Mechanisms Involved in Induced Resistance to Plant Viruses

  • Androulla Gilliland
  • Alex M. Murphy
  • Chui Eng Wong
  • Rachael A. J. Carson
  • John P. Carr


Salicylic Acid Hypersensitive Response Tobacco Mosaic Virus Cucumber Mosaic Virus Plant Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abbink, T.E.M., Tjernberg, P.A., Bol, J.F., and Linthorst, H.J.M. 1998. Tobacco mosaic virus helicase domain induces necrosis in N gene-carrying tobacco in the absence of virus replication. Mol. Plant Microbe Interact. 11:1242–1246.Google Scholar
  2. Affourtit, C., Albury, M.S.W., Crichton, P.G., and Moore, A.L. 2002. Exploring the molecular nature of alternative oxidase regulation and catalysis. FEBS Lett. 510:121–126.PubMedGoogle Scholar
  3. Ahlquist, P. 2002. RNA-dependent RNA polymerases, viruses, and RNA silencing. Science 296:1270–1273.PubMedGoogle Scholar
  4. Alexander, D., Goodman, R.M., Gutrella, M., Glascock, C., Weymann, K., Friedrich, L., Maddox, D., Ahl-Goy, P., Luntz, T., Ward, E., and Ryals, J. 1993. Increased tolerance to 2 oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein-1a. Proc. Natl. Acad. Sci. USA 90:7327–7331.PubMedGoogle Scholar
  5. Baulcombe, D.C. 2001. Diced defence: RNA silencing. Nature 409:295–296.PubMedGoogle Scholar
  6. Béclin, C., Berthomé, R., Palauqui, J.C., Tepfer, M., and Vaucheret, H. 1998. Infection of tobacco or Arabidopsis plants by CMV counteracts systemic post-transcriptional silencing of nonviral (trans)genes. Virology 252:313–317.PubMedGoogle Scholar
  7. Bendahmane, A., Kahm, B.A., Dedi, C., and Baulcombe, D.C. 1995. The coat protein of potato virus X is a strain specific elicitor of Rx1-mediated virus resistance in potato. Plant J. 8:933–941.PubMedGoogle Scholar
  8. Bergelson, J., Kreitman, M., Stahl, E.A., and Tian, D. 2001. Evolutionary dynamics of plant R-genes. Science 292:2281–2285.PubMedGoogle Scholar
  9. Bergstrom, G.C., Johnson, M.C., and Kuć, J. 1982. Effects of local infection of cucumber by Colletotrichum lagenarium, Pseudomonas lachrymans or tobacco necrosis virus on systemic resistance to cucumber mosaic virus. Phytopathology 72:922–925.Google Scholar
  10. Bernstein, E., Caudy, A.A., Hammond, S.M., and Hannon, G.J. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366.PubMedGoogle Scholar
  11. Bi, Y., Kenton, P., Mur, L., Darby, R., and Draper, J. 1995. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J 8:235–245.PubMedGoogle Scholar
  12. Birch, P.R.J., Avrova, A.O., Dellagi, A., Lacomme, C., Santa Cruz, S., and Lyon, G.D. 2000. Programmed cell death in plants in response to pathogen attack. In Molecular Plant Pathology, eds. M. Dickinson, and J. Beynon, Vol. 4, pp. 175–197. Sheffield, UK: CRC Press.Google Scholar
  13. Bowler, C., and Fluhr, R. 2000. The role of calcium and activated oxygen as signals for controlling cross-tolerance. Trends Plant Sci. 5:241–246.PubMedGoogle Scholar
  14. Brigneti, G., Voinnet, O., Li, W.X., Ji, L.-H., Ding, S.W., and Baulcombe, D.C. 1998. Viral pathogenicity determinants are supressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17:6739–6746.PubMedGoogle Scholar
  15. Bucher, G.L., Tarina, C., Heinlein, M., Di Serio, F., Meins, F. Jr, Iglesias, V.A. 2001. Local expression of enzymatically active class I beta-1, 3-glucanase enhances symptoms of TMV infection in tobacco. Plant J. 28:361–369.PubMedGoogle Scholar
  16. Buck, K.W. 1996. Comparison of the replication of positive stranded RNA viruses of plant and animals. Adv. Virus Res. 47:159–251.PubMedGoogle Scholar
