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The evolution and functional significance of nested gene structures in Drosophila melanogaster.

Lee YC, Chang HH - Genome Biol Evol (2013)

Bottom Line: Interestingly, significantly fewer nested genes are transcribed from the same strand as the including gene.We found that same-strand nested genes are more likely to be single-exon genes.These results support our hypothesis that selection against potential erroneous mRNA splicing when nested and including genes are on the same strand plays an important role in the evolution of nested gene structures.

View Article: PubMed Central - PubMed

Affiliation: Center for Population Biology and Department of Evolution and Ecology, University of California.

ABSTRACT
Nearly 10% of the genes in the genome of Drosophila melanogaster are in nested structures, in which one gene is completely nested within the intron of another gene (nested and including gene, respectively). Even though the coding sequences and untranslated regions of these nested/including gene pairs do not overlap, their intimate structures and the possibility of shared regulatory sequences raise questions about the evolutionary forces governing the origination and subsequent functional and evolutionary impacts of these structures. In this study, we show that nested genes experience weaker evolutionary constraint, have faster rates of protein evolution, and are expressed in fewer tissues than other genes, while including genes show the opposite patterns. Surprisingly, despite completely overlapping with each other, nested and including genes are less likely to display correlated gene expression and biological function than the nearby yet nonoverlapping genes. Interestingly, significantly fewer nested genes are transcribed from the same strand as the including gene. We found that same-strand nested genes are more likely to be single-exon genes. In addition, same-strand including genes are less likely to have known lethal or sterile phenotypes than opposite-strand including genes only when the corresponding nested genes have introns. These results support our hypothesis that selection against potential erroneous mRNA splicing when nested and including genes are on the same strand plays an important role in the evolution of nested gene structures.

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The distributions of tissues where genes have their highest expression. Nested genes, especially same-strand nested genes, are enriched with genes having their highest expression level in testis when compared with both including and control genes. On the contrary, including genes are enriched with genes having their highest expression in brain.
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evt149-F3: The distributions of tissues where genes have their highest expression. Nested genes, especially same-strand nested genes, are enriched with genes having their highest expression level in testis when compared with both including and control genes. On the contrary, including genes are enriched with genes having their highest expression in brain.

Mentions: We also found that nested and including genes have unusual gene expression patterns. Nested genes are expressed in significantly fewer tissues (have narrower breadth of expression) than either including genes or control genes (table 2). They also have significantly higher expression specificity (see Materials and Methods) than either including or control genes (MWU, P < 10−12 for both comparisons; fig. 2). While same- and opposite-strand nested genes do not differ in their breadth of expression (MWU, P = 0.15), same-strand nested genes have significantly higher expression specificity than opposite-strand nested genes (0.95 [same-strand] vs. 0.93 [opposite-strand]; MWU, P = 0.009). The composition of tissues where genes have their highest expression is also significantly different between including genes, nested genes, and control genes (chi-square test, P < 10−16 for all comparisons; fig. 3). This composition is not different between same- and opposite-strand including genes but significantly different between same- and opposite-strand nested genes (chi-square test, P = 0.024; fig. 3). Including genes are more enriched with genes having their highest expression in brain than either nested genes or control genes (table 2). In contrast, nested genes are significantly enriched with genes having highest expression in testis but are deficient for genes having highest expression in ovaries (table 2). The enrichment of high testis expression is especially strong for same-strand nested genes (58.46% [same strand] vs. 38.18% [opposite strand]; FET, P = 1.67 × 10−6).Fig. 2.—


The evolution and functional significance of nested gene structures in Drosophila melanogaster.

Lee YC, Chang HH - Genome Biol Evol (2013)

The distributions of tissues where genes have their highest expression. Nested genes, especially same-strand nested genes, are enriched with genes having their highest expression level in testis when compared with both including and control genes. On the contrary, including genes are enriched with genes having their highest expression in brain.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814207&req=5

evt149-F3: The distributions of tissues where genes have their highest expression. Nested genes, especially same-strand nested genes, are enriched with genes having their highest expression level in testis when compared with both including and control genes. On the contrary, including genes are enriched with genes having their highest expression in brain.
Mentions: We also found that nested and including genes have unusual gene expression patterns. Nested genes are expressed in significantly fewer tissues (have narrower breadth of expression) than either including genes or control genes (table 2). They also have significantly higher expression specificity (see Materials and Methods) than either including or control genes (MWU, P < 10−12 for both comparisons; fig. 2). While same- and opposite-strand nested genes do not differ in their breadth of expression (MWU, P = 0.15), same-strand nested genes have significantly higher expression specificity than opposite-strand nested genes (0.95 [same-strand] vs. 0.93 [opposite-strand]; MWU, P = 0.009). The composition of tissues where genes have their highest expression is also significantly different between including genes, nested genes, and control genes (chi-square test, P < 10−16 for all comparisons; fig. 3). This composition is not different between same- and opposite-strand including genes but significantly different between same- and opposite-strand nested genes (chi-square test, P = 0.024; fig. 3). Including genes are more enriched with genes having their highest expression in brain than either nested genes or control genes (table 2). In contrast, nested genes are significantly enriched with genes having highest expression in testis but are deficient for genes having highest expression in ovaries (table 2). The enrichment of high testis expression is especially strong for same-strand nested genes (58.46% [same strand] vs. 38.18% [opposite strand]; FET, P = 1.67 × 10−6).Fig. 2.—

Bottom Line: Interestingly, significantly fewer nested genes are transcribed from the same strand as the including gene.We found that same-strand nested genes are more likely to be single-exon genes.These results support our hypothesis that selection against potential erroneous mRNA splicing when nested and including genes are on the same strand plays an important role in the evolution of nested gene structures.

View Article: PubMed Central - PubMed

Affiliation: Center for Population Biology and Department of Evolution and Ecology, University of California.

ABSTRACT
Nearly 10% of the genes in the genome of Drosophila melanogaster are in nested structures, in which one gene is completely nested within the intron of another gene (nested and including gene, respectively). Even though the coding sequences and untranslated regions of these nested/including gene pairs do not overlap, their intimate structures and the possibility of shared regulatory sequences raise questions about the evolutionary forces governing the origination and subsequent functional and evolutionary impacts of these structures. In this study, we show that nested genes experience weaker evolutionary constraint, have faster rates of protein evolution, and are expressed in fewer tissues than other genes, while including genes show the opposite patterns. Surprisingly, despite completely overlapping with each other, nested and including genes are less likely to display correlated gene expression and biological function than the nearby yet nonoverlapping genes. Interestingly, significantly fewer nested genes are transcribed from the same strand as the including gene. We found that same-strand nested genes are more likely to be single-exon genes. In addition, same-strand including genes are less likely to have known lethal or sterile phenotypes than opposite-strand including genes only when the corresponding nested genes have introns. These results support our hypothesis that selection against potential erroneous mRNA splicing when nested and including genes are on the same strand plays an important role in the evolution of nested gene structures.

Show MeSH
Related in: MedlinePlus