Plant Science 234 (2015) 155–162
Contents lists available at ScienceDirect
Plant Science
journal homepage: www.elsevier.com/locate/plantsci
Review
The evolution of drought escape and avoidance in natural herbaceous
populations
Nicholas J. Kooyers ∗
Department of Biology, University of Virginia, Charlottesville, VA 22904, USA
a r t i c l e
i n f o
Article history:
Received 31 October 2014
Received in revised form 4 February 2015
Accepted 19 February 2015
Available online 25 February 2015
Keywords:
Adaptation
Plasticity
Drought resistance
Water-use efficiency
Gene by environment interactions
Flowering time
a b s t r a c t
While the functional genetics and physiological mechanisms controlling drought resistance in crop plants
have been intensely studied, less research has examined the genetic basis of adaptation to drought stress
in natural populations. Drought resistance adaptations in nature reflect natural rather than humanmediated selection and may identify novel mechanisms for stress tolerance. Adaptations conferring
drought resistance have historically been divided into alternative strategies including drought escape
(rapid development to complete a life cycle before drought) and drought avoidance (reducing water loss
to prevent dehydration). Recent studies in genetic model systems such as Arabidopsis, Mimulus, and Panicum have begun to elucidate the genes, expression profiles, and physiological changes responsible for
ecologically important variation in drought resistance. Similar to most crop plants, variation in drought
escape and avoidance is complex, underlain by many QTL of small effect, and pervasive gene by environment interactions. Recently identified major-effect alleles point to a significant role for genetic constraints
in limiting the concurrent evolution of both drought escape and avoidance strategies, although these constraints are not universally found. This progress suggests that understanding the mechanistic basic and
fitness consequences of gene by environment interactions will be critical for crop improvement and
forecasting population persistence in unpredictable environments.
© 2015 Published by Elsevier Ireland Ltd.
Contents
1.
2.
3.
4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The evolution of drought escape in natural populations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Prevalence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Fitness consequences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
Genetic basis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The evolution of drought avoidance in natural populations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1.
Prevalence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.
Fitness consequences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3.
Genetic basis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.4.
Resource reserves as drought avoidance adaptations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.5.
Genetic tradeoffs in the evolution of drought resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
A path toward understanding drought resistance adaptations in natural populations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
∗ Tel.: +1 434 924 0162.
E-mail address: [email protected]
http://dx.doi.org/10.1016/j.plantsci.2015.02.012
0168-9452/© 2015 Published by Elsevier Ireland Ltd.
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1. Introduction
Climate models forecast an increase in both the severity and
frequency of drought in the coming 50 years [1]. This change is
especially difficult for sessile organisms such as plants, which
must be able to respond to wide fluctuations in growing season conditions while still maintaining the ability to correctly time
developmental processes in response to environmental cues. At
a population level, increasing aridity and drought should lead
to strong directional selection for plants with higher fitness
under drought conditions (i.e., drought-resistant plants); however, a more nuanced understanding of genes and traits under
selection is limited by an incomplete knowledge of the mechanisms that plants use to resist drought stress [2]. Without
understanding the innate resistance mechanisms plants possess,
it is difficult to accurately assess future population persistence.
Determining the prevalence and variation in the mechanisms
underlying stress resistance and adaptation is a key goal for plant
biologists.
Unlike in natural populations, responses to drought stress have
been widely studied in a few major crop plants [3–7]. This literature has resulted in an improved understanding of the physiological
pathways involved in drought perception and response as well as
identified major-effect genes controlling drought resistance [3].
However, wild populations often harbor large pools of genetic and
phenotypic diversity that can provide insights into novel mechanisms of acquiring drought resistance. These insights can range
from characterizing new phenotypes to identifying new roles for
genes involved in abiotic stress-response pathways. While understanding the diversity and prevalence of mechanisms underlying
drought resistance in natural populations clearly benefits evolutionary biologists, these results can also help agronomists more
effectively improve or develop crops. Here I synthesize recent
progress describing how drought resistance has evolved in natural
populations of herbaceous plants. I focus on studies that identify the
genetic basis of drought strategies as well as describe the evidence
that these strategies are advantageous in natural populations.
