Chiasmata promote monopolar attachment of sister chromatids and their co-segregation toward the proper pole during meiosis I

PLoS Genet. 2011 Mar;7(3):e1001329. doi: 10.1371/journal.pgen.1001329. Epub 2011 Mar 10.

Abstract

The chiasma is a structure that forms between a pair of homologous chromosomes by crossover recombination and physically links the homologous chromosomes during meiosis. Chiasmata are essential for the attachment of the homologous chromosomes to opposite spindle poles (bipolar attachment) and their subsequent segregation to the opposite poles during meiosis I. However, the overall function of chiasmata during meiosis is not fully understood. Here, we show that chiasmata also play a crucial role in the attachment of sister chromatids to the same spindle pole and in their co-segregation during meiosis I in fission yeast. Analysis of cells lacking chiasmata and the cohesin protector Sgo1 showed that loss of chiasmata causes frequent bipolar attachment of sister chromatids during anaphase. Furthermore, high time-resolution analysis of centromere dynamics in various types of chiasmate and achiasmate cells, including those lacking the DNA replication checkpoint factor Mrc1 or the meiotic centromere protein Moa1, showed the following three outcomes: (i) during the pre-anaphase stage, the bipolar attachment of sister chromatids occurs irrespective of chiasma formation; (ii) the chiasma contributes to the elimination of the pre-anaphase bipolar attachment; and (iii) when the bipolar attachment remains during anaphase, the chiasmata generate a bias toward the proper pole during poleward chromosome pulling that results in appropriate chromosome segregation. Based on these results, we propose that chiasmata play a pivotal role in the selection of proper attachments and provide a backup mechanism that promotes correct chromosome segregation when improper attachments remain during anaphase I.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anaphase
  • Cell Cycle Proteins / genetics
  • Centromere / metabolism
  • Centromere / ultrastructure
  • Chromatids / metabolism*
  • Chromatids / ultrastructure
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosome Segregation / physiology*
  • Chromosomes, Fungal / genetics
  • Chromosomes, Fungal / metabolism*
  • Chromosomes, Fungal / ultrastructure
  • DNA-Binding Proteins / genetics
  • Gene Deletion
  • Mad2 Proteins
  • Meiosis / physiology*
  • Nuclear Proteins / genetics
  • Schizosaccharomyces / cytology
  • Schizosaccharomyces / genetics*
  • Schizosaccharomyces pombe Proteins / genetics
  • Sister Chromatid Exchange / physiology*

Substances

  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • MRC1 protein, S pombe
  • Mad2 Proteins
  • Moa1 protein, S pombe
  • Nuclear Proteins
  • Schizosaccharomyces pombe Proteins
  • Sgo1 protein, S pombe
  • mad2 protein, S pombe
  • rec12 protein, S pombe