Identification of the domains of cauliflower mosaic virus protein P6 responsible for suppression of RNA silencing and salicylic acid signalling

Journal of General Virology

Volumn 94, Issue PART 12, 2013, Pages 2777-2789

  Laird, Janet ^a   McInally, Carol ^a   Carr, Craig ^a   Doddiah, Sowjanya ^a   Yates, Gary ^a   Chrysanthou, Elina ^a   Khattab, Ahmed ^a   Love, Andrew J ^a,e   Geri, Chiara ^a,b   Sadanandom, Ari ^c   Smith, Brian O ^a   Kobayashi, Kappei ^d   Milner, Joel J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b Institute of Agricultural Biology and Biotechnology   (Italy)

^c DURHAM UNIVERSITY   (United Kingdom)

^d EHIME UNIVERSITY   (Japan)

^e SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAULIFLOWER MOSAIC VIRUS PROTEIN P6; RNA; SALICYLIC ACID; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALLERGIC REACTION; APOPTOSIS; ARABIDOPSIS; ARTICLE; BIOSAFETY; CAULIFLOWER MOSAIC VIRUS; CELL DEATH; CONTROLLED STUDY; MUTANT; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; TOBACCO; TOMATO; TRANSGENIC PLANT; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ARABIDOPSIS; CAULIMOVIRUS; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; SALICYLIC ACID; SEQUENCE DELETION; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; VIRUS REPLICATION;

EID: 84887508745     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.057729-0     Document Type: Article

References (69)

