Figure 2 RNA blot with a dose-response experiment on salicylic acid-regulated genes in tobacco. A tobacco cell line (BY-2) was treated with different concentrations of salicylic acid (SA) or flufenamate (Flu) and collected for RNA isolation 5 hours later. The blot was hybridized with two tobacco genes (88) of unknown function, which exhibit different induction patterns. Whereas salicylic acid strongly induces the G8-1 gene, flufenamate is largely inactive in this response. In contrast, the C14-1b gene shows a reversed gene induction pattern with weak induction by salicylic acid and a strong increase in mRNA caused by flufenamate. The equal loading was verified by rehybridi-zation of the blot with a gene for the tobacco histone 1 (H1).
3. LC Van Loon, A van Kämmen. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var "Samsun" and "Samsun NN." II Changes in protein constitution after infection with tobacco mosaic virus. Virology 40:199-211, 1970.
4. A Schlumbaum, F Mauch, U Vögeli, T Boiler. Plant chitinases are potent inhibitors of fungal growth. Nature 324:365-367, 1986.
5. S Kauffmann, M Legrand, P Geoffroy, B Fritig. Biological function of "path-ogenesis-related" proteins: four PR proteins of tobacco have 1,3-ß-glucanase activity. EMBO J 6:3209-3212, 1987.
6. M Legrand, S Kauffmann, P Geoffroy, B Fritig. Biological function of path-ogenesis-related proteins: four tobacco pathogenesis-related proteins are chitinases. Proc Natl Acad Sci USA 84:6750-6754, 1987.
7. LC Van Loon, EA Van Strien. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85-97, 1999.
8. JM Neuhaus, P Ahl-Goy, U Hinz, S Flores, F Meins Jr. High level expression of a tobacco chitinase gene in Nicotiana sylvestris. Plant Mol Biol 16:141151, 1991.
9. K Broglie, I Chet, M Holliday, R Cressman, P Biddle, S Knowlton, CJ Mauvais, R Broglie. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254:1194-1197, 1991.
10. Q Zhu, EA Mäher, S Massoud, RA Dixon, CJ Lamb. Enhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco. Biotechnology 12:807-812, 1994.
11. R Grison, B Grezes-Besset, M Schneider, N Lucante, L Olsen, JJ Leguay, A Toppan. Field tolerance to fungal pathogens of Brassica napus constitutively expressing a chimeric chitinase gene. Nat Biotechnol 14:643-646, 1996.
12. H Vierheilig, M Alt, JM Neuhaus, T Boiler, A Wiemken. Colonization of transgenic Nicotiana sylvestris plants, expressing different forms of Nicotiana tabacum chitinase, by the root pathogen Rhizoctonia solani and by the my-corrhizal symbiont Glomus mossae. Mol Plant Microbe Interact 6:261-264, 1993.
13. W Lin, CS Anuratha, K Datta, I Potrykus, S Muthukrishnan, SK Datta. Genetic engineering of rice for resistance to sheath blight. Biotechnology 13:686-691, 1995.
14. M Bliffeld, J Mundy, I Potrykus, J Fütterer. Genetic engineering of wheat for increased resistance to powdery mildew disease. Theor Appl Genet 98:10791086, 1999.
15. E Kombrink, IE Somssich. Pathogenesis-related proteins and plant defense. In: GC Carroll, P Tudzynski, eds. The Mycota V. Part A: Plant Relationships. Berlin: Springer, 1997, pp 107-128.
16. T Boiler. Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Plant Mol Biol 46:189-214, 1995.
17. J Ebel. Oligoglucoside elicitor-mediated activation of plant defense. Bioessays 20:569-576, 1998.
18. RA Dixon, CJ Lamb. Molecular communication in interactions between plants and microbial pathogens. Annu Rev Plant Physiol Plant Mol Biol 41:339-367, 1990.
19. RA Dixon, MJ Harrison, CJ Lamb. Early events in the activation of plant defense responses. Annu Rev Phytopathol 32:479-501, 1994.
20. D Alexander, RM Goodman, M Gut-Rella, C Glascock, K Weymann, L Friedrich, D Maddox, P Ahl-Goy, T Luntz, E Ward, J Ryals. Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein la. Proc Natl Acad Sci USA 90:7327-7331, 1993.
