Salicylic acid-dependent restriction of tomato ringspot virus spread in tobacco is accompanied by a hypersensitive response, local RNA silencing, and moderate systemic resistance

Molecular Plant-Microbe Interactions

Volumn 24, Issue 6, 2011, Pages 706-718

  Jovel, Juan ^a,b   Walker, Melanie ^a   Sanfaçon, Hélène ^a  

^a SUMMERLAND RESEARCH AND DEVELOPMENT CENTRE   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SALICYLIC ACID; SMALL INTERFERING RNA; VEGETABLE PROTEIN;

ARTICLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT VIRUS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TEMPERATURE; TOBACCO; VIROLOGY;

GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PLANT VIRUSES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SALICYLIC ACID; SIGNAL TRANSDUCTION; TEMPERATURE; TOBACCO;

NEPOVIRUS; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; TOBACCO MOSAIC VIRUS; TOMATO RINGSPOT VIRUS;

EID: 79955735551     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-09-10-0224     Document Type: Article

References (82)

1. Alamillo, J. M., Saenz, P., and Garcia, J. A. 2006. Salicylic acid-mediated and RNA-silencing defense mechanisms cooperate in the restriction of systemic spread of Plum pox virus in tobacco. Plant J. 48:217-227. (Pubitemid 44484863)
2. 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.
3. Anandalakshmi, R., Marathe, R., Ge, X., Herr, J. M., Jr., Mau, C., Mallory, A., Pruss, G., Bowman, L., and Vance, V. B. 2000. A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290:142-144.
4. Atsumi, G., Kagaya, U., Kitazawa, H., Nakahara, K. S., and Uyeda, I. 2009. Activation of the salicylic acid signaling pathway enhances Clover yellow vein virus virulence in susceptible pea cultivars. Mol. PlantMicrobe Interact. 22:166-175.
5. Beffa, R. S., Hofer, R. M., Thomas, M., and Meins, F., Jr. 1996. Decreased susceptibility to viral disease of [beta]-1,3-glucanase-deficient plants generated by antisense transformation. Plant Cell 8:1001-1011.
6. Bhattacharjee, S., Zamora, A., Azhar, M. T., Sacco, M. A., Lambert, L. H., and Moffett, P. 2009. Virus resistance induced by NB-LRR proteins involves Argonaute4-dependent translational control. Plant J. 58:940-951.
7. 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 viral systemic movement in Arabidopsis. J. Virol. 84:7793-7802.
8. Carr, J. P., Lewsey, M. G., and Palukaitis, P. 2010. Signaling in induced resistance. Adv. Virus Res. 76:57-121.
9. Cawly, J., Cole, A. B., Kiraly, L., Qiu, W., and Schoelz, J. E. 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. (Pubitemid 40263616)
10. Chandra-Shekara, A. C., Navarre, D., Kachroo, A., Kang, H. G., Klessig, D., and Kachroo, P. 2004. Signaling requirements and role of salicylic acid in HRT- and rrt-mediated resistance to Turnip crinkle virus in Arabidopsis. Plant J. 40:647-659. (Pubitemid 39623240)
11. Cole, A. B., Kiraly, L., Ross, K., and Schoelz, J. E. 2001. Uncoupling resistance from cell death in the hypersensitive response of Nicotiana species to Cauliflower mosaic virus infection. Mol. Plant-Microbe Interact. 14:31-41. (Pubitemid 32062625)
12. Collmer, C. W., Marston, M. F., Taylor, J. C., and Jahn, M. 2000. The I gene of bean: A dosage-dependent allele conferring extreme resistance, hypersensitive resistance, or spreading vascular necrosis in response to the potyvirus Bean common mosaic virus. Mol. Plant-Microbe Interact. 13:1266-1270.
13. Diaz-Pendon, 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.
14. Ding, S. W. 2010. RNA-based antiviral immunity. Nat. Rev. Immunol. 10:632-644.
15. Dunoyer, P., Brosnan, C.A., Schott, G., Wang, Y., Jay, F., Alioua, A., Himber, C., and Voinnet, O. 2010a. An endogenous, systemic RNAi pathway in plants. EMBO (Eur. Mol. Biol. Organ.) J. 29:1699-1712.
16. Dunoyer, P., Schott, G., Himber, C., Meyer, D., Takeda, A., Carrington, J. C., and Voinnet, O. 2010b. Small RNA duplexes function as mobile silencing signals between plant cells. Science 328:912-916.
