SIZ1 SUMOylates and stabilizes WRI1 to safeguard seed filling and fatty acid biosynthesis under high-temperature stress

Abstract High-temperature stress hinders seed filling, reducing seed quality and crop yield. However, the molecular mechanisms underlying this process remain unclear. Here, we identify SAP AND MIZ1 DOMAIN-CONTAINING LIGASE1 (SIZ1) as a key regulator of seed filling under prolonged high temperatures in Arabidopsis (Arabidopsis thaliana). SIZ1 and WRINKLED1 (WRI1) are co-expressed during seed filling, and overexpressing either gene enhances seed filling and promotes fatty acid biosynthesis under high-temperature stress. Genetic and biochemical analyses revealed that SIZ1 stabilizes WRI1 by promoting its SUMOylation at Lys-257 and Lys-266, thereby inhibiting its interaction with the CULLIN3-based ubiquitin E3 ligase adaptor protein BTB/POZMATH (BPM) and preventing its ubiquitination and degradation. Mutating these SUMOylation sites accelerates WRI1 degradation, impairing its function in seed filling under high-temperature stress. Furthermore, high-temperature stress induces SIZ1 expression and reduces WRI1 levels, suggesting that SIZ1-mediated SUMOylation counteracts high-temperature stress-induced WRI1 instability. These findings establish SIZ1 as a crucial factor maintaining WRI1 stability and seed filling under high-temperature stress, providing valuable genetic resources and a theoretical foundation for addressing prolonged high-temperature stress in agricultural production.