Journal of APPLIED BIOMEDICINE
ISSN 1214-0287 (on-line)
ISSN 1214-021X (printed)
Volume 8 (2010), No 4, p 189-198
DOI 10.2478/v10136-009-0026-4
Temperature-perception, molecules and mechanisms
Rafael Catala, Julio Salinas
Address: Julio Salinas, Department of Environmental Biology, Centro de Investigaciones Biologicas (CIB - CSIC)
Ramiro de Maeztu 9, 28040 Madrid, Spain
salinas@cib.csic.es
Received 5th March 2010.
Revised 11th May 2010.
Published online 24th May 2010.
Full text article (pdf)
Abstract in xml format
Summary
Key words
Introduction
Physiological changes induced by low temperature
The process of cold acclimation
Adaptive responses to low temperature in other organisms
Conclusions and perspectives
Acknowledgements
References
SUMMARY
The strategies used by living organisms to survive under low and freezing temperatures reveal the extraordinary adaptability of life on Earth. Understanding the molecular mechanisms underlying cold adaptation and freezing survival will provide new insights into the existing relationships between living organisms and their environment, and the possibility of developing multiple biotechnological applications. In the case of plants, the use of classical genetic and new "omics" approaches is allowing to the identification of new elements involved in regulating the cold acclimation response. The challenge ahead is to determine temperature-perception molecules and mechanisms, to uncover new internodes of multiple responses, and to integrate the regulation not only at the transcriptome but also at proteome and metabolome levels. Attaining these goals will significantly contribute global understanding the adaptive strategies plants have evolved to cope with hostile environmental conditions, and to the development biotechnological strategies to improve crop tolerance to freezing and other important abiotic stresses.
KEY WORDS
Arabidopsis; low temperature response; cold acclimation; freezing tolerance; cold signalling
INTRODUCTION
Low and freezing temperatures severely conditioned
life of all organisms in many different ways, from the
reduction of biochemical reaction rates or changes in
membrane fluidity and protein conformation, to the
need for protection against freezing. Regarding
plants, freezing temperatures limit their development
and geographical distribution, and account for
important losses in crop production. In temperate
regions, many species have evolved a low
temperature response, known as cold acclimation,
whereby they can increase their freezing tolerance
after a period of exposure to low-nonfreezing
temperatures (Levitt 1980). Understanding the
molecular mechanisms governing this adaptive
response is important in learning how plants grow and
reproduce under hostile conditions, and should help
to develop biotechnological strategies to improve
crop tolerance to freezing. The process of cold
acclimation is quite complex and involves a high
number of physiological and biochemical changes,
most of them controlled by low temperatures through
changes in gene expression, which during cold
acclimation is mainly regulated at the transcriptional
level (Salinas 2002, Yamaguchi-Shinozaki and
Shinozaki 2006, Van Buskirk and Thomashow 2006),
although recent findings indicate that regulation at the
posttranscriptional, translational and posttranslational
levels may also be important (Mazzucotelli et al.
2006, Zhu et al. 2007, Catala and Salinas 2008). For
some years, our lab has been using the model plant
Arabidopsis and a collection of experimental
approaches to uncover signalling intermediates
involved in regulating plant responses to low
temperature. Some of them resulted in the mediation
of metabolic adjustments or changes in the
composition of plasma membrane induced by cold
conditions. Furthermore, by screening a cDNA library
from cold-acclimated seedlings of Arabidopsis with
a subtracted probe enriched in cold-induced
transcripts (Jarillo et al. 1994), we identified a series
of Rare Cold Inducible (RCI) genes that have been
shown to be implicated in cold signalling. The
functional characterization of these genes has
provided important insights into the molecular
mechanisms underlying plant responses to low
temperature, including cold acclimation. A number of
reviews covering plant responses to low temperature
and cold acclimation have been recently published
(Mazzucotelli et al. 2006, Van Buskirk and
Thomashow 2006, Yamaguchi-Shinozaki and
Shinozaki 2006, Zhu et al. 2007, Catalá and Salinas
2008, Penfield 2008). In this paper, we will describe
and discuss some of our contributions to the
understanding of how plants respond when facing low
temperature conditions, and how the process of cold
acclimation is regulated.
