1887

Abstract

Potyviruses have variable single-stranded RNA genomes and many show clear evidence of recombination. This report studied the distribution of recombination sites in the genomes of 92 isolates of the potyvirus (TuMV); 42 came from the international gene sequence databases and an additional 50 complete genomic sequences were generated from field samples collected in Europe and Asia. The sequences were examined for evidence of recombination using seven different sequence comparison methods and the exact position of each site was confirmed by sequence composition analysis. Recombination sites were found throughout the genomes, except in the small 6K1 protein gene, and only 24 of the genomes (26 %) showed no evidence of recombination. Statistically significant clusters of recombination sites were found in the P1 gene and in the CI/6K2/VPg gene region. Most recombination sites were bordered by an upstream (5′) region of GC-rich and downstream (3′) region of AU-rich sequence of a similar length. Correlations between the presence and type of recombination site and provenance, host type and phylogenetic relationships are discussed, as is the role of recombination in TuMV evolution.

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2007-01-01
2024-04-19
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References

  1. Bateson M. F., Lines R. E., Revill P., Chaleeprom W., Ha C. V., Gibbs A. J., Dale J. L. 2002; On the evolution and molecular epidemiology of the potyvirus Papaya ringspot virus . J Gen Virol 83:2575–2585
    [Google Scholar]
  2. Bousalem M., Douzery E. J. P., Fargette D. 2000; High genetic diversity, distant phylogenetic relationships and intraspecies recombination events among natural populations of Yam mosaic virus : a contribution to understanding potyvirus evolution. J Gen Virol 81:243–255
    [Google Scholar]
  3. Chare E. R., Holmes E. C. 2006; A phylogenetic survey of recombination frequency on plant RNA viruses. Arch Virol 151:933–946 [CrossRef]
    [Google Scholar]
  4. Chen Y.-K., Goldbach R., Prins M. 2002a; Inter- and intramolecular recombinations in the Cucumber mosaic virus genome related to adaptation in alstroemeria. J Virol 76:4119–4124 [CrossRef]
    [Google Scholar]
  5. Chen J., Zheng H. Y., Chen J. P., Adams M. J. 2002b; Characterisation of a potyvirus, and a potexvirus from Chinese scallion. Arch Virol 147:683–693 [CrossRef]
    [Google Scholar]
  6. Chen J., Chen J. P., Langeveld S. A., Derks A. F. L. M., Adams M. J. 2003a; Molecular characterization of carla- and potyviruses from Narcissus in China. J Phytopathol 151:26–29 [CrossRef]
    [Google Scholar]
  7. Chen C. C., Chao C. H., Chen C. C., Yeh S. D., Tsai H. T., Chang C. A. 2003b; Identification of Turnip mosaic virus isolates causing yellow stripe and spot on calla lily. Plant Dis 87:901–905 [CrossRef]
    [Google Scholar]
  8. Choi J. K., Maeda T., Wakimoto S. 1977; An improved method for purification of turnip mosaic virus. Ann Phytopathol Soc Jpn 43:440–448 [CrossRef]
    [Google Scholar]
  9. Conover W. J. 1999; Statistics of the Kolmogorov–Smirnov type. In Practical Nonparametric Statistics , 3rd edn. pp  428–473 New York: John Wiley & Sons;
    [Google Scholar]
  10. Dayhoff M. O., Barker W. C., Hunt L. T. 1983; Establishing homologies in protein sequences. Methods Enzymol 91:524–545
    [Google Scholar]
  11. 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]
  12. Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. (editors) 2005; Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses San Diego: Elsevier Academic Press;
    [Google Scholar]
  13. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [CrossRef]
    [Google Scholar]
  14. Felsenstein J. 1993; phylip (phylogeny interference package), version 3.5. Department of Genetics, University of Washington; Seattle, USA:
