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Plant Response to
Water-deficit Stress
Secondary article
Article Contents
. Effects of Water Deficit on Plant Growth and
Development
Elizabeth Ann Bray, University of California, Riverside, California, USA
. Resistance Can Occur Through Avoidance or Tolerance
of Water-deficit Stress
When plants do not receive sufficient water they are subjected to a stress called water
deficit. Plants have evolved many different mechanisms to deal with the occurrence of this
stress as it occurs in their environments.
. Water Dynamics of the Plant Cell
. Whole Plant and Physiological Responses
. Osmotic Adjustment Permits Water Uptake and Turgor
Recovery
. The Role of the Signalling Molecule Abscisic Acid
Effects of Water Deficit on Plant Growth
and Development
. Genes Regulated by Water Deficit Affect Water-deficit
Resistance
. Mechanisms of Gene Regulation
Drought, a period of abnormally dry weather, results in
soil-water deficit and subsequently plant-water deficit. The
lack of water in the environment constitutes a stress when it
induces an injury in the plant. Water deficit in the plant
disrupts many cellular and whole plant functions, having a
negative impact on plant growth and reproduction. Crop
yields are reduced by 69% on average when plants are
exposed to unfavourable conditions in the field (Boyer,
1982). Availability of water is the most important factor in
the environment that reduces the production of our crops.
As water is increasingly needed for human populations and
prime agricultural lands are used for housing, the
availability of water will have a greater impact on our
ability to produce crops.
In nature, certain species are adapted to dry environments. The genotype determines the ability of the plant to
survive and thrive in environments with low water
availability. In addition, the duration of the water-deficit
stress, the rate of stress imposition, and the developmental
stage of the plant at the time of stress imposition also affect
plant growth. Whether the amount of water present in the
environment is a stress is different for each species. A
sensing mechanism initiates the responses to water deficit,
which occur at the molecular, metabolic, physiological and
developmental levels. Many of these responses are driven
by changes in gene expression.
Resistance Can Occur Through
Avoidance or Tolerance of Water-deficit
Stress
Resistance to water deficit may arise from the ability to
tolerate water deficit or from mechanisms that allow
avoidance of the water deficit (Figure 1). Some species, such
as desert ephemerals, are able to escape drought by
completing their life cycle when water is plentiful. Others
avoid water deficit with the development of a large root
. Biotechnological Approaches to Developing Waterdeficit-resistant Crops
system that permits improved extraction of water from the
soil. Avoidance of water deficit may also be achieved by
using mechanisms that save water as in succulents. Some
plants may also have improved water use efficiency, such as
found in crassulacean acid metabolism plants, in which
stomata are open at night and an alternative form of
carbon assimilation promotes the use of less water.
However, these plants do not tolerate water deficit. Other
plants have biochemical and morphological mechanisms
such as found in mosses and resurrection plants that permit
the plants to withstand dehydration.
Morphological characteristics of some species permit
continued survival in arid environments, while other plants
must acclimate to the stress to permit survival. Some
responses may promote physiological adaptation to water
deficit; other responses may indicate that an injury has
Resistance to
water-deficit stress
Avoidance of
water deficit
Escape by completing
life cycle in a wet season
Avoid water deficit
using strategies of
maximum water acquisition
Tolerance of
water deficit
Tolerate low water
potential while maintaining
turgor pressure (Ψp)
Tolerate cellular
dehydration using biochemical
and morphological strategies
to protect cells from injury
Avoid water deficit
by maintaining water
in the cells
Figure 1 Resistance to water deficit stress can arise from mechanisms
involving avoidance or tolerance of the water deficit.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
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Plant Response to Water-deficit Stress
occurred. It is difficult to distinguish functions of the
responses to water deficit-stress – which responses are a
direct result of water deficit and are effective in preparing
the cell to function in a water-deficit condition? Some
mechanisms promote survival and limit injury, but may do
this using a mechanism that slows crop production, and are
therefore not useful strategies to develop in crop plants. It
is important to identify mechanisms that permit continued
growth during periods of water deficit to promote crop
production.
Water Dynamics of the Plant Cell
The water within the cell is defined in terms of its free
energy content or ability to do work. The free energy per
unit volume of water is the water potential (Cw). Water is
taken into the plant if the water potential is less than that of
the environment surrounding the cell (Figure 2), since water
moves down a chemical gradient. If the water potential in
the soil solution is higher than that of the cells, water can be
transported into the cells of the root. The water potential of
the cell is dependent upon two important parameters: the
osmotic potential (Cs) and the turgor pressure (Cp). The
content of solutes in the water of the cell (Cs) and the
pressure of the cellular contents against the cell wall (Cp)
decrease the water potential. An additional component,
the matric potential (Cm), or the binding of water to
surfaces, also reduces the cell water potential. Equation [1]
is used to describe cell water potential.
