1887

Abstract

The prevalence of necrotic potato virus Y (PVY) in natural populations could reflect increased fitness of necrotic isolates. In this paper, the effects of the acquisition of molecular determinants (A/G and A/C) involved in necrosis capacity on both the number of progeny produced and the competitiveness of PVY were characterized. The relationship between necrosis and fitness was tested using (i) cv. Xanthi and , (ii) necrotic PVY-605 and non-necrotic PVY-139 isolates, (iii) single-mutated (PVY and PVY) and double-mutated (PVY) versions of PVY-605 and (iv) three quantitative PCR assays specific for nt A, G and A of the PVY genome. The data demonstrated effects of both the genetic background and nt 2213 and 2271 on the fitness of PVY. Quantification of PVY RNA in singly infected plants revealed that both the PVY-605 genetic background and the acquisition of necrotic capacity resulted in a decrease in the number of progeny produced. Competition experiments revealed that the genetic background of PVY had a positive impact on competitiveness. In contrast, nucleotides involved in necrotic properties were associated with decreased fitness. Finally, in the host that did not respond to infection with necrosis, the benefit associated with the PVY-605 genetic background was higher than the cost associated with the acquisition of molecular determinants involved in necrosis capacity. The opposite result was obtained in the host responding to the infection with necrosis. These results indicate that the emergence of necrotic isolates from a non-necrotic population is unlikely in tobacco.

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2009-01-01
2019-11-21
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References

  1. Aaziz, R. & Tepfer, M. ( 1999; ). Recombination in RNA viruses and in virus-resistant transgenic plants. J Gen Virol 80, 1339–1346.
    [Google Scholar]
  2. Balme-Sinibaldi, V., Tribodet, M., Croizat, F., Lefeuvre, P., Kerlan, C. & Jacquot, E. ( 2006; ). Improvement of Potato virus Y (PVY) detection and quantitation using PVYN- and PVYO-specific real-time RT-PCR assays. J Virol Methods 134, 261–266.[CrossRef]
    [Google Scholar]
  3. Banik, M. T. & Zitter, T. A. ( 1990; ). Determination of cucumber mosaic virus titer in muskmelon by enzyme-linked immunosorbent assay and correlation with aphid transmission. Plant Dis 74, 857–859.[CrossRef]
    [Google Scholar]
  4. Carrasco, P., Daros, J. A., Agudelo-Romero, P. & Elena, S. F. ( 2007a; ). A real-time RT-PCR assay for quantifying the fitness of tobacco etch virus in competition experiments. J Virol Methods 139, 181–188.[CrossRef]
    [Google Scholar]
  5. Carrasco, P., de la Iglesia, F. & Elena, S. F. ( 2007b; ). Distribution of fitness and virulence effects caused by single-nucleotide substitutions in tobacco etch virus. J Virol 81, 12979–12984.[CrossRef]
    [Google Scholar]
  6. Cecchini, E., Gong, Z., Geri, C., Covey, S. N. & Milner, J. J. ( 1997; ). Transgenic Arabidopsis lines expressing gene VI from cauliflower mosaic virus variants exhibit a range of symptom-like phenotypes and accumulate inclusion bodies. Mol Plant Microbe Interact 10, 1094–1101.[CrossRef]
    [Google Scholar]
  7. Cerovska, N. ( 1998; ). Production of monoclonal antibodies to potato virus YNTN strain and their use for strain differentiation. Plant Pathol 47, 505–509.[CrossRef]
    [Google Scholar]
  8. Chao, L. ( 1990; ). Fitness of RNA virus decreased by Muller's ratchet. Nature 348, 454–455.[CrossRef]
    [Google Scholar]
  9. Chrzanowska, M. ( 1991; ). New isolates of the necrotic strain of potato virus Y (PVYN) found recently in Poland. Potato Res 34, 179–182.[CrossRef]
    [Google Scholar]
