The Responses of Plants to Pathogens

  • David B. Collinge
  • Jonas Borch
  • Kenneth Madriz-Ordeñana
  • Mari-Anne Newman
Part of the Springer Handbook Series of Plant Ecophysiology book series (KLEC, volume 1)


Some of the most serious and universal challenges faced by plants come from pathogenic microorganisms. These represent highly diverse types of organisms ranging from viruses, bacteria, Oomycetes, protozoa and fungi sensu stricto (ascomycetes, basidiomycetes), see Agrios (1997), for an overview. In addition, aphids and nematodes often induce similar responses in the plant as microorganisms. Plants have responded to this onslaught by evolving a plethora of defence mechanisms. These represent visible physical attributes and inducible alterations in the structure of exposed organs and tissues as well as the more cryptic production of chemicals and proteins which can damage or inhibit the development of the pathogen (see table 1). The defence mechanisms can be induced following the perception of the pathogen, and/or constitutively present in the host (figure 1). Recent advances in molecular techniques have led to an increased understanding of the regulation of the defence mechanisms and the role of different signal transduction pathways in their regulation. The knowledge gained has also led to the demonstration that manipulation (addition, alteration in regulation or removal by antisense technology) of a single defence factor in a plant can alter the outcome of the interaction, for example, resulting in reduced levels of infection by a pathogen (see Cornelissen and Schram, 2000).


Salicylic Acid Defence Response Powdery Mildew Hypersensitive Response Active Oxygen Species 
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. Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J. and Parker. J.E. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA 95, 10306–10311.CrossRefGoogle Scholar
  2. Agrios, G. N. 1997. Plant Pathology. Academic Press, San Diego, Calif.Google Scholar
  3. Aist, J. R. and Bushnell. W. R. 1991. “Invasion of plants by powdery mildew fungi, and cellular mechanisms of resistance”. In: The Fungal spore and disease initiation in plants and animals. eds. G.T. Cole and H.C. Hoch, pp. 321–343. Plenum Press, New York.CrossRefGoogle Scholar
  4. Alfano, J. R. and Collmer, A. 1996. Bacterial pathogenicity in plants: life up against the wall. Plant Cell 8, 1683–1698.PubMedGoogle Scholar
  5. Antoniw, J.F., Ritter, C.E.,. Pierpoint, W.S, and van Loon, L.C. 1980. Comparison of three pathogenesis-related proteins from plants of two cultivars of tobacco infected with TMV. J. Gen.Virol. 47, 79–87.Google Scholar
  6. Atkinson, M.M. and Baker, C.J. 1987. Alteration of plasmalemma sucrose transport in Phaseolus vulgaris by Pseudomonas syringae pv syringae and its association with K’/H’ exchange. Phytopathology 77, 1573–1578.CrossRefGoogle Scholar
  7. Baker, B., Zambryski, P., Staskawicz, B. and Dinesh-Kumar, S.P. 1997. Signaling in plant-microbe interactions. Science 276, 726–733.PubMedCrossRefGoogle Scholar
  8. Blount, J.W., Korth, K.L., Masoud, S.A., Rasmussen, S., Lamb, C. and Dixon, R.A. 2000. Altering expression of cinnamic acid 4-hydroxylase in transgenic plants provides evidence for a feedback loop at the entry point into the phenylpropanoid pathway. Plant Physiol. 122, 107–116.PubMedCrossRefGoogle Scholar
  9. Bolwell, G.P. 1999. Role of active oxygen species and NO in plant defence responses. Curr. Opin. Plant Biol. 2, 287–294.PubMedCrossRefGoogle Scholar
  10. Bowling, S.A., Clarke, J.D., Liu, Y.D., Klessig, D.F., and Dong, X.N. 1997. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and. NPR1-independent resistance. Plant Cell 9, 1573–1584.PubMedGoogle Scholar