17. 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. Published online.
18. Forouhar, F., Yang, Y., Kumar, D., Chen, Y., Fridman, E., Park, S. W., Chiang, Y., Acton, T. B., Montelione, G. T., Pichersky, E., Klessig, D. F., and Tong, L. 2005. Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc. Natl. Acad. Sci. U.S.A. 102:1773-1778. (Pubitemid 40209243)
19. Friedrich, L., Vernooij, B., Gaffney, T., Morse, A., and Ryals, J. 1995. Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol. Biol. 29:959-968. (Pubitemid 3020807)
20. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754-756. (Pubitemid 23278389)
21. Garcia-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.
22. He, X. F., Fang, Y. Y., Feng, L., and Guo, H. S. 2008. Characterization of conserved and novel microRNAs and their targets, including a TuMV- induced TIR-NBS-LRR class R gene-derived novel miRNA in Brassica. FEBS (Fed. Eur. Biochem. Soc.) Lett. 582:2445-2452.
23. Hirai, K., Kubota, K., Mochizuki, T., Tsuda, S., and Meshi, T. 2008. Antiviral RNA silencing is restricted to the marginal region of the dark green tissue in the mosaic leaves of Tomato mosaic virus-infected tobacco plants. J. Virol. 82:3250-3260. (Pubitemid 351429904)
24. Holmes, F. O. 1938. Inheritance of resistance to tobacco-mosaic disease in tobacco. Phytopathology 28:553-561.
25. Huang, Z., Yeakley, J. M., Garcia, E. W., Holdridge, J. D., Fan, J. B., and Whitham, S. A. 2005. Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiol. 137:1147-1159. (Pubitemid 43138184)
26. Jafarpour, B., and Sanfacon, H. 2009. Insertion of large amino acid repeats and point mutations contribute to a high degree of sequence diversity in the X4 protein of tomato ringspot virus (genus Nepovirus). Arch. Virol. 154:1713-1717.
27. Ji, L. H., and Ding, S. W. 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.
28. Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. (Pubitemid 44764102)
29. Jovel, J., Walker, M., and Sanfacon, H. 2007. Recovery of Nicotiana benthamiana plants from a necrotic response induced by a Nepovirus is associated with RNA silencing but not with reduced virus titer. J. Virol. 81:12285-12297. (Pubitemid 350085843)
30. Kachroo, P., Yoshioka, K., Shah, J., Dooner, H. K., and Klessig, D. F. 2000. Resistance to Turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. Plant Cell 12:677-690. (Pubitemid 30343581)
31. Kachroo, P., Chandra-Shekara, A. C., and Klessig, D. F. 2006. Plant signal transduction and defense against viral pathogens. Adv. Virus Res. 66:161-191. (Pubitemid 44107833)
32. Katiyar-Agarwal, S., and Jin, H. 2010. Role of small RNAs in host-microbe interactions. Annu. Rev. Phytopathol. 48:225-246.
33. Kiraly, L., Hafez, Y. M., Fodor, J., and Kiraly, Z. 2008. Suppression of Tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. J. Gen. Virol. 89:799-808.
34. Komatsu, K., Hashimoto, M., Ozeki, J., Yamaji, Y., Maejima, K., Senshu, H., Himeno, M., Okano, Y., Kagiwada, S., and Namba, S. 2010. Viralinduced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol. Plant-Microbe Interact. 23:283-293.
35. Lewsey, M. G., and Carr, J. P. 2009. The 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.
36. Lewsey, M. G., Murphy, A. M., Maclean, D., Dalchau, N., Westwood, J.H., Macaulay, K., Bennett, M. H., Moulin, M., Hanke, D. E., Powell, G., Smith, A. G., and Carr, J. P. 2010. Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol. Plant-Microbe Interact. 23:835-845.
37. Liu, P.-P., Bhattacharjee, S., Klessig, D., and Moffett, P. 2010a. Systemic acquired resistance is induced by R gene-mediated responses independent of cell death. Mol. Plant Pathol. 11:155-160.
38. Liu, P. P., Yang, Y., Pichersky, E., and Klessig, D. F. 2010b. Altering expression of benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in Arabidopsis. Mol. Plant-Microbe Interact. 23:82-90.
