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.
Similar content being viewed by others
References
D. Baulcombe, RNA silencing in plants. Nature 431, 356–363 (2004)
A.J. Hamilton, D.C. Baulcombe, A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952 (1999)
D. Silhavy, J. Burgyan, Effects and side effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci. 9, 76–83 (2004)
O. Voinnet, Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 6, 206–220 (2005)
V.V. Dolja, J.F. Kreuze, J.P.T. Valkonen, Comparative and functional genomics of closteroviruses. Virus Res. 117, 38–51 (2006)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
O. Voinnet, D.C. Baulcombe, Systemic signalling in gene silencing. Nature 389, 553 (1997)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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
Corresponding author
Additional information
Edited by Seung-Kook Choi.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-015-1244-3