Signaling in plant resistance responses: Divergence and cross-talk of defense pathways

Multigenic and Induced Systemic Resistance in Plants

Volumn , Issue , 2006, Pages 166-196

  Pieterse, Corné M J ^a   Schaller, Andreas ^b   Mauch Mani, Brigitte ^c   Conrath, Uwe ^d  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF HOHENHEIM   (Germany)

^c Institute of Botany University of Neuchâtel Case Postale 2   (Switzerland)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84919875002     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/0-387-23266-4_8     Document Type: Chapter

References (202)

1. Abad, M. S., Hakimi, S. M., Kaniewski, W. K., Rommens, C. M. T., Shulaev, V., Lam, E., and Shah, D. M. 1997. Characterization of acquired resistance in lesion-mimic transgenic potato expressing bacterio-opsin. Mol. Plant Microbe Interact. 10:635-645.
2. Abeles, F. B., Morgan, P. W., and Saltveit, M. E. J. 1992. Ethylene in Plant Biology. San Diego, CA: Academic Press.
3. Ajlan, A. M., and Potter, D. A. 1992. Lack of effect of tobacco mosaic virus-induced systemic acquired resistance on arthropod herbivores in tobacco. Phytopathology 82:647-651.
4. Bakker, P. A. H. M., Van Peer, R., and Schippers, B. 1991. Suppression of soil-borne plant pathogens by fluorescent pseudomonads: mechanisms and prospects. In Biotic Interactions and Soil-Borne Diseases, eds. A. B. R. Beemster, G. J. Bollen, M. Gerlagh, M. A. Ruissen, B. Schippers, and A. Tempel, pp. 217-230. Amsterdam, The Netherlands: Elsevier Scientific Publishers.
5. Bent, A. F., Innes, R. W., Ecker, J. R., and Staskawicz, B. J. 1992. Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol. Plant Microbe Interact. 5:372-378.
6. Bergey, D. R., and Ryan, C. A. 1999. Wound- and systemin-inducible calmodulin gene expression in tomato leaves. Plant Mol. Biol. 40:815-823.
7. Bergey, D. R., Orozco-Cardenas, M., De Moura, D. S., and Ryan, C. A. 1999. A woundand systemin-inducible polygalacturonase in tomato leaves. Proc. Natl. Acad. Sci. USA 96:1756-1760.
8. Bleecker, A. B., Estelle, M. A., Somerville, C., and Kende, H. 1988. Insensivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241:1086-1089.
9. Blume, B., Nürnberger, T., Nass, N., and Scheel, D. 2000. Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12:1425-1440.
10. Boch, J., Verbsky, M. L., Robertson, T. L., Larkin, J. C., and Kunkel, B. N. 1998. Analysis of resistance gene-mediated defense responses in Arabidopsis thaliana plants carrying a mutation in CPR5. Mol. Plant Microbe Interact. 12:1196-1206.
11. Bowles, D. 1998. Signal transduction in the wound response of tomato plants. Philos. Trans. R. Soc. 353:1495-1510.
12. Bowling, S. A., Guo, A., Cao, H., Gordon, A. S., Klessig, D. F., and Dong, X. 1994. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6:1845-1857.
13. Bowling, S. A., Clarke, J. D., Liu, Y., Klessig, D. F., and Dong, X. 1997. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9:1573-1584.
14. Burtseva, T. I., and Kofanova, N. N. 1996. Inhibitor of trypsin and microbial serine proteinases isolated from Yersinia pseudotuberculosis. Biochemistry (Moskow) 61:1335-1341.
15. Büschges, R., Hollricher, K., Panstruga, R., Simons, G., Wolter, M., Frijters, A., Van Daelen, R., Van Der Lee, T., Diergaarde, P., Groenendijk, J., Töpsch, S., Vos, P., Salamini, F., and Schulze-Lefert, P. 1997. The barley MLO gene: a novel control element of plant pathogen resistance. Cell 88:695-705.
16. Cameron, R. K., Paiva, N. L., Lamb, C. J., and Dixon, R. A. 1999. Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiol. Mol. Plant Pathol. 55:121-130.
17. Cao, H., Bowling, S. A., Gordon, A. S., and Dong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 8:1583-1592.
18. Chico, J. M., Ráices, M., Téllez-Iñón, M. T., and Ulloa, R. M. 2002. A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants. Plant Physiol. 128:256-270.