[1]
Cw 5 Cs 1 Cp 1 Cm
Changes in cellular water relations trigger further events
that are manifested in plant responses at the molecular,
metabolic, physiological and developmental levels.
Ψw outside > Ψw inside
Ψw outside < Ψw inside
Whole Plant and Physiological
Responses
The water of the plant can also be viewed in the context of a
soil–plant–air continuum: the plant is a column of water
between the soil and the air. Transpiration, release of water
from the plant, will continue when water is available.
Under drought conditions in the field, soil water content
drops, which does not favour water movement into the
root cells. Water will be lost through transpiration and will
not be fully replaced, causing a loss in turgor. As a defence
against water loss, transpiration decreases. In the leaf, the
pore of the stomatal complex closes in response to whole
plant water deficit. As turgor decreases in the guard cells
surrounding the stomatal pore, the cells fill the pore, thus
reducing the stomatal aperture; this is the main cause of
reduced transpiration. When the stomata are closed,
uptake of carbon dioxide is also reduced, reducing the
carbon assimilation rate of the plant. Depending upon the
duration of the water deficit, this may reduce crop
production and cause injury to the chloroplasts through
the process of photoinhibition. There may also be an
interaction with other stresses, such as heat stress, when
transpiration is reduced that will also contribute to the
strain on the plant.
As cellular turgor approaches zero, growth will be
inhibited. Cellular expansion or growth depends upon
cellular turgor. The pressure of the cellular contents
against the cell wall is the driving force for cell expansion
and turgor is dependent upon uptake of water. The stage of
development of the plant at the time of the occurrence of
water deficit will alter the outcome. Growth will return if
turgor is restored as the plant acclimatizes to water-deficit
stress.
Osmotic Adjustment Permits Water
Uptake and Turgor Recovery
H2O
H2O
Osmotic
adjustment
H2O
H2O
Figure 2 Cellular and soil water potential control water uptake into the
cell. Osmotic adjustment, a lowering of cellular osmotic potential, can
permit water uptake and restore cellular turgor.
2
In a process called osmotic adjustment, metabolism may be
altered to maintain cellular water content through an
increase in the concentration of solutes. In these cells, the
osmotic potential is lowered and thus the chemical
potential of water is lowered, permitting water uptake to
be maintained (Figure 2). Turgor will fully or partially
recover depending upon the external water potential. The
cells will avoid a loss of water, yet they must be able to
withstand low cellular water potential. The solutes that
accumulate, called osmolytes, include sugars, proline and
glycine betaine. They are generally thought to be neutral to
metabolic processes, and therefore do not disrupt plant
function. The ability to adjust osmotically is dependent
upon the genotype and is a more successful defence in
resistant genotypes. Interestingly, the production of
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
Plant Response to Water-deficit Stress
The Role of the Signalling Molecule
Abscisic Acid
osmolytes may have multiple functions and also inhibit
oxidative stress that may arise when plants are subjected to
water deficit (Bohnert and Jensen, 1996).
Membrane permeability to water and ions is also
involved in the control of cellular water potential and
turgor. The water channels, called aquaporins, are proteins
that form a channel in the membrane that specifically
facilitates transport of water across the membrane. These
channels facilitate water transport using osmotic or
hydraulic driving force. They are not involved in the
transport of ions or metabolites. Genes encoding aquaporins are induced in response to water deficit and may
promote increased water uptake in periods of drought.
Other transport proteins including K 1 channels are also
likely to be involved in the response to water deficit.
O2
Cleavage
site
O
Loss of water is a physical stress in the environment that
initiates biochemical events. The mechanism to sense the
stress and the signal transduction events that follow are not
understood. However, it is certain that the cell must have a
mechanism to recognize a decrease in water, which is
probably related to turgor pressure. One intermediary in
the signalling pathway is the plant hormone abscisic acid
(ABA). The biosynthesis of ABA increases in response to
water deficit. ABA accumulates in all of the plant organs
and this response is important for physiological and
molecular responses to the water deficit.
