The role of thionins in the resistance of plants

Pathogenesis-Related Proteins in Plants

Volumn , Issue , 1999, Pages 207-234

  Bohlmann, Holger ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0009129319     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9781420049299     Document Type: Chapter

References (216)

1. Ride, J. P., Non-host resistance to fungi, in Mechanisms of Resistance to Plant Diseases, Fraser, R. S. S., Ed., Martinus Nijhoff/Dr. W. Junk, Dordrecht, The Netherlands, 1985, 29.
2. Harborne, J. B., Introduction to Ecological Biochemistry, Academic Press, London, 1988.
3. Dixon, R. A., The phytoalexin response: elicitation, signalling and control of host gene expression, Biol. Rev., 61, 239, 1986.
4. Linthorst, H. J. M., Pathogenesis-related proteins of plants, Crit. Rev. Plant Sci., 10, 123, 1991.
5. Aist, J. R., Structural responses as resistance mechanisms, in The Dynamics of Host Defense, Bailey, J. A., Ed., Academic Press, New York, 1983, 33.
6. Brisson, L. F., Tenhaken, R., and Lamb, C., Functions of oxidative cross-linking of cell wall structural proteins in plant disease resistance, Plant Cell, 6, 1703, 1994.
7. Dangl, J. L., Dietrich, R. A., and Richberg, M. H., Death don’t have no mercy: cell death programs in plant-microbe interactions, Plant Cell, 8, 1793, 1996.
8. Mittler, R. and Lam, E., Sacrifice in the face of foes: pathogen-induced programmed cell death in plants, Trends Microbiol., 4, 10, 1996.
9. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G. Uknes, S., Ward, E., Kessmann, H., and Ryals, J., Requirement of salicylic acid for the induction of systemic acquired resistance, Science, 261, 754, 1993.
10. Hunt, M. D. and Ryals, J. A., Systemic acquired resistance signal transduction, Crit. Rev. Plant Sci., 15, 583, 1996.
11. Doares, S. H., Syrovets, T., Weiler, E. W., and Ryan, C., Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway, Proc. Natl. Acad. Sci. U.S.A., 92, 4095, 1995.
12. Peña-Cortés, H., Fisahn, J., and Willmitzer, L., Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants, Proc. Natl. Acad. Sci. U.S.A., 92, 4106, 1995.
13. Pearce, G., Strydom, D., Johnson, S., and Ryan, C., A polypeptide from tomato leaves activates the expression of proteinase inhibitor genes, Science, 253, 895, 1991.
14. Farmer, E. E. and Ryan, C., Interplant communication. Airborne methyl jasmonate induces synthesis of wound-inducible proteinase inhibitors in plant leaves, Proc. Natl. Acad. Sci. U.S.A., 87, 7713, 1990.
15. Hancock, R. E. W., Falla, T., and Brown, M., Cationic bactericidal peptides, Adv. Microb. Physiol., 37, 135, 1995.
16. Nicolas, P. and Mor, A., Peptides as weapons against microorganisms in the chemical defense system of vertebrates, Annu. Rev. Microbiol., 49, 277, 1995.
17. García-Olmedo, F., Molina, A., Segura, A., and Moreno, M., The defensive role of nonspecific lipid-transfer proteins in plants, Trends Microbiol., 3, 72, 1995.
18. Terras, F. R. G., Eggermont, K., Kovaleva, V., Raikhel, N. V., Osborn, R. W., Kester, A., Rees, S. B. Torrekens, S., Van Leuven, F., Vanderleyden, J., Cammue, B. P. A., and Broekaert, W. F., Small cysteine-rich antifungal proteins from radish: their role in host defense, Plant Cell, 7, 573, 1995.
19. García-Olmedo, F., Rodriguez-Palenzuela, P., Hernandez-Lucas, C., Ponz, F., Marana, C., Carmona, J. J., Lopez-Fando, J., Fernandez, J. A., and Carbonero, P., The thionins: a protein family that includes purothionins, viscotoxins and crambins, Oxf. Surv. Plant Mol. Cell Biol., 6, 31, 1989.
20. Bohlmann, H. and Apel, K., Thionins, Annu. Rev. Plant Phys. Plant Mol. Biol., 42, 227, 1991.
21. Bohlmann, H., The role of thionins in plant protection, Crit. Rev. Plant Sci., 13, 1, 1994.
22. Florack, D. E. A. and Stiekema, W. J., Thionins: properties, possible biological roles, and mechanisms of action, Plant Mol. Biol., 26, 25, 1994.
23. Ohtani, S., Okada, T., Yoshizumi, H., and Kagamiyama, H., Complete primary structures of two subunits of purothionin A, a lethal protein for brewer’s yeast from wheat flour, J. Biochem., 82, 53, 1977.
24. Balls, A. K. and Hale, W. S., A sulphur-bearing constituent of the petroleum ether extract of wheat flour (preliminary report), Cereal Chem., 17, 43, 1940.
25. Balls, A. K., Hale, W. S., and Harris, T. H., A crystalline protein obtained from a lipoprotein of wheat flour, Cereal Chem., 19, 79, 1942.
26. Jones, B. L. and Mak, A. S., Amino acid sequences of the two α-purothionins of hexaploid wheat, Cereal Chem., 54, 11, 1977.
27. Ohtani, S., Okada, T., Kagamiyama, H., and Yoshizumi, H., The amino acid sequence of purothionin A, a lethal toxic protein for brewer’s yeasts from wheat, Agric. Biol. Chem., 39, 2269, 1975.
28. Mak, A. S. and Jones, B. L., The amino acid sequence of wheat ß-purothionin, Can. J. Biochem., 22, 835, 1976.
29. Bekes, F. and Lasztity, R., Isolation and determination of amino acid sequence of avenothionin, a new purothionin analogue from oat, Cereal Chem., 58, 360, 1981.
30. Ponz, F., Paz-Ares, J., Hernandez-Lucas, C., García-Olmedo, F., and Carbonero, P., Cloning and nucleotide sequence of a cDNA encoding the precursor of the barley toxin α-hordothionin, Eur. J. Biochem., 156, 131, 1986.
