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Current Opinion in
ScienceDirect
Plant Biology
Recent advances in understanding
thermomorphogenesis signaling
Carolin Delker1, Marcel Quint1 and Philip A. Wigge2,3
Abstract
Plants show remarkable phenotypic plasticity and are able to
adjust their morphology and development to diverse environmental stimuli. Morphological acclimation responses to
elevated ambient temperatures are collectively termed thermomorphogenesis. In Arabidopsis thaliana, morphological
changes are coordinated to a large extent by the transcription
factor PHYTOCHROME-INTERACTING FACTOR 4 (PIF4),
which in turn is regulated by several thermosensing mechanisms and modulators. Here, we review recent advances in the
identification of factors that regulate thermomorphogenesis of
Arabidopsis seedlings by affecting PIF4 expression and PIF4
activity. We summarize newly identified thermosensing mechanisms and highlight work on the emerging topic of organ- and
tissue-specificity in the regulation of thermomorphogenesis.
Addresses
1
Institute of Agricultural and Nutritional Sciences, Martin Luther University Halle-Wittenberg, Betty-Heimann-Str. 5, D-06120, Halle (Saale),
Germany
2
Leibniz-Institut für Gemüse- und Zierpflanzenbau, Großbeeren,
Germany
3
Institute of Biochemistry and Biology, University of Potsdam, Potsdam, Germany
Corresponding authors: Delker, Carolin (carolin.delker@landw.unihalle.de); Wigge, Philip A. (wigge@igzev.de)
Current Opinion in Plant Biology 2022, 68:102231
This review comes from a themed issue on Cell biology and cell
signalling
Edited by Stefanie Sprunck, Claus Schwechheimer and Miyo Morita
For a complete overview see the Issue and the Editorial
Available online xxx
https://doi.org/10.1016/j.pbi.2022.102231
1369-5266/© 2022 The Authors. Published by Elsevier Ltd. This is an
open access article under the CC BY license (http://creativecommons.
org/licenses/by/4.0/).
Thermomorphogenesis and the core
signaling pathway
Climate change and ongoing extreme weather events
are increasingly perturbing ecosystems and agriculture
[1]. Plants sense and integrate temperature information into their growth and development to maximise
fitness. Morphological acclimation responses to temperature elevation below damaging heat stress levels
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are termed thermomorphogenesis [2], which include
the elongation of hypocotyls, stems, petioles and
roots, leaf hyponasty and a reduction in leaf blade
size (reviewed by Quint et al., Casal et al. [3,4]). In
Arabidopsis, shoot thermomorphogenesis results in
an open rosette structure, which promotes efficient
leaf cooling and thus may aid in maintaining photosynthetic efficiency under warm temperatures [5,6]. A
central regulator of plant thermomorphogenesis is
the transcription factor (TF) PHYTOCHROMEINTERACTING FACTOR 4 (PIF4 [7,8]), which orchestrates transcriptome reprogramming in response to
elevated ambient temperatures in Arabidopsis [9].
Warm temperatures affect PIF4 on multiple levels,
including PIF4 expression (Figure 1a), protein levels
(Figure 1b), and its function as a transcription factor by
altering chromatin states (Figure 1c) and promotor
binding (Figure 1d). While some regulatory components in thermomorphogenesis may potentially act
independently of PIF4 (Figure 1e), the core signaling
pathway is dominated by PIF4 and other factors that
regulate plant growth and development in response to
temperature as well as different light conditions.
Phytochrome B (phyB) and other light sensors have
been shown to act as thermosensors in addition to
sensing specific wave lengths of the light spectrum
(reviewed by Bouré et al. [10]). Elevated ambient
temperatures promote the conversion of active phyB to
its inactive Pr configuration [11,12] (see details below).
