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An overview of research seeking and studying the potential low temperature sensors in plants is provided. It was shown that the number of potential candidates for low temperature sensors is quite wide and includes both individual intracellular structures and substances: membranes, cytoskeletal elements, chroma-tin, phytochromes, DNA, RNA, specific proteins, and sugars. It was noted that, depending on the mode of thermal exposure (intensity, cooling rate, duration, etc.), the leading role of temperature sensors may be played by different structures or substances. Apparently, this variety allows plants to respond to cold more flexibly and appropriately.
ISSN 1062-3590, Biology Bulletin, 2017, Vol. 44, No. 2, pp. 150–158. © Pleiades Publishing, Inc., 2017.
Original Russian Text © E.F. Markovskaya, T.G. Shibaeva, 2017, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2017, No. 2, pp. 120–128.
Low Temperature Sensors in Plants:
Hypotheses and Assumptions
E. F. Markovskayaa and T. G. Shibaevab, *
aPetrozavodsk State University, pr. Lenina 33, Petrozavodsk, 185910 Russia
bInstitute of Biology, Karelian Research Center, Russian Academy of Sciences,
ul. Pushkinskaya 11, Petrozavodsk, 185910 Russia
Received January 18, 2016
AbstractAn overview of research seeking and studying the potential low temperature sensors in plants is
provided. It was shown that the number of potential candidates for low temperature sensors is quite wide and
includes both individual intracellular structures and substances: membranes, cytoskeletal elements, chroma-
tin, phytochromes, DNA, RNA, specific proteins, and sugars. It was noted that, depending on the mode of
thermal exposure (intensity, cooling rate, duration, etc.), the leading role of temperature sensors may be
played by different structures or substances. Apparently, this variety allows plants to respond to cold more
flexibly and appropriately.
DOI: 10.1134/S1062359017020145
Adaptation of plant organisms to changing envi-
ronmental conditions is one of the key issues in evolu-
tionary biology. The vast majority of plants are sessile.
To evaluate the living conditions and to complete the
life cycle successfully, they need a very sensitive sen-
sory system, allowing them to assess a wide range of
environmental conditions, where temperature is one
of the leading factors. For a long time, scientists have
been trying to find the temperature sensors in plants
(Los, 2005; Samach and Wigge, 2005; Lee et al., 2008;
Penfield, 2008; Franklin and Knight, 2010; Kumar
and Wigge, 2010; Ruelland and Zachowski, 2010).
However, despite significant advances in studying the
signal transduction pathways induced in plants by
temperature and physiological responses of plants to
temperature changes (Los and Murata, 2004;
Nakashima et al., 2009; Ruelland et al., 2009), little is
known about low-temperature perception mecha-
nisms and temperature sensors. The difficulty of
studying these issues is related to the fact that tem-
perature is a physical parameter affecting molecular
(proteins, DNA) and supramolecular (membranes,
chromosomes) structures through simple thermody-
namic effects. In this sense, every molecule can sense
temperature. However, to consider a molecule or
structure as a temperature sensor, any modification
induced should be upstream of a signalling cascade
leading to a particular plant response (Ruelland and
Zachowski, 2010). According to McClung and Davis
(2010), the temperature sensor should be able to detect
absolute temperature or relative temperature changes,
to mediate a temperature perception event at the bio-
physical level, and to operate over a majority of the
temperature range likely to be encountered. In addi-
tion, the temperature sensor should distinguish a bona
fide temperature signal from transient noise and thus,
relay information that requires a response.
Apparently, plants have a set of temperature sen-
sors (McClung and Davis, 2010; Ruelland and Zach-
owski, 2010) and it is quite difficult to identify any
leading mechanism. Firstly, this occurs because the
temperature changes can be sensed in all organelles
because of its physical nature (Xiong et al., 2004;
Ruelland and Zachowski, 2010). Secondly, not all the
temperature sensors can be activated concomitantly in
plants because of different response rates of structures
to temperature changes (Nordin Henriksson and Tre-
wavas, 2003). Thirdly, different sensing devices may
not have the same temperature threshold for their
switching on (Ruelland and Zachowski, 2010).
Not only is perception of the temperature by the
plant important, so is the subsequent signal transduc-
tion. It should be noted that temperature perception is
only a step when physical parameters are converted
into biochemical ones. Sometimes, such negative
feedback mechanisms may switch off the appropriate
temperature sensing devices (Ruelland and Zach-
owski, 2010). In addition, the mechanisms for memo-
rizing the previous temperature information, informa-
tion storage and possible subsequent retrieval may
BIOLOGY BULLETIN Vol. 44 No. 2 2017
function apparently with the involvement of thermo-
sensors (McClung and Davis, 2010).
A hypothetical list of possible thermometers in
plants for sensing the environmental temperature (cel-
lular membranes, cytoskeleton, chromatin, phyto-
chromes, DNA, RNA, and proteins) was made on the
basis of numerous experiments. There is also specula-
tion about the involvement of sugars in the perception
of the temperature signal.
Membranes. Membranes were one of the first con-
tenders for the role of temperature sensory systems.
Decreased or increased temperature greatly affects the
physical properties of membrane lipids and regulates
membrane fluidity, and, hence, their functional activ-
ity. It has been established for various organisms
(Pehowich et al., 1988; Carratu et al., 1996; Inaba
et al., 2003) and demonstrates the universality of the
phenomenon. It has been shown that the reduction in
membrane fluidity at low temperatures is compen-
sated by the low-temperature induction of expression
of desaturases, which is typical for organisms from dif-
ferent taxonomic groups (Los and Murata, 1998,
2000). Thus, the desaturation of fatty acids increases
membrane fluidity, which is required for the survival
at and tolerance to low temperatures (Ishizaki-Nishi-
zawa et al., 1996; Murata and Los, 1997; Orlova et al.,
The results, which demonstrate the crucial role of
fatty acid desaturases in plant cold tolerance (Miquel
et al., 1993; Browse and Xin, 2001), and the data
obtained in experiments using chemical agents that
cause membrane fluidization or rigidification (Orvar
et al., 2000; Sangwan et al., 2001, 2002; Vaultier et al.,
2006) allowed to suggest that the membranes are the
primary sites for signal perception of decreasing tem-
perature, and the sensors that receive temperature sig-
nals are localized in membranes. It has been hypothe-
sized that the principles of low temperature signal per-
ception in plants are the same as in bacteria and
cyanobacteria (Murata and Los, 1997; Los, 2005).
Later, these assumptions were conf irmed in experi-
ments, where the physical state of membranes was
changed using genetic engineering (mutants deficient
in fatty acid desaturases). It has been found that the
low-temperature induction of genes encoding desatu-
rases is dependent on the extent of temperature
change, but not the absolute temperature (Los et al.,
1993; Vigh et al., 1993, Los, 2014). Furthermore, it has
been shown that the expression of a large number of
cold-induced genes depends on the fluidity of the cel-
lular membrane (Inaba et al., 2003). However, tran-
scriptomic experiments showed no significant differ-
ence in cold-induced gene expression between Arabi-
dopsis mutants, significantly differing in the degree of
membrane lipid saturation (Knight, M.R. and Knight, H.,
With a simplistic model in which membrane fluid-
ity acts as a sensing mechanism, it is difficult to envis-
age how such a cellular thermometer could report
absolute temperature. One solution to this conundrum
could be that different domains within the membrane
are responsible for reporting within particular tem-
perature ranges. In mammalian cells, distinct recep-
tors are responsible for reporting different temperature
ranges (Bali et al., 2009). It is possible that such higher
order organization in plant cells occurs and is part of
cold sensing (Knight, M.R. and Knight, H., 2012).
There is some preliminary evidence that enzymatic
modification of specific sphingolipids, occurring in
response to a decrease of temperature, may be linked
to down-stream gene expression (Dutilleul et al.,
2012). This may imply that such changes, rather than
membrane fluidity per se, are important for cold per-
ception (Knight, M.R. and Knight, H., 2012).
Membrane or membrane-bound proteins, such as
Hik33, DesK, and the mechanosensory Са2+- and
К+-channels could presumably be sensors localized in
Histidine kinase Hik33. This is the first low-tem-
perature sensor. It was originally identified in the cells
of cyanobacteria Synechocystis as a regulator of cold-
inducible expression of the desB gene, encoding the
ω3-desaturase (Suzuki et al., 2000). This family of
regulatory proteins is regarded as sensors of various
environmental changes: concentrations of salts, metal
ions, etc. Genome expression analysis showed that
Hik33 regulates the expression of 50% of cold-induc-
ible genes. It means that there are other sensory sys-
tems that function independently of Hik33 (Suzuki
et al., 2001). However, it is still remains unclear what
physical and chemical processes are sensed by this
protein: changes in the physical motion of fatty acids
in membrane lipids or changes in the surface charges
of membrane lipids (Nazarenko et al., 2003). The
Hik33-like histidine kinase DesK was identified in
Bacillus subtilis (Aguilar et al., 2001), where it regu-
lates the cold-inducible expression of the des gene for
the Δ5-desaturase. However, it should be noted that
no higher plant orthologues for these specific histidine
kinases exist (Knight, M.R. and Knight, H., 2012).
Mechanosensory Са2+-channels. In animal cells
transmembrane calcium (Са2+) channels were identi-
fied as the low temperature sensors (McKemy et al.,
2002; Peier et al., 2002; Patapoutian et al., 2003). Evi-
dence for the existence of cold-sensitive calcium
channels in plants has been accumulated (Minorsky
and Spanswick, 1989; Ding and Pickard, 1993; Car-
paneto et al., 2007). It was hypothesized that they are
primary sensors of cold (Plieth, 1999; White, 2009). In
plants, low temperature, drought, and salt stress cause
the influx of calcium ions in the cell cytoplasm. Rapid
entry of calcium ions into plant cells under cold stress
BIOLOGY BULLETIN Vol. 44 No. 2 2017
(Knight et al., 1996; Trewavas et al., 1996) suggests
that calcium or any nonspecific ion channels may
function as plant sensors of low temperature (Monroy
et al., 1993; Trewavas et al., 1996). It was found that
the influx of calcium ions into the cell occurs within
milliseconds. So, the process is regarded as the pri-
mary signal perception (McKemy et al., 2002) and
calcium channels in the plasma membrane are under-
stood as playing the role of sensors that perceive the
changes in the physical state of the plasma membrane
affected by different stress factors (Knight et al., 1996;
Kiegle et al., 2000; Orvar et al., 2000; Knight, M.R.
and Knight, H., 2001; McKemy et al., 2002; Sangwan
et al., 2002). However, no channel have been identi-
fied at the molecular level so far (Knight, M.R. and
Knight, H., 2012).
There are clear functional parallels between animal
and plant systems because in both cases the elevations
in cytosolic Ca2+ concentration via calcium channels
occur at the very early stages of low temperature expo-
sure (Knight et al., 1991; Peier et al., 2002). It is most
likely to be physically and temporally close to the pri-
mary temperature-sensing event.
