1887

Abstract

Banana bunchy top virus (BBTV; family , genus ) is a multi-component, ssDNA virus, which causes widespread banana crop losses throughout tropical Africa and Australasia. We determined the full genome sequences of 12 BBTV isolates from the Kingdom of Tonga and analysed these together with previously determined BBTV sequences to show that reassortment and both inter- and intra-component recombination have all been relatively frequent occurrences during BBTV evolution. We found that whereas DNA-U3 components display evidence of complex inter- and intra-component recombination, all of the South Pacific DNA-R components have a common intra-component recombinant origin spanning the replication-associated protein gene. Altogether, the DNA-U3 and DNA-M components display a greater degree of inter-component recombination than the DNA-R, -S, -C and -M components. The breakpoint distribution of the inter-component recombination events reveals a primary recombination hotspot around the 5′ side of the common region major and, in accordance with recombination hotspots detectable in related ssDNA viruses, a secondary recombination hotspot near the origin of virion-strand replication.

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2012-05-01
2020-01-28
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References

  1. Beetham P. R. , Hafner G. J. , Harding R. M. , Dale J. L. . ( 1997; ). Two mRNAs are transcribed from banana bunchy top virus DNA-1. . J Gen Virol 78:, 229–236.[PubMed]
    [Google Scholar]
  2. Bell K. E. , Dale J. L. , Ha C. V. , Vu M. T. , Revill P. A. . ( 2002; ). Characterisation of Rep-encoding components associated with banana bunchy top nanovirus in Vietnam. . Arch Virol 147:, 695–707. [CrossRef] [PubMed]
    [Google Scholar]
  3. Boni M. F. , Posada D. , Feldman M. W. . ( 2007; ). An exact nonparametric method for inferring mosaic structure in sequence triplets. . Genetics 176:, 1035–1047. [CrossRef] [PubMed]
    [Google Scholar]
  4. Burns T. M. , Harding R. M. , Dale J. L. . ( 1995; ). The genome organization of banana bunchy top virus: analysis of six ssDNA components. . J Gen Virol 76:, 1471–1482. [CrossRef] [PubMed]
    [Google Scholar]
  5. Chen Y. F. , Chen J. S. , Zhang H. R. , Tang X. S. , Du Z. Y. . ( 2007; ). Molecular evidence and sequence analysis of a natural reassortant between cucumber mosaic virus subgroup IA and II strains. . Virus Genes 35:, 405–413. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chen L. F. , Rojas M. , Kon T. , Gamby K. , Xoconostle-Cazares B. , Gilbertson R. L. . ( 2009; ). A severe symptom phenotype in tomato in Mali is caused by a reassortant between a novel recombinant begomovirus (Tomato yellow leaf curl Mali virus) and a betasatellite. . Mol Plant Pathol 10:, 415–430. [CrossRef] [PubMed]
    [Google Scholar]
  7. Dale J. L. . ( 1987; ). Banana bunchy top: an economically important tropical plant virus disease. . Adv Virus Res 33:, 301–325. [CrossRef] [PubMed]
    [Google Scholar]
  8. Duffy S. , Holmes E. C. . ( 2008; ). Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus tomato yellow leaf curl virus. . J Virol 82:, 957–965. [CrossRef] [PubMed]
    [Google Scholar]
  9. Duffy S. , Holmes E. C. . ( 2009; ). Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses. . J Gen Virol 90:, 1539–1547. [CrossRef] [PubMed]
