Poly(ADP-ribose) polymerase FonPARP1-catalyzed PARylation of protein disulfide isomerase FonPdi1 regulates pathogenicity of Fusarium oxysporum f. sp. niveum on watermelon.

Poly(ADP-ribosyl)ation (PARylation), catalyzed by poly(ADP-ribose) polymerases (PARPs) and hydrolyzed by poly(ADP-ribose) glycohydrolase (PARG), is an important reversible post-translational protein modification in all eukaryotes, including plant pathogenic fungi. Previously, we revealed that FonPARP1, an active PARP, is crucial for the pathogenicity of Fusarium oxysporum f. sp. niveum (Fon), the causative agent of watermelon Fusarium wilt. This study explores the enzymatic activity and substrates of FonPARP1 in regulating Fon pathogenicity. FonPARP1 is localized in nuclei of Fon macroconidia and hyphae. Essential conserved domains and a key glutamic acid residue at position 729 are critical for FonPARP1 enzyme activity and pathogenicity function in Fon. FonPARP1 interacts with protein disulfide isomerase FonPdi1 and PARylates it at 13 glutamic acid residues, affecting the interaction ability, PDI activity, ER homeostasis, and pathogenicity function. FonPARG1, interacting with both FonPARP1 and FonPdi1, hydrolyzes poly(ADP-ribose) chains from auto-PARylated FonPARP1 and FonPARP1-PARylated FonPdi1. These findings underscore the role of FonPARP1-catalyzed PARylation in regulating Fon pathogenicity and its significance in plant pathogenic fungi.