Key importance of small RNA binding for the activity of a Glycine-Tryptophan (GW) motif-containing viral suppressor of RNA silencing

Journal of Biological Chemistry

Volumn 290, Issue 5, 2015, Pages 3106-3120

  Pérez Cañamás, Miryam ^a   Hernández, Carmen ^a  

^a UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; PROTEINS; RNA; VIRUSES;

BINDING CAPABILITY; CONCOMITANT EFFECTS; EFFICIENT INTERACTION; NUCLEOLAR LOCALIZATION; PARTICLE ASSEMBLIES; RELATIVE CONTRIBUTION; SITE DIRECTED MUTAGENESIS; VIRAL INFECTIONS;

NUCLEIC ACIDS;

ARGONAUTE PROTEIN; GLYCINE; PROTEIN P37; TRYPTOPHAN; SMALL INTERFERING RNA;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE SILENCING; GENE TARGETING; GLYCINE TRYPTOPHAN MOTIF; MOLECULAR INTERACTION; NONHUMAN; PELARGONIUM; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA BINDING; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; VIRAL SUPPRESSOR OF RNA SILENCING; CHEMISTRY; FLUORESCENCE MICROSCOPY; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; PLANT VIRUS; RNA INTERFERENCE;

PELARGONIUM LINE PATTERN VIRUS; TOMBUSVIRIDAE; TURNIP CRINKLE VIRUS;

ARGONAUTE PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GLYCINE; MICROSCOPY, FLUORESCENCE; PLANT VIRUSES; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRYPTOPHAN;

EID: 84921903560     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.593707     Document Type: Article

References (94)

