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Position matters: multiple functions of LINC-dependent chromosome positioning during meiosis

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Abstract

Chromosome positioning is crucial for multiple chromosomal events, including DNA replication, repair, and recombination. The linker of nucleoskeleton and cytoskeleton (LINC) complexes, which consist of conserved nuclear membrane proteins, were shown to control chromosome positioning and facilitate various biological processes by interacting with the cytoskeleton. However, the precise functions and regulation of LINC-dependent chromosome positioning are not fully understood. During meiosis, the LINC complexes induce clustering of telomeres, forming the bouquet chromosome arrangement, which promotes homologous chromosome pairing. In fission yeast, the bouquet forms through LINC-dependent clustering of telomeres at the spindle pole body (SPB, the centrosome equivalent in fungi) and detachment of centromeres from the SPB-localized LINC. It was recently found that, in fission yeast, the bouquet contributes to formation of the spindle and meiotic centromeres, in addition to homologous chromosome pairing, and that centromere detachment is linked to telomere clustering, which is crucial for proper spindle formation. Here, we summarize these findings and show that the bouquet chromosome arrangement also contributes to nuclear fusion during karyogamy. The available evidence suggests that these functions are universal among eukaryotes. The findings demonstrate that LINC-dependent chromosome positioning performs multiple functions and controls non-chromosomal as well as chromosomal events, and that the chromosome positioning is stringently regulated for its functions. Thus, chromosome positioning plays a much broader role and is more strictly regulated than previously thought.

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Acknowledgements

We thank Akira Shinohara for reagents used for this study, and Takashi Ushimaru and Motoaki Hiraoka for critical reading of the manuscript and helpful comments. This work was supported by JSPS KAKENHI Grant Number 16K07248 (Grant-in-Aid for Scientific Research C) and performed under the Cooperative Research Program of the Institute for Protein Research, Osaka University (CR-13/14/15/16-03).

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  1. Department of Science, Graduate School of Integrated Science and Technology, Shizuoka University, Ohya 836, Suruga-ku, Shizuoka, 422-8529, Japan

    Kazuhiro Katsumata, Eriko Nishi, Sadia Afrin & Ayumu Yamamoto

  2. Department of Chemistry, Faculty of Science, Shizuoka University, Ohya 836, Suruga-ku, Shizuoka, 422-8529, Japan

    Kaoru Narusawa & Ayumu Yamamoto

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  1. Kazuhiro Katsumata
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Correspondence to Ayumu Yamamoto.

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Communicated by M. Kupiec.

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Katsumata, K., Nishi, E., Afrin, S. et al. Position matters: multiple functions of LINC-dependent chromosome positioning during meiosis. Curr Genet 63, 1037–1052 (2017). https://doi.org/10.1007/s00294-017-0699-2

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