Journal of Molecular Evolution

, Volume 71, Issue 4, pp 298–307 | Cite as

Phylogenetic Analysis Reveals Rapid Evolutionary Dynamics in the Plant RNA Virus Genus Tobamovirus

Article

Abstract

Early studies on the evolutionary dynamics of plant RNA viruses suggested that they may evolve more slowly than their animal counterparts, sometimes dramatically so. However, these estimates were often based on an assumption of virus–host codivergence over time-scales of many millions of years that is difficult to verify. An important example are viruses of the genus Tobamovirus, where the assumption of host–virus codivergence over 100 million years has led to rate estimates in the range of ~1 × 10−8 nucleotide substitutions per site, per year. Such a low evolutionary rate is in apparent contradiction with the ability of some tobamoviruses to quickly overcome inbred genetic resistance. To resolve how rapidly molecular evolution proceeds in the tobomaviruses, we estimated rates of nucleotide substitution, times to common ancestry, and the extent of congruence between virus and host phylogenies. Using Bayesian coalescent methods applied to time-stamped sequences, we estimated mean evolutionary rates at the nucleotide and amino acid levels of between 1 × 10−5 and 1.3 × 10−3 substitutions per site, per year, and hence similar to those seen in a broad range of animal and plant RNA viruses. Under these rates, a conservative estimate for the time of origin of the sampled tobamoviruses is within the last 100,000 years, and hence a far more recently than proposed assuming codivergence. This is supported by our cophylogeny analysis which revealed significantly discordant evolutionary histories between the tobamoviruses and the plant families they infect.

Keywords

Tobamoviruses Evolutionary dynamics Virus–host codivergence 

Supplementary material

239_2010_9385_MOESM1_ESM.pdf (361 kb)
Supplementary material 1 (PDF 360 kb)

