https://doi.org/10.

1093/plcell/koab302 THE PLANT CELL 2021: 00: 1–12

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How plants coordinate their development in response
to light and temperature signals
Xu Li ,1 Tong Liang 2
and Hongtao Liu 1, ,†
*

1 National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and
Ecology, Chinese Academy of Sciences, Shanghai, 200032, China
2 Keck School of Medicine, University of Southern California, Los Angeles, California 90089, USA
Review

*Author for correspondence: htliu@cemps.ac.cn

†
Senior author.
X. L and H.L wrote the manuscript. T. L gave suggestions.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the
Instructions for Authors (https://academic.oup.com/plcell) is: Hongtao Liu (htliu@cemps.ac.cn).

Abstract
Light and temperature change constantly under natural conditions and profoundly affect plant growth and development.
Light and warmer temperatures promote flowering, higher light intensity inhibits hypocotyl and petiole elongation, and
warmer temperatures promote hypocotyl and petiole elongation. Moreover, exogenous light and temperature signals must
be integrated with endogenous signals to fine-tune phytohormone metabolism and plant morphology. Plants perceive and
respond to light and ambient temperature using common sets of factors, such as photoreceptors and multiple light signal
transduction components. These highly structured signaling networks are critical for plant survival and adaptation. This re-
view discusses how plants respond to variable light and temperature conditions using common elements to coordinate
their development. Future directions for research on light and temperature signaling pathways are also discussed.

Introduction
Plants perceive changes in their environment, especially
local illumination and temperature conditions, and re-
spond by adjusting their developmental programs to ac-
climate to new conditions. For example, seedling
morphology changes in response to the initial dark-to-
light transition when the shoot breaks the soil surface
(photomorphogenesis). Light-grown seedlings have short
hypocotyls and green cotyledons that are open and ex-
panded, allowing the seedlings to increase their photosyn-
thetic output. Plants also alter their development in
response to changes in ambient temperature (thermo-
morphogenesis). Thermomorphogenesis is characterized
by hypocotyl and petiole elongation, leaf elevation, and
hyponastic growth at the seedling stage, which may
enhance leaf cooling capacity and thus improve plant sur-
vival at higher temperatures (Smith, 1970; Quint et al.,
2016). Daylength (photoperiod) and ambient tempera-
tures also affect the onset of flowering, allowing plants to
synchronize reproduction with the seasons (Li et al.,
2016a). A long-day photoperiod promotes flowering in
long-day species such as Arabidopsis (Arabidopsis thali-
ana). Increases in temperature also accelerate flowering in
many plants (Sparks et al., 2000; Andres and Coupland,
2012).
Photomorphogenesis has been studied for over a century
in a wide variety of plant species, whereas thermomorpho-
genesis has been explored only more recently (Smith, 1970;
Quint et al., 2016). In this review, we highlight recent devel-
opments in research on the regulatory mechanisms

Received August 17, 2021. Accepted December 06, 2021. Advance access publication December 14, 2021
C American Society of Plant Biologists 2021. All rights reserved. For permissions, please email: journals.permissions@oup.com
V
 2 | THE PLANT CELL 2021: Page 2 of 12
governing light and temperature sensing, signaling, and de-
velopmental responses in Arabidopsis.
Light sensing in plants
Plants sense light via photoreceptors, including the red/far-
red light receptors phytochromes A–E (phyA–E); the blue/
ultraviolet-A (UV-A) light receptors cryptochromes (CRYs);
phototropins (phots); ZEITLUPE (ZTL) family members ZTL,
light/oxygen/voltage (LOV) KELCH PROTEIN2 (LKP2), and
FLAVIN-BINDING KELCH REPEAT-BOX1 (FKF1); and the
ultraviolet-B (UV-B) light receptor UV RESISTANCE LOCUS8
(UVR8; Kami et al., 2010). These photoreceptors integrate
various light signals to optimize plant growth and develop-
ment, such as photomorphogenesis in seedlings and light-
mediated development and photoperiodic flowering in older
plants (Kami et al., 2010).
Phys are widespread in plants; they absorb red and far-red
light through their chromophore phytochromobilin and
control a variety of developmental responses (Li et al., 2011).
The phy family in Arabidopsis consists of five members,
phyA–phyE. Phys exist as dimers and occur in two photo-
switchable forms: the biologically inactive red light-absorbing
Pr form and the biologically active far-red light-absorbing Pfr
form (Li et al., 2011). During dark-to-light transitions, phys
translocate from the cytoplasm to the nucleus and form
subnuclear compartments known as photobodies (PBs;
Hiltbrunner et al., 2005; Klose et al., 2015). Higher light in-
tensity stabilizes the Pfr form and promotes the assembly of
phyB-PBs; darkness or shade (which is enriched in far-red
light) enhances phy conversion to the Pr form and stimu-
lates phy redistribution from phyB-PBs to small foci in the
nucleoplasm (Hahm et al., 2020).
