1887

Abstract

The possibility of creating novel genes from pre-existing sequences, known as overprinting, is a widespread phenomenon in small viruses. Here, the origin and evolution of gene overlap in the bacteriophages belonging to the family have been investigated. The distinction between ancestral and derived frames was carried out by comparing the patterns of codon usage in overlapping and non-overlapping genes. By this approach, a gradual increase in complexity of the phage genome – from an ancestral state lacking gene overlap to a derived state with a high density of genetic information – was inferred. Genes encoding less-essential proteins, yet playing a role in phage growth and diffusion, were predicted to be novel genes that originated by overprinting. Evaluation of the rates of synonymous and non-synonymous substitution yielded evidence for overlapping genes under positive selection in one frame and purifying selection in the alternative frame.

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2006-04-01
2019-10-19
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References

  1. Bläsi, U. & Lubitz, W. ( 1985; ). Influence of C-terminal modifications of ϕX174 lysis gene E on its lysis-inducing properties. J Gen Virol 66, 1209–1213.[CrossRef]
    [Google Scholar]
  2. Bozarth, C. S., Weiland, J. J. & Dreher, T. W. ( 1992; ). Expression of ORF-69 of turnip yellow mosaic virus is necessary for viral spread in plants. Virology 187, 124–130.[CrossRef]
    [Google Scholar]
  3. Brentlinger, K. L., Hafenstein, S., Novak, C. R., Fane, A. B., Borgon, R., McKenna, R. & Agbandje-McKenna, M. ( 2002; ). Microviridae, a family divided: isolation, characterization, and genome sequence of ϕMH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibrio bacteriovorus. J Bacteriol 184, 1089–1094.[CrossRef]
    [Google Scholar]
  4. Bull, J. J., Badgett, M. R. & Wichman, H. A. ( 2000; ). Big-benefit mutations in a bacteriophage inhibited with heat. Mol Biol Evol 17, 942–950.[CrossRef]
    [Google Scholar]
  5. Dokland, T., McKenna, R., Ilag, L. L., Bowman, B. R., Incardona, N. L., Fane, B. A. & Rossmann, M. G. ( 1997; ). Structure of a viral procapsid with molecular scaffolding. Nature 389, 308–313.[CrossRef]
    [Google Scholar]
  6. Gibbs, A. & Keese, P. K. ( 1995; ). In search of the origins of viral genes. In Molecular Basis of Virus Evolution, pp. 76–90. Edited by A. Gibbs, C. H. Calisher & F. García-Arenal. Cambridge: Cambridge University Press.
  7. Gillam, S., Atkinson, T., Markham, A. & Smith, M. ( 1985; ). Gene K of bacteriophage ϕX174 codes for a protein which affects the burst size of phage production. J Virol 53, 708–709.
    [Google Scholar]
  8. Godson, G. N., Barrell, B. G., Staden, R. & Fiddes, J. C. ( 1978; ). Nucleotide sequence of bacteriophage G4 DNA. Nature 276, 236–247.[CrossRef]
    [Google Scholar]
  9. Guyader, S. & Ducray, D. G. ( 2002; ). Sequence analysis of Potato leafroll virus isolates reveals genetic stability, major evolutionary events and differential selection pressure between overlapping reading frame products. J Gen Virol 83, 1799–1807.
    [Google Scholar]
  10. Hughes, A. L., Westover, K., da Silva, J., O'Connor, D. H. & Watkins, D. I. ( 2001; ). Simultaneous positive and purifying selection on overlapping reading frames of the tat and vpr genes of simian immunodeficiency virus. J Virol 75, 7966–7972.[CrossRef]
    [Google Scholar]
  11. Hutchinson, C. A., III & Sinsheimer, R. L. ( 1966; ). The process of infection with bacteriophage ϕX174. X. Mutations in a ϕX lysis gene. J Mol Biol 18, 429–447.[CrossRef]
    [Google Scholar]
