Download 5.Temperature stress and plant sexual reproduction

Review
Global warming and sexual plant
reproduction
Afif Hedhly1,2, José I. Hormaza2 and Marı́a Herrero1
1
2
Departamento de Pomologı́a, Estación Experimental de Aula Dei, CSIC, Zaragoza, 50059, Spain
Estación Experimental la Mayora, CSIC, Málaga, 29760, Spain
The sexual reproductive phase in plants might be
particularly vulnerable to the effects of global warming.
The direct effect of temperature changes on the reproductive process has been documented previously, and
recent data from other physiological processes that are
affected by rising temperatures seem to reinforce the
susceptibility of the reproductive process to a changing
climate. But the reproductive phase also provides the
plant with an opportunity to adapt to environmental
changes. Understanding phenotypic plasticity and
gametophyte selection for prevailing temperatures,
along with possible epigenetic changes during this process, could provide new insights into plant evolution
under a global-warming scenario.
Consequences of global climate change
An increasing body of evidence indicates that global climate change is taking place and that it will have important
effects on biological processes over the next decades. The
expected climate changes include, among other factors, an
increase in average temperatures, an increase in atmospheric CO2 concentrations and an alteration of rainfall
regimes [1]. Although the reasons behind global warming
are still controversial, its adverse consequences are clear
and of increasing concern worldwide. Observed changes in
phenotypic traits of different plant and animal species
indicate that natural populations are responding to this
change [2]. Indeed, global warming has been shown to
affect species ecology, ranging from effects on geographical
distribution, phenology or species interaction to extinction
risks (reviewed in Ref. [3]). In agricultural systems, the
fertilizing effect of increasing CO2 concentration and the
consequent increase in yield dominated early conclusions
[4]; however, the lower than previously thought crop
response to CO2 [5] and its interaction with other factors,
such as rising temperatures, is changing the view of climate change effects in crop plants and in modelling strategies [6]. Nonetheless, current estimates indicate that the
moderate increase in temperature forecasted for the first
half of this century might result in an increase in average
yields in temperate and high latitude regions, whereas
yield would be reduced in semi-arid and tropical regions
[7]. The additional warming forecasted for the second half
of the century would have a negative effect on yield in all
regions, although the forecasts are variable depending on
the crop and the geographical area. Reports are already
showing a negative effect of climate change on yield in
Corresponding author: Hedhly, A. ([email protected]).
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some crop species [8,9]. Respiration and photosynthesis
[10] have been proposed as the main physiological processes affected by temperature and CO2 increases. However, the acclimation registered in such processes [11,12],
the spatial–temporal heterogeneity of the climate change
and the threshold responses of some plant developmental
stages suggest that additional processes are also affected
[6]. Little is known, however, on the actual effect that
changes in temperature might have on the different plant
developmental stages. Here, we discuss the effect of
temperature change on the reproductive phase from an
ecological, agricultural and physiological perspective, and
we evaluate the potential implications of the forecasted
global warming on this phase.
Effects of increasing temperatures on the sexual plant
reproductive phase
We believe that three main points support the idea that the
reproductive phase is a good candidate to be affected by
climate change: (i) the events of irregular and reduced
cropping; (ii) the forecasted change in temperature mainly
in the spring, during the flowering season of many plant
species; and (iii) the available information on the direct
effect of temperature stress on the reproductive phase.
(i) The processes that take place during the reproductive
phase are determinant for final production in crop
species cultivated by their seeds and/or fruits. The
effect of high temperatures on the reproductive phase
seems to be more pronounced in plant species that are
at the limit of their cultivation range and, consequently, highly sensitive to short episodes of
extreme temperatures [13]. A characteristic of global
climatic change is the increase in the frequency of
extreme temperatures, which are likely to reduce crop
fertility and yield [6,7,14]. Possible yield increases
due to CO2 enrichment might not offset the negative
effects of high temperatures on reproductive processes, particularly if high temperatures coincide
with sensitive stages of reproductive development
[6,15]. Recent examples of the effect of global
warming on yield include a 17% reduction in corn
(Zea mays) and soybean (Glycine max [L.] Merr.) grain
yields in the US Midwest [8] and a 15% reduction in
rice (Oryza sativa) grain yield in the Philippines [9]
for each 1 8C increase in temperature during the
growing season. In fact, a recent modelling of extreme
high temperatures forecasts a reduction of premium
grapevine production in the US by 81% at the end of
1360-1385/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2008.11.001 Available online 4 December 2008
Review
the 21st century [16]. The mechanisms underlying
these effects are still unknown but, as outlined above,
some evidence points to the reproductive phase as a
potentially sensitive stage. High temperatures are
likely to shorten the growing cycle of many crop
species and, during some developmental stages, such
as the reproductive phase, most crops are only able to
tolerate narrow temperature changes, which, if
exceeded, can reduce seed set and thus yield [14].
