Mechanisms that protect against abiotic stress are essential for plant survival, yet
their activation generally comes at the expense of growth and productivity, which
is particularly serious for agriculture. Recent developments in molecular genetics
have contributed substantially to our understanding of the basis of abiotic stress
defense. Progress has also been made towards understanding how plants control the
switch between growth and defense, especially with regard to timing and mechanism.
This ongoing research is critical for the improvement of crop plants.
Cell proliferation and growth require nutrients, biosynthetic capacity and energy.
Restricting any one of these factors will lead to arrested growth and eventually death.
To ensure their survival it is therefore necessary for living organisms to anticipate
changes in the environment that might affect their capacity to grow, and then to mount
an effective acclimatory response. This is particularly important in plants, which
are typically immobile and encounter large fluctuations in temperature, light, humidity
and nutrient availability in their natural environment (see Box 1). Environmental
stress causes massive agricultural losses (Godfray et al., 2010; Cramer et al., 2011),
and improving crop tolerance is a major goal of crop improvement programs. However,
tolerance can come with trade-offs; for example, it has long been known that stress-tolerant
plants have lower growth rates and productivity (reviewed by Chapin, 1991). Therefore,
in addition to understanding the basis of tolerance, it is also important to understand
the trade-offs between tolerance and growth/productivity for effective crop improvement.
Box 1. Plant growth during abiotic stress
Carbohydrate resources and energy generated by photosynthesis (circular arrows) are
allocated to growth and reproduction. Nutrient limitation or abiotic stress exposure
can limit growth and also lead to over-excitation of the photosynthetic electron transport
chain and the production of potentially damaging ROS. Timely perception of stress
leads to the modulation of plant growth and the activation of defense and acclimation
pathways that can act within specific plant organs, or across the entire plant. Key
players in the control of plant growth during abiotic stress are shown. Chloro, chloroplast;
GA, gibberellins; BR, brassinosteroids; SA, salicylic acid; ET, ethylene.
The impact of abiotic stress on plant performance is being explored at many different
levels, in a great variety of model and crop species, and includes metabolic/physiological
responses, molecular signaling pathways, ecophysiology and crop breeding studies.
In addition, abiotic stress is not a single entity but rather comprises all the environmental
perturbations that plants may encounter in nature. Consequently, the literature on
abiotic stress responses is vast, and covers very diverse research areas. Here, we
focus on a selection of recent advances made in our understanding of the molecular
mechanisms that control plant growth during abiotic stress.
Nutrient and water limitation: the root perspective
Nutrient limitation has drastic effects on plant growth and development. Under mild
nutrient deprivation plant architecture may be modified to increase nutrient uptake,
while severe nutrient limitation may lead to complete growth arrest. Roots are essential
for water and nutrient uptake, but also serve a variety of other functions, such as
forming symbioses with other microorganisms in the rhizosphere, anchoring the plant
to the soil, and acting as storage organs. Consequently, roots are essential for optimal
plant productivity. Many abiotic stresses are first encountered at the root level
often leading to changes in root biomass and architecture. For example, primary root
growth stops when Arabidopsis seedlings are transferred to media without phosphate.
This growth arrest is the consequence of a signaling pathway mediated by STOP1, ALMT1
and LPR2 (Balzergue et al., 2017). Strikingly, knockout mutants of these genes lose
the root growth arrest response on phosphate removal, indicating that root growth
arrest is not a result of metabolic limitation.
Importantly, when roots encounter changes in environmental conditions they will change
growth direction in order to optimize plant survival. Such directional changes in
response to stimuli (tropisms) include where roots sense the soil water content and
grow towards water to avoid dry soil by either changing direction or halting growth.
