Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis

Abstract

In Saccharomyces cerevisiae meiosis, recombination occurs frequently between sequences at the same location on homologs (allelic recombination) and can take place between dispersed homologous sequences (ectopic recombination). Ectopic recombination occurs less often than does allelic, especially when homologous sequences are on heterologous chromosomes. To account for this, it has been suggested that homolog pairing (homolog colocalization and alignment) either promotes allelic recombination or restricts ectopic recombination. The latter suggestion was tested by examining ectopic recombination in two cases where normal interhomolog relationships are disrupted. In the first case, one member of a homolog pair was replaced by a homoeologous (related but not identical) chromosome that has diverged sufficiently to prevent allelic recombination. In the second case, ndj1 mutants were used to delay homolog pairing and synapsis. Both circumstances resulted in a substantial increase in the frequency of ectopic recombination between arg4-containing plasmid inserts located on heterologous chromosomes. These findings suggest that, during normal yeast meiosis, progressive homolog colocalization, alignment, synapsis, and allelic recombination restrict the ability of ectopically located sequences to find each other and recombine. In the absence of such restrictions, the meiotic homology search may encompass the entire genome.homolog pairing ͉ sequence divergence ͉ NDJ1

Examination of Interchromosomal Interactions in Vegetatively Growing DiploidSchizosaccharomyces pombeCells by Cre/loxP Site-Specific Recombination

“…Chromosome disposition and ectopic recombination: Chromosome disposition within the nucleus is suspected to be a primary factor in determining the frequency of homologous recombination, as seen, e.g., in studies of ectopic recombination in budding yeast meiosis (Goldman and Lichten 2000;Schlecht et al 2004) and of mouse double-strand-break dynamics (Soutoglou et al 2007). We are now in a position to assess this possibility for S. pombe by comparing the results of previously presented mitotic recombination data (Virgin et al 2001) with the current data obtained by Cre/loxP analysis.…”

MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae

“…47). Finally, telomere movements could contribute to the dissolution of nonhomologous associations such as those between heterologous centromeres (48) and other ectopic interactions (18,39), essentially editing out connections that might hinder rather than promote appropriate disjunction in the first meiotic division (49). The role played by transient accumulation of telomeres adjacent to the spindle pole, specifically, remains unclear.…”

“…Ndj1p is a meiosisspecific protein that accumulates at telomeres in S. cerevisiae (15,16) and is required for bouquet formation (17). Deletion of NDJ1 delays axial element formation, homolog pairing, synapsis and onset of the first meiotic division, causes an elevated frequency of nondisjunction and of ectopic recombination, and reduces spore formation and viability (15)(16)(17)(18)(19)(20)(21). Early recombination intermediates form between homologs with wild-type kinetics in ndj1⌬, suggesting that some aspect of bouquet formation is required for the normal coupling of the molecular and cytological events of pairing (22).…”

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

“…For example, attachment of telomeres to the nuclear envelope alone could provide a basis for pairing by constraining chromosome mobility or topology (Zickler and Kleckner 1998). Indeed, a role for meiotic telomere reorganization in homology searching through limitation of the available search region has been proposed based on the observation that homologous recombination between heteroalleles placed at ectopic locations is apparently restricted to a lesser extent in an ndj1⌬ mutant than in wild type (Goldman and Lichten 2000). Moreover, a role for Ndj1 in telomere-mediated interactions has been proposed by Rockmill and Roeder (1998).…”