, salinity, and alkalinity, either inherent or induced via
improper irrigation practices have been mounting in recent years and are
expected to worsen further with lack of good quality water and excessive
irrigation to cope with the rising temperatures. The unique feature of rice to
thrive in flooded soils made it one of the few crops that can be used to
rehabilitate most salt affected coastal and inland soils, despite being sensitive
to salt stress (Maas and Hoffman, 1977). This will help in leaching of harmful
salts, in addition to its high potential for genetic improvement. Besides, rice
is the only possible crop in some coastal areas because of excessive wetness
due to tidal movements and/or monsoon rain. Nonetheless, rice productiv-
ity in salt-affected areas is currently very low, 1–1.5 tons ha
–1
, but can
reasonably be raised by at least 2 tons ha
–1
(Ponnamperuma, 1994), providing
food for millions of the poorest people.
Salt stress negatively affects growth and productivity of most crop plants,
and recent research has begun to unravel the complexities of traits involved
in its tolerance. The most common mechanisms across crop plants are
control of sodium transport, cellular ion homeostasis, and salt response
signaling (Hasegawa et al., 2000; Horie and Schroeder, 2004; Zhu, 2003;
Tester and Davenport, 2003). The fundamental knowledge of salt response
mechanisms in plants forms the basis for strategies to improve salt tolerance
in crop species such as rice (Flowers, 2004; Ismail et al., 2007; Yamaguchi
and Blumwald, 2005). As with other crops, tolerance of salt stress in rice is
complex and varies with the stage of development, being relatively more
sensitive during the early vegetative and reproductive stage (Akbar et al.,
1972), and tolerance at these two sensitive stages is weakly associated
(Moradi et al., 2003). Hence, discovering and combining suitable tolerance
Climate Change Affecting Rice Production 107
Author's personal copy

traits at both stages as well as for various other mechanisms are essential for
developing resilient varieties with broader adaptation.
The vast genetic variability in tolerance to salinity in rice (Akbar et al.,
1972; Flowers and Yeo, 1981) makes it amenable for further genetic
improvements. In recent years, good progress was made in unraveling the
traits associated with tolerance to salt stress, and in breeding (Ismail et al.,
2007; Moradi and Ismail, 2007). The current efforts at IRRI target major
QTLs and candidate genes for the development and use in marker-assisted
backcrossing system to combine major QTLs into suitable genetic back-
grounds, and this implies that developing highly tolerant varieties for future
challenges is feasible. Longer-term strategies will involve combining multi-
ple tolerances of salinity at different stages for conditions where salt stress is
expected any time during the season.
3.4. Flexibility for adjusting and coping with climate changes
The multifaceted abiotic stresses experienced in unfavorable rice ecosystems
(high salinity and other soil problems, submergence, stagnant flooding, and
drought), forced farmers to grow mostly a single crop to rice during the
monsoon season. Local rice varieties have some level of tolerance to these
conditions but their productivity is low. During the rest of the year, large
areas remain fallow due to high soil and water salinity and lack of good
quality irrigation water. Combining tolerance of multiple stresses such as
flash-flooding through incorporation of Sub1A gene, tolerance to longer-
duration partial flooding, tolerance of salt stress conferred by different traits,
and so on will help in developing more robust varieties with wider adapta-
tion. This is particularly feasible in rice because of the enormous progress
made in disentangling the traits associated with tolerance and in developing
DNA-based technologies for precise and speedy breeding of more adapted
varieties. Once these varieties were developed, they are normally more
responsive to management practices that can further boost and stabilize
their performance. Incorporating some of these tolerance mechanisms will
also help cope with heat stress, such as varieties with extreme discrimination
against toxic salts, but with ability to maintain high stomatal conductance
and transpiration cooling.
In some areas, adjustments of the cropping sequence will be necessary to
match the changing ecosystem boundaries. Rice ecosystems might shift
north and southward, and the cropping calendar might need to be adjusted
within the season in some areas. Earlier planting will help avoid high
temperature during the most sensitive reproductive stages but this will
have implications on subsequent crops and will entail development of
suitable varieties of both rice as well as non-rice crops to suit the new
climate patterns. In some areas rice might not be feasible and other crops
might be of better choice in terms of adaptation and economic returns,
108 R. Wassmann et al.
Author's personal copy

while in others, rice might emerge as a new option. In all cases, rice will
remain the crop of choice in areas with increasing wetness, but less so in
areas where water become progressively inadequate.
4. Outlook: Current Advances and
Future Prospects
Traditional breeding methods that comprise pedigree and bulk selec-
tion based on morphological markers have been successfully used in rice
breeding for stress tolerance and will remain important as a standard tech-
nique in many rice breeding institutions scattered throughout Asia. How-
ever, as the molecular genetic basis of heat tolerance in rice is elucidated and
QTLs are identified and suitable markers developed, molecular breeding
approaches are expected to be utilized for developing superior heat tolerant
varieties more precisely and expeditiously. The availability of tolerant rice
germplasm with major QTLs for abiotic stresses anticipated to increase in a
future adverse climate is an encouraging accomplishment. The develop-
ment of rice varieties that can tolerate these stresses will help—at least to
some extend—limiting yield losses and major food shortages in the future.
With the identification and fine mapping of major QTLs for important
abiotic stresses (e.g., submergence, stagnant flooding, salinity, drought,
heat) in conjunction with improved marker technologies, it will become
possible in the near future to pyramid these major tolerance QTLs into any
genetic background. The MAB approach developed for Sub1 now facil-
itates the restoration of the genetic background of the recipient parent.
Using widely grown, high-yielding varieties with good grain quality as
recipient parent furthermore reduces the risk of adverse traits, speeds up
outscaling, and guarantees rapid adoption by farmers. To assure success in
this strategy, the combined efforts of plant breeders, molecular biologists,
plant physiologists, and agronomists, among other scientists, would be
essential. Moreover, the role of the informal seed sector and alternative
seed systems as a key seed supplier in the rice research to production chain,
particularly in the unfavorable areas affected by heat stress, would become
more important (Bishaw and Turner, 2008) even as rice breeding programs
may continue to strongly rely on the formal seed sector that played a key
role in spurring and sustaining the first ‘‘Green Revolution.’’
One of the key features for successful implementation, however, will be
the combination of these crop technology options with advanced climatol-
ogy tools. Although climate change is a global phenomenon, it will manifest
itself as locally variable impacts. This variation carries uncertainty about the
nature of change at local scale that cannot be addressed by the inherently
coarse spatial resolution of global climate models. More targeted approaches
Climate Change Affecting Rice Production 109
Author's personal copy

