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.
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References
Agrios GN (2005) Plant pathology, 5th edn. Elsevier, Amsterdam
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 92:1033–1037
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 75–138
Domingo E, Holland JJ (1997) RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178
Drake JW, Charlesworth B, Charlesworth D, Crow JF (1998) Rates of spontaneous mutation. Genetics 148:1667–1686
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88
Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797
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:e1000125
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 Diego
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
Flor HH (1955) Host-parasite interactions in flax-its genetic and other implications. Phytopathology 45:680–685
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 223:148–155
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 71:8316–8320
French R, Stenger DC (2003) Evolution of Wheat streak mosaic virus: dynamics of population growth within plants may explain limited variation. Annu Rev Phytopathol 41:199–214
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 78:4231–4235
García-Arenal F, McDonald BA (2003) An analysis of the durability of resistance to plant viruses. Phytopathology 93:941–952
Gibbs AJ (1980) How ancient are the tobamoviruses? Intervirology 14:101–108
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 167–180
Gibbs AJ (1999) Evolution and origin of tobamoviruses. Phil Trans R Soc Lond B 354:593–602
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 229–250
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:e2523
Gibbs AJ, Fargette D, García-Arenal F, Gibbs MJ (2010) Time—the emerging dimension of plant virus studies. J Gen Virol 91:13–22
Hadidi A, Khetarpal RK, Koganezawa H (1998) Plant virus disease control. APS Press, St. Paul
Holmes FO (1951) Indications of a new world origin of tobacco mosaic virus. Phytopathology 41:341–349
Jackson PA, Charleston MA (2004) A cophylogenetic perspective of RNA-virus evolution. Mol Biol Evol 21:45–57
Lartey RT, Voss TC, Melcher U (1996) Tobamovirus evolution: gene overlaps, recombination, and taxonomic implications. Mol Biol Evol 13:1327–1338
Li H, Roossinck MJ (2004) Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol 78:10582–10587
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 162:1505–1511
Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262
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 161–168
Pagán I, Holmes EC (2010) Long-term evolution of the Luteoviridae: time scale and mode of virus speciation. J Virol 84:6177–6187
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Rambaut A (1996) Se-Al: sequence alignment editor. http://evolve.zoo.ox.ac.uk/
Rambaut A (2009) Path-O-Gen: temporal signal investigation tool. http://tree.bio.ed.ac.uk/software/pathogen/
Rast ATB (1988) Pepper tobamoviruses and pathotypes used in resistance breeding. Capsicum Newslett 7:20–24
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 32:328–332
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 109–124
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 77:9906–9911
Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R (2010) Viral mutation rates. J Virol
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 55:257–309
Simmons HE, Holmes EC, Stephenson AG (2008) Rapid evolutionary dynamics of zucchini yellow mosaic virus. J Gen Virol 89:1081–1085
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
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 18:691–699
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 8:335
Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7
Acknowledgments
This work was supported by Marie Curie Fellowship PIOF-GA-2009-236470 to IP, NSERC Canada to CF, and NIH grant R01-GM080533 to ECH. We thank Dr. Andrew Kitchen for valuable comments, and all the authors who kindly provided collection information for their sequence data.
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Pagán, I., Firth, C. & Holmes, E.C. Phylogenetic Analysis Reveals Rapid Evolutionary Dynamics in the Plant RNA Virus Genus Tobamovirus . J Mol Evol 71, 298–307 (2010). https://doi.org/10.1007/s00239-010-9385-4
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DOI: https://doi.org/10.1007/s00239-010-9385-4