A TT1-SCE1 module integrates ubiquitination and SUMOylation to regulate heat tolerance in rice.

Abstract

Heat stress poses a significant threat to grain yield. Our previous study identified TT1, which encodes an α2 subunit of the 26S proteasome, as a critical regulator for rice heat tolerance, representing the first cloned QTL for crop heat tolerance. However, the mechanisms mediated by TT1 still remained elusive. In this study, we unveil SUMO-conjugating enzyme 1 (SCE1), which interacts with TT1 and acts as a downstream component of TT1, engaging in the TT1-mediated 26S proteasome degradation. SCE1 functions as a negative regulator of heat tolerance and can be linked to ubiquitination modification. Additionally, we observed that sHSPs such as Hsp24.1 and Hsp40 can undergo SUMOylation mediated by SCE1, leading to increased accumulation of sHSPs in the absence of SCE1. Furthermore, we propose that the global SUMOylation modulated by SCE1 serves as a crucial signal in response to heat stress, and the rapid decline in elevated SUMOylation is considered a positive effect to enhance heat tolerance due to the loss of SCE1 gene function. Reducing protein levels of SCE1 significantly enhanced grain yield under high-temperature stress by improving seed-setting rate and rice grain filling capacity. Our results uncover the critical role of SCE1 in TT1-mediated heat tolerance pathway, regulating the abundance of sHSP proteins and SUMOylation, and ultimately impacting rice heat tolerance. These findings underscore the significant potential of the TT1-SCE1 module in improving the heat tolerance of crops.