Molecular communication in interactions between plants and microbial pathogens

Annual Review of Plant Physiology and Plant Molecular Biology

Volumn 41, Issue 1, 1990, Pages 339-367

  Dixon, Richard A ^a   Lamb, Christopher J ^b  

^a PLANT BIOLOGY DIVISION   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Avirulence genes; Defense genes; Disease resistance genes; Elicitors; Pathogenicity genes

Indexed keywords

EID: 0000720222     PISSN: 10402519     EISSN: None     Source Type: Journal    
DOI: 10.1146/annurev.pp.41.060190.002011     Document Type: Article

References (126)

1. - generation during a bacterially induced hypersensitive reaction in tobacco: deterioration of membrane lipids. Physiol. Mol. Plant Pathol. 34:13-26
2. An, G., Mitra, A., Choi, H. K., Costa, M. A., An, K., et al. 1989. Functional analysis of the 3′ control region of the potato wound-inducible proteinase inhibitor II gene. The Plant Cell 1:115-22
3. Anderson, A. J. 1989. The biology of glycoproteins as elicitors. In Plant:Microbe Interactions: Molecular and Genetic Perspectives, ed. T. Kosuge, E. W. Nester, 3:87-130. New York: McGraw-Hill
4. Apostol, I., Heinstein, P. F., Low, P. S. 1989. Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Plant Physiol. 90:109-16
5. Baydoun, E. A.-H., Fry, S. C. 1985. The immobility of pectic substances in injured tomato leaves and its bearing on the identity of the wound hormone. Planta 165:269-76
6. Bennetzen, J. L., Qin, M.-M., Ingels, S., Ellingboe, A. H. 1989. Allelespecific and Mutator-associated instability at the Rp1 disease-resistance locus of maize. Nature 332:369-70
7. Binns, A. N., Chen, R. H., Wood, H. N., Lynn, D. G. 1987. Cell division promoting activity of naturally occurring dehydrodiconiferyl glucosides: Do cell wall components control cell division? Proc. Natl. Acad. Sci. USA 84:980-84
8. Bohlmann, H., Clausen, S., Behuke, S., Giese, H., Hiller, C., et al. 1988. 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. 7:1559-65
9. Bolwell, G. P., Mavandad, M., Millar, D. J., Edwards, K. H., Schuch, W., Dixon, R. A. 1989. Inhibition of mRNA levels and activities by trans-cinnamic acid in elicitor-induced bean cells. Phytochemistry 27:2109-17
10. Bowler, C., Alliotte, T., DeLoose, M., Van Montagu, M., Inze, D. 1989. The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. EMBO J. 8:31-38
11. Breitender, H., Pettenburger, K., Bito, A., Valenta, R., Kraft, D., et al. 1989. The gene coding for the major birch pollen allergen Betvl is highly homologous to a pea disease resistance response gene. EMBO J. 8: 1935-38
12. Broglie, K. E., Biddle, P., Cressman, R., Broglie, R. 1989. Functional analysis of DNA sequences responsible for ethylene regulation of a bean chitinase gene in transgenic tobacco. The Plant Cell 1:599-607
13. Cervone, F. C., Hahn, M. G., De Lorenzo, G., Darvill, A., Albersheim, P. 1989. Host-pathogen interactions. XXXIII. A plant protein converts a fungal pathogenesis factor into an elicitor of plant defense responses. Plant Physiol. 90:542-48
14. Chappell, J., Hahlbrock, K., Boller, T. 1984. Rapid induction of ethylene biosynthesis in cultured parsley cells by fungal elicitor and its relationship to the induction of phenylalanine ammonialyase. Planta 161:475-80
15. Cloud, A. M. E., Deverall, B. J. 1987. Induction and expression of systemic resistance to the anthracnose disease of bean. Plant Pathol. 36:551-57
16. Colling, C., Hahlbrock, K., Scheel, D. 1989. Studies on signal transduction in plant defense gene activations. NATO Int. Symp. Signal Perception and Transduction in Higher Plants, Toulouse, July 9-13, 1989 (Abstr.)