  17. Cao, H., Bowling, S.A., Gordon, A.S., and Dong, X.N. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592.PubMedGoogle Scholar
  18. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S., and Dong, X.N. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63.PubMedGoogle Scholar
  19. Carrington, J.C. 1999. Reinventing plant virus movement. Trends Microbiol. 8:312–313.Google Scholar
  20. Carson, R.A.J. 1999. The effects of salicylic acid on the responses of plants to heat stress and virus infection. PhD thesis, University of Cambridge.Google Scholar
  21. Chivasa, S., and Carr, J.P. 1998. Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase. Plant Cell 10:1489–1498.PubMedGoogle Scholar
  22. Chivasa, S., Murphy, A.M., Naylor, M., and Carr, J.P. 1997. Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 9:547–557.PubMedGoogle Scholar
  23. Chong, J., Baltz, R., Schmitt, C., Beffa, R., Fritig, B., and Saindrenan, P. 2002. Downregulation of a pathogen-responsive tobacco UDP-Glc: phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. Plant Cell 14:1093–1107.PubMedGoogle Scholar
  24. Citovsky, V., Ghoshroy, S., Tsui, F., and Klessig, D.F. 1998. Non-toxic concentrations of cadmium inhibit systemic movement of turnip vein clearing virus by a salicylic acid-independent mechanism Plant J. 16:13–20.PubMedGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. Cooley, M.B., Pathirana, S., Wu, H.J., Kachroo, P., and Klessig, D.F. 2000. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12:663–676.PubMedGoogle Scholar
  27. Covey, S.N., Al-Kaff, N.S., Langara, A., and Turner, D.S. 1997. Plants combat infection by gene silencing. Nature 385:781–782.Google Scholar
  28. Culver J.N., and Dawson, W.O. 1989. Tobacco mosaic virus coat protein-an elicitor of the hypersensitive reaction but not required for the development of mosaic symptoms in Nicotiana sylvestris. Virology 173:755–758.PubMedGoogle Scholar
  29. Culver, J.N., Stubbs, G., and Dawson W.O. 1994. Structure-function relationship between tobacco mosaic-virus coat protein and hypersensitivity in Nicotiana sylvestris. J. Mol. Biol. 242:130–138.PubMedGoogle Scholar
  30. Cutt, J.R., Harpster, M.H., Dixon, D.C., Carr, J.P., Dunsmuir, P., and Klessig, D.F. 1989. Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related PR1b gene. Virology 173:89–97.PubMedGoogle Scholar
  31. Dangl, J.L., and Jones, J.D.G. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826–833.PubMedGoogle Scholar
  32. Dangl, J.L., Dietrich, R.A., and Richberg, M.H. 1996. Death don’t have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8:1793–1807.PubMedGoogle Scholar
  33. Darby, R.M., Maddison, A., Mur, L.A.J., Bi, Y.M., and Draper, J. 2000. Cell-specific expression of salicylate hydroxylase in an attempt to separate localized HR and systemic signalling establishing SAR in tobacco. Mol. Plant Pathol. 1:115–123.Google Scholar
  34. Delaney, T.P., Friedrich, L., and Ryals, J.A. 1995. Arabidopsis signal-transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl Acad. Sci. USA 92:6602–6606.PubMedGoogle Scholar
  35. Delaney, T.P., Ukness, S., Vernoij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247–1250.Google Scholar
  36. Dempsey, D.A., Shah, J., and Klessig, D.F. 1999. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18:547–575.Google Scholar
  37. Dietrich, R.A. 2000. Emerging technologies and their application in the study of host-pathogen interactions. In (eds.), Molecular Plant Pathology, eds. M. Dickinson, and J. Beynon, Vol. 4. pp. 253–286. Sheffield, UK: CRC Press.Google Scholar
