Skip to main content
Top
Published in: Archives of Virology 10/2019

01-10-2019 | Original Article

Genetic structure and variability of tobacco vein banding mosaic virus populations

Authors: Shiqing Wei, Xiaorong He, Die Wang, Jinyou Xiang, Yide Yang, Shu Yuan, Jing Shang, Hui Yang

Published in: Archives of Virology | Issue 10/2019

Login to get access

Abstract

Tobacco vein banding mosaic virus (TVBMV) is of increasing importance in tobacco production. Knowledge of the genetic structure and variability of the virus population is vital for developing sustainable management. In this study, 24 new TVBMV isolates from Sichuan Province together with 46 previous isolates were studied based on their coat protein sequences. Two distinguishable clades were supported by phylogenetic analysis. The summary statistics PS, AI and MC showed a strong TVBMV-geography association between the isolates from Southwest China (SW) and Mainland China (MC). Further analysis indicated that the spatial genetic structure of TVBMV populations is likely to have been caused by natural selection. Phylogeographic analysis provided strong support for spatial diffusion pathways between the Southwest and Northwest tobacco-producing regions. The TVBMV CP gene was found to be under negative selection, and no significant positive selection of amino acids was detected in the SW group; however, the isolates of the MC group experienced significant positive selection pressure at the first and third amino acid sites of CP. This study suggests that natural selection and habitat heterogeneity are important evolutionary mechanisms affecting the genetic structure of the TVBMV population.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gibbs A, Ohshima K (2010) Potyviruses and the digital revolution. Annu Rev Phytopathol 48:205–223CrossRefPubMed Gibbs A, Ohshima K (2010) Potyviruses and the digital revolution. Annu Rev Phytopathol 48:205–223CrossRefPubMed
2.
go back to reference Biebricher CK, Eigen M (2006) What is a Quasispecies? Curr Top Microbiol 299:1–31 Biebricher CK, Eigen M (2006) What is a Quasispecies? Curr Top Microbiol 299:1–31
3.
go back to reference Zhan J, McDonald BA (2004) The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 41:590–599CrossRefPubMed Zhan J, McDonald BA (2004) The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 41:590–599CrossRefPubMed
4.
go back to reference Gao FL, Zou W, Xie LX (2017) Zhan JS (2017) Adaptive evolution and demographic history contribute to the divergent population genetic structure of Potato virus Y between China and Japan. Evol Appl 10:379–390CrossRefPubMedPubMedCentral Gao FL, Zou W, Xie LX (2017) Zhan JS (2017) Adaptive evolution and demographic history contribute to the divergent population genetic structure of Potato virus Y between China and Japan. Evol Appl 10:379–390CrossRefPubMedPubMedCentral
5.
go back to reference Thrall PH, Oakeshott JG, Fitt G, Southerton S, Burdon JJ, Sheppard A, Denison RF (2011) Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems. Evol Appl 4:200–215CrossRefPubMedPubMedCentral Thrall PH, Oakeshott JG, Fitt G, Southerton S, Burdon JJ, Sheppard A, Denison RF (2011) Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems. Evol Appl 4:200–215CrossRefPubMedPubMedCentral
6.
go back to reference Pérez-Losada M, Arenas M, Galán JG, Palero F, González-Candelas F (2015) Recombination in viruses: mechanisms, methods of study, and evolutionary consequences. Infect Genet Evol 30:296–300CrossRefPubMed Pérez-Losada M, Arenas M, Galán JG, Palero F, González-Candelas F (2015) Recombination in viruses: mechanisms, methods of study, and evolutionary consequences. Infect Genet Evol 30:296–300CrossRefPubMed
8.
go back to reference Yu XQ, Lan Y, Wang H, Liu J, Zhu X, Valkonen J, Li XD (2007) The complete genomic sequence of tobacco vein banding mosaic virus and its similarities with other potyviruses. Virus Genes 35:801–806CrossRefPubMed Yu XQ, Lan Y, Wang H, Liu J, Zhu X, Valkonen J, Li XD (2007) The complete genomic sequence of tobacco vein banding mosaic virus and its similarities with other potyviruses. Virus Genes 35:801–806CrossRefPubMed
9.
