SUMOylation controls peptide processing to generate damage-associated molecular patterns in Arabidopsis

Abstract

Upon injury, both mammalian and plant cells activate a survival mechanism by sensing endogenous damage-associated molecular patterns (DAMPs). Plant elicitor peptides (Peps), a representative DAMP, are released from their precursors (PROPEPs; Precursors of Peps) through cleavage by metacaspases (MCs), but the control of Pep generation remains unclear. Here, we discovered that several PROPEPs in Arabidopsis thaliana are substrates for SUMOylation and that Ca²⁺ upregulates PROPEP1 SUMOylation, facilitated by the SUMO E3 ligase SAP and MIZ1 domain-containing ligase1 (SIZ1). Mutations at the SUMOylation site on PROPEP1, or at the SUMO-interacting motifs (SIMs) on its protease MC4, reduced the PROPEP1-MC4 association and PROPEP1 cleavage. Overexpression of the wild-type form, but not the SUMOylation-defective variant of PROPEP1, enhanced plant tolerance to cell wall damage. Consistently, SIZ1 contributes to PROPEP1 processing and cell wall damage responses. These findings support the idea that SUMOylation promotes PROPEP1 cleavage via MC4 and provide insights into how DAMP generation is controlled in eukaryotic cells.