References

  1. Agrios GN (2005) Plant pathology, 5th edn. Elsevier, AmsterdamGoogle Scholar
  2. Antignus Y, Lachman O, Pearlsman M, Maslenin L, Rosner A (2008) A new pathotype of pepper mild mottle virus (PMMoV) overcomes the L4 resistance genotype of pepper cultivars. Plant Dis 92:1033–1037CrossRefGoogle Scholar
  3. D’Arcy WG (1991) The Solanaceae since 1976, with a review of its biogeography. In: Hawkes JG, Lester RN, Nee M, Estrada N (eds) Solanaceae III: taxonomy, chemistry, evolution. Royal Botanic Garden and Linnaean Society of London, London, pp 75–138Google Scholar
  4. Domingo E, Holland JJ (1997) RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178CrossRefPubMedGoogle Scholar
  5. Drake JW, Charlesworth B, Charlesworth D, Crow JF (1998) Rates of spontaneous mutation. Genetics 148:1667–1686PubMedGoogle Scholar
  6. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedGoogle Scholar
  7. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88CrossRefPubMedGoogle Scholar
  8. Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276CrossRefPubMedGoogle Scholar
  9. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797CrossRefPubMedGoogle Scholar
  10. Fargette D, Pinel-Galzi A, Sereme D, Lacombe S, Hebrard E, Traore O, Konate G (2008) Diversification of Rice yellow mottle virus and related viruses spans the history of agriculture from the Neolithic to the present. PLoS Pathog 4:e1000125CrossRefPubMedGoogle Scholar
  11. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball BA (2005) Virus taxonomy: classification and nomenclature of viruses. 8th Report of the International Committee. Academic Press, San DiegoGoogle Scholar
  12. Firth C, Kitchen A, Shapiro C, Suchard MA, Holmes EC, Rambaut A (2010) Using time-structured data to estimate evolutionary rates of double-stranded DNA viruses. Mol Biol Evol. doi:10.1093/molbev/msq088
  13. Flor HH (1955) Host-parasite interactions in flax-its genetic and other implications. Phytopathology 45:680–685Google Scholar
  14. Fraile A, Malpica JM, Aranda MA, Rodríguez-Cerezo E, García-Arenal F (1996) Genetic diversity in tobacco mild green mosaic tobamovirus infecting the wild plant Nicotiana glauca. Virology 223:148–155CrossRefPubMedGoogle Scholar
  15. Fraile A, Escriu F, Aranda MA, Malpica JM, Gibbs AJ, García-Arenal F (1997) A century of tobamovirus evolution in an Australian population of Nicotiana glauca. J Virol 71:8316–8320PubMedGoogle Scholar
  16. French R, Stenger DC (2003) Evolution of Wheat streak mosaic virus: dynamics of population growth within plants may explain limited variation. Annu Rev Phytopathol 41:199–214CrossRefPubMedGoogle Scholar
  17. Fukuda M, Meshi T, Okada Y, Otsuki Y, Takebe I (1981) Correlation between particle multiplicity and location on virion RNA of the assembly initiation site for viruses of the tobacco mosaic virus group. Proc Natl Acad Sci USA 78:4231–4235CrossRefPubMedGoogle Scholar
  18. García-Arenal F, McDonald BA (2003) An analysis of the durability of resistance to plant viruses. Phytopathology 93:941–952CrossRefPubMedGoogle Scholar
  19. Gibbs AJ (1980) How ancient are the tobamoviruses? Intervirology 14:101–108CrossRefPubMedGoogle Scholar
  20. Gibbs AJ (1986) Tobamovirus classification. In: van Regenmortel MHV, Fraenkel-Conrat H (eds) The plant viruses. 2. The rod-shaped plant viruses. Plenum Press, New York, pp 167–180Google Scholar
  21. Gibbs AJ (1999) Evolution and origin of tobamoviruses. Phil Trans R Soc Lond B 354:593–602CrossRefGoogle Scholar
  22. Gibbs AJ, Gibbs MJ, Ohshima K, García-Arenal F (2008a) More plant virus evolution; past present and future. In: Domingo E, Parrish CR, Holland JJ (eds) Origin and evolution of viruses, 2nd edn. Academic Press, London, pp 229–250Google Scholar
  23. Gibbs AJ, Ohshima K, Phillips MJ, Gibbs MJ (2008b) The prehistory of potyviruses: their initial radiation was during the dawn of agriculture. PLoS One 3:e2523CrossRefPubMedGoogle Scholar
  24. Gibbs AJ, Fargette D, García-Arenal F, Gibbs MJ (2010) Time—the emerging dimension of plant virus studies. J Gen Virol 91:13–22CrossRefPubMedGoogle Scholar
  25. Hadidi A, Khetarpal RK, Koganezawa H (1998) Plant virus disease control. APS Press, St. PaulGoogle Scholar
  26. Holmes FO (1951) Indications of a new world origin of tobacco mosaic virus. Phytopathology 41:341–349Google Scholar
  27. Jackson PA, Charleston MA (2004) A cophylogenetic perspective of RNA-virus evolution. Mol Biol Evol 21:45–57CrossRefPubMedGoogle Scholar
  28. Lartey RT, Voss TC, Melcher U (1996) Tobamovirus evolution: gene overlaps, recombination, and taxonomic implications. Mol Biol Evol 13:1327–1338PubMedGoogle Scholar
  29. Li H, Roossinck MJ (2004) Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol 78:10582–10587CrossRefPubMedGoogle Scholar
  30. Malpica JM, Fraile A, Moreno I, Obies CI, Drake JW, García-Arenal F (2002) The rate and character of spontaneous mutation in an RNA virus. Genetics 162:1505–1511PubMedGoogle Scholar
  31. Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262CrossRefPubMedGoogle Scholar
  32. Olmstead R, Palmer JD (1991) Chloroplast DNA and systematics of the Solanaceae. In: Hawkes JG, Lester RN, Nee M, Estrada N (eds) Solanaceae III: taxonomy, chemistry, evolution. Royal Botanic Garden and Linnaean Society of London, London, pp 161–168Google Scholar
  33. Pagán I, Holmes EC (2010) Long-term evolution of the Luteoviridae: time scale and mode of virus speciation. J Virol 84:6177–6187CrossRefPubMedGoogle Scholar
  34. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  35. Rambaut A (1996) Se-Al: sequence alignment editor. http://evolve.zoo.ox.ac.uk/
  36. Rambaut A (2009) Path-O-Gen: temporal signal investigation tool. http://tree.bio.ed.ac.uk/software/pathogen/
  37. Rast ATB (1988) Pepper tobamoviruses and pathotypes used in resistance breeding. Capsicum Newslett 7:20–24Google Scholar
  38. Rodriguez-Cerezo E, García-Arenal F (1991) High genetic stability in natural populations of the plant RNA virus Tobacco mild green mosaic virus. J Mol Evol 32:328–332CrossRefGoogle Scholar
  39. Roossinck M, Ali A (2007) Mechanisms of plant virus evolution and identification of genetic bottlenecks: impact on disease management. In: Punja ZK, De Boer SH, Sanfaçon S (eds) Biotechnology and plant disease management. CABI Publishing, Wallingford, pp 109–124CrossRefGoogle Scholar
  40. Sacristan S, Malpica JM, Fraile A, Garcia-Arenal F (2003) Estimation of population bottlenecks during movement of tobacco mosaic virus in tobacco plants. J Virol 77:9906–9911CrossRefPubMedGoogle Scholar
  41. Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R (2010) Viral mutation rates. J Virol Google Scholar
  42. Savolainen V, Fay MF, Albach DC, Backlund A, van der Bank M, Cameron KM, Johnson SA, Lledó MD, Pintaud J-C, Powell M, Sheaman MC, Soltis DE, Soltis PS, Weston P, Whitten WM, Wurdack KJ, Chase MW (2000) Phylogeny of the Eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bull 55:257–309CrossRefGoogle Scholar
  43. Simmons HE, Holmes EC, Stephenson AG (2008) Rapid evolutionary dynamics of zucchini yellow mosaic virus. J Gen Virol 89:1081–1085CrossRefPubMedGoogle Scholar
  44. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  45. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699PubMedGoogle Scholar
  46. Wu B, Melcher U, Guo X, Wang X, Fan L, Zhou G (2008) Assessment of codivergence of Mastrevirus with their plant hosts. BMC Evol Biol 8:335CrossRefPubMedGoogle Scholar
  47. Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Israel Pagán
    • 1
  • Cadhla Firth
    • 1
    • 3
  • Edward C. Holmes
    • 1
    • 2
  1. 1.Department of Biology, Center for Infectious Disease DynamicsThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Fogarty International CenterNational Institutes of HealthBethesdaUSA
  3. 3.Center for Infection and ImmunityColumbia UniversityNew YorkUSA

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