go back to reference Rodamilans B, Valli A, Mingot A, San León D, Baulcombe D, López-Moya JJ, García JA (2015) RNA polymerase slippage as a mechanism for the production of frameshift gene products in plant viruses of the Potyviridae family. J Virol 89:6965–6967CrossRefPubMedPubMedCentral Rodamilans B, Valli A, Mingot A, San León D, Baulcombe D, López-Moya JJ, García JA (2015) RNA polymerase slippage as a mechanism for the production of frameshift gene products in plant viruses of the Potyviridae family. J Virol 89:6965–6967CrossRefPubMedPubMedCentral
10.
go back to reference Zhou GC, Wu XY, Zhang YM, Wu P, Wu XZ, Liu LW, Chen JQ (2014) A genomic survey of thirty soybean-infecting bean common mosaic virus (BCMV) isolates from China pointed BCMV as a potential threat to soybean production. Virus Res 191:125–133CrossRefPubMed Zhou GC, Wu XY, Zhang YM, Wu P, Wu XZ, Liu LW, Chen JQ (2014) A genomic survey of thirty soybean-infecting bean common mosaic virus (BCMV) isolates from China pointed BCMV as a potential threat to soybean production. Virus Res 191:125–133CrossRefPubMed
11.
go back to reference Zhou GC, Shao ZQ, Ma FF, Wu P, Wu XY, Xie ZY, Chen JQ (2015) The evolution of soybean mosaic virus: an updated analysis by obtaining 18 new genomic sequences of Chinese strains/isolates. Virus Res 208:189–198CrossRefPubMed Zhou GC, Shao ZQ, Ma FF, Wu P, Wu XY, Xie ZY, Chen JQ (2015) The evolution of soybean mosaic virus: an updated analysis by obtaining 18 new genomic sequences of Chinese strains/isolates. Virus Res 208:189–198CrossRefPubMed
12.
go back to reference Lecoq H, Wipf Scheibel C, Chandeysson C, LêVan A, Fabre F, Desbiez C (2009) Molecular epidemiology of Zucchini yellow mosaic virus in France: an historical overview. Virus Res 141:190–200CrossRefPubMed Lecoq H, Wipf Scheibel C, Chandeysson C, LêVan A, Fabre F, Desbiez C (2009) Molecular epidemiology of Zucchini yellow mosaic virus in France: an historical overview. Virus Res 141:190–200CrossRefPubMed
13.
go back to reference 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 83:1511–1521CrossRefPubMed 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 83:1511–1521CrossRefPubMed
14.
go back to reference Nguyen HD, Tran HTN, Ohshima K (2013) Genetic variation of the Turnip mosaic virus population of Vietnam: a case study of founder, regional and local influences. Virus Res 171:138–149CrossRefPubMed Nguyen HD, Tran HTN, Ohshima K (2013) Genetic variation of the Turnip mosaic virus population of Vietnam: a case study of founder, regional and local influences. Virus Res 171:138–149CrossRefPubMed
15.
go back to reference Habera LF, Berger PH, Reddick BB (1994) Molecular evidence from 3´-terminus sequence-analysis that tobacco vein-banding mosaic virus is a distinct member of the Potyvirus group. Arch Virol 138:27–38CrossRefPubMed Habera LF, Berger PH, Reddick BB (1994) Molecular evidence from 3´-terminus sequence-analysis that tobacco vein-banding mosaic virus is a distinct member of the Potyvirus group. Arch Virol 138:27–38CrossRefPubMed
16.
go back to reference Chin WT (1966) A survey of tobacco mosaic viruses in central Taiwan. J Agric Ass Chin 55:85–88 Chin WT (1966) A survey of tobacco mosaic viruses in central Taiwan. J Agric Ass Chin 55:85–88
17.
go back to reference Dean CE, Clark F (1968) Vein-banding on tobacco in North Florida. Plant Dis Rep 52:887–889 Dean CE, Clark F (1968) Vein-banding on tobacco in North Florida. Plant Dis Rep 52:887–889
18.
go back to reference Reddick BB, Collins-Shepard MH, Christie RG, Gooding GV (1992) A new virus-disease in North-America caused by Tobacco vein-banding mosaic virus. Plant Dis 76:856–859CrossRef Reddick BB, Collins-Shepard MH, Christie RG, Gooding GV (1992) A new virus-disease in North-America caused by Tobacco vein-banding mosaic virus. Plant Dis 76:856–859CrossRef
19.
go back to reference Zhang CL, Gao R, Wang J, Zhang GM, Li XD, Liu HT (2011) Molecular variability of Tobacco vein banding mosaic virus populations. Virus Res 15:188–198CrossRef Zhang CL, Gao R, Wang J, Zhang GM, Li XD, Liu HT (2011) Molecular variability of Tobacco vein banding mosaic virus populations. Virus Res 15:188–198CrossRef
20.