The pathway of ABA biosynthesis is complex and
required a number of dedicated scientists using genetic,
biochemical and molecular approaches to unravel it. The
breakdown of carotenoids, rather than synthesis from a
smaller carbon backbone, is the pathway taken. Violaxanthin is cleaved to xanthoxin (Figure 3). There are two
O
HO
HO
O
cis-Xanthoxin
9-cis Xanthophylls
OH
O
O
ABA aldehyde
OH
I
HO
−
O
O
O
or
HO
Recognition of ABA
OH
OH
Neoxanthin
O
Abscisic acid
OH
Violaxanthin
−
O
O
O
8′ Hydroxy ABA
Signal transduction
ABA action
O
O
OH
−
O
O
Phaseic acid
Figure 3 ABA biosynthesis beginning with a carotenoid and proceeding through catabolism. Both synthesis and breakdown contribute to the level of ABA
in a particular organ of the plant in response to water deficit. The increased concentration of ABA initiates a signal transduction pathway through an
unknown sensing mechanism. This leads to induction of specific genes.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
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Plant Response to Water-deficit Stress
steps remaining in the synthesis of ABA with ABAaldehyde as the immediate precursor to abscisic acid. These
steps are catalysed by constitutively expressed enzymes.
Therefore, it is proposed that the step in the pathway that
regulates the concentration of ABA in the plant is the
cleavage step, since this is the first committed step in the
ABA biosynthetic pathway. Indeed, the gene encoding this
cleavage dioxygenase was cloned when a maize mutant,
vp14, was discovered (Tan et al., 1997). VP14 completes the
oxidative cleavage of 9-cis-xanthophylls, neoxanthin or
violaxanthin, to cis-xanthoxin.
Since the plant hormone is rapidly degraded to phaseic
acid, the breakdown of the molecule also has an important
role in controlling the concentration of ABA in the plant.
ABA analogues that are metabolized more slowly, such as
8’-methylene ABA, are more effective than ABA because of
their persistence (Abrams et al., 1997).
The accumulation of ABA in turn initiates a series of
events (Figure 3), many of which promote plant adaptation
to the conditions of water deficit. One of these events is the
induction of specific genes. ABA is recognized in the cell by
a mechanism that has not been described. This initiates a
signal transduction pathway that is composed of kinases
and phosphatases, but also has not been fully described.
One step of this pathway is a protein phosphatase encoded
by two genes, ABI1 and ABI2. Plants in which these genes
are mutated are more responsive to ABA in many ways.
Signal transduction fulfils the action of ABA by activating
gene expression.
Genes Regulated by Water Deficit Affect
Water-deficit Resistance
The information contained within the genome of each
species dictates the plant response. The genome controls
the regulation of the response to water deficit as well as the
effectiveness of the response. Specific genes are induced
and others repressed as plants are subjected to water-deficit
stress, which has been visualized using 2D polyacrylamide
gel electrophoresis. The extent of the response is not
known, but at least 30 abundant proteins are upregulated
and more than 10 downregulated in tomato leaves. The
induced genes may function in the regulation of the plant
response or in the adaptation of the plant to the stress. The
regulatory genes include components of the signal
transduction pathway, such as the stress sensing mechanism, protein kinases and phosphatases in the signalling
cascade, and the transcription factors that induce specific
genes. The chain of events is concluded with the
accumulation of proteins encoded by genes that have
metabolic or structural functions. The class of genes
encoding enzymes includes those involved in osmotic
adjustment and repair and degradation of damaged
cellular contents. The structural genes are those that alter
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the structural components of the cell such as cell wall or
may protect the structural components of the cell.
A number of different types of proteins are likely to
function to improve stress tolerance. Genes encoding the
enzymes of osmolyte biosynthesis permit the synthesis of
these osmotic compounds in response to stress. The
accumulation of proline is widespread among species.
The accumulation of proline in response to water deficit
occurs through increased synthesis and decreased degradation. Proline is synthesized from l-glutamic acid
through D1-pyrroline-5-carboxylate (P5C) by two enzymes: P5C synthetase and P5C reductase. Proline
dehydrogenase and P5C dehydrogenase are the enzymes
that degrade proline to l-glutamic acid. In response to
water deficit, P5C synthetase is induced and proline
dehydrogenase is repressed, resulting in a net accumulation
of proline.
Another class of genes, which may be unique to plants, is
induced in plants subjected to water deficit. These genes
called the late embryogenesis abundant genes, abbreviated
as lea genes, are also developmentally programmed for
expression in desiccating seeds. These genes encode small
hydrophilic proteins that are predicted to protect proteins
and membranes when cellular dehydration occurs.
Mechanisms of Gene Regulation
The expression of genes in response to water deficit can be
regulated at the transcriptional, posttranscriptional, and
translational levels. The majority of research has been done
to explore the mechanism of transcriptional regulation.
