Plant Stress Physiology
Nicholas Smirnoff, College of Life and Environmental Sciences, University of Exeter, Exeter,
UK
Over the last few years there has been an explosion of
information on responses to abiotic stresses in the model
plant Arabidopsis thaliana as well as crops such as rice.
Much of the research has focussed on changes in gene
transcription following stress imposition. The approach
identifies potential ‘stress tolerance genes’ followed by
assessment of their effects in mutants and genetically
modified plants. Although this approach has produced
plants that are apparently more stress resistant, evidence
for translation to improved performance in the field has
been very limited. Possible reasons include the use of
unrealistic laboratory stress treatments and the use of
plants that are not fully acclimatised to the variable and
interacting environmental factors encountered in the
field. Stress research is beginning to address this issue and
more recent approaches are highlighting the importance
of putting stress responses in the context of the control of
plant growth by hormones, the initial perception of stress
signals and in the context of understanding the physio-
logical and metabolic adjustments that are needed for
stress tolerance.
Stress in an Ecological and
Agricultural Context
This chapter will focus on some recent developments and
trends in stress physiology and will emphasise progress in
the translation of basic research into the improvement of
crop stress resistance. Within the context of increasing
world food supply, improving abiotic stress resistance and
eLS subject area: Plant Science
How to cite:
Smirnoff, Nicholas (October 2014) Plant Stress Physiology. In: eLS.
John Wiley & Sons, Ltd: Chichester.
DOI: 10.1002/9780470015902.a0001297.pub2
eLS & 2014, John Wiley & Sons, Ltd. www.els.net
Introductory article
Article Contents
. Stress in an Ecological and Agricultural Context
. Translation from Laboratory to Crops: Progress and
Problems
. Drought Resistance
. Temperature Extremes
. ROS: Pervasive Players in Stress Responses
. Soil Chemistry: Nutrient Deficiency; High Salinity and
Toxins
. The Plant Microbiome: Role in Mineral Nutrition,
Growth Modulation and Stress Resistance
. Concluding Remarks
Online posting date: 15th October 2014
the efficiency with which plants use finite resources such as
water and mineral nutrients will play an important role.
This will need to be achieved in partnership with
improvements in crop yield potential, nutritional quality,
and pest and disease resistance. This article should be read
in conjunction with the previous introductory articles in
the series to provide a more complete background to the
range of stresses and stress responses. See also: Abiotic
Stress; Plant Stress Physiology
Abiotic stress can be defined very simply as any envir-
onmental condition that limits plant growth. These con-
ditions include: temperature extremes; unfavourable soil
texture; limited or excessive soil water; toxic minerals; air
pollutants; UV-B radiation; limited or excessive light and
limited supply of mineral nutrients. In the natural envir-
onment, the prevailing conditions rarely support max-
imum growth rate so the ability to deal with stress is a
fundamental aspect of plant physiology. In a wider ecolo-
gical context it is known that plant species adapted to
‘stressful’ environments (e.g. where nutrients are severely
limiting or temperature in the growing season is low) have
intrinsically slow growth rates and are largely unresponsive
to improved conditions. In other words, natural selection
in stressful environments has favoured plants with a con-
servative habit in terms of resource use. Such plants often
have long-lived leaves which are physically tough and high
in toxic or unpalatable defensive compounds that decrease
the loss of hard-won resources to herbivores. This suggests
that the sensing and signalling systems linking resource
availability and temperature with cell division and expan-
sion are insensitive in these plants. In contrast, most of our
high yielding agricultural species are derived from annual
weeds whose control systems are wired up to respond in a
rapid and sensitive manner to changes in conditions and, in
particular, to slow their vegetative growth and accelerate
reproduction at the expense of productivity under stressful
and resource-limited conditions. Therefore, there is a
general tension between stress tolerance and productivity.
Introducing extreme stress tolerance characteristics as seen
in arctic–alpine plants, desiccation resistant plants, desert
succulents or plants adapted to highly infertile soils into
1
 Plant Stress Physiology

crops could decrease yield potential, which is not an agri- 1200

culturally desirable outcome.

Number of publications (2010−2013)

To assess the state of play in abiotic stress research, it is 1000
instructive to see which crop species are predominantly
being used. Research publications for the main agricultural
800
field crops containing abiotic stress-related terms in their
titles were retrieved using the Web of Knowledge database
(http://apps.webofknowledge.com) for the period 2010– 600
2013 (Figure 1a). This analysis shows that the model plant
Arabidopsis thaliana, along with wheat and rice (the key 400
food crops), are the predominant plant species used for
stress research. These are followed by maize, soybean and
200
tomato which account for about half the number of pub-
lications. This pattern follows both the total area of these
crops and their importance in world commerce. Crops 0