Arabidopsis PHOT1, initially named NONPHOTOTROPIC
HYPOCOTYL1 (NPH1; Briggs et al., 2001), was first identified
from a genetic screen for Arabidopsis mutants lacking or
with greatly weakened phototropic responses (Liscum and
Briggs, 1995). PHOT1 encodes a 120-kDa plasma membrane-
associated protein that contains two LOV domains in its
N-terminus and a serine–threonine kinase domain in its
C-terminus (Liscum and Briggs, 1995; Huala et al., 1997). The
LOV domains in the phot1 apoprotein noncovalently bind
to the blue light-absorbing chromophore flavin mononucle-
otide (Christie et al., 1999). NPH1-LIKE1 (NPL1), a phot1 ho-
molog renamed phot2, is a photoreceptor that regulates
chloroplast movement in response to high-intensity blue
light (Jarillo et al., 2001; Kagawa et al., 2001).
In contrast to phys and phots, CRYs are present in a wide
range of organisms from bacteria to humans (Yu et al.,
2010). Plant CRYs mediate blue light-inhibited hypocotyl
elongation, the photoperiodic promotion of floral initiation,
and blue light-mediated regulation of the circadian clock,
tropism growth, and the shade avoidance response (Wang
and Lin, 2020). The Arabidopsis genome encodes at least
two CRY photoreceptors, CRY1 and CRY2, which undergo
photoresponsive photoreduction and homo-oligomerization
Li et al.
to become physiologically active (Liu et al., 2020; Ma et al.,
2020; Shao et al., 2020).
The third type of blue light receptor, ZTL family members,
mainly influence the circadian clock and photoperiodic flow-
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ering, although they also modulate light-regulated develop-
ment (Baudry et al., 2010; Song et al., 2014). As with other
photoreceptors, UVR8 was identified from a screen for
mutants showing increased susceptibility to UV-B stress
(Kliebenstein et al., 2002).
Light signaling in plants
Distinct photoreceptors transduce light signals using similar
mechanisms to regulate downstream gene expression. For
example, phys and CRYs regulate cell elongation primarily
via the activities of two transcription factor families with op-
posite functions. Photoactivated phys or CRYs translocate
into the nucleus, where they interact with the basic helix–
loop–helix (bHLH) transcription factors PHYTOCHROME-
INTERACTING FACTOR4 (PIF4) and PIF5, which are positive
regulators of cell elongation, and regulate the protein stabil-
ity or DNA binding activity of PIF proteins (Huq and Quail,
2002; Shen et al., 2007; Ni et al., 2014; Ma et al., 2016;
Pedmale et al., 2016). CRYs and UVR8 interact with the
transcription factors BRI1-EMS-SUPPRESSOR1 (BES1) and
BES1-INTERACTING MYC-LIKE1 (BIM1), which mediate
brassinosteroid (BR)-regulated gene expression and plant
growth, to inhibit their DNA binding activity and thus re-
press transcription and hypocotyl elongation (Liang et al.,
2018; Wang et al., 2018). CRYs and phys interact with the
AUXIN/INDOLE-3-ACETIC ACID-INDUCIBLE (AUX/IAA)
transcriptional regulators to protect them from degradation
and thus modulate auxin signaling and cell elongation (Xu
et al., 2018). The phy, CRY, and UVR8 photoreceptors also
repress the activity of the E3 ubiquitin ligase
CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1), thus sta-
bilizing ELONGATED HYPOCOTYL5 (HY5), a positive regula-
tor of cell elongation (Osterlund et al., 2000; Favory et al.,
2009; Liu et al., 2011).
In addition, PhyA and CRY2 stabilize CONSTANS (CO) to
promote the floral transition by inhibiting the activity of the
SUPPRESSOR OF PHYA (SPA)–COP1 complex (Valverde
et al., 2004; Zuo et al., 2011). In contrast to phyA and CRY2,
phyB promotes CO degradation and thus inhibits flowering
(Valverde et al., 2004).
Thermosensing in plants
Temperature regulates many essential processes in living
organisms, from bacteria to plants, animals, and humans
(Xiao and Xu, 2021). In bacteria, temperature regulates the
extent of DNA supercoiling and the structures of some
mRNA stem–loops; these complex, changeable structures
might act as temperature sensors (Kataoka et al., 1996;
Mizushima et al., 1997; Kortmann and Narberhaus, 2012).
Studies from Drosophila (Drosophila melanogaster) have
revealed many conserved molecular thermosensors, includ-
ing thermosensitive membrane ion channels and receptors,
 Light and temperature-regulated development
such as transient receptor potential (TRP) channels, the ion-
otropic gustatory receptor Gr28b(D), Drosophila rhodopsin
(Rh1, Rh5, and Rh6), and phospholipase Cb (PLCb). The
temperature activation thresholds and molecular mecha-
nisms of these proteins are discussed in a recent review
(Xiao and Xu, 2021).
Several factors are involved in temperature signaling, in-
cluding putative plant thermosensors (Kumar and Wigge,
2010; Chung et al., 2020; Jung et al., 2020). For example, a
forward genetic screen in Arabidopsis revealed that nucleo-
somes containing the histone variant H2A.Z mediate a ther-
mosensory response, whereby H2A.Z occupancy on
chromatin decreases with increasing temperature (Kumar
and Wigge, 2010). A more recent study showed that an
RNA-based thermoswitch located in the 50 -untranslated re-
gion (UTR) of PIF7 transcripts results in higher PIF7 transla-
tion rates at warmer temperatures (27 C), a response that is
gated by diurnal PIF7 transcript levels (Chung et al., 2020).
