Telomere-mediated chromosome pairing during meiosis in budding yeast

Abstract

Certain haploid strains of Saccharomyces cerevisiae can undergo meiosis, but meiotic prophase progression and subsequent nuclear division are delayed if these haploids carry an extra chromosome (i.e., are disomic). Observations indicate that interactions between homologous chromosomes cause a delay in meiotic prophase, perhaps to allow time for interhomolog interactions to be completed. Analysis of meiotic mutants demonstrates that the relevant aspect of homolog recognition is independent of meiotic recombination and synaptonemal complex formation. A disome in which the extra chromosome is circular sporulates without a delay, indicating that telomeres are important for homolog recognition. Consistent with this hypothesis, fluorescent in situ hybridization demonstrates that a circular chromosome has a reduced capacity to pair with its homolog, and a telomere-associated meiotic protein (Ndj1) is required to delay sporulation in disomes. A circular dimer containing two copies of the same chromosome delays meiosis to the same extent as two linear homologs, implying that physical proximity bypasses the requirement for telomeres in homolog pairing. Analysis of a disome carrying two linear permuted chromosomes suggests that even nonhomologous chromosome ends can promote homolog pairing to a limited extent. We speculate that telomere-mediated chromosome movement and/or telomere clustering promote homolog pairing.

Irregular telomeres impair meiotic synapsis and recombination in mice

“…Genetic analysis of Saccharomyces cerevisiae strains has indicated that meiotic telomere clustering contributes to efficient homologue alignment and synaptic pairing telomeres. Telomere-associated meiotic protein (Ndj1) is required for tethering meiotic telomeres to the nuclear periphery (7,38). Also, proteins Hop2 and Mnd1 work as a complex to promote meiotic chromosome pairing (39).…”

“…In the fission yeast and Caenorhabditis elegans, loss of telomere function decreases meiotic recombination and increases chromosome missegregation and loss (4)(5)(6). Telomere-mediated chromosome movement and͞or telomere clustering in lower eukaryotes and plants promote homologue pairing (7)(8)(9)(10)(11). Telomeres have been postulated to function similarly in mammalian meiosis (12).…”

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

“…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).…”

“…First, the role of NDJ1 in meiotic telomere reorganization could contribute directly to interactions between homologs, independent of interactions mediated through DSB repair, through the role of Ndj1 in tethering telomeres to the nuclear envelope (Rockmill and Roeder 1998). Alternatively, the ndj1⌬ mutation could elicit a defect in CSHJ through a negative effect on recombination.…”

MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae

“…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).…”