Rice
Wheat
Arabidopsis
Maize
Soybean
Tomato
Brassica
Barley
Cotton
Potato
Chickpea
Sorghum
Millet
Banana
Sugar beet
Cassava
Sugar cane
Lentil
Buckwheat
which are predominantly grown by subsistence farmers
(e.g. cassava, bananas/plantains, chickpea, lentil, sor-
ghum, and millet) and which tend to be grown on less fertile
soils and in climatic zones subject to drought, high salinity (a)
and high temperature stress receive a small proportion of
the research effort. This situation is intertwined with a lack
of genome sequences or other genomic resources for these 1000
crops. The cassava genome has now been sequenced which
Arabidopsis papers on stress

may accelerate improvement of its stress resistance and

800
other traits. However, as long as research on the model
species is translatable, the lack of basic research on less
tractable species is not necessarily disadvantageous. Likely 600
changes in climate over the next few decades may increase
the importance of stresses such as temperature extremes 400
and drought. Drought and crop water use efficiency
(WUE) are particularly critical because a large proportion 200
of the total supply of fresh water is already used in agri-
culture, and this use will increase with the need to increase
food production. Fresh water supply is projected to be a 0
critical social and political issue because of the increasing 6
human population. We can add to this scenario the large
energy cost for manufacturing nitrogenous fertiliser and
Arabidopsis papers on stress (%)

the very limited rock phosphate reserves which will

increase the price of these two strongly yield-limiting
nutrients in the future. Therefore, key goals must be to 4
improve water, nitrogen and phosphorus use efficiency and
to improve responses to water shortage, high salinity and
temperature extremes. Although classical approaches to
plant breeding such as selecting for high yield in the 2
appropriate environments have (and will continue) to
improve stress resistance, the hope is that ‘smart’ applica-
tion of basic research into plant stress responses will
accelerate this effort. The next section will review this
progress, with the conclusion that we need to do better. 0
1994−1997

1998−2001

2002−2005

2006−2009

2010−2013

Translation from Laboratory to Crops: (b)

Progress and Problems
As noted above, one of the driving forces for fundamental
research into plant stress responses is the hope that it will
provide a foundation for improving crop stress resistance
Figure 1 Publications related to plant stress responses. (a) Number of
publication for Arabidopsis thaliana and selected crop plants in the period
2010–2013. (b) Number and proportion (% of all Arabidopsis publications)
of stress-related Arabidopsis thaliana publications between 1994 and 2013.
Data were extracted from the Web of Science database.