19. Ciardi, J. A., Tieman, D. M., Lund, S. T., Jones, J. B., Stall, R. E., and Klee, H. J. 2000. Response to Xanthomonas campestris pv. vesicatoria in tomato involves regulation of ethylene receptor gene expression. Plant Physiol. 123:81-92.
20. Clarke, J. D., Aarts, N., Feys, B. J., Dong, X., and Parker, J. E. 2001. Constitutive disease resistance requires EDS1 in the Arabidopsis mutants cpr1 and cpr6 and is partially EDS1-dependent in cpr5. Plant J. 26:409-420.
21. Cohen, Y. 1994. 3-aminobutyric acid induces systemic resistance against Peronospora tabacina. Physiol. Mol. Plant Pathol. 44:273-288.
22. Cohen, Y., and Gisi, U. 1994. Sytemic translocation of 14C-DL-3-aminobutyric acid in tomato plants in relation to induced resistance against Phytophthora infestans. Physiol. Mol. Plant Pathol. 45:441-446.
23. Cohen, Y., Ovadia, A., and Oka, Y. 2000. Is induced-resistance reversible? The BABA case. (Abstract), First International Symposium on Induced Resistance to Plant Diseases, Island of Corfu, Greece, 22-27 May 2000, p. 68.
24. Conconi, A., Miquel, M., Browse, J. A., and Ryan, C. A. 1996. Intracellular levels of free linolenic and linoleic acids increase in tomato leaves in response to wounding. Plant Physiol. 111:797-803.
25. + release, and increases coumarin synthesis in parsley cells. FEBS Lett. 279:141-144.
26. Conrath, U., Chen, Z., Ricigliano, J. R., and Klessig, D. F. 1995. Two inducers ofplant defense responses, 2, 6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proc. Natl. Acad. Sci. USA 92:7143-7147.
27. Conrath, U., Pieterse; C. M. J., and Mauch-Mani, B. 2002. Priming in plant-pathogen interactions. Trends Plant Sci. 5:210-216.
28. Constabel, C. P. 1999. A survey of herbivory-inducible defensive proteins and phytochemicals. In Induced Plant Defenses Against Pathogens and Herbivores. Biochemistry, Ecology, and Agriculture, eds. A. A. Agrawal, S. Tuzun, and E. Bent, pp. 137-166. St. Paul, MN: APS Press.
29. Constabel, P. C., Yip, L., and Ryan, C. A. 1998. Prosystemin from potato, black nightshade, and bell pepper: primary structure and biological activity of predicted systemin polypeptides. Plant Mol. Biol. 36:55-62.
30. De Bruxelles, G. L., and Roberts, M. R. 2001. Signals regulating multiple responses towounding and herbivores. Crit. Rev. Plant Sci. 20:487-521.
31. De Laat, A. M. M., and Van Loon, L. C. 1981. Regulation of ethylene biosynthesis in virusinfected tobacco leaves. I. Determination of the role of methionine as a precursor of ethylene. Plant Physiol. 68:256-260.
32. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E., and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247-1250.
33. Delaney, T. P., Friedrich, L., and Ryals, J. 1995. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. USA 92:6602-6606.
34. Dempsey, D. A, Shah, J., and Klessig, D. F. 1999. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18:547-575.
35. Dhondt, S., Geoffroy, P., Stelmach, B. A., Legrand, M., and Heitz, T. 2000. Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virusinfected tobacco leaves and is contributed by patatin-like enzymes. Plant J. 23:431-440.
36. Díaz, J., Ten Have, A., and Van Kan, J. A. L. 2002. The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol. 129:1314-1315.
37. Doares, S. H., Syrovets, T., Weiler, E. W., and Ryan, C. A. 1995a Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 92:4095-4098.
38. Doares, S. H., Narváez-Vásquez, J., Conconi, A, and Ryan, C. A. 1995b. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108:1741-1746.
39. Doherty, H. M., and Bowles, D. J. 1990. The role of pH and ion transport in oligosaccharideinduced proteinase inhibitor accumulation in tomato plants. Plant Cell Environ. 13:851-855.
40. Doherty, H. M., Selvendran, R. R., and Bowles, D. J. 1988. The wound response of tomato plants can be inhibited by aspirin and related hydroxy-benzoic acids. Physiol. Mol. Plant Pathol. 33:377-384.
41. Doke, N., Miura, Y., Sanchez, L. M., Park, H. J., Noritake, T., Yoshiola, H., and Kawakita, K. 1996. The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence: a review. Gene 179:45-51.
42. Dombrowski, J. E., Pearce, G., and Ryan, C. A. 1999. Proteinase inhibitor-inducing activity of the prohormone prosystemin resides exclusively in the C-terminal systemin domain. Proc. Natl. Acad. Sci. USA 96:12947-12952.
