1887

Journal of General Virology header logo

Volume 92, Issue 4

Evolution and structure of populations: evidence of extensive reassortment and insights into emergence processes Free

Abstract

Tomato spotted wilt virus (TSWV; genus , family ) genetic diversity was evaluated by sequencing parts of the three RNA genome segments of 224 isolates, mostly from pepper and tomato crops in southern Europe. Eighty-three per cent of the isolates showed consistent clustering into three clades, corresponding to their geographical origin, Spain, France or the USA, for the three RNA segments. In contrast, the remaining 17 % of isolates did not belong to the same clade for the three RNA segments and were shown to be reassortants. Among them, eight different reassortment patterns were observed. Further phylogenetic analyses provided insights into the dynamic processes of the worldwide resurgence of TSWV that, since the 1980s, has followed the worldwide dispersal of the western flower thrips () tospovirus vector. For two clades composed essentially of Old World (OW) isolates, tree topology suggested a local re-emergence of indigenous TSWV populations following introductions, while it could not be excluded that the ancestors of two other OW clades were introduced from North America contemporarily with . Finally, estimation of the selection intensity that has affected the evolution of the NSs and nucleocapsid proteins encoded by RNA S of TSWV suggests that the former could be involved in the breakdown of resistance conferred by the gene in pepper.

  • Received:
  • Accepted:
  • Published Online:
© SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.029082-0
2011-04-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/4/961.html?itemId=/content/journal/jgv/10.1099/vir.0.029082-0&mimeType=html&fmt=ahah

