Skip to main content
SpringerLink
Log in

Identification of novel Bromus- and Trifolium-associated circular DNA viruses

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The genomes of a large number of highly diverse novel circular DNA viruses from a wide range of sources have been characterised in recent years, including circular single-stranded DNA (ssDNA) viruses that share similarities with plant-infecting ssDNA viruses of the family Geminiviridae. Here, we describe six novel circular DNA viral genomes that encode replication-associated (Rep) proteins that are most closely related to those of either geminiviruses or gemycircularviruses (a new group of ssDNA viruses that are closely related to geminiviruses). Four possible viral genomes were recovered from Bromus hordeaceus sampled in New Zealand, and two were recovered from B. hordeaceus and Trifolium resupinatum sampled in France. Two of the viral genomes from New Zealand (one from the North Island and one from the South Island each) share >99 % sequence identity, and two genomes recovered from B. hordeaceus and T. resupinatum sampled in France share 74 % identity. All of the viral genomes that were recovered were found to have a major open reading frame on both their complementary and virion-sense strands, one of which likely encodes a Rep and the other a capsid protein. Although future infectivity studies are needed to identify the host range of these viruses, this is the first report of circular DNA viruses associated with grasses in New Zealand.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  1. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. System Biol 55:539–552

    Article  Google Scholar 

  2. Barker NP, Clark LG, Davis JI, Duvall MR, Guala GF, Hsiao C, Kellogg EA, Linder HP (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88:373–457

    Article  Google Scholar 

  3. Bernardo P, Golden M, Akram M, Naimuddin, Nadarajan N, Fernandez E, Granier M, Rebelo AG, Peterschmitt M, Martin DP, Roumagnac P (2013) Identification and characterisation of a highly divergent geminivirus: evolutionary and taxonomic implications. Virus Res 177:35–45

  4. Candresse T, Filloux D, Muhire B, Julian C, Galzi S, Fort G, Bernardo P, Daugrois JH, Fernandez E, Martin DP, Varsani A, Roumagnac P (2014) Appearances can be deceptive: revealing a hidden viral infection with deep sequencing in a plant quarantine context. PLoS One 9:e102945

    Article  PubMed Central  PubMed  Google Scholar 

  5. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165

    Article  CAS  PubMed  Google Scholar 

  6. Dayaram A, Opong A, Jäschke A, Hadfield J, Baschiera M, Dobson RCJ, Offei SK, Shepherd DN, Martin DP, Varsani A (2012) Molecular characterisation of a novel cassava associated circular ssDNA virus. Virus Res 166:130–135

    Article  CAS  PubMed  Google Scholar 

  7. Dayaram A, Potter KA, Pailes R, Marinov M, Rosenstein DD, Varsani A (2015) Identification of diverse circular single-stranded DNA viruses in adult dragonflies and damselflies (Insecta: Odonata) of Arizona and Oklahoma, USA. Infection, Genetics and Evolution (In press)

  8. Dekker EL, Woolston CJ, Xue Y, Cox B, Mullineaux PM (1991) Transcript mapping reveals different expression strategies for the bicistronic RNAs of the geminivirus wheat dwarf virus. Nucleic Acids Res 19:4075–4081

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Du Z, Tang Y, Zhang S, She X, Lan G, Varsani A, He Z (2014) Identification and molecular characterization of a single-stranded circular DNA virus with similarities to Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1. Arch Virol 159:1527–1531

    Article  CAS  PubMed  Google Scholar 

  10. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Ge X, Li J, Peng C, Wu L, Yang X, Wu Y, Zhang Y, Shi Z (2011) Genetic diversity of novel circular ssDNA viruses in bats in China. J General Virol 92:2646–2653

    Article  CAS  Google Scholar 

  12. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. System Biol 59:307–321

    Article  CAS  Google Scholar 

  13. Heydarnejad J, Keyvani N, Razavinejad S, Massumi H, Varsani A (2013) Fulfilling Koch’s postulates for beet curly top Iran virus and proposal for consideration of new genus in the family Geminiviridae. Arch Virol 158:435–443

    Article  CAS  PubMed  Google Scholar 

  14. Ilyina TV, Koonin EV (1992) Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Research 20:3279–3285

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Koonin EV, Ilyina TV (1992) Geminivirus replication proteins are related to prokaryotic plasmid rolling circle DNA replication initiator proteins. Journal of General Virology 73:2763–2766

