SnRK2-mediated phosphorylation of SIZ1 enhances global SUMOylation under osmotic stress in Arabidopsis

Abstract

AbstractSUMOylation is a highly dynamic posttranslational modification that plays a critical role in regulating plant stress responses. The global SUMOylation is quickly induced by dehydration and hyperosmotic stresses in plants, while the detailed mechanism underlying such SUMOylation dynamics is largely unknown. Here, we report that the SNF1-related protein kinase 2 (SnRK2) and SUMO E3 ligase SIZ1 module is crucial for the stress-induced increment of SUMOylation in Arabidopsis. Under osmotic stress, or application of phytohormone Abscisic Acid (ABA), the rapidly activated SnRK2s physically interact with and phosphorylate SIZ1, enhancing its stability. The Ser820 residue in C-terminal region of SIZ1 proteins is a functional SnRK2 phosphosite, whose phosphorylation is abolished in the high-order mutant ofSnRK2s. The non-phosphorylatable SIZ1S820Ais unstable bothin vivoandin vitro. We also noticed the degradation of SIZ1 is largely darkness-dependent, interestingly, independent of COP1, a key ubiquitin E3 ligase regulating photomorphogenesis. Multiple SUMOylation, Ubiquitination, and phosphorylation sites in SIZ1 proteins, which may coordinate the dynamics of SIZ1 proteins and global SUMOylation upon environmental changes. Our findings highlight the critical role of the SnRK2-SIZ1 module in regulating SUMOylation dynamics during plant stress responses and provide new insights into the regulatory mechanisms underlying this essential posttranslational modification.