1887

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Volume 91, Issue 1

Sequence diversity, population genetics and potential recombination events in grapevine rupestris stem pitting-associated virus in Pacific North-West vineyards Free

Abstract

Grapevine rupestris stem pitting-associated virus (GRSPaV; genus , family ) is present in many grape-growing regions of the world. A total of 84 full-length coat protein (CP) sequences and 57 sequences representing the helicase-encoding region (HR) of the RNA-dependent RNA polymerase were obtained from wine grape cultivars grown in the Pacific North-West (PNW) of the United States and their molecular diversity was compared with corresponding sequences previously reported from other grape-growing regions. In pairwise comparisons, the CP sequences from PNW isolates showed identities between 80 and 100 % at the nucleotide level and the HR sequences showed identities between 79 and 100 %. A global phylogenetic analysis of the CP and HR sequences revealed segregation of GRSPaV isolates into four major lineages with isolates from PNW distributed in all four lineages, indicating a lack of clustering by geographical origin. Scion cultivars grafted onto rootstock were found to contain mixtures of more genetic variants belonging to different lineages than own-rooted cultivars. Assessment of population genetic parameters found that the CP was more variable than the HR region. The discordant gene phylogenies obtained for some CP and HR sequences and the identification of potential recombination events involving parents from different lineages provided strong evolutionary evidence for genetic diversity among GRSPaV isolates. These results underscore the highly variable nature of the virus with implications for grapevine health status and distribution of virus-tested planting materials. This study also contributes to an increased understanding of molecular population genetics of viruses infecting deciduous woody perennials.

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2010-01-01
2024-04-19
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References

  1. Adams, M. J., Antoniw, J. F., Bar-Joseph, M., Brunt, A. A., Candresse, T., Foster, G. D., Martelli, G. P., Milne, R. G. & Fauquet, C. M.(2004). The new plant virus family Flexiviridae and assessment of molecular criteria for species demarcation. Arch Virol 149, 1045–1060. [Google Scholar]
  2. Adams, M. J., Accotto, G. P., Agranovsky, A. A., Bar-Joseph, M., Boscia, D., Brunt, A. A., Candresse, T., Coutts, R. H. A., Dolja, V. V. & other authors(2005). Family Flexiviridae. In Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses, pp. 1089–1124. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. Amsterdam: Elservier.
  3. Al Rwahnih, M., Daubert, S., Golino, D. & Rowhani, A.(2009). Deep sequencing analysis of RNAs from a grapevine showing Syrah decline symptoms reveals a multiple virus infection that includes a novel virus. Virology 387, 395–401.[CrossRef] [Google Scholar]
  4. Bouyahia, H., Boscia, D., Savino, V., La Notte, P., Pirolo, C., Castellano, M. A., Minafra, A. & Martelli, G. P.(2005).Grapevine rupestris stem pitting-associated virus is linked with grapevine necrosis. Vitis 44, 133–137. [Google Scholar]
  5. Bracho, M. A., Moya, A. & Barrio, E.(1998). Contribution of Taq polymerase-induced errors to the estimation of RNA virus diversity. J Gen Virol 79, 2921–2928. [Google Scholar]
  6. Castresana, J.(2007). Topological variation in single-gene phylogenetic trees. Genome Biol 8. [Google Scholar]
