POPULATION GENETICS ANALYSIS OF Garlic virus A, Garlic virus B, Garlic virus C AND Garlic virus X
Maria Bereda
Department of Plant Pathology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, PolandElżbieta Paduch-Cichal
Department of Plant Pathology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, PolandAbstract
Garlic virus A (GarV-A), Garlic virus B (GarV-B), Garlic virus C (GarV-C) and Garlic virus X (GarV-X) are members of the genus Allexivirus in the family Alphaflexiviridae. In this study, we collected 10, 30, 10 and 14 isolates of GarV-A, GarV-B, GarV-C and GarV-X, respectively, from different parts of Poland. All sequences of coat protein (CP) and nucleic-acid binding protein (NABP) regions of Allexivirus isolates available in GenBank were also included in this study. The nucleotide and amino acid sequences identities within each population differed substantially depending on the region of the genome and virus species. The results of selection pressure analysis showed that populations of each Allexivirus underwent negative selection, but the extent of the negative selection varied. It was also concluded that the GarV-A and GarV-C populations underwent a decrease in population size or balancing selection, while the GarV-B and GarV-X populations underwent an increase in population size. It was concluded that both populations of GarV-X evolved independently in each respective area, in contrast to populations of GarV-A, GarV-B and GarV-C.
Keywords:
allexiviruses, recombination, sequences similarities, phylogenetic analysisReferences
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Bereda, M., Paduch-Cichal, E., Kalinowska, E., Szyndel, M.S. (2015a). Genetic diversity and evidence of recombination in the coat protein gene of Onion yellow dwarf virus. Eur. J. Plant Pathol., 142, 377–387.
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Chare, E.R., Holmes, E.C. (2005). A phylogenetic survey of recombination frequency in plant RNA viruses. Arch. Virol., 151, 933–946.
Chen, J., Chen, J. (2002). Genome organization and phylogenetic tree analysis of Garlic virus E, a new member of genus Allexivirus. Chin. Sci. Bull., 47, 33–37.
Chen, J., Zheng, H.Y., Antoniw, J.F., Adams, M.J., Chen, J.P., Lin, L. (2004). Detection and classification of allexiviruses from garlic in China. Arch. Virol., 149, 435–445.
Chodorska, M., Paduch-Cichal, E., Kalinowska, E., Szyndel, M.S. (2014). Assessment of allexiviruses infection in garlic plants in Poland. Acta Sci. Pol. Hortorum Cultus, 13(2), 179–186.
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.
Domingo, E., Holland, J.J. (1997). RNA virus mutations and fitness for survival. Annu. Rev. Microbiol., 51, 151–178.
Drake, J.W., Holland, J.J. (1999). Mutation rates among RNA viruses. Proc. Natl. Acad. Sci., 96, 13910–13913.
Eigen, M., Biebricher, C.K. (1988). Sequence space and quasispecies distribution: In: RNA genetics, Domingo, E., Holland, J.J., Ahlquist, P. (ed.), vol. 3. CRC Press, Boca Raton, 211–245.
Eigen, M. (1996). On the nature of virus quasispecies. Trends Microbiol., 4, 216–218.
Feng, X., Poplawsky, A.R., Nikolaeva, O.V., Myers, J.R., Karasev, A.V. (2014). Recombinants of Bean common mosaic virus (BCMV) and genetic determinants of BCMV involved in overcoming resistance in common bean. Phytopathology, 104, 786–793.
Fidan, H., Çağlar, B.K., Baloğlu, S., Yılmaz, M.A. (2015). Urginea maritime (L.) is a new host of Allexivirus group on onion and garlic plants in Turkey. Acta Hortic., 1002, 309–312.
Fu, Y.X., Li, W.H. (1993). Statistical tests of neutrality of mutations. Genetics, 133, 693–709.
García-Arenal, F., Fraile, M., Malpica, J.M. (2001). Variability and genetic structure of plant virus populations. Annu. Rev. Phytopathol., 39, 157–186.
García-Arenal, F., Fraile, A., Malpica, J.M. (2003). Variation and evolution of plant virus populations. Int. Microbiol., 6, 225–232.
Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser., 41, 95–98.
King, A.M., Adams, M.J., Lefkowitz, E.J., Carstens, E.B. (2012). Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier.
Kosakovsky Pond, S.L., Frost, S.D.W. (2005). Datamonkey: rapid detection of selective pressures on individual sites of codon alignments. Bioinformatics, 21, 2531–2533.
