Citrus tristeza virus p23: Determinants for nucleolar localization and their influence on suppression of RNA silencing and pathogenesis

Molecular Plant-Microbe Interactions

Volumn 26, Issue 3, 2013, Pages 306-318

  Ruiz Ruiz, Susana ^a,b   Soler, Nuria ^b   Sánchez Navarro, Jesús ^a   Fagoaga, Carmen ^b   López, Carmelo ^a,c   Navarro, Luis ^b   Moreno, Pedro ^b   Peña, Leandro ^b   Flores, Ricardo ^a  

^a Universitat Politècnica de València   (Spain)

^b INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

^c UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; VIRUS PROTEIN;

ACTIVE TRANSPORT; AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; CITRUS; CLOSTEROVIRUS; COILED BODY; CONFOCAL MICROSCOPY; CYTOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MOLECULAR GENETICS; NUCLEOLUS; PATHOGENICITY; PLANT DISEASE; PLANT LEAF; PLASMODESMA; POINT MUTATION; POTEXVIRUS; PROTEIN MOTIF; RNA INTERFERENCE; TOBACCO; TRANSGENE; TRANSGENIC PLANT; VIROLOGY; VIRULENCE;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL NUCLEOLUS; CITRUS; CLOSTEROVIRUS; COILED BODIES; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PLASMODESMATA; POINT MUTATION; POTEXVIRUS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SEQUENCE DELETION; TOBACCO; TRANSGENES; VIRAL PROTEINS; VIRULENCE;

EID: 84874084428     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-08-12-0201-R     Document Type: Article

References (70)

