Chiasmata Promote Monopolar Attachment of Sister Chromatids and Their Co-Segregation toward the Proper Pole during Meiosis I
Open Access
- 10 March 2011
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLoS Genetics
- Vol. 7 (3), e1001329
- https://doi.org/10.1371/journal.pgen.1001329
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. Gametes form through a special type of cell division called meiosis. During meiosis, two nuclear divisions take place successively; the first division is specific only to meiosis, in that homologous chromosomes segregate from each other. Homologous chromosome segregation requires physical association of the homologous chromosomes by a structure called chiasma that forms at the site of recombination. This association is thought to contribute to proper attachment of homologous chromosomes to the spindle, leading to their proper segregation. In this study, we examined the functions of chiasmata during the first division in fission yeast by analyzing chromosome dynamics and segregation in several different mutants lacking chiasmata. We found that, in addition to proper spindle attachment of homologous chromosomes, chiasmata contribute to proper spindle attachment of replicated chromosomes more substantially than previously had been thought. In addition, even when chromosomes are improperly attached to the spindle, chiasmata eventually cause proper chromosome segregation. Our findings reinforce the significance of the physical association of homologous chromosomes in proper spindle attachment of chromosomes and have unveiled a previously unidentified, chiasma-dependent mechanism that ensures proper chromosome segregation.Keywords
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