AFP2 Coordinates the Activity of PIF7 for Thermomorphogenesis in Arabidopsis Seedlings

Ambient temperature induces the hypocotyl elongation of seedling,called as thermomorphogenesis.It has been reported that the bHLH transcriptional factor PIF7 acts as the critical component to modulate plant thermomorphogenesis,but the underlying mechanism remains elusive.The phytohormone abscisic acid(ABA)suppresses the hypocotyl elongation under high temperature(HT)stress.As the ABI5 binding protein,AFP2 acts as the negative factor to control ABA signaling.In this study,we first identified AFP2 as the interaction protein of PIF7 in vitro and in vivo.Phenotype analysis revealed that overexpressing AFP2 reduced the hypocotyl elongation,while loss-of-function afp2 mutant showed longer hypocotyl under HT.Consistently,overexpressing AFP2 impaired the transactivation effect of PIF7 on auxin biosynthesis related genes YUC8 and IAA19,which possibly resulted into the shorter hypocotyl in the transgenic line overexpressing AFP2 or co-overexpressing AFP2 and PIF7.Thus,these data suggest that AFP2 suppressed PIF7 activity to suppress hypocotyl elongation.Furthermore,we found that HT gradually induced the degradation of AFP2 that possibly released the inhibitory effect of AFP2 on PIF7,thus induced hypocotyl elongation under HT.Taken together,our result reveals the novel function of AFP2 in coordinating thermomorphogenesis through sophistically modulating PIF7 activity.

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℃)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℃,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.

Activation tagging identifies WRKY14 as a repressor of plant thermomorphogenesis in Arabidopsis

Increases in recorded high temperatures around the world are causing plant thermomorphogenesis and decreasing crop productivity.PHYTOCHROME INTERACTING FACTOR 4(PIF4)is a central positive regulator of plant thermomorphogenesis.However,the molecular mechanisms underlying PIF4-regulated thermomorphogenesis remain largely unclear.In this study,we identified ABNORMAL THERMOMORPHOGENESIS 1(ABT1)as an important negative regulator of PIF4 and plant thermomorphogenesis.Overexpression of ABT1 in the activation tagging mutant abt1-D caused shorter hypocotyls and petioles under moderately high temperature(HT).ABT1 encodes WRKY14,which belongs to subgroup II of the WRKY transcription factors.Overexpression of ABT1/WRKY14 or its close homologs,including ABT2/WRKY35,ABT3/WRKY65,and ABT4/WRKY69in transgenic plants caused insensitivity to HT,whereas the quadruple mutant abt1 abt2 abt3 abt4 exhibited greater sensitivity to HT.ABTs were expressed in hypocotyls,cotyledons,shoot apical meristems,and leaves,but their expression were suppressed by HT.Biochemical assays showed that ABT1 can interact with TCP5,a known positive regulator of PIF4,and interrupt the formation of the TCP5-PIF4 complex and repress its transcriptional activation activity.Genetic analysis showed that ABT1 functioned antagonistically with TCP5,BZR1,and PIF4 in plant thermomorphogenesis.Taken together,our results identify ABT1/WRKY14 as a critical repressor of plant thermomorphogenesis and suggest that ABT1/WRKY14,TCP5,and PIF4 may form a sophisticated regulatory module to fine-tune PIF4 activity and temperature-dependent plant growth.

HOOKLESS1 is a positive regulator in Arabidopsis thermomorphogenesis

Dear Editor,With the inevitable trend of global warming,it is urgent to understand how plants sense and respond to temperature increases for designing new crop varieties that can tolerate high ambient temperature.In Arabidopsis thaliana,high ambient temperature promotes hypocotyl elongation in seedlings and stimulates petiole elongation and hyponasty in rosette leaves.These changes in architecture are collectively tenned thermomorphogenesis.Thennomorphogenesis protects seedling meristems from the heat reflected from the ground and reduces the heat flux among leaves in adult plants.

