Journal of Experimental Botany, Vol. 65, No. 11, pp. 2859–2871, 2014
doi:10.1093/jxb/eru059 Advance Access publication 25 February, 2014
Review paper
Interaction of light and temperature signalling
Keara A. Franklin1, Gabriela Toledo-Ortiz2, Douglas E. Pyott2 and Karen J. Halliday2,*
1 2 School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK
SynthSys, University of Edinburgh, C.H. Waddington Building, King’s Buildings, Edinburgh EH9 3JD, UK
* To whom correspondence should be addressed. E-mail: [email protected]
Received 11 November 2013; Revised 15 January 2014; Accepted 20 January 2014
Abstract
Light and temperature are arguably two of the most important signals regulating the growth and development of
plants. In addition to their direct energetic effects on plant growth, light and temperature provide vital immediate and
predictive cues for plants to ensure optimal development both spatially and temporally. While the majority of research
to date has focused on the contribution of either light or temperature signals in isolation, it is becoming apparent that
an understanding of how the two interact is essential to appreciate fully the complex and elegant ways in which plants
utilize these environmental cues. This review will outline the diverse mechanisms by which light and temperature
signals are integrated and will consider why such interconnected systems (as opposed to entirely separate light and
temperature pathways) may be evolutionarily favourable.
Key words: Circadian clock, cold acclimation, flowering, HY5, light, photoreceptors, phytochrome, phytochrome-interacting
factors, signalling, temperature.
Introduction
Light signalling in plants is mediated by discrete protein
receptors which undergo a conformational shift following absorption of specific wavelengths of light. Previously,
analysis of plant phototransduction was confined to phytochromes, which absorb red and far-red light, and the
phototropins, cryptochromes, and members of the zeitlupe
family, which absorb in blue/UV-A wavelengths (Franklin
and Quail, 2010). More recently, UVR8 (UV RESISTANCE
LOCUS 8) has been added to the list of bona fide photoreceptors responsible for mediating responses to UV-B light
(Wu et al., 2012). This array of photoreceptors with different wavelength specificities allows plants to react to subtle
changes in the quality, quantity, and direction of light. An
enormous body of work has provided a remarkably detailed
understanding of the structure, photochemistry, and signalling components regulated by these photoreceptors. For a
detailed discussion of these areas, the reader is directed to
recent review articles (Christie, 2007; Fankhauser and Ulm,
2011; Ulijasz and Vierstra, 2011; Casal, 2013; Tilbrook
et al., 2013).
In contrast to the relatively well-defined light signalling
pathways, molecular characterization of temperature perception and signalling has been harder to resolve. This is
largely due to the complex and ubiquitous effects of temperature on cellular responses. Indeed, if one were loosely
to define a temperature receptor as a cellular component
that exhibits temperature-dependent activity, then the list
of putative temperature receptors would be extensive, as
temperature affects most, if not all, enzymatic processes
(Laider, 1997). As a consequence, research on temperature
perception has traditionally taken a reductionist approach;
examining specific responses to temperature and identifying components that are necessary and sufficient. For
instance, CNGC2 (a calcium-conducting cyclic nucleotidegated channel) has been shown to have a thermosensory
role in the induction of HEAT SHOCK PROTEIN (HSP)
expression in response to elevated temperature (Finka et al.,
2012). Other studies have shown that cold treatment activates calcium-permeable channels in Arabidopsis mesophyll
cells (Carpaneto et al., 2007). However, in these instances,
© The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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2860 | Franklin et al.
the primary temperature-sensing event(s) has yet to be
uncovered. Another study has identified a central molecular process through which gene expression can be tuned by
relatively moderate changes in ambient temperature (Kumar
and Wigge, 2010). Specifically, this mechanism involves
the nucleosomes containing the histone variant H2AZ
which exhibit temperature-sensitive binding to promoter
sequences. H2AZ nucleosome occupancy at specific promoters has been shown to prevent gene expression. Elevated
temperature leads to the expulsion of H2AZ nucleosomes,
opening up access for transcription factors that activate
gene expression. While these studies provide important
insights into the different modes of temperature signalling,
further study is required to elucidate the primary biochemical events that react to temperature.
There is now a growing recognition that light and temperature signalling are connected. Indeed there is an expanding
catalogue of cross-talk and nodes at which light and temperature signals converge. This review highlights the pathways
that operate at the confluence of light and temperature signalling and examines the adaptive value of signal integration
in a changing environment.
Temperature modification of photoreceptor
activity
Phytochrome—dark reversion
Temperature directly affects the properties of phytochrome.
Among the earliest demonstrations of this phenomenon were
the pioneering ‘flip flop’ experiments of Harry Borthwick
and colleagues, showing red/far-red reversibility in the promotion of lettuce seed germination (Borthwick et al., 1952).
In this study, the authors observed that the effectiveness of
red light pulses was temperature dependent, with significantly
greater germination recorded at 20 °C than at 30 °C. They
concluded that germination was controlled by two opposing pigments, with accumulation of the inactive ‘dormant’
pigment favoured at higher temperatures (Borthwick et al.,
1952). We now know this process to be the thermally sensitive non-photochemical or ‘dark reversion’ of phytochrome
from the biologically active Pfr form to the biologically inactive Pr form.
Dark reversion has been observed in multiple phytochromes, in multiple species, with PfrPr heterodimers showing significantly faster reversion than PfrPfr homodimers
(Brockman and Schafer, 1987; Hennig and Schafer, 2001).
