1887

Abstract

Recombination and segment reassortment are important contributors to the standing genetic variation of RNA viruses and are often involved in the genesis of new, emerging viruses. This study explored the role played by these two processes in the evolutionary radiation of the plant virus family . The evolutionary history of this family has been explored previously using standard molecular phylogenetic methods, but incongruences have been found among the trees inferred from different gene sequences. This would not be surprising if RNA exchange was a common event, as it is well known that recombination and reassortment of genomes are poorly described by standard phylogenetic methods. In an attempt to reconcile these discrepancies, this study first explored the extent of segment reassortment and found that it was common at the origin of the bromoviruses and cucumoviruses and at least at the origin of alfalfa mosaic virus, American plum line pattern virus and citrus leaf rugose virus. Secondly, recombination analyses were performed on each of the three genomic RNAs and it was found that recombination was very common in members of the genera , and . Several cases of recombination involving species from different genera were also identified. Finally, a phylogenetic network was constructed reflecting these genetic exchanges. The network confirmed the taxonomic status of the different genera within the family, despite the phylogenetic noise introduced by genetic exchange.

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2008-07-01
2019-11-21
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References

  1. Abascal, F., Zardoya, R. & Posada, D. ( 2005; ). prottest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.[CrossRef]
    [Google Scholar]
  2. Allison, R., Thompson, C. & Ahlquist, P. ( 1990; ). Regeneration of a functional RNA virus genome by recombination between deletion mutants and requirement for cowpea chlorotic mottle virus 3a and coat protein genes for systemic infection. Proc Natl Acad Sci U S A 87, 1820–1824.[CrossRef]
    [Google Scholar]
  3. Althaus, C. L. & Bonhoeffer, S. ( 2005; ). Stochastic interplay between mutation and recombination during the acquisition of drug resistance mutations in human immunodeficiency virus type 1. J Virol 79, 13572–13578.[CrossRef]
    [Google Scholar]
  4. Aranda, M. A., Fraile, A., Dopazo, J., Malpica, J. M. & García-Arenal, F. ( 1997; ). Contribution of mutation and RNA recombination to the evolution of plant pathogenic RNA. J Mol Evol 44, 81–88.[CrossRef]
    [Google Scholar]
  5. Boni, M. F., Posada, D. & Feldman, M. W. ( 2007; ). An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176, 1035–1047.
    [Google Scholar]
  6. Bonnet, J., Fraile, A., Sacristán, S., Malpica, J. M. & García-Arenal, F. ( 2005; ). Role of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virus. Virology 332, 359–368.[CrossRef]
    [Google Scholar]
  7. Bousalem, M., Dallot, S., Fuji, S. & Natsuaki, K. T. ( 2003; ). Origin, world-wide dispersion, biogeographical diversification, radiation and recombination: an evolutionary history of the Yam mild mosaic virus (YMMV). Infect Genet Evol 3, 189–206.[CrossRef]
    [Google Scholar]
  8. Bujarski, J. J. & Kaesberg, P. ( 1986; ). Genetic recombination between RNA components of a multipartite plant virus. Nature 321, 528–531.[CrossRef]
    [Google Scholar]
  9. Chare, E. R. & Holmes, E. C. ( 2006; ). A phylogenetic survey of recombination in plant viruses. Arch Virol 151, 933–946.[CrossRef]
    [Google Scholar]
  10. Chare, E. R., Gould, E. A. & Holmes, E. C. ( 2003; ). Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J Gen Virol 84, 2691–2703.[CrossRef]
    [Google Scholar]
  11. Chen, Y. K., Goldbach, R. & Prins, M. ( 2002; ). Inter- and intramolecular recombinations in Cucumber mosaic virus genome related to adaptation to alstroemeria. J Virol 76, 4119–4124.[CrossRef]
    [Google Scholar]
  12. Cheng, C. P. & Nagy, P. D. ( 2003; ). Mechanism of RNA recombination in carmo- and tombusviruses: evidence for template switching by the RNA-dependent RNA polymerase in vitro. J Virol 77, 12033–12047.[CrossRef]
    [Google Scholar]
  13. Codoñer, F. M. & Elena, S. F. ( 2006; ). Evolutionary relationships among members of the Bromoviridae deduced from whole proteome analysis. Arch Virol 151, 299–307.[CrossRef]
    [Google Scholar]
  14. Codoñer, F. M., Cuevas, J. M., Sánchez-Navarro, J. A., Pallás, V. & Elena, S. F. ( 2005; ). Molecular evolution of the plant virus family Bromoviridae based on RNA 3-encoded proteins. J Mol Evol 61, 697–705.[CrossRef]
    [Google Scholar]
  15. Codoñer, F. M., Fares, M. A. & Elena, S. F. ( 2006; ). Adaptive covariation between the coat and movement proteins of prunus necrotic ringspot virus. J Virol 80, 5833–5840.[CrossRef]
    [Google Scholar]
  16. de Wispelaere, M., Gaubert, S., Troilloud, S., Belin, C. & Tepfer, M. ( 2005; ). A map of the diversity of RNA3 recombinants appearing in plants infected with Cucumber mosaic virus and Tomato aspermy virus. Virology 331, 117–127.[CrossRef]
    [Google Scholar]
  17. Fernández-Cuartero, B., Burgyan, J., Aranda, M. A., Salanki, K., Moriones, E. & García-Arenal, F. ( 1994; ). Increase in the relative fitness of a plant virus RNA associated with its recombinant nature. Virology 203, 373–377.[CrossRef]
    [Google Scholar]
  18. Fraile, A., Alonso-Prados, J. L., Aranda, M. A., Bernal, J. J., Malpica, J. M. & García-Arenal, F. ( 1997; ). Genetic exchange by recombination or reassortment is infrequent in natural populations of a tripartite RNA plant virus. J Virol 71, 934–940.