  15. Fuji S., Nakamae H. 1999; Complete nucleotide sequence of the genomic RNA of a Japanese yam mosaic virus, a new potyvirus in Japan. Arch Virol 144:231–240 [CrossRef]
    [Google Scholar]
  16. Fuji S., Nakamae H. 2000; Complete nucleotide sequence of the genomic RNA of a mild strain of Japanese yam mosaic potyvirus in Japan. Arch Virol 145:635–640 [CrossRef]
    [Google Scholar]
  17. García-Arenal F., McDonald B. A. 2003; An analysis of the durability of the resistance to plant viruses. Phytopathology 93:941–952 [CrossRef]
    [Google Scholar]
  18. García-Arenal F., Fraile A., Malpica J. M. 2001; Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 39:157–186 [CrossRef]
    [Google Scholar]
  19. 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 available at http://www.anu.edu.au/BoZo/software/ [CrossRef]
    [Google Scholar]
  20. Glasa M., Palkovics L., Komínek P., Labonne G., Pittnerová S., Kúdela O., Candresse T., Šubr Z. 2004; Geographically and temporally distant natural recombinant isolates of Plum pox virus (PPV) are genetically very similar and form a unique PPV subgroup. J Gen Virol 85:2671–2681 [CrossRef]
    [Google Scholar]
  21. Green S. K., Deng T. C. 1985; Turnip mosaic virus strains in cruciferous hosts in Taiwan. Plant Dis 69:28–31 [CrossRef]
    [Google Scholar]
  22. Hall T. A. 1999; BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
    [Google Scholar]
  23. Hamlyn B. M. G. 1953; Quantitative studies on the transmission of cabbage black ringspot virus by Myzus persicae (Sulz.). Ann Appl Biol 40:393–402 [CrossRef]
    [Google Scholar]
  24. Hasegawa M., Kishino H., Yano T. 1985; Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174 [CrossRef]
    [Google Scholar]
  25. Hughes S. L., Hunter P. J., Sharpe A. G., Kearsey M. J., Lydiate D. J., Walsh J. A. 2003; Genetic mapping of the novel Turnip mosaic virus resistance gene TuRB03 in Brassica napus . Theor Appl Genet 107:1169–1173 [CrossRef]
    [Google Scholar]
  26. Jeanmougin F., Thompson J. D., Gouy M., Higgins D. G., Gibson T. J. 1998; Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405 [CrossRef]
    [Google Scholar]
  27. Jenner C. E., Walsh J. A. 1996; Pathotypic variation in turnip mosaic virus with special reference to European isolates. Plant Pathol 45:848–856 [CrossRef]
    [Google Scholar]
  28. Jenner C. E., Tomimura K., Ohshima K., Hughes S. L., Walsh J. A. 2002; Mutations in Turnip mosaic virus P3 and cylindrical inclusion protein are required to overcome two Brassica napus resistance genes. Virology 300:50–59 [CrossRef]
    [Google Scholar]
  29. Jenner C. E., Wang X., Tomimura K., Ohshima K., Ponz F., Walsh J. A. 2003; The dual role of the potyvirus P3 protein on Turnip mosaic virus as a symptom and avirulence determinant in brassicas. Mol Plant Microbe Interact 16:777–784 [CrossRef]
    [Google Scholar]
  30. Kimura M. 1980; A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequence. J Mol Evol 16:111–120 [CrossRef]
    [Google Scholar]
  31. Liu X.-P., Lu W.-C., Liu Y.-K., Li J.-L. 1990; A study on TuMV strain differentiation of cruciferous vegetables from ten provinces in China. Chin Sci Bull 35:1734–1739
    [Google Scholar]
  32. Martin D., Rybicki E. 2000; rdp: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563 [CrossRef]
    [Google Scholar]
  33. Martin D. P., Williamson C., Posada D. 2005; rdp2: recombination detection and analysis from sequence alignment. Bioinformatics 21:260–262 [CrossRef]
    [Google Scholar]
  34. Maynard Smith J. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129
    [Google Scholar]
  35. Monci F., Sánchez-Campos S., Navas-Castillo J., Moriones E. 2002; A natural recombinant between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303:317–326 [CrossRef]
    [Google Scholar]
