Interorganelle interactions and inheritance patterns of nuclei and vacuoles in budding yeast meiosis

Autophagy. 2014 Feb;10(2):285-95. doi: 10.4161/auto.27192. Epub 2013 Dec 4.

Abstract

Many of the mechanisms by which organelles are inherited by spores during meiosis are not well understood. Dramatic chromosome motion and bouquet formation are evolutionarily conserved characteristics of meiotic chromosomes. The budding yeast bouquet genes (NDJ1, MPS3, CSM4) mediate these movements via telomere attachment to the nuclear envelope (NE). Here, we report that during meiosis the NE is in direct contact with vacuoles via nucleus-vacuole junctions (NVJs). We show that in meiosis NVJs are assembled through the interaction of the outer NE-protein Nvj1 and the vacuolar membrane protein Vac8. Notably, NVJs function as diffusion barriers that exclude the nuclear pore complexes, the bouquet protein Mps3 and NE-tethered telomeres from the outer nuclear membrane and nuclear ER, resulting in distorted NEs during early meiosis. An increase in NVJ area resulting from Nvj1-GFP overexpression produced a moderate bouquet mutant-like phenotype in wild-type cells. NVJs, as the vacuolar contact sites of the nucleus, were found to undergo scission alongside the NE during meiotic nuclear division. The zygotic NE and NVJs were partly segregated into 4 spores. Lastly, new NVJs were also revealed to be synthesized de novo to rejoin the zygotic NE with the newly synthesized vacuoles in the mature spores. In conclusion, our results revealed that budding yeast nuclei and vacuoles exhibit dynamic interorganelle interactions and different inheritance patterns in meiosis, and also suggested that nvj1Δ mutant cells may be useful to resolve the technical challenges pertaining to the isolation of intact nuclei for the biochemical study of meiotic nuclear proteins.

Keywords: bouquet formation; meiosis; nuclear envelope; nucleus-vacuole junction; piecemeal microautophagy of the nucleus; rapid prophase movements; vacuoles.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy / genetics
  • Autophagy / physiology*
  • Cell Cycle Proteins / genetics
  • Cell Nucleus / metabolism*
  • Inheritance Patterns / genetics
  • Inheritance Patterns / physiology*
  • Meiosis / physiology*
  • Nuclear Envelope / metabolism
  • Saccharomycetales / cytology
  • Saccharomycetales / genetics
  • Saccharomycetales / metabolism*
  • Vacuoles / metabolism*

Substances

  • Cell Cycle Proteins