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Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes.

Shabalina SA, Ogurtsov AY, Spiridonov AN, Novichkov PS, Spiridonov NA, Koonin EV - Mol. Biol. Evol. (2010)

Bottom Line: Comparison of expression levels and breadth and evolutionary rates of intronless and intron-containing mammalian genes shows that intronless genes are expressed at lower levels, tend to be tissue specific, and evolve significantly faster than spliced genes.Alternative splicing is most common in ancient genes, whereas intronless genes appear to have relatively recent origins.These results imply tight coupling between different stages of gene expression, in particular, transcription, splicing, and nucleocytosolic transport of transcripts, and suggest that formation of intronless genes is an important route of evolution of novel tissue-specific functions in animals.

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ABSTRACT
Comparison of expression levels and breadth and evolutionary rates of intronless and intron-containing mammalian genes shows that intronless genes are expressed at lower levels, tend to be tissue specific, and evolve significantly faster than spliced genes. By contrast, monomorphic spliced genes that are not subject to detectable alternative splicing and polymorphic alternatively spliced genes show similar statistically indistinguishable patterns of expression and evolution. Alternative splicing is most common in ancient genes, whereas intronless genes appear to have relatively recent origins. These results imply tight coupling between different stages of gene expression, in particular, transcription, splicing, and nucleocytosolic transport of transcripts, and suggest that formation of intronless genes is an important route of evolution of novel tissue-specific functions in animals.

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Means of evolutionary rates in intronless, monomorphic, and polymorphic (Poly) genes with different numbers of isoforms (from 2 to 4 and more). Rates of synonymous (dS) and non-synonymous (dN) substitutions in the protein CDSs and evolutionary rates in 5′UTRs (K5) and 3′UTRs (K3) were estimated from sequence alignments of approximately 9,000 human and macaque orthologous genes, as described previously (Ogurtsov et al. 2008).
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fig3: Means of evolutionary rates in intronless, monomorphic, and polymorphic (Poly) genes with different numbers of isoforms (from 2 to 4 and more). Rates of synonymous (dS) and non-synonymous (dN) substitutions in the protein CDSs and evolutionary rates in 5′UTRs (K5) and 3′UTRs (K3) were estimated from sequence alignments of approximately 9,000 human and macaque orthologous genes, as described previously (Ogurtsov et al. 2008).

Mentions: We further found that the rates of evolution of the CDS among approximately 9,000 pairs of orthologous genes from human and macaque were significantly higher for intronless genes, as compared with spliced genes, in both non-synonymous and synonymous positions (P < 0.0001 for Kn and P < 10−7 for Ks); by contrast, the difference between the evolutionary rates of monomorphic and polymorphic genes was not significant (fig. 3). It has been shown previously that mammalian and primate-specific human and mouse genes including intronless ones evolve faster than genes of more ancient origin (Agarwal 2005; Wolf et al. 2009); however, we observed the exact same trends among “old,” evolutionarily conserved intronless genes (i.e., when mammal-specific and primate-specific genes were excluded from the analysis; see supplementary fig. S1C, Supplementary Material online). Of course, it has to be kept in mind that genes obviously are highly dynamic units, so the divide between “old” and “new” intronless genes is to some extent conditional given that some evolutionary conserved intronless could evolve by retroposition of spliced genes. For the evolutionary rates of the UTRs (K5 and K3), a different trend was observed; these domains evolve at approximately the same rates in human intronless and monomorphic genes (fig. 3). Evolutionary rates of CDSs in the group of genes with intronless CDSs and intron-containing 5′UTRs are close to those of intronless genes and the differences for both Kn and Ks are marginal between these two groups.


Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes.

Shabalina SA, Ogurtsov AY, Spiridonov AN, Novichkov PS, Spiridonov NA, Koonin EV - Mol. Biol. Evol. (2010)

Means of evolutionary rates in intronless, monomorphic, and polymorphic (Poly) genes with different numbers of isoforms (from 2 to 4 and more). Rates of synonymous (dS) and non-synonymous (dN) substitutions in the protein CDSs and evolutionary rates in 5′UTRs (K5) and 3′UTRs (K3) were estimated from sequence alignments of approximately 9,000 human and macaque orthologous genes, as described previously (Ogurtsov et al. 2008).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2908711&req=5

fig3: Means of evolutionary rates in intronless, monomorphic, and polymorphic (Poly) genes with different numbers of isoforms (from 2 to 4 and more). Rates of synonymous (dS) and non-synonymous (dN) substitutions in the protein CDSs and evolutionary rates in 5′UTRs (K5) and 3′UTRs (K3) were estimated from sequence alignments of approximately 9,000 human and macaque orthologous genes, as described previously (Ogurtsov et al. 2008).
Mentions: We further found that the rates of evolution of the CDS among approximately 9,000 pairs of orthologous genes from human and macaque were significantly higher for intronless genes, as compared with spliced genes, in both non-synonymous and synonymous positions (P < 0.0001 for Kn and P < 10−7 for Ks); by contrast, the difference between the evolutionary rates of monomorphic and polymorphic genes was not significant (fig. 3). It has been shown previously that mammalian and primate-specific human and mouse genes including intronless ones evolve faster than genes of more ancient origin (Agarwal 2005; Wolf et al. 2009); however, we observed the exact same trends among “old,” evolutionarily conserved intronless genes (i.e., when mammal-specific and primate-specific genes were excluded from the analysis; see supplementary fig. S1C, Supplementary Material online). Of course, it has to be kept in mind that genes obviously are highly dynamic units, so the divide between “old” and “new” intronless genes is to some extent conditional given that some evolutionary conserved intronless could evolve by retroposition of spliced genes. For the evolutionary rates of the UTRs (K5 and K3), a different trend was observed; these domains evolve at approximately the same rates in human intronless and monomorphic genes (fig. 3). Evolutionary rates of CDSs in the group of genes with intronless CDSs and intron-containing 5′UTRs are close to those of intronless genes and the differences for both Kn and Ks are marginal between these two groups.

Bottom Line: Comparison of expression levels and breadth and evolutionary rates of intronless and intron-containing mammalian genes shows that intronless genes are expressed at lower levels, tend to be tissue specific, and evolve significantly faster than spliced genes.Alternative splicing is most common in ancient genes, whereas intronless genes appear to have relatively recent origins.These results imply tight coupling between different stages of gene expression, in particular, transcription, splicing, and nucleocytosolic transport of transcripts, and suggest that formation of intronless genes is an important route of evolution of novel tissue-specific functions in animals.

View Article: PubMed Central - PubMed

ABSTRACT
Comparison of expression levels and breadth and evolutionary rates of intronless and intron-containing mammalian genes shows that intronless genes are expressed at lower levels, tend to be tissue specific, and evolve significantly faster than spliced genes. By contrast, monomorphic spliced genes that are not subject to detectable alternative splicing and polymorphic alternatively spliced genes show similar statistically indistinguishable patterns of expression and evolution. Alternative splicing is most common in ancient genes, whereas intronless genes appear to have relatively recent origins. These results imply tight coupling between different stages of gene expression, in particular, transcription, splicing, and nucleocytosolic transport of transcripts, and suggest that formation of intronless genes is an important route of evolution of novel tissue-specific functions in animals.

Show MeSH