Cauliflower mosaic virus Protein P6 Inhibits Signaling Responses to Salicylic Acid and Regulates Innate Immunity

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Love, Andrew J ^a,e   Geri, Chiara ^a,b   Laird, Janet ^a   Carr, Craig ^a   Yun, Byung Wook ^c,f   Loake, Gary J ^c   Tada, Yasuomi ^d,g   Sadanandom, Ari ^a,h   Milner, Joel J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b Institute of Agricultural Biology and Biotechnology   (Italy)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d DUKE UNIVERSITY   (United States)

^e SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^f Kyungpook National University   (South Korea)

^g KAGAWA UNIVERSITY   (Japan)

^h DURHAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

JASMONIC ACID; SALICYLIC ACID; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN P6;

ARABIDOPSIS; ARTICLE; BACTERIAL VIRULENCE; BOTRYTIS CINEREA; CAULIFLOWER MOSAIC VIRUS; CAULIFLOWER MOSAIC VIRUS INFECTION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FUNGAL VIRULENCE; GENE; GENE CONTROL; GENE EXPRESSION; GENE INACTIVATION; GENE INTERACTION; GENE REPRESSION; GENETIC LINE; GENETIC TRANSCRIPTION; INNATE IMMUNITY; INOCULATION; JA GENE; NICOTIANA BENTHAMIANA; NONHUMAN; PSEUDOMONAS SYRINGAE; RHIZOBIUM; SA GENE; SIGNAL TRANSDUCTION; TOMATO; TRANSGENIC PLANT; TRANSGENICS; TRANSIENT EXPRESSION; VIRUS INFECTION; WILD TYPE;

ANALYSIS OF VARIANCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BOTRYTIS; CYCLOPENTANES; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; IMMUNITY, INNATE; MICROSCOPY, FLUORESCENCE; OXYLIPINS; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; SALICYLIC ACID; SIGNAL TRANSDUCTION; TOBACCO; TRANS-ACTIVATORS; TRYPAN BLUE; VIRULENCE FACTORS;

EID: 84867417481     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047535     Document Type: Article

References (68)

