Regulation of RNA granule dynamics by phosphorylation of serine-rich, intrinsically-disordered proteins in C. elegans

  1. Jennifer T Wang
  2. Jarrett Smith
  3. Bi-Chang Chen
  4. Helen Schmidt
  5. Dominique Rasoloson
  6. Alexandre Paix
  7. Bramwell G Lambrus
  8. Deepika Calidas
  9. Eric Betzig
  10. Geraldine Seydoux  Is a corresponding author
  1. Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, United States
  2. Academica Sinica, Taiwan
  3. Janelia Farm Research Campus, Howard Hughes Medical Institute, United States

Abstract

RNA granules have been likened to liquid droplets whose dynamics depend on the controlled dissolution and condensation of internal components. The molecules and reactions that drive these dynamics in vivo are not well understood. Here, we present evidence that a group of intrinsically-disordered, serine-rich proteins regulate the dynamics of P granules in C. elegans embryos. The MEG (maternal-effect germline defective) proteins are germ plasm components that are required redundantly for fertility. We demonstrate that MEG-1 and MEG-3 are substrates of the kinase MBK-2/DYRK and the phosphatase PP2APPTR-1/2. Phosphorylation of the MEGs promotes granule disassembly and dephosphorylation promotes granule assembly. Using lattice light sheet microscopy on live embryos, we show that GFP-tagged MEG-3 localizes to a dynamic domain that surrounds and penetrates each granule. We conclude that, despite their liquid-like behavior, P granules are non-homogeneous structures whose assembly in embryos is regulated by phosphorylation.

Article and author information

Author details

  1. Jennifer T Wang

    Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jarrett Smith

    Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Bi-Chang Chen

    Research Center for Applied Sciences, Academica Sinica, Taipei, Taiwan
    Competing interests
    The authors declare that no competing interests exist.
  4. Helen Schmidt

    Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Dominique Rasoloson

    Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexandre Paix

    Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Bramwell G Lambrus

    Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Deepika Calidas

    Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Eric Betzig

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Geraldine Seydoux

    Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United States
    For correspondence
    gseydoux@jhmi.edu
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2014, Wang 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. Jennifer T Wang
  2. Jarrett Smith
  3. Bi-Chang Chen
  4. Helen Schmidt
  5. Dominique Rasoloson
  6. Alexandre Paix
  7. Bramwell G Lambrus
  8. Deepika Calidas
  9. Eric Betzig
  10. Geraldine Seydoux
(2014)
Regulation of RNA granule dynamics by phosphorylation of serine-rich, intrinsically-disordered proteins in C. elegans
eLife 3:e04591.
https://doi.org/10.7554/eLife.04591

Share this article

https://doi.org/10.7554/eLife.04591

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