Preferences help
enabled [disable] Abstract
Number of results
2001 | 48 | 2 | 391-407
Article title

How RNA viruses exchange their genetic material.

Title variants
Languages of publication
One of the most unusual features of RNA viruses is their enormous genetic variability. Among the different processes contributing to the continuous generation of new viral variants RNA recombination is of special importance. This process has been observed for human, animal, plant and bacterial viruses. The collected data reveal a great susceptibility of RNA viruses to recombination. They also indicate that genetic RNA recombination (especially the nonhomologous one) is a major factor responsible for the emergence of new viral strains or species. Although the formation and accumulation of viral recombinants was observed in numerous RNA viruses, the molecular basis of this phenomenon was studied in only a few viral species. Among them, brome mosaic virus (BMV), a model (+)RNA virus offers the best opportunities to investigate various aspects of genetic RNA recombination in vivo. Unlike any other, the BMV-based system enables homologous and nonhomologous recombination studies at both the protein and RNA levels. As a consequence, BMV is the virus for which the structural requirements for genetic RNA recombination have been most precisely established. Nevertheless, the previously proposed model of genetic recombination in BMV still had one weakness: it could not really explain the role of RNA structure in nonhomologous recombination. Recent discoveries concerning the latter problem give us a chance to fill this gap. That is why in this review we present and thoroughly discuss all results concerning nonhomologous recombination in BMV that have been obtained until now.
Physical description
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • 1. Holland, J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S. & Van de Pol, S. (1982) Rapid evolution of RNA genomes. Science 215, 1577-1585.
  • 2. Pathak, V.K. & Hu, W.S. (1997) Might as well Jump! Temple switching by retroviral reverse transcriptase, defective genome formation and recombination. Semin. Virol. 8, 141-150.
  • 3. Holland, J., DelaTorre, J.C. & Steinhauer, D.A. (1992) RNA virus populations as quasispecies; in Genetic Diversity of RNA Viruses. (Holland, J., ed.) pp. 1-20, Springer Verlag.
  • 4. Domingo, E., Holland, J., Biebricher, C. & Eigen, M. (1995) Quasi-species: The concept and the word; in Molecular Basis of Virus Evolution (Gibbs, A.G., Calisher, C.H. & Garcia-Arenal, F., eds.) pp.181-191, Cambridge University Press, Cambridge.
  • 5. Eigen, M. (1996) On the nature of virus quasispecies. Trends Microbiol. 4, 216-217.
  • 6. Steinhauer, D.A. & Holland, J.J. (1983) Rapid evolution of RNA viruses. Annu. Rev. Microbiol. 41, 409-433.
  • 7. Smith, D.B. & Inglis, S.C. (1987) The mutation rate and variability of eucaryotic viruses: An analytical review. J. Gen. Virol. 68, 2729- 2740.
  • 8. Pathak, V.K. & Temin, H.M. (1990) Broad spectrum of in vivo forward mutations, hypermutations, and hotspots in a retroviral shuttle vector after a single replication cycle: Substitutions, frameshifts, and hypermutations. Proc. Natl. Acad. Sci. U.S.A. 87, 6019-6023.
  • 9. Pathak, V.K. & Temin, H.M. (1990) Broad spectrum of in vivo forward mutations, hypermutations, and hotspots in a retroviral shuttle vector after a single replication cycle: Deletions and deletions with insertions. Proc. Natl. Acad. Sci. U.S.A. 87, 6024-6028.
  • 10. Kim, T., Mudry, R.A., Jr., Rexrode, C.A. & Pathak, V.K. (1996) Retroviral mutation rates and A-to-G hypermutation during different stages of retroviral replication. J. Virol. 70, 7594-7602.
  • 11. Coffin, J.M. (1979) Structure, replication and recombination of retrovirus genomes. Some unifying hypotheses. J. Gen. Virol. 42, 1-26.
  • 12. Lai, M.M.C. (1992) RNA recombination in animal and plant viruses. Microbiol. Rev. 56, 61-79.
  • 13. Zhang, J. & Temin, H.M. (1993) Rate and mechanism of nonhomologous recombination during a single cycle of retroviral replication. Science 259, 234-238.
  • 14. Simon, A.E. & Bujarski, J.J. (1994) RNA-RNA recombination and evolution in virus-infected plants. Annu. Rev. Phytopathol. 32, 337-362.
  • 15. Khatchikian, D., Orlich, M. & Rott, R. (1989) Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the hemagglutinin gene of an influenza virus. Nature 340, 156-157.
  • 16. Meyers, G., Tautz, N., Dubovi, E.J. & Thiel, H.J. (1991) Viral cytopathogenicity correlated with integration of ubiquitin-coding sequences. Virology 180, 602-616.
