Abstract
Establishment of proper chromosome attachments to the spindle requires elimination of erroneous attachments, but the mechanism of this process is not fully understood. During meiosis I, sister chromatids attach to the same spindle pole (mono-oriented attachment), whereas homologous chromosomes attach to opposite poles (bi-oriented attachment), resulting in homologous chromosome segregation. Here, we show that chiasmata that link homologous chromosomes and kinetochore component Dam1 are crucial for elimination of erroneous attachments and oscillation of centromeres between the spindle poles at meiosis I in fission yeast. In chiasma-forming cells, Mad2 and Aurora B kinase, which provides time for attachment correction and destabilizes erroneous attachments, respectively, caused elimination of bi-oriented attachments of sister chromatids, whereas in chiasma-lacking cells, they caused elimination of mono-oriented attachments. In chiasma-forming cells, in addition, homologous centromere oscillation was coordinated. Furthermore, Dam1 contributed to attachment elimination in both chiasma-forming and chiasma-lacking cells, and drove centromere oscillation. These results demonstrate that chiasmata alter attachment correction patterns by enabling error correction factors to eliminate bi-oriented attachment of sister chromatids, and suggest that Dam1 induces elimination of erroneous attachments. The coincidental contribution of chiasmata and Dam1 to centromere oscillation also suggests a potential link between centromere oscillation and attachment elimination.
Highlights
Faithful segregation of chromosomes during cell division is essential for genome integrity
We hypothesized that chiasmata change the attachment types that are eliminated by the error correction mechanism such that, in the presence of chiasmata, the mechanism selectively eliminates bi-oriented attachment of sister chromatids, thereby retaining mono-oriented attachment in contrast with the situation in mitosis
We deleted the sgo1 gene, which encodes one of two Shugoshin proteins of fission yeast that functions as a centromere cohesion protector during meiosis and prevents separation of sister chromatids attached to opposite poles [28,30,31,32,33]
Summary
Faithful segregation of chromosomes during cell division is essential for genome integrity. During division of a somatic cell (mitosis), duplicated chromosomes (sister chromatids) attach to opposite spindle poles (bi-oriented attachment) via microtubules (MTs) and segregate from each other (equational segregation). Such a division generates two genetically identical daughter cells (figure 1a, mitosis) [2]. By contrast, during the first of two consecutive divisions of a germ cell (meiosis), homologous chromosomes attach to opposite poles and segregate, leading to generation of gametes containing half the original number of chromosomes (figure 1a, meiosis I). Chromosomes attach to the spindle randomly via kinetochores, which are protein complexes that assemble at centromeres [7,8,9]. Kinetochores initially attach to royalsocietypublishing.org/journal/rsob Open Biol. 11: 200308
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