    [Google Scholar]
  10. Duffy S. , Shackelton L. A. , Holmes E. C. . ( 2008; ). Rates of evolutionary change in viruses: patterns and determinants. . Nat Rev Genet 9:, 267–276. [CrossRef] [PubMed]
    [Google Scholar]
  11. Gibbs M. J. , Armstrong J. S. , Gibbs A. J. . ( 2000; ). Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. . Bioinformatics 16:, 573–582. [CrossRef] [PubMed]
    [Google Scholar]
  12. Grigoras I. , Timchenko T. , Katul L. , Grande-Pérez A. , Vetten H. J. , Gronenborn B. . ( 2009; ). Reconstitution of authentic nanovirus from multiple cloned DNAs. . J Virol 83:, 10778–10787. [CrossRef] [PubMed]
    [Google Scholar]
  13. Grigoras I. , Timchenko T. , Grande-Pérez A. , Katul L. , Vetten H. J. , Gronenborn B. . ( 2010; ). High variability and rapid evolution of a nanovirus. . J Virol 84:, 9105–9117. [CrossRef] [PubMed]
    [Google Scholar]
  14. Gu H. , Zhang C. , Ghabrial S. A. . ( 2007; ). Novel naturally occurring Bean pod mottle virus reassortants with mixed heterologous RNA1 genomes. . Phytopathology 97:, 79–86. [CrossRef] [PubMed]
    [Google Scholar]
  15. Guindon S. , Gascuel O. . ( 2003; ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. . Syst Biol 52:, 696–704. [CrossRef] [PubMed]
    [Google Scholar]
  16. Hanley-Bowdoin L. , Settlage S. B. , Orozco B. M. , Nagar S. , Robertson D. . ( 2000; ). Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. . Crit Rev Biochem Mol Biol 35:, 105–140.[PubMed]
    [Google Scholar]
  17. Harding R. M. , Burns T. M. , Dale J. L. . ( 1991; ). Virus-like particles associated with banana bunchy top disease contain small single-stranded DNA. . J Gen Virol 72:, 225–230. [CrossRef] [PubMed]
    [Google Scholar]
  18. Harding R. M. , Burns T. M. , Hafner G. , Dietzgen R. G. , Dale J. L. . ( 1993; ). Nucleotide sequence of one component of the banana bunchy top virus genome contains a putative replicase gene. . J Gen Virol 74:, 323–328. [CrossRef] [PubMed]
    [Google Scholar]
  19. Harkins G. W. , Martin D. P. , Duffy S. , Monjane A. L. , Shepherd D. N. , Windram O. P. , Owor B. E. , Donaldson L. , van Antwerpen T. . & other authors ( 2009; ). Dating the origins of the maize-adapted strain of maize streak virus, MSV-A. . J Gen Virol 90:, 3066–3074.[PubMed] [CrossRef]
    [Google Scholar]
  20. Heath L. , van der Walt E. , Varsani A. , Martin D. P. . ( 2006; ). Recombination patterns in aphthoviruses mirror those found in other picornaviruses. . J Virol 80:, 11827–11832.[PubMed] [CrossRef]
    [Google Scholar]
  21. Horser C. L. , Karan M. , Harding R. M. , Dale J. L. . ( 2000; ). Additional Rep-encoding DNAs associated with banana bunchy top virus. . Arch Virol 145:, 1–6.[PubMed] [CrossRef]
    [Google Scholar]
  22. Horser C. L. , Karan M. , Harding R. M. , Dale J. L. . ( 2001; ). Additional rep-encoding DNAs associated with banana bunchy top virus. . Arch Virol 6:, 71–86. [CrossRef] [PubMed]
    [Google Scholar]
  23. Hou Y. M. , Gilbertson R. L. . ( 1996; ). Increased pathogenicity in a pseudorecombinant bipartite geminivirus correlates with intermolecular recombination. . J Virol 70:, 5430–5436.[PubMed]
    [Google Scholar]
  24. Hu J. M. , Fu H. C. , Lin C. H. , Su H. J. , Yeh H. H. . ( 2007; ). Reassortment and concerted evolution in banana bunchy top virus genomes. . J Virol 81:, 1746–1761. [CrossRef] [PubMed]