  12. Jordan, I. K., Sutter, B. A., IV & McClure, M. A. ( 2000; ). Molecular evolution of the paramyxoviridae and rhabdoviridae multiple-protein-encoding P gene. Mol Biol Evol 17, 75–86.[CrossRef]
    [Google Scholar]
  13. Keese, P. K. & Gibbs, A. ( 1992; ). Origin of genes: “big bang” or continuous creation? Proc Natl Acad Sci U S A 89, 9489–9493.[CrossRef]
    [Google Scholar]
  14. Kodaira, K., Nakano, K., Okada, S. & Taketo, A. ( 1992; ). Nucleotide sequence of the genome of the bacteriophage α3: interrelationship of the genome structure and the gene products with those of the phages, ΦX174, G4 and ΦK. Biochim Biophys Acta 1130, 277–288.[CrossRef]
    [Google Scholar]
  15. Krakauer, D. C. ( 2000; ). Stability and evolution of overlapping genes. Evolution 54, 731–739.[CrossRef]
    [Google Scholar]
  16. Miyata, T. & Yasunaga, T. ( 1978; ). Evolution of overlapping genes. Nature 272, 532–535.[CrossRef]
    [Google Scholar]
  17. Mizokami, M., Orito, E., Ohba, K., Ikeo, K., Lau, J. Y. N. & Gojobori, T. ( 1997; ). Constrained evolution with respect to gene overlap of hepatitis B virus. J Mol Evol 44 (Suppl. 1), S83–S90.[CrossRef]
    [Google Scholar]
  18. Morrison, D. F. ( 1976; ). Multivariate Statistical Methods. New York: McGraw-Hill.
  19. Narechania, A., Terai, M. & Burk, R. D. ( 2005; ). Overlapping reading frames in closely related human papillomaviruses result in modular rates of selection within E2. J Gen Virol 86, 1307–1313.[CrossRef]
    [Google Scholar]
  20. Nei, M. & Gojobori, T. ( 1986; ). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418–426.
    [Google Scholar]
  21. Pavesi, A. ( 2000; ). Detection of signature sequences in overlapping genes and prediction of a novel overlapping gene in hepatitis G virus. J Mol Evol 50, 284–295.
    [Google Scholar]
  22. Pavesi, A., De Iaco, B., Granero, M. I. & Porati, A. ( 1997; ). On the informational content of overlapping genes in prokaryotic and eukaryotic viruses. J Mol Evol 44, 625–631.[CrossRef]
    [Google Scholar]
  23. Renaudin, J., Pascarel, M.-C. & Bové, J.-M. ( 1987; ). Spiroplasma virus 4: nucleotide sequence of the viral DNA, regulatory signals, and proposed genome organization. J Bacteriol 169, 4950–4961.
    [Google Scholar]
  24. Sander, C. & Schulz, G. E. ( 1979; ). Degeneracy of the information contained in amino acid sequences: evidence from overlaid genes. J Mol Evol 13, 245–252.[CrossRef]
    [Google Scholar]
  25. Sanger, F., Air, G. M., Barrell, B. G., Brown, N. L., Coulson, A. R., Fiddes, C. A., Hutchinson, C. A., Slocombe, P. M. & Smith, M. ( 1977; ). Nucleotide sequence of bacteriophage ΦX174 DNA. Nature 265, 687–695.[CrossRef]
    [Google Scholar]
  26. Sharp, P. M. & Li, W.-H. ( 1987; ). The codon adaptation index – a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15, 1281–1295.[CrossRef]
    [Google Scholar]
  27. Spiropoulou, C. F. & Nichol, S. T. ( 1993; ). A small highly basic protein is encoded in overlapping frame within the P gene of vesicular stomatitis virus. J Virol 67, 3103–3110.
    [Google Scholar]
  28. Storey, C. C., Lusher, M. & Richmond, S. J. ( 1989; ). Analysis of the complete nucleotide sequence of Chp1, a phage which infects avian Chlamydia psittaci. J Gen Virol 70, 3381–3390.[CrossRef]
    [Google Scholar]
  29. Tessman, E. S., Tessman, I. & Pollock, T. J. ( 1980; ). Gene K of bacteriophage ϕX174 codes for a nonessential protein. J Virol 33, 557–560.
    [Google Scholar]
  30. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  31. Walewski, J. L., Keller, T. R., Stump, D. D. & Branch, A. D. ( 2001; ). Evidence for a new hepatitis C virus antigen encoded in an overlapping reading frame. RNA 7, 710–721.[CrossRef]
    [Google Scholar]
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