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Depletion of CpG Dinucleotides in Papillomaviruses and Polyomaviruses: A Role for Divergent Evolutionary Pressures.

Upadhyay M, Vivekanandan P - PLoS ONE (2015)

Bottom Line: We analyzed the relative abundance of dinucleotides, effective codon number (ENC), differences in synonymous codon usage.CpG dinucleotide depletion was more pronounced among papillomaviruses and polyomaviruses infecting human and other mammals as compared to those infecting birds.The extent of CpG depletion among papillomaviruses and polyomaviruses is linked to the evolutionary lineage of the infected host.

View Article: PubMed Central - PubMed

Affiliation: Kusuma School of Biological Sciences, Indian Institute of Technology Delhi, New Delhi, 006, India.

ABSTRACT

Background: Papillomaviruses and polyomaviruses are small ds-DNA viruses infecting a wide-range of vertebrate hosts. Evidence supporting co-evolution of the virus with the host does not fully explain the evolutionary path of papillomaviruses and polyomaviruses. Studies analyzing CpG dinucleotide frequencies in virus genomes have provided interesting insights on virus evolution. CpG dinucleotide depletion has not been extensively studied among papillomaviruses and polyomaviruses. We sought to analyze the relative abundance of dinucleotides and the relative roles of evolutionary pressures in papillomaviruses and polyomaviruses.

Methods: We studied 127 full-length sequences from papillomaviruses and 56 full-length sequences from polyomaviruses. We analyzed the relative abundance of dinucleotides, effective codon number (ENC), differences in synonymous codon usage. We examined the association, if any, between the extent of CpG dinucleotide depletion and the evolutionary lineage of the infected host. We also investigated the contribution of mutational pressure and translational selection to the evolution of papillomaviruses and polyomaviruses.

Results: All papillomaviruses and polyomaviruses are CpG depleted. Interestingly, the evolutionary lineage of the infected host determines the extent of CpG depletion among papillomaviruses and polyomaviruses. CpG dinucleotide depletion was more pronounced among papillomaviruses and polyomaviruses infecting human and other mammals as compared to those infecting birds. Our findings demonstrate that CpG depletion among papillomaviruses is linked to mutational pressure; while CpG depletion among polyomaviruses is linked to translational selection. We also present evidence that suggests methylation of CpG dinucleotides may explain, at least in part, the depletion of CpG dinucleotides among papillomaviruses but not polyomaviruses.

Conclusions: The extent of CpG depletion among papillomaviruses and polyomaviruses is linked to the evolutionary lineage of the infected host. Our results highlight the existence of divergent evolutionary pressures leading to CpG dinucleotide depletion among small ds-DNA viruses infecting vertebrate hosts.

No MeSH data available.