PHYSIOLOGICAL CHANGES INDUCED BY LOW TEMPERATURE
One of the primary effects of low temperature in cells
is the alteration of membrane fluidity properties and
fatty acid composition due to an increase in the
content of polyunsaturated lipids (Murata and Los
1997, Aguilar et al. 1998, Suzuki et al. 2001,
Hayward et al. 2007). In plants, this increase is
essential for low-temperature survival and directly
affects membrane-bound metabolic processes such as
respiration and photosynthesis (Cossins 1994). A shift
toward an anaerobic metabolism has been reported in
different species (i.e., maize and rice) when exposed
to low temperature, which provokes a rapid increase
of alcohol dehydrogenase gene (ADH) expression and
activity (Christie et al. 1991). In Arabidopsis, we
have demonstrated that ADH expression is also
induced by cold stress, and that this induction is
mediated by abscisic acid (ABA) (Jarillo et al. 1993).
Nevertheless, in spite of the induction, our results
revealed that ADH is not essential for the correct
development of cold acclimation response (Jarillo et
al. 1993).
Photoinhibition, a reduction of photosynthetic
activity that may be caused by a combination of light
and cold, has been directly correlated with low
temperature sensitivity due to an increase in
photoxidative stress (Harvaux and Kloppstech 2001).
Anthocyanins, which function in photoprotection
acting as light-screening pigments, accumulate in
leaves and stems in response to low temperature and
changes in light intensity (Mancinelli 1984, Christie
et al. 1994). The synthesis of these pigments is
controlled, in part, by the key enzymes phenyl
ammonia lyase (PAL) and chalcone synthase (CHS).
In our laboratory, Leyva et al. (1995) reported that the
expression of Arabidopsis PAL and CHS genes is
induced in response to cold in a light-dependent
manner, and that this induction is regulated at the
transcriptional level. As in the case of ADH, genetic
analysis has revealed that CHS is not essential for the
increase in freezing tolerance originated by cold
acclimation (Leyva et al. 1995). Taken together, all
these results suggest that the function of ADH, PAL
and CHS would be related more to the response to
chilling stress than to cold acclimation. Low
temperature also affects the protein composition of
photosystems (Gray et al. 1997, Krol et al. 1999). We
could show that the expression of CAB1, a gene
encoding a light-harvesting chlorophyll a/b binding
protein, is induced when Arabidopsis plants are
exposed to 4 °C (Capel et al. 1998). In contrast to
PAL and CHS, the induction of CAB1 in response to
cold is light-independent (Capel et al. 1998),
indicating that it is regulated through a different
pathway. Interestingly, it has been reported that
Arabidopsis light-harvesting complex (LHC) proteins,
including CAB1, play an important role in protecting
photosystem I from photoinhibition (Alboresi et al.
2009).
In addition of modifying the content of
polyunsaturated lipids in the plasma membrane, low
temperature also induces changes in the composition
of plasma membrane proteins. Kawamura and
Uemura (2003) reported the isolation of 38 proteins
from Arabidopsis plasma membrane whose levels
increase or decrease in response to cold. Among
them, they identified proteins involved in CO2
fixation, membrane repair, protection of membrane to
osmotic stress, or proteolysis (Kawamura and Uemura
2003). One of these proteins, with function in
membrane repairing, SYT1, has been demonstrated to
play a role in freezing tolerance and cold acclimation
(Schapire et al. 2008, Yamazaki et al. 2008).
Recently, we described a family of eight Arabidopsis
small hydrophobic proteins (AtRCI2A-H) that are
also located in the plasma membrane (Medina et al.
2007). The expression of AtRCI2 genes is
differentially regulated in Arabidopsis organs and in
response to low temperature (Capel et al. 1997,
Medina et al. 2001, 2007). AtRCI2A-C and AtRCI2H
are able to complement for the loss of the yeast
AtRCI2A-homologue PMP3 (Medina et al. 2007),
which has been involved in the maintenance of
plasma membrane potential, suggesting a similar role
for AtRCI2 during cold stress (Medina et al. 2007).
It has been well known for several years that
exposition to low temperatures also provokes changes
in the composition of cell wall components in several
plant species. Wei et al. (2006) reported that
expression of C3H, a Rhododendron gene encoding
a protein implicated in lignin accumulation in the cell
wall, is cold induced, suggesting a possible role of
lignin in low temperature responses. On the same
way, we reported the identification of RCI3 gene of
Arabidopsis, that encodes an active cationic
peroxidase, a kind of protein that has been involved
in lignin and suberin depositions in the cell wall
(Llorente et al. 2002).
