Skip to main content

Genetic diversity and silencing suppression activity of the p22 protein of Tomato chlorosis virus isolates from tomato and sweet pepper

Virus Genes volume 51, pages 283–289 (2015)Cite this article

Abstract

As for other bipartite criniviruses (genus Crinivirus, family Closteroviridae), the genome of Tomato chlorosis virus encodes an RNA silencing suppressor, the protein p22, in the 3′-proximal region of RNA1. This protein has been reported as having one of the longest lasting local suppressor activities when transiently expressed in Nicotiana benthamiana. Here, we examined the genetic diversity of the p22 gene in ToCV isolates from tomato and sweet pepper. The p22 gene sequences clearly grouped into two separated clades. However, functional analysis of both types of p22 proteins indicated no evident differences in suppressor activity. Our findings provide experimental evidence that the presence of a “strong” silencing suppressor is a conserved feature of ToCV isolates.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3

References

  1. D. Baulcombe, RNA silencing in plants. Nature 431, 356–363 (2004)

    CAS  Article  PubMed  Google Scholar 

  2. A.J. Hamilton, D.C. Baulcombe, A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952 (1999)

    CAS  Article  PubMed  Google Scholar 

  3. D. Silhavy, J. Burgyan, Effects and side effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci. 9, 76–83 (2004)

    CAS  Article  PubMed  Google Scholar 

  4. O. Voinnet, Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 6, 206–220 (2005)

    CAS  Article  PubMed  Google Scholar 

  5. V.V. Dolja, J.F. Kreuze, J.P.T. Valkonen, Comparative and functional genomics of closteroviruses. Virus Res. 117, 38–51 (2006)

    CAS  Article  PubMed  Google Scholar 

  6. S.W. Ding, B.J. Shi, W.X. Li, R.H. Symons, An interspecies hybrid RNA virus is significantly more virulent than either parental virus. Proc. Natl. Acad. Sci. USA 93, 7470–7474 (1996)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  7. G. Pruss, X. Ge, X.M. Shi, J.C. Carrington, V.B. Vance, Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9, 859–868 (1997)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  8. J.C. Reed, K.D. Kasschau, A.I. Prokhnevsky, K. Gopinath, G.P. Pogue, J.C. Carrington, V.V. Dolja, Suppressor of RNA silencing encoded by Beet yellows virus. Virology 306, 203–209 (2003)

    CAS  Article  PubMed  Google Scholar 

  9. R. Lu, A.S. Folimonov, M. Shintaku, W.X. Li, B.W. Falk, W.O. Dawson, S.W. Ding, Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. USA 101, 15742–15747 (2004)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  10. J.F. Kreuze, E.I. Savenkov, M. Cuellar, X. Li, J.P.T. Valkonen, Viral class 1 RNase III involved in suppression of RNA silencing. J. Virol. 79, 7227–7238 (2005)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  11. M. Chiba, J.C. Reed, A.I. Prokhnevsky, E.J. Chapman, M. Mawassi, E.V. Koonin, J.C. Carrington, V.V. Dolja, Diverse suppressors of RNA silencing enhance agroinfection by a viral replicon. Virology 346, 7–14 (2006)

    CAS  Article  PubMed  Google Scholar 

  12. M.C. Cañizares, J. Navas-Castillo, E. Moriones, Multiple suppressors of RNA silencing encoded by both genomic RNAs of the crinivirus, Tomato chlorosis virus. Virology 379, 168–174 (2008)

    Article  PubMed  Google Scholar 

  13. P. Gouveia, S. Dandlen, A. Costa, N. Marques, G. Nolasco, Identification of an RNA silencing suppressor encoded by Grapevine leafroll-associated virus 3. Eur. J. Plant Pathol. 133, 237–245 (2012)

    CAS  Article  Google Scholar 

  14. J.A. Díaz-Pendón, S.W. Ding, Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. Ann. Rev. Phytopahol. 46, 303–326 (2008)