This process is strongly temperature dependent, with accelerated dark reversion recorded at increased temperatures
(Schafer and Schmidt, 1974; Eichenberg et al., 1999; Hennig
and Schafer, 2001). The thermoinhibition of lettuce seed germination at high temperature can be reduced by increasing
the frequency of red light treatments, effectively counteracting accelerated dark reversion of Pfr in these conditions
(Saini et al., 1989). Genetic screens have identified multiple
mutants with altered phytochrome dark reversion. Examples
include the light-hypersensitive phyB-401 mutant and the
light-hyposensitive phyB-101 mutant (Elich and Chory, 1997;
Kretsch et al., 2000). More recently, it has been shown that
the dark reversion of phyB involves targeted phosphorylation
of a specific serine residue at the N-terminus of the PHYB
protein (Medzihradszky et al., 2013). Furthermore, it has
been demonstrated that altering the dark reversion process
by targeted mutagenesis can be a useful tool for manipulating
plant photomorphogenesis (Zhang et al., 2013). The role of
phytochrome dark reversion in plant temperature responses
has, however, yet to be fully explored.
Phytochrome—functional hierarchy
It is well established that phyA is the most abundant phytochrome in dark-grown seedlings (Clough et al., 1995) while,
in de-etiolated plants, phyB abundance is highest (Sharrock
and Clack, 2002). Unsurprisingly, phyB dominates phytochrome signalling in the light. This is demonstrated by the
obvious elongated architecture and early flowering phenotype
of phyB-deficient plants when compared with other single
phytochrome mutants (Franklin and Quail, 2010). The relative functional hierarchies of different phytochrome family
members can be altered by growth temperature at multiple
stages of the plant life cycle. Heschel and colleagues (2007)
used Arabidopsis mutants deficient in different combinations
of phytochrome to investigate their individual roles in promoting germination at different temperatures. At low temperature
(10 °C), phyE assumed the most dominant role, followed by
phyB. An involvement of phyA was observed, but only after
prolonged cold. At high temperature (28 °C), phyB was the
principal regulator, followed by phyA and phyE. At an intermediate temperature (19 °C), loss of phyA, phyB, and phyE
had little effect on seed germination, suggesting a novel role
for phyC and/or phyD. The authors suggest that different phytochrome family members may differentially regulate gibberellin (GA) signalling at different temperatures. Alternatively,
dark reversion and/or the threshold level of Pfr required to
break dormancy may differ between phytochrome family
members at different temperatures (Heschel et al., 2007).
An example of temperature altering the functional hierarchy of phytochromes in adult plants is provided by the work
of Halliday and colleagues who observed that Arabidopsis
phyB mutants displayed accelerated flowering at 22 °C, but
not at 16 °C (Halliday and Whitelam, 2003). As with seed
germination, a dominant role for phyE was observed at the
cooler temperature, although no difference in PHYE abundance was detected between plants grown at 16 °C and 22 °C
Halliday et al., 2003). The molecular events that underlie
these temperature-mediated alterations in functional hierarchy are not yet known. However, flowering responses at
both temperatures correlated with transcript abundance of
the floral activator FLOWERING LOCUS T (FT) (Halliday
et al., 2003). Elongated petioles were observed in phyB
mutants at both temperatures, suggesting the existence of
discrete pathways controlling architectural and flowering
responses.
Phytochrome—signalling
In addition to flowering, Arabidopsis leaf area responses to
a low red:far-red ratio (R:FR) have been shown to display
Interaction of light and temperature signalling | 2861
temperature dependence. At 22 °C, low R:FR-grown plants
exhibited characteristic shade avoidance phenotypes, including reduced leaf size, thickness, and biomass. At 16 °C,
however, this response was reversed, with low R:FR-grown
plants displaying considerably greater leaf area and thickness than high R:FR-grown controls (Patel et al., 2013). Low
R:FR treatment at 16 °C, but not at 22 °C, also resulted in an
increase in soluble sugars and expression of the C-REPEAT
BINDING FACTOR (CBF) regulon of cold acclimation genes (see later), suggesting that temperature and phytochrome signalling are tightly integrated (Franklin and
Whitelam, 2007; Patel et al., 2013).
Cryptochromes and phototopins
Cryptochrome
Cryptochrome has been shown to act redundantly with
phytochrome to regulate plant architecture at warmer temperatures. When grown at temperatures >20 °C, cry1 can
compensate for phyB loss by repressing internode elongation
in Arabidopsis rosettes (Mazzella et al., 2000). In the presence
of cry1, phyB acts redundantly with phyA and phyE to mediate this response (Devlin et al., 1999). At cooler temperatures,
however, internode growth is arrested, even in severely photoreceptor-deficient mutants (Mazzella et al., 2000; Halliday
and Whitelam, 2003). Temperature dependency of cry function has also been observed in the regulation of flowering
time. Mutants deficient in cry1 displayed wild-type flowering
behaviour at 23 °C, but were significantly late flowering at
16 °C (Blazquez et al., 2003). In addition, the late flowering
phenotype of cry2 (Guo et al., 1998) was significantly exaggerated at 16 °C (Blazquez et al., 2003). Analyses of multiple
photoreceptor-deficient mutants showed that the temperature sensitivity of the cry2 phenotype results, in part, from
reduced phyA activity at cooler temperature.
Phototropin
Few reports exist describing the integration of temperature
and phototropin signalling. In ferns, the low temperaturemediated relocation of chloroplasts from periclinal to anticlinal cell walls was shown to require phot2 (Kodama et al.,
2008). No cold-mediated reorientation of chloroplasts was,
however, observed in summer-green ferns or Arabidopsis. The
authors propose that low temperature chloroplast positioning may be a survival mechanism in some wintering plants
(Kodama et al., 2008). The dimerization of Arabidopsis phot1
has been observed to show temperature dependency in vitro,
but the physiological significance of these findings remains
unexplored (Nakasako et al., 2008)
Shared signalling components
Given that light and temperature signals regulate many of the
same responses, it is perhaps not surprising that both signals
converge on shared downstream regulators. Some of the key
molecular components involved in integrating photoreceptor
and temperature signalling pathways are discussed below.
PIF4
Plants grown at high temperature display phenotypes reminiscent of the shade avoidance syndrome (Casal, 2012).
