Abstract
The genetic structure of the populations of Turnip mosaic virus in Kyushu and central Honshu, Japan was assessed. The host specificity of isolates was determined, and their gene sequences compared utilizing a population genetic approach. Phylogenetic analysis of partial sequences revealed that 32 of 49 Honshu isolates (65%) collected during 1997–2001 belonged to the basal-BR group as did 23 of 64 isolates from Kyushu. All these basal-BR isolates infected both Brassica and Raphanus plants. However, analyses of the positions of recombination sites in five regions of the genome (one third of the full sequence) showed that at least four intra-lineage recombinants were present in these populations. These analyses showed that Kyushu and Honshu shared none of these subpopulations, and genetically distinct basal-BR populations were present in the two districts. We conclude that different basal-BR subpopulations had expanded into those districts.
Similar content being viewed by others
References
Atreya PL, Atreya CD, Pirone TP (1991) Amino acid substitutions in the coat protein result in loss of insect transmissibility of a plant virus. Proc Natl Acad Sci USA 88:11919–11923
Bermingham E, Moritz C (1998) Comparative phylogeography: concepts and application. Mol Ecol 7:367–369
Briddon RW, Stanley J (2006) Subviral agents associated with plant single-stranded DNA viruses. Virology 344:198–210
Brown JK (2001) The molecular epidemiology of begomoviruses. In: Khan JA, Dykstra J (eds) Trends in plant pathology. Haworth Press, New York, pp 279–316
Chare ER, Holmes EC (2006) A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151:933–946
Chen J, Chen JS (2000) Occurrence and control of mosaic disease [turnip mosaic virus] in saffron (Crocus sativus). Zhejiang Nongye Kexue 3:132–135
Chen J, Zheng HY, Chen JP, Adams MJ (2002) Characterisation of a potyvirus and a potexvirus from Chinese scallion. Arch Virol 147:683–693
Chen J, Chen JP, Langeveld SA, Derks AFLM, Adams MJ (2003) Molecular characterization of Carla- and Potyviruses from Narcissus in China. J Phytopathol 151:26–29
Dolja VV, Haldeman R, Robertson NL, Dougherty WG, Carrington JC (1994) Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J 13:1482–1491
Excoffier L, Laval G, Schneider S (2005) Arlequin (Version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (2005) Virus taxonomy. In: 8th Report of the international committee on taxonomy of Viruses. Elsevier Academic, San Diego
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J (1993) PHYLIP (Phylogeny interference package), Version 3.5. Department of Genetics, University of Washington, Seattle
Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
Fuji S, Nakamae H (1999) Complete nucleotide sequence of the genomic RNA of a Japanese yam mosaic virus, a new potyvirus in Japan. Arch Virol 144:231–240
Fuji S, Nakamae H (2000) Complete nucleotide sequence of the genomic RNA of a mild strain of Japanese yam mosaic potyvirus in Japan. Arch Virol 145:635–640
García-Arenal F, Escriu F, Aranda MA, Alonso-Prados JL, Malpica JM, Fraile A (2000) Molecular epidemiology of Cucumber mosaic virus and its satellite RNA. Virus Res 71:1–8
Gera A, Lesemann DE, Cohen J, Franck A, Levy S, Salomon R (1997) The natural occurrence of turnip mosaic potyvirus in Allium ampeloprasum. J Phytopathol 145:289–293
Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582; http://www.anu.edu.au/BoZo/software/
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hamlyn BMG (1953) Quantitative studies on the transmission of cabbage black ringspot virus by Myzus persicae (Sulz.). Ann Appl Biol 40:393–402
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hey J, Harris E (1999) Population bottlenecks and patterns of human polymorphism. Mol Biol Evol 16:1423–1426
Hu WQ, Pu ZQ, Xu ZG, Fang ZD (1996) A viral disease of broad bean caused by a non-aphid-transmissible strain of turnip mosaic virus. Plant Pathol 45:843–847
Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Klein PG, Klein RR, Rodríquez-Cerezo E, Hunt AG, Shaw JG (1994) Mutational analysis of the tobacco vein mottling virus genome. Virology 204:759–769
Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563
Martin D, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignment. Bioinformatics 21:260–262
Maynard Smith J (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129
Moreno IM, Malpica JM, Díaz-Pendón JA, 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
Moyer JW (1999) Tospoviruses (Bunyaviridae). In: Webster R, Granoff A (eds) Encyclopedia of virology. Academic, London, pp 1803–1807
Ohshima K, Tanaka M, Sako N (1996) The complete nucleotide sequence of turnip mosaic virus RNA Japanese strain. Arch Virol 141:1991–1997
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. (2002) Molecular evolution of Turnip mosaic virus; evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol 83:1511–1521