  11. Bowyer, P., Clarke, B.R., Lunness, P., Daniels, M.J. and Osboum, A.E. 1995. Host-range of a plant-pathogenic fungus determined by a saponin detoxifying enzyme. Science 267, 37 1374.Google Scholar
  12. Brandt, J., Thordal-Christensen, H., Vad, K., Gregersen, P.L. and Collinge, D.B. 1992. A pathogen-induced gene of barley encodes a protein showing high similarity to a protein kinase regulator. Plant Journal 2, 815–820.PubMedGoogle Scholar
  13. Brent, R. and Finley, R.L. 1997. Understanding gene and allele function with two-hybrid methods. Ann. Rev. Genet. 31, 663–704.PubMedCrossRefGoogle Scholar
  14. Broekaert, W.F., Terras, F.R.G. and Cammue, B.P.A. 2000. “Induced and Preformed Antimicrobial Proteins”. In: Mechanisms of Resistance to Plant Diseases. eds. A.J. Slusarenko, R.S.S. Fraser, and L.C. van Loon, pp. 371–477. Kluwer Academic Publishers, Dordrecht.CrossRefGoogle Scholar
  15. Brown, I., Mansfield, J. Irlam, I. Conrads-Strauch, J. and Bonas, U. 1993. Ultrastructure of interactions between Xanthomonas campestris pv vesicatoria and pepper, including immunocytochemical localization of extracellular polysaccharides and the AvrBs3 protein. Mol. Plant Microbe Interact. 6, 376–386.CrossRefGoogle Scholar
  16. Cao, H., Li, X. and Dong, X.N. 1998. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc. Natl. Acad. Sci. USA 95, 6531–6536.PubMedCrossRefGoogle Scholar
  17. Chamnongpol, S., Willekens, H., Langebartels, C., van Montagu, M., Inzé, D., and van Camp, W. 1996. Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant J. 10, 491–503.CrossRefGoogle Scholar
  18. Chandra, S., Heinstein, P.F. and Low, P.S. 1996. Activation of phospholipase A by plant defense elicitors. Plant Physiol. 110, 979–986.PubMedGoogle Scholar
  19. Chen, Z.Y., Kloek, A.P. Boch, J. Katagiri, F. and Kunkel, B.N. 2000. The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. Mol. Plant Microbe Interact. 13, 1312–1321.Google Scholar
  20. Chester, K. 1933. The problem of acquired physiological immunity in plants. Quarterly Review of Biology 8, 275–324.CrossRefGoogle Scholar
  21. Collinge, D.B., Gregersen, P.L. and Thordal-Christensen, H. 2000. “The nature and role of defence response genes in cereals”. In: The Powdery Mildews: A Comprehensive Treatise. eds. R.R. Belanger and W.R. Bushnell. APS Press, St. Paul, Minnesota, USA.Google Scholar
  22. Conrath, U., Silva, H. and Klessig, D.F. 1997. Protein dephosphorylation mediates salicylic acid-induced expression of PR-1 genes in tobacco. Plant Journal 11, 747–757.CrossRefGoogle Scholar
  23. Cornelissen, B.J.C. and Schram, A. 2000. “Transgenic approaches to control epidemic spread of diseases”. In: Mechanisms of Resistance to Plant Diseases. eds. A.J. Slusarenko, R.S.S. Fraser, and L.C. van Loon, pp. 575–599. Kluwer Academic Publishers, Dordrecht.CrossRefGoogle Scholar
  24. Croft, K.P.C., Voisey, C.R. and Slusarenko, A.J. 1990. Mechanism of hypersensitive cell collapse–correlation of increased lipoxygenase activity with membrane damage in leaves of Phaseolus vulgaris (L) inoculated with an avirulent race of Pseudomonas syringae pv phaseolicola. Physiol. Mol. Plant Path. 36, 49–62.CrossRefGoogle Scholar
  25. 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
  26. de Wit, P.J. and Joosten, M.H. 1999. Avirulence and resistance genes in the Cladosporium fulvum-tomato interaction. Curr. Opin Microbiol. 2, 368–373.PubMedCrossRefGoogle Scholar
  27. Delaney, T.P. 2000. New mutants provide clues into regulation of systemic acquired resistance. Trends Plant Sci. 5, 49–51.PubMedCrossRefGoogle Scholar
