1887

Abstract

Recent studies have suggested that antagonistic epistasis (i.e. mutations having smaller effects in combination than alone) may be common among RNA viruses, in contrast to other biological systems. Here, by re-analysing previously published data from a random viral library, selection and epistasis coefficients were estimated in the U5-IR stem and loop of the , a region that adopts a conserved secondary structure and is involved in various essential steps of viral infection. The estimated mutational fitness effects are extremely high and genetic interactions are antagonistic on average. This pattern might be representative of RNA virus genomes, which show high compaction and frequent secondary structures. The implications for RNA virus adaptability are explored.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81585-0
2006-06-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/6/1595.html?itemId=/content/journal/jgv/10.1099/vir.0.81585-0&mimeType=html&fmt=ahah

References

  1. Bonhoeffer, S., Chappey, C., Parkin, N. T., Whitcomb, J. M. & Petropoulos, C. J. ( 2004; ). Evidence for positive epistasis in HIV-1. Science 306, 1547–1550.[CrossRef]
    [Google Scholar]
  2. Bruggeman, J., Debets, A. J., Wijngaarden, P. J., de Visser, J. A. G. M. & Hoekstra, R. F. ( 2003; ). Sex slows down the accumulation of deleterious mutations in the homothallic fungus Aspergillus nidulans. Genetics 164, 479–485.
    [Google Scholar]
  3. Buckling, A., Wills, M. A. & Colegrave, N. ( 2003; ). Adaptation limits diversification of experimental bacterial populations. Science 302, 2107–2109.[CrossRef]
    [Google Scholar]
  4. Burch, C. L. & Chao, L. ( 2004; ). Epistasis and its relationship to canalization in the RNA virus ϕ6. Genetics 167, 559–567.[CrossRef]
    [Google Scholar]
  5. Burch, C. L., Turner, P. E. & Hanley, K. A. ( 2003; ). Patterns of epistasis in RNA viruses: a review of the evidence from vaccine design. J Evol Biol 16, 1223–1235.[CrossRef]
    [Google Scholar]
  6. Butcher, D. ( 1995; ). Muller's ratchet, epistasis and mutation effects. Genetics 141, 431–437.
    [Google Scholar]
  7. Chao, L. ( 1990; ). Fitness of RNA virus decreased by Muller's ratchet. Nature 348, 454–455.[CrossRef]
    [Google Scholar]
  8. Crow, J. F. ( 1970; ). Genetic loads and the cost of natural selection. In Mathematical Topics in Population Genetics, pp. 128–177. New York: Springer.
  9. de Visser, J. A. G. M. & Hoekstra, R. F. ( 1998; ). Synergistic epistasis between loci affecting fitness: evidence in plants and fungi. Genet Res 71, 39–49.[CrossRef]
    [Google Scholar]
  10. de Visser, J. A. G. M., Hoekstra, R. F. & van den Ende, H. ( 1996; ). The effect of sex and deleterious mutations on fitness in Chlamydomonas. Proc R Soc Lond B Biol Sci 263, 193–200.[CrossRef]
    [Google Scholar]
  11. Dobzhansky, T. H. ( 1936; ). Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21, 113–135.
    [Google Scholar]
  12. Domingo, E. & Holland, J. J. ( 1997; ). RNA virus mutations and fitness for survival. Annu Rev Microbiol 51, 151–178.[CrossRef]
    [Google Scholar]
  13. Domingo, E., Escarmís, C., Sevilla, N., Moya, A., Elena, S. F., Quer, J., Novella, I. S. & Holland, J. J. ( 1996; ). Basic concepts in RNA virus evolution. FASEB J 10, 859–864.
    [Google Scholar]
  14. Domingo, E., Biebricher, C. K., Eigen, M. & Holland, J. J. ( 2001; ). Quasispecies and RNA Virus Evolution: Principles and Consequences. Edited by Landes Bioscience, Austin, Texas.
  15. Elena, S. F. ( 1999; ). Little evidence for synergism among deleterious mutations in a nonsegmented RNA virus. J Mol Evol 49, 703–707.[CrossRef]
    [Google Scholar]
  16. Elena, S. F. & Lenski, R. E. ( 1997; ). Test of synergistic interactions among deleterious mutations in bacteria. Nature 390, 395–398.[CrossRef]
    [Google Scholar]
  17. Elena, S. F. & Lenski, R. E. ( 2001; ). Epistasis between new mutations and genetic background and a test of genetic canalization. Evolution Int J Org Evolution 55, 1746–1752.[CrossRef]
    [Google Scholar]
  18. Elena, S. F., Ekunwe, L., Hajela, N., Oden, S. A. & Lenski, R. E. ( 1998; ). Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica 102–103, 349–358.
    [Google Scholar]
  19. Elena, S. F., Carrasco, P., Daròs, J. A. & Sanjuán, R. ( 2006; ). Mechanisms of genetic robustness in RNA viruses. EMBO Rep 7, 168–173.[CrossRef]
    [Google Scholar]
