1887

Abstract

Since their introduction in south-eastern France around 1999, new, ‘emerging’ (EM) strains of watermelon mosaic virus (WMV) coexist with the ‘classic’ (CL) strains present for more than 40 years. This situation constitutes a unique opportunity to estimate the frequency of recombinants appearing in the few years following introduction of new strains of a plant RNA virus. Molecular analyses performed on more than 1000 isolates from epidemiological surveys (2004–2008) and from experimental plots (2009–2010), and targeting only recombinants that became predominant in at least one plant, revealed at least seven independent CL/EM or EM/EM recombination events. The frequency of recombinants involving at least one EM parent in the natural populations tested was on the order of 1 %. No new recombinant was detected for more than 1 year, and none but one in more than one location. In tests comparing host range and aphid transmissibility, the new recombinants did not display a better fitness than their ‘parental’ isolates. No recombinant was detected from artificial mixed infections of CL and EM isolates of various hosts after testing more than 1500 subcultures obtained after single-aphid transmission. These results constitute one of the first estimations of the frequency of recombinants in natural conditions for a plant RNA virus. This suggests that although viable recombinants of WMV are not rare, and although recombination may potentially lead to new highly damaging strains, the new recombinants observed so far had a lower fitness than the parental strains and did not emerge durably in the populations.

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2011-08-01
2024-04-26
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References

  1. Aaziz R., Tepfer M. 1999; Recombination between genomic RNAs of two cucumoviruses under conditions of minimal selection pressure. Virology 263:282–289 [View Article][PubMed]
    [Google Scholar]
  2. Andersen K., Johansen I. E. 1998; A single conserved amino acid in the coat protein gene of pea seed-borne mosaic potyvirus modulates the ability of the virus to move systemically in Chenopodium quinoa. Virology 241:304–311 [View Article][PubMed]
    [Google Scholar]
  3. Atreya P. L., Atreya C. D., Pirone T. P. 1991; Amino acid substitutions in the coat protein result in loss of insect transmissibility of a plant virus. Proc Natl Acad Sci U S A 88:7887–7891 [View Article][PubMed]
    [Google Scholar]
  4. 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 [View Article][PubMed]
    [Google Scholar]
  5. Chare E. R., Holmes E. C. 2006; A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151:933–946 [View Article][PubMed]
    [Google Scholar]
  6. Desbiez C., Lecoq H. 2004; The nucleotide sequence of Watermelon mosaic virus (WMV, Potyvirus) reveals interspecific recombination between two related potyviruses in the 5′ part of the genome. Arch Virol 149:1619–1632 [View Article][PubMed]
    [Google Scholar]
  7. Desbiez C., Lecoq H. 2008; Evidence for multiple intraspecific recombinants in natural populations of Watermelon mosaic virus (WMV, Potyvirus). Arch Virol 153:1749–1754 [View Article][PubMed]
    [Google Scholar]
  8. Desbiez C., Costa C., Wipf-Scheibel C., Girard M., Lecoq H. 2007; Serological and molecular variability of watermelon mosaic virus (genus Potyvirus). Arch Virol 152:775–781 [View Article][PubMed]
    [Google Scholar]
  9. Desbiez C., Joannon B., Wipf-Scheibel C., Chandeysson C., Lecoq H. 2009; Emergence of new strains of Watermelon mosaic virus in South-eastern France: evidence for limited spread but rapid local population shift. Virus Res 141:201–208 [View Article][PubMed]
    [Google Scholar]
  10. de Wispelaere M., Gaubert S., Trouilloud S., Belin C., Tepfer M. 2005; A map of the diversity of RNA3 recombinants appearing in plants infected with Cucumber mosaic virus and Tomato aspermy virus.. Virology 331:117–127 [View Article][PubMed]
