Plant Breeding 132, 21–32 (2013)
© 2012 Blackwell Verlag GmbH

doi:10.1111/pbr.12004

Review
Drought stress adaptation: metabolic adjustment and regulation of gene
expression
S U J A T A B H A R G A V A 1 and K S H I T I J A S A W A N T
Department of Botany, University of Pune, Ganeshkhind, Pune, Maharashtra 411007, India; 1Corresponding author, E-mail:

With 2 figures and 2 tables
Received March 15, 2012/Accepted August 6, 2012
Communicated by R. Tuberosa

Abstract
Plants cope with drought stress by manipulating key physiological processes like photosynthesis, respiration, water relations, antioxidant and
hormonal metabolism. There exist multiple and often redundant stress
sensors, which transduce the stress signal through secondary signalling
molecules to the nucleus, where the expression of stress-response genes
is regulated. Transcription factors play an important role in regulating
the expression of the stress-response genes. Another level of regulation
of gene expression is at the epigenetic level and involves modifications
either at the chromatin level or at the mRNA level. Crop plants show
various adaptive and acclimatization strategies to drought stress, which
range from seemingly simple morphological or physiological traits that
serve as important stress tolerance markers to major upheavals in gene
expression in which a large number of transcription factors are induced.
Studies on contrasting crop genotypes or genetic engineering of crops
help in differentiating responses to drought from those leading to
drought tolerance. Of specific importance to crop plants is not whether

they survive stress, but whether they show good yields under stress conditions.

stress-induced damage. The molecular machinery involved in
drought stress perception, signalling and regulation of gene
expression has been fairly well understood. However, there are
lacunae in our understanding of how it correlates with phenotypic alterations in the plant (Blum 2011). On the other hand,
several phenotypic markers have been identified in crop plants
that correlate with drought tolerance, but we know little of either
the gene expression involved in these phenotypic traits or how
they correlate with the yield parameters.
The review attempts at going through the breadth of processes
involved in giving rise to a drought-response phenotype. Some
of these processes have been compared in contrasting genotypes
of crops, with the objective of understanding those that correlate
with better yields under drought conditions. Genetic engineering
of crop plants has also emerged as an important technique to
validate the role of specific genes in giving rise to the drought
phenotype.

Key words: crop adaptation — drought stress responses —
stress perception — stress signalling

Drought Responses of Plants

Global climate changes are leading to increases in temperature
and atmospheric CO2 levels as well as alterations in rainfall patterns. Periods of inadequate rainfall leading to drought are predicted to arise more frequently under such conditions. Terminal
drought conditions bring about a progressive decrease in soil
water availability to plants and cause premature plant death,
while intermittent drought conditions affect the plant growth and
development but are not usually lethal. The ability to survive

longer and maintain function under intermittent or terminal
drought conditions leads to subsistence yields, which are much
lower than those observed under hydrated conditions. Drought
tolerance enables plants to grow and maintain relatively high
yields in spite of drought conditions and is an outcome of the
plant’s efforts to withstand or recover from stress. If the tolerance is restricted to that particular generation, the plant is said to
be acclimated to drought. If it persists over generations, the plant
genotype is said to be adapted to drought conditions.
A large number of molecular, biochemical and physiological
processes at the cellular or whole plant level are altered in
response to drought and play an important role in mitigating
stress. What is crucial but difficult is to distinguish between the
responses that lead to tolerance from those that arise due to

A primary response of plants subjected to drought stress is
growth arrest. Shoot growth inhibition under drought reduces
metabolic demands of the plant and mobilizes metabolites for
the synthesis of protective compounds required for osmotic
adjustment. Root growth arrest enables the root meristem to
remain functional and gives rise to rapid root growth when the
stress is relieved (Hsaio and Xu 2000). Lateral root inhibition
has also been seen to be an adaptive response, which leads to
growth promotion of the primary root, enabling extraction of
water from the lower layers of soil (Xiong et al. 2006). Growth
inhibition can arise due to the loss of cell turgor arising from the
lack of water availability to the growing cells. Water availability
to cells is low because of poor hydraulic conductance from roots
to leaves caused by stomatal closure. Although a decrease in
hydraulic conductance decreases the supply of nutrients to the
shoot, it also prevents embolism in xylem and could constitute

an adaptive response. Osmotic adjustment is another way by
which plants cope with drought stress. Synthesis of compatible
solutes like polyols and proline under stress prevents the water
loss from cells and plays an important role in turgor maintenance
(Blum 2005, DaCosta and Huang 2006). Modification of growth
priorities as well as reduction in the performance of photosynthetic organs due to stress exposure leads to alterations in carbon

Growth and water relations

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S. BHARGAVA and K. SAWANT

partitioning between the source and sink tissues (Roitsch 1999).
Hence, carbohydrates that contribute to growth under normal
growth conditions are now available for selective growth of roots
or for the synthesis of solutes for osmotic adjustment (Lei et al.
2006, Xue et al. 2008).
Photosynthesis
Water deficit–induced ABA synthesis brings about stomatal closure, which causes a decrease in intercellular carbon dioxide
concentration and inhibits photosynthesis. This inhibition is
reversible and photosynthesis can resume if stomata open upon
stress removal (Chaves et al. 2009). On the other hand, open
stomata and high hydraulic conductance under drought enable
photosynthesis and nutrient supply to the shoot at the cost of
risking turgor loss (Sade et al. 2012). Some plants appear to
adopt the latter strategy to enable the synthesis of osmotic

metabolites from photoassimilates, which help in preventing turgor loss.
Carbon dioxide limitation due to prolonged stomatal closure
in the face of continued photosynthetic light reactions leads to
the accumulation of reduced photosynthetic electron transport
components, which can reduce molecular oxygen and give rise
to reactive oxygen species (ROS), thus causing indiscriminate
damage to the photosynthetic apparatus. This metabolic inhibition of photosynthesis is irreversible and leads to injury (Lawlor
and Cornic 2002). Hence, photophosphorylation and ATP generation is reduced, which inhibits Rubisco activity. Adaptive
responses to prevent drought-induced damage to photosynthetic
apparatus include thermal dissipation of light energy, photodestruction of D1 protein of PSII, the xanthophyll cycle, water–
water cycle and dissociation of the light-harvesting complexes
from photosynthetic reaction centres (Niyogi 1999, DemmigAdams and Adams 2006) (Table 1).