PIF4 and HOOKLESS1 Impinge on Common Transcriptome and Isoform Regulation in Thermomorphogenesis

High temperature activates the transcription factor PHYTOCHROME-INTERACTING FACTOR4(PIF4)to stimulate auxin signaling,which causes hypocotyl elongation and leaf hyponasty(thermomorphogenesis).HOOKLESS1(HLS1)is a recently reported positive regulator of thermomorphogenesis,but the molecular mechanisms by which HLS1 regulates thermomorphogenesis remain unknown.In this study,we initially compared PIF4-and/or HLS1-dependent differential gene expression(DEG)upon high-temperature treatment.We found that a large number of genes are coregulated by PIF4 and HLS1,especially genes involved in plant growth or defense responses.Moreover,we found that HLS1 interacts with PIF4 to form a regulatory module and that,among the HLS1-PIF4-coregulated genes,27.7%are direct targets of PIF4.We also identified 870 differentially alternatively spliced genes(DASGs)in wild-type plants under high temperature.Interestingly,more than half of these DASG events(52.4%)are dependent on both HLS1 and PIF4,and the spliceosome-defective mutant plantsexhibit a hyposensitive response to high temperature,indicating that DASGs are required for thermomorphogenesis.Further comparative analyses showed that the HLS1/PIF4-coregulated DEGs and DASGs exhibit almost no overlap,suggesting that high temperature triggers two distinct strategies to control plant responses and thermomorphogenesis.Taken together,these results demonstrate that the HLS1-PIF4 module precisely controls both transcriptional and posttranscriptional regulation during plant thermomorphogenesis.

Roles of plant hormones in thermomorphogenesis

Global warming has great impacts on plant growth and development,as well as ecological distribution.Plants constantly perceive environmental temperatures and adjust their growth and development programs accordingly to cope with the environment under non-lethal warm temperature conditions.Plant hormones are endogenous bioactive chemicals that play central roles in plant growth,developmental,and responses to biotic and abiotic stresses.In this review,we summarize the important roles of plant hormones,including auxin,brassinosteroids(BRs),Gibberellins(GAs),ethylene(ET),and jasmonates(JAs),in regulating plant growth under warm temperature conditions.This provides a picture on how plants sense and transduce the warm temperature signals to regulate downstream gene expression for controlling plant growth under warm temperature conditions via hormone biosynthesis and signaling pathways.

Epigenetic regulation of thermomorphogenesis in Arabidopsis thaliana

Temperature is a key factor in determining plant growth and development,geographical distribution,and seasonal behavior.Plants accurately sense subtle changes in ambient temperature and alter their growth and development accordingly to improve their chances of survival and successful propagation.Thermomorphogenesis encompasses a variety of morphological changes that help plants acclimate to warm environmental temperatures.Revealing the molecular mechanism of thermomorphogenesis is important for breeding thermo-tolerant crops and ensuri ng food security under global climate change.Plant adaptation to elevated ambient temperature is regulated by multiple signaling pathways and epigenetic mechanisms such as histone modifications,histone variants,and non-coding RNAs.In this review,we summarize recent advances in the mechanism of epigenetic regulation during thermo-morphogenesis with a focus on the model plant Arabidopsis thaliana and briefly discuss future pro-spects for this field.

The molecular basis of heat stress responses in plants

Global warming impacts crop production and threatens food security.Elevated temperatures are sensed by different cell components.Temperature increases are classified as either mild warm temperatures or excessively hot temperatures,which are perceived by distinct signaling pathways in plants.Warm temperatures induce thermomorphogenesis,while high-temperature stress triggers heat acclimation and has destructive effects on plant growth and development.In this review,we systematically summarize the heat-responsive genetic networks in Arabidopsis and crop plants based on recent studies.In addition,we highlight the strategies used to improve grain yield under heat stress from a source-sink perspective.We also discuss the remaining issues regarding the characteristics of thermosensors and the urgency required to explore the basis of acclimation under multifactorial stress combination.

HOP co-chaperones contribute to GA signaling by promoting the accumulation of the F-box protein SNE in Arabidopsis

Gibberellins(GAs)play important roles in multiple developmental processes and in plant response to the environment.Within the GA pathway,a central regulatory step relies on GA-dependent degradation of the DELLA transcriptional regulators.Nevertheless,the relevance of the stability of other key proteins in this pathway,such as SLY1 and SNE(the F-box proteins involved in DELLA degradation),remains unknown.Here,we take advantage of mutants in the HSP70-HSP90 organizing protein(HOP)co-chaperones and reveal that these proteins contribute to the accumulation of SNE in Arabidopsis.Indeed,HOP proteins,along with HSP90 and HSP70,interact in vivo with SNE,and SNE accumulation is significantly reduced in the hop mutants.Concomitantly,greater accumulation of the DELLA protein RGA is observed in these plants.In agreement with these molecular phenotypes,hop mutants show a hypersensitive response to the GA inhibitor paclobutrazol and display a partial response to the ectopic addition of GA when GA-regulated processes are assayed.These mutants also display different phenotypes associated with alterations in the GA pathway,such as reduced germination rate,delayed bolting,and reduced hypocotyl elongation in response to warm temperatures.Remarkably,ectopic overexpression of SNE reverts the delay in germination and the thermally dependent hypocotyl elongation defect of the hop1 hop2 hop3 mutant,revealing that SNE accumulation is the key aspect of the hop mutant phenotypes.Together,these data reveal a pivotal role for HOP in SNE accumulation and GA signaling.