17. Conrath, U., Domard, A., Kauss, H. 1989. Chitosan-elicited synthesis of callose and of coumarin derivatives in parsley cell suspension cultures. Plant Cell Rep. 8:152-55
18. Cosio, E. G., Popperl, H., Schmidt, W. E., Ebel, J. 1988. High-affinity binding of fungal glucan fragments to soybean (Glycine max L.) microsomal fractions and protoplasts. Eur. J. Biochem. 175:309-15
19. Cramer, C. L., Edwards, K., Dron, M., Liang, X., Dildine, S. L., et al. 1989. Phenylalanine ammonia-lyase gene organization and structure. Plant Mol. Biol. 12:367-83
20. Dangl, J. L., Hanfle, K. D., Lipphardt, S., Hahlbrock, K., Scheel, D. 1987. Parsley protoplasts retain differential responsiveness to u.v. light and fungal elicitor. EMBO J. 6:2551-56
21. Daniels, M. J., Dow, J. M., Osbourn, A. E. 1988. Molecular genetics of pathogenicity in phytopathogenic bacteria. Annu. Rev. Phytopathol. 26:285-312
22. Darvill, A. G., Albersheim, P. 1984. Phytoalexins and their elicitors - a defense against microbial infection in plants. Annu. Rev. Plant. Physiol. 35: 243-75
23. Davis, K. R., Hahlbrock, K. 1987. Induction of defense responses in cultured parsley cells by plant cell wall fragments. Plant Physiol. 85:1286-90
24. Davis, K. R., Darvill, A. G., Albersheim, P. 1986. Host-pathogen interactions. XXXI. Several biotic and abiotic elicitors act synergistically in the induction of phytoalexin accumulation in soybean. Plant Mol. Biol. 6:23-32
25. Dean, R. A., Kuc', J. 1986. Induced systemic protection in cucumbers: the source of the "signal". Physiol. Mol. Plant Pathol. 28:227-33
26. Dixon, R. A., Harrison, M. J. 1990. Activation, structure and organization of genes involved in microbial defense in plants. Adv. Genet. In press
27. Doherty, H. M., Selvendran, R. R., Bowles, D. J. 1988. The wound response of tomato plants can be inhibited by aspirin and related hydroxy-benzoic acids. Physiol. Mol. Plant Pathol. 33:377-84
28. Doke, N., Chai, H. B. 1985. Activation of superoxide generation and enhancement of resistance against compatible races of Phytophthora infestons in potato plants treated with digitonin. Physiol. Plant Pathol. 27:323-34
29. Doke, N., Garas, N. A., Kuc', J. 1979. Partial characterization and aspects of the mode of action of a hypersensitivity-inhibiting factor (HIF) isolated from Phytophthora infestons. Physiol. Plant Pathol. 15:127-40
30. Doubrava, N. S., Dean, R. A., Kuc', J. 1988. Induction of systemic resistance to anthracnose caused by Colletotrichum lagenarium in cucumber by oxalate and extracts from spinach and rhubarb leaves. Physiol. Mol. Plant Pathol. 33:69-79
31. Downie, J. A., Johnston, A. W. B. 1986. Nodulation of legumes by Rhizobium: The recognized root? Cell 47:153-54
32. Dron, M., Clouse, S. D., Lawton, M. A., Dixon, R. A., Lamb, C. J. 1988. Glutathione and fungal elicitor regulation of a plant defense gene promoter in electroporated protoplasts. Proc. Natl. Acad. Sci. USA 85:6738-42
33. Ebel, J. 1986. Phytoalexin synthesis: the biochemical analysis of the induction process. Annu. Rev. Phytopathol. 24: 235-64
34. Ebel, J. 1989. Elicitor-binding proteins and signal transduction in elicitor action. J. Cell Biochem. 13D (Suppl.):248
35. Eberhard, S., Doubrava, N., Marfa, B., Mohnen, D., Southwick, A., et al. 1989. Pectic cell wall fragments regulate tobacco thin-cell-layer explant morphogenesis. The Plant Cell 1:747-55
36. Ecker, J. R., Davis, R. W. 1987. Plant defense genes are regulated by ethylene. Proc. Natl. Acad. Sci. USA 84:5202-6
37. Ellingboe, A. H. 1981. Changing concepts in host-pathogen genetics. Annu. Rev. Phytopathol. 19:125-43
38. Farmer, E. E., Pearce, G., Ryan, C. A. 1989. In vitro phosphorylation of plant plasma membrane proteins in response to the proteinase inhibitor inducing factor. Proc. Natl. Acad. Sci. USA 86: 1539-42
39. Fedoroff, N. V. 1989. About maize transposable elements and development. Cell 56:181-91
