Salicylic acid reduces ELF3 phase separation and suppresses thermomorphogenic growth in Arabidopsis

Abstract

Salicylic acid (SA), a long-characterized defense hormone, is increasingly recognized for its roles in plant growth and development. However, its involvement in mediating plant growth responses to environmental cues remains less understood. Here, we show that SA negatively affects thermomorphogenic growth in Arabidopsis thaliana. SA levels decrease in Arabidopsis when exposed to warm temperatures (29°C). Seedlings treated with exogenous SA, as well as transgenic plants with elevated SA levels, exhibit significantly reduced thermoresponsive hypocotyl elongation compared with control seedlings. By contrast, SA-deficient mutant seedlings display enhanced elongation. SA significantly decreases warmth-induced expression of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), a central regulator of thermomorphogenesis, and of downstream auxin biosynthesis and signaling genes. Furthermore, the inhibitory effects of SA on thermomorphogenic growth and warmth-induced PIF4 expression are largely dependent on EARLY FLOWERING 3 (ELF3). SA reduces liquid-liquid phase separation (LLPS) of ELF3 prion-like domain (ELF3-Prd) in vitro, although the underlying mechanism remains to be elucidated. Correspondingly, elevated SA levels in plants decrease ELF3 nuclear speckle formation and enhance ELF3 binding to the PIF4 promoter at warm temperatures, whereas reduced SA levels in plants lead to the opposite effect. Collectively, our study uncovers a previously unrecognized role of SA in plant growth adaptation to the changing climate.