Meiotic Cohesin Promotes Pairing of Nonhomologous Centromeres in Early Meiotic Prophase

A period of pairing between nonhomologous centromeres occurs early in meiosis in a diverse collection of organisms. This early, homology-independent, centromere pairing, referred to as centromere coupling in budding yeast, gives way to an alignment of homologous centromeres as homologues synapse later in meiotic prophase. The regulation of centromere coupling and its underlying mechanism have not been elucidated. In budding yeast, the protein Zip1p is a major component of the central element of the synaptonemal complex in pachytene of meiosis, and earlier, is essential for centromere coupling. The experiments reported here demonstrate that centromere coupling is mechanistically distinct from synaptonemal complex assembly. Zip2p, Zip3p, and Red1p are all required for the assembly of Zip1 into the synaptonemal complex but are dispensable for centromere coupling. However, the meiotic cohesin Rec8p is required for centromere coupling. Loading of meiotic cohesins to centromeres and cohesin-associated regions is required for the association of Zip1 with these sites, and the association of Zip1 with the centromeres then promotes coupling. These findings reveal a mechanism that promotes associations between centromeres before the assembly of the synaptonemal complex, and they demonstrate that chromosomes are preloaded with Zip1p in a manner that may promote synapsis.