Mixed infections of Pepino mosaic virus strains modulate the evolutionary dynamics of this emergent virus

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12378-12387

  Gomez P ^a   Sempere, R N ^a   Elena, S F ^b,c   Aranda, M A ^a  

^a RESEARCH GROUP ON QUALITY   (Spain)

^b Ciudad Politécnica de la Innovación   (Spain)

^c SANTA FE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CROP PRODUCTION; ECOLOGICAL GENETICS; ECONOMICS; FLEXIVIRIDAE; GENETIC VARIABILITY; HOST RANGE; HYBRIDIZATION; MIXED INFECTION; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPINO MOSAIC VIRUS; POPULATION GENETICS; PRIORITY JOURNAL; SOLANUM; TOMATO; VIRUS INFECTION; VIRUS STRAIN;

CLUSTER ANALYSIS; EVOLUTION, MOLECULAR; GENETIC VARIATION; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HYBRIDIZATION; PHYLOGENY; PLANT DISEASES; POTEXVIRUS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

LYCOPERSICON ESCULENTUM; PEPINO MOSAIC VIRUS;

EID: 70450159535     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01486-09     Document Type: Article

References (80)

1. Aaziz, R., and M. Tepfer. 1999. Recombination between genomic RNAs of two cucumoviruses under conditions of minimal selection pressure. Virology 263:282-289. (Pubitemid 29521521)
2. AbouHaidar, M. G., H. M. Xu, and K. L. Hefferon. 1998. Potexvirus isolation and RNA extraction. Plant Virol. Protoc. 81:131-143.
3. Aguilar, J. M., M. D. Hernandez-Gallarod, J. L. Cenis, A. Lacasa, and M. A. Aranda. 2002. Complete sequence of the Pepino mosaic virus RNA genome. Arch. Virol. 147:2009-2015.
4. Arends, H. M., D. Winstanley, and J. A. Jehle. 2005. Virulence and competitiveness of Cydia pomonella granulovirus mutants: parameters that do not match. J. Gen. Virol. 86:2731-2738.
5. Beuve, M., M. Stevens, H. Y. Liu, W. M. Wintermantel, S. Hauser, and O. Lemaire. 2008. Biological and molecular characterization of an American sugar beet-infecting Beet western yellow virus isolate. Plant Dis. 92:51-60.
6. Bonnet, J., A. Fraile, S. Sacristan, J. M. Malpica, and F. Garcia-Arenal. 2005. Role of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virus. Virology 332:359-368.
7. Carrasco, P., F. de la Iglesia, and S. F. Elena. 2007. Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco etch virus. J. Virol. 81:12979-12984.
8. Christen, L., J. Seto, and E. G. Niles. 1990. Superinfection exclusion of vaccinia virus in virus-infected cell cultures. Virology 174:35-42. (Pubitemid 20030948)
9. Cicin-Sain, L., J. Podlech, M. Messerle, M. J. Reddehase, and U. H. Koszinowski. 2005. Frequent coinfection of cells explains functional in vivo complementation between cytomegalovirus variants in the multiply infected host. J. Virol. 79:9492-9502. (Pubitemid 41022293)
10. Cordoba, M. C., L. Martinez-Priego, and C. Jorda. 2004. New natural hosts of Pepino mosaic virus in Spain. Plant Dis. 88:906-908.
11. Cotillon, A. C., M. Girard, and S. Ducouret. 2002. Complete nucleotide sequence of the genomic RNA of a French isolate of Pepino mosaic virus (PepMV). Arch. Virol. 147:2231-2238.
12. Cruz, S. S., A. G. Roberts, D. A. M. Prior, S. Chapman, and K. J. Oparka. 1998. Cell-to-cell and phloem-mediated transport of Potato virus X: the role of virions. Plant Cell 10:495-510.
13. Desbiez, C., B. Joannon, C. Wipf-Scheibel, C. Chandeysson, and H. Lecoq. 2009. Emergence of new strains of Watermelon mosaic virus in southeastern France: evidence for limited spread but rapid local population shift. Virus Res. 141:201-208.
14. Dietrich, C., J. Miller, G. McKenzie, L. Palkovics, E. Balazs, P. Palukaitis, and E. Maiss. 2007. No recombination detected in artificial potyvirus mixed infections and between potyvirus derived transgenes and heterologous challenging potyviruses. Environ. Biosafety Res. 6:207-218.
