Abstract

Pairing of homologous chromosomes in meiosis is essential for sexual reproduction. We have previously demonstrated that the fission yeast sme2 RNA, a meiosis-specific long noncoding RNA (lncRNA), accumulates at the sme2 chromosomal loci and mediates their robust pairing in meiosis. However, the mechanisms underlying lncRNA-mediated homologous pairing have remained elusive. In this study, we identify conserved RNA-binding proteins that are required for robust pairing of homologous chromosomes. These proteins accumulate mainly at the sme2 and two other chromosomal loci together with meiosis-specific lncRNAs transcribed from these loci. Remarkably, the chromosomal accumulation of these lncRNA–protein complexes is required for robust pairing. Moreover, the lncRNA–protein complexes exhibit phase separation properties, since 1,6-hexanediol treatment reversibly disassembled these complexes and disrupted the pairing of associated loci. We propose that lncRNA–protein complexes assembled at specific chromosomal loci mediate recognition and subsequent pairing of homologous chromosomes.

Highlights

  • Pairing of homologous chromosomes in meiosis is essential for sexual reproduction

  • Homologous pairing observed in live meiotic cells demonstrated that telomere clustering and oscillatory chromosome movements spatially align homologous chromosomes in early stages of the meiotic prophase to promote their contact[10]

  • We identified a group of protein factors required for robust pairing and examined the mechanisms by which these protein factors together with long noncoding RNA (lncRNA) mediate the pairing of homologous chromosomes during meiosis

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Summary

Introduction

Pairing of homologous chromosomes in meiosis is essential for sexual reproduction. We have previously demonstrated that the fission yeast sme[2] RNA, a meiosis-specific long noncoding RNA (lncRNA), accumulates at the sme[2] chromosomal loci and mediates their robust pairing in meiosis. We identify conserved RNA-binding proteins that are required for robust pairing of homologous chromosomes These proteins accumulate mainly at the sme[2] and two other chromosomal loci together with meiosis-specific lncRNAs transcribed from these loci. S. pombe demonstrate recombinationindependent pairing of homologous chromosomes, in which the robust pairing is mediated by noncoding RNA accumulated at the specific sme[2] gene locus[11,12]. The sme[2] RNA ( called meiRNA13) is a meiosis-specific, 1500-nt long noncoding RNA (lncRNA)[11,12] It accumulates at its gene locus and plays an active role in recombination-independent pairing, leading to robust pairing[11]. We demonstrate the roles of lncRNA–protein complexes assembled at specific chromosomal loci to tether homologous chromosomes

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