Elucidating tissue and subcellular specificity of the entire SUMO network reveals how stress responses are fine-tuned in a eukaryote

Abstract

SUMOylation is essential in plant and animal cells, but it remains unknown how small ubiquitin-like modifier (SUMO) components act in concert to modify specific targets in response to environmental stresses. In this study, we characterize every SUMO component in the Arabidopsis root to create a complete SUMO Cell Atlas in eukaryotes. This unique resource reveals wide spatial variation, where SUMO proteins and proteases have subfunctionalized in both their expression and subcellular localization. During stress, SUMO conjugation is mainly driven by tissue-specific regulation of the SUMO E2-conjugating enzyme. Stress-specific modulation of the SUMO pathway reveals unique combinations of proteases being targeted for regulation in distinct root tissues by salt, osmotic, and biotic signals. Our SUMO Cell Atlas resources reveal how this posttranslational modification (PTM) influences cellular-and tissue-scale adaptations during root development and stress responses. To our knowledge, we provide the first comprehensive study elucidating how multiple stress inputs can regulate an entire PTM system.