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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.

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.

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Means of expression levels and breadth in human intronless (Int0), monomorphic (Mono), and polymorphic (Poly) genes with different numbers of isoforms (from 2 to 4 and more). Gene expression levels and breadths were evaluated by tallying the numbers of gene-specific EST sequences from normal human tissues in GenBank (Ogurtsov et al. 2008) and from GenAtlas expression data, as described in Supplementary Material online.
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fig2: Means of expression levels and breadth in human intronless (Int0), monomorphic (Mono), and polymorphic (Poly) genes with different numbers of isoforms (from 2 to 4 and more). Gene expression levels and breadths were evaluated by tallying the numbers of gene-specific EST sequences from normal human tissues in GenBank (Ogurtsov et al. 2008) and from GenAtlas expression data, as described in Supplementary Material online.

Mentions: Intronless genes typically are expressed at a significantly lower level and in a narrower range of tissues than monomorphic or polymorphic genes (fig. 2; P < 10−65 and P < 10−82 for expressed sequence tag [EST], P < 10−13 and P < 10−12 for the Genomics Institute of the Novartis Research Foundation [GNF] Atlas 2, respectively). The same trends were observed when mammal-specific and primate-specific intronless genes were excluded from the analysis in order to eliminate any possibility of contamination of the set of intronless genes with pseudogenes (data not shown). By contrast, there was no dramatic difference in the expression of monomorphic as compared with polymorphic genes, and among the polymorphic genes, no strong dependence of expression on the number of isoforms was observed (fig. 2). The same trends were observed for mouse intronless, monomorphic, and polymorphic genes, as inferred from the analysis of the mouse GNF Atlas 2 expression data (supplementary fig. S1A, Supplementary Material online). Notably, when monomorphic and intronless genes were pooled together, as it was done in a previous study (Wegmann et al. 2008), expression of the pooled group significantly and consistently differed from the expression of polymorphic genes (supplementary fig. S1B, Supplementary Material online), in agreement with the observations of Wegmann et al. (2008). Taking into account that retroposed genes have a characteristic property to acquire introns in 5′UTRs after retroposition (Brosius and Gould 1992; Brosius 1999), we also analyzed separately the group of genes with completely intronless CDSs and with intron-containing 5′UTRs. These genes are few in numbers and show intermediate values of expression level and breadth between intronless and monomorphic genes (supplementary table S2, Supplementary Material online). The expression breadth for this group of genes (with intronless CDS and intron-containing 5′UTRs) was significantly different from the expression levels of both intronless and monomorphic genes (P < 5 × 10−3 and P < 10−9 from EST data; P < 10−2 and P < 5 × 10−5 from GNF Atlas 2 data; supplementary table S2, Supplementary Material online). Similar relationships were observed for expression level in these three groups of genes.


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 expression levels and breadth in human intronless (Int0), monomorphic (Mono), and polymorphic (Poly) genes with different numbers of isoforms (from 2 to 4 and more). Gene expression levels and breadths were evaluated by tallying the numbers of gene-specific EST sequences from normal human tissues in GenBank (Ogurtsov et al. 2008) and from GenAtlas expression data, as described in Supplementary Material online.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig2: Means of expression levels and breadth in human intronless (Int0), monomorphic (Mono), and polymorphic (Poly) genes with different numbers of isoforms (from 2 to 4 and more). Gene expression levels and breadths were evaluated by tallying the numbers of gene-specific EST sequences from normal human tissues in GenBank (Ogurtsov et al. 2008) and from GenAtlas expression data, as described in Supplementary Material online.
Mentions: Intronless genes typically are expressed at a significantly lower level and in a narrower range of tissues than monomorphic or polymorphic genes (fig. 2; P < 10−65 and P < 10−82 for expressed sequence tag [EST], P < 10−13 and P < 10−12 for the Genomics Institute of the Novartis Research Foundation [GNF] Atlas 2, respectively). The same trends were observed when mammal-specific and primate-specific intronless genes were excluded from the analysis in order to eliminate any possibility of contamination of the set of intronless genes with pseudogenes (data not shown). By contrast, there was no dramatic difference in the expression of monomorphic as compared with polymorphic genes, and among the polymorphic genes, no strong dependence of expression on the number of isoforms was observed (fig. 2). The same trends were observed for mouse intronless, monomorphic, and polymorphic genes, as inferred from the analysis of the mouse GNF Atlas 2 expression data (supplementary fig. S1A, Supplementary Material online). Notably, when monomorphic and intronless genes were pooled together, as it was done in a previous study (Wegmann et al. 2008), expression of the pooled group significantly and consistently differed from the expression of polymorphic genes (supplementary fig. S1B, Supplementary Material online), in agreement with the observations of Wegmann et al. (2008). Taking into account that retroposed genes have a characteristic property to acquire introns in 5′UTRs after retroposition (Brosius and Gould 1992; Brosius 1999), we also analyzed separately the group of genes with completely intronless CDSs and with intron-containing 5′UTRs. These genes are few in numbers and show intermediate values of expression level and breadth between intronless and monomorphic genes (supplementary table S2, Supplementary Material online). The expression breadth for this group of genes (with intronless CDS and intron-containing 5′UTRs) was significantly different from the expression levels of both intronless and monomorphic genes (P < 5 × 10−3 and P < 10−9 from EST data; P < 10−2 and P < 5 × 10−5 from GNF Atlas 2 data; supplementary table S2, Supplementary Material online). Similar relationships were observed for expression level in these three groups of genes.

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