Pagán I, Córdoba-Sellés MC, Martínez-Priego L, Fraile A, Malpica JM, Jordá C, García-Arenal F (2006) Genetic structure of the population of Pepino mosaic virus infecting tomato crops in Spain. Phytopathology 96:274–279
Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computer. Comput Appl Biosci 12:357–358
Page RDM, Holmes EC (1998) Molecular evolution: a phylogenetic approach. Blackwell Science, Oxford, pp 89–134
Parks TD, Howard ED, Wolpert TJ, Arp DJ, Dougherty WG (1995) Expression and purification of a recombinant tobacco etch virus NIa proteinase: biochemical analyses of the full-length and a naturally occurring truncated proteinase form. Virology 210:194–201
Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98:13757–13762
Provvidenti R (1996) Turnip mosaic potyvirus. In: Brunt AA, Crabtree K, Dallwitz MJ, Gibbs AJ, Watson L (eds) Viruses of plants. CABI, Wallingford, pp 1340–1343
Restrepo-Hartwig MA, Carrington JC (1994) The tobacco etch potyvirus 6-kilodalton protein is membrane associated and involved in viral replication. J Virol 68:2388–2397
Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Rozas J, Sánchez-DeI, Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Rubio L, Angeles M, Ayllón A, Kong P, Fernándes A, Polek M, Guerri J, Moreno P, Falk BW (2001) Genetic variation of Citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombination. J Virol 75:8054–8062
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Salminen MO, Carr JK, Burke DS, McCutchan FE (1995) Identification of breakpoints in intergenotypic recombinants of HIV type 1 by Bootscanning. AIDS Res Hum Retroviruses 11:1423–1425
Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. Distributed by the author. Department of Mathematics, Washington University in St. Louis, available at http://www.math.wustl.edu/∼sawyer
Schaad MC, Lellis AD, Carrington JC (1997) VPg of tobacco etch potyvirus is a host genotype-specific determinant for long-distance movement. J Virol 71:8624–8631
Strimmer K, von Haeseler A (1996) Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969
Strimmer K, Goldman N, von Haeseler A (1997) Bayesian probabilities and quartet puzzling. Mol Biol Evol 14:210–211
Swofford DL (1998) PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer, Sunderland, Massachusetts
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tan Z, Wada Y, Chen J, Ohshima K (2004) Inter- and intra-lineage recombinants are common in natural populations of Turnip mosaic virus. J Gen Virol 85:2683–2696
Tomimura K, Gibbs AJ, Jenner CE, Walsh JA, Ohshima K (2003) The phylogeny of Turnip mosaic virus; comparisons of thirty-eight genomic sequences reveal a Eurasian origin and a recent ‘emergence’ in east Asia. Mol Ecol 12:2099–2111
Tomimura K, Špak J, Katis N, Jenner CE, Walsh JA, Gibbs AJ, Ohshima K (2004) Comparisons of the genetic structure of populations of Turnip mosaic virus in west and east Eurasia. Virology 330:408–423
Tomitaka Y, Ohshima K (2006) A phylogeographic study of the Turnip mosaic virus population in east Asia reveals an ‘emergent’ lineage in Japan. Mol Ecol 15:4437–4457
Tomlinson JA (1987) Epidemiology and control of virus diseases of vegetables. Ann Appl Biol 110:661–681
Tsompana M, Abad J, Purugganan M, Moyer JW (2005) The molecular population genetics of the Tomato spotted wilt virus (TSWV) genome. Mol Ecol 14:53–66
Urcuqui-Inchima S, Haenni A-L, Bernardi F (2001) Potyvirus proteins: a wealth of functions. Virus Res 74:157–175
Verchot J, Herndon KL, Carrington JC (1992) Mutational analysis of the tobacco etch potyviral 35-kDa proteinase: identification of essential residues and requirements for autoproteolysis. Virology 190:298–306
Walsh JA, Jenner CE (2002) Turnip mosaic virus and the quest for durable resistance. Mol Plant Pathol 3:289–300
Weiller GF (1998) Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Mol Biol Evol 15:326–335
Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556; http://abacus.gene.ucl.ac.uk/software/paml.html
Acknowledgments
We thank Eri Muraguchi, Yui Nakamizu, Akemi Sato and Kenta Tomimura (Saga University, Japan) for their careful technical assistance, and Teruo Sano (Hirosaki University, Japan) for supplying TuMV isolates. We thank Adrian Gibbs for very kindly reading the manuscript. This work was supported by Grant-in-Aid for Scientific Research no. 17580040 from the Japan Society for the Promotion of Science.
Author information
Authors and Affiliations
Corresponding author
Additional information
The nucleotide sequences are deposited in the DDBJ/EMBL/GenBank databases under accession numbers AB267281-AB267376.
Rights and permissions
About this article
Cite this article
Tomitaka, Y., Yamashita, T. & Ohshima, K. The genetic structure of populations of Turnip mosaic virus in Kyushu and central Honshu, Japan. J Gen Plant Pathol 73, 197–208 (2007). https://doi.org/10.1007/s10327-007-0003-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10327-007-0003-2