Adaptation to soil water availability is common across the
ranges of plant species and is associated with the formation of
ecotypes [8,9]. Adaptations conferring drought resistance have historically been divided into three alternative strategies: drought
escape, drought avoidance, and drought tolerance [10]. Each of
these strategies may evolve as a constitutive response that occurs
independently of environmental cues such as water deficit, or can
evolve as a heritable plastic response that is dependent on one
or more environmental cues. Drought escape occurs when plants
develop rapidly and reproduce before drought conditions become
severe. Cession of vegetative growth may or may not accompany
a drought escape response. In contrast, drought avoidance occurs
when plants increase water-use efficiency (WUE) by reducing transpiration, limiting vegetative growth, or increasing root growth,
and avoid dehydration during transient periods of drought stress.
Drought avoidance has also been referred to as dehydration avoidance in recent literature. Finally, drought-tolerant plants are able
to withstand dehydration through osmotic adjustment and production of molecules that stabilize proteins (Fig. 1; [10]). These
strategies are coordinated physiological syndromes that involve
many physiological and structural traits [11]. For instance, drought
avoidance through increased WUE is mediated by lowering stomatal conductance, which in turn can be influenced by a number
of different potentially correlated traits such as leaf area, leaf lobing, succulence, or stomatal density. Here, I will focus on recent
advances understanding drought escape and avoidance. These
advances are largely limited to studies examining flowering time
as a measure of drought escape and leaf-level WUE as a measure
of drought avoidance as these are the traits that have received
the most attention. Mechanisms of drought tolerance have been
covered in detail elsewhere [3,12].
Although each of these strategies is predicted to evolve in areas
of frequent drought stress, they are often viewed as alternative
strategies or syndromes that can be optimally employed in specific seasonal contexts for plants with specific life history strategies
(Fig. 1; [6,13]). For instance, drought escape may be optimal for
annual plants in environments with short growing seasons that are
ended by severe terminal drought; whereas drought avoidance may
be more optimal if the growing season is punctuated by transient
droughts. These strategies are unlikely to evolve together because
plants devoting all of their resources to rapid reproduction need
to have high rate of carbon fixation and thus also high stomatal
conductance. However, plants typically avoid drought by lowering
stomatal conductance to conserve water and thus reducing the rate
of carbon fixation and growth. The literature has largely supported
this view with the most detailed examples pointing toward the
independent evolution of drought escape and avoidance strategies
[14,15]. There is limited evidence in some systems that suggests
that there are not genetic constraints to the concurrent evolution
of both strategies within individual populations [16]. The environmental conditions that favor evolution of specific strategies is still
an open topic and identifying the genetic constraints and fitness
ramifications associated with each strategy is an area of strong
interest.
While phenotypes associated with escape or avoidance strategies have often been studied (e.g., [14,17,18]), obtaining a detailed
understanding of the genetic and physiological mechanisms that
plants use to escape or avoid drought in natural populations has
been challenging. Recreating realistic drought conditions in an
experimental setting is difficult and may not necessarily reflect field
conditions [19]. Drought can combine the effects of water deficit
and possible heat stress. Manipulating water availability is complicated in dry-down experiments because water uptake is greater in
bigger plants; a problem that can create heterogeneity in the timing of water deficits [20]. An additional challenge is finding species
with populations that thrive across a range of aridity conditions and
that also possess a genetic toolbox amenable to exploring the genes
and pathways responsible for adaptive divergence in morphology
and physiology. In model genetic species where the genetic basis
of drought escape or avoidance has been characterized, there are
often multiple QTL (quantitative trait loci), each of small effect that
underlie variation in drought resistance. This makes it difficult to
identify the phenotypic effects of a given locus [21,22]. Further,
drought escape and avoidance can both be dependent on environmental context where a water deficit or other environmental cue
may induce rapid flowering or changes in WUE [23,24]. This inherent plasticity can complicate linkage mapping and make it difficult
to predict drought resistance and fitness consequences in a seasonal
environment.
