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Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture

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dc.contributor.author Grau Bové, Xavier
dc.contributor.author Ruiz Trillo, Iñaki
dc.contributor.author Irimia, Manuel
dc.date.accessioned 2019-11-19T07:55:58Z
dc.date.available 2019-11-19T07:55:58Z
dc.date.issued 2018
dc.identifier.citation Grau-Bové X, Ruiz-Trillo I, Irimia M. Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture. Genome Biol. 2018; 19(1):135. DOI 10.1186/s13059-018-1499-9
dc.identifier.issn 1474-7596
dc.identifier.uri http://hdl.handle.net/10230/42890
dc.description.abstract Background: Alternative splicing, particularly through intron retention and exon skipping, is a major layer of pre-translational regulation in eukaryotes. While intron retention is believed to be the most prevalent mode across non-animal eukaryotes, animals have unusually high rates of exon skipping. However, when and how this high prevalence of exon skipping evolved is unknown. Since exon skipping can greatly expand proteomes, answering these questions sheds light on the evolution of higher organismal complexity in metazoans. Results: We used RNA-seq data to quantify exon skipping and intron retention frequencies across 65 eukaryotic species, with particular focus on early branching animals and unicellular holozoans. We found that only bilaterians have significantly increased their exon skipping frequencies compared to all other eukaryotic groups. Unlike in other eukaryotes, however, exon skipping in nearly all animals, including non-bilaterians, is strongly enriched for frame-preserving sequences, suggesting that exon skipping involvement in proteome expansion predated the increase in frequency. We also identified architectural features consistently associated with higher exon skipping rates within all studied eukaryotic genomes. Remarkably, these architectures became more prevalent during animal evolution, indicating co-evolution between genome architectures and exon skipping frequencies. Conclusion: We suggest that the increase of exon skipping rates in animals followed a two-step process. First, exon skipping in early animals became enriched for frame-preserving events. Second, bilaterian ancestors dramatically increased their exon skipping frequencies, likely driven by the interplay between a shift in their genome architectures towards more exon definition and recruitment of frame-preserving exon skipping events to functionally diversify their cell-specific proteomes.
dc.description.sponsorship This work was supported by the following grants to MI: European Research Council (ERC) Starting Grant (agreement ERC-StG-LS2–637591, under the EU Horizon 2020 Plan) and the Spanish Ministry of Economy and Competitiveness (MINECO, agreement BFU2014–55076-P; part of the Severo Ochoa Excellence Centre plan 2013–2017, SEV-2012-0208). It was also supported by the following research grants to IRT: ERC Consolidator (ERC-2012-Co-616960), the Secretary’s Office for Universities and Research of the Generalitat de Catalunya (2014 SGR 619) and MINECO (MINECO BFU2014–57779-P, with European Regional Development Fund support). XGB was supported by a pre-doctoral FPI grant from MINECO and the ERC Consolidator Grant to IRT.
dc.format.mimetype application/pdf
dc.language.iso eng
dc.publisher BioMed Central
dc.relation.ispartof Genome Biol. 2018; 19(1):135
dc.rights © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
dc.rights.uri http://creativecommons.org/licenses/by/4.0/
dc.title Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture
dc.type info:eu-repo/semantics/article
dc.identifier.doi http://dx.doi.org/10.1186/s13059-018-1499-9
dc.subject.keyword Alternative splicing
dc.subject.keyword Ancestral reconstruction
dc.subject.keyword Evolution of transcriptome regulation
dc.subject.keyword Exon skipping
dc.subject.keyword Gene architecture
dc.subject.keyword Intron retention
dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/637591
dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/BFU2014–55076-P
dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/616960
dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/BFU2014–57779-P
dc.rights.accessRights info:eu-repo/semantics/openAccess
dc.type.version info:eu-repo/semantics/publishedVersion

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