1887

Abstract

Experimental investigations into virus recombination can provide valuable insights into the biochemical mechanisms and the evolutionary value of this fundamental biological process. Here, we describe an experimental scheme for studying recombination that should be applicable to any recombinogenic viruses amenable to the production of synthetic infectious genomes. Our approach is based on differences in fitness that generally exist between synthetic chimaeric genomes and the wild-type viruses from which they are constructed. In mixed infections of defective reciprocal chimaeras, selection strongly favours recombinant progeny genomes that recover a portion of wild-type fitness. Characterizing these evolved progeny viruses can highlight both important genetic fitness determinants and the contribution that recombination makes to the evolution of their natural relatives. Moreover, these experiments supply precise information about the frequency and distribution of recombination breakpoints, which can shed light on the mechanistic processes underlying recombination. We demonstrate the value of this approach using the small single-stranded DNA geminivirus, maize streak virus (MSV). Our results show that adaptive recombination in this virus is extremely efficient and can yield complex progeny genomes comprising up to 18 recombination breakpoints. The patterns of recombination that we observe strongly imply that the mechanistic processes underlying rolling circle replication are the prime determinants of recombination breakpoint distributions found in MSV genomes sampled from nature.

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2009-03-01
2020-01-24
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References

  1. Casado, C. G., Javier, O. G., Padron, E., Bean, S. J., McKenna, R., Agbandje-McKenna, M. & Boulton, M. I. ( 2004; ). Isolation and characterization of subgenomic DNAs encapsidated in “single” T = 1 isometric particles of Maize streak virus. Virology 323, 164–171.[CrossRef]
    [Google Scholar]
  2. Chao, L. ( 1990; ). Fitness of RNA virus decreased by Muller's ratchet. Nature 348, 454–455.[CrossRef]
    [Google Scholar]
  3. Chare, E. R. & Holmes, E. C. ( 2006; ). A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151, 933–946.[CrossRef]
    [Google Scholar]
  4. Chenault, K. D. & Melcher, U. ( 1994; ). Phylogenetic relationships reveal recombination among isolates of cauliflower mosaic virus. J Mol Evol 39, 496–505.
    [Google Scholar]
  5. Delatte, H., Martin, D. P., Naze, F., Goldbach, R., Reynaud, B., Peterschmitt, M. & Lett, J. M. ( 2005; ). South West Indian Ocean islands tomato begomovirus populations represent a new major monopartite begomovirus group. J Gen Virol 86, 1533–1542.[CrossRef]
    [Google Scholar]
  6. de Visser, J. A. & Elena, S. F. ( 2007; ). The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 8, 139–149.
    [Google Scholar]
  7. Donson, J., Morris-Krsinich, B. A., Mullineaux, P. M., Boulton, M. I. & Davies, J. W. ( 1984; ). A putative primer for second-strand DNA synthesis of maize streak virus is virion-associated. EMBO J 3, 3069–3073.
    [Google Scholar]
  8. Drummond, D. A., Silberg, J. J., Meyer, M. M., Wilke, C. O. & Arnold, F. H. ( 2005; ). On the conservative nature of intragenic recombination. Proc Natl Acad Sci U S A 102, 5380–5385.[CrossRef]
    [Google Scholar]
  9. Felsenstein, J. ( 1974; ). The evolutionary advantage of recombination. Genetics 78, 737–756.
    [Google Scholar]
  10. García-Andrés, S., Monci, F., Navas-Castillo, J. & Moriones, E. ( 2006; ). Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: evidence for the presence of a new virus species of recombinant nature. Virology 350, 433–442.[CrossRef]
    [Google Scholar]
  11. García-Andrés, S., Accotto, G. P., Navas-Castillo, J. & Moriones, E. ( 2007a; ). Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the Mediterranean basin. Virology 359, 302–312.[CrossRef]
    [Google Scholar]
  12. García-Andrés, S., Tomas, D. M., Sanchez-Campos, S., Navas-Castillo, J. & Moriones, E. ( 2007b; ). Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology 365, 210–219.[CrossRef]
    [Google Scholar]
  13. Ge, L., Zhang, J., Zhou, X. & Li, H. ( 2007; ). Genetic structure and population variability of tomato yellow leaf curl China virus. J Virol 81, 5902–5907.[CrossRef]
    [Google Scholar]
  14. Gerrish, P. J. & Lenski, R. E. ( 1998; ). The fate of competing beneficial mutations in an asexual population. Genetica 102–103, 127–144.
