Csm4-Dependent Telomere Movement on Nuclear Envelope Promotes Meiotic Recombination

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Abstract
During meiotic prophase, chromosomes display rapid movement, and their telomeres attach to the nuclear envelope and cluster to form a “chromosomal bouquet.” Little is known about the roles of the chromosome movement and telomere clustering in this phase. In budding yeast, telomere clustering is promoted by a meiosis-specific, telomere-binding protein, Ndj1. Here, we show that a meiosis-specific protein, Csm4, which forms a complex with Ndj1, facilitates bouquet formation. In the absence of Csm4, Ndj1-bound telomeres tether to nuclear envelopes but do not cluster, suggesting that telomere clustering in the meiotic prophase consists of at least two distinct steps: Ndj1-dependent tethering to the nuclear envelope and Csm4-dependent clustering/movement. Similar to Ndj1, Csm4 is required for several distinct steps during meiotic recombination. Our results suggest that Csm4 promotes efficient second-end capture of a double-strand break following a homology search, as well as resolution of the double-Holliday junction during crossover formation. We propose that chromosome movement and associated telomere dynamics at the nuclear envelope promotes the completion of key biochemical steps during meiotic recombination. Meiosis is a specialized cell division that produces haploid gametes. Homologous recombination plays a pivotal role in the segregation of homologous chromosomes during meiosis I by creating physical linkages between the chromosomes. Drastic reorganization of chromosomes in the nucleus is a prominent feature of meiotic prophase I, during which telomeres get associated with the nuclear envelope and move within the envelope, culminating in the formation of telomere clusters, often referred to as “chromosome bouquets.” The roles that telomere movement and clustering play in meiotic prophase I are largely unknown. In the budding yeast Saccharomyces cerevisiae, tethering of telomeres to the nuclear envelope is mediated by a meiosis-specific telomere-binding protein, Ndj1. We studied the functions of a meiosis-specific gene, CSM4, in telomere clustering and during meiotic recombination. CSM4 is necessary for the clustering of Ndj1-associated telomeres. Interestingly, csm4 mutants show pleiotropic defects during meiotic recombination. It is likely that the chromosome movement promotes various biochemical reactions during meiotic recombination.