Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Eichhorn, Stephen W, Subtelny, Alexander O, Kronja, Iva, Kwasnieski, Jamie C, Orr-Weaver, Terry L, Bartel, David P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4988829/
https://www.ncbi.nlm.nih.gov/pubmed/27474798
http://dx.doi.org/10.7554/eLife.16955
_version_ 1782448479876939776
author Eichhorn, Stephen W
Subtelny, Alexander O
Kronja, Iva
Kwasnieski, Jamie C
Orr-Weaver, Terry L
Bartel, David P
author_facet Eichhorn, Stephen W
Subtelny, Alexander O
Kronja, Iva
Kwasnieski, Jamie C
Orr-Weaver, Terry L
Bartel, David P
author_sort Eichhorn, Stephen W
collection PubMed
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. DOI: http://dx.doi.org/10.7554/eLife.16955.001
format Online
Article
Text
id pubmed-4988829
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-49888292016-08-19 mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos Eichhorn, Stephen W Subtelny, Alexander O Kronja, Iva Kwasnieski, Jamie C Orr-Weaver, Terry L Bartel, David P eLife Developmental Biology and Stem Cells 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. DOI: http://dx.doi.org/10.7554/eLife.16955.001 eLife Sciences Publications, Ltd 2016-07-30 /pmc/articles/PMC4988829/ /pubmed/27474798 http://dx.doi.org/10.7554/eLife.16955 Text en © 2016, Eichhorn et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology and Stem Cells
Eichhorn, Stephen W
Subtelny, Alexander O
Kronja, Iva
Kwasnieski, Jamie C
Orr-Weaver, Terry L
Bartel, David P
mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
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 Developmental Biology and Stem Cells
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4988829/
https://www.ncbi.nlm.nih.gov/pubmed/27474798
http://dx.doi.org/10.7554/eLife.16955
work_keys_str_mv AT eichhornstephenw mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos
AT subtelnyalexandero mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos
AT kronjaiva mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos
AT kwasnieskijamiec mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos
AT orrweaverterryl mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos
AT barteldavidp mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos