Thermosensing and thermal responses in plants.

Thermosensors have been identified in plants in recent years. Understanding how plants sense and respond to rising temperatures is of utmost importance currently in terms of global warming and its actual and potential impact on us. This forum explores the recent understanding of plant thermosensing and thermal responses.

Auxin-dependent regulation of cell division rates governs root thermomorphogenesis.

Roots are highly plastic organs enabling plants to adapt to a changing below-ground environment. In addition to abiotic factors like nutrients or mechanical resistance, plant roots also respond to temperature variation. Below the heat stress threshold, Arabidopsis thaliana seedlings react to elevated temperature by promoting primary root growth, possibly to reach deeper soil regions with potentially better water saturation. While above-ground thermomorphogenesis is enabled by thermo-sensitive cell elongation, it was unknown how temperature modulates root growth. We here show that roots are able to sense and respond to elevated temperature independently of shoot-derived signals. This response is mediated by a yet unknown root thermosensor that employs auxin as a messenger to relay temperature signals to the cell cycle. Growth promotion is achieved primarily by increasing cell division rates in the root apical meristem, depending on de novo local auxin biosynthesis and temperature-sensitive organization of the polar auxin transport system. Hence, the primary cellular target of elevated ambient temperature differs fundamentally between root and shoot tissues, while the messenger auxin remains the same.

Warm temperature-triggered developmental reprogramming requires VIL1-mediated, genome-wide H3K27me3 accumulation in Arabidopsis.

Changes in ambient temperature immensely affect developmental programs in many species. Plants adapt to high ambient growth temperature in part by vegetative and reproductive developmental reprogramming, known as thermo-morphogenesis. Thermo-morphogenesis is accompanied by massive changes in the transcriptome upon temperature change. Here, we show that transcriptome changes induced by warm ambient temperature require VERNALIZATION INSENSITIVE 3-LIKE 1 (VIL1), a facultative component of the Polycomb repressive complex PRC2, in Arabidopsis. Warm growth temperature elicits genome-wide accumulation of H3K27me3 and VIL1 is necessary for the warm temperature-mediated accumulation of H3K27me3. Consistent with its role as a mediator of thermo-morphogenesis, loss of function of VIL1 results in hypo-responsiveness to warm ambient temperature. Our results show that VIL1 is a major chromatin regulator in responses to high ambient temperature.

Delta-5 elongase knockout reduces docosahexaenoic acid and lipid synthesis and increases heat sensitivity in a diatom.

Recent global marine lipidomic analysis reveals a strong relationship between ocean temperature and phytoplanktonic abundance of omega-3 long-chain polyunsaturated fatty acids (LC-PUFAs), especially eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), which are essential for human nutrition and primarily sourced from phytoplankton in marine food webs. In phytoplanktonic organisms, EPA may play a major role in regulating the phase transition temperature of membranes, while the function of DHA remains unexplored. In the oleaginous diatom Phaeodactylum tricornutum, DHA is distributed mainly on extraplastidial phospholipids, which is very different from the EPA enriched in thylakoid lipids. Here, CRISPR/Cas9-mediated knockout of delta-5 elongase (ptELO5a), which encodes a delta-5 elongase (ELO5) catalyzing the elongation of EPA to synthesize DHA, led to a substantial interruption of DHA synthesis in P. tricornutum. The ptELO5a mutants showed some alterations in transcriptome and glycerolipidomes, including membrane lipids and triacylglycerols under normal temperature (22°C), and were more sensitive to elevated temperature (28°C) than wild type. We conclude that PtELO5a-mediated synthesis of small amounts of DHA has indispensable functions in regulating membrane lipids, indirectly contributing to storage lipid accumulation, and maintaining thermomorphogenesis in P. tricornutum. This study also highlights the significance of DHA synthesis and lipid composition for environmental adaptation of P. tricornutum.

Integrative phenotyping analyses reveal the relevance of the phyB-PIF4 pathway in Arabidopsis thaliana reproductive organs at high ambient temperature.