Molecular Regulation of Plant Responses to Environmental Temperatures

Temperature is a key factor governing the growth and development,distribution,and seasonal behavior of plants.The entireplant life cycle is affected by environmental temperatures.Plants grow rapidly and exhibit specific changes in morphology under mild average temperature conditions,a response termed thermomorphogenesis.When exposed to chilling or moist chilling low temperatures,flowering or seed germination is accelerated in some plant species;these processes are known as vernalization and cold stratification,respectively.Interestingly,once many temperate plants are exposed to chilling temperatures for some time,they can acquire the ability to resist freezing stress,a process termed cold acclimation.In the face of global climate change,heat stress has emerged as a frequent challenge,which adversely affects plant growth and development.In this review,we summarize and discuss recent progress in dissecting them olecular mechanism sregulating plant thermomorphogenesis,vernalization,and responses to extreme temperatures.We also discuss the remaining issues that are crucial for understanding the interactions between plants and temperature.

The INO80 chromatin remodeling complex promotes thermo-morphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis.

Global warming imposes a major threat to plant growth and crop production. In some plants including Arabidopsis thaliana, elevated temperatures induce a series of morphological and developmental adjustments, termed thermomorphogenesis to facilitate plant cooling under high-temperature conditions. Plant thermal response is suppressed by histone variant H2A.Z. At warm temperatures, H2A.Z is evicted from nucleosomes at thermo-responsive genes, resulting in their expression changes. However, the mechanisms that regulate H2A.Z eviction and subsequent transcription changes are largely unknown. Here, we show that the INO80 chromatin remodeling complex (INO80-C) promotes thermomorphogenesis and activates the expression of thermo-responsive and auxin-related genes. INO80-C associates with PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), a potent regulator in thermomorphogenesis, and mediates temperature-induced H2A.Z eviction at PIF4 targets. Moreover, INO80-C directly interacts with COMPASS-like and transcription elongation factors to promote active histone modification Histone H3 lysine 4 trimethylation (H3K4me3) and RNA Polymerase II (RNA Pol II) elongation, leading to the thermal induction of transcription. Notably, transcription elongation factors SPT4 and SPT5 are required for the H2A.Z eviction at PIF4 targets, suggesting the cooperation of INO80-C and transcription elongation in H2A.Z removal. Our results demonstrate that the (PIF4)-(INO80-C)-(COMPASS-like)-(transcription elongator) module controls plant thermal response, and establish a link between H2A.Z eviction and active transcription.

GIGANTEA Shapes the Photoperiodic Rhythms of Thermomorphogenic Growth in Arabidopsis

Plants maintain their internal temperature under environments with fluctuating temperatures by adjusting their morphology and architecture,an adaptive process termed thermomorphogenesis.Notably,the rhythmic patterns of plant thermomorphogenesis are governed by day-length information.However,it remains elusive how thermomorphogenic rhythms are regulated by photoperiod.Here,we show that warm temperatures enhance the accumulation of the chaperone GIGANTEA(Gl),which thermostabilizes the DELLA protein,REPRESSOR OF ga1-3(RGA),under long days,thereby attenuating PHYTOCHROME INTERACTING FACTOR 4(PIF4)-mediated thermomorphogenesis.In contrast,under short days,when Gl accumulation is reduced,RGA is readily degraded through the gibberellic acid-mediated ubiquitination-proteasome pathway,promoting thermomorphogenic growth.These data indicate that the GI-RGA-PIF4 signaling module enables plant thermomorphogenic responses to occur in a day-length-dependent manner.We propose that the Gl-mediated integration of photoperiodic and temperature information shapes thermomorphogenic rhythms,which enable plants to adapt to diel fluctuations in day length and temperature during seasonal transitions.

