Skip to main content

Advertisement

Log in

Identification of two RNA silencing suppressors from banana bunchy top virus

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

In order to suppress RNA silencing, many plant and some animal viruses encode RNA silencing suppressors to achieve infection. In this study, we report that B3 and B4, encoded by DNA3 and DNA4 of banana bunchy top virus (BBTV), exhibit RNA silencing suppression activity. B3 and B4 were able to increase the transient expression of green fluorescent protein (GFP) and dramatically enhanced the pathogenicity of potato virus X (PVX) in Nicotiana benthamiana. B4 was able to reverse established gene silencing on an inoculated leaf or on an upper leaf. B3, however, was only active during infection of an inoculated leaf. Furthermore, B4, but not B3, was able to enhance GFP expression in the transgenic N. benthamiana line 16c. In conclusion, B3 and B4 are the RNA silencing suppressors of BBTV, and they may act at different steps in the RNA silencing pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Anandalakshmi RG, Pruss J, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci USA 95:13079–13084

    Article  CAS  PubMed  Google Scholar 

  2. Andersson MG, Joost HPC, Xu N, Berenjian S, Berkhout B, Akusjarvi G (2005) Suppression of RNA interference by adenovirus virus-associated RNA. J Virol 79:9556–9565

    Article  CAS  PubMed  Google Scholar 

  3. Baulcombe DC (2004) RNA silencing in plants. Nature 431:356–363

    Article  CAS  PubMed  Google Scholar 

  4. Beetham PR, Hafner GJ, Harding RM, Dale JL (1997) Two mRNAs are transcribed from banana bunchy top virus DNA-1. J Gen Virol 78:229–236

    CAS  PubMed  Google Scholar 

  5. Beetham PR, Harding RM, Dale JL (1999) Banana bunchy top virus DNA2 to 6 are monocistronic. Arch Virol 144:89–105

    Article  CAS  PubMed  Google Scholar 

  6. Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW, Baulcombe DC (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17:6739–6746

    Article  CAS  PubMed  Google Scholar 

  7. Bucher HH, Haan P, Goldbach R, Prins M (2004) The influenza A virus NS1 protein binds small interfering RNAs and suppresses RNA silencing in plants Etienne. J Gen Virol 85:983–991

    Article  CAS  PubMed  Google Scholar 

  8. Cao XS, Peng Z, Zhang XM, Zhu SF, Zhong XH, Xiao Q, Ding B, Li Y (2005) Identification of an RNA silencing suppressor from a plant Double-Stranded RNA virus. J Virol 79:13018–13027

    Article  CAS  PubMed  Google Scholar 

  9. Chapman EJ, Prokhnevsky AI, Gopinath K, Dolja VV, Carrington JC (2004) Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev 18:1179–1186

    Article  CAS  PubMed  Google Scholar 

  10. Chen J, Wan XL, Xie DX, Peng JR, Ding SW (2004) Viral virulence protein suppresses RNA silencing–mediated defense but upregulates the role of microRNA in host gene expression. Plant Cell 16:1302–1313

    Article  CAS  PubMed  Google Scholar 

  11. Cui XF, Li GX, Wang DW, Hu DW, Zhou XP (2005) A Begomovirus DNA-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79:10764–10775

    Article  CAS  PubMed  Google Scholar 

  12. Delgadillo MO, Pilar S, Beatriz S, Juan AG, Carmen SM (2004) Human influenza virus NS1 protein enhances viral pathogenicity and acts as an RNA silencing suppressor in plants. J Gen Virol 85:993–999

    Article  CAS  PubMed  Google Scholar 

  13. Dong XL, Wezel RV, Stanley J, Hong YG (2003) Functional characterization of the nuclear localization signal for a suppressor of posttranscriptional gene silencing. J Virol 77:7026–7033

    Article  CAS  PubMed  Google Scholar 

  14. Feng Q, Morris TJ (2005) Suppressors of RNA silencing encoded by plant viruses and their role in viral infections. FEBS Lett 579:5958–5964

    Article  Google Scholar 

  15. Feng Q, Tao R, Morris TJ (2003) The coat protein of Turnip Crinkle Virus suppresses posttranscriptional gene silencing at an early initiation step. J Virol 77:511–522