These include elongated hypocotyls and petioles, leaf elevation (hyponasty), and early flowering (Gray et al., 1998; Koini
et al., 2009). Such responses are thought to facilitate leaf
cooling and accelerate seed set in unfavourable conditions
(Gray et al., 1998; Crawford et al., 2012; Bridge et al., 2013).
The signalling pathways regulating shade avoidance and high
temperature acclimation converge on a shared transcriptional
regulator, PHYTOCHROME INTERACTING FACTOR 4
(PIF4) (Lorrain et al., 2008; Koini et al., 2009; Stavang et al.,
2009). The PIFs are a subgroup of basic helix–loop–helix
(bHLH) transcription factors that physically interact with
phytochrome (Toledo-Ortiz et al., 2003). Unlike shade avoidance, where redundancy between multiple PIFs is observed,
PIF4 dominates in the regulation of high temperature acclimation (Lorrain et al., 2008; Koini et al., 2009; Stavang et al.,
2009; Li et al., 2012). PIF4 was originally isolated in a screen
for mutants displaying hypersensitivity to red light (Huq and
Quail, 2002). In these conditions, phytochrome binds PIF4,
leading to proteosomal degradation of the transcription factor and hypocotyl growth inhibition. During shade avoidance,
low R:FR stabilizes PIF4, driving the elongation growth of
plant stems (Lorrain et al., 2008). PIF4 transcript levels display transient elevation following transfer to high temperature (Koini et al., 2009; Stavang et al., 2009; Sun et al., 2012),
but mixed reports exist as to whether significant increases in
PIF4 protein levels result. These discrepancies may reflect
differences in experimental conditions and whether measurements reflect dynamic or steady-state levels (Stavang et al.,
2009; Foreman et al., 2011; Kumar et al., 2012; Yamashino
et al., 2013). Phosphorylation of PIF4 has been shown to
increase at high temperature, suggesting that post-translational modification may contribute to the enhanced PIF4
activity observed in these conditions (Foreman et al., 2011).
The mechanisms through which PIF4 regulates shade
avoidance and high temperature acclimation have recently
started to emerge. Both processes require elevated auxin
biosynthesis (Gray et al., 1998; Tao et al., 2008). Roles for
PIF4 and PIF5 in auxin signalling were initially suggested
based on transcriptomic analyses (Nozue et al., 2011). It
was subsequently demonstrated that at high temperature,
PIF4 displays enhanced binding to three genes involved in
tryptophan-dependent auxin biosynthesis (TAA1, CYP79B2,
and YUCCA8), resulting in enhanced transcript abundance,
auxin levels, and elongation growth (Franklin et al., 2011;
Sun et al., 2012). Mutants deficient in PIF4 are unable to upregulate auxin at high temperature and display significantly
reduced architectural responses in these conditions (Franklin
et al., 2011; Sun et al., 2012). In high R:FR, mutants deficient in PIF4 and PIF5 display a dwarfed architecture. This
phenotype is exacerbated in shaded conditions. During shade
avoidance, PIF4, PIF5, and PIF7 act redundantly to promote
auxin biosynthesis, although the dominance of each appears
to depend on the experimental conditions used (Hornitschek
et al., 2012; Li et al., 2012).
2862 | Franklin et al.
In addition to auxin, the hormones GA and brassinosteroids (BRs) are involved in PIF4-mediated light and temperature signalling. DELLAs are growth-repressing proteins
that physically bind PIFs, preventing the activation of target
genes (de Lucas et al., 2008; Feng et al., 2008). GA degrades
DELLAs, promoting PIF-mediated elongation growth (see
later). Functional GA and BR signalling is required for PIF4mediated elongation growth at high temperature (Gray et al.,
1998; Stavang et al., 2009). More recently, PIF4 has been
shown to bind the BR-activated transcription factor, BZR1,
providing a molecular mechanism integrating BR, auxin, and
GA signalling during plant adaptation to light and temperature signals (Oh et al., 2012).
A further example of PIF4 integrating light and temperature signals involves the regulation of Arabidopsis flowering
time. Overexpression of PIF4 dramatically accelerates flowering, suggesting that PIF4 stabilization in low R:FR may
contribute to the early flowering component of the shade
avoidance syndrome (Lorrain et al., 2008; Casal, 2012). In
short days, PIF4 performs a dominant role in the high temperature-mediated acceleration of flowering (Kumar et al.,
2012). In these conditions, PIF4 displays enhanced binding
to the floral promoter, FT, elevating transcript abundance
(Kumar et al., 2012). The authors propose that PIF4 binding to the FT promoter is facilitated at high temperature by
increased accessibility, resulting from decreased H2A.Z occupancy (see above).
HFR1
LONG HYPOCOTYL IN FAR RED (HFR1) performs an
important dual function, limiting PIF-mediated elongation
growth in low R:FR and high temperature conditions. The
hfr1 mutant was initially identified in a screen for seedlings
displaying hyposensitivity to far-red (Fairchild et al., 2000;
Fankhauser and Chory, 2000). In de-etiolated plants, HFR1
transcript levels increase in low R:FR (Sessa et al., 2005).
Mutants deficient in HFR1 were shown to display exaggerated elongation growth in these conditions, suggesting that
HFR1 operates as a negative regulator of shade avoidance.
This was confirmed by subsequent studies showing that
HFR1 binds PIF4 and PIF5, limiting their DNA binding and
transcriptional activity (Galstyan et al., 2011; Hornitschek
et al., 2012). HFR1 protein levels also increase at elevated
temperature in blue light (Foreman et al., 2011). Here, hfr1
mutants displayed exaggerated elongation responses, suggesting that HFR1 imposes significant restrictions on PIF4
activity in warm environments. The importance of multiple
photoreceptors in controlling growth at high temperature was
further demonstrated by the extreme elongation and reduced
biomass observed in phyB/cry1 double mutants in these conditions (Foreman et al., 2011).
