1887

Abstract

Nematodes are the most abundant multicellular animals on earth, yet little is known about their natural viral pathogens. To date, only two nematode virus genomes have been reported. Consequently, nematode viruses have been overlooked as important biotic factors in the study of nematode ecology. Here, we show that one plant parasitic nematode species, , the soybean cyst nematode (SCN), harbours four different RNA viruses. The nematode virus genomes were discovered in the SCN transcriptome after high-throughput sequencing and assembly. All four viruses have negative-sense RNA genomes, and are distantly related to nyaviruses and bornaviruses, rhabdoviruses, bunyaviruses and tenuiviruses. Some members of these families replicate in and are vectored by insects, and can cause significant diseases in animals and plants. The novel viral sequences were detected in both eggs and the second juvenile stage of SCN, suggesting that these viruses are transmitted vertically. While there was no evidence of integration of viral sequences into the nematode genome, we indeed detected transcripts from these viruses by using quantitative PCR. These data are the first finding of virus genomes in parasitic nematodes. This discovery highlights the need for further exploration for nematode viruses in all tropic groups of these diverse and abundant animals, to determine how the presence of these viruses affects the fitness of the nematode, strategies of viral transmission and mechanisms of viral pathogenesis.

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2011-08-01
2021-08-02
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410[PubMed] [CrossRef]
    [Google Scholar]
  2. Ansorge W. J. 2009; Next-generation DNA sequencing techniques. New Biotechnol 25:195–203 [View Article][PubMed]
    [Google Scholar]
  3. Bailey T. L., Williams N., Misleh C., Li W. W. 2006; MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369-W373 [View Article][PubMed]
    [Google Scholar]
  4. Belyi V. A., Levine A. J., Skalka A. M. 2010; Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog 6:e1001030 [View Article][PubMed]
    [Google Scholar]
  5. Brown D. J., Robertson W. M., Trudgill D. L. 1995; Transmission of viruses by plant nematodes. Annu Rev Phytopathol 33:223–249 [View Article][PubMed]
    [Google Scholar]
  6. 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 [View Article][PubMed]
    [Google Scholar]
  7. Cubitt B., Oldstone C., de la Torre J. C. 1994; Sequence and genome organization of Borna disease virus. J Virol 68:1382–1396[PubMed]
    [Google Scholar]
  8. Culley A. I., Lang A. S., Suttle C. A. 2006; Metagenomic analysis of coastal RNA virus communities. Science 312:1795–1798 [View Article][PubMed]
    [Google Scholar]
  9. Edwards R. A., Rohwer F. 2005; Viral metagenomics. Nat Rev Microbiol 3:504–510 [View Article][PubMed]
    [Google Scholar]
  10. Endo B. Y. 1971; Nematode-induced syncytia (giant cells) host–parasite relationships of Heteroderidae. In Plant Parasitic Nematodes pp. 91–117 Edited by Zuckerman B. M., Mai W. F., Rohde R. A. New York: Academic Press;
    [Google Scholar]
  11. Falk B. W., Tsai J. H. 1998; Biology and molecular biology of viruses in the genus Tenuivirus . Annu Rev Phytopathol 36:139–163 [View Article][PubMed]
    [Google Scholar]
  12. Félix M. A., Ashe A., Piffaretti J., Wu G., Nuez I., Bélicard T., Jiang Y., Zhao G., Franz C. J. et al. 2011; Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol 9:e1000586 [View Article][PubMed]
    [Google Scholar]
  13. Flick R., Elgh F., Pettersson R. F. 2002; Mutational analysis of the Uukuniemi virus (Bunyaviridae family) promoter reveals two elements of functional importance. J Virol 76:10849–10860 [View Article][PubMed]
    [Google Scholar]
  14. Foor W. E. 1972; Viruslike particles in a nematode. J Parasitol 58:1065–1070 [View Article][PubMed]
    [Google Scholar]
  15. Gray S. M., Banerjee N. 1999; Mechanisms of arthropod transmission of plant and animal viruses. Microbiol Mol Biol Rev 63:128–148[PubMed]
    [Google Scholar]
  16. Liu W. H., Lin Y. L., Wang J. P., Liou W., Hou R. F., Wu Y. C., Liao C. L. 2006; Restriction of vaccinia virus replication by a ced-3 and ced-4-dependent pathway in Caenorhabditis elegans . Proc Natl Acad Sci U S A 103:4174–4179 [View Article][PubMed]
    [Google Scholar]
  17. Loewenberg J. R., Sullivan T., Schuster M. L. 1959; A virus disease of Meloidogyne incognita incognita, the southern root knot nematode. Nature 184:Suppl 241896 [View Article][PubMed]
    [Google Scholar]
  18. 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 [View Article][PubMed]
    [Google Scholar]