  38. Dinesh-Kumar, S.P., Whitham, S., Choi, D., Hehl, R., Corr, C., and Baker, B. 1995. Transposon tagging of tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway. Proc. Natl Acad. Sci. USA 92:4175–4180.PubMedGoogle Scholar
  39. Di Serio, F., Schöb, H., Iglesias, A., Tarina, C., Bouldoires, E., and Meins, J., F. 2001. Sense-and antisense-mediated gene silencing in tobacco is inhibited by the same viral suppressors and is associated with accumulation of small RNAs. Proc. Natl Acad. Sci. USA 98:6506–6510.PubMedGoogle Scholar
  40. Dixon, R.A. 2001. Natural products and plant disease resistance. Nature 411:843–847.PubMedGoogle Scholar
  41. Erickson, F.L., Holzberg, S., Calderon-Urrea, A., Handley, V., Axtell, M., Corr, C., and Baker, B. 1999. The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. Plant J. 18:67–75.PubMedGoogle Scholar
  42. Fitchen J.H., and Beachy R.N. 1993. Genetically-engineered protection against viruses in transgenic plants. Annu. Rev. Microbiol. 47:739–763.PubMedGoogle Scholar
  43. Flor, H.H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopath. 9:275–296.Google Scholar
  44. Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Gut-Rella, M., Meier, B., Dincher, S., Staub, T., Uknes, S., Métraux, J.P., Kessmann, H., and Ryals, J. 1996. A benzothiadiazole derivative induces systemic acquired resistnce in tobacco. Plant J. 10:60–70.Google Scholar
  45. Gaffney, T., Friedrich, L., Vernoij, B., Negrotto, D., Nye, G., Ukness, S., Ward, E., Kessmann, H., and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756.Google Scholar
  46. Genoud, T., and Métraux, J.P. 1999. Crosstalk in plant cell signalling: structure and function of the genetic network. Trends Plant Sci. 4:503–507.PubMedGoogle Scholar
  47. Ghoshroy, S., Freedman, K., Lartey, R., and Citovsky, V. 1998. Inhibition of plant viral systemic infection by non-toxic concentrations of cadmium. Plant J. 13:591–602.PubMedGoogle Scholar
  48. Gilchrist, D.G. 1998. Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu. Rev. Phytopathol. 36:393–414.PubMedGoogle Scholar
  49. Gilliland, A., Singh, D.P., Hayward, J.M., Moore, C.A., Murphy, A.M., York, C.J., Slator, J., and Carr, J.P. 2003. Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus. Plant Physiol. 132:1518–1528.PubMedGoogle Scholar
  50. Glazebrook, J., Rogers, E.E., and Ausubel, F.M. 1996. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143:973–982.PubMedGoogle Scholar
  51. Goodman, R.N., and Novacky, A.J. 1994. The Hypersensitive Reaction in Plants to Pathogens. A Resistance Phenomenon. St.Paul, MN: APS Press.Google Scholar
  52. Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Oostendorp, M., Staub, T., Ward, E., Kessman, H., and Ryals, J. 1996. Benzothiadiazole, a novel class of inducers of systemic acquire resistance, activates genes expression and disease resistance in wheat. Plant Cell 8:629–643.PubMedGoogle Scholar
  53. Grant, S.R. 1999. Dissecting the mechanism of posttranscriptional gene silencing: divide and conquer. Cell 96:303–306.PubMedGoogle Scholar
  54. Guo, H.S., and Ding, S.W. 2002. A viral protein inhibits the long range signalling activity of the gene silencing signal. EMBO J. 21:398–407.PubMedGoogle Scholar
  55. Hamilton, A.J., and Baulcombe, D.C. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952.PubMedGoogle Scholar
  56. Hammerschmidt, R. 1999. Phytoalexins: What have we learned after 60 years? Annu. Rev. Phytopathol. 37:285–306.PubMedGoogle Scholar
  57. Hammond-Kosack, K.E., and Jones, J.D.G. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791.PubMedGoogle Scholar
