1887

Abstract

The genetic basis for virulence in potyviruses is largely unknown. Earlier studies showed that there are two host types of (TuMV); the / (BR)-host type infects both and systemically, whereas the (B)-host type infects fully and systemically, but not . The genetic basis of this difference has been explored by using the progeny of an infectious clone, p35Tunos; this clone is derived from the UK1 isolate, which is of the B-host type, but rarely infects systemically and then only asymptomatically. Two inocula from one such infection were adapted to by passaging, during which the infectivity and concentration of the virions of successive infections increased. The variant genomes in the samples, 16 in total, were sequenced fully. Four of the 39 nucleotide substitutions that were detected among the -adapted variant genomes were probably crucial for adaptation, as they were found in several variants with independent passage histories. These four were found in the protein 1 (P1), protein 3 (P3), cylindrical inclusion protein (CI) and genome-liked viral protein (VPg) genes. One of four ‘parallel evolution’ substitutions, G→A, resulted in a Met→Ile amino acid change in the C terminus of P3. It seems likely that this site is important in the initial stages of adaptation to . Other independent substitutions were mostly found in the P3, CI and VPg genes.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80540-0
2005-02-01
2019-11-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/2/vir860501.html?itemId=/content/journal/jgv/10.1099/vir.0.80540-0&mimeType=html&fmt=ahah