    Article  Google Scholar 

  16. Geley S, Muller C (2004) RNAi: ancient mechanism with a promising future. Exp Gerontol 39:985–998

    Article  CAS  PubMed  Google Scholar 

  17. Guo HS, Ding SW (2002) A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J 21:398–407

    Article  CAS  PubMed  Google Scholar 

  18. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952

    Article  CAS  PubMed  Google Scholar 

  19. Hamilton A, Voinnet O, Chappell L, Baulcombe DC (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21:4671–4679

    Article  CAS  PubMed  Google Scholar 

  20. Hannon GJ (2002) RNA interference. Nature 418:244–251

    Article  CAS  PubMed  Google Scholar 

  21. Horser CL, Karan M, Harding RM, Dale JL (2001) Additional re-encoding DNAs associated with banana bunchy top virus. Arch Virol 146:71–86

    Article  CAS  PubMed  Google Scholar 

  22. Horser CL, Harding RM, Dale JL (2001) Banana bunchy top nanovirus DNA-1 encodes the ‘master’ replication initiation protein. J Gen Virol 82:459–464

    CAS  PubMed  Google Scholar 

  23. Kasschau KD, Xie ZX, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217

    Article  CAS  PubMed  Google Scholar 

  24. Li HW, Li WX, Ding SW (2002) Induction and suppression of RNA silencing by an animal virus. Science 296:1319–1321

    Article  CAS  PubMed  Google Scholar 

  25. Llave C, Kasschau KD, Carrington JC (2000) Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proc Natl Acad Sci USA 97:13401–13406

    Article  CAS  PubMed  Google Scholar 

  26. Lu R, Folimonov A, Shintaku M, Li WX, Falk BW, Dawson WO, Ding SW (2004) Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc Natl Acad Sci USA 101:15742–15747

    Article  CAS  PubMed  Google Scholar 

  27. Mallory AC, Ely L, Smith TH, Marathe R, Anandalakshmi R, Fagard M, Vaucheret H, Pruss G, Bowman L, Vance VB (2001) HC-Pro suppression of transgene silencing eliminates the small RNAs but not transgene methylation or the mobile signal. Plant Cell 13:571–583

    Article  CAS  PubMed  Google Scholar 

  28. Meng CY, Chen J, Ding SW, Peng JR, Wong SM (2008) Hibiscus chlorotic ringspot virus coat protein inhibits trans-acting small interfering RNA biogenesis in Arabidopsis. J Gen Virol 89:2349–2358

    Article  CAS  PubMed  Google Scholar 

  29. Mlotshwa S, Voinnet O, Mette MF, Matzke M, Vaucheret H, Ding SW, Pruss G, Vance VB (2002) RNA silencing and the mobile silencing signal. Plant Cell 14(Suppl):S289–S301

    Google Scholar 

  30. Moissiard G, Voinnet O (2004) Viral suppression of RNA silencing in plants. Mol Plant Path 5:71–82

    Article  CAS  Google Scholar 

  31. Palauqui JC, Elmayan T, Pollien JM, Vaucheret H (1997) Systemic acquired silencing: transgene-specific posttranscriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16:4738–4745

    Article  CAS  PubMed  Google Scholar 

  32. Pruss G, Ge X, Shi XM, Carrington JC, Vance VB (1997) Synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9:859–868

    Article  CAS  PubMed  Google Scholar 

  33. Qi YJ, Zhong XH, Itaya A, Ding B (2004) Dissecting RNA silencing in protoplasts uncovers novel effects of viral suppressors on the silencing pathway at the cellular level. Nucleic Acids Res. 32:e179

  34. Ramachandran V, Chellappan P, Pita JS, Fauquet CM (2004) Differential roles of AC2 and AC4 of Cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J Virol 78:9487–9498

    Article  Google Scholar 

  35. Roth BM, Pruss GJ, Vance VB (2004) Plant viral suppressors of RNA silencing. Virus Res 102:97–108

    Article  CAS  PubMed  Google Scholar 

  36. Schwarz DS, Hutvagner G, Haley B, Zamore PD (2002) Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol Cell 10:37–548

    Article  Google Scholar 

  37. Silhavy D, Burgyan J (2004) Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci 9:1360–1385

    Article  Google Scholar 

  38. Silhavy D, Molnar A, Lucioli A, Szittya G, Hornyik C, Tavazza M, Burgyan J (2002) A viral protein suppresses RNA silencing and binds silencing- generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21:3070–3080