39. Love, A. J., Yun, B. W., Laval, V., Loake, G. J., and 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. (Pubitemid 43907118)
40. Malamy, J., Hennig, J., and Klessig, D. F. 1992. Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4:359-366.
41. Mas, P., and Pallas, V. 1996. Long-distance movement of cherry leaf roll virus in infected tobacco plants. J. Gen. Virol. 77:531-540. (Pubitemid 26073361)
42. Maule, A. J., Caranta, C., and Boulton, M. I. 2007. Sources of natural resistance to plant viruses: Status and prospects. Mol. Plant Pathol. 8:223-231.
43. Mishina, T. E., and Zeier, J. 2007. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50:500-513. (Pubitemid 46634490)
44. Mlotshwa, S., Pruss, G. J., and Vance, V. 2008. Small RNAs in viral infection and host defense. Trends Plant Sci. 13:375-382.
45. Moffett, P. 2009. Mechanisms of recognition in dominant R gene mediated resistance. Adv. Virus Res. 75:1-33.
46. Moissiard, G., and 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. (Pubitemid 46026075)
47. Molnar, A., Melnyk, C.W., Bassett, A., Hardcastle, T. J., Dunn, R., and Baulcombe, D. C. 2010. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872-875.
48. Mur, L. A. J., Kenton, P., Lloyd, A. J., Ougham, H., and Prats, E. 2008. The hypersensitive response; the centenary is upon us but how much do we know? J. Exp. Bot. 59:501-520. (Pubitemid 351640730)
49. Murphy, A. M., Chivasa, S., Singh, D. P., and Carr, J. P. 1999. Salicylic acid-induced resistance to viruses and other pathogens: A parting of the ways? Trends Plant Sci. 4:155-160. (Pubitemid 29178031)
50. Naylor, M., Murphy, A. M., Berry, J. O., and Carr, J. P. 1998. Salicylic acid can induce resistance in plant virus movement. Mol. Plant-Microbe Interact. 11:860-868. (Pubitemid 28398224)
51. Oparka, K. J., and Cruz, S. S. 2000. The Great Escape: Phloem transport and unloading of macromolecules1. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:323-347.
52. Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., and Klessig, D. F. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113-116. (Pubitemid 47538045)
53. Pruss, G. J., Lawrence, C. B., Bass, T., Li, Q. Q., Bowman, L. H., and Vance, V. 2004. The potyviral suppressor of RNA silencing confers enhanced resistance to multiple pathogens. Virology 320:107-120. (Pubitemid 38296718)
54. Rakhshandehroo, F., Takeshita, M., Squires, J., and Palukaitis, P. 2009. The influence of RNA-dependent RNA polymerase 1 on Potato virus Y infection and on other antiviral response genes. Mol. Plant-Microbe Interact. 22:1312-1318.
55. Ratcliff, F., Harrison, B. D., and Baulcombe, D. C. 1997. A similarity between viral defense and gene silencing in plants. Science 276:1558-1560. (Pubitemid 27255318)
56. Rochon, D., and Sanfacon, H. 2001. Nepoviruses. Pages 704-708 in: Encyclopedia of Plant Pathology. O. C. Maloy and T. D. Murray, eds. John Wiley & Sons, Inc., New York.
57. Ross, A. F. 1961. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340-358.
58. Ruiz-Ferrer, V., and Voinnet, O. 2009. Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60:485-510.
59. Schwach, F., Vaistij, F. E., Jones, L., and 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. (Pubitemid 43733532)
60. Shams-Bakhsh, M., Canto, T., and Palukaitis, P. 2007. Enhanced resistance and neutralization of defense responses by suppressors of RNA silencing. Virus Res. 130:103-109. (Pubitemid 350064321)
61. Siddiqui, S. A., Sarmiento, C., Kiisma, M., Koivumaki, S., Lemmetty, A., Truve, E., and Lehto, K. 2008. Effects of viral silencing suppressors on Tobacco ringspot virus infection in two Nicotiana species. J. Gen. Virol. 89:1502-1508.
62. Singh, D. P., Moore, C. A., Gilliland, A., and Carr, J. P. 2004. Activation of multiple antiviral defence mechanisms by salicylic acid. Mol. Plant Pathol. 5:57-63. (Pubitemid 38171209)