References

  1. Atreya, C. D., Atreya, P. L., Thornbury, D. W. & Pirone, T. P. ( 1992; ). Site-directed mutations in the potyvirus HC-PRO gene affect helper component activity, virus accumulation, and symptom expression in infected tobacco plants. Virology 191, 106–111.[CrossRef]
    [Google Scholar]
  2. 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]
  3. Bonhoeffer, S. & Sniegowski, P. ( 2002; ). The importance of being erroneous. Nature 420, 367–369.[CrossRef]
    [Google Scholar]
  4. 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]
  5. Brown, E. G., Liu, H., Chang Kit, L., Baird, S. & Nesrallah, M. ( 2001; ). Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes. Proc Natl Acad Sci U S A 98, 6883–6888.[CrossRef]
    [Google Scholar]
  6. Bull, J. J., Badgett, M. R., Wichman, H. A., Huelsenbeck, J. P., Hillis, D. M., Gulati, A., Ho, C. & Molineux, I. J. ( 1997; ). Exceptional convergent evolution in a virus. Genetics 147, 1497–1507.
    [Google Scholar]
  7. Bull, J. J., Badgett, M. R., Rokyta, D. & Molineux, I. J. ( 2003; ). Experimental evolution yields hundreds of mutations in a functional viral genome. J Mol Evol 57, 241–248.[CrossRef]
    [Google Scholar]
  8. Chao, L. ( 1990; ). Fitness of RNA virus decreased by Muller's ratchet. Nature 348, 454–455.[CrossRef]
    [Google Scholar]
  9. Chu, M., Lopez-Moya, J. J., Llave-Correas, C. & Pirone, T. P. ( 1997; ). Two separate regions in the genome of the tobacco etch virus contain determinants of the wilting response of tabasco pepper. Mol Plant Microbe Interact 10, 472–480.[CrossRef]
    [Google Scholar]
  10. Clark, M. F. & Adams, A. N. ( 1977; ). Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34, 475–485.[CrossRef]
    [Google Scholar]
  11. Crill, W. D., Wichman, H. A. & Bull, J. J. ( 2000; ). Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154, 27–37.
    [Google Scholar]
  12. Dallot, S., Quiot-Douine, L., Sáenz, P., Cervera, M. T., García, J.-A. & Quiot, J.-B. ( 2001; ). Identification of Plum pox virus determinants implicated in specific interactions with different Prunus spp. Phytopathology 91, 159–164.[CrossRef]
    [Google Scholar]
  13. Domingo, E. ( 2000; ). Viruses at the edge of adaptation. Virology 270, 251–253.[CrossRef]
    [Google Scholar]
  14. Domingo, E., Sabo, D., Taniguchi, T. & Weissmann, C. ( 1978; ). Nucleotide sequence heterogeneity of an RNA phage population. Cell 13, 735–744.[CrossRef]
    [Google Scholar]
  15. Domingo, E., Holland, J. J., Biebricher, C. & Eigen, M. ( 1995; ). Quasispecies: the concept and the word. In Molecular Basis of Virus Evolution, pp. 181–191. Edited by A. Gibbs, C. H. Calisher & F. García-Arenal. Cambridge: Cambridge University Press.
  16. Domingo, E., Menéndez-Arias, L. & Holland, J. J. ( 1997; ). RNA virus fitness. Rev Med Virol 7, 87–96.[CrossRef]
    [Google Scholar]
  17. Duarte, E., Clarke, D., Moya, A., Domingo, E. & Holland, J. ( 1992; ). Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. Proc Natl Acad Sci U S A 89, 6015–6019.[CrossRef]
    [Google Scholar]
  18. Elena, S. F. & Lenski, R. E. ( 2003; ). Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4, 457–469.
    [Google Scholar]
  19. 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]
  20. Gibbs, A., Calisher, C. H. & García-Arenal, F. ( 1995; ). Introduction and guide. In Molecular Basis of Virus Evolution, pp. 1–10. Edited by A. Gibbs, C. H. Calisher & F. García-Arenal. Cambridge: Cambridge University Press.
  21. Gordo, I., Navarro, A. & Charlesworth, B. ( 2002; ). Muller's ratchet and the pattern of variation at a neutral locus. Genetics 161, 835–848.
    [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. Hall, J. S., French, R., Hein, G. L., Morris, T. J. & Stenger, D. C. ( 2001; ). Three distinct mechanisms facilitate genetic isolation of sympatric wheat streak mosaic virus lineages. Virology 282, 230–236.[CrossRef]
    [Google Scholar]
  24. 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]
  25. Hjulsager, C. K., Lund, O. S. & Johansen, I. E. ( 2002; ). A new pathotype of Pea seedborne mosaic virus explained by properties of the P3-6k1- and viral genome-linked protein (VPg)-coding regions. Mol Plant Microbe Interact 15, 169–171.[CrossRef]