for climate change adaptation will have to rely on higher-resolved data, that
is, for identifying regional hot-spots of aggravating stresses in rice produc-
tion. IRRI has initiated the integration of advanced GIS, and climatology
approaches into ongoing and envisaged research and extension programs for
improving rice production systems. The dissemination of seeds with the
flood resistant Sub1 gene rice seed is streamlined through GIS analysis of
flood prone areas under present conditions and future climate scenarios
(Hijmans, personal communication). Apart from individual projects, IRRI
has launched the ‘‘Rice and Climate Change Consortium’’ in 2007 as a
strategic platform in the endeavor to fuse different disciplines related to
impact assessment, adaptation to climate change impacts as well as mitiga-
tion of Greenhouse Gas emissions.
Germplasm improvement and natural resource management have a
proved track record of decreasing susceptibility of agricultural systems to
individual stresses and will offer increasingly important solutions for adapt-
ing to progressive climate change. These measures, however, need to be
adapted, both individually and at landscape level, to new combinations of
stresses that a changing climate will impose. Risks not only include imme-
diate impacts on production and livelihood, but also long-term
degradation/conservation issues for soil, water, and biodiversity.
The uptake of innovative management strategies must be greatly accel-
erated particularly in those regions where persistent poverty contributes to
high vulnerability of food security to climate change impacts. Adaptive
management to continually refine these strategies will be required and can
be supported by the predictive capacity of downscaled global climate
models. The challenge is made more difficult by the lead time required to
develop, test, and disseminate scientific/technical agricultural innovations,
and the substantial uncertainty about the magnitude and, in the case of
rainfall patterns, often the direction of climatic shifts over the coming
decades. While we do not ignore the enormous task of adaptation to climate
change, we remain convinced that the basic understanding of stress physi-
ology and agronomy of the rice production systems—as synthesized in
review—can serve as a great asset for the work ahead.
REFERENCES
Abeysiriwardena, D. S. D. Z., Ohba, K., and Maruyama, M. (2002). Influence of tempera-
ture and relative humidity on grian sterility. J. Natl. Sci. Found. Sri Lanka 30, 33–41.
Ackerly, D. D., Coleman, J. S., Morse, S. R., and Bazzaz, F. A. (1992). CO
2
and tempera-
ture effects on leaf-area production in 2 annual plant-species. Ecology 73, 1260–1269.
Aggarwal, P. K., and Mall, R. K. (2002). Climate change and rice yields in diverse agro-
environments of India. II. Effect of uncertainties in scenarios and crop models on impact
assessment. Clim. Change 52, 331–343.
110 R. Wassmann et al.
Author's personal copy

Aggarwal, P. K., Bandyopadhyay, S. K., Pathak, H., Kalra, N., Chander, S., and Kumar, S.
(2000). Analysis of yield trends of the rice–wheat system in north-western India. Outlook
on Agriculture 29, 259–268.
Ahmed, F. E., and Hall, A. E. (1993). Heat injury during early floral bud development in
cowpea. Crop Sci. 33, 764–767.
Ahmed, F. E., Hall, A. E., and DeMason, D. A. (1992). Heat injury during floral develop-
ment in cowpea (Vigna Unguiculata, Fabaceae). Amer.J. Bot. 79, 784–791.
Akbar, M., Yabuno, T., and Nakao, S. (1972). Breeding for saline resistant varieties of rice.
I. Variability for salt tolerance among some rice varieties. Jpn. J. Breed. 22, 277–284.
Al-Khatib, K., and Paulsen, G. M. (1999). High-temperature effects on photosynthetic
processes in temperate and tropical cereals. Crop Sci. 39, 119–125.
Allen, J. A., Pezeshki, S. R., and Chambers, J. L. (1996). Interaction of flooding and salinity
stress on baldcypress (Taxodium distichum). Tree Physiol. 16, 307–313.
Allen, L. H., Valle, R. R., Mishoe, J. W., and Jones, J. W. (1994). Soybean leaf gas-exchange
responses to carbon-dioxide and water-stress. Agron. J. 86, 625–636.
Apse, M. P., Aharon, G. S., Snedden, W. A., and Blumwald, E. (1999). Salt tolerance
conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.Science 285,
1256–1258.
Apse, M. P., Sottosanto, J. B., and Blumwald, E. (2003). Vacuolar cation/H+ exchange, ion
homeostasis, and leaf development are altered in a T-DNA insertional mutant of
AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36, 229–239.
Atlin, G. N., Lafitte, H. R., Tao, D., Laza, A., Amante, A., and Courtois, B. (2006).
Developing rice cultivars for high-fertility upland systems in the Asian tropics. Field
Crops Res. 97, 43–52.
Bailey-Serres, J., and Voesenek, L. (2008). Flooding stress: Acclimations and genetic diver-
sity. Annu. Rev. Plant Biol. 59, 313–339.
Barker, R., and Molle, F. (2004). Evolution of Irrigation in South and Southeast Asia.
Comprehensive Assessment of WatED Management in Agriculture, Research Report
No. 5. Colombo: IWMI.
Baker, J. T., Allen, L. H., and Boote, K. J. (1992). Response of rice to carbon-dioxide and
temperature. Agric. For. Meteorol. 60, 153–166.
Baker, J. T., Allen, L. H., Boote, K. J., and Pickering, N. B. (1997a). Rice responses to
drought under carbon dioxide enrichment.1. Growth and yield. Glob. Chang. Biol. 3,
119–128.
Baker, J. T., Allen, L. H., Boote, K. J., and Pickering, N. B. (1997b). Rice responses to
drought under carbon dioxide enrichment. 2. Photosynthesis and evapotranspiration.
Glob. Chang. Biol. 3, 129–138.
Baloch, M. S., Awan, I. U., and Hassan, G. (2006). Growth and yield of rice as affected by
transplanting dates and seedlings per hill under high temperature of Dera Ismail Khan,
Pakistan. J. Zhejiang Univ. Sci. B. 7, 572–579.
Barnabas, B., Jager, K., and Feher, A. (2008). The effect of drought and heat stress on
reproductive processes in cereals. Plant Cell Environ. 31, 11–38.
Bates, B. C., Kundzewicz, Z. W., Wu, S., and Palutikof, J. P., Eds. (2008). “Climate Change
and Water,” 210 pp. Technical Paper of the Intergovernmental Panel on Climate Change,
IPCC Secretariat, Geneva. http://www.ipcc.ch/ipccreports/tp-climate-change-water.
htm.
Belder, P., Bouman, B. A. M., Cabangon, R., Lu, G., Quilang, E. J. P., Li, Y. H.,
Spiertz, J. H. J., and Tuong, T. P. (2004). Effect of water-saving irrigation on rice
yield and water use in typical lowland conditions in Asia. Agric. Water Manage. 65,
193–210.
Bernier, J., Atlin, G. N., Serraj, R., Kumar, A., and Spaner, D. (2008). Breeding upland rice
for drought resistance (A review). J. Sci. Food Agric. 88, 927–939.
Climate Change Affecting Rice Production 111
Author's personal copy