The PIF7 50 -UTR takes on a hairpin structure that changes
between 17 C and 27 C (Chung et al., 2020). Similarly, the
core Evening Complex (EC) member EARLY FLOWERING3
(ELF3) controls thermoresponsive growth in Arabidopsis
(Box et al., 2015). ELF3 may serve as a thermosensor via its
prion-like domain, which undergoes a reversible liquid–
liquid phase transition in response to temperature changes
(Jung et al., 2020). These recent findings reveal that light sig-
naling factors play unexpected roles as putative thermosen-
sors, suggesting that light and temperature signaling may
not constitute distinct signaling modules but may in fact
rely on the same players. In this review, we elaborate on this
hypothesis by exploring the overlap and interactions be-
tween light and temperature signaling pathways in plants.
Photoreceptors function in temperature
perception and responses
All known photoreceptors appear to be involved in temper-
ature responses, although to date, only phys and phots have
been shown to function as bona fide thermosensors
(Miyazaki et al., 2015; Jung et al., 2016; Legris et al., 2016; Ma
et al., 2016; Fujii et al., 2017; Hayes et al., 2017). For instance,
phyB was proposed to act as a thermosensor, as higher tem-
peratures reduce the pool of light-activated Pfr (active form
of phytochrome) and thus affect the physiological output of
the photoreceptor (Jung et al., 2016; Legris et al., 2016;
Hahm et al., 2020). Plants harboring null phyB mutations
display a constitutive warm-temperature response with an
over-elongated hypocotyl (Jung et al., 2016; Legris et al.,
2016). At lower temperatures, active Pfr persists until the
end of the night, but rising ambient temperatures from
10 C to 30 C at dusk accelerate the dark reversion rate of
phyB, reducing the amount of active Pfr present (Jung et al.,
2016; Legris et al., 2016).
Chromatin immunoprecipitation followed by DNA sequenc-
ing (ChIP-seq) revealed that phyB directly associates with the
promoters of temperature-responsive genes, some of which
are also bound by PIFs (Jung et al., 2016). The dynamics of
THE PLANT CELL 2021: Page 3 of 12 | 3
phyB-PB formation and movement in response to tempera-
ture changes are different from those elicited by shade (Hahm
et al., 2020). PhyB also plays a major role in controlling hypo-
cotyl elongation in response to warm temperatures in the day-
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time (when seedlings are grown in long days and constant
light conditions), primarily via the regulation of PIF4 activity
and stability, which requires the transcriptional activator
HEMERA (HMR; Qiu et al., 2019).
Besides ambient temperature responses, phys are also in-
volved in plant freezing tolerance by interacting with the
transcription factor C-REPEAT BINDING FACTOR1 (CBF1).
Cold induces CBF1 transcription, and CBF1 is essential for
mediating freezing tolerance, positively regulating cold accli-
mation, and promoting hypocotyl growth at ambient tem-
peratures (Dong et al., 2020b).
The temperature-sensing properties of phots are based on
the temperature-dependent lifetimes of their photoactivated
chromophores (Fujii et al., 2017). Chloroplasts adjust their
intracellular positions in response to both light and temper-
ature, a process integral to the phot family, based on the
phenotypes of phot1, phot2, and phot1 phot2 mutants
(Kodama et al., 2008; Fujii et al., 2017). Phots perceive both
blue light and temperature in the liverwort Marchantia poly-
morpha, where they arrange chloroplasts for optimal photo-
synthesis while minimizing photodamage. The lifetime (i.e.
the kinetics of dark reversion) of photoactivated LOV2
determines chloroplast positioning at different temperatures
(Fujii et al., 2017).
CRYs also participate in thermosensing. For example, low-
ering the temperature delays flowering in wild-type
Arabidopsis accessions in short days to some extent, and
cry2 mutants show an exaggerated response when the ambi-
ent temperature is reduced from 22 C to 16 C in short
days, raising the possibility that CRY2 is directly involved in
temperature sensing (Blazquez et al., 2003). CRY1 and CRY2
also maintain the pace of the circadian clock and circadian
rhythmicity across a range of physiologically relevant tem-
peratures, in contrast to a typical biochemical reaction,
whose rate doubles for any 10 C increase in temperature
(Gould et al., 2013). The longer circadian period displayed
by cry mutants at higher ambient temperatures (27 C) in
combined red light and blue light underscores the impor-
tance of CRYs in temperature compensation of the circadian
clock, whereby the pace of the clock remains close to 24 h
over a range of physiologically relevant temperatures (Gould
et al., 2013). Blue light represses high temperature-mediated
hypocotyl elongation via CRY1, as cry1 seedlings exhibit far
more pronounced hypocotyl elongation when grown at
28 C than at 22 C compared to the wild-type (Ma et al.,
2016).