2 eLS & 2014, John Wiley & Sons, Ltd. www.els.net


and therefore contribute to the perceived imperative to
increase crop yield to accommodate population growth.
This translational research should identify physiological
traits or genes that will be useful in breeding programs –
either by providing molecular markers that can speed up
selection of desired genes or alleles during a breeding
programme (termed molecular or precision breeding) or by
production of transgenic plants expressing one or more
useful genes. Alternatively, a deeper understanding of
specific physiological and morphological characteristics
(which may be under the influence of multiple genes)
associated with stress resistance would also allow their
selection in breeding programs. A welcome development in
this regard is the recent realisation by the plant science
research community that it would be useful to look more
closely at plants; something that plant breeders have
always done. This change in emphasis is leading to the
development and installation of so-called ‘phenomics
platforms’ where large numbers of plants are grown under
strictly controlled conditions with continuous monitoring
by cameras to record features such as morphology, leaf
reflectance, leaf temperature (by IR photography) and
chlorophyll fluorescence. Phenomics is also being extended
to roots in soil using X-ray tomography. Another often
forgotten aspect of translational research is that physio-
logical understanding can also inform agronomic prac-
tises. For example, optimising the amount of irrigation
water applied to balance water use and productivity
(known as deficit irrigation) requires information on
transpiration and crop growth responses to limited water
at various growth stages.
How well are we doing in translating stress research into
crop varieties? The proportion of research papers on stress
in the predominant model plant A. thaliana has steadily
grown from 1.5% in 1998–2001 to 4.4% in 2010–2013
(Figure 1b). Interestingly, in 1994–1997, 5% of papers were
stress-related although smaller in absolute terms than
1998–2001 because five times fewer papers were published
in this period. The upward trend in recent times indicates a
sustained emphasis on fundamental research into plant
stress responses. Recent developments include increased
use of ‘-omics’ and systems biology approaches that
employ mathematical modelling to identify, for example,
transcriptional networks involved in stress responses. Such
approaches are driven by the hope that understanding the
control networks involved in stress responses will allow
them to be tweaked at a basic level by manipulating stress-
responsive transcription factors. As we move into the
synthetic biology era, there is sure to be interest in how
this knowledge can be used as the basis for introducing
synthetic signalling networks into plants that will produce
responses in metabolism and development tailored to
improve yield under specific stresses. The reduced cost
of genome sequencing and easy detection of single
nucleotide polymorphisms across many Arabidopsis gen-
otypes is enabling genes associated with specific traits to
be identified efficiently by genome-wide association ana-
lysis (Verslues et al., 2014). The last decade of research has
eLS & 2014, John Wiley & Sons, Ltd. www.els.net
Plant Stress Physiology
resulted in an explosion of information on signal trans-
duction systems, stress-induced changes in gene expres-
sion, the physiological and metabolic outputs that improve
performance or provide protection (changes in cell division
and expansion; synthesis of antioxidants, molecular cha-
perones and osmolytes; changes in ion transport, primary
and secondary metabolism). However, the output, in terms
of crop varieties specifically produced as a result of this
information is very limited. One factor explaining this
situation is that breeding a new variety takes time, so there
is an inherent delay in applying new information. Even the
apparent quick fix of transgenic approaches could take up
to a decade because of the extensive field trials are still
required to assess the performance of new varieties across
years and environments. Safety and regulatory issues must
also be addressed before release of transgenic crops. For
this reason, it may be too early to make a judgment on the
practical value of a couple of decades worth of research on
signal transduction systems, stress-induced gene expres-
sion and the production many transgenic Arabidopsis
plants which are proposed to be more stress resistant. This
is not to say that there has been no progress and an
important example of the application of basic research has
been the production of rice varieties better able to tolerate
submergence. Although rice in paddy fields is well adapted
to soil waterlogging by having roots with aerenchyma
(large intercellular air spaces) that allows oxygen to diffuse
from the aerial parts, it is less able to survive episodes
of total submergence. Genetic variability exists in sub-
mergence tolerance and the underlying locus (Sub1) was
identified by quantitative trait locus (QTL) analysis. This
resulted in identification of 3 ethylene-responsive tran-
scription factors (ERFs) involved in submergence toler-
ance (Xu et al., 2006). The required genes can be identified
in breeding populations of rice and so has been transferred
to agronomically useful varieties that are now being used
by farmers (http://indica.ucdavis.edu/news/new-flood-
tolerant-rice-offers-relief-for-worlds).
Although the example of submergence resistant rice
suggests future promise for other crops and stresses, it is
worth considering some current barriers to translation.
For Arabidopsis, and increasingly for crop plants, there are
numerous examples of studies in which genes that are
putatively involved in stress tolerance have been over-
expressed, resulting in transgenic plants reported to have
increased resistance to one or more stresses (Deikman
et al., 2012). The large number of reports on this effect is
perhaps surprising. If increasing the expression of a single
gene by a modest amount is all it takes to improve drought
or salt resistance, these results raise the question of why
natural selection has not tuned the expression of such
proteins in an appropriate manner. This question is at
the crux of why so few of these genes are being used for
crop breeding. A possible general explanation is that
laboratory growth conditions rarely resemble the natural
environment with respect to fluctuations in tempera-
ture, light, water supply, humidity and interactions with