Cytoskeleton. The state of the cytoskeleton plays an
important role in the mechanism of cold perception in
higher plants through the changes in membrane fluid-
ity, leading to the inf lux of calcium ions into the cell
cytoplasm and their release from the vacuole (Mazars
et al., 1997; Orvar et al., 2000; Sangwan et al., 2001).
It may influence the plant response, depending on the
previous “stress history” (Knight, M.R. and Knight, H.,
2012). Earlier, it was noted that a sharp decrease in
temperature causes the depolymerization of microtu-
bules and actin microfilaments (Ilker et al., 1979).
Drugs that stabilize microfilaments reduce cold sensi-
tivity, whereas drugs that destabilize microfilaments
can induce cold-dependent downstream processes in
the absence of cold (Orvar et al., 2000). However, the
observed kinetics of microfilament/microtubule
depolymerization in response to cold (Pokorna et al.,
2004) seem unlikely to be sufficiently fast to account
for the very rapid increases in calcium ions levels that
occur (Knight et al., 1991). Stabilizing microfilaments
with drugs did not completely inhibit downstream
cold gene expression (Orvar et al., 2000), suggesting
that cytoskeleton remodelling is not an absolute
requirement for cold-induced responses. Although the
cytoskeleton performs some function in temperature
detection in plants, it is not the primary cold sensor
(Knight, M.R. and Knight, H., 2012). Despite the
dominance of the membrane fluidity hypothesis in the
literature, membranes are not the only possible cellu-
lar thermometers.
Chromatin. British scientists have proposed that
temperature could be sensed via chromatin remodel-
ing and have suggested the existence of a thermosen-
sory mechanism in plants, in which the main role is
played by a H2A.Z histone (Kumar and Wigge, 2010;
Kumar et al., 2012). In the almost optimal tempera-
ture range, Arabidopsis plants have significant
changes in the transcriptome composition in response
to temperature changes. Thus, when the temperature
varies from 12 to 27°C, the abundance of about 2500
transcripts increases and another about 2900 tran-
scripts decreases. It is known that in Arabidopsis
actin-related protein ARP6 encodes a component of
the chromatin remodelling SWR1 complex, which is
required for the replacement of H2A histone by
H2A.Z in the nucleosomes (Lee et al., 2005). It is also
responsible for the induction of H2A.Z containing
nucleosomes in response to the ambient temperature.
It was shown that H2A.Z-containing nucleosomes
wrap DNA more tightly. It affects the ability of the
RNA polymerase II to transcribe genes in response to
temperature. A mechanism of transcriptome tempera-
ture regulation that is able to perceive graded tempera-
ture changes was proposed (Kumar and Wigge, 2010).
It was proved experimentally that the protein is
involved in the regulation of f lowering at low tempera-
tures and may play a role in the perception of the
ambient temperature. Kumar and Wigge (2010) also
provide evidence for the existence of the parallel
mechanism in yeast, suggesting that H2A.Z deposi-
tion may be an evolutionarily conserved mechanism
for temperature sensing across eukaryotes. However,
the question on the initial temperature signal percep-
tion and the translation of this information into nucle-
osomes remains open. It has been suggested (Kumar
and Wigge, 2010) that post-translational modifica-
tions, such as histone acetylation, might modify the
tightness of the nucleosome cores and such modifica-
tions could themselves be directly thermally respon-
Phytochromes. It is well known that phytochromes
are the main photoreceptors in plants. In the last
decade, significant progress was made in studying the
transmission of phytochrome signals. Phytochromes
are actively involved in light and temperature regula-
tion of flowering (Franklin and Knight, 2010), and the
phytochrome balance is sensitive to temperature
(Borthwick et al., 1952). In Arabidopsis, phytochrome E
plays an important role at 16°C; phytochromes B and D,
at 22°C; and phytochrome A, over the entire tempera-
ture range (Halliday et al., 2003; Heschel еt al., 2007).
It is suggested that phytochromes can act as tempera-
ture sensors (Franklin, 2009; Franklin and Quail,
2010) or may regulate temperature sensors, with each
specialized for different temperatures.
Nucleic acids: DNA and RNA. In the cyanobacte-
rium Synechocystis, with a decrease of temperature,
the degree of DNA supercoiling increases in the
genomic region containing the regulatory elements of
desB, a gene strongly induced by cold (Los, 2004).
Novobiocin, an inhibitor of DNA gyrase, added before
decreasing the temperature, prevents cold-induced
changes in DNA supercoiling and completely inhibits
BIOLOGY BULLETIN Vol. 44 No. 2 2017
cold-induced transcription of desB (Los, 2004).
Genes were identified whose cold-inducibility is sig-
nificantly repressed by novobiocin. At the same time,
there are genes with enhanced heat-inducibility in the
presence of novobiocin (Prakash et al., 2009). Perhaps
the structure of DNA in plant mitochondria and chlo-
roplasts, which do not have any histones, as in cyano-
bacteria, is regulated by temperature. It is known also
that novobiocin affects transcription in pea chloro-
plasts (Lam and Chua, 1987).
It is also known that cold stabilizes the secondary
RNA structure, while high temperatures melt RNA
secondary structures. Are these effects of temperature
change can be considered a form of temperature per-
ception? It is shown that many steps of RNA process-
ing, such as splicing, editing, or export from the
nucleus can be affected by the (de)stabilization of sec-
ondary structures. Thus, low and high temperatures
affect the rate of alternative splicing (Iida et al., 2004;
Filichkin et al., 2010), regulating gene expression.
Since the temperature influences the RNA secondary
structure and is responsible for alternative splicing,
these changes can be considered as a sensing process
since it is upstream of a cellular response (gene expres-
sion). However, more experimental data are necessary
to establish DNA or RNA as thermometers, and this
research direction is very promising (Ruelland and
Zachowski, 2010).