  58. Hanley-Bowdoin, L., Settlage, S.B., Orozco, B.M., Nagar, S., and Robertson, D. 1999. Geminiviruses: Models for plant DNA replication, transcription, and cell cycle regulation Crit. Rev. Plant Sci. 18:71–106.Google Scholar
  59. Heath, M.C. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44:321–334.PubMedGoogle Scholar
  60. Heinlein, M. 2002. The spread of Tobacco Mosaic Virus infection: insights into the cellular mechanism of RNA transport. Cell. Mol. Life Sci. 59:58–82.PubMedGoogle Scholar
  61. Hohn, T., and Futterer, J. 1997. The proteins and functions of plant pararetroviruses: knowns and unknowns. Crit. Rev. Plant Sci. 16:133–161.Google Scholar
  62. Hooft van Huijsduijnen, R.A.M., Alblas, S.W., DeRijk, R. H., and Bol, J. F. 1986. Induction by salicylic acid of pathogenesis-related proteins and resistance to alfalfa mosaic virus in various plant species. J. Gen. Virol. 67:2135–2143.Google Scholar
  63. Hull, R. 2002. Matthews’ Plant Virology. Fourth Edition. London: Academic Press.Google Scholar
  64. Jakab, G., Cottier, V., Toquin, V., Rigoli, G., Zimmerli, L., Métraux, J.P., and Mauch-Mani, B. 2001. β-Aminobutyric acid-induced resistance in plants. Eur. J. Plant Pathol. 107:29–37.Google Scholar
  65. 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. 6:715–724.Google Scholar
  66. Jones, D.A. 2000. Resistance genes and resistance protein function. In Molecular Plant Pathology, eds. M. Dickinson, and J. Beynon, Vol. 4, pp. 108–143. Sheffield, UK: CRC Press.Google Scholar
  67. 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.PubMedGoogle Scholar
  68. Kessmann, H., Staub, T., Hoffmann, C., Maetzke, T., Herzog, J., Ward, E., Uknes, S., and Ryals, J. 1994. Induction of systemic acquired resistance in plants by chemicals. Ann Rev. Phytopathol. 32:439–459.Google Scholar
  69. Kim, C.H., and Palukaitis, P. 1997. The plant defense response to cucumber mosaic virus in cowpea is elicited by the viral polymerase gene and affects virus accumulation in single cells. EMBO J. 16:4060–4068.PubMedGoogle Scholar
  70. Kombrink, E., and Schmelzer, E. 2001. The hypersensitive response and its role in local and systemic disease resistance. Eur J. Plant Pathol. 107:69–78.Google Scholar
  71. Kuć, J. 1995. Phytoalexins, stress metabolism, and disease resistance in plants. Ann. Rev. Phytopathol. 33:275–297.Google Scholar
  72. Kuć, J. 2001. Concepts and direction of induced systemic resistance in plants and its application. Eur. J. Plant Pathol. 107:7–12.Google Scholar
  73. Lacomme, C., and Roby, D. 1999. Identification of new early markers of the hypersensitive response in Arabidopsis thaliana. FEBS Lett. 459:149–153.PubMedGoogle Scholar
  74. Lacomme, C., and Santa Cruz, S. 1999. Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc. Natl. Acad. Sci. USA 96:7956–7961.PubMedGoogle Scholar
  75. Lam, E., and del Pozo, O. 2000. Caspase-like involvement in the control of plant cell death. Plant Mol. Biol. 44:417–428.PubMedGoogle Scholar
  76. Laties, G.G. 1982. The cyanide-resistant, alternative path in plant mitochondria. Annu. Rev. Plant Physiol. 33:519–555.Google Scholar
  77. Lawton, K.A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., Staub, T., and Ryals, J. 1996. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10:71–82.PubMedGoogle Scholar
  78. Lebel, E., Heifetz, P., Thorne, L., Uknes, S., Ryals, J., and Ward, E. 1998. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J. 16:223–233.PubMedGoogle Scholar
  79. Leisner, S.M., and Turgeon, R. 1993. Movement of virus and photoassimilate in the phloem—a comparative-analysis. Bioessays 15:741–748.PubMedGoogle Scholar