    [Google Scholar]
  15. Gussow, D. & Clackson, T. ( 1989; ). Direct clone characterization from plaques and colonies by the polymerase chain reaction. Nucleic Acids Res 17, 4000 [CrossRef]
    [Google Scholar]
  16. Heath, L., Martin, D. P., Warburton, L., Perrin, M., Horsfield, W., Kingsley, C., Rybicki, E. P. & Williamson, A. L. ( 2004; ). Evidence of unique genotypes of beak and feather disease virus in southern Africa. J Virol 78, 9277–9284.[CrossRef]
    [Google Scholar]
  17. Heath, L., van der Walt, E., Varsani, A. & Martin, D. P. ( 2006; ). Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80, 11827–11832.[CrossRef]
    [Google Scholar]
  18. Huertas, P. & Aguilera, A. ( 2003; ). Cotranscriptionally formed DNA : RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12, 711–721.[CrossRef]
    [Google Scholar]
  19. Inoue-Nagata, A. K., Albuquerque, L. C., Rocha, W. B. & Nagata, T. ( 2004; ). A simple method for cloning the complete begomovirus genome using the bacteriophage φ29 DNA polymerase. J Virol Methods 116, 209–211.[CrossRef]
    [Google Scholar]
  20. Isnard, M., Granier, M., Frutos, R., Reynaud, B. & Peterschmitt, M. ( 1998; ). Quasispecies nature of three maize streak virus isolates obtained through different modes of selection from a population used to assess response to infection of maize cultivars. J Gen Virol 79, 3091–3099.
    [Google Scholar]
  21. Jeske, H., Lutgemeier, M. & Preiss, W. ( 2001; ). DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. EMBO J 20, 6158–6167.[CrossRef]
    [Google Scholar]
  22. Katz, R. A. & Skalka, A. M. ( 1990; ). Generation of diversity in retroviruses. Annu Rev Genet 24, 409–445.[CrossRef]
    [Google Scholar]
  23. Keightley, P. D. & Otto, S. P. ( 2006; ). Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443, 89–92.[CrossRef]
    [Google Scholar]
  24. Lefeuvre, P., Lett, J. M., Reynaud, B. & Martin, D. P. ( 2007a; ). Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3, e181 [CrossRef]
    [Google Scholar]
  25. Lefeuvre, P., Martin, D. P., Hoareau, M., Naze, F., Delatte, H., Thierry, M., Varsani, A., Becker, N., Reynaud, B. & Lett, J. M. ( 2007b; ). Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. J Gen Virol 88, 3458–3468.[CrossRef]
    [Google Scholar]
  26. Martin, D. P. & Rybicki, E. P. ( 1998; ). Microcomputer-based quantification of maize streak virus symptoms in Zea mays. Phytopathology 88, 422–427.[CrossRef]
    [Google Scholar]
  27. Martin, D. P. & Rybicki, E. P. ( 2000; ). Improved efficiency of Zea mays agroinoculation with Maize streak virus. Plant Dis 84, 1096–1098.[CrossRef]
    [Google Scholar]
  28. Martin, D. P. & Rybicki, E. P. ( 2002; ). Investigation of Maize streak virus pathogenicity determinants using chimaeric genomes. Virology 300, 180–188.[CrossRef]
    [Google Scholar]
  29. Martin, D. P., Willment, J. A. & Rybicki, E. P. ( 1999; ). Evaluation of Maize streak virus pathogenicity in differentially resistant Zea mays genotypes. Phytopathology 89, 695–700.[CrossRef]
    [Google Scholar]
  30. Martin, D. P., Willment, J. A., Billharz, R., Velders, R., Odhiambo, B., Njuguna, J., James, D. & Rybicki, E. P. ( 2001; ). Sequence diversity and virulence in Zea mays of Maize streak virus isolates. Virology 288, 247–255.[CrossRef]
    [Google Scholar]
  31. Martin, D. P., van der Walt, E., Posada, D. & Rybicki, E. P. ( 2005a; ). The evolutionary value of recombination is constrained by genome modularity. PLoS Genet 1, e51 [CrossRef]
    [Google Scholar]
  32. Martin, D. P., Williamson, C. & Posada, D. ( 2005b; ). RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef]
    [Google Scholar]
  33. Meinschad, C. & Winnacker, E. L. ( 1980; ). Recombination in adenovirus. I. Analysis of recombinant viruses under non-selective conditions. J Gen Virol 48, 219–224.[CrossRef]
    [Google Scholar]
