Noncanonical mono(ADP-ribosyl)ation of zinc finger SZF proteins counteracts ubiquitination for protein homeostasis in plant immunity

Protein ADP-ribosylation is a reversible post-translational modification that transfers ADP-ribose from NAD+ onto acceptor proteins1-3. Poly(ADP-ribosy)lation (PARylation), catalyzed by poly(ADP-ribose) polymerases (PARPs), and poly(ADP-ribose) glycohydrolases (PARGs), which remove the modification, regulates diverse cellular processes1-3. However, the chemistry and physiological functions of mono(ADP-ribosy)lation (MARylation) remain elusive. Here, we report that the Arabidopsis zinc finger proteins SZF1 and SZF2, key regulators of immune gene expression, are MARylated by the noncanonical ADP-ribosyltransferase SRO2. Immune elicitation promotes MARylation of SZF1/SZF2 via dissociation from PARG1, which has an unconventional activity in hydrolyzing both poly(ADP-ribose) and mono(ADP-ribose) from acceptor proteins. MARylation antagonizes the polyubiquitination of SZF1 mediated by the SH3 domain-containing proteins SH3P1/SH3P2, thereby stabilizing SZF1 proteins to relay immune signaling. Our study uncovers the previously unrecognized enzymes mediating MARylation of vital immune regulators and underpins a unique mechanism of maintaining protein homeostasis by the counter-regulation of ADP-ribosylation and polyubiquitination to ensure proper immune responses.