  80. Lennon, A., Neuenschwander, U.H., Ribas-Carbo, M., Giles, L., Ryals, J.A., and Siedow, J.N. 1997. The effects of salicylic acid and tobacco mosaic virus infection on the alternative oxidase of tobacco. Plant Physiol. 115:783–791.PubMedGoogle Scholar
  81. Li, W.X., and Ding, S.W. 2001. Viral suppressors of RNA silencing. Curr. Opin. Biotech. 12:150–154.PubMedGoogle Scholar
  82. Li, H., Li, W.X., and Ding, S.W. 2002. Induction and suppression of RNA silencing by an animal virus. Science 296:1319–1321.PubMedGoogle Scholar
  83. Linthorst, H.J.M., Meuwissen, R.L.J., Kauffmann, S., and Bol, J.F. 1989. Constitutive expression of pathogenesis-related proteins PR-1, GRP and PR-S in tobacco has no effect on virus infection. Plant Cell 1:285–291.PubMedGoogle Scholar
  84. Lipardi, C., Wei, Q., and Paterson, B.M. 2001. RNAi as random degradative PCR: siRNA primers convert mRNA into dsRNAs that are degraded to generate new siRNAs. Cell 107:297–307.PubMedGoogle Scholar
  85. Lucy, A.P., Guo, H.-S., Li, W.-X., and Ding, S.W. 2000. Suppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus. EMBO J. 19:1672–1680.PubMedGoogle Scholar
  86. Malamy, J., Carr, J.P., Klessig, D.F., and Raskin, I. 1990. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004.Google Scholar
  87. Maldonado, A.M., Doerner P., Dixon, R.A., Lamb, C.J., and Cameron, R.K. 2002. Aputative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403.PubMedGoogle Scholar
  88. Mallory, A.C., Ely, L., Smith, T.H., Marathe, R., Anandalakshmi, R., Fagard, M., Vaucheret, H., Pruss, G., Bowman, L., and Vance, V.B. 2001. HC-Pro suppression of transgene silencing eliminates the small RNAs but not transgene methylation or the mobile signal. Plant Cell 13:571–583.PubMedGoogle Scholar
  89. Mauch, F., Hadwiger, L.A., and Boller, T. 1988. Antifungal hydrolases in pea tissue 1. Purification and characterization of two chitinases and two β-1, 3-glucanases differentially regulated during development and in response to fungal infection. Plant Physiol. 87:325–333.PubMedGoogle Scholar
  90. Maxwell, D.P., Wang, Y., and McIntosh, L. 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl Acad. Sci. USA 96:8271–8276.PubMedGoogle Scholar
  91. Mayers, C.N., Palukaitis, P., and Carr, J.P. 2000. Sub-cellular distribution analysis of the cucumber mosaic virus 2b protein. J. Gen. Virol. 81:219–226.PubMedGoogle Scholar
  92. Métraux, J.P., Signer, H., Ryals, J., Ward, E., Wyssbenz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., and Inverardi, B. 1990. Increase in salicylic-acid at the onset of systemic acquired-resistance in cucumber. Science 250:1004–1006.Google Scholar
  93. Mittler, R., Shulaev, V., Seskar, M., and Lam, E. 1996. Inhibition of programmed cell death in tobacco plants during pathogen-induced hypersensitive response at low oxygen pressure. Plant Cell 8:1991–2001.PubMedGoogle Scholar
  94. Møller, S.G., and Chua, N.H. 1999. Interactions and intersections of plant signalling pathways. J. Mol. Biol. 293:219–234.PubMedGoogle Scholar
  95. Moore, A.L., and Siedow, J.N. 1991. The regulation of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim. Biophys. Acta. 1059:121–140.PubMedGoogle Scholar
  96. Morrain, P., Béclin, C., Elmayan, T., Feuerbach, F., Gordon, C., Morel, J-B., Jouette, D., Lacombe, A-M., Nikic, S., Picault, N., Remoue., K., Sanial, M., Vo, T-A., and Vaucheret, H. 2000. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542.Google Scholar