1. Agama, K., Beach, S., Schoelz, J. & Leisner, S. M. (2002). The 5' third of Cauliflower mosaic virus gene VI conditions resistance breakage in Arabidopsis ecotype Tsu-0. Phytopathology 92, 190-196.
2. Alonso-Peral, M. M., Li, J., Li, Y., Allen, R. S., Schnippenkoetter, W., Ohms, S., White, R. G. & Millar, A. A. (2010). The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol 154, 757-771.
3. Angel, C. A. & Schoelz, J. E. (2013). A survey of resistance to Tomato bushy stunt virus in the genus Nicotiana reveals that the hypersensitive response is triggered by one of three different viral proteins. Mol Plant Microbe Interact 26, 240-248.
4. Angel, C. A., Lutz, L., Yang, X., Rodriguez, A., Adair, A., Zhang, Y., Leisner, S. M., Nelson, R. S. & Schoelz, J. E. (2013). The P6 protein of Cauliflower mosaic virus interacts with CHUP1, a plant protein which moves chloroplasts on actin microfilaments. Virology 443, 363-374.
5. Baughman, G. A., Jacobs, J. D. & Howell, S. H. (1988). Cauliflower mosaic virus gene VI produces a symptomatic phenotype in transgenic tobacco plants. Proc Natl Acad Sci U S A 85, 733-737.
6. Bazzini, A. A., Mongelli, V. C., Hopp, H. E., del Vas, M. & Asurmendi, S. (2007). A practical approach to the understanding and teaching of RNA silencing in plants. Electron J Biotechnol 10, 178-190.
7. Blevins, T., Rajeswaran, R., Shivaprasad, P. V., Beknazariants, D., Si-Ammour, A., Park, H. S., Vazquez, F., Robertson, D., Meins, F., Jr & other authors (2006). Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34, 6233-6246.
8. Bonneville, J. M., Sanfaçon, H., Fü tterer, J. & Hohn, T. (1989). Posttranscriptional trans-activation in cauliflower mosaic virus. Cell 59, 1135-1143.
9. Bureau, M., Leh, V., Haas, M., Geldreich, A., Ryabova, L., Yot, P. & Keller, M. (2004). P6 protein of Cauliflower mosaic virus, a translation reinitiator, interacts with ribosomal protein L13 from Arabidopsis thaliana. J Gen Virol 85, 3765-3775.
10. Burgyá n, J. & Havelda, Z. (2011). Viral suppressors of RNA silencing. Trends Plant Sci 16, 265-272.
11. Cecchini, E., Gong, Z. H., Geri, C., Covey, S. N. & Milner, J. J. (1997). Transgenic Arabidopsis lines expressing gene VI from cauliflower mosaic virus variants exhibit a range of symptom-like phenotypes and accumulate inclusion bodies. Mol Plant Microbe Interact 10, 1094-1101.
12. Cecchini, E., Al Kaff, N. S., Bannister, A., Giannakou, M. E., McCallum, D. G., Maule, A. J., Milner, J. J. & Covey, S. N. (1998). Pathogenic interactions between variants of cauliflower mosaic virus and Arabidopsis thaliana. J Exp Bot 49, 731-737.
13. Cerritelli, S. M., Fedoroff, O. Y., Reid, B. R. & Crouch, R. J. (1998). A common 40 amino acid motif in eukaryotic RNases H1 and caulimovirus ORF VI proteins binds to duplex RNAs. Nucleic Acids Res 26, 1834-1840.
14. Cole, C., Barber, J. D. & Barton, G. J. (2008). The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36 (Web Server issue), W197-W201.
15. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. & 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.
16. De Tapia, M., Himmelbach, A. & Hohn, T. (1993). Molecular dissection of the cauliflower mosaic virus translation transactivator. EMBO J 12, 3305-3314.
17. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-1797.
18. Endres, M. W., Gregory, B. D., Gao, Z. H., Foreman, A. W., Mlotshwa, S., Ge, X., Pruss, G. J., Ecker, J. R., Bowman, L. H. & Vance, V. (2010). Two plant viral suppressors of silencing require the ethyleneinducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog 6, e1000729.
19. Fu, Z. Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., Mohan, R., Spoel, S. H., Tada, Y. & other authors (2012). NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228-232.
20. Geri, C., Love, A. J., Cecchini, E., Barrett, S. J., Laird, J., Covey, S. N. & Milner, J. J. (2004). Arabidopsis mutants that suppress the phenotype induced by transgene-mediated expression of cauliflower mosaic virus (CaMV) gene VI are less susceptible to CaMV-infection and show reduced ethylene sensitivity. Plant Mol Biol 56, 111-124.
21. Haas, M., Bureau, M., Geldreich, A., Yot, P. & Keller, M. (2002). Cauliflower mosaic virus: still in the news. Mol Plant Pathol 3, 419-429.
22. Haas, M., Geldreich, A., Bureau, M., Dupuis, L., Leh, V., Vetter, G., Kobayashi, K., Hohn, T., Ryabova, L. & other authors (2005). The open reading frame VI product of Cauliflower mosaic virus is a nucleocytoplasmic protein: its N terminus mediates its nuclear export and formation of electron-dense viroplasms. Plant Cell 17, 927-943.
