Environmentally adaptive reshaping of plant photomorphogenesis by karrikin and strigolactone signaling.

Coordinated morphogenic adaptation of growing plants is critical for their survival and propagation under fluctuating environments. Plant morphogenic responses to light and warm temperatures, termed photomorphogenesis and thermomorphogenesis, respectively, have been extensively studied in recent decades. During photomorphogenesis, plants actively reshape their growth and developmental patterns to cope with changes in light regimes. Accordingly, photomorphogenesis is closely associated with diverse growth hormonal cues. Notably, accumulating evidence indicates that light-directed morphogenesis is profoundly affected by two recently identified phytochemicals, karrikins (KARs) and strigolactones (SLs). KARs and SLs are structurally related butenolides acting as signaling molecules during a variety of developmental steps, including seed germination. Their receptors and signaling mediators have been identified, and associated working mechanisms have been explored using gene-deficient mutants in various plant species. Of particular interest is that the KAR and SL signaling pathways play important roles in environmental responses, among which their linkages with photomorphogenesis are most comprehensively studied during seedling establishment. In this review, we focus on how the phytochemical and light signals converge on the optimization of morphogenic fitness. We also discuss molecular mechanisms underlying the signaling crosstalks with an aim of developing potential ways to improve crop productivity under climate changes.

25 Years of thermomorphogenesis research: milestones and perspectives.

In 1998, Bill Gray and colleagues showed that warm temperatures trigger arabidopsis hypocotyl elongation in an auxin-dependent manner. This laid the foundation for a vibrant research discipline. With several active members of the 'thermomorphogenesis' community, we here reflect on 25 years of elevated ambient temperature research and look to the future.

Complexity of SMAX1 signaling during seedling establishment.

Karrikins (KARs) are small butenolide compounds identified in the smoke of burning vegetation. Along with the stimulating effects on seed germination, KARs also regulate seedling vigor and adaptive behaviors, such as seedling morphogenesis, root hair development, and stress acclimation. The pivotal KAR signaling repressor, SUPPRESSOR OF MAX2 1 (SMAX1), plays central roles in these developmental and morphogenic processes through an extensive signaling network that governs seedling responses to endogenous and environmental cues. Here, we summarize the versatile roles of SMAX1 reported in recent years and discuss how SMAX1 integrates multiple growth hormone signals into optimizing seedling establishment. We also discuss the evolutionary relevance of the SMAX1-mediated signaling pathways during the colonization of aqueous plants to terrestrial environments.

SMAX1 Integrates Karrikin and Light Signals into GA-Mediated Hypocotyl Growth during Seedling Establishment.

Morphogenic adaptation of young seedlings to light environments is a critical developmental process that ensures plant survival and propagation, as they emerge from the soil. Photomorphogenic responses are facilitated by a network of light and growth hormonal signals, such as auxin and gibberellic acid (GA). Karrikins (KARs), a group of butenolide compounds produced from burning plant materials in wildfires, are known to stimulate seed germination in fire-prone plant species. Notably, recent studies support that they also regulate seedling growth, while underlying molecular mechanisms have been unexplored yet. Here, we demonstrate that SUPPRESSOR OF MAX2 1 (SMAX1), a negative regulator of KAR signaling, integrates light and KAR signals into GA-DELLA pathways that regulate hypocotyl growth during seedling establishment. We found that SMAX1 facilitates degradation of DELLA proteins in the hypocotyls. Interestingly, light induces the accumulation of SMAX1 proteins, and SMAX1-mediated degradation of DELLA is elevated in seedling establishment during the dark-to-light transition. Our observations indicate that SMAX1-mediated integration of light and KAR signals into GA pathways elaborately modulates seedling establishment.

SMAX1 potentiates phytochrome B-mediated hypocotyl thermomorphogenesis.

Plant thermosensors help optimize plant development and architecture for ambient temperatures, and morphogenic adaptation to warm temperatures has been extensively studied in recent years. Phytochrome B (phyB)-mediated thermosensing and the gene regulatory networks governing thermomorphogenic responses are well understood at the molecular level. However, it is unknown how plants manage their responsiveness to fluctuating temperatures in inducing thermomorphogenic behaviors. Here, we demonstrate that SUPPRESSOR OF MAX2 1 (SMAX1), known as a karrikin signaling repressor, enhances the thermosensitivity of hypocotyl morphogenesis in Arabidopsis thaliana. Hypocotyl thermomorphogenesis was largely disrupted in SMAX1-deficient mutants. SMAX1 interacts with phyB to alleviate its suppressive effects on the transcription factor activity of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), promoting hypocotyl thermomorphogenesis. Interestingly, the SMAX1 protein is slowly destabilized at warm temperatures, preventing hypocotyl overgrowth. Our findings indicate that the thermodynamic control of SMAX1 abundance serves as a molecular gatekeeper for phyB function in thermosensitizing PIF4-mediated hypocotyl morphogenesis.

