1887

Abstract

(PrV) is a member of the family , a family of small, positive-sense, ssRNA viruses that exclusively infect lepidopteran insects. PrV is the only known tetravirus that replicates in tissue culture. We have analysed the genome and characterized the viral translation products, showing that PrV has a monopartite genome encoding three ORFs: (i) p130, unique to PrV and of unknown function; (ii) p104, which contains a read-through stop signal, producing an N-terminal product of 40 kDa (p40) and (iii) the capsid protein precursor (p81). There are three 2A-like processing sequences: one at the N terminus of p130 (PrV-2A) and two more (PrV-2A and PrV-2A) at the N terminus of p81. Metabolic radiolabelling identified viral translation products corresponding to all three ORFs in persistently infected cells and showed that the read-through stop in p104 and PrV-2A in p81 are functional and these results were confirmed by translation experiments. The RNA-dependent RNA polymerase domain of the PrV replicase is phylogenetically most closely related to members of the families and rather than to members of the family . The unique genome organization, translational control systems and phylogenetic relationship with the replicases of (+ve) plant viruses lead us to propose that PrV represents a novel family of small insect RNA viruses, distinct from current members of the family .

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.023796-0
2010-11-01
2024-12-02
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/11/2826.html?itemId=/content/journal/jgv/10.1099/vir.0.023796-0&mimeType=html&fmt=ahah