  97. Mur, L.A.J., Bi, Y.M., Darby, R.M., Firek, S., and Draper, J. 1997. Compromising early salicylic acid accumulation delays the hypersensitive response and increases viral dispersal during lesion establishment in TMV-infected tobacco. Plant J. 12:1113–1126.PubMedGoogle Scholar
  98. Murphy, A.M. and Carr, J.P. 2002. Salicylic acid has cell-specific effects on Tobacco mosaic virus replication and cell-to-cell movement. Plant Physiol. 128:543–554.Google Scholar
  99. Murphy, A.M., Chivasa, S., Singh, D.P., and Carr, J.P. 1999. Salicylic acid-induced resistance to viruses and other pathogens: Aparting of theways? Trends Plant Sci. 4:155–160.PubMedGoogle Scholar
  100. Nawrath, C., and Métraux, J.P. 1999. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–404.PubMedGoogle Scholar
  101. Naylor, M. 1999. The effects of salicylic acid on RNA plant viruses. PhD thesis, University of Cambridge.Google Scholar
  102. Naylor, M., Murphy, A.M., Berry, J.O., and Carr, J.P. 1998. Salicylic acid can induce resistance to plant virus movement. Mol. Plant Microbe Interact. 11:860–868.Google Scholar
  103. Nelson, R.S., and van Bel, A.J.E. 1998. The mystery of virus trafficking into, through and out of the vascular tissue. Prog. Bot. 59:476–533.Google Scholar
  104. Niderman, T., Genetet, I., Bruyère, T., Gees, R., Stintzi, A., Legrand, M., Fritig, B., and Mösinger, E. 1995. Pathogenesis-related PR-1 proteins are antifungal. Plant Physiol. 108:17–27.PubMedGoogle Scholar
  105. Nurnberger, T., and Scheel, D. 2001. Signal Transmission in the plant immune response. Trends Plant Sci. 6:372–379.PubMedGoogle Scholar
  106. Oparka, K.J., and Santa Cruz, S. 2000. The great escape: Phloem transport and unloading of macromolecules. Ann. Rev. Plant Physiol. Plant Mol. Biol. 51:323–347.Google Scholar
  107. Oostendorp, M. Kunz, W., Dietrich, B., and Staub, T. 2001. Induced resistance in plants by chemicals. Eur. J. Plant Pathol. 107:19–28.Google Scholar
  108. Ordog, S.H., Higgins, V.J., and Vanlerberghe, G.C. 2002. Mitochondrial alternative oxidase is not a critical component of plant viral resistance butmayplay a role in the hypersensitive response. Plant Physiol. 129:1858–1865.PubMedGoogle Scholar
  109. Osbourn, A. 1996. Preformed antimicrobial compunds and plant defense against fungal attack. Plant Cell 8:1821–1831.PubMedGoogle Scholar
  110. Otsuki, Y., Shimomura, T., and Takebe, I. 1972. Tobacco mosaic virus multiplication and expression of the Ngene in necrotic responding tobacco varieties. Virology 50:45–50.PubMedGoogle Scholar
  111. Padgett, H.S., Watanabe, Y., and Beachy, R.N. 1997. Identification of the TMV replicase sequence that activates the N gene-mediated hypersensitive response. Mol. Plant Microbe Interact. 10:709–715.Google Scholar
  112. Palauqui, J.C., Elmayan, T., Pollien, J.M., and Vaucheret, H. 1997. Systemic acquired silencing: transgene specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J. 16:4738–4745.PubMedGoogle Scholar
  113. Parker, J.E. 2000. Signalling in plant disease resistance. In Molecular Plant Pathology, eds. M. Dickinson, and J. Beynon, Vol. 4, pp. 144–174. Sheffield, UK: CRC Press.Google Scholar
  114. Pennell, R.I., and Lamb, C. 1997. Programmed cell death in plants. Plant Cell 9:1157–1168.PubMedGoogle Scholar
  115. Pieterse, C.M.J., Van Pelt, J.A., Van Wees, S.C.M., Ton, J., Leon-Kloosterziel, J.K.M., Keurentjes, J.J.B., Verhagen, B.W.M., Knoester, M., Van der Sluis, I., Bakker, P.A.H.M., and Van Loon, L.M. 2001. Rhizobacteria-mediated induced systemic resistance: triggering, signaling and expression. Eur. J. Plant Path. 107:51–61.Google Scholar
  116. Ratcliff, F., Harrison, B.D., and Baulcombe, D.C. 1997. A similarity between viral defence and gene silencing in plants. Science 276:1558–1560.Google Scholar