other organisms (Atkinson and Urwin, 2012). Plants can
3
 Plant Stress Physiology
respond differently to mixtures of stresses than to each one
singly. This is illustrated by the different patterns of gene
expression that are found if stresses are applied singly or
together (Rasmussen et al., 2013). It is quite likely that, in
plants whose defences are not primed by exposure to nat-
ural fluctuations in the environment, a small increase in the
expression of one gene can cause an easily observable
improvement in tolerance. This effect may well disappear
in the real world. To add to this problem, molecular
geneticists looking for a ‘phenotype’ in their mutants tend
(subconsciously but sometimes deliberately) to arrange
their growth conditions to show the advantages of simple
gene manipulations to best effect. Such a reductive
approach may well reveal significant information about the
system but might pose a problem for translatability. An
example to illustrate this problem is the possible benefit of
increasing ascorbate (vitamin C) concentration for stress
resistance. Since it has been proposed that many stresses
result in increased generation of reactive oxygen species
(ROS) that may then cause oxidative stress, the idea that
increasing antioxidant defences will improve stress resis-
tance has received much attention (see ROS section).
Ascorbate accumulation can be increased by over-expres-
sion of biosynthesis or recycling enzymes (Smirnoff, 2011).
These approaches have produced modest increases in
ascorbate along with reported improvements in resistance
to various stresses (Lisko et al., 2013). Such results are
valuable in providing an understanding of the physiologi-
cal functions of ascorbate but are more problematic as a
basis for crop improvement. This is because plants grown
in outdoor light intensities could have 5–10 times higher
ascorbate concentration than those grown in the labora-
tory. This difference dwarfs the increases achieved by
transgenic approaches, making it very unlikely that a
measureable benefit would accrue outside the laboratory.
Since ascorbate status also influences susceptibility to
pathogens, the concentration in leaves represents a balance
between antioxidant defence and disease. We must con-
clude that if laboratory-based studies are to have an
improved probability of being translatable to crops, future
research must quickly move to testing the effects of over-
expressing genes under natural conditions. Another reason
that translatability could be limited is that laboratory stress
treatments may not replicate field stress and are often
‘shock’ treatments that do not give time for acclimatory
responses to take place. Acclimation is a term that refers to
the changes that take place after perception of a stress that
lead to increased resistance. Additionally, the conclusion
that over-expression of a single gene improves stress
resistance is rarely based on the growth of plants to
maturity under a realistic stress with measurement of all the
relevant physiological parameters and yield components.
Until the plant research community does this more fre-
quently, one can predict that the translatability of stress
research will remain low. See also: Anoxia in Plants; Ara-
bidopsis thaliana as an Experimental Organism; Geneti-
cally Modified Plants; Quantitative Trait Loci and
Breeding
4 eLS & 2014, John Wiley & Sons, Ltd. www.els.net
Drought Resistance
Drought is recognised as a significant limiting factor for
crop production in many regions and application of fun-
damental science to improving crop drought resistance is
an important goal. A key gap in our knowledge, despite the
large research effort in drought stress, is the mechanism for
the initial perception of plant water status: do plants have
osmosensors, as found in other organisms? An Arabi-
dopsis histidine kinase (AHK1) able to complement
osmosensing in a yeast mutant could be a candidate
osmosensor (Kumar et al., 2013). However, further ana-
lysis of AHK1 mutants and over-expressers indicated that
it influences abscisic acid (ABA) signalling rather than
acting as the primary osmosensor. ABA is a hormone
involved in coordinating a number of responses to water
deficit in plants. Clearly, if we could identify osmosensors,
this would potentially provide a route to tuning plant
response to water status at a fundamental level. Following
perception of drought, most plants respond by decreasing
their stomatal aperture and density, slowing shoot growth,
accumulating compatible solutes to maintain turgor and
accelerating senescence and abscission of older leaves. The
compatible solutes accumulated include proline, sugar
alcohols and glycine betaine. They are termed compatible
because they promote protein folding and therefore may
also have osmoprotective effects. Synthesis of proline
might also aid in dissipating excess reductant (Sharma
et al., 2011). Leaves developing during water stress often
develop thicker cuticles to minimise water loss or have
reflective epicuticular wax and epidermal hairs (trichomes)
which decrease leaf temperature and reduce transpiration
rate – with the potential cost of decreased photosynthesis.
Drought-induced changes in leaf orientation to avoid
direct sun also decrease leaf temperature. Hydraulic
architecture (e.g. xylem vessel diameter) influences the ease
of water transport. Wide vessels allow aid transport with
minimum water potential gradients but are subject to
cavitation (breakage of the water column leading to
blockage of flow) that results in increased water stress in the
shoots. Selection for xylem vessel diameter has been used in
wheat breeding. Photosynthesis is limited by restricted CO2
supply due to stomatal closure and in some cases by more
direct effects on metabolism. As with other stresses that
constrain the rate of carbon assimilation (such as low
temperature or nutrient deficiency), this can result in
exposure to the chloroplasts to excess excitation energy
leading to photooxidative stress and the need for photo-
protective and antioxidant mechanisms. Roots are gen-
erally less sensitive to water deficit than the shoot and can
maintain growth during early stages of soil drying as well as
sending hormonal signals (including ABA and possibly
cytokinin and strigolactone) to the shoots. The suite of
responses to water deficit represents a strategy to minimise
use of water, increase WUE and in the longer term avoid
catastrophic soil drying. Decreased growth involves the
interplay of decreased turgor, altered cell wall extensibility
and decreased rate of cell division. These processes,
 Plant Stress Physiology