Active phyB inhibits PIF4 function and promotes its
degradation via phosphorylation [13] (Figure 1b). The
warm temperature-mediated conversion of phyB to the
inactive Pr conformation relieves PIF4 repression
[12]. Furthermore, essential regulators of photomorphogenesis such as the DE-ETIOLATED 1 (DET1)CONSTITUTIVE
PHOTOMORPHOGENIC
1
(COP1)-SUPPRESSOR OF PHYA (SPA) pathway have
been shown to promote thermomorphogenesis, in part
by targeting the transcription factor ELONGATED
HYPOCOTYL 5 (HY5) for proteasomal degradation
[2,14,15] (Figure 1a, d). HY5 antagonizes thermomorphogenesis by repressing PIF4 expression (Figure 1a)
and by competing for PIF binding sites (i.e. G-boxes)
in target promoters [2,14] (Figure 1d). EARLY
FLOWERING 3 (ELF3) also has a prominent role
in restricting PIF4-mediated thermomorphogenesis.
Firstly, ELF3 acts as a subunit in the evening complex
(EC) of the circadian clock, which restricts PIF4
Current Opinion in Plant Biology 2022, 68:102231
2 Cell biology and cell signalling
Figure 1
Molecular mechanism underlying Arabidopsis thaliana shoot thermomorphogenesis. Several distinct mechanisms detect warm temperatures in
the shoot which results in the induction of PIF4 expression (a), promoting PIF4 stability (b), altering chromatin state (c) and PIF4 function as a transcriptional regulator (d). Temperature sensing occurs on different levels: warm temperatures cause reversible liquid–liquid phase separation of the
evening complex subunit ELF3, which de-represses PIF4 expression (a), the thermal reversion of phyB from the active Pfr to the inactive Pr conformation
(b), and alters the RNA secondary structure of transcripts, in particular of mRNA encoding PIF7 which acts in concert with PIF4 to regulate target genes
(d). Numerous other factors are influenced by temperature, e.g., the DET-COP1-SPA-HY5 cascade (a,d) and chromatin remodeling factors such as HDAs
and INO80 (c, d) but it is as of yet unclear, how temperature affects these components mechanistically. A recently identified plasma membrane-localized
kinase (TOT3) is also involved in the regulation of thermomorphogenesis, putatively by modulation of BR signaling (e). Ultimately, PIF4/PIF7-mediated
regulation of temperature-responsive genes which include auxin biosynthesis genes initiates a signaling cascade to promote cell elongation in petioles
and hypocotyls, resulting in the characterisitc thermomorphogenesis model phenotypes (f). Red and blue colors indicate the function of components at
higher or lower ambient temperature, respectively. Solid lines show experimentally verified connections, dotted lines indicate that the exact mechanism or
connection is not yet elucidated. Abbreviations: FUS3-COMPLEMENTING GENE 2 (AFC2), brassinosteroids (BR), BRASSINAZOLE-RESISTANT 1
(BZR1), CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1), DE-ETIOLATED 1 (DET1), EARLY FLOWERING (ELF), HISTONE DEACETYLASE
(HDA), HECATE 2 (HEC2), LONG HYPOCOTYL IN FAR-RED (HFR1), HERMERA (HMR), ELONGATED HYPOCOTYL 5 (HY5), INO80, LUX
ARRYTHMO (LUX), PHOTOPERIODIC CONTROL OF HYPOCOTYL 1 (PCH1), phytochrome B (phyB), PHYTOCHROME INTERACTING FACTOR
(PIF), PICKLE (PKL), plasma membrane (pm), POWERDRESS (PWR), REGULATOR OF CHLOROPLAST BIOGENESIS (RCB), RELATIVE OF EARLY
FLOWERING 6 (REF6), TEOSINTE BRANCHED 1/CYCLOIDEA/PCF (TCP5), TARGET OF TEMPERATURE 3 (TOT3), SUPPRESSOR OF PHYA
(SPA), XB3 ORTHOLOG 1 IN ARABIDOPSIS THALIANA (XBAT31).