  10. Chrzanowska, M. ( 1994; ). Differentiation of potato virus Y (PVY) isolates. Phytopathologica Polonica 8, 15–20.
    [Google Scholar]
  11. Chung, B. Y. W., Miller, W. A., Atkins, J. F. & Firth, A. E. ( 2008; ). An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci U S A 105, 5897–5902.[CrossRef]
    [Google Scholar]
  12. Crosslin, J. M., Hamm, P. B., Hane, D. C., Jaeger, J., Brown, C. R., Shiel, P. J., Berger, P. H. & Thornton, R. E. ( 2006; ). The occurrence of PVYO, PVYN, and PVYN : O strains of Potato virus Y in certified potato seed lot trials in Washington and Oregon. Plant Dis 90, 1102–1105.[CrossRef]
    [Google Scholar]
  13. Dedic, P., Ptacek, J. & Cerovska, N. (2007). A shift of PVY strain spectrum on potatoes in CR in the course of past years. In The 13th EAPR Virology Section Meeting, p. 59. Coylumbridge, Aviemore, Scotland, UK.
  14. Domingo, E. & Holland, J. J. ( 1997; ). RNA virus mutations and fitness for survival. Annu Rev Microbiol 51, 151–178.[CrossRef]
    [Google Scholar]
  15. Dougherty, W. G. & Carrington, J. C. ( 1988; ). Expression and function of potyviral gene products. Annu Rev Phytopathol 26, 123–143.[CrossRef]
    [Google Scholar]
  16. 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]
  17. 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]
  18. Fernández-Cuartero, B., Burgyán, J., Aranda, M. A., Salanki, K., Moriones, E. & García-Arenal, F. ( 1994; ). Increase in the relative fitness of a plant virus RNA associated with its recombinant nature. Virology 203, 373–377.[CrossRef]
    [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. Glais, L., Tribodet, M. & Kerlan, C. ( 2005; ). Specific detection of the PVYN-W variant of Potato virus Y. J Virol Methods 125, 131–136.[CrossRef]
    [Google Scholar]
  21. Gray, S. M., Power, A. G., Smith, D. M., Seaman, A. J. & Altman, N. S. ( 1991; ). Aphid transmission of barley yellow dwarf virus: acquisition access periods and virus concentration requirements. Phytopathology 81, 539–545.[CrossRef]
    [Google Scholar]
  22. Herrera, M., García-Arriaza, J., Pariente, N., Escarmis, C. & Domingo, E. ( 2007; ). Molecular basis for a lack of correlation between viral fitness and cell killing capacity. PLoS Pathog 3, e53 [CrossRef]
    [Google Scholar]
  23. Hirata, H., Lu, X., Yamaji, Y., Kagiwada, S., Ugaki, M. & Namba, S. ( 2003; ). A single silent substitution in the genome of Apple stem grooving virus causes symptom attenuation. J Gen Virol 84, 2579–2583.[CrossRef]
    [Google Scholar]
  24. Holland, J. J., de la Torre, J. C., Clarke, D. K. & Duarte, E. ( 1991; ). Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol 65, 2960–2967.
    [Google Scholar]
  25. Jacquot, E., Tribodet, M., Croizat, F., Balme-Sinibaldi, V. & Kerlan, C. ( 2005; ). A single nucleotide polymorphism-based technique for specific characterization of YO and YN isolates of Potato virus Y (PVY). J Virol Methods 125, 83–93.[CrossRef]
    [Google Scholar]
  26. Jakab, G., Droz, E., Brigneti, G., Baulcombe, D. & Malnoe, P. ( 1997; ). Infectious in vivo and in vitro transcripts from a full-length cDNA clone of PVY-N605, a Swiss necrotic isolate of potato virus Y. J Gen Virol 78, 3141–3145.