  34. Muller, H. J. ( 1964; ). The relation of recombination to mutational advance. Mutat Res 106, 2–9.
    [Google Scholar]
  35. Ndunguru, J., Legg, J. P., Aveling, T. A., Thompson, G. & Fauquet, C. M. ( 2005; ). Molecular biodiversity of cassava begomoviruses in Tanzania: evolution of cassava geminiviruses in Africa and evidence for East Africa being a center of diversity of cassava geminiviruses. Virol J 2, 21 [CrossRef]
    [Google Scholar]
  36. Odelberg, S. J., Weiss, R. B., Hata, A. & White, R. ( 1995; ). Template-switching during DNA synthesis by Thermus aquaticus DNA polymerase I. Nucleic Acids Res 23, 2049–2057.[CrossRef]
    [Google Scholar]
  37. Owor, B. E., Martin, D. P., Shepherd, D. N., Edema, R., Monjane, A. L., Rybicki, E. P., Thomson, J. A. & Varsani, A. ( 2007a; ). Genetic analysis of maize streak virus isolates from Uganda reveals widespread distribution of a recombinant variant. J Gen Virol 88, 3154–3165.[CrossRef]
    [Google Scholar]
  38. Owor, B. E., Shepherd, D. N., Taylor, N. J., Edema, R., Monjane, A. L., Thomson, J. A., Martin, D. P. & Varsani, A. ( 2007b; ). Successful application of FTA Classic Card technology and use of bacteriophage φ29 DNA polymerase for large-scale field sampling and cloning of complete maize streak virus genomes. J Virol Methods 140, 100–105.[CrossRef]
    [Google Scholar]
  39. Padidam, M., Sawyer, S. & Fauquet, C. M. ( 1999; ). Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218–225.[CrossRef]
    [Google Scholar]
  40. Palmer, K. E., Schnippenkoetter, W. H. & Rybicki, E. P. ( 1998; ). Geminivirus isolation and DNA extraction. Methods Mol Biol 81, 41–52.
    [Google Scholar]
  41. Posada, D. & Crandall, K. A. ( 2002; ). The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 54, 396–402.[CrossRef]
    [Google Scholar]
  42. Prasanna, H. C. & Rai, M. ( 2007; ). Detection and frequency of recombination in tomato-infecting begomoviruses of south and southeast Asia. Virol J 4, 111 [CrossRef]
    [Google Scholar]
  43. Preiss, W. & Jeske, H. ( 2003; ). Multitasking in replication is common among geminiviruses. J Virol 77, 2972–2980.[CrossRef]
    [Google Scholar]
  44. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  45. Saunders, K., Lucy, A. & Stanley, J. ( 1991; ). DNA forms of the geminivirus African cassava mosaic virus consistent with a rolling circle mechanism of replication. Nucleic Acids Res 19, 2325–2330.[CrossRef]
    [Google Scholar]
  46. Scheffler, K., Martin, D. P. & Seoighe, C. ( 2006; ). Robust inference of positive selection from recombining coding sequences. Bioinformatics 22, 2493–2499.[CrossRef]
    [Google Scholar]
  47. Schierup, M. H. & Hein, J. ( 2000; ). Recombination and the molecular clock. Mol Biol Evol 17, 1578–1579.[CrossRef]
    [Google Scholar]
  48. Schnippenkoetter, W. H., Martin, D. P., Willment, J. A. & Rybicki, E. P. ( 2001; ). Forced recombination between distinct strains of Maize streak virus. J Gen Virol 82, 3081–3090.
