Advertisement

Archives of Virology

, Volume 161, Issue 4, pp 1019–1026 | Cite as

Identification and in silico characterisation of defective molecules associated with isolates of banana bunchy top virus

  • Daisy Stainton
  • Darren P. Martin
  • David A. Collings
  • John E. Thomas
  • Arvind VarsaniEmail author
Brief Report

Abstract

Banana bunchy top virus (BBTV) is a multi-component single-stranded DNA virus. From 267 potentially infected Musa plants, 24 apparently ‘defective’ BBTV components have been identified. Interestingly, 23/24 of these defective molecules were apparently derived from DNA-R. All of the identified defective molecules had retained at least part of the CR-SL and CR-M but had insertions and/or deletions that in most cases resulted in open reading frame disruptions. Our detection of three monophyletic but diverse (and therefore likely circulating) defective DNA-R lineages suggests that, in many cases, defective DNA-R molecules might remain associated with BBTV genomes for prolonged periods.

Keywords

Banana bunchy top virus Nanovirus Defective molecules 

Notes

Acknowledgments

D.S was supported by a postgraduate scholarship from the Marsden Fund of New Zealand (UOC0903). AV and DPM are supported by the National Research Foundation of South Africa. This work was supported by the Marsden Fund Council from government funding, administered by the Royal Society of New Zealand (grant UOC0903) awarded to AV.

Supplementary material

705_2015_2736_MOESM1_ESM.txt (26 kb)
Supplementary Data 1 Fasta file of defective BBTV sequences (TXT 25 kb)
705_2015_2736_MOESM2_ESM.pdf (361 kb)
Supplementary Figure 1 Insert and deletion breakpoint distribution plot where total numbers of breakpoints falling within a 200-nt moving window have been plotted across DNA-R (black line). Points where the black line emerges above the dark grey (95% confidence interval on the expected number of breakpoints at particular genome sites) and light grey (99% confidence interval) areas indicate statistically significant degrees of breakpoint clustering. Two breakpoint hotspots detected at a p–value significance threshold ≤ 0.01) are highlighted in red. (PDF 361 kb)
705_2015_2736_MOESM3_ESM.pdf (977 kb)
Supplementary Figure 2 Maximum-likelihood phylogenetic tree of the rep coding region of the defective DNA-R molecule sequences (insert regions removed) and 302 DNA-R components (see Supplementary Table 1). The phylogenetic tree was rooted with ABTV DNA-R sequences, and branches with < 60% bootstrap support were collapsed. Isolate information is available in Supplementary Table 1 for the DNA-R sequences and in Table 1 for the defective genomes (PDF 977 kb)
705_2015_2736_MOESM4_ESM.doc (282 kb)
Supplementary Table 1 List of DNA-R sequences used in Figure 2 with two-letter country codes: AU, Australia; BI, Burundi; CD, Democratic Republic of Congo; CG, Congo; CN, China; EG, Egypt; FJ, Fiji; ID, Indonesia; IN, India; JP, Japan; LK, Sri Lanka; MM, Myanmar; MY, Malaysia; MW, Malawi; PH, Philippines; PK, Pakistan; RW, Rwanda; TO, Tonga; TW, Taiwan; US, United States of America; VN, Vietnam; WS, Samoa (DOC 282 kb)