Bishaw, Z., and Turner, M. (2008). Linking participatory plant breeding to the seed supply
system. Euphytica 163, 31–44.
Bohnert, H. J., and Jensen, R. G. (1996). Strategies for engineering water-stress tolerance in
plants. Trends Biotechnol. 14, 89–97.
Bohnert, H. J., Nelson, D. E., and Jensen, R. G. (1995). Adaptations to environmental
stresses. Plant Cell 7, 1099–1111.
Boonjung, H., and Fukai, S. (1996). Effects of soil water deficit at different growth stages on
rice growth and yield under upland conditions.2. Phenology, biomass production and
yield. Field Crops Res. 48, 47–55.
Bouman, B. A. M., Humphreys, E., Tuong, T. P., and Barker, R. (2007). Rice and water. In
“Advances in Agronomy,” Vol. 92, pp. 187–237. IRRI, Los Ban
˜os, Philippines.
Bouman, B. A. M., Peng, S., Castaneda, A. R., and Visperas, R. M. (2005). Yield and water
use of irrigated tropical aerobic rice systems. Agricultural Water Management 74, 87–105.
Bouman, B. A. M., and Tuong, T. P. (2001). Field water management to save water and
increase its productivity in irrigated lowland rice. Agric. Water Manage. 49, 11–30.
Bouman, B. A. M., Xiaoguang, Y., Huaqi, W., Zhiming, W., Junfang, Z., Changgui, W.,
and Bin, C. (2002). Aerobic rice (Han Dao): A new way of growing rice in water-short
areas. Proceedings of the 12th International Soil Conservation Organization Conference,
26–31 May, 2002, Beijing, China. Tsinghua University Press, pp. 175–181.
Bowman, W. D., and Strain, B. R. (1987). Interaction between co2 enrichment and salinity
stress in the c-4 nonhalophyte andropogon-glomeratus (walter) bsp. Plant Cell Environ.
10, 267–270.
Boyer, J. S. (1982). Plant productivity and environment. Science 218, 443–448.
Butt, T. A., McCarl, B. A., Angerer, J., Dyke, P. T., and Stuth, J. W. (2005). The economic
and food security implications of climate change in Mali. Clim. Change 68, 355–378.
Challinor, A. J., Wheeler, T. R., Craufurd, P. Q., Ferro, C. A. T., and Stephenson, D. B.
(2007). Adaptation of crops to climate change through genotypic responses to mean and
extreme temperatures. Agric. Ecosyst. Environ. 119, 190–204.
Chen, T. H. H., and Murata, N. (2000). Enhancement of tolerance of abiotic stress by
metabolic engineering of betaines and other compatible solutes. Curr. Opin. Plant Biol. 5,
250–257.
Cho, N. (1956). Double fertilization in Oryza sativa L. and development of the endosperm
with special reference to the aleurone layer. Bull. Natl. Inst. Agric. Sci. 6, 61–101.
Cooper, M., Fukai, S., and Wade, L. J. (1999). How can breeding contribute to more
productive and sustainable rainfed lowland rice systems? Field Crops Res. 64, 199–209.
Craufurd, P. Q., Prasad, P. V. V., Kakani, V. G., Wheeler, T. R., and Nigam, S. N. (2003).
Heat tolerance in groundnut. Field Crops Res. 80, 63–77.
Das, K. K., Sarkar, R. K., and Ismail, A. M. (2005). Elongation ability and non-structural
carbohydrate levels in relation to submergence tolerance in rice. Plant Sci. 168, 131–136.
Dey, M., and Upadhyaya, H. (1996). In ‘‘Rice research in Asia: Progress and Priorities’’
(R. Evenson, R. Herdt, and M. Hossain, Eds.), pp. 291–303. CAB International, Oxon,
UK.
Downton, J., and Slatyer, R. O. (1972). Temperature dependence of photosynthesis in
cotton. Plant Physiol. 50, 518–522.
Easterling, W. E., Chhetri, N., and Niu, X. Z. (2003). Improving the realism of modelling
agronomic adaptation to climate change: Simulating technological submission. Clim.
Change 60, 149–173.
Ekanayake, I. J., Steponkus, P. L., and Dedatta, S. K. (1990). Sensitivity of pollination to
water deficits at anthesis in upland rice. Crop Sci. 30, 310–315.
Ella, E., Kawano, N., Yamauchi, Y., Tanaka, K., and Ismail, A. (2003). Blocking ethylene
perception enhances flooding tolerance in rice. Funct. Plant Biol. 30, 813–819.
112 R. Wassmann et al.
Author's personal copy

Ella, E. S., and Ismail, A. M. (2006). Seedling nutrient status before submergence affects
survival after submergence in rice. Crop Sci. 46, 1673–1681.
Enomoto, N., Yamada, I. and Hozumi, K. (1956). On artificial germination of pollen in rice
plants. IV. Temperature limits of pollen germination in rice varieties. (In Japanese with
English summary). Proc. of the Crop Science Society of Japan, pp. 25–69.
Evenson, R. E., and Gollin, D. (1997). Genetic resources, international organizations, and
improvement in rice varieties. Econ. Dev. Cult. Change 45, 471–500.
Fischer, G., Shah, M., and Velthuizen, H. V. (2002). “Climate Change and Agricultural
Vulnerability,” 152 pp. International Institute for Applied Systems Analysis, Laxenburg.
Flowers, T. J. (2004). Improving crop salt tolerance. J. Exp. Bot. 55, 307–319.
Flowers, T. J., Duque, E., Hajibagheri, M. A., McGonigle, T. P., and Yeo, A. R. (1985).
The effect of salinity on leaf ultrastructure and net photosynthesis of 2 varieties of rice—
Further evidence for a cellular-component of salt-resistance. New Phytol. 100, 37–43.
Flowers, T. J., Troke, P. F., and Yeo, A. R. (1977). Mechanism of salt tolerance in
halophytes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 28, 89–121.
Flowers, T. J., and Yeo, A. R. (1981). Variability in the resistance of sodium-chloride salinity
within rice (oryza-sativa-l) varieties. New Phytol. 88, 363–373.
Fukao, T., and Bailey-Serres, J. (2008). Ethylene—A key regulator of submergence
responses in rice. Plant Sci. 175, 43–51.
Fukao, T., Xu, K. N., Ronald, P. C., and Bailey-Serres, J. (2006). A variable cluster of
ethylene response factor-like genes regulates metabolic and developmental acclimation
responses to submergence in rice (W). Plant Cell 18, 2021–2034.
Fukuda, A., Nakamura, A., Tagiri, A., Tanaka, H., Miyao, A., Hirochika, H., and
Tanaka, Y. (2004). Function, intracellular localization and the importance in salt
tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol. 45, 146–159.
Ghassemi, F., Jakeman, A. J., and Nix, H. A. (1995). ‘‘Salinisation of Land and Water
Resources’’. CAB International, Wallingford.
Goto, A., Sasahara, H., Shigemune, A., and Miura, K. (2008). Estimation of cool tolerance at
the booting and flowering stages in indica rice varieties. Jpn. J. Crop Sci. 77, 167–173.
Grashoff, C., Dijkstra, P., Nonhebel, S., Schapendonk, A., and VandeGeijn, S. C. (1995).
Effects of climate change on productivity of cereals and legumes; model evaluation of
observed year-to-year variability of the CO
2
response. Glob. Chang. Biol. 1, 417–428.
Hall, A. E. (1992). Breeding for heat tolerance. Plant Breed Rev. 10, 129–169.
Hall, A. E. (1993). Physiology and breeding for heat tolerance in cowpea, and comparison
with other crops. In “Adaptation of Food Crops to Temperature and Water Stress”
(C. G. Kuo, Ed.), pp. 271–284. Publ. No. 93–410. Asian Vegetable Research and
Development Center, Shanhua, Taiwan.
Hall, A. E. (2004). Breeding for adaptation to drought and heat in cowpea. Eur. J. Agron. 21,
447–454.
Hall, A. E., Singh, B. B., and Ehlers, J. D. (1997). Cowpea breeding. Plant Breed. Rev. 15,
215–274.
Hasegawa, P. M., Bressan, R. A., Zhu, J. K., and Bohnert, H. J. (2000). Plant cellular and
molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463–499.
Heinemann, A. B., Dingkuhn, M., Luquet, D., Combres, J. C., and Chapman, S. (2008).
Characterization of drought stress environments for upland rice and maize in central
Brazil. Euphytica 162, 395–410.
Herve
´, P., and Serraj, R. (2009). Gene technology and drought: A simple solution for a
complex trait. Afr. J. Biotech. (in press).
Horie, T., Nakagawa, H., Centeno, H. G. S., and kropff, H. J. (1995). “The rice Crop
Simulation Model SIMRIW and Tts Testing.” CABI in association with IRRI, Los
Ban
˜os, Philippines.
Horie, T., and Schroeder, J. I. (2004). Sodium transporters in plants. Diverse genes and
physiological functions. Plant Physiol. 136, 2457–2462.
Climate Change Affecting Rice Production 113
Author's personal copy