40. Gottstein, H. D., Kuc', J. 1989. Induction of systemic resistance to anthracnose in cucumber by phosphates. Phytopathology 79:176-79
41. Green, P. J., Yong, M.-H., Cuozzo, M., Kano-Murakami, Y., Silverstein, P., Chua, N.-H. 1988. Binding site requirements for pea nuclear protein factor GT-1 correlate with sequences required for light-dependent transcriptional activation of the rbcS-3A gene. EMBO J. 7:4035-44
42. Grimm, C., Panopoulos, N. J. 1989. The predicted protein product of a pathogenicity locus from Pseudomonas syringae pv. phaseolicola is homologous to a highly conserved domain of several procaryotic regulatory proteins. J. Bacteriol. 171:5031-38
43. Hahlbrock, K., Scheel, D. 1989. Physiology and molecular biology of phenylpropanoid metabolism. Annu. Rev. Plant Phvsiol. Plant Mol. Biol. 40:347-64
44. Hahn, M. G., Grisebach, H. 1983. Cyclic AMP is not involved as a second messenger in the response of soybean to infection by Phytophthora megasperma f. sp. glycinea. Z. Naturforsch. 38C: 578-82
45. Hahn, M. G., Bucheli, P., Cervone, F., Doares, S. H., O'Neill, R. A., et al. 1989. Roles of cell wall constituents in plant-pathogen interactions. See Ref. 3, pp. 131-81
46. Hamdan, M. A. M. S., Dixon, R. A. 1987. Differential patterns of protein synthesis in bean cells exposed to elicitor fractions from Colletotrichum lindemuthianum. Physiol. Mol. Plant Pathol. 31:105-21
47. +-ATPase) of Arabidopsis thaliana. Proc. Natl. Acad. Sd. USA 86:1234-38
48. Hughes, R. K., Dickerson, A. G. 1989. The effect of ethylene on phenylalanine ammonia-lyase (PAL) induction by a fungal elicitor in Phaseolus vulgaris. Physiol. Mol. Plant Pathol. 34:361-78
49. Huynh, T. V., Dahlbeck, D., Staskawicz, B. J. 1989. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245:1374-77
50. Jacobs, M., Rubery, P. H. 1988. Naturally occurring auxin transport regulators. Science 241:346-49
51. Katagiri, F., Lam, E., Chua, N.-H. 1989. Two tobacco DNA-binding proteins with homology to the nuclear factor CREB. Nature 340:727-29
52. Kaufmann, S., Legrand, M., Geoffroy, P., Fritig, B. 1987. Biological functions of "pathogenesis-related" proteins: Four PR proteins of tobacco have 1.3-β-glucanase activity. EMBO J. 6:3209-12
53. Kauss, H., Jeblick, W., Domard, A. 1989. The degrees of polymerization and N-acetylation of chitosan determine its ability to elicit callose formation in suspension cells and protoplasts of Catharanthus roseus. Planta 178:385-92
54. Kearney, B., Ronald, P. C., Dahlbeck, D., Staskawicz, B. J. 1988. Molecular basis for evasion of plant host defense in bacterial spot disease of pepper. Nature 332:541-43
55. Keen, N. T., Staskawicz, B. 1988. Host range determinants in plant pathogens and symbionts. Annu. Rev. Microbiol. 42:421-40
56. Keen, N. T., Kobayashi, D., Tamaki, S., Thordal-Christensen, H., Masaghi, I., et al. 1988. In Molecular Genetics of Plant-Microbe Interactions, ed. R. Palacios, D. P. S. Verma, pp 15-19. Minneapolis: APS Press
57. Keller, B., Schmid, J., Lamb, C. J. 1989. Vascular expression of a bean cell wall glycine-rich protein-β-glucuronidase gene fusion in transgenic tobacco. EMBO J. 8:1309-14
58. Keller, B., Lamb, C. J. 1989. Specific expression of a novel cell wall hydroxyproline-rich glycoprotein gene in lateral root initiation. Genes Devel. 3:1639-46
59. Kendra, D. F., Hadwiger, L. A. 1987. Calcium and calmodulin may not regu-late the disease resistance and pisatin formation responses of Pisum sativum to chitosan or Fusarium solani. Physiol. Mol. Plant Pathol. 31:337-48
60. Kessmann, H., Barz, W. 1986. Elicitation and suppression of phytoalexin and isoflavone accumulation in cotyledons of Cicer arietinum L. as caused by wounding and by polymeric components from the fungus Ascochyta rabiei. J. Phytopathol. 117:321-35
61. Kobayashi, D. Y., Tamaki, S. J., Keen, N. T. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. USA 86:157-61