BACKGROUND: The increasing ambient temperature significantly impacts plant growth, development, and reproduction. Uncovering the temperature-regulating mechanisms in plants is of high importance, for increasing our fundamental understanding of plant thermomorphogenesis, for its potential in applied science, and for aiding plant breeders in improving plant thermoresilience. Thermomorphogenesis, the developmental response to warm temperatures, has been primarily studied in seedlings and in the regulation of flowering time. PHYTOCHROME B and PHYTOCHROME-INTERACTING FACTORs (PIFs), particularly PIF4, are key components of this response. However, the thermoresponse of other adult vegetative tissues and reproductive structures has not been systematically evaluated, especially concerning the involvement of phyB and PIFs. RESULTS: We screened the temperature responses of the wild type and several phyB-PIF4 pathway Arabidopsis mutant lines in combined and integrative phenotyping platforms for root growth in soil, shoot, inflorescence, and seed. Our findings demonstrate that phyB-PIF4 is generally involved in the relay of temperature signals throughout plant development, including the reproductive stage. Furthermore, we identified correlative responses to high ambient temperature between shoot and root tissues. This integrative and automated phenotyping was complemented by monitoring the changes in transcript levels in reproductive organs. Transcriptomic profiling of the pistils from plants grown under high ambient temperature identified key elements that may provide insight into the molecular mechanisms behind temperature-induced reduced fertilization rate. These include a downregulation of auxin metabolism, upregulation of genes involved auxin signalling, miRNA156 and miRNA160 pathways, and pollen tube attractants. CONCLUSIONS: Our findings demonstrate that phyB-PIF4 involvement in the interpretation of temperature signals is pervasive throughout plant development, including processes directly linked to reproduction.

Phosphoproteome analyses pinpoint the F-box protein SLOW MOTION as a regulator of warm temperature-mediated hypocotyl growth in Arabidopsis.

Hypocotyl elongation is controlled by several signals and is a major characteristic of plants growing in darkness or under warm temperature. While already several molecular mechanisms associated with this process are known, protein degradation and associated E3 ligases have hardly been studied in the context of warm temperature. In a time-course phosphoproteome analysis on Arabidopsis seedlings exposed to control or warm ambient temperature, we observed reduced levels of diverse proteins over time, which could be due to transcription, translation, and/or degradation. In addition, we observed differential phosphorylation of the LRR F-box protein SLOMO MOTION (SLOMO) at two serine residues. We demonstrate that SLOMO is a negative regulator of hypocotyl growth, also under warm temperature conditions, and protein-protein interaction studies revealed possible interactors of SLOMO, such as MKK5, DWF1, and NCED4. We identified DWF1 as a likely SLOMO substrate and a regulator of warm temperature-mediated hypocotyl growth. We propose that warm temperature-mediated regulation of SLOMO activity controls the abundance of hypocotyl growth regulators, such as DWF1, through ubiquitin-mediated degradation.

Too hot to handle: temperature-induced plasticity influences pollinator behaviour and plant fitness.

Increased temperature can induce plastic changes in many plant traits. However, little is known about how these changes affect plant interactions with insect pollinators and herbivores, and what the consequences for plant fitness and selection are. We grew fast-cycling Brassica rapa plants at two temperatures (ambient and increased temperature) and phenotyped them (floral traits, scent, colour and glucosinolates). We then exposed plants to both pollinators (Bombus terrestris) and pollinating herbivores (Pieris rapae). We measured flower visitation, oviposition of P. rapae, herbivore development and seed output. Plants in the hot environment produced more but smaller flowers, with lower UV reflectance and emitted a different volatile blend with overall lower volatile emission. Moreover, these plants received fewer first-choice visits by bumblebees and butterflies, and fewer flower visits by butterflies. Seed production was lower in hot environment plants, both because of a reduction in flower fertility due to temperature and because of the reduced visitation of pollinators. The selection on plant traits changed in strength and direction between temperatures. Our study highlights an important mechanism by which global warming can change plant-pollinator interactions and negatively impact plant fitness, as well as potentially alter plant evolution through changes in phenotypic selection.

Contrasting and conserved roles of NPR pathways in diverged land plant lineages.