  19. Lu R., Maduro M., Li F., Li H. W., Broitman-Maduro G., Li W. X., Ding S. W. 2005; Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans . Nature 436:1040–1043 [View Article][PubMed]
    [Google Scholar]
  20. Mihindukulasuriya K. A., Nguyen N. L., Wu G., Huang H. V., da Rosa A. P., Popov V. L., Tesh R. B., Wang D. 2009; Nyamanini and midway viruses define a novel taxon of RNA viruses in the order Mononegavirales. J Virol 83:5109–5116 [View Article][PubMed]
    [Google Scholar]
  21. Neumann G., Whitt M. A., Kawaoka Y. 2002; A decade after the generation of a negative-sense RNA virus from cloned cDNA – what have we learned?. J Gen Virol 83:2635–2662[PubMed]
    [Google Scholar]
  22. Niblack T. L., Heinz R. D., Smith G. S., Donald P. A. 1993; Distribution, density, and diversity of Heterodera glycines populations in Missouri. J Nematol 25:880–886
    [Google Scholar]
  23. Opperman C. H., Bird D. M. 1998; The soybean cyst nematode, Heterodera glycines: a genetic model system for the study of plant-parasitic nematodes. Curr Opin Plant Biol 1:342–346 [View Article][PubMed]
    [Google Scholar]
  24. Poinar G. O. Jr, Hess R. 1977; Virus-like particles in the nematode Romanomermis culicivorax (Mermithidae). Nature 266:256–257 [View Article][PubMed]
    [Google Scholar]
  25. Poinar G. O. Jr, Hess R. T., Cole A. 1980; Replication of an Iridovirus in a nematode (Mermithidae). Intervirology 14:316–320 [View Article][PubMed]
    [Google Scholar]
  26. Quan P. L., Junglen S., Tashmukhamedova A., Conlan S., Hutchison S. K., Kurth A., Ellerbrok H., Egholm M., Briese T., Leendertz F. H. 2010; Moussa virus: a new member of the Rhabdoviridae family isolated from Culex decens mosquitoes in Côte d’Ivoire. Virus Res 147:17–24 [View Article][PubMed]
    [Google Scholar]
  27. Rassa J. C., Wilson G. M., Brewer G. A., Parks G. D. 2000; Spacing constraints on reinitiation of paramyxovirus transcription: the gene end U tract acts as a spacer to separate gene end from gene start sites. Virology 274:438–449 [View Article][PubMed]
    [Google Scholar]
  28. Revill P., Trinh X., Dale J., Harding R. 2005; Taro vein chlorosis virus: characterization and variability of a new nucleorhabdovirus. J Gen Virol 86:491–499 [View Article][PubMed]
    [Google Scholar]
  29. Riddle D. L., Blumenthal T., Meyer B. J., Priess J. R. 1997 C. elegans II, 2nd edn Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  30. Schubert M., Keene J. D., Herman R. C., Lazzarini R. A. 1980; Site on the vesicular stomatitis virus genome specifying polyadenylation and the end of the L gene mRNA. J Virol 34:550–559[PubMed]
    [Google Scholar]
  31. Shaham S. 2006; Worming into the cell: viral reproduction in Caenorhabditis elegans . Proc Natl Acad Sci U S A 103:3955–3956 [View Article][PubMed]
    [Google Scholar]
  32. Takahashi M., Yunker C. E., Clifford C. M., Nakano W., Fujino N., Tanifuji K., Thomas L. A. 1982; Isolation and characterization of Midway virus: a new tick-borne virus related to Nyamanini . J Med Virol 10:181–193 [View Article][PubMed]
    [Google Scholar]
  33. Tanno F., Nakatsu A., Toriyama S., Kojima M. 2000; Complete nucleotide sequence of Northern cereal mosaic virus and its genome organization. Arch Virol 145:1373–1384 [View Article][PubMed]
    [Google Scholar]
  34. Taylor D. J., Leach R. W., Bruenn J. 2010; Filoviruses are ancient and integrated into mammalian genomes. BMC Evol Biol 10:193 [View Article][PubMed]
    [Google Scholar]
  35. Telford M. J., Bourlat S. J., Economou A., Papillon D., Rota-Stabelli O. 2008; The evolution of the Ecdysozoa . Philos Trans R Soc Lond B Biol Sci 363:1529–1537 [View Article][PubMed]
    [Google Scholar]
  36. Toriyama S., Takahashi M., Sano Y., Shimizu T., Ishihama A. 1994; Nucleotide sequence of RNA 1, the largest genomic segment of rice stripe virus, the prototype of the tenuiviruses. J Gen Virol 75:3569–3579 [View Article][PubMed]
    [Google Scholar]
  37. Wang C. L., Lower S., Williamson V. M. 2009; Application of Pluronic gel to the study of root-knot nematode behaviour. Nematology 11:453–464 [View Article]
    [Google Scholar]
  38. Wilson E. O. 2003; The encyclopedia of life. Trends Ecol Evol 18:77–80 [View Article]
    [Google Scholar]
  39. 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]
  40. Zeigler R. S., Morales F. J. 1990; Genetic determination of replication of Rice hoja blanca virus within its planthopper vector Sogatodes oryzicola . Phytopathology 80:559–566 [View Article]
    [Google Scholar]
  41. Zuckerman B. M., Himmelho S., Kisiel M. 1973; Virus-like particles in Dolichodorus heterocephalus . Nematologica 19:117 [View Article]
    [Google Scholar]
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