1887

Abstract

A virus with a large genome was identified in the transcriptome of the potato aphid () and was named virus 1 (MeV-1). The MeV-1 genome is 22 780 nt in size, including 3′ and 5′ non-coding regions, with a single large ORF encoding a putative polyprotein of 7333 aa. The C-terminal region of the predicted MeV-1 polyprotein contained sequences with similarities to helicase, methyltransferase and RNA-dependent RNA polymerase (RdRp) motifs, while the N-terminal region lacked any motifs including structural proteins. Phylogenetic analysis of the helicase placed MeV-1 close to pestiviruses, while the RdRp region placed it close to pestiviruses and flaviviruses, suggesting MeV-1 has a positive-polarity ssRNA genome and is a member of the family . Since the MeV-1 genome is predicted to contain a methyltransferase, a gene present typically in flaviviruses but not pestiviruses, MeV-1 is likely a member of the genus . MeV-1 was present in nymphal and adult stages of the aphid, aphid saliva and plant tissues fed upon by aphids. However, the virus was unable to multiply and spread in tomato plants. In addition, dsRNA, the replication intermediate of RNA viruses, was isolated from virus-infected and not from tomato plants infested with the aphid. Furthermore, nymphs laid without exposure to infected plants harboured the virus, indicating that MeV-1 is an aphid-infecting virus likely transmitted transovarially. The virus was present in populations from Europe but not from North America and was absent in all other aphid species tested.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000414
2016-05-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/5/1261.html?itemId=/content/journal/jgv/10.1099/jgv.0.000414&mimeType=html&fmt=ahah

References

  1. Agranovsky A. A., Dolja V. V., Kavsan V. M., Atabekov J. G. 1978; Detection of polyadenylate sequences in RNA components of barley stripe mosaic virus. Virology 91:95–105 [View Article][PubMed]
    [Google Scholar]
  2. Asghar N., Lindblom P., Melik W., Lindqvist R., Haglund M., Forsberg P., Överby A. K., Andreassen Å., Lindgren P. E., Johansson M. 2014; Tick-borne encephalitis virus sequenced directly from questing and blood-feeding ticks reveals quasispecies variance. PLoS One 9:e103264 [View Article][PubMed]
    [Google Scholar]
  3. Atamian H. S., Chaudhary R., Cin V. D., Bao E., Girke T., Kaloshian I. 2013; In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity. Mol Plant Microbe Interact 26:67–74 [View Article][PubMed]
    [Google Scholar]
  4. Ban L., Didon A., Jonsson L. M., Glinwood R., Delp G. 2007; An improved detection method for the Rhopalosiphum padi virus (RhPV) allows monitoring of its presence in aphids and movement within plants. J Virol Methods 142:136–142 [View Article][PubMed]
    [Google Scholar]
  5. Bao E., Jiang T., Kaloshian I., Girke T. 2011; SEED: efficient clustering of next-generation sequences. Bioinformatics 27:2502–2509[PubMed]
    [Google Scholar]
  6. 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 [View Article][PubMed]
    [Google Scholar]
  7. Bekal S., Domier L. L., Gonfa B., McCoppin N. K., Lambert K. N., Bhalerao K. 2014; A novel flavivirus in the soybean cyst nematode. J Gen Virol 95:1272–1280 [View Article][PubMed]
    [Google Scholar]
  8. 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]
  9. Bhattarai K. K., Atamian H. S., Kaloshian I., Eulgem T. 2010; WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1 . Plant J 63:229–240 [View Article][PubMed]
    [Google Scholar]
  10. Blackman R. L., Eastop V. F. 2000 Aphids on the World's Crops John Wiley & Sons; Chichester, UK:
    [Google Scholar]
  11. Carolan J. C., Fitzroy C. I. J., Ashton P. D., Douglas A. E., Wilkinson T. L. 2009; The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9:2457–2467 [View Article][PubMed]
    [Google Scholar]
  12. Carolan J. C., Caragea D., Reardon K. T., Mutti N. S., Dittmer N., Pappan K., Cui F., Castaneto M., Poulain J., other authors. 2011; Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach. J Proteome Res 10:1505–1518 [View Article][PubMed]
    [Google Scholar]