Potential candidates in the signaling mechanism
linking temperature sensing to the transition to f low-
ering is class of micro-RNAs (miRNAs) responsive to
ambient temperature (Lee et al., 2010). Altered accu-
mulation of a specific miRNA as a reaction to chang-
ing ambient temperatures, is important in the genera-
tion of a temperature response. The role of miRNAs in
plant temperature response has been remained very
poorly understood (McClung and Davis, 2010).
Changes in protein conformation. A decrease in tem-
perature causes unfolding of proteins (Pastore et al.,
2007), and these confirmatory changes may be
involved in cold perception (Ruelland and Zachowski,
2010). In barley, the DNA binding activity of CBF2 is
temperature-dependent (Xue, 2003). The SBF/CRT
regulon can be considered as the major genetic regu-
lon in the cold response of higher plants (Benedict
et al., 2006; Nakashima et al., 2009; Ruelland et al.,
2009). While HvCBF2 does not bind to the
CRT/DRE motif at 30°C, its binding activity gradu-
ally increases with decreasing temperature. Since an
increase in HvCBF2 activity is reversible and is
achieved in a cell-free system simply by temperature
change, it has been suggested that it is likely to be due
to a cold-induced change in conformation (Xue,
2003). It has been found that there are 54 nuclear pro-
teins in Arabidopsis (Bae et al., 2003) and 60 proteins
in rice (Cui et al., 2005), which are up- or down-regu-
lated by cold temperature.
Sugars. Performing the energy function, they play a
major role in many vital processes of photosynthetic
plants and are considered as important signals, which
regulate plant metabolism and development. Plants
have the capacity to sense the presence as well as levels
of sugars through various pathways that directly or
indirectly recognize trehalose, fructose, glucose, or
sucrose (Rolland et al., 2006). The mechanism behind
the phenomenon of sugar sensing has not yet been
described. It is supposed that a core component in this
mechanism is hexokinase AtHXK1, which plays vital
functions as the glucose sensor that integrates the
nutrient and hormonal signals to govern the gene
expression and plant growth in response to environ-
mental aberrations such as cold (Moore et al., 2003;
Cho et al., 2006). It was revealed that AtHXK1 func-
tions as a mediator in the sugar repression like the
photosynthetic CAB genes (encoding chlorophyll
a”/“b”-binding proteins) (Cho et al., 2006). Inde-
pendent of the signaling function of HXK1, glucose
metabolism induces the expression of defense-related
genes (Xiao et al., 2000).
Multifunctional sensors. At present, the idea on a
universal system of transduction of external signals
into the genome as one of the main mechanisms for
launching the adaptive reactions of the organism,
which is especially important for sessile plants, is being
considered (Seki et al., 2001). Existing signal systems
are integrated into the network, which is caused by the
presence of common signaling intermediates (Kaur
and Gupta, 2005). They include, in particular, reac-
tive oxygen species, calcium ions, nitrogen oxide, sal-
icylic acid, jasmonic acid, products of lipid degrada-
tion, etc. (Tarchevsky, 2002; Kaur and Gupta, 2005).
There is increasing evidence on the existence of mul-
tiple links between different regulatory pathways con-
trolling stress and hormonal effects (Ishitani et al.,
1997; Kasuga et al., 1999; Xiong et al., 1999; Ichimura
et al., 2000; Los and Murata, 2000; Xiong et al., 2002;
Mikami et al., 2003).
It is clear that various external stimuli may be per-
ceived by common sensory systems. For example, the
histidine kinase Hik33 of Synechocystis was first iden-
tified as a component of a system that endows resis-
tance to chemical agents inhibiting photosynthesis
(Bartsevich and Shestakov, 1995), and then as a sensor
of low temperature (Suzuki et al., 2000, 2001) and
hyperosmotic (Mikami et al., 2003) and salt stresses
(Marin et al., 2003). Studying Hik33 with DNA
microarrays revealed that the sensor controls different
sets of genes under different kinds of stress. The phys-
ical mechanisms by which Hik33 recognizes cold
stress, osmotic stress and salt stress are still not entirely
clear (Los, 2010). It is likely that Hik33 perceives
changes in membrane fluidity (Los and Murata, 2004;
Los et al., 2008; Allakhverdiev et al., 2009; Los and
Zinchenko, 2009). However, it remains unclear what
exactly causes the activation of the sensor, i.e.,
changes in the physical motion of fatty acids in mem-
BIOLOGY BULLETIN Vol. 44 No. 2 2017
brane lipids or changes in the surface charges of mem-
brane lipids associated with the altered mobility (Los,
2010), although there is evidence for the second
hypothesis (Nazarenko et al., 2003).
Low temperature, dehydration, and salt stress
induce a transient influx of Ca2+ ions into the cyto-
plasm of plant cells (Kiegle et al., 2000; Knight, M.R.
and Knight, H., 2001; Scrase-Field and Knight,
2003). It is suggested that calcium channels can serve
as multifunctional sensors (Medvedev, 2005) that
sense stress-induced perturbations in plasma mem-
branes, including changing fluidity (Orvar et al., 2000;
Knight, M.R. and Knight, H., 2001; Sangwan et al.,
2001, 2002). Considering membrane f luidity as the
key parameter that allows cells to perceive environ-
mental signals appropriately, it was possible to con-
clude that there might be sensors perceiving changes in
the physical state of the membrane, no matter what
the nature of the stress. Such sensors should be either
bound to membranes or at least associated with mem-
branes as are, for example, histidine kinases or ion
channels (Lo s, 2010).