  28. Dempsey, D.A., Shah, J. and Klessig, D.F. 1999. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18, 547–575.CrossRefGoogle Scholar
  29. Desikan, R., Clarke, A., Atherfold, P., Hancock, J.T., and Neill, S.J. 1999. Harpin induces mitogen-activated protein kinase activity during defence responses in Arabidopsis thaliana suspension cultures. Planta 210, 97–103.PubMedCrossRefGoogle Scholar
  30. Dixon, R.A. and Harrison, M.J. 1990. Activation, structure and organization of genes involved in microbial defence of plants. Adv. Genet. 28, 165–234.PubMedCrossRefGoogle Scholar
  31. Du, L. and Chen, Z. X. 2001. Identification of genes encoding receptor-like protein kinases as possible targets of pathogen-and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant.1. 24, 837–847.Google Scholar
  32. Dumer, J., Shah, J. and Klessig, D.F. 1997. Salicylic acid and disease resistance in plants. Trends Plant Sci. 2, 266–274.CrossRefGoogle Scholar
  33. Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E. and Jones, J.D.G. 2000. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12, 953–977.Google Scholar
  34. Ebel, J. and Cosio, E.G. 1994. Elicitors of plant defense responses. Int. Rev. Cytol. 148, 1–36. Ellis, J., Dodds, P. N. and Pryor, T. 2000a. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3, 278–284.Google Scholar
  35. Ellis, J., Dodds, P.N. and Pryor, T. 2000b. The generation of plant disease resistance gene specificities. Trends Plant Sci. 5, 373–379.PubMedCrossRefGoogle Scholar
  36. Ellis, J.G., Lawrence, G.J., Luck, J.E., and Dodds, P.N. 1999. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11, 495–506.PubMedGoogle Scholar
  37. Feys, B..J. and Parker, J.E. 2000. Interplay of signaling pathways in plant disease resistance. Trends Genet. 16, 449–455.PubMedCrossRefGoogle Scholar
  38. Finnie, C., Borch, J. and Collinge, D.B. 1999. 14–3–3 proteins: eukaryotic regulatory proteins with many functions. Plant Mol. Biol. 40, 545 – 554.Google Scholar
  39. Flor, H.H. 1971. Current status of the gene-for-gene concept. Ann. Rev. Phytopath. 9, 275296.Google Scholar
  40. Friedrich, L., Vemooij, 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.PubMedCrossRefGoogle Scholar
  41. Gabriel, D.W. and Rolfe, B.G. 1990. Working models of specific recognition in plant-microbe interactions. Ann. Rev. Phytopath. 28, 365–391.CrossRefGoogle Scholar
  42. Gaffney, T., Friedrich, L., Vemooij, 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.PubMedCrossRefGoogle Scholar
  43. Gilchrist, D.G. 1998. Programmed cell death in plant disease: The purpose and promise of cellular suicide. Ann. Rev. Phytopath. 36, 393–414.CrossRefGoogle Scholar
  44. Glazebrook, J. and Ausubel, F.M. 1994. Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc. Natl. Acad. Sci. USA 91, 8955–8959.PubMedCrossRefGoogle Scholar
  45. 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
  46. Glazebrook, J., Rogers, E.E. and. Ausubel, F.M 1997b. Use of Arabidopsis for genetic dissection of plant defense responses. Ann. Rev. Genet. 31, 569.Google Scholar
  47. Glazebrook, J., Zook, M., Mert, F., Kagan, I., Rogers, E.E., Crute, I.R., Holub, E.B., Hammerschmidt, R. and Ausubel, F.M. 1997a. Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146, 381–392.PubMedGoogle Scholar
  48. Goodwin, P.H., Hsiang, T. and Erickson, L. 2000. A comparison of stilbene and chalcone synthases including a new stilbene synthase gene from Vitis riparia cv. Gloire de Montpellier. Plant Sci. 151, 1–8.CrossRefGoogle Scholar
  49. Goodwin, T.W. and Mercer, E.I. 1983. Introduction to plant biochemistry. Pergamon, Oxford.Google Scholar
  50. Govrin, E.M. and Levine, A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10, 751–757.CrossRefGoogle Scholar
