Citrus tristeza virus p23: A unique protein mediating key virus-host interactions

Frontiers in Microbiology

Volumn 4, Issue MAY, 2013, Pages

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

^a UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

^b Instituto Valenciano de Investigaciones Agraria   (Spain)

Author keywords

Closteroviruses; Nucleolar proteins; RNA silencing suppressor; Small interfering RNAs; Zinc finger domain

Indexed keywords

MALTOSE BINDING PROTEIN; PROTEIN P20; PROTEIN P23; PROTEIN P25;

BINDING AFFINITY; BIOCHEMISTRY; CAULIFLOWER MOSAIC VIRUS; CITRUS TRISTEZAVIRUS; CLOSTEROVIRUS; CONFOCAL LASER MICROSCOPY; GENE EXPRESSION; GENE SILENCING; GRAPEFRUIT; NONHUMAN; NUCLEOLAR LOCALIZATION SIGNAL; POTEXVIRUS; PROTEIN EXPRESSION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; REVIEW; RNA SILENCING; SEEDLING YELLOW SYNDROME; SLOT BLOT HYBRIDIZATION; SOUR ORANGE; VIRAL PLANT DISEASE; VIRUS CELL INTERACTION; VIRUS REPLICATION; ZINC FINGER MOTIF;

BEET YELLOWS VIRUS; CITRUS; CITRUS AURANTIUM; CITRUS TRISTEZA VIRUS; CITRUS X PARADISI; CLOSTEROVIRUS;

EID: 84884244696     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00098     Document Type: Review

References (53)

