A selfish DNA element engages a meiosis-specific motor and telomeres for germ-line propagation

J Cell Biol. 2014 Jun 9;205(5):643-61. doi: 10.1083/jcb.201312002.

Abstract

The chromosome-like mitotic stability of the yeast 2 micron plasmid is conferred by the plasmid proteins Rep1-Rep2 and the cis-acting locus STB, likely by promoting plasmid-chromosome association and segregation by hitchhiking. Our analysis reveals that stable plasmid segregation during meiosis requires the bouquet proteins Ndj1 and Csm4. Plasmid relocalization from the nuclear interior in mitotic cells to the periphery at or proximal to telomeres rises from early meiosis to pachytene. Analogous to chromosomes, the plasmid undergoes Csm4- and Ndj1-dependent rapid prophase movements with speeds comparable to those of telomeres. Lack of Ndj1 partially disrupts plasmid-telomere association without affecting plasmid colocalization with the telomere-binding protein Rap1. The plasmid appears to engage a meiosis-specific motor that orchestrates telomere-led chromosome movements for its telomere-associated segregation during meiosis I. This hitherto uncharacterized mode of germ-line transmission by a selfish genetic element signifies a mechanistic variation within the shared theme of chromosome-coupled plasmid segregation during mitosis and meiosis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Cell Cycle Proteins / genetics
  • Chromosome Segregation
  • Chromosomes, Fungal / genetics
  • Cytoskeletal Proteins / genetics
  • DNA, Fungal / genetics*
  • Gene Expression Regulation, Fungal*
  • Genes, Reporter
  • Green Fluorescent Proteins / metabolism
  • Kinetochores
  • Meiosis*
  • Membrane Proteins / genetics
  • Mitosis
  • Nuclear Proteins / genetics
  • Plasmids / metabolism
  • Prophase
  • Repetitive Sequences, Nucleic Acid / genetics*
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae Proteins / genetics
  • Spindle Apparatus / genetics
  • Telomere / ultrastructure*
  • Telomere-Binding Proteins / genetics
  • Transcription Factors / genetics

Substances

  • CSM4 protein, S cerevisiae
  • CTF19 protein, S cerevisiae
  • Cell Cycle Proteins
  • Cytoskeletal Proteins
  • DNA, Fungal
  • Membrane Proteins
  • Mps3 protein, S cerevisiae
  • Ndj1 protein, S cerevisiae
  • Nuclear Proteins
  • RAP1 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Telomere-Binding Proteins
  • Transcription Factors
  • Green Fluorescent Proteins