go back to reference Hu XJ, Alexander VK, Celeste JB, Jim HL (2009) Sequence characteristics of potato virus Y recombinants. J Gen Virol 90:3033–3041CrossRefPubMed Hu XJ, Alexander VK, Celeste JB, Jim HL (2009) Sequence characteristics of potato virus Y recombinants. J Gen Virol 90:3033–3041CrossRefPubMed
21.
go back to reference Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463CrossRefPubMedPubMedCentral Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463CrossRefPubMedPubMedCentral
22.
go back to reference Nylander JAA (2008) MrModeltest v2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University Nylander JAA (2008) MrModeltest v2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
23.
24.
go back to reference Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentral Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentral
25.
go back to reference Parker J, Rambaut A, Pybus OG (2008) Correlating viral phenotypes with phylogeny: Accounting for phylogenetic uncertainty. Infect Genet Evol 8:239–246CrossRefPubMed Parker J, Rambaut A, Pybus OG (2008) Correlating viral phenotypes with phylogeny: Accounting for phylogenetic uncertainty. Infect Genet Evol 8:239–246CrossRefPubMed
27.
go back to reference Kosakovsky Pond SL, Frost SDW, Grossman Z, Gravenor MB, Richman DD, Leigh Brown AJ (2006) Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PLoS Comput Biol 2:e62CrossRefPubMedCentral Kosakovsky Pond SL, Frost SDW, Grossman Z, Gravenor MB, Richman DD, Leigh Brown AJ (2006) Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PLoS Comput Biol 2:e62CrossRefPubMedCentral
28.
go back to reference Kosakovsky Pond SL, Murrell B, Fourment M, Frost SDW, Delport W, Scheffler K (2011) A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol 28:3033–3043CrossRefPubMedPubMedCentral Kosakovsky Pond SL, Murrell B, Fourment M, Frost SDW, Delport W, Scheffler K (2011) A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol 28:3033–3043CrossRefPubMedPubMedCentral
29.
go back to reference Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764CrossRefPubMedPubMedCentral Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764CrossRefPubMedPubMedCentral
30.
31.
go back to reference Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22(4):1107–1118CrossRefPubMed Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22(4):1107–1118CrossRefPubMed
32.
go back to reference Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMed Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMed
33.
go back to reference Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentral Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentral
34.
go back to reference Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentral Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentral
36.
go back to reference Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV (2012) Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29(9):2157–2167CrossRefPubMedPubMedCentral Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV (2012) Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29(9):2157–2167CrossRefPubMedPubMedCentral
37.
go back to reference Vaughan TG, Kühnert D, Popinga A, Welch D, Drummond AJ (2014) Efficient Bayesian inference under the structured coalescent. Bioinformatics 30(16):2272–2279CrossRefPubMedPubMedCentral Vaughan TG, Kühnert D, Popinga A, Welch D, Drummond AJ (2014) Efficient Bayesian inference under the structured coalescent. Bioinformatics 30(16):2272–2279CrossRefPubMedPubMedCentral
38.
go back to reference Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22(5):1185–1192CrossRefPubMed Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22(5):1185–1192CrossRefPubMed
41.
go back to reference Minin VN, Suchard MA (2008) Counting labeled transitions in continuous-time Markov models of evolution. J Math Biol 56:391–412CrossRefPubMed Minin VN, Suchard MA (2008) Counting labeled transitions in continuous-time Markov models of evolution. J Math Biol 56:391–412CrossRefPubMed
42.
