1887

Abstract

, the soybean cyst nematode (SCN), is a subterranean root pathogen that causes the most damaging disease of soybean in the USA. A novel nematode virus genome, soybean cyst nematode virus 5 (SbCNV-5), was identified in RNA sequencing data from SCN eggs and second-stage juveniles. The SbCNV-5 RNA-dependent RNA polymerase and RNA helicase domains had homology to pestiviruses in the family , suggesting that SbCNV-5 is a positive-polarity ssRNA virus. SbCNV-5 RNA was present in all nematode developmental stages, indicating a transovarial mode of transmission, but is also potentially sexually transmitted via the male. SbCNV-5 was common in SCN laboratory cultures and in nematode populations isolated from the field. Transmission electron microscopy of sections from a female SCN showed virus particles budding from the endoplasmic reticulum and in endosomes. The size of the viral genome was 19 191 nt, which makes it much larger than other known pestiviruses. Additionally, the presence of a methyltransferase in the SbCNV-5 genome is atypical for a pestivirus. When cDNA sequences were mapped to the genome of SbCNV-5, a disproportionate number aligned to the 3′ NTR, suggesting that SbCNV-5 produces a subgenomic RNA, which was confirmed by RNA blot analysis. As subgenomic RNAs and methyltransferases do not occur in pestiviruses, we conclude that SbCNV-5 is a new flavivirus infecting SCNs.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.060889-0
2014-06-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/6/1272.html?itemId=/content/journal/jgv/10.1099/vir.0.060889-0&mimeType=html&fmt=ahah