1. Baulcombe, D. (2005) RNA silencing. Trends Biochem. Sci. 30, 290-293
2. Pickford A. S., and Cogoni C. (2003) RNA-mediated gene silencing. Cell Mol. Life Sci. 60, 871-882
3. Bivalkar-Mehla, S., Vakharia, J., Mehla, R., Abreha, M., Kanwar, J. R., Tikoo, A., Chauhan, A. (2011) Viral RNA silencing suppressors (RSS): novel strategy of viruses to ablate the host RNA interference (RNAi) defense system. Virus Res. 155, 1-9
4. Ding, S. W., and Voinnet, O. (2007) Antiviral immunity directed by small RNAs. Cell 130, 413-426
5. Lu, R., Maduro, M., Li, F., Li, H. W., Broitman-Maduro, G., Li, W. X., and Ding, S. W. (2005) Animal virus replication and RNAi mediated antiviral silencing in Caenorhabditis elegans. Nature 436, 1040-1043
6. Segers, G. C., Zhang, X., Deng, F., Sun, Q., Nuss, D. L. (2007) Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc. Natl. Acad. Sci. U.S.A. 104, 12902-12906
7. Wang, X. H., Aliyari, R., Li, W. X., Li, H. W., Kim, K., Carthew, R., Atkinson, P., and Ding, S. W. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312, 452-454
8. Wu, Q., Wang, X., and Ding, S. W. (2010) Viral suppressors of RNA-based viral immunity: host targets. Cell Host Microbe 8, 12-15
9. Ding, S. W. (2010) RNA based antiviral immunity. Nat. Rev. Immunol. 10, 632-644
10. Baumberger, N., and Baulcombe, D. C. (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. U.S.A. 102, 11928-11933
11. Qi Y., Denli A. M., and Hannon G. J. (2005) Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19, 421-428
12. Vaucheret, H. (2008) Plant ARGONAUTES. Trends Plant Sci. 13, 350-358
13. Ghildiyal, M., and Zamore, P. D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10, 94-108
14. Lipardi, C., Wei, Q., and Paterson, B. M. (2001) RNAi as random degradative PCR: siRNA primers convert mRNA into dsRNAs that are degraded to generate new siRNAs. Cell 107, 297-307
15. Moissiard, G., Parizotto, E. A., Himber, C., and Voinnet, O. (2007) Transitivity in Arabidopsis can be primed, requires the redundant action of the antiviral Dicer-like 4 and Dicer-like 2, and is compromised by viral-encoded suppressor proteins. RNA 13, 1268-1278
16. Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K. D., Carrington, J. C., and Voinnet, O. (2006) Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313, 68-71
17. García-Ruiz, H, Takeda, A., Chapman, E. J., Sullivan, C. M., Fahlgren, N., Brempelis, K. J., and Carrington, J. C. (2010) Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 22, 481-496
18. Harvey, J. J., Lewsey, M. G., Patel, K., Westwood, J., Heimstädt, S., Carr, J. P., and Baulcombe, D. C. (2011) An antiviral defense role of AGO2 in plants. PLoS One 6, e14639
19. Jaubert, M., Bhattacharjee, S., Mello, A. F., Perry, K. L., and Moffett, P. (2011) ARGONAUTE2 mediates RNA silencing antiviral defenses against Potato virus X in Arabidopsis. Plant Physiol. 156, 1556-1564
20. Qu, F., Ye, X., and Morris, T. J. (2008) Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc. Natl. Acad. Sci. U.S.A. 105, 14732-14737
21. Scholthof, H. B., Alvarado, V. Y., Vega-Arreguin, J. C., Ciomperlik, J., Odokonyero, D., Brosseau, C., Jaubert, M., Zamora, A., and Moffett, P. (2011) Identification of an ARGONAUTE for antiviral RNA silencing in Nicotiana benthamiana. Plant Physiol. 156, 1548-1555
22. Wang, X. B., Jovel, J., Udomporn, P., Wang, Y., Wu, Q., Li, W. X., Gasciolli, V., Vaucheret, H., and Ding, S. W. (2011) The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative Argonautes in Arabidopsis thaliana. Plant Cell 23, 1625-1638
23. Li, F., and Ding, S. W. (2006) Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu. Rev. Microbiol. 60, 503-531
24. Alvarado, V., and Scholthof, H. B. (2009) Plant responses against invasive nucleic acids: RNA silencing and its suppression by plant viral pathogens. Semin. Cell Dev. Biol. 20, 1032-1040
25. Qu, F., and Morris, T. J. (2005) Suppressors of RNA silencing encoded by plant viruses and their role in viral infections. FEBS Lett. 579, 5958-5964
26. Mangwende, T., Wang, M. L., Borth, W., Hu, J., Moore, P. H., Mirkov, T. E., and Albert, H. H. (2009) The P0 gene of sugarcane yellow leaf virus encodes an RNA silencing suppressor with unique activities. Virology 384, 38-50
27. Martínez-Turiño, S., and Hernández, C. (2009) Inhibition of RNA silencing by the coat protein of Pelargonium flower break virus: distinctions from closely related suppressors. J. Gen. Virol. 90, 519-525