Plants face hypothermia in different ways. It may
be long-term (days) or short-term (hours) effects of
low hardening or damaging temperature or the effect
of alternating temperatures. The question arises: what
exactly is perceived by sensors? Different authors show
similar gene profiles in plants after long-term and
periodic short-term exposure to low hardening tem-
perature (Markovskaya et al., 2007); similar transcrip-
tome profile in Solanum species differing in cold accli-
mation capacity (Carvallo et al., 2011); an increased
level of CBF-transcripts in Arabidopsis regardless of
the cooling rate (Zarka et al., 2003). All these facts can
be regarded as evidence for plant perception of the
absolute temperature. Temperature f luctuations can
occur from low to high values, or vice versa. It is shown
that a temperature drop is more informative, i.e., a
drop from high to low values (Kumar and Wigge,
2010). This is confirmed in physiological experiments
with different types of temperature effects (Mar-
kovskaya et al., 2013), and by the discovery of the
genes responsible for the plant response to tempera-
ture changes (Knight, M.R. and Knight, H., 2012).
It is known that the development of cold and frost
tolerance and changes in the intensity of physiological
processes depend on the cooling rate. Plants can actu-
ally “measure” the rate of cooling. Thus, it has been
shown that the range of membrane depolarization in
cucumber root positively correlated with the cooling
rate (Minorsky et al., 1989), suggesting a role of Са2+
in the perception of the cooling rate by plants, which
was confirmed by direct measurement of the Са2+
kinetics (Pieth et al., 1999). Presumably, the rate of
temperature change might be the determinant factor
when the exposure to temperature change is short
(Minorsky, 1989; Minorsky and Spanswick, 1989) or
when the response monitored is a rapid one, such as
calcium entry (Nordin Hendrikson and Trewavas,
2003). The absolute value of the temperature is a more
important factor under prolonged exposure (Zarka
et al., 2003).
For plants, the time of exposure to low tempera-
tures during the day is also essential. Thus, retardation
of plant growth in height occurs only when the tem-
perature decreases in the early morning and morning
hours; a similar change in the middle of the night or
during the day does not affect plant growth (Moe and
Heins, 1990; Markovskaya et al., 2013). Turned out
that plants have the ability to distinguish natural (e.g.,
seasonal) temperature decreases from changes associ-
ated with cooling that can occur throughout the grow-
ing season. It was found that plants respond to sea-
sonal (during a number of days) exposure to low tem-
peratures only under illumination (in autumn), and
the phytochromes play a role of sensors in this case.
This information serves for the plant as a signal for the
approach of adverse conditions associated with sea-
sonal changes, and adopting plants respond by
increasing the tolerance (Junttila, 1996; Robertson
et al., 200 9). Low temperatures at night do not provid e
system information for the plant (Robertson et al.,
2009). A biological clock seems to play an important
role in the mechanisms of plant responses to low tem-
Studies have shown that there is no single simple
connection between the temperature and plant
responses. In the presence of complete nucleotide
sequences of many genomes in combination with the
technology of genomic DNA microarrays, gene
expression can be studied on a higher level. Groups of
genes that respond to different stresses specifically and
non-specifically can be identified. There is also an
opportunity to search for the sensors and transducers
of various stress signals. However, even identified sen-
sors contain much uncertainty regarding the fine
mechanisms of signal perception.
Questions remain on how the sensory transmem-
brane proteins recognize changes in membrane fluid-
ity and what distinct domains and amino acids are
involved in signal perception and on specific lipids and
their domains that interact with sensory proteins and
are involved in the modulation of their conformation
and/or activity (Los, 2010). The mechanisms of
changes in the state of chromatin are still not com-
pletely clear. They may be the result of direct effect of
temperature on protein functioning or the result of sig-
nal perception in response to the change in tempera-
ture associated with changes in the membrane fluidity
or transfer of calcium ions, or the result of integration
of the chromatin remodeling process and changes in
membrane fluidity in addition to the direct effect of
BIOLOGY BULLETIN Vol. 44 No. 2 2017
temperature on protein stability and activity. Ques-
tions on plant perception of different parameters of
low-temperature effects are also still poorly investi-
gated. Possibly, the leading role of thermosensors may
be played by different structures or substances
depending on the nature of low-temperature exposure
(its intensity, cooling rate, duration, etc.). This vari-
ability apparently allows plants to respond more flexi-
bly and adequately.
The reported study was partially supported by Rus-
sian Foundation for Basic Research, research project
№ 14-04-00840 and Federal Agency for Scientific
Organizations (№ 0221-2014-0032). Experimental
facilities for this study were offered by the Shared
Equipment Center of the Institute of Biology, Kare-
lian Research Center of RAS.
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Translated by M. Shulskaya
... In recent decades, the world has made progress in understanding the mechanisms of plant cell perception of cold, low-temperature signal transduction into the genetic apparatus (Markovskaya and Shibaeva, 2017;Guo et al., However, the regulation of plant adaptive responses to hypothermia is extremely complex, since it is carried out by a multicomponent network of signaling molecules and plant hormones (Guo et al., 2018;Hassan et al., 2021). The functional interaction between them remains poorly understood. ...
... Temperature is a physical factor affecting molecules (proteins, nucleic acids, lipids) and supramolecular complexes through conventional thermodynamic effects. In this regard, each of the mentioned molecules (structures) can hypothetically act as a thermosensor (Markovskaya and Shibaeva, 2017). ...
... Exposure to cold or frost affects not only the permeability, flexibility, and resilience of the primary cell wall but if severe, may damage the plasma membrane. Low temperatures induce a hardening of the cell membrane, and a number of studies on cold perception suggest a dependency on membrane fluidity changes (Markovskaya and Shibaeva, 2017). As a major site of freezing-induced injury, the plasma membrane undergoes structural changes, a consequence of cellular dehydration (reviewed in Ingram and Bartels, 1996). ...
