Filamentation Regulatory Pathways Control Adhesion-Dependent Surface Responses in Yeast

Genetics. 2019 Jul;212(3):667-690. doi: 10.1534/genetics.119.302004. Epub 2019 May 3.

Abstract

Signaling pathways can regulate biological responses by the transcriptional regulation of target genes. In yeast, multiple signaling pathways control filamentous growth, a morphogenetic response that occurs in many species including fungal pathogens. Here, we examine the role of signaling pathways that control filamentous growth in regulating adhesion-dependent surface responses, including mat formation and colony patterning. Expression profiling and mutant phenotype analysis showed that the major pathways that regulate filamentous growth [filamentous growth MAPK (fMAPK), RAS, retrograde (RTG), RIM101, RPD3, ELP, SNF1, and PHO85] also regulated mat formation and colony patterning. The chromatin remodeling complex, SAGA, also regulated these responses. We also show that the RAS and RTG pathways coregulated a common set of target genes, and that SAGA regulated target genes known to be controlled by the fMAPK, RAS, and RTG pathways. Analysis of surface growth-specific targets identified genes that respond to low oxygen, high temperature, and desiccation stresses. We also explore the question of why cells make adhesive contacts in colonies. Cell adhesion contacts mediated by the coregulated target and adhesion molecule, Flo11p, deterred entry into colonies by macroscopic predators and impacted colony temperature regulation. The identification of new regulators (e.g., SAGA), and targets of surface growth in yeast may provide insights into fungal pathogenesis in settings where surface growth and adhesion contributes to virulence.

Keywords: MAPK pathways; biofilm; complex colony; expression profiling; fungal pathogenesis; invasive growth; mat; microbial predator–prey relationships; pseudohyphal growth; signaling networks; temperature control.

Publication types

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

MeSH terms

  • Biofilms*
  • Cell Adhesion*
  • Cyclin-Dependent Kinases / genetics
  • Cyclin-Dependent Kinases / metabolism
  • Gene Expression Regulation, Fungal*
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism
  • Hyphae / genetics*
  • Hyphae / growth & development
  • MAP Kinase Signaling System
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / pathogenicity
  • Saccharomyces cerevisiae / physiology
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Virulence / genetics
  • ras Proteins / genetics
  • ras Proteins / metabolism

Substances

  • FLO11 protein, S cerevisiae
  • Membrane Glycoproteins
  • RIM101 protein, S cerevisiae
  • Repressor Proteins
  • SAGA complex, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Trans-Activators
  • SNF1-related protein kinases
  • Protein Serine-Threonine Kinases
  • Cyclin-Dependent Kinases
  • PHO85 protein, S cerevisiae
  • RPD3 protein, S cerevisiae
  • Histone Deacetylases
  • ras Proteins