Despite water sensing being the subject of very early plant physiology studies, until
recently the mechanisms of this growth response were essentially unknown. Some genes
required for hydrotropism, such as MIZ1 and MIZ2/GNOM, have now been identified (Kobayashi
et al., 2007; Miyazawa et al., 2008), and a role identified for the action of plant
hormones such as auxin, ABA and cytokinin (Moriwaki et al., 2011; Moriwaki et al.,
2012; Saucedo et al., 2012). More recently the site of water perception and growth
control was localized to the root cortex (Dietrich et al., 2017), and progress and
perspectives in the active hydrotropism field are reviewed in this issue by Dietrich
(2018). The review highlights the many outstanding questions that remain regarding
the signaling pathways involved in hydrotropism, as well as the need for further research
in this area. Indeed, it has been suggested that the genes involved in hydrotropism
could be important targets for crop improvement by enhancing drought avoidance. A
recent demonstration that a robust hydrotropic response leads to better growth under
drought and partial lateral irrigation in different maize cultivars strongly supports
this notion (Eapen et al., 2017).
Growing pains: abiotic stress
Abiotic stress leads to altered biosynthetic capacity and nutrient acquisition that
can inhibit plant growth. This phenomenon is documented in many research papers on
model and crop species alike. Consequently, research into understanding the responses
to abiotic stress has moved to the forefront over the past decade, leading to the
discovery of several signaling pathways involving a large number of genes, proteins
and post-translational modifications. These include the MAPK, ABF/bZIP, Ca2+-CBL-CIPK
and CBF/DREB signaling pathways, which employ numerous stress-responsive transcription
factors to orchestrate the downstream responses required to mount an effective defense
to specific abiotic challenges (Wang et al., 2016; Zhu, 2016).
Importantly, these molecular signaling pathways can anticipate the effects of abiotic
stress to regulate the balance between growth and acclimation. More recently, efforts
into understanding how plant growth is regulated under stress conditions has resulted
in the identification of candidate genes that may integrate both processes. For example,
the molecular mechanisms that control leaf growth under mild drought conditions link
both growth and transcriptional responses to the circadian clock. Specifically, two
ETHYLENE RESPONSE FACTORS (ERFs), ERF2 and ERF8, were found to affect leaf growth
under drought and well-watered conditions (Dubois et al., 2017). Interestingly, in
the same study the specific up-regulation of three genes encoding growth-repressing
DELLA proteins was observed during the early drought response (Dubois et al., 2017).
DELLA proteins have previously been shown to accumulate under nutrient deficiency,
low temperature treatment and in response to salt stress (Achard et al., 2008; Xie
et al., 2016). DELLAs promote stress-inducible anthocyanin biosynthesis through the
formation of a JAZ–DELLA–MYBL2 complex (Xie et al., 2016) and can also promote ROS
scavenging to delay cell death (Achard et al., 2008). Stress-induced anthocyanin accumulation
is significantly inhibited in della mutants (Xie et al., 2016), while under salt stress
della quadruple mutants produce significantly more ROS than the wild type (Achard
et al., 2008). DELLA proteins therefore promote survival under abiotic stress conditions.
Interestingly, reduced anthocyanin accumulation in response to high light was also
observed in the ascorbate-deficient mutants vtc2-1 and vtc2-4, yet both vtc mutants
experienced identical levels of photodamage compared to wild type. This suggests that
ascorbate is not essential for photoprotection during high light, but intriguingly
is required for the accumulation of rosette biomass under low-light and short-day
conditions (Plumb et al., 2018).
Signal transduction pathways mediated by phytohormones can play a critical role in
abiotic stress responses (reviewed by Verma et al., 2016). For example, ABA plays
a key role in stress responses, while auxin plays a major role in promoting plant
growth. The interplay between phytohormones is therefore an important mechanism for
balancing growth and stress resistance. Brassinosteroids are a class of plant steroid
hormones that promote growth via the activation of the transcription factors BZR1
and BES1. A recent study has shown that drought stress represses the brassinosteroid
signaling pathway, and thereby growth, by promoting the degradation of BES1 via ubiquitination
and selective autophagy (Nolan et al., 2017). This example highlights the importance
that plant hormones can have as major integrators of environmental stress and nutrient
Hunger games: nutrient and energy signaling
Over recent years it has become clear that plants integrate energy/nutrient status
to regulate growth and stress responses using antagonistic signaling pathways mediated
by the evolutionarily conserved protein kinases TOR (TARGET OF RAPAMYCIN) and SnRK1
(Snf1-RELATED PROTEIN KINASE1) (Robaglia et al., 2012; Broeckx et al., 2016; Baena-González
and Hanson, 2017). The central role of these kinases in energy metabolism is underlined
by their wide conservation in the eukaryotes, from yeast and animals to plants and
fungi (Roustan et al., 2016). SnRK1 is activated by low-energy conditions, such as
those that may occur during stress exposure, to trigger catabolism and repress growth.
