Drought inhibits thermomorphogenesis via salicylic acid-mediated suppression of ELF3 phase separation

Plants are constantly exposed to environmental changes and must respond carefully to ensure survival and growth. Under high temperatures, many plants exhibit a series of morphological and developmental adjustments, including increased hypocotyl and petiole elongation. These adaptations, collectively termed thermomorphogenesis, promote transpiration and water loss, thereby enhancing evaporative cooling. However, this phenomenon has primarily been described under well-watered conditions, whereas in nature, heat often coincides with other environmental challenges, such as drought. How thermomorphogenesis integrates with water shortage conditions, where excess water loss can be detrimental, remains unclear. Here, we demonstrate that restricting water availability and mimicking drought stress with mannitol or PEG inhibit thermomorphogenesis. Mechanistically, both mannitol and PEG treatments reduce high temperature-induced transcriptional activation of PHYTOCHROME INTERACTING FACTOR 4 (PIF4), a central regulator of thermomorphogenesis. This suppression is contributed to by the enhanced production of plant phytohormone salicylic acid (SA), which disrupts phase separation and prevents the deactivation of EARLY FLOWERING 3 (ELF3), a repressor of PIF4, at high temperatures, thereby inhibiting PIF4 activation. Our study highlights the trade-off between cooling at high temperatures and minimizing excessive water loss under water-limited conditions, providing insights into plant responses to complex environmental challenges.