The NPR proteins function as salicylic acid (SA) receptors in Arabidopsis thaliana. AtNPR1 plays a central role in SA-induced transcriptional reprogramming whereby positively regulates SA-mediated defense. NPRs are found in the genomes of nearly all land plants. However, we know little about the molecular functions and physiological roles of NPRs in most plant species. We conducted phylogenetic and alignment analyses of NPRs from 68 species covering the significant lineages of land plants. To investigate NPR functions in bryophyte lineages, we generated and characterized NPR loss-of-function mutants in the liverwort Marchantia polymorpha. Brassicaceae NPR1-like proteins have characteristically gained or lost functional residues identified in AtNPRs, pointing to the possibility of a unique evolutionary trajectory for the Brassicaceae NPR1-like proteins. We find that the only NPR in M. polymorpha, MpNPR, is not the master regulator of SA-induced transcriptional reprogramming and negatively regulates bacterial resistance in this species. The Mpnpr transcriptome suggested roles of MpNPR in heat and far-red light responses. We identify both Mpnpr and Atnpr1-1 display enhanced thermomorphogenesis. Interspecies complementation analysis indicated that the molecular properties of AtNPR1 and MpNPR are partially conserved. We further show that MpNPR has SA-binding activity. NPRs and NPR-associated pathways have evolved distinctively in diverged land plant lineages to cope with different terrestrial environments.

HOP stabilizes the HSFA1a and plays a main role in the onset of thermomorphogenesis.

Living organisms have the capacity to respond to environmental stimuli, including warm conditions. Upon sensing mild temperature, plants launch a transcriptional response that promotes morphological changes, globally known as thermomorphogenesis. This response is orchestrated by different hormonal networks and by the activity of different transcription factors, including the heat shock factor A1 (HSFA1) family. Members of this family interact with heat shock protein 70 (HSP70) and heat shock protein 90 (HSP90); however, the effect of this binding on the regulation of HSFA1 activity or of the role of cochaperones, such as the HSP70-HSP90 organizing protein (HOP) on HSFA1 regulation, remains unknown. Here, we show that AtHOPs are involved in the folding and stabilization of the HSFA1a and are required for the onset of the transcriptional response associated to thermomorphogenesis. Our results demonstrate that the three members of the AtHOP family bind in vivo to the HSFA1a and that the expression of multiple HSFA1a-responsive-responsive genes is altered in the hop1 hop2 hop3 mutant under warm temperature. Interestingly, HSFA1a is accumulated at lower levels in the hop1 hop2 hop3 mutant, while control levels are recovered in the presence of the proteasome inhibitor MG132 or the synthetic chaperone tauroursodeoxycholic acid (TUDCA). This uncovers the HSFA1a as a client of HOP complexes in plants and reveals the participation of HOPs in HSFA1a stability.

Molecular dialogue between light and temperature signaling in plants: From perception to thermotolerance.

Light and temperature are the two most variable environmental signals, which significantly regulate plant growth and development. Plants in the natural environment usually encounter warmer temperatures during the day and cooler temperatures at night, suggesting both light and temperature are closely linked signals. Due to global warming, it has become important to understand how light and temperature signaling pathways converge, and regulate plant development. This review outlines diverse mechanisms of light and temperature perception and downstream signaling, with an emphasis on their integration and interconnection. The recent research has highlighted the regulation of thermomorphogenesis by photoreceptors and their downstream light signaling proteins under different light conditions, and circadian clock components at warm temperatures. We have made an attempt to comprehensively describe these studies and demonstrate their connection with plant developmental responses. We have also explained how gene signaling pathways of light and thermomorphogenesis, are interconnected with HSR-mediated thermotolerance, which reveals new avenues to manipulate plants for climate resilience. In addition, the role of sugars as signaling molecules between light and temperature is also highlighted. Thus, we envisage that such detailed knowledge will enhance the understanding of how plants perceive light and temperature cues simultaneously and bring about responses that help in their adaptation.

The circadian clock and thermal regulation in plants: novel insights into the role of positive circadian clock regulators in temperature responses.

The impact of rising global temperatures on crop yields is a serious concern, and the development of heat-resistant crop varieties is crucial for mitigating the effects of climate change on agriculture. To achieve this, a better understanding of the molecular basis of the thermal responses of plants is necessary. The circadian clock plays a central role in modulating plant biology in synchrony with environmental changes, including temperature fluctuations. Recent studies have uncovered the role of transcriptional activators of the core circadian network in plant temperature responses. This expert view highlights key novel findings regarding the role of the RVE and LNK gene families in controlling gene expression patterns and plant growth under different temperature conditions, ranging from regular diurnal oscillations to extreme stress temperatures. These findings reinforce the essential role of the circadian clock in plant adaptation to changing temperatures and provide a basis for future studies on crop improvement.