CRY1 is also linked to H2A.Z occupancy, as CRY1 physically
interacts with the core subunits of the Swi2/Snf2-related
(SWR1) complex, SWR1 COMPLEX6 (SWC6), and ACTIN-
RELATED PROTEIN6 (ARP6). These interactions destabilize
protein–protein and protein–DNA interactions within the
nucleosome, thus controlling photomorphogenesis by
 4 | THE PLANT CELL 2021: Page 4 of 12
modulating H2A.Z deposition (Mao et al., 2021). H2A.Z oc-
cupancy decreases with increasing temperature, and ARP6
globally controls developmental responses to ambient tem-
peratures (Kumar and Wigge, 2010). These findings suggest
a new potential mechanism for CRYs and their tempera-
ture responses. In addition, CRY2 protein levels were very
recently shown to be modulated by ambient temperatures,
with CRY2 protein being degraded at low ambient temper-
atures by Light-Response Bric-a-Brac/Tramtrack/Broad
(LRB) proteins via the 26S proteasome (Ma et al., 2021).
Interestingly, CRY2 degradation at low ambient tempera-
tures occurs only under blue light and not under red light
or in the dark. The stabilization of CRY2 at high tempera-
ture makes CRY2 a better negative regulator of temperature
responses (Ma et al., 2021). LRBs physically interact with
photoexcited and phosphorylated CRY1 and CRY2 to facili-
tate their polyubiquitination and degradation in response to
blue light (Chen et al., 2021; Miao et al., 2021). It appears
that ambient temperature and blue light regulate CRY2 deg-
radation through the same class of E3 ubiquitin ligases,
LRBs. In addition to protein stability, an in vitro experiment
showed that temperature affects the photoreduction of
CRY, as the concentration of the biologically active
FADH.redox form of CRY increased at lower temperatures
(Pooam et al., 2021). However, the details and mechanisms
of the responses of CRYs to ambient temperature remain to
be fully elucidated.
ZEITLUPE (ZTL) is also involved in warm-temperature
responses, as it positively regulates hypocotyl elongation in
warm temperatures and functions in temperature compen-
sation of the circadian clock (Edwards et al., 2005; Miyazaki
et al., 2015). Indeed, ztl mutants showed reduced hypocotyl
growth at higher ambient temperatures (27 C) and a char-
acteristic prolonged photoperiod at all temperatures tested
(12 C, 16 C, 22 C, and 28 C; Edwards et al., 2005; Miyazaki
et al., 2015). The loss of ZTL function results in defects in
warm temperature-promoted hypocotyl elongation, mainly
by affecting PIF4 and auxin-related gene expression (Saitoh
et al., 2015, 2021). Although much evidence indicates that
ZTL is involved in temperature responses, the underlying
molecular mechanism is unclear. Whether the expression of
ZTL or ZTL protein levels change as a function of tempera-
ture is unknown.
Complex crosstalk also takes place between UV-B signal-
ing and high ambient temperature signaling. UVR8 perceives
UV-B light and attenuates thermomorphogenesis via multi-
ple mechanisms, such as inhibiting PIF4 activity and auxin
signaling (Hayes et al., 2017). UVR8 interacts with the
COP1–SPA1 complex to inhibit PIF4 transcription, leading
to a strong repression of PIF4 protein abundance at 22 C
and 28 C when seedlings are exposed to UV-B light. This
UV-B-induced degradation of PIF4 at high temperatures is
partially compensated for by the stabilization of the bHLH
protein LONG HYPOCOTYL IN FAR-RED1 (HFR1) under
these conditions, which in turn binds to PIF4 to prevent it
from performing its normal functions (Hayes et al., 2017).
Li et al.
These findings suggest that plants use various photorecep-
tors to sense or respond to ambient temperature and that
temperature sensing requires the activation of these photo-
receptors by light, as the perception of ambient temperature
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relies on the temperature-dependent lifetime of photoacti-
vated phy and phot. Similarly, the modulation of CRY2 deg-
radation by ambient temperatures is blue-light dependent
(Figure 1). Phys, CRYs, and UVR8 modify the common
downstream factor PIF4 by affecting its transcriptional activ-
ity or its protein stability to regulate both light-induced de-
velopment and thermomorphogenesis (Figure 1). The events
in temperature signal transduction downstream of phots
still need to be elucidated. Moreover, it is intriguing that
two types of blue light receptors, ZTL and CRYs, play oppo-
site roles in thermoresponses; the mechanism and potential
physiological significance of this remain to be explored.
Light signaling hubs function in temperature
responses
PIFs are pivotal components of light and temperature signal
transduction pathways. These proteins repress seed germina-
tion and promote seedling de-etiolation and shade avoid-
ance syndrome (Paik et al., 2017). The phyB-PIF4/PIF5
signaling module also regulates leaf senescence at higher am-
bient temperatures (Kim et al., 2020a). PIFs are growth pro-
moters, based on the shorter hypocotyls and petioles seen
in the pif4 and pif5 single mutants and the pif4 pif5 double
mutant in response to warmer temperatures (Koini et al.,
2009; Ma et al., 2016). Both elevated temperatures and
higher light intensity stimulate PIF4 and PIF5 transcription
rates (Zheng et al., 2021). PIF4 protein levels are strongly
regulated by light but only moderately by ambient tempera-
tures (Kumar et al., 2012; Ma et al., 2016). PIF7 is required
for plant thermomorphogenesis, especially during the day-
time. Transcriptome deep sequencing (RNA-seq) and chro-
matin immunoprecipitation (ChIP)-seq analysis revealed that
PIF7 directly activates a group of warm temperature-
responsive genes (Chung et al., 2020). Elevated temperatures
enhance PIF7 protein accumulation, which may contribute
to the thermomorphogenic response (Fiorucci et al., 2020).