Nevertheless, development of new ecological model systems
such as Mimulus guttatus, Avena barbata, and Panicum hallii as well
as renewed efforts to study Brassica rapa and Arabidopsis sp. in
ecological contexts has begun to provide new insights into the
genetics underlying adaptive drought escape and avoidance strategies. Specifically, work in these systems has begun to address
longstanding questions about ecophysiological traits regarding the
prevalence, adaptive value, and genetic architecture underlying
variation in these traits in natural populations [6]. Here I review
the advances made in the last decade toward identifying the fitness benefits and genetic basis of drought escape and avoidance
strategies as well as the constraints that limit concurrent evolution
of both strategies. This large body of the literature establishes that
variation in drought escape and avoidance traits is prevalent and
adaptive, and highlights promising systems where QTLs and genes
responsible for this variation are known. In addition, this review
N.J. Kooyers / Plant Science 234 (2015) 155–162
157
Fig. 1. Schematic diagram describing the three ways herbaceous plants evolve drought resistance. Each strategy has specific traits and phenotypes that have historically
been associated. The phenotypes listed here are examples and do not represent a complete list. Arrows designate the environmental context that would most favor each
strategy.
highlights the importance of gene by environmental interactions
in drought escape and avoidance—a useful insight for engineering
drought resistance in crop plants or predicting population persistence in natural populations.
2. The evolution of drought escape in natural populations
2.1. Prevalence
Plants can escape drought by developing rapidly and reproducing before the onset of drought. Thus, flowering time is often the
primary trait associated with drought escape in annual populations
of herbaceous plants. Earlier flowering during a drought-shortened
growing season presumably results in relatively greater fitness
through higher seed set or greater seed mass. Extensive variation in
flowering time in natural populations has been well documented
(e.g. [25]), and several studies have demonstrated that earlier flowering time evolves due to selection caused by drought [26,27]. A
central line of evidence for drought escape comes from common
garden experiments where plants from xeric areas flower earlier
in a common garden than plants from mesic areas. This approach
has yielded patterns consistent with drought escape in Arabidopsis
lyrata [28], Arabidopsis thaliana [29], Panicum hallii [21], Helianthus
anomalus [30], Mimulus guttatus [16], and Boechera holboellii [31].
These results have demonstrated that extensive genetic variation
in drought escape exists in natural populations.
Evolution of drought escape occurs not only through a constitutive difference in developmental timing, but also through changes
in the mechanisms by which populations respond to environmental cues, i.e., a plastic drought escape response. Plant time the
transition to flowering through temperature, vernalization, photoperiod, and water availability cues [32–34]. Adaptive drought
escape responses occur through temperature and photoperiod cues
[35,36]. The role of water availability as an environmental cue for
the transition to flowering is typically considered secondary to
photoperiod and vernalization cues; but may be the most important for breeding a drought escape response because it provides
the most accurate environmental assessment of drought. Evidence
for an adaptive drought escape response to water deficit in natural populations is limited. For example, the degree of plasticity
in flowering time between wet and dry experimental environments was constant for several Arabidopsis lyrata populations that
spanned a latitudinal gradient indicating that enhanced drought
escape response has not evolved within any of these populations
[28].
2.2. Fitness consequences
Evidence for drought escape as an adaptive strategy comes from
temporally replicated series of observations examining changes
in populations following drought events (longitudinal studies;
e.g.[26]), phenotypic selection analyses under water-limiting conditions (e.g., [18]), and reciprocal transplant experiments (e.g. [37]).
Adaptive drought responses have been well-characterized in multiple species. For instance, there was strong selection for earlier
flowering in two Brassica rapa populations following drought that
resulted in flowering an average of 1.9 days and 8.6 days earlier
in each population [26]. However, the general importance of a
plastic drought escape response in natural populations is debatable given the limited number of species with a documented
drought escape response. The drought escape response in the same
Brassica rapa populations described above was also examined,
and there was no evidence for increased plasticity for flowering
time after the aforementioned drought event [38]. While these
experiments do not identify plastic drought escape responses as
adaptive, few experiments have explicitly tested the adaptive value
of plastic responses to drought. Further empirical and theoretical
studies are necessary to identify conditions when such acclimation may be advantageous. For instance, evolving a highly plastic
drought escape response may be more likely where severe droughts
have occurred infrequently over the evolutionary history of a lineage, whereas evolving a constitutive drought escape response
may occur if droughts have occurred frequently over the same
timespan.
2.3. Genetic basis
The genetic architecture underlying variation in drought escape
has been elucidated in a number of species, although the specific
genes and their physiological effects remain relatively uncharacterized. One promising system is Panicum hallii, a switchgrass relative
found along an aridity gradient in the U.S. desert southwest. Both
a xeric ecotype (P. hallii var. hallii) and a mesic ecotype (P. hallii
var. filipes) exist. There is extreme divergence in flowering time
between these ecotypes where var. hallii flowers in approximately
half the time (∼44 days) it takes var. filipes (∼85 days) in a common
mesic environment. QTL mapping experiments have identified two
regions that account for small but significant portions of this difference [21]. This extensive variation in flowering time between
geographically close populations provides a promising system to
study the ecological genetics of drought resistance.