Plants and global warming: challenges and strategies for a warming world.

KEY MESSAGE: In this review, we made an attempt to create a holistic picture of plant response to a rising temperature environment and its impact by covering all aspects from temperature perception to thermotolerance. This comprehensive account describing the molecular mechanisms orchestrating these responses and potential mitigation strategies will be helpful for understanding the impact of global warming on plant life. Organisms need to constantly recalibrate development and physiology in response to changes in their environment. Climate change-associated global warming is amplifying the intensity and periodicity of these changes. Being sessile, plants are particularly vulnerable to variations happening around them. These changes can cause structural, metabolomic, and physiological perturbations, leading to alterations in the growth program and in extreme cases, plant death. In general, plants have a remarkable ability to respond to these challenges, supported by an elaborate mechanism to sense and respond to external changes. Once perceived, plants integrate these signals into the growth program so that their development and physiology can be modulated befittingly. This multifaceted signaling network, which helps plants to establish acclimation and survival responses enabled their extensive geographical distribution. Temperature is one of the key environmental variables that affect all aspects of plant life. Over the years, our knowledge of how plants perceive temperature and how they respond to heat stress has improved significantly. However, a comprehensive mechanistic understanding of the process still largely elusive. This review explores how an increase in the global surface temperature detrimentally affects plant survival and productivity and discusses current understanding of plant responses to high temperature (HT) and underlying mechanisms. We also highlighted potential resilience attributes that can be utilized to mitigate the impact of global warming.

Heat Shock Factor A1s are required for phytochrome-interacting factor 4-mediated thermomorphogenesis in Arabidopsis.

Thermomorphogenesis and the heat shock (HS) response are distinct thermal responses in plants that are regulated by PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) and HEAT SHOCK FACTOR A1s (HSFA1s), respectively. Little is known about whether these responses are interconnected and whether they are activated by similar mechanisms. An analysis of transcriptome dynamics in response to warm temperature (28°C) treatment revealed that 30 min of exposure activated the expression of a subset of HSFA1 target genes in Arabidopsis thaliana. Meanwhile, a loss-of-function HSFA1 quadruple mutant (hsfa1-cq) was insensitive to warm temperature-induced hypocotyl growth. In hsfa1-cq plants grown at 28°C, the protein and transcript levels of PIF4 were greatly reduced, and the circadian rhythm of many thermomorphogenesis-related genes (including PIF4) was disturbed. Additionally, the nuclear localization of HSFA1s and the binding of HSFA1d to the PIF4 promoter increased following warm temperature exposure, whereas PIF4 overexpression in hsfa1-cq partially rescued the altered warm temperature-induced hypocotyl growth of the mutant. Taken together, these results suggest that HSFA1s are required for PIF4 accumulation at a warm temperature, and they establish a central role for HSFA1s in regulating both thermomorphogenesis and HS responses in Arabidopsis.

Transcriptome analysis of thermomorphogenesis in ovules and during early seed development in Brassica napus.

BACKGROUND: Plant sexual reproduction is highly sensitive to elevated ambient temperatures, impacting seed development and production. We previously phenotyped this effect on three rapeseed cultivars (DH12075, Topas DH4079, and Westar). This work describes the transcriptional response associated with the phenotypic changes induced by heat stress during early seed development in Brassica napus. RESULTS: We compared the differential transcriptional response in unfertilized ovules and seeds bearing embryos at 8-cell and globular developmental stages of the three cultivars exposed to high temperatures. We identified that all tissues and cultivars shared a common transcriptional response with the upregulation of genes linked to heat stress, protein folding and binding to heat shock proteins, and the downregulation of cell metabolism. The comparative analysis identified an enrichment for a response to reactive oxygen species (ROS) in the heat-tolerant cultivar Topas, correlating with the phenotypic changes. The highest heat-induced transcriptional response in Topas seeds was detected for genes encoding various peroxidases, temperature-induced lipocalin (TIL1), or protein SAG21/LEA5. On the contrary, the transcriptional response in the two heat-sensitive cultivars, DH12075 and Westar, was characterized by heat-induced cellular damages with the upregulation of genes involved in the photosynthesis and plant hormone signaling pathways. Particularly, the TIFY/JAZ genes involved in jasmonate signaling were induced by stress, specifically in ovules of heat-sensitive cultivars. Using a weighted gene co-expression network analysis (WGCNA), we identified key modules and hub genes involved in the heat stress response in studied tissues of either heat-tolerant or sensitive cultivars. CONCLUSIONS: Our transcriptional analysis complements a previous phenotyping analysis by characterizing the growth response to elevated temperatures during early seed development and reveals the molecular mechanisms underlying the phenotypic response. The results demonstrated that response to ROS, seed photosynthesis, and hormonal regulation might be the critical factors for stress tolerance in oilseed rape.