    [Google Scholar]
  25. Hughes A. L. . ( 2004; ). Birth-and-death evolution of protein-coding regions and concerted evolution of non-coding regions in the multi-component genomes of nanoviruses. . Mol Phylogenet Evol 30:, 287–294. [CrossRef] [PubMed]
    [Google Scholar]
  26. Hyder M. Z. , Shah S. H. , Hameed S. , Naqvi S. M. S. . ( 2011; ). Evidence of recombination in the Banana bunchy top virus genome. . Infect Genet Evol 11:, 1293–1300. [CrossRef] [PubMed]
    [Google Scholar]
  27. Jeske H. , Lütgemeier M. , Preiss W. . ( 2001; ). DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. . EMBO J 20:, 6158–6167. [CrossRef] [PubMed]
    [Google Scholar]
  28. Jones D. R. . ( 2000; ). Introduction to Banana, Abaca and Enset. . In Disease of Banana, Abaca and Enset. Edited by Jones D. R. . . Wallingford:, Oxon, UK: CABI Publishing;.
    [Google Scholar]
  29. Jovel J. , Reski G. , Rothenstein D. , Ringel M. , Frischmuth T. , Jeske H. . ( 2004; ). Sida micrantha mosaic is associated with a complex infection of begomoviruses different from Abutilon mosaic virus . . Arch Virol 149:, 829–841. [CrossRef] [PubMed]
    [Google Scholar]
  30. Kagy V. , Thomas J. E. , Sharman M. , Mademba-Sy F. . ( 2001; ). First record of banana bunchy top disease in New Caledonia. . Australas Plant Pathol 30:, 71. [CrossRef]
    [Google Scholar]
  31. Karan M. , Harding R. M. , Dale J. L. . ( 1994; ). Evidence for two groups of banana bunchy top virus isolates. . J Gen Virol 75:, 3541–3546. [CrossRef] [PubMed]
    [Google Scholar]
  32. Karan M. , Harding R. M. , Dale J. L. . ( 1997; ). Association of banana bunchy top virus DNA components 2 to 6 with bunchy top disease. . Mol Plant Pathol On-line. http://www.bspp.org.uk/mppol/citation.php
    [Google Scholar]
  33. Kumar P. L. , Hanna R. , Alabi O. J. , Soko M. M. , Oben T. T. , Vangu G. H. , Naidu R. A. . ( 2011; ). Banana bunchy top virus in sub-Saharan Africa: investigations on virus distribution and diversity. . Virus Res 159:, 171–182. [CrossRef] [PubMed]
    [Google Scholar]
  34. Lefeuvre P. , Lett J. M. , Varsani A. , Martin D. P. . ( 2009; ). Widely conserved recombination patterns among single-stranded DNA viruses. . J Virol 83:, 2697–2707. [CrossRef] [PubMed]
    [Google Scholar]
  35. Magee C. J. P. . ( 1927; ). Investigation on the bunchy top disease of the banana, vol. 30, p. 67. New Delhi, India:: Council of Scientific and Industrial Research;.
    [Google Scholar]
  36. Magee C. J. P. . ( 1953; ). Some aspects of the bunchy top disease of banana and other Musa spp. . J Proc R Soc New South Wales 87:, 3–18.
    [Google Scholar]
  37. Maoka T. , Hayano Y. S. , Iwasaki M. , Yoshida K. , Masuta C. . ( 2010; ). Mixed infection in tomato to ensure frequent generation of a natural reassortant between two subgroups of Cucumber mosaic virus . . Virus Genes 40:, 148–150. [CrossRef] [PubMed]
    [Google Scholar]
  38. Martin D. , Rybicki E. . ( 2000; ). rdp: detection of recombination amongst aligned sequences. . Bioinformatics 16:, 562–563. [CrossRef] [PubMed]
    [Google Scholar]
  39. Martin D. P. , Posada D. , Crandall K. A. , Williamson C. . ( 2005; ). A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. . AIDS Res Hum Retroviruses 21:, 98–102. [CrossRef] [PubMed]
    [Google Scholar]
