A ZIP1 Separation-of-Function Allele Reveals that Meiotic Centromere Pairing Drives Meiotic Segregation of Achiasmate Chromosomes in Budding Yeast

Abstract

ABSTRACTIn meiosis I, homologous chromosomes segregate away from each other - the first of two rounds of chromosome segregation that allow the formation of haploid gametes. In prophase I, homologous partners become joined along their length by the synaptonemal complex (SC) and crossovers form between the homologs to generate links called chiasmata. The chiasmata allow the homologs to act as a single unit, called a bivalent, as the chromosomes attach to the microtubules that will ultimately pull them away from each other at anaphase I. Recent studies, in several organisms, have shown that when the SC disassembles at the end of prophase, residual SC proteins remain at the homologous centromeres providing an additional link between the homologs. In budding yeast, this centromere pairing is correlated with improved segregation of the paired partners in anaphase. However, the causal relationship of prophase centromere pairing and subsequent disjunction in anaphase has been difficult to demonstrate as has been the relationship between SC assembly and the assembly of the centromere pairing apparatus. Here, a series of in-frame deletion mutants of the SC component Zip1 were used to address these questions. The identification of separation-of-function alleles that disrupt centromere pairing, but not SC assembly, have made it possible to demonstrate that centromere pairing and SC assembly have mechanistically distinct features and that prophase centromere pairing function of Zip1 drives disjunction of the paired partners in anaphase I.AUTHOR SUMMARYThe generation of gametes requires the completion of a specialized cell división called meiosis. This division is unique in that it produces cells (gametes) with half the normal number of chromosomes (such that when two gametes fuse the normal chromosome number is restored). Chromosome number is reduced in meiosis by following a single round of chromosome duplication with two rounds of segregation. In the first round, meiosis I, homologous chromosomes first pair with each other, then attach to cellular cables, called microtubules, that pull them to opposite sides of the cell. It has long been known that the homologous partners become linked to each other by genetic recombination in a way that helps them behave as a single unit when they attach to the microtubules that will ultimately pull them apart. Recently, it was shown, in budding yeast and other organisms, that homologous partners can also pair at their centromeres. Here we show that this centromere pairing also contributes to proper segregation of the partners away from each other at meiosis I, and demonstrate that one protein involved in this process is able to participate in multiple mechanisms that help homologous chromosomes to pair with each other before being segregated in meiosis I.