Ectopic overexpression of TaHsfA5 promotes thermomorphogenesis in Arabidopsis thaliana and thermotolerance in Oryza sativa.

Heat stress transcription factors (Hsfs) play an important role in regulating the heat stress response in plants. Among the Hsf family members, the group A members act upstream in initiating the response upon sensing heat stress and thus, impart thermotolerance to the plants. In the present study, wheat HsfA5 (TaHsfA5) was found to be one of the Hsfs, which was upregulated both in heat stress and during the recovery period after the stress. TaHsfA5 was found to interact with TaHsfA3 and TaHsfA4, both of which are known to positively regulate the heat stress-responsive genes. Apart from these, TaHsfA5 also interacted with TaHSBP2 protein, whose role has been implicated in attenuating the heat stress response. Further, its heterologous overexpression in Arabidopsis and Oryza sativa promoted thermotolerance in these plants. This indicated that TaHsfA5 positively regulated the heat stress response. Interestingly, the TaHsfA5 overexpression Arabidopsis plants when grown at warm temperatures showed  a hyper-thermomorphogenic response in comparison to the wild-type plants. This was found to be consistent with the higher expression of PIF4 and its target auxin-responsive genes in these transgenics in contrast to the wild-type plants. Thus, these results suggest the involvement of TaHsfA5 both in the heat stress response as well as in the thermomorphogenic response in plants.

HY5 and phytochrome activity modulate shoot-to-root coordination during thermomorphogenesis in Arabidopsis.

Temperature is one of the most impactful environmental factors to which plants adjust their growth and development. Although the regulation of temperature signaling has been extensively investigated for the aerial part of plants, much less is known and understood about how roots sense and modulate their growth in response to fluctuating temperatures. Here, we found that shoot and root growth responses to high ambient temperature are coordinated during early seedling development in Arabidopsis A shoot signaling module that includes HY5, the phytochromes and the PIFs exerts a central function in coupling these growth responses and maintaining auxin levels in the root. In addition to the HY5/PIF-dependent shoot module, a regulatory axis composed of auxin biosynthesis and auxin perception factors controls root responses to high ambient temperature. Taken together, our findings show that shoot and root developmental responses to temperature are tightly coupled during thermomorphogenesis and suggest that roots integrate energy signals with local hormonal inputs.

A competition-attenuation mechanism modulates thermoresponsive growth at warm temperatures in plants.

Global warming has profound impact on growth and development, and plants constantly adjust their internal circadian clock to cope with external environment. However, how clock-associated genes fine-tune thermoresponsive growth in plants is little understood. We found that loss-of-function mutation of REVEILLE5 (RVE5) reduces the expression of circadian gene EARLY FLOWERING 4 (ELF4) in Arabidopsis, and confers accelerated hypocotyl growth under warm-temperature conditions. Both RVE5 and CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) accumulate at warm temperatures and bind to the same EE cis-element presented on ELF4 promoter, but the transcriptional repression activity of RVE5 is weaker than that of CCA1. The binding of CCA1 to ELF4 promoter is enhanced in the rve5-2 mutant at warm temperatures, and overexpression of ELF4 in the rve5-2 mutant background suppresses the rve5-2 mutant phenotype at warm temperatures. Therefore, the transcriptional repressor RVE5 finetunes ELF4 expression via competing at a cis-element with the stronger transcriptional repressor CCA1 at warm temperatures. Such a competition-attenuation mechanism provides a balancing system for modulating the level of ELF4 and thermoresponsive hypocotyl growth under warm-temperature conditions.

