Arabidopsis WSS1A, a DNA-protein crosslink repair protease, delays leaf senescence in cooperation with SUMO3

Leaf senescence, the final stage of leaf development, is regulated by complex interplays of intrinsic genetic programs and environmental cues. Throughout their lifetimes, all living organisms encounter various endogenous and environmental challenges, many of which can cause potentially fatal DNA damage. Among these, DNA-protein crosslinks (DPCs) are particularly deleterious, as they obstruct essential processes such as replication and transcription, thereby compromising genome integrity and ultimately leading to premature aging across species. However, the biological significance of DPCs and their repair mechanisms in leaf senescence remains unexplored. Here, we demonstrate that cis-platin (cis-Pt), a potent DPC inducer, accelerates leaf senescence in Arabidopsis. We reveal that Arabidopsis DPC repair factor WSS1A, a WLM/Spr-T metalloprotease, plays a negative role in leaf senescence induced by cis-Pt treatment, darkness, and leaf age. WSS1A forms nuclear condensates via liquid-liquid phase separation both in vitro and in vivo, which is cooperatively driven by its N-terminal segment and intrinsically disordered region. Mechanistically, WSS1A non-covalently interacts with SMALL UBIQUITIN MODIFIER 3 (SUMO3) through its SUMO-interacting motif and is also covalently SUMOylated by SUMO3. Genetic analysis further reveals that WSS1A and SUMO3 act in the same pathway to control cis-Pt-induced leaf senescence. Together, this study establishes a conceptual framework connecting DPC repair and SUMO3-dependent regulation of WSS1A in modulating leaf senescence in Arabidopsis.