  51. Grant, J.J. and Loake, G.J. 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124, 21–30.PubMedCrossRefGoogle Scholar
  52. Greenberg, J.T. 2001. Programmed cell death in plant pathogen interactions. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48, 525–545.CrossRefGoogle Scholar
  53. Gregersen, P.L., Thordal-Christensen, H., Forster, H., and Collinge. D.B., 1997. Differential gene transcript accumulation in barley leaf epidermis and mesophyll in response to attack by Blumeria graminis f.sp. hordei (syn. Erysiphe graminis f.sp. hordei). Physiol. Mol. Plant Path. 51, 85–97.Google Scholar
  54. Hain, R., Reif, H.J., Krause, E., Langebartels, R., Kindl, H., Vomam, B., Wiese, W., Schmelzer, E., Schreier, P.H., Stocker, R.H., and Stenzel, K. 1993. Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361, 153–156.PubMedCrossRefGoogle Scholar
  55. Hammerschmidt, R. 1999. Phytoalexins: what have we learned after 60 years? Ann. Rev. of Phytopath. 37, 285–306.CrossRefGoogle Scholar
  56. Hammond-Kosack, K.E. and Jones, J.D.G. 1997. Plant disease resistance genes. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48, 575–607.CrossRefGoogle Scholar
  57. Heath, M.C. 2000a. Hypersensitive response-related death. Plant Mol. Biol. 44, 321–334.PubMedCrossRefGoogle Scholar
  58. Heath, M.C. 2000b. Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3, 315–319.PubMedCrossRefGoogle Scholar
  59. Herbers, K., Meuwly, P., Frommer, W. B., Metraux, J. P. and Sonnewald, U. 1996. Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8, 793–803.PubMedGoogle Scholar
  60. Ishihara, M., Hasegawa, M., Taira, T. and Toyama, S. 2000. Isolation and antimicrobial activity of feruloyl oligosaccharide ester from pineapple stem residues. Journal of the Japanese Society for Food Science and Technology-Nippon Shokuhin Kagaku Kogaku Kaishi 47, 23–29.CrossRefGoogle Scholar
  61. Jabs, T. 1999. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals Biochem. Pharm. 57, 261–245.CrossRefGoogle Scholar
  62. Jabs, T., Tschope, M., Coiling, C., Hahlbrock, K., and Scheel, D. 1997. Elicitor-stimulated ion fluxes and 02 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. USA 94, 48004805.Google Scholar
  63. Jia, Y.L., McAdams, S.A., Bryan, G.T., Hershey, H.P. and Valent, B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19, 404–4014.CrossRefGoogle Scholar
  64. Jorgensen, J.H. 1994. Genetics of powdery mildew resistance in barley. Crit. Rev. Plant Sci. 13, 97–119.CrossRefGoogle Scholar
  65. Kajava, A.V. 1998. Structural Diversity of Leucine-rich Repeat Proteins. J. Mol. Biol. 277, 519–527.PubMedCrossRefGoogle Scholar
  66. Keen, N.T. 1971. Hydroxyphaseollin production by soybeans resistant and susceptible to Phytophthora megasperma var. soyae. Physiol. Plant Path. 1, 265–275.CrossRefGoogle Scholar
  67. Kjemtrup, S., Nimchuk, Z. and Dangl, J. 2000. Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition. Curr. Opin. Microbiol. 3, 73–78.PubMedCrossRefGoogle Scholar
  68. Klement, Z. 1963. Rapid detection of the pathogenicity of phytopathogenic Pseudomonas. Nature 199, 300.CrossRefGoogle Scholar
  69. Klement, Z. 1982. “Hypersensitivity”. In: Phytopathogenic Procaryotes. eds. M.S. Mount and G.S. Lacy, pp. 150–178. Academic Press, New York.Google Scholar
  70. Kobe, B. and Deisenhofer, J. 1995. The leucine rich repeat: a versatile binding motif. Trends Biochem. Sci. 19, 415–421.CrossRefGoogle Scholar
  71. Kumar, D. and Klessig, D.F. 2000. Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Mol. Plant Microbe Interact. 13, 347–351.PubMedCrossRefGoogle Scholar