15. EPPO. 2009. EPPO alert list-viruses: Pepino mosaic potexvirus, a new virus of tomato introduced into Europe. EPPO, Paris, France. www.eppo.org/quarantine/Alert-List/alert-list.htm.
16. Escriu, F., A. Fraile, and F. Garcia-Arenal. 2007. Constraints to genetic exchange support gene coadaptation in a tripartite RNA virus. PLoS Pathog. 3:67-74.
17. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
18. Foster, J. E., S. N. Bennett, C. V. Carrington, H. Vaughan, and W. O. McMillan. 2004. Phylogeography and molecular evolution of dengue 2 in the Caribbean basin, 1981-2000. Virology 324:48-59.
19. Fraile, A., F. Escriu, M. A. Aranda, J. M. Malpica, A. J. Gibbs, and F. GarciaArenal. 1997. A century of tobamovirus evolution in an Australian population of Nicotiana glauca. J. Virol. 71:8316-8320.
20. French, C. J., M. Bouthillier, M. Bernardy, G. Ferguson, M. Sabourin, R. Johnson, C. Masters, S. Godkin, and R. Mumford. 2001. First report of Pepino mosaic virus in Canada and the United States. Plant Dis. 85:1121-1123.
21. Garcia-Andres, S., F. Monci, J. Navas-Castillo, and E. Moriones. 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.
22. Garcia-Andres, S., D. M. Tomas, S. Sanchez-Campos, J. Navas-Castillo, and E. Moriones. 2007. Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology 365:210-219. (Pubitemid 46907240)
23. Garcia-Arenal, F., A. Fraile, and J. M. Malpica. 2001. Variability and genetic structure of plant virus populations. Annu. Rev. Phytopathol. 39:157-186.
24. Goldman, N., and Z. H. Yang. 1994. Codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11:725-736.
25. Grenfell, B. T., O. G. Pybus, J. R. Gog, J. L. N. Wood, J. M. Daly, J. A. Mumford, and E. C. Holmes. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327-332.
26. Hanssen, I. M., A. Paeleman, E. Vandewoestijne, L. V. Bergen, C. Bragard, B. Lievens, A. C. R. C. Vanachter, and B. P. H. J. Thomma. 2009. Pepino mosaic virus isolates and differential symptomatology in tomato. Plant Pathol. 58:450-460.
27. Hanssen, I. M., A. Paeleman, L. Wittemans, K. Goen, B. Lievens, C. Bragard, A. Vanachter, and B. Thomma. 2008. Genetic characterization of Pepino mosaic virus isolates from Belgian greenhouse tomatoes reveals genetic recombination. Eur. J. Plant Pathol. 121:131-146.
28. Hasegawa, M., H. Kishino, and T. A. Yano. 1985. Dating of the human ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174.
29. Hasiow, B., N. Borodynko, and H. Pospieszny. 2008. Complete genomic RNA sequence of the Polish Pepino mosaic virus isolate belonging to the US2 strain. Virus Genes 36:209-214.
30. Jones, R. A. C., R. Koenig, and D. E. Lesemann. 1980. Pepino mosaic virus, a new potexvirus from pepino (Solanum muricantum). Ann. Appl. Biol. 94:61-68.
31. Kassem, M. A., R. N. Sempere, M. Juarez, M. A. Aranda, and V. Truniger. 2007. Cucurbit aphid-borne yellows virus is prevalent in field-grown cucurbit crops of southeastern Spain. Plant Dis. 91:232-238.
32. Kimura, M. 1981. Possibility of extensive neutral evolution under stabilizing selection with special reference to nonrandom usage of synonymous codons. Proc. Natl. Acad. Sci. USA 78:5773-5777.
33. Kosakovsky-Pond, S. L., S. D. W. Frost, and S. V. Muse. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
34. Krishnamurthy, K. 2003. The Potato virus X TGBp3 protein associates with the ER network for virus cell-to-cell movement. Virology 309:135-151.
35. Ling, K.-S., W. M. Wintermantel, and M. Bledsoe. 2008. Genetic composition of Pepino mosaic virus population in North American greenhouse tomatoes. Plant Dis. 92:1683-1688.
36. Ling, K. S. 2007. Molecular characterization of two Pepino mosaic virus variants from imported tomato seed reveals high levels of sequence identity between Chilean and US isolates. Virus Genes 34:1-8.
