Jiayu Wang

To over-top the neighbors, shade-intolerant plants trigger shade avoidance responses with increasing the elongation of stem-like organs at the expense of leaf development. Shade-induced elongation growth has been extensively studied, while the regulatory mechanisms underlying shade-suppressed leaf development remain poorly understood. Here we find sucrose can rescue shade-inhibited leaf development, which requires the functions of phytochrome A (phyA) and TARGET OF RAPAMYCIN (TOR) complex. We confirm an interaction between PHYA and LETHAL WITH SEC THIRTEEN 8 (LST8), a component of TOR complex. Shade and phyA affect TOR activity, in turn TOR affects the protein stability of PHYA. The sucrose-TOR mediated accumulation of PHYA requires CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1)/SUPPRESSOR OF PHYA-105 (SPA) complex. Transcriptome analysis further reveals that sucrose and phyA regulate the expression of leaf development-related genes under shade, particularly those involved in cytokinin metabolism. Our work uncovers a critical role for TOR and PHYA in linking light signaling with cellular energy status, a mechanism that fine-tunes leaf development specifically under shade conditions.

Summary: Light and temperature are two key environmental signals that share several molecular components that, in turn, regulate plant growth. Darkness and high ambient temperatures promote skoto‐ and thermomorphogenesis, including stem elongation. Heat shock proteins 90 (HSP90s) facilitate the adaptation of organisms to various adverse environmental stimuli. Here, we showed that HSP90s are required for hypocotyl elongation during both skoto‐ and thermomorphogenesis. When HSP90s activities are impaired by the knockdown of HSP90s expression or the application of HSP90 inhibitors, the expression levels and protein abundance of PHYTOCHROME‐INTERACTING FACTOR 4 (PIF4) markedly decreased. EARLY FLOWERING 3 (ELF3) deficiency was resistant to the inhibition of HSP90s activities. Furthermore, HSP90s interacted with and destabilized ELF3. In the CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) mutant, the changes in endogenous PIF4 and ELF3 protein levels caused by the inhibition of HSP90s activities were abolished. HSP90s enhanced the interaction between COP1 and ELF3, reduced ELF3 functional effects on PIF4 and modulated hypocotyl elongation during skoto‐ and thermomorphogenesis. Our results indicated that HSP90s participate in light and temperature signalling via the COP1–ELF3–PIF4 module to regulate hypocotyl growth in changing environments.