Skip to main content
SpringerLink
Log in

Multiple polyadenylated RNA viruses detected in pooled cultivated and wild plant samples

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

RNA extracted from 120 leaf specimens from 17 plant species was pooled, and polyadenylated RNA species were sequenced together without barcoding in one lane using massively parallel sequencing technology. After analysis, complete or partial genome sequences representing 20 virus isolates of 16 polyadenylated RNA species were identified. In three cases, 2-3 distinct isolates of a virus species co-infected the same plant. Twelve of the viruses identified were described previously and belonged to the genera Potyvirus, Nepovirus, Allexivirus, and Carlavirus. Four were unknown and are proposed as members of the genera Potyvirus, Sadwavirus, and Trichovirus. Virus sequences were subsequently matched to original host plants using RT-PCR assays.

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
Fig. 4

Similar content being viewed by others

References

  1. Adams MJ, Antoniw JF, Bar-Joseph M, Brunt AA, Candresse T, Foster GD, Martelli GP, Milne RG, Fauquet CM (2004) The new plant virus family Flexiviridae and assessment of molecular criteria for species demarcation. Arch Virol 149:1045–1060

    PubMed  CAS  Google Scholar 

  2. Adams MJ, Antoniw JF, Fauquet CM (2005) Molecular criteria for genus and species discrimination within the family Potyviridae. Arch Virol 150:459–479

    Article  PubMed  CAS  Google Scholar 

  3. Adams IP, Glover RH, Monger WA, Mumford R, Jackeviciene E, Navalinskiene M, Samuitiene M, Boonham N (2009) Next-generation sequencing and metagenomic analysis: a universal diagnostic tool in plant virology. Mol Plant Pathol 10:537–545

    Article  PubMed  CAS  Google Scholar 

  4. Al Rwahnih M, Daubert S, Golino D, Rowhani A (2009) Deep sequencing analysis of RNAs from a grapevine showing Syrah decline symptoms reveals a multiple virus infection that includes a novel virus. Virology 387:395–401

    Article  PubMed  CAS  Google Scholar 

  5. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  6. Asjes CJ (1998) Data Sheet on Lily Mottle Potyvirus for CABI Crop Protection Compendium. CABI Information. Wallingford, Oxon

    Google Scholar 

  7. Balijja A, Kvarnheden A, Turchetti T (2008) A non-phenol–chloroform extraction of double-stranded RNA from plant and fungal tissues. J Virol Methods 152:32–37

    Article  PubMed  CAS  Google Scholar 

  8. Blouin AG, Greenwood DR, Chavan RR, Pearson MN, Clover GRG, MacDiarmid RM, Cohen D (2010) A generic method to identify plant viruses by high-resolution tandem mass spectrometry of their coat proteins. J Virol Methods 163:49–56

    Article  PubMed  CAS  Google Scholar 

  9. Boonham N, Adams I, Glover R, Monger W, Hodges T, Ashton P (2010) High throughput sequencing—next wave diagnostics. Phytopathology 100(suppl. 1):S154

    Google Scholar 

  10. Carstens EB (2010) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2009). Arch Virol 155:133–146

    Article  PubMed  CAS  Google Scholar 

  11. Chen J, Zheng HY, Antoniw JF, Adams MJ, Chen JP, Lin L (2004) Detection and classification of allexiviruses from garlic in China. Arch Virol 149:435–445

    Article  PubMed  CAS  Google Scholar 

  12. Chung BYW, Miller WA, Atkins JF, Firth AE (2008) An over-lapping essential gene in the Potyviridae. Proc Natl Acad Sci USA 105:5897–5902

    Article  PubMed  CAS  Google Scholar 

  13. Coetzee B, Freeborough M-J, Maree HJ, Celton J-M, Rees DJG, Burger JT (2010) Deep sequencing analysis of viruses infecting grapevines: virome of a vineyard. Virology 400:157–163

