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Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development

Drosophila syncytial nuclear divisions limit transcription unit size of early zygotic genes. As mitosis inhibits not only transcription, but also pre-mRNA splicing, we reasoned that constraints on splicing were likely to exist in the early embryo, being splicing avoidance a possible explanation why...

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Autores principales: Guilgur, Leonardo Gastón, Prudêncio, Pedro, Sobral, Daniel, Liszekova, Denisa, Rosa, André, Martinho, Rui Gonçalo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3989599/
https://www.ncbi.nlm.nih.gov/pubmed/24755291
http://dx.doi.org/10.7554/eLife.02181
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author Guilgur, Leonardo Gastón
Prudêncio, Pedro
Sobral, Daniel
Liszekova, Denisa
Rosa, André
Martinho, Rui Gonçalo
author_facet Guilgur, Leonardo Gastón
Prudêncio, Pedro
Sobral, Daniel
Liszekova, Denisa
Rosa, André
Martinho, Rui Gonçalo
author_sort Guilgur, Leonardo Gastón
collection PubMed
description Drosophila syncytial nuclear divisions limit transcription unit size of early zygotic genes. As mitosis inhibits not only transcription, but also pre-mRNA splicing, we reasoned that constraints on splicing were likely to exist in the early embryo, being splicing avoidance a possible explanation why most early zygotic genes are intronless. We isolated two mutant alleles for a subunit of the NTC/Prp19 complexes, which specifically impaired pre-mRNA splicing of early zygotic but not maternally encoded transcripts. We hypothesized that the requirements for pre-mRNA splicing efficiency were likely to vary during development. Ectopic maternal expression of an early zygotic pre-mRNA was sufficient to suppress its splicing defects in the mutant background. Furthermore, a small early zygotic transcript with multiple introns was poorly spliced in wild-type embryos. Our findings demonstrate for the first time the existence of a developmental pre-requisite for highly efficient splicing during Drosophila early embryonic development and suggest in highly proliferative tissues a need for coordination between cell cycle and gene architecture to ensure correct gene expression and avoid abnormally processed transcripts. DOI: http://dx.doi.org/10.7554/eLife.02181.001
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spelling pubmed-39895992014-04-24 Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development Guilgur, Leonardo Gastón Prudêncio, Pedro Sobral, Daniel Liszekova, Denisa Rosa, André Martinho, Rui Gonçalo eLife Developmental Biology and Stem Cells Drosophila syncytial nuclear divisions limit transcription unit size of early zygotic genes. As mitosis inhibits not only transcription, but also pre-mRNA splicing, we reasoned that constraints on splicing were likely to exist in the early embryo, being splicing avoidance a possible explanation why most early zygotic genes are intronless. We isolated two mutant alleles for a subunit of the NTC/Prp19 complexes, which specifically impaired pre-mRNA splicing of early zygotic but not maternally encoded transcripts. We hypothesized that the requirements for pre-mRNA splicing efficiency were likely to vary during development. Ectopic maternal expression of an early zygotic pre-mRNA was sufficient to suppress its splicing defects in the mutant background. Furthermore, a small early zygotic transcript with multiple introns was poorly spliced in wild-type embryos. Our findings demonstrate for the first time the existence of a developmental pre-requisite for highly efficient splicing during Drosophila early embryonic development and suggest in highly proliferative tissues a need for coordination between cell cycle and gene architecture to ensure correct gene expression and avoid abnormally processed transcripts. DOI: http://dx.doi.org/10.7554/eLife.02181.001 eLife Sciences Publications, Ltd 2014-04-22 /pmc/articles/PMC3989599/ /pubmed/24755291 http://dx.doi.org/10.7554/eLife.02181 Text en Copyright © 2014, Guilgur et al http://creativecommons.org/licenses/by/3.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology and Stem Cells
Guilgur, Leonardo Gastón
Prudêncio, Pedro
Sobral, Daniel
Liszekova, Denisa
Rosa, André
Martinho, Rui Gonçalo
Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development
title Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development
title_full Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development
title_fullStr Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development
title_full_unstemmed Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development
title_short Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development
title_sort requirement for highly efficient pre-mrna splicing during drosophila early embryonic development
topic Developmental Biology and Stem Cells
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3989599/
https://www.ncbi.nlm.nih.gov/pubmed/24755291
http://dx.doi.org/10.7554/eLife.02181
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