Available online at www.sciencedirect.com 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 (2022) Edited by Dr. Stefanie Sprunck, Dr. Claus Schwechheimer and Dr. Miyo Morita For complete overview of the section, please refer the article collection Cell biology and cell signalling (2022) Available online 27 May 2022 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 www.sciencedirect.com
fitness. Morphological acclimation responses to temperature elevation below damaging heat stress levels 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. Current Opinion in Plant Biology 2022, 68:102231
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).
Firstly, ELF3 acts as a subunit in the evening complex (EC) of the circadian clock, which restricts PIF4 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) www.sciencedirect.com
[31] (Figure 1b). PCH1 acts to stabilise active Pfr. phyB PBs in the pch1 mutant background are smaller and 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 Current Opinion in Plant Biology 2022, 68:102231
close to the translation initiation site. This hairpin structure serves as an RNA thermometer by altering its 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 Current Opinion in Plant Biology 2022, 68:102231
include BZR1 [18], and three members of the TEOSINTE BRANCHED 1/CYCLOIDEA/PCF (TCP) 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 temperatureregulated 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 FARRED 1 (HFR1), indicating that HFR1 likely recruits HDA15 to targets to control their expression at lower temperatures [47] (Figure 1c). The regulation of H2A.Znucleosome 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 www.sciencedirect.com
histone H3K27 demethylase RELATIVE OF EARLY 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 www.sciencedirect.com
genes [22]. As such, they form a negative feedback loop 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 Current Opinion in Plant Biology 2022, 68:102231
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).
authors identified PIN-LIKES 6 (PILS6) as a repressor 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 www.sciencedirect.com
thus have pleiotropic effects when targeted for changing 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.
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.