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Selective elimination of messenger RNA prevents an incidence of untimely meiosis

Nature volume 442, pages 45–50 (2006)Cite this article

Abstract

Much remains unknown about the molecular regulation of meiosis. Here we show that meiosis-specific transcripts are selectively removed if expressed during vegetative growth in fission yeast. These messenger RNAs contain a cis-acting region—which we call the DSR—that confers this removal via binding to a YTH-family protein Mmi1. Loss of Mmi1 function severely impairs cell growth owing to the untimely expression of meiotic transcripts. Microarray analysis reveals that at least a dozen such meiosis-specific transcripts are eliminated by the DSR–Mmi1 system. Mmi1 remains in the form of multiple nuclear foci during vegetative growth. At meiotic prophase these foci precipitate to a single focus, which coincides with the dot formed by the master meiosis-regulator Mei2. A meiotic arrest due to the loss of the Mei2 dot is released by a reduction in Mmi1 activity. We propose that Mei2 turns off the DSR–Mmi1 system by sequestering Mmi1 to the dot and thereby secures stable expression of meiosis-specific transcripts.

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Figure 1: Selective removal of mei4 mRNA in mitotic cells.
Figure 2: DSRs found on meiosis-specific mRNAs.
Figure 3: The mmi1 gene and expression of meiotic mRNAs in the absence of mmi1 function.
Figure 4: The Mei2 dot anchors Mmi1.

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Acknowledgements

We thank A. M. Carr for providing the chromosomal N-terminal tagging system, G. R. Smith for fission yeast strains, and M. Sato for help in strain construction. This work was supported by a Grant-in-Aid for Specially Promoted Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to M.Y.) and a Grant from the Japan Science and Technology Agency (to Y. Hiraoka). Y. Harigaya was a recipient of a JSPS Research Fellowship for Young Scientists (DC) associating with a 21st Century COE Program led by M.Y.

Author information

Author notes

  1. Hirotsugu Tanaka

    Present address: Toukoudai Research Center, Astellas Pharma Inc., Toukoudai, Tsukuba, 300-2698, Japan

  2. Yoshinori Watanabe

    Present address: Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi, Tokyo, 113-0032, Japan

Authors and Affiliations

  1. Department of Biophysics and Biochemistry, Graduate School of Science,

    Yuriko Harigaya, Hirotsugu Tanaka, Soichiro Yamanaka, Kayoko Tanaka, Yoshinori Watanabe & Masayuki Yamamoto

  2. Molecular Genetics Research Laboratory, University of Tokyo, Hongo, Tokyo, 113-0033, Japan

    Akira Yamashita & Masayuki Yamamoto

  3. Kansai Advanced Research Center, National Institute of Information and Communications Technology, Kobe, 651-2492, Japan

    Chihiro Tsutsumi, Yuji Chikashige & Yasushi Hiraoka

  4. Toukoudai Research Center, Astellas Pharma Inc., Toukoudai, Tsukuba, 300-2698, Japan

    Yoshinori Watanabe

  5. Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi, Tokyo, 113-0032, Japan

    Hirotsugu Tanaka

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Correspondence to Masayuki Yamamoto.

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The entire microarray data obtained in this study has been deposited in the Gene Expression Omnibus (GEO), under the accession number GSE3314. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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Harigaya, Y., Tanaka, H., Yamanaka, S. et al. Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442, 45–50 (2006). https://doi.org/10.1038/nature04881

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