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Genetic diversity and population structure of Watermelon mosaic virus

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Abstract

Watermelon mosaic virus (WMV) is one of the most important viruses infecting a wide range of plant species. Population genetic analysis of WMV was performed based on the virus coat protein (CP) gene sequences of ten isolates identified in this study and 89 additional isolates from five different countries (China, France, Iran, Spain and the USA) in three continents: Asia, Europe and North America. Phylogenetic analysis showed that WMV isolates clustered in three phylogroups: Classical, Group 2 and Emerging with significant F ST values (>0.43). Chinese, French, Iranian, Spanish and USA WMV populations were composed of multiple lineages. Genetic differentiation analysis of WMV populations showed that the Iranian and Spanish populations were statistically distinct from the other populations. The ratio of non-synonymous to synonymous nucleotide diversity (dN/dS = ω) was <1, indicating that the CP gene of WMV has been under negative selection. Most of the codons in the CP were under negative selection (ω < 1) except for codon 87, which were significantly under positive selection. This study suggests that host adoption selection and founder effect were important evolutionary factors driving the genetic diversification of WMV.

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References

  • Bergua M, Luis-Arteaga M, Escriu F (2014) Genetic diversity, reassortment, and recombination in Alfalfa mosaic virus Population in Spain. Phytopathology 104:1241–1250

    Article  CAS  PubMed  Google Scholar 

  • Callaway A, Giesman-Cookmeyer D, Gillock ET, Sit TL, Lommel SA (2001) The multifunctional capsid proteins of plant RNA viruses. Annu Rev Phytopathol 39:419–460

    Article  CAS  PubMed  Google Scholar 

  • Chare ER, Holmes EC (2006) A phylogenetic survey of recombination frequency in plant RNA viruses. Adv Virol 151:933–946

    CAS  Google Scholar 

  • Chung CT, Niemela SA, Miller RH (1989) One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci 86:2172–2175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung BYW, Miller WA, Atkins JF, Firth AE (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci 105:5895–5902

    Google Scholar 

  • Deng XG, Zhu F, Li JY, Feng H, Xi DH, Lin HH (2014) Genetic diversity and phylogentic analysis of sweet potato feathery mottle virus and sweet potato virus g in Sichuan, China. J Plant Pathol 96:215–218

    Google Scholar 

  • 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. Adv Virol 149:1619–1632

    CAS  Google Scholar 

  • Desbiez C, Lecoq H (2008) Evidence for multiple intraspecific recombinants in natural populations of Watermelon mosaic virus (WMV Potyvirus). Adv Virol 153:1749–1754

    CAS  Google Scholar 

  • Desbiez C, Costa C, Wipf-Scheibel C, Girard M, Lecoq H (2007) Serological and molecular variability of Watermelon mosaic virus (genus Potyvirus). Adv Virol 152:775–781

    CAS  Google Scholar 

  • Desbiez C, Joannon B, Wipf-Scheibel C, Chandeysson C, Lecoq H (2009) Emergence of new strains of Watermelon mosaic virus in South-eastern France: evidence for limited spread but rapid local population shift. Virus Res 141:201–208

    Article  CAS  PubMed  Google Scholar 

  • Desbiez C, Joannon B, Wipf-Scheibel C, Chandeysson C, Lecoq H (2011) Recombination in natural populations of Watermelon mosaic virus: new agronomic threat or damp squib? J Gen Virol 92:1939–1948

    Article  CAS  PubMed  Google Scholar 

  • Domingo E, Holland JJ (1997) RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178

    Article  CAS  PubMed  Google Scholar 

  • Elena SF, Agudelo-Romero P, Carrasco P, Codoñer FM, Martín S, Torres-Barceló C, Sanjuán R (2008) Experimental evolution of plant RNA viruses. Heredity 100:478–483

    Article  CAS  PubMed  Google Scholar 

  • Foissac X, Savalle-Dumas P, Dulucq MJ, Gentit MJ, Candresse T (2000) Polyvalent detection of fruit tree Tricho, Capillo and Faveaviruses by nested RT-PCR using degenerated and inosine containing primers (PDO RT-PCR). Acta Hortic 550:37–43

    Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao F, Lin W, Shen J, Liao F (2015) Genetic diversity and molecular evolution of arabis mosaic virus based on the CP gene sequence. Adv Virol 161:1047–1051

    Google Scholar 

  • García-Andrés S, Gian Accotto GP, Navas-Castillo J, Moriones E (2007) Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the Mediterranean basin. Virology 359:302–312

    Article  PubMed  Google Scholar 

  • García-Arenal F, Fraile A, Malpica JM (2001) Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 39:157–186

    Article  PubMed  Google Scholar 

  • García-Arenal F, Fraile A, Malpica JM (2003) Variation and evolution of plant virus populations. Int Microbiol 6:225–232

    Article  PubMed  Google Scholar 

  • Glasa M, Bananej K, Predajňa L, Vahdat A (2011) Genetic diversity of watermelon mosaic virus in Slovakia and Iran shows distinct pattern. Plant Dis 95:38–42

    Article  Google Scholar 

  • Hajizadeh M, Mohammadi K (2016) Capsicum annum, a new host of watermelon mosaic virus. VirusDisease 27:107–109

    Article  PubMed  PubMed Central  Google Scholar 

  • He Z, Yasaka R, Lie W, Lia S, Ohshimac K (2016) Genetic structure of populations of Sugarcane streak mosaic virus in China: comparison with the populations in India. Virus Res 211:103–116

    Article  CAS  PubMed  Google Scholar 

  • Hudson RR, Boos DD, Kaplan NL (1992a) A statistical test for detecting population subdivision. Mol Biol Evol 9:138–151