  13. Chaudhary R., Atamian H. S., Shen Z., Briggs S. P., Kaloshian I. 2014; GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proc Natl Acad Sci U S A 111:8919–8924 [View Article][PubMed]
    [Google Scholar]
  14. Chaudhary R., Atamian H. S., Shen Z., Briggs S. P., Kaloshian I. 2015; Potato aphid salivary proteome: enhanced salivation using resorcinol and identification of aphid phosphoproteins. J Proteome Res 14:1762–1778 [View Article][PubMed]
    [Google Scholar]
  15. Chiu C. Y. 2013; Viral pathogen discovery. Curr Opin Microbiol 16:468–478 [View Article][PubMed]
    [Google Scholar]
  16. Cooper W. R., Dillwith J. W., Puterka G. J. 2010; Salivary proteins of Russian wheat aphid (Hemiptera: Aphididae). Environ Entomol 39:223–231 [View Article][PubMed]
    [Google Scholar]
  17. Cooper W. R., Dillwith J. W., Puterka G. J. 2011; Comparisons of salivary proteins from five aphid (Hemiptera: Aphididae) species. Environ Entomol 40:151–156 [View Article][PubMed]
    [Google Scholar]
  18. Daly M., Ward F. 2003; Liver disease. In Clinical Pharmacy and Therapeutics, 3rd edn. pp 209–228Edited by Walker R., Edwards C. London: Churchill Livingstone;
    [Google Scholar]
  19. De Barro P. J. 1992; The role of temperature, photoperiod, crowding and plant quality on the production of alate viviparous females of the bird cherry-oat aphid, Rhopalosiphum padi . Entomol Exp Appl 65:205–214 [View Article]
    [Google Scholar]
  20. Finn R. D., Bateman A., Clements J., Coggill P., Eberhardt R. Y., Eddy S. R., Heger A., Hetherington K., Holm L., other authors. 2014; Pfam: the protein families database. Nucleic Acids Res 42:D222–D230 [View Article][PubMed]
    [Google Scholar]
  21. Harmel N., Létocart E., Cherqui A., Giordanengo P., Mazzucchelli G., Guillonneau F., De Pauw E., Haubruge E., Francis F. 2008; Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae . Insect Mol Biol 17:165–174 [View Article][PubMed]
    [Google Scholar]
  22. International Aphid Genomics Consortium 2010; Genome sequence of the pea aphid Acyrthosiphon pisum . PLoS Biol 8:e1000313 [View Article][PubMed]
    [Google Scholar]
  23. Junglen S., Drosten C. 2013; Virus discovery and recent insights into virus diversity in arthropods. Curr Opin Microbiol 16:507–513 [View Article][PubMed]
    [Google Scholar]
  24. Khan A. H., Morita K., del Carmen Parquet M., Hasebe F., Mathenge E. G. M., Igarashi A. 2002; Complete nucleotide sequence of chikungunya virus and evidence for an internal polyadenylation site. J Gen Virol 83:3075–3084 [View Article][PubMed]
    [Google Scholar]
  25. King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. editors 2012; Ninth Report of the International Committee on Taxonomy of Viruses. In Virus Taxonomy p ii San Diego: Elsevier; [CrossRef]
    [Google Scholar]
  26. Kobayashi K., Atsumi G., Iwadate Y., Tomita R., Chiba K.-i., 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 [View Article]
    [Google Scholar]
  27. Li C. X., Shi M., Tian J. H., Lin X. D., Kang Y. J., Chen L. J., Qin X. C., Xu J., Holmes E. C., Zhang Y. Z. 2015; Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4:4 [View Article][PubMed]
    [Google Scholar]
  28. Lipkin W. I., Firth C. 2013; Viral surveillance and discovery. Curr Opin Virol 3:199–204 [View Article][PubMed]
    [Google Scholar]
  29. Liu Y., Liu H., Zou J., Zhang B., Yuan Z. 2014; Dengue virus subgenomic RNA induces apoptosis through the Bcl-2-mediated PI3k/Akt signaling pathway. Virology 448:15–25 [View Article][PubMed]
    [Google Scholar]
  30. Liu S., Chen Y., Bonning B. C. 2015; RNA virus discovery in insects. Curr Opin Insect Sci 8:54–61 [View Article]
    [Google Scholar]
  31. 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]
  32. Miles P. W. 1968; Insect secretions in plants. Annu Rev Phytopathol 6:137–164 [View Article]
    [Google Scholar]
  33. Moon J. S., Domier L. L., McCoppin N. K., D'Arcy C. J., Jin H. 1998; Nucleotide sequence analysis shows that Rhopalosiphum padi virus is a member of a novel group of insect-infecting RNA viruses. Virology 243:54–65 [View Article][PubMed]
    [Google Scholar]