  7. Chare, E. R. & Holmes, E. C.(2004). Selection pressures in the capsid genes of plant RNA viruses reflect mode of transmission. J Gen Virol 85, 3149–3157.[CrossRef] [Google Scholar]
  8. 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]
  9. Credi, R.(1997). Characterization of grapevine rugose wood disease sources from Italy. Plant Dis 81, 1288–1292.[CrossRef] [Google Scholar]
  10. d'Urso, F., Ayllón, M. A., Rubio, L., Sambade, A., Hermoso de Mendoza, A., Guerri, J. & Moreno, P.(2000). Contribution of uneven distribution of genomic RNA variants of Citrus tristeza virus (CTV) within the plant to changes in the viral population following aphid transmission. Plant Pathol 49, 288–294.[CrossRef] [Google Scholar]
  11. Fajardo, T. V. M., Dianese, É. C., Eiras, M., Cerqueira, D. M., Lopes, D. B., Ferreira, M. A. S. V. & Martins, C. R. F.(2007). Variability of the coat protein gene of Grapevine leafroll-associated virus 3 in Brazil. Fitopatol Bras 32, 335–340.[CrossRef] [Google Scholar]
  12. Fu, Y. X. & Li, W. H.(1993). Statistical tests of neutrality of mutations. Genetics 133, 693–709. [Google Scholar]
  13. 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]
  14. Habili, N., Farrokhi, N., Lima, M. F., Nicholas, P. & Randles, J. W.(2006). Distribution of Rupestris stem-pitting-associated virus variants in two Australian vineyards showing different symptoms. Ann Appl Biol 148, 91–96.[CrossRef] [Google Scholar]
  15. Hey, J. & Harris, E. E.(1999). Population bottlenecks and patterns of human polymorphism. Mol Biol Evol 16, 1423–1426.[CrossRef] [Google Scholar]
  16. Huerta-Cepas, J., Dopazo, H., Dopazo, J. & Gabaldón, T.(2007). The human phylome. Genome Biol 8, R109[CrossRef] [Google Scholar]
  17. Jeffroy, O., Brinkmann, H., Delsuc, F. & Philippe, H.(2006). Phylogenomics: the beginning of incongruence? Trends Genet 22, 225–231.[CrossRef] [Google Scholar]
  18. Jridi, C., Martin, J.-F., Marie-Jeanne, V., Labonne, G. & Blanc, S.(2006). Distinct viral populations differentiate and evolve independently in a single perennial host plant. J Virol 80, 2349–2357.[CrossRef] [Google Scholar]
  19. Karan, M., Harding, R. M. & Dale, J. L.(1994). Evidence of two groups of Banana bunchy top virus isolates. J Gen Virol 75, 3541–3546.[CrossRef] [Google Scholar]
  20. Kimura, M.(1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16, 111–120.[CrossRef] [Google Scholar]
  21. Komar, V., Vigne, E., Demangeat, G., Cornuet, P. & Fuchs, M.(2006). Effect of virus combinations on the performance of Vitis vinifera var. Chardonnay. In Extended abstracts of the XV meeting of the International Council for the Study of Viruses and Virus-like Diseases of the Grapevine, Stellenbosch, South Africa, April 3–7 2006, pp. 134–135.
  22. Koonin, E. V. & Dolja, V. V.(1993). Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28, 375–430.[CrossRef] [Google Scholar]
  23. Korber, B.(2000). HIV signatures and similarities. In Computational and Evolutionary Analysis of HIV Molecular Sequences, pp. 55–72. Edited by A. G. Rodrigo & G. H. Learn, Jr. Dordrecht, The Netherlands: Kluwer Academic Publishers.
  24. Lima, M. F., Alkowni, R., Uyemoto, J. K., Golino, D., Osman, F. & Rowhani, A.(2006). Molecular analysis of a California strain of Rupestris stem pitting-associated virus isolated from declining Syrah grapevines. Arch Virol 151, 1889–1894.[CrossRef] [Google Scholar]
  25. Lima, M. F., Golino, D. A. & Rowhani, A.(2007). Seed transmission of Rupestris stem pitting associated virus in grapevine. In Proceedings of the 1st Annual National Viticulture Research Conference, University of California, Davis, USA, July 18–20 2007, pp. 61–62.