(ii) In some regions, mainly at higher latitudes, temperatures during the spring – when blooming of many
crop plants takes place – are changing rapidly. In fact,
the pronounced increase in temperature experienced
so far has been mainly registered in late-winter and
early-spring [17–19]. Indeed, for biological and
agricultural systems, the timing and frequency of
extreme temperature events could be more important
than the increase in mean temperatures [16]. Likewise, the most recent best estimates of global average
surface air warming range from 1.8 8C for the lowincrease scenario (with a range of predictions from
1.1 8C to 2.8 8C) to 4.0 8C for the high-increase
scenario (with a range of predictions from 2.4 8C to
6.4 8C) at the end of the 21st century, and warming is
expected to be greatest over land and at higher
northern latitudes [1]. Besides the well-documented
effect of winter–springtime temperature on the
advancement of flowering time [2,3], subsequent
reproductive processes, which are known to be
sensitive to temperature stress, will necessarily be
affected in these changing conditions. Irregular
production in warm springs can indeed be explained
by an effect of temperature on the reproductive phase
(e.g. [20]). Thus, based on the narrow threshold
responses during flowering time and the projected
increase in extreme events, more data on spatiotemporal temperature climatic variation and their
overlap with sensitive developmental stages such as
flowering is needed for better modelling of future
effects of global warming [6].
(iii) Before the current worldwide concern over global
warming, information had built up showing that
temperature stress affects the reproductive process.
The response varies depending on the plant species,
but both male and female functions are affected, along
with the reproductive process itself. Due to the role
that temperature has in crop adaptation and expansion to new latitudes, studies have mainly concentrated on cultivated and economically important
annual crop species, in which the reproductive phase
seems to be recurrently affected by temperature and
is considered among the most sensitive stages of the
plant life cycle [21]. In the different experiments
performed, the stress was generally applied simultaneously to several different developmental stages,
and this seemed to affect the final product. However,
this approach misses developmental-stage-specific
responses, which seem to be uncoupled and not
necessary additive [6,22]. Thus, a better estimation of
the effect of temperature could be obtained by
studying the sensitive stages independently and then
Trends in Plant Science
Vol.14 No.1
integrating those effects into the whole plant
response. In this sense, evaluation of temperature
stress on the sexual reproductive process could be
separated into three consecutive and interdependent
developmental stages (Figure 1): gamete development, the progamic phase from pollination to
fertilization and postzygotic early embryo development. In the next sections we will discuss the
available data that deal with the effect of temperature
variation on sexual plant reproduction, from gamete
development to the beginning of the next plant
generation.
Gamete development
High temperature stress during gamete development has
been shown to affect plant reproduction with immediate
and long-term effects. Some immediate effects on the
female gametes mediated through flower production and
their viability have been recorded [23,24]. However, probably because it is easier to handle, most of the work has
concentrated on the male function. Thus, the quantity and
morphology of pollen, anther dehiscence and pollen wall
architecture, as well as the chemical composition and
metabolism of pollen [15,24–26], have been shown to be
affected by high temperatures. All these effects could alter
male fitness by reducing the available amount of pollen
and could also – if the pollen limitation is severe –indirectly
limit female fitness by reducing the number of seeds sired.
However, given the great amounts of pollen produced in
most plant species, small variations in temperature,
although inducing an effect, are not expected to produce
very dramatic effects in terms of reproductive output.
More subtle, but perhaps more important, is the effect
that the temperature during pollen development seems to
have on pollen performance. Although the range of
temperature tolerance threshold is highly variable between species, mild increases in temperature negatively
affect characteristics such as pollen viability [26,27], pollen
germinative ability [24,28,29], pollen tube growth rate [29]
and seed and fruit set [25,27]. Several studies across a
range of unrelated genera on the effect of diverse biotic and
abiotic factors during pollen development indicate that
selection among developing microgametophytes has an
effect beyond the gametophytic generation by altering
the composition and performance of the next sporophytic
generation [30–32], and temperature stress is one of the
factors governing selection [29].
