Reductional Meiosis I Chromosome Segregation Is Established by Coordination of Key Meiotic Kinases

Dev Cell. 2019 May 20;49(4):526-541.e5. doi: 10.1016/j.devcel.2019.04.003. Epub 2019 Apr 25.

Abstract

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.

Keywords: DDK; Hrr25; Polo kinase; Spo13; chromosome segregation; cohesin; kinetochore; meiosis; monoorientation; shugoshin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Cycle Proteins / metabolism
  • Centromere / metabolism
  • Chromatids / physiology
  • Chromosomal Proteins, Non-Histone / metabolism
  • Chromosome Segregation / genetics
  • Chromosome Segregation / physiology*
  • Cohesins
  • Kinetochores / metabolism
  • Kinetochores / physiology*
  • Meiosis / physiology*
  • Nuclear Proteins / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • Protein Serine-Threonine Kinases / physiology
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / metabolism
  • Saccharomyces cerevisiae Proteins / physiology
  • Schizosaccharomyces / genetics
  • Schizosaccharomyces / metabolism
  • Schizosaccharomyces pombe Proteins / metabolism
  • Schizosaccharomyces pombe Proteins / physiology

Substances

  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • Moa1 protein, S pombe
  • Nuclear Proteins
  • SPO13 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Schizosaccharomyces pombe Proteins
  • Plo1 protein, S pombe
  • Protein Serine-Threonine Kinases