31. Rodriguez-Palenzuela, P., Pintor-Toro, J. A., Carbonero, P., and García-Olmedo, F., Nucleotide sequence and endosperm-specific expression of the structural gene for the toxin α-hordothionin in barley (Hordeum vulgare L.), Gene, 70, 271, 1988.
32. Hernandez-Lucas, C., Royo, J., Paz-Ares, J., Poz, F., García-Olmedo, F., and Carbonero, P., Polyadenylation site heterogeneity in mRNA encoding the precursor of the barley toxin ß-hordothionin, FEBS Lett., 200, 103, 1986.
33. Castagnaro, A., Marana, C., Carbonero, P., and García-Olmedo, F., Extreme divergence of a novel wheat thionin generated by a mutational burst specifically affecting the mature protein domain of the precursor, J. Mol. Biol., 224, 1003, 1992.
34. Castagnaro, A., Segura, A. and García-Olmedo, F., High conservation among sequences encoding type-V thionins in wheat and Aegilops, Plant Physiol., 107, 1475, 1995.
35. Bohlmann, H. and Apel, K., Isolation and characterization of cDNAs coding for leafspecific thionins closely related to the endosperm-specific hordothionin of barley (Hordeum vulgare L.), Mol. Gen. Genet., 207, 446, 1987.
36. Gausing, K., Thionin genes specifically expressed in barley leaves, Planta, 171, 241, 1987.
37. De Boer, D. A. D., Tulipa gesneriana thionin cDNAs, EMBL database, 1994.
38. Carbonero, P. and García-Olmedo, F., Purothionins in Aegilops-Triticum spp., Experientia, 25, 1110, 1969.
39. Redman, D. G. and Fisher, N., Purothionin analogues from barley flour, J. Sci. Food Agric., 20, 427, 1969.
40. Fernandez de Caleya, R., Hernandez-Lucas, C., Carbonero, P., and García-Olmedo, F., Gene expression in alloploids: genetic control of lipopurothionins in wheat, Genetics, 83, 687, 1976.
41. Hernandez-Lucas, C., Carbonero, P., and García-Olmedo, F., Identification and purification of a purothionin homologue from rye (Secale cereale L.), J. Agric. Food Chem., 26, 794, 1978.
42. Jones, B. L., Lookhart, G. L., Mak, A. S., and Cooper, D. B., Sequences of purothionins and their inheritance in diploid, tetraploid, and hexaploid wheats, J. Hered., 73, 143, 1982.
43. Wada, K., Localization of purothionins and genome expression in wheat plants, Plant Cell Physiol., 23, 1357, 1982.
44. Jones, B. L. and Cooper, D. B., Purification and characterization of a corn (Zea mays) protein similar to purothionins, J. Agric. Food Chem., 28, 904, 1980.
45. Wada, K. and Buchanan, B. B., Purothionins and related proteins: seed proteins with thioredoxin activity, in Thioredoxins. Structure and Function, Gadal, P., Ed., International Conference CNRS-NASA, Berkeley, CA, 1981, 213.
46. Duvick, J. P., Rood, T., Rao, A. G., and Marshak D. R., Purification and characterization of a novel antimicrobial peptide from maize (Zea mays L.) kernels, J. Biol. Chem., 267, 18814, 1992.
47. Vernon, L. P., Evett, G. E., Zeikus, R. D., and Gray, W. R., A toxic thionin from Pyrularia pubera: purification, properties, and amino acid sequence, Arch. Biochem. Biophys., 238, 18, 1985.
48. Schrader-Fischer, G. and Apel, K., cDNA-derived identification of novel thionin precursors in Viscum album that contain highly divergent thionin domains but conserved signal and acidic polypeptide domains, Plant Mol. Biol., 23, 1233, 1993.
49. Olson, T. and Samuelsson, G., The amino acid sequence of viscotoxin A2 from the European mistletoe (Viscum album L., Loranthaceae), Acta Chem. Scand., 26, 585, 1972.
50. Samuelsson, G., Seger, L., and Olson, T., The amino acid sequence of oxidized viscotoxin A3 from the European mistletoe (Viscum album L., Loranthaceae), Acta Chem. Scand., 22, 2624, 1968.
51. Schrader, G. and Apel, K., Isolation and characterization of cDNAs encoding viscotoxins of mistletoe (Viscum album), Eur. J. Biochem., 198, 549, 1991.
52. Samuelsson, G. and Pettersson, B., The amino acid sequence of viscotoxin B from the European mistletoe (Viscum album L., Loranthaceae), Eur. J. Biochem., 21, 86, 1971.
53. Samuelsson, G. and Jayawardene, A. L., Isolation and characterization of viscotoxin 1Ps from Viscum album L. ssp. austriacum (Wiesb.) Vollmann, growing on Pinus silvestris, Acta Pharmacol. Suecica, 11, 175, 1974.
54. Mellstrand, S. T. and Samuelsson, G., Phoratoxin, a toxic protein from the mistletoe Phoradendron tomentosum subsp. macrophyllum (Loranthaceae). The amino acid sequence, Acta Pharmacol. Suecica, 11, 347, 1974.
55. Thunberg, E., Phoratoxin B, a toxic protein from the mistletoe Phoradendron tomentosum subsp. macrophyllum, Acta Pharmacol. Suecica, 20, 115, 1983.
56. Thunberg, E. and Samuelsson, G., The amino acid sequence of ligatoxin A, from the mistletoe Phoradendron liga, Acta Pharmacol. Suecica, 19, 447, 1982.
57. Samuelsson, G. and Pettersson, B., Toxic proteins from the mistletoe Dendrophtora clavata. II. The amino acid sequence of denclatoxin B, Acta Pharmacol. Suecica, 14, 245, 1977.
58. Teeter, M. M., Mazer, J. A., and L’Italien, J. J., Primary structure of the hydrophobic plant protein crambin, Biochemistry, 20, 5437, 1981.