28. Senshu, H., Ozeki, J., Komatsu, K., Hashimoto, M., Hatada, K., Aoyama, M., Kagiwada, S., Yamaji Y., and Namba, S. (2009) Variability in the level of RNA silencing suppression caused by triple gene block protein 1 (TGBp1) from various potexviruses during infection. J. Gen. Virol. 90, 1014-1024
29. Cuellar, W. J., Tairo, F., Kreuze, J. F., and Valkonen, J. P. T. (2008) 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
30. Marques, N. T., Costa, A. A., Lopes, D., Silva, G, and Nolasco, G. (2012) Comparing p20's RNA silencing suppressing activity among five phylogenetic groups of Citrus tristeza virus. Eur. J. Plant Pathol. 10.1007/s10658-011-9877-0
31. Burgyán, J., and Havelda, Z. (2011) Viral suppressors of RNA silencing. Trends Plant Sci. 16, 265-272
32. Pumplin, N., and Voinnet, O. (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat. Rev. Microbiol. 11, 745-760
33. Vargason, J. M., Szittya, G., Burgyán, J., and Hall, T. M. (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell 15, 799-811
34. Ye, K., Malinina, L., and Patel, D. J. (2003) Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 426, 874-878
35. Csorba, T., Bovi, A., Dalmay, T., and Burgyán, J. (2007) The p122 subunit of Tobacco mosaic virus replicase is a potent silencing suppressor and compromises both small interfering RNA- and microRNA-mediated pathways. J. Virol. 81, 11768-11780
36. Hemmes, H., Lakatos, L., Goldbach, R., Burgyán, J., and Prins, M. (2007) The NS3 protein of Rice hoja blanca tenuivirus suppresses RNA silencing in plant and insect hosts by efficiently binding both siRNAs and miRNAs. RNA 13, 1079-1089
37. Lakatos, L., Csorba, T., Pantaleo, V., Chapman, E. J., Carrington, J. C., Liu, Y. P., Dolja, V. V., Calvino, L. F., López-Moya, J. J., and Burgyán, J. (2006) Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25, 2768-2780
38. Mérai, Z., Kerényi, Z., Kertész, S., Magna, M., Lakatos, L., and Silhavy, D. (2006) Double-stranded RNA binding may be a general plant RNA viral strategy to suppress RNA silencing. J. Virol. 80, 5747-5756
39. Chao, J. A., Lee, J. H., Chapados, B. R., Debler, E. W., Schneemann, A., and Williamson, J. R. (2005) Dual modes of RNA-silencing suppression by Flock house virus protein B2. Nat. Struct. Mol. Biol. 12, 952-957
40. Mérai, Z., Kerényi, Z., Molnár, A., Barta, E., Válóczi, A., Bisztray, G., Havelda, Z., Burgyán, J., and Silhavy, D. (2005) Aureusvirus P14 is an efficient RNA silencing suppressor that binds double-stranded RNAs without size specificity. J. Virol. 79, 7217-7226
41. Haas, G., Azevedo, J., Moissiard, G., Geldreich, A., Himber, C., Bureau, M., Fukuhara, T., Keller, M., and Voinnet, O. (2008) Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J. 27, 2102-2112
42. Zhang, X., Yuan, Y. R., Pei, Y., Lin, S. S., Tuschl, T., Patel, D. J., and Chua, N. H. (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute 1 cleavage activity to counter plant defense. Genes Dev. 20, 3255-3268
43. Baumberger, N., Tsai, C. H., Lie, M., Havecker, E., and Baulcombe, D. C. (2007) The polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17, 1609-1614
44. Bortolamiol, D., Pazhouhandeh, M., Marrocco, K., Genschik, P., and Ziegler-Graff, V. (2007) The polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 17, 1615-1621
45. Csorba, T., Lózsa, R., Hutvágner, G., and Burgyán, J. (2010) Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. Plant J. 62, 463-472
46. Azevedo, J., Garcia, D., Pontier, D., Ohnesorge, S., Yu, A., Garcia, S., Braun, L., Bergdoll, M., Hakimi, M. A., Lagrange, T., and Voinnet, O. (2010) Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev. 24, 904-915
47. Giner, A., Lakatos, L., García-Chapa, M., López-Moya, J. J., and Burgyán, J. (2010). Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathog. 6, e1000996
48. El-Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., Hakimi, M. A., Jacobsen, S. E., Cooke, R., and Lagrange T. (2007) Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21, 2539-2544
49. Rochon, D., Lommel, S., Martelli, G. P., Rubino, L., and Russo, M. (2012) Family Tombusvirdae. in Ninth Report of the International Committee on Taxonomy of Viruses, pp. 1111-1138, Elsevier Academic Press, San Diego, CA
50. Castaño, A., and Hernández, C. (2005) Complete nucleotide sequence and genome organization of Pelargonium line pattern virus and its relationship with the family Tombusviridae. Arch. Virol. 150, 949-965
51. Castaño, A., Ruiz, L., and Hernández, C. (2009) Insights into the translational regulation of biologically active open reading frames of Pelargonium line pattern virus. Virology 386, 417-426
