Isaac Scientific Publishing

Journal of Advances in Molecular Biology

Evidence for Recombination in the Emerged Phylogroup SW6 of Prunus Necrotic Ringspot Virus and Estimate of Selection Pressure Acting on Capsid Protein of Affiliated Members

Download PDF (689.6 KB) PP. 53 - 71 Pub. Date: June 8, 2017

DOI: 10.22606/jamb.2017.11004

Author(s)

  • Moncef Boulila*
    Institut de l’Olivier B.P. 14; 4061 Sousse Ibn-Khaldoun, Tunisia

Abstract

Recombination plays a key role in virus evolution. Except a limited number of works carried out so far on recombination in Prunus necrotic ringspot virus (PNRSV) genome, knowledge is still poor. Numerous phylogenetic studies particularly those based on capsid (CP) and movement protein (MP) of PNRSV showed that all accessions described so far split into three major phylogroups, i.e., PV96, PV32, and PE5. With the recent characterization of Chilean and Indian isolates which were phylogenetically closely related to the oldest member, i.e., SW6 (AF013287) from USA, a new phylogroup baptized SW6, emerged since it was outside of the evolutionary behavior of the classical PV96, PV32, and PE5 clusters. In order to understand how it evolved, six computerized methods were used to detect potential recombination in the CP sequences of nine components forming SW6 phylogroup. It was clearly demonstrated that various members underwent recombination. Additionally, networked relationships among them proved that numerous incompatibilities occurred in these sequences illustrated by the presence of boxes in the network implying therefore the possibility of recombination. According to inferred network, several sequences contained conflicting signals as illustrated by various splits and edges with special reference to Chilean (EF565255, EF565256), polish (AF332614) and Indian (AM494934) isolates. It is worth noting that the phylogenetic network provided a different clustering compared to the bifurcating tree. In fact, three distinct groups were delineated with SplitsTree4 software instead of a globally homogenous ensemble generated by MEGA7 algorithm. Furthermore, this study pointed out that members of SW6 phylogroup were the only recombinants among 205 tested accessions confirming that SW6 should be considered as the fourth phylogenetic group of PNRSV. On the other hand, CP was predominantly under purifying selection. However, positive selection was evidenced particularly in the C-terminal region of CP comprising part of dimerization region (DR). Such adaptive selection was exerted on a CP segment of AM494934 accession exchanged by recombination.

Keywords

Recombination, network, bifurcating tree, selection, bioinformatics, PNRSV

References

[1] E.P. Rybicki, “Bromoviridae. In the sixth report of the International Committee on Taxonomy of Viruses,”. Eds, F.A. Murphy, C.M. Fauquet, D.H.L. Bishop, S.A. Ghabrial, A.W. Jarvis, G.P. Martelli, M.A. Mayo, and M.D. Summers (eds.) , Springer-Verlag, Vienna, Austria, pp. 405-457, 1995.

[2] A.M.Q. Adams M.J. King, E.B. Carstens, E.J. Lefkowitz, “Classification and nomenclature of viruses. In: Virus taxonomy,”. Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, 2011.

[3] L. Van Vloten-Doting, R.I.B. Francki, R.W. Fulton, J.M. Kaper, L.C. Lane, “Tricornaviridae- a proposed family of plant viruses with tripartite single-stranded RNA genomes,”. Intervirology, vol. 15, pp. 198-203, 1981.

[4] E.J. Bachman, S.W. Scott, G.E. Xin, V.B. Vance, “The complete nucleotide sequence of Prune dwarf virus RNA3: implication for coat protein activation of genome replication in ilarviruses,”. Virology, vol. 201, pp. 127-131, 1994.

[5] D. Guo, E. Maiss, G. Adam, R. Casper, “Prunus necrotic ringspot ilarvirus: Nucleotide sequence of RNA 3 and the relationship to other ilarviruses based on coat protein comparison,”. J. Gen. Virol., vol. 76, pp. 1073-1079, 1995.

[6] R.W. Hammond, J.M. Crosslin, “The complete nucleotide sequence of RNA 3 of a peach isolate of Prunus necrotic ringspot virus,”. Virology, vol. 208, pp. 349-353, 1995.

[7] S.W. Scott, X. Ge,“The complete nucleotide sequence of RNA 3 of Citrus leaf rugose and Citrus variegation ilarviruses,“. J. Gen. Virol., vol. 76, pp. 957-963, 1995.