Current Opinion in Plant Biology 2022, 68:102231
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Thermomorphogenesis Delker et al.
expression in a photoperiod-dependent manner [16]
(Figure 1a). Secondly, ELF3 can interact with PIF4
independently of the EC which restricts PIF4 function
as a transcriptional regulator [17]. PIF4 directly activates auxin biosynthesis, which either directly or indirectly induces brassinosteroid (BR) biosynthesis and
signaling [18,19] to promote elongation growth
(Figure 1f). Recently, PIF7 was identified as an
important regulator of thermomorphogenesis that also
contributes to temperature sensing [20,21], whereas
other PIF family members have a relatively weak
contribution to thermomorphogenesis [22].
In this review, we provide a concise overview of recent
findings in the areas of plant temperature sensing,
PIF4 regulation, and the emerging importance of
tissue- and organ-specific analyses of temperature
sensing and responses. For more details on other aspects of thermomorphogenesis, we refer the reader to
recent reviews [10,23e28].
Temperature sensing: Sensors and
modulators
Diverse molecular mechanisms enable the plant to
sense changes in ambient temperature and to coordinate
the response with other internal and external stimuli.
Several photosensors serve the dual purpose of sensing
specific wave lengths of the light spectrum and sensing
ambient temperature changes (reviewed by Hayes et al.
[29]) among which phyB is the best studied, so far. Red
light-mediated phyB photoconversion to the active Pfr
conformation can occur within milliseconds, while
temperature signals act through modifying the dark
reversion rate to the inactive Pr form which occurs over
several hours [11,12] (Figure 1b). Activation of phyB can
be observed by the formation of bright speckles or
photobodies (PBs) of fluorescent protein (FP)-labeled
phyB in the nucleus, which are indicative of the amount
of active Pfr phyB. Analysis of phyB PBs in response to
temperature reveals interesting parallels and differences
to light signaling. While FR light treatment results in a
very rapid loss of PBs, increasing the temperature from
12 C to 27 C causes a more gradual reduction in the
number of PBs in hypocotyl and cotyledon cells [30].
Hahm et al. [30] also observed distinct forms of PBs,
associated with nucleoli or separate from the nucleoli.
While the specific function of nucleolar and nonnucleolar PBs remains to be elucidated, the nonnucleolar PBs are the most thermoresponsive [30].
Furthermore, PBs from different tissues can show
different temperature response dynamics, pointing to
mechanisms that can potentially fine-tune the temperature response in a tissue specific manner. An important
factor that regulates phyB dark reversion is PHOTOPERIODIC CONTROL OF HYPOCOTYL 1 (PCH1)
[31] (Figure 1b). PCH1 acts to stabilise active Pfr. phyB
PBs in the pch1 mutant background are smaller and
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3
insensitive to temperature. Consistent with the role of
PCH1 in stabilising active Pfr phyB, pch1 mutants have
an exaggerated hypocotyl response to warm temperature
[31]. Protein levels of PCH1 are lower at high temperature, suggesting it may act to enhance the effect of
thermal reversion on phyB. Controlling the stability and
expression levels of PCH1 provides a mechanism to alter
the thermal responsiveness of phyB in a tissue-specific
and temporal fashion. These observations are consistent with PCH1 being a modulator of temperature
sensing rather than being a sensor itself.
A major theme emerging from thermomorphogenesis
research in recent years has been the remarkable degree
of interconnectedness with light signalling and circadian
clock pathways both of which modulate the temperature
response (reviewed by Li et al., Hayes et al. [10,29]). A
key player in light signalling is COP1, and cop1 mutants
show a reduced thermomorphogenesis hypocotyl
phenotype [2,14,15,32]. COP1 interacts with numerous
negative regulators of PIF4 (e.g. HY5, ELF3 and phyB,
reviewed by Ponnu et al. [33]) and is essential to
transmit the thermosignal into the PIF4 pathway
[15,32]. As such, COP1 can be considered as a sensing
and signaling modulator that has the capacity to adjust
temperature responses in accordance with other signals (Figure 1a, d).