Phytochrome B Conveys Low Ambient Temperature Cues to the Ethylene-Mediated Leaf Senescence in Arabidopsis.

Leaf senescence is an active developmental process that is tightly regulated through extensive transcriptional and metabolic reprogramming events, which underlie controlled degradation and relocation of nutrients from aged or metabolically inactive leaves to young organs. The onset of leaf senescence is coordinately modulated by intrinsic aging programs and environmental conditions, such as prolonged darkness and temperature extremes. Seedlings growing under light deprivation, as often experienced in severe shading or night darkening, exhibit an accelerated senescing process, which is mediated by a complex signaling network that includes sugar starvation responses and light signaling events via the phytochrome B (phyB)-PHYTOCHROME-INTERACTING FACTOR (PIF) signaling routes. Notably, recent studies indicate that nonstressful ambient temperatures profoundly influence the onset and progression of leaf senescence in darkness, presumably mediated by the phyB-PIF4 signaling pathways. However, it is not fully understood how temperature signals regulate leaf senescence at the molecular level. Here, we demonstrated that low ambient temperatures repress the nuclear export of phyB and the nuclear phyB suppresses the transcriptional activation activity of ethylene signaling mediator ETHYLENE INSENSITIVE3 (EIN3), thus delaying leaf senescence. Accordingly, leaf senescence was insensitive to low ambient temperatures in transgenic plants overexpressing a constitutively nuclear phyB form, as observed in ein3 eil1 mutants. In contrast, leaf senescence was significantly promoted in phyB-deficient mutants under identical temperature conditions. Our data indicate that phyB coordinately integrates light and temperature cues into the EIN3-mediated ethylene signaling pathway that regulates leaf senescence under light deprivation, which would enhance plant fitness under fluctuating natural environments.

The two clock proteins CCA1 and LHY activate VIN3 transcription during vernalization through the vernalization-responsive cis-element.

Vernalization, a long-term cold-mediated acquisition of flowering competence, is critically regulated by VERNALIZATION INSENSITIVE 3 (VIN3), a gene induced by vernalization in Arabidopsis. Although the function of VIN3 has been extensively studied, how VIN3 expression itself is upregulated by long-term cold is not well understood. In this study, we identified a vernalization-responsive cis-element in the VIN3 promoter, VREVIN3, composed of a G-box and an evening element (EE). Mutations in either the G-box or the EE prevented VIN3 expression from being fully induced upon vernalization, leading to defects in the vernalization response. We determined that the core clock proteins CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) and LATE-ELONGATED HYPOCOTYL (LHY) associate with the EE of VREVIN3, both in vitro and in vivo. In a cca1 lhy double mutant background harboring a functional FRIGIDA allele, long-term cold-mediated VIN3 induction and acceleration of flowering were impaired, especially under mild cold conditions such as at 12°C. During prolonged cold exposure, oscillations of CCA1/LHY transcripts were altered, while CCA1 abundance increased at dusk, coinciding with the diurnal peak of VIN3 transcripts. We propose that modulation of the clock proteins CCA1 and LHY participates in the systems involved in sensing long-term cold for the activation of VIN3 transcription.

iRegNet: an integrative Regulatory Network analysis tool for Arabidopsis thaliana.

Gene expression is delicately controlled via multilayered genetic and/or epigenetic regulatory mechanisms. Rapid development of the high-throughput sequencing (HTS) technology and its derivative methods including chromatin immunoprecipitation sequencing (ChIP-seq) and DNA affinity purification sequencing (DAP-seq) have generated a large volume of data on DNA-protein interactions (DPIs) and histone modifications on a genome-wide scale. However, the ability to comprehensively retrieve empirically validated upstream regulatory networks of genes of interest (GOIs) and genomic regions of interest (ROIs) remains limited. Here, we present integrative Regulatory Network (iRegNet), a web application that analyzes the upstream regulatory network for user-queried GOIs or ROIs in the Arabidopsis (Arabidopsis thaliana) genome. iRegNet covers the largest empirically proven DNA-binding profiles of Arabidopsis transcription factors (TFs) and non-TF proteins, and histone modifications obtained from all currently available Arabidopsis ChIP-seq and DAP-seq data. iRegNet not only catalogs upstream regulomes and epigenetic chromatin states for single-query gene/genomic region but also suggests significantly overrepresented upstream genetic regulators and epigenetic chromatin states of user-submitted multiple query genes/genomic regions. Furthermore, gene-to-gene coexpression index and protein-protein interaction information were also integrated into iRegNet for a more reliable identification of upstream regulators and realistic regulatory networks. Thus, iRegNet will help discover upstream regulators as well as molecular regulatory networks of GOI(s) and/or ROI(s), and is freely available at http://chromatindynamics.snu.ac.kr:8082/iRegNet_main.