1. Albiach-Martí, M. R., Robertson, C., Gowda, S., Tatineni, S., Belliure, B., Garnsey, S. M., et al. (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., et al. (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. Bar-Joseph, M., and Dawson, W. O. (2008). "Citrus tristeza virus," in Encyclopedia of Virology, eds B. W. J. Mahy and M. H. V. Van Regenmortel (Oxford: Elsevier), 520-525.
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. Batuman, O., Mawassi, M., and Bar-Joseph, M. (2006). Transgenes consisting of a dsRNA of an RNAi suppressor plus the 3'UTR provide resistance to Citrus tristeza virus sequences in Nicotiana benthamiana but not in citrus. Virus Genes 33, 319-327.
6. 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.
7. Carthew, R. W., and Sontheimer, E. J. (2009). Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642-655.
8. Chen, X. (2009). Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25, 21-44.
9. Chiba, M., Reed, J. C., Prokhnevsky, A. I., Chapman, E. J., Mawassi, M., Koonin, E. V., et al. (2006). Diverse suppressors of RNA silencing enhance agroinfection by a viral replicon. Virology 346, 7-14.
10. Chiba, S., Hleibieh, K., Delbianco, A., Klein, E., Ratti, C., Ziegler-Graff, V., et al. (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.
11. Csorba, T., Pantaleo, V., and Burgyán, J. (2009). RNA silencing: an antiviral mechanism. Adv. Virus Res. 75, 35-71.
12. 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.
13. Ding, S. W. (2010). RNA-based antiviral immunity. Nat. Rev. Immunol. 10, 632-644.
14. Dolja, V. V., Karasev, A. V., and Koonin, E. V. (1994). Molecular biology and evolution of closteroviruses: sophisticated build-up of large RNA genomes. Annu. Rev. Phytopathol. 32, 261-285.
15. Dolja, V. V., Kreuze, J. F., and Valkonen, J. P. (2006). Comparative and functional genomics of closteroviruses. Virus Res. 117, 38-51.
16. Duan, C. G., Fang, Y. Y., Zhou, B. J., Zhao, J. H., Hou, W. N., Zhu, H., et al. (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.
17. Fagoaga, C., López, C., Hermoso de Mendoza, A. H., Moreno, P., Navarro, L., Flores, R., et al. (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.
18. 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 gene 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.
19. 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.
20. Febres, V. J., Lee, R. F., and Moore, G. A. (2008). Transgenic resistance to Citrus tristeza virus in grapefruit. Plant Cell Rep. 27, 93-104.
21. Folimonov, A. S., Folimonova, S. Y., Bar-Joseph, M., and Dawson, W. O. (2007). A stable RNA virus-based vector for citrus trees. Virology 368, 205-216.
22. 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.
23. Ghorbel, R., López, C., Fagoaga, C., Moreno, P., Navarro, L., Flores, R., et al. (2001). Transgenic citrus plants expressing the Citrus tristeza virus p23 protein exhibit viral-like symptoms. Mol. Plant Pathol. 2, 27-36.
24. 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.
25. Jay, F., Wang, Y., Yu, A., Taconnat, L., Pelletier, S., Colot, V., et al. (2011). Misregulation of AUXIN RESPONSE FACTOR 8 underlies the developmental abnormalities caused by three distinct viral silencing suppressors in Arabidopsis. PLoS Pathog. 7:e1002035. doi: 10.1371/journal.ppat.1002035
26. Karasev, A. V., Boyko, V. P., Gowda, S., Nikolaeva, O. V., Hilf, M. E., Koonin, E. V., et al. (1995). Complete sequence of the Citrus tristeza virus RNA genome. Virology 208, 511-520.
27. Kasschau, K. D., Xie, Z., Allen, E., Llave, C., Chapman, E. J., Krizan, K. A., et al. (2003). P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 4, 205-217.
28. López, C., Ayllón, M. A., Navas-Castillo, J., Guerri, J., Moreno, P., and Flores, R. (1998). Molecular variability of the 5'- and 3'-terminal regions of Citrus tristeza virus RNA. Phytopathology 88, 685-691.
29. López, C., Cervera, M., Fagoaga, C., Moreno, P., Navarro, L., Flores, R., et al. (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.
30. 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.
31. Lu, R., Folimonov, A., Shintaku, M., Li, W. X., Falk, B. W., Dawson, W. O., et al. (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.
32. 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.
33. Mallory, A., and Vaucheret, H. (2010). Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22, 3879-3889.
34. 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.
35. Medberry, S. L., Lockhart, B. E., and Olszewski, N. E. (1992). The commelina yellow mottle virus promoter is a strong promoter in vascular and reproductive tissues. Plant Cell 4, 185-192.
36. Morel, J. B., Godon, C., Mourrain, P., Beclin, C., Boutet, S., Feuerbach, F., et al. (2002). Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14, 629-639.
37. 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.
38. Navas-Castillo, J., Albiach-Martí, M. R., Gowda, S., Hilf, M. E., Garnsey, S. M., and Dawson, W. O. (1997). Kinetics of accumulation of Citrus tristeza virus RNAs. Virology 228, 92-97.
39. Pappu, H. R., Karasev, A. V., Anderson, E. J., Pappu, S. S., Hilf, M. E., Febres, V. J., et al. (1994). Nucleotide sequence and organization of eight 3' open reading frames of the citrus tristeza closterovirus genome. Virology 199, 35-46.
40. Pappu, S. S., Febres, V. J., Pappu, H. R., Lee, R. F., and Niblett, C. L. (1997). Characterization of the 3' proximal gene of the citrus tristeza closterovirus genome. Virus Res. 47, 51-57.
41. Roy, G., Sudarshana, M. R., Ullman, D. E., Ding, S. W., Dandekar, A. M., and Falk, B. W. (2006). Chimeric cDNA sequences from Citrus tristeza virus confer RNA silencing-mediated resistance in transgenic Nicotiana benthamiana plants. Phytopathology 96, 819-827.
42. Ruiz-Ruiz, S., Navarro, B., Gisel, A., Peña, L., Navarro, L., Moreno, P., et al. (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.
43. Ruiz-Ruiz, S., Soler, N., Sánchez-Navarro, J., Fagoaga, C., López, C., Navarro, L., et al. (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.
44. 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.
45. Satyanarayana, T., Bar-Joseph, M., Mawassi, M., Albiach-Martí, M. R., Ayllón, M. A., Gowda, S., et al. (2001). Amplification of Citrus tristeza virus from a cDNA clone and infection of citrus trees. Virology 280, 87-96.
46. 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.
47. Satyanarayana, T., Gowda, S., Boyko, V. P., Albiach-Martí, M. R., Mawassi, M., Navas-Castillo, J., et al. (1999). An engineered closterovirus RNA replicon and analysis of heterologous terminal sequences for replication. Proc. Natl. Acad. Sci. U.S.A. 96, 7433-7438.
48. Smith, N. A., Singh, S. P., Wang, M. B., Stoutjesdijk, P. A., Green, A. G., and Waterhouse, P. M. (2000). Total silencing by intron-spliced hairpin RNAs. Nature 407, 319-320.
49. Soler, N., Plomer, M., Fagoaga, C., Moreno, P., Navarro, L., Flores, R., et al. (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.
50. Varallyay, E., Valoczi, A., Agyi, A., Burgyán, J., and Havelda, Z. (2010). Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J. 29, 3507-3519.
51. Vives, M. C., Rubio, L., López, C., Navas-Castillo, J., Albiach-Martí, M. R., Dawson, W. O., et al. (1999). The complete genome sequence of the major component of a mild Citrus tristeza virus isolate. J. Gen. Virol. 80, 811-816.
52. 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.
53. 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.