    [Google Scholar]
  49. Shackelton, L. A., Hoelzer, K., Parrish, C. R. & Holmes, E. C. ( 2007; ). Comparative analysis reveals frequent recombination in the parvoviruses. J Gen Virol 88, 3294–3301.[CrossRef]
    [Google Scholar]
  50. Sharp, P. M., Robertson, D. L. & Hahn, B. H. ( 1995; ). Cross-species transmission and recombination of ‘AIDS’ viruses. Philos Trans R Soc Lond B Biol Sci 349, 41–47.[CrossRef]
    [Google Scholar]
  51. Shepherd, D. N., Mangwende, T., Martin, D. P., Bezuidenhout, M., Thomson, J. A. & Rybicki, E. P. ( 2007; ). Inhibition of maize streak virus (MSV) replication by transient and transgenic expression of MSV replication-associated protein mutants. J Gen Virol 88, 325–336.[CrossRef]
    [Google Scholar]
  52. Shepherd, D. N., Varsani, A., Windram, O. P., Lefeuvre, P., Monjane, A. L., Owor, B. E. & Martin, D. P. ( 2008a; ). Novel Sugarcane streak and Sugarcane streak Réunion mastreviruses from southern Africa and La Réunion. Arch Virol 153, 605–609.[CrossRef]
    [Google Scholar]
  53. Shepherd, D. N., Martin, D. P., Lefeuvre, P., Monjane, A. L., Owor, B. E., Rybicki, E. P. & Varsani, A. ( 2008b; ). A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. J Virol Methods 149, 97–102.[CrossRef]
    [Google Scholar]
  54. Stenger, D. C., Revington, G. N., Stevenson, M. C. & Bisaro, D. M. ( 1991; ). Replicational release of geminivirus genomes from tandemly repeated copies: evidence for rolling-circle replication of a plant viral DNA. Proc Natl Acad Sci U S A 88, 8029–8033.[CrossRef]
    [Google Scholar]
  55. Suzuki, Y., Gojobori, T. & Nakagomi, O. ( 1998; ). Intragenic recombinations in rotaviruses. FEBS Lett 427, 183–187.[CrossRef]
    [Google Scholar]
  56. Takeuchi, Y., Horiuchi, T. & Kobayashi, T. ( 2003; ). Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev 17, 1497–1506.[CrossRef]
    [Google Scholar]
  57. van der Walt, E., Martin, D. P., Varsani, A., Polston, J. E. & Rybicki, E. P. ( 2008; ). Experimental observations of rapid Maize streak virus evolution reveal a strand-specific nucleotide substitution bias. Virol J 5, 104 [CrossRef]
    [Google Scholar]
  58. Varsani, A., van der Walt, E., Heath, L., Rybicki, E. P., Williamson, A. L. & Martin, D. P. ( 2006; ). Evidence of ancient papillomavirus recombination. J Gen Virol 87, 2527–2531.[CrossRef]
    [Google Scholar]
  59. Varsani, A., Oluwafemi, S., Windram, O. P., Shepherd, D. N., Monjane, A. L., Owor, B. E., Rybicki, E. P., Lefeuvre, P. & Martin, D. P. ( 2008a; ). Panicum streak virus diversity is similar to that observed for maize streak virus. Arch Virol 153, 601–604.[CrossRef]
    [Google Scholar]
  60. Varsani, A., Shepherd, D. N., Monjane, A. L., Owor, B. E., Erdmann, J. B., Rybicki, E. P., Peterschmitt, M., Briddon, R. W., Markham, P. G. & other authors ( 2008b; ). Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen. J Gen Virol 89, 2063–2074.[CrossRef]
    [Google Scholar]
  61. Willment, J. A., Martin, D. P. & Rybicki, E. P. ( 2001; ). Analysis of the diversity of African streak mastreviruses using PCR-generated RFLPs and partial sequence data. J Virol Methods 93, 75–87.[CrossRef]
    [Google Scholar]
  62. Willment, J. A., Martin, D. P., van der Walt, E. & Rybicki, E. P. ( 2002; ). Biological and genomic sequence characterization of Maize streak virus isolates from wheat. Phytopathology 92, 81–86.[CrossRef]
    [Google Scholar]
  63. Willment, J. A., Martin, D. P., Palmer, K. E., Schnippenkoetter, W. H., Shepherd, D. N. & Rybicki, E. P. ( 2007; ). Identification of long intergenic region sequences involved in maize streak virus replication. J Gen Virol 88, 1831–1841.[CrossRef]
    [Google Scholar]
  64. Worobey, M. ( 2000; ). Extensive homologous recombination among widely divergent TT viruses. J Virol 74, 7666–7670.[CrossRef]
    [Google Scholar]
  65. Zhou, X., Liu, Y., Robinson, D. J. & Harrison, B. D. ( 1998; ). Four DNA-A variants among Pakistani isolates of cotton leaf curl virus and their affinities to DNA-A of geminivirus isolates from okra. J Gen Virol 79, 915–923.
    [Google Scholar]
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