  26. Lundberg, K. S., Shoemaker, D. D., Adams, M. W., Short, J. M., Sorge, J. A. & Mathur, E. J.(1991). High-fidelity amplification using a thermostable DNA polymerase isolated from Pyrococcus furiosus. Gene 108, 1–6.[CrossRef] [Google Scholar]
  27. Magome, H., Yoshikawa, N. & Takahashi, T.(1999). Single-strand conformation polymorphism analysis of Apple stem grooving capillovirus sequence variants. Phytopathology 89, 136–140.[CrossRef] [Google Scholar]
  28. Makarova, K. S., Aravind, L. & Koonin, E. V.(2000). A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem Sci 25, 50–52.[CrossRef] [Google Scholar]
  29. Martelli, G. P.(1993). Rugose wood complex. In Graft-Transmissible Diseases of Grapevines, Handbook for Detection and Diagnosis, pp. 45–54. Edited by G. P. Martelli. Rome, Italy: Food and Agriculture Organization of the United Nations.
  30. Martelli, G. P. & Jelkmann, W.(1998).Foveavirus, a new plant virus genus. Arch Virol 143, 1245–1249.[CrossRef] [Google Scholar]
  31. Martelli, G. P., Adams, M. J., Kreuze, J. F. & Dolja, V. V.(2007). Family Flexiviridae: a case study in virion and genome plasticity. Annu Rev Phytopathol 45, 73–100.[CrossRef] [Google Scholar]
  32. Martin, D. P., Williamson, C. & Posada, D.(2005).rdp2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef] [Google Scholar]
  33. Meng, B., Pang, S. Z., Forsline, P. L., McFerson, J. R. & Gonsalves, D.(1998). Nucleotide sequence and genome structure of grapevine rupestris stem pitting associated virus-1 reveal similarities to apple stem pitting virus. J Gen Virol 79, 2059–2069. [Google Scholar]
  34. Meng, B., Johnson, R., Peressini, S., Forsline, P. L. & Gonsalves, D.(1999). Rupestris stem pitting associated virus-1 is consistently detected in grapevines that are infected with rupestris stem pitting. Eur J Plant Pathol 105, 191–199.[CrossRef] [Google Scholar]
  35. Meng, B., Rebelo, A. R. & Fisher, H.(2006). Genetic diversity analyses of grapevine Rupestris stem pitting-associated virus reveal distinct population structures in scion versus rootstock varieties. J Gen Virol 87, 1725–1733.[CrossRef] [Google Scholar]
  36. Minafra, A. & Boscia, D.(2003). An overview of rugose wood-associated viruses: 2000–2003. In The 14th Meeting of the International Council for the Study of Virus-like Diseases of the Grapevine, Locorotondo, Italy, pp. 116–119.
  37. Minafra, A., Casati, P., Elicio, V., Rowhani, A., Saldarelli, P., Savino, V. & Martelli, G. P.(2000). Serological detection of Grapevine Rupestris stem pitting-associated virus (GRSPaV) by a polyclonal antiserum to recombinant virus coat protein. Vitis 39, 115–118. [Google Scholar]
  38. Naidu, R. A., Soule, M. J. & Jarugula, S.(2006). Single and mixed infections of Grapevine leafroll-associated viruses in Washington State vineyards. Phytopathology 96, S83 [Google Scholar]
  39. Nakaune, R., Inoue, K., Nasu, H., Kakogawa, K., Nitta, H., Imada, J. & Nakano, M.(2008). Detection of viruses associated with rugose wood in Japanese grapevines and analysis of genomic variability of Rupestris stem pitting-associated virus. J Gen Plant Pathol 74, 156–163.[CrossRef] [Google Scholar]
  40. Nei, M. & Kumar, S.(2000).Molecular Evolution and Phylogenetics. New York: Oxford University Press.
  41. Nolasco, G., Santos, C., Petrovic, N., Teixeira Santos, M., Cortez, I., Fonseca, F., Boben, J., Nazare Pereira, A. M. & Sequeria, O.(2006).Rupestris stem pitting associated virus isolates are composed by mixtures of genomic variants which share a highly conserved coat protein. Arch Virol 151, 83–96.[CrossRef] [Google Scholar]
  42. Penny, D., Foulds, L. R. & Hendy, M. D.(1982). Testing the theory of evolution by comparing phylogenetic trees constructed from five different protein sequences. Nature 297, 197–200.[CrossRef] [Google Scholar]
  43. Petrovic, N., Penev, B., Krastanova, T., Meng, B. & Gonsalves, D.(2000). Distribution of Rupestris stem pitting associated virus in green-house and field grown Vitis rupestris St George. In Extended Abstracts of the 13th Meeting of the International Council for the Study of Virus-like Diseases of the Grapevine, Adelaide, Australia, March 12–17 2000.
