The bZIP transcription factor VdAtf1 regulates virulence by mediating nitrogen metabolism in Verticillium dahliae

Authors: TANG, CHEN - Beijing Forestry University; LI, TIANYU - Beijing Forestry University; Klosterman, Steven; TIAN, CHENGMING - Beijing Forestry University; WANG, YONGLIN - Beijing Forestry University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/4/2020
Publication Date: 2/10/2020
Citation: Tang, C., Li, T., Klosterman, S.J., Tian, C., Wang, Y. 2020. The bZIP transcription factor VdAtf1 regulates virulence by mediating nitrogen metabolism in Verticillium dahliae. New Phytologist. 226(5):1461-1479. https://doi.org/10.1111/nph.16481.
DOI: https://doi.org/10.1111/nph.16481

Interpretive Summary: The soilborne fungus Verticillium dahliae causes the plant disease known as Verticillium wilt on a wide range of plant species. Determining how this fungus responds to stress and how it can utilize different carbon sources in the environment, and also how this organism responds to stress, may lead to alternative approaches to manage the disease or reduce its incidence. One particular gene in fungi that regulates the expression of genes whose protein products allow for the usage of different nitrogen sources is known as Atf, which is a gene regulatory factor. This study revealed that the Atf homolog in Verticillium dahliae, designated VdAtf1, controls pathogenesis via regulation of nitric oxide resistance and inorganic nitrogen metabolism and it is also critically important for plant infection. Insights on the functioning of VdAtf1 contributes to our knowledge of how V. dahliae infects plants, and how it responds to stress, and therefore may be useful to devise new molecular targets or strategies to eliminate or reduce the pathogen in the soil or as it infects the plant.

Technical Abstract: The fungus Verticillium dahliae causes vascular wilt disease on hundreds of plant species. Homologs of the bZIP transcription factor Atf1 are required for virulence in most pathogenic fungi, but the molecular basis for their involvement is largely unknown. We performed targeted gene deletion, expression analysis, biochemistry and pathogenicity assays to demonstrate that VdAtf1 governs pathogenesis via the regulation of nitrosative resistance and nitrogen metabolism in V. dahliae. VdAtf1 controls pathogenesis via the regulation of nitric oxide (NO) resistance and inorganic nitrogen metabolism rather than oxidative resistance and is important for penetration peg formation in V. dahliae. VdAtf1 affects ammonium and nitrate assimilation in response to various nitrogen sources. VdAtf1 may be involved in regulating the expression of VdNut1. VdAtf1 responds to NO stress by strengthening the fungal cell wall, and by causing over-accumulation of methylglyoxal and glycerol, which in turn impacts NO detoxification. We also verified that the VdAtf1 ortholog in Fusarium graminearum mediates nitrogen metabolism, suggesting conservation of this function in related plant pathogenic fungi. Our findings revealed new functions of VdAtf1 in pathogenesis, response to nitrosative stress and nitrogen metabolism in V. dahliae. The results provide novel insights into the regulatory mechanisms of the transcription factor VdAtf1 in virulence.