Kosakovsky Pond, S.L., Posada, D., Gravenor, M.B., Woelk, C.H., Frost, S.D.W. (2006). Automated phylogenetic detection of recombination using a genetic algorithm. Mol. Biol. Evol., 23, 1891–1901.
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Lian, S., Lee, J., Cho, W., Yu, J., Kim, M., Choi, H., Kim, K. (2013). Phylogenetic and recombination analysis of tomato spotted wilt virus. PloS ONE, 8(5), e63380.
Librado, P., Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
Malinowski, T. (1997). Silica capture-reverse transcription-polymerase chain reaction (SC-RT-PCR): application for the detection of several plant viruses. In: Diagnosis and identification of plant pathogens, proceedings of 4th international EFPP symposium Bonn, 9–12 September 1996, Dehne, H.W., Adam, G., Diekmann, M., Rahm, J., Mauler-Machnik, A., van Halteren, P. (eds.). Kluwer Academic Publishers, Budapest, 445–448 pp.
Martin, D.P. (2009). Recombination detection and analysis using RDP3. Methods Mol. Biol., 537, 185–205.
Melo-Filho, P.A., Nagata, T., Dusi, A.N., Buso, J.A., Torres, A.C., Eiras, M., Resende, R.O. (2004). Detection of three Allexivirus species infecting garlic in Brazil. Pesq. Agropec. Bras., 39, 375–340.
Mohammed, H.S., Zicca, S., Manglli, A., Mohamed, M.E., El Siddig, M.A.R., El Hussein, A.A., Tomassoli, L. (2013). Occurrence and phylogenetic analysis of Potyviruses, Carlaviruses and Allexiviruses in garlic in Sudan. J. Phytopathol, 161, 642–650.
Moradi, Z., Nazifi, E., Mehrvar, M. (2017). Occurrence and evolutionary analysis of coat protein gene sequences of Iranian isolates of Sugarcane mosaic virus. Plant Path. J., 33, 296–306.
Moutailler, S., Roche, B., Thiberge, J.M., Caro, V., Rougeon, F., Failloux, A.B. (2011). Host alternation is necessary to maintain the genome stability of Rift valley fever virus. PLoS Negl. Trop. Dis., 5, e1156.
Ohshima, K., Yamaguchi, Y., Hirota, R., Hamamoto, T., Tomimura, K., Tan, Z., et al. (2002). Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J. Gen. Virol., 83, 1511–1521.
Ohshima, K., Akaishi, S., Kajiyama, H., Koga, R., Gibbs, A.J. (2010). Evolutionary trajectory of turnip mosaic virus populations adapting to a new host. J. Gen. Virol., 91, 788–801.
Olarte Castillo, X.A., Ferminb, G., Tabimaa, J., Rojasb, Y., Tennantc, P.F., Fuchs, M., et al. (2011). Phylogeography and molecular epidemiology of Papaya ringspot virus. Virus Res., 159, 132–140.
Oliveira, M.L., De Marchi, D.R., Mituti, T., Pavan, M.A., Krause-Sakate, R. (2014). Identification and sequence analysis of five allexiviruses species infecting garlic crops in Brazil. Trop. Plant. Pathol., 39, 483–489.
Seo, J.K., Ohshima, K., Lee, H.G., So, M., Choi, H.S., Lee, S.H., Sohn, S.H., Kim, K.H. (2009). Molecular variability and genetic structure of the population of Soybean mosaic virus based on the analysis of complete genome sequences. Virology, 393, 91–103.
Simon-Loriere, E., Holmes, E.C. (2011). Why do RNA viruses recombine? Nat. Rev. Microbiol., 9, 617–626.
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.
Uzcategui, N.Y., Camacho, D., Comach, G., Cuello de Uzcategui, R., Holmes, E.C., Gould, E.A. (2001). Molecular epidemiology of dengue type 2 virus in Venezuela: evidence for in situ virus evolution and recombination. J. Gen. Virol., 82, 2945–2953.
Vishnichenko, V.K., Konareva, T.N., Zavriev, S.K. (1993). A new filamentous virus in shallot. Plant Pathol., 42, 12–126.
Wylie, S.J., Li, H., Jones, M.G.K. (2012). Phylogenetic analysis of allexiviruses identified on garlic from Australia. Australas. Plant Dis. Notes, 7, 23–27.
Wylie, S.J., Li, H., Saqib, M., Jones, M.G.K. (2014). The global trade in fresh produce and the vagility of plant viruses: a case study in garlic. PloS ONE, 9, e105044.
