A highly redundant gene network controls assembly of the outer spore wall in S. cerevisiae

PLoS Genet. 2013;9(8):e1003700. doi: 10.1371/journal.pgen.1003700. Epub 2013 Aug 15.

Abstract

The spore wall of Saccharomyces cerevisiae is a multilaminar extracellular structure that is formed de novo in the course of sporulation. The outer layers of the spore wall provide spores with resistance to a wide variety of environmental stresses. The major components of the outer spore wall are the polysaccharide chitosan and a polymer formed from the di-amino acid dityrosine. Though the synthesis and export pathways for dityrosine have been described, genes directly involved in dityrosine polymerization and incorporation into the spore wall have not been identified. A synthetic gene array approach to identify new genes involved in outer spore wall synthesis revealed an interconnected network influencing dityrosine assembly. This network is highly redundant both for genes of different activities that compensate for the loss of each other and for related genes of overlapping activity. Several of the genes in this network have paralogs in the yeast genome and deletion of entire paralog sets is sufficient to severely reduce dityrosine fluorescence. Solid-state NMR analysis of partially purified outer spore walls identifies a novel component in spore walls from wild type that is absent in some of the paralog set mutants. Localization of gene products identified in the screen reveals an unexpected role for lipid droplets in outer spore wall formation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Cell Wall / genetics*
  • Cell Wall / metabolism
  • Chitosan / metabolism
  • Gene Expression Regulation, Fungal
  • Gene Regulatory Networks*
  • Lipid Metabolism / genetics*
  • Magnetic Resonance Spectroscopy
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / growth & development
  • Spores, Fungal / genetics*
  • Spores, Fungal / growth & development
  • Spores, Fungal / metabolism
  • Tyrosine / analogs & derivatives
  • Tyrosine / genetics
  • Tyrosine / metabolism

Substances

  • Tyrosine
  • Chitosan
  • dityrosine

Grant support

The research was funded by NIH grant R01 GM072540 to AMN. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.