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Molecular Evidence for Recombination in Prunus Necrotic Ringspot Virus

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Abstract

Genetic RNA recombination plays an important role in viral evolution. The evolutionary history of Prunus necrotic ringspot virus (PNRSV) has been extensively studied, but knowledge of recombination in its genome is still lacking. To investigate the recombination events in this virus, 67 accessions composed by 62 isolates retrieved from the databanks and five Tunisian isolates described in this study were analyzed. The use of RECCO algorithm which is based on cost minimization allowed us to detect several breakpoints in the coat protein gene (CP) of three out of five isolates from Tunisia and one from Poland. Moreover, a recombination signal was also detected in the putative cell-to-cell movement protein-encoding gene of an isolate from the USA. Tajima Neutrality test implemented in MEGA4 program indicated the occurrence of a high level of deletion/insertion events in the sequences. The evolutionary historical relationships were determined by constructing a dendrogram using neighbor joining, minimum evolution, maximum parsimony, maximum likelihood, and unweighted pair group method with arithmetic mean (UPGMA). The first four analyses gave similar results. Three classical groups (PE 5, PV 32, and PV 96) were delineated. The recombinant isolates from Tunisia clustered in a distinct clade except for one nonrecombinant (Ghernghezel) which revealed to be a member of PV 32 group. In contrast, UPGMA algorithm divided the Tunisian isolates in three distinct subgroups. Apart from recombination, reassortment is still an open question among many others and may also represent another way to explore the genetic diversity of PNRSV.

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Abbreviations

PNRSV:

Prunus necrotic ringspot virus

CP:

Coat Protein

MP:

Movement Protein

Tajima’s D :

Tajima’s statistic test

References

  • Altschul SF, Gish W, Miller W, Meyers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215:403–10.

    PubMed  CAS  Google Scholar 

  • Altschul SF, Boguski MS, Gish W, Wooton JC. Issues in searching molecular sequence databases. Nat Genet 1994;6:119–29. doi:10.1038/ng0294-119.

    Article  PubMed  CAS  Google Scholar 

  • Aparicio F, Myrta A, Di Terlizzi B, Pallas V. Molecular variability among isolates of Prunus necrotic ringspot virus from different Prunus spp. Phytopathology 1999;89:991–9. doi:10.1094/PHYTO.1999.89.11.991.

    Article  PubMed  CAS  Google Scholar 

  • Bachman EJ, Scott SW, Xin GE, Vance VB. The complete nucleotide sequence of prune dwarf virus RNA3: implication for coat protein activation of genome replication in ilarviruses. Virology 1994;201:127–31. doi:10.1006/viro.1994.1272.

    Article  PubMed  CAS  Google Scholar 

  • Barbara DJ, Clark MF, Thresh JM, Casper R. Rapid detection and serotyping of Prunus necrotic ringspot virus in perennial crops by enzyme-linked immunosorbent assay. Ann Appl Biol 1978;90:395–9. doi:10.1111/j.1744-7348.1978.tb02648.x.

    Article  Google Scholar 

  • Bol JF. Alfalfa mosaic virus and ilarviruses: involvement of coat protein in multiple steps of the replication cycle. J Gen Virol 1999;80:1089–102.

    PubMed  CAS  Google Scholar 

  • Boulila M, Marrakchi M. Amplification de séquences (RT-PCR) et analyse du polymorphisme des fragments de restriction (RFLP) de quelques isolats du virus des taches annulaires nécrotiques des Prunus. EPPO Bull 2001;31:173–8. doi:10.1111/j.1365-2338.2001.tb00987.x.

    Article  Google Scholar 

  • Bousalem M, Dizery EJP, Fargette D. High genetic diversity, distant phylogenetic relationships and intraspecies recombination events among natural populations of yam mosaic virus: a contribution to understanding potyvirus evolution. J Gen Virol 2000;81:243–55.

    PubMed  CAS  Google Scholar 

  • Chare ER, Holmes EC. Selection pressure in the capsid genes of plant RNA viruses reflect mode of transmission. J Gen Virol 2004;85:3149–57. doi:10.1099/vir.0.80134-0.