    Article  PubMed  CAS  Google Scholar 

  14. Conci VC, Canavelli AE, Balzarini MG (2010) The distribution of garlic viruses in leaves and bulbs during the first year of infection. J Phytopath 158:186–193

    Article  Google Scholar 

  15. Donaire L, Wang Y, Gonzalez-Ibeas D, Mayer KF, Aranda MA, Llave C (2009) Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology 392:203–214

    Article  PubMed  CAS  Google Scholar 

  16. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.4. http://www.geneious.com. Accessed 15 June 2011

  17. Eisen JA (2007) Environmental shotgun sequencing: its potential and challenges for studying the hidden world of microbes. PLoS Biol 5:e82

    Article  PubMed  Google Scholar 

  18. Gibbs AJ, Mackenzie AM, Wei KJ, Gibbs MJ (2008) The potyviruses of Australia. Arch Virol 153:1411–1420

    Article  PubMed  CAS  Google Scholar 

  19. Gorbalenya AE, Donchenko AP, Blinov VM, Koonin EV (1989) Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases. FEBS Lett 243:103–114

    Article  PubMed  CAS  Google Scholar 

  20. Gorbalenya AE, Koonin EV, Wolf YI (1990) A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. FEBS Lett 262:145–148

    Article  PubMed  CAS  Google Scholar 

  21. Hagen C, Frizzi A, Kao J, Jia L, Huang M, Zhang Y, Huang S (2011) Using small RNA sequences to diagnose, sequence, and investigate the infectivity characteristics of vegetable-infecting viruses. Arch Virol 156:1209–1216

    Article  PubMed  CAS  Google Scholar 

  22. Haible D, Kober S, Jeske H (2006) Rolling circle amplification revolutionizes diagnosis and genomics of geminiviruses. J Virol Methods 135:9–16

    Article  PubMed  CAS  Google Scholar 

  23. Hanada K, Fukumoto F, Kusunoki M, Kameya-Iwaki M, Tanaka Y, Iwanami T (2006) Cycas necrotic stunt virus isolated from gladiolus plants in Japan. J Gen Plant Pathol 72:383–386

    Article  CAS  Google Scholar 

  24. Hiramatsu M, Ii K, Okubo H, Huang K-L, Huang C-W (2001) Biogeography and origin of Lilium longiflorum and L. formosanum (Liliaceae) endemic to the Ryukyu Archipelago and Taiwan as determined by allozyme diversity. Am J Bot 88:1230–1239

    Article  PubMed  CAS  Google Scholar 

  25. 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  PubMed  CAS  Google Scholar 

  26. Kusunoki M, Hanada K, Iwaki M, Chang MU, Doi Y, Yora K (1986) Cycas necrotic stunt virus, a new member of nepoviruses found in Cycas revolute-Host range, purification, serology and some other properties. Ann Phytopathol Soc Japan 52:302–311

    Article  Google Scholar 

  27. Le Gall O, Iwanami T, Jones AT, Lehto K, Sanfacon H, Wellink J, Wetzel T, Yoshikawa N (2005) Comoviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy, eighth report of the international committee on the taxonomy of viruses. Elsevier Academic Press, London, pp 807–818

    Google Scholar 

  28. Le Gall O, Sanfaçon H, Ikegami M, Iwanami T, Jones T, Karasev A, Lehto K, Wellink J, Wetzel T, Yoshikawa N (2007) Cheravirus and Sadwavirus: two unassigned genera of plant positive-sense single-stranded RNA viruses formerly considered atypical members of the genus Nepovirus (family Comoviridae). Arch Virol 152:1767–1774

    Article  PubMed  CAS  Google Scholar 

  29. Luo H, Wylie SJ, Jones MGK (2010) Identification of plant viruses using one-dimensional gel electrophoresis and peptide mass fingerprints. J Virol Meth 165:297–301