Hossain, M., and Fischer, K. S. (1995). Rice research for food security and sustainable
agricultural development in Asia: Achievements and challenges. GeoJournal 35, 286–298.
Hossain, M., Gollin, D., Cabanilla, V., Cabrera, E., Jonson, N., Khush, G. S., and
McLaren, G. (2002). International research and genetic improvement in rice—Evidence
from Asia and Latin America. In ‘‘Crop Variety Improvement and Its Effect on Produc-
tivity—The Impact of International Agricultural Research’’ (R. E. Evenson and
D. Gollin, Eds.), pp. 71–107. CABI Publishing, UK.
Howden, S. M., Soussana, J. -F., Tubiello, F. N., Chhetri, N., Dunlop, M., and Meinke, H.
(2007). Adapting agriculture to climate change. Pnas 104(5), 19691–19696 http:// www.
pnas.org/cgi/doi/10.1073/pnas.0701890104.
Imin, N., Kerim, T., Rolfe, B. G., and Weinman, J. J. (2004). Effect of early cold stress on
the maturation of rice anthers. Proteomics 4, 1873–1882.
International Rice Research Institute. (1976). ‘‘Symposium on Climate and Rice.’’
Los Ban
˜os, Philippines.
International Rice Research Institute. (1980). Annual Report, 1979, Los Ban
˜os, Philippines.
IPCC. (2007a). IPCC Fourth Assessment Report (AR4). Comprises the AR4 Synthesis
Report (online at http://www.ipcc.ch/ipccreports/ar4-syr.htm); Working Group I
Report ‘The Physical Science Basis (online at http://www.ipcc.ch/ipccreports/
ar4-wg1.htm); Working Group II Report ‘Impacts, Adaptation and Vulnerability’
(online at http://www.ipcc.ch/ipccreports/ar4-wg2.htm); and Working Group III
Report ‘Mitigation of Climate Change’ (online at http://www.ipcc.ch/ipccreports/ar4-
wg3.htm).
IPCC-WG1. (2007b). “Climate Change 2007: The Scientific Basis.” WMO/UNEP,
Geneva.
IPCC-WG2. (2007c). “Climate Change 2007: Impacts, Adaptation and Vulnerability.”
WMO/UNEP, Geneva.
Ismail, A. M., Ella, E. S., Vergara, G. V., and Mackill, D. J. (2008). Mechanisms associated
with tolerance of flooding during germination and early seeding growth in rice (Orayza
sativa). Ann. Bot. 103, 107–209.
Ismail, A. M., and Hall, A. E. (1998). Positive and potential negative effects of heat-tolerance
genes in cowpea. Crop Sci. 38, 381–390.
Ismail, A. M., and Hall, A. E. (1999). Reproductive-stage heat tolerance, leaf membrane
thermostability and plant morphology in cowpea. Crop Sci. 39, 1762–1768.
Ismail, A. M., and Hall, A. E. (2000). Semidwarf and standard-height cowpea responses to
row spacing in different environments. Crop Sci. 40, 1618–1623.
Ismail, A. M., Heuer, S., Thomson, M. J., and Wissuwa, M. (2007). Genetic and genomic
approaches to develop rice germplasm for problem soils. Plant Mol. Biol. 65, 547–570.
Jagadish, S. V. K. (2007). Molecular and physiological dissection of heat tolerance during
anthesis in rice (Oryza sativa L.). Thesis, The University of Reading, UK.
Jagadish, S. V. K., Craufurd, P. Q., and Wheeler, T. R. (2007). High temperature stress and
spikelet fertility in rice (Oryza sativa L.). J. Exp. Bot. 58, 1627–1635.
Jagadish, S. V. K., Craufurd, P. Q., and Wheeler, T. R. (2008). Phenotyping parents of
mapping populations of rice (Oryza sativa L.) for heat tolerance during anthesis. Crop Sci.
48, 1140–1146.
Jena, K. K., and Mackill, D. J. (2008). Molecular markers and their usein marker-assisted
selection in rice. Crop Sci. 48, 1266–1276.
Jennings, P. R., Coffman, W. R., and Kauffman, H. E. (1979). ‘‘Rice Improvement.’’
IRRI, Los Ban
˜os, Philippines.
Ji, X. M., Raveendran, M., Oane, R., Ismail, A., Lafitte, R., Bruskiewich, R., Cheng, S. H.,
and Bennett, J. (2005). Tissue-specific expression and drought responsiveness of cell-wall
invertase genes of rice at flowering. Plant Mol. Biol. 59, 945–964.
114 R. Wassmann et al.
Author's personal copy

Kakani, V. G., Prasad, P. V. V., Craufurd, P. Q., and Wheeler, T. R. (2002). Response of
in vitro pollen germination and pollen tube growth of groundnut (Arachis hypogaea L.)
genotypes to temperature. Plant Cell Environ. 25, 1651–1661.
Kakani, V. G., Reddy, K. R., Koti, S., Wallace, T. P., Prasad, P. V. V., Reddy, V. R., and
Zhao, D. (2005). Differences in in vitro pollen germination and pollen tube growth of
cotton cultivars in response to high temperature. Ann. Bot. 96, 59–67.
Karim, M. A., Fracheboud, Y., and Stamp, P. (1997). Heat tolerance of maize with reference
of some physiological characteristics. Ann. Bangladesh Agri. 7, 27–33.
Kenny, G. J., Harrison, P. A., Olesen, J. E., and Parry, M. J. (1993). The effects of climate
change on land suitability of grain maize, winter wheat and cauliflower in Europe. Eur. J.
Agron. 2, 325–338.
Khush, G. S. (1999). Green revolution: Preparing for the 21st century. Genome 42, 646–655.
Khush, G. S. (2001). Challenges for meeting the global food and nutrient needs in the new
millennium. Proc. Nutr. Soc. 60, 15–26.
Kobata, T., and Moriwaki, N. (1990). Grain growth rate as a function of dry-matter
production rate: An experiment with two rice cultivars under different radiation envir-
onments. Jpn. J. Crop Sci. 59, 1–7.
Kobata, T., Sugawara, M., and Takatu, S. (2000). Shading during the early grain filling
period does not affect potential grain dry matter increase in rice. Agron. J. 92, 411–417.
Kobata, T., and Uemuki, N. (2004). High temperatures during the grain-filling period do
not reduce the potential grain dry matter increase of rice. Agron. J. 96, 406–414.
Krishnan, P., Swain, D. K., Bhaskar, B. C., Nayak, S. K., and Dash, R. N. (2007). Impact of
elevated CO2 and temperature on rice yield and methods of adaptation as evaluated by
crop simulation studies. Agric. Ecosyst. Environ. 122, 233–242.
Kropff, M. J., Matthews, R. B., Van Laar, H. H., and Ten Berge, H. F. M. (1995). ‘‘The rice
model Oryza 1 and its testing.’’ CABI in association with IRRI Los Ban
˜os, Philippines.
Kumar, A., Bernier, J., Verulkar, S., Lafitte, H. R., and Atlin, G. N. (2008). Breeding for
drought tolerance: Direct selection for yield, response to selection and use of drought-
tolerant donors in upland and lowland-adapted populations. Field Crop Res. 107,
221–231.
Lafitte, H. R., and Courtois, B. (2002). Interpreting cultivar environment interactions for
yield in upland rice: Assigning value to drought-adaptive traits. Crop Sci. 42, 1409–1420.
Lampayan, R. M., Bouman, B. A. M., De Dios, J. L., Lactaoen, A. T., Espiritu, A. J., Norte,
T. M., Quilang, E. J. P., Tabbal, D. F., Llorca, L. P., Soriano, J. B., Corpuz, A. A.,
Malasa, R. B., et. al. (2005). Transfer of water saving technologies in rice production in
the Philippines. In ‘‘Transitions in Agriculture for Enhancing Water Productivity.’’
(T. M. Thiyagarajan, H. Hengsdijk, and P. Bindraban, Eds.), pp 111–132. Proceedings
of the International Symposium on Transitions in Agriculture for Enhancing
Water Productivity, 23–25 September 2003, Kilikulam, Tamil Nadu Agricultural
University, Tamil Nadu, India.
Li, Y. H., and Baker, R. (2004). Increasing water productivity for rice field irrigation in
China. Rice Field Water Environ. 2, 187–193.
Liu, J. X., Liao, D. Q., Oane, R., Estenor, L., Yang, X. E., Li, Z. C., and Bennett, J. (2005).
Genetic variation in the sensitivity of anther dehiscence to drought stress in rice. Field
Crops Res. 97, 87–100.
Maas, E. V., and Hoffman, G. J. (1977). Crop salt tolerance—Current assessment. ASCEJ
Irrig Drain Div. 103,115–34.
Mackill, D. J. (1981). Studies on the mechanism and genetics of high temperature tolerance
in rice. Ph.D. Dissertation, University of California Davis, California, USA.
Mackill, D. J. (2006). Breeding for resistance to abiotic stresses in rice: The value of
quantitative trait loci. In ‘‘Plant Breeding: The Arnel R Hallauer International Sympo-
sium’’ (K. R. Lamkey and M. Lee, Eds.), pp. 201–212. Blackwell Pub, Ames, IA.
Climate Change Affecting Rice Production 115
Author's personal copy