    [Google Scholar]
  11. Dietrich C., Maiss E. 2003; Fluorescent labelling reveals spatial separation of potyvirus populations in mixed infected Nicotiana benthamiana plants. J Gen Virol 84:2871–2876 [View Article][PubMed]
    [Google Scholar]
  12. Dietrich C., Al Abdallah Q., Lintl L., Pietruszka A., Maiss E. 2007a; A chimeric plum pox virus shows reduced spread and cannot compete with its parental wild-type viruses in a mixed infection. J Gen Virol 88:2846–2851 [View Article][PubMed]
    [Google Scholar]
  13. Dietrich C., Miller J., McKenzie G., Palkovics L., Balázs E., Palukaitis P., Maiss E. 2007b; No recombination detected in artificial potyvirus mixed infections and between potyvirus derived transgenes and heterologous challenging potyviruses. Environ Biosafety Res 6:207–218 [View Article][PubMed]
    [Google Scholar]
  14. Fabre F., Chadoeuf J., Costa C., Lecoq H., Desbiez C. 2010; Asymmetrical over-infection as a process of plant virus emergence. J Theor Biol 265:377–388 [View Article][PubMed]
    [Google Scholar]
  15. Froissart R., Roze D., Uzest M., Galibert L., Blanc S., Michalakis Y. 2005; Recombination every day: abundant recombination in a virus during a single multi-cellular host infection. PLoS Biol 3:e89 [View Article][PubMed]
    [Google Scholar]
  16. Gal-On A., Meiri E., Raccah B., Gaba V. 1998; Recombination of engineered defective RNA species produces infective potyvirus in planta.. J Virol 72:5268–5270[PubMed]
    [Google Scholar]
  17. García-Andrés S., Monci F., Navas-Castillo J., Moriones E. 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 [View Article][PubMed]
    [Google Scholar]
  18. García-Andrés S., Accotto G. P., Navas-Castillo J., Moriones E. 2007a; Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the Mediterranean basin. Virology 359:302–312 [View Article][PubMed]
    [Google Scholar]
  19. García-Andrés S., Tomás D. M., Sánchez-Campos S., Navas-Castillo J., Moriones E. 2007b; Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology 365:210–219 [View Article][PubMed]
    [Google Scholar]
  20. Glais L., Tribodet M., Kerlan C. 2002; Genomic variability in Potato potyvirus Y (PVY): evidence that PVY(N)W and PVY(NTN) variants are single to multiple recombinants between PVY(O) and PVY(N) isolates. Arch Virol 147:363–378 [View Article][PubMed]
    [Google Scholar]
  21. Glasa M., Palkovics L., Komínek P., Labonne G., Pittnerová S., Kúdela O., Candresse T., Subr Z. 2004; Geographically and temporally distant natural recombinant isolates of Plum pox virus (PPV) are genetically very similar and form a unique PPV subgroup. J Gen Virol 85:2671–2681 [View Article][PubMed]
    [Google Scholar]
  22. Jaag H. M., Nagy P. D. 2010; The combined effect of environmental and host factors on the emergence of viral RNA recombinants. PLoS Pathog 6:e1001156 [View Article][PubMed]
    [Google Scholar]
  23. Joannon B., Lavigne C., Lecoq H., Desbiez C. 2010; Barriers to gene flow between emerging populations of Watermelon mosaic virus in Southeastern France. Phytopathology 100:1373–1379 [View Article][PubMed]
    [Google Scholar]
  24. Kosakovsky Pond S. L., Posada D., Gravenor M. B., Woelk C. H., Frost S. D. W. 2006; Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23:1891–1901 [View Article][PubMed]
    [Google Scholar]
  25. Kumar S., Tamura K., Nei M. 2004; mega3: Integrated software for Molecular Evolutionary Genetic Analysis and sequence alignment. Brief Inform 5:150–163
    [Google Scholar]
  26. Larsen R. C., Miklas P. N., Druffel K. L., Wyatt S. D. 2005; NL-3 K strain is a stable and naturally occurring interspecific recombinant derived from Bean common mosaic necrosis virus and Bean common mosaic virus. Phytopathology 95:1037–1042 [View Article][PubMed]
    [Google Scholar]
  27. Lecoq H., Fabre F., Joannon B., Wipf-Scheibel C., Chandeysson C., Schoeny A., Desbiez C. 2011; Search for factors involved in the rapid shift in Watermelon mosaic virus (WMV) populations in south-eastern France. Virus Res (in press) [View Article]
