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Functional conservation of DNA methylation in the pea aphid and the honeybee.

Hunt BG, Brisson JA, Yi SV, Goodisman MA - Genome Biol Evol (2010)

Bottom Line: We found that highly methylated orthologs in A. pisum and Ap. mellifera exhibited greater conservation of methylation status, suggesting that highly methylated genes in ancestral species may remain highly methylated over time.We also found that methylated genes tended to show different rates of evolution than unmethylated genes.Finally, methylated genes were preferentially ubiquitously expressed among alternate phenotypes in both species, whereas genes lacking signatures of methylation were preferentially associated with condition-specific gene regulation expression.

View Article: PubMed Central - PubMed

Affiliation: School of Biology, Georgia Institute of Technology, GA, USA.

ABSTRACT
DNA methylation is a fundamental epigenetic mark known to have wide-ranging effects on gene regulation in a variety of animal taxa. Comparative genomic analyses can help elucidate the function of DNA methylation by identifying conserved features of methylated genes and other genomic regions. In this study, we used computational approaches to distinguish genes marked by heavy methylation from those marked by little or no methylation in the pea aphid, Acyrthosiphon pisum. We investigated if these two classes had distinct evolutionary histories and functional roles by conducting comparative analysis with the honeybee, Apis (Ap.) mellifera. We found that highly methylated orthologs in A. pisum and Ap. mellifera exhibited greater conservation of methylation status, suggesting that highly methylated genes in ancestral species may remain highly methylated over time. We also found that methylated genes tended to show different rates of evolution than unmethylated genes. In addition, genes targeted by methylation were enriched for particular biological processes that differed from those in relatively unmethylated genes. Finally, methylated genes were preferentially ubiquitously expressed among alternate phenotypes in both species, whereas genes lacking signatures of methylation were preferentially associated with condition-specific gene regulation expression. Overall, our analyses support a conserved role for DNA methylation in insects with comparable methylation systems.

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High CpGO/E genes exhibit significantly greater nucleotide divergence but lower amino acid divergence when compared with low CpGO/E genes with three-way orthology. (A) DNA percent difference is significantly higher between Acyrthosiphon pisum and Apis mellifera for conserved high CpGO/E orthologs (HCG) and orthologs with nonconserved CpGO/E status (NC) than those with conserved low CpGO/E status (LCG; Kruskal-Wallis rank sum test P = 0.0003). (B) In contrast, the nonsynonymous substitution rate (dN) is lower for conserved high CpGO/E orthologs compared with orthologs with nonconserved CpGO/E status or low CpGO/E status (Kruskal-Wallis rank sum test P = 0.0012). Means with 95% confidence intervals are plotted.
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fig3: High CpGO/E genes exhibit significantly greater nucleotide divergence but lower amino acid divergence when compared with low CpGO/E genes with three-way orthology. (A) DNA percent difference is significantly higher between Acyrthosiphon pisum and Apis mellifera for conserved high CpGO/E orthologs (HCG) and orthologs with nonconserved CpGO/E status (NC) than those with conserved low CpGO/E status (LCG; Kruskal-Wallis rank sum test P = 0.0003). (B) In contrast, the nonsynonymous substitution rate (dN) is lower for conserved high CpGO/E orthologs compared with orthologs with nonconserved CpGO/E status or low CpGO/E status (Kruskal-Wallis rank sum test P = 0.0012). Means with 95% confidence intervals are plotted.

Mentions: We next determined whether the differential conservation of low CpGO/E and high CpGO/E status was associated with differential conservation of nucleotide and amino acid sequence. We found that genes from the low CpGO/E class in A. pisum and Ap. mellifera both harbored significantly greater proportions of genes with detectable three-way orthologs than genes from the high CpGO/E class (table 2; Pearson's Chi-squared test with Yates' continuity correction P < 1 × 10−15). We also found that DNA sequence conservation was significantly higher between A. pisum and Ap. mellifera orthologs from the low CpGO/E class than orthologs from the high CpGO/E class (Kruskal–Wallis rank sum test P = 0.0003; fig. 3A, supplementary table S1, Supplementary Material online). Both of these results suggested that densely methylated genes, as a whole, were considerably more conserved at the sequence level than sparsely methylated genes. However, in contrast to the results obtained from analysis of ortholog loss and DNA sequence identity, amino acid substitution rates among genes with detectable three-way orthologs were slightly higher among low CpGO/E genes than high CpGO/E genes (Kruskal–Wallis rank sum test P = 0.0012; fig. 3B and supplementary fig. S1 and tables S1 and S2, Supplementary Material online). Furthermore, an alternate analysis, presented in our supplementary material, also found that densely methylated genes with detectable orthologs exhibited slightly higher rates of amino acid substitution than sparsely methylated genes.