PIF7 and PIF4 depend on each other for thermomorphogen-
esis by forming heterodimers (Fiorucci et al., 2020).
In addition to being a key regulatory light signaling path-
way, the DE-ETIOLATED1 (DET1)-COP1-HY5 module also
mediates hypocotyl elongation at higher ambient tempera-
tures, likely by regulating PIF4 transcription via HY5 (Delker
et al., 2014). Both det1 and cop1 mutants are insensitive to
elevated ambient temperatures, as revealed by the lack of
temperature-induced hypocotyl elongation, whereas hy5
mutants exhibit the opposite phenotype, with more elon-
gated hypocotyls than the wild-type, indicating they are hy-
persensitive to a rise in ambient temperatures (Delker et al.,
2014). Just as dark exposure promotes the translocation of
COP1 into the nucleus, elevated temperatures also stimulate
the relocation of COP1 into the nucleus, which is accompa-
nied by the degradation of HY5 and the alleviation of
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Figure 1 Ambient temperature-sensing and signaling pathways interact with light signaling pathways. All known photoreceptors (phys, phots,
CRYs, ZTL family members, and UVR8) and several light signaling hubs (COP1-HY5, PIFs) involved in ambient temperature responses are shown.
Phys, phots, H2A.Z, ELF3, and PIF7 were shown to be functional thermosensors, although the components that function in temperature signal
transduction downstream of phots are not clear. Additional light-signaling components (SWR1-C, HMR, SEU, INO80-C) contribute to temperature
responses through the DET1-COP1-HY5 or PIF pathways to regulate downstream gene expression and plant growth.

inhibited hypocotyl elongation (Park et al., 2017). In addi-
tion, HY5 competitively binds to the promoters of PIF4 tar-
get genes and represses their transcription (Gangappa and
Kumar, 2017). However, genetic evidence suggests that
DET1- or COP1-mediated hypocotyl elongation in response
to higher temperatures is independent of HY5 but depen-
dent on DET1- and COP1-mediated stabilization of PIF4
protein (Gangappa and Kumar, 2017). COP1 regulates the
rate of hypocotyl elongation in response to shade and warm
temperatures in a DELLA-dependent manner (Blanco-
Tourinan et al., 2020). COP1 physically interacts with and
destabilizes DELLAs, which are negative regulators of gibber-
ellin (GA) signaling, in response to environmental cues
(Blanco-Tourinan et al., 2020). The COP1 and PIF pathways
crisscross in transducing light and temperature signaling.
Additional light signaling components contribute to tem-
perature responses, mainly through the above-mentioned
pathways (Figure 1). SPAs are required for thermomorpho-
genesis by regulating the activity of the phyB-PIF4 module.
In spa mutants at high ambient temperatures, the thermo-
sensor phyB is stabilized and PIF4 fails to accumulate
(Lee et al., 2020). PHOTOPERIODIC CONTROL OF
HYPOCOTYL1 (PCH1) functions in both light-regulated devel-
opment and thermomorphogenesis by interacting with phyB
as a structural component of phyB-PBs, thus protecting Pfr
from thermal reversion back to Pr (Huang et al., 2019).
The loss of functional PCH1 compromises PB formation and
disrupts phyB signaling, including light-regulated development
and circadian rhythmicity (Huang et al., 2016; Huang et al.,
2019). SEUSS (SEU), a negative transcriptional regulator of
light-mediated development, positively regulates thermomor-
phogenesis by directly interacting with PIF4 (Huai et al.,
2018). The SUMOylation of SEU is regulated by light and is a
prerequisite for its functions in photomorphogenesis, light-
regulated development, and thermomorphogenesis and for its
interaction with PIF4 (Zhang et al., 2020).
The INO80 chromatin remodeling complex (INO80-C)
promotes thermomorphogenesis by associating with PIF4
and mediating temperature-induced H2A.Z eviction at PIF4
target promoters (Xue et al., 2021). These findings offer a
possible mechanism for the eviction of H2A.Z from chroma-
tin at high temperatures. Two additional players are COLD-
REGULATED GENE27 (COR27) and COR28, which were
identified as cold-responsive genes in Arabidopsis transcrip-
tome profiling studies (Fowler and Thomashow, 2002;
Mikkelsen and Thomashow, 2009). COR27 and COR28 are
involved in regulating the circadian clock as well as the
tradeoff between flowering and freezing tolerance (Li et al.,
2016b; Wang et al., 2017). COR27 and COR28 promote hy-
pocotyl growth via their interactions with the COP1-HY5
regulatory hub. COR27 and COR28 physically interact with
COP1 and undergo COP1-mediated degradation in the dark.
 6 | THE PLANT CELL 2021: Page 6 of 12
COR27 and COR28 also negatively regulate photomorpho-
genesis by repressing HY5 transcriptional activity, thereby
fine-tuning the output of the COP1-HY5 regulatory hub to
ensure proper photomorphogenic and light-regulated devel-
opment (Li et al., 2020; Zhu et al., 2020).