References

  1. Agrawal, D. K. & Johnson, J. E.(1992). Sequence and analysis of the capsid protein of Nudaurelia capensis omega virus, an insect virus with T=4 icosahedral symmetry. Virology 190, 806–814.[CrossRef] [Google Scholar]
  2. Albariño, C. G., Price, B. D., Eckerle, L. D. & Ball, L. A.(2001). Characterization and template properties of RNA dimers generated during flock house virus RNA replication. Virology 289, 269–282.[CrossRef] [Google Scholar]
  3. Bawden, A. L., Gordon, K. H. J. & Hanzlik, T. N.(1999). The specificity of Helicoverpa armigera stunt virus infectivity. J Invertebr Pathol 74, 156–163.[CrossRef] [Google Scholar]
  4. Brooks, E. M., Gordon, K. H. J., Dorrian, S. J., Hines, E. R. & Hanzlik, T. N.(2002). Infection of its lepidopteran host by the Helicoverpa armigera stunt virus (Tetraviridae). J Invertebr Pathol 80, 97–111.[CrossRef] [Google Scholar]
  5. Cavener, D. R.(1987). Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res 15, 1353–1361.[CrossRef] [Google Scholar]
  6. Cavener, D. R. & Ray, S. C.(1991). Eukaryotic start and stop translation sites. Nucleic Acids Res 19, 3185–3192.[CrossRef] [Google Scholar]
  7. Christian, P. D., Dorian, S. J., Gordon, K. H. J. & Hanzlik, T. N.(2001). Pathology and properties of the tetravirus Helicoverpa armigera stunt virus. Biol Control 20, 65–75.[CrossRef] [Google Scholar]
  8. Du Plessis, L., Hendry, D. A., Dorrington, R. A., Hanzlik, T. N., Johnson, J. E. & Appel, M.(2005). Revised RNA2 sequence of the tetravirus, Nudaurelia capensisω virus (NωV). Arch Virol 150, 2397–2402.[CrossRef] [Google Scholar]
  9. Gorbalenya, A. E., Pringle, F. M., Zeddam, Z.-L., Luck, B. T., Cameron, C. E., Kalmakoff, J., Hanzlik, T. N., Gordon, K. H. & Ward, V. K.(2002). The palm subdomain-based active site is internally permuted in viral RNA-dependent RNA polymerases of an ancient lineage. J Mol Biol 324, 47–62.[CrossRef] [Google Scholar]
  10. Gordon, K. H. J. & Hanzlik, T. N.(1998). The Tetraviridae. In The Insect Viruses, pp. 269–299. Edited by Miller, L. K. & Ball, L. A.. New York. : Plenum. [Google Scholar]
  11. Gordon, K. H. J., Johnson, K. N. & Hanzlik, T. N.(1995). The larger genomic RNA of Helicoverpa armigera stunt virus encodes the viral RNA polymerase and has a novel 3′-terminal tRNA-like structure. Virology 208, 84–98.[CrossRef] [Google Scholar]
  12. Gordon, K. H. J., Williams, M. R., Hendry, D. A. & Hanzlik, T. N.(1999). Sequence of the genomic RNA of Nudaurelia capensis β virus (Tetraviridae) defines a novel genome organization. Virology 258, 42–53.[CrossRef] [Google Scholar]
  13. Hanzlik, T. N., Dorrian, S. J., Johnson, K. N., Brooks, E. M. & Gordon, K. H. J.(1995). Sequence of RNA 2 of the Helicoverpa armigera stunt virus (Tetraviridae) and bacterial expression of its genes. J Gen Virol 76, 799–811.[CrossRef] [Google Scholar]
  14. Hanzlik, T. N., Gordon, K. H. J., Gorbalenya, A. E., Hendry, D. A., Pringle, F. M., Ward, V. K. & Zeddam, J.-L.(2005). Family Tetraviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 877–883. Edited by Hanzlik, C. M., Mayo, M. A., Maniloff, J., Desselberger, U. & Ball, L. A.. San Diego, London. : Elsevier Academic Press. [Google Scholar]
  15. Harrell, L., Melcher, U. & Atkins, F. J.(2002). Predominance of six different hexanucleotide recoding signals 3′ of read-through stop codons. Nucleic Acids Res 30, 2011–2017.[CrossRef] [Google Scholar]
  16. Helgstrand, C., Munshi, S., Johnson, J. E. & Liljas, L.(2004). The refined structure of Nudaurelia capensisω virus reveals control elements for a T=4 capsid maturation. Virology 318, 192–203.[CrossRef] [Google Scholar]
  17. Kamer, G. & Argos, P.(1984). Primary structural comparison of RNA dependent polymerases from plant, animal and bacterial virus. Nucleic Acids Res 12, 7269–7282.[CrossRef] [Google Scholar]
  18. Kariuki, C. W., McIntosh, A. H. & Goodman, C. L.(2000).In vitro host range studies with a new baculovirus isolate from the diamondback moth Plutella xylostella (L.) (Plutellidae: Lepidoptera). In Vitro Cell Dev Biol Anim 36, 271–276.[CrossRef] [Google Scholar]
  19. King, L. A. & Moore, N. F.(1984). The RNAs of two viruses of the Nudaurelia β family share little homology and have no terminal poly(A) tracts. FEMS Microbiol Lett 26, 41–43. [Google Scholar]
  20. Koonin, E. V.(1991). The phylogeny of RNA-dependent RNA polymerases of positive strand RNA viruses. J Gen Virol 72, 2197–2206.[CrossRef] [Google Scholar]
  21. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & other authors(2007).clustalw and clustal_x version 2.0. Bioinformatics 23, 2947–2948.[CrossRef] [Google Scholar]
  22. Luke, G. A., de Felipe, P., Lukashev, A., Kallioinen, S. E., Bruno, E. A. & Ryan, M. D.(2008). Occurrence, function and evolutionary origins of ‘2A-like’ sequences in virus genomes. J Gen Virol 89, 1036–1042.[CrossRef] [Google Scholar]
  23. Moore, N. F.(1991). The Nudaurelia β family of insect viruses. In Viruses of Invertebrates, pp. 277–285. Edited by Kursak, E.. New York. : Marcel Dekker. [Google Scholar]
  24. Moore, N. F., Reavy, B. & King, L. A.(1985). General characteristics, gene organization and expression of small RNA viruses of insects. J Gen Virol 66, 647–659.[CrossRef] [Google Scholar]
  25. Munshi, S., Liljas, L., Cavarelli, J., Bomu, W., McKinney, B., Reddy, V. & Johnson, J. E.(1996). The 2.8 Å structure of a T=4 animal virus and its implications for membrane translocation of RNA. J Mol Biol 261, 1–10.[CrossRef] [Google Scholar]
  26. Olson, N. H., Baker, T. S., Johnson, J. E. & Hendry, D. A.(1990). The three-dimensional structure of frozen-hydrated Nudaurelia capensis β virus, a T=4 insect virus. J Struct Biol 105, 111–122.[CrossRef] [Google Scholar]
  27. Page, R. D. M.(1996). TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357–358. [Google Scholar]
  28. Poch, O., Sauvaget, I., Delarue, M. & Tordo, N.(1989). Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8, 3867–3874. [Google Scholar]
  29. Pringle, F. M., Gordon, K. H. J., Hanzlik, T. N., Kalmakoff, J., Scottii, P. D. & Ward, V.(1999). A novel capsid expression strategy for Thosea asigna virus (Tetraviridae). J Gen Virol 80, 1855–1863. [Google Scholar]
  30. Pringle, F. M., Kalmakoff, J. & Ward, V. K.(2001). Analysis of the capsid processing strategy of Thosea asigna virus using baculovirus expression of virus-like particles. J Gen Virol 82, 259–266. [Google Scholar]
  31. Pringle, F. M., Johnson, K. N., Goodman, C. L., McIntosh, A. H. & Ball, L. A.(2003). Providence virus: a new member of the Tetraviridae that infects cultured insect cells. Virology 306, 359–370.[CrossRef] [Google Scholar]
  32. Skuzeski, J. M., Nichols, L. M., Gesteland, R. F. & Atkins, J. F.(1991). The signal for a leaky UAG stop codon in several plant viruses includes the two downstream codons. J Mol Biol 218, 365–373.[CrossRef] [Google Scholar]
  33. Speir, J. A., Taylor, D. J., Natarajana, P., Pringle, F. M., Ball, L. A. & Johnson, J. E.(2010). Evolution in action: N and C termini of subunits in related T=4 viruses exchange roles as molecular switches. Structure 18, 700–709.[CrossRef] [Google Scholar]
  34. Thompson, J. D., Higgins, D. G. & Gibson, T. J.(1994).clustalw: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef] [Google Scholar]
  35. van der Heijden, M. W. & Bol, J. F.(2002). Composition of alphavirus-like replication complexes: involvement of virus and host encoded proteins. Arch Virol 147, 875–898.[CrossRef] [Google Scholar]
  36. Yi, F., Zhang, J., Yu, H., Liu, C., Wang, J. & Hu, Y.(2005). Isolation and identification of a new tetravirus from Dendrolimus punctatus larvae collected from Yunnan province, China. J Gen Virol 86, 789–796.[CrossRef] [Google Scholar]
  37. Zeddam, J.-L., Gordon, K. H. J., Lauber, C., Felipe Alves, C. A., Luke, B. T., Hanzlik, T. N., Ward, V. K. & Gorbalenya, A. E.(2010).Euprosterna elaeasa virus genome sequence and evolution of the Tetraviridae family: emergence of bipartite genomes and conservation of the VPg signal with the dsRNA Birnaviridae family. Virology 397, 145–154.[CrossRef] [Google Scholar]
/content/journal/jgv/10.1099/vir.0.023796-0
Loading
/content/journal/jgv/10.1099/vir.0.023796-0
Loading

Data & Media loading...

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