Decreased assimalate import into developing

grain. Decreased cell expansion and division

Decreased leaf expansion

Osmolyte accumulation,
turgor maintenance
Epicuticular wax or trichomes to reflect
light and reduce leaf temperature/transpiration

ABA accumulation and

stomatal closure Leaf movement or rolling
to reduce leaf temperature
Decreased photosynthesis and
increased photoxidative stress/ROS
production

Increased cuticle development

Turgor loss, accelerated
senescence and assimilate export

Xylem vessel diameter and number

influence water soil/leaf potential gradient

ABA synthesis and

transport to shoot
Osmolyte accumulation, turgor
maintenance. Root growth maintained
under mild water deficit
Figure 2 The key features involved in drought responses and tolerance of plants illustrated with a cereal plant during the phase of grain filling. To improve
drought tolerance, changes in multiple traits are likely to be required and different traits may be important for dealing with drought during seedling,
vegetative and reproductive stages. ABA, absciscic acid; ROS, reactive oxygen species.

originally regarded as being the physical consequence of
reduced turgor, also involve restraint of growth by the
action of hormones (Claeys and Inzé, 2013). The role of
hormones in drought responses is receiving renewed
attention. ABA is the most widely studied hormone, con-
trolling stomatal aperture as well as gene expression during
drought and desiccation. There have recently been major
advances in understanding the mechanisms of ABA per-
ception and signal transduction (Weiner et al., 2010) which
could lead to rational approaches to modulating drought
responses. Care will be needed in manipulating ABA
because it can also increase the virulence of pathogens (de
Torres Zabala et al., 2009). Other hormones also have a
role in modulating growth and allocation during drought
(Reguera et al., 2013). Histone modification affects gene
expression by altering the accessibility of gene promoters to
the binding of transcription factors. Recently, it has been
shown that over-expression of histone deacetylation com-
plex 1 (HDC1), which is part of the multiprotein complex
containing histone deacetylase, influences drought
responses. High expression of HDC1 promotes histone
deacetylation, which in turn prevents ABA-mediated
derepression of various target genes. Since ABA target
genes are associated with growth retardation, this manip-
ulation improves growth under both well-watered and
drought conditions (Perrella et al., 2013). The plant
responses to drought described above are summarised in
Figure 2.
Although the initial perception of water status and the
mechanism of its effect on hormone levels are not