    [Google Scholar]
  27. Jones, R. A. C. ( 1990; ). Strain group specific and virus specific hypersensitive reactions to infection with potyviruses in potato cultivars. Ann Appl Biol 117, 93–105.[CrossRef]
    [Google Scholar]
  28. Kogovsek, P., Gow, L., Pompe-Novak, M., Gruden, K., Foster, G. D., Boonham, N. & Ravnikar, M. ( 2008; ). Single-step RT real-time PCR for sensitive detection and discrimination of Potato virus Y isolates. J Virol Methods 149, 1–11.[CrossRef]
    [Google Scholar]
  29. Kong, Q., Oh, J. & Simon, A. E. ( 1995; ). Symptom attenuation by a normally virulent satellite RNA of turnip crinkle virus is associated with the coat protein open reading frame. Plant Cell 7, 1625–1634.[CrossRef]
    [Google Scholar]
  30. Lindner, K. & Billenkamp, N. ( 2005; ). Changes in the spectrum of PVY strains and strain groups: could this be a cause for the increase of virus susceptibility of potato and tobacco varieties? Nachrichtenblatt des Deutschen Pflanzenschutzdienstes 57, 245–253.
    [Google Scholar]
  31. Lorenzen, J., Nolte, P., Martin, D., Pasche, J. & Gudmestad, N. ( 2008; ). NE-11 represents a new strain variant class of Potato virus Y. Arch Virol 153, 517–525.[CrossRef]
    [Google Scholar]
  32. Milne, R. G. ( 1988; ). The Filamentous Plant Viruses. In The Plant Viruses, pp. 331–407. Edited by H. Fraenkel-Conrat & R. R. Wagner. New York & London: Plenum Press.
  33. Moreno, I. M., Malpica, J. M., Rodríguez-Cerezo, E. & García-Arenal, F. ( 1997; ). A mutation in tomato aspermy cucumovirus that abolishes cell-to-cell movement is maintained to high levels in the viral RNA population by complementation. J Virol 71, 9157–9162.
    [Google Scholar]
  34. Moury, B., Fabre, F. & Senoussi, R. ( 2007; ). Estimation of the number of virus particles transmitted by an insect vector. Proc Natl Acad Sci U S A 104, 17891–17896.[CrossRef]
    [Google Scholar]
  35. Ounouna, H., Kerlan, C., Lafaye, P., Loukili, M. J. & ElGaaied, A. ( 2002; ). Production of monoclonal antibodies against synthetic peptides of the N-terminal region of Potato virus Y coat protein and their use in PVY strain differentiation. Plant Pathol 51, 487–494.[CrossRef]
    [Google Scholar]
  36. Piche, L. M., Singh, R. P., Nie, X. & Gudmestad, N. C. ( 2004; ). Diversity among Potato virus Y isolates obtained from potatoes grown in the United States. Phytopathology 94, 1368–1375.[CrossRef]
    [Google Scholar]
  37. Pirone, T. P. & Thornbury, D. W. ( 1988; ). Quantity of virus required for aphid transmission of a potyvirus. Phytopathology 78, 104–107.[CrossRef]
    [Google Scholar]
  38. Rigden, J. E., Krake, L. R., Rezaian, M. A. & Dry, I. B. ( 1994; ). ORF C4 of tomato leaf curl geminivirus is a determinant of symptom severity. Virology 204, 847–850.[CrossRef]
    [Google Scholar]
  39. Rolland, M., Tribodet, M., Glais, L., Kerlan, C. & Jacquot, E. ( 2007; ). Impact of acquisition of necrosis properties on the Potato Virus Y fitness. In The 13th EAPR Virology Section Meeting, p. 19. Coylumbridge, Aviemore, Scotland, UK.
  40. Rolland, M., Glais, L., Kerlan, C. & Jacquot, E. ( 2008; ). A multiple single nucleotide polymorphisms interrogation assay for reliable Potato virus Y group and variant characterization. J Virol Methods 147, 108–117.[CrossRef]
    [Google Scholar]
  41. Rolot, J. L. ( 2007; ). Balance between PVYN and PVYO strains in Belgium: first approaches. In The 13th EAPR Virology Section Meeting, p. 70. Coylumbridge, Aviemore, Scotland, UK.
