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

Abstract

A unique aspect of meiosis is the segregation of homologous chromosomes at the meiosis I division. Homologs are physically connected prior to segregation by crossing over between nonsister chromatids. Crossovers arise from the repair of induced double-strand breaks (DSBs). In many organisms, more DSBs are formed than crossovers in a given nucleus. It has been previously suggested that repair of DSBs to noncrossover recombination products aids homolog alignment. Here we explore how two modes of the meiotic recombination pathway (crossover and noncrossover) and meiotic telomere reorganization contribute to the pairing and close juxtaposition of homologous chromosomes in budding yeast. We found that intermediates in the DSB repair pathway leading to both crossover and noncrossover recombination products contribute independently to close, stable homolog juxtaposition (CSHJ), a measurable state of homolog pairing. Analysis of the ndj1⌬ mutant indicates that the effect of meiotic telomere reorganization on CSHJ is exerted through recombination intermediates at interstitial chromosomal loci, perhaps through the noncrossover branch of the DSB repair pathway. We suggest that transient, early DSB-initiated interactions, including those that give rise to noncrossovers, are important for homolog recognition and juxtaposition.[Keywords: Homolog; meiosis; pairing; recombination; telomeres]Received December 28, 2004; revised version accepted February 15, 2005. Meiosis is the process in which a parent diploid cell undergoes two rounds of chromosome segregation, after one round of replication, to yield four haploid gametes. A universal component of meiosis I is the reductional segregation of homologous chromosomes. Nondisjunction, or improper segregation of homologs, at this stage can lead to gamete aneuploidy. Three factors contribute to the tension required for the reductional segregation of homologs at anaphase I in most organisms: (1) crossing over between homologous chromosomes, (2) cohesion between sister chromatids, and (3) monopolar spindle attachment of sister chromatids at metaphase (Page and Hawley 2003).Crossing over involves the reciprocal exchange of chromosome arms and can be visualized at late stages of meiotic prophase as chiasmata. Such exchange events are a manifestation of double-strand break (DSB)-promoted homologous recombination. Formation and repair of meiotically induced DSBs involve both DSB repair enzymes and meiosis-specific factors (for reviews, see Zickler and Kleckner 1999;Keeney 2001). Meiosis-specific factors bias recombination between homologous chromosomes instead of sister chromatids (Schwacha and Kleckner 1997) and ensure that at least one crossover occurs between every homolog pair (for review, see Bishop and Zickler 2004).A key event in crossover formation is the recognition and pairing of homologous chromosomes. An outstanding question is what brings homologs together in meiosis. Is it early molecular events, late-forming molecules in which homologs are clearly linked by chemical or hyd...

Chromosome Organization and Dynamics during Interphase, Mitosis, and Meiosis in Plants

“…This intimate dependence of pairing on recombination exists also in fungi and mammals (Baudat et al, 2000;Peoples-Holst and Burgess, 2005), but, interestingly, not in Drosophila melanogaster or Caenorhabditis elegans (Dernburg et al, 1998;McKim et al, 1998).…”

The Nucleoporin Nup2 Contains a Meiotic-Autonomous Region that Promotes the Dynamic Chromosome Events of Meiosis

“…It is well established that homologous chromosome pairing is delayed in ndj1D and csm4D mutants (Chua and Roeder 1997;Peoples-Holst and Burgess 2005;Conrad et al 2008;Lee et al 2012;Lui et al 2013). We used a previously described "onespot, two-spot" assay (Brar et al 2009;Sonntag Brown et al 2011;Lui et al 2013), in which chromosome V homologs, each …”

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).…”