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The SUMOylation Pathway Components Are Required for Vegetative Growth, Asexual Development, Cytotoxic Responses, and Programmed Cell Death Events in Fusarium oxysporum f. sp. niveum

Azizullah,Muhammad Noman,Yizhou Gao,Hui Wang,Xiaohui Xiong,Jiajing Wang,Dayong Li,Fengming Song

SUMOylation is an essential protein modification process that regulates numerous crucial cellular and biochemical processes in phytopathogenic fungi, and thus plays important roles in multiple biological functions. The present study characterizes the SUMOylation pathway components, including SMT3 (SUMO), AOS1 (an E1 enzyme), UBC9 (an E2 enzyme), and MMS21 (an E3 ligase), inFusarium oxysporumf. sp.niveum(Fon), the causative agent of watermelon Fusarium wilt, in terms of the phylogenetic relationship, gene/protein structures, and basic biological functions. The SUMOylation components FonSMT3, FonAOS1, FonUBC9, and FonMMS21 are predominantly located in the nucleus.FonSMT3,FonAOS1,FonUBC9, andFonMMS21are highly expressed in the germinating macroconidia, but their expression is downregulated gradually in infected watermelon roots with the disease progression. The disruption ofFonUBA2andFonSIZ1seems to be lethal inFon. The deletion mutant strains forFonSMT3,FonAOS1,FonUBC9, andFonMMS21are viable, but exhibit significant defects in vegetative growth, asexual reproduction, conidial morphology, spore germination, responses to metal ions and DNA-damaging agents, and apoptosis. The disruption ofFonSMT3,FonAOS1,FonUBC9, andFonMMS21enhances sensitivity to cell wall-perturbing agents, but confers tolerance to digestion by cell wall-degrading enzymes. Furthermore, the disruption ofFonSMT3,FonAOS1, andFonUBC9negatively regulates autophagy inFon. Overall, these results demonstrate that the SUMOylation pathway plays vital roles in regulating multiple basic biological processes inFon, and, thus, can serve as a potential target for developing a disease management approach to control Fusarium wilt in watermelon.Keywords:asexual reproduction;cell death;cell wall integrity;Fusarium oxysporumf. sp.niveum;mycelial growth;stress response;SUMOylation pathway;watermelon