    Article  PubMed  CAS  Google Scholar 

  • Chrzanowska M. Importance of different strains of PVY in potato production and breeding program in Poland. In: Proceedings of the 11th European Association of Potato Research, Virology section, Trest, Czech Republic Edition, Potato Research Institute, Havlièkuv Brod; 2001. p. 12–14.

  • Codoner FM, Fares MA, Elena SF. Adaptive covariation between the coat and movement proteins of Prunus necrotic ringspot virus. J Virol 2006;80(12):5833–40. doi:10.1128/JVI.00122-06.

    Article  PubMed  CAS  Google Scholar 

  • Crosslin JM, Mink GI. Biophysical differences among Prunus necrotic ringspot ilarviruses. Phytopathology 1992;82:200–6. doi:10.1094/Phyto-82-200.

    Article  CAS  Google Scholar 

  • Crowle DR, Pethybridge SJ, Leggett GW, Sherriff LJ, Wilson CR. Diversity of the coat protein-coding region among ilarvirus isolates infecting hop in Australia. Plant Pathol 2003;52:655–62. doi:10.1046/j.1365-3059.2003.00918.x.

    Article  CAS  Google Scholar 

  • Di Terlizzi B, Skrzeczkowski LJ, Mink GI, Scott SW, Zimmerman MT. The RNA 5 of Prunus necrotic ringspot virus is a biologically inactive copy of the 3′-UTR of the genomic RNA 3. Arch Virol 2001;146(4):825–33. doi:10.1007/s007050170151.

    Article  PubMed  Google Scholar 

  • Domingo E, Holland J, Biebricher C, Eigen M. Quasispecies: the concept and the world. In: Gibbs AJ, Calisher CH, Garcia-Arenal F, editors. Molecular Basis of virus evolution. Cambridge: Cambridge University Press; 1995. p. 181–91.

    Google Scholar 

  • Domingo E, Escarmis C, Sevilla N, Moya A, Elena SF, Quer J, Novella IS, Holland JJ. Basic concepts in RNA virus evolution. FASEB J 1996;10:859–64.

    PubMed  CAS  Google Scholar 

  • Drake JW, Holland JJ. Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 1999;96:13910–3. doi:10.1073/pnas.96.24.13910.

    Article  PubMed  CAS  Google Scholar 

  • Eigen M. On the nature of virus quasispecies. Trends Microbiol 1996;4:216–8. doi:10.1016/0966-842X(96)20011-3.

    Article  PubMed  CAS  Google Scholar 

  • Elena SF. Restrictions to RNA virus adaptation: an experimental approach. Antonie Van Leeuwenhoek 2002;81:135–42. doi:10.1023/A:1020589929125.

    Article  PubMed  CAS  Google Scholar 

  • Fanigliulo A, Comes S, Pacella R, Harrach B, Martin DP, Crescenzi A. Characterisation of Potato virus Y nnp strain inducing veinal necrosis in pepper: a naturally occurring recombinant strain of PVY. Arch Virol 2005;150(4):709–20. doi:10.1007/s00705-004-0449-x.

    Article  PubMed  CAS  Google Scholar 

  • Fraile A, Alonso-Prados JL, Aranda MA, Bernal JJ, Malpica JM, Garcia-Arenal F. Reports about recombination in virus natural populations. J Virol 1997;71:934–40.

    PubMed  CAS  Google Scholar 

  • Galtier N, Gouy M, Gautier C. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. CABIOS 1996;12(6):543–8.

    PubMed  CAS  Google Scholar 

  • Garcia-Arenal F, Fraile A, Malpica JM. Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 2001;39:157–86. doi:10.1146/annurev.phyto.39.1.157.

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Arenal F, Fraile A, Malpica JM. Variation and evolution of plant virus populations. Int Microbiol 2003;6:225–32. doi:10.1007/s10123-003-0142-z.

