Quiescent Saccharomyces cerevisiae forms telomere hyperclusters at the nuclear membrane vicinity through a multifaceted mechanism involving Esc1, the Sir complex, and chromatin condensation

Mol Biol Cell. 2016 Jun 15;27(12):1875-84. doi: 10.1091/mbc.E16-01-0069. Epub 2016 Apr 27.

Abstract

Like other eukaryotes, Saccharomyces cerevisiae spatially organizes its chromosomes within the nucleus. In G1 phase, the yeast's 32 telomeres are clustered into 6-10 foci that dynamically interact with the nuclear membrane. Here we show that, when cells leave the division cycle and enter quiescence, telomeres gather into two to three hyperclusters at the nuclear membrane vicinity. This localization depends on Esc1 but not on the Ku proteins. Telomere hypercluster formation requires the Sir complex but is independent of the nuclear microtubule bundle that specifically assembles in quiescent cells. Importantly, mutants deleted for the linker histone H1 Hho1 or defective in condensin activity or affected for histone H4 Lys-16 deacetylation are impaired, at least in part, for telomere hypercluster formation in quiescence, suggesting that this process involves chromosome condensation. Finally, we establish that telomere hypercluster formation is not necessary for quiescence establishment, maintenance, and exit, raising the question of the physiological raison d'être of this nuclear reorganization.

MeSH terms

  • Adenosine Triphosphatases / metabolism
  • Chromatin / metabolism
  • Chromatin / physiology
  • Chromatin Assembly and Disassembly / physiology
  • DNA-Binding Proteins / metabolism
  • G1 Phase
  • Heterochromatin / metabolism
  • Histones / metabolism
  • Multiprotein Complexes / metabolism
  • Nuclear Envelope / metabolism
  • Nuclear Envelope / physiology
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Silent Information Regulator Proteins, Saccharomyces cerevisiae / genetics
  • Silent Information Regulator Proteins, Saccharomyces cerevisiae / metabolism
  • Telomere / metabolism*
  • Telomere / physiology*

Substances

  • Chromatin
  • DNA-Binding Proteins
  • Esc1 protein, S cerevisiae
  • Heterochromatin
  • Histones
  • Multiprotein Complexes
  • Nuclear Proteins
  • Saccharomyces cerevisiae Proteins
  • Silent Information Regulator Proteins, Saccharomyces cerevisiae
  • condensin complexes
  • Adenosine Triphosphatases