Thus, it seems that temperature variation during pollen
development can alter pollen performance and that this
effect might lead to changes in the genetic frequencies of
the next sporophytic generation. But the extent to which
this might be a general phenomenon remains to be
explored.
From pollination to fertilization
Considering uniform and optimum conditions during
gamete development, temperature variation during the
postpollination–prezygotic stage affects both male and
female functions, as well as the interaction between the
two. The two main effects on the postpollination–prezygo31
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Trends in Plant Science Vol.14 No.1
Figure 1. Temperature stress experienced during gamete development (blue), the postpollination–prezygotic stage (red) and the postzygotic stage (green) alters these
stages (large coloured arrows) and also has long-lasting consequences on subsequent stages (small coloured arrows). Some processes warrant further investigation, such
as how temperature stress at a given level might affect stress response at a different level (red question marks) or the nature of the reported transmitted effects for each
stress level (green question marks). Gametophytic and sporophytic stages are shown with yellow and blue background colours, respectively.
tic stage are (i) the acceleration or retardation of the whole
process and (ii) the potential influence of the prevailing
temperatures on pollen selection.
Male–female synchrony for successful mating
On the male side, temperature affects the quantity of
pollen that succeeds in germinating [33,34], as well as
the rate of pollen tube growth along the reproductive tract.
John T. Buchholz and Albert F. Blakeslee [35] were the
first to show an effect of high temperature on pollen tube
growth rate in Datura stramonium L. Since then, data
from both herbaceous [34,36] and woody plant species [37–
39] suggest that an acceleration of pollen tube growth
under high temperatures and a slowing-down under low
temperatures seem to be a general phenomenon.
Although relatively less attention has been paid to the
female counterpart, an effect of temperature on the female
side has also been put forward. High temperatures accelerate overall female development, whereas low temperatures slow it down. Thus, high temperatures accelerate
stigma and ovule development, reducing the duration for
which they are receptive to pollen and pollen tubes,
whereas low temperatures prolong both stigmatic receptivity and ovule longevity [40,41], extending the receptivity
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period. Consequently, temperature stress seems to have a
complementary effect on the male and female counterparts, accelerating or slowing down the reproductive process. However, this idea is true only within a given range of
temperature, that to which a particular genotype is
adapted, and exceeding this range might be detrimental
to the reproductive process due to the shortening of the
female receptive time. This might have severe consequences for the reproductive output, inducing low seed
and/or fruit set [15,20,27,28]. Male–female synchrony
seems to be a prerequisite for successful mating in plants
[42], and fertilization occurs when the two gametes are at
the same phase of the cell cycle [43]. Also a reduction in
female receptivity might jeopardize pollination, especially
under suboptimal pollinator activity, which can also be
affected by changing environmental conditions. Pollination
failure in insect-pollinated crops is of rising worldwide
concern because weather change in spring can cause the
uncoupling of insect cycles and flowering phenology [44].
Pollen competition and selection
Temperature might also affect pollen selection during the
progamic phase. The existence of pollen selection has
caused some controversy (Box 1). During the reproductive
Review
Box 1. Hallmarks in pollen selection theory
At the beginning of the 20th century, John T. Buchholz [70] was
among the first to address what he called developmental selection,
the potential evolutionary consequences, for both gymnosperms
and angiosperms, of selection among male gametophytes represented by pollen tubes. J.B.S. Haldane [71] noted the ‘serious
overcrowding’ of pollen grains in the stigma, which makes pollen
competition likely. In 1979, David L. Mulcahy [45] synthesized these
findings and integrated them in a hypothesis to explain the rise of
angiosperms. He proposed that insect pollination and closed
carpels, which are characteristics of primitive angiosperms, might
intensify gametophytic competition and selection. In this way,
flowering plants might take advantage of sexual recombinants while
eliminating poorly functioning haploid individuals. Thanks to the
correlation between pollen tube growth rate and performance of the
next generation, he stated that the effect of gametophytic selection
is not limited to the haploid generation and could influence the next
sporophytic generation. This is further supported by the overlap in
gene expression between the gametophytic and sporophytic
phases.