  34. Nicholson S. J., Hartson S. D., Puterka G. J. 2012; Proteomic analysis of secreted saliva from Russian wheat aphid (Diuraphis noxia Kurd.) biotypes that differ in virulence to wheat. J Proteomics 75:2252–2268 [View Article][PubMed]
    [Google Scholar]
  35. Rao S. A. K., Carolan J. C., Wilkinson T. L. 2013; Proteomic profiling of cereal aphid saliva reveals both ubiquitous and adaptive secreted proteins. PLoS One 8:e57413 [View Article][PubMed]
    [Google Scholar]
  36. Ryabov E. V. 2007; A novel virus isolated from the aphid Brevicoryne brassicae with similarity to Hymenoptera picorna-like viruses. J Gen Virol 88:2590–2595 [View Article][PubMed]
    [Google Scholar]
  37. Ryabov E. V., Keane G., Naish N., Evered C., Winstanley D. 2009; Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea . Proc Natl Acad Sci U S A 106:8465–8470 [View Article][PubMed]
    [Google Scholar]
  38. Rybicki E. P., von Wechmar M. B. 1982; Characterisation of an aphid-transmitted virus disease of small grains. Isolation and partial characterization of three viruses. J Phytopathol 103:306–322 [View Article]
    [Google Scholar]
  39. Salem N. M., Chen A. Y., Tzanetakis I. E., Mongkolsiriwattana C., Ng J. C. 2009; Further complexity of the genus Crinivirus revealed by the complete genome sequence of Lettuce chlorosis virus (LCV) and the similar temporal accumulation of LCV genomic RNAs 1 and 2. Virology 390:45–55 [View Article][PubMed]
    [Google Scholar]
  40. Schulz M. H., Zerbino D. R., Vingron M., Birney E. 2012; Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28:1086–1092 [View Article][PubMed]
    [Google Scholar]
  41. Srinivasan K. G., Min B. E., Ryu K. H., Adkins S., Wong S. M. 2005; Determination of complete nucleotide sequence of Hibiscus latent Singapore virus: evidence for the presence of an internal poly(A) tract. Arch Virol 150:153–166 [View Article][PubMed]
    [Google Scholar]
  42. 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]
  43. Tjallingii W. F. 2006; Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 57:739–745 [View Article][PubMed]
    [Google Scholar]
  44. Valverde R. A., Nameth S. T., Jordan R. L. 1990; Analysis of double-stranded RNA for plant virus diagnosis. Plant Dis 74:255–258 [CrossRef]
    [Google Scholar]
  45. van der Wilk F., Dullemans A. M., Verbeek M., van den Heuvel J.F.J.M. 1997; Nucleotide sequence and genomic organization of Acyrthosiphon pisum virus. Virology 238:353–362 [View Article][PubMed]
    [Google Scholar]
  46. van Munster M., Dullemans A. M., Verbeek M., Van Den Heuvel J.F.J.M., Clérivet A., van der Wilk F. 2002; Sequence analysis and genomic organization of Aphid lethal paralysis virus: a new member of the family Dicistroviridae . J Gen Virol 83:3131–3138 [View Article][PubMed]
    [Google Scholar]
  47. van Munster M., Dullemans A. M., Verbeek M., van den Heuvel J. F., Reinbold C., Brault V., Clérivet A., van der Wilk F. 2003a; Characterization of a new densovirus infecting the green peach aphid Myzus persicae . J Invertebr Pathol 84:6–14 [View Article][PubMed]
    [Google Scholar]
  48. van Munster M., Dullemans A. M., Verbeek M., van den Heuvel J.F.J.M., Reinbold C., Brault V., Clérivet A., van der Wilk F. 2003b; A new virus infecting Myzus persicae has a genome organization similar to the species of the genus Densovirus . J Gen Virol 84:165–172 [View Article][PubMed]
    [Google Scholar]
  49. Vandermoten S., Harmel N., Mazzucchelli G., De Pauw E., Haubruge E., Francis F. 2014; Comparative analyses of salivary proteins from three aphid species. Insect Mol Biol 23:67–77 [View Article][PubMed]
    [Google Scholar]
  50. Vlachakis D., Koumandou V. L., Kossida S. 2013; A holistic evolutionary and structural study of Flaviviridae provides insights into the function and inhibition of HCV helicase. PeerJ 1:e74 [View Article][PubMed]
    [Google Scholar]
  51. Williamson C., Rybicki E. P., Kasdorf G. G. F., Von Wechmar M. B. 1988; Characterization of a new picorna-like virus isolated from aphids. J Gen Virol 69:787–795 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000414
Loading
/content/journal/jgv/10.1099/jgv.0.000414
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
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