    [Google Scholar]
  19. Galetto, R. & Negroni, M. ( 2005; ). Mechanistic features of recombination in HIV. AIDS Rev 7, 92–102.
    [Google Scholar]
  20. Gallitelli, D., Finetti-Sialer, M. & Matelli, G. P. ( 2005; ). Anulavirus, a proposed new genus of plant viruses in the family Bromoviridae. Arch Virol 150, 407–411.[CrossRef]
    [Google Scholar]
  21. Gibbs, M. J., Armstrong, J. S. & Gibbs, A. J. ( 2000; ). Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16, 573–582.[CrossRef]
    [Google Scholar]
  22. Grassly, N. C. & Holmes, E. C. ( 1997; ). A likelihood method for the detection of selection and recombination using nucleotide sequences. Mol Biol Evol 14, 239–247.[CrossRef]
    [Google Scholar]
  23. Holmes, E. C., Worobey, M. & Rambaut, A. ( 1999; ). Phylogenetic evidence for recombination in Dengue virus. Mol Biol Evol 16, 405–409.[CrossRef]
    [Google Scholar]
  24. Huson, D. H. & Bryant, D. ( 2006; ). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23, 254–267.
    [Google Scholar]
  25. Huson, D. H. & Kloepper, T. H. ( 2005; ). Computing recombination networks from binary sequences. Bioinformatics 21 (Suppl. 2), ii159–ii165.[CrossRef]
    [Google Scholar]
  26. Ji, L. H. & Ding, S. W. ( 2001; ). The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant Microbe Interact 14, 715–724.[CrossRef]
    [Google Scholar]
  27. Lai, M. M. ( 1992; ). RNA recombination in animal and plant viruses. Microbiol Rev 56, 61–79.
    [Google Scholar]
  28. Lefeuvre, P., Martin, D. P., Hoareau, M., Naze, F., Delatte, H., Thierry, M., Varsani, A., Becker, N., Reynaud, B. & Lett, J. M. ( 2007; ). 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]
  29. Macken, C. A., Webby, R. J. & Bruno, W. J. ( 2006; ). Genotype turnover by reassortment of replication complex genes from avian Influenza A virus. J Gen Virol 87, 2803–2815.[CrossRef]
    [Google Scholar]
  30. Martin, D. & Rybicki, E. ( 2000; ). rdp: detection of recombination amongst aligned sequences. Bioinformatics 16, 562–563.[CrossRef]
    [Google Scholar]
  31. Martin, D. P., Posada, D., Crandall, K. A. & Williamson, C. ( 2005a; ). A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21, 98–102.[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. Melcher, U. ( 2000; ). The ‘30K’ superfamily of viral movement proteins. J Gen Virol 81, 257–266.
    [Google Scholar]
  34. Moreno, I. M., Malpica, J. M., Diaz-Pendon, J. A., Moriones, E., Fraile, A. & García-Arenal, F. ( 2004; ). Variability and genetic structure of the population of watermelon mosaic virus infecting melon in Spain. Virology 318, 451–460.[CrossRef]
    [Google Scholar]
  35. 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.[CrossRef]
    [Google Scholar]
  36. Olsthoorn, R. C., Bruyere, A., Dzianott, A. & Bujarski, J. J. ( 2002; ). RNA recombination in brome mosaic virus: effects of strand-specific stem-loop insert. J Virol 76, 12654–12662.[CrossRef]
    [Google Scholar]
  37. Padidam, M., Sawyer, S. & Fauquet, C. M. ( 1999; ). Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218–225.[CrossRef]
    [Google Scholar]
  38. Page, R. D. M. ( 1994; ). Maps between trees and cladistic analysis of historical associations among genes, organisms and areas. Syst Biol 43, 58–77.