43. Ebel, J., and Mithöfer, A. 1998. Early events in the elicitation of plant defence. Planta 206:335-348.
44. Engelberth, J., Koch, T., Schueler, G., Bachmann, N., Rechtenbach, J., and Boland, W. 2001. Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signalinginlima bean. Plant Physiol. 125:369-377.
45. Farmer, E. E., and Ryan, C., A. 1990. Interplant Communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl. Acad. Sci. USA 87:7713-7716.
46. Farmer, E. E., and Ryan, C. A. 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129-134.
47. Farmer, E. E., Johnson, R. R., and Ryan, C. A. 1991. Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol. 98:995-1002.
48. 2 in hypocotyls of cucumber is induced by breaching the cuticle and is enhanced by salicylic acid. Plant Physiol. 110:347-354.
49. Felix, G., and Boller, T. 1995. Systemin induces rapid ion fluxes and ethylene biosynthesis in Lycopersicon peruvianum cells. Plant J. 7:381-389.
50. Felton, G. W., Korth, K. L., Bi, J. L., Wesley, S. V., Huhman, D. V., Mathews, M. C., Murphy, J. B., Lamb, C., and Dixon, R. A. 1999. Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr. Biol. 9:317-320.
51. Feys, B. J., Moisan, L. J., Newmann, M. A., and Parker, J. E. 2001. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20:5400-5411.
52. Fidantsef, A. L., Stout, M. J., Thaler, J. S., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiol. Mol. Plant. Pathol. 54:97-114.
53. Frick, U. B., and Schaller, A. 2002 cDNA microarray analysis of fusicoccin-induced changes in gene expression in tomato plants. Planta 216:83-94.
54. Frye, C. A., and Innes, R. W. 1998. An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10:947-956.
55. Frye, C. A., Tang, D., and Innes, R. W. 2001. Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. USA 98:373-378.
56. Fukuda, Y. 1996. Coordinated activation of chitinase genes and extracellular alkalinization in suspension-cultured tobacco cells. Biosci. Biotech. Biochem. 60:2005-2010.
57. 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.
58. Gamliel, A., and Katan, J. 1992. Influence of seed and root exudates on fluorescent Pseudomonas and fungi in solarized soil. Phytopathology 82:320-327.
59. Govrin, E. M., and Levine, A. 2000. The hypersensitive reaction facilitates plant infection by the necrotrophic fungus Botrytis cinerea. Curr. Biol. 10:751-757.
60. Graham, T. L., and Graham, M. Y. 1994. Wound-associated competency factors are required for the proximal cell responses of soybean to the Phytophthora sojae wall glucan elicitor. Plant Physiol. 105:571-578.
61. Green, T. R., and Ryan, C. A. 1972. Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science 175:776-777.
62. Gundlach, H., Mueller, M. J., Kutchan, T. M., and Zenk, M. H. 1992. Jasmonic acidis a signal transducer in elicitor-induced plant cell cultures. Proc. Natl. Acad. Sci. USA 89:2389-2393.
63. Hammerschmidt, R., and Kuć, J. 1982. Lignification as a mechanism for induced systemic resistance in cucumber. Physiol. Plant Pathol. 20:61-71.
64. Hammerschmidt, R., Métraux, J. P., and Van Loon, L. C. 2001. Inducing resistance: a summary of papers presented at the First International Symposium on Induced Resistance to Plant Diseases, Corfu, May 2000. Eur. J. Plant Pathol. 107:1-6.
65. Harms, K., Ramirez, I., and Peña-Cortés, H. 1998. Inhibition of wound-induced accumulation of allene oxide synthase transcripts in flax leaves by aspirin and salicylic acid. Plant Physiol. 118:1057-1065.
66. Hause, B., Stenzel, I., Miersch, O., Maucher, H., Kramell, R., Ziegler, J., and Wasternack, B. 2000. Tissue-specific oxylipin signature of tomato flowers: allene-oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J. 24:113-126.
67. He, P., Warren, R. F., Zhao, T., Shan, L., Zhu, L., Tang, X., and Zhou, J.-M. 2001. Overexpression of PTI5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Mol. Plant Microbe Interact. 14:1453-1457.
68. Hilpert, B., Bohlmann, H., Op Den Camp, R., Przybyla, D., Miersch, O., Buchala, A., and Apel, K. 2001. Isolation and characterization of signal transduction mutants of Arabidopsis thaliana that constitutively activate the octadecanoid pathway and form necrotic microlesions. Plant J. 26:435-446.