Functional conservation of DNA methylation in the pea aphid and the honeybee.

Hunt BG, Brisson JA, Yi SV, Goodisman MA - Genome Biol Evol (2010)

High CpGO/E genes exhibit significantly greater nucleotide divergence but lower amino acid divergence when compared with low CpGO/E genes with three-way orthology. (A) DNA percent difference is significantly higher between Acyrthosiphon pisum and Apis mellifera for conserved high CpGO/E orthologs (HCG) and orthologs with nonconserved CpGO/E status (NC) than those with conserved low CpGO/E status (LCG; Kruskal-Wallis rank sum test P = 0.0003). (B) In contrast, the nonsynonymous substitution rate (dN) is lower for conserved high CpGO/E orthologs compared with orthologs with nonconserved CpGO/E status or low CpGO/E status (Kruskal-Wallis rank sum test P = 0.0012). Means with 95% confidence intervals are plotted.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2962555&req=5

fig3: High CpGO/E genes exhibit significantly greater nucleotide divergence but lower amino acid divergence when compared with low CpGO/E genes with three-way orthology. (A) DNA percent difference is significantly higher between Acyrthosiphon pisum and Apis mellifera for conserved high CpGO/E orthologs (HCG) and orthologs with nonconserved CpGO/E status (NC) than those with conserved low CpGO/E status (LCG; Kruskal-Wallis rank sum test P = 0.0003). (B) In contrast, the nonsynonymous substitution rate (dN) is lower for conserved high CpGO/E orthologs compared with orthologs with nonconserved CpGO/E status or low CpGO/E status (Kruskal-Wallis rank sum test P = 0.0012). Means with 95% confidence intervals are plotted.
Mentions: We next determined whether the differential conservation of low CpGO/E and high CpGO/E status was associated with differential conservation of nucleotide and amino acid sequence. We found that genes from the low CpGO/E class in A. pisum and Ap. mellifera both harbored significantly greater proportions of genes with detectable three-way orthologs than genes from the high CpGO/E class (table 2; Pearson's Chi-squared test with Yates' continuity correction P < 1 × 10−15). We also found that DNA sequence conservation was significantly higher between A. pisum and Ap. mellifera orthologs from the low CpGO/E class than orthologs from the high CpGO/E class (Kruskal–Wallis rank sum test P = 0.0003; fig. 3A, supplementary table S1, Supplementary Material online). Both of these results suggested that densely methylated genes, as a whole, were considerably more conserved at the sequence level than sparsely methylated genes. However, in contrast to the results obtained from analysis of ortholog loss and DNA sequence identity, amino acid substitution rates among genes with detectable three-way orthologs were slightly higher among low CpGO/E genes than high CpGO/E genes (Kruskal–Wallis rank sum test P = 0.0012; fig. 3B and supplementary fig. S1 and tables S1 and S2, Supplementary Material online). Furthermore, an alternate analysis, presented in our supplementary material, also found that densely methylated genes with detectable orthologs exhibited slightly higher rates of amino acid substitution than sparsely methylated genes.

Bottom Line: We found that highly methylated orthologs in A. pisum and Ap. mellifera exhibited greater conservation of methylation status, suggesting that highly methylated genes in ancestral species may remain highly methylated over time.We also found that methylated genes tended to show different rates of evolution than unmethylated genes.Finally, methylated genes were preferentially ubiquitously expressed among alternate phenotypes in both species, whereas genes lacking signatures of methylation were preferentially associated with condition-specific gene regulation expression.

View Article: PubMed Central - PubMed

Affiliation: School of Biology, Georgia Institute of Technology, GA, USA.

ABSTRACT
DNA methylation is a fundamental epigenetic mark known to have wide-ranging effects on gene regulation in a variety of animal taxa. Comparative genomic analyses can help elucidate the function of DNA methylation by identifying conserved features of methylated genes and other genomic regions. In this study, we used computational approaches to distinguish genes marked by heavy methylation from those marked by little or no methylation in the pea aphid, Acyrthosiphon pisum. We investigated if these two classes had distinct evolutionary histories and functional roles by conducting comparative analysis with the honeybee, Apis (Ap.) mellifera. We found that highly methylated orthologs in A. pisum and Ap. mellifera exhibited greater conservation of methylation status, suggesting that highly methylated genes in ancestral species may remain highly methylated over time. We also found that methylated genes tended to show different rates of evolution than unmethylated genes. In addition, genes targeted by methylation were enriched for particular biological processes that differed from those in relatively unmethylated genes. Finally, methylated genes were preferentially ubiquitously expressed among alternate phenotypes in both species, whereas genes lacking signatures of methylation were preferentially associated with condition-specific gene regulation expression. Overall, our analyses support a conserved role for DNA methylation in insects with comparable methylation systems.

Show MeSH