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Selective elimination of messenger RNA prevents an incidence of untimely meiosis

Author

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  • Yuriko Harigaya

    (Graduate School of Science)

  • Hirotsugu Tanaka

    (Graduate School of Science
    Toukoudai Research Center, Astellas Pharma Inc.
    University of Tokyo, Yayoi)

  • Soichiro Yamanaka

    (Graduate School of Science)

  • Kayoko Tanaka

    (Graduate School of Science)

  • Yoshinori Watanabe

    (Graduate School of Science
    Toukoudai Research Center, Astellas Pharma Inc.
    University of Tokyo, Yayoi)

  • Chihiro Tsutsumi

    (Kansai Advanced Research Center, National Institute of Information and Communications Technology)

  • Yuji Chikashige

    (Kansai Advanced Research Center, National Institute of Information and Communications Technology)

  • Yasushi Hiraoka

    (Kansai Advanced Research Center, National Institute of Information and Communications Technology)

  • Akira Yamashita

    (University of Tokyo, Hongo)

  • Masayuki Yamamoto

    (Graduate School of Science
    University of Tokyo, Hongo)

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.

Suggested Citation

  • Yuriko Harigaya & Hirotsugu Tanaka & Soichiro Yamanaka & Kayoko Tanaka & Yoshinori Watanabe & Chihiro Tsutsumi & Yuji Chikashige & Yasushi Hiraoka & Akira Yamashita & Masayuki Yamamoto, 2006. "Selective elimination of messenger RNA prevents an incidence of untimely meiosis," Nature, Nature, vol. 442(7098), pages 45-50, July.
    • Handle: RePEc:nat:nature:v:442:y:2006:i:7098:d:10.1038_nature04881
    DOI: 10.1038/nature04881
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    Cited by:

    1. Ebru Aydin & Silke Schreiner & Jacqueline Böhme & Birte Keil & Jan Weber & Bojan Žunar & Timo Glatter & Cornelia Kilchert, 2024. "DEAD-box ATPase Dbp2 is the key enzyme in an mRNP assembly checkpoint at the 3’-end of genes and involved in the recycling of cleavage factors," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Anne-Emmanuelle Foucher & Leila Touat-Todeschini & Ariadna B. Juarez-Martinez & Auriane Rakitch & Hamida Laroussi & Claire Karczewski & Samira Acajjaoui & Montserrat Soler-López & Stephen Cusack & Cam, 2022. "Structural analysis of Red1 as a conserved scaffold of the RNA-targeting MTREC/PAXT complex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Song-Yao Zhang & Shao-Wu Zhang & Lian Liu & Jia Meng & Yufei Huang, 2016. "m6A-Driver: Identifying Context-Specific mRNA m6A Methylation-Driven Gene Interaction Networks," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
    4. Komal Soni & Anusree Sivadas & Attila Horvath & Nikolay Dobrev & Rippei Hayashi & Leo Kiss & Bernd Simon & Klemens Wild & Irmgard Sinning & Tamás Fischer, 2023. "Mechanistic insights into RNA surveillance by the canonical poly(A) polymerase Pla1 of the MTREC complex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.

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