Shrinking Daughters: Rlm1-Dependent G1/S Checkpoint Maintains Saccharomyces cerevisiae Daughter Cell Size and Viability

Genetics. 2017 Aug;206(4):1923-1938. doi: 10.1534/genetics.117.204206. Epub 2017 Jun 21.

Abstract

The Rlm1 transcription factor is a target of the cell wall integrity pathway. We report that an rlm1Δ mutant grown on a nonfermentable carbon source at low osmolarity forms cell groups in which a mother cell is surrounded by smaller "satellite-daughter" cells. Mother cells in these groups progressed through repeated rounds of cell division with normal rates of bud growth and genetic stability; however, these cells underwent precocious START relative to wild-type mothers. Thus, once activated, Rlm1 delays the transition from G1 to S, a mechanism we term the cell wall/START (CW/START) checkpoint. The rlm1Δ satellite-cell phenotype is suppressed by deletion of either SLT2, which encodes the kinase that activates Rlm1, or SWI4, which is also activated by Slt2; suggesting that Slt2 can have opposing roles in regulating the START transition. Consistent with an Rlm1-dependent CW/START checkpoint, rlm1Δ satellite daughters were unable to grow or divide further even after transfer to rich medium, but UV irradiation in G1 could partially rescue rlm1Δ satellite daughters in the next division. Indeed, after cytokinesis, these satellite daughters shrank rapidly, displayed amorphous actin staining, and became more permeable. As a working hypothesis, we propose that duplication of an "actin-organizing center" in late G1 may be required both to progress through START and to reestablish the actin cytoskeleton in daughter cells.

Keywords: Paracoccidioides; Swe1; actin-organizing center; cytokinesis; satellite-cell group.

MeSH terms

  • Actins / metabolism
  • Cytokinesis*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • G1 Phase Cell Cycle Checkpoints*
  • MADS Domain Proteins / genetics*
  • MADS Domain Proteins / metabolism
  • Mitogen-Activated Protein Kinases / genetics
  • Mitogen-Activated Protein Kinases / metabolism
  • Osmolar Concentration
  • S Phase Cell Cycle Checkpoints*
  • Saccharomyces cerevisiae / cytology
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / physiology
  • Saccharomyces cerevisiae Proteins / genetics*
  • Saccharomyces cerevisiae Proteins / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Actins
  • DNA-Binding Proteins
  • MADS Domain Proteins
  • RLM1 protein, S cerevisiae
  • SWI4 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Transcription Factors
  • Mitogen-Activated Protein Kinases
  • SLT2 protein, S cerevisiae