  72. Lamb, C. 1996. A ligand-receptor mechanism in plant-pathogen recognition. Science 274, 2038–2039.CrossRefGoogle Scholar
  73. Lange, J., Xie, Z.-P., Broughton, W.J., Vögeli-Lange, R. and Boller, T. 1999. A gene encoding a receptor-like protein kinase in the roots of common bean is differentially regulated in response to pathogens, symbionts and nodulation factors. Plant Sci. 142, 133–145.CrossRefGoogle Scholar
  74. Lawton, K., Weymann, K. Friedrich, L. Vernooij, B. Uknes, S. and Ryals, J. 1995. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol. Plant Microbe Interact. 8, 863–870.PubMedCrossRefGoogle Scholar
  75. Leckband, G. and Lorz, H. 1998. Transformation and expression of a stilbene synthase gene of Vitis vinifera L. in barley and wheat for increased fungal resistance. Theor. Appl. Genet. 96, 1004–1012.CrossRefGoogle Scholar
  76. Leister, R.T. and Katagiri, F. 2000. A resistance gene product of the nucleotide binding site–leucine rich repeats class can form a complex with bacterial avirulence proteins in vivo. Plant J. 22, 345–354.CrossRefGoogle Scholar
  77. Levine, A., Pennell, R.I., Alvarez, M.E., Palmer, R., and Lamb, C. 1996. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6, 427–437.PubMedCrossRefGoogle Scholar
  78. Liu, Y.H., S.Q. Mang, and D.F. Klessig. 2000. Molecular cloning and characterization of a tobacco MAP kinase kinase that interacts with SIPK. Mol. Plant Microbe Interact. 13, 118–124.PubMedCrossRefGoogle Scholar
  79. Lucas, J.A. 1998. Plant Pathology and Plant Pathogens. Blackwell Science, Oxford, UK.Google Scholar
  80. Luck, J.E., Lawrence, G.J., Dodds, P.N., Shepherd, K.W., and Ellis. J.G., 2000. Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell 12, 1367–1377.PubMedGoogle Scholar
  81. Malamy, J., Can, 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.PubMedCrossRefGoogle Scholar
  82. Mansfield, J.W. 2000. “Antimicrobial compounds and resistance. the role of phytoalexins and phytoanticipins”. In: Mechanisms of Resistance to Plant Diseases. eds. A.J. Slusarenko, R.S.S. Fraser, and L.C. van Loon, pp. 325–370. Kluwer Academic Publishers, Dordrecht.Google Scholar
  83. Martin, G.B. 1999. Functional analysis of plant disease resistance genes and their downstream effectors. Curr. Opin. Plant Biol. 2, 273–279.PubMedCrossRefGoogle Scholar
  84. Mauch-Mani, B. and Slusarenko, A.J. 1996. Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8, 203–212.Google Scholar
  85. Mazeyrat, F., Mouzeyar, S., Courbou, I., Badaoui, S., Roeckel-Drevet, P., de Labrouhe, D.T. and Ledoigt, G. 1999. Accumulation of defense related transcripts in sunflower hypocotyls (Helianthus annuus L.) infected with Plasmopara halstedii. Eur. J. Plant Path. 105, 333340.Google Scholar
  86. Mehdy, M.C. 1994. Active oxygen species in plant defence against pathogens. Plant Physiol. 105, 467–472.PubMedGoogle Scholar
  87. Meyers, B.C., Dickerman, A.W., Michelmore, R.W., Sivaramakrishnan, S., Sobral, B.W. and Young, N.D. 2001. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 20, 317–332.CrossRefGoogle Scholar
  88. 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.PubMedCrossRefGoogle Scholar
  89. Michelmore, R.W. 2000. Genomic approaches to plant disease resistance. Curr. Opin. Plant Biol. 3, 125–131.PubMedCrossRefGoogle Scholar
  90. Mittler, R., Lam, E. Shulaev, V. and Cohen, M. 1999. Signals controlling the expression of cytosolic ascorbate peroxidase during pathogen-induced programmed cell death in tobacco. Plant Mol. Biol. 39, 1025–1035.Google Scholar
  91. Navarre, D.A. and Wolpert, T.J. 1999. Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell 11, 237–249.PubMedGoogle Scholar