1. Albiach-Martí, M. R., Robertson, C., Gowda, S., Tatineni, S., Belliure, B., Garnsey, S. M., Folimonova, S. Y., Moreno, P., and Dawson, W. O. 2010. The pathogenicity determinant of Citrus tristeza virus causing the seedling yellows syndrome maps at the 3'-terminal region of the viral genome. Mol. Plant Pathol. 11:55-67.
2. Ambrós, S., El-Mohtar, C., Ruiz-Ruiz, S., Peña, L., Guerri, J., Dawson, W. O., and Moreno, P. 2011. Agroinoculation of Citrus tristeza virus causes systemic infection and symptoms in the presumed nonhost Nicotiana benthamiana. Mol. Plant-Microbe Interact. 24:1119-1131.
3. Ancillo, G., Gadea, J., Forment, J., Guerri, J., and Navarro, L. 2007. Class prediction of closely related plant varieties using gene expression profiling. J. Exp. Bot. 58:1927-1933.
4. Bar-Joseph, M., Marcus, R., and Lee, R. F. 1989. The continuous challenge of citrus tristeza virus control. Annu. Rev. Phytopathol. 27:291-316.
5. Barneche, F., Steinmetz, F., and Echeverria, M. 2000. Fibrillarin genes encode both a conserved nucleolar protein and a novel small nucleolar RNA involved in ribosomal RNA methylation in Arabidopsis thaliana. J. Biol. Chem. 275:27212-27220.
6. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
7. 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 (Eur. Mol. Biol. Organ.) J. 17:6739-6746.
8. Canetta, E., Kim, S. H., Kalinina, N. O., Shaw, J., Adya, A. K., Gillespie, T., Brown, J. W. S., and Taliansky, M. 2008. A plant virus movement protein forms ringlike complexes with the major nucleolar protein, fibrillarin, in vitro. J. Mol. Biol. 376:932-937.
9. Carpenter, C. D., and Simon, A. E. 1998. Preparation of RNA. Methods Mol. Biol. 82:85-89.
10. Carrington, J. C., Freed, D. D., and Leinicke, A. J. 1991. Bipartite signal sequence mediates nuclear translocation of the plant potyviral NIa protein. Plant Cell 3:953-962.
11. Chiba, M., Reed, J. C., Prokhnevsky, A. I., Chapman, E. J., Mawassi, M., Koonin, E. V., Carrington, J. C., and Dolja, V. V. 2006. Diverse suppressors of RNA silencing enhance agroinfection by a viral replicon. Virology 346:7-14.
12. Chiba, S., Hleibieh, K., Delbianco, A., Klein, E., Ratti, C., Ziegler-Graff, V., Bouzoubaa, S. E., and Gilmer, D. 2013. The benyvirus RNA silencing suppressor is essential for long-distance movement, requires both Zn-finger and NoLS basic residues but not a nucleolar localization for its silencing suppression activity. Mol. Plant-Microbe Interact. 26:168-181.
13. Csorba, T., Pantaleo, V., and Burgyán, J. 2009. RNA silencing: An antiviral mechanism. Adv. Virus Res. 75:35-71.
14. Dalmay, T., Hamilton, A., Rudd, S., Angell, S., and Baulcombe, D. C. 2000. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543-553.
15. Dellaporta, S., Wood, J., and Hicks, J. 1983. A plant DNA minipreparation: Version II. Plant Mol. Biol. Rep. 1:19-21.
16. Díaz-Pendón, J. A., and Ding, S. W. 2008. Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. Annu. Rev. Phytopathol. 46:303-326.
17. Ding, S. W. 2010. RNA-based antiviral immunity. Nat. Rev. Immunol. 10:632-644.
18. Dolja, V. V., Kreuze, J. F., and Valkonen, J. P. 2006. Comparative and functional genomics of closteroviruses. Virus Res. 117:38-51.
19. 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 ARGO-NAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b protein. Plant Cell 24:259-274.
20. Fagoaga, C., López, C., Moreno, P., Navarro, L., Flores, R., and Peña, L. 2005. Viral-like symptoms induced by the ectopic expression of the p23 of Citrus tristeza virus are citrus specific and do not correlate with the pathogenicity of the virus strain. Mol. Plant-Microbe Interact. 18:435-445.
21. Fagoaga, C., López, C., Hermoso De Mendoza, A. H., Moreno, P., Navarro, L., Flores, R., and Peña, L. 2006. Post-transcriptional gene silencing of the p23 silencing suppressor of Citrus tristeza virus confers resistance to the virus in transgenic Mexican lime. Plant Mol. Biol. 66:153-165.
22. Fagoaga, C., Pensabene, G., Moreno, P., Navarro, L., Flores, R., and Peña, L. 2011. Ectopic expression of the p23 silencing suppressor of Citrus tristeza virus differentially modifies viral accumulation and tropism in two transgenic woody hosts. Mol. Plant Pathol. 12:898-910.
23. Flores, R. 1986. Detection of citrus exocortis viroid in crude extracts by dot-blot hybridization: Conditions for reducing spurious hybridization results and for enhancing the sensitivity of the technique. J. Virol. Methods 13:161-169.