eLS & 2014, John Wiley & Sons, Ltd. www.els.net 5

 Plant Stress Physiology
understood, the transcriptional responses have been widely
investigated, leading to the identification of transcriptional
networks (Urano et al., 2010). Many of these studies have
involved rapidly developing water stress or osmotic shocks
of a severity that would rarely be seen in the field (except
perhaps during seed germination and early seedling
growth) and therefore elicit emergency protective mea-
sures. Although this has provided information on shock
responses, this is not necessarily relevant to the milder
long-term water deficits that limit crop productivity. There
have been numerous reports of improved drought (and
salt) resistance resulting from single gene manipulations
(Hu and Xiong, 2014). As discussed in the previous section,
many of these have been assessed under rapid stress
application and in plants not acclimated to field conditions.
The supposition that many of these transformations would
not produce drought tolerant plants has been tested by
subjecting 25 Arabidopsis lines transformed to over-
express stress-related transcription factors and protective
proteins that were previously reported to confer improved
tolerance to drought and related stresses. In an experiment
where shoot biomass was measured after slow soil drying,
none of these lines performed better than the wild type
strains (Skirycz et al., 2011). This result indicates that
current approaches are producing a very high proportion
of false positive drought tolerance candidate genes. How-
ever, there is one example of the success of this approach.
DroughtGard maize hybrids, released in 2013 in the United
States, are the first drought tolerant crop based on genetic
modification with a single gene to be marketed (http://
www.monsanto.com/products/Pages/droughtgard-
hybrids.aspx). The development of this variety is based on
the observation that expression of bacterial cold shock
proteins (CSPs) in Arabidopsis and maize caused an
increase in drought tolerance under laboratory conditions
(Castiglioni et al., 2008). Their yield advantage under
water-limited conditions has been transferable to field
crops in multiple locations and bodes well for the success of
future manipulations. CSPs are ribonucleic acid (RNA)
chaperones but, interestingly, their mode of action in the
transgenic plants is not fully understood. There is spec-
ulation that epigenetic changes caused by altering deox-
yribonucleic acid (DNA) (e.g. methylation of cytosine) or
the structure of chromatin (histone modifications such as
acetylation) could contribute to stress memory (Gutzat
and Mittelsten Scheid, 2012; Molinier et al., 2006). Epi-
genetic changes are well-established in the case of vernali-
sation – the persistence across development of a cold signal
that induces flowering (Song et al., 2012). Epigenetic
modifications can be persistent and passed on to offspring,
resulting in epigenetic inheritance of altered gene expres-
sion patterns. An example of drought stress memory is
provided by the demonstration that a specific subset of
drought-inducible genes is more rapidly induced for up to 5
days after the plants have been trained with an initial
drought stress (Ding et al., 2012). The mechanism in this
case is related to the association of the messenger RNA
(mRNA) with stalled RNA polymerase II. Further
6 eLS & 2014, John Wiley & Sons, Ltd. www.els.net
investigations are needed before we can assess the wider
implications for stress resistance. See also: Energy,
Radiation and Temperature Regulation in Plants; Plant
Response to Water-deficit Stress; Turgor Pressure; Water
Use Efficiency of Cultivated Crops
Temperature Extremes
Plants have a wide range of temperature tolerances,
although the high temperature limits of some thermophilic
bacteria (above 100 8C) are not reached. Some semi-buried
desert succulent plants (e.g. ‘living stones’ such as Lithops)
can survive long periods at close to 60 8C, while most plants
cannot survive for long above 40 8C. At the lower end, the
dormant tissues of some arctic trees survive at 280 8C,
while many plants of tropical origin show damage at
temperatures as high as 10 8C. These chilling sensitive
plants include crops such as maize, tomatoes, and the
squash family. The productivity and geographical range of
maize would be significantly increased if its chilling sensi-
tivity was decreased.
Plants generally respond to low temperature by
decreasing their growth and photosynthesis rate. The
response of plants to low temperature and cold stress has
been studied in some detail in Arabidopsis and includes
rapidly altered gene expression, accumulation of ascorbic
acid and triacylglycerol, flavonoids (e.g. red and purple
anthocyanins) and compatible solutes such as raffinose.
Additionally, membrane lipids undergo re-tailoring to
decrease fatty acid chain length and increase degree of
unsaturation. The changed fatty acid properties decrease
the transition temperature of membrane lipid bilayers and
probably maintain fluidity and function at lower tempera-
ture. In general, although metabolic processes including
photosynthesis slow down as temperature decreases, accli-
mation can occur by accumulation of higher concentra-
tions of enzymes and ribosomes (Pyl et al., 2012). These
responses provide some degree of compensation for
decreased reaction rate at low temperature. Cold acclima-
tion also tends to increase antioxidant defences because
lower photosynthesis rate in the face of continued light
absorption can cause photooxidative stress (see section on
ROS). It is important to remember that plants experience
regular day to night temperature fluctuations and it
has been found that decreased growth rate and changes
in metabolism are controlled by day time temperature
with little response occurring to low night temperature
(Bhaskara et al., 2012). Differences in day to night responses
to temperature (and most likely other environmental
stresses) are under control of the circadian clock. This is a
temperature-compensated oscillator that controls (largely
via influencing gene expression) many aspects of growth
and development that require to be cued to time of day.
Many of the changes in gene expression caused by low
temperature are mediated by transcription factors (known
as CRT or DREB) that have a range of target genes (the
CRT/DREB regulon). Amongst the CRT/DREB regulon