  40. Martin D. P. , Lemey P. , Lott M. , Moulton V. , Posada D. , Lefeuvre P. . ( 2010; ). rdp3: a flexible and fast computer program for analyzing recombination. . Bioinformatics 26:, 2462–2463. [CrossRef] [PubMed]
    [Google Scholar]
  41. Martin D. P. , Biagini P. , Lefeuvre P. , Golden M. , Roumagnac P. , Varsani A. . ( 2011a; ). Recombination in eukaryotic single stranded DNA viruses. . Viruses 3:, 1699–1738. [CrossRef] [PubMed]
    [Google Scholar]
  42. Martin D. P. , Lefeuvre P. , Varsani A. , Hoareau M. , Semegni J. Y. , Dijoux B. , Vincent C. , Reynaud B. , Lett J. M. . ( 2011b; ). Complex recombination patterns arising during geminivirus coinfections preserve and demarcate biologically important intra-genome interaction networks. . PLoS Pathog 7:, e1002203. [CrossRef] [PubMed]
    [Google Scholar]
  43. Owor B. E. , Shepherd D. N. , Taylor N. J. , Edema R. , Monjane A. L. , Thomson J. A. , Martin D. P. , Varsani A. . ( 2007; ). Successful application of FTA Classic Card technology and use of bacteriophage Φ29 DNA polymerase for large-scale field sampling and cloning of complete maize streak virus genomes. . J Virol Methods 140:, 100–105. [CrossRef] [PubMed]
    [Google Scholar]
  44. Padidam M. , Sawyer S. , Fauquet C. M. . ( 1999; ). Possible emergence of new geminiviruses by frequent recombination. . Virology 265:, 218–225. [CrossRef] [PubMed]
    [Google Scholar]
  45. Perrier X. , De Langhe E. , Donohue M. , Lentfer C. , Vrydaghs L. , Bakry F. , Carreel F. , Hippolyte I. , Horry J. P. . & other authors ( 2011; ). Multidisciplinary perspectives on banana (Musa spp.) domestication. . Proc Natl Acad Sci U S A 108:, 11311–11318. [CrossRef] [PubMed]
    [Google Scholar]
  46. Pita J. S. , Fondong V. N. , Sangaré A. , Otim-Nape G. W. , Ogwal S. , Fauquet C. M. . ( 2001; ). Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. . J Gen Virol 82:, 655–665.[PubMed]
    [Google Scholar]
  47. Posada D. , Crandall K. A. . ( 2001; ). Evaluation of methods for detecting recombination from DNA sequences: computer simulations. . Proc Natl Acad Sci U S A 98:, 13757–13762. [CrossRef] [PubMed]
    [Google Scholar]
  48. Qiu W. P. , Moyer J. W. . ( 1999; ). Tomato spotted wilt tospovirus adapts to the TSWV N gene-derived resistance by genome reassortment. . Phytopathology 89:, 575–582. [CrossRef] [PubMed]
    [Google Scholar]
  49. Roberts S. , Stanley J. . ( 1994; ). Lethal mutations within the conserved stem-loop of African cassava mosaic virus DNA are rapidly corrected by genomic recombination. . J Gen Virol 75:, 3203–3209. [CrossRef] [PubMed]
    [Google Scholar]
  50. Rohde W. , Randles J. W. , Langridge P. , Hanold D. . ( 1990; ). Nucleotide sequence of a circular single-stranded DNA associated with coconut foliar decay virus. . Virology 176:, 648–651. [CrossRef] [PubMed]
    [Google Scholar]
  51. Saunders K. , Salim N. , Mali V. R. , Malathi V. G. , Briddon R. , Markham P. G. , Stanley J. . ( 2002; ). Characterisation of Sri Lankan cassava mosaic virus and Indian cassava mosaic virus: evidence for acquisition of a DNA B component by a monopartite begomovirus. . Virology 293:, 63–74. [CrossRef] [PubMed]
    [Google Scholar]
  52. Sharman M. , Thomas J. E. , Skabo S. , Holton T. A. . ( 2008; ). Abacá bunchy top virus, a new member of the genus Babuvirus (family Nanoviridae). . Arch Virol 153:, 135–147. [CrossRef] [PubMed]