1. Mudgett MB, (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Ann Rev Plant Biology 56: 509-531.
2. Birch PRJ, Boevink PC, Gilroy EM, Hein I, Pritchard L, et al. (2008) Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr Opin Plant Biol 11: 373-379.
3. Dodds PN, Rafiqi M, Gan PHP, Hardham AR, Jones DA, et al. (2009) Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance. New Phytologist 183: 993-999.
4. Moissiard G, Voinnet O, (2004) Viral suppression of RNA silencing in plants. Mol Plant Pathol 5: 71-82.
5. Huang ZL, Yeakley JM, Garcia EW, Holdridge JD, Fan JB, et al. (2005) Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiol 137: 1147-1159.
6. Lewsey MG, Murphy AM, MacLean D, Dalchau N, Westwood JH, et al. (2010) Disruption of Two Defensive Signaling Pathways by a Viral RNA Silencing Suppressor. Mol Plant-Microbe Interact 23: 835-845.
7. Chivasa S, Murphy AM, Naylor M, Carr JP, (1997) Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 9: 547-557.
8. Murphy AM, Carr JP, (2002) Salicylic acid has cell-specific effects on Tobacco mosaic virus replication and cell-to-cell movement. Plant Physiol 128: 552-563.
9. Mayers CN, Lee KC, Moore CA, Wong SM, Carr JP, (2005) Salicylic acid-induced resistance to Cucumber mosaic virus in squash and Arabidopsis thaliana: Contrasting mechanisms of induction and antiviral action. Mol Plant Microbe Interact 18: 428-434.
10. Love AJ, Laval V, Geri C, Laird J, Tomos AD, et al. (2007) Components of Arabidopsis defense- and ethylene-signaling pathways regulate susceptibility to Cauliflower mosaic virus by restricting long-distance movement. Mol Plant-Microbe Interact 20: 559-570.
11. Ji LH, Ding SW, (2001) The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant-Microbe Interact 14: 715-724.
12. Lewsey MG, Carr JP, (2009) Effects of DICER-like proteins 2, 3 and 4 on cucumber mosaic virus and tobacco mosaic virus infections in salicylic acid-treated plants. J Gen Virol 90: 3010-3014.
13. Haas M, Bureau M, Geldreich A, Yot P, Keller M, (2002) Cauliflower mosaic virus: still in the news. Mol Plant Pathol 3: 419-429.
14. Love AJ, Yun BW, Laval V, Loake GJ, Milner JJ, (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defence signalling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139: 935-948.
15. Roberts K, Love AJ, Laval V, Laird J, Tomos AD, et al. (2007) Long-distance movement of Cauliflower mosaic virus and host defence responses in Arabidopsis follow a predictable pattern that is determined by the leaf orthostichy. New Phytologist 175: 707-717.
16. Love AJ, Roberts K, Hooks MA, Tomos AD, Milner JJ, (2008) Exploiting Arabidopsis leaf orthistichy to dissect signalling pathways during plant-pathogen interactions. Plant Signaling & Behavior 3: 740-742.
17. Haas M, Geldreich A, Bureau M, Dupuis L, Leh W, et al. (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.
18. Ryabova LA, Pooggin MM, Hohn T, (2002) Viral strategies of translation initiation: Ribosomal shunt and reinitiation. Prog Nucl Acid Res and Mol Biol 72: 1-39.
19. Harries P, Palanichelvam K, Yu W, Schoelz J, Nelson R, (2009) The cauliflower mosaic virus protein P6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiol 149: 1005-1016.
20. Hapiak M, Li YZ, Agama K, Swade S, Okenka G, Falk J, et al. (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.
21. Hohn T, Futterer J, (1997) The proteins and functions of plant pararetroviruses: Knowns and unknowns. Crit Rev Plant Sci 16: 133-161.
22. Covey SN, McCallum DG, Turner DS, Al Kaff NS, Dale P, et al. (2000) Pararetrovirus-crucifer interactions: attack and defence or modus vivendi. Mol Plant Pathol 1: 77-86.
23. Yu WC, Murfett J, Schoelz JE, (2003) Differential induction of symptoms in Arabidopsis by P6 of Cauliflower mosaic virus. Mol Plant-Microbe Interact 16: 35-42.
24. Cawly J, Cole AB, Kiraly L, Qiu WP, Schoelz JE, (2005) The plant gene CCD1 selectively blocks cell death during the hypersensitive response to cauliflower mosaic virus infection. Mol Plant-Microbe Interact 18: 212-219.
25. Palanichelvam K, Schoelz JE, (2002) A comparative analysis of the avirulence and translational transactivator functions of gene VI of Cauliflower mosaic virus. Virology 293: 225-233.
26. Love AJ, Laird J, Holt J, Hamilton AJ, Sadanandom A, et al. (2007) Cauliflower mosaic virus protein P6 is a suppressor of RNA silencing. J Gen Virol 88: 3439-3444.
27. Haas G, Azevedo J, Moissiard G, Geldreich A, Himber C, et al. (2008) Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J 27: 2102-2112.
28. Cecchini E, Gong ZH, Geri C, Covey SN, Milner JJ, (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.
29. Geri C, Love AJ, Cecchini E, Barrett SJ, Laird J, et al. (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.
30. Smith LA (2007) Interactions between Cauliflower mosaic virus and auxin signalling. PhD Thesis, University of Glasgow.
31. Volko SM, Boller T, Ausubel FM, (1998) Isolation of new Arabidopsis mutants with enhanced disease susceptibility to Pseudomonas syringae by direct screening. Genetics 149: 537-548.