Respiration
Plant growth is determined by the ratio between photosynthetic
CO2 assimilation and respiratory CO2 release. The rate of respiration is regulated by processes that use the respiratory products
– ATP (water and solute uptake by roots, translocation of assimilates to sink tissues), NADH and TCA cycle intermediates (biosynthetic processes in growing parts of a plant), which together
contribute to plant growth. Under drought stress, these processes
are affected and lead to a decrease in respiration rate. On the
other hand, increased respiratory rates have also been observed
under water scarcity and these lead to an increase in the intercellular CO2 levels in leaves (Lawlor and Tezara 2009). Higher respiration may arise due to uncoupling of respiratory oxygen
evolution from oxidative phosphorylation, which prevents the
accumulation of reductants and reduces the generation of ROS.
Increased respiratory rates are also observed due to the activation
of energy-intensive processes like osmolyte synthesis and antioxidant metabolism that occur under drought conditions.
Interdependence of metabolic processes in chloroplasts and
mitochondria has been reported (Raghavendra and Padmasree
2003). For example, mitochondria are involved in processing the
glycolate produced in chloroplasts during photorespiration (Taira
et al. 2004). Mitochondrial respiration also plays an important

role in dissipating the NADPH generated during photosynthetic
light reactions through type II NADPH dehydrogenases situated
on the matrix side (Plaxton and Podesta 2006). Hence, leaf mitochondria act as a safety engine that enables the plant to cope
with variations in chloroplast metabolism under water stress
(Atkin and Macherel 2009). Plant mitochondria also prevent
ROS generation within themselves by employing the alternative
oxidase (AOX) pathway, in which the complexes III and IV of
the respiratory electron transport system are bypassed and electrons are directly transferred to oxygen, with the generation of
thermal energy instead of ATP (Siedow and Umbach 2000). The

Table 1: Physiological responses contributing to drought tolerance in plants
No.
1

Responses

Function

2

Adjustment of chlorophyll antenna size.
Photodestruction of D1 protein of PSII
Thermal dissipation of light energy

3

Xanthophyll cycle, water–water cycle

4


Stomatal closure, reduced hydraulic
conductance.
Delay in stomatal closure under stress
Altered source–sink relations and carbon
partitioning

Prevention of water loss through transpiration.
Maintenance of photosynthetic activity under stress

7

Alternative oxidase pathway, uncoupling
proteins, NADPH dehydrogenases
Prohibitins

8

GABA shunt

9

Antioxidant enzymes and substrates

Uncoupling of oxidative phosphorylation and electron
transport
Maintenance of protein structure in inner mitochondrial
membranes
Bypass in TCA cycle, prevents the generation of
reductants
Scavenging ROS


10
11

Synthesis of osmotically active solutes
ABA biosynthesis

5
6

ROS, reactive oxygen species.

Reduction in photosynthetic electron
transport
Uncoupling of photophosphorylation and electron
transport
Protection against ROS generated in chloroplasts

Induction of root growth, inhibition of shoot growth
Osmolyte synthesis

Osmotic adjustment
Stomatal closure, regulation of aquaporin activity,
inhibition of ethylene accumulation

References
Niyogi (1999)
Vass et al. (2007)
Kopecky et al. (2005)
Demmig-Adams and Adams (2006)

Asada (1999)
Jahns and Holzwarth (2012)
Ghannoum (2009)
Sade et al. (2012)
Roitsch (1999)
Lei et al. (2006)
Xue et al. (2008)
Xu et al. (2011)
Van Aken et al. (2010)
Fait et al. (2007)
Miller et al. (2010)
Rouhier et al. (2006)
Shao et al. (2008)
DaCosta and Huang (2006)
Thameur et al. (2011)
Parent et al. (2009)
Sharp (2002)


Drought stress adaptation

AOX pathway as well as the photorespiratory pathway is operational when a plant is exposed to stress and serves a role in
maintaining cell function by preventing the accumulation of
ROS (Lambers et al. 2005, Florez-Sarasa et al. 2007).
In addition, the TCA cycle is modified to prevent the generation of excess reductants. One of the modifications is GABA
synthesis, in which two steps in the TCA cycle related to the
generation of reducing power are bypassed. GABA accumulation
occurs during stress conditions and may constitute a stress adaptive response (Fait et al. 2007).
Prohibitins are large protein complexes that localize to the
inner mitochondrial membrane, where they appear to play a role