    Article  CAS  PubMed  Google Scholar 

  16. Koonin EV (1993) A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication. Nucleic Acids Res 21:2541–2547

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Kraberger S, Thomas JE, Geering ADW, Dayaram A, Stainton D, Hadfield J, Walters M, Parmenter KS, van Brunschot S, Collings DA, Martin DP, Varsani A (2012) Australian monocot-infecting mastrevirus diversity rivals that in Africa. Virus Res 169:127–136

    Article  CAS  PubMed  Google Scholar 

  18. Kraberger S, Stainton D, Dayaram A, Zawar-Reza P, Gomez C, Harding JS, Varsani A (2013) Discovery of Sclerotinia sclerotiorum Hypovirulence-Associated Virus-1 in Urban River Sediments of Heathcote and Styx Rivers in Christchurch City, New Zealand. Genome Announc 1:e00559-13

  19. Kreuze JF, Perez A, Untiveros M, Quispe D, Fuentes S, Barker I, Simon R (2009) Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: A generic method for diagnosis, discovery and sequencing of viruses. Virology 388:1–7

    Article  CAS  PubMed  Google Scholar 

  20. Lamberto I, Gunst K, Muller H, Zur Hausen H, de Villiers EM (2014) Mycovirus-like DNA virus sequences from cattle serum and human brain and serum samples from multiple sclerosis patients. Genome Announc 2:e00848-14

  21. Liu H, Fu Y, Li B, Yu X, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D (2011) Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes. BMC Evol Biol 11:e276

    Article  Google Scholar 

  22. Loconsole G, Saldarelli P, Doddapaneni H, Savino V, Martelli GP, Saponari M (2012) Identification of a single-stranded DNA virus associated with citrus chlorotic dwarf disease, a new member in the family Geminiviridae. Virology 432:162–172

    Article  CAS  PubMed  Google Scholar 

  23. Martin D, Willment J, Rybicki E (1999) Evaluation of Maize streak virus pathogenicity in differentially resistant Zea mays genotypes. Phytopathology 89:695–700

    Article  CAS  PubMed  Google Scholar 

  24. Martin DP, Linderme D, Lefeuvre P, Shepherd DN, Varsani A (2011) Eragrostis minor streak virus: an Asian streak virus in Africa. Arch Virol 156:1299–1303

    Article  CAS  PubMed  Google Scholar 

  25. Monjane AL, Harkins GW, Martin DP, Lemey P, Lefeuvre P, Shepherd DN, Oluwafemi S, Simuyandi M, Zinga I, Komba EK, Lakoutene DP, Mandakombo N, Mboukoulida J, Semballa S, Tagne A, Tiendrebeogo F, Erdmann JB, van Antwerpen T, Owor BE, Flett B, Ramusi M, Windram OP, Syed R, Lett JM, Briddon RW, Markham PG, Rybicki EP, Varsani A (2011) Reconstructing the history of Maize streak virus strain a dispersal to reveal diversification hot spots and its origin in southern Africa. J Virol 85:9623–9636

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Muhire BM, Varsani A, Martin DP (2014) SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277

    Article  PubMed Central  PubMed  Google Scholar 

  27. Nash TE, Dallas MB, Reyes MI, Buhrman GK, Ascencio-Ibañez JT, Hanley-Bowdoin L (2011) Functional analysis of a novel motif conserved across geminivirus Rep proteins. J Virol 85:1182–1192

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Ng TF, Chen LF, Zhou Y, Shapiro B, Stiller M, Heintzman PD, Varsani A, Kondov NO, Wong W, Deng X, Andrews TD, Moorman BJ, Meulendyk T, MacKay G, Gilbertson RL, Delwart E (2014) Preservation of viral genomes in 700-y-old caribou feces from a subarctic ice patch. Proceedings of the National Academy of Sciences of the United States of America 111:16842–16847

    Article  PubMed  Google Scholar 

  29. Ng TFF, Willner DL, Lim YW, Schmieder R, Chau B, Nilsson C, Anthony S, Ruan Y, Rohwer F, Breitbart M (2011) Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS One 6:e20579

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Ng TFF, Marine R, Wang C, Simmonds P, Kapusinszky B, Bodhidatta L, Oderinde BS, Wommack KE, Delwart E (2012) High variety of known and new RNA and DNA viruses of diverse origins in nntreated sewage. J Virol 86:12161–12175

