Regulation of Polo Kinase by Matrimony Is Required for Cohesin Maintenance during Drosophila melanogaster Female Meiosis

Curr Biol. 2020 Feb 24;30(4):715-722.e3. doi: 10.1016/j.cub.2019.12.027. Epub 2020 Jan 30.

Abstract

Polo-like kinases (PLKs) have numerous roles in both mitosis and meiosis, including functions related to chromosome segregation, cohesin removal, and kinetochore orientation [1-7]. PLKs require specific regulation during meiosis to control those processes. Genetic studies demonstrate that the Drosophila PLK Polo kinase (Polo) is inhibited by the female meiosis-specific protein Matrimony (Mtrm) in a stoichiometric manner [8]. Drosophila Polo localizes strongly to kinetochores and to central spindle microtubules during prometaphase and metaphase I of female meiosis [9, 10]. Mtrm protein levels increase dramatically after nuclear envelope breakdown [11]. We show that Mtrm is enriched along the meiotic spindle and that loss of mtrm results in mislocalization of the catalytically active form of Polo. The mtrm gene is haploinsufficient, and heterozygosity for mtrm (mtrm/+) results in high levels of achiasmate chromosome missegregation [8, 12]. In mtrm/+ heterozygotes, there is a low level of sister centromere separation, as well as precocious loss of cohesion along the arms of achiasmate chromosomes. However, mtrm-null females are sterile [13], and sister chromatid cohesion is abolished on all chromosomes, leading to a failure to properly congress or orient chromosomes in metaphase I. These data demonstrate a requirement for the inhibition of Polo, perhaps by sequestering Polo to the microtubules during Drosophila melanogaster female meiosis and suggest that catalytically active Polo is a distinct subset of the total Polo population within the oocyte that requires its own regulation.

Keywords: Polo kinase; centromere fusion; chromosome segregation; cohesion; kinetochores; meiosis; microtubules.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Cycle Proteins / metabolism*
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / physiology*
  • Female
  • Meiosis*
  • Protein-Serine-Threonine Kinases / metabolism*

Substances

  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • Drosophila Proteins
  • cohesins
  • mtrm protein, Drosophila
  • polo protein, Drosophila
  • Protein-Serine-Threonine Kinases