59. Vermeulen, J. A. W. H., Lamerichs, R. M. J. N., Berliner, L., De Marco, A., Llinas, M., Boelens, R., Alleman, U., and Kaptein, R., 1H-NMR characterization of two crambin species, FEBS Lett., 219, 426, 1987.
60. Epple, P., Apel, K., and Bohlmann, H., An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesisrelated proteins, Plant Physiol., 109, 813, 1995.
61. Terras, F. R. G., Torrekens, S., Van Leuven, F., and Broekaert, W. F., A six-cysteine type thionin from the radish storage organ displays weak in vitro antifungal activity against Fusarium culmorum, Plant Physiol. Biochem., 34, 599, 1996.
62. Rosell, S. and Samuelsson, G., Effect of mistletoe viscotoxin and phoratoxin on blood circulation, Toxicon, 4, 107, 1966.
63. Lankisch, P. G. and Vogt, W., Potentiation of haemolysis by the combined action of phospholipase A and a basic peptide containing S-S-bonds (viscotoxin B), Experientia, 27, 122, 1971.
64. Andersson, K. E. and Johannsson, M., Effects of viscotoxin on rabbit heart and aorta, and on frog skeletal muscle, Eur. J. Pharm., 23, 223, 1973.
65. Carrasco, L., Vazques, D., and Hernandez-Lucas, C., Thionins: plant peptides that modify membrane permeability in cultured mammalian cells, Eur. J. Biochem., 116, 185, 1981.
66. Selawry, O. S., Vester, F., and Mai, W., Zur kenntnis der inhaltsstoffe von Viscum album. II. tumorhemmende inhaltsstoffe, Hoppe-Seyler’s Z. Physiol. Chem., 324, 262, 1961.
67. Buessing, A., Suzart, K., and Bergmann, J., Induction of apoptosis in human lymphocytes treated with Viscum album L. is mediated by the mistletoe lectins, Cancer Lett., 99, 59, 1996.
68. Winterfeld, K. and Bijl, L. H., Viscotoxin, ein neuer inhaltsstoff der mistel (Viscum album L.), Liebigs Ann. Chem., 561, 107, 1948.
69. Samuelsson, G., Chromatography of viscotoxin and oxidized viscotoxin on phosphate cellulose, Acta Chem. Scand., 20, 1546, 1966.
70. Samuelsson, G. and Pettersson, B., Separation of viscotoxins from the European mistletoe, Viscum album L. (Loranthaceae) by chromatography on sulfoethyl sephadex, Acta Chem. Scand., 24, 2751, 1970.
71. Konopa, J., Woynarowski, J. M., and Lewandowska-Gumieniak, M., Isolation of viscotoxins. Cytotoxic basic polypeptides from Viscum album L., Hoppe-Seyler’s Z. Physiol. Chem., 361, 1525, 1980.
72. Schaller, G., Urech, K., and Giannattasio, M., Cytotoxicity of different viscotoxins and extracts from the European subspecies of Viscum album L., Phytotherapy Res., 10, 473, 1996.
73. Van Etten, C. H., Nielsen, H. C., and Peters, J. E., A crystalline polypeptide from the seed of Crambe abyssinica, Phytochemistry, 4, 467, 1965.
74. Van Etten, C. H., Gagne W. E., Robbins, D., Booth, A. N., Daxenbichler, M. E., and Wolff, I. A., Biological evaluation of Crambe seed meals and derived products by rat feeding, Cereal Chem., 46, 145, 1969.
75. Angerhofer, C. K., Shier, W. T., and Vernon, L. P., Phospholipase activation in the cytotoxic mechanism of thionin purified from nuts of Pyrularia pubera, Toxicon, 28, 547, 1990.
76. Schrader-Fischer, G. and Apel, K., Organ-specific expression of highly divergent thionin variants that are distinct from the seed-specific crambin in the crucifer Crambe abyssinica, Mol. Gen. Genet., 245, 380, 1994.
77. Daley, L. S. and Theriot, L. J., Electrophoretic analysis, redox activity, and other characteristics of proteins similar to purothionins from tomato (Lycopersicum esculenta), mango (Mangifera indica), papaya (Carica papaya), and walnut (Juglans regia), J. Agric. Food Chem., 35, 680, 1987.
78. Bohlmann, H., Apel, K., and García-Olmedo, F., Thionins, Plant Mol. Biol. Rep., 12, S75, 1994.
79. Hendrickson, W. A. and Teeter, M. M., Structure of the hydrophobic protein crambin determined directly from the anomalous scattering of sulfur, Nature, 290, 107, 1981.
80. Teeter, M. M., Water structure of a hydrophobic protein at atomic resolution: pentagon rings of water molecules in crystals of crambin, Proc. Natl. Acad. Sci. U.S.A., 81, 6014, 1984.
81. Stec, B., Zhou, R., and Teeter, M. M., Full-matrix refinement of the protein crambin at 0.83 Å and 130 K, Acta Cryst., D51, 663, 1995.
82. Weeks, C. M., Hauptman, H. A., Smith, G. D., Blessing, R. H., Teeter, M. M., and Miller, R., Crambin: a direct solution for a 400-atom structure, Acta Cryst., D51, 33, 1995.
83. Teeter, M. M. and Hendrickson, W. A., Highly ordered crystals of the plant seed protein crambin, J. Mol. Biol., 127, 219, 1979.
84. Whitlow, M. and Teeter, M. M., Energy minimization for tertiary structure prediction of homologous proteins: (1-purothionin and viscotoxin A3 models from crambin, J. Biochem. Struct. Dynam., 2, 831, 1985.
85. Rao, U. and Teeter, M. M., Improvement of turn structure prediction by molecular dynamics: a case study of a1-purothionin, Protein Eng., 6, 837, 1993.
86. Rao, U., Stec, B., and Teeter, M. M., Refinement of purothionins reveals solute particles important for lattice formation and toxicity. Part 1: a1-purothionin revisited, Acta Cryst., D51, 904, 1995.
