Abstract
Chrysanthemums worldwide suffer from a high incidence of infection with chrysanthemum virus B (CVB), a member of the genus Carlavirus, family Betaflexiviridae. Three major lineages or strains of this virus have been found in India, but none have been characterized beyond the genetic variation they display in their coat protein genes. Here, we describe the analysis of four near-complete genome sequences (from the three lineages) representing the genetic diversity of these strains. Ranging in size from 8815 to 8855 nucleotides (excluding the polyA tail), these four isolates have a genome organization very similar to that of the recently reported Japanese isolate of CVB, with which they share between 70 and 73% genome-wide sequence identity. We present further evidence that recombination may feature quite prominently in the evolution of CVB.
References
Berg J (1986) Potential metal binding domains in nucleic acid binding proteins. Science 232:485–486
Boni MF, Posada D, Feldman MW (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:1035–1047
Cavileer TD, Halpern BT, Lawrence DM, Podleckis EV, Martin RR, Hillman BI (1994) Nucleotide sequence of the carlavirus associated with blueberry scorch and similar diseases. J Gen Virol 75:711–720
Corpet F (1988) Multiple sequence alignment with hierarchial clustering. Nucl Acids Res 16:10881–10890
Desbiez C, Lecoq H (2004) The nucleotide sequence of Watermelon mosaic virus (WMV, Potyvirus) reveals interspecific recombination between two related potyviruses in the 5′ part of the genome. Arch Virol 149:1619–1632
Desbiez C, Lecoq H (2008) Evidence for multiple intraspecific recombinants in natural populations of Watermelon mosaic virus (WMV, Potyvirus). Arch Virol 153:1749–1754
Dinesen M, Lundmark M, Albrechtsen M (2009) Complete genome sequences of two isolates of Kalanchoe latent virus. Arch Virol 154(7):1173–1175
Erhardt M, Vetter G, Gilmer D, Bouzoubaa S, Richard K, Jonard G, Guilley H (2005) Subcellular localization of the Triple Gene Block movement proteins of Beet necrotic yellow vein virus by electron microscopy. Virology 340(1):155–166
Foster GD (1998) Carlavirus isolation and RNA extraction. In: Foster GD, Taylor SC (eds) Plant virology protocols, from virus isolation to transgenic resistance. Humana Press, Totowa, pp 145–150
Foster GD, Millar AW, Meehan BM, Mills PR (1990) Nucleotide sequence of the 3′-terminal region of Helenium virus S. J Gen Virol 71:1877–1880
Foster GD, Mills PR (1991) Translation of Potato virus S RNA in vitro: evidence of protein processing. Virus Genes 6:45–52
Fuji S, Yamamoto H, Inoue M, Yamashita K, Fukui Y, Furuya H, Naito H (2002) Complete nucleotide sequence of the genomic RNA of Aconitum latent virus (genus Carlavirus) isolated from Delphinium sp. Arch Virol 147:865–870
Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582
Gorbalenya AE, Blinov VM, Donchenko AP, Koonin EV (1989) An NTP-binding motif is the most conserved sequence in a highly diverged monophyletic group of proteins involved in positive strand RNA viral replication. J Mol Evol 28:256–268
Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hashimoto M, Komatsu K, Maejima K, Yamaji Y, Okano Y, Shiraishi T, Takahashi S, Kagiwada S, Namba S (2009) Complete nucleotide sequence and genome organization of Butterbur mosaic virus. Arch Virol 154(12):1955–1958
Hataya T, Uchino K, Arimoto R, Suda N, Sano T, Shikata E, Uyeda I (2000) Molecular characterization of Hop latent virus and phylogenetic relationships among viruses closely related to carlaviruses. Arch Virol 145:2503–2524
Heath L, van der Walt E, Varsani A, Martin DP (2006) Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80:11827–11832
Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680
Hu X, Karasev AV, Brown CJ, Lorenzen JH (2009) Sequence characteristics of potato virus Y recombinants. J Gen Virol 90:3033–3041
Klug A, Rhodes D (1987) ‘Zinc fingers’: a novel protein motif for nucleic acid recognition. Trends Biochem Sci 12:464–469
Kraus J, Tzanetakis IE, Putnam ML, Martin RR (2008) Complete nucleotide sequence of an isolate of coleus vein necrosis virus from verbena. Arch Virol 153:381–384
Lawrence DM, Hillman BI (1994) Synthesis of infectious transcripts of Blueberry scorch carlavirus in vitro. J Gen Virol 75:2509–2512
Lee BY, Min BE, Ha JH, Lee MY, Paek KH, Ryu KH (2006) Genome structure and complete sequence of genomic RNA of Daphne virus S. Arch Virol 151:193–200
Lefeuvre P, Martin DP, Hoareau M, Naze F, Delatte H, Thierry M, Varsani A, Becker N, Reynaud B, Lett JM (2007a) Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. J Gen Virol 88:3458–3468
Lefeuvre P, Lett JM, Reynaud B, Martin DP (2007b) Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3(11):e181. doi:10.1371/journal.ppat.0030181
Lefeuvre P, Lett JM, Varsani A, Martin DP (2009) Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83(6):2697–2707
Lim S-H, Bragg JN, Ganesan U, Lawrence DM, Yu J, Isogai M, Hammond J, Jackson AO (2008) Triple gene block protein interactions involved in movement of Barley stripe mosaic virus. J Virol 82(10):4991–5006
Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26(19):2462–2463
Martin DP, Posada D, Crandall KA, Williamson C (2005) A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retrovir 21:98–102
Martin DP, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563
Massa GA, Portantier M, Segretin ME, Bravo-Almonacid FF, Feingold SE (2008) Comparison of complete sequences of Potato rough dwarf virus and Potato virus P and their relationships to other carlaviruses. Arch Virol 153:1787–1789
Matousek J, Schubert J, Ptacek J, Kozlová P, Dědič P (2005) Complete nucleotide sequence and molecular probing of Potato virus S genome. Acta Virol 49(3):195–205
Maydt J, Lengauer T (2006) Recco: recombination analysis using cost optimization. Bioinformatics 22(9):1064–1071
Maynard Smith J (1992) Analysing the mosaic structure of genes. J Mol Evol 34:126–129
Menzel W, Winter S, Vetten HJ (2010) Complete nucleotide sequence of the type isolate of Cowpea mild mottle virus from Ghana. Arch Virol 155:2069–2073
Novitsky V, Wang R, Margolin L, Baca J, Rossenkhan R, Moyo S, van Widenfelt E, Essex M (2011) Transmission of single and multiple viral variants in primary HIV-1 subtype C infection. PLoS One 6(2):e16714. doi:10.1371/journal.pone.0016714
Nyström K, Le Gall-Reculé G, Grassi P, Abrantes J, Ruvoën-Clouet N, Le Moullac-Vaidye B, Lopes AM, Esteves PJ, Strive T, Marchandeau S, Dell A, Haslam SM, Le Pendu J (2011) Histo-blood group antigens act as attachment factors of rabbit hemorrhagic disease virus infection in a virus strain-dependent manner. PLoS Pathog 7(8):e1002188. doi:10.1371/journal.ppat.1002188
Padidam M, Sawyer S, Fauquet C (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225
Poke FS (2008) Hop mosaic virus: complete nucleotide sequence and relationship to other carlaviruses. Arch Virol 153:1615–1619
Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98:13757–13762
Ohkawa A, Yamada M, Sayama H, Sugiyama N, Okuda S, Natsuaki T (2007) Complete nucleotide sequence of a Japanese isolate of Chrysanthemum virus B (genus Carlavirus). Arch Virol 152(12):2253–2258
Ram R, Verma N, Singh AK, Singh L, Hallan V, Zaidi AA (2005) Indexing and production of virus-free chrysanthemums. Biol Plant 49:149–152
