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PMID: 16557338 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses.

Journal of molecular evolution ·Vol. 62 ·No. 5 ·2006-05-00 ·Pages 551-63

Shackelton LA, Parrish CR, Holmes EC

Abstract

Understanding the extent and causes of biases in codon usage and nucleotide composition is essential to the study of viral evolution, particularly the interplay between viruses and host cells or immune responses. To understand the common features and differences among viruses we analyzed the genomic characteristics of a representative collection of all sequenced vertebrate-infecting DNA viruses. This revealed that patterns of codon usage bias are strongly correlated with overall genomic GC content, suggesting that genome-wide mutational pressure, rather than natural selection for specific coding triplets, is the main determinant of codon usage. Further, we observed a striking difference in CpG content between DNA viruses with large and small genomes. While the majority of large genome viruses show the expected frequency of CpG, most small genome viruses had CpG contents far below expected values. The exceptions to this generalization, the large gammaherpesviruses and iridoviruses and the small dependoviruses, have sufficiently different life-cycle characteristics that they may help reveal some of the factors shaping the evolution of CpG usage in viruses.

MeSH Terms
Animals Base Composition/genetics Codon/genetics DNA Viruses/genetics Evolution, Molecular Genome, Viral/genetics Mutation/genetics Nucleotides/chemistry Selection, Genetic Vertebrates/virology
Chemicals
Codon Nucleotides
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Shackelton Laura A
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.
Parrish Colin R
Holmes Edward C
References (54)
54 references, click to expand
  1. Herpes simplex virus type 1 DNA is immunostimulatory in vitro and in vivo.
    J Virol. 2003 Oct;77(20):11158-69 PMID: 14512563
  2. Compositional constraints and genome evolution.
    J Mol Evol. 1986;24(1-2):1-11 PMID: 3104608
  3. Methylation pattern of fish lymphocystis disease virus DNA.
    J Virol. 1985 Mar;53(3):1005-7 PMID: 3973962
  4. Similar rates but different modes of sequence evolution in introns and at exonic silent sites in rodents: evidence for selectively driven codon usage.
    Mol Biol Evol. 2004 Jun;21(6):1014-23 PMID: 15014158
  5. Predicting DNA duplex stability from the base sequence.
    Proc Natl Acad Sci U S A. 1986 Jun;83(11):3746-50 PMID: 3459152
  6. Stealth technology: how Epstein-Barr virus utilizes DNA methylation to cloak itself from immune detection.
    Clin Immunol. 2003 Oct;109(1):53-63 PMID: 14585276
  7. Nucleotide composition as a driving force in the evolution of retroviruses.
    J Mol Evol. 1994 May;38(5):506-32 PMID: 8028030
  8. Analysis of synonymous codon usage in SARS Coronavirus and other viruses in the Nidovirales.
    Virus Res. 2004 May;101(2):155-61 PMID: 15041183
  9. Intercodon dinucleotides affect codon choice in plant genes.
    Nucleic Acids Res. 2000 Sep 1;28(17):3339-45 PMID: 10954603
  10. Local DNA demethylation in vertebrates: how could it be performed and targeted?
    FEBS Lett. 2001 Apr 13;494(3):135-40 PMID: 11311228
  11. Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases.
    Nucleic Acids Res. 1994 Jul 11;22(13):2437-46 PMID: 8041603
  12. Compartmentation of intracellular nucleotides in mammalian cells.
    CRC Crit Rev Biochem. 1985;19(1):45-61 PMID: 2416510
  13. Synonymous codon bias is not caused by mutation bias in G+C-rich genes in humans.
    Mol Biol Evol. 2001 Jun;18(6):982-6 PMID: 11371586
  14. The structure of B-helical C-G-A-T-C-G-A-T-C-G and comparison with C-C-A-A-C-G-T-T-G-G. The effect of base pair reversals.
    J Biol Chem. 1991 May 15;266(14):8861-83 PMID: 2026600
  15. Mammalian mutation pressure, synonymous codon choice, and mRNA degradation.
    J Mol Evol. 2003 Dec;57(6):694-701 PMID: 14745538
  16. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells.
    J Exp Med. 2003 Aug 4;198(3):513-20 PMID: 12900525
  17. Structural deviations at CpG provide a plausible explanation for the high frequency of mutation at this site. Phosphorus nuclear magnetic resonance and circular dichroism studies.
    J Mol Biol. 1993 Mar 20;230(2):373-8 PMID: 8464051
  18. Evolution of the genome and the genetic code: selection at the dinucleotide level by methylation and polyribonucleotide cleavage.
    Proc Natl Acad Sci U S A. 1989 Jan;86(1):192-6 PMID: 2463621
  19. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes.
    Nucleic Acids Res. 1986 Jul 11;14(13):5125-43 PMID: 3526280
  20. Codon usage bias and A+T content variation in human papillomavirus genomes.