  36. Moreno I. M., Malpica J. M., Díaz-Pendón 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]
  37. Moury B., Morel C., Johansen E., Jacquemond M. 2002; Evidence for diversifying selection in Potato virus Y and in the coat protein of other potyviruses. J Gen Virol 83:2563–2573
    [Google Scholar]
  38. Nagy P. D., Burjarski 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
    [Google Scholar]
  39. Nagy P. D., Burjarski J. J. 1996; Homologous RNA recombination in brome mosaic virus: AU-rich sequences decrease the accuracy of crossovers. J Virol 70:415–426
    [Google Scholar]
  40. Nagy P. D., Burjarski J. J. 1997; Engineering of homologous recombination hotspots with AU-rich sequences in brome mosaic virus. J Virol 71:3799–3810
    [Google Scholar]
  41. Nagy P. D., Ogiela C., Burjarski J. J. 1999a; Mapping sequences active on homologous RNA recombination in brome mosaic virus: prediction of recombination hot spots. Virology 254:92–104 [CrossRef]
    [Google Scholar]
  42. Nagy P. D., Zhang C., Simon A. E. 1999b; Dissecting RNA recombination in vitro : role of RNA sequences and the viral replicase. EMBO J 17:2392–2403
    [Google Scholar]
  43. Nicolas O., Laliberté J.-F. 1992; The complete nucleotide sequence of turnip mosaic potyvirus RNA. J Gen Virol 73:2785–2793 [CrossRef]
    [Google Scholar]
  44. Ohshima K., Tanaka M., Sako N. 1996; The complete nucleotide sequence of turnip mosaic virus RNA Japanese strain. Arch ViroI 141:1991–1997 [CrossRef]
    [Google Scholar]
  45. Ohshima K., Yamaguchi Y., Hirota R., Hamamoto T., Tomimura K., Tan Z., Sano T., Azuhata F., Walsh J. A. other authors 2002; Molecular evolution of Turnip mosaic virus : evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol 83:1511–1521
    [Google Scholar]
  46. Page R. D. 1996; TreeView: an application to display phylogenetic trees on personal computer. CABIOS 12:357–358
    [Google Scholar]
  47. Posada D. 2002; Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19:708–717 [CrossRef]
    [Google Scholar]
  48. Posada D., Crandall K. A. 2001; Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762 [CrossRef]
    [Google Scholar]
  49. Provvidenti R. 1980; Evaluation of chinese cabbage cultivars from Japan and the People's Republic of China for resistance to turnip mosaic virus and cauliflower mosaic virus. J Am Soc Hortic Sci 105:571–573
    [Google Scholar]
  50. Provvidenti R. 1996 Turnip mosaic potyvirus . In Viruses of Plants , pp. 1340–1343 Edited by Brunt A. A., Crabtree K., Dallwitz M. J., Gibbs A. J., Watson L. Wallingford, UK: CAB International;
    [Google Scholar]
  51. Riechmann J. L., Laín S., García J. A. 1992; Highlights and prospects of potyvirus molecular biology. J Gen Virol 73:1–16 [CrossRef]
    [Google Scholar]
  52. Roossinck M. J. 1997; Mechanisms of plant virus evolution. Annu Rev Phytopathol 35:191–209 [CrossRef]
    [Google Scholar]
  53. Roth B. M., Pruss G. J., Vance V. B. 2004; Plant viral suppressors of RNA silencing. Virus Res 102:97–108 [CrossRef]
    [Google Scholar]
  54. Rubio L., Ayllón M. A., Kong P., Fernández A., Polek M., Guerri J., Moreno P., Falk B. W. 2001; Genetic variation of Citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombination. J Virol 75:8054–8062 [CrossRef]
    [Google Scholar]
  55. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
    [Google Scholar]
  56. Salminen M. O., Carr J. K., Burke D. S., McCutchan F. E. 1995; Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 11:1423–1425 [CrossRef]
    [Google Scholar]
  57. Sawyer S. A. 1999; geneconv: a computer package for the statistical detection of gene conversion. Distributed by the author. Department of Mathematics, Washington University in St Louis, USA. Available at http://www.math.wustl.edu/∼sawyer
  58. Shukla D. D., Ward C. W., Brunt A. A. 1994; Introduction. In The Potyviridae pp  1–26 Edited by Shukla D. D., Ward C. W., Brunt A. A. Wallingford, UK: CAB International;