are hydrophilic proteins (dehydrins and related proteins)
that may act in maintaining protein structure during low
temperature and freezing. Accordingly, it has been found
that over-expressing CRT/DREB transcription factors can
increase freezing tolerance and also tolerance to water
stress shock treatments. This is because other members of
the DREB family are responsive to drought and ABA and
have many target genes in common leading to cross toler-
ance. Freezing imposes severe water stress because it occurs
first in cell walls. Formation of ice crystals in the cell wall
draws water from the protoplast (ice has a more negative
water potential than liquid water), so freezing acts as a
desiccation stress. Dehydrins and compatible solutes (e.g.
proline, sucrose and raffinose) protect protein and mem-
brane structure and in severe cases (very low temperature
or extreme desiccation) allow the cytoplasm to enter a
glassy state thereby avoiding the damage that would be
caused by crystallisation of solutes. These responses are
very similar to changes that occur during the desiccation
phase of seed development and in the relatively small
proportion of terrestrial plants whose leaves can recover
from desiccation (e.g. mosses). Freezing of cytoplasmic
water is lethal, so the maximum low temperature tolerance
of plants is determined by this occurrence. Ice crystal for-
mation only occurs if the water contains nucleation sites
(small particles) and pure water can remain liquid to
240 8C. Bacteria living on leaf surfaces can cause damage
by forming proteins that encourage ice nucleation (http://
microbewiki.kenyon.edu/index.php/Bacterial_
nucleation_in_pseudomonas_syringae).
Plants that exhibit tolerance of very low temperatures
achieve this by avoiding ice nucleation – a phenomenon
termed deep supercooling.
A side effect of CRT/DREB over-expression in trans-
genic plants, unless carefully controlled, is that growth is
retarded. Although some of this effect may be because the
acclimatory responses outlined above are incompatible
with rapid growth, it has more recently become apparent
that growth is actively restrained in the cold. CRT/DRB
induces expression of DELLA proteins. These proteins
repress expression of genes involved in growth (e.g. cell
expansion). DELLA mutants show less growth inhibition
at low temperature (Achard et al., 2008). DELLAs are also
involved in the growth promoting action of the plant
hormone gibberellic acid (GA), which works by causing
their proteolytic destruction. This finding suggests that it
may be possible to separate low temperature-reduced
growth from the other responses needed for cold or freez-
ing acclimation. There may be situations where faster
growth of a crop in the cold will have a yield advantage. If
autumn-sown wheat or barley produces a bigger leaf
canopy by spring, crop growth rate will be enhanced as
temperature rises. In Mediterranean environments where a
cold winter is followed by rapidly developing drought in
spring and early summer, cold tolerant varieties of barley
are more ‘drought resistant.’ They mature before severe
soil drought develops because they grow faster in the
spring.
eLS & 2014, John Wiley & Sons, Ltd. www.els.net
Plant Stress Physiology
The higher temperatures predicted by climate change
models are likely to impact agriculture. Higher tempera-
ture will cause faster evaporation and therefore increase the
likelihood of drought. On the other side of the coin, limits
for crop growth are likely to move further towards the
poles and to higher altitudes. In terms of temperature
extremes, the frequency of high temperature episodes could
increase. High temperature could decrease productivity by
increasing the rate of photorespiration relative to photo-
synthesis in crops with the C3 pathway (most crops with the
exception of maize, sugar cane, sorghum and millet).
However, one of the most frequent effects of short high
temperature episodes is to disrupt reproductive growth of
cereals (e.g. maize), resulting in full or partial sterility and
severely reduced grain production. As with freezing, cha-
perone proteins (heat shock proteins) provide protection
during high temperature stress and, interestingly, if over-
expressed under appropriate conditions, may also improve
growth and WUE and also improve resistance to bacterial
pathogens (Bechtold et al., 2013). See also: Cold Accli-
mation and Freezing Tolerance in Plants; Plant Tempera-
ture Stress
ROS: Pervasive Players in Stress
Responses
Oxidative stress is the term applied to damage caused by
the ROS produced as a by-product of metabolism. ROS
include superoxide, hydrogen peroxide, singlet oxygen
and hydroxyl radicals. ROS are removed by a range of
antioxidants including glutathione, ascorbate, superoxide
dismutase, catalase, and ascorbate and glutathione per-
oxidases. There is a general consensus that, in various
ways, stresses disrupt metabolism and thereby cause
increased ROS production, which is manifest as damage to
proteins and membranes and in severe cases can result in
cell death. ROS and also reactive nitrogen species (RNS)
such as nitric oxide also act as signals, including propa-
gating long distance signals to provide systemic responses,
and have specific effects on gene expression (Suzuki et al.,
2013). This means that the production and perception of
ROS and RNS might be important in activating defence
responses. An example of how ROS can activate gene
expression is shown in Figure 3, which uses the publicly
available gene expression data derived from microarrays.
In these experiments, the expression (measured by abun-
dance of their mRNA) of most of the genes in the Arabi-
dopsis genome has been compared under different
conditions using the Genevestigator tool (Zimmermann
et al., 2004). For this analysis, the expression of genes that
respond most strongly to increased hydrogen peroxide
(caused by mutation in a catalase gene, CAT2) has been
compared across a range of stress conditions. The false
colour scale indicates fold change in gene expression
compared to controls. The genes and stresses are grouped
into sets that respond similarly to various conditions by
7
8