  • 17. Green, A.M. & Allison, R.F. (1994) Recombination between viral RNA and transgenic plant transcripts. Science 263, 1423-1425.
  • 18. Kirkegaard, K. & Baltimore, D. (1986) The mechanism of RNA recombination in poliovirus. Cell 47, 433-443.
  • 19. Figlerowicz, M., Nagy, P.D. & Bujarski, J.J. (1997) A mutation in the putative RNA polymerase gene inhibits nonhomologous, but not homologous, genetic recombination in RNA virus. Proc. Natl. Acad. Sci. U.S.A. 94, 2073-2078.
  • 20. Figlerowicz, M., Nagy, P.D., Tang, N., Kao, C.C. & Bujarski, J.J. (1998) Mutations in the N-terminus of the brome mosaic virus polymerase affect genetic RNA-RNA recombination. J. Virol. 72, 9192-9200.
  • 21. Stuhlmann, H. & Berg, P. (1992) Homologous recombination of copackage retrovirus RNAs during reverse transcription. J. Virol. 66, 2378-2381.
  • 22. Figlerowicz, M. & Bujarski, J.J. (1998) RNA recombination in brome mosaic virus, a model plus stranded RNA virus. Acta Biochim. Polon. 45, 847-68.
  • 23. Nagy, P.D., Zhang, C. & Simon, A.E. (1998) Dissecting RNA recombination in vitro: Role of RNA sequences and the viral replicase. EMBO J. 17, 2392-2403.
  • 24. Romanova, L.I., Blinov, V.M., Tolskaya, E.A., Viktorova, E.G., Kolesnikova, M.S., Guseva, E.A. & Agol, V.I. (1986) The primary structure of crossovers regions of intertypic poliovirus recombinants: A model of recombination between RNA genomes. Virology 155, 202-213.
  • 25. Nagy, P.D. & Bujarski, J.J. (1993) Targeting the site of RNA-RNA recombination in brome mosaic virus with antisense sequences. Proc. Natl. Acad. Sci. U.S.A. 90, 6390-6394.
  • 26. Zhang, X. & Lai, M.M.C. (1994) Unusual heterogeneity of leader-mRNA fusion in a murine coronavirus: Implications for the mechanism of RNA transcription and recombination. J. Virol. 68, 6626-6633.
  • 27. Vogt, P.K. (1971) The genome of avian RNA tumor viruses: A discussion of four models; in Possible Episomes in Eukaryotes (Sylvestri, L., ed.) pp. 35-41, North-Holland, Amsterdam.
  • 28. Chetverin, A.B., Chetverina, H.V., Demidenko, A.A. & Ugarov, V.I. (1997) Nonhomologous RNA recombination in a cell-free system: Evidence for a transesterification mechanism guided by secondary structure. Cell 88, 503-513.
  • 29. King, A.M.Q. (1988) Genetic recombination in positive strand RNA viruses; in RNA Genetics (Domingo, P., Holland, J.J. & Ahlquist, P., eds.) vol. 2, pp. 149-165, CRC Press, Boca Raton.
  • 30. Fields Virology (1996) (Fields, B.M., ed.) 3rd edn., Lippincott-Raven Publishers, Philadelphia, New Jork.
  • 31. Hirst, G.K. (1962) Genetic recombination with Newcastle disease virus, poliovirus and influenza. Cold Spring Harbor Symp. Qant. Biol. 27, 303-309.
  • 32. Ledinko, N. (1963) Genetic recombination with poliovirus type 1 studies of crosses between a normal horse serum-resistant mutant and several guanidine-resistant mutants of the same strain. Virology 20, 107-119.
  • 33. Pringle, C.R. (1965) Evidence of genetic recombination in foot-and-mouth disease virus. Virology 25, 48-54.
  • 34. Jarvis, T.C. & Kirkegaard, K. (1992) Poliovirus RNA recombination: Mechanistic studies in the absence of selection. EMBO J. 11, 3135-3145.
  • 35. Pilipenco, E.V., Gmyl, A.P. & Agol, V.I. (1995) A model for rearrangements in RNA genomes. Nucleic Acids Res. 23, 1870-1875.
  • 36. Fu, K. & Baric, R.S. (1992) Evidence for variable rates of recombination in MHV genome. Virology 189, 88-102.
  • 37. Fu, K. & Baric, R.S. (1994) Map locations of mouse hepatitis virus temperature-sensitive mutants: Confirmation of variable rates of recombination. J. Virol. 68, 7458-7466.
