Meiosis: cell-cycle controls shuffle and deal

Key Points Meiosis is a specialized type of cell division in which two rounds of chromosome segregation follow a single round of DNA replication. In diploid organisms, meiosis generates gametes with a haploid number of chromosomes. Both general cell-cycle regulators and meiosis-specific proteins bring about this modified cell division. Although pre-meiotic S phase uses the same replicative machinery as pre-mitotic S phase, its completion takes longer, probably because interactions between homologous chromosomes (homologues) — such as meiotic recombination, pairing of homologues and the formation of the synaptonemal complex — are being initiated during S phase. Meiosis I is a unique chromosome-segregation event in which homologues segregate away from each other. Meiotic recombination during G2 generates chiasmata, which are important in holding homologues together, in preparation for their segregation during meiosis I. Sister-chromatid cohesion is lost in a stepwise manner during meiosis. In yeast, the loss of the cohesin Rec8 on chromosome arms during meiosis I allows homologues to segregate away from each other. Rec8 at the centromere is retained, however, and holds sister chromatids together until meiosis II. MEI-S332/Sgo1 has an important role in protecting Rec8 from loss at the centromere during meiosis I. In meiosis I, sister chromatids uniquely attach to microtubules from the same pole (monopolar attachment), whereas, in meiosis II, kinetochores attach to microtubules from opposite poles (bipolar attachment). In budding yeast, a complex known as monopolin was identified, which ensures the monopolar attachment of kinetochores during meiosis I. The existence of two consecutive chromosome-segregation events during meiosis, without an intervening S phase, requires specialization of cell-cycle controls to execute the meiosis-I–meiosis-II transition. In some organisms this is achieved by a partial reduction in cyclin-dependent-kinase activity. Meiosis is the type of cell division that gives rise to eggs and sperm. Errors in the execution of this process can result in the generation of aneuploid gametes, which are associated with birth defects and infertility in humans. Here, we review recent findings on how cell-cycle controls ensure the coordination of meiotic events, with a particular focus on the segregation of chromosomes.