title: Multiple Pairwise Analysis of Non-homologous Centromere Coupling Reveals Preferential Chromosome Size-Dependent Interactions and a Role for Bouquet Formation in Establishing the Interaction Pattern.
abstract: During meiosis, chromosomes undergo a homology search in order to locate their homolog to form stable pairs and exchange genetic material. Early in prophase, chromosomes associate in mostly non-homologous pairs, tethered only at their centromeres. This phenomenon, conserved through higher eukaryotes, is termed centromere coupling in budding yeast. Both initiation of recombination and the presence of homologs are dispensable for centromere coupling (occurring in spo11 mutants and haploids induced to undergo meiosis) but the presence of the synaptonemal complex (SC) protein Zip1 is required. The nature and mechanism of coupling have yet to be elucidated. Here we present the first pairwise analysis of centromere coupling in an effort to uncover underlying rules that may exist within these non-homologous interactions. We designed a novel chromosome conformation capture (3C)-based assay to detect all possible interactions between non-homologous yeast centromeres during early meiosis. Using this variant of 3C-qPCR, we found a size-dependent interaction pattern, in which chromosomes assort preferentially with chromosomes of similar sizes, in haploid and diploid spo11 cells, but not in a coupling-defective mutant (spo11 zip1 haploid and diploid yeast). This pattern is also observed in wild-type diploids early in meiosis but disappears as meiosis progresses and homologous chromosomes pair. We found no evidence to support the notion that ancestral centromere homology plays a role in pattern establishment in S. cerevisiae post-genome duplication. Moreover, we found a role for the meiotic bouquet in establishing the size dependence of centromere coupling, as abolishing bouquet (using the bouquet-defective spo11 ndj1 mutant) reduces it. Coupling in spo11 ndj1 rather follows telomere clustering preferences. We propose that a chromosome size preference for centromere coupling helps establish efficient homolog recognition.
authors: Department of Molecular, Cellular and Developmental Biology Yale University New Haven, United States of America.|Faculty of Medicine University of Montreal, Montreal, CANADA.
authors: Philippe
authors: P
authors: Lefrançois
authors: Department of Molecular, Cellular and Developmental Biology Yale University New Haven, United States of America.|Department of Molecular and Cell Biology University of California Berkeley, Berkeley, United States of America.
authors: Beth
authors: B
authors: Rockmill
authors: Faculty of Medicine McGill University Montreal, CANADA.
authors: Pingxing
authors: P
authors: Xie
authors: Department of Molecular, Cellular and Developmental Biology Yale University New Haven, United States of America.
authors: G Shirleen
authors: GS
authors: Roeder
authors: Department of Genetics Stanford University School of Medicine Stanford, United States of America.
authors: Michael
authors: M
authors: Snyder
mesh_terms: D018797:Cell Cycle Proteins / Q000235:genetics* / Q000378:metabolism; D002503:Centromere / Q000235:genetics*; D023902:Chromosome Pairing / Q000235:genetics; D015825:Chromosomes, Fungal / Q000235:genetics; D004706:Endodeoxyribonucleases / Q000235:genetics* / Q000378:metabolism; D059765:Homologous Recombination / Q000235:genetics*; D008540:Meiosis / Q000235:genetics*; D009687:Nuclear Proteins / Q000235:genetics; D012441:Saccharomyces cerevisiae / Q000235:genetics; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics* / Q000378:metabolism; D013573:Synaptonemal Complex / Q000235:genetics; D016615:Telomere / Q000235:genetics; D000099257:Meiotic Recombination Protein SPO11
chemical_list: D018797:Cell Cycle Proteins; D004706:Endodeoxyribonucleases; D009687:Nuclear Proteins; D029701:Saccharomyces cerevisiae Proteins; C433703:Ndj1 protein, S cerevisiae; C518938:Spo11 protein, S cerevisiae; D000099257:Meiotic Recombination Protein SPO11