Plants adjust their architecture to optimize growth and reproductive success under changing climates. Hypocotyl elongation is a pivotal morphogenic trait that is profoundly influenced by light and temperature conditions. While hypocotyl photomorphogenesis has been well characterized at the molecular level, molecular mechanisms underlying hypocotyl thermomorphogenesis remains elusive. Here, we demonstrate that the E3 ubiquitin ligase CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) conveys warm temperature signals to hypocotyl thermomorphogenesis. To investigate the roles of COP1 and its target ELONGATED HYPOCOTYL 5 (HY5) during hypocotyl thermomorphogenesis, we employed Arabidopsis mutants that are defective in their genes. Transgenic plants overexpressing the genes were also produced. We examined hypocotyl growth and thermoresponsive turnover rate of HY5 protein at warm temperatures under both light and dark conditions. Elevated temperatures trigger the nuclear import of COP1, thereby alleviating the suppression of hypocotyl growth by HY5. While the thermal induction of hypocotyl growth is circadian-gated, the degradation of HY5 by COP1 is uncoupled from light responses and timing information. We propose that thermal activation of COP1 enables coincidence between warm temperature signaling and circadian rhythms, which allows plants to gate hypocotyl thermomorphogenesis at the most profitable time at warm temperatures.

No abstract

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.

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.

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 that is 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 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.