in maintaining the superstructure of the inner mitochondrial
membrane and the protein complexes associated with it (Van
Aken et al. 2010). They have been implied in stress tolerance
not only because of their role in protecting mitochondrial structure, but also in triggering retrograde signalling between mitochondria and the nucleus in response to stress, thus altering the
expression of several stress-responsive transcripts, including
AOX, heat-shock proteins (HSP) and genes involved in hormone
homoeostasis.
Antioxidant metabolism
Reactive oxygen species are generated due to metabolic perturbation of cells, and these cause cell damage and death. While
mechanisms to prevent the generation of ROS have been mentioned earlier, an important adaptive mechanism consists of their
effective scavenging if and when these harmful species do arise.
Antioxidant substrates like ascorbate, a-tocopherol and carotenoids and antioxidant enzymes like superoxide dismutase, catalase, ascorbate peroxidase and glutathione reductase exist in cell
organelles and the cytoplasm and play an important role in
detoxifying these reactive species (Shao et al. 2008). Methionine
sulfoxide reductases are another class of antioxidant enzymes
that play a role in preventing damage to proteins due to ROS
generation in plastids (Rouhier et al. 2006). These enzymes use
thioredoxin to reduce the methionine sulfoxide residues generated in proteins due to oxidative stress.
Hormonal regulation
Plant hormones regulate diverse processes in plants, which
enable acclimation to stress. On exposure to water deficits,
ABA synthesized in roots is known to be translocated to leaves,
where it brings about stomatal closure and inhibits plant
growth, thus enabling the plant to adapt to stress conditions
(Wilkinson and Davies 2010). In barley, fivefold increase in
endogenous ABA levels was observed in drought-tolerant varieties as compared to susceptible ones, indicating its role in
improving stress tolerance (Thameur et al. 2011). The role of
ABA in regulating aquaporin activity, which contributes to the
maintenance of a favourable plant water status, has also been
reported (Parent et al. 2009). Improvement of shoot growth

under drought was observed when 9-cis-epoxycarotenoid dioxygenase (NCED3), a key enzyme in abscisic acid biosynthesis,
was overexpressed in Arabidopsis (Iuchi et al. 2001). ABA
accumulation during the expression of drought tolerance is
known to bring about a reduction in ethylene production and
an inhibition of ethylene-induced senescence and abscission.
ABA-deficient maize seedlings showed drought susceptibility as
well as an increase in ethylene production (Sharp 2002). Auxins
have been identified as negative regulators of drought tolerance.

23

In wheat leaves, drought stress tolerance was accompanied by a
decrease in ndole-3-acetic acid (IAA) content (Xie et al. 2003).
Downregulation of IAA was seen to facilitate the accumulation
of late embryogenesis-abundant (LEA) mRNA, leading to
drought stress adaptation in rice (Zhang et al. 2009). However,
there are evidences of a transient increase in IAA content in
maize leaves during the initial stages of exposure to water
stress, which later drops sharply as the plant acclimates to water
stress (Wang et al. 2008). A rapid decline in endogenous zeatin
and gibberellin (GA3) levels was also observed in maize leaves
subjected to water stress, which correlated with higher levels of
cell damage and plant growth inhibition. Reduced cytokinin
content and activity caused by either reduced biosynthesis or
enhanced degradation was observed in drought-stressed plants.
(Pospisilova et al. 2000). In alfalfa, decreased cytokinin content
during drought led to accelerated senescence (Goicoechea et al.
1995). Cytokinins are known to delay senescence, and an
increase in the endogenous levels of cytokinins through the
overexpression of the ipt gene involved in cytokinin biosynthesis led to stress adaptation by delaying drought-induced senescence (Peleg and Blumwald 2011). Cytokinins are also negative

regulators of root growth and branching, and root-specific degradation of cytokinin contributed to primary root growth and
branching induced by drought stress, hence increasing drought
tolerance in Arabidopsis (Werner et al. 2010).
Brassinosteroids (BRs) have also been reported to protect
plants against various abiotic stresses (Kagale et al. 2007).
Application of BR was seen to increase water uptake and membrane stability, as well as to reduce ion leakage arising from
membrane damage in wheat plants subjected to drought stress
(Sairam 1994). However, it was shown that changes in endogenous BR levels did not occur during the exposure of pea plants
to water stress (Jager et al. 2008).

Stress Perception and Signalling
Acclimation to stress involves processes starting from perception
of stress to the expression of large number of genes involved in
the manifestation of a morphological or physiological response
that increases the chances of survival under the stress condition
(Fig. 1).
Stress perception
Molecular mechanisms that sense stress consist of a number of
classes of cell surface receptors like serine/threonine-like
receptor kinases called receptor-like kinases (RLKs), ion channel
–linked receptors, G-protein-coupled receptors (GPCRs) and
two-component histidine kinase receptors. RLKs are major contributors to the processing of a vast array of plant developmental
and environmental cues. Their activity is regulated by receptor
oligomerization and phosphorylation, receptor internalization and
dephosphorylation or regulation at the transcriptional level (Chae
et al. 2009). Brassinosteroid receptor BR1 belongs to the RLK
family, which in response to BR or stress is internalized by the
responding cells and the stress signal transduced. Cre 1 (cytokinin response 1) is a two-component histidine kinase receptor that
transduces signal via a phosphorelay pathway. This receptor
kinase, besides binding cytokinins, is also thought to act as a

sensor of osmotic stress (Bartels and Sunkar 2005). Ca2+ channels are responsible for the influx of Ca2+ into the cytoplasm
when activated by various stress situations (Xiong et al. 2002).
These channels therefore act as ion channel–linked receptors of


24

S. BHARGAVA and K. SAWANT

Fig. 1: Signalling cascade from
perception of the drought signal to
the regulation of gene expression

stress. GPCRs are another group of membrane receptors, which
on sensing stress activate enzymes like phospholipase C or D
which in turn release second messengers and transduce the stress
signal (Tuteja and Sopory 2008).
An intracellular receptor for ABA, PYR/RCAR, has been
shown to signal for drought stress through the activation of a
serine/threonine kinase SnRK2, in response to ABA binding
(Sheard and Zheng 2009). Because ABA synthesis is known to
be induced in response to stress, the ABA receptor can be considered to be a stress sensor.
Sugar signalling has emerged as an important component of
stress responses. Hexokinases were identified as glucose sensors
in plants, which played a role in repressing photosynthetic gene
expression when the hexose levels in leaf cells were high (Kim
et al. 2000, Hanson and Smeekens 2009). The trehalose biosynthesis pathway, in which trehalose 6 phosphate (T6P) acts as an
indicator of G6P and UDPG pool size, is known to link growth
and development to metabolite content, because both sucrose
synthesis and trehalose synthesis pathways feed into the same

metabolite pool (Vogel et al. 2001, Paul et al. 2008). Trehalose
phosphate phosphatases are upregulated under stress conditions
and in turn regulate the T6P levels. Hence, multiple facets of
drought stress appear to be simultaneously perceived by a cell
through various receptors that respond to osmotic pressure,
membrane rigidity, metabolic status, Ca2+-level perturbations,
respectively, thereby ensuring plant response and improving the
chances of survival on drought exposure.