... Candidates of membrane-bound proteins that could serve as cold sensors are Histidine kinase Hik33, Bacillus subtilis histidine kinase DesK, and the mechanosensory Ca 2+ -and K + -channels (Markovskaya and Shibaeva, 2017). Since low temperature induces a transient influx of Ca 2+ ions into the cytoplasm (Kiegle et al., 2000;Knight and Knight, 2001;Scrase-Field and Knight, 2003), it is thought that calcium channels serve as multifunctional sensors (Medvedev, 2005) that sense stress-induced changes in plasma membranes, including changing fluidity. ...
Full-text available
Over the last three decades, there have been significant advances in the understanding of brassinosteroid (BR) biosynthesis and signaling, particularly in the model plant species Arabidopsis thaliana. BRs regulate a variety of morphogenetic and physiological processes throughout plant life. Notably, BR biosynthesis and signaling are interconnected with the signaling pathways of other phytohormones and environmental stresses. Gathering knowledge about these aspects in monocot and dicot crops is of particular importance as it may allow modulation of these processes and enable the development cultivars better adapted to ongoing climate change. This e-book is an outcome of the Research Topic 'An Update on Brassinosteroids: Homeostasis, Crosstalk, and Adaptation to Environmental Stress which was aimed at introducing the latest findings in the regulation of BR metabolism, the interconnection of the BR signalosome with phytohormonal and stress signaling pathways, and the BR-mediated adaptation of plants to environmental conditions.
... Exposure to cold or frost affects not only the permeability, flexibility, and resilience of the primary cell wall but if severe, may damage the plasma membrane. Low temperatures induce a hardening of the cell membrane, and a number of studies on cold perception suggest a dependency on membrane fluidity changes (Markovskaya and Shibaeva, 2017). As a major site of freezing-induced injury, the plasma membrane undergoes structural changes, a consequence of cellular dehydration (reviewed in Ingram and Bartels, 1996). ...
... Candidates of membrane-bound proteins that could serve as cold sensors are Histidine kinase Hik33, Bacillus subtilis histidine kinase DesK, and the mechanosensory Ca 2+ -and K + -channels (Markovskaya and Shibaeva, 2017). Since low temperature induces a transient influx of Ca 2+ ions into the cytoplasm (Kiegle et al., 2000;Knight and Knight, 2001;Scrase-Field and Knight, 2003), it is thought that calcium channels serve as multifunctional sensors (Medvedev, 2005) that sense stress-induced changes in plasma membranes, including changing fluidity. ...
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Cold stress is a significant environmental factor that negatively affects plant growth and development in particular when it occurs during the growth phase. Plants have evolved means to protect themselves from damage caused by chilling or freezing temperatures and some plant species, in particular those from temperate geographical zones, can increase their basal level of freezing tolerance in a process termed cold acclimation. Cold acclimation improves plant survival, but also represses growth, since it inhibits activity of the growth-promoting hormones gibberellins (GAs). In addition to GAs, the steroid hormones brassinosteroids (BRs) also take part in growth promotion and cold stress signaling; however, in contrast to Gas, BRs can improve cold stress tolerance with fewer trade-offs in terms of growth and yields. Here we summarize our current understanding of the roles of BRs in cold stress responses with a focus on freezing tolerance and cold acclimation pathways.
... Защита растений от последствий действия абиотических стрессоров -сложная система взаимосвязанных метаболических процессов, в которой существенную роль играют неструктурные углеводы (моносахариды и водорастворимые полисахариды) (Krasavina et al., 2014;Dong, Beckles, 2019). Наряду с осморегуляцией и энергообеспечением, они могут выполнять и криопротекторную функцию, играя важную роль в обеспечении структурной и функциональной стабильности клеток в условиях потери ими воды (Майор та ін., 2010), а также принимать участие в механизмах восприятия растительной клеткой холодового воздействия и трансдукции сигнала в генетический аппарат John et al., 2016;Markovskaya, Shibaeva, 2017). ...
... Многочисленными исследованиями было установлено, что под действием низких температур в растениях происходят значительные изменения практически на всех уровнях их организации -от организменного до молекулярного (Tarkowski, Van den Ende, 2015;John et al., 2016;Колупаев и др., 2018). Низкотемператур-ная акклимация -это процесс формирования свойств морозо-или холодоустойчивости растений в соответствующих генотипу условиях, который включает в себя изменение гомеостаза в целом и, в частности, перепрограммирование углеводного метаболизма (Nägele et al., 2011;Hoermiller et al., 2017;Markovskaya, Shibaeva, 2017;Leuendorf et al., 2020). Одним из обязательных условий развития максимальной морозо-и холодоустойчивости является накопление в тканях соответствующих растений достаточного количества растворимых углеводов, включая сахарозу, стахиозу, сорбитол, глюкозу, раффинозу, фруктозу и маннитол (Mollo et al., 2011, Krasensky, Jonak, 2012. ...
