SUMO-Specific Proteases SPF1 and SPF2 Negatively Regulate Seed Oil Synthesis by Mediating WRI1 deSUMOylation
    作者: Xiao Liu, Linpo Liu, Shuangshuang Li, Jingzhi Zhao, Yuhong Chen, Wei Ma, Shan Tang, Liang Guo, Xupeng Guo, Chengming Fan, Zanmin Hu
    刊物名称: Plant Communications
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    发布时间: 2025-12-12
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    摘要:
    SUMO PROTEASE RELATED TO FERTILITY1 (SPF1) and SPF2 are responsible for deSUMOylation of SUMO-conjugated protein substrates and maintaining protein SUMOylation homeostasis. While, the reasons are unclear for the increase in seed size and seed oil content (SOC) in spf1-1, spf2-1 and spf1-1 spf2-1 in Arabidopsis thaliana. Here, we discovered that SPF1 and SPF2 affected the SUMOylation state of WRINKLED1 (WRI1), a master regulator in transcriptional control of plant oil synthesis. Genetic analyses indicate that double mutants spf1-1 wri1-3, spf2-1 wri1-3 and triple-mutant spf1-1 spf2-1 wri1-3 phenocopy wri1-3, exhibiting severe seed shriveling, indicating that SPF1 and SPF2 act upstream of WRI1. Intriguingly, WRI1 was identified as a substrate of SUMO1, with two conserved SUMOylation sites, lysine-257 (K257) and K266, in cruciferous plants, and the K257 site being the dominant SUMOylation site required for seed oil synthesis. SUMOylation enhanced WRI1 stability, while SPF1 and SPF2-mediated deSUMOylation promote WRI1 degradation. Additionally, in spf1-1, spf2-1 and spf1-1 spf2-1 mutants, the abundance of SUMOylated-WRI1 showed an accumulation trend during seed development, correlating with increased seed oil accumulation. This finding reveals that SPF1 and SPF2 negatively regulate oil synthesis by deSUMOylating WRI1, establishing a dynamic SUMOylation-deSUMOylation switch centered on the SPF1/SPF2-WRI1 module that precisely regulates seed development and oil synthesis.