69. Hoffman, T., Schmidt, J. S., Zheng, X., and Bent, A. F. 1999. Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiol. 119:935-949.
70. Howe, G. A., and Ryan, C. A. 1999. Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153:1411-1421.
71. Howe, G. A., Lightner, J., Browse, J., and Ryan, C. A. 1996. An octadecanoid pathway mutant (JL5 of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067-2077.
72. Inbar, M., Doostdar, H., Sonoda, R. M., Leibee, G. L., Mayer, R. T. 1998. Elicitors of plant defensive systems reduce insect densities and disease incidence. J. Chem. Ecol. 24:135-149.
73. Ishiguro, S., Kawai-Oda, A., Nishida, I., and Okada, K. 2001. The defective in anther dehiscence1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191-2209.
74. - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin biosynthesis in parsley. Proc. Natl. Acad. Sci. USA 94:4800-4805.
75. Jacinto, T., McGurl, B., Franceschi, V., Delano-Freier, J., and Ryan, C. A. 1997. Tomato prosystemin promoter confers wound-inducible, vascular bundle-specific expression of the β-glucuronidase gene in transgenic tomato plants. Planta 203:406-412.
76. 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.
77. Jirage, D., Zhou, N., Cooper, B., Clarke, J. D., Dong, X., and Glazebrook, J. 2001. Constitutive salicylic acid-dependent signaling in cpr1 and cpr6 mutants requires PAD4. Plant J. 26:395-407.
78. Jonak, C., Beisteiner, D., Beyerly, J., and Hirt, H. 2000. Wound-induced expression and activation of WIG, a novel glycogen synthase kinase 3. Plant Cell 12:1467-1475.
79. Kachroo, P., Shanklin, J., Shah, J., Whittle, E. J., and Klessig, D. F. 2001. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc. Natl. Acad. Sci. USA 98:9448-9453.
80. Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. Chicago: University of Chicago Press.
81. Katz, V. A., Thulke, O. U., and Conrath, U. 1998. A benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Physiol. 117:1333-1339.
82. Katz, V. A., Fuchs, A., and Conrath, U. 2002. Pretreatment with salicylic acid primes parsley cells for enhanced ion transport following elicitation. FEBS Lett. 520:53-57.
83. 2. Plant Physiol. 108:1171-1178.
84. Kauss, H., Theisinger-Hinkel, E., Mindermann, R., and Conrath, U. 1992a. Dichloroisonicotinic and salicylic acid, inducers of systemic acquired resistance, enhance fungal elicitor responses in parsley cells. Plant J. 2:655-660.
85. Kauss, H., Krause, K., and Jeblick, W. 1992b. Methyl jasmonate conditions parsley suspension cells for increased elicitation of phenylpropanoid defense responses. Biochem. Biophys. Res. Comm. 189:304-308.
86. Kauss, H., Franke, R., Krause, K., Conrath, U., Jeblick, W., Grimmig, B., and Matern, U. 1993. Conditioning of parsley Petroselinum crispum) suspension cells increases elicitorinduced incorporation of cell wall phenolics. Plant Physiol. 102:459-466.
87. Kauss, H., Jeblick, W., Ziegler, J., and Krabler, W. 1994. Pretreatment of parsley (Petroselinum crispum L.) suspension cultures with methyl jasmonate enhances elicitation of activated oxygen species. Plant Physiol. 105:89-104.
88. Klessig, D. F., and Malamy, J. 1994. The salicylic acid signal in plants. Plant Mol. Biol. 26:1439-1485.
89. Klüsener, B., and Weiler, E. W. 1999. Pore-forming properties of elicitors of plant defense reactions and cellulolytic enzymes. FEBS Lett. 459:263-266.
90. Knoester, M., Van Loon, L. C., Van Den Heuvel, J., Hennig, J., Bol, J. F., and Linthorst, H. J. M. 1998. Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc. Natl. Acad. Sci. USA 95:1933-1937.
91. Knoester, M., Linthorst, H. J. M., Bol, J. F., and Van Loon, L. C. 2001. Involvement ofethylene in lesion development and systemic acquired resistance in tobacco during the hypersensitive reaction to tobacco mosaic virus. Physiol. Mol. Plant Pathol. 59:45-57.
92. Kohler, A., Schwindling, S., and Conrath, U. 2002. Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol. 128:1046-1056.
93. Kubigsteltig, I., Laudert, D., and Weiler, E. W. 1999. Structure and regulation of the Arabidopsis thaliana allene oxide synthase gene. Planta 208:463-471.
