Bouquet formation, rapid prophase movements and homologous pairing during meiotic prophase in Saccharomyces cerevisiae

Telomeres associate with the nuclear envelope, cluster and accumulate adjacent to the centrosome to form the chromosome bouquet in meiotic prophase. Cytological studies that span three centuries have demonstrated the bouquet in most species and generally have supported the consensus view that bouquet formation promotes homologous chromosome interactions that lead to chromosome pairing. A separation of function mutant, mps3 Delta240-430, was identified and further investigation revealed that the long-standing hypothesis that bouquet formation is required to facilitate homologous pairing is unlikely. Instead, homologous pairing is facilitated by active telomere-led rapid prophase movements (RPMs) that persist throughout meiotic prophase. Bouquet formation and RPMs depend on Mps3, Ndj1 and Csm4 (MNC complex). The MNC complex provides structural connections between telomeres, nuclear envelope and cytoskeleton. Ndj1p and Mps3p are interdependent for localization to the telomeres and link telomeres to the nuclear envelope. The SUN domain of Mps3p further extends the link to cytoplasmic actin cables with the involvement of Csm4 to generate RPMs. RPMs not only facilitate homologous pairing but also synchronize the process of pairing among homologs of different lengths. We conclude that chromosome length is an important determinant of homologous pairing, synapsis and cross over regulation during meiotic prophase.