THE PROCESS OF COLD ACCLIMATION
As already mentioned, cold acclimation is an adaptive
response whereby some plants acquire an increase in
freezing tolerance upon a prior low-nonfreezing
temperature exposition (Levitt 1980). Plants are able
to acclimate to cold by extensively reprogramming
their transcriptome, proteome and metabolome. In
recent years, the efforts of several laboratories,
including our own, have began to elucidate the
regulatory networks that mediate cold acclimation. In
the next paragraphs, we intend to present the progress
in our understanding of how low temperature signals
are perceived and transduced leading to the activation
of this adaptive response.
Signal transduction in cold acclimation
The first step in any signalling pathway implies the
recognition of the signal by a receptor. It has been
proposed that changes in the fluidity of cell
membranes could act as a receptor of temperature
changes in plant cells (Orvar et al. 2000, Sangwan et
al. 2002). Nevertheless, experimental evidence
demonstrating that this is the case has not yet been
provided, and how plants perceive low temperatures
still remains to be elucidated. What seems to be clear
is that transient increases in cytosolic calcium
concentration ([Ca2+]cyt) are essential for plant
response to low temperature (Knight 2000). Increases
in [Ca2+]cyt mainly result from Ca2+ influx through
permeable channels in the plasma membrane and/or
Ca2+ discharge from internal stores (Piñeros and
Tester 1997). After Ca2+ influx, efflux systems to
internal stores and out of the cell restore [Ca2+]cyt to
unstimulated levels via Ca2+ pumps and Ca2+/H+
exchangers (Knight 2000). One of the RCI genes
identified in our lab, RCI4, turned out to be identical
to CAX1, an Arabidopsis gene encoding a H+/Ca2+
antiporter essential for correct regulation of [Ca2+]cyt
(Hirschi et al. 1996). RCI4/CAX1 expression is
induced by cold through an ABA-independent
pathway (Catala et al. 2003). Functional analysis
revealed that RCI4/CAX1 is involved in the increase
of freezing tolerance that is induced by cold
acclimation (Catala et al. 2003). In fact, rci4/cax1
mutants show enhanced capacity to cold acclimate,
which correlates with a higher induction of
CBF/DREB1 genes and their corresponding targets in
response to low temperature (see below) (Catalá et al.
2003). We proposed that RCI4/CAX1 would function
to restore [Ca2+]cyt to unstimulated levels after the
increase induced by low temperatures (Fig. 1). The
absence of RCI4/CAX1 activity would result in an
extended cold signal that would provoke a higher
induction of the CBFs/DREB1s and their target genes,
and, therefore, an increase in Arabidopsis freezing
tolerance. These results demonstrate that an accurate
[Ca2+]cyt regulation is essential for the correct
development of cold acclimation response, and that
RCI4/CAX1 is an essential partner of the regulatory
mechanisms controlling [Ca2+]cyt homeostasis in
Arabidopsis.
Generally, Ca2+ signals mediating regulatory
pathways are associated with reversible
phosphorylation events. Reversible phosphorylation
of pre-existing proteins has been demonstrated to be
essential for cold acclimation in alfalfa and
Arabidopsis (Tahtiharju et al. 1997, Monroy et al.
1998). RCI1A and RCI1B are two Rare Cold Inducible
genes of Arabidopsis identified in our laboratory that
encode two members of the 14-3-3 protein family
(Jarillo et al. 1994, Abarca et al. 1999). The 14-3-3
proteins function as dimmers to regulate the activity
of other previously phosphorylated proteins to which
they interact (Abarca et al. 1999, Roberts et al. 2002).
The kinetics of RCI1A and RCI1B expression in
response to low temperature correlates with the
increase of freezing tolerance induced by cold
acclimation, suggesting a role for these proteins in
this adaptive process (Jarillo et al. 1994). The 14-3-3
protein family of Arabidopsis includes 12 isoforms,
but only RCI1A and RCI1B are cold inducible (Jarillo
et al. 1994, Roberts et al. 2002). Preliminary data with
a null mutant for RCI1A indicate that the
corresponding protein acts as a negative regulator of
cold acclimation and is involved in regulating
cold-induced gene expression (Catala et al.
unpublished).
Fig. 1. Functional model of RCI4/CAX1 during cold acclimation. A. Exposition to low temperature induces a transient
increase in [Ca2+]cyt as a consequence of Ca2+ influx through permeable channels in the plasma membrane and discharge from internal stores. This increase, conveniently decoded and transduced by downstream effectors, enhances the expression of the CBF
genes and their targets, activating the cold acclimation response. B. When the cold signal vanishes, RCI4/CAX1 introduces
cytoplasmic Ca2+ into the vacuole, contributing, together with other Ca2+ transporters, to restore [Ca2+]cyt to unstimulated levels.
