An autonomous meiosis-specific region of yeast Nup2 (hNup50) promotes normal meiotic chromosome dynamics in Saccharomyces cerevisiae.

Abstract

Meiosis is a specialized cellular program required to create haploid gametes from diploid parent cells. Prior to the first meiotic division, homologous chromosomes pair, synapse, and recombine to ensure their proper disjunction at anaphase I. Additionally, telomeres tethered at the nuclear envelope cluster in the bouquet configuration where they are subjected to dramatic pulling forces acting from outside of the nucleus. In Saccharomyces cerevisiae, the telomere-associated protein Ndj1 is required for bouquet formation. When Ndj1 is absent, these dramatic motions cease and multiple steps of meiosis I prophase progression are delayed. Here we identified Nup2 in a pool of enriched proteins that co-purify with tagged Ndj1 from meiotic cell extracts. Nup2 is a nonessential nucleoporin that functions in nuclear transport, boundary activity, and telomere silencing in mitotically dividing cells. We found that deletion of NUP2 delayed pairing and synapsis during meiosis, and led to decreased spore viability, similar to the ndj1{Delta} mutant phenotype. Surprisingly, the nup2{Delta} ndj1{Delta} double mutant failed to segregate chromosomes, even though the meiotic program continued. These results suggest that a physical impediment to nuclear division is created in the absence of Nup2 and Ndj1. Our deletion analysis of NUP2 identified a previously uncharacterized 125-amino acid region that is both necessary and sufficient to complement all of nup2{Delta}s meiotic phenotypes, which we call the meiotic autonomous region (MAR). We propose that Ndj1 and Nup2 function in parallel pathways to promote the dynamic chromosome events of meiotic chromosome dynamics, perhaps through the establishment or maintenance of higher-order chromosome organization.