DELLAs
As discussed previously, the inactivation of key transcription
factors in light and temperature responses is also achieved
by the binding of DELLA proteins. Targets include PIF3
(Feng et al., 2008), PIF4 (de Lucas et al., 2008), and the
BR-induced transcription factors, BZR1 and BES1, placing DELLAs as a node of cross-talk between GA and BR
signalling (Bai et al., 2012; Gallego-Bartolome et al., 2012;
Li et al., 2012). In Arabidopsis, there are five DELLA proteins, GAI, RGA, RGL1, RGL2, and RGL3 (Cao et al., 2005;
Hauvermale et al., 2012). These accumulate in the light and
are degraded in prolonged low R:FR (Achard et al., 2007;
Djakovic-Petrovic et al., 2007). DELLAs regulate photomorphogenesis throughout the plant life cycle, from the timing
of seed germination, through to reproductive development
(Cao et al., 2006). During de-etiolation, DELLA-mediated
transcriptional repression acts to suppress hypocotyl elongation and promote chlorophyll and carotenoid biosynthesis
(Achard et al., 2007; Cheminant et al., 2011), although a temporally regulated growth promotion effect of DELLAs has
been observed (Stewart Lilley et al., 2013).
In addition to regulating high temperature signalling,
DELLAs act at low temperature to inhibit the growth and
flowering of Arabidopsis rosettes. Achard and colleagues
showed that these phenotypes could be mimicked at warmer
temperature by overexpression of CBF1, a transcription factor involved in cold acclimation and the acquisition of freezing tolerance (Achard et al., 2008). They further demonstrated
that increased CBF1 expression in the cold up-regulates GA2oxidase enzymes, inactivating GA and stabilizing DELLAs to
retard development. The flexible modulation of plant growth
and development by DELLAs is thought to confer adaptive
significance in natural environments, possibly via the reallocation of resources toward stress tolerance (Achard et al., 2008).
HY5
ELONGATED HYPOCOTYL 5 (HY5) is a bZIP transcription factor with a central role in promoting plant photomorphogenesis (Lau and Deng, 2012). Mutants deficient in hy5
display impaired de-etiolation, with significantly elongated
hypocotyls and reduced pigment accumulation (Ang and
Deng, 1994). HY5 is degraded in the dark by the E3 ubiquitin ligase CONSTITUTIVE PHOTOMORPHOGENESIS 1
(COP1) and SUPPRESSOR OF PHYA-105 (SPA) complex
of WD40-domain proteins (Lau and Deng, 2012). In the
light, COP1 inactivation by phytochrome and cryptochrome
stabilizes HY5 which promotes photomorphogenesis.
Transcriptomic studies have shown that HY5 directly binds
>9000 genes, affects the expression of >1100, and integrates
multiple hormone signalling pathways (Lee et al., 2007; Lau
and Deng, 2010; H. Zhang et al., 2011). HY5 additionally
modulates phyA signalling through negatively regulating
transcript abundance of the phyA nuclear transport proteins
FAR-RED ELONGATED HYPOCOTYL 1 (FHY1) and its
homologue FHY1-LIKE (FHL) (Li et al., 2010). In UV-B,
HY5 acts redundantly with a closely related protein, HY5
HOMOLOG (HYH), to control both photomorphogenic
and protective responses (Brown and Jenkins, 2008). In contrast to classical photomorphogenesis, where COP1 and HY5
act antagonistically, COP1 and HY5 act together to promote
UV-B signalling (Favory et al., 2009). In these conditions,
Interaction of light and temperature signalling | 2863
HY5 positively regulates COP1 transcription, providing a
positive feedback loop (Huang et al., 2012).
In addition to photomorphogenesis, HY5 performs a central role in low temperature signalling. Transcriptomic profiling of Arabidopsis wild-type and hy5 mutants exposed to 4 °C
showed HY5 to regulate ~10% of cold-induced genes (Catala
et al., 2011). Fewer than half of the cold-induced targets were
also light regulated, suggesting that HY5 regulates both distinct and overlapping regulons. HY5 levels increased at low
temperature, through both elevated transcription and protein
stabilization resulting from the nuclear exclusion of COP1
(Catala et al., 2011). Freezing tolerance assays showed hy5
mutants to display a higher LT50 (the temperature at which
50% lethality is observed), confirming that HY5 acts as a
positive regulator of cold acclimation. The sensitivity of hy5
mutants to freezing temperatures was attributed, in part, to
reduced anthocyanin production, leading to elevated levels of
reactive oxygen species (ROS) (Catala et al., 2011; Y. Zhang
et al., 2011). Anthocyanins have been suggested to enhance
plant freezing tolerance in multiple species, but the underlying mechanisms remain unclear (Chalker-Scott, 1999). Zhang
and colleagues further demonstrated that GA can reduce low
temperature-induced anthocyanin production (Y. Zhang
et al., 2011). In the cold, HY5 acts redundantly with HYH to
up-regulate GA2ox1, thereby reducing GA levels and enhancing protective anthocyanin accumulation alongside growth
restraint (Achard et al., 2008; Y. Zhang et al., 2011).
The circadian clock
Circadian clocks are internal time-keeping machines that generate rhythms with a periodicity of ~24 h, allowing the synchronization of signalling and physiological events to favourable
times of the day (reviewed by Nagel and Kay, 2012; TroncosoPonce and Mas, 2012). The circadian clock comprises three
interlocking feedback loops (Zhang and Kay, 2010). The socalled morning loop involves two Myb-related transcription
factors CIRCADIAN CLOCK ASSOCIATED (CCA1) and
LONG ELONGATED HYPOCOTYL (LHY) that activate
their repressors PSEUDO RESPONSE REGULATORS
PRR9, PRR7, and PRR5. Evening loop genes include
TIMING OF CAB EXPRESSION (TOC1), GIGANTEA (GI),
ZEITLUPE (ZTL), and the evening complex (EC) formed
by LUX ARRYTHMO (LUX), EARLY FLOWERING 3
(ELF3), and EARLY FLOWERING 4 (ELF4) (Pokhilko
et al., 2012). This loop is driven through mutual repression
between TOC1/GI and EC. The current Arabidopsis circadian
clock model proposes a central repressilator structure that connects the morning and evening loops through the sequential
repression (represented by the symbol |–): CCA1/LHY |– PRR
|– EC |–CCA1/LHY, whereby each component represses the
expression of preceding components and is repressed by subsequent components (Pokhilko et al., 2012).
