An interplay between Shugoshin and Spo13 for centromeric cohesin protection and sister kinetochore mono-orientation during meiosis I in Saccharomyces cerevisiae

Curr Genet. 2018 Oct;64(5):1141-1152. doi: 10.1007/s00294-018-0832-x. Epub 2018 Apr 11.

Abstract

Meiosis is a specialized cell division process by which haploid gametes are produced from a diploid mother cell. Reductional chromosome segregation during meiosis I (MI) is achieved by two unique and conserved events: centromeric cohesin protection (CCP) and sister kinetochore mono-orientation (SKM). In Saccharomyces cerevisiae, a meiosis-specific protein Spo13 plays a role in both these centromere-specific events. Despite genome-wide association of Spo13, we failed to detect its function in global processes such as cohesin loading, cohesion establishment and homologs pairing. While Shugoshin (Sgo1) and protein phosphatase 2A (PP2ARts1) play a central role in CCP, it is not fully understood whether Spo13 functions in the process through a Sgo1- PP2ARts1-dependent or -independent mechanism. To delineate this and to find the relative contribution of each of these proteins in CCP and SKM, we meticulously observed the sister chromatid segregation pattern in the wild type, sgo1Δ, rts1Δ and spo13Δ single mutants and in their respective double mutants. We found that Spo13 protects centromeric cohesin through a Sgo1- PP2ARts1-independent mechanism. To our surprise, we observed a hitherto unknown role of Sgo1 in SKM. Further investigation revealed that Sgo1-mediated recruitment of aurora kinase Ipl1 to the centromere facilitates monopolin loading at the kinetochore during MI. Hence, this study uncovers the role of Sgo1 in SKM and demonstartes how the regulators (Sgo1, PP2ARts1, Spo13) work in a coordinated manner to achieve faithful chromosome segregation during meiosis, the failure of which leads to aneuploidy and birth defects.

Keywords: Cohesin; Meiosis; Mono-orientation; Saccharomyces cerevisiae; Sgo1; Spo13.

MeSH terms

  • Aurora Kinases / metabolism
  • Cell Cycle Proteins / metabolism*
  • Centromere / metabolism*
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Chromosome Segregation*
  • Chromosomes, Fungal
  • Cohesins
  • Genome, Fungal
  • Kinetochores / metabolism*
  • Meiosis*
  • Nuclear Proteins / metabolism*
  • Proton Pumps / metabolism
  • Saccharomyces cerevisiae / cytology
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / metabolism*

Substances

  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • Mam1 protein, S cerevisiae
  • Nuclear Proteins
  • Proton Pumps
  • SPO13 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Sgo1 protein, S cerevisiae
  • Aurora Kinases
  • IPL1 protein, S cerevisiae
  • PPA2 protein, S cerevisiae