23. Haas, G., Azevedo, J., Moissiard, G., Geldreich, A., Himber, C., Bureau, M., Fukuhara, T., Keller, M. & 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.
24. Hapiak, M., Li, Y. Z., Agama, K., Swade, S., Okenka, G., Falk, J., Khandekar, S., Raikhy, G., Anderson, A. & other authors (2008). Cauliflower mosaic virus gene VI product N-terminus contains regions involved in resistance-breakage, self-association and interactions with movement protein. Virus Res 138, 119-129.
25. Harries, P. A., Palanichelvam, K., Yu, W., Schoelz, J. E. & Nelson, R. S. (2009). The cauliflower mosaic virus protein P6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiol 149, 1005-1016.
26. Kirá ly, L., Bourque, J. E. & Schoelz, J. E. (1998). Temporal and spatial appearance of recombinant viruses formed between cauliflower mosaic virus (CaMV) and CaMV sequences present in transgenic Nicotiana bigelovii. Mol Plant Microbe Interact 11, 309-316.
27. Kobayashi, K. & Hohn, T. (2003). Dissection of cauliflower mosaic virus transactivator/viroplasmin reveals distinct essential functions in basic virus replication. J Virol 77, 8577-8583.
28. Kobayashi, K. & Hohn, T. (2004). The avirulence domain of Cauliflower mosaic virus transactivator/viroplasmin is a determinant of viral virulence in susceptible hosts. Mol Plant Microbe Interact 17, 475-483.
29. Latham, J. & Wilson, A. (2013). Potentially dangerous virus gene hidden in commercial GM crops. Institute of Science in Society (Report). http://www.i-sis.org.uk/Hazardous_Virus_Gene_Discovered_in_GM_Crops.php.
30. Leh, V., Yot, P. & Keller, M. (2000). The cauliflower mosaic virus translational transactivator interacts with the 60S ribosomal subunit protein L18 of Arabidopsis thaliana. Virology 266, 1-7.
31. Lewsey, M. G., Murphy, A. M., Maclean, D., Dalchau, N., Westwood, J. H., Macaulay, K., Bennett, M. H., Moulin, M., Hanke, D. E. & other authors (2010). Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact 23, 835-845.
32. Li, Y. Z. & Leisner, S. M. (2002). Multiple domains within the Cauliflower mosaic virus gene VI product interact with the full-length protein. Mol Plant Microbe Interact 15, 1050-1057.
33. Li, F., Pignatta, D., Bendix, C., Brunkard, J. O., Cohn, M. M., Tung, J., Sun, H. Y., Kumar, P. & Baker, B. (2012). MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci U S A 109, 1790-1795.
34. Love, A. J., Yun, B. W., Laval, V., Loake, G. J. & Milner, J. J. (2005). Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139, 935-948.
35. Love, A. J., Laird, J., Holt, J., Hamilton, A. J., Sadanandom, A. & Milner, J. J. (2007). Cauliflower mosaic virus protein P6 is a suppressor of RNA silencing. J Gen Virol 88, 3439-3444.
36. Love, A. J., Geri, C., Laird, J., Carr, C., Yun, B. W., Loake, G. J., Tada, Y., Sadanandom, A. & Milner, J. J. (2012). Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity. PLoS ONE 7, e47535.
37. Lozano-Durá n, R., Rosas-Díaz, T., Gusmaroli, G., Luna, A. P., Taconnat, L., Deng, X. W. & Bejarano, E. R. (2011). Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23, 1014-1032.
38. Lutz, L., Raikhy, G. & Leisner, S. M. (2012). Cauliflower mosaic virus major inclusion body protein interacts with the aphid transmission factor, the virion-associated protein, and gene VII product. Virus Res 170, 150-153.
39. Moissiard, G. & Voinnet, O. (2006). RNA silencing of host transcripts by cauliflower mosaic virus requires coordinated action of the four Arabidopsis Dicer-like proteins. Proc Natl Acad Sci U S A 103, 19593-19598.
40. Mukhtar, M. S., Nishimura, M. T. & Dangl, J. (2009). NPR1 in plant defense: it's not over 'til it's turned over. Cell 137, 804-806.
41. Palanichelvam, K. & Schoelz, J. E. (2002). A comparative analysis of the avirulence and translational transactivator functions of gene VI of Cauliflower mosaic virus. Virology 293, 225-233.
42. Palanichelvam, K., Cole, A. B., Shababi, M. & Schoelz, J. E. (2000). Agroinfiltration of Cauliflower mosaic virus gene VI elicits hypersensitive response in Nicotiana species. Mol Plant Microbe Interact 13, 1275-1279.
43. Park, H. S., Himmelbach, A., Browning, K. S., Hohn, T. & Ryabova, L. A. (2001). A plant viral "reinitiation" factor interacts with the host translational machinery. Cell 106, 723-733.
