Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals

Elife. 2021 Oct 12:10:e68058. doi: 10.7554/eLife.68058.

Abstract

Fungal Hülle cells with nuclear storage and developmental backup functions are reminiscent of multipotent stem cells. In the soil, Hülle cells nurse the overwintering fruiting bodies of Aspergillus nidulans. The genome of A. nidulans harbors genes for the biosynthesis of xanthones. We show that enzymes and metabolites of this biosynthetic pathway accumulate in Hülle cells under the control of the regulatory velvet complex, which coordinates development and secondary metabolism. Deletion strains blocked in the conversion of anthraquinones to xanthones accumulate emodins and are delayed in maturation and growth of fruiting bodies. Emodin represses fruiting body and resting structure formation in other fungi. Xanthones are not required for sexual development but exert antifeedant effects on fungivorous animals such as springtails and woodlice. Our findings reveal a novel role of Hülle cells in establishing secure niches for A. nidulans by accumulating metabolites with antifeedant activity that protect reproductive structures from animal predators.

Keywords: Hülle cells; aspergillus nidulans; biochemistry; chemical biology; ecology; emodin; folsomia candida; secondary metabolites; sexual development; sordaria macrospora; tenebrio molitor; trichorhina tomentosa; verticillium; xanthones.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anthraquinones / metabolism
  • Arthropods*
  • Aspergillus nidulans / genetics
  • Aspergillus nidulans / growth & development
  • Aspergillus nidulans / metabolism*
  • Crustacea
  • Feeding Behavior*
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism*
  • Gene Expression Regulation, Developmental
  • Gene Expression Regulation, Fungal
  • Mutation
  • Predatory Behavior*
  • Secondary Metabolism*
  • Soil Microbiology*
  • Spores, Fungal / genetics
  • Spores, Fungal / growth & development
  • Spores, Fungal / metabolism*
  • Tenebrio
  • Time Factors
  • Xanthones / metabolism

Substances

  • Anthraquinones
  • Fungal Proteins
  • Xanthones

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.