Zhou, Z.S., Dell’Orco, M., Saldarelli, P., Turturo, C., Minafra, A., Martelli, G.P. (2006). Identification of an RNA silencing suppressor in the genome of Grapevine virus A. J. Gen. Virol., 87, 2387–2395.
Bereda, M., Kalinowska, E., Paduch-Cichal, E., Szyndel, M.S. (2015). Low genetic diversity of a natural population of Garlic virus D from Poland. Eur. J. Plant Pathol., 142, 411–417.
Bereda, M., Paduch-Cichal, E., Kalinowska, E., Szyndel, M.S. (2015a). Genetic diversity and evidence of recombination in the coat protein gene of Onion yellow dwarf virus. Eur. J. Plant Pathol., 142, 377–387.
Boom, R., Sol, C.J.A., Salimans, M.M.M., Jansen, C.L., Wertheim-Van Dillen, P.M.E., van der Nordaa, J., (1990). Rapid and simple method for purification of nucleic acids. J. Clin. Microbiol., 28, 495–503.
Chare, E.R., Holmes, E.C. (2005). A phylogenetic survey of recombination frequency in plant RNA viruses. Arch. Virol., 151, 933–946.
Chen, J., Chen, J. (2002). Genome organization and phylogenetic tree analysis of Garlic virus E, a new member of genus Allexivirus. Chin. Sci. Bull., 47, 33–37.
Chen, J., Zheng, H.Y., Antoniw, J.F., Adams, M.J., Chen, J.P., Lin, L. (2004). Detection and classification of allexiviruses from garlic in China. Arch. Virol., 149, 435–445.
Chodorska, M., Paduch-Cichal, E., Kalinowska, E., Szyndel, M.S. (2014). Assessment of allexiviruses infection in garlic plants in Poland. Acta Sci. Pol. Hortorum Cultus, 13(2), 179–186.
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.
Domingo, E., Holland, J.J. (1997). RNA virus mutations and fitness for survival. Annu. Rev. Microbiol., 51, 151–178.
Drake, J.W., Holland, J.J. (1999). Mutation rates among RNA viruses. Proc. Natl. Acad. Sci., 96, 13910–13913.
Eigen, M., Biebricher, C.K. (1988). Sequence space and quasispecies distribution: In: RNA genetics, Domingo, E., Holland, J.J., Ahlquist, P. (ed.), vol. 3. CRC Press, Boca Raton, 211–245.
Eigen, M. (1996). On the nature of virus quasispecies. Trends Microbiol., 4, 216–218.
Feng, X., Poplawsky, A.R., Nikolaeva, O.V., Myers, J.R., Karasev, A.V. (2014). Recombinants of Bean common mosaic virus (BCMV) and genetic determinants of BCMV involved in overcoming resistance in common bean. Phytopathology, 104, 786–793.
Fidan, H., Çağlar, B.K., Baloğlu, S., Yılmaz, M.A. (2015). Urginea maritime (L.) is a new host of Allexivirus group on onion and garlic plants in Turkey. Acta Hortic., 1002, 309–312.
Fu, Y.X., Li, W.H. (1993). Statistical tests of neutrality of mutations. Genetics, 133, 693–709.
García-Arenal, F., Fraile, M., Malpica, J.M. (2001). Variability and genetic structure of plant virus populations. Annu. Rev. Phytopathol., 39, 157–186.
García-Arenal, F., Fraile, A., Malpica, J.M. (2003). Variation and evolution of plant virus populations. Int. Microbiol., 6, 225–232.
Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser., 41, 95–98.
King, A.M., Adams, M.J., Lefkowitz, E.J., Carstens, E.B. (2012). Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier.
Kosakovsky Pond, S.L., Frost, S.D.W. (2005). Datamonkey: rapid detection of selective pressures on individual sites of codon alignments. Bioinformatics, 21, 2531–2533.
Kosakovsky Pond, S.L., Posada, D., Gravenor, M.B., Woelk, C.H., Frost, S.D.W. (2006). Automated phylogenetic detection of recombination using a genetic algorithm. Mol. Biol. Evol., 23, 1891–1901.
Kumar, S., Stecher, G., Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol., 33(7), 1870–1874.
Lian, S., Lee, J., Cho, W., Yu, J., Kim, M., Choi, H., Kim, K. (2013). Phylogenetic and recombination analysis of tomato spotted wilt virus. PloS ONE, 8(5), e63380.
