Archives of Virology

, Volume 151, Issue 5, pp 933–946 | Cite as

A phylogenetic survey of recombination frequency in plant RNA viruses

  • E. R. Chare
  • E. C. Holmes


The severe economic consequences of emerging plant viruses highlights the importance of studies of plant virus evolution. One question of particular relevance is the extent to which the genomes of plant viruses are shaped by recombination. To this end we conducted a phylogenetic survey of recombination frequency in a wide range of positive-sense RNA plant viruses, utilizing 975 capsid gene sequences and 157 complete genome sequences. In total, 12 of the 36 RNA virus species analyzed showed evidence for recombination, comprising 17% of the capsid gene sequence alignments and 44% of the genome sequence alignments. Given the conservative nature of our analysis, we propose that recombination is a relatively common process in some plant RNA viruses, most notably the potyviruses.


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  1. Aaziz, R, Tepfer, M 1999Recombination in RNA viruses and in virus-resistant transgenic plantsJ Gen Virol8013391346PubMedGoogle Scholar
  2. Allison, RF, Schneider, WL, Greene, AE 1996Recombination in plants expressing viral transgenesSemin Virol7417422CrossRefGoogle Scholar
  3. Blok J, Gibbs AJ (1995) Molecular systematics of the flaviviruses and their relatives. In: Gibbs AJ, Calisher CH, Garcia-Arenal F (eds), Molecular basis of virus evolution. Cambridge University Press, Cambridge, pp 270–289Google Scholar
  4. Bonnet, J, Fraile, A, Sacristan, S, Malpica, JM, Garcia-Arenal, F 2005Role of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virusVirology332359368CrossRefPubMedGoogle Scholar
  5. Bousalem, M, Dallot, S, Fuji, S, Natsuaki, KT 2003Origin, world-wide dispersion, bio-geographical diversification, radiation and recombination: an evolutionary history of the Yam mild mosaic virus (YMMV)Infect Genet Evol3189206CrossRefPubMedGoogle Scholar
  6. Bousalem, M, Douzery, EJP, Fargette, D 2000High genetic diversity, distant phylogenetic relationships and intraspecies recombination events among natural populations of Yam mosaic virus: a contribution to understanding potyvirus evolutionJ Gen Virol81243255PubMedGoogle Scholar
  7. Bujarski, JJ, Kaesberg, P 1986Genetic recombination between RNA components of a multipartite plant virusNature321528531CrossRefPubMedGoogle Scholar
  8. Chare, ER, Gould, EA, Holmes, EC 2003Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA virusesJ Gen Virol8426912703CrossRefPubMedGoogle Scholar
  9. Crochu, S, Cook, S, Attoui, H, Charrel, RN, De Chesse, RN, Belhouchet, M, Lemasson, JJ, de Micco, P, de Lamballerie, X 2004Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoesJ Gen Virol8519711980CrossRefPubMedGoogle Scholar
  10. Domingo, E, Holland, JJ 1997RNA virus mutations for fitness and survivalAnnu Rev Microbiol51151178CrossRefPubMedGoogle Scholar
  11. Drake, JW, Holland, JJ 1999Mutation rates among RNA virusesProc Natl Acad Sci USA961391013913CrossRefPubMedGoogle Scholar
  12. Elena, SF, Moya, A 1999Rate of deleterious mutation and the distribution of its effects on fitness in Vesicular stomatitis virusJ Evol Biol1210781088CrossRefGoogle Scholar
  13. Fraile, A, Alonso-Prados, JL, Aranda, MA, Bernal, JJ, Malpica, JM, Garcia-Arenal, F 1997Genetic exchange by recombination or reassortment is infrequent in natural populations of a tripartite RNA plant virusJ Virol71934940PubMedGoogle Scholar
