Pyrrocidine, a molecular off switch for fumonisin biosynthesis

PLoS Pathog. 2020 Jul 6;16(7):e1008595. doi: 10.1371/journal.ppat.1008595. eCollection 2020 Jul.

Abstract

Sarocladium zeae is a fungal endophyte of maize and can be found co-inhabiting a single seed with Fusarium verticillioides, a major mycotoxigenic food safety threat. S. zeae produces pyrrocidines A and B that inhibit the growth of F. verticillioides and may limit its spread within the seed to locations lacking S. zeae. Although coinhabiting single seeds, the fungi are generally segregated in separate tissues. To understand F. verticillioides' protective physiological response to pyrrocidines we sequenced the F. verticillioides transcriptome upon exposure to purified pyrrocidine A or B at sub-inhibitory concentrations. Through this work we identified a F. verticillioides locus FvABC3 (FVEG_11089) encoding a transporter critical for resistance to pyrrocidine. We also identified FvZBD1 (FVEG_00314), a gene directly adjacent to the fumonisin biosynthetic gene cluster that was induced several thousand-fold in response to pyrrocidines. FvZBD1 is postulated to act as a genetic repressor of fumonisin production since deletion of the gene resulted in orders of magnitude increase in fumonisin. Further, pyrrocidine acts, likely through FvZBD1, to shut off fumonisin biosynthesis. This suggests that S. zeae is able to hack the secondary metabolic program of a competitor fungus, perhaps as preemptive self-protection, in this case impacting a mycotoxin of central concern for food safety.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acremonium*
  • Bridged-Ring Compounds / metabolism
  • Bridged-Ring Compounds / pharmacology
  • Coinfection
  • Disease Resistance / genetics
  • Fumonisins / metabolism*
  • Fusarium / genetics*
  • Genes, Fungal
  • Mycoses / metabolism
  • Mycoses / microbiology*
  • Plant Diseases / microbiology*
  • Pyrrolidinones / metabolism
  • Pyrrolidinones / pharmacology
  • Zea mays / microbiology*

Substances

  • Bridged-Ring Compounds
  • Fumonisins
  • Pyrrolidinones
  • pyrrocidine A
  • pyrrocidine B

Grants and funding

This work was supported by US Department of Agriculture, Agricultural Research Service (USDA-ARS) project number 6040-42000-043-00D. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.