Safeguarding genome integrity under heat stress in plants.

Heat stress adversely affects an array of molecular and cellular events in plant cells, such as denaturation of protein and lipid molecules and malformation of cellular membranes and cytoskeleton networks. Genome organization and DNA integrity are also disturbed under heat stress, and accordingly, plants have evolved sophisticated adaptive mechanisms that either protect their genomes from deleterious heat-induced damages or stimulate genome restoration responses. In particular, it is emerging that DNA damage responses are a critical defense process that underlies the acquirement of thermotolerance in plants, during which molecular players constituting the DNA repair machinery are rapidly activated. In recent years, thermotolerance genes that mediate the maintenance of genome integrity or trigger DNA repair responses have been functionally characterized in various plant species. Furthermore, accumulating evidence supports that genome integrity is safeguarded through multiple layers of thermoinduced protection routes in plant cells, including transcriptome adjustment, orchestration of RNA metabolism, protein homeostasis, and chromatin reorganization. In this review, we summarize topical progresses and research trends in understanding how plants cope with heat stress to secure genome intactness. We focus on molecular regulatory mechanisms by which plant genomes are secured against the DNA-damaging effects of heat stress and DNA damages are effectively repaired. We will also explore the practical interface between heat stress response and securing genome integrity in view of developing biotechnological ways of improving thermotolerance in crop species under global climate changes, a worldwide ecological concern in agriculture.

A Multifaceted Action of Phytochrome B in Plant Environmental Adaptation.

Light acts as a vital external cue that conveys surrounding information into plant growth and performance to facilitate plants to coordinate with changing environmental conditions. Upon exposure to light illumination, plants trigger a burst of molecular and physiological signaling cascades that induces not only photomorphogenic responses but also diverse adaptive behaviors. Notably, light responses and photomorphogenic traits are often associated with plant responses to other environmental cues, such as heat, cold, drought, and herbivore and pathogen attack. Growing evidence in recent years demonstrate that the red/far-red light-absorbing phytochrome (phy) photoreceptors, in particular phyB, play an essential role in plant adaptation responses to abiotic and biotic tensions by serving as a key mediator of information flow. It is also remarkable that phyB mediates the plant priming responses to numerous environmental challenges. In this minireview, we highlight recent advances on the multifaceted role of phyB during plant environmental adaptation. We also discuss the biological relevance and efficiency of the phy-mediated adaptive behaviors in potentially reducing fitness costs under unfavorable environments.

A dual mode of ethylene actions contributes to the optimization of hypocotyl growth under fluctuating temperature environments.

The gaseous phytohormone ethylene plays versatile roles in sustaining plant growth and fitness in response to environmental changes, such as light illumination, flooding, and mechanical pressure. Interestingly, it is well known that the effects of ethylene on plant growth vary profoundly, depending on external conditions. For example, light/dark conditions alter the directionality of ethylene action on hypocotyl growth. Similarly, a recent study has shown that the effects of ethylene on hypocotyl growth are reversed during temperature increases: ethylene attenuates hypocotyl elongation in the light at warm temperatures (28°C), while promoting it at normal temperatures (22°C). The ethylene-activated ETHYLENE-INSENSITIVE 3 (EIN3) transcription factor directly promotes the transcription of both PHYTOCHROM INTERACTING FACTOR 3 (PIF3) and ARABIDOPSIS PP2C CLADE D7 (APD7) genes. At 22°C, the auxin activity is tuned down, and thus ethylene promotes hypocotyl growth via the PIF3-mediated microtubule reorganization. On the other hand, when auxin highly accumulates at 28°C, the ethylene-directed growth repression is potentiated through the APD7-mediated repression of auxin responses. APD7 plays a role in integrating ethylene cues into auxin signaling. We propose that the dual mode of EIN3-mediated ethylene actions enables plants to optimize growth under constantly changing environments.

External and Internal Reshaping of Plant Thermomorphogenesis.