  14. Froissart, R, Rose, D, Uzest, M, Galibert, L, Blanc, S, Michalakis, Y 2005Recombination every day: Abundant recombination in a virus during a single multi-cellular host infectionPloS Biol3e89CrossRefPubMedGoogle Scholar
  15. Gal, S, Pisan, B, Hohn, T, Grimsley, N, Hohn, B 1992Agroinfection of transgenic plants leads to viable Cauliflower mosaic virus by intermolecular recombinationVirology187525533CrossRefPubMedGoogle Scholar
  16. Gibbs M (1995) The luteovirus supergroup: rampant recombination and persistent partnerships. In: Gibbs AJ, Calisher CH, Garcia-Arenal F (eds), Molecular basis of virus evolution. Cambridge University Press, Cambridge, pp 351–368Google Scholar
  17. Greene, AE, Allison, RF 1994Recombination between viral RNA and transgenic plant transcriptsScience26314231425PubMedGoogle Scholar
  18. Greene, AE, Allison, RF 1996Deletions in the 3′ untranslated region of Cowpea chlorotic mottle virus transgene reduce recovery of recombinant viruses in transgenic plantsVirology225231234PubMedGoogle Scholar
  19. Hayakawa, T, Zhu, Y, Itoh, K, Kimura, Y, Izawa, T, Shimamoto, K, Toriyama, S 1992Genetically engineered rice resistant to Rice stripe virus, an insect-transmitted virusProc Natl Acad Sci USA8998659869PubMedGoogle Scholar
  20. Hu, WS, Temin, HM 1990Retroviral recombination and reverse transcriptionScience25012271233PubMedGoogle Scholar
  21. Jung, A, Maier, R, Vartanian, JP, Bocharov, G, Jung, V, Fischer, U, Meese, E, Wain-Hobson, S, Meyerhans, A 2002Multiply infected spleen cells in HIV patientsNature418144CrossRefPubMedGoogle Scholar
  22. Lai, MMC 1992RNA recombination in animal and plant virusesMicrobiol Rev566179PubMedGoogle Scholar
  23. Lain, S, Riechmann, JL, Martin, MT, Garcia, JA 1989Homologous potyvirus and flavivirus proteins belonging to a superfamily of helicase-like proteinsGene82357362PubMedGoogle Scholar
  24. Le Gall, OL, Lanneau, M, Candresse, T, Dunez, J 1995The nucleotide sequence of the RNA-2 of an isolate of the English serotype of Tomato black ring virus: RNA recombination in the history of nepovirusesJ Gen Virol7612791283PubMedGoogle Scholar
  25. Lin, HX, Rubio, L, Smythe, A, Jiminez, M, Falk, BW 2003Genetic diversity and biological variation among California isolates of Cucumber mosaic virusJ Gen Virol84249258CrossRefPubMedGoogle Scholar
  26. MacFarlane, S 1997Natural recombination among plant virus genomes: evidence from tobravirusesSemin Virol82531CrossRefGoogle Scholar
  27. Moreno, IM, Malpica, JM, Diaz-Pendon, JA, Moriones, E, Fraile, A, Garcia-Arenal, F 2004Variability and genetic structure of the population of Watermelon mosaic virus infecting melon in SpainVirology318451460CrossRefPubMedGoogle Scholar
  28. Nagy, PD, Bujarski, JJ 1997Engineering of homologous recombination hotspots with AU-rich sequences in Brome mosaic virusJ Virol7137993810PubMedGoogle Scholar
  29. Ohshima, K, Yamaguchi, Y, Hirota, R, Hamamoto, T, Tomimura, K, Tan, Z, Sano, T, Azuhata, F, Walsh, JA, Fletcher, J, Chen, J, Gera, A, Gibbs, A 2002Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spreadJ Gen Virol8315111521PubMedGoogle Scholar
  30. Padidam, M, Sawyer, S, Fauquet, CM 1999Possible emergence of new geminiviruses by frequent recombinationVirology265218255CrossRefPubMedGoogle Scholar
  31. Posada, D, Crandall, KA, Holmes, EC 2002Recombination in evolutionary genomicsAnnu Rev Genet367597CrossRefPubMedGoogle Scholar