87. Stec, B., Rao, U., and Teeter, M. M., Refinement of purothionins reveals solute particles important for lattice formation and toxicity. Part 2: Structure of ß-purothionin at 1.7 Å resolution, Acta Cryst., D51, 914, 1995.
88. Lecomte, J. T. J., Jones, B. L., and Llinas, M., Proton magnetic resonance studies of barley and wheat thionins: structural homology with crambin., Biochemistry, 21, 4843, 1987.
89. Han, K. H., Park, K. H., Yoo, H. J., Cha, H., Suh, S. W., Thomas, F., Moon, T. S., and Kim, S. M., Determination of the three-dimensional structure of hordothionin-a by nuclear magnetic resonance, Biochem J., 313, 885, 1996.
90. Lecomte, J. T. J., Kaplan, D., Llinas, M., Thunberg, E., and Samuelsson, G., Proton magnetic resonance characterization of phoratoxins and homologous proteins related to crambin, Biochemistry, 26, 1187, 1987.
91. Teeter, M. M. and Whitlow, M., Test of circular dichroism (CD) methods for crambin and CD-assisted secondary structure prediction of its homologous toxins, Proteins: Struct. Funct. Genet., 4, 262, 1988.
92. Markman, O., Rao, U., Lewis, K., Heffron, G. J., Stec, B., and Teeter, M. M., Mode of phospholipid binding to the membrane active plant toxin phoratoxin-A, in New Developments in Lipid-Protein Interactions and Receptor Function, Wirtz, K. W. A., Ed., Plenum Press, New York, 1993, 263.
93. Mellstrand, S. T. and Samuelsson, G., Phoratoxin, a toxic protein from the mistletoe Phoradendron tomentosum subsp. macrophyllum (Loranthaceae). The disulfide bonds, Acta Pharmacol. Suecica, 11, 367, 1974.
94. Olson, T. and Samuelsson, G., The disulfide bonds of viscotoxin A2 from the European mistletoe (Viscum album L., Loranthaceae), Acta Pharmacol. Suecica, 11, 381, 1974.
95. Hase, T., Matsubara, H., and Yoshizumi, H., Disulfide bonds of purothionin, a lethal toxin for yeasts, J. Biochem., 83, 1671, 1978.
96. Stuart, L. S and Harris, T. H., Bactericidal and fungicidal properties of a crystalline protein isolated from unbleached wheat flour, Cereal Chem., 19, 288, 1942.
97. Coulson, E. J., Harris, T. H., and Axelrod, B., Effect on small laboratory animals of the injection of the crystalline hydrochloride of a sulfur protein from wheat flour, Cereal Chem., 19, 301, 1942.
98. Samuelsson, G., Mistletoe toxins, Syst. Zool., 22, 566, 1974.
99. Samuelsson, G., Pettersson, B., and Ljunggren, A., Toxic proteins from the mistletoe Dendrophtora clavata. I. Isolation and properties of denclatoxin A and denclatoxin B, Acta Pharmacol. Suecica, 14, 237, 1977.
100. Evett, G. E., Donaldson, D. M., and Vernon, L. P., Biological properties of Pyrularia thionin prepared from nuts of Pyrularia pubera, Toxicon, 24, 622, 1986.
101. Kramer, K. J., Klassen, L. W., Jones, B. L., Speirs, R. D., and Kammer, A. E., Toxicity of purothionin and its homologues to the tobacco hornworm, Manduca sexta (L.) (Lepidoptera: Sphingidae), Toxicol. Appl. Pharmacol., 48, 179, 1979.
102. Woolley, D. W. and Krampitz, L. O., Reversal by phosphatides of the antimicrobial action of a crystalline protein from wheat, J. Biol. Chem., 146, 273, 1942.
103. Nose, Y. and Ichikawa, M., Studies on the effects of flour extract on baker’s yeast, J. Ferment. Technol., 46, 915, 1968.
104. Okada, T. and Yoshizumi, H., A lethal toxic substance for brewing yeast in wheat and barley. Part II. Isolation and some properties of toxic principle, Agr. Biol. Chem., 34, 1089, 1970.
105. Okada, T., Yoshizumi, H., and Terashima, Y., A lethal toxic substance for brewing yeast in wheat and barley. Part I. Assay of toxicity on various grains, and sensitivity of various yeast strains, Agr. Biol. Chem., 34, 1084, 1970.
106. Okada, T. and Yoshizumi, H., The mode of action of toxic protein in wheat and barley on brewing yeast, Agr. Biol. Chem., 37, 2289, 1973.
107. Hernandez-Lucas, C., Fernandez de Caleya, R., and Carbonero, P., Inhibition of brewer’s yeasts by wheat purothionins, Appl. Microbiol., 28, 165, 1974.
108. Wada, K., Ozaki, Y., Matsubara, H., and Yoshizumi, H., Studies on purothionin by chemical modifications, J. Biochem., 91, 257, 1982.
109. Fernandez de Caleya, R., Gonzalez-Pascual, B., García-Olmedo, F., and Carbonero, P., Susceptibility of phytopathogenic bacteria to wheat purothionins in vitro, Appl. Microbiol., 23, 998, 1972.
110. Cammue, B. P. A., De Bolle, M. F. C., Terras, F. R. G., Proost, P., Van Damme, J., Rees, S. B., Vanderleyden, J., and Broekaert, W. F., Isolation and characterization of a novel class of plant antimicrobial peptides from Mirabilis jalapa L. seeds, J. Biol. Chem., 267, 2228, 1992.
111. Florack, D. E. A., Visser, B., De Vries, P. H. M., Van Vuurde, J. W. L., and Stiekema, W. J., Analysis of the toxicity of purothionins and hordothionins for plant pathogenic bacteria, Neth. J. Pl. Path., 99, 259, 1993.
112. Molina, A., Ahl-Goy, P., Fraile, A., Sanchez-Monge, R., and García-Olmedo, F., Inhibition of bacterial and fungal plant pathogens by thionins of types I and II, Plant Science, 92, 169, 1993.
113. Molina, A., Segura, A., and García-Olmedo, F., Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens, FEBS Lett., 316, 119, 1993.