References

  1. Alatoom A. , Payne D. . ( 2009; ). An overview of arboviruses and bunyaviruses. . LabMedicine 40:, 237–240.
    [Google Scholar]
  2. Armstrong P. M. , Rico-Hesse R. . ( 2001; ). Differential susceptibility of Aedes aegypti to infection by the American and Southeast Asian genotypes of dengue type 2 virus. . Vector Borne Zoonotic Dis 1:, 159–168. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bekal S. , Domier L. L. , Niblack T. L. , Lambert K. N. . ( 2011; ). Discovery and initial analysis of novel viral genomes in the soybean cyst nematode. . J Gen Virol 92:, 1870–1879. [CrossRef] [PubMed]
    [Google Scholar]
  4. Belyi V. A. , Levine A. J. , Skalka A. M. . ( 2002; ). Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. . PLoS Pathog 6:, e1001030.[CrossRef]
    [Google Scholar]
  5. Bredenbeek P. J. , Kooi E. A. , Lindenbach B. , Huijkman N. , Rice C. M. , Spaan W. J. . ( 2003; ). A stable full-length yellow fever virus cDNA clone and the role of conserved RNA elements in flavivirus replication. . J Gen Virol 84:, 1261–1268. [CrossRef] [PubMed]
    [Google Scholar]
  6. Brinton M. A. , Dispoto J. H. . ( 1988; ). Sequence and secondary structure analysis of the 5′-terminal region of flavivirus genome RNA. . Virology 162:, 290–299. [CrossRef] [PubMed]
    [Google Scholar]
  7. Brinton M. A. , Fernandez A. V. , Dispoto J. H. . ( 1986; ). The 3′-nucleotides of flavivirus genomic RNA form a conserved secondary structure. . Virology 153:, 113–121. [CrossRef] [PubMed]
    [Google Scholar]
  8. Bryant J. E. , Vasconcelos P. F. , Rijnbrand R. C. , Mutebi J. P. , Higgs S. , Barrett A. D. . ( 2005; ). Size heterogeneity in the 3′ noncoding region of South American isolates of yellow fever virus. . J Virol 79:, 3807–3821. [CrossRef] [PubMed]
    [Google Scholar]
  9. Burrack S. , Aberle D. , Bürck J. , Ulrich A. S. , Meyers G. . ( 2012; ). A new type of intracellular retention signal identified in a pestivirus structural glycoprotein. . FASEB J 26:, 3292–3305. [CrossRef] [PubMed]
    [Google Scholar]
  10. Craig J. P. , Bekal S. , Hudson M. , Domier L. , Niblack T. , Lambert K. N. . ( 2008; ). Analysis of a horizontally transferred pathway involved in vitamin B6 biosynthesis from the soybean cyst nematode Heterodera glycines . . Mol Biol Evol 25:, 2085–2098. [CrossRef] [PubMed]
    [Google Scholar]
  11. Félix M. A. , Ashe A. , Piffaretti J. , Wu G. , Nuez I. , Bélicard T. , Jiang Y. , Zhao G. , Franz C. J. . & other authors ( 2011; ). Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. . PLoS Biol 9:, e1000586. [CrossRef] [PubMed]
    [Google Scholar]
  12. Foor W. E. . ( 1972; ). Viruslike particles in a nematode. . J Parasitol 58:, 1065–1070. [CrossRef] [PubMed]
    [Google Scholar]
  13. Funk A. , Truong K. , Nagasaki T. , Torres S. , Floden N. , Balmori Melian E. , Edmonds J. , Dong H. , Shi P. Y. , Khromykh A. A. . ( 2010; ). RNA structures required for production of subgenomic flavivirus RNA. . J Virol 84:, 11407–11417. [CrossRef] [PubMed]
    [Google Scholar]
  14. Gough J. , Karplus K. , Hughey R. , Chothia C. . ( 2001; ). Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. . J Mol Biol 313:, 903–919. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hobson-Peters J. , Yam A. W. Y. , Lu J. W. F. , Setoh Y. X. , May F. J. , Kurucz N. , Walsh S. , Prow N. A. , Davis S. S. . & other authors ( 2013; ). A new insect-specific flavivirus from northern Australia suppresses replication of West Nile virus and Murray Valley encephalitis virus in co-infected mosquito cells. . PLoS ONE 8:, e56534. [CrossRef] [PubMed]
    [Google Scholar]
  16. Hooper D. J. . ( 1974; ). Virus vector nematodes – taxonomy and general introduction. . In Nematode Vectors of Plant Viruses, pp. 1–14. Edited by Lamberti F. , Taylor C. E. , Seinhorst J. W. . . London:: Plenum Press;.
    [Google Scholar]
  17. Hoshino K. , Isawa H. , Tsuda Y. , Yano K. , Sasaki T. , Yuda M. , Takasaki T. , Kobayashi M. , Sawabe K. . ( 2007; ). Genetic characterization of a new insect flavivirus isolated from Culex pipiens mosquito in Japan. . Virology 359:, 405–414. [CrossRef] [PubMed]
    [Google Scholar]
  18. Huhtamo E. , Moureau G. , Cook S. , Julkunen O. , Putkuri N. , Kurkela S. , Uzcátegui N. Y. , Harbach R. E. , Gould E. A. . & other authors ( 2012; ). Novel insect-specific flavivirus isolated from northern Europe. . Virology 433:, 471–478. [CrossRef] [PubMed]