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Растворимые углеводы, являясь продуктами фотосинтеза, депо для кратковременного запасания энергии, источниками углерода и компонентами для синтеза олиго- и полисахаридов, принимают участие в ключевых физиологических, биохимических и молекулярно-генетических процессах, обеспечивающих рост, развитие, размножение и защиту от неблагоприятных биотических и абиотических факторов, среди которых важное место занимает холодовой стресс. Хотя глобальная температура Земли постепенно повышается, заморозки и случаи похолодания становятся более частыми во всем мире. В обзоре обсуждается влияние холода на всех уровнях организации растения, в результате которого проявляются функции растворимых углеводов в качестве криопротекторов, осмолитов, антиоксидантов и сигнальных молекул. В холодовой акклимации растений принимает участие весь комплекс компонентов сетей, обеспечивающих метаболизм растворимых углеводов, включая ферменты, транспортеры, гены, транскрипционные факторы и т.д. Методами геномики и генной инженерии, позволившими трансформировать определенные гены, путем изменения углеводного обмена, транспорта углеводов и/или их сигналинга, были достигнуты определенные успехи в области создания новых холодоустойчивых сортов растений, что может служить важной предпосылкой для повышения урожайности сельскохозяйственных растений в зонах с нестабильными погодными условиями.
... However, there are still many unresolved aspects regarding the integrated response of the plant to this biological "syndrome" (Beck et al. 2004). For instance, it is still unclear how plant cells sense cold and transduce this signal into specific gene expression patterns (Markovskaya & Shibaeva 2017;Ding et al. 2019, but see: Shi et al. 2018). ...
... Broadly, the meta-analyses here suggests a cascade of events in the physiological responses of symbiotic plants to chilling and freezing stresses, starting with the up-regulation of coldregulated genes, transcription factors and inductors in cold response pathways (Theocharis et al. 2012;Su et al. 2015;Subramanian et al. 2015), which apparently leads to increased concentrations of osmolytes and antioxidants (Howarth & Ougham 1993;Hamilton et al. 2012;Theocharis et al. 2012;Subramanian et al. 2015;Markovskaya & Shibaeva 2017;Shi et al. 2018), decreased concentrations in tissues of reactive oxygen species (Hamilton et al. 2012;Theocharis et al. 2012), and, most probably, reduced plasmalemma disruption (Subramanian et al. 2015). These responses, coupled with enhanced water relations and improved photosynthetic performance, possibly arising from better nutrition (Zhu et al. 2010a-c;Rho & Kim 2017), apparently lead to improved aboveground biomass in symbiotic plants at low temperatures (Ait Barka et al. 2006;Chu et al. 2016). ...
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In this review, we examine the functional roles of microbial symbionts in plant tolerance to cold and freezing stresses. The impacts of symbionts on antioxidant activity, hormonal signaling and host osmotic balance are described, including the effects of the bacterial endosymbionts Burkholderia, Pseudomonas and Azospirillum on photosynthesis and the accumulation of carbohydrates such as trehalose and raffinose that improve cell osmotic regulation and plasma membrane integrity. The influence of root fungal endophytes and arbuscular mycorrhizal fungi on plant physiology at low temperatures, for example their effects on nutrient acquisition and the accumulation of indole‐3‐acetic acid and antioxidants in tissues, are also reviewed. Meta‐analyses are presented showing that aspects of plant performance (shoot biomass, relative water content, sugar and proline concentrations and Fv/Fm) are enhanced in symbiotic plants at low (−1 to 15 °C), but not at high (20–26 °C), temperatures. We discuss the implications of microbial symbionts for plant performance at low and sub‐zero temperatures in the natural environment and propose future directions for research into the effects of symbionts on the cold and freezing tolerances of plants, concluding that further studies should routinely incorporate symbiotic microbes in their experimental designs.
... Sugars, at millimolar concentrations, are known to control plant ontogenesis through activation/repression of the genes governing morphophysiological and biochemical processes such as the cell cycle, growth, organogenesis, pollen grain germination, flowering, fruit maturation, senescence, photosynthesis, and biosynthesis of metabolites (proteins, lipids, organic acids, etc.). These phenomena occur under both normal and stress conditions of different nature including cold impact (Koch, 1996;Gupta and Kaur, 2005;Rosa et al., 2009;Ruan, 2012;Li and Sheen, 2016;Sami et al., 2016;Markovskaya and Shibaeva, 2017;Ciereszko, 2018;Ahmad, 2019). In addition, the concentration and pool of sugars act as signals for expression of the genes of carbohydrate metabolism, for example, the ones encoding invertase and sucrose synthase (NDP-α-D-glucose:D-fructose 2-α-D-glucosyltransferase, EC ...
... This allows more flexible and adequate responses of plants to cooling. The potential candidates to be sensors of low temperature include both individual intracellular structures and substances, namely, membranes, cytoskeleton elements, chromatin, phytochromes, DNA, RNA, and certain proteins and sugars [100]. The mechanisms of the morphogenetic effect of a temperature drop and those of accompanying rise in plant chilling tolerance are inadequately disclosed. ...
... The answer may reside in cold-induced changes in plant cell membranes and/or cytoskeleton. These coldinduced changes are thought to be transduced by the cytoskeleton, membrane-bound mechanoreceptors and/or focal adhesion complexes (Blume et al., 2017;Markovskaya and Shibaeva, 2017). Treatment of plants with individual phytohormones has been shown to cause changes in the stability and orientation of microtubules and actin filaments; however, studies that measure the effect of changes in phytohormone concentration on these structural elements during plant stress are lacking (reviewed in Blume et al., 2017). ...