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N.J. Kooyers / Plant Science 234 (2015) 155–162
Studies in more established systems have progressed to identify
the molecular genetic basis and physiological mechanisms underlying drought escape. For instance, Mimulus guttatus is quickly
becoming a model plant for studying drought escape and avoidance in natural populations [39]. The growing season of annual
ecotypes of M. guttatus is ended by terminal drought; however,
there is extensive variation in the timing and duration of the growing season. A survey of flowering time in a common environment
that utilized 51 populations collected along 10 separate altitudinal transects demonstrated that populations with shorter growing
seasons flower earlier under inductive conditions [16]. Reciprocal
transplant experiments between annual and perennial M. guttatus ecotypes reveal a clear connection between earlier flowering
and fitness in a population with a short growing season typically
ended by drought [40]. QTL mapping following up on these reciprocal transplant experiments identified several regions contributing
to fitness through earlier flowering and higher survival, including the candidate gene DIV2 [41]. Subsequent work demonstrated
that a single inversion that includes DIV2 is responsible for a large
portion of divergence in flowering time and fitness between ecotypes and that this inversion is widespread throughout the range of
M. guttatus [42]. Interestingly, this QTL represented only 1 of 6 QTL
found for flowering time, indicating that many additional loci of
smaller effect also contribute to drought escape in this system [41].
Collectively, this work demonstrates a clear fitness advantage for
rapidly developing plants in populations with drought-shortened
growing seasons, as well as identifies an inversion as the molecular
genetic basis for variation in drought escape. QTL studies such as
the ones described above provide information about which genes or
locations in the flowering regulatory network can be successfully
tweaked to induce earlier flowering without producing negative
tradeoffs in growth or reproduction.
The above examples target the genes involved in constitutive
differences in drought escape, but less is known about drought
escape as a plastic response to water deficit. Two experiments utilizing genetic knockouts in Arabidopsis thaliana have connected
water availability cues to abscisic acid (ABA) signaling as well as
to several genes in the flowering gene regulatory network [33,43].
Water deficit is largely perceived by the roots and promotes an
increase in ABA levels throughout the plant. ABA promotes transcriptional upregulation of FT, TSF, and SOC1 leading to flowering
only under long days [33]. The expression of GIGANTEA (GI), a member of the photoperiod pathway, is key in ensuring that drought
escape response only occurs under long day conditions. Under long
day conditions, GI is expressed and interacts independently of other
photoperiod pathway members such as FKF1, ZTL, or CO to enable
ABA-mediated expression of FT and SOC1. It is hypothesized that GI
regulates chromatin accessibility and blocks repressors of FT and
SOC1 (such as SVP and FLC) to allow drought escape responses to
occur [33]. However, GI does have other roles in starch metabolism
and carbon signaling in Arabidopsis as well as interactions with the
gibberellic acid signaling pathway that could promote expression
of FT and lead to a drought escape response [44,45]. These links
between the ABA signaling network, the flowering gene regulatory
network, and water availability signals have not been fully synthesized into a coherent framework. Development of this connection is
a major priority for understanding how drought escape responses
are elicited and able to vary in natural populations.
While the role for heritable genetic variation in the evolution of constitutive and plastic drought escape is well established,
the role of epigenetic variation is more controversial. There are
numerous examples detailing how DNA methylation, histone modification, and chromatin remodeling regulate gene expression
constitutively and in response to environmental cues such as
drought [46]. However, researchers have yet to identify an epigenetic variant that underlies phenotypic differences in phenology
and fitness differences within natural populations. In a set of
Arabidopsis epiRILs (lines with nearly identical genomes but contrasting DNA methylation profiles), variation in DNA methylation
has been associated with heritable variation in flowering time as
well as several other important ecological traits [47,48]. This experiment demonstrates the potential of epigenetic variation as an
underlying molecular basis for adaptive evolution. Additionally,
drought may act to environmentally induce epigenetic changes
and lead to a drought escape response. Evidence that epigenetic
variants create adaptive variation in drought escape in natural
populations is currently nonexistent, but this does not mean it
does not exist. Identifying the role of this variation is an open
and important question in the drought literature given the significant role that epigenetic modification plays in eliciting stress
responses [46].