94. Kuć, J. 1987. Translocated signals for plant immunization. Ann. N. Y. Acad. Sci. 494:221-223.
95. Latunde-Dada, A. O., and Lucas, J. A. 2001. The plant defense activator acibenzolar-S-methyl primes cowpea [Vigna unguiculata (L.) Walp.] seedlings for rapid induction of resistance. Physiol. Mol. Plant Pathol. 58:199-208.
96. Lawton, K. A., Potter, S. L., Uknes, S., and Ryals, J. 1994. Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6:581-588.
97. Lee, S., Suh, S., Kim, S., Crain, R. C., Kwak, J. M., Nam, H.-G., and Lee, Y. 1997. Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. Plant J. 12:547-556.
98. Leeman, M., Van Pelt, J. A., Hendrickx, M. J., Scheffer, R. J., Bakker, P. A. H. M., and Schippers, B. 1995. Biocontrol of fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374. Phytopathology 85:1301-1305.
99. León, J., Rojo, E., and Sánchez-Serrano, J. J. 2001. Wound signalling in plants. J. Exp. Bot. 52:1-9.
100. Li, L., and Howe, G. A. 2001. Alternative splicing of prosystemin pre-mRNA produces two isoforms that are active as signals in the wound response pathway. Plant Mol. Biol 46:409-419.
101. Li, L., Li, C., and Howe, G. A. 2001. Genetic analysisofwound signalingin tomato. Evidence for a dual role of jasmonic acid in defense and female fertility. Plant Physiol. 127:1414-1417.
102. Li, L., Li, C., Lee, G. I., and Howe, G. A. 2002. Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc. Natl. Acad. Sci. USA 99:6416-6421.
103. Lund, S. T., Stall, R. E., and Klee, H. J. 1998. Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10:371-382.
104. Malamy, J., and Klessig, D. F. 1992. Salicylic acid and plant disease resistance. Plant J. 2:643-654.
105. Mauch, F., Hadwiger, L. A., and Boller, T. 1994. Ethylene: symptom, not signal for the induction of chitinase and β-1, 3-glucanase in pea pods by pathogens and elicitors. Plant Physiol. 76:607-611.
106. McConn, J., Creelman, R. A., Bell, E., Mullet, J. E., and Browse, J. 1997. Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 94:5473-5477.
107. McGurl, B., and Ryan, C. A. 1992. The organization of the prosystemin gene. Plant Mol. Biol. 20:405-409.
108. McGurl, B., Pearce, G., Orozco-Cardenas, M., and Ryan, C. A. 1992. Structure, expression and antisense inhibition of the systemin precursor gene. Science 255:1570-1573.
109. McGurl, B., Orozco-Cardenas, M., Pearce, G., and Ryan, C. A. 1994. Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc. Natl. Acad. Sci. USA 91:9799-9802.
110. Meindl, T., Boller, T., and Felix, G. 1998. The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell 10:1561-1570.
111. Mittler, R., and Lam, E. 1996. Sacrifice in the face of foes: pathogen-induced programmed cell death in plants. Trends Microbiol. 4:10-15.
112. Mittler, R., Shulaev, V., and Lam, E. 1995. Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pump. Plant Cell 7:29-42.
113. Moran, P. 1998. Plant-mediated interactions between insects and fungal plant pathogen and the role of chemical responses to infection. Oecologia 115:513-530.
114. Moyen, C., and Johannes, E. 1996. Systemin transiently depolarizes the tomato mesophyll cell membrane and antagonizes fusicoccin-induced extracellular acidification of mesophyll tissue. Plant Cell Environ. 19:464-470.
115. 2+ mobilization from intra- and extracellular compartments. Plant Cell Environ. 21:1101-1111.
116. Mur, L. A. J., Brown, I. R., Darby, R. M., Bestwick, C. S., Bi, Y.-M., Mansfield, J. W., and Draper, J. 1996. Salicylic acid potentiates defense gene expression in tissue exhibiting acquired resistance to pathogen attack. Plant J. 9:559-571.
117. Mur, L. A., Brown, I. R., Darby, R. M., Bestwick, C. S., Bi, Y.-M., Mansfield, J. W., Draper, J. 2000. A loss of resistance to avirulent bacterial pathogens in tobacco is associated with the attenuation of a salicylic acid-potentiated oxidative burst. Plant J. 23:609-621.
118. Narváez-Vásquez, J., Florin-Christensen, J., and Ryan, C. A. 1999. Positional specificity of a phospholipase A activity induced by wounding, systemin, and oligosaccharide elicitors in tomato leaves. Plant Cell 11:2249-2260.
119. Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N., and Ohashi, Y. 1998. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39:500-507.
120. Norman-Setterblad, C., Vidal, S., and Palva, T. E. 2000. Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Mol. Plant Microbe Interact. 13:430-438.
121. O'Donnell, P. J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H. M. O., and Bowles, D. J. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914-1917.
122. Orozco-Cárdenas, M. L. 2000. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179-191.
123. Orozco-Cardenas, M., and Ryan, C. A. 1999. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 96:6553-6557.
124. Orozco-Cardenas, M., McGurl, B., and Ryan, C. A. 1993. Expressionofan antisense prosystemin gene in tomato plants reduces the resistance toward Manduca sexta larvae. Proc. Natl. Acad. Sci. USA 90:8273-8276.
125. Pearce, G., Strydom, D., Johnson, S., and Ryan, C. A. 1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895-898.
126. Pearce, G., Moura, D. S., Stratmann, J., and Ryan, C. A. 2001. Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817-820.
127. Peña-Cortés, H., Albrecht, T., Prat, S., Weiler, E. W., and Willmitzer, L. 1993. Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123-128.
128. Penninckx, I. A. M. A., Eggermont, K., Terras, F. R. G., Thomma, B. P. H. J., De Samblanx, G. W., Buchala, A., Métraux, J.-P., Manners, J. M., and Brokaert, W. F. 1996. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309-2323.
129. Penninckx, I. A. M. A., Thomma, B. P. H. J., Buchala, A., and Métraux, J.-P. 1998. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103-2113.
130. 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.
131. Pieterse, C. M. J., Van Wees, S. C. M., Van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P. J., and Van Loon, L. C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-1580.
132. Pieterse, C. M. J., Van Pelt, J. A., Ton, J., Parchmann, S., Mueller, M. J., Buchala, A. J., Métraux, J.-P., and Van Loon, L. C. 2000. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiol. Mol. Plant Pathol. 57:123-134.
133. Pieterse, C. M. J., Van Wees, S. C. M., Ton, J., Van Pelt, J. A., and Van Loon, L. C. 2002. Signaling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biol. 4:535-544.
134. Preston, C. A., Lewandowski, C., Enyedi, A. J., and Baldwin, I. T. 1999. Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants. Planta 209:87-95.
135. Raskin, I. 1992. Role of salicylic acid in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:439-463.
136. Reymond, P., Weber, H., Damond, M., and Farmer, E. E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707-719.
137. Rizhsky, L., and Mittler, R. 2001. Inducible expression of bacterio-opsin in transgenic tobacco and tomato plants. Plant Mol. Biol. 46:313-323.
138. Roberts, M. R., and Bowles, D. J. 1999. Fusicoccin, 14-3-3 proteins, and defense responses in tomato plants. Plant Physiol. 119:1243-1250.
139. Rojo, E., Titarenko, E., León, J., Berger, S., Vancanneyt, G., and Sánchez-Serrano, J. J. 1998. Reversible protein phosphorylation regulates jasmonic acid-dependent and -independent wound signal transduction pathways in Arabidopsis thaliana. Plant J. 13:153-165.
140. Rojo, E., León, J., and Sánchez-Serrano, J. J. 1999. Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J. 20:135-142.
141. 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.
142. Ryan, C. A. 1992. The search for the proteinase inhibitor-inducing factor, PIIF. Plant Mol. Biol. 19:123-133.
143. Ryan, C. A. 2000. The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta 1477:112-121.
144. Schaller, A. 1998. Action of proteolysis-resistant systemin analogues in wound signalling. Phytochemistry 47:605-612.
145. Schaller, A. 1999. Oligopeptide signalling and the action of systemin. Plant Mol. Biol. 40:763-769.
146. Schaller, A. 2001. Bioactive peptides as signal molecules in plant defense, growth, and development. In Bioactive Natural Products, ed. Atta-Ur-Rahman, Vol. 25, pp. 367-411. Amsterdam, The Netherlands: Elsevier.
147. Schaller, A., and Frasson, D. 2001. Induction of wound response gene expression in tomato leaves by ionophores. Planta 212:431-435.
148. +-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263-272.
149. Schaller, A., and Ryan, C. A. 1995. Systemin-a polypeptide defense signal in plants. BioEssays 18:27-33.
150. Schaller, A., Roy, P., and Amrhein, N. 2000. Salicylic acid-independent induction of pathogenesis-related gene expression by fusicoccin. Planta 210:599-606.