References

  1. 1.
    Aronson MN, Meyer AD, Györgyey J, Katul L, Vetten HJ, Gronenborn B, Timchenko T (2000) Clink, a nanovirus-encoded protein, binds both pRB and SKP1. J Virol 74:2967–2972CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Bach J, Jeske H (2014) Defective DNAs of beet curly top virus from long-term survivor sugar beet plants. Virus Res 183:89–94CrossRefPubMedGoogle Scholar
  3. 3.
    Bell KE, Dale JL, Ha CV, Vu MT, Revill PA (2002) Characterisation of Rep-encoding components associated with banana bunchy top nanovirus in Vietnam. Arch Virol 147:695–707CrossRefPubMedGoogle Scholar
  4. 4.
    Burns TM, Harding RM, Dale JL (1995) The genome organisation of banana bunchy top virus: analysis of six ssDNA components. J Gen Virol 76:1471–1482CrossRefPubMedGoogle Scholar
  5. 5.
    Casado CG, Javier Ortiz G, Padron E, Bean SJ, McKenna R, Agbandje-McKenna M, Boulton MI (2004) Isolation and characterization of subgenomic DNAs encapsidated in “single” T = 1 isometric particles of Maize streak virus. Virology 323:164–171CrossRefPubMedGoogle Scholar
  6. 6.
    Dale JL (1987) Banana bunchy top—an economically important tropical plant-virus disease. Adv Virus Res 33:301–325CrossRefPubMedGoogle Scholar
  7. 7.
    Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Frischmuth T, Stanley J (1992) Characterization of beet curly top virus subgenomic DNA localizes sequences required for replication. Virology 189:808–811CrossRefPubMedGoogle Scholar
  9. 9.
    Fu HC, Hu JM, Hung TH, Su HJ, Yeh HH (2009) Unusual events involved in banana bunchy top virus strain evolution. Phytopathology 99:812–822CrossRefPubMedGoogle Scholar
  10. 10.
    Hadfield J, Thomas JE, Schwinghamer MW, Kraberger S, Stainton D, Dayaram A, Parry JN, Pande D, Martin DP, Varsani A (2012) Molecular characterisation of dicot-infecting mastreviruses from Australia. Virus Res 166:13–22CrossRefPubMedGoogle Scholar
  11. 11.
    Hafner GJ, Harding RM, Dale JL (1995) Movement and transmission of banana bunchy top virus DNA component one in bananas. J Gen Virol 76:2279–2285CrossRefPubMedGoogle Scholar
  12. 12.
    Hafner GJ, Harding RM, Dale JL (1997) A DNA primer associated with banana bunchy top virus. J Gen Virol 78:479–486CrossRefPubMedGoogle Scholar
  13. 13.
    Hafner GJ, Stafford MR, Wolter LC, Harding RM, Dale JL (1997) Nicking and joining activity of banana bunchy top virus replication protein in vitro. J Gen Virol 78:1795–1799CrossRefPubMedGoogle Scholar
  14. 14.
    Harding RM, Burns TM, Dale JL (1991) Virus-like particles associated with banana bunchy top disease contain small single-stranded DNA. J Gen Virol 72:225–230CrossRefPubMedGoogle Scholar
  15. 15.
    Herrera-Valencia VA, Dugdale B, Harding RM, Dale JL (2006) An iterated sequence in the genome of banana bunchy top virus is essential for efficient replication. J Gen Virol 87:3409–3412CrossRefPubMedGoogle Scholar
  16. 16.
    Horn J, Lauster S, Krenz B, Kraus J, Frischmuth T, Jeske H (2011) Ambivalent effects of defective DNA in beet curly top virus-infected transgenic sugarbeet plants. Virus Res 158:169–178CrossRefPubMedGoogle Scholar
  17. 17.
    Horser CL, Karan M, Harding RM, Dale JL (2001) Additional Rep-encoding DNAs associated with banana bunchy top virus. Arch Virol 146:71–86CrossRefPubMedGoogle Scholar
  18. 18.
    Idris AM, Shahid MS, Briddon RW, Khan AJ, Zhu JK, Brown JK (2011) An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. J Gen Virol 92:706–717CrossRefPubMedGoogle Scholar
  19. 19.
    Liu Y, Robinson DJ, Harrison BD (1998) Defective forms of cotton leaf curl virus DNA-A that have different combinations of sequence deletion, duplication, inversion and rearrangement. J Gen Virol 79:1501–1508CrossRefPubMedGoogle Scholar
  20. 20.
    Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. doi: 10.1093/ve/vev003 Google Scholar
  22. 22.
    Ndunguru J, Legg JP, Fofana IBF, Aveling TAS, Thompson G, Fauquet CM (2006) Identification of a defective molecule derived from DNA-A of the bipartite begomovirus of East African cassava mosaic virus. Plant Pathol 55:2–10CrossRefGoogle Scholar
  23. 23.
    Paprotka T, Boiteux LS, Fonseca MEN, Resende RO, Jeske H, Faria JC, Ribeiro SG (2010) Genomic diversity of sweet potato geminiviruses in a Brazilian germplasm bank. Virus Res 149:224–233CrossRefPubMedGoogle Scholar
  24. 24.
    Patil BL, Dasgupta I (2006) Defective interfering DNAs of plant viruses. Crit Rev Plant Sci 25:47–64CrossRefGoogle Scholar
  25. 25.
    Patil BL, Dutt N, Briddon RW, Bull SE, Rothenstein D, Borah BK, Dasgupta I, Stanley J, Jeske H (2007) Deletion and recombination events between the DNA-A and DNA-B components of Indian cassava-infecting geminiviruses generate defective molecules in Nicotiana benthamiana. Virus Res 124:59–67CrossRefPubMedGoogle Scholar
  26. 26.