Related in: MedlinePlus

Relative synonymous codon usage (RSCU) values of CpG-containing codons.Box plots showing the RSCU values of CpG-containing codons among (a) papillomaviruses and (b) polyomaviruses. CpG-containing codons are shown in red colour. The encoded amino acid is shown in parenthesis. Both group of viruses avoided CpG-containing synonymous codons as 100% (8 out of 8) of these codons had an RSCU value below one. (c) RSCU values of CpG-containing codons among papillomaviruses infecting different host groups: papillomaviruses infecting humans or other mammals had significantly lower RSCU values than those infecting aves/reptiles [0.47(95% CI of 0.42 to 0.52) vs 0.8(95% CI of 0.68 to 0.92); P = 0.0004; 0.55(95% CI of 0.53 to 0.58) vs 0.8(95% CI of 0.68 to 0.92); P = 0.0002]. (d) RSCU values of CpG-containing codons among polyomaviruses infecting different host groups: polyomaviruses infecting humans had significantly lower RSCU values as compared to those infecting other mammals [0.11(95% CI of 0.09 to 0.14) vs 0.17(95% CI of 0.16 to 0.19), P = 0.0007] or aves [0.11(95% CI of 0.09 to 0.14) vs 0.45(95% CI of 0.34 to 0.57); P = 0.0003].
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pone.0142368.g003: Relative synonymous codon usage (RSCU) values of CpG-containing codons.Box plots showing the RSCU values of CpG-containing codons among (a) papillomaviruses and (b) polyomaviruses. CpG-containing codons are shown in red colour. The encoded amino acid is shown in parenthesis. Both group of viruses avoided CpG-containing synonymous codons as 100% (8 out of 8) of these codons had an RSCU value below one. (c) RSCU values of CpG-containing codons among papillomaviruses infecting different host groups: papillomaviruses infecting humans or other mammals had significantly lower RSCU values than those infecting aves/reptiles [0.47(95% CI of 0.42 to 0.52) vs 0.8(95% CI of 0.68 to 0.92); P = 0.0004; 0.55(95% CI of 0.53 to 0.58) vs 0.8(95% CI of 0.68 to 0.92); P = 0.0002]. (d) RSCU values of CpG-containing codons among polyomaviruses infecting different host groups: polyomaviruses infecting humans had significantly lower RSCU values as compared to those infecting other mammals [0.11(95% CI of 0.09 to 0.14) vs 0.17(95% CI of 0.16 to 0.19), P = 0.0007] or aves [0.11(95% CI of 0.09 to 0.14) vs 0.45(95% CI of 0.34 to 0.57); P = 0.0003].

Mentions: The extent of CpG dinucleotide depletion varies greatly across papillomaviruses and polyomaviruses. Nonetheless, all papillomaviruses and polyomaviruses are CpG depleted. In order to analyze CpG-containing synonymous codon usage preferences we studied the RSCU values of CpG-containing synonymous codons. Amino acids for which none of the synonymous codons contained CpG dinucleotides were not analyzed. Clearly, both group of viruses avoided CpG-containing synonymous codons as 100% (8 out of 8) of CpG-containing synonymous codon had an RSCU value below one (Fig 3a and 3b).


Depletion of CpG Dinucleotides in Papillomaviruses and Polyomaviruses: A Role for Divergent Evolutionary Pressures.

Upadhyay M, Vivekanandan P - PLoS ONE (2015)

Relative synonymous codon usage (RSCU) values of CpG-containing codons.Box plots showing the RSCU values of CpG-containing codons among (a) papillomaviruses and (b) polyomaviruses. CpG-containing codons are shown in red colour. The encoded amino acid is shown in parenthesis. Both group of viruses avoided CpG-containing synonymous codons as 100% (8 out of 8) of these codons had an RSCU value below one. (c) RSCU values of CpG-containing codons among papillomaviruses infecting different host groups: papillomaviruses infecting humans or other mammals had significantly lower RSCU values than those infecting aves/reptiles [0.47(95% CI of 0.42 to 0.52) vs 0.8(95% CI of 0.68 to 0.92); P = 0.0004; 0.55(95% CI of 0.53 to 0.58) vs 0.8(95% CI of 0.68 to 0.92); P = 0.0002]. (d) RSCU values of CpG-containing codons among polyomaviruses infecting different host groups: polyomaviruses infecting humans had significantly lower RSCU values as compared to those infecting other mammals [0.11(95% CI of 0.09 to 0.14) vs 0.17(95% CI of 0.16 to 0.19), P = 0.0007] or aves [0.11(95% CI of 0.09 to 0.14) vs 0.45(95% CI of 0.34 to 0.57); P = 0.0003].
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pone.0142368.g003: Relative synonymous codon usage (RSCU) values of CpG-containing codons.Box plots showing the RSCU values of CpG-containing codons among (a) papillomaviruses and (b) polyomaviruses. CpG-containing codons are shown in red colour. The encoded amino acid is shown in parenthesis. Both group of viruses avoided CpG-containing synonymous codons as 100% (8 out of 8) of these codons had an RSCU value below one. (c) RSCU values of CpG-containing codons among papillomaviruses infecting different host groups: papillomaviruses infecting humans or other mammals had significantly lower RSCU values than those infecting aves/reptiles [0.47(95% CI of 0.42 to 0.52) vs 0.8(95% CI of 0.68 to 0.92); P = 0.0004; 0.55(95% CI of 0.53 to 0.58) vs 0.8(95% CI of 0.68 to 0.92); P = 0.0002]. (d) RSCU values of CpG-containing codons among polyomaviruses infecting different host groups: polyomaviruses infecting humans had significantly lower RSCU values as compared to those infecting other mammals [0.11(95% CI of 0.09 to 0.14) vs 0.17(95% CI of 0.16 to 0.19), P = 0.0007] or aves [0.11(95% CI of 0.09 to 0.14) vs 0.45(95% CI of 0.34 to 0.57); P = 0.0003].
Mentions: The extent of CpG dinucleotide depletion varies greatly across papillomaviruses and polyomaviruses. Nonetheless, all papillomaviruses and polyomaviruses are CpG depleted. In order to analyze CpG-containing synonymous codon usage preferences we studied the RSCU values of CpG-containing synonymous codons. Amino acids for which none of the synonymous codons contained CpG dinucleotides were not analyzed. Clearly, both group of viruses avoided CpG-containing synonymous codons as 100% (8 out of 8) of CpG-containing synonymous codon had an RSCU value below one (Fig 3a and 3b).