Mackill, D. J., and Coffman, W. R. (1983). Inheritance of high temperature tolerance and
pollen shedding in a rice cross. Z Pflanzesuchtg 91, 61–69.
Mackill, D. J., Coffman, W. R., and Rutger, J. N. (1982). Pollen shedding and combining
ability for high temperature tolerance in rice. Crop Sci. 22, 730–733.
Maclean, J.L., Dawe, D., Hardy, B., and Hettel, G.P. (Eds.), ‘‘Rice Almanac,’’ p. 253.
International Rice Research Institute, Los Ban
˜os, Philippines.
Maestri, E., Klueva, N., Perrotta, C., Gulli, M., Nguyen, H. T., and Marmiroli, N. (2002).
Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol. Biol.
48, 667–681.
Mallik, S., Mandal, B. K., Sen, S. N., and Sarkarung, S. (2002). Shuttle-breeding: An
effective tool for rice varietal improvement in rainfed lowland ecosystem in eastern
India. Curr. Sci. 83, 1097–1102.
Manabe, S., and Stouffer, R. J. (1994). Multiple-century response of a coupled ocean-
atmosphere model to an increase of atmospheric carbon-dioxide. J. Climate 7, 5–23.
Manderscheid, R., and Weigel, H. J. (2007). Drought stress effects on wheat are mitigated by
atmospheric CO
2
enrichment. Agron. Sustainable Dev. 27, 79–87.
Matsui, T., and Kagata, H. (2003). Characteristics of floral organs related to reliable self
pollination in rice (Oryza sativa L.). Ann. Bot. 91, 473–477.
Matsui, T., and Omasa, K. (2002). Rice (Oryza sativa L) cultivars tolerant to high tempera-
ture at flowering: Anther characteristics. Annals of Botany 89, 683–687.
Matsui, T., Kobayashi, K., Kagata, H., and Horie, T. (2005). Correlation between variability
of pollination and length of basal dehiscence of the theca in rice and a hot-and-humid
condition. Plant. Prod. Sci. 8, 109–114.
Matsui, T., Kobayasi, K., Yoshimoto, M., and Hasegawa, T. (2007). Stability of rice
pollination in the field under hot and dry conditions in the Riverina region of New
Soth wales, Australia. Plant Prod. Sci. 10, 57–63.
Matsui, T., Namuco, O. S., Ziska, L. H., and Horie, T. (1997a). Effect of high temperature
and CO2 concentration on spikelet sterility in indica rice. Field Crops Res. 51, 213–219.
Matsui, T., Omasa, K., and Horie, T. (1997b). High temperature induced florets sterility of
japonica rice at flowering in relation to air temperature, humidity and wind velocity
condition. Jpn. J. Crop Sci. 66, 449–455.
Matsui, T., Omasa, K., and Horie, T. (1999a). Rapid swelling of pollen grains in response to
floret opening unfolds locule in rice (Oryza sativa L.). Plant Prod. Sci. 2, 196–199.
Matsui, T., Omasa, K., and Horie, T. (1999b). Mechanism of anther dehiscence in rice
(Oryza sativa L.). Ann. Bot. 84, 501–506.
Matsui, T., Omasa, K., and Horie, T. (2000a). High temperature at flowering inhibit
swelling of pollen grains, a driving force for thecae dehiscence in rice (Oryza sativa L.).
Plant Prod. Sci. 3, 430–434.
Matsui, T., Omasa, K., and Horie, T. (2000b). Mechanism of septum opening in anthers of
two rowed barley. Ann. Bot. 86, 47–51.
Matsui, T., Omasa, K., and Horie, T. (2001). The difference in sterility due to high
temperatures during the flowering period among japonica rice varieties. Plant Prod. Sci.
4, 90–93.
Mishra, H. S., Rathore, T. R., and Pant, R. C. (1990). Effect of intermittent irrigation on
groundwater table contribution, irrigation requirement and yield of rice in Mollisols of
the Tarai Region. Agric. Water Management 18, 231–241.
Moradi, F., and Gilani, A. (2007). Impact of global warming and high temperature stress on
Iranian rice cultivars: An overview. Proc. Intl. Workshop on Cool Rice for a Warmer
World, Huazhong Agricultural University, Wuhan, Hubei, China. 26-30 March 2007.
Moradi, F., and Ismail, A. M. (2007). Responses of photosynthesis, chlorophyll fluorescence
and ROS-Scavenging systems to salt stress during seedling and reproductive stages in rice.
Ann. Bot. 99, 1161–1173.
116 R. Wassmann et al.
Author's personal copy

Moradi, F., Ismail, A. M., Gregorio, G. B., and Egdane, J. A. (2003). Salinity tolerance of
rice during reproductive development and association with tolerance at the seeding stage.
Ind. J. Plant Physiol. 8, 105–116.
Morita, S., Yonemaru, J., and Takanashi, J. (2005). Grain growth and endosperm cell size
under high night temperatures in rice (Oryza sativa L.)Ann. Bot. 95, 695–701.
Morris, M. L., and Bellon, M. R. (2004). Participatory plant breeding research: Opportunities
and challenges for the international crop improvement system. Euphytica 136, 21–35.
Mutters, R. G., Ferreira, L. G. R., and Hall, A. E. (1989a). Photoperiod and light quality
effects on cowpea floral development at high temperatures. Crop Sci. 29, 1501–1505.
Mutters, R. G., and Hall, A. E. (1992). Reproductive responses of cowpea to high
temperature during different night periods. Crop Sci. 32, 202–206.
Mutters, R. G., Hall, A. E., and Patel, P. N. (1989b). Photoperiod and light quality effects on
cowpea floral development at high temperatures. Crop Sci. 29, 1501–1505.
Nakagawa, H., Horie, T., and Matsui, T. (2002). Effects of climate change on rice produc-
tion and adaptive technologies. In ‘‘Rice Science: Innovations and Impact for Liveli-
hood’’ (T. W. Mew, D. S. Brar, S. Peng, D. Dawe, and B. Hardy, Eds.), pp. 635–657.
International Rice Research Institute, China.
Nakazono, M., Tsuji, H., Li, Y. H., Saisho, D., Arimura, S., Tsutsumi, N., and Hirai, A.
(2000). Expression of a gene encoding mitochondrial aldehyde dehydrogenase in rice
increases under submerged conditions. Plant Physiol. 124, 587–598.
Naich, A. N., and Mari, N. (2007). Research work on the development of rice varieties
suitable for high temperature at Rice Research Institute Dokri, Sindh, Pakistan. Proc.
Intl. Workshop on Cool Rice for a Warmer World, Huazhong Agricultural University,
Wuhan, Hubei, China. 26–30 March 2007.
Nandi, S., Subudhi, P. K., Senadhira, D., Manigbas, N. L., SenMandi, S., and Huang, N.
(1997). Mapping QTLs for submergence tolerance in rice by AFLP analysis and selective
genotyping. Mol. General Genet. 255, 1–8.
Neeraja, C. N., Maghirang-Rodriguez, R., Pamplona, A., Heuer, S., Collard, B. C. Y.,
Septiningsih, E. M., Vergara, G., Sanchez, D., Xu, K., Ismail, A. M., and Mackill, D. J.
(2007). A marker-assisted backcross approach for developing submergence-tolerant rice
cultivars. Theor. Appl. Genet. 115, 767–776.
Nielsen, C. L., and Hall, A. E. (1985). Responses of cowpea (Vigna unguiulata [L.] walp.) in
the field to high night temperatures during flowering. II. Plant responses. Field Crop Res.
10, 181–196.
Oh-e, I., Saitoh, K., and Kuroda, T. (2007). Effects of high temperature on growth, yield
and dry-matter production of rice grown in the paddy field. Plant Prod. Sci. 10, 412–422.
Osada, A., Sasiprada, V., Rahong, M., Dhammanuvong, S., and Chakrabandhu, M. (1973).
Abnormal occurrence of empty grains of indica rice plants in the dry, hot season in
Thailand. Proc. Crop Sci. Soc. Jpn. 42, 103–109.
O’Toole, T. C. (2004). Rice water: The final frintier. In “First International Conference on
Rice for the Future”, Aug. 31–Sept. 2, 2004 Bangko, Tailand.
O’Toole, J. C., and Namuco, O. S. (1983). Role of panicle exsertion in water stress induced
sterility. Crop Sci. 23, 1093–1097.
Ouk, M., Basnayake, J., Tsubo, M., Fukai, S., Fischer, K. S., Cooper, M., and Nesbitt, H.
(2006). Use of drought response index for identification of drought tolerant genotypes in
rainfed lowland rice. Field Crops Res. 99, 48–58.
Pandey, S., Bhandari, H., and Hardy, B. (2007). “Economic Costs of Drought and
Rice Farmers’ Coping Mechanisms: A Cross-country Comparative Analysis,” 203 pp.
International Rice Research Institute, Manila.
Pathak, H., Ladha, J. K., Aggarwal, P. K., Peng, S., Das, S., Singh, Y., Singh, B.,
Kamra, S. K., Mishra, B., Sastri, A., Aggarwal, H. P., Das, D. K., et al. (2003). Trends
Climate Change Affecting Rice Production 117
Author's personal copy