151. Scheel, D. 1998. Resistance response physiology and signal transduction. Curr. Opin. Plant Biol. 1:305-310.
152. Scheer, J. M., and Ryan, C. A. 1999. A 160 kDa systemin receptor on the cell surface of Lycopersicon peruvianum suspension cultured cells: kinetic analyses, induction by methyl jasmonate and photoaffinity labeling. Plant Cell 11:1525-1535.
153. Scheer, J. M., and Ryan, C. A. 2002. The systemin receptor SR160 from Lycopersicon perivianum is a member of the LRR receptor kinase family. Proc. Natl. Acad. Sci. USA 99:9585-9590.
154. Schenk, P. M., Kazal, 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. 97:11655-11660.
155. Schmele, I., and Kauss, H. 1990. Enhanced activity of the plasma membrane localized callose synthase in cucumber leaves with induced resistance. Physiol. Mol. Plant Pathol. 37:221-228.
156. Schweizer, P., Buchala, A., and Métraux, J.-P. 1997. Gene expression patterns and levels of jasmonic acid in rice treated with the resistance inducer 2, 6-dichloroisonicotinic acid. Plant Physiol. 115:61-70.
157. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H., and Ohashi, Y. 1995. Tobacco MAP kinase: A possible mediator in wound signal transduction pathways. Science 270:1988-1992.
158. Seo, S., Sano, H., and Ohashi, Y. 1999. Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco miotogen-activated protein kinase. Plant Cell Physiol. 11:289-298.
159. Shah, J., and Klessig, D. F. 1999. Salicylic acid: signal perception and transduction. In Biochemistry and Molecular Biology of Plant Hormones, eds. P. P. J. Hooykaas, M. A. Hall, and K. R. Libbenga, pp. 513-541. Amsterdam, The Netherlands: Elsevier Science.
160. 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.
161. Shelp, B. J., Bown, A. W., and McLean, M. D. 1999. Metabolism and function of gammaaminobutyric acid. Trends Plant Sci. 4:446-452.
162. Shirasu, K., Nakajima, H., Rajasekhar, 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.
163. Shumway, L. K., Yang, V. V., and Ryan, C. A. 1976. Evidence for the presence of proteinase inhibitor I in vacuolar bodies of plant cells. Planta 129:161-165.
164. Siegrist, J., Orober, M., and Buchenauer, H. 2000. β-aminobutyric acid-mediated enhancement of resistance in tobacco to tobacco mosaic virus depends on the accumulation of salicylic acid. Physiol. Mol. Plant. Pathol. 56:95-106.
165. Stankovic, B., and Davies, E. 1997. Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato. Planta 202:402-406.
166. Staswick, P. E., Su, W. P., and Howell, S. H. 1992. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl. Acad. Sci. USA 89:6837-6840.
167. Staswick, P. E., Yuen, G. Y., and Lehman, C. C. 1998. Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J. 15:747-754.
168. Stennis, M. J., Chandra, S., Ryan, C. A., and Low, P. 1998. Systemin potentiates the oxidative burst in cultured tomato cells. Plant Physiol. 117:1031-1036.
169. Sticher, L., Mauch-Mani, B., and Métraux, J.-P. 1997. Systemic acquired resistance. Annu. Rev. Phytopath. 35:235-270.
170. Stintzi, A., Weber, H., Reymond, P., Browse, J., and Farmer, E. E. 2001. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc. Natl. Acad. Sci. USA 98:12837-12842.
171. Stout, M. J., Fidantsef, A. L., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathol. 54:115-130.
172. Strassner, J., Schaller, F., Frick, U. B., Howe, G. A., Weiler, E. W., Amrhein, N., Macheroux, P., and Schaller, A. 2002. Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound response. Plant J. 32:585-601.
173. Stratmann, J. W., and Ryan, C. A. 1997. Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Proc. Natl. Acad. Sci. USA 94:11085-11089.
174. Stratmann, J., Scheer, J., and Ryan, C. A. 2000. Suramin inhibits initiation of defense signaling by systemin, chitosan, and a β-glucan elicitor in suspension-cultured. Lycopersicon peruvianum cells. Proc. Natl. Acad. Sci. USA 97:8862-8867.
175. Stumm, D., and Gessler, C. 1986. Role of papillae in the induced systemic resistance of cucumbers against Colletotrichum lagenarium. Physiol. Mol. Plant Pathol. 29:405-410.
176. Thain, J. F., Gubb, I. R., and Wildon, D. C. 1995. Depolarization of tomato leaf cells by oligogalacturonide elicitors. Plant Cell Environ. 18:211-214.
