mRNA Poly(A)-tail Changes Specified by Deadenylation Broadly Reshape Translation in Drosophila Oocytes and Early Embryos

  1. Stephen William Eichhorn
  2. Alexander Orest Subtelny
  3. Iva Kronja
  4. Jamie C Kwasnieski
  5. Terry L Orr-Weaver  Is a corresponding author
  6. David P Bartel  Is a corresponding author
  1. Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, United States
  2. Whitehead Institute for Biomedical Research, Harvard-MIT Division of Health Sciences and Technology, United States
  3. Whitehead Institute for Biomedical Research, United States
  4. Howard Hughes Medical Institute, Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, United States

Abstract

Because maturing oocytes and early embryos lack appreciable transcription, posttranscriptional regulatory processes control their development. To better understand this control, we profiled translational efficiencies and poly(A)-tail lengths throughout Drosophila oocyte maturation and early embryonic development. The correspondence between translational-efficiency changes and tail-length changes indicated that tail-length changes broadly regulate translation until gastrulation, when this coupling disappears. During egg activation, relative changes in poly(A)-tail length, and thus translational efficiency, were largely retained in the absence of cytoplasmic polyadenylation, which indicated that selective poly(A)-tail shortening primarily specifies these changes. Many translational changes depended on PAN GU and Smaug, and both acted primarily through tail-length changes. Our results also revealed the presence of tail-length-independent mechanisms that maintained translation despite tail-length shortening during oocyte maturation, and prevented essentially all translation of bicoid and several other mRNAs before egg activation. In addition to these fundamental insights, our results provide valuable resources for future studies.

Data availability

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Stephen William Eichhorn

    Department of Biology, Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6410-4699
  2. Alexander Orest Subtelny

    Department of Biology, Whitehead Institute for Biomedical Research, Harvard-MIT Division of Health Sciences and Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Iva Kronja

    Department of Biology, Whitehead Institute for Biomedical Research, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jamie C Kwasnieski

    Department of Biology, Whitehead Institute for Biomedical Research, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Terry L Orr-Weaver

    Department of Biology, Whitehead Institute for Biomedical Research, Cambridge, United States
    For correspondence
    weaver@wi.mit.edu
    Competing interests
    The authors declare that no competing interests exist.
  6. David P Bartel

    Department of Biology, Howard Hughes Medical Institute, Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    dbartel@wi.mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3872-2856

Funding

Howard Hughes Medical Institute

  • David P Bartel

American Cancer Society

  • Terry L Orr-Weaver

Alexander von Humboldt-Stiftung (Feodor Lynen Postdoctoral Fellowship)

  • Iva Kronja

National Institutes of Health (GM39341 and GM118098)

  • Terry L Orr-Weaver

National Institutes of Health (GM067031)

  • David P Bartel

National Institutes of Health (Medical Scientist Training Program fellowship T32GM007753)

  • Alexander Orest Subtelny

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

Reviewing Editor

  1. Elisa Izaurralde, Max Planck Institute for Developmental Biology, Germany

Publication history

  1. Received: April 15, 2016
  2. Accepted: July 29, 2016
  3. Accepted Manuscript published: July 30, 2016 (version 1)
  4. Version of Record published: August 17, 2016 (version 2)

Copyright

© 2016, Eichhorn 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. Stephen William Eichhorn
  2. Alexander Orest Subtelny
  3. Iva Kronja
  4. Jamie C Kwasnieski
  5. Terry L Orr-Weaver
  6. David P Bartel
(2016)
mRNA Poly(A)-tail Changes Specified by Deadenylation Broadly Reshape Translation in Drosophila Oocytes and Early Embryos
eLife 5:e16955.
https://doi.org/10.7554/eLife.16955
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