  117. Ratcliff, F.G., MacFarlane, S.A., and Baulcombe, D.C. 1999. Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell 11:1207–1215.PubMedGoogle Scholar
  118. Rauscher, M., Adam, A.L., Wirtz, S., Guggenheim, R., Mendgen, K., and Deising H.B. 1999. PR-1 protein inhibits the differentiation of rust infection hyphae in leaves of acquired resistant broad bean. Plant J. 19:625–633.PubMedGoogle Scholar
  119. Ross, A.F. 1961a. Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14:329–339.PubMedGoogle Scholar
  120. Ross, A.F. 1961b. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340–358.PubMedGoogle Scholar
  121. Ross, A.F. 1966. Systemic effects of local lesion formation. In Viruses of Plants, eds. A.B.R. Beemster, and J. Dijkstra, pp. 127–150. Amsterdam: North Holland Publishing.Google Scholar
  122. Ryals, J., Lawton, K.A., Delaney, T.P., Friedrich, L, Kessmann, H., Neuenschwander, U.H., Uknes S., Vernooij, B., Weymann, K. 1995. Signal transduction in systemic acquired resistance. Proc. Natl Acad. Sci. USA 92:4202–4205.PubMedGoogle Scholar
  123. Ryals, J., Weymann, K., Lawton, K., Friedrich, L., Ellis, D., Steiner, H. Y., Johnson, J., Delaney, T.P., Jesse, T., Vos, P., and Uknes, S. 1997. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell 9:425–439.PubMedGoogle Scholar
  124. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C., and Manners, J.M. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97:11655–11660.PubMedGoogle Scholar
  125. Schlumbaum, A., Mauch, F., Vogeli, U., and Boller, T. 1986. Plant chitinases are potent inhibitors of fungal growth. Nature 324:365–367.Google Scholar
  126. Shah, J., Tsui, F., and Klessig, D.F. 1997. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol. Plant Microbe Interact. 10:69–78.PubMedGoogle Scholar
  127. Shirasu, K., and Schulze-Lefert, P. 2000. Regulators of cell death in disease resistance. Plant Mol. Biol. 44:371–385.PubMedGoogle Scholar
  128. Simons, B.H., Millenaar, F.F., Mulder, L., Van Loon, L.C., and Lambers, H. 1999. Enhanced expression and activation of the alternative oxidase during infection of Arabidopsis with Pseudomonas syringae pv tomato. Plant Phys. 120:529–538.Google Scholar
  129. Soards, A.J., Murphy, A.M., Palukaitis, P., and Carr, J.P. 2002. Virulence and differential local and systemic spread of Cucumber mosaic virus in tobacco are affected by the CMV 2b protein. Mol. Plant Microbe Interact. 15:647–653.PubMedGoogle Scholar
  130. Stuiver, M., and Custers, J.H.V. 2001. Engineering disease resistance in plants. Nature 411:865–868.PubMedGoogle Scholar
  131. Ton, J. Van Pelt, J.A. Van Loon, L.C., and Pieterse, C.M.J. 2002. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol. Plant Microbe Interact. 15:27–34.PubMedGoogle Scholar
  132. Ueki, S., and Citovsky, V. 2001. Inhibition of systemic onset of post-transcriptional gene silencing by non-toxic concentrations of cadmium. Plant J. 28:283–291.PubMedGoogle Scholar
  133. Ueki, S., and Citovsky, V. 2002. The systemic movement of a tobamovirus is inhibited by a cadmium ion-induced glycine-rich protein. Nat. Cell Biol. 4:478–485.PubMedGoogle Scholar
  134. Vance, V., and Vaucheret, H. 2001. RNA silencing in plants-defense and counterdefense. Science 292:2277–2280.PubMedGoogle Scholar
  135. van Loon, L.C., and van Strien, E.A. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55:85–97.Google Scholar
  136. van Loon, L.C., Bakker, P.A.H.M., and Pieterse, C.M.J. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453–483.PubMedGoogle Scholar
