OTS1-dependent deSUMOylation increases tolerance to high copper levels in Arabidopsis

The conjugation of SUMO (small ubiquitin-like modifier) to protein substrates is a reversible process (SUMOylation/deSUMOylation) that regulates plant development and stress responses. The essential metal copper (Cu) is required for normal plant growth, but excess amounts are toxic. The SUMO E3 ligase, SIZ1, and SIZ1-mediated SUMOylation function in plant tolerance to excess Cu. It is unknown whether deSUMOylation also contributes to Cu tolerance in plants. Here, we report that OTS1, a protease that cleaves SUMO from its substrate proteins, participates in Cu tolerance in Arabidopsis thaliana (Arabidopsis). OTS1 loss-of-function mutants (ots1-2 and ots1-3) displayed increased sensitivity to excess Cu. Redox homeostasis and the balance between SUMOylation and deSUMOylation were disrupted in the ots1-3 mutant under excess Cu conditions. The ots1-3 mutant accumulated higher levels of Cu in both shoots and roots compared to wild type. Specific Cu-related metal transporter genes were upregulated due to the loss-of-function of OTS1, which might explain the high Cu levels in ots1-3. These results suggest that the SUMOylation/deSUMOylation machinery is activated in response to excess Cu, and modulates Cu homeostasis and tolerance by regulating both Cu uptake and detoxification. Together, our findings provide insight into the biological function and regulatory role of SUMOylation/deSUMOylation in plant tolerance to Cu.