Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture
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...
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| Format: | Article |
| Language: | English |
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BMC
2018-09-01
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| Series: | Genome Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s13059-018-1499-9 |
| _version_ | 1818335248697524224 |
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| author | Xavier Grau-Bové Iñaki Ruiz-Trillo Manuel Irimia |
| author_facet | Xavier Grau-Bové Iñaki Ruiz-Trillo Manuel Irimia |
| author_sort | Xavier Grau-Bové |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-13T14:20:25Z |
| format | Article |
| id | doaj.art-e98fbdfc73774c09ac75f6d861e289d9 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-12-13T14:20:25Z |
| publishDate | 2018-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-e98fbdfc73774c09ac75f6d861e289d92022-12-21T23:42:07ZengBMCGenome Biology1474-760X2018-09-0119112110.1186/s13059-018-1499-9Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architectureXavier Grau-Bové0Iñaki Ruiz-Trillo1Manuel Irimia2Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra)Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra)Centre de Regulació Genòmica, Barcelona Institute of Science and TechnologyAbstract 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.http://link.springer.com/article/10.1186/s13059-018-1499-9Alternative splicingExon skippingIntron retentionAncestral reconstructionGene architectureEvolution of transcriptome regulation |
| spellingShingle | Xavier Grau-Bové Iñaki Ruiz-Trillo Manuel Irimia Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture Genome Biology Alternative splicing Exon skipping Intron retention Ancestral reconstruction Gene architecture Evolution of transcriptome regulation |
| title | Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture |
| title_full | Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture |
| title_fullStr | Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture |
| title_full_unstemmed | Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture |
| title_short | Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture |
| title_sort | origin of exon skipping rich transcriptomes in animals driven by evolution of gene architecture |
| topic | Alternative splicing Exon skipping Intron retention Ancestral reconstruction Gene architecture Evolution of transcriptome regulation |
| url | http://link.springer.com/article/10.1186/s13059-018-1499-9 |
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