Reactive oxygen species, which are toxic by-products of stress
metabolism, also serve as important signalling molecules (Miller
et al. 2010) and the oxidative signal is transduced via secondary
signalling intermediates like Ca2+ or phosphatidic acid (PA)–
activated serine/threonine protein kinases and mitogen-activated
protein (MAP) kinases to bring about transcription of genes that
play a role in acclimation (Cheeseman 2007). Due to the short
half-life of ROS, redox signalling is likely to occur through the
redox status of ascorbate/dehydroascorbate and reduced glutathione/oxidized glutathione couples (Foyer and Noctor 2000).
Nitric oxide radical (NO) is synthesized in plants, probably
either from arginine via a nitric oxide synthase or by nitrite
reduction, and has been shown to be a component of secondary
messenger cascades (Mazid et al. 2011), involving cyclic GMP
and Ca2+.
Signal transduction
Signal perception is followed by the generation of secondary
signalling molecules such as protein kinases and phosphatases
(serine/threonine phosphatases), phospholipids like phosphoinositides (Bartels and Sunkar 2005), ROS, Ca2+, nitric oxide, cAMP
and sugars, which play an important role in signal transduction
(Tuteja and Sopory 2008). Many of these secondary messengers
are common to diverse stress situations, indicating that cross-talk

between different stress-response pathways may occur through
these common signal transducers.


Drought stress adaptation

Mitogen-activated protein kinases bring about protein phosphorylation and constitute one of the major mechanisms for signal transduction. They are located in the cytoplasm and consist
of three classes of enzymes (MAPK, MAPKK and MAPKKK)
that form a signalling cascade from the stress sensor located on
the plasma membrane to the regulation of gene expression in the
nucleus. Translocation of the MAPK into the nucleus brings
about the activation of transcription factors through phosphorylation (Tena et al. 2001).
Calcium levels in the cytoplasm have been shown to increase
transiently on stress exposure. The source of this stress-induced
cytoplasmic Ca2+ is either from the apoplast or from the cellular
reserves. Several Ca2+ sensors like calmodulin (CaM) or CaMbinding proteins have been identified in the cells, which transduce the stress signal to the nucleus through other messengers
like phospholipase D or Ca2+-dependent protein kinases (Tuteja
and Sopory 2008).
Phospholipids like phosphoinositides that are located in the
plasma membranes are a source of several secondary signalling
molecules like phosphotidylinositol phosphates, which are phosphorylated by kinases (e.g. PI3Kase) (Drobak and Watkins
2000). Phospholipases act on these phospholipids to generate
signalling molecules like inositol 1,4,5-trisphosphate (IP3), diacylglycerol (DAG) and PA, which play a role in the transmission
of the signal across plasma membrane and in intracellular signalling.
Transcriptional regulation of gene expression
A large number of genes are seen to be involved in the expression of the stress phenotype (Xiong et al. 2002, Shinozaki and
Yamaguchi-Shinozaki 2003). The transcriptional response initially is composed of a core set of multistress-responsive genes
and becomes increasingly stress specific as time progresses (Ma
and Bohnert 2007). DNA microarrays provide a high-throughput
means of analysing gene expression at the whole-genome level

and have been used to study the patterns of gene expression in
response to drought or high-salinity stresses in several plant species (Seki et al. 2002, Guo et al. 2009, Hayano-Kanashiro et al.
2009).
Some of the genes seen to be upregulated under drought stress
conditions include the genes involved in osmolyte synthesis,
genes coding for LEA proteins, aquaporins, signalling molecules
and transcription factors (TFs). Of these, the genes coding for
TFs were particularly interesting because TFs act as master
switches and trigger the simultaneous expression of a large number of stress-response genes that contribute to the stress phenotype (Bartels and Souer 2004). About 104 TFs, whose
expression was increased on exposure to dehydration stress, have
been identified by transcriptome analysis in Arabidopsis plants
exposed to drought stress (Rhizsky et al. 2004). While most of
the transcription factors were upregulated under stress, a few
transcription factors that played a role in primary growth processes were downregulated. Drought stress–induced gene expression was seen to be regulated by TFs belonging to bZIP, AP2/
ERF, HD-ZIP, MYB, bHLH, NAC, NF-Y, EAR and ZPT2 families (Yang et al. 2010). These TFs are activated at the transcriptional or protein level by the transduced drought signal. Because
drought stress is accompanied by an increase in ABA levels,
some TFs are activated specifically by ABA. The ABA-responsive TFs (ABFs) predominantly belong to the bZIP family of
TFs and bind to ABA-response elements (ABRE) present in the
promoters of stress-response genes (Jakoby et al. 2002, Yoshida