    Rey MEC, Ndunguru J, Berrie LC, Paximadis M, Berry S, Cossa N, Nuaila VN, Mabasa KG, Abraham N, Rybicki EP, Martin D, Pietersen G, Esterhuizen LL (2012) Diversity of dicotyledenous-infecting geminiviruses and their associated DNA molecules in Southern Africa, including the South-west Indian Ocean Islands. Viruses 4:1753–1791CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Rybicki EP, Pietersen G (1999) Plant virus disease problems in the developing world. Adv Virus Res 53:127–175CrossRefPubMedGoogle Scholar
  28. 28.
    Rybicki EP (2015) A Top Ten list for economically important plant viruses. Arch Virol 160:17–20CrossRefPubMedGoogle Scholar
  29. 29.
    Schubert J, Habekuß A, Wu B, Thieme T, Wang X (2014) Analysis of complete genomes of isolates of the Wheat dwarf virus from new geographical locations and descriptions of their defective forms. Virus Genes 48:133–139CrossRefPubMedGoogle Scholar
  30. 30.
    Stainton D, Kraberger S, Walters M, Wiltshire EJ, Rosario K, Halafihi M, Lolohea S, Katoa I, Faitua TH, Aholelei W, Taufa L, Thomas JE, Collings DA, Martin DP, Varsani A (2012) Evidence of inter-component recombination, intra-component recombination and reassortment in banana bunchy top virus. J Gen Virol 93:1103–1119CrossRefPubMedGoogle Scholar
  31. 31.
    Stainton D, Martin D, Muhire B, Lolohea S, Halafihi M, Lepoint P, Blomme G, Crew KS, Sharman M, Kraberger S, Dayaram A, Walters M, Collings DA, Mabvakure B, Lemey P, Harkins G, Thomas JE, Varsani A (2015) The global distribution of Banana bunchy top virus reveals little evidence for frequent recent, human-mediated long distance dispersal events. Virus Evol. doi: 10.1093/ve/vev009 Google Scholar
  32. 32.
    Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Stanley J, Townsend R (1985) Characterisation of DNA forms associated with cassava latent virus infection. Nucleic Acids Res 13:2189–2206CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Stanley J, Frischmuth T, Ellwood S (1990) Defective viral DNA ameliorates symptoms of geminivirus infection in transgenic plants. Proc Natl Acad Sci USA 87:6291–6295CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Stanley J, Saunders K, Pinner MS, Wong SM (1997) Novel defective interfering DNAs associated with ageratum yellow vein geminivirus infection of Ageratum conyzoides. Virology 239:87–96CrossRefPubMedGoogle Scholar
  36. 36.
    Stenger DC, Stevenson MC, Hormuzdi SG, Bisaro DM (1992) A number of subgenomic DNAs are produced following agroinoculation of plants with beet curly top virus. J Gen Virol 73:237–242CrossRefPubMedGoogle Scholar
  37. 37.
    Su HJ, Tsao LY, Wu ML, Hung TH (2003) Biological and molecular categorization of strains of Banana bunchy top virus. J Phytopathol 151:290–296CrossRefGoogle Scholar
  38. 38.
    Thomas JE, Dietzgen RG (1991) Purification, characterization and serological detection of virus-like particles associated with banana bunchy top disease in Australia. J Gen Virol 72:217–224CrossRefPubMedGoogle Scholar
  39. 39.
    van der Walt E, Rybicki EP, Varsani A, Polston JE, Billharz R, Donaldson L, Monjane AL, Martin DP (2009) Rapid host adaptation by extensive recombination. J Gen Virol 90:734–746CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Wanitchakorn R, Hafner GJ, Harding RM, Dale JL (2000) Functional analysis of proteins encoded by banana bunchy top virus DNA-4 to -6. J Gen Virol 81:299–306CrossRefPubMedGoogle Scholar
  41. 41.
    Wanitchakorn R, Harding RM, Dale JL (2000) Sequence variability in the coat protein gene of two groups of banana bunchy top isolates. Arch Virol 145:593–602CrossRefPubMedGoogle Scholar
  42. 42.
    Wu R-Y, You L-R, Soong T-S (1994) Nucleotide sequences of two circular single-stranded DNAs associated with banana bunchy top virus. Phytopathology 84:952–957CrossRefGoogle Scholar
  43. 43.
    Yu NT, Zhang YL, Feng TC, Wang JH, Kulye M, Yang WJ, Lin ZS, Xiong Z, Liu ZX (2012) Cloning and sequence analysis of two banana bunchy top virus genomes in Hainan. Virus Genes 44:488–494CrossRefPubMedGoogle Scholar
  44. 44.
    Zaffalon V, Mukherjee SK, Reddy VS, Thompson JR, Tepfer M (2012) A survey of geminiviruses and associated satellite DNAs in the cotton-growing areas of northwestern India. Arch Virol 157:483–495CrossRefPubMedGoogle Scholar
  45. 45.
    Zhou XP, Xie Y, Zhang ZK, Qi YJ, Wu JJ (2001) Molecular characterization of a novel defective DNA isolated from tobacco tissues infected with tobacco leaf curl virus. Acta Virol 45:45–50PubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.School of Biological Sciences and Biomolecular Interaction CentreUniversity of CanterburyChristchurchNew Zealand
  2. 2.Department of Clinical Laboratory SciencesUniversity of Cape TownCape TownSouth Africa
  3. 3.Ecosciences Precinct, Queensland Alliance for Agriculture and Food Innovation, Centre for Plant ScienceThe University of QueenslandBrisbaneAustralia
  4. 4.Department of Plant Pathology, Emerging Pathogens InstituteUniversity of FloridaGainesvilleUSA

Personalised recommendations