3. The evolution of drought avoidance in natural
populations
3.1. Prevalence
Drought avoidance adaptations can occur through a myriad of
morphological and physiological traits. Accessions adapted to xeric
conditions may have lower specific leaf area [49], greater succulence [50], increased leaf reflectance [51], accentuated leaf lobing
[52], and altered stomatal size and density [53], although these
traits do not necessarily coordinately evolve in a drought avoidance syndrome. Many of these traits are expected to contribute to
variation in transpiration efficiency, with drought-avoiding plants
from xeric populations having greater WUE through higher photosynthetic capacity and lower transpiration. Transpiration efficiency
is a measure of performance, and is approximated at leaf-level
through both instantaneous WUE and an integrated measure of lifelong transpirational efficiency (␦13 C; [54] for review). In addition to
reducing water loss, plants may slow or cease growth in response to
incipient drought as a method of avoiding dehydration [55]. Adaptations conferring drought avoidance may also involve higher ratios
of root to shoot growth prior to drought conditions [31]; this adaptation may be more advantageous for longer-lived perennial plants
as a larger root system may provide a cost-effective advantage in
multiple growing seasons [56,57]. Unfortunately, root to shoot ratio
has proven difficult to measure in natural populations and better
methodology is a key need for deciphering the importance of this
phenotype. Here I focus on a drought avoidance strategy achieved
by regulating WUE as this phenotype has constituted the majority
of studies.
Similar to drought escape strategies, drought avoidance can
evolve as a constitutive change in WUE or as a plastic response to
water deficit or other environmental cues. Despite strong evidence
that traits conferring drought avoidance are prevalent in populations located in xeric areas, there are few cases where xeric-adapted
ecotypes have consistently higher WUE than mesic-adapted ecotypes across several environments [17,31,37,39]. Instantaneous
WUE appears to be a more plastic phenotype than flowering time
with a generally low broad sense heritability (h < 0.1) [6]. Some
plants with high instantaneous WUE in adequately watered conditions have low instantaneous WUE in water-limited conditions
[23,58]. Indeed, accessions from xeric areas are frequently reported
to have higher WUE than accessions from mesic areas only under
drought conditions indicating that improved WUE is the product
of a gene by environment interaction contingent on the presence
of a water deficit [17,37,59]. Thus, although many studies have
measured water-use efficiencies in lines from natural populations,
few conclusions can be drawn about the prevalence of drought
avoidance adaptations in nature. Future experiments need to examine the degree of plasticity in natural populations to draw more
N.J. Kooyers / Plant Science 234 (2015) 155–162
nuanced conclusions about the frequency of drought avoidance
adaptations.
3.2. Fitness consequences
The innate plasticity in WUE has made it difficult to characterize relationships between WUE and fitness in natural populations.
Results from those that have measured fitness are mixed. Boechera
holboellii from xeric environments had higher instantaneous WUE
through lower stomatal conductance as well as increased investment in root biomass and lower leaf mass per unit area [31]. Plants
from the xeric area were more fit in their native environment in a
reciprocal transplant experiment suggesting that these phenotypic
differences led to higher fitness in xeric conditions. Phenotypic
selection analyses also suggest that plants with lower stomatal
conductance are more fit in xeric environments [17]. However,
in the natural populations where these experiments were conducted, plants from the xeric environment do not necessarily have
higher WUE or lower stomatal conductance than plants from the
mesic environments. This suggests that while higher WUE may be
selected in one particular year, directional selection is not consistently strong enough to cause adaptive differentiation between
populations from xeric and mesic areas. The results from other systems are more nuanced and context dependent. There is evidence
for selection for high WUE varieties of Impatiens capensis during
a normal relatively dry growing season [60], but low WUE plants
that flower earlier were selected during an early season drought
in a subsequent experiment [61]. This suggests that the type of
drought strategy under selection depends on when drought stress
occurs in development and the intensity of the drought. The fitness
consequences of having higher WUE are often unintuitive in annual
plants. A series of papers contrasting xeric- and mesic-adapted ecotypes of Avena barbata find that plants that are able to acquire
resources, develop quickly, and flower early are favored in both
environments [62–64]. Notably, plants with lower stomatal conductance, such as that found in the xeric ecotype, had no advantage
in any environment, but those with elevated rates of carbon fixation
acquire resources and flower more quickly in both environments.
