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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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 |
work_keys_str_mv |
AT leonardogastonguilgur requirementforhighlyefficientpremrnasplicingduringdrosophilaearlyembryonicdevelopment AT pedroprudencio requirementforhighlyefficientpremrnasplicingduringdrosophilaearlyembryonicdevelopment AT danielsobral requirementforhighlyefficientpremrnasplicingduringdrosophilaearlyembryonicdevelopment AT denisaliszekova requirementforhighlyefficientpremrnasplicingduringdrosophilaearlyembryonicdevelopment AT andrerosa requirementforhighlyefficientpremrnasplicingduringdrosophilaearlyembryonicdevelopment AT ruigoncalomartinho requirementforhighlyefficientpremrnasplicingduringdrosophilaearlyembryonicdevelopment |
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1721477129304014848 |