    Article  PubMed  Google Scholar 

  • Glais L, Tribodet M, Kerlan C. Genomic variability in Potato potyvirus Y (PVY): evidence that PVYN-W and PVYNTN variants are single to multiple recombinants between PVYO and PVYN isolates. Arch Virol 2002;147:363–78. doi:10.1007/s705-002-8325-0.

    Article  PubMed  CAS  Google Scholar 

  • Glais L, Tribodet M, Kerlan C. Specific detection of the PVYN-W variant of Potato virus Y. J Virol Methods 2005;125:131–6. doi:10.1016/j.jviromet.2005.01.007.

    Article  PubMed  CAS  Google Scholar 

  • Glasa M, Bertinova E, Kudela O, Subr Z. Biological and molecular characterization of Prunus necrotic ringspot virus isolates and possible approaches to their phylogenetic typing. Ann Appl Biol 2002;140:279–83. doi:10.1111/j.1744-7348.2002.tb00182.x.

    Article  CAS  Google Scholar 

  • Glasa M, Palkovics L, Kominek P, Labonne G, Pittnerova S, Kudela O, Candresse T, Subr Z. Geographically and temporally distant natural recombinant isolates of Plum pox virus (PPV) are genetically very similar and form a unique PPV subgroup. J Gen Virol 2004;85:2671–81. doi:10.1099/vir.0.80206-0.

    Article  PubMed  CAS  Google Scholar 

  • Grenfell BT, Pybus OG, Gog JR, Wood JLN, Daly JM, Mumford JA, Holmes EC. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 2004;303:327–32. doi:10.1126/science.1090727.

    Article  PubMed  CAS  Google Scholar 

  • Guo D, Maiss E, Adam G, Casper R. Prunus necrotic ringspot ilarvirus: Nucleotide sequence of RNA 3 and the relationship to other ilarviruses based on coat protein comparison. J Gen Virol 1995;76:1073–9. doi:10.1099/0022-1317-76-5-1073.

    Article  PubMed  CAS  Google Scholar 

  • Hammond RW. Phylogeny isolates of Prunus necrotic ringspot virus from the ilarvirus ringtest and identification of group-specific features. Arch Virol 2003;148:1195–210. doi:10.1007/s00705-003-0013-0.

    Article  PubMed  CAS  Google Scholar 

  • Hammond RW, Crosslin JM. The complete nucleotide sequence of RNA 3 of a peach isolate of Prunus necrotic ringspot virus. Virology 1995;208:349–53. doi:10.1006/viro.1995.1159.

    Article  PubMed  CAS  Google Scholar 

  • Hammond RW, Crosslin JM. Virulence and molecular polymorphism of Prunus necrotic ringspot virus isolates. J Gen Virol 1998;79:1815–23.

    PubMed  CAS  Google Scholar 

  • Hammond RW, Crosslin JM, Pasini R, Howell WE, Mink GI. Differenciation of closely related but biologically distinct cherry isolates of Prunus necrotic ringspot virus by polymerase chain reaction. J Virol Methods 1999;80:203–12. doi:10.1016/S0166-0934(99)00051-8.

    Article  PubMed  CAS  Google Scholar 

  • Holland JJ, DeLaTorre JC, Steinhauer DA. RNA virus populations as quasispecies. In: Holland JJ, editor. Genetic diversity of RNA viruses. Berlin: Springer; 1992. p. 1–20.

    Google Scholar 

  • Howell WE, Mink GI. Natural spread of cherry rugose mosaic disease and two Prunus necrotic ringspot virus biotypes in a central Washington sweet cherry orchard. Plant Dis 1988;72:636–40. doi:10.1094/PD-72-0636.

    Article  Google Scholar 

  • Koonin EV, Gorbalenya AE. Evolution of RNA genomes does the high mutation rate necessitate high rate of evolution of virus protein? J Mol Evol 1989;28:524–7. doi:10.1007/BF02602932.

    Article  PubMed  CAS  Google Scholar 

  • Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW. Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 2006;23(10):1891–901. doi:10.1093/molbev/msl051.

    Article  PubMed  Google Scholar 

  • Larkin MA, Blackshileds G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics 2007;23(21):2947–8. doi:10.1093/bioinformatics/btm404.