References

  1. Akaike, H.(1974). The new look at the statistical model identification. IEEE Trans Automat Contr 19, 716–723.[CrossRef] [Google Scholar]
  2. Allen, W. R. & Broadbent, A. B.(1986). Transmission of tomato spotted wilt virus in Ontario greenhouses by Frankliniella occidentalis. Can J Plant Pathol 8, 33–38.[CrossRef] [Google Scholar]
  3. Ayme, V., Souche, S., Caranta, C., Jacquemond, M., Chadoeuf, J., Palloix, A. & Moury, B.(2006). Different mutations in the genome-linked protein VPg of potato virus Y confer virulence on the pvr2(3) resistance in pepper. Mol Plant Microbe Interact 19, 557–563.[CrossRef] [Google Scholar]
  4. Ayme, V., Petit-Pierre, J., Souche, S., Palloix, A. & Moury, B.(2007). Molecular dissection of the potato virus Y VPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. J Gen Virol 88, 1594–1601.[CrossRef] [Google Scholar]
  5. 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]
  6. Brittlebank, C. C.(1919). Tomato diseases. J Agric 17, 231–235. [Google Scholar]
  7. Brown, J. K., Idris, A. M., Alteri, C. & Stenger, D. C.(2002). Emergence of a new Cucurbit-infecting begomovirus species capable of forming viable reassortants with related viruses in the Squash leaf curl virus cluster. Phytopathology 92, 734–742.[CrossRef] [Google Scholar]
  8. Desbiez, C., Gal-On, A., Girard, M., Wipf-Scheibel, C. & Lecoq, H.(2003). Increase in Zucchini yellow mosaic virus symptom severity in tolerant zucchini cultivars is related to a point mutation in P3 protein and is associated with a loss of relative fitness on susceptible plants. Phytopathology 93, 1478–1484.[CrossRef] [Google Scholar]
  9. Dietzgen, R. G., Twin, J., Talty, J., Selladurai, S., Carroll, M. L., Coutts, B. A., Berryman, D. I. & Jones, R. A. C.(2005). Genetic variability of Tomato spotted wilt virus in Australia and validation of real time RT-PCR for its detection in single and bulked leaf samples. Ann Appl Biol 146, 517–530.[CrossRef] [Google Scholar]
  10. Escriu, F., Fraile, A. & García-Arenal, F.(2007). Constraints to genetic exchange support gene coadaptation in a tripartite RNA virus. PLoS Pathog 3, e8,[CrossRef] [Google Scholar]
  11. Excoffier, L., Smouse, P. E. & Quattro, J. M.(1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491. [Google Scholar]
  12. Excoffier, L., Laval, G. & Schneider, S.(2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1, 47–50. [Google Scholar]
  13. Fabre, F., Bruchou, C., Palloix, A. & Moury, B.(2009). Key determinants of resistance durability to plant viruses: insights from a model linking within- and between-host dynamics. Virus Res 141, 140–149.[CrossRef] [Google Scholar]
  14. 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]
  15. García-Arenal, F. & McDonald, B. A.(2003). An analysis of the durability of resistance to plant viruses. Phytopathology 93, 941–952.[CrossRef] [Google Scholar]
  16. Greenough, D. R., Black, L. L., Story, R. N., Newsom, L. D. & Bond, W. P.(1985). Occurrence of Frankliniella occidentalis in Louisiana, a possible cause for the increased incidence of tomato spotted wilt virus. Phytopathology 75, 1362. [Google Scholar]
  17. Guindon, S. & Gascuel, O.(2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.[CrossRef] [Google Scholar]
  18. Harrison, B. D.(2002). Virus variation in relation to resistance breaking in plants. Euphytica 124, 181–192.[CrossRef] [Google Scholar]
  19. Henderson, W. W., Monroe, M. C., St Jeor, S. C., Thayer, W. P., Rowe, J. E., Peters, C. J. & Nichol, S. T.(1995). Naturally occurring Sin Nombre virus genetic reassortants. Virology 214, 602–610.[CrossRef] [Google Scholar]
  20. Hoffmann, K., Qiu, W. P. & Moyer, J. W.(2001). Overcoming host- and pathogen-mediated resistance in tomato and tobacco maps to the M RNA of Tomato spotted wilt virus. Mol Plant Microbe Interact 14, 242–249.[CrossRef] [Google Scholar]
  21. Ihaka, R. & Gentleman, R.(1996). R, a language for data analysis and graphics. J Comput Graph Statist 5, 299–314. [Google Scholar]
  22. Iturriza-Gómara, M., Isherwood, B., Desselberger, U. & Gray, J.(2001). Reassortment in vivo: driving force for diversity of human rotavirus strains isolated in the United Kingdom between 1995 and 1999. J Virol 75, 3696–3705.[CrossRef] [Google Scholar]
  23. Jahn, M., Paran, I., Hoffmann, K., Radwanski, E. R., Livingstone, K. D., Grube, R. C., Aftergoot, E., Lapidot, M. & Moyer, J.(2000). Genetic mapping of the Tsw locus for resistance to the Tospovirus Tomato spotted wilt virus in Capsicum spp. and its relationship to the Sw-5 gene for resistance to the same pathogen in tomato. Mol Plant Microbe Interact 13, 673–682.[CrossRef] [Google Scholar]
