Nitrogen-Metabolism Inhibitor NmrA Regulates Conidial Production, Melanin Synthesis, and Virulence in Phytopathogenic Fungus Verticillium dahliae

NmrA homologs have been reported as conserved regulators of nitrogen metabolite repression in various fungi. Here, we identified an NmrA homolog in Verticillium dahliae and reported its functions in nitrogen utilization, growth and development, and pathogenesis. VdNmrA interacts with the V. dahliae AreA protein and regulates the expression of a typical NMR target, the formamidase gene. VdNmrA deletion mutants exhibited significantly slower colony growth on media with Gln or Arg. Furthermore, VdNmrA deletion impaired hyphal growth, spore production, hyperosmotic stress tolerance, and melanin biosynthesis. Fewer reactive oxygen species were produced in VdNmrA mutants, and the NADPH oxidase genes noxA and noxB showed lowered expression levels compared with the wild type. VdNmrA mutants exhibited reduced virulence on cotton and Arabidopsis compared with wild-type strains. Our results indicated that VdNmrA functioned as a nitrogen metabolite repression repressor and played important roles in nutrient utilization, fungal development, stress tolerance, and pathogenicity in V. dahliae.