Abstract
The pairing and recombination of homologous chromosomes during the meiotic prophase is necessary for the accurate segregation of chromosomes in meiosis. However, the mechanism by which homologous chromosomes achieve this pairing has remained an open question. Meiotic cohesins have been shown to affect chromatin compaction; however, the impact of meiotic cohesins on homologous pairing and the fine structures of cohesion-based chromatin remain to be determined. A recent report using live-cell imaging and super-resolution microscopy demonstrated that the lack of meiotic cohesins alters the chromosome axis structures and impairs the pairing of homologous chromosomes. These results suggest that meiotic cohesin-based chromosome axis structures are crucial for the pairing of homologous chromosomes.
Similar content being viewed by others
References
Bähler J, Wyler T, Loidl J, Kohli J (1993) Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis. J Cell Biol 121:241–256
Chikashige Y, Ding DQ, Funabiki H, Haraguchi T, Mashiko S, Yanagida M, Hiraoka Y (1994) Telomere-led premeiotic chromosome movement in fission yeast Schizosaccharomyces pombe. Science 264:270–273
Ding DQ, Chikashige Y, Haraguchi T, Hiraoka Y (1998) Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules as revealed by continuous observation of chromosomes and microtubules in living cells. J Cell Sci 111:701–712
Ding DQ, Yamamoto A, Haraguchi T, Hiraoka Y (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6:329–341
Ding DQ, Sakurai N, Katou Y, Itoh T, Shirahige K, Haraguchi T, Hiraoka Y (2006) Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast. J Cell Biol 174:499–508
Ding DQ, Okamasa K, Yamane M, Tsutsumi C, Haraguchi T, Yamamoto M, Hiraoka Y (2012) Meiosis-specific non-coding RNA mediates robust pairing of homologous chromosomes in meiosis. Science 336:732–736
Ding DQ, Haraguchi T, Hiraoka Y (2013) The role of chromosomal retention of noncoding RNA in meiosis. Chromosome Res 21:665–672
Ding DQ, Matusda A, Okamasa K, Nagahama Y, Haraguchi T, Hiraoka Y (2015) Meiotic cohesin builds a platform of chromosome architectures for homologous chromosome pairing. Chromosoma. doi:10.1007/s00412-015-0551-8
Hiraoka Y, Dernburg AF (2009) The SUN rises on meiotic chromosome dynamics. Dev Cell 17:598–605
Ishiguro K, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y (2011) A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep 12:267–275
Ishiguro K, Kim J, Shibuya H, Hernández-Hernández A, Suzuki A, Fukagawa T, Shioi G, Kiyonari H, Li XC, Schimenti J, Höög C, Watanabe Y (2014) Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes. Genes Dev 28:594–607
Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300:1152–1155
Lee J, Hirano T (2011) RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol 192:263–276
Loidl J (2006) S. pombe linear elements: the modest cousins of synaptonemal complexes. Chromosoma 115:260–271
Lorenz A, Wells JL, Pryce DW, Novatchkova M, Eisenhaber F, McFarlane RJ, Loidl J (2004) S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J Cell Sci 117:3343–3351
Nagaoka SI, Hassold TJ, Hunt PA (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13:493–504
Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20:525–558
Ruan K, Yamamoto TG, Asakawa H, Chikashige Y, Kimura H, Masukata H, Haraguchi T, Hiraoka Y (2015) Histone H4 acetylation required for loosening chromatin during DNA replication. Sci Rep 5:12720
Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2:621–627
Tanaka K, Hao Z, Kai M, Okayama H (2001) Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J 20:5779–5790
Tomonaga T, Nagao K, Kawasaki Y, Furuya K, Murakami A, Morishita J, Yuasa T, Sutani T, Kearsey SE, Uhlmann F, Nasmyth K, Yanagida M (2000) Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. Genes Dev 14:2757–2770
Tsai JH, McKee BD (2011) Homologous pairing and the role of pairing centers in meiosis. J Cell Sci 124(12):1955–1963
Wang SW, Read RL, Norbury CJ (2002) Fission yeast Pds5 is required for accurate chromosome segregation and for survival after DNA damage or metaphase arrest. J Cell Sci 115:587–598
Watanabe Y, Yamamoto M (1994) S. pombe mei2 + encodes an RNA-binding protein essential for premeiotic DNA synthesis and meiosis I, which cooperates with a novel RNA species meiRNA. Cell 78:487–498
Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Kupiec.
Rights and permissions
About this article
Cite this article
Ding, DQ., Haraguchi, T. & Hiraoka, Y. A cohesin-based structural platform supporting homologous chromosome pairing in meiosis. Curr Genet 62, 499–502 (2016). https://doi.org/10.1007/s00294-016-0570-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-016-0570-x