    Article  CAS  Google Scholar 

  30. Lutcke HA, Chow KC, Mickel FS, Moss KA, Kern HF, Scheele GA (1987) Selection of AUG initiation codons differs in plants and animals. EMBO J 6:43–48

    PubMed  CAS  Google Scholar 

  31. Martelli GP, Adams MJ, Kreuze JF, Dolja VV (2007) Family Flexiviridae: a case study in virion and genome plasticity. Ann Rev Phytopathol 45:73–100

    Article  CAS  Google Scholar 

  32. Mayo MA, Fritsch C (1994) A possible consensus sequence for VPg of viruses in the family Comoviridae. FEBS Lett 354:129–130

    Article  PubMed  CAS  Google Scholar 

  33. Melcher U, Muthukumar V, Wiley GB, Min BE, Palmer MW, Verchot-Lubicz J, Ali A, Nelson RS, Roe BA, Thapa V, Pierce ML (2008) Evidence for novel viruses by analysis of nucleic acids in virus-like particle fractions from Ambrosia psilostachya. J Virol Meth 152:49–55

    Article  CAS  Google Scholar 

  34. Morschel JR (1966) Recorded plant diseases in and outside australia: part 4–forest trees and ornamental plants. Commonwealth Department of Health Division of Plant Quarantine, Canberra

    Google Scholar 

  35. Mushegian AR (1994) The putative movement domain encoded by nepovirus RNA-2 is conserved in all sequenced nepoviruses. Arch Virol 135:437–441

    Article  PubMed  CAS  Google Scholar 

  36. Ochoa-Corona FM, Elliot DR, Tang Z, Lebas BSM, Alexander BJR (2003) Detection of Cycas necrotic stunt virus (CNSV) in post-entry quarantine stocks of ornamentals in New Zealand. Phytopathology 93:S67

    Google Scholar 

  37. Remah A, Jones AT, Mitchell MJ (1986) Purification and properties of lucerne Australian symptomless virus, a new virus infecting lucerne in Australia. Ann Appl Biol 109:307–315

    Article  Google Scholar 

  38. Riechmann JL, Lain S, Garcia JA (1992) Highlights and prospects of potyvirus molecular biology. J Gen Virol 73:1–16

    Article  PubMed  CAS  Google Scholar 

  39. Ritzenthaler C, Viry M, Pinck M, Margis R, Margis R, Fuchs M, Pinck L (1991) Complete nucleotide sequence and genetic organization of grapevine fanleaf nepovirus RNA1. J Gen Virol 72:2357–2365

    Article  PubMed  CAS  Google Scholar 

  40. Roossinck MJ, Saha P, Wiley GB, Quan J, White JD, Lai H, Chavarŕia F, Shen G, Roe BA (2010) Ecogenomics: using massively parallel pyrosequencing to understand virus ecology. Mol Ecol 19(Suppl. 1):81–88

    Article  PubMed  Google Scholar 

  41. Rott ME, Gilchrist A, Lee L, Rochon DM (1995) Nucleotide sequence of tomato ringspot virus RNA1. J Gen Virol 76:465–471

    Article  PubMed  CAS  Google Scholar 

  42. Sanfaçon H, Wellink J, Le Gall O, Karasev A, van der Vlugt R, Wetzel T (2009) Secoviridae: a proposed family of plant viruses within the order Picornavirales that combines the families Sequiviridae and Comoviridae, the unassigned genera Cheravirus. Arch Virol 154:899–907

    Article  PubMed  Google Scholar 

  43. Shukla DD, Ward CW, Brunt AA (1994) The Potyviridae. CAB International, Wallingford

    Google Scholar 

  44. Sward RJ (1990) Lettuce necrotic yellows rhabdovirus and other viruses infecting garlic. Australas Plant Pathol 19:46–51

    Article  Google Scholar 

  45. 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. doi:10.1093/molbev/msr121