One of the hallmarks of the circadian clock is its ability
to operate robustly when subject to unpredictable variations
in temperature (McClung and Davis, 2010). This buffering
against environmental variations contrasts with the need to
remain sensitive to light and temperature changes to entrain
the clock accurately. This section explores how the clock is
able to cope with these apparently conflicting requirements.
Clock temperature compensation
Biochemical reaction rates are temperature sensitive, yet the
speed of the circadian clock is remarkably stable over a broad
temperature range (Gardner and Feldman, 1981; Mattern
et al., 1982; Edwards et al., 2005). This property of the clock
is widely known as temperature compensation (McClung and
Davis, 2010). Part of this compensating mechanism is counterbalance control of morning and evening loop components
(Gould et al., 2006). At higher physiological temperatures, the
amplitude of LHY expression decreases, but this is balanced
by a complementary rise in TOC1. Interestingly, the cca1
mutation was shown to have a larger impact on CAB::LUC
rhythmicity at 12 °C compared with higher temperatures,
suggesting that CCA1 had a more prominent role in regulating target genes at cooler temperatures.
Genetic analysis of the morning loop has aided our understanding of temperature compensation. PRR9 and PRR7 act
as transcriptional repressors of CCA1 and LHY that respond
preferentially to warm temperatures (Nakamichi et al., 2010;
Salome et al., 2010). This is evident in the prr7;prr9 double
mutant where, in contrast to the wild type, the period of
CCA1::LUC lengthens dramatically with increasing temperature in the 12–27 °C range (Salome et al., 2010). Depletion
of either CCA1 or LHY by artificial micro RNA (amiRNA)
knockdown partially restores periodicity to prr7;prr9 plants.
This illustrates that PRR7 and PRR9 suppression of CCA1
and LHY is required to maintain a stable period when temperatures rise. Another temperature-buffering mechanism
was uncovered by analysing the effects of protein kinase CK2
that phosphorylates CCA1 in the modulation of its activity
(Sugano et al., 1998; Daniel et al., 2004; Portoles and Mas,
2010). High temperatures have been shown to enhance CCA1
binding to the morning genes PRR9 and PRR7, and the evening genes TOC1 and LUX. However, CK2 can counteract
CCA1 activity by reducing the ability of CCA1 to bind to
target promoters (Salome et al., 2010).
Light is implicated in temperature compensation
A recent systems biology study demonstrated a prominent
role for light receptors in temperature buffering of the clock.
Statistical analysis of an extensive data set that quantified the
impact of genetic, light quality, and temperature perturbation
on period length identified strong coupling between the temperature and light input pathways to the clock (Gould et al.,
2013). Model analysis supported the hypothesis that light and
temperature signalling converge at common clock parameters.
In this study, red and blue light photoreceptors were shown to
act in opposition to control period length in warmer conditions.
CRY1 was identified as the principal blue light receptor regulating the circadian period at 27 °C. A non-intuitive prediction
that LHY protein levels rose with temperature was validated
experimentally. As LHY is an activator of PRR9, this finding
provided a potential explanation for an observed rise in PRR9
2864 | Franklin et al.
transcript levels at higher temperature. This work illustrates
that the collective photoreceptor action is required to maintain
period length at higher temperatures and it identifies key temperature-activated processes in the clock. Interestingly, a recent
theoretical study using balance equations indicates that buffering of the free-running period to light or temperature arises as
a consequence of phase buffering (Domijan and Rand, 2011).
As temperature compensation is often studied under constant
conditions, this work illustrates the relevance of thermal buffering to clock function under more natural diurnal conditions.
Clock sensitivity to light and temperature signals
While it is imperative that the circadian clockwork is resistant
to temperature change, elements of sensitivity to incoming
light and temperature signals are necessary for entrainment
across the seasons. The main entraining photoreceptors are
the phytochromes, the cryptochromes, and the family of
LOV-domain F-box proteins including ZTL (Somers et al.,
1998; Devlin and Kay, 2000; Yanovsky et al., 2000; Imaizumi
et al., 2003; Kim et al., 2007; Baudry et al., 2010). Light
has multiple entry points to the oscillator (Pokhilko et al.,
2012). It modulates the clock through transcriptional control of CCA1, LHY, PRR9, GI, and ELF4 (Kikis et al., 2005;
Nakamichi et al., 2005; Ito et al., 2007; McWatters et al.,
2007; Yamashino et al., 2008; Wenden et al., 2011; Hemmes
et al., 2012). PRR5, PRR7, and TOC1 protein levels are subject to strong diurnal regulation with increased abundance
during the daytime (Mas et al., 2003; Farre and Kay, 2007;
Kiba et al., 2007; Fujiwara et al., 2008). The stability of
PRR5 and TOC1 has been shown to be modulated directly by
ZTL that mediates their proteolytic degradation in darkness
(Mas et al., 2003; Kiba et al., 2007; Fujiwara et al., 2008).
ELF3 has been implicated in the gating light input to the circadian oscillator (McWatters et al., 2000). The stability of
the EC protein ELF3 is controlled by CONSTITUTIVELY
PHOTOMORPHOGENIC 1 (COP1) E3 ligase, while levels
of GI are modulated by the COP1–ELF3 complex (Yu et al.,
2008). These studies, which are by no means exhaustive, illustrate that the clock is strongly regulated by light through transcriptional and post-transcriptional mechanisms.
