Independent manipulation of histone H3 modifications in individual nucleosomes reveals the contributions of sister histones to transcription

  1. Zhen Zhou
  2. Yu-Ting Liu
  3. Li Ma
  4. Ting Gong
  5. Yanan Hu
  6. Hong-Tao Li
  7. Chen Cai
  8. Ling-Li Zhang
  9. Gang Wei
  10. Jin-Qiu Zhou  Is a corresponding author
  1. Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, China
  2. CAS-MPG Partner Institute for Computational Biology, China

Abstract

Histone tail modifications can greatly influence chromatin-associated processes. Asymmetrically modified nucleosomes exist in multiple cell types; however, whether modifications on both sister histones contribute equally to chromatin dynamics remains elusive. Here, we devised a bivalent nucleosome system that allowed for the constitutive assembly of asymmetrically modified sister histone H3s in nucleosomes in Saccharomyces cerevisiae. The sister H3K36 methylations independently affected cryptic transcription in gene coding regions, whereas sister H3K79 methylation had cooperative effects on gene silencing near telomeres. H3K4 methylation on sister histones played an independent role in suppressing the recruitment of Gal4 activator to the GAL1 promoter and inhibiting GAL1 transcription. Under starvation stress, sister H3K4 methylations acted cooperatively, independently or redundantly to regulate transcription. Thus, we provide a unique tool for comparing symmetrical and asymmetrical modifications of sister histone H3s in vivo.

Article and author information

Author details

  1. Zhen Zhou

    State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Yu-Ting Liu

    State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Li Ma

    Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Ting Gong

    State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yanan Hu

    Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Hong-Tao Li

    State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Chen Cai

    State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Ling-Li Zhang

    State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Gang Wei

    Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Jin-Qiu Zhou

    State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, Shanghai, China
    For correspondence
    jqzhou@sibcb.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1986-8611

Funding

National Natural Science Foundation of China (31521061)

  • Jin-Qiu Zhou

National Natural Science Foundation of China (31230040)

  • Jin-Qiu Zhou

Ministry of Science and Technology of the People's Republic of China (2016YFA0500701)

  • Jin-Qiu Zhou

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

Reviewing Editor

  1. Tim Formosa, University of Utah School of Medicine, United States

Publication history

  1. Received: July 5, 2017
  2. Accepted: October 12, 2017
  3. Accepted Manuscript published: October 13, 2017 (version 1)
  4. Version of Record published: November 8, 2017 (version 2)

Copyright

© 2017, Zhou 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. Zhen Zhou
  2. Yu-Ting Liu
  3. Li Ma
  4. Ting Gong
  5. Yanan Hu
  6. Hong-Tao Li
  7. Chen Cai
  8. Ling-Li Zhang
  9. Gang Wei
  10. Jin-Qiu Zhou
(2017)
Independent manipulation of histone H3 modifications in individual nucleosomes reveals the contributions of sister histones to transcription
eLife 6:e30178.
https://doi.org/10.7554/eLife.30178
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