114. Bohlmann, H., Clausen, S., Behnke, S., Giese, H., Hiller, C., Schrader, G., Barkholt, V., and Apel, K., Leaf-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, 1988.
115. Terras, F. R. G., Schoofs, H. M. E., De Bolle, M. F. C., Van Leuven, R., Rees, S. B., Vanderleyden, J., Cammue, B. P. A., and Broekaert, W. F., Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds, J. Biol. Chem., 267, 15302, 1992.
116. Terras, F. R. G., Schoofs, H. M. E., Thevissen, K., Osborn, R. W., Vanderleyden, J., Cammue, B. P. A., and Broekaert, W. F., Synergistic enhancement of the antifungal activity of wheat and barley thionins by radish and oilseed rape 2S albumins and by barley trypsin inhibitors, Plant Physiol., 103, 1311, 1993.
117. Kashimoto, T., Sakakibara, R., Huynh, Q. K., Wada, H., and Yoshizumi, H., The effect of purothionin on bovine adrenal medullary cells, Res. Commun. Chem. Pathol. Pharmacol., 26, 221, 1979.
118. Nakanishi, T., Yoshizumi, H., Tahara, S., Hakura, A., and Toyoshima, K., Cytotoxicity of purothionin-A on various animal cells, Gann., 70, 323, 1979.
119. Shaw, K. P., Kauffman, F. C., Vernon, L. P., and Albuquerque, E. X., Cytotoxic mechanism of Pyrularia thionin, Soc. Neurosc. Abstr., 13, 930, 1987.
120. Osorioe Castro, V. R., Van Kuiken, B A., Vernon, L P., and Albuquerque, E. X., Action of a thionin isolated from nuts of Pyrularia pubera on human erythrocytes, Toxicon, 27, 501, 1989.
121. Thevissen, K., Ghazi, A., De Samblanx, G. W., Brownlee, C., Osborn, R. W., and Broekaert, W. F., Fungal membrane responses induced by plant defensins and thionins, J. Biol. Chem., 271, 15018, 1996.
122. Oka, T., Murata, Y., Nakanishi, T., Yoshizumi, H., Hayashida, H., Ohtsuki, Y., and Toyoshima, K., Similarity, in molecular structure and function, between the plant toxin purothionin and the mammalian pore-forming proteins, Mol. Biol. Evol., 9, 707, 1992.
123. Guihard, G., Bénédetti, H., Besnard, M., and Letellier, L., Phosphate efflux through the channels formed by colicins and phage T5 in Escherichia coli cells is responsible for the fall in cytoplasmic ATP, J. Biol. Chem., 268, 17775, 1993.
124. Jones, B. L., Lookhart, G. L., and Johnson, D. E., Improved separation and toxicity analysis methods for purothionins, Cereal Chem., 62, 327, 1985.
125. Vernon, L. P. and Rogers, A., Effect of calcium and phosphate ions on hemolysis induced by Pyrularia thionin and Naja naja kaouthia cardiotoxin, Toxicon, 30, 701, 1992.
126. Evans, J., Wang, Y., Shaw, K. P., and Vernon, L. P., Cellular responses to Pyrularia thionin are mediated by Ca2+ influx and phospholipase A2 activation and are inhibited by thionin tyrosine iodination, Proc. Natl. Acad. Sci. U.S.A., 86, 5849, 1989.
127. Jackson, S. L. and Heath, I. B., Roles of calcium ions in hyphal tip growth, Microbiol. Rev., 57, 367, 1993.
128. Rao, U., Teeter, M. M., Erickson-Viitanen, S., and DeGrado, W. F., Calmodulin binding to a1-purothionin: solution binding and modeling of the complex, Proteins: Struct. Funct. Genet., 14, 127, 1992.
129. Vernon, L. P., Pyrularia thionin: physical properties, biological responses and comparison to other thionins and cardiotoxins, J. Toxicol. Toxin Rev., 11, 169, 1992.
130. Gasanov, S. E., Vernon, L. P., and Aripov, T. F., Modification of phospholipid membrane structure by the plant toxic peptide Pyrularia thionin, Arch. Biochem. Biophys., 301, 367, 1993.
131. Hernandez-Lucas, C., Fernandez de Caleya, R., Carbonero, P., and García-Olmedo, F., Reconstitution of petroleum ether soluble wheat lipopurothionin by binding of digalactosyl diglyceride to the chloroform-soluble form, J. Agric. Food Chem., 25, 1287, 1977.
132. Carbonero, P., García-Olmedo, F., and Hernandez-Lucas, C., External association of hordothionin with protein bodies in mature barley, J. Agric. Food Chem., 28, 399, 1980.
133. Harvey, A. L., Cardiotoxins from cobra venoms: possible mechanisms of action, J. Toxicol. Toxin Rev., 4, 41, 1985.
134. Harvey, A. L., Cardiotoxins from cobra venoms, in Handbook of Natural Toxins, Vol. 5 Reptile Venoms and Toxins, Tu, A. T., Ed., Marcel-Decker,
135. Osorio e Castro, V. R. and Vernon, L. P., Hemolytic activity of thionin from Pyrularia pubera nuts and snake venom toxins of Naja naja species: Pyrularia thionin and snake venom cardiotoxin compete for the same membrane site, Toxicon, 27:511-517, 1989.
136. Jiang, M. S., Fletcher, J. E., and Smith, L. A., Factors influencing the hemolysis of human erythrocytes by cardiotoxins from Naja naja kaouthia and Naja naja atra venoms and a phospholipase A2 with cardiotoxin-like activities from Bungarus fasciatus venom, Toxicon, 27, 47, 1989.
137. Louw, A. I. and Visser, L., The synergism of cardiotoxin and phospholipase A2 in hemolysis, Biochim. Biophys. Acta, 163, 512, 1989.
138. Huang, W., Vernon, L. P., and Bell, J. D., Enhancement of adenylate cyclase activity in S49 lymphoma cell membranes by the toxin thionin from Pyrularia pubera, Toxicon, 32, 789, 1994.