62. +2-dependent process. Plant Physiol. 77:544-S1
63. Kolattukudy, P. E., Podila, G. K., Mohan, R. 1989. Molecular basis of the early events in plant-fungus interaction. Genome 31:342-49
64. Kombrink, E., Schröder, M., Hahlbrock, K. 1988. Several "pathogenesisrelated" proteins in potato are l,3-β glucanases and chitinases. Proc. Natl. Acad. Sci. USA 85:782-86
65. Kurosaki, F., Tsurukawa, Y., Nishi, A. 1987. Breakdown of phosphatidyl inositol during the elicitation of phytoalexin production in cultured carrot cells. Plant Physiol. 85:601-4
66. Kurosaki, F., Tsurukawa, Y., Nishi, A. 1987. The elicitation of phytoalexins by Ca2+ and cyclic AMP in carrot cells. Photochemistry 26:1919-23
67. Lamb, C. J., Lawton, M. A., Dron, M., Dixon, R. A. 1989. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56:215-24
68. Lawton, M. A., Yamamoto, R. T., Hanks, S. K., Lamb, C. J. 1989. Molecular cloning of plant transcripts encoding protein kinase homologs. Proc. Natl. Acad. Sci. USA 86:3140-44
69. Lawton, M. A., Clouse, S. D., Lamb, C. J. 1990. Glutathione-elicited changes in chromatin configuration in the promoter of the plant defense gene encoding chalcone synthase. Plant Cell Rep. In press
70. Legrand, M., Kauffmann, S., Geoffroy, P., Fritig, B. 1987. Biological function of pathogenesis-related proteins: four tobacco pathogenesis-related proteins are chitinases. Proc. Natl. Acad. Sci. USA 84:6750-54
71. Liang, X., Dron, M., Cramer, C. L., Dixon, R. A., Lamb, C. J. 1989. Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J. Biol. Chem. 264:14486-92
72. Liang, X., Dron, M., Schmid, J., Dixon, R. A., Lamb, C. J. 1989. Developmental and environmental regulation of a phenylanine ammonia-lyase: β glucuronidase gene fusion in transgenic tobacco plants. Proc. Natl. Acad. Sci. USA 86:9284-88
73. Lincoln, J. E., Fischer, R. L. 1988. Diverse mechanisms for the regulation of ethylene-inducible gene expression. Mol. Gen. Genet. 212:71-75
74. Lindgren, P. B., Panopoulos, N. J., Staskawicz, B. J., Dahlbeck, D. 1988. Genes required for pathogenicity and hypersensitivity are conserved and interchangeable among pathovars of Pseudomonas syringae. Mol. Gen. Genet. 211:499-506
75. Logemann, J., Lipphardt, S., Lörz, H., Häuser, I., Willmitzer, L., Schell, J. 1989. 5′ Upstream sequences from the wunl gene are responsible for gene activation by wounding in transgenic plants. The Plant Cell 1:151-58
76. Lois, R., Dietrich, A., Hahlbrock, K., Schulz, W. 1989. A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J. 8:1641-48
77. Matsui, M., Sasamoto, S., Kunieda, T., Nomura, N., Ishizaki, R. 1989. Cloning of ara, a putative Arabidopsis thaliana gene homologous to the raj-related gene family. Gene 76:313-19
78. Mauch, F., Staehlin, L. A. 1989. Functional implications of the subcellular localization of ethylene-induced chitinase and β-1,3-glucanase in bean leaves. The Plant Cell 1:447-57
79. Mayer, M. G., Ziegler, E. 1988. An elicitor from Phytophthora megasperma f. sp. glycinea influences the membrane potential of soybean cotyledonary cells. Physiol. Mol. Plant Pathol. 33:397-407
80. Meeks-Wagner, D. R., Dennis, E. S., Thanh Van, K. T., Peacock, W. J. 1989. Tobacco genes expressed during in vitro floral initiation and their expression during normal development. The Plant Cell 1:25-35
81. Meister, A., Anderson, M. E. 1983. Glutathione. Annu. Rev. Biochem. 52:711-60
82. 2+ -stimulated polyphosphoinositide phospholipase C in isolated plant plasma membranes. FEBS Lett. 223:87-91
83. Memelink, J., Hoge, J. H. C., Schilperoort, R. A. 1987. Cytokinin stress changes the developmental regulation of several defense-related genes in tobacco. EMBO J. 6:3579-84
84. Metraux, J. P., Burkhart, W., Moyer, M., Dincher, S., Middlesteadt, W., et al. 1989. Isolation of a complementary cDNA encoding a chitinase with a structural homology to a bifunctional lysozyme/chitinase. Proc. Natl. Acad. Sci. USA 86:896-900