Since then the gametophytic competition and selection hypothesis has faced some questioning. First, owing to technical limitations, the finding of overlap in gene expression was initially based
on data from few genes. However, with the help of high-throughput
technology, we now know that the overlap of expression patterns is
extensive [72]. Second, for gametophytic competition to occur,
there must be more pollen grains in the stigma than ovules to be
fertilized. Because the first results were obtained in cultivated
plants, a question arose about the occurrence and magnitude of
pollen surplus in natural systems. However, pollen surplus was also
registered in natural populations [73]. Third, the genetic variation of
pollen tube growth rate versus plastic response, reflecting environmental and nutritional conditions during development, provided
another challenge. The key to gametophytic competition and
selection – and its potential evolutionary implication – is the
existence of genetic additive variation. This subject has been
addressed [74], but variation in pollen tube growth could also be
explained as the after-effects of gametophyte developmental
conditions [32]. Fourth, because pollen performance is related to
fitness and fitness is exposed to natural selection, we would expect
genes controlling pollen performance to have been fixed during the
evolutionary process. However, mechanisms such as male–female
and genotype–environment interactions result in the modulation of
pollen performance depending on the female genotype and the
environmental factors and, consequently, variability for pollen
performance can be maintained [30].
However, an additional question still needs to be addressed. So
far, there is no direct evidence at the cellular and molecular levels of
male–male competition or female choice, and works are generally
based on indirect evidence (e.g. [75]). The only advance in this field
comes from interspecific crosses, in which pollen tube paternity
analysis revealed that conspecific fertilization precedence was
mediated by favourable or unfavourable male–female interactions
[76]; results are lacking at the intraspecific level. Further work is
needed not only to give further support to the theory of pollen
selection but also to mark the boundaries between genetically based
variation in pollen competition (with respect to the plastic behaviour
of pollen tubes in response to prezygotic differential provision of
pollen grains) and selective postzygotic embryo abortion.
Currently, non-random fertilization is widely accepted in plants,
whereas both male competition and female choice are becoming
unifying concepts of mate choice in plants and animals. Recent
advances in molecular biology are revealing additional nonmendelian segregations during sexual plant reproduction, and
these discoveries could answer some old questions that could not
be addressed with traditional genetic approaches.
process, an intense pollen competition that seems to be the
substrate for gametophytic selection takes place in the
pistil [45]. The first evidence for differential selection at
the gametophytic level in response to low temperature
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stress was demonstrated in cultivated and wild tomato
(Lycopersicon esculentum Mill. and Lycopersicon hirsutum
Humb. and Bonpl.) [46]. After mixed pollinations using
pollen from genotypes with a differential temperature
adaptation, a different paternity contribution occurred
depending on the prevailing temperatures during the
reproductive process. Later work demonstrated that cold
tolerance was determined by genes expressed in the pollen
genome [47] and that selection at the gametophytic level
correlates to root elongation capacity under the same
conditions [48]. Similar results were obtained in several
unrelated plant species and confirmed a genotype–
temperature interaction for pollen performance and for
siring success [38,49]. Recent studies in sweet cherry
(Prunus avium L.), a woody perennial species that promotes intense pollen competition, show that temperature
affects pollen tube dynamics and, as a consequence, influences the proportion of pollen tubes that succeed in reaching the ovary [33]. Similarly, a clear genotype–temperature
interaction that reflects climatic adaptation of the pollen
donor has been observed [39]. More work needs to be done
in different plant species, but these results suggest a
natural selection of the best-adapted pollen tubes to the
prevailing temperature during the reproductive phase.
Future findings will contribute to the understanding of
rapid adaptation to temperature and the rapid emergence
of landraces that are well-adapted to new latitudes.
Postzygotic stage
Target oriented experiments analysing the effect of
temperature stress at the postzygotic level are scarce.
However, the study of the relative importance of preversus postzygotic temperature variation (15 8C nights/
20 8C days and 20 8C nights/26 8C days at both stages)
on offspring fitness and performance in field experiments
in Plantago lanceolata L. [50] showed a major effect of
postzygotic variation on offspring fitness. Higher temperature increased offspring fitness by 50%; furthermore, genotype-specific responses for seed germination, flowering
time and spikelet production were observed. Likewise, in
Norway spruce (Picea abies [L.] Karst.), cold and warm
environments experienced during zygotic embryogenesis
and seed maturation advanced and delayed, respectively,
several progeny adaptive traits, such as bud set, cold
acclimation in the autumn and dehardening and flushing
in spring [51], and the changes last for at least two growing
seasons [52]. Similar postfertilization effects have been
registered in Arabidopsis thaliana, under both high and
low temperatures [53]. Interestingly, the registered progeny hardening in P. abies was suggested to reflect
temperature-induced epigenetic changes during embryo
development and seed maturation.
