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
2020-02-19
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. Virology91:95–105 [CrossRef][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 One9:e103264 [CrossRef][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 Interact26:67–74 [CrossRef][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 Methods142:136–142 [CrossRef][PubMed]
    [Google Scholar]
  5. Bao E., Jiang T., Kaloshian I., Girke T.. 2011; SEED: efficient clustering of next-generation sequences. Bioinformatics27:2502–2509[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 Virol92:1870–1879 [CrossRef][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 Virol95:1272–1280 [CrossRef][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 Pathog6:e1001030 [CrossRef][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 J63:229–240 [CrossRef][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. Proteomics9:2457–2467 [CrossRef][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 Res10:1505–1518 [CrossRef][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 A111:8919–8924 [CrossRef][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 Res14:1762–1778 [CrossRef][PubMed]
    [Google Scholar]
  15. Chiu C. Y.. 2013; Viral pathogen discovery. Curr Opin Microbiol16:468–478 [CrossRef][PubMed]
    [Google Scholar]
  16. Cooper W. R., Dillwith J. W., Puterka G. J.. 2010; Salivary proteins of Russian wheat aphid (Hemiptera: Aphididae). Environ Entomol39:223–231 [CrossRef][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 Entomol40:151–156 [CrossRef][PubMed]
    [Google Scholar]
  18. Daly M., Ward F.. 2003; Liver disease. In Clinical Pharmacy and Therapeutics, 3rd edn. pp209–228Edited 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 Appl65:205–214 [CrossRef]
    [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 Res42:D222–D230 [CrossRef][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 Biol17:165–174 [CrossRef][PubMed]
    [Google Scholar]
  22. International Aphid Genomics Consortium 2010; Genome sequence of the pea aphid Acyrthosiphon pisum . PLoS Biol8:e1000313 [CrossRef][PubMed]
    [Google Scholar]
  23. Junglen S., Drosten C.. 2013; Virus discovery and recent insights into virus diversity in arthropods. Curr Opin Microbiol16:507–513 [CrossRef][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 Virol83:3075–3084 [CrossRef][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 pii 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 Pathol79:56–63 [CrossRef]
    [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. eLife4:4 [CrossRef][PubMed]
    [Google Scholar]
  28. Lipkin W. I., Firth C.. 2013; Viral surveillance and discovery. Curr Opin Virol3:199–204 [CrossRef][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. Virology448:15–25 [CrossRef][PubMed]
    [Google Scholar]
  30. Liu S., Chen Y., Bonning B. C.. 2015; RNA virus discovery in insects. Curr Opin Insect Sci8:54–61 [CrossRef]
    [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 Sci277:35–44 [CrossRef][PubMed]
    [Google Scholar]
  32. Miles P. W.. 1968; Insect secretions in plants. Annu Rev Phytopathol6:137–164 [CrossRef]
    [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. Virology243:54–65 [CrossRef][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 Proteomics75:2252–2268 [CrossRef][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 One8:e57413 [CrossRef][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 Virol88:2590–2595 [CrossRef][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 A106:8465–8470 [CrossRef][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 Phytopathol103:306–322 [CrossRef]
    [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. Virology390:45–55 [CrossRef][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. Bioinformatics28:1086–1092 [CrossRef][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 Virol150:153–166 [CrossRef][PubMed]
    [Google Scholar]
  42. Taylor D. J., Leach R. W., Bruenn J.. 2010; Filoviruses are ancient and integrated into mammalian genomes. BMC Evol Biol10:193 [CrossRef][PubMed]
    [Google Scholar]
  43. Tjallingii W. F.. 2006; Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot57:739–745 [CrossRef][PubMed]
    [Google Scholar]
  44. Valverde R. A., Nameth S. T., Jordan R. L.. 1990; Analysis of double-stranded RNA for plant virus diagnosis. Plant Dis74:255–258[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. Virology238:353–362 [CrossRef][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 Virol83:3131–3138 [CrossRef][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 Pathol84:6–14 [CrossRef][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 Virol84:165–172 [CrossRef][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 Biol23:67–77 [CrossRef][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. PeerJ1:e74 [CrossRef][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 Virol69:787–795 [CrossRef]
    [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

Most cited articles

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