Regulatory insight for a Zn2Cys6 transcription factor controlling effector-mediated virulence in a fungal pathogen of wheat

PLoS Pathog. 2024 Sep 23;20(9):e1012536. doi: 10.1371/journal.ppat.1012536. eCollection 2024 Sep.

Abstract

The regulation of virulence in plant-pathogenic fungi has emerged as a key area of importance underlying host infections. Recent work has highlighted individual transcription factors (TFs) that serve important roles. A prominent example is PnPf2, a member of the Zn2Cys6 family of fungal TFs, which controls the expression of effectors and other virulence-associated genes in Parastagonospora nodorum during infection of wheat. PnPf2 orthologues are similarly important for other major fungal pathogens during infection of their respective host plants, and have also been shown to control polysaccharide metabolism in model saprophytes. In each case, the direct genomic targets and associated regulatory mechanisms were unknown. Significant insight was made here by investigating PnPf2 through chromatin-immunoprecipitation (ChIP) and mutagenesis approaches in P. nodorum. Two distinct binding motifs were characterised as positive regulatory elements and direct PnPf2 targets identified. These encompass known effectors and other components associated with the P. nodorum pathogenic lifestyle, such as carbohydrate-active enzymes and nutrient assimilators. The results support a direct involvement of PnPf2 in coordinating virulence on wheat. Other prominent PnPf2 targets included TF-encoding genes. While novel functions were observed for the TFs PnPro1, PnAda1, PnEbr1 and the carbon-catabolite repressor PnCreA, our investigation upheld PnPf2 as the predominant transcriptional regulator characterised in terms of direct and specific coordination of virulence on wheat, and provides important mechanistic insights that may be conserved for homologous TFs in other fungi.

MeSH terms

  • Ascomycota* / genetics
  • Ascomycota* / metabolism
  • Ascomycota* / pathogenicity
  • Fungal Proteins* / genetics
  • Fungal Proteins* / metabolism
  • Gene Expression Regulation, Fungal*
  • Plant Diseases* / microbiology
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism
  • Triticum* / microbiology
  • Virulence

Substances

  • Transcription Factors
  • Fungal Proteins

Grants and funding

This study was supported by the Centre for Crop and Disease Management, a joint initiative of Curtin University (https://www.curtin.edu.au/) and the Grains Research and Development Corporation (https://grdc.com.au/) under the research grant CUR00023 Project F3 awarded to K-CT). EJ and SM were supported by an Australian Government Research Training Program Scholarship (https://www.dese.gov.au/) administered through Curtin University (https://www.curtin.edu.au/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.