24. Folimonova, S. Y., Folimonov, A. S., Tatineni, S., and Dawson, W. O. 2008. Citrus tristeza virus: Survival at the edge of the movement continuum. J. Virol. 82:6546-6556.
25. Ghorbel, R., López, C., Fagoaga, C., Moreno, P., Navarro, L., Flores, R., and Peña, L. 2001. Transgenic citrus plants expressing the Citrus tristeza virus p23 protein exhibit viral-like symptoms. Mol. Plant Pathol. 2:27-36.
26. 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.
27. 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.
28. Hamilton, A. J., and Baulcombe, D. C. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950-952.
29. Herranz, M. C., Sánchez-Navarro, J. A., Saurí, A., Mingarro, I., and Pallás, V. 2005. Mutational analysis of the RNA-binding domain of the Prunus necrotic ringspot virus (PNRSV) movement protein reveals its requirement for cell-to-cell movement. Virology 339:31-41.
30. Hilf, M. E., Karasev, A. V., Pappu, H. R., Gumpf, D. J., Niblett, C. L., and Garnsey, S. M. 1995. Characterization of citrus tristeza virus subgenomic RNAs in infected tissue. Virology 208:576-582.
31. Hiscox, J. A. 2007. RNA viruses: Hijacking the dynamic nucleolus. Nat. Rev. Microbiol. 5:119-127.
32. Jacobson, S. E., Running, M. P., and Meyerowitz, E. M. 1999. Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126:5231-5243.
33. 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.
34. Kanazawa, A., Inaba, J., Shimura, H., Otagaki, S., Tsukahara, S., Matsuzawa, A., Kim, B. M., Goto, K., and Masuta, C. 2011. Virusmediated efficient induction of epigenetic modifications of endogenous genes with phenotypic changes in plants. Plant J. 65:156-168.
35. Karasev, A. V., Boyko, V. P., Gowda, S., Nikolaeva, O. V., Hilf, M. E., Koonin, E. V., Niblett, C. L., Cline, K., Gumpf, D. J., Lee, R. F., Garnsey, S. M., Lewandowski, D. J., and Dawson, W. O. 1995. Complete sequence of the Citrus tristeza virus RNA genome. Virology 208:511-520.
36. Kasschau, K. D., and Carrington, J. C. 1998. A counterdefensive strategy of plant viruses: Suppression of posttranscriptional gene silencing. Cell 95:461-470.
37. Kim, S. H., Ryabov, E. V., Kalinina, N. O., Rakitina, D. V., Gillespie, T., MacFarlane, S., Haupt, S., Brown, J. W. S., and Taliansky, M. 2007. Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO (Eur. Mol. Biol. Organ.) J. 26:2169-2179.
38. 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.
39. Kosugi, S., Hasebe, M., Matsumura, N., Takashima, H., Miyamoto-Sato, E., Tomita, M., and Yanagawa, H. 2009. Six classes of nuclear localization signals specific to different binding grooves of importin alpha. J. Biol. Chem. 284:478-485.
40. López, C., Navas-Castillo, J., Gowda, S., Moreno, P., and Flores, R. 2000. The 23 kDa protein coded by the 3'-terminal gene of Citrus tristeza virus is an RNA-binding protein. Virology 269:462-470.
41. López, C., Cervera, M., Fagoaga, C., Moreno, P., Navarro, L., Flores, R., and Peña, L. 2010. Accumulation of transgene-derived siRNAs is not sufficient for RNAi-mediated protection against Citrus tristeza virus (CTV) in transgenic Mexican lime. Mol. Plant Pathol. 11:33-41.
42. Lu, R., Folimonov, A., Shintaku, M., Li, W. X., Falk, B. W., Dawson, W. O., and Ding, S. W. 2004. Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. U. S. A. 101:15742-15747.
43. Lukhovitskaya, N. I., Ignatovich, I. V., Savenkov, E. I., Schiemann, J., Morozov, S. Y., and Solovyev, A. G. 2009. Role of the zinc-finger and basic motifs of Chrysanthemum virus B p12 protein in nucleic acid binding, protein localization and induction of a hypersensitive response upon expression from a viral vector. J. Gen. Virol. 90:723-733.
44. Martínez-Touriño, 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.
45. Mawassi, M., Mietkiewska, E., Gofman, R., Yang, G., and Bar-Joseph, M. 1996. Unusual sequence relationships between two isolates of Citrus tristeza virus. J. Gen. Virol. 77:2359-2364.
46. Molnar, A., Csorba, T., Lakatos, L., Varallyay, E., Lacomme, C., and Burgyán, J. 2005. Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J. Virol. 79:7812-7818.
47. Moreno, P., Ambrós, S., Albiach-Martí, M. R., Guerri, J., and Peña, L. 2008. Citrus tristeza virus: A pathogen that changed the course of the citrus industry. Mol. Plant Pathol. 9:251-268.
48. Omarov, R. T., Cioperlik, J. J., and Sholthof, H. B. 2007. RNAi-associated ssRNA-specific ribonucleases in tombusvirus P19 mutant-infected plants and evidence for a discrete siRNA-containing effector complex. Proc. Natl. Acad. Sci. U. S. A. 104:1714-1719.