of climatic potential and on-farm yields of rice and wheat in the Indo-Gangetic Plains.
Field Crops Res. 80, 223–234.
Peng, S., Bouman, B. A. M., Visperas, R. M., Castaneda, A., Nie, L., and Park, H. K.
(2006). Comparison between aerobic and flooded rice: Agronomic performance in a
long-term (8-season) experiment. Field Crops Res. 96, 252–259.
Peng, S. B., Huang, J. L., Sheehy, J. E., Laza, R. C., Visperas, R. M., Zhong, X. H.,
Centeno, G. S., Khush, G. S., and Cassman, K. G. (2004). Rice yields decline with
higher night temperature from global warming. Proc. Natl. Acad. Sci. USA 101,
9971–9975.
Peng, S. B., Khush, G. S., Virk, P., Tang, Q. Y., and Zou, Y. B. (2008). Progress in ideotype
breeding to increase rice yield potential. Field Crops Res. 108, 32–38.
Pinheiro, B., da, S., de Castro, E., da, M., and Guimaraes, C. M. (2006). Sustainability and
profitability of aerobic rice production in Brazil. Field Crops Res. 97, 34–42.
Ponnamperuma, F. N. (1994). Evaluation and improvement of lands for wetland rice
production. In “Rice and Problem Soils in South and Southeast Asia” IRRI Discussion
Paper Series No. 4 (D. Senadhira, Ed.), pp 3–19. International Rice Research Institute,
Manila, Philippines.
Porter, J. R., and Semenov, M. A. (2005). Crop responses to climatic variation. Philos. Trans.
Roy. Soc.B Biol. Sci. 360, 2021–2035.
Potvin, C. (1994). Interactive effects of temperature and atmospheric CO2 on physiology
and growth. In ‘‘Plant Responses to the Gaseous Environment, Molecular, Metabolic
and Physiological Aspects’’ (R. B. Alscher and A. R. Wellburn, Eds.), pp. 39–54.
Chapman & Hall, London.
Prasad, P. V. V., Boote, K. J., Allen, L. H., Sheehy, J. E., and Thomas, J. M. G. (2006).
Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in
response to high temperature stress. Field Crops Res. 95, 398–411.
Redon
˜a, E. D., Laza, M. A., and Manigbas, N. L. (2007). Breeding rice for adaptation and
tolerance to high temperatures. Proc. Intl. Workshop on Cool Rice for a Warmer
World, Huazhong Agricultural University, Wuhan, Hubei, China, 26–30 March 2007.
Ren, Z. H., Gao, J. P., Li, L. G., Cai, X. L., Huang, W., Chao, D. Y., Zhu, M. Z.,
Wang, Z. Y., Luan, S., and Lin, H. X. (2005). A rice quantitative trait locus for salt
tolerance encodes a sodium transporter. Nat. Genet. 37, 1141–1146.
Robredo, A., Perez-Lopez, U., de la Maza, H. S., Gonzalez-Moro, B., Lacuesta, M., Mena-
Petite, A., and Munoz-Rueda, A. (2007). Elevated CO
2
alleviates the impact of drought
on barley improving water status by lowering stomatal conductance and delaying its
effects on photosynthesis. Environ. Exp. Bot. 59, 252–263.
Rosegrant, M. W., Paisner, M. S., Meijer, S., and Witcover, J. (2001). “Global Food
Projections To 2020: Emerging Trends and Alternative Futures,” p. 206. International
Food Policy Research Institute, Washington, D.C.
Rozema, J., Lenssen, G. M., Arp, W. J., and van de Staay, J. W. M. (1991). Global change, the
impact of the greenhouse effect (atmospheric CO
2
enrichment) and the increased UV-B
radiation on terrestrial plants. In ‘‘Ecological Responses to Environmental Stresses’’
( J. Rozema and J. A. C. Verkleij, Eds.), pp. 220–231. Kluwer Academic, Dordrecht.
Saika, H., Okamoto, M., Miyoshi, K., Kushiro, T., Shinoda, S., Jikumaru, Y.,
Fujimoto, M., Arikawa, T., Takahashi, H., Ando, M., Arimura, S., Miyao, A., et al.
(2007). Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that
encodes ABA 8-Hydroxylase in rice. Plant Cell Physiol. 48(2), 287–298.
Saini, H. S. (1997). Effects of water stress on male gametophyte development in plants.
Sexual Plant Reprod. 10, 67–73.
Saini, H. S., and Aspinall, D. (1982). Abnormal sporogenesis in wheat (triticum-aestivum l)
induced by short periods of high-temperature. Ann. Bot. 49, 835–846.
118 R. Wassmann et al.
Author's personal copy

