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Galander, Stefan; Barton, Rachael E.; Borek, Weronika E.; Spanos, Christos; Kelly, David A.; Robertson, Daniel; Rappsilber, Juri; Marston, Adèle L.
Developmental cell, 05/2019, Volume: 49, Issue: 4Journal Article
Meiosis produces gametes through a specialized, two-step cell division, which is highly error prone in humans. Reductional meiosis I, where maternal and paternal chromosomes (homologs) segregate, is followed by equational meiosis II, where sister chromatids separate. Uniquely during meiosis I, sister kinetochores are monooriented and pericentromeric cohesin is protected. Here, we demonstrate that these key adaptations for reductional chromosome segregation are achieved through separable control of multiple kinases by the meiosis-I-specific budding yeast Spo13 protein. Recruitment of Polo kinase to kinetochores directs monoorientation, while independently, cohesin protection is achieved by containing the effects of cohesin kinases. Therefore, reductional chromosome segregation, the defining feature of meiosis, is established by multifaceted kinase control by a master regulator. The recent identification of Spo13 orthologs, fission yeast Moa1 and mouse MEIKIN, suggests that kinase coordination by a meiosis I regulator may be a general feature in the establishment of reductional chromosome segregation. Display omitted •Spo13 recruits Polo kinase to kinetochores to direct sister chromatid co-segregation•Kinetochore-associated Polo drives co-segregation independently of monopolin•Spo13 counteracts cohesin kinases to prevent premature loss of centromeric cohesion•Spo13 restricts CK1δ to allow shugoshin reaccumulation after meiosis I Segregation of homologs—rather than sister chromatids—is unique to meiosis I. Galander et al. show that the meiosis-I-specific Spo13 protein prevents sister chromatid segregation by controlling the effects of multiple kinases to both enforce sister kinetochore co-orientation and prevent premature loss of cohesion.
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