Molecular architecture of the 90S small subunit pre-ribosome

  1. Qi Sun
  2. Xing Zhu
  3. Jia Qi
  4. Weidong An
  5. Pengfei Lan
  6. Dan Tan
  7. Rongchang Chen
  8. Bing Wang
  9. Sanduo Zheng
  10. Cheng Zhang
  11. Xining Chen
  12. Wei Zhang
  13. Jing Chen
  14. Meng-Qiu Dong
  15. Keqiong Ye  Is a corresponding author
  1. School of Life Sciences, Tsinghua University, China
  2. Chinese Academy of Sciences, China
  3. National Institute of Biological Sciences, China

Abstract

Eukaryotic small ribosomal subunits are first assembled into 90S pre-ribosomes. The complete 90S is a gigantic complex with a molecular mass of approximately 5 megadaltons. Here, we report the nearly complete architecture of Saccharomyces cerevisiae 90S determined from three cryo-electron microscopy single particle reconstructions at 4.5 to 8.7 angstrom resolution. Majority of the density maps were modeled and assigned to specific RNA and protein components. The nascent ribosome is assembled into isolated native-like substructures that are stabilized by abundant assembly factors. The 5' external transcribed spacer and U3 snoRNA nucleate a large subcomplex that scaffolds the nascent ribosome. U3 binds four sites of pre-rRNA, including a novel site on helix 27 but not the 3' side of the central pseudoknot, and crucially organizes the 90S structure. The 90S model provides significant insight into the principle of small subunit assembly and the function of assembly factors.

Article and author information

Author details

  1. Qi Sun

    PTN Joint Graduate Program, School of Life Sciences, Tsinghua University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Xing Zhu

    Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4839-4857
  3. Jia Qi

    Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Weidong An

    Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Pengfei Lan

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Dan Tan

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Rongchang Chen

    Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Bing Wang

    Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Sanduo Zheng

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Cheng Zhang

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Xining Chen

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Wei Zhang

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Jing Chen

    PTN Joint Graduate Program, School of Life Sciences, Tsinghua University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Meng-Qiu Dong

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6094-1182
  15. Keqiong Ye

    Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    For correspondence
    yekeqiong@ibp.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6169-7049

Funding

National Natural Science Foundation of China (91540201; 31430024; 31325007)

  • Keqiong Ye

Chinese Academy of Sciences (XDB08010203)

  • Keqiong Ye

Ministry of Science and Technology of the People's Republic of China (2014CB84980001)

  • Meng-Qiu Dong

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Alan G Hinnebusch, National Institutes of Health, United States

Version history

  1. Received: October 7, 2016
  2. Accepted: February 26, 2017
  3. Accepted Manuscript published: February 28, 2017 (version 1)
  4. Version of Record published: March 16, 2017 (version 2)
  5. Version of Record updated: June 26, 2017 (version 3)

Copyright

© 2017, Sun et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Qi Sun
  2. Xing Zhu
  3. Jia Qi
  4. Weidong An
  5. Pengfei Lan
  6. Dan Tan
  7. Rongchang Chen
  8. Bing Wang
  9. Sanduo Zheng
  10. Cheng Zhang
  11. Xining Chen
  12. Wei Zhang
  13. Jing Chen
  14. Meng-Qiu Dong
  15. Keqiong Ye
(2017)
Molecular architecture of the 90S small subunit pre-ribosome
eLife 6:e22086.
https://doi.org/10.7554/eLife.22086

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https://doi.org/10.7554/eLife.22086

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