    [Google Scholar]
  59. Simon A. E., Bujarski J. J. 1994; RNA–RNA recombination and evolution in virus-infected plants. Annu Rev Phytopathol 32:337–362 [CrossRef]
    [Google Scholar]
  60. Stenger D. C., Seifers D. L., French R. 2002; Patterns of polymorphism in Wheat streak mosaic virus : sequence space explored by a clade of closely related viral genotypes rivals that between the most divergent strains. Virology 302:58–70 [CrossRef]
    [Google Scholar]
  61. Strimmer K., von Haeseler A. 1996; Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969 [CrossRef]
    [Google Scholar]
  62. Strimmer K., Goldman N., von Haeseler A. 1997; Bayesian probabilities and quartet puzzling. Mol Biol Evol 14:210–211 [CrossRef]
    [Google Scholar]
  63. Suehiro N., Natsuaki T., Watanabe T., Okuda S. 2004; An important determinant of the ability of Turnip mosaic virus to infect Brassica spp. and/or Raphanus sativus is in its P3 protein. J Gen Virol 85:2087–2098 [CrossRef]
    [Google Scholar]
  64. 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]
  65. Tan Z., Gibbs A. J., Tomitaka Y., Sánchez F., Ponz F., Ohshima K. 2005; Mutations in Turnip mosaic virus genomes that have adapted to Raphanus sativus . J Gen Virol 86:501–510 [CrossRef]
    [Google Scholar]
  66. Tomimura K., Gibbs A. J., Jenner C. E., Walsh J. A., Ohshima K. 2003; The phylogeny of Turnip mosaic virus ; comparisons of 38 genomic sequences reveal a Eurasian origin and a recent ‘emergence’ in east Asia. Mol Ecol 12:2099–2111 [CrossRef]
    [Google Scholar]
  67. Tomimura K., Špak J., Katis N., Jenner C. E., Walsh J. A., Gibbs A. J., Ohshima K. 2004; Comparison of the genetic structure of populations of Turnip mosaic virus in West and East Eurasia. Virology 330:408–423 [CrossRef]
    [Google Scholar]
  68. Tomitaka Y., Ohshima K. 2006; A phylogeographical study of the Turnip mosaic virus population in East Asia reveals an ‘emergent’ lineage in Japan. Mol Ecol 15:4437–4457 [CrossRef]
    [Google Scholar]
  69. Tomlinson J. A. 1987; Epidemiology and control of virus diseases of vegetables. Ann Appl Biol 110:661–681 [CrossRef]
    [Google Scholar]
  70. Tomlinson J. A., Ward C. M. 1978; The reactions of swede ( Brassica napus ) to infection by turnip mosaic virus. Ann Appl Biol 89:61–69 [CrossRef]
    [Google Scholar]
  71. Urcuqui-Inchima S., Haenni A.-L., Bernardi F. 2001; Potyvirus proteins: a wealth of functions. Virus Res 74:157–175 [CrossRef]
    [Google Scholar]
  72. Vives M. C., Rubio L., Sambade A., Mirkov T. E., Moreno P., Guerri J. 2005; Evidence of multiple recombination events between two RNA sequence variants within a Citrus tristeza virus isolate. Virology 331:232–237 [CrossRef]
    [Google Scholar]
  73. Walsh J. A. 1989; Genetic control of immunity to turnip mosaic virus in winter oilseed rape ( Brassica napus ssp. oleifera ) and the effect of foreign isolates of the virus. Ann Appl Biol 115:89–99 [CrossRef]
    [Google Scholar]
  74. Walsh J. A., Jenner C. E. 2002; Turnip mosaic virus and the quest for durable resistance. Mol Plant Pathol 3:289–300 [CrossRef]
    [Google Scholar]
  75. Weiller G. F. 1998; Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Mol Biol Evol 15:326–335 [CrossRef]
    [Google Scholar]
  76. White K. A., Morris T. J. 1994; Recombination between defective tombusvirus RNAs generates functional hybrid genomes. Proc Natl Acad Sci U S A 91:3642–3646 [CrossRef]
    [Google Scholar]
  77. Worobey M., Holmes E. C. 1999; Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80:2535–2543
    [Google Scholar]
  78. Worobey M., Holmes E. C. 2001; Homologous recombination in GB virus C/hepatitis G virus. Mol Biol Evol 18:254–261 [CrossRef]
    [Google Scholar]
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