32. Laird J, Armengaud P, Giuntini P, Laval V, Milner JJ, (2004) Inappropriate annotation of a key defence marker in Arabidopsis: will the real PR-1 please stand up? Planta 219: 1089-1092.
33. Pitzschke A, Schikora A, Hirt H, (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12: 421-426.
34. Dean JD, Goodwin PH, Hsiang T, (2005) Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot 56: 1525-1533.
35. Park HS, Himmelbach A, Browning KS, Hohn T, Ryabova LA, (2001) A plant viral "reinitiation" factor interacts with the host translational machinery. Cell 106: 723-733.
36. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34-41.
37. Beckers GJM, Spoel SH, (2006) Fine-tuning plant defence signalling: Salicylate versus jasmonate. Plant Biology 8: 1-10.
38. Endres MW, Gregory BD, Gao ZH, Foreman AW, Mlotshwa S, et al. (2010) Two Plant Viral Suppressors of Silencing Require the Ethylene-Inducible Host Transcription Factor RAV2 to Block RNA Silencing. Plos Pathogens 6(1): e1000729 doi:10.1371/journal.ppat.1000729.
39. Truman W, de Zabala MT, Grant M, (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 46: 14-33.
40. Wildermuth MC, Dewdney J, Wu G, Ausubel FM, (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565.
41. Dong XN, (2004) NPR1, all things considered. Curr Opin Plant Biol 7: 547-552.
42. Pieterse CM, Van Loon L, (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7: 456-464.
43. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, et al. (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15: 760-770.
44. Clarke JD, Volko SM, Ledford H, Ausubel FM, Dong XN, (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12: 2175-2190.
45. Mukhtar M, Nishimura M, Dangl J, (2009) NPR1 in plant defense: it's not over 'til it's turned over. Cell 137: 804-806.
46. Mou Z, Fan WH, Dong XN, (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935-944.
47. Boch J, Verbsky ML, Robertson TL, Larkin JC, Kunkel BN, (1998) Analysis of resistance gene-mediated defense responses in Arabidopsis thaliana plants carrying a mutation in CPR5. Mol Plant-Microbe Interact 11: 1196-1206.
48. Lozano-Duran R, Rosas-Diaz T, Gusmaroli G, Luna AP, Taconnat L, et al. (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.
49. Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, et al. (2008) beta C1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes & Development 22: 2564-2577.
50. Ziebell H, Murphy AM, Groen SC, Tungadi T, Westwood JH, et al. (2011) Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco. Scientific Reports 1.
51. 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.
52. 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.
53. Jones JDG, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
54. Shivaprasad PV, Rajeswaran R, Blevins T, Schoelz J, Meins F, et al. (2008) The CaMV transactivator/viroplasmin interferes with RDR6-dependent trans-acting and secondary siRNA pathways in Arabidopsis. Nucleic Acids Res 36: 5896-5909.
55. 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: 19953-19958.
56. Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, et al. (2006) Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34: 6233-6246.
57. Yu DQ, Fan BF, MacFarlane SA, Chen ZX, (2003) Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant-Microbe Interact 16: 206-216.
58. Diaz-Pendon JA, Li F, Li WX, Ding SW, (2007) Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19: 2053-2063.
59. Wang X, Wu Q, Ito T, Cillo F, Li W, et al. (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107: 484-489.
60. Spoel S, Mou Z, Tada Y, Spivey N, Genschik P, et al. (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137: 860-872.
61. Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou ZL, Song JQ, et al. (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321: 952-956.
62. Zhang X, Chen S, X, Mou Z, (2010) Nuclear localization of NPR1 is required for regulation of salicylate tolerance, isochorismate synthase 1 expression and salicylate accumulation in Arabidopsis. J Plant Physiol 167: 144-148.
63. Vlot AC, Dempsey DA, Klessig DF, (2009) Salicylic Acid, a Multifaceted Hormone to Combat Disease. Annu Rev Phytopathol 47: 177-206.
64. Cecchini E, Al Kaff NS, Bannister A, Giannakou ME, McCallum DG, et al. (1998) Pathogenic interactions between variants of cauliflower mosaic virus and Arabidopsis thaliana. J Exp Bot 49: 731-737.
65. Grant JJ, Yun BW, Loake GJ, (2000) Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J 24: 569-582.
66. Glazebrook J, Weigel D (2002) Arabidopsis: A laboratory manual. In: Glazebrook J, Weigel D, editors. Cold Spring Harbor NY: Cold Spring Harbor Press. 86.
67. Grant JJ, Chini A, Basu D, Loake GJ, (2003) Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol Plant-Microbe Interact 16: 669-680.
68. Bazzini AA, Mongelli VC, Hopp HE, del Vas M, Asurmendi S, (2007) A practical approach to the understanding and teaching of RNA silencing in plants. Electronic J Biotechnology 10: 178-190.