  92. Oldroyd, G.E.D. and Staskawicz, B. J. 1998. Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl. Acad. Sci. USA. 95, 10300–10305.PubMedCrossRefGoogle Scholar
  93. Pallas, J.A., Paiva, N.L, Lamb, C. and Dixon, R.A. 1996. Tobacco plants epigenetically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J. 10, 281–293.CrossRefGoogle Scholar
  94. Pan, Q., Wendel, J. and Ruhr, R. 2000. divergent evolution of plant nbs-lrr resistance gene homologues in dicot and cereal genomes. J. Mol. Evol. 50, 203–213.Google Scholar
  95. Parker, J.E., Feys, B.J., van der Biezen, E.A., Noël, L., Aarts, N., Austin, M.J., Botella, M.A., Frost, L.N., Daniels, M.J. and Jones, J.D.G. 2000. Unravelling R gene-mediated disease resistance pathways in Arabidopsis. Mol. Plant Path. 1, 17–24.CrossRefGoogle Scholar
  96. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H.B., Lacy, M., Austin, M.J., Parker, J.E., Sharma, S.B., Klessig, D.F., Martienssen R., Mattsson, O., Jensen, A.B. and Mundy, J. 2000. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111–1120.Google Scholar
  97. Pieterse, C.M.J. and van Loon, L.C. 1999. Salicylic acid-independent plant defence pathways. Trends Plant Sci. 4, 52–58.PubMedCrossRefGoogle Scholar
  98. Pieterse, C.M.J., van Wees, S.C.M. Hoffland, E. van Pelt, J.A. and van Loon, L.C. 1996. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8, 1225 1237.Google Scholar
  99. Pieterse, C.M.J., van Wees, S.C.M., van Pelt, J.A., Knoester, M., Laan, R., Gerrits, N., Weisbeek, P.J. and van Loon, L.C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10, 1571–1580.Google Scholar
  100. Piffanelli, P., Devoto, A. and Schulze-Lefert, P. 1999. Defence signaling pathways in cereals. Curr. Opin. Plant Biol. 2, 295–300.PubMedCrossRefGoogle Scholar
  101. Richmond, T. and Somerville, S. 2000. Chasing the dream: plant EST micro-arrays. Curr. Opin. Plant Biol. 3, 108–116.PubMedCrossRefGoogle Scholar
  102. Roberts, M.R. and Bowles, D.J. 1999. Fusicoccin, 14–3–3 proteins, and defense responses in tomato plants. Plant Physiol. 119, 1243 – 1250.PubMedCrossRefGoogle Scholar
  103. Romeis, T., Piedras, P., Zhang, S.Q., Klessig, D.F., Hirt, H. and Jones, J.D.G. 1999. Rapid Avr9- and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11, 273–287.PubMedGoogle Scholar
  104. Ross, A.F. 1961a. Localized acquired resistance to plant virus infections in hypersensitive hosts. Virology 14, 329–339.PubMedCrossRefGoogle Scholar
  105. Ross, A.F. 1961b. Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340–358.PubMedCrossRefGoogle Scholar
  106. Rushton, P.J. and Somssich, I.E. 1998. Transcriptional control of plant genes responsive to pathogens. Curr. Opin. Plant Biol. 1, 311–315.PubMedCrossRefGoogle Scholar
  107. Rushton, P.J. and Somssich, I.E. 1999. “Transcriptional regulation of plant genes responsive to pathogens and elicitors”. In: Plant-Microbe Interactions. eds. G. Stacey and N.T. Keen, pp. 251–274. APS Press, St. Paul, Minnesota.Google Scholar
  108. Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.Y. and Hunt, M.D. 1996. Systemic acquired resistance. Plant Cell 8, 1809–1819.PubMedGoogle Scholar
  109. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S., and Manners, J.M. 2000. Coordinated plant defense responses in Arabidopsis revealed by micro-array analysis. Proc. Natl. Acad. Sci. USA 97, 11655–11660.PubMedCrossRefGoogle Scholar
  110. Schweizer, P., Pokorny, J. Schulze-Lefert, P. and Dudler, R. 2000. Double-stranded RNA interferes with gene function at the single-cell level in cereals. Plant Journal 24, 895–903.PubMedCrossRefGoogle Scholar
  111. Scofield, S.R., Tobias, C.M., Rathjen, J.P., Chang, J.H., Lavelle, D.T., Michelmore, R.W. and Staskawicz, B.J. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274, 2063–2065.PubMedCrossRefGoogle Scholar