    [Google Scholar]
  39. Posada, D. & Crandall, K. A. ( 1998; ). modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef]
    [Google Scholar]
  40. Posada, D. & Crandall, K. A. ( 2001; ). Evaluation of methods for detection recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98, 13757–13762.[CrossRef]
    [Google Scholar]
  41. Posada, D. & Crandall, K. A. ( 2002; ). The effect of recombination on the accuracy of phylogenetic estimation. J Mol Evol 54, 396–402.[CrossRef]
    [Google Scholar]
  42. Prljic, J., Veljkovic, N. & Veljkovic, V. ( 2004; ). Recombination property of the HIV-1 gp120 gene. Int Rev Immunol 23, 447–454.[CrossRef]
    [Google Scholar]
  43. Rampitsch, C. & Eastwell, K. C. ( 1997; ). The complete sequence of prune dwarf ilarvirus RNA 1. Arch Virol 142, 1911–1918.[CrossRef]
    [Google Scholar]
  44. Revers, F., Le Gall, O., Candresse, T., Le Romancer, M. & Dunez, J. ( 1996; ). Frequent occurrence of recombinant potyvirus isolates. J Gen Virol 77, 1953–1965.[CrossRef]
    [Google Scholar]
  45. Roossinck, M. J., Zhang, L. & Hellwald, K. H. ( 1999; ). Rearrangements in the 5′ nontranslated region and phylogenetic analysis of cucumber mosaic virus RNA 3 indicate radial evolution of three subgroups. J Virol 73, 6752–6758.
    [Google Scholar]
  46. Sánchez-Navarro, J. A. & Pallás, V. ( 1997; ). Evolutionary relationships in the ilarviruses: nucleotide sequence of prunus necrotic ringspot virus RNA 3. Arch Virol 142, 749–763.[CrossRef]
    [Google Scholar]
  47. Scott, S. W., Zimmerman, M. T. & Ge, X. ( 1998; ). The sequence of RNA 1 and RNA 2 of tobacco streak virus: additional evidence for the inclusion of alfalfa mosaic virus in the genus Ilarvirus. Arch Virol 143, 1187–1198.[CrossRef]
    [Google Scholar]
  48. Shi, B. J., Palukaitis, P. & Symons, R. H. ( 2002; ). Differential virulence by strains of Cucumber mosaic virus is mediated by the 2b gene. Mol Plant Microbe Interact 15, 947–955.[CrossRef]
    [Google Scholar]
  49. Shiel, P. J. & Berger, P. H. ( 2000; ). The complete nucleotide sequence of apple mosaic virus (ApMV) RNA 1 and RNA 2: ApMV is more closely related to alfalfa mosaic virus than to other ilarviruses. J Gen Virol 81, 273–278.
    [Google Scholar]
  50. Smith, J. M. ( 1992; ). Analyzing the mosaic structure of genes. J Mol Evol 34, 126–129.
    [Google Scholar]
  51. Swofford, D. L. ( 1998; ). paup*: phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA: Sinauer Associates.
  52. Tan, Z., Wada, Y., Chen, J. & Ohshima, K. ( 2004; ). Inter- and intralineage recombinants are common in natural populations of Turnip mosaic virus. J Gen Virol 85, 2683–2696.[CrossRef]
    [Google Scholar]
  53. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  54. Urbanowicz, A., Alejska, M., Formanowicz, P., Blazewicz, J., Figlorowicz, M. & Bujarski, J. J. ( 2005; ). Homologous crossovers among molecules of brome mosaic virus RNA 1 or RNA 2 segments in vivo. J Virol 79, 5732–5742.[CrossRef]
    [Google Scholar]
  55. Weng, Z., Barthelson, R., Gowda, S., Hilf, M. E., Dawson, W. O., Galbraith, D. W. & Xiong, Z. ( 2007; ). Persistent infection and promiscuous recombination of multiple genotypes of an RNA virus within a single host generate extensive diversity. PLoS ONE 2, e917 [CrossRef]
    [Google Scholar]
  56. White, P. S., Morales, F. J. & Roosinck, M. J. ( 1995; ). Interspecific reassortment in the evolution of cucumoviruses. Virology 207, 334–337.[CrossRef]
    [Google Scholar]
  57. Wilson, V., Taylor, P. & Desselberger, U. ( 1988; ). Crossover regions in foot-and-mouth disease virus (FMDV) recombinants correspond to regions of high local secondary structure. Arch Virol 102, 131–139.[CrossRef]
    [Google Scholar]
  58. Worobey, M. & Holmes, E. C. ( 1999; ). Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80, 2535–2543.
    [Google Scholar]
  59. Xia, X. & Xie, Z. ( 2001; ). dambe: data analysis in molecular biology and evolution. J Hered 92, 371–373.[CrossRef]
    [Google Scholar]
  60. Yang, Z. ( 2007; ). paml 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24, 1586–1591.[CrossRef]
    [Google Scholar]
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