Plant Stress Physiology

eLS & 2014, John Wiley & Sons, Ltd. www.els.net

Figure 3 Comparison of the 100 genes most strongly induced by hydrogen peroxide in Arabidopsis thaliana with the response of the same genes to various abiotic stresses. Increased hydrogen peroxide was
generated by using a catalase (cat2) mutant. The data are presented as a heatmap showing the extent of increased or decreased expression relative to controls. Genes are listed on the horizontal axis and stress
conditions on the vertical axis. Hierarchical clustering analysis groups the genes and conditions that are most similar. Oxidative stresses cluster strongly together (orange box). The other stresses (see text for
details) form a separate cluster that shows a tendency for a selection of hydrogen peroxide-responsive genes to have higher expression. The analysis was carried out with the Genevestigator tool (Zimmermann
et al., 2004).

hierarchical clustering. Conditions corresponding to
oxidative stress (indicated by the orange coloured box)
are clustered together indicating that the 100 hydrogen
peroxide-responsive genes also tend to respond to singlet
oxygen (which is produced in the flu mutant) and to
ozone (which generates oxidative stress). The cluster of
genes responding most strongly to all the oxidative
stresses is in the top right of the diagram. Inspection of
the other stresses exemplified by drought, salt, osmotic
stress, cold, high temperature, low oxygen (submergence
and hypoxia), UV-B radiation, high light, nitrogen defi-
ciency and phosphorus deficiency, suggests that the oxi-
dative stress-responsive genes have a tendency to be
more highly expressed under these conditions. The result
of the apparently ubiquitous production of ROS during
stress is that a large amount of research has been based
on the hypothesis that improving antioxidant defence
is a potentially useful way to improve stress resistance.
Experiments in which over-expression of a single anti-
oxidant gene reportedly increases resistance to a range
of stresses are abundant. For the reasons discussed
previously, such experiments may not translate to the
field. It may well be that improving specific aspects of the
antioxidant system could complement other more stress-
specific manipulations. See also: Oxidative Stress and
Redox Signalling in Plants; Ozone and Reactive Oxygen
Species
Soil Chemistry: Nutrient Deficiency;
High Salinity and Toxins
Unfavourable soil conditions are widespread and can limit
crop productivity. The most common are nitrogen (nitrate
or ammonium) and phosphate limitation but other nutri-
ents (e.g. zinc or iron) are often limited in some soils.
Nutrient deficiency slows crop growth and strategies for
improving the ability of crops to use limited supplies need
to focus on a number of separate aspects. Firstly, improved
mining of the soil by changes in root architecture (e.g.
branching pattern, size and density of root hairs) and
amount of root relative to shoot. Plants are able to alter
root branching in response to overall or local nutrient
concentrations and increase root growth relative to shoot
growth. Advances are being made in understanding the
mechanisms that roots use to sense nutrient concentration
and link this to root development. Roots also signal
nutrient status to leaves, and hormones such as cytokinins
and strigolactone, form part of this signal, allowing shoot
development to be coordinated with root growth and
nutrient supply. Control of gene expression by micro
RNAs (miRNA) appears to be a general response to
nutrient deficiency and, for example, is involved in
response to both N, P, S and Cu supply. An example of
the importance of root development is provided by rice
(Gamuyao et al., 2012). QTL analysis of a traditional (land
race) rice identified a gene encoding a protein kinase
eLS & 2014, John Wiley & Sons, Ltd. www.els.net
Plant Stress Physiology
(Pstol1) which enhances growth on low P soil by influen-
cing early root growth. Interestingly, this gene is not pre-
sent in the genomes of modern rice cultivars and is,
therefore, a candidate for introduction into agronomically
desirable lines to improve phosphate uptake efficiency. The
second strategy is to improve the efficiency with which
nutrients are moved from older to younger tissues to
maintain growth and reproduction. This process involves
efficient remobilisation of organic nitrogen from proteins,
chlorophyll and nucleotides and transport of amino acids
to sink tissues and involves complex signalling pathways
mediated by hormones.
Toxic ions limit growth in some soils, for example,
aluminium in acidic soils and salt (NaCl). Salt accumu-
lation can be caused by irrigation with poor quality water
over long periods. Salt affects plant growth by an osmotic
effect (and so has some aspects in common with water
stress) as well as by sodium toxicity. It is interesting to note
that specialised plants are able to grow in seawater
(halophytes) or in soils contaminated with toxic elements
such as cadmium, nickel, copper, zinc and arsenic
(metallophytes and metal hyperaccumulators) with little
penalty in growth rate – indeed salt marshes can have very
high productivity. Similarly, most halophytes and metal
hyperaccumulators also accumulate very high con-
centrations of these otherwise toxic metals. Therefore, the
ability to deal with salt, for example, is not intrinsically
incompatible with growth and should be relatively easy to
engineer. Non-halophytes have presumably lost this
ability and success in increasing salt tolerance by intro-
ducing appropriate transporter genes for salt uptake and
storage in the vacuole are proving successful (Schroeder
et al., 2013). Notably, a gene encoding a high affinity
potassium transporter (HKT) family from the relatively
salt-tolerant Triticum monnococcum was associated with
salt tolerance and sodium exclusion from leaves by QTL
mapping. This allele was then introduced into durum
wheat by marker assisted breeding resulting in line with
improved yield under saline conditions in the field. The
interesting point about this trait is that over-expression of
the gene in transgenic plants is not effective at improving
salt tolerance. The reason appears to be that the protein is
specifically expressed in the vascular tissue where it con-
trols sodium transport to the shoot. Transgenic plants
express it in all cell types, so in this case marker assisted
breeding ensures that the gene is not only selected but its
expression is correctly localised (Roy et al., 2014). This
review also makes a number of useful points about
selecting characters to manipulate for salt tolerance that
are relevant to the specific crop or situation and the
importance of considering a trait-centred approach com-
pared to the more widely used gene-centric approach
whose limitations were discussed in the section on trans-
lation from laboratory to field. See also: Flooding-Stress
in Plants; Heavy Metal Adaptation; Improving Nutrient
Use Efficiency in Crops; Iron in Plants; Plant Salt Stress;
Potassium in Plants; Rhizobium and Other N-fixing
Symbioses
9
 Plant Stress Physiology
The Plant Microbiome: Role in
Mineral Nutrition, Growth
Modulation and Stress Resistance
Large organisms live in association with complex microbial
communities known as their microbiome. Most plants
have symbiotic mycorrhizal associations with fungi that
colonise their roots and improve uptake of relatively
insoluble mineral nutrients such as phosphate via hyphae
that ramify into the soil. These associations are probably as
old as the emergence of terrestrial plants and are essential
for plant nutrition – there are only a few groups of plants
that lack mycorrhizal associations (including the Brassi-
caceae – the family containing the model plant A. thaliana
as well as cabbages and oilseed rape). The other well-
established associations that improve nutrition are sym-
biotic associations with nitrogen fixing bacteria, which
range from loosely associated bacteria in the rhizosphere to
bacteria that enter the roots and live in specialised nodules
(e.g. legumes). One way to improve efficiency of mineral
nutrient use would be to manipulate these symbioses, for
example, to introduce mycorrhizas or symbiotic nitrogen
fixation into a wider range of crops. This is a ‘grand chal-
lenge’ but recent work has shown that here are common-
alities between the signalling pathways involved in
establishing both types of symbiosis (Oldroyd and
Robatzek, 2011). The influence of plant-microbe interac-
tions on plant performance goes well beyond these exam-
ples. Some plants harbour endophytic fungi that live in the
intercellular spaces of roots and shoots. In some cases, they
produce alkaloids that deter herbivores and recent work
suggests that endophytes can improve resistance to
drought and high temperature (Hubbard et al., 2014;
Redman et al., 2011). Soil fungi (e.g. Trichoderma species)
and bacteria also influence plant growth, pathogen resis-
tance and possibly abiotic stress resistance. There is a
potential to use an increased understanding how stress
resistance is influenced by interactions with soil micro-
organisms and fungal endophytes to tailor the crop
microbiomes for growth enhancement and stress resis-
tance. One can predict that this promising area is very likely
to attract increased research effort in coming years.
Concluding Remarks
Despite problems with translating the current reductive
approach into new stress resistant crop varieties, there are a
number of exciting developments underway that should
not only give new insights into stress physiology but may
also improve translatability. Rapid identification of can-
didate stress resistance genes is being enabled by the
increased availability of genomic resources produced by
faster and cheaper DNA sequencing in model species such
as Arabidopsis and rice. However, the successful transla-
tion to crops will depend on the model systems being
subjected to realistic levels of stress relevant to the target
10 eLS & 2014, John Wiley & Sons, Ltd. www.els.net
crop and environment. We are beginning to appreciate that
plants deliberately restrain their growth when they perceive
stress and that we can potentially interfere with these sig-
nalling systems to delay stress responses. This would enable
crops to continue their growth (which improves the final
yield potential) under mild stress. Since stress is usually
mild in environments that allow reasonably productive
agriculture, this approach may provide benefits. Impor-
tantly, it differs conceptually from current research which
is focussed on more extreme stresses. Another emerging
area is the plant microbiome: manipulating the types of
microorganisms present around roots and within plant
tissues has great promise for improving both resource use
and stress resistance.
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