25

et al. 2010). TFs belonging to the AP2/ERF family bind to the
drought-response element (DRE) present in their promoters of a
large number of drought-response genes (Yamaguchi-Shinozaki
and Shinozaki 2005, Maruyama et al. 2009). The HD-ZIP TFs
are plant specific and show the presence of a homeodomain adjacent to leucine zipper. Among several functions attributed to this
family of transcription factors, one function is the regulation of
ABA-dependent genes under dehydration stress (Deng et al.
2002). Most of the plant MYBs consist of two repeats R2R3 (Jin

and Martin 1999) and play a role in regulating the expression of
dehydration-responsive genes (Abe et al. 2003). The ZPT2 TFs
are characterized by the presence of two zinc finger motifs separated by a single long linker. These act as transcriptional repressors by downregulating the activity of other transcription factors
(Sakamoto et al. 2004) and are induced during dehydration stress
as well as with ABA treatment. Transcription factors belonging
to NAC family bind to promoters of not only dehydrationresponse genes (Tran et al. 2004), but also auxin-response genes
(Hegedus et al. 2003).
The promoters of stress-response genes are known to have
several types of cis elements to which TFs of the same family or
different families can bind (Narusaka et al. 2003, Srivastav et al.
2010). Hence, gene expression under different stress situations
can be combinatorially regulated by employing suitable TFs,
which often form homo- or heterodimers in bringing about transcriptional activation under specific stress situations. However,
manipulations of transcription factors in engineering complex
traits such as abiotic stress tolerance are known to produce unintended pleiotropic effects which may have adverse effects on the
growth and development of plants (Abdeen et al. 2010).
Post-transcriptional regulation of gene expression
Besides stress-induced regulation of gene expression at the transcription level, stress conditions also bring about epigenetic regulation of gene expression (Table 2). Stress-induced changes in
histone variants, histone N-tail modifications and DNA methylation have been shown to regulate stress-responsive gene expression and plant development under stress. Drought stress induced
the expression of a variant of histone H1 called H1-S, which
appeared to play a role in stomatal closure (Scippa et al. 2004).
ABA downregulated the expression of a histone deacetylase
AtHD2C, while overexpression of this enzyme brought about
enhanced expression of ABA-responsive genes and greater salt
and drought tolerance than the wild-type plants (Sridha and Wu
2006). Drought-induced expression of stress-responsive genes
was also seen to be associated with modifications in histones H3
and H4. Histone H3K4 trimethylation, H3K9 acetylation, H3
Ser-10 phosphorylation, H3 phosphoacetylation and H4 acetylation were observed, which correlated with the expression of
stress-induced genes (Sokol et al. 2007). Histone acetyltransferases (HATs), which interact with transcription factors, were also

seen to be involved in activating stress-responsive genes. Stresses can induce changes in gene expression through hypomethylation or hypermethylation of DNA. In tobacco, stress-induced
DNA demethylation was observed in the coding sequence of a
glycerophosphodiesterase-like protein gene, while DNA hypermethylation was induced by drought stress in pea (Chinnusamy
and Zhu 2009).
MicroRNAs (miRNAs) are ~20- to 22-nt non-coding RNAs
that specifically base pair to target mRNAs and induce the cleavage of target mRNAs or repress their translation. Hence, they constitute a gene-silencing mechanism that regulates the expression


26

S. BHARGAVA and K. SAWANT

Table 2: Epigenetic regulation and RNA-related processes in response to drought stress
Regulatory process
Histone/DNA modifications
Histone variants – Chromatin state regulation
Histone modifications – Chromatin state regulation

DNA methylation – Chromatin state regulation
RNA-mediated regulation
miRNA-/siRNA-mediated gene silencing
RNA helicase-mediated rearrangement of RNA
secondary structure
RNA chaperone-mediated
RNA misfolding correction
Alternate splicing – intron retention and
generation of non-sense codons in TFs
RNA stress granules (SG) and processing bodies
(P-bodies) – temporary storage of mRNA
in cell, translation repression

Post-translational regulation
Phosphorylation
Ubiquitination
Sumoylation

Details
H1S substitutes H1
Downregulation of HDACs
Upregulation of HATs
H3K4 methylation, H3 K9 acetylation,
H3S10 phosphorylation, H4 acetylation
Demethylation,
Hypermethylation

References
Scippa et al. (2004)
Sokol et al. (2007)

Chinnusamy and Zhu (2009)

miR398, miR393, miR159, miR169, miR172, miR395
NATsiRNAs, tasiRNAs
PDH45, PDH47

Sunkar et al. (2006); Shukla et al.
(2008); Calvino et al. (2011)
Owttrim (2006)

CspA, CspB


Castiglioni et al.(2008)

Wdreb2
CCA1/LHY
SGs containing marker proteins eIFE4, RBP47, UBP1.
P-bodies with DCP1, DCP2, XRN4 activities

Egawa et al. (2006); Filichkin et al.
(2010)
Weber et al. (2008)
Xu and Chua (2011)

ABFs/AREBs,
XERICO
AtSUMO1, AtSUMO2

Kline et al. 2010,
Ko et al. 2006,
Kurepa et al. 2003

HATs, histone acetyltransferases; SUMO, small ubiquitin-like modifier.

of target genes post-transcriptionally. Regulation of stressresponse genes by miRNAs has been demonstrated recently (Shukla et al. 2008). For example, abiotic stress brought about downregulation of miR398 that targets stress-inducible Cu-Zn SOD
genes that play a role in scavenging superoxide radicals generated
in plants on exposure to stress (Sunkar et al. 2006). MiRNA159
was seen to be upregulated in response to ABA, and this miRNA
silenced several MYB transcription factors that are known to positively regulate ABA responses. MiR169 regulated target genes for
carbohydrate metabolism, leading to stem sugar accumulation in
sweet sorghum (Calvino et al. 2011). MiRNAs miR172 and
miR395 were reported to target genes related to time of flowering