21. T Niderman, I Genetet, T Bruyère, R Gees, A Stintzi, M Legrand, B Fritig, E Môsinger. Pathogenesis-related PR-1 proteins are antifungal. Plant Physiol 108: 17-27, 1995.
22. K Datta, R Velazhahan, N Oliva, I Ona, T Mew, GS Khush, S Muthukrishnan, SK Datta. Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease. Theor Appl Genet 98:11381145, 1999.
23. B Zhu, THH Chen, PH Li. Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for an osmotin-like protein. Planta 198:70-77, 1996.
24. J Gôrlach, S Volrath, G Knauf-Beiter, G Hengy, U Beckhove, KH Kogel, M Oostendorp, T Staub, E Ward, H Kessmann, J Ryals. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629-643, 1996.
25. K Malek, A Levine, T Eulgem, A Morgan, J Schmid, KA Lawton, JL Dangl, RA Dietrich. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403-410, 2000.
26. RE Hancock, R Lehrer. Cationic peptides: a new source of antibiotics. Trends Biotechnol 16:82-88, 1998.
27. M Meister, C Hetru, JA Hoffmann. The antimicrobial host defense of Dro-sophila. Curr Top Microbiol Immunol 248:17-36, 2000.
28. JA Hoffmann, FC Kafatos, CA Janeway Jr, RAB Ezekowitz. Phylogenetic perspectives in innate immunity. Science 284:1313-1318, 1999.
29. FRG Terras, K Eggermont, V Kovaleva, NV Raikhel, RW Osborn, A Kester, SB Rees, S Torrekens, F van Leuven, J Vanderleyden, BPA Cammue, WF Broekaert. Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7:573-588, 1995.
30. JC Kader. Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 47:627-654, 1996.
31. FRG Terras, HME Schoofs, MFC De Bolle, F Van Leuven, SB Rees, J Vanderleyden, BPA Cammue, WF Broekart. Analysis of two novel classes of antifungal proteins from radish (Raphanus sativus L.) seeds. J Biol Chem 267: 15301-15309, 1992.
32. A Molina, F Garcia-Olmedo. Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins. Plant J 4:983-991, 1993.
33. A Molina, F García-Olmedo. Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J 12: 669-675, 1997.
34. H Bohlmann, S Clausen, S Behnke, H Giese, C Hiller, U Reimann-Philipp, G Schräder, V Barkholt, K Apel. Leaf-specific thionins of barley—a novel class of cell wall proteins toxic to plant pathogenic fungi and possibly involved in the defense mechanism of plants. EMBO J 7:1559-1565, 1988.
35. P Epple, K Apel, H Bohlmann. Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell 9: 509-520, 1997.
36. S Holtorf, J Ludwig-Müller, K Apel, H Bohlmann. High level expression of a viscotoxin in Arabidopsis thaliana gives enhanced resistance against Plasmo-diophora brassicae. Plant Mol Biol 36:673-680, 1998.
37. M Osusky, G Zhou, L Osuska, RE Hancock, WW Kay, S Misra. Transgenic plants expressing cationic peptide chimeras exhibit broad-spectrum resistance to phytopathogens. Nat Biotechnol 18:1162-1166, 2000.
38. F Stirpe, L Barbieri, MG Bateiii, M Soria, DA Lappi. Ribosome inactivating proteins from plants: present status and future prospects. Biotechnology 10: 405-412, 1992.
39. J Logemann, G Jach, H Tommerup, J Mundy, J Schell. Expression of a barley ribosome-inactivating protein leads to increased fungal protection in transgenic tobacco plants. Biotechnology 10:305-308, 1992.
40. O Zoubenko, F Uckun, Y Hur, I Chet, N Turner. Plant resistance to fungal infection by nontoxic pokeweed antiviral protein mutants. Nat Biotechnol 15: 992-996, 1997.
41. RL Nicholson, R Hammerschmidt. Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30:369-389, 1992.
42. JP Morrissey, AE Osbourn. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol Mol Biol Rev 63:708-724, 1999.
43. R Hain, HJ Reif, E Krause, R Langebartels, H Kindl, B Vornam, W Wiese, E Schmelzer, PH Schreier, RH Stöcker, K Stenzel. Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361:153-156, 1993.
