mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos

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 embryoni...

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Main Authors: Stephen W Eichhorn, Alexander O Subtelny, Iva Kronja, Jamie C Kwasnieski, Terry L Orr-Weaver, David P Bartel
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/16955
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author Stephen W Eichhorn
Alexander O Subtelny
Iva Kronja
Jamie C Kwasnieski
Terry L Orr-Weaver
David P Bartel
author_facet Stephen W Eichhorn
Alexander O Subtelny
Iva Kronja
Jamie C Kwasnieski
Terry L Orr-Weaver
David P Bartel
author_sort Stephen W Eichhorn
collection DOAJ
description 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 these changes were largely attributable to 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.
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spelling doaj.art-9e766beef5c54d13b5626e53ed04c1662022-12-22T03:51:18ZengeLife Sciences Publications LtdeLife2050-084X2016-07-01510.7554/eLife.16955mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryosStephen W Eichhorn0https://orcid.org/0000-0002-6410-4699Alexander O Subtelny1Iva Kronja2Jamie C Kwasnieski3Terry L Orr-Weaver4David P Bartel5https://orcid.org/0000-0002-3872-2856Howard Hughes Medical Institute, Whitehead Institute for Biomedical Research, Cambridge, United States; Department of Biology, Massachusetts Institute of Technology, Cambridge, United StatesHoward Hughes Medical Institute, Whitehead Institute for Biomedical Research, Cambridge, United States; Department of Biology, Massachusetts Institute of Technology, Cambridge, United States; Harvard-MIT Division of Health Sciences and Technology, Cambridge, United StatesDepartment of Biology, Massachusetts Institute of Technology, Cambridge, United States; Whitehead Institute for Biomedical Research, Cambridge, United StatesHoward Hughes Medical Institute, Whitehead Institute for Biomedical Research, Cambridge, United States; Department of Biology, Massachusetts Institute of Technology, Cambridge, United StatesDepartment of Biology, Massachusetts Institute of Technology, Cambridge, United States; Whitehead Institute for Biomedical Research, Cambridge, United StatesHoward Hughes Medical Institute, Whitehead Institute for Biomedical Research, Cambridge, United States; Department of Biology, Massachusetts Institute of Technology, Cambridge, United StatesBecause 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 these changes were largely attributable to 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.https://elifesciences.org/articles/16955Drosophila oogenesisDrosophila embryogenesisposttranscriptional gene regulationribosome footprint profilingPAL-seqwispy
spellingShingle Stephen W Eichhorn
Alexander O Subtelny
Iva Kronja
Jamie C Kwasnieski
Terry L Orr-Weaver
David P Bartel
mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
eLife
Drosophila oogenesis
Drosophila embryogenesis
posttranscriptional gene regulation
ribosome footprint profiling
PAL-seq
wispy
title mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
title_full mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
title_fullStr mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
title_full_unstemmed mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
title_short mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
title_sort mrna poly a tail changes specified by deadenylation broadly reshape translation in drosophila oocytes and early embryos
topic Drosophila oogenesis
Drosophila embryogenesis
posttranscriptional gene regulation
ribosome footprint profiling
PAL-seq
wispy
url https://elifesciences.org/articles/16955
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