    Article  PubMed  CAS  Google Scholar 

  • Legg JP, Thresh JM. Cassava mosaic virus disease in East Africa: a dynamic disease in a changing environment. Virus Res 2000;71:135–49. doi:10.1016/S0168-1702(00)00194-5.

    Article  PubMed  CAS  Google Scholar 

  • Malpica JM, Fraile A, Moreno I, Obies CI, Drake JW, Garcia-Arenal F. The rate and character of spontaneous mutations in an RNA virus. Genetics 2002;162:1505–11.

    PubMed  CAS  Google Scholar 

  • Martelli GP, Savino V. Infectious diseases of almond with special reference to the Mediterranean area. EPPO Bull 1997;27:525–34. doi:10.1111/j.1365-2338.1997.tb00679.x.

    Article  Google Scholar 

  • Masuta C, Ueda S, Suzuki M, Uyeda I. Evolution of a quadripartite hybrid virus by interspecific exchange and recombination between replicase components of two related tripartite RNA viruses. Proc Natl Acad Sci U S A 1998;95:10487–92. doi:10.1073/pnas.95.18.10487.

    Article  PubMed  CAS  Google Scholar 

  • Maydt J, Lengauer T. Recco: recombination analysis using cost optimization. Bioinformatics 2006;22(9):1064–71. doi:10.1093/bioinformatics/btl057.

    Article  PubMed  CAS  Google Scholar 

  • Mink GI, Howell WE, Cole A, Regev S. Three serotypes of Prunus necrotic ringspot virus isolated from rugose mosaic disease sweet cherry trees in Washington. Plant Dis 1987;68:207–10. doi:10.1094/PD-69-207.

    Article  Google Scholar 

  • Monci F, Sanchez-Campos S, Navas-Castillo J, Moriones E. A natural recombinant between the geminiviruses tomato yellow leaf curl Sardinia virus and tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 2002;303:317–26. doi:10.1006/viro.2002.1633.

    Article  PubMed  CAS  Google Scholar 

  • Moury B, Cardin L, Onesto JP, Candresse T, Poupet A. Surveys of Prunus necrotic ringspot virus in rose and its variability in rose and Prunus spp. Phytopathology 2001;91:84–91. doi:10.1094/PHYTO.2001.91.1.84.

    Article  PubMed  CAS  Google Scholar 

  • Nie X, Singh RP. Probable geographical grouping of PVYN and PVYNTN based on sequence variation in P1 and 5′-UTR of PVY genome and methods for differentiating North American PVYNTN. J Virol Methods 2002;103:145–56. doi:10.1016/S0166-0934(02)00023-X.

    Article  PubMed  CAS  Google Scholar 

  • Nie X, Singh RP. Specific differentiation of recombinant PVYN:O and PVYNTN isolates by multiplex RT-PCR. J Virol Methods 2003;113:69–77. doi:10.1016/S0166-0934(03)00221-0.

    Article  PubMed  CAS  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. Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol 2002;83:1511–21.

    PubMed  CAS  Google Scholar 

  • Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A 1988;85:2444–8. doi:10.1073/pnas.85.8.2444.

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall K. Evaluation of methods for detecting recombination from DNA sequences. Computer simulation. Proc Natl Acad Sci U S A 2001;98:13757–62.

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA. The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 2002;54:396–402.

    PubMed  CAS  Google Scholar 

  • Pressing J, Reaney DC. Divided genomes and intrinsic noise. J Mol Evol 1984;20:135–46. doi:10.1007/BF02257374.

    Article  PubMed  CAS  Google Scholar 

  • Rigotti S, Gugerli P. Rapid identification of Potato virus Y strains by one-step triplex RT-PCR. J Virol Methods 2007;140:90–4. doi:10.1016/j.jviromet.2006.11.002.

    Article  PubMed  CAS  Google Scholar 

  • Roossinck MJ. Mechanisms of plant virus evolution. Annu Rev Phytopathol 1997;35:191–209. doi:10.1146/annurev.phyto.35.1.191.