Saini, H. S., Sedgley, M., and Aspinall, D. (1983). Effect of heat-stress during
floral development on pollen-tube growth and ovary anatomy in wheat (triticum-
aestivum-l). Aust. J. Plant Physiol. 10, 137–144.
Saini, H. S., and Westgate, M. E. (2000). Reproductive development in grain crops during
drought. ‘‘Advances in Agronomy,’’ Vol. 68, pp. 59–96.
Sairam, R. K., and Tyagi, A. (2004). Physiology and molecular biology of salinity stress
tolerance in plants. Curr. Sci. 86, 407–421.
Sakamoto, A., and Murata, N. (2002). The role of glycine betaine in the protection of plants
from stress: Clues from transgenic plants. Plant Cell Environ. 25, 163–171.
Salem, M. A., Kakani, V. G., Koti, S., and Reddy, K. R. (2007). Pollen-based screening of
soybean genotypes for high temperatures. Crop Sci. 47, 219–231.
Sarkar, R. K., Reddy, J. N., Sharma, S. G., and Ismail, A. M. (2006). Physiological basis of
submergence tolerance in rice and implications for crop improvement. Current Science 91,
899–906.
Sarkarung, S., and Pantuwan, G. (1999). Improving rice for drought-prone rainfed lowland
environments. In ‘‘Genetic Improvement of Rice for Water-Limited Environments’’
(O. Ito, J. C. O’Toole, and B. Hardy, Eds.), pp. 57–70. International Rice Research
Institute, Los Banos, The Philippines.
Satake, T. (1995). High temperature injury. In ‘‘Science of the Rice Plant, Vol. 2. Physiology’’
(T. Matsuo and K. Hoshikawa, Eds.), pp. 805–812. Food and Agricultural Policy Research
Centre, Tokyo.
Satake, T., and Yoshida, S. (1978). High temperature-induced sterility in indica rice at
flowering. Jpn. J. Crop Sci. 47, 6–17.
Savchenko, G. E., Klyuchareva, E. A., Abrabchik, L. M., and Serdyuchenko, E. V. (2002).
Effect of periodic heat shock on the membrane system of etioplasts. Russ. J. Plant Physiol.
49, 349–359.
Septiningsih, E. M., Pamplona, A. M., Sanchez, D. L., Neeraja, C. N., Vergara, G. V.,
Heuer, S., Ismail, A. M., and Mackill, D. J. (2008). Development of submergence tolerant
rice cultivars: The Sub1 locus and beyond. Ann. Bot. 103, doi:10.1093/aob/mcn206.
Serraj, R., Dimayuga, G., Gowda, V., Guan, Y., He, Hong, Impa, S., Liu, D. C., Mabesa,
R. C., Sellamuthu, R., and Torres, R. (2008). Drought-resistant rice: Physiological
framework for an integrated research strategy. In ‘‘Drought frontiers in rice – Crop
improvement for increased rainfed production’’ (R. Serraj, J. Bennett, and B. Hardy,
Eds.), World Scientific Publishing (in press).
Serraj, R., Allen, L. H., and Sinclair, T. R. (1999). Soybean leaf growth and gas exchange
response to drought under carbon dioxide enrichment. Glob. Chang. Biol. 5, 283–291.
Sharma, P. K., Bhushan, L., Ladha, J. K., Naresh, R. K., Gupta, R. K.,
Balasubramanian, B. V., and Bouman, B. A. M. (2002). Crop water relations in rice–
wheat cropping under different tillage systems and water management practices in a
marginally sodic, medium-textured soil. In ‘‘Water-wise Rice Production. Proceedings
of the International Workshop on Water-Wise Rice Production,’’ (B. A. M. Bouman,
H. Hengsdijk, B. Hardy, T. P. Toung, and J. K. Ladha, Eds.), Los Bano
˜s, Philippines.
11 April 2002, pp. 223–235.
Sharma, G., Patil, S. K., Buresh, R. J., Mishra, V. N., Das, R. O., Haefele, S. M., and
Shrivastava, L. K. (2005). Rice establishment method aVects nitrogen use and crop produc-
tion of rice–legume systems in drought-prone eastern India. Field Crops Res. 92, 17–33.
Sharma, P. C., and Singh, R. K. (2008). Approaches to enhance salt tolerance in crop plants:
Progress and prospects. In ‘‘Crop Improvement: Strategies and Applications’’
(R. C. Setia, H. Nayyar, and N. Setia, Eds.), pp. 179–205. I.K. International Publishing
House Pvt. Ltd., New Delhi.
Sheehy, J., Elmido, A., Centeno, G., and Pablico, P. (2005). Searching for new plants for
Climate Change. J. Agric. Meteorol. 60, 463–468.
Climate Change Affecting Rice Production 119
Author's personal copy

Sheoran, I. S., and Saini, H. S. (1996). Drought-induced male sterility in rice: Changes in
carbohydrate levels and enzyme activities associated with the inhibition of starch accu-
mulation in pollen. Sexual Plant Reprod. 9, 161–169.
Singh, A. K., Choudhury, B. U., and Bouman, B. A. M. (2002). EVects of rice establishment
methods on crop performance, water use, and mineral nitrogen. In ‘‘Water-Wise Rice
Production’’ (B. A. M. Bouman, H. Hengsdijk, B. Hardy, P. S. Bindraban, T. P. Tuong,
and J. K. Ladha, Eds.), pp. 237–246. International Rice Research Institute, Los Banos,
Philippines.
Sombilla, M. A., Rosegrant, M. W., and Meijer, S. A. (2002). Along-term outlook of rice
supply and demand balances in South, Southeast and East Asia. In ‘‘Developments in the
Asian Rice Economy’’ (B. Sombilla, Hossain, and M. Hardy, Eds.), pp. 291–316. IRRI,
Los Ban
˜os, Philippines.
Song, Z. P., Lu, B. R., and Chen, J. K. (2001). A study of pollen viability and longevity in
Oryza rufipogon,O. sativa and their hybrids. IRRN 26, 31–32.
Stitt, M. (1991). Rising CO
2
levels and their potential significance for carbon flow in
photosynthetic cells. Plant Cell and Environment 14, 741–762.
Svensson, J., Ismail, A. M., Palva, T. E., and Close, T. J. (2002). ‘‘Cell and Molecular
Responses to Stress,’’ Elsevier Science, Amsterdam.
Tabbal, D. F., Bouman, B. A. M., Bhuiyan, S. I., Sibayan, E. B., and Sattar, M. A. (2002).
On-farm strategies for reducing water input in irrigated rice; case studies in the
Philippines. Agric. Water Manage. 56, 93–112.
Takeoka, Y., Al Mamun, A., Wada, T., and Kaufman, P. B. (1992). Primary features of
the effect of environmental stress on rice spikelet morphogenesis. Reproductive adapta-
tion of rice to environmental stress. “Developments on Crop Science,” Vol. 22, Chapter
5, pp. 113–141. Japan Scientific Societies Press, Elsevier, Tokyo.
Tanaka, K., Kasai, Z., and Ogawa, M. (1995). Physiology of ripening. In ‘‘Science of the
Rice Plant. Vol. 2. Physiology’’ (T. Matsuo, K. Kumazawa, K. I. Ishii, and H. Hirata,
Eds.), pp. 07–118. Food and Agriculture Policy Research Center, Tokyo.
Tang, R. S., Zheng, J. C., Jin, Z. Q., Zhang, D., Huang, H., and Chen, L. G. (2008).
Possible correlation between high temperature-induced floret sterility and endogenous
levels of IAA, GAs and ABA in rice (Oryza sativa L.). Plant Growth Regul. 54, 37–43.
Tao, F., Yokozawa, M., Zhang, Z., Hayashi, Y., Grassl, H., and Fu, C. (2004). variability in
climatology ang agricultural production with the East Asia summer monsoon and El
Nin
˜o South Oscillation, clim.Res. 28, 23–30.
Tester, M., and Davenport, R. (2003). Na+ tolerance and Na+ transport in higher plants.
Ann. Bot. 91, 503–527.
Thomson, M., Septiningsih, E., Suwardjo, F., Santoso, T., Silitonga, T., and McCouch, S.
(2007). Genetic diversity analysis of traditional and improved Indonesian rice (Oryza
sativa L.) germplasm using microsatellite markers. Theor. Appl. Genet. 114, 559–568.
Toojinda, T., Siangliw, M., Tragoonrung, S., and Vanavichit, A. (2003). Molecular genetics
of submergence tolerance in rice: QTL analysis of key traits. Ann. Bot. 91, 243–253.
Travasso, M. I., Magrin, G. O., Baethgen, W. E., Castao, J. P., Rodriguez, G. R.,
Rodriguez, R., Pires, J. L., Gimenez, A., Cunha, G., and Fernandes, M. (2006).
Adaptation measures for maize and soybean in Southeastern South America.
Working Paper No. 28, Assessments of Impacts andAdaptations to Climate Change
(AIACC), 38 pp.
Tripathy, J. N., Zhang, J., Robin, S., Nguyen, T. T., and Nguyen, H. T. (2000). QTLs for
cell-membrane stability mapped in rice (Oryza sativa l.) under drought stress. Theor. Appl.
Genet. 100, 1197–1202.
Tsukaguchi, T., and Yusuke, L. I. D. A. (2008). Effects of assimilate supply and high
temperature during grain filling period on the occurrence of various types of chalky
kernels in rice plants (Oryza sativa L.). Plant Prod. Sci. 11, 203–210.
120 R. Wassmann et al.
Author's personal copy