  42. Rose, D. G. & Hubbard, A. L. ( 1986; ). Production of monoclonal antibodies for the detection of potato virus Y. Ann Appl Biol 109, 317–321.[CrossRef]
    [Google Scholar]
  43. Schubert, J., Fomitcheva, V. & Sztangret-Wisniewska, J. ( 2007; ). Differentiation of Potato virus Y strains using improved sets of diagnostic PCR-primers. J Virol Methods 140, 66–74.[CrossRef]
    [Google Scholar]
  44. Shukla, D. D., Ward, C. W. & Brunt, A. A. ( 1994; ). The Potyviridae. Wallingford, UK: CAB International.
  45. Singh, M. & Singh, R. P. ( 1996; ). Nucleotide sequence and genome organization of a Canadian isolate of the common strain of potato virus Y (PVYO). Can J Plant Pathol 18, 209–224.[CrossRef]
    [Google Scholar]
  46. Singh, R. P., Valkonen, J. P. T., Gray, S. M., Boonham, N., Jones, R. A. C., Kerlan, C. & Schubert, J. ( 2008; ). Discussion paper: the naming of Potato virus Y strains infecting potato. Arch Virol 153, 1–13.[CrossRef]
    [Google Scholar]
  47. Smith, K. M. ( 1931; ). On the composite nature of certain potato virus diseases of the mosaic group as revealed by the use of plant indicators and selective methods of transmission. Proc R Soc Lond B Biol Sci 109, 251–267.[CrossRef]
    [Google Scholar]
  48. Tribodet, M., Glais, L., Kerlan, C. & Jacquot, E. ( 2005; ). Characterization of Potato virus Y (PVY) molecular determinants involved in the vein necrosis symptom induced by PVYN isolates in infected Nicotiana tabacum cv. Xanthi. J Gen Virol 86, 2101–2105.[CrossRef]
    [Google Scholar]
  49. Uzest, M., Gargani, D., Drucker, M., Hebrard, E., Garzo, E., Candresse, T., Fereres, A. & Blanc, S. ( 2007; ). A protein key to plant virus transmission at the tip of the insect vector stylet. Proc Natl Acad Sci U S A 104, 17959–17964.[CrossRef]
    [Google Scholar]
  50. Valkonen, J. P. T. ( 1997; ). Novel resistances to four potyviruses in tuber-bearing potato species, and temperature-sensitive expression of hypersensitive resistance to potato virus Y. Ann Appl Biol 130, 91–104.[CrossRef]
    [Google Scholar]
  51. Van der Vlugt, R. A. A., Verbeek, M., Cuperus, C. & Piron, P. ( 2007; ). Strains of Potato virus Y in Dutch seed potato culture. In The 13th EAPR Virology Section Meeting, p. 44. Coylumbridge, Aviemore, Scotland, UK.
  52. Van der Vossen, E. A. G., Neeleman, L. & Bol, J. F. ( 1996; ). The 5′ terminal sequence of alfalfa mosaic virus RNA 3 is dispensable for replication and contains a determinant for symptom formation. Virology 221, 271–280.[CrossRef]
    [Google Scholar]
  53. Van Maarseveen, N. M., Huigen, M. C. D. G., de Jong, D., Smits, A. M., Boucher, C. A. B. & Nijhuis, M. ( 2006; ). A novel real-time PCR assay to determine relative replication capacity for HIV-1 protease variants and/or reverse transcriptase variants. J Virol Methods 133, 185–194.[CrossRef]
    [Google Scholar]
  54. Weber, J., Rangel, H. R., Chakraborty, B., Tadele, M., Martinez, M. A., Martinez-Picado, J., Marotta, M. L., Mirza, M., Ruiz, L. & other authors ( 2003; ). A novel TaqMan real-time PCR assay to estimate ex vivo human immunodeficiency virus type 1 fitness in the era of multi-target (pol and env) antiretroviral therapy. J Gen Virol 84, 2217–2228.[CrossRef]
    [Google Scholar]
  55. Weidemann, H. L. & Maiss, E. ( 1996; ). Detection of the potato tuber necrotic ringspot strain of potato virus Y (PVYNTN) by reverse transcription and immunocapture polymerase chain reaction. Z Pflanzenkr Pflanzenschutz 103, 337–345.
    [Google Scholar]
  56. Zhang, L., Hanada, K. & Palukaitis, P. ( 1994; ). Mapping local and systemic symptom determinants of cucumber mosaic cucumovirus in tobacco. J Gen Virol 75, 3185–3191.[CrossRef]
    [Google Scholar]
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