Another thermosensory mechanism is provided by a
prion-like domain in ELF3. This subdomain, which is
found in ELF3 proteins of many but not all plant species, is rich in glutamine residues. The prion-like
domain causes ELF3 to form reversible aggregates by
liquideliquid phase separation in higher ambient temperature [34] (Figure 1a), thereby depleting active
ELF3 from integrating into the evening complex or
inhibiting PIF4 function. In addition to this general
thermosensory function, which is restricted to plants
that contain an ELF3 prion-like domain, ELF3 is
important for the transmission of temperature cues to
the circadian clock. It acts as a Zeitnehmer for light and
temperature sensing of the central oscillator, thereby
gating thermoresponsive behaviours such as rhythmic
growth and cotyledon movement [35,36]. ELF3 itself is
targeted for degradation by the E3 ubiquitin ligase XB3
ORTHOLOG 1 IN ARABIDOPSIS THALIANA
(XBAT31), which acts as a positive factor in the thermomorphogenesis pathway [37] (Figure 1a).
Another recently discovered sensing mechanism that
contributes to thermomorphogenesis is based on temperature effects on RNA secondary structures. It may
be one of the most basal or ancient mechanisms of
thermosensing, as it is also found in animals, bacteria
and viruses [38]. Chung et al. [21] have identified a
hairpin structure in the 50 region of the PIF7 transcript
close to the translation initiation site. This hairpin
structure serves as an RNA thermometer by altering its
Current Opinion in Plant Biology 2022, 68:102231
4 Cell biology and cell signalling
conformation in warmer temperatures which then improves its translation efficiency and results in higher
PIF7 protein levels in warm temperatures during the
daytime [21] (Figure 1d). As PIF7 seems to act in
concert with PIF4, putatively by forming heterodimers
that regulate thermomorphogenesis-relevant genes
[20], this RNA-based thermosensor directly connects
to the central regulatory hub of thermomorphogenesis
(Figure 1d). Similar hairpin structures were also identified in other transcripts (e.g. HEAT SHOCK FACTOR
2 [21]), indicating that this mechanism may also
contribute to processes other than the core thermomorphogenesis pathway.
While membrane temperature signalling has been
shown to be important in cyanobacteria and animals,
the presence of membrane-localised temperature
transducers is less well understood in plants. The
identification of a plasma membrane-localised kinase is
therefore of interest. TARGET OF TEMPERATURE 3
(TOT3) was identified in a phosphoproteomic screen
for factors that rapidly change in response to 27 C
[39]. Interestingly, tot3-1 mutants have a reduced
thermomorphogenesis phenotype, and the TOT3
pathway appears genetically to be parallel to the well
established
phyB-ELF3-PIF4
pathway
[39]
(Figure 1e). The authors propose that TOT3 signalling
may transmit warm temperature signals to influence
brassinosteroid signalling, potentially via gating
BRASSINAZOLE-RESISTANT 1 (BZR1) activity.
Temperature regulation of PIF4 expression
The thermosensing and modulating mechanisms
described above primarily converge at the level of PIFs.
PIF4 in particular is regulated on multiple levels in
response to temperature, ranging from transcriptional
activation to protein stability (reviewed by Qui et al.
[23]). Temperature induction of PIF4 is controlled by
the EC of the circadian clock. The EC acts as a transcriptional repressor and its association with DNA is
higher at lower temperatures [40] (Figure 1a).
Temperature-mediated phase change of ELF3 abolishes
EC activity at high temperatures, enabling target genes
such as PIF4 to be expressed in a photoperioddependent manner [34,41,42]. Under long days, the
clock gene GIGANTEA gates hypocotyl elongation in
response to temperature [43]. HY5 restricts PIF4
expression (Figure 1a) and antagonizes PIF4 function
(Figure 1d) under cold temperatures whereas elevated
temperatures promote HY5 degradation by the DET1COP1-SPA cascade which contributes to a transient
increase in PIF4 expression and activity [2,14,15]
(Figure 1a, d). More recently, the first TFs serving as
positive transcriptional regulators of temperatureinduced PIF4 expression have been identified. These
include BZR1 [18], and three members of the
TEOSINTE BRANCHED 1/CYCLOIDEA/PCF (TCP)
Current Opinion in Plant Biology 2022, 68:102231
family TCP5, TCP13, and TCP17 [44] (Figure 1a).
Apart from inducing PIF4 transcription, TCP5 can
interact with PIF4 to enhance its activity. Furthermore,
PIF4 can bind to its own promoter under high temperatures and induce its expression which creates an
autoregulatory feed-forward loop [22].
Chromatin-related thermomorphogenesis
regulation
The induction of genes in response to warmer ambient
temperature has been shown to involve chromatin
remodeling, even though the exact mechanisms by
which temperature influences these dynamics are still
fairly unresolved. Nucleosomes containing the alternative H2A histone H2A.Z seem to have a particular
relevance for thermomorphogenesis as they are preferentially evicted at elevated temperatures [45]
(Figure 1c, d). Interestingly, the chromatin modifying
enzyme HISTONE DEACETYLASE 9 (HDA9) is
necessary for hypocotyl elongation at elevated temperature, whereas other thermoresponses such as early
flowering are not perturbed [46]. This suggests that
HDA9 affects specific aspects of the temperature
response pathway. HDA9 was shown to trigger
H3K9K14 deacetylation at the YUCCA 8 (YUC8) locus,
leading to its increased expression in elevated temperature [46]. While H2A.Z nucleosomes were depleted
from YUC8 in response to high temperature, this
response was abolished in hda9-1 mutants, demonstrating that deacetylation of these nucleosomes in
response to temperature is an important step in activating gene expression [46] (Figure 1c). In contrast to
HDA9, the histone deacetylase HDA15 has an opposite
role in temperature-regulated gene expression [47]. On
the phenotypic level hda15 mutants show thermomorphogenic phenotypes and up-regulation of thermoresponsive genes already at 20 C. HDA15 interacts with an
antagonist of thermomorphogenesis, LONG HYPOCOTYL IN FAR-RED 1 (HFR1), indicating that HFR1
likely recruits HDA15 to targets to control their
expression at lower temperatures [47] (Figure 1c). The
regulation of H2A.Z-nucleosome occupancy in response
to temperature is also controlled by the INOSITOL
REQUIRING80 (INO80) chromatin remodelling complex [48] (Figure 1d). Ino80 mutants have a greatly
reduced hypocotyl elongation in response to elevated
temperature and are unable to transcriptionally induce
key thermomorphogenesis genes including YUC8 at high
temperature. INO80 interacts with PIF4, indicating a
direct mechanism by which PIF4 recruits INO80 to the
promoters of target genes and induces their expression
by evicting the repressive H2A.Z nucleosomes
[48] (Figure 1d).
An additional connection to chromatin-mediated thermoresponsive gene expression is provided by the histone H3K27 demethylase RELATIVE OF EARLY
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Thermomorphogenesis Delker et al.
FLOWERING 6 (REF6) [49] (Figure 1c). Loss of REF6
function severely inhibits hypocotyl elongation in
elevated temperature, most likely a consequence of the
failure to efficiently induce thermoresponse genes like
GIBBERELLIN 20-OXIDASE (GA20ox2). In summary,
temperature-induced chromatin dynamics modulate
thermomorphogenesis on several levels which include
the regulation of PIF4 expression as well as its function
as a transcriptional regulator of temperature-relevant
target genes.
Temperature-induced regulation of PIF4
function
Numerous proteins affect PIF4 function in addition to
chromatin remodellers. These includes, proteineprotein
interactions as well as posttranslational modifications.