and permitted greater biomass build-up.
The mRNA transcribed is processed to give rise to the mature
mRNA, and RNA-binding proteins are involved in post-transcriptional RNA modifications through processes like splicing and
regulation of its stability and turnover. Under stress conditions,
alternative splicing of some mRNAs coding for transcription factors has been reported in wheat (Egawa et al. 2006). There are
reports indicating the occurrence of alternative splicing in at least
42% of genes in Arabidopsis during abiotic stress conditions (Filichkin et al. 2010, Nakaminami et al. 2012). Degradation or stabilization of mRNA levels under stress conditions is brought
about by processing bodies (PBs) and stress granules (SGs),
respectively (Weber et al. 2008, Xu and Chua 2011). P-bodies
are RNP complexes known to play a role in translational repression and mRNA decapping. Removal of 5′ m7GDP by decapping
proteins (DCP1, DCP2) from the mRNA cap takes place in Pbodies, which leads to further degradation of the mRNA by exonucleases (XRN4). SGs have been shown to contain nuclear proteins (UBP1 and RBP47), polyA+ mRNA and translation
initiation factors, which under stress conditions are observed as
distinct complexes in the cytoplasm (Weber et al. 2008).
Post-translational modification of proteins also plays an important role in the drought stress response. The importance of phosphorylation cascades in signal transduction has already been

mentioned earlier. Protein modifications are also known to affect
the conformation, activity, localization and stability of transcription factors (Kline et al. 2010). Ubiquitin-dependent protein degradation is another post-translational protein modification, which
was shown to play an important role in hormonal signalling
(Santner and Estelle 2009). Upregulation of an E3 ubiquitin ligase
XERICO in Arabidopsis enhanced the expression of an ABA biosynthesis gene, AtNCED3, thereby increasing the cellular ABA
levels and hence drought tolerance (Ko et al. 2006). In addition
to ubiquitin, plants use a variety of other polypeptide tags to posttranslationally modify and regulate various intracellular proteins.
Small ubiquitin-like modifier (SUMO) is one such peptide that
brings about sumoylation. In Arabidopsis, the amount of
AtSUMO1 and AtSUMO2 conjugates increased in response to
various stress treatments, and when these were overexpressed, the
increased sumoylation levels induced ABA-/stress-responsive
genes by masking ubiquitin sites on regulatory proteins (Kurepa
et al. 2003). Hence, the post-translational modifications like
sumoylation and ubiquitination modulate plants response to

stress.

Drought Adaptation Strategies in Crop Plants
Drought-tolerant plants like xerophytes, halophytes, resurrection
plants show morphological and physiological adaptations to cope
with poor water availability either through growth arrest till
favourable conditions return, or through shortened growth cycles
comprising limited vegetative growth followed by flowering and
seed set during the short periods of water availability. Such
adaptations are not desirable traits in crop species, which
develop large yields over long growth periods. Genotypes that
differ in drought tolerance serve as important systems for studying adaptive responses to drought in crop species, and
exploitation of natural variation for drought-related traits has
resulted in an improvement of crop performance (Ribaut et al.
2004, Reynolds and Tuberosa 2008).


Drought stress adaptation

27

Physiological studies on contrasting genotypes provide information on the mechanisms involved in drought tolerance and
provide a useful screening strategy for drought tolerance, albeit
at a smaller scale and often in an ‘unnatural’ drought exposure
(Fig. 2). For example, drought tolerance in durum wheat was
attributed to alterations in mitochondrial metabolism. The mitochondria showed an active AOX pathway and an uncoupling
protein, both of which played a role in the dissipation of energy
and prevented the accumulation of ROS (Pastore et al. 2007). In
addition, the cytosolic NADH produced was oxidized by an
active malate/oxaloacetate shuttle in the mitochondria. On comparing drought responses of wheat genotypes with the related

Aegilops biuncialis genotypes, a higher photosynthetic activity
was observed in Aegilops, which are adapted to drier habitats.
Higher CO2 fixation was attributed to better stomatal conductance and more efficient non-radiative energy dissipation in
Aegilops (Molnar et al. 2002). In comparisons made between
drought-tolerant and drought-susceptible sorghum genotypes, it
was observed that the genotypes differed in stress thresholds at
which transition from stomatal to metabolic inhibition of photosynthesis occurred (Bhargava and Paranjpe 2004). This has
important implications because stomatal inhibition of photosynthesis is reversible and an ability to delay metabolic inhibition of
photosynthesis would facilitate the recovery from stress. Tolerant
genotypes of sorghum were also seen to have higher levels of
Rubisco under drought stress than susceptible genotypes, and
this correlated with higher transcript levels of the chloroplast
chaperone HSP60, which probably protected the Rubisco protein
from drought-induced damage (Jagtap et al. 1998). Source–sink
relationships also play an important role in drought tolerance of
crop plants because carbohydrate reserves are utilized for grain
filling and their availability is a critical factor in sustaining grain
filling and grain yield under drought stress (Yang and Zhang
2006). Although osmotic adjustment is another mechanism for
coping with drought stress, it is seen to be of relevance mainly
in root development into deeper soils, which can give plants
access to water. This was seen in wheat lines showing better

osmotic adjustment as compared to those showing low osmotic
adjustment (Morgan 1995). However, in drought-tolerant genotypes of prairie junegrass, genes involved in proline and fructan
biosynthesis were seen to play an important role in drought tolerance (Jiang et al. 2010). Efficiency of antioxidant metabolism
in protecting plants against oxidative damage has been reported
in drought-tolerant crop genotypes as compared to drought-susceptible ones. Drought-tolerant genotypes of sorghum showed
higher activities of antioxidant enzymes on exposure to stress,
but not under non-stress conditions (Jagtap and Bhargava 1995).