Bottom Line: We analyzed the relative abundance of dinucleotides, effective codon number (ENC), differences in synonymous codon usage.CpG dinucleotide depletion was more pronounced among papillomaviruses and polyomaviruses infecting human and other mammals as compared to those infecting birds.The extent of CpG depletion among papillomaviruses and polyomaviruses is linked to the evolutionary lineage of the infected host.

View Article: PubMed Central - PubMed

Affiliation: Kusuma School of Biological Sciences, Indian Institute of Technology Delhi, New Delhi, 006, India.

ABSTRACT

Background: Papillomaviruses and polyomaviruses are small ds-DNA viruses infecting a wide-range of vertebrate hosts. Evidence supporting co-evolution of the virus with the host does not fully explain the evolutionary path of papillomaviruses and polyomaviruses. Studies analyzing CpG dinucleotide frequencies in virus genomes have provided interesting insights on virus evolution. CpG dinucleotide depletion has not been extensively studied among papillomaviruses and polyomaviruses. We sought to analyze the relative abundance of dinucleotides and the relative roles of evolutionary pressures in papillomaviruses and polyomaviruses.

Methods: We studied 127 full-length sequences from papillomaviruses and 56 full-length sequences from polyomaviruses. We analyzed the relative abundance of dinucleotides, effective codon number (ENC), differences in synonymous codon usage. We examined the association, if any, between the extent of CpG dinucleotide depletion and the evolutionary lineage of the infected host. We also investigated the contribution of mutational pressure and translational selection to the evolution of papillomaviruses and polyomaviruses.

Results: All papillomaviruses and polyomaviruses are CpG depleted. Interestingly, the evolutionary lineage of the infected host determines the extent of CpG depletion among papillomaviruses and polyomaviruses. CpG dinucleotide depletion was more pronounced among papillomaviruses and polyomaviruses infecting human and other mammals as compared to those infecting birds. Our findings demonstrate that CpG depletion among papillomaviruses is linked to mutational pressure; while CpG depletion among polyomaviruses is linked to translational selection. We also present evidence that suggests methylation of CpG dinucleotides may explain, at least in part, the depletion of CpG dinucleotides among papillomaviruses but not polyomaviruses.

Conclusions: The extent of CpG depletion among papillomaviruses and polyomaviruses is linked to the evolutionary lineage of the infected host. Our results highlight the existence of divergent evolutionary pressures leading to CpG dinucleotide depletion among small ds-DNA viruses infecting vertebrate hosts.

No MeSH data available.


Related in: MedlinePlus