  • 38. Banner, L.R., Keck, J.G. & Lai, M.M.C. (1990) A clustering of RNA recombination sites adjacent to a hyper-variable region of the peplomer gene of murine coronavirus. Virology 175, 548-555.
  • 39. Simon, A.E. & Howell, S.H. (1986) The virulent satellite RNA of turnip crinkle virus has a major domain homologous to the 3'-end of the helper virus genome. EMBO J. 7, 3423-3428.
  • 40. Oh, J.W., Kong, Q., Song, C., Carpenter, C.D. & Simon, A.E. (1995) Open reading frames of turnip crinkle virus involved in satellite symptom expression and incompatibility with Arabidopsis thaliana ecotype Dijon. Mol. Plant Microbe Interact. 8, 979-987.
  • 41. Li, X.H., Heaton, L.A., Morris, T.J. & Simon, A.E. (1989) Turnip crinkle virus defective interfering RNAs intensify viral symptoms and are generated de novo. Proc. Natl. Acad. Sci. U.S.A. 86, 9173-9177.
  • 42. Cascone, P.J., Carpenter, C.D., Li, X.H. & Simon, A.E. (1990) RNA recombination between satellite RNAs of turnip crinkle virus. EMBO J. 9, 1709-1715.
  • 43. Cascone, P.J., Haydar, T.F. & Simon, A.E. (1993) Sequences and structures required for recombination between virus-assisted RNAs. Science 260, 801-805.
  • 44. Zhang, C., Cascone, P.J. & Simon, A.E. (1991) Recombination between satellite and genomic RNAs of turnip crinkle virus. Virology 184, 791-794.
  • 45. Carpenter, C.D., Oh, J.W., Zhang, C. & Simon, A.E. (1995) Involvement of a stem-loop structure in the location of junction sites in viral RNA recombination. J. Mol. Biol. 245, 608-622.
  • 46. Mindich, L., Qiao, X., Onodera, S., Gottlieb, P. & Strassman, J. (1992) Heterologous recombination in the double-stranded RNA bacteriophage Φ6. J. Virol. 66, 2605-2610.
  • 47. Onodera, S., Qiao, X., Gottlieb, P., Strassman, J., Frilander, M. & Mindich, L. (1993) RNA structure and heterologous recombination in the double-stranded RNA bacteriophage Φ6. J. Virol. 67, 4914-4922.
  • 48. Li, Y. & Ball, L.A. (1993) Non-homologous RNA recombination during negative strand synthesis of flock house virus RNA. J Virol. 67, 3854-3860.
  • 49. Raju, R., Subramaniam, S.V. & Hajjou, M. (1995) Genesis of Sindbis virus by in vivo recombination of nonreplicative RNA precursors. J. Virol. 69, 7391-7401.
  • 50. Ahlquist, P. (1992) Bromovirus RNA replication and transcription. Curr. Opin. Genet. Dev. 2, 71-76.
  • 51. Bujarski, J.J. & Kaesberg, P. (1986) Genetic recombination in a multipartite plant virus Nature 321, 528-531.
  • 52. Nagy, P.D. & Bujarski, J.J. (1995) Efficient system of homologous RNA recombination in brome mosaic virus: Sequence and structure requirements and accuracy of crossovers. J. Virol. 69, 131-140.
  • 53. Figlerowicz, M. (2000) Role of RNA structure in heteroduplex-mediated and site-specific nonhomologous recombination in brome mosaic virus. Nucleic Acids Res. 28, 1714-1723.
  • 54. Figlerowicz, M. & Bibiłło, A. (2000) RNA motifs mediating in vivo site-specific nonhomologous recombination in (+) RNA virus enforce in vitro nonhomologous crossovers with HIV-1 reverse transcriptase. RNA 6, 339-351.
  • 55. von Hippel, P.H. (1998) An integrated model of the transcription complex in elongation, termination and editing. Science 281, 660-665.
  • 56. Bibiłło, A., Figlerowicz, M. & Kierzek, R. (1999) The non-enzymatic hydrolysis of oligoribonucleotides. VI. The role of biogenic polyamines. Nucleic Acids Res. 27, 3931-3937.
  • 57. Bibiłło, A., Figlerowicz, M. & Kierzek, R. (1999) Nonenzymatic hydrolysis of oligoribonucleotides. VII Structural elements affecting hydrolysis. Nucleosides Nucleotides Nucleic Acids 19, 977-994.
  • 58. Kierzek, R. (1992) Hydrolysis of oligoribonucleotides: Influence of sequence and length. Nucleic Acids Res. 20, 5073-5077.
  • 59. Kierzek, R. (1992) Nonenzymatic hydrolysis of oligoribonucleotides. Nucleic Acids Res. 20, 5079-5084.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.