The restoration of [Ca2+]cyt levels restrains induction of CBFs.
Regulation of gene expression during cold acclimation
Global expression analyses have revealed that about
one thousand genes are regulated by low temperature
in Arabidopsis (Lee et al. 2005, Matsui et al. 2008,
Zeller et al. 2009). Among these genes, one third is
repressed, with only one gene encoding a
transcription factor, which indicates that gene
expression during cold acclimation is mainly
activated (Lee et al. 2005). In addition, many early
cold-induced genes encode transcription factors or
proteins involved in transcription. Thus, more than
one hundred genes have been annotated to function in
transcription, 95 of them coding for transcription
factors (Lee et al. 2005). These results indicate that
cold-induced gene expression is regulated through
different signal transduction pathways. To date, the
most important pathways that have been identified
and characterized are those mediated by ABA and the
CBF/DREB1 transcription factors, respectively.
ABA and cold-induced gene expression
It is well documented that ABA levels increase in
plants in response to different environmental adverse
conditions, including low temperatures, and that
exogenous treatment with ABA enhances freezing
tolerance (Chen and Gusta 1983, Lang et al. 1989).
Moreover, it has been described that ABA-defective
or -insensitive Arabidopsis mutants have a lower
capacity to cold acclimate, indicating that ABA is
essential for a full cold acclimation response (Heino
et al. 1990, Gilmour and Thomashow 1991). In our
laboratory, Llorente et al. (2000) isolated a mutant of
Arabidopsis, named freezing sensitive 1 (frs1), that
showed reduced freezing tolerance before and after
cold acclimation. frs1 resulted to be an allele of
ABA3, which encodes an important component of
ABA biosynthesis. Actually, frs1 mutants have lower
ABA levels compared to wild-type plants. The fact
that frs1 is affected in its constitutive freezing
tolerance indicates that ABA not only plays an
important role in cold acclimation but also has a
function in the constitutive tolerance of Arabidopsis
to freezing temperatures (Llorente et al. 2000).
Molecular characterization of frs1 demonstrated that
ABA mediates the induction of gene expression in
response to low temperatures (Llorente et al. 2000).
Confirming our results, Xiong et al. (2001) reported
the identification and characterization of los5, which
resulted to be another allele of ABA3. Similar to frs1
mutants, los5 plants have reduced levels of ABA,
decreased accumulation of transcripts corresponding
to different cold-inducible genes, and reduced
tolerance to freezing (Xiong et al. 2001). All these
data demonstrate that ABA mediates cold acclimation
by controlling cold-regulated gene expression.
The CBF family of transcriptional activators
The best characterized signalling pathway controlling
cold-inducible gene expression in Arabidopsis is that
mediated by the small family of transcriptional
activators named C-repeat binding
factors/dehydration responsive element binding
factors 1 (CBFs/DREB1s). These factors regulate the
expression of around 12% of the Arabidopsis
cold-inducible genes (Fowler and Thomashow 2002),
which gives an idea about their significance in cold
acclimation. CBF1 was the first to be isolated due to
its ability to bind to the COR15A promoter and to
induce its expression (Stockinger et al. 1997).
Subsequently, three different labs, including our own,
independently reported that CBF1 belongs to a
protein family composed by three members (CBF1-3)
(Gilmour et al. 1998, Liu et al. 1998, Medina et al.
1999). CBFs have an acidic C-terminal region that
acts as a transcriptional activator motif and an AP2
DNA-biding domain to recognize and interact with
the C-repeat (CRT)/dehydration responsive element
(DRE) motif (CCGAC) present in the promoters of a
number of cold-inducible genes that constitute the
CBF regulon (Stockinger et al. 1997, Gilmour et al.
1998, Liu et al. 1998). The three CBF genes are
organized in tandem in chromosome 4 of Arabidopsis
and their expression is rapidly and transiently induced
by cold (Gilmour et al. 1998, Liu et al. 1998, Medina
et al. 1999). Using a quantitative trait loci (QTL)
mapping approach, we determined that the genetic
basis of the natural variation for freezing tolerance in
Arabidopsis is mainly produced by a QTL that
colocalize with the CBF cluster (Alonso-Blanco et al.