An increase in activities of specific isozymes of antioxidant
enzymes has also been reported in drought-tolerant rapeseed
genotypes subjected to drought stress (Abedi and Pakniyat
2010). However, a drought-tolerant genotype Oryza longistaminata of rice accumulated smaller amounts of ROS as well as
antioxidant substrates, indicating that it had other acclimation
mechanisms that prevented oxidative stress (Kumar et al. 2011).
The role of ABA in drought tolerance has been studied in barley
genotypes differing in their ability to survive water-limiting conditions (Thameur et al. 2011). Drought tolerance correlated with
an increase in ABA accumulation, and the genotype showing
highest tolerance had fivefold more ABA levels as compared to
the susceptible genotype.
At the molecular level, differences in gene expression in
drought-susceptible and drought-tolerant genotypes have been
observed. Generally, the genes involved in protecting plants
from drought stress through stress perception, signal transduction, transcriptional regulatory networks in cellular responses or
tolerance to dehydration were seen to be upregulated in droughttolerant barley genotypes, while those concerned with primary
metabolic processes like photosynthesis were downregulated
(Guo et al. 2009). In tolerant land races of maize, genes encoding hormones, aquaporins, HSPs, LEAs and detoxification
enzymes were induced to a greater extent than in the susceptible
land races (Hayano-Kanashiro et al. 2009).
Many of the drought-related traits have been tagged using
molecular markers, and the loci associated with these traits

Morpho-physiological

Fig. 2: Stress factors
adaptive traits in crops

and


stress

Root architecture – Rice (Steele et al. 2007)
Anthesis-silking time – Maize (Duvick 2005)
Stay-green phenotype – Sorghum (Harris et al. 2007)
Reversible inhibition of photosynthesis – Sorghum (Bhargava and
Paranjpe, 2004)
Mitochondrial alternative oxidase – Wheat (Pastore et al. 2007)
Antioxidant enzymes – Sorghum (Jagtap and Bhargava, 1995)
Osmotic adjustment – Junegrass (Jiang et al. 2010)
ABA biosynthesis – Barley (Thameur et al. 2011)

Gene regulation
Signalling pathway
intermediates and stress
induced transcription
factors – Barley (Guo et
al. 2009)
Aquaporins, HSPs,
LEAs – Maize (HayanoKanashiro et al. 2009)


28

[quantitative trait loci, (QTLs)] have been used to select genotypes that are able to yield better under field drought conditions.
For example, the ‘anthesis-silking interval’ typically increased
under water deficit and negatively correlated with yield in maize
(Duvick 2005). Screening genotypes for QTLs associated with
lower anthesis-silking interval enabled the identification of genotypes showing better yields under water-limiting conditions. In
sorghum, genotypes resistant to post-flowering drought stress,

referred to as the stay-green phenotypes, have been shown to
have a positive impact on yield under terminal drought. Four
major QTLs designated as Stg2, Stg3 and Stg4 and additional
minor QTLs were identified in sorghum, which modulate the
expression of the stay-green trait (Harris et al. 2007). In rice, a
QTL with a large effect on grain yield in upland rice growing
under drought stress was associated with improved root architecture (Bernier et al. 2007). In maize, QTLs like root-ABA and
root-yield-1.06 were identified, which were associated with root
traits, ABA concentration as well as agronomic traits, especially
grain yield across water regimes. These QTLs have been used to
improve yield stability in maize under water-limiting conditions
by marker-assisted selection (Landi et al. 2005, 2010). In cotton,
QTLs for a physiological trait like low osmotic potential showed
a strong association with plant height as well as with productivity in water-limiting conditions. Eleven QTLs associated with
low osmotic potential were seen to be associated with thirteen
QTLs associated with seed cotton yield (Saranga et al. 2004).
Similarly, two significant QTLs affecting osmotic potential
(qtlOP-2) and plant height (qtlPH-1) under drought conditions
were also identified (Saeed et al. 2011). Such QTLs have been
used for developing high-yielding cotton cultivars under waterstress conditions using marker-assisted selection. In wheat, two
QTLs were found to be associated with plant height, kernel
weight and yield under varying water availability (Maccaferri
et al. 2008). However, contribution of QTLs to a trait is often
low and QTLs associated with adaptive responses to drought differ across environments, while those that are constitutive are stable across environments (Collins et al. 2008). Dissecting the
phenotypic traits into smaller and simpler traits, which show
high heritability in genotypes exhibiting drought tolerance, has
led to the identification of stable QTLs associated with these
traits across diverse environments (Tardieu and Tuberosa 2010).
Identification of stable QTLs enables gene discovery through
map-based cloning, and this serves as an important input in

breeding for drought tolerance using transgenic approaches. Two
approaches have been mainly used for the molecular dissection
of a QTL: positional cloning and association mapping. Positional
cloning enables the identification of the genetic and physical
interval cosegregating with the QTL, while association mapping
establishes a statistical association between allelic variation at a
locus and the phenotypic value of a trait across a large number
of unrelated accessions. Identification of the candidate genes
associated with a QTL is difficult because a QTL is known to
span a large genomic region. For example, a QTL was shown to
span a region of over 12 Mb and 310 genes in maize (Salvi and
Tuberosa 2005). A few genes identified from the QTL regions
include the CRY2 gene that is involved in cryptochrome synthesis from the rice QTL for flowering time ED1, or a gene coding
for a transcription factor from the plant architecture QTL Tb1 in
maize (Salvi and Tuberosa 2005). The candidate genes or
sequences that cosegregate with the QTL are then functionally
tested with reverse genetics tools based on gene tagging, TILLING or RNAi and validated for function by producing transgenic
plants (Tuberosa and Salvi 2006).

S. BHARGAVA and K. SAWANT

Transgenic Technology for Improved Drought
Tolerance in Crops
Drought tolerance has been achieved using genetic engineering
strategies to improve (i) water-use efficiency of plants, (ii) cell
protection mechanisms against ROS, (iii) hormonal balance to
alter the growth and development in order to avoid drought and
(iv) alter the expression of drought-induced transcription factors
that act as master switches in regulating a large number of
downstream drought-response genes.