Notably, SnRK1 can be activated by the inhibition of photosynthesis with the inhibitor
DCMU, and can be inhibited by the addition of sugars. SnRK1 directly targets metabolic
and regulatory enzymes in the cytosol, and also affects gene expression via the phosphorylation
of transcription factors such as BZIP63 (Mair et al., 2015; Nukarinen et al., 2016).
In contrast, TOR promotes cell growth and proliferation in response to light, sugars,
and growth-promoting hormones through the phosphorylation of target proteins (recently
reviewed by Schepetilnikov and Ryabova, 2018). Over the past 10 years a growing number
of TORC client proteins and downstream effectors have been firmly identified in plants,
including the S6 kinase, E2F, and the brassinosteroid pathway. A very recent study
has shown that TOR can also phosphorylate the ABA receptor PYL to prevent activation
of the ABA-signaling effector kinase SnRK2 in non-stressed plants (Wang et al., 2018).
In turn, under stress conditions, ABA is able to activate SnRK2, which then phosphorylates
a member of the TOR complex RAPTOR, which triggers complex dissociation and TOR inactivation.
This antagonistic signaling loop is an excellent example of how plants are able make
the decision between growth and stress acclimation. Interestingly, both TOR and SnRK1
have been implicated in the regulation of chloroplast function (Dong et al., 2015;
Dobrenel et al., 2016; Nukarinen et al., 2016; Sun et al., 2016; Imamura et al., 2018).
It all comes down to light: chloroplasts at the centre of stress perception and regulation
Chloroplasts are one of the powerhouses for plant productivity, but photosynthesis
is highly sensitive to light, CO2 levels, and plant metabolic capacity. Excess light,
or limitation in CO2 supply or metabolic capacity, during abiotic stress exposure
rapidly leads to over-excitation and reduction of the photosynthetic electron transport
chain. Over-excitation is potentially highly dangerous for the plant because it can
lead to the production of ROS such as 1O2 and H2O2 that can irreversibly damage proteins,
membranes and DNA. However, changes in chloroplast redox status during overexcitation
act as a signal that leads to the rapid activation of energy-dissipating mechanisms,
changes in chloroplast genome expression, and over the longer term to changes in chloroplast
protein composition and position to allow acclimation. Importantly, chloroplast stress
triggers acclimation at the cellular level as well as the organellar level, and as
the severity of stress increases can lead to growth inhibition and eventually programmed
cell death (Laloi and Havaux, 2015). The majority of chloroplast proteins are encoded
in the nuclear genome. Remodelling of the chloroplast proteome during abiotic stress
acclimation therefore requires signaling from the nucleus to the chloroplast (anterograde
signaling), and from the chloroplast to the nucleus (retrograde signaling). An overview
of chloroplast proteome remodelling, with a focus on stress-regulated import of proteins,
nuclear control of the chloroplast genome and protein turnover within the chloroplast
is reviewed in this special issue (Watson et al., 2018). Stress-induced retrograde
signaling from the chloroplast is also considered from a different perspective by
Crawford et al. (2018). In particular, these authors discuss how the stress-induced
down-regulation of photosynthesis and respiration in the mitochondria can lead to
a reduction in the supply of energy available for cellular stress acclimation. They
propose a new hypothesis for the integration of different organellar retrograde signals
in the nucleus to coordinate transcriptional responses that regulate the allocation
of energy to either growth or stress acclimation. Notably, and in relation to this
hypothesis, recent work indicates that chloroplast-generated H2O2 acts as a retrograde
signal that is directly transferred from the chloroplast to the nucleus, avoiding
the cytosol, to drive a transcriptional response (Exposito-Rodriguez et al., 2017).