49. Pantaleo, V., Szittya, G., and Burgyán, J. 2007. Molecular bases of viral RNA targeting by viral small interfering RNA-programmed RISC. J. Virol. 81:3797-3806.
50. Pruss, G., Ge, X., Shi, X. M., Carrington, J. C., and Vance, V. B. 1997. Plant vira1 synergism: The potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9:859-868.
51. Qi, Y., Denli, A. M., and Hannon, G. J. 2005. Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19:421-428.
52. Qiu, W. P., Park, J. W., and Scholthof, H. B. 2002. Tombusvirus P19-mediated suppression of virus induced gene silencing is controlled by genetic and dosage features that influence pathogenicity. Mol. Plant-Microbe Interact. 15:269-280.
53. Rajamäki, M. L., and Valkonen, J. P. T. 2009. Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like Po t a t o virus A in Nicotiana species. Plant Cell 21:2485-2502.
54. Ruiz, M. T., Voinnet, O., and Baulcombe, D. C. 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10:937-946.
55. Ruiz-Ruiz, S., Navarro, B., Gisel, A., Peña, L., Navarro, L., Moreno, P., Di Serio, F., and Flores, R. 2011. Citrus tristeza virus infection induces the accumulation of viral small RNAs (21-24-nt) mapping preferentially at the 3'-terminal region of the genomic RNA and affects the host small RNA profile. Plant Mol. Biol. 75:607-619.
56. Ryabov, E. V., Kim, S. H., and Taliansky, M. 2004. Identification of a nuclear localization signal and nuclear export signal of the umbraviral long-distance RNA movement protein. J. Gen. Virol. 85:1329-1333.
57. Sablowski, R. W. M., Baulcombe, D. C., and Bevan, M. 1995. Expression of a flower-specific Myb protein in leaf cells using a viral vector causes ectopic activation of a target promoter. Proc. Natl. Acad. Sci. U. S. A. 92:6901-6905.
58. Sambade, A., López, C., Rubio, L., Flores, R., Guerri, J., and Moreno, P. 2003. Polymorphism of a specific region in gene p23 of Citrus tristeza virus allows discrimination between mild and severe isolates. Arch. Virol. 148:2325-2340.
59. Satyanarayana, T., Bar-Joseph, M., Mawassi, M., Albiach-Martí, M. R., Ayllón, M. A., Gowda, S., Hilf, M. E., Moreno, P., Garnsey, S. M., and Dawson, W. O. 2001. Amplification of Citrus tristeza virus from a cDNA clone and infection of citrus trees. Virology 280:87-96.
60. Satyanarayana, T., Gowda, S., Ayllón, M. A., Albiach-Martí, M. R., Rabindram, R., and Dawson, W. O. 2002. The p23 protein of Citrus tristeza virus controls asymmetrical RNA accumulation. J. Virol. 76:473-483.
61. Schaad, M. C., Haldeman-Cahill, R., Cronin, S., and Carrington, J. C. 1996. Analysis of the VPg-proteinase (NIa) encoded by Tobacco etch potyvirus: Effects of mutations on subcellular transport, proteolytic processing and genome amplification. J. Virol. 70:7039-7048.
62. Soler, N., Plomer, M., Fagoaga, C., Moreno, P., Navarro, L., Flores, R., and Peña, L. 2012. Transformation of Mexican lime with an intron-hairpin construct expressing untranslatable versions of the genes coding for the three silencing suppressors of Citrus tristeza virus confers complete resistance to the virus. Plant Biotechnol. J. 10:597-608.
63. Taliansky, M. E., Brown, J. W. S., Rajamäki, M. L., Valkonen, J. P. T., and Kalinina, N. O. 2010. Involvement of the plant nucleolus in virus and viroid infections: Parallels with animal pathosystems. Adv. Virus Res. 77:119-158.
64. Tomenius, K., Clapham, D., and Meshi, T. 1987. Localization by immunogold cytochemistry of the virus-coded 30K protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160:363-371.
65. Vaucheret, H. 2008. Plant ARGONAUTES. Trends Plant Sci. 13:350-358.
66. Vives, M. C., Rubio, L., López, C., Navas-Castillo, J., Albiach-Martí, M. R., Dawson, W. O., Guerri, J., Flores, R., and Moreno, P. 1999. The complete genome sequence of the major component of a mild Citrus tristeza virus isolate. J. Gen. Virol. 80:811-816.
67. Voinnet, O. 2008. Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci. 13:317-328.
68. 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.
69. Yang, Z. N., Mathews, D. H., Dodds, J. A., and Mirkov, T. E. 1999. Molecular characterization of an isolate of Citrus tristeza virus that causes severe symptoms in sweet orange. Virus Genes 19:131-142.
70. 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 Argonaute1 cleavage activity to counter plant defense. Genes Dev. 20:3255-3268.