Richard CL, Stephen DW, Keri LD (2009) The complete nucleotide sequence and genome organization of red clover vein mosaic virus (genus Carlavirus). Arch Virol 154:891–894
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Scott SW, Zimmerman MT (2008) The complete sequence of ligustrum necrotic ringspot virus, a novel carlavirus. Arch Virol 153:393–396
Singh L, Hallan V, Jabeen N, Singh AK, Ram R, Martin DP, Zaidi AA (2007) Coat protein gene diversity among Chrysanthemum virus B isolates from India. Arch Virol 152:405–413
Tan Z, Wada Y, Chen J, Ohshima K (2004) Inter- and intralineage recombinants are common in natural populations of Turnip mosaic virus. J Gen Virol 85:2683–2696
Tsuneyoshi T, Matsumi T, Deng TC, Sako I, Sumi S (1998) Differentiation of Allium carlaviruses isolated from different parts of the world based on the viral coat protein sequence. Arch Virol 143:1093–1107
Tugume AK, Mukasa SB, Kalkkinen N, Valkonen JPT (2010) Recombination and selection pressure in the ipomovirus sweet potato mild mottle virus (Potyviridae) in wild species and cultivated sweet potato in the centre of evolution in East Africa. J Gen Virol 91:1092–1108
Van Dijk P (1993) Carlavirus isolates from cultivated Allium species represent three viruses. Neth J Plant Pathol 99:233–257
Wetter C, Milne RG (1981) Carlaviruses. In: Kurstak E (ed) Plant virus infections: comparative diagnosis. Elsevier/North Holland, Amesterdam, pp 695–730
Wu B, Blanchard-Letort A, Liu Y, Zhou G, Wang X, Elena SF (2011) Dynamics of molecular evolution and phylogeography of barley yellow dwarf virus-PAV. PLoS One 6(2):e16896. doi:10.1371/journal.pone.0016896
Xianzhou N (2009) The complete nucleotide sequence and genome structure of potato latent virus. Arch Virol 154:361–364
Yang Z, Holmes EC (2007) Bayesian estimates of the evolutionary rate and age of Hepatitis B. Virus J Mol Evol 65:197–205
Zavriev SK, Kanyuka KV, Levay KE (1991) The genome organization of Potato virus M RNA. J Gen Virol 72:9–14
Acknowledgments
The authors are thankful to the Director, Council of Scientific and Industrial Research, Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh, India, for providing the necessary facilities to carry out the work, and to Digvijay Singh for technical help with nucleotide sequencing. A fellowship to LS and financial support from the Department of Biotechnology, Govt. of India, and Council of Scientific and Industrial Research are duly acknowledged. This is IHBT publication number: 2206.
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705_2011_1190_MOESM1_ESM.doc
Supplementary Fig. 1 ClustalW multiple alignment of the complete genomes of five CVB isolates. Sequences in green boxes represent initiation codons, and those in red boxes, stop codons (DOC 170 kb)
705_2011_1190_MOESM2_ESM.doc
Supplementary Fig. 2 ClustalW multiple alignment of the replicase, TGB1, TGB2, TGB3, CP and NABP protein sequences from five CVB isolates. Conserved motifs are indicated by green shading (DOC 77 kb)
705_2011_1190_MOESM4_ESM.doc
Supplementary Fig. 4 Mechanical inoculation of various CVB isolates on Petunia hybrida, showing variation in biological reaction. a Mottling induced by CVB-UK. b Narrowing of leaf lamina induced by CVB-TN. c Leaf deformation induced by CVB-UP. d Mosaic induced by CVB-AR (partially sequenced isolate of CVB Arunachal Pradesh 109287621). e Mosaic puckering induced by CVB-PB (DOC 1155 kb)
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Singh, L., Hallan, V., Martin, D.P. et al. Genomic sequence analysis of four new chrysanthemum virus B isolates: evidence of RNA recombination. Arch Virol 157, 531–537 (2012). https://doi.org/10.1007/s00705-011-1190-x
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DOI: https://doi.org/10.1007/s00705-011-1190-x