Taking all these effects together, it seems that the
sexual phase in flowering plants is an active developmental process subjected to different selective forces. Heat
stress affects male and female gametogenesis, pollen–pistil
interaction and embryo development. Moreover, the three
processes interact and have a bearing on each other.
Finally, in addition to observed effects on reproductive
output, the genetic composition, phenology of adaptive
traits and fitness of the next generation might also be
33
Review
influenced. From this perspective, we will discuss in the
next sections both the ecological and evolutionary implications of global warming.
Immediate implications
The immediate effects of global warming are already
observable, both in natural populations and in agricultural
systems. These effects mainly concern: (i) the early onset of
sexual reproductive development; (ii) higher or lower
reproductive output, depending on the regions and species
under study; and (iii) the expansion of crop plants and
shifts in geographic distribution of natural populations
towards higher latitudes.
Early flowering in response to higher temperatures [2]
is actually an advancement of the whole reproductive
process that could potentially alter plant–pollinator interaction and subsequent reproductive stages; the effect of
global change on plant phenology has been extensively
reviewed elsewhere (e.g. Ref. [54]). The second immediate
effect is the reproductive output. Although the dominant
picture of the effect of global warming is an extension of the
growing season and an increase in yield in some species
and regions [1], the forecasted increase in the frequency of
exposure to extreme temperatures and to short episodes of
heat waves, changes in frost frequency and heat-induced
shortening of developmental phases [6,14,55] are likely to
cause irregular cropping. Current data indicate that
temperature stress experienced during gamete development, the progamic phase and embryo development reduce
final seed and fruit set. Different tools are available for
investigating the cause further. First, determining the
weak steps of the process provides a frame for disentangling the causes of erratic crops. These studies have the
advantage that they do not require high technology
because simple methods are available for evaluating both
stigma and ovule receptivity, as well as pollen germination
and pollen tube behaviour and their influence on the
subsequent fruit set. Second, enough genetic variability
is still present within many crops to enable the selection of
new cultivars for new situations. Interestingly, this genetic
variability has been previously selected and conserved
owing to the adaptation of the different crops to different
habitats and latitudes.
A third expected immediate effect is plant migration.
This can already be observed in natural populations
(reviewed in Ref. [3]) and is expected to happen in agricultural systems (e.g. [16]). Geographical displacement of
some crops might represent an advantage for higher latitude regions, opening the possibility for new crops not
previously grown in those locations. However, this might
represent a problem with socio-economical implications at
lower latitudes, where most developing and undeveloped
countries are located and where local populations can be
highly dependant on specific crops, the disappearance of
which could cause food shortages. Again, the search for
new genotypes adapted to the changing environmental
conditions might be an alternative.
Long-term evolutionary and ecological implications
The evolutionary implications of climate change in plants
have received less attention than in animals. The best way
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Trends in Plant Science Vol.14 No.1
to forecast the potential evolutionary implications of climate change is to learn from past experience, such as the
different climate changes over the Quaternary period (the
last 2.6 million years of geological time). During the Quaternary, sparse speciation events have been registered in
plants, unlike in mammals [56]. However, the finding that
abundant genetic differentiation has taken place during
the Quaternary within different populations of the same
plant species gives support for rapid evolutionary adaptation processes [57]. Clinal variation in physiological,
phenological and fitness traits in relation to latitudinal
or altitudinal climate gradients is the best example of such
differentiation [58–60]. Furthermore, common garden
experiments show that most tree and herbaceous plant
species comprise a series of populations adapted to their
respective local environments [57]. Thus, the palaeoecological idea that species, if climate change is outside their
tolerance limits, will have to shift their geographic distribution or, alternatively, face extinction has been reviewed,
and it has been argued that plant migration actually occurs
via evolutionary adaptive processes [57,60]. However, the
mechanisms underlying these adaptive processes are not
yet well understood. Plant reproduction, together with
death, represent two basic processes of population
dynamics [61]. Thus, if climate change could modulate
sexual plant reproduction, the consequences could be far
reaching. Global change is already affecting animal sexual
reproduction, leading to potential ecological and evolutionary implications [62]. In plants, genetic variation in fitness
has been reported to be elicited by spatial climate variation. Thus, it is plausible that climate change might cause
adaptive evolution of fitness-related traits [60]. Consequently, if climate change can modulate sexual plant
reproduction, which strongly contributes to fitness, it is
tempting to speculate that the sexual reproductive phase
will have an important role in these adaptive processes.