  46. Tsuneyoshi T, Matsumi T, Natsuaka KT, Sumi S (1998) Nucleotide sequence analysis of virus isolates indicates the presence of three potyvirus species in Allium plants. Arch Virol 143:97–113

    Article  PubMed  CAS  Google Scholar 

  47. Webster C, Jones RAC, Coutts BA, Jones MGK, Wylie SJ (2007) Virus impact at the interface of an ancient ecosystem and a recent agroecosystem: studies on three legume-infecting potyviruses in the southwest Australian floristic region. Plant Pathol 56:729–742

    Article  CAS  Google Scholar 

  48. Westphal MI, Browne M, MacKinnon K, Noble I (2008) The link between international trade and the global distribution of invasive alien species. Biol Invasions 10:391–398

    Article  Google Scholar 

  49. Wren JD, Roossinck MJ, Nelson RS, Scheets K, Palmer MW, Melcher U (2006) Plant virus biodiversity and ecology. PLoS Biol 4:e80

    Article  PubMed  Google Scholar 

  50. Wu Q, Luo Y, Lu R, Lau N, Lai EC, Li WX, Ding SW (2010) Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc Natl Acad Sci USA 107:1606–1611

    Article  PubMed  CAS  Google Scholar 

  51. Wylie SJ, Jones MGK (2011) Characterisation and quantitation of mutant and wild-type genomes of Hardenbergia mosaic virus isolates co-infecting a wild plant of Hardenbergia comptoniana. Arch Virol 156:1287–1290

    Article  PubMed  CAS  Google Scholar 

  52. Wylie SJ, Jones MGK (2011) Hardenbergia virus A, a novel member of the Betaflexiviridae from a wild legume in South-west Australia. Arch Virol 156:1245–1250

    Article  PubMed  CAS  Google Scholar 

  53. Wylie SJ, Jones MGK (2011) The complete genome sequence of Passionfruit woodiness virus determined using deep sequencing, and its relationship to other potyviruses. Arch Virol 156:479–482

    Article  PubMed  CAS  Google Scholar 

  54. Yan F, Zhang HM, Adams MJ, Yang J, Peng JJ, Antoniw JF, Zhou YJ, Chen JP (2010) Characterization of siRNAs derived from rice stripe virus in infected rice plants by deep sequencing. Arch Virol 155:935–940

    Article  PubMed  CAS  Google Scholar 

  55. Yeh SD, Gonsalves D, Wang HL, Namba R (1988) Control of papaya ringspot virus by cross protection. Plant Dis 72:375–380

    Article  Google Scholar 

  56. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  PubMed  CAS  Google Scholar 

  57. Zheng HY, Chen J, Zhao MF, Lin L, Chen JP, Antoniw JF, Adams MJ (2003) Occurrence and sequences of Lily mottle virus and Lily symptomless virus in plants grown from imported bulbs in Zhejiang province, China. Arch Virol 148:2419–2428

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by an Australian Research Council Linkage Grant (LP110200180) and the Murdoch University Institutes of Sustainable Ecosystems, and Crop and Plant Research. Thanks to Professor Kingsley Dixon and Mr. Steve Easton, Botanic Gardens and Parks Authority, for authorizing collections at Kings Park and for assistance in collecting and identifying the plants used from there.

Author information

Authors and Affiliations

  1. Plant Virology Group, Western Australian State Agricultural Biotechnology Centre, School of Biological Sciences and Biotechnology, Murdoch University, Perth, WA, 6150, Australia

    Stephen J. Wylie, Hao Luo, Hua Li & Michael G. K. Jones

Authors
  1. Stephen J. Wylie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hao Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael G. K. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen J. Wylie.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 108 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wylie, S.J., Luo, H., Li, H. et al. Multiple polyadenylated RNA viruses detected in pooled cultivated and wild plant samples. Arch Virol 157, 271–284 (2012). https://doi.org/10.1007/s00705-011-1166-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-011-1166-x

Keywords

Search

Navigation