    CAS  PubMed  Google Scholar 

  • Hudson RR, Slatkin M, Maddison WP (1992b) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Juarez M, Legua P, Mangual CM, Kassem MA, Sempere RN, Gomez P, Truniger V, Aranda MA (2013) Relative incidence, spatial distribution and genetic diversity of cucurbit viruses in eastern Spain. Ann Appl Biol 162:362–370

    Article  CAS  Google Scholar 

  • Kondo T, Kang D-K, Fuji S, Chung M-U (2003) Sequence diversity in the coat protein and 3-untranslated region of Chinese yam necrotic mosaic virus RNA. J Gen Plant Pathol 69:397–399

    Article  CAS  Google Scholar 

  • Laney AG, Avanzato MV, Tzanetakis IE (2012) High incidence of seed transmission of Papaya ringspot virus and Watermelon mosaic virus, two viruses newly identified in Robinia pseudoacacia. Eur J Plant Pathol 134:227–230

    Article  Google Scholar 

  • Moradi Z, Jafarpour B (2010) Mixed infections of Watermelon mosaic potyvirus and Cucumber green mottle mosaic tobamovirus in Cucurbit hosts. Plant Prot J 2:353–365

    Google Scholar 

  • Moreno IM, Malpica JM, Diaz-Pendon JA, Moriones E, Fraile A, Garcia-Arenal F (2004) Variability and genomic structure of the population of watermelon mosaic virus infecting melon in Spain. Virology 318:451–460

    Article  CAS  PubMed  Google Scholar 

  • Nakaune R, Inoue K, Nasu H, Kakogawa K, Nitta H, Imada J, Nakano M (2008) Detection of viruses associated with rugose wood in Japanese grapevines and analysis of genomic variability of Rupestris stem pitting-associated virus. J Gen Plant Pathol 74:156–163

    Article  CAS  Google Scholar 

  • Ogawa T, Tomitaka Y, Nakagawa A, Ohshima K (2008) Genetic structure of a population of Potato virus Y inducing potato tuber necrotic ringspot disease in Japan; comparison with North American and European populations. Virus Res 131:199–212

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pond SLK, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  CAS  PubMed  Google Scholar 

  • Purcifull D, Hiebert E, Edwardson J (1984) Watermelon mosaic virus 2. CMI/AAB Descriptions of Plant Viruses no. 293 (no. 63 revised). Kew, England, UK

  • Quemada H, Sieu LC, Siemieniak DR, Gonsalves D, Slightom JL (1990) Watermelon mosaic virus2 and Zucchini yellow mosaic virus: cloning of 3’-terminal regions, nucleotide sequences, and phylogenetic comparisons. J Gen Virol 71:1451–1460

    Article  CAS  PubMed  Google Scholar 

  • Rana T, Chandel V, Kumar Y, Ram R, Hallan V, Zaidi AA (2010) Molecular variability analyses of Apple chlorotic leaf spot virus capsid protein. J Biosci 35:605–615

    Article  CAS  PubMed  Google Scholar 

  • Rozas J (2009) DNA Sequence Polymorphism Analysis using DnaSP. In: Posada D (ed) Bioinformatics for DNA sequence analysis; methods in molecular biology. Humana Press, NJ, pp 337–350

    Chapter  Google Scholar 

  • Rubio L, Guerri J, Moreno P (2013) Genetic variability and evolutionary dynamics of viruses of the family Closteroviridae. Front Microbiol 4:1–15

    Article  Google Scholar 

  • Salvaudon L, De Moraes CM, Mescher MC (2013) Outcomes of co-infection by two potyviruses: implications for the evolution of manipulative strategies. Proc Biol Sci 280:20122959

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharifi M, Massumi H (2008) Analysis of the biological and molecular variability of Watermelon mosaic virus (WMV) isolate from Iran. Virus Genes 37:304–313

    Article  CAS  PubMed  Google Scholar 

  • Shimomoto Y, Takeuchi S (2006) Simultaneous detection of three Potyvirus species from Cucurbitaceae crops by multiplex RT-PCR. Jpn J Phytopathol 72:146–149

    Article  CAS  Google Scholar 

  • Shoeibi SM, Massumi S, Nasrollahnezhad S, Heydari K, Izadpanah K, Ahmadikhah A (2009) Sequencing of six Iranian isolates of Watermelon mosaic virus and phylogenetic comparison of Iranianisolates with other isolates of the world. Iran J Plant Pathol 45:34–37

    Google Scholar 

  • Skotnicki ML, Mackenzie AM, Gibbs AJ (1996) Genetic variation in populations of kennedya yellow mosaic tymovirus. Adv Virol 141:99–110

    CAS  Google Scholar 

  • Sokhandan-Bashir N, Melcher U (2012) Population genetic analysis of grapevine fanleaf vius. Adv Virol 157:1919–1929

    CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Feng C, Hao X, Sou M, Zhang J, Wang Q, Wu Y (2014) Complete genome sequence analyses of Watermelon mosaic virus isolate from China. J Plant Pathol 96:585–588

    Google Scholar 

Download references

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Authors and Affiliations

  1. Plant Protection Department, Faculty of Agriculture, University of Kurdistan, P.O. Box 416, Sanandaj, Iran

    Mohammad Hajizadeh, Hajareh Bahrampour & Jafar Abdollahzadeh

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  1. Mohammad Hajizadeh
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  2. Hajareh Bahrampour
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  3. Jafar Abdollahzadeh
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Correspondence to Mohammad Hajizadeh.

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Hajizadeh, M., Bahrampour, H. & Abdollahzadeh, J. Genetic diversity and population structure of Watermelon mosaic virus . J Plant Dis Prot 124, 601–610 (2017). https://doi.org/10.1007/s41348-017-0114-8

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