Endogenous circadian rhythms participate in
temperature responses
The circadian clock helps plants integrate exogenous and
endogenous cues to coordinate growth and developmental
processes at the right time of day and/or season. Light and
temperature cycles are the two major input signals feeding
into the central oscillator, which is composed of a set of
transcription–translation feedback loops. The genes
CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE
ELONGATED HYPOCOTYL (LHY) are expressed just before
dawn and early in the morning; members of the PSEUDO-
RESPONSE REGULATOR (PRR) gene family are then
expressed sequentially, starting with PRR9 and roughly fol-
lowed in order by PRR7, PRR5, PRR3, and TIMING OF CAB2
EXPRESSION1 (TOC1, also named PRR1); PRR9, PRR7, and
PRR5 repress CCA1 and LHY expression. At night,
GIGANTEA (GI), ELF3, ELF4, and LUX ARRHYTHMO (LUX)
are expressed, and the proteins encoded by ELF3, ELF4, and
LUX form the EC to repress TOC1’s and their own expres-
sion. CCA1 and LHY inhibit the transcription of evening
genes, whose encoded proteins in turn repress CCA1, LHY,
and PRR9 transcription (McClung, 2014).
The expression of photoreceptors is under circadian con-
trol, and most photoreceptors (phys and CRYs) participate
in light entrainment of the circadian clock (Sanchez et al.,
2020). Most organisms also exhibit temperature compensa-
tion (Edwards et al., 2005). Based on genetic evidence, the
flowering time protein GI and the blue light receptor ZTL
are strong candidates for influencing temperature compen-
sation between 12 C and 27 C in Arabidopsis (Edwards
et al., 2005). Warm temperatures enhance the accumulation
of GI, which then stabilizes DELLA proteins and thus attenu-
ates PIF4 function during thermomorphogenesis (Park et al.,
2020). The transcript levels of the core clock components
TOC1, CCA1, and LHY have varied amplitudes and peak lev-
els in gi null mutants in response to changing temperatures
(Gould et al., 2006). PRR7 and PRR9 appear to maintain a
constant circadian period at various temperatures by adjust-
ing the transcript levels of CCA1 and LHY (Salome et al.,
2010).
In addition, the physical interaction of TOC1 and PIF4
mediates the circadian gating (modulation of growth pace
as a function of time of day) of thermoresponsive growth
(Zhu et al., 2016). The EC plays a pivotal role in the circa-
dian clock, light signaling, and temperature signaling (Ezer
et al., 2017) and directly binds to the PIF4 and PIF5 pro-
moters to repress their transcription at night (Nusinow
et al., 2011). Furthermore, the EC has been proposed to act
as a temperature-responsive transcriptional repressor affect-
ing rhythmicity and thermoresponsive growth (Ezer et al.,
Li et al.
2017). ELF3 might function as a thermosensor, as described
above (Jung et al., 2020). ELF4 also plays a role in buffering
the temperature responsiveness of ELF3 by stabilizing ELF3
in an active state at high temperatures (Jung et al., 2020).
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Consistent with the notion that ambient temperatures regu-
late ELF3 stability, recent studies identified XB3 ORTHOLOG
1 IN ARABIDOPSIS THALIANA (XBAT31) as the E3 ligase
that mediates ELF3 degradation at warm temperatures, a
process requiring the thermomorphogenesis regulator B-
BOX18 (BBX18; Ding et al., 2018; Zhang et al., 2021).
Taken together, these findings confirm the notion that
the circadian clock plays important roles in the transduction
of both light and temperature signals, suggesting that light
and ambient temperatures may modulate seedling and plant
development via the same regulatory mechanism
(Figure 2A).
Endogenous phytohormones and
environmental factors
The growth mediated by light and ambient temperatures is
inseparable from endogenous phytohormones.
Photoreceptors regulate cell growth via various phytohor-
mones, including auxin, BRs, ethylene, GAs, and jasmonate
(JA; Luo and Shi, 2019; Fernandez-Milmanda et al., 2020).
Here, we describe recent progress in determining which
(and how) endogenous phytohormones mediate plant de-
velopment in response to environmental signals.
Auxin mediates architectural changes in plants in response
to shade and warm temperatures, as demonstrated by the
short hypocotyl phenotype exhibited by mutants of SHADE
AVOIDANCE DEFICIENT3 (SAV3), encoding an L-Trp amino-
transferase involved in auxin biosynthesis. This mutant fails
to rapidly produce free IAA in response to changing light or
ambient temperature conditions, in the shade, or at high
ambient temperatures (Tao et al., 2008; Zheng et al., 2016).
Local auxin metabolism in the hypocotyl plays a critical
role in hypocotyl elongation (Zheng et al., 2016). The
warmer temperature-induced rise in YUC8 transcription and
repression of UDP-GLYCOSYLTRANSFERASE 76F1 (UGT76F1)
fine-tune endogenous free IAA levels and depend on PIF4
function (Sun et al., 2012; Chen et al., 2020). However, hypo-
cotyl cell elongation also requires cotyledon-derived auxin,
pointing to both autonomous and organ-interdependent
temperature sensing and signaling (Bellstaedt et al., 2019).