  32. Poutaraud, A, Desbiez, C, Lemaire, O, Lecoq, H, Herrbach, E 2004Characterisation of a new potyvirus species infecting meadow saffron (Colchicum autumnale)Arch Virol14912671277CrossRefPubMedGoogle Scholar
  33. Roossinck, MJ 1997Mechanisms of plant virus evolutionAnnu Rev Phytopathol35191209CrossRefPubMedGoogle Scholar
  34. Rubio, L, Ayllon, MA, Kong, P, Fernandez, A, Polek, M, Guerri, J, Moreno, P, Falk, BW 2001Genetic variation of Citrus tristeza virus isolates from California and Spain: Evidence for mixed infections and recombinationJ Virol7580548062PubMedGoogle Scholar
  35. Sawyer, S 1989Statistical tests for detecting gene conversionMol Biol Evol6526538PubMedGoogle Scholar
  36. Schoelz, JE, Wintermantel, WM 1993Expansion of viral host range through comple- mentation and recombination in transgenic plantsPlant Cell516691679CrossRefPubMedGoogle Scholar
  37. Scholthof, K, Scholthof, HB, Jackson, AO 1993Control of plant virus diseases by pathogen-derived resistance in transgenic plantsPlant Physiol102712PubMedGoogle Scholar
  38. Shapka, N, Nagy, PD 2004The AU-rich RNA recombination hot spot sequence of Brome mosaic virus is functional in tombusviruses: Implications for the mechanism of RNA recombinationJ Virol7822882300CrossRefPubMedGoogle Scholar
  39. Shukla DD, Ward WW, Brunt AA (1994) The potyviridae. CAB International, WallingfordGoogle Scholar
  40. Strimmer, K, von Haesler, A 1996Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologiesMol Biol Evol13964969Google Scholar
  41. Suzuki, M, Hibi, T, Masuta, C 2003RNA recombination between cucumoviruses: possible role of predicted stem-loop structures and an internal subgenomic promoter-like motifVirology3067786CrossRefPubMedGoogle Scholar
  42. Swofford DL (2002) PAUP*: Phylogenetics analysis using parsimony (*and other methods). Version 4 Sinauer Associates, Sunderland, MassGoogle Scholar
  43. Tan, Z, Wada, Y, Chen, J, Ohshima, K 2004Inter- and intralineage recombinants are common in natural populations of Turnip mosaic virusJ Gen Virol8526832696PubMedGoogle Scholar
  44. Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F, Higgins, DG 1997The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignments aided by quality analysis toolsNucleic Acids Res2548764882CrossRefPubMedGoogle Scholar
  45. Vives, MC, Rubio, L, Sambade, A, Mirkov, TE, Moreno, P, Guerri, J 2005Evidence of multiple recombination events between two RNA sequence variants within a Citrus tristeza virus isolateVirology331232237CrossRefPubMedGoogle Scholar
  46. White, KA, Morris, TJ 1999Defective and defective interfering RNAs of monopartite plus-strand RNA plant virusesCurr Top Microbiol Immunol239117PubMedGoogle Scholar
  47. Wintermantel, WM, Schoelz, JE 1996Isolation of recombinant virus between Cauliflower mosaic virus and a viral gene in transgenic plants under conditions of moderate selection pressureVirology223156164CrossRefPubMedGoogle Scholar
  48. Worobey, M, Holmes, EC 1999Evolutionary aspects of recombination in RNA virusesJ Gen Virol8025352543PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • E. R. Chare
    • 1
  • E. C. Holmes
    • 2
  1. 1.Department of ZoologyUniversity of OxfordOxfordU.K.
  2. 2.Center for Infectious Disease Dynamics, Department of BiologyThe Pennsylvania State University, Mueller LaboratoryUniversity ParkU.S.A.

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