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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Main Authors: Leonardo Gastón Guilgur, Pedro Prudêncio, Daniel Sobral, Denisa Liszekova, André Rosa, Rui Gonçalo Martinho
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2014-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/02181
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spelling doaj-808fc39447d84b1cbef90e7ccad3f67f2021-05-04T23:04:42ZengeLife Sciences Publications LtdeLife2050-084X2014-04-01310.7554/eLife.02181Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic developmentLeonardo Gastón Guilgur0Pedro Prudêncio1Daniel Sobral2Denisa Liszekova3André Rosa4Rui Gonçalo Martinho5https://orcid.org/0000-0002-1641-3403Instituto Gulbenkian de Ciência, Oeiras, Portugal; Departamento de Ciências Biomédicas e Medicina, Universidade do Algarve, Faro, Portugal; IBB-Institute for Biotechnology and Bioengineering, Centro de Biomedicina Molecular e Estrutural, Universidade do Algarve, Faro, PortugalInstituto Gulbenkian de Ciência, Oeiras, Portugal; Departamento de Ciências Biomédicas e Medicina, Universidade do Algarve, Faro, Portugal; IBB-Institute for Biotechnology and Bioengineering, Centro de Biomedicina Molecular e Estrutural, Universidade do Algarve, Faro, PortugalInstituto Gulbenkian de Ciência, Oeiras, PortugalInstituto Gulbenkian de Ciência, Oeiras, PortugalInstituto Gulbenkian de Ciência, Oeiras, PortugalInstituto Gulbenkian de Ciência, Oeiras, Portugal; Departamento de Ciências Biomédicas e Medicina, Universidade do Algarve, Faro, Portugal; IBB-Institute for Biotechnology and Bioengineering, Centro de Biomedicina Molecular e Estrutural, Universidade do Algarve, Faro, PortugalDrosophila 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.https://elifesciences.org/articles/02181fast developmentearly zygotic genemRNA splicingPrp19/NTCSyf1/Xab2
collection DOAJ
language English
format Article
sources DOAJ
author Leonardo Gastón Guilgur
Pedro Prudêncio
Daniel Sobral
Denisa Liszekova
André Rosa
Rui Gonçalo Martinho
spellingShingle Leonardo Gastón Guilgur
Pedro Prudêncio
Daniel Sobral
Denisa Liszekova
André Rosa
Rui Gonçalo Martinho
Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development
eLife
fast development
early zygotic gene
mRNA splicing
Prp19/NTC
Syf1/Xab2
author_facet Leonardo Gastón Guilgur
Pedro Prudêncio
Daniel Sobral
Denisa Liszekova
André Rosa
Rui Gonçalo Martinho
author_sort Leonardo Gastón Guilgur
title 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_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_sort requirement for highly efficient pre-mrna splicing during drosophila early embryonic development
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2014-04-01
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.
topic fast development
early zygotic gene
mRNA splicing
Prp19/NTC
Syf1/Xab2
url https://elifesciences.org/articles/02181
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AT pedroprudencio requirementforhighlyefficientpremrnasplicingduringdrosophilaearlyembryonicdevelopment
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AT denisaliszekova requirementforhighlyefficientpremrnasplicingduringdrosophilaearlyembryonicdevelopment
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