Coordinated histone variant H2A.Z eviction and H3.3 deposition control plant thermomorphogenesis.

Plants can sense temperature changes and adjust their development and morphology accordingly in a process called thermomorphogenesis. This phenotypic plasticity implies complex mechanisms regulating gene expression reprogramming in response to environmental alteration. Histone variants often associate with specific chromatin states; yet, how their deposition/eviction modulates transcriptional changes induced by environmental cues remains elusive. In Arabidopsis thaliana, temperature elevation-induced transcriptional activation at thermo-responsive genes entails the chromatin eviction of a histone variant H2A.Z by INO80, which is recruited to these loci via interacting with a key thermomorphogenesis regulator PIF4. Here, we show that both INO80 and the deposition chaperones of another histone variant H3.3 associate with ELF7, a critical component of the transcription elongator PAF1 complex. H3.3 promotes thermomorphogenesis and the high temperature-enhanced RNA Pol II transcription at PIF4 targets, and it is broadly required for the H2A.Z removal-induced gene activation. Reciprocally, INO80 and ELF7 regulate H3.3 deposition, and are necessary for the high temperature-induced H3.3 enrichment at PIF4 targets. Our findings demonstrate close coordination between H2A.Z eviction and H3.3 deposition in gene activation induced by high temperature, and pinpoint the importance of histone variants dynamics in transcriptional regulation.

HSP90s are required for hypocotyl elongation during skotomorphogenesis and thermomorphogenesis via the COP1-ELF3-PIF4 pathway in Arabidopsis.

Light and temperature are two key environmental signals that share several molecular components that, in turn, regulate plant growth. Darkness and high ambient temperatures promote skoto- and thermomorphogenesis, including stem elongation. Heat shock proteins 90 (HSP90s) facilitate the adaptation of organisms to various adverse environmental stimuli. Here, we showed that HSP90s are required for hypocotyl elongation during both skoto- and thermomorphogenesis. When HSP90s activities are impaired by the knockdown of HSP90s expression or the application of HSP90 inhibitors, the expression levels and protein abundance of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) markedly decreased. EARLY FLOWERING 3 (ELF3) deficiency was resistant to the inhibition of HSP90s activities. Furthermore, HSP90s interacted with and destabilized ELF3. In the CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) mutant, the changes in endogenous PIF4 and ELF3 protein levels caused by the inhibition of HSP90s activities were abolished. HSP90s enhanced the interaction between COP1 and ELF3, reduced ELF3 functional effects on PIF4 and modulated hypocotyl elongation during skoto- and thermomorphogenesis. Our results indicated that HSP90s participate in light and temperature signalling via the COP1-ELF3-PIF4 module to regulate hypocotyl growth in changing environments.

Glutathione-mediated thermomorphogenesis and heat stress responses in Arabidopsis thaliana.

In the context of climate change, the global rise of temperature and intense heat waves affect plant development and productivity. Among the molecular perturbations that high temperature induces in living cells is the accumulation of reactive oxygen species (ROS), which perturbs the cellular redox state. In plants, the dynamics of the cellular and subcellular redox state have been poorly investigated under high temperature. Glutathione plays a major role in maintaining the cellular redox state. We investigated its contribution in adaptation of Arabidopsis thaliana to contrasting high temperature regimes: high ambient temperature inducing thermomorphogenesis and heat stress affecting plant viability. Using the genetically encoded redox marker roGFP2, we show that high temperature regimes lead to cytoplasmic and nuclear oxidation and impact the glutathione pool. This pool is restored within a few hours, which probably contributes to plant adaptation to high temperatures. Moreover, low glutathione mutants fail to adapt to heat stress and to induce thermomorphogenesis, suggesting that glutathione is involved in both heat adaptation mechanisms. We also evaluate the transcriptomic signature in the two high temperature regimes and identified gene expression deviations in low glutathione mutants, which might contribute to their sensitivity to high temperature. Thus, we define glutathione as a major player in the adaptation of Arabidopsis to contrasting high temperature regimes.