2005), confirming the relevance of these factors in
cold acclimation. Constitutive overexpression of each
individual CBF gene in Arabidopsis induces the
accumulation of mRNAs from genes belonging to the
CBF regulon as well as an increase in freezing
tolerance, suggesting that the CBFs might be
functionally redundant (Kasuga et al. 1999, Gilmour
et al 2004). Genetic analysis, however, uncovered a
different and more interesting scenario. In fact, the
molecular and functional characterization of a
knock-out mutant for CBF2 revealed that the absence
of CBF2 increases Arabidopsis tolerance to freezing
temperatures, before and after cold acclimation
(Novillo et al. 2004). Furthermore, this increase
correlates with a higher accumulation of CBF1 and
CBF3 transcripts, and, consequently, of mRNAs
corresponding to CBF-target genes, under both
control and low-temperature conditions (Novillo et al.
2004). These data indicate that CBF2 negatively
modulates the expression of CBF1 and CBF3,
ensuring the adequate expression of the CBF-regulon
during cold acclimation (Novillo et al. 2004). On the
other hand, the characterization of Arabidopsis plants
with reduced induction of CBF1 or CBF3 in response
to low temperature revealed that, contrary to CBF2,
CBF1 and CBF3 are not involved in regulating the
expression of other CBF genes, demonstrating that
the three CBFs do not have the same function (Fig. 2)
(Novillo et al. 2007). Moreover, results showed that
although CBF1 and CBF3 seem to positively regulate
the induction of the same target genes, they are
concertedly required to induce the whole
CBF-regulon and, therefore, the complete
development of the cold acclimation response in
Arabidopsis (Novillo et al. 2007).
The results described above evidence the high
complexity to which the regulation of CBF expression
is subjected, and prompt the importance of an
accurate control of their induction levels. Different
transcription factors have been reported as interacting
with the promoters of the CBF genes and regulating
their induction (Fig. 2). Thus, MYB15 binds to the
CBF promoters to repress their expression (Agarwal
et al. 2006). The ICE1 MYC-like bHLH transcription
factor binds to the CBF3 promoter to activate its
expression (Chinnusamy et al. 2003). Moreover, ICE1
interacts to and represses MYB15 (Agarwal et al.
2006). Vogel et al. (2005) reported that the
overexpression of an Arabidopsis zinc finger, ZAT12,
significantly dumped the induction of the CBFs in
response to low temperature. Strikingly, ZAT12 does
not seem to affect CBF-targeted gene expression,
which suggests a complex role for this protein in the
regulation of cold-inducible gene expression and cold
acclimation (Vogel et al. 2005). ICE2, another
MYC-like bHLH transcription factor that activates
CBF1 expression (Fursova et al. 2009), has also been
described. In addition to these factors, other proteins
involved in regulating the expression of CBFs have
been identified (Zhu et al. 2007), confirming that
these genes are, in fact, subjected to a tight regulation.
Fig. 2. CBFs are central factors in cold-acclimation.
CBFs are subjected to a tightly regulation. ICE1 and ICE2
have been described to positively regulate CBF3 and CBF1
expression, respectively. ZAT12 and MYB15 negatively
regulate CBF expression. In addition, CBF2 represses
CBF1 and CBF3 expression. ICE1 has also been described
to repress MYB15. The expression of CBFs leads to the
induction of the CBF regulon and the subsequent activation
of cold acclimation response.
Interplay between cold acclimation and plant
responses to other abiotic stresses
It has already been mentioned that about one
thousand genes are regulated by low temperature in
Arabidopsis (Lee et al. 2005, Matsui et al. 2008,
Zeller et al. 2009). Interestingly, many of these genes
are also regulated by salt and water stresses (Matsui
et al. 2008, Zeller et al. 2009), indicating that plant
responses to abiotic stresses are closely related and
share common components. Ishitani et al. (1997),
trying to dissect the complex network that regulates
Arabidopsis response to cold and osmotic stresses,
screened for Arabidopsis mutants with deregulated
expression of a luciferase reporter gene driven by the
promoter of RD29A, a CBF-target gene whose
expression is induced in response to cold,
dehydration, high salt and ABA. This genetic
approach allowed them to isolate and characterize a
number of mutants (hos and los) with altered capacity
to cold acclimate. Most of these mutants were also
affected in their tolerance to water and/or salt stress
(Xiong et al. 2002), supporting the idea that plant
responses to low temperature, water stress and high
salt have several features in common. Using a similar
experimental approach, we identified Arabidopsis
mutants with high (hor) or low (lor) expression of
AtRCI2A (see above) in response to low temperature,
dehydration, high salt or ABA (Medina et al. 2005).