44. Pei, H., Ma, N., Chen, J., Zheng, Y., Tian, J., Li, J., Zhang, S., Fei, Z. & Gao, J. (2013). Integrative analysis of miRNA and mRNA profiles in response to ethylene in rose petals during flower opening. PLoS ONE 8, e64290.
45. Podevin, N. & du Jardin, P. (2012). Possible consequences of the overlap between the CaMV 35S promoter regions in plant transformation vectors used and the viral gene VI in transgenic plants. GM Crops Food 3, 296-300.
46. Rubio-Somoza, I. & Weigel, D. (2011). MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16, 258-264.
47. Rubio-Somoza, I., Cuperus, J. T., Weigel, D. & Carrington, J. C. (2009). Regulation and functional specialization of small RNA-target nodes during plant development. Curr Opin Plant Biol 12, 622-627.
48. Ryabova, L. A., Pooggin, M. M. & Hohn, T. (2002). Viral strategies of translation initiation: ribosomal shunt and reinitiation. Prog Nucleic Acid Res Mol Biol 72, 1-39.
49. Ryabova, L., Park, H. S. & Hohn, T. (2004). Control of translation reinitiation on the cauliflower mosaic virus (CaMV) polycistronic RNA. Biochem Soc Trans 32, 592-596.
50. Ryabova, L. A., Pooggin, M. M. & Hohn, T. (2006). Translation reinitiation and leaky scanning in plant viruses. Virus Res 119, 52-62.
51. Sansregret, R., Dufour, V., Langlois, M., Daayf, F., Dunoyer, P., Voinnet, O. & Bouarab, K. (2013). Extreme resistance as a host counter-counter defense against viral suppression of RNA silencing. PLoS Pathog 9, e1003435.
52. Schoelz, J. E. & Shepherd, R. J. (1988). Host range control of cauliflower mosaic virus. Virology 162, 30-37.
53. Schoelz, J., Shepherd, R. J. & Daubert, S. (1986). Region VI of cauliflower mosaic virus encodes a host range determinant. Mol Cell Biol 6, 2632-2637.
54. Schommer, C., Palatnik, J. F., Aggarwal, P., Ché telat, A., Cubas, P., Farmer, E. E., Nath, U. & Weigel, D. (2008). Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6, e230.
55. Schwach, F., Vaistij, F. E., Jones, L. & Baulcombe, D. C. (2005). An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138, 1842-1852.
56. Shivaprasad, P. V., Rajeswaran, R., Blevins, T., Schoelz, J., Meins, F., Jr, Hohn, T. & Pooggin, M. M. (2008). The CaMV transactivator/viroplasmin interferes with RDR6-dependent trans-acting and secondary siRNA pathways in Arabidopsis. Nucleic Acids Res 36, 5896-5909.
57. Smith, L. A. (2007). Interactions between cauliflower mosaic virus and auxin signalling. PhD Thesis, University of Glasgow, UK.
58. Stratford, R. & Covey, S. N. (1989). Segregation of cauliflower mosaic virus symptom genetic determinants. Virology 172, 451-459.
59. Tsuge, S., Kobayashi, K., Nakayashiki, H., Okuno, T. & Furusawa, I. (1994). Replication of cauliflower mosaic virus ORF 1 mutants in turnip protoplasts. Ann Phytopathological Soc Jpn 60, 27-35.
60. Vain, P., Harvey, A., Worland, B., Ross, S., Snape, J. W. & Lonsdale, D. (2004). The effect of additional virulence genes on transformation efficiency, transgene integration and expression in rice plants using the pGreen/pSoup dual binary vector system. Transgenic Res 13, 593-603.
61. Vazquez, F., Legrand, S. & Windels, D. (2010). The biosynthetic pathways and biological scopes of plant small RNAs. Trends Plant Sci 15, 337-345.
62. Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33, 949-956.
63. Volko, S. M., Boller, T. & Ausubel, F. M. (1998). Isolation of new Arabidopsis mutants with enhanced disease susceptibility to Pseudomonas syringae by direct screening. Genetics 149, 537-548.
64. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M. & Barton, G. J. (2009). Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191.
65. Wu, Y., Zhang, D., Chu, J. Y., Boyle, P., Wang, Y., Brindle, I. D., De Luca, V. & Despré s, C. (2012). The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1, 639-647.
66. Yang, J. Y., Iwasaki, M., Machida, C., Machida, Y., Zhou, X. & Chua, N. H. (2008). bC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22, 2564-2577.
67. Zhang, B., Jin, Z. & Xie, D. (2012). Global analysis of non-coding small RNAs in Arabidopsis in response to jasmonate treatment by deep sequencing technology. J Integr Plant Biol 54, 73-86.
68. Zijlstra, C. & Hohn, T. (1992). Cauliflower mosaic virus gene VI controls translation from dicistronic expression units in transgenic Arabidopsis plants. Plant Cell 4, 1471-1484.
69. Zijlstra, C., Schä rer-Herná ndez, N., Gal, S. & Hohn, T. (1996). Arabidopsis thaliana expressing the cauliflower mosaic virus ORF VI transgene has a late flowering phenotype. Virus Genes 13, 5-17.