An important feature of the clock is that it can be entrained
by either light or temperature cycles (Salome and McClung,
2004). In terms of thermocycle entrainment cues, high temperatures appear to be equivalent to daylight and low temperatures are interpreted as darkness (McClung, 2006). This
suggests that light and temperature signals may converge
at some shared entrainment mechanisms. Indeed, PRR7,
PRR9, ELF3, and ZTL, that are known to be light regulated,
have also been implicated in the maintenance of periodicity
by thermal cycles (McWatters et al., 2000; Kevei et al., 2006;
Thines and Harmon, 2010; James et al., 2012b).
Temperature-activated isoform switching
Alternative splicing is another mechanism through which
environmental shifts in temperature are perceived (Filichkin
and Mockler, 2012; James et al., 2012a; Staiger and Brown,
2013). In the clock, the CCA1 gene is subject to alternative
splicing, resulting in two splice variants: full-length CCA1α,
and CCA1β that makes a protein lacking the MYB DNAbinding domain. CCA1β acts as a dominant-negative regulator interfering with the formation of functional CCA1α and
LHY homodimers, as well as CCA1α–LHY heterodimers
and preventing DNA binding (Park et al., 2012; Seo et al.,
2012). High (37 °C) temperature elevated levels of CCA1β
transcript compared with CCA1α, while exposure to cold
(4 °C) boosted CCA1α and suppressed CCA1β. The cold
repression of CCA1β was shown to be important to permit
CCA1α accumulation and transcriptional control of CBF
genes that promote freezing tolerance (see later). LHY and
PRR7 also appear to be subject to temperature-dependent
alternative splicing. Shifts from 20 °C to 4 °C led to the production of non-functional variants and nonsense-mediated
transcript decay (James et al., 2012a). Another study has
demonstrated that alternative splicing is a widespread phenomenon amongst clock genes (Filichkin and Mockler,
2012). For CCA1 and LHY, generation of transcripts with
in-frame premature stop codons was shown to be temperature dependent, suggesting that alternative splicing may be
involved in temperature compensation.
Temperature-activated alternative splicing has also been
reported for the central clock gene FREQUENCY (FRQ)
in Neurospora crassa. At cool temperatures, a short form (sFRQ) predominates, while in warmer conditions a long form
(l-FRQ) is more abundant (Liu et al., 1997; Diernfellner et al.,
2005). In this way, the thermosensitive isoforms s-FRQ and
l-FRQ are proposed to maintain clock function across temperatures. Modelling has shown that this relatively simple
counterbalance mechanism is an effective means of achieving
control over a broad temperature range (Akman et al., 2008).
It is evident from work on Arabidopsis that temperature-activated isoform switching is a widely exploited mechanism that
accomplishes a range of signalling responses to temperature
(Kalyna et al., 2012; Syed et al., 2012).
Central splicing components integrate light–temperature
signals
PRMT5 encodes a type II protein arginine methyltransferase
that targets spliceosomal proteins, modulating a range of splicing events. While PRMT5 participates in extensive splicing regulation, it also has a specific role in the circadian clock, at least
in part through controlling PRR9 splicing (Hong et al., 2010;
Sanchez et al., 2010). PRMT5 may provide a portal through
which light and temperature can regulate alternative splicing
as PRMT5 expression is sensitive to both these external signals
(Hong et al., 2010). Additionally, the splicing factor SNW/SKI
INTERACTING PROTEIN (SKIP) appears to be required for
temperature and light input to the clock. SKIP has been implicated in a variety of wide-ranging splicing events, including the
alternative splicing of PRR7 and PRR9 (Wang et al., 2012).
Circadian gating of light and temperature cues
Cold acclimation
Due to circadian control, stimuli of the same strength applied
at different times of the day can result in different magnitudes
Interaction of light and temperature signalling | 2865
of response, a phenomenon known as circadian ‘gating’ (Mas
and Yanovsky, 2009). Light and low temperature are amongst
the wide spectrum of responses that are gated by the clock
(Mas, 2008). Cold acclimation allows plants to increase their
freezing tolerance following a priming period of low temperatures (Thomashow, 1999; Browse and Xin, 2001; Miura and
Furumoto, 2013). Exposure to cold leads to the rapid induction of CBF1, CBF2, and CBF3 followed by CBF-targeted
genes (the CBF regulon) (Gilmour et al., 1998; Browse and
Xin, 2001; Thomashow, 2001, 2010; Medina et al., 2011).
However, the extent to which cold induces CBF expression
varies according to the time of day at which the plants were
exposed to low temperature (Fowler et al., 2005). A number
of studies have shown that CBF genes are themselves regulated by the clock (Salome and McClung, 2005; PrunedaPaz and Kay, 2010; Maibam et al., 2013). Instrumental in
this process are LHY and CCA1 that directly bind to CBF
promoters (Dong et al., 2011). Consistent with this regulation, the prr5;prr7;prr9 triple mutant has elevated levels of
cold stress genes (i.e. DREB1, LT1, LT130, ATGOL3, and
ADS2) and increased freezing tolerance (Nakamichi et al.,
2009). Recent mathematical modelling has further identified
that the EC and TOC1 act as regulators of CBF3 expression, in addition to the transcriptional activator INDUCER
OF CBF EXPRESSION 1 (ICE1) (Chinnusamy et al., 2003;
Zhou et al., 2011; Keily et al., 2013).
Photoperiod and light quality are instrumental regulators
of the cold acclimation pathway (Kim et al., 2002; Lee and
Thomashow, 2012). When grown in daily light/dark cycles,
expression of the CBF regulon genes peaks at ~8 h, but the
amplitude of this peak is greatly increased in short days relative to long days (Lee and Thomashow, 2012). Interestingly,
the action of phyB, PIF4, and PIF7 is required to repress the
peak of expression in long days. In this way freezing tolerance
is enhanced in short days relative to long photoperiods. Other
studies have shown that light quality can have a dramatic
impact on the CBF response, but, similarly to cold temperature induction, this is dependent on the clock. Exposure to
bursts of low R:FR light that deactivate phytochrome significantly increases the amplitude of the CBF rhythm (Franklin
and Whitelam, 2007). This dramatic response depends upon
phyB and phyD inactivation. Furthermore, plants grown
under low R:FR significantly increased freezing tolerance,
illustrating that light quality can have a substantial impact on
the priming of cold acclimation.