177. Thaler, J. S., Fidantsef, A. L., Duffey, S. S., and Bostock, R. M. 1999. Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. J. Chem. Ecol. 25:1597-1609.
178. Thomma, B. P. H. J., Eggermont, K., Penninckx, I. A. M. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A., and Broekaert, W. F. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA 95:15107-15111.
179. Thomma, B. P. H. J., Eggermont, K., Tierens, K. F. M., and Broekaert, W. F. 1999. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121:1093-1102.
180. Thulke, O. U., and Conrath, U. 1998. Salicylic acid has a dual role in the activation of defense-related genes in parsley. Plant J. 14:35-42.
181. Ton, J., Davison, S., Van Wees, S. C. M., Van Loon, L. C., and Pieterse, C. M. J. 2001. The Arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signaling. Plant Physiol. 125:652-661.
182. Ton, J., De Vos, M., Robben, C., Buchala, A. J., Métraux, J.-P., Van Loon, L. C., and Pieterse, C. M. J. 2002a. Characterisation of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J. 29:11-21.
183. Ton, J., Van Pelt, J. A., Van Loon, L. C., and Pieterse, C. M. J. 2002b. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol. Plant Microbe Interact. 15:27-34.
184. 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.
185. 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.
186. Van Wees, S. C. M., Pieterse, C. M. J., Trijssenaar, A., Van't Westende, Y. A. M., Hartog, F., and Van Loon, L. C. 1997. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol. Plant Microbe Interact. 10:716-724.
187. Van Wees, S. C. M., Luijendijk, M., Smoorenburg, I., Van Loon, L. C., and Pieterse, C. M. J. 1999. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on known defense-genes but stimulates the expression of the jasmonate-inducible gene ATVSP upon challenge. Plant Mol. Biol. 41:537-549.
188. Van Wees, S. C. M., De Swart, E. A. M., Van Pelt, J. A., Van Loon, L. C., and Pieterse, C. M. J. 2000. Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97:8711-8716.
189. Vanacker, H., Lu, H., Rate, D. N., and Greenberg, J. T. 2001. A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis. Plant J. 28:209-216.
190. Vetsch, M., Janzik, I., and Schaller, A. 2000. Characterization of prosystemin expressed in the baculovirus/insect cell system reveals biological activity of the systemin precursor. Planta 211:91-91.
191. Vian, A., Henry-Vian, C., Schantz, R., Ledoigt, G., Frachisse, J.-M., Desbiez, M.-O., and Julien, J.-L. 1996. Is membrane potential involved in calmodulin gene expression after external stimulation in plants? FEBS Lett. 380:93-96.
192. Vidal, S., Ponce De Léon, I., Denecke, J., and Palva, T. E. 1997. Salicylic acid and the plant pathogen Erwinia carotovora induce defense genes via antagonistic pathways. Plant J. 11:115-123.
193. Vijayan, P., Shockey, J., Levesque, C. A., Cook, R. J., and Browse, J. 1998. A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl. Acad. Sci. USA 95:7209-7214.
194. Walker-Simmons, M. K., and Ryan, C. A. 1977. Immunological identification of proteinase inhibitors I and II in isolated leaf vacuoles. Plant Physiol. 60:61-63.
195. Walling, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19:195-216.
196. Wang, C., Zien, C. A., Afitlhile, M., Welti, R., Hildebrand, D. F., and Wang, X. 2000. Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in Arabidopsis. Plant Cell 12:2237-2246.
197. Weymann, K., Hunt, M., Uknes, S., Neuenschwander, U., Lawton, K., Steiner, H.-Y., and Ryals, J. 1995. Suppression and restauration of lesion formation in Arabidopsis lsd mutants. Plant Cell 7:2013-2022.
198. Xu, Y., Chang, P.-F.-L., Liu, D., Narasimhan, M. L., Raghothama, K. G., Hasegawa, P. M., and Bressan, R. A. 1994. Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077-1085.
199. 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.
200. Ziegler, J., Keinänen, M., and Baldwin, I. 2001. Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuata. Phytochemistry 58:729-738.
201. Zimmerli, L., Jakab, G., Métraux, J. P., and Mauch-Mani, B. 2000. Potentiation of pathogenspecific defense mechanisms in Arabidopsis by beta-aminobutyric acid. Proc. Natl. Acad. Sci. USA 97:12920-12925.
202. Zimmerli, L., Métraux, J. P., and Mauch-Mani, B. 2001. β-aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol. 126:517-523.