Warm temperature-induced autophagy mediates selective degradation of TIMING OF CAB EXPRESSION 1 thus promoting plant thermomorphogenesis.

Abstract

Plant thermomorphogenesis is a critical adaptive response to elevated ambient temperatures. The transcription factor PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) integrates diverse environmental and phytohormone signals to coordinate thermoresponsive growth. However, the cellular mechanisms underlying plant thermomorphogenic growth remain poorly understood. In this study, we show that elevated ambient temperature activates autophagy in a PIF4-dependent manner. The autophagy-deficient mutants autophagy-related 5 (atg5)-1 and autophagy-related 7 (atg7)-2 exhibit shorter hypocotyls compared with the wild type at 28 °C, highlighting the important role of autophagy in regulating thermomorphogenic growth in Arabidopsis (Arabidopsis thaliana). Moreover, we identified TIMING OF CAB EXPRESSION 1 (TOC1), a negative regulator of PIF4, as a target of selective autophagy. TOC1 directly interacts with AUTOPHAGY-RELATED 8 (ATG8) via the conserved ATG8-interacting motif-LIR/AIM docking site interface and is degraded through the autophagy pathway in response to elevated temperature. TOC1 accumulates in the autophagy-deficient mutant atg5-1 at 28 °C, where it inhibits PIF4 function and reduces thermosensitivity. Conversely, the reduced TOC1 level in atg5-1 toc1-21 rescues the short-hypocotyl phenotype of atg5-1 at 28 °C. Our study demonstrates that warm temperature-induced autophagy promotes plant thermomorphogenic growth by mediating the selective degradation of TOC1. This study reveals the reciprocal regulation between autophagy and thermomorphogenic signaling and identifies a molecular mechanism underlying this crosstalk.