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

Jiajing Wang; Yizhou Gao; Xiaohui Xiong; Yuqing Yan; Jiajun Lou; Mengmeng Guo; Muhammad Noman; Dayong Li; Fengming Song

doi:10.1016/j.ijbiomac.2024.139046

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

Int J Biol Macromol. 2024 Dec 19:139046. doi: 10.1016/j.ijbiomac.2024.139046. Online ahead of print.

Authors

Jiajing Wang¹, Yizhou Gao², Xiaohui Xiong¹, Yuqing Yan¹, Jiajun Lou¹, Mengmeng Guo¹, Muhammad Noman³, Dayong Li¹, Fengming Song⁴

Affiliations

¹ Key Laboratory of Crop Diseases and Insect Pests of Ministry of Agriculture and Rural Affairs, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; Zhejiang Provincial Key Laboratory of Biology of Crop Pathogens and Insects, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; State Key Laboratory of Rice Biology and Breeding, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China.
² Key Laboratory of Crop Diseases and Insect Pests of Ministry of Agriculture and Rural Affairs, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; Zhejiang Provincial Key Laboratory of Biology of Crop Pathogens and Insects, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; State Key Laboratory of Rice Biology and Breeding, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; School of Biological and Chemical Engineering, Zhejiang University of Science and Technology, Hangzhou 310023, People's Republic of China.
³ Key Laboratory of Crop Diseases and Insect Pests of Ministry of Agriculture and Rural Affairs, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; Zhejiang Provincial Key Laboratory of Biology of Crop Pathogens and Insects, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; State Key Laboratory of Rice Biology and Breeding, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310022, People's Republic of China.
⁴ Key Laboratory of Crop Diseases and Insect Pests of Ministry of Agriculture and Rural Affairs, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; Zhejiang Provincial Key Laboratory of Biology of Crop Pathogens and Insects, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China; State Key Laboratory of Rice Biology and Breeding, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, People's Republic of China. Electronic address: [email protected].

PMID: 39708869
DOI: 10.1016/j.ijbiomac.2024.139046

Abstract

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.

Keywords: FonPARP1; FonPdi1; PARylation; Pathogenicity; Watermelon Fusarium wilt.