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Oluwafemi S, Varsani A, Monjane AL, Shepherd DN, Owor BE, Rybicki EP, Martin DP (2008) A new African streak virus species from Nigeria. Arch Virol 153:1407–1410

    Article  CAS  PubMed  Google Scholar 

  32. Oluwafemi S, Kraberger S, Shepherd DN, Martin DP, Varsani A (2014) A high degree of African streak virus diversity within Nigerian maize fields includes a new mastrevirus from Axonopus compressus. Arch Virol 159:2765–2770

    Article  CAS  PubMed  Google Scholar 

  33. Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL (2011) The fecal viral flora of wild rodents. PLoS Pathog 7:e1002218

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Poojari S, Alabi OJ, Fofanov VY, Naidu RA (2013) A leafhopper-transmissible DNA virus with novel evolutionary lineage in the family Geminiviridae implicated in grapevine redleaf disease by next-generation sequencing. PLoS One 8:e64194

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Rosario K, Duffy S, Breitbart M (2009) Diverse circovirus-like genome architectures revealed by environmental metagenomics. J Gen Virol 90:2418–2424

    Article  CAS  PubMed  Google Scholar 

  36. Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S, Stainton D, Breitbart M, Varsani A (2011) Diverse circular single-stranded DNA viruses discovered in dragonflies (Odonata: Epiprocta). J Gen Virol 93:2668–2681

    Article  Google Scholar 

  37. Rosario K, Duffy S, Breitbart M (2012) A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 157:1851–1871

    Article  CAS  PubMed  Google Scholar 

  38. Shepherd DN, Varsani A, Windram OP, Lefeuvre P, Monjane AL, Owor BE, Martin DP (2008) Novel sugarcane streak and Sugarcane streak Reunion mastreviruses from southern Africa and La Reunion. Arch Virol 153:605–609

    Article  CAS  PubMed  Google Scholar 

  39. Shepherd DN, Martin DP, Van Der Walt E, Dent K, Varsani A, Rybicki EP (2010) Maize streak virus: An old and complex ‘emerging’ pathogen. Mol Plant Pathol 11:1–12

    Article  CAS  PubMed  Google Scholar 

  40. Sikorski A, Massaro M, Kraberger S, Young LM, Smalley D, Martin DP, Varsani A (2013) Novel myco-like DNA viruses discovered in the faecal matter of various animals. Virus Res 177:209–216

    Article  CAS  PubMed  Google Scholar 

  41. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol İ (2009) ABySS: A parallel assembler for short read sequence data. Genome Res 19:1117–1123

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. van den Brand JMA, van Leeuwen M, Schapendonk CM, Simon JH, Haagmans BL, Osterhaus ADME, Smits SL (2012) Metagenomic analysis of the viral flora of pine marten and European badger feces. J Virol 86:2360–2365

    Article  PubMed Central  PubMed  Google Scholar 

  43. Varsani A, Shepherd DN, Monjane AL, Owor BE, Erdmann JB, Rybicki EP, Peterschmitt M, Briddon RW, Markham PG, Oluwafemi S, Windram OP, Lefeuvre P, Lett JM, Martin DP (2008) Recombination, decreased host specificity and increased mobility may have driven the emergence of Maize streak virus as an agricultural pathogen. J Gen Virol 89:2063–2074

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Varsani A, Monjane AL, Donaldson L, Oluwafemi S, Zinga I, Komba EK, Plakoutene D, Mandakombo N, Mboukoulida J, Semballa S, Briddon RW, Markham PG, Lett JM, Lefeuvre P, Rybicki EP, Martin DP (2009) Comparative analysis of Panicum streak virus and Maize streak virus diversity, recombination patterns and phylogeography. Virol J 6:e194

  45. Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci 107:8387–8392

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Zawar-Reza P, Arguello-Astorga GR, Kraberger S, Julian L, Stainton D, Broady PA, Varsani A (2014) Diverse small circular single-stranded DNA viruses identified in a freshwater pond on the McMurdo Ice Shelf (Antarctica). Infect Genet Evol 26:132–138

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

SK is supported by a scholarship from the School of Biological Sciences (University of Canterbury, New Zealand). We thank Captain Milen Marinov for assistance with grass sampling. This work was supported by the Marsden Fund Council from Government funding, administered by the Royal Society of New Zealand (grant UOC0903). AV and DPM are supported by the National Research Foundation of South Africa. PB was supported by a fellowship funded by the MEM-INRA Metaprogram and the DGA (Département Général des Armées, France).