Perhaps the xeric ecotype would be favored during years with more
extreme drought conditions, and reciprocal transplant experiments
failed to catch this variation. Collectively, these experiments suggest that WUE is not a simple performance phenotype that can be
used easily for breeding.
3.3. Genetic basis
Given the phenotypic complexity of WUE it is not surprising
that the physiological mechanisms connecting genetic variation
with phenotypic variation are just beginning to be elucidated [53].
A limited number of genes underlying variation in WUE in natural populations have been identified. Two notable examples of
genes underlying variation in WUE have recently been identified in divergent Arabidopsis thaliana accessions, Tus-1 and Kas-1.
These accessions have distinctly different physiological strategies
where Tus-1 plants flower earlier and have lower WUE than Kas-1
plants. This physiological difference is caused by loss of function
allele at FRI (FRIDIGA) in Tus-1 plants conferring an enhanced
drought escape strategy. The loss of a function FRI allele also
causes decreased WUE through increased stomatal conductance
[15,65,66].
A separate cross between divergent Arabidopsis lines Landsberg
erecta (Ler) and Cape Verde Islands (CVI) have uncovered several
small-effect QTL that underlie variation in stomatal conductance
[22]. One of these QTL has a single non-synonymous substitution at a highly conserved glycine residue in the gene MPK12,
and is responsible for a sizable portion of variance in stomatal
159
conductance [59]. MPK12 encodes a protein that regulates stomatal guard cell physiology. Plants with this substitution have larger
guard cells and stomatal openings. Interestingly, this substitution
also has environment-dependent effects; when subjected to ABA
treatment (as occurs following perception of water deficit), plants
with this substitution are not able to retain stomatal closure as
long as plants without this substitution. This suggests a partially
impaired ability to respond to a critical environmental cue. All of
the work conducted on drought avoidance has demonstrated the
need for a greater understanding of gene by environment interactions [24]. Future progress in identifying the adaptive significance
and genetic basis of drought avoidance will rely on developing a
better understanding about how water deficit is perceived, as well
as the pathways involved in signal transduction and developmental
responses. A solid understanding of both the stomatal developmental pathway [67] and the ABA response pathway [68] already exists
and connections are rapidly being synthesized. This framework is
necessary for candidate gene approaches, such as those utilized in
the above Arabidopsis research.
3.4. Resource reserves as drought avoidance adaptations
Much of the drought avoidance research has focused on transpiration efficiency despite the existence of other drought avoidance
mechanisms. The production of compounds that act as stress protectants or stabilize critical proteins during water deficits are
normally associated with the evolution of a drought tolerance
strategy. However, plants may rely on either developing large
stores of nutrients in prime conditions and/or diverting resources
maintaining homeostasis during initial water deficits as a drought
avoidance strategy. For example, Lupinus alba diverts organic nitrogen and carbohydrate resources from stems to seed pods at the
first sign of water deficit. This reallocation results in similar seed
set as plants that have not been subjected to drought stress [69].
Enhanced carbohydrate storage may be beneficial to all plants that
frequently undergo drought stress as closing stomata to reduce
water loss also reduces CO2 uptake and growth. Whether these
short-term reserves are used to maintain homeostasis or support
a reduced level of metabolism over longer stretches may depend
on the history of drought intensity and frequency within a given
population. Populations adapted to frequent short-term droughts
may be able to maintain homeostasis, while those accustom to
longer droughts may reduce growth rates and adjust metabolism
accordingly.
During the beginning stages of drought, nitrogen also becomes
limited due to diminished nitrogen reductase activity. Thus, developing basic reserves of usable plant nitrogen would be useful during
short-term droughts. Cyanogenic glucosides may play this nitrogen reserve role in white clover (Trifolium repens). The presence
of cyanogenic glucosides is polymorphic in white clover, and the
presence of cyanogenic glucosides has long been thought to act
as an herbivore deterrent. New evidence suggests that the ability
to produce cyanogenic glucosides also confers a fitness advantage under drought conditions [70]. Cyanogenic glucosides have
been identified as a nitrogen transport or storage molecules in several other species [71], and the regulatory network detailing the
breakdown of cyanogenic glucosides in useable plant nitrogen has
been characterized in sorghum [72]. Further work must demonstrate that concentrations of cyanogenic glucosides decrease during
drought, and levels of NO3 − are maintained throughout short-term
droughts. Other common molecules may serve a similar reservoir
or buffering role. For instance, trehalose, a previously identified
osmoprotectant, may serve as a reserve carbohydrate [73]. Identification of other such short-term reserves may serve as useful
untapped variation for introducing into crop-breeding programs.