Seedling morphogenesis:when ethylene meets high ambient temperature

Unlike animals,plant development is plastic and sensitive to environmental changes.For example,Arabidopsis thaliana seedlings display distinct growth patterns when they are grown under different light or temperature conditions.M oreover,endogenous plant hormone such as ethylene also impacts seedling morphol ogy.Ethylene induces hypocotyl elongation in light-grown seedlings but strongly inhibits hypocotyl elongation in etiolated(dark-grown)seedlings.Another characteristic ethylene response in etiolated seedlings is the formation of exaggerated apical hooks.Although it is well known that high ambient temperature promotes hypocotyl elongation in light-grown seedlings(thermomor-phogenesis),ethylene suppresses thermomorphogenesis.On another side,high ambient temperature also inhibits the ethylene-responsive hypocotyl shortening and exaggerated hook for mation in etiolated seedlings.Therefore,the simplest phytohormone ethylene exhibits almost the most complicated responses,depending on temperature and/or light conditions.In this review,we will focus on two topics related to the main theme of this special issue(response to high temperature):(1)how does high temperature suppress ethylene-induced seedling morphology in dark grown seedlings,and(2)how does ethylene inhibit high temperature-induced seedling growth in light-grown seedlings.Controlling ethylene biosynthesis through antisense technology was the hallmark event in plant genetic engi-neering in 1990,we assume that manipulations on plant ethylene signaling in agricultural plants may pave the way for coping with climate change in future.

Transcriptional memory and response to adverse temperatures in plants

Temperature is one of the major environmental signals controlling plant development,geographical distribution,and seasonal behavior.Plants perceive adverse temperatures,such as high,low,and freezing temperatures,as stressful signals that can cause physiological defects and even death.As sessile organisms,plants have evolved sophisticated mechanisms to adapt to recurring stressful environments through changing gene expression or transcriptional reprogramming.Transcriptional memory refers to the ability of primed plants to remember previously experienced stress and acquire enhanced tolerance to similar or different stresses.Epigenetic modifications mediate transcriptional memory and play a key role in adapting to adverse temperatures.Understanding the mechanisms of the formation,maintenance,and resetting of stress-induced transcriptional memory will not only enable us to understand why there is a trade-off between plant defense and growth,but also provide a theoretical basis for generating stress-tolerant crops optimized for future climate change.In this review,we summarize recent advances in dissecting the mechanisms of plant transcriptional memory in response to adverse temperatures,based mainly on studies of the model plant Arabidopsis thaliana.We also discuss remaining questions that are important for further understanding the mechanisms of transcriptional memory during the adverse temperature response.

Temperature-mediated regulation of flowering time in Arabidopsis thaliana

Throughout a plant's life cyde,temperature plays a major role in development.Regulatory modules use temperature cues to control gene expression,facilitating physiological change from germination to flowering.These regulatory modules control morphological and molecular responses to temperature changes caused by seasonal changes or by temporary fluctuations,providing a versatile plasticity of plants.In this review,we outline how temperature changes affect the regu latory modules that induce and repress flowering,in addition to general temperature regulation.Recent studies have identified several regulatory modules by which floral transition and growth responses are controlled in a tem-perature-dependent manner.This review will report on recent studies related to floral transition and ambient temperature response.

Post-translational modification:a strategic response to high temperature in plants

With the increasing global warming high-temperature stress is affecting plant growth and develop-ment with greater frequency.Therefore,an increasing number of studies examining the mechanism of temperature response contribute to a more optimal understanding of plant growth under environ-mental pressure.Post-translational modification(PTM)provides the rapid reconnection of tr anscrip-tional programs including transcription factors and signaling proteins.It is vital that plants quickly respond to changes in the environment in order to survive under stressful situations.Herein,we discuss several types of PTMs that occur in response to warm-temperature and high-temperature stress,including ubiquitination,SUMOylation,phosphorylation,histone methylation,and acetylation.This review provides a valuable resolution to this issue to enable increased crop productivity at high temperatures.

Light signaling‑mediated growth plasticity in Arabidopsis grown under high‑temperature conditions

Growing concern around global warming has led to an increase in research focused on plant responses to increased temperature.In this review,we highlight recent advances in our understanding of plant adaptation to high ambient temperature and heat stress,emphasizing the roles of plant light signaling in these responses.We summarize how high temperatures regulate plant cotyledon expansion and shoot and root elongation and explain how plants use light signaling to combat severe heat stress.Finally,we discuss several future avenues for this research and identify various unresolved questions within this field.