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Pre-meiotic S phase is linked to reductional chromosome segregation and recombination

Nature volume 409, pages 359–363 (2001)Cite this article

Abstract

Meiosis is initiated from G1 of the cell cycle and is characterized by a pre-meiotic S phase followed by two successive nuclear divisions. The first of these, meiosis I, differs from mitosis in having a reductional pattern of chromosome segregation1,2. Here we show that meiosis can be initiated from G2 in fission yeast cells by ectopically activating the meiosis-inducing network. The subsequent meiosis I occurs without a pre-meiotic S phase and with decreased recombination, and exhibits a mitotic pattern of equational chromosome segregation. The subsequent meiosis II results in random chromosome segregation. This behaviour is similar to that observed in cells lacking the meiotic cohesin Rec8 (refs 3, 4), which becomes associated with chromosomes at G1/S phase, including the inner centromere, a region that is probably critical for sister-centromere orientation5. If the expression of Rec8 is delayed to S phase/G2, then the centromeres behave equationally. We propose that the presence of Rec8 in chromatin is required at the pre-meiotic S phase to construct centromeres that behave reductionally and chromosome arms capable of a high level of recombination, and that this explains why meiosis is initiated from G1 of the cell cycle.

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Figure 1: Comparison between G1-exit and G2-exit meioses.
Figure 2: Association of Rec8 with centromeres and arms before the pre-meiotic S phase.
Figure 3: Meiotic cohesin Rec8 must be expressed before the pre-meiotic S phase for reductional division.
Figure 4: A model for the regulation of kinetochore orientation during meiosis by Rec8.

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Acknowledgements

We thank J. P. Cooper for critical reading of the manuscript and M. Yanagida for CHIP method. Y.W. thanks all the members of P.N.'s laboratory for help and discussion, particularly J. Hayles, H. Murakami and G. Simchen. Y.W. was supported by JSPS and Uehara fellowships and grants from the Ministry of Education, Science and Culture of Japan.

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Authors and Affiliations

  1. Department of Biophysics and Biochemistry Graduate School of Science, University of Tokyo, Hongo, 113-0033, Tokyo, Japan

    Yoshinori Watanabe, Shihori Yokobayashi & Masayuki Yamamoto

  2. PRESTO, Japan Science and Technology Corporation, Kawaguchi, 332-0012, Saitama, Japan

    Yoshinori Watanabe

  3. Imperial Cancer Research Fund, 44 Lincoln's Inn Field, London, WC2A 3PX, UK

    Yoshinori Watanabe & Paul Nurse

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  1. Yoshinori Watanabe
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Correspondence to Yoshinori Watanabe.

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Watanabe, Y., Yokobayashi, S., Yamamoto, M. et al. Pre-meiotic S phase is linked to reductional chromosome segregation and recombination. Nature 409, 359–363 (2001). https://doi.org/10.1038/35053103

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