52. Kinard, G. R., and Jordan, R. (2002) Genome organization of Pelargonium chlorotic ring pattern virus: further implications for Tombusviridae taxonomy. Acta Hortic. 568, 17-27
53. Qu, F., Ren, T., and Morris, T. J. (2003) The coat protein of Turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. J. Virol. 77, 511-522
54. Meng, C., Chen, J., Peng, J., and Wong, S. M. (2006) Host-induced avirulence of Hibiscus chlorotic ringspot virus mutant correlates with reduced gene-silencing suppression activity. J. Gen. Virol. 87, 451-459
55. Voinnet, O., Pinto, Y. M., and Baulcombe, D. C. (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. U.S.A. 96, 14147-14152
56. Takeda, A., Tsukuda, M., Mizumoto, H., Okamoto, K., Kaido, M., Mise, K., and Okuno, T. (2005) A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J. 24, 3147-3157
57. Powers, J. G., Sit, T. L., Heinsohn, C., George, C. G., Kim, K. H., and Lommel, S. A. (2008) The Red clover necrotic mosaic virus RNA-2 encoded movement protein is a second suppressor of RNA silencing. Virology 381, 277-286
58. Castaño, A., and Hernández, C. (2007) Biological activity of transcripts from cDNA of Pelargonium line pattern virus. Acta Virol. 51, 271-274
59. Knoester, M., van Loon, L. C., van den Heuvel, J., Hennig, J., Bol, J. F., and Linthorst, H. J. M. (1998) Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc. Natl. Acad. Sci. U.S.A. 95, 1933-1937
60. Sambrock, J., Fritsch, E. F., and Maniatis, T. (2001) Molecular Cloning: A Laboratory Manual, 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
61. Powers, J. G., Sit, T. L., Qu, F., Morris, T. J., Kim, K. H., and Lommel, S. A. (2008) A versatile assay for the identification of RNA silencing suppressors based on complementation of viral movement. Mol. Plant Microbe Interact. 21, 879-890
62. González, I., Martínez, L., Rakitina, D. V., Lewsey, M. G., Atencio, F. A., Llave, C., Kalinina, N. O., Carr, J. P., Palukaitis, P., and Canto, T. (2010) Cucumber mosaic virus 2b protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. Mol. Plant Microbe Interact. 23, 294-303
63. Kim, S. H., Macfarlane, S., Kalinina, N. O., Rakitina, D. V., Ryabov, E. V., Gillespie, T., Haupt, S., Brown, J. W., and Taliansky, M. (2007) Interaction of a plant virus encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc. Natl. Acad. Sci. U.S.A. 104, 11115-11120
64. Verwoerd, T. C., Dekker, B. M., and Hoekema, A. (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17, 2362
65. Ivars, P., Alonso, M., Borja, M., and Hernández, C. (2004) Development of a non-radioactive dot-blot hybridisation assay for the detection of Pelargonium flower break virus and Pelargonium line pattern virus. Eur. J. Plant Pathol. 10.1023/B:EJPP.0000019798.87567.22
66. Martínez-Turiño, S., and Hernández, C. (2011) A membrane-associated movement protein of Pelargonium flower break virus shows RNA binding activity and contains a biologically relevant leucine zipper-like motif. Virology 413, 310-319
67. Johansen, L. K., and Carrington, J. C. (2001) Silencing on the spot: induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol. 126, 930-938
68. Chen, H. Y., Yang, J., Lin, C., and Yuan, Y. A. (2008) Structural basis for RNA-silencing suppression by Tomato aspermy virus protein 2b. EMBO Rep. 9, 754-760
69. Vaewhongs, A. A., and Lommel S. A. (1995) Virion formation is required for the long-distance movement of Red clover necrotic mosaic virus in movement protein transgenic plants. Virology 212, 607-613
70. Cao, M., Ye, X., Willie, K., Lin, J., Zhang, X., Redinbaugh, M. G., Simon, A. E., Morris, T. J., and Qu, F. (2010) The capsid protein of Turnip crinkle virus overcomes two separate defense barriers to facilitate systemic movement of the virus in Arabidopsis. J. Virol. 84, 7793-7802
71. Valli, A., Dujovny, G., and García, J. A. (2008) Protease activity, self interaction, and small interfering RNA binding of the silencing suppressor P1b from cucumber vein yellowing ipomovirus. J. Virol. 82, 974-986
72. Takeda, A., Sugiyama, K., Nagano, H., Mori, M., Kaido, M., Mise, K., Tsuda, S., and Okuno, T. (2002) Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Lett. 532, 75-79
73. Lucy, A. P., Guo, H. S., Li, W. X., and Ding, S. W. (2000) Suppression of posttranscriptional gene silencing by a plant viral protein localized in the nucleus. EMBO J. 19, 1672-1680