Plants dynamically adapt to changing temperatures to ensure propagation and reproductive success, among which morphogenic responses to warm temperatures have been extensively studied in recent years. As readily inferred from the cyclic co-oscillations of environmental cues in nature, plant thermomorphogenesis is coordinately reshaped by various external conditions. Accumulating evidence supports that internal and developmental cues also contribute to harmonizing thermomorphogenic responses. The external and internal reshaping of thermomorphogenesis is facilitated by versatile temperature sensing and interorgan communication processes, circadian and photoperiodic gating of thermomorphogenic behaviors, and their metabolic coordination. Here, we discuss recent advances in plant thermal responses with focus on the diel and seasonal reshaping of thermomorphogenesis and briefly explore its application to developing climate-smart crops.

EIN3-Mediated Ethylene Signaling Attenuates Auxin Response during Hypocotyl Thermomorphogenesis.

The gaseous phytohormone ethylene plays vital roles in diverse developmental and environmental adaptation processes, such as fruit ripening, seedling establishment, mechanical stress tolerance and submergence escape. It is also known that in the light, ethylene promotes hypocotyl growth by stimulating the expression of PHYTOCHROME INTERACTING FACTOR3 (PIF3) transcription factor, which triggers microtubule reorganization during hypocotyl cell elongation. In particular, ethylene has been implicated in plant responses to warm temperatures in recent years. However, it is currently unclear how ethylene signals are functionally associated with hypocotyl thermomorphogenesis at the molecular level. Here, we show that ETHYLENE-INSENSITIVE3 (EIN3)-mediated ethylene signals attenuate hypocotyl thermomorphogenesis by suppressing auxin response. At warm temperatures, when the activity of the PIF4 thermomorphogenesis promoter is prominently high, the ethylene-activated EIN3 transcription factor directly induces the transcription of ARABIDOPSIS PP2C CLADE D7 (APD7) gene encoding a protein phosphatase that inactivates the plasma membrane (PM) H+-ATPase proton pumps. In conjunction with the promotive role of the PM H+-ATPases in hypocotyl cell elongation, our observations strongly support that the EIN3-directed induction of APD7 gene is linked with the suppression of auxin-induced cell expansion, leading to the reduction in thermomorphogenic hypocotyl growth. Our data demonstrate that APD7 acts as a molecular hub that integrates ethylene and auxin signals into hypocotyl thermomorphogenesis. We propose that the ethylene-auxin signaling crosstalks via the EIN3-APD7 module facilitate the fine-tuning of hypocotyl thermomorphogenesis under natural environments, which often fluctuate in a complex manner.

HOS1 activates DNA repair systems to enhance plant thermotolerance.

Plants possess an astonishing capability of effectively adapting to a wide range of temperatures, ranging from freezing to near-boiling temperatures1,2. Yet, heat is a critical obstacle to plant survival. The deleterious effects of heat shock on cell function include misfolding of cellular proteins, disruption of cytoskeletons and membranes, and disordering of RNA metabolism and genome integrity3-5. Plants stimulate diverse heat shock response pathways in response to abrupt temperature increases. While it is known that stressful high temperatures disturb genome integrity by causing nucleotide modifications and strand breakages or impeding DNA repair6, it is largely unexplored how plants cope with heat-induced DNA damages. Here, we demonstrated that high expression of osmotically reponsive genes 1 (HOS1) induces thermotolerance by activating DNA repair components. Thermotolerance and DNA repair capacity were substantially reduced in HOS1-deficient mutants, in which thermal induction of genes encoding DNA repair systems, such as the DNA helicase RECQ2, was markedly decreased. Notably, HOS1 proteins were thermostabilized in a heat shock factor A1/heat shock protein 90 (HSP90)-dependent manner. Our data indicate that the thermoresponsive HSP90-HOS1-RECQ2 module contributes to sustaining genome integrity during the acquisition of thermotolerance, providing a distinct molecular link between DNA repair and thermotolerance.

Auxin mediates the touch-induced mechanical stimulation of adventitious root formation under windy conditions in Brachypodium distachyon.