While the phosphorylation of PIF4 by phyB or
BRASSINOSTEROID-INSENSITIVE 2 leads to
PIF degradation via the 26S proteasome [13,50],
temperature-induced phosphorylation of PIF4 by SPAs
rather stabilize PIF4 protein levels while simultaneously
reducing phyB stability [51] (Figure 1b). So far, it is likely
but unclear whether these differential effects are caused
by different phospho-sites in PIF4 and if the stabilizing
phosphorylation affects PIF4 affinity for specific interaction partners or DNA target sequences. PIF4 stability
is also increased by HERMERA (HMR) [52] and the
HMR-interacting protein REGULATOR OF CHLOROPLAST BIOGENESIS [53] (Figure 1b).
PIFs can form both homo- and heterodimers. While
PIF4 is the predominant PIF in thermomorphogenesis,
other PIFs contribute to varying extents [22]. PIF7 is
emerging as a key player, which is emphasised by the
identification of PIF4-PIF7 heterodimers and their role
in the activation of target genes for seedling development [20] (Figure 1d). PIF4 also interacts with other
classes of TFs. The interaction of BZR1, AUXIN
RESPONSE FACTOR 6 (ARF6) and PIF4 (BAP
module) has been proposed as a regulatory entity in
elongation growth such as thermomorphogenesis
(reviewed by Li et al. [54]). While all three (classes) of
transcription factors undoubtedly contribute to the
regulation of thermomorphogenesis, it is as of yet unclear to what extent their physical interaction is
required and if temperature has a direct effect on the
assembly of the BAP complex.
PIF4 function is further regulated by interactions with
several proteins that scavenge active PIF4 to prevent
promoter binding and/or its capacity for transcriptional
regulation. Among these, several HLH/bHLH proteins
regulate PIF4 or PIF7 under varying environmental
stimuli [55,56]. In a thermomorphogenesis context,
HECATE 1 (HEC1) and 2 have recently been identified
as interactors of PIF4 which prevent its binding to target
genes [22]. As such, they form a negative feedback loop
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5
to restrict temperature-induced hypocotyl elongation as
the expression of HEC1 and HEC2 is induced under
warm temperatures. Interestingly, PIF4 protein stability
is increased and decreased in HEC overexpression and
loss-of-function lines, respectively. However, the
amount of PIF protein in this case is not correlated with
thermomorphogenesis phenotypes which are short and
long, respectively [22]. In addition to the scavenging of
PIF4 protein, alternative splicing also contributes to the
attenuation of temperature-induced elongation growth
of the hypocotyl. The ARABIDOPSIS FUSCA3
COMPLEMENTING GENE 2 (AFC2) kinase is
required for temperature-induced alternative splicing in
numerous auxin-relevant transcripts which are regulated
by PIF4 (e.g., ARF6, IAA29, PILS5) [57]. Interestingly,
several of these genes did not show differential
expression in response to temperature. Induction of
alternative splicing may provide an alternate means to
reduce the amount of the respective functional proteins
and thereby contribute to the attenuation of PIF4mediated elongation growth [57].
Tissue- and organ-specific temperature
responses
In comparison to the shoot, root thermomorphogenesis
pathways are less well understood. Interestingly, PIF4
and other PIFs do not appear to be necessary for root
thermomorphogenesis in Arabidopsis seedlings [53]. In
contrast to its function in the shoot, HY5 acts as a positive regulator of root thermomorphogenesis and also
requires phosphorylation by SPAs [58] (Figure 2).
Interestingly, phosphorylated HY5 seems to be less
active while simultaneously being more stable. The
increased stability may counteract the decrease in HY5
activity and thus allow HY5 to promote root elongation
[58]. HY5 has also been proposed to act as a mobile
signal in temperature-mediated inter-organ communication between the shoot and the root [59]. However, as
excised roots behave thermomorphogenic also in the
absence of a shoot [60], it is possible that shoot-root
transfer of HY5 is only of secondary importance.
Possibly, ectopic HY5 expression is induced in the detached root or mobile HY5 from the shoot acts as a
modulator of root thermomorphogenesis. Further
studies will need to clarify these questions.