Late embryogenesis-abundant proteins are known to accumulate during seed desiccation and in vegetative tissues when plants
experience water deficit. Transgenic expression of a group 3
LEA protein from barley (HVA1) showed improved drought and
salt tolerance in rice and wheat plants (Xu et al. 1996, Sivamani
et al. 2000). Overexpression of trehalose or polyamines was also
seen to confer tolerance to abiotic stress in rice (Garg et al.
2002, Capell et al. 2004). Transgenic alfalfa plants overexpressing the antioxidant enzyme superoxide dismutase showed
improved tolerance to drought stress (McKersie et al. 1996).
Transgenic rice plants overexpressing the isopentenyl transferase
(IPT) gene, which plays a role in cytokinin biosynthesis, showed
increased expression of brassinosteroid-related genes and repression of jasmonate-related genes (Peleg et al. 2011). Besides
alterations in hormone homoeostasis, the transgenic rice plants
also showed a change in source–sink relationships and a stronger
sink capacity when subjected to water limitation.
Attempts at overexpressing TFs that show higher expression
under drought stress in tolerant as compared to susceptible genotypes (Hayano-Kanashiro et al. 2009) have led to an improvement
of drought tolerance in several crops. Wheat transgenics expressing the DREB1 gene from Arabidopsis showed better tolerance to
drought under glasshouse conditions (Pellegrineschi et al. 2004).
Rice transgenics overexpressing ABA-inducible TF (ABF3) or
drought-inducible TF (DREB2) showed improved survivability
and significantly higher number of panicles, respectively, in
response to drought stress, as compared to wild-type plants (Oh
et al. 2005, Bihani et al. 2011). Overexpression of OsbZIP23 in
rice exhibited significantly improved tolerance to drought and high
salinity and sensitivity to ABA (Hadiarto and Tran 2011).
Although transgenic technologies provide a targeted approach
for improving drought tolerance, the transgenic plants are often
tested under ‘unnatural’ stress conditions and it is not clear
whether they would also give rise to better yields under field
stress conditions. However, such studies are important as they

give an indication of genes that could serve as potential candidates for improving stress tolerance in crops, because the slow
progression of dehydration that is seen in the field does not lead
to drastic changes in gene expression that are observed in potted
plants (Barker et al. 2005).

Climate Change and Crop Adaptation
Drought stress, especially in the tropics, is accompanied by
high temperature stress, and the responses of crops to a combination of these two stress factors appear to differ from the
responses to either of the stresses applied singly (Sreenivasulu
et al. 2007). Hence, yield responses of crop plants when
exposed to abiotic stress combinations may differ from individual stress exposures. Besides, climate change–induced higher
temperatures are predicted to increase the water requirements of
crops (Nelson et al. 2009). Exploiting the genetic variability
available in crop species in adjusting to climate change may be


Drought stress adaptation

a useful strategy for identifying traits contributing to improved
tolerance to a combination of stresses expected to occur due to
climate change. For example, pearl millet varieties have shown
adaptation to persistent drought as well as high temperatures in
Sahel region (Niger) of Africa. Changes in morphological and
phenological characteristics (flowering time, plant height and
spike length) in varieties sampled in 2003, during which
drought and high temperatures prevailed as compared to the
same varieties sampled in 1976, when such stress situations did
not occur (Bezancon et al. 2009), showed a significant shift in
adaptive traits. The varieties flowered slightly earlier and had
shorter spikes in 2003 than in 1976, suggesting that selection

for these traits occurred in the face of environmental change
over this time period. Two genes, PHY and PgMADS11, that
play a role in flowering time regulation were found to show
polymorphism, which could also have arisen in response to
selection. In the context of climate change, a shorter life cycle
may mitigate the effect of climate change by allowing flowering and seed production in stressed environments. Similarly,
there would be a large number of genes involved in different
adaptive processes occurring in response to unpredictable stresses arising due to climate change, which could be mined by
comparative studies on genotypes adapted to different environments.

Conclusion
A number of advancements have been made in our understanding of how a plant responds to drought stress. Adaptation to
drought is seen to involve metabolic and morphological alterations that prevent injury to plants. Underlying these physiological and morphological alterations are molecular mechanisms that
regulate the expression of genes involved in the various adaptive
processes. Although much is known now about the different type
of stress sensors, the secondary signalling molecules involved
and entire stress-specific signalling pathways have not been deciphered, largely due to cross-talk between different stress-signalling pathways.
Stress-response gene expression is regulated largely by transcription factors, which in turn are subjected to very intricate
regulation at the chromatin level, RNA level and protein level.
Stress-induced chromatin remodelling may mediate acclimation
responses and help a plant to cope better with subsequent stress
situations. Micro-RNA-mediated gene silencing of stressresponse TFs under non-stress conditions and their activation by
downregulation of miRNA expression have emerged as another
important means of regulating downstream stress-response gene
expression.
Information on the stress adaptive mechanisms shown by
drought-tolerant genotypes of crop species has been fragmentary. Gene expression studies in response to drought provide
information on processes involved in stress tolerance, but the
sheer magnitude of information generated in such studies
makes it a daunting task to distinguish the adaptive responses

from those that arise secondarily as an outcome of growth
arrest or cell damage. Phenotypic traits associated with
drought-tolerant crops serve as important breeding tools in
identifying stress-tolerant genotypes and in introgressing the
tolerance traits into cultivated genotypes. Dissecting these complex phenotypic traits into simpler, heritable traits has led to
the identification of genes associated with some QTLs for
drought tolerance. Understanding stress-tolerant strategies using
model plants and testing these in crop genotypes that show

29

adaptation to stress appear to be a useful approach in improving drought tolerance of crops. However for studies on adaptation of crop plants to complex stress situations arising due to
climate change, there is a need to exploit the available biodiversity in crop genotypes growing in diverse environments to
understand the mechanisms involved in coping with different
stress combinations.
Acknowledgements
KS acknowledges University Grants Commission, Government of India,
for financial assistance through award of a research fellowship.

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