go back to reference Traore O, Sorho F, Pinel A, Abubakar Z, Banwo O, Maley J et al (2010) Processes of diversification and dispersion of rice yellow mottle virus inferred from large-scale and high-resolution phylogeographical studies. Mol Ecol 14(7):2097–2110CrossRef Traore O, Sorho F, Pinel A, Abubakar Z, Banwo O, Maley J et al (2010) Processes of diversification and dispersion of rice yellow mottle virus inferred from large-scale and high-resolution phylogeographical studies. Mol Ecol 14(7):2097–2110CrossRef
43.
go back to reference Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process and rate. Syst Biol 57:591–601CrossRefPubMed Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process and rate. Syst Biol 57:591–601CrossRefPubMed
44.
go back to reference Caruso T, Chan Y, Lacap DC, Lau MC, McKay CP, Pointing SB (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413CrossRefPubMedPubMedCentral Caruso T, Chan Y, Lacap DC, Lau MC, McKay CP, Pointing SB (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413CrossRefPubMedPubMedCentral
45.
go back to reference Banke S, Lillemark MR, Gerstoft J, Obel N, Jørgensen LB (2009) Positive selection pressure introduces secondary mutations at Gag cleavage sites in Human immunodeficiency virus Type 1 harboring major protease resistance mutations. J Virol 83:8916–8924CrossRefPubMedPubMedCentral Banke S, Lillemark MR, Gerstoft J, Obel N, Jørgensen LB (2009) Positive selection pressure introduces secondary mutations at Gag cleavage sites in Human immunodeficiency virus Type 1 harboring major protease resistance mutations. J Virol 83:8916–8924CrossRefPubMedPubMedCentral
46.
go back to reference Yu SF, Benton P, Bovee M, Sessions J, Lloyd RE (1995) Defective RNA replication by poliovirus mutants deficient in 2A protease cleavage activity. J Virol 69:247–252PubMedPubMedCentral Yu SF, Benton P, Bovee M, Sessions J, Lloyd RE (1995) Defective RNA replication by poliovirus mutants deficient in 2A protease cleavage activity. J Virol 69:247–252PubMedPubMedCentral
47.
go back to reference Petrik K, Sebestyen E, Gell G, Balazs E (2010) Natural insertions within the N-terminal region of the coat protein of Maize dwarf mosaic potyvirus (MDMV) have an effect on the RNA stability. Virus Genes 40:135–139CrossRefPubMed Petrik K, Sebestyen E, Gell G, Balazs E (2010) Natural insertions within the N-terminal region of the coat protein of Maize dwarf mosaic potyvirus (MDMV) have an effect on the RNA stability. Virus Genes 40:135–139CrossRefPubMed
48.
go back to reference Ullah Z, Chai B, Hammar S, Raccah B, Galon A, Grumet R (2003) Effect of substitution of the amino termini of coat proteins of distinct potyvirus species on viral infectivity and host specificity. Physiol Mol Plant Pathol 63(3):129–139CrossRef Ullah Z, Chai B, Hammar S, Raccah B, Galon A, Grumet R (2003) Effect of substitution of the amino termini of coat proteins of distinct potyvirus species on viral infectivity and host specificity. Physiol Mol Plant Pathol 63(3):129–139CrossRef
49.
go back to reference Feki S, Bouslama L (2008) Molecular phylogeny and genetic variability of the Potato virus Y (PVY) strains on the CP-encoding region. Ann Microbiol 58(3):433–438CrossRef Feki S, Bouslama L (2008) Molecular phylogeny and genetic variability of the Potato virus Y (PVY) strains on the CP-encoding region. Ann Microbiol 58(3):433–438CrossRef
50.
go back to reference Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446PubMedPubMedCentral Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446PubMedPubMedCentral
51.
go back to reference Gao FL, Liu XW, Du ZG, Han Hou H, Wang XY, Wang FL, Yang JG (2019) Bayesian phylodynamic analysis reveals the dispersal patterns of tobacco mosaic virus in China. Virology 528:110–117CrossRefPubMed Gao FL, Liu XW, Du ZG, Han Hou H, Wang XY, Wang FL, Yang JG (2019) Bayesian phylodynamic analysis reveals the dispersal patterns of tobacco mosaic virus in China. Virology 528:110–117CrossRefPubMed
Metadata
Title
Genetic structure and variability of tobacco vein banding mosaic virus populations
Authors
Shiqing Wei
Xiaorong He
Die Wang
Jinyou Xiang
Yide Yang
Shu Yuan
Jing Shang
Hui Yang
Publication date
01-10-2019
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 10/2019
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-019-04342-6

Other articles of this Issue 10/2019

Archives of Virology 10/2019 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.