External coincidence—interactions between clock
outputs and light/temperature
Interactions between environmental signals and circadian
clock outputs form the basis of the phenomenon known
as external coincidence, first introduced by Erwin Bunning
(Pittendrigh, 1972). In plants, external coincidence has been
most extensively described in terms of the photoperiodic control of developmental responses such as hypocotyl elongation
and floral induction. PIF4 and PIF5 have recently emerged
as key components for the external coincidence control of
hypocotyl elongation (Nozue et al., 2007; Kunihiro et al.,
2011; Nomoto et al., 2012, 2013; Yamashino et al., 2013).
When Arabidopsis plants are grown in short-day conditions,
PIF4/PIF5 transcript abundance is rhythmic, with a peak
occurring at the end of the long night (Nozue et al., 2007;
Kunihiro et al., 2011; Nomoto et al., 2013). This peak coincides with a fall in activity of the EC (ELF3–ELF4–LUX)
that binds directly to PIF promoters via the LUX-binding
domain to suppress transcription at the start of the night
(Nusinow et al., 2011). Light promotes the degradation and
inactivation of PIFs. PIF4 and PIF5 are thought to regulate
diurnal hypocotyl elongation by up-regulating the expression of auxin-associated genes (GH3.5, IAA19, and IAA29),
GA-associated genes (GAI), BR-associated genes (BR6ox2),
ethylene-associated genes (ACS8), cytokinin-associated genes
(CKX5), and genes encoding cell wall-modifying enzymes
(XTR7) (Nomoto et al., 2012). Hence hypocotyl expansion occurs just before dawn in short days, when the intrinsic rhythm of PIF4/5 expression coincides with darkness. In
long days, the peak in PIF4/5 expression occurs during the
light period, where degradation by phyB prevents the induction of hypocotyl growth (Kunihiro et al., 2011). Recently,
this external coincidence model has been extended to account
for the observation that high temperatures induce hypocotyl
expansion in a PIF4-dependent manner, even in long days.
To account for this, a ‘dual coincidence’ model has been proposed whereby high temperatures can shift the peak of PIF4
expression to coincide with darkness in long-day conditions
(Yamashino et al., 2013). Hence, temperature is effective at
modulating the interactions between light and circadian
clock outputs in external coincidence signalling. An interesting parallel to this phenomenon is the PIF4-mediated thermal
induction of flowering in short days. Arabidopsis is a facultative long-day plant, meaning that flowering is accelerated by
lengthening photoperiods. This relies upon an external coincidence mechanism driving the expression of the FT inducer,
CONSTANS (CO), in long days. Persistent warm growth temperatures can, however, over-ride this long-day requirement
to induce flowering in short days. As described previously,
the thermal induction of flowering involves increased binding
of PIF4 to the FT promoter at high temperatures (Kumar
et al., 2012). This once again demonstrates that temperature
signalling can alter responses driven by external coincidence
between light and the clock.
Independent actions of light and
temperature on flowering control
Vernalization—floral competence
The transition from vegetative to reproductive growth is
a critical event which could be considered the most important stage of a flowering plant’s life cycle. Accordingly, floral
induction is precisely tuned to the environment to maximize
reproductive success, and light and temperature signalling
play key roles in this process. Previously we described how
light and temperature signals converge on the common component, PIF4, to regulate expression of FT (see above). This
2866 | Franklin et al.
provides a highly tuneable system, crucial for coupling the
flowering response to the current environment. Certain species (termed ‘winter annuals’) require a prolonged period of
cold to reach floral competence, followed by warming temperatures and lengthening photoperiods to induce flowering
(Henderson and Dean, 2004). This represents an additional
level at which light and temperature are integrated to control
flowering, only this time acting through distinct pathways.
The phenomenon of cold-induced floral competence is
known as vernalization and has long been recognized as
an epigenetic response (Gendall et al., 2001; Bastow et al.,
2004; Schmitz and Amasino, 2007). In vernalization-sensitive
Arabidopsis plants, the response involves the de-repression of
key genes required for floral development by the epigenetic
silencing of the MADS box transcriptional suppressor FLC
(FLOWERING LOCUS C) (Searle et al., 2006). FLC silencing is triggered by a period of prolonged cold and is mediated
by several independent mechanisms which occur at the apical
meristem (Lang, 1965). An early response to chilling involves
the expression of non-coding transcripts at the FLC locus
including a sense transcript named ‘COLDAIR’ and an antisense transcript called ‘COOLAIR’ (Swiezewski et al., 2009).
It has recently been shown that the initiation of COOLAIR
transcription involves cold-induced disruption of an inhibitory gene loop (Crevillen et al., 2013). A proposed function
of these non-coding transcripts is to recruit the histonemodifying enzyme FLD (FLOWERING LOCUS D), which
removes active histone marks at FLC by de-methylation of
the H3 histone tail at Lys4 (H3K4) (Liu and Mara, 2010). In
parallel to this, chilling promotes the transcription of a DNAbinding protein, VIN3 (VERNALISATION INSENSITIVE
3). VIN3 localizes to the promoter and first exon of the FLC
locus (Sung and Amasino, 2004). When in position, VIN3
recruits additional chromatin-remodelling factors such as
VRN2, VRN5, and SWINGER, which together comprise a
plant homeodomain polycomb-repressive complex (PHD–
PRC2) capable of adding the transcriptionally repressive
H3K27me3 histone marks to the FLC locus by tri-methylation of Lys27 of histone 3. Importantly, during the chilling
period, these H3K27me3 marks only appear at the nucleation site on the FLC locus, where VIN3 initially binds (Angel
et al., 2011). A return to warm temperatures is required for
the H3K27me3-mediated silencing to spread across the FLC
locus to ensure stable silencing of FLC transcription, a process shown to be dependent on VRN2 and VRN5 (Gendall
et al., 2001). Furthermore, the ‘epigenetic memory’ of the
vernalization is extremely sophisticated as it able to code the
duration of the chilling period into the response to the effect
that longer cold periods result in more extensive FLC silencing upon return to warm temperatures (Shindo et al., 2006;
Angel et al., 2011; Coustham et al., 2012). It was recently
shown, through a combination of experimental and modelling approaches, that the duration of the cold period is measured by a population-averaging process of cells at the apical
meristem (Angel et al., 2011). In brief, longer periods of cold
result in a higher proportion of cells initiating FLC silencing.