ELF4 has been implicated as a mobile signal that
transmits temperature information from the root to the
shoot to set the pace of the root clock to enable longer
and shorter circadian periods under cold and warm
temperatures, respectively [61] (Figure 2). Yet, how this
impacts on root thermomorphogenesis remains to
be elucidated.
Another fragment of information on root-specific responses was recently published by Feraru et al. [62]. The
authors identified PIN-LIKES 6 (PILS6) as a repressor
Current Opinion in Plant Biology 2022, 68:102231
6 Cell biology and cell signalling
Figure 2
Tissue- and organ-specific aspects of thermomorphogenesis. Shoot thermomorphogenesis involves independent and inter-dependent temperature
sensing and responses in different tissues and organs. Shoot responses require the phyB-PIF4-IAA cascade to be active in epidermal cells to promote
cell elongation in petioles and hypocotyls. Cotyledon-derived IAA is transported to petioles and hypocotyls where it initiates cell elongation. In petioles,
preferential polar auxin transport to the lower (abaxial) side of the petiole causes asymmetric elongation of cells which leads to thermo-/hyponastic leaf
movement. In hypocotyls, cotyledon-derived auxin induces BR biosynthesis and signaling, which orchestrates cell elongation. GA contributes to interorgan communication between root and shoot. The inactive gibberellin GA12 is transported from the root to the shoot where it is converted to the active
GA4 which contributes to shoot thermomorphogenesis. While the root can, in principle, sense and respond to warm temperatures autonomously, ELF4
and HY5 have been implicated as shoot derived signals that contribute to root thermomorphogenesis. In general, mechanisms involved in root thermomorphogenesis are far less understood. Apart from IAA which is induced by temperature-induced repression of PILS6, BR and ET seem to contribute
to temperature-induced root elongation. In contrast to its role in the shoot, HY5 acts as a positive regulator of root thermomorphogenesis. HY5 is
phosphorylated by SPAs which promotes HY5 stability under warm temperatures. Red and blue colors indicate the function of components at higher or
lower ambient temperature, respectively. Solid lines show experimentally verified connections, whereas dotted lines indicate that the exact mechanism or
connection is not yet elucidated. Abbreviations: brassinosteroids (BR), BRASSINAZOLE-RESISTANT 1 (BZR1), EARLY FLOWERING 4 (ELF4), ethylene
(ET), gibberrellic acid (GA), ELONGATED HYPOCOTYL 5 (HY5), indole-3-acetic acid (IAA), phytochrome B (phyB), PHYTOCHROME INTERACTING
FACTOR 4 (PIF4), PIN-LIKES 6 (PILS6), PIN-FORMED (PIN), SUPPRESSOR OF PHYA (SPA).
Current Opinion in Plant Biology 2022, 68:102231
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Thermomorphogenesis Delker et al.
of root thermomorphogenesis (Figure 2). Warm ambient
temperature destabilizes PILS6, thereby increasing nuclear auxin levels and promoting root elongation [62]. In
addition to auxin, brassinosteroids and ethylene have
also been implicated to regulate root temperature responses (reviewed by Fonseca de Lima et al. [63]).
Phytohormones also play a role in temperature-relevant
inter-organ communication (Figure 2). While gibberellic acid (GA) seems to be involved in root to shoot
signaling that contributes to hypocotyl elongation [64],
auxin transmits warm temperature cues that are sensed
in cotyledons to the hypocotyls to induce elongation
[60]. Petiole elongation and leaf thermonasty similarly
rely on polar auxin transport, primarily to the abaxial side
of the petiole to induce asymmetric induction of elongation [6] (Figure 2). Kim et al. [65] have recently
demonstrated that temperature-induced hypocotyl and
petiole elongation specifically require the activity of the
phyB-PIF4 signaling cascade in the epidermis. Their
analysis of tissue-specific PIF4 expression also indicates
that temperature-induced de-repression of PIF4
expression may actually account for a large proportion of
the hypocotyl thermomorphogenesis response [65].