    [Google Scholar]
  26. Holland, J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S. & VandePol, S. ( 1982; ). Rapid evolution of RNA genomes. Science 215, 1577–1585.[CrossRef]
    [Google Scholar]
  27. Jenner, C. E., Tomimura, K., Ohshima, K., Hughes, S. L. & Walsh, J. A. ( 2002; ). Mutations in Turnip mosaic virus P3 and cylindrical inclusion proteins are separately required to overcome two Brassica napus resistance genes. Virology 300, 50–59.[CrossRef]
    [Google Scholar]
  28. Jenner, C. E., Wang, X., Tomimura, K., Ohshima, K., Ponz, F. & Walsh, J. A. ( 2003; ). The dual role of the potyvirus P3 protein of Turnip mosaic virus as a symptom and avirulence determinant in brassicas. Mol Plant Microbe Interact 16, 777–784.[CrossRef]
    [Google Scholar]
  29. Johansen, I. E., Dougherty, W. G., Keller, K. E., Wang, D. & Hampton, R. O. ( 1996; ). Multiple viral determinants affect seed transmission of pea seedborne mosaic virus in Pisum sativum. J Gen Virol 77, 3149–3154.[CrossRef]
    [Google Scholar]
  30. Johansen, I. E., Lund, O. S., Hjulsager, C. K. & Laursen, J. ( 2001; ). Recessive resistance in Pisum sativum and potyvirus pathotype resolved in a gene-for-cistron correspondence between host and virus. J Virol 75, 6609–6614.[CrossRef]
    [Google Scholar]
  31. Kearney, C. M., Thomson, M. J. & Roland, K. E. ( 1999; ). Genome evolution of tobacco mosaic virus populations during long-term passaging in a diverse range of hosts. Arch Virol 144, 1513–1526.[CrossRef]
    [Google Scholar]
  32. Klein, P. G., Klein, R. R., Rodriguez-Cerezo, E., Hunt, A. G. & Shaw, J. G. ( 1994; ). Mutational analysis of the tobacco vein mottling virus genome. Virology 204, 759–769.[CrossRef]
    [Google Scholar]
  33. Kurath, G. & Dodds, J. A. ( 1995; ). Mutation analyses of molecularly cloned satellite tobacco mosaic virus during serial passage in plants: evidence for hotspots of genetic change. RNA 1, 491–500.
    [Google Scholar]
  34. Kurath, G. & Palukaitis, P. ( 1989; ). RNA sequence heterogeneity in natural populations of three satellite RNAs of cucumber mosaic virus. Virology 173, 231–240.[CrossRef]
    [Google Scholar]
  35. Liang, X.-Z., Lee, B. T. K. & Wong, S.-M. ( 2002; ). Covariation in the capsid protein of Hibiscus chlorotic ringspot virus induced by serial passaging in a host that restricts movement leads to avirulence in its systemic host. J Virol 76, 12320–12324.[CrossRef]
    [Google Scholar]
  36. Merits, A., Guo, D., Järvekülg, L. & Saarma, M. ( 1999; ). Biochemical and genetic evidence for interactions between potato A potyvirus-encoded proteins P1 and P3 and proteins of the putative replication complex. Virology 263, 15–22.[CrossRef]
    [Google Scholar]
  37. 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]
  38. Moya, A., Elena, S. F., Bracho, A., Mralles, R. & Barrio, E. ( 2000; ). The evolution of RNA viruses: a population genetics view. Proc Natl Acad Sci U S A 97, 6967–6973.[CrossRef]
    [Google Scholar]
  39. Muller, H. J. ( 1964; ). The relation of recombination to mutational advance. Mutat Res 106, 2–9.
    [Google Scholar]
  40. Nijhuis, M., Boucher, C. A. B., Schipper, P., Leitner, T., Schuurman, R. & Albert, J. ( 1998; ). Stochastic processes strongly influence HIV-1 evolution during suboptimal protease-inhibitor therapy. Proc Natl Acad Sci U S A 95, 14441–14446.[CrossRef]
    [Google Scholar]
  41. Novella, I. S. ( 2004; ). Negative effect of genetic bottlenecks on the adaptability of vesicular stomatitis virus. J Mol Biol 336, 61–67.[CrossRef]
    [Google Scholar]
  42. Ohshima, K., Yamaguchi, Y., Hirota, R. & 10 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]
  43. Provvidenti, R. ( 1996; ). Turnip mosaic potyvirus. In Viruses of Plants, pp. 1340–1343. Edited by A. A. Brunt, K. Crabtree, M. J. Dallwitz, A. J. Gibbs & L. Watson. Wallingford, UK: CAB International.
  44. 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]
  45. Rodríguez-Cerezo, E., Klein, P. G. & Shaw, J. G. ( 1991; ). A determinant of disease symptom severity is located in the 3′-terminal noncoding region of the RNA of a plant virus. Proc Natl Acad Sci U S A 88, 9863–9867.[CrossRef]
    [Google Scholar]