  112. Scott, K.J., Davidson, A.D., Jutidamrongphan, W., Mackinnon G. and Manners, J.M. 1990. The activation of genes of wheat and barley by fungal phytopathogens. Aust. J. Plant Physiol. 17, 229–238.CrossRefGoogle Scholar
  113. Seehaus, K. and Tenhaken, R. 1998. Cloning of genes by mRNA differential display induced during the hypersensitive reaction of soybean after inoculation with Pseudomonas syringae pv. glycinea. Plant Mol. Biol. 38, 1225–1234.CrossRefGoogle Scholar
  114. Shirasu, K., Nakajima, H., Rajasekhar, V.K., Dixon, R.A. and Lamb, C. 1997. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261–270.PubMedGoogle Scholar
  115. Shulaev, V., Leon, J. and Raskin, I. 1995. Is salicylic acid a translocated signal of systemic acquired-resistance in tobacco. Plant Cell 7, 1691–1701.PubMedGoogle Scholar
  116. Skou, J.P. 1982. Callose formation responsible for the powdery mildew resistance in barley with genes in the ml-o locus. Phytopathologische Zeitschrift 104, 90–95.CrossRefGoogle Scholar
  117. Smith-Becker, J., Marois, E., Huguet, E.J., Midland, S.L., Sims, J.J. and Keen, N.T. 1998. Accumulation of salicylic acid and 4-hydroxybenzoic acid in phloem fluids of cucumber during systemic acquired resistance is preceded by a transient increase in phenylalanine ammonia-lyase activity in petioles and stems. Plant Physiol. 116, 231–238.PubMedCrossRefGoogle Scholar
  118. Stakman, E.C. 1915. Relation between Puccinia graminis and plants highly resistant to its attack. J. Agricult. Res. 4, 193–200.Google Scholar
  119. Stark-Lorenzen, P., B. Nelke, G. Hanssler, H.P. Muhlbach, and J.E. Thomzik. 1997. Transfer of a grapevine stilbene synthase gene to rice (Oryza sativa L). Plant Cell Rep. 16, 668–673.CrossRefGoogle Scholar
  120. Takken, F.L.W. and Joosten, M.H. 2000. Plant resistance genes: their structure, function and evolution. Eur. J. Plant Path. 106, 699–713.CrossRefGoogle Scholar
  121. Tang, X.Y., Frederick, R.D., Zhou, J.M., Halterman, D A, Jia, Y. and Martin, G.B. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274, 2060–2063.PubMedCrossRefGoogle Scholar
  122. The Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815.CrossRefGoogle Scholar
  123. Thomzik, J E, Stenzel K., Stocker, R., Schreier, P.H.,Hain, R. and Stahl, D.J. 1997. Synthesis of a grapevine phytoalexin in transgenic tomatoes (Lycopersicon esculentum Mill.) conditions resistance against Phytophthora infestans. Physiol. Mol. Plant Path. 51, 265278.Google Scholar
  124. Thordal-Christensen, H., Brandt, J., Cho, B.H., Rasmussen, S.K., Gregersen, P.L., Smedegaard-Petersen, L. and Collinge, D.B. 1992. cDNA cloning and characterization of two barley peroxidase transcripts induced differentially by the powdery mildew fungusGoogle Scholar
  125. Erysiphe graminis. Physiol. Mol. Plant Pathol. 40, 395–409.Google Scholar
  126. Thordal-Christensen, H., Gregersen, P.L. and Collinge, D.B. 2000. “The barleylBlumeria (syn. Erysiphe) graminis interaction: a case study.” In: Mechanisms of Resistance to Plant Diseases. eds. A.J. Slusarenko, R.S.S. Fraser, and L.C. van Loon, pp. 77–100. Kluwer Academic Publishers, Dordrecht.CrossRefGoogle Scholar
  127. Thordal-Christensen, H., Zhang, Z.G., Wei, Y.D. and Collinge, D.B. 1997. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187–1194.CrossRefGoogle Scholar
  128. Thulke, O. and Conrath, U. 1998. Salicylic acid has a dual role in the activation of defence-related genes in parsley. Plant J. 14, 35–43.PubMedCrossRefGoogle Scholar
