Chiasmata Promote Monopolar Attachment of Sister Chromatids and Their Co-Segregation toward the Proper Pole during Meiosis I

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.

Meiosis and Maternal Aging: Insights from Aneuploid Oocytes and Trisomy Births

“…Recently, a meiosis-specific kinetochore protein (Meiken) has been reported to facilitate monopolar attachment in mouse oocytes (Kim et al 2014). Monopolar attachment in fission yeast is also promoted by chiasmata (Hirose et al 2011;Sakuno et al 2011). Consistent with this, sister kinetochores of univalent chromosomes frequently establish microtubule attachments with both poles of the MI spindle in mouse oocytes (Le Maire-Adkins et al 1997;Kouznetsova et al 2007;Nagaoka et al 2011) and yeast (Sakuno et al 2011).…”

Origins of Eukaryotic Sexual Reproduction

“…Independent assortment produces diversity in the meiotic products of heterozygotes regardless of levels of crossing over, and chiasmata have been shown to play an additional role, aligning homologous chromosomes and providing tension on the spindle for accurate meiosis I segregation (Hirose et al 2011). …”

Sister chromatid segregation in meiosis II: Deprotection through phosphorylation

“…70 Furthermore in S. pombe the absence of chiasmata leads to a bipolar attachment of sister chromatids in meiosis I and, in contrast to the situation observed in Bub1 mutants, 66 also to a failure in removing centromeric cohesin and separating sisters. [71][72][73] In mammalian meiosis, subtle changes in the localization of Sgo2 in meiosis I and II are visible on squashes of spermatocytes and whole-mount immunofluorescence of oocytes. 53,55 In short, in meiosis I, a colocalization of cohesin with Sgo2 is observed, whereas in meiosis II, Sgo2 is relocalized-apparently in a tension-dependent manner-toward the outside of the centromere, and colocalization with centromeric cohesin is therefore lost.…”