139. Lobb, L., Stec, B., Kantrowitz, E. K., Yamano, A., Stojanoff, V., Markman, O., and Teeter, M. M., Expression, purification and characterization of recombinant crambin, Prot. Engineering, 9, 1233, 1996.
140. Rao, A. G., Hassan, M., and Hempel, J. C., Structure-function validation of high lysine analogs of α-hordothionin designed by protein modeling, Protein Engineering, 7, 1485, 1994.
141. Wada, K. and Buchanan, B. B., Purothionin: a seed protein with thioredoxin activity, FEBS Lett., 124, 237, 1981.
142. Johnson, T. C., Wada, K., Buchanan, B. B., and Holmgren, A., Reduction of purothionin by the wheat seed thioredoxin system, Plant Physiol., 85, 446, 1987.
143. Diaz, I., Carmona, M. J., and García-Olmedo, F., Effects of thionins on ß-glucuronidase in vitro and in plant protoplasts, FEBS Lett., 296, 279, 1992.
144. García-Olmedo, F., Piñeiro, M., and Diaz, I., Dances to a redox tune, Plant Mol. Biol., 26, 11, 1994.
145. Piñeiro, M., García-Olmedo, F., and Diaz, I., Redox modulation of the expression of bacterial genes encoding cysteine-rich proteins in plant protoplasts, Proc. Natl. Acad. Sci. U.S.A., 91, 3867, 1994.
146. Piñeiro, M., Diaz, I., Rodriguez-Palenzuela, P., Titarenko, E., and García-Olmedo, F., Selective disulfide linkage of plant thionins with other protein, FEBS Lett., 369, 239, 1995.
147. Woynarowski, J. M. and Konopa, J., Interaction between DNA and viscotoxins, cytotoxic basic polypeptides from Viscum album L., Hoppe-Seyler’s Z. Physiol. Chem., 361, 1535, 1980.
148. García-Olmedo, F., Carbonero, P., Hernandez-Lucas, C., Paz-Ares, J., Ponz, F., Vicente, O., and Sierra, J. M., Inhibition of eukaryotic cell-free protein synthesis by thionins from wheat endosperm, Biochim. Biophys. Acta, 740, 52, 1983.
149. Brümmer, J., Thole, H., and Kloppstech, K., Hordothionins inhibit protein synthesis at the level of initiation in the wheat-germ system, Eur. J. Biochem., 219, 425, 1994.
150. Jones, B. L. and Meredith, P., Inactivation of α-amylase activity by purothionins, Cereal Chem., 59, 321, 1982.
151. Richardson, M., Seed storage proteins: the enzyme inhibitors, Meth. Plant Biochem., 5, 259, 1991.
152. Andresen, I., Becker, W., Schlüter, K., Burges, J., Parthier, B., and Apel, K., The identification of leaf thionin as one of the main jasmonate-induced proteins of barley (Hordeum vulgare), Plant Mol. Biol., 19, 193, 1992.
153. Bergey, D. R., Howe, G. A., and Ryan, C. A., Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals, Proc. Natl. Acad. Sci. U.S.A., 93, 12053, 1996.
154. Bloch, C., Jr. and Richardson, M., A new family of small (5 kDa) protein inhibitors of insect α-amylases from seeds of sorghum (Sorghum bicolor (L) Moench) have sequence homologies with wheat γ-purothionins, FEBS Lett., 279, 101, 1991.
155. Campos, F. A. P. and Richardson, M., The complete amino acid sequence of the bifunctional α-amylase/trypsin inhibitor from seeds of ragi (Indian finger millet; Eleusine coracana Goertn.), FEBS Lett., 152, 300, 1984.
156. Schrader-Fischer, G. and Apel, K., The anticyclic timing of leaf senescence in the parasitic plant Viscum album is closely correlated with the selective degradation of sulphur-rich viscotoxins, Plant Physiol., 101, 745, 1993.
157. Bohlmann, H., Significance of sulfur-rich proteins in seeds and leaves, in Sulfur Nutrition and Assimilation in Higher Plants, DeKok, L. J., Stulen, I., Rennenberg, H., Brunold, C., and Rauser, W. E., Eds., Academic Publishing, The Hague, 1993, 211.
158. Carmona, M. J., Molina, A., Fernandez, J. A., Lopez-Fando, J. M., and García-Olmedo, F., Expression of the alpha-thionin gene from barley in tobacco confers enhanced resistance to bacterial pathogens, Plant J., 3, 457, 1993.
159. Florack, D. E. A., Dirkse, W. G., Visser, B., Heidekamp, F., and Stiekema, W. J., Expression of biologically active hordothionin in tobacco. Effects of pre-and prosequences at the amino and carboxyl termini of the hordothionin precursor on mature protein expression and sorting, Plant Mol. Biol., 24, 83, 1994.
160. Maddox, J., Duvick, J., Hastings, C., Rouch, H., Ross, M., Lane, S., and Daywalt, M., Cloning of a barley gene, α-hordothionin, and expression in transgenic tobacco, J. Cell Biochem., Suppl 16F, 217, 1992.
161. Epple, P., Apel, K., and Bohlmann, H., Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum, Plant Cell, 9, 509, 1997.
162. Ponz, F., Paz-Ares, J., Hernandez-Lucas, C., Carbonero, P., and García-Olmedo, F., Synthesis and processing of thionin precursors in developing endosperm from barley (Hordeum vulgare L.), EMBO J., 2, 1035, 1983.
163. Von Heijne, G., A new method for predicting signal sequence cleavage sites, Nucl. Acids Res., 14, 4683, 1986.
164. Reimann-Philipp, U., Schrader, G., Martinoia, E., Barkholt, V., and Apel, K., Intracellular thionins of barley. A second group of leaf thionins closely related to but distinct from cell wall-bound thionins, J. Biol. Chem., 264, 8978, 1989.
165. Carmona, M. J., Hernandez-Lucas, C., San Martin, C., Gonzales, P., and García-Olmedo, F., Subcellular localization of type I thionins in the endosperms of wheat and barley, Protoplasma, 173, 1, 1993.