GenBank accession numbers

BasCV-1 [NZ-NZG01-Sef-2012] KM510189, BasCV-1 [NZ-NZG03-Wel-2012] KM510190, BasCV-2 [NZ-NZG03-Wel-2012] KM510191, BasCV-3 [NZ-NZG01-Sef-2012] KM510192, BasCV-4 [FR- FR38-38-Cam-2010] KP005454, TasCV-1 [FR- FR34-34-Cam-2010] KP0054543

Author information

Authors and Affiliations

  1. School of Biological Sciences and Biomolecular Interaction Centre, University of Canterbury, Private Bag 4800, Christchurch, 8140, New Zealand

    Simona Kraberger, Kata Farkas & Arvind Varsani

  2. CIRAD-INRA-SupAgro, UMR BGPI, Campus International de Montferrier-Baillarguet, 34398, Montpellier Cedex-5, France

    Pauline Bernardo & Philippe Roumagnac

  3. 818 Marshmans Road, Sefton, RD2, 7472, Rangiroa, New Zealand

    Cameron Booker

  4. División de Biología Molecular, Instituto Potosino de Investigación Científica y Tecnológica, Camino a la Presa San José 2055, 78216, San Luis Potosí, S.L.P., Mexico

    Gerardo R. Argüello-Astorga

  5. Université d’Avignon et des Pays de Vaucluse, UMR CNRS/IRD IMBE 7263/237, Institut Méditerranéen de Biodiversité et d’Écologie, IUT Agroparc, BP 61207 Avignon Cedex 9, France

    François Mesléard

  6. Tour du Valat, Centre de recherche pour la conservation des zones humides méditerranéennes, 13 200 Le Sambuc-Arles, France

    François Mesléard

  7. Computational Biology Group, Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Cape Town, 7925, South Africa

    Darren P. Martin

  8. Electron Microscope Unit, Division of Medical Biochemistry, Department of Clinical Laboratory Sciences, University of Cape Town, Rondebosch, Cape Town, 7700, South Africa

    Arvind Varsani

  9. Department of Plant Pathology and Emerging Pathogens Institute, University of Florida, Gainesville, FL, 32611, USA

    Arvind Varsani

Authors
  1. Simona Kraberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kata Farkas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pauline Bernardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cameron Booker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gerardo R. Argüello-Astorga
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. François Mesléard
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Darren P. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Philippe Roumagnac
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Arvind Varsani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Philippe Roumagnac or Arvind Varsani.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1 Details of grass samples collected and screened for this study (DOC 73 kb)

705_2015_2358_MOESM2_ESM.doc

Supplementary Table 2 Details for bromus-associated circular DNA viral isolates and back-to-back primers used to recover full genomes (DOC 32 kb)

705_2015_2358_MOESM3_ESM.pdf

Supplementary Figure 1 Comparisons of the replication origin regions of BasCV-3 and SsHADV-1, illustrating the resemblance between their putative Rep-binding sites (iterons). Note that the nick site (the conserved nonanucleotide) of BasCV-3 differs from that of SsHADV-1 at position N5 (PDF 406 kb)

705_2015_2358_MOESM4_ESM.pdf

Supplementary Figure 2 Correlations between iteron core sequences and potential Rep DNA-binding SPDs of BasCV-3 and selected gemycircularviruses. Amino acid residues identified as putative SPDs in the beta-1 strand (r1) are shaded in yellow, whereas SPDs in the beta-strand (r-2) associated with motif II are shaded in blue. The conserved RCR motifs I and II are indicated at the top of the alignments. The N-terminus of the Rep of BasCV-1 is also aligned to show the similarity of its RCR motifs with those of gemycircularviruses (PDF 431 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kraberger, S., Farkas, K., Bernardo, P. et al. Identification of novel Bromus- and Trifolium-associated circular DNA viruses. Arch Virol 160, 1303–1311 (2015). https://doi.org/10.1007/s00705-015-2358-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-015-2358-6

Keywords

Search

Navigation