160
N.J. Kooyers / Plant Science 234 (2015) 155–162
3.5. Genetic tradeoffs in the evolution of drought resistance
While drought escape and drought avoidance are frequently
viewed as alternative strategies for adapting to drought stress,
phenotypic selection analyses in the field suggest that directional
selection acts to both increase WUE and reduce time to flowering
if this variation is present [74]. Empirical studies have often provided evidence of negative genetic correlations between drought
escape and avoidance traits, where plants that have evolved rapid
development and earlier flowering often have reduced WUE and
capacity for drought avoidance [14,15,17,22,66]. Physiologically,
this negative correlation makes sense: if a plant closes its stomata to
reduce stomatal conductance, there should be a reduction in photosynthetic rate due to limited CO2 uptake that slows growth and
development. Empirically, a negative genetic correlation between
flowering time and WUE has been shown in Arabidopsis thaliana.
This correlation is attributable to antagonistic pleiotropy at the
FRI locus where a loss of function allele is associated with earlier
flowering and lower WUE [15,65,66]. This result suggests that the
evolution of drought resistance is subject to a genetic constraint
that may prevent breeding programs from developing lines that
have high WUE as well as rapid generation time.
However, several counterexamples to this trend have reported
associations between flowering time and either ␦13 C or instantaneous WUE where earlier flowering plants also have higher
WUE [16,29,37,75]. For instance, in a study examining Arabidopsis
thaliana from populations along an aridity gradient in Northeastern
Spain, populations that bolt earlier also have lower transpiration
rates and higher WUE [29]. Notably, this result was opposite of
the well-documented negative genetic correlation in A. thaliana
described above (i.e. [15]). This discrepancy could be due to timing of when gas exchange rates were measured, the environmental
context that the measurements were taken under or, in this specific
example, a lack of the FRI allele from all populations sampled. A similar negative correlation between flowering time and WUE (␦13 C)
was found for Mimulus guttatus populations distributed across a
series of aridity gradients (Fig. 2; [16]). This study also examined several traits (succulence, stomatal density, trichome number,
and specific leaf area) often associated with WUE, and found little evidence for genetic correlations between traits associated
with drought escape and avoidance within the most arid populations surveyed. A caveat to this study is that the common garden
was conducted under well-watered conditions and not under
water-limiting conditions or in a reciprocal transplant design.
Other studies in the M. guttatus conducted under both wet and
dry conditions demonstrate that the correlation between WUE and
flowering time switches direction depending on environment [58].
An additional explanation for these results is that another unmeasured tradeoff axis may exist. For instance, plants that are able
to escape or avoid drought may invest very little into vegetative
growth or drought tolerance.
The combined results of these studies suggest that the adaptation to drought is not ubiquitously constrained to alternative
strategies, and suggest that we have a limited understanding of
the physiological constraints involved in evolving drought resistance. Notably, few studies examine genetic correlations between
strategies within individual populations, where these constraints
may actually impact the evolutionary trajectory of populations
under drought stress. The role of genetic constraints in adaptation
to drought stress require further study, particularly in identifying
how often QTL underlying variation for flowering time and WUE
colocalize, how much of this variation occurs within populations,
and whether these correlations result in constraint to evolutionary responses. Future work should ideally utilize populations that
both undergo frequent drought stress and where substantial variation in flowering time and WUE exist. It is also clear that future
δ13C(%)
Fig. 2. Scatterplots describing the relationship between carbon isotope ratio (␦13 C)
and flowering time as group means for 39 accessions of Arabidopsis thaliana (black
circles) and line means for 41 lines from 11 populations of Mimulus guttatus (blue
triangles). Note that the x-axis is reversed so that higher values reflect greater wateruse efficiency. The negative genetic correlation between ␦13 C and flowering time for
A. thaliana suggests that both increased drought escape and increased avoidance are
unable to coordinately evolve, whereas the positive genetic correlation in M. guttatus
suggests that this same constraint does not exist. A. thaliana data taken from McKay
et al. [15] and used with permission of J. McKay; M. guttatus data taken from Kooyers
et al. [16].
studies must test for genetic correlations in multiple environments
as WUE is subject to gene by environment interactions.