  46. Sacristán, S., Malpica, J. M., Fraile, A. & García-Arenal, F. ( 2003; ). Estimation of population bottlenecks during systemic movement of Tobacco mosaic virus in tobacco plants. J Virol 77, 9906–9911.[CrossRef]
    [Google Scholar]
  47. Sáenz, P., Cervera, M. T., Dallot, S., Quiot, L., Quiot, J.-B., Riechmann, J. L. & García, J. A. ( 2000; ). Identification of a pathogenicity determinant of Plum pox virus in the sequence encoding the C-terminal region of protein P3+6K1. J Gen Virol 81, 557–566.
    [Google Scholar]
  48. Sánchez, F., Martínez-Herrera, D., Aguilar, I. & Ponz, F. ( 1998; ). Infectivity of turnip mosaic potyvirus cDNA clones and transcripts on the systemic host Arabidopisis thaliana and local lesion hosts. Virus Res 55, 207–219.[CrossRef]
    [Google Scholar]
  49. Schneider, W. L. & Roossinck, M. J. ( 2000; ). Evolutionarily related Sindbis-like plant viruses maintain different levels of population diversity in a common host. J Virol 74, 3130–3134.[CrossRef]
    [Google Scholar]
  50. Schneider, W. L. & Roossinck, M. J. ( 2001; ). Genetic diversity in RNA virus quasispecies is controlled by host-virus interactions. J Virol 75, 6566–6571.[CrossRef]
    [Google Scholar]
  51. Shukla, D. D., Ward, C. W. & Brunt, A. A. ( 1994; ). The Potyviridae. Wallingford, UK: CAB International.
  52. Simón-Buela, L., Guo, H. S. & García, J. A. ( 1997; ). Long sequences in the 5′ noncoding region of plum pox virus are not necessary for viral infectivity but contribute to viral competitiveness and pathogenesis. Virology 233, 157–162.[CrossRef]
    [Google Scholar]
  53. Spetz, C. & Valkonen, J. P. T. ( 2004; ). Potyviral 6K2 protein long-distance movement and symptom-induction functions are independent and host-specific. Mol Plant Microbe Interact 17, 502–510.[CrossRef]
    [Google Scholar]
  54. 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]
  55. 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]
  56. 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]
  57. Tomimura, K., Špak, J., Katis, N., Jenner, C. E., Walsh, J. A., Gibbs, A. J. & Ohshima, K. ( 2004; ). Comparisons of the genetic structure of populations of Turnip mosaic virus in West and East Eurasia. Virology 330, 408–423.[CrossRef]
    [Google Scholar]
  58. Tomlinson, J. A. ( 1987; ). Epidemiology and control of virus diseases of vegetables. Ann Appl Biol 110, 661–681.[CrossRef]
    [Google Scholar]
  59. Ullah, Z. & Grumet, R. ( 2002; ). Localization of Zucchini yellow mosaic virus to the veinal regions and role of viral coat protein in veinal chlorosis conditioned by the zym potyvirus resistance locus in cucumber. Physiol Mol Plant Pathol 60, 79–89.[CrossRef]
    [Google Scholar]
  60. Urcuqui-Inchima, S., Haenni, A.-L. & Bernardi, F. ( 2001; ). Potyvirus proteins: a wealth of functions. Virus Res 74, 157–175.[CrossRef]
    [Google Scholar]
  61. Valli, P. J. S. & Goudsmit, J. ( 1998; ). Structured-tree topology and adaptive evolution of the simian immunodeficiency virus SIVsm envelope during serial passage in rhesus macaques according to likelihood mapping and quartet puzzling. J Virol 72, 3673–3683.
    [Google Scholar]
  62. van Regenmortel, M. H. V., Fauquet, C. M., Bishop, D. H. L. & 8 other editors ( 2000; ). Virus Taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses. San Diego: Academic Press.
  63. 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]
  64. 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]
  65. Wichman, H. A., Badgett, M. R., Scott, L. A., Boulianne, C. M. & Bull, J. J. ( 1999; ). Different trajectories of parallel evolution during viral adaptation. Science 285, 422–424.[CrossRef]
    [Google Scholar]
  66. Yuste, E., Sánchez-Palomino, S., Casado, C., Domingo, E. & López-Galíndez, C. ( 1999; ). Drastic fitness loss in human immunodeficiency virus type 1 upon serial bottleneck events. J Virol 73, 2745–2751.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80540-0
Loading
/content/journal/jgv/10.1099/vir.0.80540-0
Loading

Data & Media loading...

Supplements

vol. , part 2, pp. 501 – 510

GenBank accession numbers of parents/variants [PDF file](81 KB)



PDF

Most Cited This Month

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