Pairing of homologous chromosomes is essential for genetic recombination during gametogenesis. In many organisms, chromosome ends are attached to cytoplasmic dynein, and dynein-driven chromosomal movements facilitate the pairing process. Factors that promote or control the cytoskeletal tethering of chromosomes are largely unknown. Here, we show that the conserved RNA-binding protein PUF-8 facilitates the tethering and pairing processes in the C. elegans germline by promoting proteasome activity. We have isolated a hypomorphic allele of pas-1, which encodes a proteasome core subunit, and find that the homologous chromosomes fail to pair in the puf-8; pas-1 double mutant due to failure of chromosome tethering. Our results reveal that the puf-8; pas-1 meiotic defects are caused by the loss of proteasome activity. The axis component HTP-3 accumulates prematurely in the double mutant, and reduction of its activity partially suppresses some of the puf-8; pas-1 meiotic defects, suggesting that HTP-3 might be an important target of the proteasome in promoting early meiotic events. In summary, our results reveal a role for the proteasome in chromosome tethering and identify PUF-8 as a regulator of proteasome activity during early meiosis.
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