4. A path toward understanding drought resistance
adaptations in natural populations
Our understanding of the genetic mechanisms and the fitness
tradeoffs associated with drought resistance adaptation has made
impressive strides during the last decade. Notably, QTLs that identify the genetic basis of variation in drought escape and avoidance
strategies have been found in many species (e.g. [21,22,41,37])
and have provided insight into the significant roles that genetic
constraint and gene by environment interactions play in evolving drought resistance. Further, greenhouse and field studies have
begun to elucidate the fitness ramifications of variation in drought
escape and avoidance mechanisms. These discoveries have been
made primarily utilizing natural populations, and suggest that wild
populations offer a diverse resource for identifying novel mechanisms of drought resistance for both ecologists and agronomists.
These studies have also highlighted areas where further research is needed for both evolutionary biologists and
agronomists. It is clear that enhanced drought escape and avoidance is triggered via environmental cues. However, we currently
lack a detailed understanding of how cues are integrated into
physiological responses, and we have not identified genes or
epigenetic variation responsible for variation in drought escape
or avoidance responses. While these are concerns that plague
genetic engineers, breeders should also consider the ramifications
of environment-dependent effects. An enhanced drought escape
or avoidance response may come at an unknown fitness or yield
cost in other environments. While increased drought resistance
could increase yield in during a drought year, it could decrease
yield in a more typical year. Although this concern is not novel in
traditional, trait-based, or molecular-assisted breeding programs,
N.J. Kooyers / Plant Science 234 (2015) 155–162
explicitly assessing these costs across a range of environments
is clearly necessary given the gene by environment interactions
associated with these traits.
Future progress is also needed in determining how seasonal
context and intensity of drought influences evolution of drought
strategies and fitness of plants in natural populations. While Fig. 1
provides ecological predictions describing the drought resistance
strategy that should evolve, these predictions are largely untested
and need to be addressed through experimental manipulation
in field conditions. Much of this review has focused on terminal droughts that end the growing season as these droughts are
often associated with strong selection for drought escape or avoidance. Less research has been devoted to transient or intermittent
drought events, and understanding how plants respond and adapt
in response would provide an interesting contrast. Given that
intermittent drought events take place within a single generation, plastic responses limiting plant growth and increasing WUE
should be highly beneficial. As greater fluctuations in precipitation
become normal, understanding which drought resistance strategies are most efficient will obtain greater importance. This includes
relatively understudied drought avoidance phenotypes such as
enhanced root:shoot ratios and buffering molecules. If these phenotypes are responsible for large increases in fitness during droughts
in natural populations, perhaps these hard to measure phenotypes
would be worth pursuing for breeders and engineers.
A continuing priority is determining the importance of adaptive constraints in the evolution of drought resistance. Natural
populations represent excellent systems to study whether genetic
constraints between drought resistance syndromes exist and when
they are adaptive. In natural populations different levels of genetic
correlation exist in different populations, and nature provides an
arena to study when these combinations are adaptive. Discovery
of these constraints will provide insights into the indirect costs of
selecting for certain traits such as flowering or heading earliness,
and could identify new directions for breeding drought-resistant
crops that also have high yield. It is naïve to suggest that an
ideal crop plant should employ both drought escape and avoidance strategies. An ideal variety allocates the maximum amount of
resources to produce the highest yield in optimal conditions, and is
capable of switching to a drought strategy during incipient drought
conditions. The optimal drought strategy depends on the specific
drought conditions of a region. Thus, focus should be directed to
synthesizing or finding varieties that are able to respond to incipient drought conditions without sacrificing yield during optimal
growing conditions. These conclusions indicate that understanding
the benefits, costs, and basis of gene by environment interactions is
critical for developing the next generation of crops and determining
how populations will respond to unpredictable environments.
Acknowledgements
I thank University of Virginia and B. Blackman for generous financial and intellectual support while writing this article
as well as the Blackman Lab group, Jack Colicchio, Christopher
Muir, Jonathan Gressel and seven anonymous reviewers for providing helpful criticism and feedback on earlier versions of this
manuscript.
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