Close, stable homolog juxtaposition during meiosis in budding yeast is dependent on meiotic recombination, occurs independently of synapsis, and is distinct from DSB-independent pairing contacts

Abstract

A site-specific recombination system that probes the relative probabilities that pairs of chromosomal loci collide with one another in living cells of budding yeast was used to explore the relative contributions of pairing, recombination, synaptonemal complex formation, and telomere clustering to the close juxtaposition of homologous chromosome pairs during meiosis. The level of Cre-mediated recombination between a pair of loxP sites located at an allelic position on homologous chromosomes was 13-fold greater than that between a pair of loxP sites located at ectopic positions on nonhomologous chromosomes. Mutations affecting meiotic recombination initiation and the processing of DNA double-strand breaks (DSBs) into single-end invasions (SEIs) reduced the levels of allelic Cre-mediated recombination levels by three-to sixfold. The severity of Cre/loxP phenotypes is presented in contrast to relatively weak DSB-independent pairing defects as assayed using fluorescence in situ hybridization for these mutants. Mutations affecting synaptonemal complex (SC) formation or crossover control gave wild-type levels of allelic Cre-mediated recombination. A delay in attaining maximum levels of allelic Cre-mediated recombination was observed for a mutant defective in telomere clustering. None of the mutants affected ectopic levels of recombination. These data suggest that stable, close homolog juxtaposition in yeast is distinct from pre-DSB pairing interactions, requires both DSB and SEI formation, but does not depend on crossovers or SC.[Key Words: Meiosis; homolog pairing; recombination; synaptonemal complex; budding yeast] Received February 11, 2002; revised version accepted May 8, 2002. During meiosis, chromosomes are segregated sequentially in two different ways. In the first meiotic division, homologous chromosomes segregate from one another. In the second meiotic division, as in mitosis, sister chromatids segregate from one another. Interactions between homologous chromosomes develop and are stabilized throughout meiosis I prophase at both the DNA level and at the homolog-axis level. Events contributing to these interactions include pairing, recombination, synapsis, and telomere clustering (for review, see

Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast

“…We refer to interactions detected by FISH as pairing interactions. DSB-independent pairing is detected by FISH in situations where it is not detected by the Cre/loxP assay (Peoples et al 2002).…”

“…For example, Caenorhabditis elegans and female Drosophila melanogaster depend on the stabilizing force of the proteinaceous synaptonemal complex to juxtapose homologs until crossing over is achieved via recombination (Dernburg et al 1998;McKim et al 2002). Saccharomyces cerevisiae, Sordaria macrospora, Mus musculus, and Zea mays all rely primarily on recombination to stabilize pairing interactions between homologs (Mahadevaiah et al 2001;Peoples et al 2002;Storlazzi et al 2003;Pawlowski et al 2004). Although recombination remains necessary for juxtaposition, an important influence on pairing, recombination, and segregation of chromosomes in Schizosaccharomyces pombe is the association and movement of telomeres (Ding et al 2004).…”

“…Elucidation of the relative contributions and interplay of these processes to accurate chromosome pairing and segregation has aided understanding of homolog associations in budding yeast. Genetic and cytological analyses have so far indicated that meiotic homologous recombination is a major determinant of close, stable homolog juxtaposition (CSHJ) during meiosis in yeast, while contributions from DSB-independent pairing and the central element of the synaptonemal complex are relatively weak (Weiner and Kleckner 1994;Nag et al 1995;Peoples et al 2002).…”

“…1B;. Frequency of Cre-mediated loxP recombination events has been used to report on the relative spatial proximity of loci pairs located at allelic positions on homologous chromosomes and at ectopic positions on a nonhomologous pair of chromosomes during meiosis (Peoples et al 2002). We define wild-type levels of allelic Cre/loxP recombination as representing close, stable homolog juxtaposition.…”

Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes

“…After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http:// creativecommons.org/licenses/by-nc/4.0/. DSB-dependent recombination and subsequent synapsis, DSB-independent mechanisms seem to promote the juxtaposition of homologs (Weiner and Kleckner 1994;Peoples et al 2002;Storlazzi et al 2003;Bhuiyan and Schmekel 2004;Ding et al 2004;Peoples-Holst and Burgess 2005). A recent study in mice reported that a DSB-independent mechanism promotes homolog pairing during premeiotic S phase prior to DSB formation (Boateng et al 2013).…”