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 inhibit thermomorphogenesis. Mechanistically, mannitol treatment reduces high temperature-induced transcriptional activation of PHYTOCHROME INTERACTING FACTOR4 (PIF4), a central regulator of thermomorphogenesis . This suppression is contributed 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. For RNA extraction, 7-day-old seedlings grown at 21°C were shifted to 27°C or kept at 21°C with or without mannitol treatment at ZT1, and seedlings were collected at ZT13. The extracted RNA was used for library preparation and sequencing

植物始终处于环境变化之中，需精准调控自身响应以保障存活与生长。在高温环境下，多数植物会出现一系列形态与发育层面的适应性调整，如下胚轴和叶柄伸长。这类适应性变化被统称为热形态建成（thermomorphogenesis），其会促进蒸腾作用与水分散失，进而增强蒸发降温效果。然而，此前该现象的相关研究多基于水分充足的环境条件，而在自然生态中，高温往往伴随干旱等其他环境胁迫。当水分匮乏时，过度蒸腾失水会对植物产生危害，那么热形态建成如何与缺水环境相整合，目前仍不明确。本研究证实，限制水分供应或利用甘露醇模拟干旱胁迫，均可抑制植物的热形态建成。从分子机制来看，甘露醇处理会减弱高温诱导的光敏色素互作因子4（PHYTOCHROME INTERACTING FACTOR4, PIF4）的转录激活——而PIF4正是热形态建成的核心调控因子。该抑制效应源于植物激素水杨酸（salicylic acid, SA）的合成增加：高温下，水杨酸会破坏相分离过程，阻遏PIF4的抑制因子早花3（EARLY FLOWERING 3, ELF3）的失活，进而抑制PIF4的激活。本研究揭示了高温降温与水分受限条件下减少过度失水之间的权衡关系，为理解植物应对复杂环境胁迫的响应机制提供了新视角。在RNA提取环节，本研究将在21℃下培养7天的幼苗分别转移至27℃环境，或继续保留在21℃环境；两组均在ZT1时刻施加或不施加甘露醇处理，并于ZT13时刻收集幼苗。提取得到的RNA用于文库构建与测序。