•Over 1000 mostly nuclear proteins are targets of SUMOylation in Arabidopsis.•Stress-induced SUMO addition is important for abiotic and biotic stress defense.•Reproductive development and success is linked to SUMOylation.•SUMO has emerging roles in transcriptional gene silencing and epigenetic regulation.•The SUMO system might be an attractive target for improving stress tolerance in crops. Conjugation of small ubiquitin-related modifier (SUMO) to intracellular proteins provides a dynamic regulatory mechanism that enables plants to rapidly defend against environmental challenges. SUMOylation of mostly nuclear proteins is among the fastest stress responses observed but precisely how this post-translational modification provides stress resilience remains unclear. Here, we describe the plant SUMO system and its expanding target catalog, which implicates this modification in DNA repair, chromatin modification/remodeling, transcriptional activation/repression, epigenetics, and RNA metabolism, with a likely outcome being extensive nuclear re-wiring to withstand stress. In parallel, studies have linked SUMO to developmental programs such as gametogenesis and gene silencing. The accumulating data support the notion that SUMOylation substantially influences the transcriptional and epigenetic landscapes to promote stress tolerance and developmental progression.