    [Google Scholar]
  19. Ibrahim I. K. A. , Hollis J. P. . ( 1973; ). Electron microscope studies on the cuticle of swarming and nonswarming Tylenchorhynchus martini . . J Nematol 5:, 275–281.[PubMed]
    [Google Scholar]
  20. Ibrahim I. K. A. , Joshi M. M. , Hollis J. P. . ( 1973; ). The swarming virus disease of Tylenchorhynchus martini . . In Second International Congress on Plant Pathology, Minneapolis:, Minnesota;, 5–12 September. Abstract no. 555.
    [Google Scholar]
  21. Kerry B. R. . ( 1987; ) Biological control. . In Principles and Practice of Nematode Control in Crops, pp. 233–264. Edited by Brown R. H. , Kerry B. R. . . Sydney, Australia:: Academic Press;.
    [Google Scholar]
  22. Kobayashi K. , Atsumi G. , Iwadate Y. , Tomita R. , Chiba K. , Akasaka S. , Nishihara M. , Takahashi H. , Yamaoka N. . & other authors ( 2013; ). Gentian Kobu-sho-associated virus: a tentative, novel double-stranded RNA virus that is relevant to gentian Kobu-sho syndrome. . J Gen Plant Pathol 79:, 56–63. [CrossRef]
    [Google Scholar]
  23. Kuhn J. H. , Bekal S. , Caì Y. , Clawson A. N. , Domier L. L. , Herrel M. , Jahrling P. B. , Kondo H. , Lambert K. N. . & other authors ( 2013; ). Nyamiviridae: proposal for a new family in the order Mononegavirales . . Arch Virol 158:, 2209–2226. [CrossRef] [PubMed]
    [Google Scholar]
  24. Liu R. , Yue L. , Li X. , Yu X. , Zhao H. , Jiang Z. , Qin E. , Qin C. . ( 2010; ). Identification and characterization of small sub-genomic RNAs in dengue 1–4 virus-infected cell cultures and tissues. . Biochem Biophys Res Commun 391:, 1099–1103. [CrossRef] [PubMed]
    [Google Scholar]
  25. Loewenberg J. R. , Sullivan T. , Schuster M. L. . ( 1959; ). A virus disease of Meloidogyne incognita incognita, the southern root knot nematode. . Nature 184: (Suppl 24), 1896. [CrossRef] [PubMed]
    [Google Scholar]
  26. Loewenstein Y. , Portugaly E. , Fromer M. , Linial M. . ( 2008; ). Efficient algorithms for accurate hierarchical clustering of huge datasets: tackling the entire protein space. . Bioinformatics 24:, i41–i49. [CrossRef] [PubMed]
    [Google Scholar]
  27. Longdon B. , Obbard D. J. , Jiggins F. M. . ( 2010; ). Sigma viruses from three species of Drosophila form a major new clade in the rhabdovirus phylogeny. . Proc Biol Sci 277:, 35–44. [CrossRef] [PubMed]
    [Google Scholar]
  28. Mackenzie J. M. , Westaway E. G. . ( 2001; ). Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. . J Virol 75:, 10787–10799. [CrossRef] [PubMed]
    [Google Scholar]
  29. Mankau R. . ( 1981; ). Microbial control of nematodes. . In Plant Parasitic Nematodes, Vol. 3, pp. 475–478. Edited by Zuckerman B. M. , Rohde R. A. . . New York:: Academic Press;. [CrossRef]
    [Google Scholar]
  30. Marklewitz M. , Handrick S. , Grasse W. , Kurth A. , Lukashev A. , Drosten C. , Ellerbrok H. , Leendertz F. H. , Pauli G. , Junglen S. . ( 2011; ). Gouleako virus isolated from West African mosquitoes constitutes a proposed novel genus in the family Bunyaviridae . . J Virol 85:, 9227–9234. [CrossRef] [PubMed]
    [Google Scholar]
  31. Markoff L. . ( 2003; ). 5′- and 3′-Noncoding regions in flavivirus RNA. . Adv Virus Res 59:, 177–228. [CrossRef] [PubMed]
    [Google Scholar]
  32. McBride J. M. , Hollis J. P. . ( 1966; ). Phenomenon of swarming in nematodes. . Nature 211:, 545–546. [CrossRef] [PubMed]
    [Google Scholar]
  33. Meyers G. , Rümenapf T. , Thiel H. J. . ( 1989; ). Molecular cloning and nucleotide sequence of the genome of hog cholera virus. . Virology 171:, 555–567. [CrossRef] [PubMed]
    [Google Scholar]
  34. Nasar F. , Palacios G. , Gorchakov R. V. , Guzman H. , Da Rosa A. P. T. , Savji N. , Popov V. L. , Sherman M. B. , Lipkin W. I. , Tesh R. B. , Weaver S. C. . ( 2012; ). Eilat virus, a newly identified host restricted alphavirus. . Proc Natl Acad Sci U S A 109:, 14622–14627. [CrossRef] [PubMed]
    [Google Scholar]
  35. Niblack T. L. , Heinz R. D. , Smith G. S. , Donald P. A. . ( 1993; ). Distribution, density, and diversity of Heterodera glycines in Missouri. . J Nematol 25: (Suppl), 880–886.[PubMed]
    [Google Scholar]
  36. Noda H. , Ishikawa K. , Hibino H. , Omura T. . ( 1991; ). A reovirus in the brown planthopper, Nilaparvata lugens . . J Gen Virol 72:, 2425–2430. [CrossRef] [PubMed]
    [Google Scholar]