Stress can also lead to transcriptional reprogramming within the chloroplast, and
the signaling nucleotides guanosine tetra- and penta-phosphate [or (p)ppGpp] potentially
play a major role (Field, 2018). Indeed, (p)ppGpp is known to accumulate in response
to a wide range of different abiotic stresses, and both in vitro and in vivo studies
show that (p)ppGpp accumulation inhibits chloroplast transcription and affects chloroplast
function. These findings and other recent advances in our understanding of (p)ppGpp
metabolism in plants and algae are reviewed by Field (2018).
While light plays an obvious role in the production of photosynthates and energy,
a perhaps less intuitive role is in the regulation of biomass partitioning and plant
architecture in response to resource availability, which can occur in a phytochrome
B (PHYB) dependent manner (Arsovski et al., 2018). The function of phytochromes as
regulators of carbon supply, metabolic status and biomass production has been recently
proposed (Yang et al., 2016), and together with the PHYB- and light-dependent development
of stomata (Casson and Hetherington, 2014) emphasizes the close connection between
light perception and photosynthetic metabolism beyond photosynthetic electron transport.
PHYB was also recently shown to act as a temperature sensor in plants. PHYB activity
decreases with increasing temperature in a light-dependent manner (Legris et al.,
2016), to allow the optimization of growth and biomass production under different
environmental conditions. Furthermore, PHYB has been demonstrated to uncouple growth
and defense pathways through the relief of transcriptional repression, thereby providing
a direct link between light, plant growth and defense signaling pathways (Campos et
al., 2016; Cerrudo et al., 2017).
The trade-off between growth and defense: a balancing act?
In light of the diverse molecular mechanisms that regulate growth and abiotic stress
acclimation the question arises as to whether the induction of stress tolerance always
leads to growth penalties, or whether we can get something for nothing. It is commonly
thought that constitutive stress tolerance comes at a cost to the organism, and this
has been extensively reviewed for disease resistance traits (Heil, 2014; Heil and
Baldwin, 2002). Early examples of engineered constitutive abiotic stress tolerances
have often led to growth penalties under benign growth conditions (Kasuga et al.,
1999; Haake et al., 2002). Another example is the Physcomitrella patens ppabi1a/b
double mutant, where ABA signaling is constitutively active, which is stress resistant
but also shows very severe growth defects (Komatsu et al., 2013). However, there are
now many indications that the cost need not always be so high. C24, an Arabidopsis
ecotype from the Iberian peninsula, is resistant to ROS, heat and drought stress yet
shows similar productivity to less-tolerant ecotypes. These features have led to research
into the genetic and molecular basis of the growth/resistance equilibrium in C24,
and is reviewed in this issue by Bechtold et al. (2018). The hope is that research
in such a tractable model species may lead to the rapid development of new strategies
for conferring stress resistance to crop plants without penalties. The basis of C24
stress resistance is likely to be complex and multigenic. However, even the overexpression
of a single transcription factor gene, such as Heat Shock Transcription FactorA1b,
can lead to penalty-less increases in abiotic stress resistance (Bechtold et al.,
2013), and other positive examples utilizing single-gene manipulations are highlighted
in Bechtold et al. (2018). Intriguingly, the molecular basis of HSFA1b stress resistance
appears to be in its ability to regulate the expression of a large hierarchical network
of stress and development genes (Albihlal et al., 2018), suggesting the HSFA1b could
be a master regulator of the switch between growth and abiotic stress defenses. It
will also be fascinating to discover how such ‘penalty-less’ improvements in stress
tolerance are able to bypass SnRK1/TOR-mediated growth control.
Research into plant responses to environmental stress and the application of this
knowledge to improve productivity under non-optimal growing conditions is becoming
ever more important. Over recent years dramatic progress has been made, and the molecular
mechanisms for many stress response pathways revealed. Identification of the cellular
hubs that integrate these diverse stress acclimation mechanisms, and the regulatory
logic behind the plant’s decision-making processes, are now emerging themes in the
field. Over coming years further research in these directions has the potential to
lead to a more unified view of plant growth and abiotic stress resistance that could
be applied for the rational improvement of crop plants.