In the light of new progress in plant response to
temperature stress during the sexual phase, two important
players, gametophytic selection and phenotypic plasticity,
seem to adjust plant behaviour against stress across generations, influencing the pace and direction of evolutionary
processes. Both processes have been proposed as underlying mechanisms of variation in pollen performance and
siring success [30–32]. Gametophytic selection under
temperature stress can affect the rate of response to selection. Evolution of a life-history pattern is, indeed, not only
dependent on genetic variation, which has been demonstrated for pollen performance and siring success (Box 1),
but also on the environment in which selection takes place
[50]. As detailed above, genotype–temperature interaction
has been reported for pollen tube growth and for siring
success. Furthermore, the finding that this selection could
reflect the origin and adaptation of the pollen-producing
sporophyte [39,46] is undoubtedly important for the
dynamics of population genetic structure [63]. Phenotypic
plasticity, defined as the ability of a genotype to adjust its
developmental programs in response to environmental
fluctuation [64], is important in terms of withstanding a
changing environment and species evolutionary dynamics.
It can accelerate or slow down the impact of environmental
factors on population dynamics, might underlie ecological
Review
success in new habitats, can influence the direction of the
response to selection [64] and has been interpreted also as
a means of maintenance of genetic variability in pollen
performance [32].
Perspectives
The susceptibility of the reproductive phase to environmental stress also hides the strength of providing an
opportunity for change by means of gametophytic selection
and phenotypic plasticity. The possibility that gametophytic selection might favour the best-adapted genotypes to
prevailing temperatures is an attractive hypothesis that
warrants further investigation, and it could explain plants’
rapid adaptation to different temperatures while maintaining variability. Although the literature on pollen competition and selection is abundant (Box 1), the molecular
mechanisms underpinning this selection are still to be
analysed. Phenotypic plasticity is, however, experiencing
a renewed interest and, although the precise mechanisms
behind phenotypic plasticity are still to be deciphered,
epigenetic mechanisms have been reported to be involved
[65], suggesting that the epigenetic machinery might be
superimposed on DNA sequence variation-based transgeneration effects. Incipient results show parent-of-origin upand downregulation of some progeny genes in P. abies [51]
and A. thaliana [53]. These memory effects, potentially
epigenetic in nature [51], are a consequence of temperature
stress during embryo development. When they are generated in this way (i.e. in somatic cells), epigenetic marks are
stable through mitosis and in some cases, such as flowering
time in Arabidopsis [66], they are reset in each generation.
However, to have evolutionary implications, these effects
have to be transmitted to the subsequent generations
through the male and/or female gametophytes. Interestingly, recent findings reveal that epigenetic marks can be
often heritable over generations through DNA methylation
[67,68]. Thus, although epigenetic modulation of embryo
development could be important for adjusting the phenotype of the progeny, the prezygotic stages in which gamete
development takes place in plants can be the key step for
transgenerational effects. Furthermore, unlike in animals,
in plants male and female gametophytes are exposed
structures, which potentially makes them especially
susceptible to environmental stress [69]. Thus, understanding epigenetic dynamics in plants, from the commitment of a sporophytic cell to be a germline to embryo
development, will undoubtedly help to clarify potential
temperature-stress-sensitive stages and, ultimately, heritable stress-induced epigenetic effects. Work aimed at
elucidating the extent of gametophytic selection and epigenetic machinery in modulating plant constitution between generations and their interaction with
environmental stresses will provide a better understanding and projection of ecological evolutionary dynamics
under the current scenario of increasing temperatures.
Acknowledgements
Financial support for this work was provided by the Spanish Ministry of
Education and Science (project grants AGL2006-13529-C02-01 and
AGL2007-60130/AGR) and by the Diputación General de Aragón
through the ‘Grupo Consolidado de la Comunidad Autónoma de Aragón,
A-43’. A.H. was supported by ‘Juan de la Cierva’ and JAE-doc grants.
Trends in Plant Science
Vol.14 No.1
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