Auxin signaling is also directly connected to photorecep-
tors, as photoactivated CRY1 and phyB physically interact
with AUX/IAA proteins to stabilize them by reducing their
interactions with the auxin receptor TRANSPORT
INHIBITOR RESPONSE1 (TIR1), an E3 ubiquitin ligase re-
sponsible for their degradation (Xu et al., 2018). Upon their
stabilization and accumulation, AUX/IAAs inhibit auxin sig-
naling by interacting with AUXIN RESPONSE FACTORs, pre-
venting the transcriptional activation of their downstream
targets (Xu et al., 2018). PIF4 and PIF5 regulate auxin biosyn-
thesis under changing light conditions and at high ambient
temperatures (Franklin et al., 2011; Hornitschek et al., 2012).
 Light and temperature-regulated development
Figure 2 Light and temperature regulate plant growth via similar
mechanisms. A, Light and temperature regulate the circadian clock.
The core clock components that are regulated by both light and tem-
perature are shown from left to right based on the time of expression
of their encoding genes throughout the day. Phy, ZTL, and PIF4 also
interact with some core clock components (CCA1/LHY, TOC1, ELF3)
to transduce light and temperature signaling information. B,
Photoreceptors modify phytohormone metabolism and signaling
through the PIF/COP1 pathways or by directly interacting with key
factors (AUX/IAA, BZR1/BES1, EBF1/2/EIN3, DELLA) involved in phy-
tohormone signaling, thus mediating light and temperature signaling
to regulate plant morphology. C, Environmental signaling, the central
oscillator, and endogenous phytohormones form an integrated net-
work to modulate plant development.
CRYs and phys interact with PIFs to inhibit their transcrip-
tional activity, thereby reducing the expression of YUCs and
many other auxin-related genes (Huq and Quail, 2002;
Franklin et al., 2011; de Wit et al., 2016; Ma et al., 2016; Kim
et al., 2020b). CRY1 represses auxin biosynthesis in response
to elevated temperatures by interacting with PIF4 (Ma et al.,
2016).
THE PLANT CELL 2021: Page 7 of 12 | 7
In addition to auxin, increased BR levels are essential for
thermomorphogenic hypocotyl growth (Ibanez et al., 2018).
A screen for mutants with defects in high temperature-
specific cell elongation identified several genes involved in
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BR biosynthesis. BRs act downstream of PIF4 and auxin to
regulate cell elongation via the BR-regulated transcription
factor BRASSINAZOLE RESISTANT1 (BZR1) in response to
elevated ambient temperatures (Ibanez et al., 2018). Besides
BZR1, another key BR regulator, BES1, associates with PIF4,
which alters the DNA recognition ability and transcriptional
activity of BES1 (Martinez et al., 2018). At higher ambient
temperatures, elevated PIF4 levels compete for binding to
BES1 and reduce the formation of BES1 homodimers, result-
ing in derepressed BR biosynthesis at dawn (Martinez et al.,
2018). The signaling distance between photoreceptors and
BES1/BZR1 may be even smaller than initially thought, as
photoactivated CRYs and phys appear to interact with
BES1/BZR1 to inhibit BR signaling (Wang et al., 2018; He
et al., 2019; Wu et al., 2019; Dong et al., 2020a). Nucleus-
localized UVR8 itself physically interacts with BIM1 and
BES1 to repress their DNA binding activity and BR-induced
gene expression (Liang et al., 2018). While most studies of
temperature-responsive growth have focused on the aerial
parts of plants such as hypocotyls and cotyledons or leaves,
elevated temperatures also enhance root elongation by re-
ducing the levels of the BR receptor BR INSENSITIVE1 (BRI1)
to diminish BR signaling (Martins et al., 2017).
PhyB and COP1 form a direct link between light and eth-
ylene signaling pathways (Zhong et al., 2012; Yu et al., 2013).
Light-activated phyB directly enhances the interaction be-
tween the nucleus-localized transcription factor ETHYLENE-
INSENSITIVE3 (EIN3) and the F-box proteins EIN3-BINDING
F-BOX PROTEIN1 (EBF1) and EBF2 to attenuate ethylene
responses (Shi et al., 2016). In contrast, nucleus-localized
COP1 directly degrades HY5 in the dark and stabilizes EIN3
by promoting the degradation of EBF1 and EBF2 (Yu et al.,
2013). Ethylene signaling is also modified by ambient tem-
peratures. The E3 ligase SALT- AND DROUGHT-INDUCED
RING FINGER1 (SDIR1) destabilizes EBF1 and EBF2 to pro-
mote the accumulation of EIN3 in response to fluctuations
in ambient temperatures (Hao et al., 2021). SDIR1 transcrip-
tion is induced by elevated ambient temperatures (Hao
et al., 2021). Whether SDIR1 is also affected by light will be
an interesting question to explore in the future.
GAs modulate light signaling to prevent seedling de-
etiolation in the dark. Blue light inhibits GA biosynthesis
through CRY (Zhao et al., 2007). As DELLAs are negative ele-
ments in the GA signaling pathway, these growth repressors
are destabilized by GAs but are also COP1 substrates, thus
promoting growth in response to light and temperature
changes (Blanco-Tourinan et al., 2020). CRY1 physically
interacts with DELLA proteins in a blue light-dependent
manner, thus stabilizing them by preventing the interaction
between DELLA proteins, the F-box protein SLEEPY1 (SLY1),
and the GA receptor GA-INSENSITIVE DWARF1 (Xu et al.,
2021; Zhong et al., 2021). Furthermore, warm temperatures
 8 | THE PLANT CELL 2021: Page 8 of 12
enhance the accumulation of GI, which stabilizes DELLA
proteins under long-day conditions, thus integrating photo-
periodic and temperature signals with the GA pathway
(Park et al., 2020).