37. Ling, K. S. 2008. Pepino mosaic virus on tomato seed: virus location and mechanical transmission. Plant Dis. 92:1701-1705.
38. Lopez, C., S. Soler, and F. Nuez. 2005. Comparison of the complete sequences of three different isolates of Pepino mosaic virus: size variability of the TGBp3 protein between tomato and L. peruvianum isolates. Arch. Virol. 150:619-627.
39. Lough, T. J., S. J. Emerson, W. J. Lucas, and R. L. S. Forster. 2001. Trans-complementation of long-distance movement of White clover mosaic virus triple gene block (TGB) mutants: phloem-associated movement of TGBp1. Virology 288:18-28.
40. Marco, C., and M. A. Aranda. 2005. Genetic diversity of a natural population of Cucurbit yellow stunting disorder virus. J. Gen. Virol. 86:815-822.
41. Marco, C. F., J. M. Aguilar, J. Abad, M. L. Gomez-Guillamon, and M. A. Aranda. 2003. Melon resistance to Cucurbit yellow stunting disorder virus is characterized by reduced virus accumulation. Phytopathology 93:844-852.
42. Maroon-Lango, C. J., M. A. Guaragna, R. L. Jordan, J. Hammond, M. Bandla, and S. K. Marquardt. 2005. Two unique US isolates of Pepino mosaic virus from a limited source of pooled tomato tissue are distinct from a third (European-like) US isolate. Arch. Virol. 150:1187-1201.
43. Mitra, R. 2003. The Potato virus X TGBp2 protein association with the endoplasmic reticulum plays a role in but is not sufficient for viral cell-to-cell movement. Virology 312:35-48.
44. Monci, F., S. Sanchez-Campos, J. Navas-Castillo, and E. Moriones. 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.
45. Moreno, I. M., J. M. Malpica, J. A. Diaz-Pendon, E. Moriones, A. Fraile, and F. Garcia-Arenal. 2004. Variability and genetic structure of the population of watermelon mosaic virus infecting melon in Spain. Virology 318:451-460.
46. Morozov, S. Y., and A. G. Solovyev. 2003. Triple gene block: modular design of a multifunctional machine for plant virus movement. J. Gen. Virol. 84:1351-1366.
47. Moya, A., E. C. Holmes, and F. Gonzalez-Candelas. 2004. The population genetics and evolutionary epidemiology of RNA viruses. Nature Rev. Microbiol. 2:279-288.
48. Mumford, R. A., and E. J. Metcalfe. 2001. The partial sequencing of the genomic RNA of a UK isolate of Pepino mosaic virus and the comparison of the coat protein sequence with other isolates from Europe and Peru. Arch. Virol. 146:2455-2460.
49. Muse, S. V., and B. S. Gaut. 1994. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol. Biol. Evol. 11:715-724.
50. Nei, M., and S. Kumar. 2000. Molecular evolution and phylogenetics. Oxford University Press, Oxford, United Kingdom.
51. Pagan, I., M. Cordoba-Selles, L. Martinez-Priego, A. Fraile, J. Malpica, C. Jorda, and F. Garcia-Arenal. 2006. Genetic structure of the population of Pepino mosaic virus infecting tomato crops in Spain. Phytopathology 96:274-279.
52. Pamilo, P., and N. O. Bianchi. 1993. Evolution of the zfx and zfy genes: rates and interdependence between the genes. Mol. Biol. Evol. 10:271-281.
53. Pepin, K., K. Lambeth, and K. Hanley. 2008. Asymmetric competitive suppression between strains of dengue virus. BMC Microbiol. 8:28.
54. Pospieszny, H., and N. Borodynko. 2006. New Polish isolate of Pepino mosaic virus highly distinct from European tomato, Peruvian, and US2 strains. Plant Dis. 90:1106-1108.
55. Pospieszny, H., B. Hasiów, and N. Borodynko. 2008. Characterization of two distinct Polish isolates of Pepino mosaic virus. Eur. J. Plant Pathol. 122:443-445.
56. Rodriguez-Cerezo, E., S. F. Elena, A. Moya, and F. Garcia-Arenal. 1991. High genetic stability in natural populations of the plant RNA virus Tobacco mild green mosaic virus. J. Mol. Evol. 32:328-332.
57. Roggero, P., V. Masenga, R. Lenzi, F. Coghe, S. Ena, and S. Winter. 2001. First report of Pepino mosaic virus in tomato in Italy. Plant Pathol. 50:798-800.
