Leaf senescence, the final stage of leaf development, is regulated by a complex interplay 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 impede essential processes such as replication and transcription, compromising genome integrity and ultimately leading to premature aging across diverse organisms. However, the biological significance of DPCs and their repair mechanisms in leaf senescence remains unexplored. In this study, we demonstrate that the accumulation of DPCs by cis-platin (cis-Pt), a well-known DPC inducer, triggers premature leaf senescence in Arabidopsis. We identify Arabidopsis WSS1A, a WLM/Spr-T metalloprotease, as a functional ortholog of yeast Wss1 in DPC repair, playing a negative role in leaf senescence induced by cis-Pt treatment, darkness, and leaf age. WSS1A forms nuclear condensates via liquid-liquid phase separation (LLPS) 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 (SIM) and is covalently SUMOylated by SUMO3. Genetic analysis further reveals that WSS1A is epistatic to SUMO3 in regulating cis-Pt-induced leaf senescence. Disrupting the SIM significantly compromises WSS1A condensate dynamics, highlighting its critical role in phase separation. Together, our findings suggest unresolved DPCs as molecular triggers promoting leaf senescence and underscore the importance of efficient DPC repair by WSS1A involving LLPS and SUMOylation in extending leaf longevity.