As in the case of hos and los mutants, several hor and
lor mutant lines are not only affected in their ability
to cold acclimate but also in their sensitivity to
dehydration, high salt and ABA treatments (Medina
et al. 2005), further supporting the narrow
relationship that exists between plant responses to
abiotic stresses. Based on the results obtained from
the physiological and molecular characterization of
the hor and lor mutants, we proposed a working
model that reflects the remarkable complexity of the
networks whereby plants appropriately respond when
exposed to adverse abiotic environmental conditions
(Fig. 3).
Fig. 3. Working model for interactions between plant
responses to cold, dehydration, high salt and ABA
treatments. From the results obtained when characterizing
the hor and lor mutants, a signalling network involved in
abiotic stress response can be proposed. The pathways
mediating AtRCI2A expression in response to cold,
dehydration, salt stress and ABA treatment interact and
converge at different levels. Indeed, we found lor mutants
affected in the expression of RCI2A in response to two
(Cold/NaCl; Cold/Dehydration; NaCl/Dehydration;
ABA/Dehydration), three (Cold/NaCl/Dehydration;
Cold/Dehydration/ABA; Cold/NaCl/ABA) and all
treatments. We also identified hor mutants altered in RCI2A
expression by all treatments. The proteins defined by the
mutants identified are placed in putative positions in the
pathways. Nevertheless, the existence of individual
pathways mediating single responses, as well as the
possibility that this signalling network interacts with other
networks cannot be excluded.
ADAPTIVE RESPONSES TO LOW TEMPERATURE IN OTHER ORGANISMS
Many microorganisms and animals have also evolved
adaptive mechanisms to cope with low and freezing
temperatures, being able to successfully colonize cold
environments, which represent most of the Earth
biosphere. Interestingly, a number of these adaptive
mechanisms are common with plants. For instance,
animals and microorganisms also preserve membrane
function and fluidity under low temperature
conditions by increasing fatty acid unsaturation
(Aguilar et al. 1998, Suzuki et al. 2001, Hayward et
al. 2007). Moreover, as in the case of plants, animals
and microorganisms produce high levels of
compatible solutes, i.e. sugars, amino acids, polyols,
to protect cells against the deleterious effects
originated by freezing tempertures (Yancey 2005).
Intracellular ice formation is lethal and most
organisms living in regions exposed to subzero
temperatures, including plants, synthesize antifreeze
proteins to inhibit, slow down, or control the growth
of ice crystals (Venketesh and Dayananda 2008).
Antioxidant defense is another common adaptive
mechanism evolved by microorganisms, plants and
animals to survive at low temperature. Strategies for
the detoxification of cold-induced reactive oxygen
species that cause membrane damage include the
production of high levels of antioxidant enzymes and
detoxifying compounds (Schulze et al. 2005,
Voituron et al. 2005, Storey 2006, Gocheva et al.
2009).
CONCLUSIONS AND PERSPECTIVES
Low temperatures are one of the most important plant
abiotic stress factors. Confronted with them, some
plants are able to adapt through mechanisms based on
membrane composition changes, protein synthesis
and activation of active oxygen scavenging systems.
One of the most interesting adaptive responses to low
temperature which plants have evolved is the so
called process of cold acclimation, whereby they
acquire an increase in freezing tolerance upon a prior
low-nonfreezing temperature treatment. This adaptive
mechanism mainly relies on gene induction, although
recent reports indicate postranscriptional, translational
and posttranslational regulation is also involved and
therefore identification of intermediaries in protein
and mRNA transport and stability will be essential in
order to completely understand the regulation of the
cold acclimation process. How plants perceive the
cold signal and how the signal is transduced to
accurately activate plant responses, including the
process of cold acclimation, still remains largely
unknown. Recent studies in our own and others'
laboratories have identified signalling components
that mediate cold acclimation. Interestingly, some of
these works have reported that several regulators are
shared with other abiotic environmental responses.
These discoveries reveal the complexity of molecular
mechanisms underlying the adaptation of plants to
their environment, raising the question of how plants
coordinate the signalling pathways involved in the
response to different abiotic stresses.
ACKNOWLEDGEMENTS
Work in our laboratory is supported by grants
GEN2006-27787-E/VEG, BIO2007-65284 and
CSD2007-00057 from the Spanish Ministry of
Science and Innovation, and grant P2006/GEN-0191
from the Regional Goverment of Madrid.
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