58. Rzhetsky, A., and M. Nei. 1992. A simple method for estimating and testing minimum-evolution trees. Mol. Biol. Evol. 9:945-967.
59. Salomone, A., and P. Roggero. 2002. Host range, seed transmission, and detection by ELISA and lateral flow of an Italian isolate of Pepino mosaic virus. J. Plant Pathol. 84:65-68.
60. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
61. Sanchez-Campos, S., J. A. Diaz, F. Monci, E. R. Bejarano, J. Reina, J. Navas-Castillo, M. A. Aranda, and E. Moriones. 2002. High genetic stability of the begomovirus Tomato yellow leaf curl Sardinia virus in southern Spain over an 8-year period. Phytopathology 92:842-849.
62. Sanchez-Campos, S., J. Navas-Castillo, R. Camero, C. Soria, J. A. Diaz, and E. Moriones. 1999. Displacement of tomato yellow leaf curl virus (TYLCV)-Sr by TYLCV-Is in tomato epidemics in Spain. Phytopathology 89:1038-1043. (Pubitemid 29514854)
63. Sanjuan, R., J. M. Cuevas, A. Moya, and S. F. Elena. 2005. Epistasis and the adaptability of an RNA virus. Genetics 170:1001-1008.
64. Sedarati, F., R. T. Javier, and J. G. Stevens. 1988. Pathogenesis of a lethal mixed infection in mice with two nonneuroinvasive herpes simplex virus strains. J. Virol. 62:3037-3039. (Pubitemid 18193905)
65. Shipp, J. L., R. Buitenhuis, L. Stobbs, K. Wang, W. S. Kim, and G. Ferguson. 2008. Vectoring of Pepino mosaic virus by bumblebees in tomato greenhouses. Ann. Appl. Biol. 153:149-155.
66. Skryabin, K. 1988. Conserved and variable elements in RNA genomes of potexvirus. FEBS Lett. 240:33-40.
67. Soler, S., C. Lopez, and F. Nuez. 2005. Natural occurrence of viruses in Lycopersicon spp. in Ecuador. Plant Dis. 89:1244-1254.
68. Soler, S., J. Prohens, M. J. Diez, and F. Nuez. 2002. Natural occurrence of Pepino mosaic virus in Lycopersicon species in central and southern Peru. J. Phytopathol. 150:49-53.
69. Spence, N. J., J. Basham, R. A. Mumford, G. Hayman, R. Edmondson, and D. R. Jones. 2006. Effect of Pepino mosaic virus on the yield and quality of glasshouse-grown tomatoes in the United Kingdom. Plant Pathol. 55:595-606.
70. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software, version 4.0. Mol. Biol. Evol. 24:1596-1599.
71. Tamura, K., and M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-526.
72. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: 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.
73. Tremblay, M. 2006. Effect of mutations K97A and E128A on RNA binding and self assembly of papaya mosaic potexvirus coat protein. The FEBS journal. 273:14-25.
74. van der Vlugt, R. A., C. M. Stijger, J. T. J. Verhoeven, and D. E. Lesemann. 2000. First report of Pepino mosaic virus on tomato. Plant Dis. 84:103-108.
75. Verchot-Lubicz, J. 2005. A new cell-to-cell transport model for potexviruses. Mol. Plant-Microbe Interact. 18:283-290.
76. Verchot-Lubicz, J., C. M. Ye, and D. Bamunusinghe. 2007. Molecular biology of potexviruses: recent advances. J. Gen. Virol. 88:1643-1655.
77. Voinnet, O., C. Lederer, and D. C. Baulcombe. 2000. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103:157-167.
78. Yang, Y., B. Ding, D. C. Baulcombe, and J. Verchot. 2000. Cell-to-cell movement of the 25K protein of Potato virus X is regulated by three other viral proteins. Mol. Plant-Microbe Interact. 13:599-605.
79. Zayakina, O., M. Arkhipenko, S. Kozlovsky, N. Nikitin, A. Smirnov, P. Susi, N. Rodionova, O. Karpova, and J. Atabekov. 2008. Mutagenic analysis of Potato virus X movement protein (TGBp1) and the coat protein (CP): in vitro TGBp1-CP binding and viral RNA translation activation. Mol. Plant Pathol. 9:37-44.
80. Zhao, X. 2007. Potential evolutionary influences on overlapping reading frames in the bovine leukemia virus pXBL region. Genomics 89:502-511. (Pubitemid 46413670)