[8] D. Vaskova, K. Petrzik, R. Karesova, “Variability and molecular typing of the woody-tree infecting Prunus necrotic ringspot ilarvirus,”. Arch. Virol., vol. 145, pp. 699-709, 2000.

[9] F. M. Codo?er, J. M. Cuevas, J. A. Sanchez-Navarro, V. Pallas, S. F. Elena, “Molecular evolution of the plant virus family Bromoviridae based on RNA3-encoded proteins”. J. Mol. Evol., vol. 61, pp. 697-705, 2005.

[10] N. Fiore, T.V.M. Fajardo, S. Prodan, M.C. Herranz, F. Aparicio, J. Montealegre, S.F. Elena, V. Pallas, J. Sanchez-Navarro, “Genetic diversity of the movement and coat protein genes of South American isolates of Prunus necrotic ringspot virus,”. Arch. Virol., vol. 153, no. 5, pp. 909-919, 2008.

[11] J.E. Oliver, J. Freer., R.L. Andersen, K.D. Cox, T.L. Robinson, M. Fuchs, “Genetic diversity of Prunus necrotic ringspot virus isolates within a cherry orchard in New York,”. Plant Dis., vol. 93, pp. 599-606, 2009.

[12] F. Aparicio, A. Myrta, B. Di Terlizzi, V. Pallas, “Molecular variability among isolates of Prunus necrotic ringspot virus from different Prunus spp. Phytopathology, vol. 89, pp. 991-999, 1999.

[13] F. Aparicio, V. Pallás “Molecular variability analysis of the RNA 3 of fifteen isolates of Prunus necrotic ringspot virus sheds light on the minimal requirements for the synthesis of the subgenomic RNA,”. Virus Genes, vol. 25,pp. 75-84, 2002.

[14] M. Glasa, E. Betinová, O. Kúdela, Z. Subr, “Biological and molecular characterization of Prunus necrotic ringspot virus isolates and possible approaches to their phylogenetic typing,”. Ann. App. Biol., vol. 140, pp. 279-283, 2002.

[15] M. Boulila, “Putative recombination events and evolutionary history of five economically important viruses of fruit trees based on the coat protein-encoding gene sequence analysis,”. Biochem. Genet. vol. 48, pp. 357-375, 2010.

[16] M. Boulila, S. Ben Tiba, S. Jilani, “Molecular adaptation within the coat-protein-encoding gene of Tunisian almond isolates of Prunus necrotic ringspot virus,”. J. Gen., vol. no. 921, pp. 11-24, 2013.

[17] M.A. Larkin, G. Blackshileds, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, D.G. Higgins, “Clustal W and Clustal X version 2.0,”. Bioinformatics, vol. 23, pp. 2947-2948, 2007.

[18] F. Corpet, “Multiple sequence alignment with hierarchical clustering,”. Nucl. Acids Res., vol. 16, pp. 10881-10890.1988.

[19] S. Kumar, G. Stecher, K. Tamura, “MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets,”. Mol. Biol. Evol., vol. 33, no. 7, pp. 1870–1874, 2016.

[20] M. Kimura, “A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences,”. J. Mol. Evol. 16, pp. 111-120, 1980.

[21] D.H. Huson, D. Brayant, “Application of phylogenetic networks in evolutionary studies,”. Mol. Biol. Evol., vol. 23, vol. 2, pp. 254–267, 2006.

[22] K.S. Lole, R.C. Bollinger, R.S. Paranjape, D. Gadkari, S.S. Kulkarni, N.G. Novak, R. Ingersoll, H.W. Sheppard, S.C. Ray, “Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination,”. J. Virol., vol. 73, no. 1, pp. 152-160.

[23] D.P. Martin, B. Murrell, M. Golden, A. Khoosal, B. Muhire, “RDP4: Detection and analysis of recombination patterns in virus genomes”. Virus Evol. vol 1, no. 1, pp. 1-5, 2015.

[24] D. Martin, E. Rybicki, RDP: “detection of recombination amongst aligned sequences,”. Bioinformatics, vol. 16, pp. 562-563, 2000

[25] M. Padidam, S. Sawyer, C.M. Fauquet, “Possible emergence of new geminiviruses by frequent recombination,”. Virology, vol. 265, pp. 218-225. 1999.

[26] D.P. Martin, D. Posada, K.A. Crandall, C. Williamson, “A modified bootscan algorithm for automated identification of recombination sequences and recombination breakpoints,”. AIDS Res. Hum Retrov., vol. 21, pp. 98-102. 2005.

