mRNA Poly(A)-tail Changes Specified by Deadenylation Broadly Reshape Translation in Drosophila Oocytes and Early Embryos
- Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology, United States
- Whitehead Institute for Biomedical Research, Harvard-MIT Division of Health Sciences and Technology, United States
- Whitehead Institute for Biomedical Research, United States
- 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
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mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryosPublicly available at the NCBI Gene Expression Omnibus (accession no. GSE83616).
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Polysome profiling and ribosome footprinting of Drosophila mature oocyte and activated eggPublicly available at the NCBI Gene Expression Omnibus (accession no. GSE52799).
Article and author information
Author details
Stephen William Eichhorn
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
- Elisa Izaurralde, Max Planck Institute for Developmental Biology, Germany
Version history
- Received: April 15, 2016
- Accepted: July 29, 2016
- Accepted Manuscript published: July 30, 2016 (version 1)
- 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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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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