Systematic analysis of F-box proteins reveals a new branch of the yeast mating pathway

J Biol Chem. 2019 Oct 4;294(40):14717-14731. doi: 10.1074/jbc.RA119.010063. Epub 2019 Aug 9.

Abstract

The mating pathway in yeast Saccharomyces cerevisiae has long been used to reveal new mechanisms of signal transduction. The pathway comprises a pheromone receptor, a heterotrimeric G protein, and intracellular effectors of morphogenesis and transcription. Polarized cell growth, in the direction of a potential mating partner, is accomplished by the G-protein βγ subunits and the small G-protein Cdc42. Transcription induction, needed for cell-cell fusion, is mediated by Gβγ and the mitogen-activated protein kinase (MAPK) scaffold protein Ste5. A potential third pathway is initiated by the G-protein α subunit Gpa1. Gpa1 signaling was shown previously to involve the F-box adaptor protein Dia2 and an endosomal effector protein, the phosphatidylinositol 3-kinase Vps34. Vps34 is also required for proper vacuolar sorting and autophagy. Here, using a panel of reporter assays, we demonstrate that mating pheromone stimulates vacuolar targeting of a cytoplasmic reporter protein and that this process depends on Vps34. Through a systematic analysis of F-box deletion mutants, we show that Dia2 is required to sustain pheromone-induced vacuolar targeting. We also found that other F-box proteins selectively regulate morphogenesis (Ydr306, renamed Pfu1) and transcription (Ucc1). These findings point to the existence of a new and distinct branch of the pheromone-signaling pathway, one that likely leads to vacuolar engulfment of cytoplasmic proteins and recycling of cellular contents in preparation for mating.

Keywords: F-box; G protein; fungal mating; mitogen-activated protein kinase (MAPK); pheromone signaling; protein sorting; ubiquitin; yeast.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Cell Cycle / genetics
  • Class III Phosphatidylinositol 3-Kinases / genetics*
  • Endosomes / genetics
  • F-Box Proteins / chemistry
  • F-Box Proteins / genetics*
  • GTP-Binding Protein alpha Subunits, Gq-G11 / genetics
  • GTP-Binding Protein beta Subunits / chemistry
  • GTP-Binding Protein beta Subunits / genetics
  • GTP-Binding Protein gamma Subunits / chemistry
  • GTP-Binding Protein gamma Subunits / genetics
  • Genes, Mating Type, Fungal / genetics*
  • Morphogenesis / genetics
  • Pheromones / genetics
  • Pheromones / metabolism
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / physiology
  • Saccharomyces cerevisiae Proteins / genetics*
  • Sequence Deletion / genetics
  • Signal Transduction
  • Transcription, Genetic
  • Vacuoles / genetics
  • Vacuoles / metabolism
  • cdc42 GTP-Binding Protein / genetics

Substances

  • Adaptor Proteins, Signal Transducing
  • Dia2 protein, S cerevisiae
  • F-Box Proteins
  • G-protein Beta gamma
  • GTP-Binding Protein beta Subunits
  • GTP-Binding Protein gamma Subunits
  • Pheromones
  • STE5 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Class III Phosphatidylinositol 3-Kinases
  • GPA1 protein, S cerevisiae
  • GTP-Binding Protein alpha Subunits, Gq-G11
  • cdc42 GTP-Binding Protein