[27] J.M. Smith, “Analyzing the mosaic structure of genes,”. J. Mol. Evol., vol. 34, pp. 126-129, 1992.

[28] D. Posada, K. “Crandall Evaluation of methods for detecting recombination from DNA sequences: Computer simulation”. Proc. Nat. Acad. Sci. vol. 98, pp. 13757-13762, 2001.

[29] M.J. Gibbs, J.S. Armstrong, A.J. Gibbs, “Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences,”. Bioinformatics, vol. 16, pp. 573-582, 2000.

[30] M.F. Boni, D. Posada, M.W. Feldman, “An exact nonparametric method for inferring mosaic structure in sequence triplets,”. Genetics, vol. 176, pp. 1035-1047, 2007.

[31] T. Huber, G. Faulkner, P. Hugenholtz, “Bellerophon: A program to detect chimeric sequences in multiple sequence alignments,”. Bioinformatics, vol. 20, 2317-2319, 2004.

[32] P. Librado, J. Rozas, DnaSP v5: “A software for comprehensive analysis of DNA polymorphism data,””. Bioinformatics, vol. 25, pp. 1451-1452, 2009.

[33] S.L. Kosakovsky Pond, D. Posada, M.B. Gravenor, C.H. Woelk, S.D. Frost, “GARD: a genetic algorithm for recombination detection,”. Bioinformatics, vol. 22, no. 24, pp. 3096-3098, 2006a.

[34] S.L. Kosakovsky Pond, D. Posada, M.B. Gravenor, C.H. Woelk, S.D. Frost, “Automated phylogenetic detection of recombination using a genetic algorithm,”. Mol. Biol. Evol. vol. 23, pp. 1891-1901, 2006b.

[35] H. Akaike, “A new look at the statistical model identification”. IEEE Trans. Autom. AC, vol. 19, pp. 716-723, 1974.

[36] H. Kishino, M. Hasegawa “Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea,”. J. Mol. Evol. vol. 29, pp. 170-179, 1989.

[37] S.L. Kosakovsky Pond, S.D.W. Frost, S.V. Muse, “HyPhy: hypothesis testing using phylogenies,”. Bioinformatics, vol. 21, pp. 676-679, 2005.

[38] F. Tajima “Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism,”. Genetics, vol. 123, pp. 585-595, 1989.

[39] Y. .X, Fu, W.H. Li, “Statistical tests of neutrality of mutations”. Genetics, vol. 133, pp. 639-709, 1993

[40] G.A. Watterson, “On the number of segregating sites in general models without recombination”. Theor. Popul. Biol., vol. 7, pp. 256-276, 1975

[41] B. Korber, “HIV signatures and similarities. In: Computational and Evolutionary Analysis of HIV Molecular Sequences”, A.G. Rodrigo and G.H. Learn Jr. Dordrecht, The Netherlands: Kluwer Academic Publishers Ed., pp. 55-72, 2000.

[42] S.L. Kosakovsky Pond, S.D.W. Frost, “Datamonkey: rapid detection of selective pressure on individual sites of codon alignments, “. Bioinformatics, vol. 21, pp. 2531-2533. 2005a.

[43] S.L. Kosakovsky Pond, S.D.W. Frost, “A genetic algorithm approach to detecting lineage-specific variation in selection pressure,”. Mol. Biol. Evol., vol. 22, pp. 478-485. 2005b.

[44] S.L. Kosakovsky Pond, S.D. Frost, Z. Grossman, M.B. Gravenor, D.D. Richman, A.J. Brown, “Adaptation to different human populations by HIV-1 revealed by codon-based analyses,”. PLOS Comput. Biol., vol. 2, pp. 530-538, 2006c.

[45] B. Murrell, J.O. Wertheim, S. Moola, T. Weighill, K. Scheffler, S.L. Kosakovsky Pond, Detecting individual sites subject to episodic diversifying selection. PLOS Genetics 8: e1002764. doi:10.1371/journal.pgen.1002764. 2012.

[46] B. Murrell, S. Moola, A Mabona., T. Weighill, D. Sheward, S.L. Kosakovsky Pond, K. Scheffler, FUBAR: A Fast, Unconstrained Bayesian AppRoximation for inferring selection. Mol. Biol. Evol., vol. 30, pp. 1196-1205, 2013.

[47] K. Scheffler, D.P. Martin, C. Seoighe “Robust inference of positive selection from recombining coding sequences,”. Bioinformatics, vol. 22, pp. 2493-2499, 2006.