  24. Janzac, B., Fabre, F., Palloix, A. & Moury, B.(2009). Constraints on evolution of virus avirulence factors predict the durability of corresponding plant resistances. Mol Plant Pathol 10, 599–610.[CrossRef] [Google Scholar]
  25. Janzac, B., Montarry, J., Palloix, A., Navaud, O. & Moury, B.(2010). A point mutation in the polymerase of Potato virus Y confers virulence toward the Pvr4 resistance of pepper and a high competitiveness cost in susceptible cultivar. Mol Plant Microbe Interact 23, 823–830.[CrossRef] [Google Scholar]
  26. Jenner, C. E., Wang, X., Ponz, F. & Walsh, J. A.(2002). A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Res 86, 1–6.[CrossRef] [Google Scholar]
  27. Khiabanian, H., Trifonov, V. & Rabadan, R.(2009). Reassortment patterns in Swine influenza viruses. PLoS ONE 4, e7366,[CrossRef] [Google Scholar]
  28. Kimura, M.(1983).The Neutral Theory of Molecular Evolution, 5th edn. Cambridge, UK. : Cambridge University Press. [Google Scholar]
  29. Kirk, W. D. J. & Terry, I. L.(2003). The spread of the western flower thrips Frankliniella occidentalis (Pergande). Agric For Entomol 5, 301–310.[CrossRef] [Google Scholar]
  30. Kosakovsky Pond, S. L. & Frost, S. D. W.(2005a). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 2531–2533.[CrossRef] [Google Scholar]
  31. Kosakovsky Pond, S. L. & Frost, S. D. W.(2005b). Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22, 1208–1222.[CrossRef] [Google Scholar]
  32. Kosakovsky Pond, S. L., Frost, S. D. W., Grossman, Z., Gravenor, M. B., Richman, D. D. & Brown, A. J.(2006). Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PLOS Comput Biol 2, e62,[CrossRef] [Google Scholar]
  33. Lin, H. X., Rubio, L., Smythe, A. B. & Falk, B. W.(2004). Molecular population genetics of Cucumber mosaic virus in California: evidence for founder effects and reassortment. J Virol 78, 6666–6675.[CrossRef] [Google Scholar]
  34. Lindstrom, S. E., Cox, N. J. & Klimov, A.(2004). Genetic analysis of human H2N2 and early H3N2 influenza viruses, 1957–1972: evidence for genetic divergence and multiple reassortment events. Virology 328, 101–119.[CrossRef] [Google Scholar]
  35. Lovato, F. A., Inoue-Nagata, A. K., Nagata, T., de Avila, A. C., Pereira, L. A. R. & Resende, R. O.(2008). The N protein of Tomato spotted wilt virus (TSWV) is associated with the induction of programmed cell death (PCD) in Capsicum chinense plants, a hypersensitive host to TSWV infection. Virus Res 137, 245–252.[CrossRef] [Google Scholar]
  36. Margaria, P., Ciuffo, M. & Turina, M.(2004). Resistance breaking strain of Tomato spotted wilt virus (Tospovirus; Bunyaviridae) on resistant pepper cultivars in Almería, Spain. Plant Pathol 53, 795.[CrossRef] [Google Scholar]
  37. Margaria, P., Ciuffo, M., Pacifico, D. & Turina, M.(2007). Evidence that the nonstructural protein of Tomato spotted wilt virus is the avirulence determinant in the interaction with resistant pepper carrying the TSW gene. Mol Plant Microbe Interact 20, 547–558.[CrossRef] [Google Scholar]
  38. Martin, D. & Rybicki, E.(2000). RDP: detection of recombination amongst aligned sequences. Bioinformatics 16, 562–563.[CrossRef] [Google Scholar]
  39. Martin, D. P., Lemey, P., Lott, M., Moulton, V., Posada, D. & Lefeuvre, P.(2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26, 2462–2463.[CrossRef] [Google Scholar]
  40. McDonald, S. M., Matthijnssens, J., McAllen, J. K., Hine, E., Overton, L., Wang, S., Lemey, P., Zeller, M., Van Ranst, M. & other authors(2009). Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog 5, e1000634,[CrossRef] [Google Scholar]
  41. Miranda, G. J., Azzam, O. & Shirako, Y.(2000). Comparison of nucleotide sequences between northern and southern Philippine isolates of rice grassy stunt virus indicates occurrence of natural genetic reassortment. Virology 266, 26–32.[CrossRef] [Google Scholar]
  42. Moury, B., Morel, C., Johansen, E., Guilbaud, L., Souche, S., Ayme, V., Caranta, C., Palloix, A. & Jacquemond, M.(2004). Mutations in potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Mol Plant Microbe Interact 17, 322–329.[CrossRef] [Google Scholar]
  43. Nelson, M. I., Viboud, C., Simonsen, L., Bennett, R. T., Griesemer, S. B., St George, K., Taylor, J., Spiro, D. J., Sengamalay, N. A. & other authors(2008). Multiple reassortment events in the evolutionary history of H1N1 influenza A virus since 1918. PLoS Pathog 4, e1000012.[CrossRef] [Google Scholar]
  44. Nemirov, K., Vapalahti, O., Lundkvist, A., Vasilenko, V., Golovljova, I., Plyusnina, A., Niemimaa, J., Laakkonen, J., Henttonen, H. & other authors(1999). Isolation and characterization of Dobrava hantavirus carried by the striped field mouse (Apodemus agrarius) in Estonia. J Gen Virol 80, 371–379. [Google Scholar]