As histone marks can propagate through mitotic divisions,
growth of the meristem amplifies the initial conditions of
the proportion of cells with FLC silencing, allowing this to
be used as an accurate measure for the duration of the cold
period (Angel et al., 2011; Song et al., 2012).
Floral induction
While vernalization represents a very precise and elegant
temperature-sensing mechanism involved in the flowering
control of certain species, it is only necessary but not sufficient to induce flowering. This is because it removes the
inhibition of flowering but does not actively induce positive
floral regulators per se. For this, inputs from separate light
and temperature signalling pathways are required. These
include: photoperiodic control of FT via external coincidence; induction of FT by light and temperature via PIF4;
and the activation of GA signalling to enhance expression
of floral-inducing genes such as LFY (LEAFY) and SOC1
(SUPPRESOR OF CO1). These responses occur primarily in
leaves, whereas vernalization occurs at the shoot apex (Lang,
1965). The various inputs to floral induction are summarized
in Fig. 1. Importantly, these processes are all distinct from
vernalization as they are separated both temporally and spatially and share few common components. This parsing of
light and temperature signalling can be viewed as an evolutionarily adaptive trait as it allows the two pathways to act in
a permissive manner; light and warm temperature-mediated
induction is ineffective without prior competence conferred
by vernalization. Hence, the dual inputs of light and temperature ensure that flowering (in vernalization-requiring species)
is tightly controlled to occur only at precisely the most optimal time of year and is not falsely initiated by environmental
fluctuations such as an early ‘cold snap’ or by thermal- or
photo-inductive conditions when the plant is too young.
Interestingly, the legume Medicago truncatula has a different
vernalization mechanism from that of Arabidopsis and does
not appear to contain any FLC homologues in its genome.
Genetic studies have, however, indicated that vernalization
acts independently of floral induction (Jaudal et al., 2013).
Hence, even in species with evolutionarily distinct mechanisms of vernalization, there appears still to be a clear divide
between thermally induced floral competence and light and
temperature inductive processes, supporting the notion that
this separation of signalling is an adaptive trait.
Summary
It is logical that light and temperature responses are associated, as darkness is normally accompanied by cooler temperature and light by warmth. It could be argued, therefore,
that one possible evolutionary driver for the convergence of
light and temperature signalling is signal redundancy. For
example, diurnal light and temperature cycles in nature will
often occur concurrently (namely warm and light during the
day, and cold and dark at night). However, the association
between light and temperature is not simple when considering
seasonal responses, latitudinal effects, or daily fluctuations in
light/temperature. A second advantage of integrating light
Interaction of light and temperature signalling | 2867
Fig. 1. An illustration of how light and temperature cues interact through both common components and distinct pathways to regulate a developmental
response, using the control of flowering as an example. Induction is indicated by black arrows and repression is indicated by black perpendicular
lines. The vernalization pathway (shown on the right) involves the cold-induced repression of FLC by both non-coding RNAs (COOLAIR/COLDAIR)
and the histone-modifying polycomb repressive complex (PRC2), which is recruited to the FLC locus by the DNA-binding protein VIN3. Blue arrows
indicate components which are regulated by cold temperature. Following vernalization, floral meristems are competent to respond to inductive light
and temperature signals (shown left) to initiate flowering. Light and warm temperature inputs are indicated by yellow and red arrows, respectively. Light
and temperature interact to entrain the phase of the circadian clock. Outputs from the clock interact with light signals for the photoperiod-dependent
induction of CONSTANS (CO) through external coincidence. Expression of FLOWERING LOCUS T (FT) is promoted by CO in long days but also by PIF4
in short days, in a light- and temperature-dependent manner. Temperature also inputs directly at the FT locus by altering accessibility of the promoter
through temperature-dependent binding of the histone H2AZ. Gibberellic acid (GA) signalling is modulated by temperature indirectly via PIF interactions
and directly through light and temperature modulation of GA anabolic and catabolic enzymes and downstream DELLA proteins. FT expression and GA
signalling converge to induce expression of the floral meristem identity genes LEAFY (LFY) and SUPPRESSOR OF CO1 (SOC1), which initiates flowering.
and temperature signals is that it allows for a finely tuned
response to be achieved. Given that minor changes in light and
temperature can dramatically alter the physiology of plants,
it is important that responses to each signal are modified by
the other. This is illustrated by the fact that the outcome of
photoperiodic responses such as hypocotyl extension or flowering induction by long days is completely dependent on the
ambient temperature. Additionally, light and temperature
can improve the fidelity of responses by signalling through
distinct pathways to control a common output. This could be
considered a form of ‘environmental licensing’ where, in the
flowering example given, vernalization results in competence
to respond to photoinductive signals. Based on the mounting
evidence for a close association between light and temperature signalling, along with the growing appreciation for taking a systems (rather than reductionist) approach of studying
biology, we speculate that advances in signal integration will
be central to achieving a comprehensive understanding of
plant growth and survival in a changing environment.
Acknowledgements
GT-O is supported by FP7-CIG (PCIG11-GA-2012–321649) and the UK
Biotechnology and Biological Sciences Research Council (BBSRC) grant
BB/F005237/1 (ROBuST project) awarded to KJH. DEP is supported by the
BBSRC EastBio DTP award BB/J01446X/1. KAF is supported by a Royal
Society University Research Fellowship.
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