DNA-protein crosslinks (DPCs) are highly toxic DNA lesions represented by covalently trapped proteins to DNA molecules. If not repaired, DPCs physically block DNA replication- and transcription-associated complex. Due to the structural and chemical diversity of the crosslinked proteins and a variety of potentially affected DNA/chromatin contexts, DPCs are very challenging lesions to repair. Although specific proteins have been linked with DPC repair, as a whole it is still only poorly understood, especially in plants. We recently described cytidine analog zebularine as a potent inducer of Type 1 DPCs between DNA methyltransferase MET1 (an ortholog of the mammalian DNMT1) and DNA in the model plant Arabidopsis thaliana. The MET1 crosslinks are greatly enriched at the heterochromatic fraction of 45S rDNA repeats (Prochazkova et al., 2022). We performed a forward-directed genetic screen to identify the molecular factors contributing to the mitigation of zebularine-induced DPCs in Arabidopsis. The SMC5/6 complex subunits were among the first characterized candidates (Dvořák Tomaštíková et al., 2023). Genetic interaction and sensitivity assays revealed that the SMC5/6 complex is essential for plant DPC repair and works parallel to the nucleolytic and proteolytic pathways. We showed that the SUMO accumulates at the crosslinked foci induced by zebularine, and the SMC5/6 complex SUMO E3 ligase subunit NSE2 is responsible for the SUMOylation. Of particular interest is a splice variant mutation in the NSE2 SUMO domain that allowed us to uncouple SUMO-related and developmental functions of the SMC5/6 complex. Further screening identified additional candidates involved in the SUMO modification. In summary, our forward-directed genetic screen shows the importance of SUMO in DPC repair in plants and identifies mutations that can be of great interest for further structural and functional studies. Importantly, we identified an additional 50 complementation groups including not yet characterized Arabidopsis proteins or proteins that have not yet been connected with DNA damage repair. This points not only to the complexity of DPC repair but also to the power of the forward-directed screen.