Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation.

Kiran Challa,Ghanim Fajish V,Miki Shinohara,Susan M Gasser,Franz Klein,Akira Shinohara,Michael Lichten

doi:10.1371/journal.pgen.1007851

Abstract

Sister chromatid cohesion on chromosome arms is essential for the segregation of homologous chromosomes during meiosis I while it is dispensable for sister chromatid separation during mitosis. It was assumed that, unlike the situation in mitosis, chromosome arms retain cohesion prior to onset of anaphase-I. Paradoxically, reduced immunostaining signals of meiosis-specific cohesin, including the kleisin Rec8, were observed on chromosomes during late prophase-I of budding yeast. This decrease is seen in the absence of Rec8 cleavage and depends on condensin-mediated recruitment of Polo-like kinase (PLK/Cdc5). In this study, we confirmed that this release indeed accompanies the dissociation of acetylated Smc3 as well as Rec8 from meiotic chromosomes during late prophase-I. This release requires, in addition to PLK, the cohesin regulator, Wapl (Rad61/Wpl1 in yeast), and Dbf4-dependent Cdc7 kinase (DDK). Meiosis-specific phosphorylation of Rad61/Wpl1 and Rec8 by PLK and DDK collaboratively promote this release. This process is similar to the vertebrate “prophase” pathway for cohesin release during G2 phase and pro-metaphase. In yeast, meiotic cohesin release coincides with PLK-dependent compaction of chromosomes in late meiotic prophase-I. We suggest that yeast uses this highly regulated cleavage-independent pathway to remove cohesin during late prophase-I to facilitate morphogenesis of condensed metaphase-I chromosomes.

Highlights

Meiosis gives rise to haploid gametes from diploid germ cells
It is currently believed that the physical connections between homologous chromosomes are maintained by meiotic cohesin with exceptional stability
Our results suggest that late meiotic prophase-I actively controls cohesin dynamics on meiotic chromosomes for chromosome segregation

Summary

Introduction

Meiosis gives rise to haploid gametes from diploid germ cells. A single round of DNA replication is followed by two consecutive chromosome segregations, meiosis I and II, which reduce the number of chromosomes by half [1]. Homologous chromosomes are separated during meiosis I (MI), and sister chromatids are segregated during meiosis II (MII). Sister chromatid cohesion (SCC) acts as physical connection between the segregating chromosomes and provides resistance to pulling forces by microtubules. SCC along chromosome arms and at the kinetochore plays a critical role in chromosome segregation during MI and MII, respectively. For accurate chromosome segregation at MI, SCC along chromosome arms, and chiasmata, which are the cytological manifestation of crossovers, are essential for generating tension between the homologous chromosomes

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Conclusion