74. Wang, Y., Tzfira, T., Gaba, V., Citovsky, V., Palukaitis, P., and Gal-On, A. (2004) Functional analysis of the Cucumber mosaic virus 2b protein: pathogenicity and nuclear localization. J. Gen. Virol. 85, 3135-3147
75. Xu, A., Zhao, Z., Chen, W., Zhang, H., Liao, Q., Chen, J., Carr, J. P., and Du, Z. (2013) Self-interaction of the cucumber mosaic virus 2b protein plays a vital role in the suppression of RNA silencing and the induction of viral symptoms. Mol. Plant Pathol. 14, 803-812
76. Hamera, S., Song, X., Su, L., Chen, X., and Fang, R. (2012) Cucumber mosaic virus suppressor 2b binds to AGO4-related small RNAs and impairs AGO4 activities. Plant J. 69, 104-115
77. Thomas, C. L., Leh, V., Lederer, C., and Maule, A. J. (2003) Turnip crinkle virus coat protein mediates suppression of RNA silencing in Nicotiana benthamiana. Virology 306, 33-41
78. González, I., Rakitina, D., Semashko, M., Taliansky, M., Praveen, S., Palukaitis, P., Carr, J. P., Kalinina, N., and Canto, T. (2012) RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization. RNA 18, 771-782
79. Chiba, S., Hleibieh, K., Delbianco, A., Klein, E., Ratti, C., Ziegler-Graff, V., Bouzoubaa, S., and Gilmer, D. (2013) The benyvirus RNA silencing suppressor is essential for long-distance movement, requires both zinc-finger and NoLS basic residues but not a nucleolar localization for its silencing-suppression activity. Mol. Plant Microbe Interact. 26, 168-181
80. Ruiz-Ruiz, S., Soler, N., Sánchez-Navarro, J., Fagoaga, C., López, C., Navarro, L., Moreno, P., Peña, L., and Flores, R. (2013) Citrus tristeza virus p23: determinants for nucleolar localization and their influence on suppression of RNA silencing and pathogenesis. Mol. Plant Microbe Interact. 26, 306-318
81. Bragg, J. N., and Jackson, A. O. (2004) The C-terminal region of the Barley stripe mosaic virus γb protein participates in homologous interactions and is required for suppression of RNA silencing. Mol. Plant Pathol. 5, 465-481
82. Duan, C. G., Fang, Y. Y., Zhou, B. J., Zhao, J. H., Hou, W. N., Zhu, H., Ding, S. W., and Guo, H. S. (2012) Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b protein. Plant Cell 24, 259-274
83. Vogler, H., Akbergenov, R., Shivaprasad, P. V., Dang, V., Fasler, M., Kwon, M. O., Zhanybekova, S., Hohn, T., and Heinlein, M. (2007) Modification of small RNAs associated with suppression of RNA silencing by tobamovirus replicase protein. J. Virol. 81, 10379-10388
84. Endres, M. W., Gregory, B. D., Gao, Z., Foreman, A. W., Mlotshwa, S., Ge, X., Pruss, G. J., Ecker, J. R., Bowman, L. H., and Vance, V. (2010) Two plant viral suppressors of silencing require the ethylene-inducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog. 6, e1000729
85. Dalmay, T., Rubino, L., Burgyán, J., and Russo, M. (1992) Replication and movement of a coat protein mutant of cymbidium ringspot tombusvirus. Mol. Plant Microbe Interact. 5, 379-383
86. Hacker, D. L., Petty, I. T., Wei, N., and Morris, T. J. (1992) Turnip crinkle virus genes required for RNA replication and virus movement. Virology 186, 1-8
87. Molnár, A., Havelda, Z., Dalmay, T., Szutorisz, H., and Burgyán, J. (1997) Complete nucleotide sequence of Tobacco necrosis virus strain DH and genes required for RNA replication and virus movement. J. Gen. Virol. 78, 1235-1239
88. Reade, R., Miller, J., Robbins, M., Xiang, Y., and Rochon, D. (2003) Molecular analysis of the Cucumber leaf spot virus genome. Virus Res. 91, 171-179
89. Rubino, L., and Russo, M. (1997) Molecular analysis of the Pothos latent virus genome. J. Gen. Virol. 78, 1219-1226
90. Sit, T. L., Johnston, J. C., ter Borg, M. G., Frison, E., McLean, M. A., and Rochon, D. (1995) Mutational analysis of the Cucumber necrosis virus coat protein gene. Virology 206, 38-48
91. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W., and Baulcombe, D. C. (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17, 6739-6746
92. Jay, F., Wang, Y., Yu, A., Taconnat, L., Pelletier, S., Colot, V., Renou, J. P., and Voinnet, O. (2011) Misregulation of AUXIN RESPONSE FACTOR 8 underlies the developmental abnormalities caused by three distinct viral silencing suppressors in Arabidopsis. PLoS Pathog. 7, e1002035
93. Kasschau, K. D., Xie, Z., Allen, E., Llave, C., Chapman, E. J., Krizan, K. A., Carrington, J. C. (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 4, 205-217
94. Alonso, M., and Borja, M. (2005) High incidence of Pelargonium line pattern virus infecting asymptomatic Pelargonium spp. in Spain. Eur. J. Plant Pathol. 10.1007/s10658-005-0803-1