    Article  Google Scholar 

  15. J.W. Cuellar, F. Tairo, J.F. Kreuze, J.P.T. Valkonen, Analysis of gene content in Sweet potato chlorotic stunt virus RNA1 reveals the presence of the p22 RNA silencing suppressor in only a few isolates: implications for viral evolution and synergism. J. Gen. Virol. 89, 573–582 (2008)

    CAS  Article  PubMed  Google Scholar 

  16. A.K. Tugume, R. Amayo, I. Weinheimer, S.B. Mukasa, P.R. Rubaihayo, J.P.T. Valkonen, Genetic variability and evolutionary implications of RNA silencing suppressor genes in RNA1 of Sweet potato chlorotic stunt virus isolates infecting sweetpotato and related wild species. PLoS ONE 8, 11 (2013)

    Article  Google Scholar 

  17. G.C. Wisler, R.H. Li, H.-Y. Liu, D.S. Lowry, J.E. Duffus, Tomato chlorosis virus: a new whitefly-transmitted, phloem-limited bipartite closterovirus of tomato. Phytopathology 88, 402–409 (1998)

    CAS  Article  PubMed  Google Scholar 

  18. G. Lozano, E. Moriones, J. Navas-Castillo, Complete sequence of the RNA1 of a European isolate of Tomato chlorosis virus. Arch. Virol. 152, 839–841 (2007)

    CAS  Article  PubMed  Google Scholar 

  19. G. Lozano, E. Moriones, J. Navas-Castillo, First report of sweet pepper (Capsicum annuum) as a natural host plant for Tomato chlorosis virus. Plant Dis. 88, 224 (2003)

    Article  Google Scholar 

  20. I.M. Fortes, E. Moriones, J. Navas-Castillo, Tomato chlorosis virus in pepper: prevalence in commercial crops in south-eastern Spain and symptomatology under experimental conditions. Plant. Pathol. 61, 994–1001 (2012)

    Article  Google Scholar 

  21. J. Wang, A.M. Sharma, S. Duffy, R.P. Almeida, Genetic diversity in the 3′terminal 4.7 kb region of Grapevine leafroll-associated virus 3. Phytopathology 101, 445–450 (2011)

    Article  PubMed  Google Scholar 

  22. O. Voinnet, D.C. Baulcombe, Systemic signalling in gene silencing. Nature 389, 553 (1997)

    CAS  Article  PubMed  Google Scholar 

  23. E.H. Bayne, D.V. Rakitina, S.Y. Morozov, D.C. Baulcombe, Cell-to-cell movement of potato potexvirus X is dependent on suppression of RNA silencing. Plant J. 44, 471–482 (2005)

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  25. E. Noris, G.P. Accotto, R. Tavazza, A. Brunetti, S. Crespi, M. Tavazza, Resistance to tomato yellow leaf curl geminivirus in Nicotiana benthamiana plants transformed with a truncated viral C1 gene. Virology 224, 130–138 (1996)

    CAS  Article  PubMed  Google Scholar 

  26. M.C. Cañizares, K.M. Taylor, G.P. Lomonossoff, Surface-exposed C-terminal amino acids of the small coat protein of Cowpea mosaic virus are required for suppression of silencing. J. Gen. Virol. 85, 3431–3435 (2004)

    Article  PubMed  Google Scholar 

  27. I.D. Thompson, T.J. Gibson, F. Plewniak, F. Jeanmougin, D.G. Higgins, The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882 (1997)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  28. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, S. Kumar, MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  29. K. Ye, D.J. Patel, RNA silencing suppressor p21 of Beet yellows virus forms an RNA binding octameric ring structure. Structure 13, 1375–1384 (2005)

    CAS  Article  PubMed  Google Scholar 

  30. A. Lingel, B. Simon, E. Izaurralde, M. Sattler, The structure of the Flock house virus B2 protein, a viral suppressor of RNA interference, shows a novel mode of double-stranded RNA recognition. EMBO Rep. 6, 1149–1155 (2005)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  31. G. Lozano, A. Grande-Pérez, J. Navas-Castillo, Populations of genomic RNAs devoted to the replication or spread of a bipartite plant virus differ in genetic structure. J. Virol. 83, 12973–12983 (2009)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  32. A.F. Orílio, I.M. Fortes, J. Navas-Castillo, Infectious cDNA clones of the crinivirus Tomato chlorosis virus are competent for systemic plant infection and whitefly-transmission. Virology 464–465, 365–374 (2014)