44. J Thomzik, K Stenzel, R Stöcker, PH Schreier, R Hain, D Stahl. Synthesis of a grapevine phytoalexin in transgenic tomatoes (Lycopersicon esculentum Mill.) conditions resistance against Phytophthora infestans. Physiol Mol Plant Pathol 51:265-278, 1997.
45. P Stark-Lorenzen, B Nelke, G Hännsler, H Mühlbach, JE Thomzik. Transfer of a grapevine stilbene synthase gene to rice (Oryza sativa L.). Plant Cell Rep 16:668-673, 1997.
46. R Fischer, I Budde, R Hain. Stilbene synthase gene expression causes changes in flower colour and male sterility in tobacco. Plant J 11:489-498, 1997.
47. MC Verberne, R Verpoorte, JF Bol, J Mercado-Blanco, HJM Linthorst. Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nat Biotechnol 18:779-783, 2000.
48. H Cao, J Glazebrook, JD Clarke, S Volko, X Dong. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57-63, 1997.
49. JA Ryals, K Weymann, K Lawton, L Friedrich, D Ellis, HY Steiner, J Johnson, TP Delaney, T Jesse, P Vos, S Uknes. The Arabidopsis Niml protein shows homology to the mammalian transcription factor inhibitor I-kB. Plant Cell 9: 425-439, 1997.
50. J Shaw, F Tsui, DF Klessig. Characterization of a salicylic acid insensitive mutant (sail) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact 10: 69-78, 1997.
51. Y Zhang, W Fan, M Kinkema X Li, X Dong. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci USA 96:65236528, 1999.
52. H Cao, X Li, X Dong. 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, 1998.
53. R Tenhaken, A Levine, LF Brisson, RA Dixon, C Lamb. Function of the oxidative burst in hypersensitive disease resistance. Proc Natl Acad Sci USA 92: 4158-4163, 1995.
54. C Lamb, RA Dixon. The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251-275, 1997.
55. LF Brisson, R Tenhaken, CJ Lamb. Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703-1712, 1994.
56. O Otte, W Barz. The elicitor-induced oxidative burst in cultured chickpea cells drives the rapid insolubilization of two cell wall structural proteins. Planta 200: 238-246, 1996.
57. P Schweizer, A Christoffel, R Dudler. Transient expression of members of the germin-like gene family in epidermal cells of wheat confers disease resistance. Plant J 20:540-552, 1999.
58. R Vogelsang, E Berger, T Hagedom, U Muhlenbeck, R Tenhaken, W Barz. Characterization of metabolic changes involved in hypersensitive-like browning reactions of chickpea (Cicer arietinum L.) cell cultures following challenge by Ascochyta rabiei culture filtrate. Physiol Mol Plant Pathol 44:141-155, 1994.
59. A Levine, R Tenhaken, RA Dixon, CJ Lamb. H202 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583593, 1994.
60. S Chamnongpol, H Willekens, W Moeder, C Langebartels, H Jr Sandermann, M Van Montagu, D Inze, W Van Camp. Defense activation and enhanced pathogen tolerance induced by H202 in transgenic tobacco. Proc Natl Acad Sci USA 95:5818-5823, 1998.
61. H Du, DF Klessig. Role for salicylic acid in the activation of defense responses in catalase-deficient transgenic tobacco. Mol Plant Microbe Interact 10:922925, 1997.
62. G Wu, BJ Shortt, EB Lawrence, EB Levine, KC Fitzsimmons, DM Shah. Disease resistance conferred by expression of a gene encoding H202 generating glucose oxidase in transgenic potato plants. Plant Cell 7:1357-1368, 1995.
63. G Wu, BJ Shortt, EB Lawrence, J Leon, KC Fitzsimmons, EB Levine, I Raskin, DM Shah. Activation of host defense mechanisms by elevated production of H202 in transgenic plants. Plant Physiol 115:427-435, 1997.