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana; 2000. p. 365–86.

    Google Scholar 

  • Rubio L, Ayllon MA, Kong P, Fernandez A, Polek M, Guerri J, Moreno P, Falk BW. Genetic variation of Citrus tristeza virus isolates from California ans Spain: evidence for mixed infections and recombination. J Virol 2001;75(17):8054–62. doi:10.1128/JVI.75.17.8054-8062.2001.

    Article  PubMed  CAS  Google Scholar 

  • Rybicki EP. Bromoviridae. In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD, editors. The sixth report of the International Committee on Taxonomy of viruses 1995. Vienna, Austria: Springer; 1995. p. 405–57.

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: A laboratory. 2nd ed. New York: Cold Spring Harbor Laboratory Press; 1989.

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 1977;74:5463–7. doi:10.1073/pnas.74.12.5463.

    Article  PubMed  CAS  Google Scholar 

  • Schierup M, Hein J. Consequences of recombination on traditional phylogenetic analyses. Genetics 2000a;156:879–91.

    PubMed  CAS  Google Scholar 

  • Schierup M, Hein J. Recombination and the molecular clock. Mol Biol Evol 2000b;17:1578–9.

    PubMed  CAS  Google Scholar 

  • Scott SW, Ge X. The complete nucleotide sequence of RNA 3 of Citrus leaf rugose and Citrus variegation ilarviruses. J Gen Virol 1995;76:957–63. doi:10.1099/0022-1317-76-4-957.

    Article  PubMed  CAS  Google Scholar 

  • Scott SW, Zimmerman MT, Ge X, Mackenzie DJ. The coat proteins and putative movement proteins of isolates of Prunus necrotic ringspot virus from different host species and geographic origins are extensively conserved. Eur J Plant Pathol 1998;104:155–61. doi:10.1023/A:1008668129926.

    Article  CAS  Google Scholar 

  • Singh RP, McLaren DL, Nie X, Singh M. Possible escape of a recombinant isolate of Potato virus Y by serological indexing and methods of its detection. Plant Dis 2003;87:679–85. doi:10.1094/PDIS.2003.87.6.679.

    Article  CAS  Google Scholar 

  • Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989;123:585–95.

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007;24(8):1596–9. doi:10.1093/molbev/msm092.

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997;24:4876–82. doi:10.1093/nar/25.24.4876.

    Article  Google Scholar 

  • Tomitaka Y, Ohshima K. A phylogeographical study of the Turnip mosaic virus population in East Asia reveals an ‘emergent’ lineage in Japan. Mol Ecol 2006;15:4437–57. doi:10.1111/j.1365-294X.2006.03094.x.

    Article  PubMed  CAS  Google Scholar 

  • van Vloten-Doting L, Francki RIB, Fulton RW, Kaper JM, Lane LC. Tricornviridae—a proposed family of plant viruses with tripartite single-stranded RNA genomes. Intervirology 1981;15:198–203. doi:10.1159/000149232.

    Article  PubMed  Google Scholar 

  • Vaskova D, Petrzik K, Karesova R. Variability and molecular typing of the woody-tree infecting Prunus necrotic ringspot ilarvirus. Arch Virol 2000;145:699–709. doi:10.1007/s007050050664.

    Article  PubMed  CAS  Google Scholar 

  • Wetzel T, Candresse T, Macquaire G, Ravelonandro M, Dunez J. A highly sensitive immunocapture polymerase chain reaction method for plum pox potyvirus detection. J Virol Methods 1992;39:27–37. doi:10.1016/0166-0934(92)90122-T.

    Article  PubMed  CAS  Google Scholar 

  • Zimmern D. Evolution of RNA viruses. In: Holland JJ, Domingo ER, Ahlquist P, editors. RNA genetics. Boca Raton: CRC; 1988. p. 211–40.

    Google Scholar 

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    Moncef Boulila

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Boulila, M. Molecular Evidence for Recombination in Prunus Necrotic Ringspot Virus. Plant Mol Biol Rep 27, 189–198 (2009). https://doi.org/10.1007/s11105-008-0071-2

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