    Article  PubMed  Google Scholar 

  33. H.Y. Chen, J. Yang, C. Lin, Y.A. Yuan, Structural basis for RNA silencing suppression of Tomato aspermy virus protein 2b. EMBO J. 9, 754–760 (2008)

    CAS  Article  Google Scholar 

  34. C. Torres-Barceló, S. Martín, J.A. Darós, S.F. Elena, From Hypo-to Hypersuppression: effect of amino acid substitutions on the RNA silencing suppressor activity of the Tobacco etch potyvirys HC-Pro. Genetics 180, 1039–1049 (2008)

    PubMed Central  Article  PubMed  Google Scholar 

  35. M.L. Yambao, H. Yagihashi, H. Sekiguchi, T. Sekiguchi, T. Sasaki, M. Sato, G. Atsumi, Y. Tacahashi, K.S. Nakahara, I. Uyeda, Point mutations in helper component protease of Clover yellow vein virus are associated with the attenuation of RNA-silencing suppression activity and symptom expression in broad bean. Arch. Virol. 153, 105–115 (2008)

    CAS  Article  PubMed  Google Scholar 

  36. J. Ye, J. Qu, J.F. Zhang, Y.F. Geng, R.X. Fang, A critical domain of the cucumber mosaic virus 2b protein for RNA silencing suppressor activity. FEBS Lett. 583, 101–106 (2009)

    CAS  Article  PubMed  Google Scholar 

  37. P. Gouveia, G. Nolasco, The p19.7 RNA silencing suppressor from Grapevine leafroll-associated virus 3 shows different levels of activity across phylogenetic groups. Virus Genes 45, 333–339 (2012)

    CAS  Article  PubMed  Google Scholar 

  38. A.R.M. Kataya, M.N.S. Suliman, K. Kalantidis, I.C. Livieratos, Cucurbit yellow stunting disorder virus p25 is a suppressor of post-transcriptional gene silencing. Virus Res. 145, 48–53 (2009)

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

Y. L.-R. was the recipient of an AECID (Spain) fellowship. M.C.C. was the recipient of an I3P contract from the CSIC (Spain) co-financed by FSE. This work was supported by Grants AGL2013-48913-C2-1-R from the Ministerio de Economía y Competitividad, Spain, and P10-AGR-6516 from Consejería de Economía, Innovación y Ciencia (CEIC), Junta de Andalucía, Spain, co-financed by FEDER-FSE. J.N.C. and E.M.A. are members of the Research Group AGR-214, partially funded by the Consejería de Economía, Innovación y Ciencia, Junta de Andalucía, Spain. We thank F. Aparicio and I.M. Fortes for providing materials and M.V. Martín and R. Tovar for technical assistance.

Author information

Authors and Affiliations

  1. Instituto de Hortofruticultura Subtropical y Mediterránea “La Mayora”- Universidad de Málaga - Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Estación Experimental “La Mayora”, Algarrobo-Costa, 29750, Málaga, Spain

    Yazmín M. Landeo-Ríos, Jesús Navas-Castillo, Enrique Moriones & M. Carmen Cañizares

Authors
  1. Yazmín M. Landeo-Ríos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jesús Navas-Castillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enrique Moriones
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Carmen Cañizares
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Carmen Cañizares.

Additional information

Edited by Seung-Kook Choi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (RTF 285 kb)

Supplementary material 2 (DOCX 26 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Landeo-Ríos, Y.M., Navas-Castillo, J., Moriones, E. et al. Genetic diversity and silencing suppression activity of the p22 protein of Tomato chlorosis virus isolates from tomato and sweet pepper. Virus Genes 51, 283–289 (2015). https://doi.org/10.1007/s11262-015-1244-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-015-1244-3

Keywords

  • Crinivirus
  • Closteroviridae
  • Plant viral suppressor