Recombination in single-stranded RNA viruses is one of the principal mechanisms responsible for their evolution. Here we show, using a variety of different methods, that the 3′ untranslated region (3′UTR) of subgroup II strains of cucumber mosaic virus [CMV(II)] is related more closely to that of tomato aspermy virus (TAV) than to those of CMV(I) strains. These results suggest that the CMV(II) 3′UTR arose by interspecific CMV/TAV recombination. The putative crossover is close to the 5′ end of the 3′UTR, at a recombination hot spot previously observed in short time-frame experiments. The CMV(II) strains show divergence from TAV at specific points along the 3′UTR that most probably indicate adaptive changes due to natural selection. Thus, for the large majority of CMV(II) strains examined, the 3′UTR has two discrete regions, W (nt 1902–1971) and Y (nt 2126–2184), that are more similar to the corresponding regions of TAV than to those of CMV(I) strains.


Article metrics loading...

Loading full text...

Full text loading...



  1. Aaziz, R. & Tepfer, M.(1999). Recombination between genomic RNAs of two cucumoviruses under conditions of minimal selection pressure. Virology 263, 282–289.[CrossRef] [Google Scholar]
  2. Blanchard, C. L., Higgins, T. J. & Anderson, B. J.(1997). RNAs 4A and 5 are present in tomato aspermy virus and both subgroups of cucumber mosaic virus. Arch Virol 142, 1273–1283.[CrossRef] [Google Scholar]
  3. Bonnet, J., Fraile, A., Sacristan, S., Malpica, J. M. & Garcia-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.[CrossRef] [Google Scholar]
  4. Burnham, K. P. & Anderson, D.(2003).Model Selection and Multimodel Inference, 2nd edn. New York: Springer.
  5. Chen, Y. K., Goldbach, R. & Prins, M.(2002). Inter- and intramolecular recombinations in the cucumber mosaic virus genome related to adaptation to Alstroemeria. J Virol 76, 4119–4124.[CrossRef] [Google Scholar]
  6. Cheng, C. P., Jaag, H. M., Jonczyk, M., Serviene, E. & Nagy, P. D.(2007). Expression of the Arabidopsis Xrn4p 5′–3′ exoribonuclease facilitates degradation of tombusvirus RNA and promotes rapid emergence of viral variants in plants. Virology 368, 238–248.[CrossRef] [Google Scholar]
  7. Codoñer, F. M. & Elena, S. F.(2008). The promiscuous evolutionary history of the family Bromoviridae. J Gen Virol 89, 1739–1747.[CrossRef] [Google Scholar]
  8. de Wispelaere, M. & Rao, A. L. N.(2008). Production of cucumber mosaic virus RNA5 and its role in recombination. Virology 384, 179–191. [Google Scholar]
  9. 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.[CrossRef] [Google Scholar]
  10. Drake, J. W. & Holland, J. J.(1999). Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96, 13910–13913.[CrossRef] [Google Scholar]
  11. Fernandez-Cuartero, B., Burgyan, J., Aranda, M. A., Salanki, K., Moriones, E. & Garcia-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]
  12. Fraile, A., Alonso-Prados, J. L., Aranda, M. A., Bernal, J. J., Malpica, J. M. & Garcia-Arenal, F.(1997). Genetic exchange by recombination or reassortment is infrequent in natural populations of a tripartite RNA plant virus. J Virol 71, 934–940. [Google Scholar]
  13. Garcia-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. Kiss, L., Sebestyen, E., Laszlo, E., Salamon, P., Balazs, E. & Salanki, K.(2008). Nucleotide sequence analysis of peanut stunt virus Rp strain suggests the role of homologous recombination in cucumovirus evolution. Arch Virol 153, 1373–1377.[CrossRef] [Google Scholar]
  15. Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H. & Frost, S. D.(2006).gard: a genetic algorithm for recombination detection. Bioinformatics 22, 3096–3098.[CrossRef] [Google Scholar]
  16. Lin, H. X., Rubio, L., Smythe, A. B. & Falk, B. W.(2004). Molecular population genetics of Cucumber mosaic virus in California: evidence for founder effects and reassortment. J Virol 78, 6666–6675.[CrossRef] [Google Scholar]
  17. Martin, D. P., Williamson, C. & Posada, D.(2005).rdp2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef] [Google Scholar]
  18. Martinez, H. M., Maizel, J. V., Jr & Shapiro, B. A.(2008).rna2d3d: a program for generating, viewing, and comparing 3-dimensional models of RNA. J Biomol Struct Dyn 25, 669–683.[CrossRef] [Google Scholar]
  19. Miller, W. A. & Koev, G.(1998). Getting a handle on RNA virus recombination. Trends Microbiol 6, 421–423.[CrossRef] [Google Scholar]
  20. Morroni, M., Thompson, J. R. & Tepfer, M.(2009). Analysis of recombination between viral RNAs and transgene mRNA under conditions of high selection pressure in favour of recombinants. J Gen Virol (in press). doi:10.1099/vir.0.013771-0. [Google Scholar]
  21. Palukaitis, P. & Garcia-Arenal, F.(2003). Cucumoviruses. Adv Virus Res 62, 241–323. [Google Scholar]
  22. Palukaitis, P., Roossinck, M. J., Dietzgen, R. G. & Francki, R. I.(1992). Cucumber mosaic virus. Adv Virus Res 41, 281–348. [Google Scholar]
  23. 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.[CrossRef] [Google Scholar]
  24. Posada, D. & Crandall, K. A.(1998).modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef] [Google Scholar]
  25. Roossinck, M. J.(2002). Evolutionary history of Cucumber mosaic virus deduced by phylogenetic analyses. J Virol 76, 3382–3387.[CrossRef] [Google Scholar]
  26. Roossinck, M. J., Kaplan, I. & Palukaitis, P.(1997). Support of a cucumber mosaic virus satellite RNA maps to a single amino acid proximal to the helicase domain of the helper virus. J Virol 71, 608–612. [Google Scholar]
  27. Shi, B., Ding, S. & Symons, R. H.(1997). Two novel subgenomic RNAs derived from RNA 3 of tomato aspermy cucumovirus. J Gen Virol 78, 505–510. [Google Scholar]
  28. Swofford, D. L.(1998).paup*: phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA: Sinauer Associates.
  29. Thompson, J. R., Buratti, E., de Wispelaere, M. & Tepfer, M.(2008). Structural and functional characterization of the 5′ region of subgenomic RNA5 of cucumber mosaic virus. J Gen Virol 89, 1729–1738.[CrossRef] [Google Scholar]
  30. Turturo, C., Friscina, A., Gaubert, S., Jacquemond, M., Thompson, J. R. & Tepfer, M.(2008). Evaluation of potential risks associated with recombination in transgenic plants expressing viral sequences. J Gen Virol 89, 327–335.[CrossRef] [Google Scholar]
  31. Valli, A., Lopez-Moya, J. J. & Garcia, J. A.(2007). Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. J Gen Virol 88, 1016–1028.[CrossRef] [Google Scholar]
  32. Xayaphoummine, A., Bucher, T. & Isambert, H.(2005). Kinefold web server for RNA/DNA folding path and structure prediction including pseudoknots and knots. Nucleic Acids Res 33, W605–W610.[CrossRef] [Google Scholar]

Data & Media loading...


[ Single PDF file] (178 KB)


[ Single PDF file] (177 KB)

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