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Plant pathogens generally employ superoxide dismutase (SOD) to detoxify host defense reactive oxygen species (ROS), and to scavenge ROS derived from their own metabolism. However, the roles of SODs in an important vascular pathogen, Verticillium dahliae, are unclear. Our previous study has shown that a putative signal-peptide-lacking manganese superoxide dismutase (VdSOD3) is present in the exoproteome of V. dahliae cultured in tissues of host cotton, suggesting that VdSOD3 may be exported out of the fungal cells and contribute to the SOD activity extracellularly. Here, we confirm that the N-terminal of VdSOD3 is not a functional signal peptide by yeast signal trap assay. Despite lacking the signal peptide, the extracellular distribution of VdSOD3 was observed in planta by confocal microscopy during infection. Loss-of-function of VdSOD3 decreased extracellular and intracellular SOD activities of V. dahliae by 58.2% and 17.4%, respectively. Deletion mutant of VdSOD3 had normal growth and conidiation but showed significantly reduced virulence to susceptible hosts of cotton and Nicotiana benthamiana. Our data show that signal-peptide-lacking VdSOD3 is a dual function superoxide dismutase, localizing and functioning intracellularly and extracellularly. Whereas nonessential for viability, VdSOD3 plays a vital role in the virulence of V. dahliae.

Unconventionally Secreted Manganese Superoxide Dismutase VdSOD3 Is Required for the Virulence of Verticillium dahliae