    Virus Res. 2003 Dec;98(2):95-104 PMID: 14659556
  21. Genomic sequencing reveals absence of DNA methylation in the major late promoter of adenovirus type 2 DNA in the virion and in productively infected cells.
    FEBS Lett. 1995 Apr 10;362(3):301-5 PMID: 7729517
  22. Frog virus 3 DNA is heavily methylated at CpG sequences.
    Virology. 1980 Nov;107(1):250-7 PMID: 6255678
  23. Dinucleotide relative abundance extremes: a genomic signature.
    Trends Genet. 1995 Jul;11(7):283-90 PMID: 7482779
  24. Over- and under-representation of short oligonucleotides in DNA sequences.
    Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1358-62 PMID: 1741388
  25. DNA methylation and the Epstein-Barr virus.
    Semin Cancer Biol. 1999 Oct;9(5):369-75 PMID: 10547345
  26. Methylation of viral DNA in vivo and in vitro.
    Virology. 1979 Nov;99(1):152-7 PMID: 227158
  27. Why is CpG suppressed in the genomes of virtually all small eukaryotic viruses but not in those of large eukaryotic viruses?
    J Virol. 1994 May;68(5):2889-97 PMID: 8151759
  28. The extent of codon usage bias in human RNA viruses and its evolutionary origin.
    Virus Res. 2003 Mar;92(1):1-7 PMID: 12606071
  29. Compositional correlation between deoxyribonucleic acid and protein.
    Cold Spring Harb Symp Quant Biol. 1961;26:35-43 PMID: 13918160
  30. Methylation, mutation and cancer.
    Bioessays. 1992 Jan;14(1):33-6 PMID: 1546979
  31. Specific correlations between relative synonymous codon usage and protein secondary structure.
    J Mol Biol. 1998 Aug 7;281(1):31-48 PMID: 9680473
  32. Compositional differences within and between eukaryotic genomes.
    Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10227-32 PMID: 9294192
  33. Accounting for background nucleotide composition when measuring codon usage bias.
    Mol Biol Evol. 2002 Aug;19(8):1390-4 PMID: 12140252
  34. High rate of viral evolution associated with the emergence of carnivore parvovirus.
    Proc Natl Acad Sci U S A. 2005 Jan 11;102(2):379-84 PMID: 15626758
  35. Genome-scale compositional comparisons in eukaryotes.
    Genome Res. 2001 Apr;11(4):540-6 PMID: 11282969
  36. Evidence for selective evolution in codon usage in conserved amino acid segments of human alphaherpesvirus proteins.
    J Mol Evol. 1991 Dec;33(6):483-94 PMID: 1663999
  37. Codon usage in bacteria: correlation with gene expressivity.
    Nucleic Acids Res. 1982 Nov 25;10(22):7055-74 PMID: 6760125
  38. The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense.
    J Exp Med. 2003 Feb 3;197(3):343-51 PMID: 12566418
  39. The 'effective number of codons' used in a gene.
    Gene. 1990 Mar 1;87(1):23-9 PMID: 2110097
  40. Evolution of codon usage bias in Drosophila.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7784-90 PMID: 9223264
  41. CpG DNA: trigger of sepsis, mediator of protection, or both?
    Scand J Infect Dis. 2003;35(9):653-9 PMID: 14620150
  42. Maximizing transcription efficiency causes codon usage bias.
    Genetics. 1996 Nov;144(3):1309-20 PMID: 8913770
  43. The evolution of large DNA viruses: combining genomic information of viruses and their hosts.
    Trends Microbiol. 2004 Oct;12(10):458-65 PMID: 15381195
  44. Replication of African swine fever virus DNA in infected cells.
    Virology. 1999 May 10;257(2):524-36 PMID: 10329562
  45. The nucleic acids of some insect viruses.
    J Gen Physiol. 1952 Nov;36(2):201-5 PMID: 13011277
  46. Effect of distortions in the phosphate backbone conformation of six related octanucleotide duplexes on CD and 31P NMR spectra.
    Biochemistry. 1993 Jul 20;32(28):7079-88 PMID: 8393703
  47. Codon usage: mutational bias, translational selection, or both?
    Biochem Soc Trans. 1993 Nov;21(4):835-41 PMID: 8132077
  48. Codon usage and genome evolution.
    Curr Opin Genet Dev. 1994 Dec;4(6):851-60 PMID: 7888755
  49. Evolution of the feline-subgroup parvoviruses and the control of canine host range in vivo.
    J Virol. 1995 Aug;69(8):4702-10 PMID: 7609035
  50. The immunobiology of the TLR9 subfamily.
    Trends Immunol. 2004 Jul;25(7):381-6 PMID: 15207506
  51. Viruses and Toll-like receptors.
    Microbes Infect. 2003 Sep;5(11):961-8 PMID: 12941388
  52. The iridoviruses.
    Adv Virus Res. 1996;46:345-412 PMID: 8824704
  53. Codon usage and secondary structure of mRNA.
    Nucleic Acids Symp Ser. 1990;(22):93-4 PMID: 2101925
  54. Initial sequencing and analysis of the human genome.
    Nature. 2001 Feb 15;409(6822):860-921 PMID: 11237011
Article Info
Journal
Journal of molecular evolution
Abbr.
J Mol Evol
ISSN
0022-2844
Published
2006-05-00
Epub
2006-00-22
Pages
551-63
Language
English
Region
Germany
NLM ID
0360051
Subset
IM
Grants
NIAID NIH HHS · R01AI028385 · United States
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