166. Weissman, J. S. and Kim, P. S., The pro region of BPTI facilitates folding, Cell, 71, 841, 1992.
167. Lee, D. W., Apel, K., and Binding, H., The formation of leaf thionins and their effect on the viability of isolated protoplasts of barley (Hordeum vulgare L.), J. Plant Physiol., 145, 131, 1995.
168. Daher, K. A., Lehrer, R. I., Ganz, T., and Kronenberg, M., Isolation and characterization of human defensin cDNA clones, Proc. Natl. Acad. Sci. U.S.A., 85, 7327, 1988.
169. Dimarcq, J. L., Zachary, D., Hoffmann, J. A., Hoffmann, D., and Reichhart, J. M., Insect immunity: expression of the two major inducible antibacterial peptides, defensin and diptericin, in Phormia terranovae, EMBO J., 9, 2507, 1990.
170. Gu, Q., Kawata, E. E., Morse, M. J., Wu, H. M., and Cheung, A. Y., A flower-specific cDNA encoding a novel thionin in tobacco, Mol. Gen. Genet., 234, 89, 1992.
171. Romero, A., Alamillo, J. M., and García-Olmedo, F., Processing of thionin precursors in barley leaves by a vacuolar proteinase, Eur. J. Biochem., 243, 202, 1997.
172. Bunge, S., Wolters, J., and Apel, K., A comparison of leaf thionin sequences of barley cultivars and wild barley species, Mol. Gen. Genetics, 231, 460, 1992.
173. Bohl, S. and Apel, K., A novel fingerprint method for analyzing the expression of complex multigene families of very low transcript abundance, Plant J., 3, 887, 1993.
174. Reimann-Philipp, U., Behnke, S., Batschauer, A., Schäfer, E., and Apel, K., The effect of light on the biosynthesis of leaf-specific thionins in barley, Hordeum vulgare, Eur. J. Biochem., 182, 283, 1989.
175. Hess, W. R., Müller, A., Nagy, F., and Börner, T., Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal, Mol. Gen. Genet., 242, 305, 1994.
176. Beator, J., Pötter, E., and Kloppstech, K., The effect of heat shock on morphogenesis in barley, Plant Physiol., 100, 1780, 1992.
177. Fischer, R., Behnke, S., and Apel, K., The effect of chemical stress on the polypeptide composition of the intercellular fluid of barley leaves, Planta, 178, 61, 1989.
178. Wasternack, C., Atzorn, R., Jarosch, B., and Kogel, K. H., Induction of a thionin, the jasmonate-induced 6 kDa protein of barley by 2,6-dichloroisonicotinic acid, J. Phytopathology, 140, 280, 1994.
179. Kogel, K. H., Ortel, B., Jarosch, B., Atzorn, R., Schiffer, R., and Wasternack, C., Resistance in barley against the powdery mildew fungus (Erysiphe graminis f. sp. hordei) is not associated with enhanced levels of endogenous jasmonates, Eur. J. Plant Pathol., 101, 319, 1995.
180. Métraux, J. P., Ahl-Goy, P., and Staub, T., Induced resistance in cucumber in response to 2,6-dichlorisonicotinic acid and pathogens, in Advances in Molecular Genetics of Plant-Microbe Interactions, Hennecke, H. and Verma, D. P. S., Eds., Kluwer Academic Publishers, Dordrecht, The Netherlands, 1991, 432.
181. Gundlach, H., Müller, M. J., Kutchan, T. M., and Aenk, M. H., Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures, Proc. Natl. Acad. Sci. U.S.A., 89, 2389, 1992.
182. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., Chandler, D., Slusarenko, A., Ward, E., and Ryals, J., Acquired resistance in Arabidopsis, Plant Cell, 4, 645, 1992.
183. Dempsey, D’ M. A. and Klessig, D. F., Salicylic acid, active oxygen species and systemic acquired resistance in plants, Trends Cell Biol., 4, 334, 1994.
184. Weidhase, R. A., Kramell, H., Lehmann, J., Liebisch, H. W., Lerbs, W., and Parthier, B., Methyljasmonate-induced changes in the polypeptide pattern of senescing barley leaf segments, Plant Sci., 51, 177, 1987.
185. Molina, A. and García-Olmedo, F., Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins, Plant J., 4, 983, 1993.
186. Titarenko, E., Hargreaves, J., Keon, J., and Gurr, S. J., Defense-related gene expression in barley coleoptile cells following infection by Septoria nodorum, in Mechanisms of Plant Defense Responses, Fritig, B. and Legrand, M., Eds., Kluwer Academic Publishers, Dordrecht, The Netherlands, 1993, 308.
187. Stevens, C., Titarenko, E., Hargreaves, J. A., and Gurr, S. J., Defense-related gene activation during an incompatible interaction between Stagonospora (Septoria) nodorum and barley (Hordeum vulgare L.) coleoptile cells, Plant Mol. Biol., 31, 741, 1996.
188. Valè, G. P., Torrigiani, E., Gatti, A., Delogu, G., Porta-Puglia, A., Vannacci, G., and Cattivelli, L., Activation of genes in barley roots in response to infection by two Drechslera graminea isolates, Physiol. Mol. Plant Pathol., 44, 207, 1994.
189. Boyd, L. A., Smith, P. H., and Brown, J. K. M., Molecular and cellular expression of quantitative resistance in barley to powdery mildew, Physiol. Mol. Plant Pathol., 45, 47, 1994.
190. Boyd, L. A., Smith, P. H., Green, R. M., and Brown, J. K. M., The relationship between the expression of defense-related genes and mildew development in barley, Mol. Plant-Microbe Interact., 7, 401, 1994.
191. Ebrahim-Nesbat, F., Behnke, S., Kleinhofs, A., and Apel, K., Cultivar-related differences in the distribution of cell-wall bound thionins in compatible and incompatible interactions between barley and powdery mildew, Planta, 179, 203, 1989.