  137. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditzjawhar, R., Ward, E., Uknes, S., Kessmann, H., and Ryals, J. 1994. Salicylic-acid is not the translocated signal responsible for inducing systemic acquired-resistance but is required in signal transduction. Plant Cell 6:959–965.PubMedGoogle Scholar
  138. Voinnet, O. 2001. RNA silencing as a plant immune system against viruses. Trends Genet. 17:449–459.PubMedGoogle Scholar
  139. Voinnet, O., and Baulcombe, D.C. 1997. Systemic signalling in gene silencing. Nature 389:553.PubMedGoogle Scholar
  140. Ward, E.R., Uknes, S.J., Williams, S.C., Dincher, S.S., Wiederhold, D.L., Alexander, D.C., Ahl-Goy, P., Metreaux, J.P., and Ryals, J.A. 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085–1094.PubMedGoogle Scholar
  141. Waterhouse, P.M., Smith, N.A., and Wang, M.B. 1999. Virus resistance and gene silencing: killing the messenger. Trends Plant Sci. 4:452–457.PubMedGoogle Scholar
  142. Waterhouse, P.M., Wang, M.B., and Lough, T. 2001. Gene silencing as an adaptive defence against viruses. Nature 411:834–842.PubMedGoogle Scholar
  143. Weber, H., and Pfitzner, A.J. 1998. Tm-2(2) resistance in tomato requires recognition of the carboxy terminus of the movement protein of tomato mosaic virus. Mol. Plant Microbe Interact. 11:498–503.PubMedGoogle Scholar
  144. Weststeijn, E.A. 1981. Lesion growth and virus localization in leaves of Nicotiana tabacum cv. Xanthi nc. after inoculation with tobacco mosaic virus and incubation alternately at 22°C and 32°C. Physiol. Plant Pathol. 18:357–368.Google Scholar
  145. White, R.F. 1979. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99:410–412.Google Scholar
  146. White, R.F., Antoniw, J.F., Carr, J.P., and Woods, R.D. 1983. The effects of aspirin and polyacrylic acid on the multiplication and spread ofTMVin different cultivars of tobacco with and without the N-gene. Phytopathol. Z. 107:224–232.Google Scholar
  147. Wilson, T.M.A. 1993. Strategies to protect crop plants against viruses-pathogen-derived resistance blossoms. Proc. Natl. Acad. Sci. USA 90:3134–3141.PubMedGoogle Scholar
  148. Wong, C.E., Carson, R.A.J., and Carr, J.P. 2002. Chemically induced virus resistance in Arabidopsis thaliana is independent of pathogenesis-related protein expression and the NPR1 gene. Mol. Plant Microbe Interact. 15:75–81.PubMedGoogle Scholar
  149. Wright, K.M., Duncan, G.H., Pradel, K.S., Carr, F., Wood, S., Oparka, K.J., and Santa Cruz, S. 2000. Analysis of the N gene hypersensitive response induced by a fluorescently tagged tobacco mosaic virus. Plant Physiol. 123:1375–1385.PubMedGoogle Scholar
  150. 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. USA 98:6516–6521.PubMedGoogle Scholar
  151. Yoshioka, K., Nakashita, H., Klessig, D.F., and Yamaguchi, I. 2001. Probenozole induces systemic acquired resistance in Arabidopsis with a novel type of action. Plant J. 25:149–157.PubMedGoogle Scholar
  152. Zehnder, G.W., Murphy, J.F., Sikora, E.J., and Kloepper, J.W. 2001. Application of rhizobacteria for induced resistance. Eur. J. Plant Pathol. 107:39–50.Google Scholar
  153. Zhou, J.-M., Trifa, Y., Silva, H., Pontier, D.F., Lam, E., Shah, J., and Klessig, D.F. 2000. NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol. Plant Microbe Interact. 13:191–202.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Androulla Gilliland
    • 1
  • Alex M. Murphy
    • 1
  • Chui Eng Wong
    • 1
  • Rachael A. J. Carson
    • 1
  • John P. Carr
    • 1
  1. 1.Department of Plant SciencesUniversity of CambridgeCambridgeUK

Personalised recommendations