Conclusions
While thermomorphogenesis has been known for
several decades [66,67], the underlying mechanisms
and pathways are only starting to be understood. Many
key questions about plant temperature responses such
as organ- and tissue-specificities, conservation of
signaling networks among plant species and temperature memory remain open (Box 1). As well as being of
fundamental biological importance, how plants sense
and respond to temperature is key in agriculture, with
global yields of major crops decreasing from 3.2 to 7.4%
for every 1 C increase in temperature [68]. Breeding
climate resilient crops is a major societal challenge,
requiring comprehensive understanding of the underlying mechanisms as well as the required methodological tools. Advances in the areas of genome editing and
synthetic biology offer the longer term perspective of
engineering plants with temperature responses adapted to new climate conditions.
A key bottleneck in applied thermomorphogenesis
research is the selection of appropriate target regulators
and/or mechanisms. While most mechanistic insight has
so far come from studies in the model plant Arabidopsis
thaliana, it is clear that studying temperature responses
in crops and crop models will be essential, since it is
quite likely that the relative roles of different components in temperature sensing pathways may be quite
different. Research so far has shown that many temperature sensors and signalling components are also
major signaling hubs, particularly light signaling and the
circadian clock. This raises the challenge that these may
thus have pleiotropic effects when targeted for changing
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7
temperature responses. Modulators that affect only
specific aspects of the temperature signaling pathway
may thus be particularly suitable candidates for selectively altering temperature behaviour. In addition, the
recently discovered, as well as yet to be described,
thermosensing mechanisms, phase separation, secondary mRNA structure, and light signalling present significant biotechnological potential. Transferring the
respective motifs or domains to other transcripts or
proteins could serve as thermosensitive switches to
modulate various pathways that may aid in the generation of crops capable of improving yield stability in a
global change context.
Box1: Key questions in
thermomorphogenesis research
What
are
the
spatio-temporal
thermomorphogenesis?
specificities
of
Tissue- and organ-specificity in thermomorphogenesis is only
starting to be understood. A good example is the root thermomorphogenesis network, which differs from the shoot. Additionally,
regulators of warm temperature phenotypes in later developmental
stages need to be elucidated to fully understand the complexity of
thermomorphogenesis signaling networks.
Are there other temperature sensing mechanisms that contribute
to thermomorphogenesis?
The recent discovery of an RNA-thermoswitch and liquid–liquid
phase separation highlights the diversity of potential temperature
sensing mechanisms. It is likely therefore that new sensors will be
detected in the coming years. The identification of the membranebound TOT3 as a regulator in thermomorphogenesis implicates
membrane-based thermosensing as an exciting possibility.
What are the molecular mechanisms involved in short-term and
trans-generational temperature memory?
It is well established that plants can establish a sort of “memory” of
previously experienced temperature that can e.g. establish an acquired thermotolerance. While these processes are being investigated, the underlying regulatory networks are far from complete.
Also, if and how thermomorphogenesis regulation connects to
temperature memory is so far not clear.
How conserved are thermomorphogenesis signaling networks/
components among plant species?
Our present understanding of thermomorphogenesis regulation is
dominated by work in Arabidopsis. Applying this knowledge to
generate temperature-resilient crop varieties will require extensive
analysis of the conservation of signaling components or the elucidation of species- or clade-specific thermomorphogenesis regulators that are absent in Arabidopsis. Here, the identification of
monocot-specific regulators may be most relevant to facilitate efficient approaches in improving major staple crops.
Current Opinion in Plant Biology 2022, 68:102231
8 Cell biology and cell signalling
Declaration of competing interest
The authors declare that they have no known competing
financial interests or personal relationships that could
have appeared to influence the work reported in
this paper.
Acknowledgments
We apologize to all authors whose work was not mentioned in this review
due to space limitations. Temperature work in the Quint lab is supported
by the DFG (http://madland.science, DFG priority programme 2237, Qu
141/10e1, Qu 141/3e2) (M.Q.). Temperature work in the Wigge lab is
supported by the European Research Council (Adv 101021246) and the
Leibniz Association.
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