  37. Poinar G. O. Jr , Hess R. . ( 1977; ). Virus-like particles in the nematode Romanomermis culicivorax (Mermithidae). . Nature 266:, 256–257. [CrossRef] [PubMed]
    [Google Scholar]
  38. Poinar G. O. Jr , Hess R. T. , Cole A. . ( 1980; ). Replication of an iridovirus in a nematode (Mermithidae). . Intervirology 14:, 316–320. [CrossRef] [PubMed]
    [Google Scholar]
  39. Prior A. , Jones J. T. , Blok V. C. , Beauchamp J. , McDermott L. , Cooper A. , Kennedy M. W. . ( 2001; ). A surface-associated retinol- and fatty acid-binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern. . Biochem J 356:, 387–394. [CrossRef] [PubMed]
    [Google Scholar]
  40. Proutski V. , Gould E. A. , Holmes E. C. . ( 1997; ). Secondary structure of the 3′ untranslated region of flaviviruses: similarities and differences. . Nucleic Acids Res 25:, 1194–1202. [CrossRef] [PubMed]
    [Google Scholar]
  41. Proutski V. , Gritsun T. S. , Gould E. A. , Holmes E. C. . ( 1999; ). Biological consequences of deletions within the 3′-untranslated region of flaviviruses may be due to rearrangements of RNA secondary structure.. . Virus Res 64:, 107–123.[CrossRef]
    [Google Scholar]
  42. Reeder J. , Steffen P. , Giegerich R. . ( 2007; ). pknotsRG: RNA pseudoknot folding including near-optimal structures and sliding windows. . Nucleic Acids Res 35: (Web Server), W320–W324. [CrossRef] [PubMed]
    [Google Scholar]
  43. Roby J. A. , Pijlman G. P. , Wilusz J. , Khromykh A. A. . ( 2014; ). Noncoding subgenomic flavivirus RNA: multiple functions in West Nile virus pathogenesis and modulation of host responses. . Viruses 6:, 404–427. [CrossRef] [PubMed]
    [Google Scholar]
  44. Sambrook J. , Russell D. W. . ( 2001; ). Molecular Cloning: a Laboratory Manual, , 3rd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory Press;.
    [Google Scholar]
  45. Schuessler A. , Funk A. , Lazear H. M. , Cooper D. A. , Torres S. , Daffis S. , Jha B. K. , Kumagai Y. , Takeuchi O. . & other authors ( 2012; ). West Nile virus noncoding subgenomic RNA contributes to viral evasion of the type I interferon-mediated antiviral response. . J Virol 86:, 5708–5718. [CrossRef] [PubMed]
    [Google Scholar]
  46. Silva P. A. , Pereira C. F. , Dalebout T. J. , Spaan W. J. , Bredenbeek P. J. . ( 2010; ). An RNA pseudoknot is required for production of yellow fever virus subgenomic RNA by the host nuclease XRN1. . J Virol 84:, 11395–11406. [CrossRef] [PubMed]
    [Google Scholar]
  47. Simmonds P. , Becher P. , Collett M. S. , Gould E. A. , Heinz F. X. , Meyers G. , Monath T. , Pletnev A. , Rice C. M. . & other authors ( 2012; ). Family Flaviviridae. . In Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses, pp. 1003–1020. Edited by King A. M. , Adams M. J. , Carstens E. B. , Lefkowitz E. J. . . Amsterdam:: Elsevier Academic Press;.
    [Google Scholar]
  48. Taylor D. J. , Leach R. W. , Bruenn J. . ( 2010; ). Filoviruses are ancient and integrated into mammalian genomes. . BMC Evol Biol 10:, 193.[CrossRef]
    [Google Scholar]
  49. Vasilakis N. , Forrester N. L. , Palacios G. , Nasar F. , Savji N. , Rossi S. L. , Guzman H. , Wood T. G. , Popov V. . & other authors ( 2013; ). Negevirus: a proposed new taxon of insect-specific viruses with wide geographic distribution. . J Virol 87:, 2475–2488. [CrossRef] [PubMed]
    [Google Scholar]
  50. Westaway E. G. , Mackenzie J. M. , Khromykh A. A. . ( 2003; ). Kunjin RNA replication and applications of Kunjin replicons. . Adv Virus Res 59:, 99–140. [CrossRef] [PubMed]
    [Google Scholar]
  51. Wrather J. A. , Koenning S. R. . ( 2006; ). Estimates of disease effects on soybean yields in the United States 2003 to 2005. . J Nematol 38:, 173–180.[PubMed]
    [Google Scholar]
  52. Zirkel F. , Kurth A. , Quan P. L. , Briese T. , Ellerbrok H. , Pauli G. , Leendertz F. H. , Lipkin W. I. , Ziebuhr J. , Drosten C. , Junglen S. . ( 2011; ). An insect nidovirus emerging from a primary tropical rainforest. mBiol 2:, e00077-11. [CrossRef]
    [Google Scholar]
  53. Zuckerman B. M. , Himmelho S. , Kisiel M. . ( 1973; ). Virus-like particles in Dolichodorus heterocephalus . . Nematologica 19:, 117. [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.060889-0
Loading
/content/journal/jgv/10.1099/vir.0.060889-0
Loading

Data & Media loading...

Supplementary material 

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error