  44. Pfosser, M. F. & Baumann, H.(2002). Phylogeny and geographical differentiation of zucchini yellow mosaic virus isolates (Potyviridae) based on molecular analysis of the coat protein and part of the cytoplasmic inclusion protein genes. Arch Virol 147, 1599–1609.[CrossRef] [Google Scholar]
  45. Prosser, S. W., Goszczynski, D. E. & Meng, B.(2007). Molecular analysis of double-stranded RNAs reveals complex infection of grapevines with multiple viruses. Virus Res 124, 151–159.[CrossRef] [Google Scholar]
  46. Rebelo, A. R., Niewiadomski, S., Prosser, S. W., Krell, P. & Meng, B.(2008). Subcellular localization of the triple gene block proteins encoded by a Foveavirus infecting grapevines. Virus Res 138, 57–69.[CrossRef] [Google Scholar]
  47. Rokas, A. & Carroll, S. B.(2006). Bushes in the tree of life. PLoS Biol 4, e352[CrossRef] [Google Scholar]
  48. Rowhani, A., Biardi, L., Johnson, R., Saldarelli, P., Zhang, Y. P., Chin, J. & Green, M.(2000a). Simplified sample preparation method and one-tube RT-PCR for grapevine viruses. In Extended Abstracts of the 13th Meeting of the International Council for the Study of Virus-like Diseases of the Grapevine, Adelaide, Australia, March 12–17 2000, p. 82.
  49. Rowhani, A., Zhang, Y. P., Chin, H., Minafra, A., Golino, D. A. & Uyemoto, J. K.(2000b). Grapevine Rupestris stem pitting associated virus: population diversity, titer in the host and possible transmission vector. In Extended Abstracts of the 13th Meeting of the International Council for the Study of Virus-like Diseases of the Grapevine, Adelaide, Australia, March 12–17 2000.
  50. Rozas, J., Sanchez-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. 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]
  52. Rzhetsky, A. & Nei, M.(1992). A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9, 945–967. [Google Scholar]
  53. Saitou, N. & Nei, M.(1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425. [Google Scholar]
  54. Shi, B. J., Habilli, N., Gafny, R. & Symons, R. H.(2004). Extensive variation of sequence within isolates of Grapevine virus B. Virus Genes 29, 279–285.[CrossRef] [Google Scholar]
  55. Tajima, F.(1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595. [Google Scholar]
  56. 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]
  57. Teycheney, P. Y., Laboureau, N., Iskre-Caruana, M. L. & Candresse, T.(2005). High genetic variability and evidence for plant to plant transfer of Banana mild mosaic virus. J Gen Virol 86, 3179–3187.[CrossRef] [Google Scholar]
  58. 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]
  59. 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]
  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(2008). 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. 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]
  62. Watterson, G. A.(1975). On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7, 256–276.[CrossRef] [Google Scholar]
  63. 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]
  64. Zhang, Y. P., Uyemoto, J. K., Golino, D. A. & Rowhani, A.(1998). Nucleotide sequence and RT-PCR detection of a virus associated with grapevine rupestris stem-pitting disease. Phytopathology 88, 1231–1237.[CrossRef] [Google Scholar]
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Sequence diversity, population genetics and potential recombination events in grapevine rupestris stem pitting-associated virus in Pacific North-West vineyards
J. Gen. Virol. 91, 265 (2010); https://doi.org/10.1099/vir.0.014423-0
/content/journal/jgv/10.1099/vir.0.014423-0
/content/journal/jgv/10.1099/vir.0.014423-0
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