63. Szittya, G., Silhavy, D., Molnar, A., Havelda, Z., Lovas, A., Lakatos, L., Banfalvi, Z., and Burgyan, J. 2003. Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO (Eur. Mol. Biol. Organ.) J. 22:633-640. (Pubitemid 36193607)
64. Tsuda, K., Sato, M., Glazebrook, J., Cohen, J. D., and Katagiri, F. 2008. Interplay between MAMP-triggered and SA-mediated defense responses. Plant J. 53:763-775. (Pubitemid 351495865)
65. Varallyay, E., Valoczi, A., Agyi, A., Burgyan, J., and Havelda, Z. 2010. Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO (Eur. Mol. Biol. Organ.) J. 29:3507-3519.
66. Vlot, A. C., Liu, P. P., Cameron, R. K., Park, S. W., Yang, Y., Kumar, D., Zhou, F., Padukkavidana, T., Gustafsson, C., Pichersky, E., and Klessig, D. F. 2008. Identification of likely orthologs of tobacco salicylic acidbinding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J. 56:445-456.
67. Vlot, A. C., Dempsey, D. A., and Klessig, D. F. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177-206.
68. Wang, A., and Sanfacon, H. 2000. Diversity in the coding regions for the coat protein, VPg, protease and putative RNA-dependent RNA polymerase among tomato ringspot Nepovirus isolates. Can. J. Plant Pathol. 22:145-149.
69. Wang, K., Uppalapati, S. R., Zhu, X., Dinesh-Kumar, S. P., and Mysore, K. S. 2010a. SGT1 positively regulates the process of plant cell death during both compatible and incompatible plant-pathogen interactions. Mol. Plant Pathol. 11:597-611.
70. Wang, X., Goregaoker, S. P., and Culver, J. N. 2009a. Interaction of the Tobacco mosaic virus replicase protein with a Nac domain transcription factor is associated with the suppression of systemic host defenses. J. Virol. 83:9720-9730.
71. Wang, X. B., Wu, Q., Ito, T., Cillo, F., Li, W. X., Chen, X., Yu, J. L., and Ding, S. W. 2010b. RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 107:484-489.
72. Wang, Y., Bao, Z., Zhu, Y., and Hua, J. 2009b. Analysis of temperature modulation of plant defense against biotrophic microbes. Mol. Plant-Microbe Interact. 22:498-506.
73. Ward, E. R., Uknes, S. J., Williams, S. C., Dincher, S. S., Wiederhold, D. L., Alexander, D. C., Ahl-Goy, P., Metraux, J. P., and Ryals, J. A. 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085-1094. (Pubitemid 21913656)
74. Wingard, S. A. 1928. Hosts and symptoms of ring spot, a virus disease of plants. J. Agric. Res. 37:127-153.
75. Xie, Z., Fan, B., Chen, C., and Chen, Z. 2001. An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc. Natl. Acad. Sci. U.S.A. 98:6516-6521. (Pubitemid 32488269)
76. Xu, P., Blancaflor, E. B., and Roossinck, M. J. 2003. In spite of induced multiple defense responses, tomato plants infected with Cucumber mosaic virus and D satellite RNA succumb to systemic necrosis. Mol. Plant-Microbe Interact. 16:467-476. (Pubitemid 36610719)
77. Yalpani, N., Shulaev, V., and Raskin, I. 1993. Endogenous salicylic acid levels correlate with accumulation of pathogenesis-related proteins and virus resistance in tobacco. Phytopathology 83:702-708.
78. Yang, S. J., Carter, S. A., Cole, A. B., Cheng, N. H., and Nelson, R. S. 2004. A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc. Natl. Acad. Sci. U.S.A. 101:6297-6302. (Pubitemid 38520568)
79. Yi, H., and Richards, E. J. 2007. A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19:2929-2939. (Pubitemid 350046238)
80. Ying, X. B., Dong, L., Zhu, H., Duan, C. G., Du, Q. S., Lv, D. Q., Fang, Y. Y., Garcia, J. A., Fang, R. X., and Guo, H. S. 2010. RNA-dependent RNA polymerase 1 from Nicotiana tabacum suppresses RNA silencing and enhances viral infection in Nicotiana benthamiana. Plant Cell 22:1358-1372.
81. Yu, D., Fan, B., MacFarlane, S. A., and Chen, Z. 2003. Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol. Plant-Microbe Interact. 16:206-216. (Pubitemid 36229936)
82. Zhu, Y., Qian, W., and Hua, J. 2010. Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 6:e1000844. Published online.