64. JL Dangl, RA Dietrich, MH Richberg. Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8:1793-1807, 1996.
65. C Richael, D Gilchrist. The hypersensitive response: a case of hold or fold? Physiol Mol Plant Pathol 55:5-12, 1999.
66. M Wolter, K Hollrichter, F Salamini, P Schulze-Lefert. The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defense mimic phenotype. Mol Gen Genet 239:122-128, 1993.
67. R Büschges, K Hollricher, R Panstruga, G Simons, M Wolter, A Frijters, R van Daelen, T van der Lee, P Diergaarde, J Groenendijk, S Töpsch, P Vos, F Salamini, P Schulze-Lefert. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695-705, 1997.
68. RA Dietrich, TP Delaney, SJ Uknes, ER Ward, JA Ryals, JL Dangl. Arabidopsis mutants simulating disease resistance response. Cell 77:565-577, 1994.
69. JT Greenberg, A Guo, DF Klessig, FM Ausubel. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551-563, 1994.
70. JT Greenberg. Programmed cell death in plant-pathogen interactions. Annu Rev Plant Physiol Plant Mol Biol 48:525-545, 1997.
71. RW Hartley. Barnase and barstar: two small proteins to fold and fit together. Trend Biochem Sci 14:450-454, 1988.
72. G Strittmatter, J Janssens, C Opsomer, J Botterman. Inhibition of fungal disease development in plants by engineering controlled cell death. Biotechnology 13: 1085-1089, 1995.
73. H Keller, N Pamboukdjian, M Ponchet, A Poupet, R Delon, JL Verrier, D Roby, P Ricci. Pathogen-induced elicitin production in transgenic tobacco generates a hypersensitive response and nonspecific disease resistance. Plant Cell 11: 223-235, 1999.
74. X Tang, M Xie, YJ Kim, J Zhou, DF Klessig GB Martin. Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11: 15-29, 1999.
75. KE Hammond-Kosack, S Tang, K Harrison, JDG Jones. The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product Avr9. Plant Cell 10:1251-1266, 1998.
76. TP Delaney, S Uknes, B Vernooij, L Friedrich, K Weymann, D Negrotto, T Gaffney, M Gut-Rella, H Kessmann, E Ward, JA Ryals. A central role of salicylic acid in plant disease resistance. Science 266:1247-1250, 1994.
77. L Friedrich, B Vernooij, T Gaffney, A Morse, J Ryals. Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol Biol 29:959-968, 1995.
78. K Weymann, M Hunt, S Uknes, U Neuenschwander, K Lawton, HY Steiner, J Ryals. Suppression and restoration of lesion formation in Arabidopsis Isd mutants. Plant Cell 7:2013-2022, 1995.
79. Z Chen, H Silva, DF Klessig. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883-1886, 1993.
80. J Dumer, DF Klessig. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci USA 92:11312-11316, 1995.
81. R Tenhaken, C Riibel. Salicylic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor. Plant Physiol 115:291-298, 1997.
82. A Ludwig, R Tenhaken. Defence gene expression in soybean is linked to the status of the cell death program. Plant Mol Biol 44:209-218, 2000.
83. R Tenhaken, C Anstatt, A Ludwig, K Seehaus. WY-14,643 and other agonists of the peroxisome proliferator-activated receptor reveal a new mode of action for salicylic acid in soybean disease resistance. Planta 212:888-895, 2001.
84. K Schoonjans, B Staels, J Auwerx. The peroxisome proliferator activated receptors (PPARs) and their effects on lipid metabolism and adipocyte differentiation. Biochim Biophys Acta 1302:93-109, 1996.
85. SA Kliewer, TM Willson. The nuclear receptor PPARy—bigger than fat. Curr Opin Genet Dev 8:576-581, 1998.
86. KA Lawton, L Friedrich, M Hunt, K Weymann, T Delaney, H Kessmann, T Staub, J Ryals. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10:71-82, 1996.
87. DM Horvath, NH Chua. Identification of an immediate-early salicylic acid-inducible tobacco gene and characterization of induction by other compounds. Plant Mol Biol 31:1061-1072, 1996.
88. DM Horvath, DJ Huang, NH Chua. Four classes of salicylate-induced tobacco genes. Mol Plant Microbe Interact 11:895-905, 1998.
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