DNA elements within water-deficit-induced genes control
the transcription of specific genes. There are more than
three different classes of cis-acting DNA elements that
regulate genes in response to water deficit. The ABA
response element (ABRE), present in many genes that are
regulated by the plant hormone ABA, with the consensus
RYACGTGGYR, is bound by a bZIP-type transcription
factor and is required for ABA regulation of gene
expression. bZIP proteins have a basic DNA-binding
domain next to a leucine zipper motif that is involved in
protein–protein interactions.
Specificity of this binding may come from nucleotides
surrounding the core ACGT DNA sequence or from
coupling DNA elements that may also be involved in the
regulation of water-deficit-induced genes. Homologues of
the transcription factors MYB and MYC also regulate
water-deficit-induced genes. Another DNA element that
acts independently of ABA, the drought-responsive
element (DRE), has the consensus TACCGACAT, and is
involved in the regulation of genes by water deficit and low
temperature. The DRE is bound by a transcription factor
DREB with a DNA-binding domain found in other plant
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
Plant Response to Water-deficit Stress
transcription factors involved in ethylene-regulated gene
expression and flower gene expression.
Biotechnological Approaches to
Developing Water-deficit-resistant
Crops
Biotechnological approaches may provide a means to
develop crops that respond to stress in a manner that
improves tolerance or avoidance of water deficit. A
number of approaches have been tested in the laboratory
situation. Optimization and tests in field conditions are yet
to come. Manipulation of the expression of regulatory
genes and metabolic genes both may be used to improve
water-deficit resistance in crops. The expression of
regulatory genes may be a means to increase the expression
of a set of genes required in the plant stress response. In
addition, the overexpression of a single gene may permit
the upregulation of a single limiting factor.
The transcription factor DREB, involved in ABAindependent gene induction, increases the drought resistance of Arabidopsis plants in which it is overexpressed
(Kasuga et al., 1999). This increases the expression of a
number of genes, many of whose identity is not known, and
results in plants that survive a period of water deficit better
than the wild-type. This is an interesting method, but the
genes that are induced and the mechanism of stress
resistance are yet to be discovered.
In methods in which metabolic genes are overexpressed,
modest increases in plant water-deficit resistance can be
achieved. Two classes of genes have been overexpressed
resulting in improved stress resistance: genes involved in
osmolyte biosynthesis and lea genes. The overexpression of
genes encoding enzymes that synthesize osmolytes has
proven successful in many cases. Accumulation of proline,
glycine betaine, trehalose, sucrose and fructans has all been
increased in transgenic plants, resulting in improved
growth characteristics in the laboratory. Further studies
are needed to test the response in the field. A lea gene
overexpressed also improves growth characteristics, providing proof that these proteins also have an adaptive
function. Future studies optimizing promoters and protein
accumulation characteristics can be used to further the
utility of this approach for the farmer.
References
Abrams SR, Rose PA, Cutler AJ et al. (1997) 8’-Methylene abscisic acid:
an effective and persistent analog of abscisic acid. Plant Physiology
114: 89–97.
Bohnert HJ and Jensen RG (1996) Strategies for engineering water-stress
tolerance in plants. Trends in Biotechnology 14: 89–97.
Boyer JS (1982) Plant productivity and environment. Science 218: 443–
448.
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K and Shinozaki K
(1999) Improving plant drought, salt, and freezing tolerance by gene
transfer of a single stress-inducible transcription factor. Nature
Biotechnology 17: 287–291.
Tan BC, Schwartz SH, Zeevaart JAD and McCarty DR (1997) Genetic
control of abscisic acid biosynthesis in maize. Proceedings of the
National Academy of Sciences of the USA 94: 12235–12240.
Further Reading
Chrispeels MJ and Maurel C (1994) Aquaporins: the molecular basis of
facilitate water movement through living plant cells? Plant Physiology
105: 9–13.
Ingram J and Bartels D (1996) The molecular basis of dehydration
tolerance in plants. Annual Review of Plant Physiology and Plant
Molecular Biology 47: 377–403.
Schwartz SH, Tan BC, Gage DA, Zeevaart JAD and McCarty DR
(1997) Specific oxidative cleavage of carotenoids by VP14 of maize.
Science 276: 1872–1874.
Shinozaki K and Yamaguchi-Shinozaki K (1997) Gene expression and
signal transduction in water-stress response. Plant Physiology 115:
327–334.
Xu DP, Duan XL, Wang BY et al. (1996) Expression of a late
embryogenesis abundant protein gene, HVA1, from barley confers
tolerance to water deficit and salt stress in transgenic rice. Plant
Physiology 110: 249–257.
Yoshiba Y, Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K and
Shinozaki K (1997) Regulation of levels of proline as an osmolyte in
plants under water stress. Plant Cell and Physiology 38: 1095–1102.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
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