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The evolutionary fate of alternatively spliced homologous exons after gene duplication.

Abascal F, Tress ML, Valencia A - Genome Biol Evol (2015)

Bottom Line: We found examples supporting two extreme evolutionary models for the behaviour of homologous axons after gene duplication.At other extreme, we identified genes in which the homologous exons were always conserved within paralogs, suggesting that the alternative splicing event cannot easily be separated from the function in these genes.That many homologous exons fall in between these two extremes highlights the diversity of biological systems and suggests that the subtle balance between alternative splicing and gene duplication is adjusted to the specific cellular context of each gene.

View Article: PubMed Central - PubMed

Affiliation: Structural Biology and Biocomputing Programme, Spanish National Cancer Research Centre (CNIO), Madrid, Spain fabascal@cnio.es mtress@cnio.es.

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The ML phylogenetic tree of MARVELD3 exons (LG+I+G+F evolutionary model), which shows the evolutionary relationship between equivalent homologous exons in different species. The exons exist either in the form of alternatively spliced exons or as constitutively spliced exons in separate genes. The numbers at each internal node indicate bootstrap support.
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evv076-F3: The ML phylogenetic tree of MARVELD3 exons (LG+I+G+F evolutionary model), which shows the evolutionary relationship between equivalent homologous exons in different species. The exons exist either in the form of alternatively spliced exons or as constitutively spliced exons in separate genes. The numbers at each internal node indicate bootstrap support.

Mentions: Our analysis revealed a complex evolutionary history for MARVELD3, and we had to consider other vertebrates to clarify it. The pattern of AS, previously reported as specific to mammals (Steed et al. 2009), is also observed in coelacanth and Xenopus. In all vertebrates but mammals, that is, in lamprey, ray-finned fishes, coelacanth, Xenopus and reptiles (including birds), there are two MARVELD3 genes instead of one. With the exception of coelacanth and Xenopus, species with duplicated MARVELD3 show no AS. Interestingly, the phylogenetic reconstruction of these exons reveals two clearly defined lineages (groups of orthology), each covering the whole set of analyzed vertebrates. In species with duplicated genes, each of the two separated exons maps to a different group of orthology. In species with AS, each alternative exon maps to each group of orthology. In coelacanth and Xenopus both things happen, as one of their duplicated genes conserved the AS pattern. Although other alternative hypotheses could be proposed, we believe that the most parsimonious interpretation for this complex scenario is that originally, in the ancestor of vertebrates, MARVELD3 acquired the pattern of AS. Then, this ancestral gene duplicated and one of the paralogs lost the pattern of AS. Later, after the split of the major vertebrate lineages, some lineages lost the paralog that had no AS (mammals) whereas other lineages lost one of the AS isoforms from the paralog that did have AS (fig. 3). According to the phylogenetic tree, splice isoform separation occurred at least three times (at the ancestors of lamprey, ray-finned fishes, and reptiles) whereas a single gene loss event took place in the ancestor of mammals. Remarkably, despite several gene and exon losses, both original splice isoforms have been always kept, either within the same or different genes, which might be taken as an indication of their biological relevance and functional independence.Fig. 3.—


The evolutionary fate of alternatively spliced homologous exons after gene duplication.

Abascal F, Tress ML, Valencia A - Genome Biol Evol (2015)

The ML phylogenetic tree of MARVELD3 exons (LG+I+G+F evolutionary model), which shows the evolutionary relationship between equivalent homologous exons in different species. The exons exist either in the form of alternatively spliced exons or as constitutively spliced exons in separate genes. The numbers at each internal node indicate bootstrap support.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4494069&req=5

evv076-F3: The ML phylogenetic tree of MARVELD3 exons (LG+I+G+F evolutionary model), which shows the evolutionary relationship between equivalent homologous exons in different species. The exons exist either in the form of alternatively spliced exons or as constitutively spliced exons in separate genes. The numbers at each internal node indicate bootstrap support.
Mentions: Our analysis revealed a complex evolutionary history for MARVELD3, and we had to consider other vertebrates to clarify it. The pattern of AS, previously reported as specific to mammals (Steed et al. 2009), is also observed in coelacanth and Xenopus. In all vertebrates but mammals, that is, in lamprey, ray-finned fishes, coelacanth, Xenopus and reptiles (including birds), there are two MARVELD3 genes instead of one. With the exception of coelacanth and Xenopus, species with duplicated MARVELD3 show no AS. Interestingly, the phylogenetic reconstruction of these exons reveals two clearly defined lineages (groups of orthology), each covering the whole set of analyzed vertebrates. In species with duplicated genes, each of the two separated exons maps to a different group of orthology. In species with AS, each alternative exon maps to each group of orthology. In coelacanth and Xenopus both things happen, as one of their duplicated genes conserved the AS pattern. Although other alternative hypotheses could be proposed, we believe that the most parsimonious interpretation for this complex scenario is that originally, in the ancestor of vertebrates, MARVELD3 acquired the pattern of AS. Then, this ancestral gene duplicated and one of the paralogs lost the pattern of AS. Later, after the split of the major vertebrate lineages, some lineages lost the paralog that had no AS (mammals) whereas other lineages lost one of the AS isoforms from the paralog that did have AS (fig. 3). According to the phylogenetic tree, splice isoform separation occurred at least three times (at the ancestors of lamprey, ray-finned fishes, and reptiles) whereas a single gene loss event took place in the ancestor of mammals. Remarkably, despite several gene and exon losses, both original splice isoforms have been always kept, either within the same or different genes, which might be taken as an indication of their biological relevance and functional independence.Fig. 3.—

Bottom Line: We found examples supporting two extreme evolutionary models for the behaviour of homologous axons after gene duplication.At other extreme, we identified genes in which the homologous exons were always conserved within paralogs, suggesting that the alternative splicing event cannot easily be separated from the function in these genes.That many homologous exons fall in between these two extremes highlights the diversity of biological systems and suggests that the subtle balance between alternative splicing and gene duplication is adjusted to the specific cellular context of each gene.

View Article: PubMed Central - PubMed

Affiliation: Structural Biology and Biocomputing Programme, Spanish National Cancer Research Centre (CNIO), Madrid, Spain fabascal@cnio.es mtress@cnio.es.

Show MeSH
Related in: MedlinePlus