85. Moreau, R. A., Osman, S. F. 1989. The properties of reducing agents released by treatment of Solanum tuberosum with elicitors from Phytophthora infestons. Physiol. Mol. Plant Pathol. 35:1-10
86. Myerowitz, E. M. 1989. Arabidopsis, a useful weed. Cell 56:263-69
87. Parker, J. E., Hahlbrock, K., Scheel, D. 1988. Different cell wall components from Phytophthora megasperma f. sp. glycinea elicit phytoalexin production in soybean and parsley. Planta 176:75-82
88. Parsons, K. A., Chumley, F. G., Valent, B. 1987. Genetic transformation of the fungal pathogen responsible for rice blast disease. Proc. Natl. Acad. Sci. USA 84:4161-65
89. Peever, T. L., Higgins, V. J. 1989. Suppression of the activity of nonspecific elicitor from Cladosporium fulvum by intercellular fluids from tomato leaves. Physiol. Mol. Plant Pathol. 34:471-82
90. Pena-Cortes, H., Prat, S., Sanchez-Serrano, J. J., Willmitzer, L. 1989. The wound-induced expression of the proteinase inhibitor II gene in potato and tomato plants is mediated by abscisic acid. NATO Int. Symp. Signal Perception and Transduction in Higher Plants, Toulouse, July 9-13, 1989 (Abstr.)
91. Pfaffmann, H., Hartmann, E., Brightman, A. O., Morré, D. J. 1987. Phosphatidylinositol specific phospholipase C of plant stems. Plant Physiol. 85:1151-55
92. Podila, G. P., Dickman, M. B., Kolattukudy, P. E. 1988. Transcriptional activation of a cutinase gene in isolated fungal nuclei by plant cutin monomers. Science 242:922-25
93. Pryor, A. 1987. The origin and structure of fungal disease resistance genes in plants. Trends Genet. 3:157-61
94. Ranjeva, R., Boudet, A. M. 1987. Phosphorylation of proteins in plants: Regulatory effects and potential involvement in stimulus/response coupling. Annu. Rev. Plant Physiol. 38:73-93
95. Ricci, P., Bonnet, P., Huet, J.-C., Sallantin, M., Beauvais-Cante, F., et al. 1989. Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. Eur. J. Biochem. 183:555-63
96. Rick, C. M. 1982. Linkage map of the tomato (Lycopersicon esculentum). Genet. Maps 2:360-65
97. Ronson, C. W., Nixon, B. T., Ausubel, F. M. 1987. Conserved domains in bacterial regulatory proteins that respond to environmental stimuli. Cell 49:579-81
98. Ryan, C. A. 1988. Oligosaccharides as recognition signals for the expression of defensive genes in plants. Biochemistry 27:8879-83
99. Salzwedel, J. L., Daub, M. E., Huag, J. 1989. Effects of singlet oxygen quenchers and pH on the bacterially induced hypersensitive reaction in tobacco suspension cell cultures. Plant Physiol. 90:25-28
100. Sato, T., Theologis, A. 1989. Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate synthase, the key enzyme for ethylene biosynthesis in plants. Proc. Natl. Acad. Sci. USA 86:6621-25
101. Scherer, G. F. E., Martiny-Baron, G., Stoffel, B. 1988. A new set of regulatory molecules in plants: A plant phospholipid similar to platelet-activating factor stimulates protein kinase and proton-translocating ATPase in membrane vesicles. Planta 175:241-53
102. Schottens-Toma, I. M. J., de Wit, P. J. G. M. 1988. Purification and primary structure of a necrosis-inducing peptide from the apoplastic fluids of tomato infected with Cladosporium fulvum (sym. Fulvia fulva). Physiol. Mol. Plant Pathol. 33:59-67
103. Schroeder, J. I., Hagiwara, S. 1989. Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338:427-30
104. Schulze-Lefert, P., Becker-Andre, M., Schulz, W., Hahlbrock, K., Dangl, J. L. 1989. Functional architecture of the light-responsive chalcone synthase promoter from parsley. The Plant Cell 1:707-14
105. Sharp, J. K., Albersheim, P., Ossowski, P., Pilotti, A., Garegg, P., Lindberg, B. 1984. Comparison of the structures and elicitor activities of a synthetic and a mycelial-wall-derived hexa-(β-D-glucopyranosyl)-D-glucitol. J. Biol. Chem. 259:11341-45