    [Google Scholar]
  53. Shepherd D. N. , Martin D. P. , Lefeuvre P. , Monjane A. L. , Owor B. E. , Rybicki E. P. , Varsani A. . ( 2008; ). A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. . J Virol Methods 149:, 97–102. [CrossRef] [PubMed]
    [Google Scholar]
  54. Smith J. M. . ( 1992; ). Analyzing the mosaic structure of genes. . J Mol Evol 34:, 126–129. [CrossRef] [PubMed]
    [Google Scholar]
  55. Tamura K. , Peterson D. , Peterson N. , Stecher G. , Nei M. , Kumar S. . ( 2011; ). mega5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731–2739. [CrossRef] [PubMed]
    [Google Scholar]
  56. Thomas J. E. , Dietzgen R. G. . ( 1991; ). Purification, characterization and serological detection of virus-like particles associated with banana bunchy top disease in Australia. . J Gen Virol 72:, 217–224. [CrossRef] [PubMed]
    [Google Scholar]
  57. Thomas J. E. , Iskra-Caruana M. L. , Jones D. R. . ( 2000; ). Diseases caused by viruses, bunchy top. . In Disease of Banana, Abaca and Enset, pp. 241–283. Edited by D. R. Jones. Wallingford: CABI Publishing.
    [Google Scholar]
  58. Timchenko T. , Katul L. , Sano Y. , de Kouchkovsky F. , Vetten H. J. , Gronenborn B. . ( 2000; ). The master rep concept in nanovirus replication: identification of missing genome components and potential for natural genetic reassortment. . Virology 274:, 189–195. [CrossRef] [PubMed]
    [Google Scholar]
  59. Timchenko T. , Katul L. , Aronson M. , Vega-Arreguín J. C. , Ramirez B. C. , Vetten H. J. , Gronenborn B. . ( 2006; ). Infectivity of nanovirus DNAs: induction of disease by cloned genome components of Faba bean necrotic yellows virus. . J Gen Virol 87:, 1735–1743. [CrossRef] [PubMed]
    [Google Scholar]
  60. van der Walt E. , Martin D. P. , Varsani A. , Polston J. E. , Rybicki E. P. . ( 2008; ). Experimental observations of rapid Maize streak virus evolution reveal a strand-specific nucleotide substitution bias. . Virol J 5:, 104. [CrossRef] [PubMed]
    [Google Scholar]
  61. Vetten H. J. , Chu P. W. , Dale J. L. , Harding R. M. , Hu J. , Katul L. , Kojima M. , Randles J. W. , Sano Y. . & other authors ( 2005; ). Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. San Diego, London:: Academic Press;.
    [Google Scholar]
  62. Wanitchakorn R. , Harding R. M. , Dale J. L. . ( 2000; ). Sequence variability in the coat protein gene of two groups of banana bunchy top isolates. . Arch Virol 145:, 593–602. [CrossRef] [PubMed]
    [Google Scholar]
  63. Wardlaw C. . ( 1961; ). Banana Diseases, Including Plantains and Abaca. London:: Longmans, Green and Co. Ltd;.
    [Google Scholar]
  64. Xie W. S. , Hu J. S. . ( 1995; ). Molecular cloning, sequence analysis, and detection of banana bunchy top virus in Hawaii. . Phytopathology 85:, 339–347. [CrossRef]
    [Google Scholar]
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Reassortment 

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DNA-C 

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DNA-M 

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DNA-N 

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DNA-R 

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DNA-S 

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Inter component recombination 

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