192. Ebrahim-Nesbat, F., Bohl, S., and Heitefuss, R., Thionin in cell walls and papillae of barley in compatible and incompatible interactions with Erysiphe graminis f. sp. hordei, Physiol. Mol. Plant Pathol., 43, 343, 1993.
193. Ebrahim-Nesbat, F., Rohringer, R., and Heitefuss, R., Effect of rust infection on cell walls of barley and wheat; immunocytochemistry using anti-barley thionin as a probe, J. Phytopathol., 141, 38, 1994.
194. Ebrahim-Nesbat, F., Apel, K., and Heitefuss, R., Immunochemical evidence for the presence of barley thionins in rachis and stalk of wheat: decrease of antibody binding at Fusarium culmorum penetration sites, J. Phytopathol., 131, 259, 1991.
195. Rasmussen, S. and Rasmussen, C. E., Full-length cDNA clone encoding barley toxin ß-hordothionin shows a signal peptide 27 amino acid residues long, Plant Mol. Biol., 21, 579, 1993.
196. Kleinhofs, A., Kilian, A., Saghai Maroof, M. A., Biyashev, R. M., Hayes, P., Chen, F. Q., Lapitan, N., Fenwick, A., Blake, T. K., Kanazin, V., Ananiev, E., Dahleen, L., Kudrna, D., Bollinger, J., Knapp, S. J., Liu, B., Sorrells, M., Heun, M., Franchowiak, J. D., Hoffman, D., Skadsen, R., and Steffenson, B. J., A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome, Theor. Appl. Genet., 86, 705, 1993.
197. Pedersen, C., Giese, H., and Linde-Laursen, I., Towards an integration of the physical and the genetic chromosome maps of barley by in situ hybridization, Hereditas, 123, 77, 1995.
198. Holtorf, S., Apel, K., and Bohlmann, H., Specific and different expression patterns of two members of the leaf thionin multigene family of barley in transgenic tobacco, Plant Sci., 111, 27, 1995.
199. Pecchioni, N., Stanca, A. M., Terzi, V., and Cattivelli, L., RFLP analysis of highly polymorphic loci in barley, Theor. Appl. Genet., 85, 926, 1993.
200. Olivera, B. M., Rivier, J., Clark, C., Ramilo, C. A., Corpuz, G. P., Abogadie, F. C., Mena, E. E., Woodward, S. R., Hillyard, D. R., and Cruz, L. J., Diversity of Conus neuropeptides, Science, 249, 257, 1990.
201. Steinmüller, K., Batschauer, A., and Apel, K., Tissue-specific and light-dependent changes of chromatin organization in barley (Hordeum vulgare), Eur. J. Biochem., 158, 519, 1986.
202. Smith, H., Signal perception, differential expression within multigene families and the molecular basis of phenotypic plasticity, Plant Cell Environ., 13, 585, 1990.
203. Lotan, T., Ori, N., and Fluhr, R., Pathogenesis-related proteins are developmentally regulated in tobacco flowers, Plant Cell, 1, 881, 1989.
204. Neale, A. D., Wahleithner, J. A., Lund, M., Bonnett, H. T., Kelly, A., Meeks-Wagner, D. R., Peacock, W. J., and Dennis, E. S., Chitinase, ß-1,3-glucanase, osmotin, and extensin are expressed in tobacco explants during flower formation, Plant Cell, 2, 673, 1990.
205. Ori, N., Sessa, G., Lotan, T., Himmelhoch, S., and Fluhr, R., A major stylar matrix polypeptide (sp41) is a member of the pathogenesis-related proteins superclass, EMBO J., 9, 3429, 1990.
206. Coté, F., Cutt, J. R., Asselin, A., and Klessig, D. F., Pathogenesis-related acidic beta-1,3-glucanase genes of tobacco are regulated by both stress and developmental signals, Mol. Plant-Microbe Interact., 4, 173, 1991.
207. 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 Broekaert, W., Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway, Plant Cell, 8, 2309, 1996.
208. Epple, P., Apel, K., and Bohlmann, H., ESTs reveal a multigene family for plant defensins in Arabidopsis thaliana, FEBS Lett., 400, 168, 1997.
209. Robson, G. D., Kuhn, P. J., and Trinci, A. P. J., Effect of validamycin A on the inositol content and branching of Rhizoctonia cerealis and other fungi, J. Gen. Microbiol., 135, 739, 1989.
210. Wiebe, M. G., Robson, G. D., and Trinci, A. P. J., Edifenphos (Hinosan) reduces hyphal extension, hyphal growth unit length and phosphatidylcholine content of Fusarium graminearum A3/5, but has no effect on specific growth rate, J. Gen. Microbiol., 136, 979, 1990.
211. Creelman, R. A. and Mullet, J. E., Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress, Proc. Natl. Acad. Sci. U.S.A., 92, 4114, 1995.
212. Jongedijk, E., Tigelaar, H., van Roekel, J. S. C., Bres-Vloemans, S. A., Dekker, I., van den Elzen, P. J. M., Cornelissen, B. J. C., and Melchers, L. S., Synergistic activity of chitinases and ß-1,3-glucanases enhances fungal resistance in transgenic tomato plants, Euphytica, 85, 173, 1995.
213. Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Gut Rella, M., Meier, B., Dincher, S., Staub, T., Uknes, S., Métraux, J. P., Kessmann, H., and Ryals, J., A benzothiadiazole derivative induces systemic acquired resistance in tobacco, Plant J., 10, 61, 1996.
214. Mitchell, A. F. and Walters, D. R., Systemic protection in barley against powdery mildew infection using methyl jasmonate, Aspects Appl. Biol., 42, 323, 1995.
215. Li, J., Zingen-Sell, I., and Buchenauer, H., Induction of resistance of cotton plants to Verticillium wilt and of tomato plants to Fusarium wilt by 3-aminobutyric acid and methyl jasmonate, J. Plant Dis. Protect., 103, 288, 1996.
216. Cohen, Y., Gisi, U., and Niderman, T., Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic methyl ester, Phytopathology, 83, 1054, 1993.