  20. Hofacker, I. L., Stadler, P. F. & Stocsits, R. R. ( 2004; ). Conserved RNA secondary structures in viral genomes: a survey. Bioinformatics 20, 1495–1499.[CrossRef]
    [Google Scholar]
  21. Holland, J. J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S. & VandePol, S. ( 1982; ). Rapid evolution of RNA genomes. Science 215, 1577–1585.[CrossRef]
    [Google Scholar]
  22. Johnson, J. B. & Omland, K. S. ( 2004; ). Model selection in ecology and evolution. Trends Ecol Evol 19, 101–108.[CrossRef]
    [Google Scholar]
  23. Johnson, M., Morris, S., Chen, A., Stavnezer, E. & Leis, J. ( 2004; ). Selection of functional mutations in the U5-IR stem and loop regions of the Rous sarcoma virus genome. BMC Biol 2, 8.[CrossRef]
    [Google Scholar]
  24. Keightley, P. D. ( 1994; ). The distribution of mutation effects on viability in Drosophila melanogaster. Genetics 138, 1315–1322.
    [Google Scholar]
  25. Kibota, T. T. & Lynch, M. ( 1996; ). Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381, 694–696.[CrossRef]
    [Google Scholar]
  26. Kondrashov, A. S. ( 1988; ). Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440.[CrossRef]
    [Google Scholar]
  27. Kondrashov, A. S. ( 1994; ). Muller's ratchet under epistatic selection. Genetics 136, 1469–1473.
    [Google Scholar]
  28. Mukai, T. ( 1969; ). The genetic structure of natural populations of Drosophila melanogaster. VII. Synergistic interaction of spontaneous mutant polygenes controlling viability. Genetics 61, 749–761.
    [Google Scholar]
  29. Muller, H. J. ( 1939; ). Reversibility of evolution considered from the standpoint of genetics. Biol Rev Camb Philos Soc 14, 261–280.[CrossRef]
    [Google Scholar]
  30. Novella, I. S. ( 2003; ). Contributions of vesicular stomatitis virus to the understanding of RNA virus evolution. Curr Opin Microbiol 6, 399–405.[CrossRef]
    [Google Scholar]
  31. Novella, I. S., Duarte, E. A. Elena S. F., Moya, A., Domingo, E. & Holland, J. J. ( 1995; ). Exponential increases of RNA virus fitness during large population transmissions. Proc Natl Acad Sci U S A 92, 5841–5844.[CrossRef]
    [Google Scholar]
  32. Novella, I. S., Zárate, S., Metzgar, D. & Ebendick-Corpus, B. E. ( 2004; ). Positive selection of synonymous mutations in vesicular stomatitis virus. J Mol Biol 342, 1415–1421.[CrossRef]
    [Google Scholar]
  33. Ruiz-Jarabo, C. M., Arias, A., Baranowski, E., Escarmís, C. & Domingo, E. ( 2000; ). Memory in viral quasispecies. J Virol 74, 3543–3547.[CrossRef]
    [Google Scholar]
  34. Sanjuán, R., Moya, A. & Elena, S. F. ( 2004a; ). The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci U S A 101, 8396–8401.[CrossRef]
    [Google Scholar]
  35. Sanjuán, R., Moya, A. & Elena, S. F. ( 2004b; ). The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci U S A 101, 15376–15379.[CrossRef]
    [Google Scholar]
  36. Sokal, R. R. & Rohlf, F. J. ( 2000; ). Biometry: the Principles and Practice of Statistics in Biological Research. New York, USA: Freeman.
  37. Whitlock, M. C. & Bourguet, D. ( 2000; ). Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution Int J Org Evolution 54, 1654–1660.[CrossRef]
    [Google Scholar]
  38. Wilke, C. O. & Adami, C. ( 2001; ). Interaction between directional epistasis and average mutational effects. Proc R Soc Lond B Biol Sci 268, 1469–1474.[CrossRef]
    [Google Scholar]
  39. Wilke, C. O., Lenski, R. E. & Adami, C. ( 2003; ). Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol 3, 3.[CrossRef]
    [Google Scholar]
  40. Wolf, J. B., Brodie, E. D., III & Wade, M. J. ( 2000; ). Epistasis and the Evolutionary Process. Edited by Oxford University Press, Oxford, UK.
  41. Wright, S. ( 1931; ). Evolution in mendelian populations. Genetics 16, 97–159.
    [Google Scholar]
  42. Wright, S. ( 1982; ). The shifting balance theory and macroevolution. Annu Rev Genet 16, 1–19.[CrossRef]
    [Google Scholar]
  43. You, L. & Yin, J. ( 2002; ). Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage T7. Genetics 160, 1273–1281.
    [Google Scholar]
  44. Yuste, E., Sánchez-Palomino, S., Casado, C., Domingo, E. & López-Galíndez, C. ( 1999; ). Drastic fitness loss in human immunodeficiency virus type 1 upon serial bottleneck events. J Virol 73, 2745–2751.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81585-0
Loading
/content/journal/jgv/10.1099/vir.0.81585-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error