JA catabolic pathways are affected by light and tempera-
ture. For instance, SULFOTRANSFERASE 2a (ST2a) provides
a direct molecular link between light/temperature and JA
signaling in plants (Fernandez-Milmanda et al., 2020; Zhu
et al., 2021). Canopy light conditions and warm tempera-
tures increase the expression of genes controlling JA catabo-
lism, such as ST2a. This gene encodes an enzyme that
reduces bioactive JA contents and thus leads to the stabiliza-
tion of JASMONATE-ZIM-DOMAIN PROTEIN (JAZ) pro-
teins, ultimately facilitating plant growth (Fernandez-
Milmanda et al., 2020; Zhu et al., 2021).
Photoreceptors (such as phys, CRYs, and UVR8) modify
phytohormone metabolism and signaling either through
PIF/COP1 pathways or by directly interacting with key fac-
tors in phytohormone signaling, thus modulating the light
and temperature signals that regulate plant morphology.
These phytohormones and related regulatory factors are
intertwined to form a precise regulatory network that helps
plants adapt to a changing environment (Figure 2B).
Conclusion and perspectives
In the natural world, daytime is typically accompanied by
higher temperatures, while evening and nighttime bring
cooler temperatures. However, what if plants are exposed to
higher ambient temperatures at a time when light signaling
is waning, when they are in the shade of another plant, or
under any other adverse condition due to climate change?
To maintain optimal growth potential, coordinated adjust-
ments in morphology are needed in response to these perhaps
conflicting external signals, likely necessitating a fine-tuning
mechanism to coordinate the effects of light and temperature
on plant growth. The findings mentioned above indicate that
crosstalk between light and temperature signaling occurs at
multiple points to coordinately regulate plant development.
Plants use photoreceptors, light signal transduction factors,
and similar transcription/post-transcriptional regulatory mech-
anisms to adjust the circadian clock and phytohormone levels,
allowing them to respond in a timely manner or protect
themselves from changing light and temperature conditions
and reach the reproductive stage (Figures 1 and 2).
Identifying the components and detailed molecular mech-
anisms of this integration process will be instrumental in
better understanding plant adaptation skills. We anticipate
that exploring the following three research questions will so-
lidify our views of light and temperature responses.
First, both light and temperature appear to affect the con-
version of phys between their active and inactive forms, but
we do not know whether the underlying molecular activa-
tion mechanism of these two signals is the same. Higher
temperatures elicit different PB dynamics from those ob-
served upon exposure to shade (Hahm et al., 2020).
Li et al.
Whether the highly conserved CRYs also function as ther-
mosensors (like phys) will need to be addressed.
Second, although several potential thermosensors have
been described, their critical thresholds and active ranges of
Downloaded from https://academic.oup.com/plcell/advance-article/doi/10.1093/plcell/koab302/6460828 by Sveriges Lantbruksuniversitet user on 18 December 2021
temperature sensing will need to be investigated. How do
these different sensors recognize and distinguish light and
temperature signals? The downstream effectors and mecha-
nisms specific to each pathway will also need to be explored
in detail.
Finally, it is unknown whether temperature or light sens-
ing and responses are universal processes that take place
uniformly and systematically throughout all plant organs.
Both light and temperature are unlikely to have the same
effects in different plant cells or organs. We already know
that temperature attenuates phyB signaling to inhibit hypo-
cotyl growth but enhances phyB signaling to promote coty-
ledon expansion (Hahm et al., 2020). Epidermis-specific
expression of PIF4 coordinates thermoresponsive growth,
which is inhibited by epidermal phyB, while vasculature-
specific expression of PIF4 has no effect on hypocotyl
growth (Kim et al., 2020b). Shade-induced activation of PIF
expression in leaves increases auxin levels in this tissue;
auxin is then transported to the stem to induce stem elon-
gation (Bellstaedt et al., 2019). HY5 acts as a key factor in
root thermomorphogenesis by directly controlling the ex-
pression of many auxin and BR pathway-related genes
(Gaillochet et al., 2020; Lee et al., 2021). These findings point
to the existence of tissue/organ-specific signaling circuitry.
How these signals are perceived or transmitted by different
cells, as well as between belowground and aboveground
plant organs, is unclear. The body of work already amassed
and what is yet to come will help us understand the mecha-
nisms by which these sophisticated regulatory systems are
integrated.
Acknowledgments
The authors apologize for not citing all relevant articles due
to space limitations. The authors thank Drs Zhiwei Zhao,
Libang Ma, Yawen Liu, Fan Feng, and Yuhan Hao for helpful
discussions and sharing unpublished data.
Funding
The authors’ laboratory is supported in part by the National
Natural Science Foundation of China (31825004, 31721001,
31730009 to H.L.), the Strategic Priority Research Program of
the Chinese Academy of Sciences to H.L. (XDB27030000),
the Program of Shanghai Academic Research Leader to H.L.
(19XD1404400), and the Foundation of Youth Innovation
Promotion Association of the Chinese Academy of Sciences
(to X.L.).
Conflict of interest statement. We declare that we have no
conflict of interest.
 Light and temperature-regulated development
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