[48] W. Delport, A.F.Y. Poon, S.D.W. Frost, S.L. Kosakovsky Pond, “Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology,”. Bioinformatics, vol. 29, pp. 2455-2457, 2010.

[49] G.C. Conant, G.P. Wagner, P.F. Stadler “Modeling amino acid substitution pattern in orthologous genes,”. Mol. Phyl. Evol., vol. 42, no. 2, pp. 298-307, 2007.

[50] W.R. Atchley, J. Zhao, A.D. Fernandes, T. Druke “Solving the protein sequence metric problem,”. PNAS, vol.102, no. 18, pp. 6395-6400, 2005.

[51] B. Murrell, S. Weaver, M. D. Smith, J. O. Wertheim, S. Murrell, A. Aylward, K. Eren, T. Pollner, D. P. Martin, D. M. Smith, K. Scheffler, S. L. Kosakovsky Pond, “Gene-Wide Identification of Episodic Selection”. Mol. Biol. Evol., vol. 32, no. 5, pp. 1365–1371, 2015.

[52] S.W. Scott, M.T. Zimmerman, Xin Ge, D.J. MacKenzie, “The coat protein and putative movement proteins of isolates of Prunus necrotic ringspot virus from different host species and geographic origins are extensively conserved,”. Europ. J. Plant Pathol., vol. 104, pp. 155–161, 1998.

[53] V. Chandel, T. Rana, V. Hallan, A.A. Zaidi, “Occurrence of Prunus necrotic ringspot virus on nectarine (Prunus persica) in India,”. Europ. Plant Prot. Org. (EPPO), vol. 38, pp. 223-225, 2008a.

[54] V. Chandel, T. Rana, A. Handa, P.D. Thakur, V. Hallan, A.A. Zaidi, “Incidence of Prunus necrotic ring spot virus on Malus domestica in India,”. J. Phytopathol., vol. 156, pp. 382-384, 2008b.

[55] V. Chandel, T. Rana, V. Hallan, A.A. Zaidi, “Detection of Prunus necrotic ringspot virus in plum, cherry and almond by serological and molecular techniques from India,”. Arch. Pytopathol. Plant Prot., vol. 44, no. 18, pp. 1779–1784, 2011.

[56] M. Boulila “Molecular evidence for recombination in Prunus necrotic ringspot virus,”. Plant Mol. Biol. Rep., vol. 27, pp. 189-198, 2009.

[57] F. Aparicio, J. A. Sánchez-Navarro, V. Pallás, “In vitro and in vivo mapping of the Prunus necrotic ringspot virus coat protein C-terminal dimerization domain by bimolecular fluorescence complementation”. J. Gen. Virol., vol. 87, pp. 1745-1750, 2006.

[58] V. Pallás, J. A. Sanchez-Navarro, J. Diez, “In vitro evidence for RNA binding properties of the coat protein of Prunus necrotic ringspot ilarvirus and their comparison to related and unrelated viruses,”. Arch. Virol., vol. 144, pp. 797-803. 1999.

[59] F. Aparicio, M. Vilar, E. Perez-Paya, V. Pallas,”The coat protein of Prunus necrotic ringspot virus specifically binds to and regulates the conformation of its genomic RNA,”. Virology, vol. 313, pp. 213-223, 2003.

[60] V. Pallas, F. Aparicio, M. C. Herranz, K. Amari, M. A. Sanchez-Pina, A. Myrta, J. A. Sanchez-Navarro Ilarviruses of Prunus spp., “A continued concern for fruit trees,”. Phytopathology, vol. 102, pp. 1108-1120, 2012.

[61] J. F. Bol, “Replication of alfamo- and ilarviruses: Role of the coat protein,”. Annu. Rev. Phytopathol., vol. 43, pp. 39-62, 2005.

[62] R.H. Alrefai, P.J. Shiel, L.L. Domier, C.J. D'Arcy, P.H. Berger, S.S. Korban, “The nucleotide sequence of Apple mosaic virus coat protein gene has no similarity with other Bromoviridae coat protein genes,”. J. Gen. Virol., vol. 75, no. 10, pp. 2847-2850, 1994.

[63] T. Malinowski B. Komorowska, “Metoda powielania genu bia?ka p?aszcza (CP) wirusanekrotycznej plamisto?ci pier?cieniowej drzew pestkowych (PNRSV) i jej zastosowanie. Polish”. Conf. Fruit Plants Prot., Skierniewice, Poland, pp.203, 1998.