106. Sinshi, H., Mohnen, D., Meins, F. Jr. 1987. Regulation of a plant pathogenesis-related enzyme: Inhibition of chitinase and chitinase mRNA accumulation in cultured tobacco tissues by auxin and cytokinin. Proc. Natl. Acad. Sci. USA 84:89-92
107. 2+ on phytoalexin induction by fungal elicitor in soybean cells. Arch. Biochem. Biophys. 257:416-23
108. Stachel, S. E., Zambryski, P. C. 1986. Agrobacterium tumefaciens and the susceptible plant cell: a novel adaptation of extracellular recognition and DNA conjugation. Cell 47:155-57
109. Stanford, A., Bevan, M., Northcote, D. 1989. Differential expression within a family of novel wound-induced genes in potato. Mol. Gen. Genet. 215:200-8
110. Stayton, M., Tamaki, S., Kobayashi, D., Keen, N. 1989. A cultivar-specific elicitor of the hypersensitive response in soybean has been identified and may be the signal molecule that interacts with the plant disease resistance gene product to trigger host defense. J. Cell Biochem. Suppl. 13D:326
111. Steffens, M., Ettle, F., Kranz, D., Kindl, H. 1989. Vanadate mimics effects of fungal cell wall in eliciting gene activation in plant cell cultures. Planta 177:160-68
112. Strasser, H., Hoffmann, C., Grisebach, H., Matern, U. 1986. Are polyphosphoinositides involved in signal transduction of elicitor-induced phytoalexin synthesis in cultured plant cells? Z. Naturforsch. 41C:717-24
113. Tamaki, S., Dahlbeck, D., Staskawicz, B., Keen, N. T. 1988. Characterization and expression of two avirulence genes cloned from Pseudomonas syringae pv. glycinea. J. Bacteriol. 170:4846-54
114. Templeton, M. D., Lamb, C. J. 1988. Elicitors and defense gene activation. Plant, Cell and Environ. 11:395-401
115. Tepper, C. S., Albert, F. G., Anderson, A. J. 1989. Differential mRNA accumulation in three cultivais of bean in response to elicitors from Colletotrichum lindemuthianum. Physiol. Mol. Plant Pathol. 34:85-98
116. Tepper, C. S., Anderson, A. J. 1986. Two cultivars of bean display a differential response to extracellular components from Colletotrichum lindemuthianum. Physiol. Mol. Plant Pathol. 29:411-20
117. Timberlake, W. E., Marshall, M. A. 1989. Genetic engineering of filamentous fungi. Science 244:1313-17
118. Tomiyama, K., Okamoto, H., Katou, K. 1983. Effect of infection by Phytophthora infestans on the membrane potential of potato cells. Physiol. Plant Pathol. 22:233-43
119. Wang, J., Holden, D. W., Leong, S. A. 1988. Gene transfer systems for the phytopathogenic fungus Ustilago maydis. Proc. Natl. Acad. Sci. USA 85:865-69
120. Weltring, K.-M., Turgeon, B. G., Yoder, O. C., VanEtten, H. D. 1988. Isolation of a phytoalexin-detoxification gene from the plant pathogenic fungus Nectria haematococca by detecting its expression in Aspergillus nidulans. Gene 68:335-44
121. Whalen, M. C., Stall, R. E., Staskawicz, B. J. 1988. Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. Proc. Natl. Acad. Sci. USA 85:6743-47
122. Wijesundera, R. L. C., Bailey, J. A., Byrde, R. J. W., Fielding, A. H. 1989. Cell wall degrading enzymes of Colletotrichum lindemuthianum: their role in the development of bean anthracnose. Physiol. Mol. Plant Pathol. 34:403-13
123. Wingate, V. P. M., Lawton, M. A., Lamb, C. J. 1988. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 87:206-10
124. Winterbourn, C. C. 1989. Inhibition of autoxidation of divicine and isouramil by the combination of superoxide dismutase and reduced glutathione. Arch. Biochem. Biophys. 271:447-55
125. Wolpert, T. J., Macko, V. 1989. Specific binding of victorin to a 100 kDa protein from oats. Proc. Natl. Acad. Sci. USA 86:4092-96
126. Yamada, T., Hashimoto, H., Shiraishi, T., Oku, H. 1989. Suppression of pisatin, phenylalanine ammonia-lyase mRNA, and chalcone synthase mRNA accumulation by a putative pathogenicity factor from the fungus Mycosphaerella pinodes. Mol. Plant Microbe Int. 2:256-61