    [Google Scholar]
  28. Lefeuvre P., Lett J.-M., Varsani A., Martin D. P. 2009; Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83:2697–2707 [View Article][PubMed]
    [Google Scholar]
  29. Martin D. P., Williamson C., Posada D. 2005; RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262 [View Article][PubMed]
    [Google Scholar]
  30. Mbanzibwa D. R., Tian Y., Mukasa S. B., Valkonen J. P. T. 2009; Cassava brown streak virus (Potyviridae) encodes a putative Maf/HAM1 pyrophosphatase implicated in reduction of mutations and a P1 proteinase that suppresses RNA silencing but contains no HC-Pro. J Virol 83:6934–6940 [View Article][PubMed]
    [Google Scholar]
  31. 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 [View Article][PubMed]
    [Google Scholar]
  32. Morilla G., Krenz B., Jeske H., Bejarano E. R., Wege C. 2004; Tête à tête of Tomato yellow leaf curl virus and Tomato yellow leaf curl sardinia virus in single nuclei. J Virol 78:10715–10723 [View Article][PubMed]
    [Google Scholar]
  33. Moury B., Desbiez C., Jacquemond M., Lecoq H. 2006; Genetic diversity of plant virus populations: towards hypothesis testing in molecular epidemiology. Adv Virus Res 67:49–87 [View Article][PubMed]
    [Google Scholar]
  34. Ohshima K., Tomitaka Y., Wood J. T., Minematsu Y., Kajiyama H., Tomimura K., Gibbs A. J. 2007; Patterns of recombination in Turnip mosaic virus genomic sequences indicate hotspots of recombination. J Gen Virol 88:298–315 [View Article][PubMed]
    [Google Scholar]
  35. Paalme V., Gammelgård E., Järvekülg L., Valkonen J. P. T. 2004; In vitro recombinants of two nearly identical potyviral isolates express novel virulence and symptom phenotypes in plants. J Gen Virol 85:739–747 [View Article][PubMed]
    [Google Scholar]
  36. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225 [View Article][PubMed]
    [Google Scholar]
  37. Pierrugues O., Guilbaud L., Fernandez-Delmond I., Fabre F., Tepfer M., Jacquemond M. 2007; Biological properties and relative fitness of inter-subgroup cucumber mosaic virus RNA 3 recombinants produced in vitro. J Gen Virol 88:2852–2861 [View Article][PubMed]
    [Google Scholar]
  38. Ray S. C. 1998; SimPlot for Windows (version 1.6). Baltimore, Md. Distributed by author. http://sray.med.som.jhmi.edu/SCRoftware/Simplot
    [Google Scholar]
  39. Revers F., Le Gall O., Candresse T., Le Romancer M., Dunez J. 1996; Frequent occurrence of recombinant potyvirus isolates. J Gen Virol 77:1953–1965 [View Article][PubMed]
    [Google Scholar]
  40. Susaimuthu J., Tzanetakis I. E., Gergerich R. C., Martin R. R. 2008; A member of a new genus in the Potyviridae infects Rubus. Virus Res 131:145–151 [View Article][PubMed]
    [Google Scholar]
  41. 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 [View Article][PubMed]
    [Google Scholar]
  42. Valli A., López-Moya J.-J., García J. A. 2007; Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae.. J Gen Virol 88:1016–1028 [View Article][PubMed]
    [Google Scholar]
  43. van der Walt E., Rybicki E. P., Varsani A., Polston J. E., Billharz R., Donaldson L., Monjane A. L., Martin D. P. 2009; Rapid host adaptation by extensive recombination. J Gen Virol 90:734–746 [View Article][PubMed]
    [Google Scholar]
  44. Vincelli P., Seebold K. 2009; Report of a Watermelon mosaic potyvirus strain in Kentucky undetected by ELISA. Plant Health Prog [View Article]
    [Google Scholar]
  45. Xia X. 2000 Data analysis in Molecular Biology and Evolution Boston, Dordrecht, London: Kluwer Academic Publishers;
    [Google Scholar]
  46. Zhou X., Liu Y., Calvert L., Munoz C., Otim-Nape G. W., Robinson D. J., Harrison B. D. 1997; Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J Gen Virol 78:2101–2111[PubMed]
    [Google Scholar]
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