  129. Tropf, S., Lanz, T, Rensing, S.A., Schroder, J. and Schroder, G. 1994. Evidence that stilbene synthases have developed from chalcone synthases several times in the course of evolution. J. Mol. Evol. 38, 610–618.PubMedCrossRefGoogle Scholar
  130. Tsuji, J., Gage, D.A., Hammerschmidt, R., and Somerville, S.C. 1992. Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv. syringae. Plant Physiol. 98, 1304–1309.CrossRefGoogle Scholar
  131. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., Chandler, D., Slusarenko, A.J., Ward, E. and Ryals, J. 1992. Acquired-resistance in Arabidopsis. Plant Cell 4, 645–656.Google Scholar
  132. van Loon, L.C. 1970. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. “Samsun” and “Samsun NN”. Virology 40, 199–211.CrossRefGoogle Scholar
  133. van Loon, L.C., Bakker, P.A. and Pieterse, C.M.J. 1998. Systemic resistance induced by rhizosphere bacteria. Ann. Rev. Phytopath. 36, 453–483.CrossRefGoogle Scholar
  134. van Loon, L.C., Pierpoint, W.S., Boller, T. and Conejero, V. 1994. Recommendations for naming plant pathogenesis-related proteins. Plant Mol. Biol.Rep. 12, 245–264.CrossRefGoogle 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 Path. 55, 85–97.CrossRefGoogle Scholar
  136. van Peer, R., Niemann, G.J. and Schippers, B. 1991. Induced resistances and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. Strain WCS417r. Phytopathology 91, 728–734.CrossRefGoogle Scholar
  137. Vanacker, H., Harrison, J., Ruisch, J., Carver, T.L.W. and Foyer, C.H. 1998. Antioxidant defences of the apoplast. Protoplasma 205, 129–140.CrossRefGoogle Scholar
  138. VanEtten, H. D., Mansfield, J. W. Bailey, J. A. and Farmer, E. E. 1994. Two classes of plant antibiotics–phytoalexins versus phytoanticipins. Plant Cell 6, 1191–1192.PubMedGoogle Scholar
  139. VanEtten, H. D., Sandrock, R.W., Wasmann, C.C., Soby, S.D., McCluskey, K. and Wang, P. 1995. Detoxification of phytoanticipins and phytoalexins by phytopathogenic fungi. Can. J. Bot. 73, S518 - S525.CrossRefGoogle Scholar
  140. Vera-Estrella, R., Barkla, B.J., Higgins, V.J. and Blumwald, E. 1994. Plant defence response to fungal pathogens, activation of host-plasma membrane H+-ATPase by elicitor-induced enzyme dephosphorylation. Plant Physiol. 104, 209–215.PubMedGoogle Scholar
  141. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, 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
  142. von Röpenack, E., Parr, A. and Schulze-Lefert, P. 1998. Structural analyses and dynamics of soluble and cell wall-bound phenolics in a broad spectrum resistance to the powdery mildew fungus in barley. J. Biol. Chem. 273, 9013–9022.CrossRefGoogle Scholar
  143. Wang, H., Li, J., Bostock, R.M. and Gilchrist, D.G. 1996. Apoptosis: A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8, 375–391.PubMedGoogle Scholar
  144. Ward, E.R., Uknes, S.J., Williams, S.C., Dincher, S.S., Wiederhold, D.L., Alexander, D.C., Ahl-Goy, P., Métraux, 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
  145. Wei, G., Kloepper, J.W. and Tuzun, S. 1991. Induction of systemic resistance of cucumber to Colletrotichum orbiculare by select strains of plant-growth promoting rhizobacteria. Phytopathology 81, 1508–1512.CrossRefGoogle Scholar
  146. White, R.F. 1979. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology, 410–412.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2001

Authors and Affiliations

  • David B. Collinge
    • 1
  • Jonas Borch
    • 1
  • Kenneth Madriz-Ordeñana
    • 2
  • Mari-Anne Newman
    • 1
  1. 1.Department of Plant BiologyRoyal Veterinary and Agricultural University1871-Frederiksberg CDenmark
  2. 2.Centro de Investigación en Biología Celular y Molecular (CIBCM)Universidad de Costa Rica San JoséCosta Rica

Personalised recommendations