    Article  CAS  PubMed  Google Scholar 

  39. Takeda A, Tsukuda M, Mizumoto H, Okamoto K, Kaido M, Mise K, Okuno T (2005) A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J 24:1–11

    Google Scholar 

  40. Teresa RM, Voinnet O, Baulcombe DC (1998) Initiation and maintenance of virus-induced gene silencing. Plant Cell 10:37–946

    Google Scholar 

  41. Tian E, Zhuang J, Liu ZX (2005) Cloning and sequencing of DNA components of Banana bunchy top virus Hainan isolate. Chin J Agric Biotech 2:91–97

    Google Scholar 

  42. Vance V, Vaucheret H (2001) RNA silencing in plants–defense and counterdefense. Science 292:2277–2280

    Article  CAS  PubMed  Google Scholar 

  43. Vastenhouw NL, Plasterk RH (2004) RNAi protects the Caenorhabditis elegans germline against transposition. Trends Genet 20:314–319

    Article  CAS  PubMed  Google Scholar 

  44. Vogler H, Kwon MO, Dang V, Sambade A, Fasler M, Ashby J, Heinlein M (2008) Tobacco mosaic virus movement protein enhances the spread of RNA silencing. PLoS Pathogens 4:e1000038.1–e1000038.12.

    Google Scholar 

  45. Voinnet O (2002) RNA silencing: small RNAs as ubiquitous regulators of gene expression. Curr Opin Plant Biol 5:444–451

    Article  CAS  PubMed  Google Scholar 

  46. Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nature 6:206–220

    CAS  Google Scholar 

  47. Voinnet O, Baulcombe DC (1997) Systemic signalling in gene silencing. Nature 389:553

    Article  CAS  PubMed  Google Scholar 

  48. Voinnet O, Vain P, Angell S, Baulcombe DC (1998) Systemic spread of sequence-specific transgene RNA degradation is initiated by localized introduction of ectopic promoterless DNA. Cell 95:177–187

    Article  CAS  PubMed  Google Scholar 

  49. Voinnet O, Pinto YM, Baulcombe DC (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses. Proc Natl Acad Sci USA 96:14147–14152

    Article  CAS  PubMed  Google Scholar 

  50. Voinnet O, Lederer C, Baulcombe DC (2000) A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103:157–167

    Article  CAS  PubMed  Google Scholar 

  51. Voinnet O, Rivas S, Mestre P, Baulcombe DC (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949–956

    Article  CAS  PubMed  Google Scholar 

  52. Wang MB, Metzlaff M (2005) RNA silencing and antiviral defense in plants. Curr Opin Plant Biol 8:216–222

    Article  PubMed  Google Scholar 

  53. Wanitchakorn NR, Harding RM, Dale JL (1997) Banana bunchy top virus DNA-3 encodes the viral coat protein. Arch Virol 142:1673–1680

    Article  CAS  PubMed  Google Scholar 

  54. Wanitchakorn NR, Hafner GJ, Harding RM, Dale JL (2000) Functional analysis of proteins encoded by banana bunchy top virus DNA4–6. J Gen Virol 81:299–306

    CAS  PubMed  Google Scholar 

  55. The 8th ICTV report. http://phene.cpmc.columbia.edu/Ictv/fs_nanov.htm

  56. Zhang LD, Wang ZH, Wang XB, Li DW, Han CG, Yu JL (2005) Two virus-encoded RNA silencing suppressors, P14 of Beet necrotic yellow vein virus and S6 of Rice black streak dwarf virus. Chin Sci Bull 50:305–310

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Professor Andrew O. Jackson (Department of Plant & Microbial Biology, University of California, Berkeley) for his helpful suggestions and constructive criticisms. This work was supported by grant KL200505 from State Key Laboratory Opening Foundation of China and by grant 80670 from Natural Science Foundation of Hainan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhixin Liu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Niu, S., Wang, B., Guo, X. et al. Identification of two RNA silencing suppressors from banana bunchy top virus. Arch Virol 154, 1775–1783 (2009). https://doi.org/10.1007/s00705-009-0515-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-009-0515-5

Keywords

Navigation