BACKGROUND: It is widely perceived that mechanical or thigmomorphogenic stimuli, such as rubbing and bending by passing animals, wind, raindrop, and flooding, broadly influence plant growth and developmental patterning. In particular, wind-driven mechanical stimulation is known to induce the incidence of radial expansion and shorter and stockier statue. Wind stimulation also affects the adaptive propagation of the root system in various plant species. However, it is unknown how plants sense and transmit the wind-derived mechanical signals to launch appropriate responses, leading to the wind-adaptive root growth. RESULTS: Here, we found that Brachypodium distachyon, a model grass widely used for studies on bioenergy crops and cereals, efficiently adapts to wind-mediated lodging stress by forming adventitious roots (ARs) from nonroot tissues. Experimental dissection of wind stimuli revealed that not bending of the mesocotyls but physical contact of the leaf nodes with soil particles triggers the transcriptional induction of a group of potential auxin-responsive genes encoding WUSCHEL RELATED HOMEOBOX and LATERAL ORGAN BOUNDARIES DOMAIN transcription factors, which are likely to be involved in the induction of AR formation. CONCLUSIONS: Our findings would contribute to further understanding molecular mechanisms governing the initiation and development of ARs, which will be applicable to crop agriculture in extreme wind climates.

Synchronization of photoperiod and temperature signals during plant thermomorphogenesis.

It is well-known that even small changes in ambient temperatures by a few degrees profoundly affect plant growth and morphology. This architectural property is intimately associated with global warming. In particular, under warm temperature conditions, plants exhibit distinct morphological changes, such as elongation of hypocotyls and leaf petioles, formation of small, thin leaves, and leaf hyponasty that describes an upward bending of leaf petioles. These thermoresponsive morphological adjustments are termed thermomorphogenesis. Under warm temperature conditions, the PHYTOCHROME INTERACTING FACTOR 4 (PIF4) transcription factor is thermoactivated and stimulates the transcription of the YUCCA8 gene encoding an auxin biosynthetic enzyme, promoting hypocotyl elongation. Notably, these thermomorphogenic growth is influenced by daylength or photoperiod, displaying relatively high and low thermomorphogenic hypocotyl growth during the nighttime under short days and long days, respectively. We have recently reported that the photoperiod signaling regulator GIGANTEA (GI) thermostabilizes the REPRESSOR OF ga1-3 transcription factor, which is known to attenuate the PIF4-mediated thermomorphogenesis. We also found that the N-terminal domain of GI interacts with PIF4, possibly destabilizing the PIF4 proteins. We propose that the GI-mediated shaping of photoperiodic rhythms of hypocotyl thermomorphogenesis helps plant adapt to fluctuations in daylength and temperature environments occurring during seasonal transitions.

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 (GI), 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 GI 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 GI-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.

Physicochemical modeling of the phytochrome-mediated photothermal sensing.

Light and temperature cues share many common signaling events towards plant photothermal morphogenesis. Particularly, the red (R)/far-red (FR)-absorbing phytochrome photoreceptors also function as temperature sensors, suggesting that light and temperature responses are intimately associated with each other. Here, we present data from physicochemical modeling of temperature sensing and thermomorphogenic patterning of hypocotyl growth, which illustrate that the two seemingly distinct stimulating cues are tightly coupled through physicochemical principles and temperature effects can be described as a function of infra-red (IR) thermal radiation. It is possible that the dark reversion from the FR-absorbing Pfr to the R-absorbing Pr phytochromes is essentially an IR-mediated thermal conversion. We propose that the phytochromes modulate photothermal responses by monitoring R:IR ratios, as they sense R:FR ratios during photomorphogenesis.

Developmental polarity shapes thermo-induced nastic movements in plants.

Directional and non-directional environmental cues are able to induce polar behaviors of plants, which are termed tropic and nastic movements, respectively. While molecular mechanisms underlying the directionality of tropic movements are relatively well studied, it is poorly understood how the polarity of nastic movements is determined in response to non-directional stimuli, such as ambient temperatures. It has recently been shown that thermal induction of leaf hyponasty is stimulated by developmentally programmed polar auxin transport in Arabidopsis. Under warm environments, the PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) transcription factor binds to the promoter of PINOID (PID) gene, whose gene product modulates the polar trafficking of the auxin transporter PIN-FORMED 3 (PIN3). Notably, PIF4 binding to the PID promoter occurs predominantly in the abaxial petiole cells than the adaxial petiole cells, leading to differential PID expression and thus asymmetric auxin accumulation in the petiole cells. In addition, ASYMMETRIC LEAVES 1 (AS1), the well-characterized leaf polarity-determining epigenetic regulator, promotes the PID expression by modulating the patterns of histone 4 acetylation (H4Ac) in the PID chromatin. These observations demonstrate that developmental programming of the thermonastic leaf movement through polar auxin distribution enables plants to bend their leaves upward in response to non-directional thermal stimuli, contributing to cooling plant body temperatures under warm temperature conditions. We propose that a developmentally predetermined polarity plays a major role in governing the directionality of various nastic movements in plants.