  45. Posada, D. & Crandall, K. A.(1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef] [Google Scholar]
  46. Qiu, W. P. & Moyer, J. W.(1999). Tomato spotted wilt tospovirus adapts to the TSWV N gene-derived resistance by genome reassortment. Phytopathology 89, 575–582.[CrossRef] [Google Scholar]
  47. Qiu, W. P., Geske, S. M., Hickey, C. M. & Moyer, J. W.(1998). Tomato spotted wilt Tospovirus genome reassortment and genome segment-specific adaptation. Virology 244, 186–194.[CrossRef] [Google Scholar]
  48. Roggero, P., Masenga, V. & Tavella, L.(2002). Field isolates of Tomato spotted wilt virus overcoming resistance in pepper and their spread to other hosts in Italy. Plant Dis 86, 950–954.[CrossRef] [Google Scholar]
  49. Roossinck, M. J.(2002). Evolutionary history of Cucumber mosaic virus deduced by phylogenetic analyses. J Virol 76, 3382–3387.[CrossRef] [Google Scholar]
  50. Rozas, J., Sánchez-DelBarrio, J. C., Messeguer, X. & Rozas, R.(2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.[CrossRef] [Google Scholar]
  51. Samuel, G., Bald, J. G. & Pittman, H. A.(1930). Investigations on ‘spotted wilt’ of tomatoes in Australia. Commonw Counc Sci Ind Res Bull 44, 8–11. [Google Scholar]
  52. Schirmer, A., Link, D., Cognat, V., Moury, B., Beuve, M., Meunier, A., Bragard, C., Gilmer, D. & Lemaire, O.(2005). Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. J Gen Virol 86, 2897–2911.[CrossRef] [Google Scholar]
  53. Sharman, M. & Persley, D. M.(2006). Field isolates of Tomato spotted wilt virus overcoming resistance in capsicum in Australia. Australas Plant Pathol 35, 123–128.[CrossRef] [Google Scholar]
  54. Silander, O. K., Weinreich, D. M., Wright, K. M., O'Keefe, K. J., Rang, C. U., Turner, P. E. & Chao, L.(2005). Widespread genetic exchange among terrestrial bacteriophages. Proc Natl Acad Sci U S A 102, 19009–19014.[CrossRef] [Google Scholar]
  55. Tamura, K., Dudley, J., Nei, M. & Kumar, S.(2007).mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef] [Google Scholar]
  56. Thomas-Carroll, M. L. & Jones, R. A. C.(2003). Selection, biological properties and fitness of resistance-breaking strains of Tomato spotted wilt virus in pepper. Ann Appl Biol 142, 235–243.[CrossRef] [Google Scholar]
  57. Thompson, J. D., Higgins, D. G. & Gibson, T. J.(1994).clustalw: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef] [Google Scholar]
  58. Tsompana, M., Abad, J., Purugganan, M. & Moyer, J. W.(2005). The molecular population genetics of the Tomato spotted wilt virus (TSWV) genome. Mol Ecol 14, 53–66. [Google Scholar]
  59. Ullman, D. E., German, T. L., Sherwood, J. L., Westcot, D. M. & Cantone, F. A.(1993). Tospovirus replication in insect vector cells, immunocytochemical evidence that the non-structural protein encoded by the S RNA of tomato spotted wilt tospovirus is present in thrips vector cells. Phytopathology 83, 456–463.[CrossRef] [Google Scholar]
  60. Watanabe, M., Nakagomi, T., Koshimura, Y. & Nakagomi, O.(2001). Direct evidence for genome segment reassortment between concurrently-circulating human rotavirus strains. Arch Virol 146, 557–570.[CrossRef] [Google Scholar]
  61. Weir, B. S. & Cockerham, C. C.(1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.[CrossRef] [Google Scholar]
  62. Whitfield, A. E., Ullman, D. E. & German, T. L.(2005). Tospovirus–thrips interactions. Annu Rev Phytopathol 43, 459–489.[CrossRef] [Google Scholar]
  63. Wijkamp, I., van Lent, J., Kormelink, R., Goldbach, R. & Peters, D.(1993). Multiplication of tomato spotted wilt virus in its insect vector, Frankliniella occidentalis. J Gen Virol 74, 341–349.[CrossRef] [Google Scholar]
  64. Wijkamp, I., Almarza, N., Goldbach, R. & Peters, D.(1995). Distinct levels of specificity in thrips transmission of tospoviruses. Phytopathology 85, 1069–1074.[CrossRef] [Google Scholar]
  65. Yang, Z.(1997).paml: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13, 555–556. [Google Scholar]
  66. Yang, Z. & Nielsen, R.(2000). Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17, 32–43.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.029082-0
Loading
Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes
J. Gen. Virol. 92, 961 (2011); https://doi.org/10.1099/vir.0.029082-0
/content/journal/jgv/10.1099/vir.0.029082-0
/content/journal/jgv/10.1099/vir.0.029082-0
Loading

Data & Media loading...

Supplements

vol. , part 4, pp. 961 - 973

Collection of TSWV isolates from Spain

Origin of TSWV isolates from the INRA and Clause collections

Primers used for reverse transcription, PCR amplifications and sequencing [Single PDF file](47 KB)

PDF

Most cited Most Cited RSS feed

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