Librado, P., Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
Malinowski, T. (1997). Silica capture-reverse transcription-polymerase chain reaction (SC-RT-PCR): application for the detection of several plant viruses. In: Diagnosis and identification of plant pathogens, proceedings of 4th international EFPP symposium Bonn, 9–12 September 1996, Dehne, H.W., Adam, G., Diekmann, M., Rahm, J., Mauler-Machnik, A., van Halteren, P. (eds.). Kluwer Academic Publishers, Budapest, 445–448 pp.
Martin, D.P. (2009). Recombination detection and analysis using RDP3. Methods Mol. Biol., 537, 185–205.
Melo-Filho, P.A., Nagata, T., Dusi, A.N., Buso, J.A., Torres, A.C., Eiras, M., Resende, R.O. (2004). Detection of three Allexivirus species infecting garlic in Brazil. Pesq. Agropec. Bras., 39, 375–340.
Mohammed, H.S., Zicca, S., Manglli, A., Mohamed, M.E., El Siddig, M.A.R., El Hussein, A.A., Tomassoli, L. (2013). Occurrence and phylogenetic analysis of Potyviruses, Carlaviruses and Allexiviruses in garlic in Sudan. J. Phytopathol, 161, 642–650.
Moradi, Z., Nazifi, E., Mehrvar, M. (2017). Occurrence and evolutionary analysis of coat protein gene sequences of Iranian isolates of Sugarcane mosaic virus. Plant Path. J., 33, 296–306.
Moutailler, S., Roche, B., Thiberge, J.M., Caro, V., Rougeon, F., Failloux, A.B. (2011). Host alternation is necessary to maintain the genome stability of Rift valley fever virus. PLoS Negl. Trop. Dis., 5, e1156.
Ohshima, K., Yamaguchi, Y., Hirota, R., Hamamoto, T., Tomimura, K., Tan, Z., et al. (2002). Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J. Gen. Virol., 83, 1511–1521.
Ohshima, K., Akaishi, S., Kajiyama, H., Koga, R., Gibbs, A.J. (2010). Evolutionary trajectory of turnip mosaic virus populations adapting to a new host. J. Gen. Virol., 91, 788–801.
Olarte Castillo, X.A., Ferminb, G., Tabimaa, J., Rojasb, Y., Tennantc, P.F., Fuchs, M., et al. (2011). Phylogeography and molecular epidemiology of Papaya ringspot virus. Virus Res., 159, 132–140.
Oliveira, M.L., De Marchi, D.R., Mituti, T., Pavan, M.A., Krause-Sakate, R. (2014). Identification and sequence analysis of five allexiviruses species infecting garlic crops in Brazil. Trop. Plant. Pathol., 39, 483–489.
Seo, J.K., Ohshima, K., Lee, H.G., So, M., Choi, H.S., Lee, S.H., Sohn, S.H., Kim, K.H. (2009). Molecular variability and genetic structure of the population of Soybean mosaic virus based on the analysis of complete genome sequences. Virology, 393, 91–103.
Simon-Loriere, E., Holmes, E.C. (2011). Why do RNA viruses recombine? Nat. Rev. Microbiol., 9, 617–626.
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.
Uzcategui, N.Y., Camacho, D., Comach, G., Cuello de Uzcategui, R., Holmes, E.C., Gould, E.A. (2001). Molecular epidemiology of dengue type 2 virus in Venezuela: evidence for in situ virus evolution and recombination. J. Gen. Virol., 82, 2945–2953.
Vishnichenko, V.K., Konareva, T.N., Zavriev, S.K. (1993). A new filamentous virus in shallot. Plant Pathol., 42, 12–126.
Wylie, S.J., Li, H., Jones, M.G.K. (2012). Phylogenetic analysis of allexiviruses identified on garlic from Australia. Australas. Plant Dis. Notes, 7, 23–27.
Wylie, S.J., Li, H., Saqib, M., Jones, M.G.K. (2014). The global trade in fresh produce and the vagility of plant viruses: a case study in garlic. PloS ONE, 9, e105044.
Zhou, Z.S., Dell’Orco, M., Saldarelli, P., Turturo, C., Minafra, A., Martelli, G.P. (2006). Identification of an RNA silencing suppressor in the genome of Grapevine virus A. J. Gen. Virol., 87, 2387–2395.
Maria Bereda
Department of Plant Pathology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland
Department of Plant Pathology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland
Elżbieta Paduch-Cichal
Department of Plant Pathology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland
Department of Plant Pathology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland
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