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Plant perception of insect feeding involves integration of the multiple signals involved: wounding, oral secretions, and substrate borne feeding vibrations. Although plant responses to wounding and oral secretions have been studied, little is known about how signals from the rapidly transmitted vibrations caused by chewing insect feeding are integrated to produce effects on plant defenses. In this study, we examined whether 24 h of insect feeding vibrations caused changes in levels of phytohormones and volatile organic compounds (VOCs) produced by leaves of Arabidopsis thaliana when they were subjected to just feeding vibrations or feeding vibrations and wounding + methyl jasmonate (MeJA), compared to their respective controls of silent sham or wounding + MeJA. We showed that feeding vibrations alone caused a decrease in the concentrations of most phytohormones, compared to those found in control plants receiving no vibrations. When feeding vibrations were combined with wounding and application of MeJA, the results were more complex. For hormones whose levels were induced by wounding and MeJA (jasmonic acid, indole-3-butyric acid), the addition of feeding vibrations caused an even larger response. If the level of hormone was unchanged by wounding and MeJA compared with controls, then the addition of feeding vibrations had little effect. The levels of some VOCs were influenced by the treatments. Feeding vibrations alone caused an increase in β-ionone and decrease in methyl salicylate, and wounding + MeJA alone caused a decrease in benzaldehyde and methyl salicylate. When feeding vibrations were combined with wounding + MeJA, the effects on β-ionone and methyl salicylate were similar to those seen with feeding vibrations alone, and levels of benzaldehyde remained low as seen with wounding + MeJA alone. The widespread downregulation of plant hormones observed in this study is also seen in plant responses to cold, suggesting that membrane fluidity changes and/or downstream signaling may be common to both phenomena.
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SOLUBLE CARBOHYDRATES AND PLANT COLD ACCLIMATION N. A. Belyavskaya, O. M. Fediuk, E. K. Zolotareva Kholodny Institute of Botany of National Academy of Sciences of Ukraine (Kyiv, Ukraine) E-mail: Soluble carbohydrates, being the products of photosynthesis, short-term depot for energy storage, carbon sources and components for the synthesis of oligo- and polysaccharides, take part in key physiological, biochemical and molecular genetic processes that ensure growth, development, reproduction and protection against adverse biotic and abiotic factors, among which cold stress occupies an important place. Although the Earth‟s global temperature is gradually rising, frosts and cold weather are becoming more frequent all over the world. The review discusses the effects of cold at all levels of plant organization, as a result of which the functions of soluble carbohydrates as cryoprotectors, osmolytes, antioxidants, and signaling molecules are manifested. The whole complex of network components providing soluble carbohydrates metabolism, including enzymes, transporters, genes, transcription factors, etc., takes part in the cold acclimation of plants. By the methods of genomics and genetic engineering, which allowed the transformation of certain genes to modificate carbohydrate metabolism, carbohydrate transport and/or their signaling, certain successes have been achieved in the field of creating new cold-resistant plant varieties, which can serve as an important prerequisite for increasing the yield of agricultural plants in areas with unstable weather conditions. Key words: soluble carbohydrates, plant, cold stress, acclimation
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Plants exhibit a variety of responses to abiotic stresses that enable them to tolerate and survive adverse conditions. As we learn more about the signalling pathways leading to these responses, it is becoming clear that they constitute a network that is interconnected at many levels. In this article, we discuss the 'cross-talk' between different signalling pathways and question whether there are any truly specific abiotic stress signalling responses.
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Plants respond to environmental conditions both by adaptation and by acclimation. The ability of the plants to grow, reproduce and survive under changing climatic conditions depends on the efficiency of adaptation and acclimation. The adaptation of developmental processes in plants to temperature and photoperiod is briefly reviewed. In annual plants this adaptation is related to growth capacity and to the timing of reproduction. In perennial plants growing under northern conditions, adaptation of the annual growth cycle to the local climatic cycle is of primary importance. Examples of the role of photothermal conditions in regulation of these phenological processes are given and discussed. The genetic and physiological bases for climatic adaptation in plants are briefly examined.
Full-length cDNAs are essential for functional analysis of plant genes. Using the biotinylated CAP trapper method, we constructed full-length Arabidopsis cDNA libraries from plants in different conditions, such as drought-treated, cold-treated, or unstressed plants, and at various developmental stages from germination to mature seed. We prepared a cDNA microarray using ∼1300 full-length Arabidopsis cDNAs to identify drought- and cold-inducible genes and target genes of DREB1A/CBF3, a transcription factor that controls stress-inducible gene expression. In total, 44 and 19 cDNAs for drought- and cold-inducible genes, respectively, were isolated, 30 and 10 of which were novel stress-inducible genes that have not been reported as drought- or cold-inducible genes previously. Twelve stress-inducible genes were identified as target stress-inducible genes of DREB1A, and six of them were novel. On the basis of RNA gel blot and microarray analyses, the six genes were identified as novel drought- and cold-inducible genes that are controlled by DREB1A. Eleven DREB1A target genes whose genomic sequences have been registered in the GenBank database contained the dehydration-responsive element (DRE) or DRE-related CCGAC core motif in their promoter regions. These results show that our full-length cDNA microarray is a useful material with which to analyze the expression pattern of Arabidopsis genes under drought and cold stresses, to identify target genes of stress-related transcription factors, and to identify potential cis-acting DNA elements by combining the expression data with the genomic sequence data.
;The desC gene for the acyl-lipid ∆9-desaturase from the thermophilic cyanobacterium Synechococcus vulcanus was introduced into Nicotiana tabacum under control of the 35S promoter. Expression of the desaturase was confirmed by Western blotting. Lipid analysis revealed that lipid content and the extent of fatty acid unsaturation significantly increased in leaves of transgenic plants. Chilling tolerance of those plants also increased, as estimated by the electrolyte leakage from the tissues damaged by cold treatments. Seeds of plants that expressed the desC gene imbibed at low temperatures demonstrated higher chilling tolerance than those of the control plants. The results demonstrate that the cyanobacterial thermophilic acyl-lipid desaturase was efficiently expressed in tobacco at ambient temperatures, and its expression resulted in the enhanced chilling tolerance of the transgenic plants.