Phase separation drives pairing of homologous chromosomes
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MINI-REVIEW
Phase separation drives pairing of homologous chromosomes Yasushi Hiraoka1 Received: 19 March 2020 / Revised: 4 April 2020 / Accepted: 6 April 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract Pairing of homologous chromosomes is crucial for ensuring accurate segregation of chromosomes during meiosis. Molecular mechanisms of homologous chromosome pairing in meiosis have been extensively studied in the fission yeast Schizosaccharomyces pombe. In this organism, meiosis-specific noncoding RNA transcribed from specific genes accumulates at the respective gene loci, and chromosome-associated RNA–protein complexes mediate meiotic pairing of homologous loci through phase separation. Pairing of homologous chromosomes also occurs in somatic diploid cells in certain situations. For example, somatic pairing of homologous chromosomes occurs during the early embryogenesis in diptera, and relies on the transcription-associated chromatin architecture. Earlier models also suggest that transcription factories along the chromosome mediate pairing of homologous chromosomes in plants. These studies suggest that RNA bodies formed on chromosomes mediate the pairing of homologous chromosomes. This review summarizes lessons from S. pombe to provide general insights into mechanisms of homologous chromosome pairing mediated by phase separation of chromosome-associated RNA–protein complexes. Keywords Fission yeast · Homologous chromosome · Noncoding RNA · Phase separation
Introduction Pairing and recombination of homologous chromosomes are crucial for ensuring accurate segregation of chromosomes during meiosis (Zickler and Kleckner 1998; Gerton and Hawley 2005). Homologous recombination is initiated by DNA double-strand break (DSB) formation. Molecular mechanisms for DSB-triggered homologous recombination have been extensively studies in the budding yeast Saccharomyces cerevisiae and extended to the other eukaryotes (Barzel and Kupiec 2008; Keeney et al. 2014; Bordelet and Dubrana 2019; Hollingsworth and Gaglione 2019). However, it has remained to be elucidated how chromosomes find their homologous partner to pair with. Involvement of chromosome-associated RNA in the pairing of homologous chromosomes has been shown in the fission yeast Schizosaccharomyces pombe. S. pombe
Communicated by M. Kupiec. * Yasushi Hiraoka [email protected]‑u.ac.jp 1
Graduate School of Frontier Biosciences, Osaka University, 1‑3 Yamadaoka, Suita 565‑0871, Japan
has provided an excellent experimental system for studying the molecular mechanisms of chromosome organization. S. pombe exhibits a drastic change in chromosome organization within the nucleus when the cell moves from mitosis to meiosis (Fig. 1a), while centromeres are clustered near the spindle-pole body (SPB) in mitotic interphase, telomeres become clustered at the SPB during meiotic prophase (Fig. 1b). Upon entering meiosis, the entire nucleus elongates and moves back and forth in the cell, and the telomeres remain clustered at the SPB, located at the leading
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