Uphoff, N. (2007). Agroecological alternatives: Capitalizing on existing genetic potentials.
J. Dev. Stud. 43, 218–236.
Vara Prasad, P. V., Craufurd, P. Q., Kakani, V. G., Wheeler, T. R., and Boote, K. J. (2001).
Influence of temperature during pre- and post-anthesis stages of floral development on
fruit-set and pollen germination in groundnut (Arachis hypogaea L.). Aust. J. Plant Physiol.
28, 233–240.
Vara Prasad, P. V., Craufurd, P. Q., and Summerfield, R. J. (1999). Fruit number in relation
to pollen production and viability in groundnut exposed to short episodes of heat stress.
Ann. Bot. 84, 381–386.
Venuprasad, R., Sta Cruz, M. T., Amante, M., Magbanua, R., Kumar, A., and Atlin, G. N.
(2008). Response to two cycles of divergent selection for grain yield under drought stress
in four rice breeding populations. Field Crops Res. 107, 232–244.
Vergara, B. S., and Mazaredo, A. (1975). Screening for resistance to submergence under
greenhouseconditions. In ‘‘Proceeding of the International Seminar on Deepwater Rice’’
pp. 67–70. Bangladesh Rice Res. Inst., Dhaka.
Wade, L. J., McLaren, C. G., Quintana, L., Harnpichitvitaya, D., Rajatasereekul, S.,
Sarawgi, A. K., Kumar, A., Ahmed, H. U., Sarwoto, A. K., Singh, A. K.,
Rodriguez, R., Siopongco, J., et al. (1999). Genotype by environment interactions across
diverse rainfed lowland rice environments. Field Crops Res. 64, 35–50.
Wahid, A., and Close, T. J. (2007). Expression of dehydrins under heat stress and their
relationship with water relations of sugarcane leaves. Biol. Plant. 51, 104–109.
Wahid, A., Gelani, S., Ashraf, M., and Foolad, M. R. (2007). Heat tolerance in plants: An
overview. Environ. Exp. Bot. 61, 199–223.
Warrag, M. O. A., and Hall, A. E. (1984). Reproductive responses of cowpea (vigna-
unguiculata (l) walp) to heat-stress.1. responses to soil and day air temperatures. Field
Crops Res. 8, 3–16.
Wassmann, R., Hien, N. X., Hoanh, C. T., and Tuong, T. P. (2004). Sea level rise affecting
the Vietnamese Mekong Delta: Water elevation in the flood season and implications for
rice production. Clim. Change 66, 89–107.
Webber, A. N., Nie, G. Y., and Long, S. P. (1994). Acclimation of photosynthetic proteins
to rising atmospheric co2. Photosynthesis Res. 39, 413–425.
Weerakoon, W. M. W., Maruyama, A., and Ohba, K. (2008). Impact of humidity on
temperature-induced grain sterility in rice (Oryza sativa L). J. Agron. Crop Sci. 194,
135–140.
Widodo, W., Vu, J. C. V., Boote, K. J., Baker, J. T., and Allen, L. H. (2003). Elevated
growth CO
2
delays drought stress and accelerates recovery of rice leaf photosynthesis.
Environ. Exp. Bot. 49, 259–272.
Xu, K., and Mackill, D. J. (1996). A major locus for submergence tolerance mapped on rice
chromosome 9. Mol. Breed. 2, 219–224.
Xu, K., Xu, X., Fukao, P., Canlas, R., Maghirang-Rodriguez, R., Heuer, S., Ismail, A. M.,
Bailey-Serres, J., Ronald, P. C., and Mackill, D. J. (2006). Sub1 A is an ethylene-
response-factor-like gene that confers submergence tolerance. Nature 442, 705–708.
Xu, K., Xu, X., Ronald, P. C., and Mackill, D. J. (2000). A high-resolution linkage map of
the vicinity of the rice submergence tolerance locus. Sub1. Mol. Gen. Genet. 263,
681–689.
Yadav, R., Flowers, T. J., and Yeo, A. R. (1996). The involvement of the transpirational
bypass flow in sodium uptake by high- and low-sodium-transporting lines of rice
developed through intravarietal selection. Plant Cell Environ. 19, 329–336.
Yamada, I. (1964). Studies on artificial germination and germination physiology of rice
pollen. Ph.D. Thesis Kyoto University, Kyoto. pp. 1–122
Yamaguchi, T., and Blumwald, E. (2005). Developing salt-tolerant crop plants: Challenges
and opportunities. Trends Plant Sci. 10, 615–620.
Climate Change Affecting Rice Production 121
Author's personal copy

Yamakawa, H., Hirose, T., Kuroda, M., and Yamaguchi, T. (2007). Comprehensive
expression profiling of rice grain filling-related genes under high temperature using
DNA microarray. Plant Physiol. 144, 258–277.
Yang, X., Bouman, B. A. M., Wang, H., Wang, Z., Zhao, J., and Chen, B. (2005).
Performance of temperate aerobic rice under different water regimes in North China.
Agricultural Water Management 74, 107–122.
Yeo, A. R., and Flowers, T. J. (1983). Varietal differences in the toxicity of sodium-ions in
rice leaves. Physiol. Plant. 59, 189–195.
Yeo, A. R., and Flowers, T. J. (1986). Salinity resistance in rice (oryza-sativa-l) and a
pyramiding approach to breeding varieties for saline soils. Aust. J. Plant Physiol. 13,
161–173.
Yeo, A. R., Yeo, M. E., Flowers, S. A., and Flowers, T. J. (1990). Screening of rice (oryza-
sativa-l) genotypes for physiological characters contributing to salinity resistance, and
their relationship to overall performance. Theor. Appl. Genet. 79, 377–384.
Yoshida, S., Satake, T., and Mackill, D. (1981). High temperature Stress. IRRI Res. Pap. 67,
1–15.
Zhang, H. X., and Blumwald, E. (2001). Transgenic salt-tolerant tomato plants accumulate
salt in foliage but not in fruit. Nat. Biotechnol. 19, 765–768.
Zhang, H. X., Hodson, J. N., Williams, J. P., and Blumwald, E. (2001). Engineering salt-
tolerant Brassica plants: Characterization of yield and seed oil quality in transgenic plants
with increased vacuolar sodium accumulation. Proc. Natl. Acad. Sci. USA 98, 12832–12836.
Zhu, J. K. (2003). Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 6,
441–445.
Zhu, Q. H., Ramm, K., Shivakkumar, R., Dennis, E. S., and Upadhyaya, N. M. (2004).
The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is
involved in anther development in rice. Plant Physiol. 135, 1514–1525.
Zhu, C., Xiao, Y., Wang, C., Jiang, L., Zhai, H., and Wan, J. (2005). Mapping QTL for
heat-tolerance at grain filling stage in rice. Rice Sci. 12, 33–38.
Ziska, L. H., and Manalo, P. A. (1996). Increasing night temperature can reduce seed set and
potential yield of tropical rice. Aust. J. Plant Physiol. 23, 791–794.
Ziska, L. H., Weerakoon, W., Namuco, O. S., and Pamplona, R. (1996). Influence of
nitrogen on the elevated CO
2
response in field-grown rice. Aust. J. Plant Physiol. 23,
45–52.
122 R. Wassmann et al.
Author's personal copy