Abstract
The normal (25° C) response of parsley (Petroselinum crispum Mill.) cell suspension cultures to ultraviolet (UV) light was suppressed by a simultaneous 37° C heat-shock treatment, as indicated by the loss of the inducibility of two enzymes of flavonoid biosynthesis, phenylalanine ammonia-lyase (EC 4.3.1.5) and chalcone synthase. The effects on enzyme activity and on enzyme synthesis in vitro and in vivo were similar, indicating that regulatory control is at an early step of gene expression, presumably transcription. When heat shock was given during the course of an ongoing UV induction, both enzyme synthesis and enzyme activities ceased rapidly. Likewise, the induction of phenylalanine ammonia-lyase by an elicitor from Phytophthora megasperma f. sp. glycinea was terminated upon transfer from 25° C to 37° C. Based on these and previously published data, it is concluded that stress responses in this system are preferentially expressed in the order of heat shock, fungal elicitor and UV light.
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Abbreviations
- CHS:
-
chalcone synthase
- HSP:
-
heat-shock protein
- PAL:
-
phenylalanine ammonia-lyase
- UV:
-
ultraviolet
References
Altschuler, M., Mascarenhas, J.P. (1982) Heat shock proteins and effects of heat shock in plants. Plant Mol. Biol. 1, 103–115
Ashburner, M., Bonner, J.J. (1979) The induction of gene activity in Drosophila by heat shock. Cell 17, 241–254
Ayers, A.R., Ebel, J., Finelli, F., Berger, N., Albersheim, P. (1976) Host-pathogen interactions: IX. Quantitative assays of elicitor activity and characterization of the elicitor present in the extracellular medium of cultures of Phytophthora megasperma var. sojae. Plant Physiol. 57, 751–759
Ayres, P.G. (1984) The interaction between environmental stress injury and biotic disease physiology. Annu. Rev. Phytopathol. 22, 53–75
Bensadoun, A., Weinstein, D. (1976) Assay of proteins in the presence of interfering materials. Anal. Biochem. 70, 241–250
Bonner, W.M., Laskey, R.A. (1974) A film detection method for tritium labeled proteins and nucleic acids in polyacrylamide gels. Eur. J. Biochem. 46, 83–88
Chappell, J., Hahlbrock, K. (1984) Transcription of plant defense genes in response to UV light or fungal elicitor. Nature 311, 76–78
Classen, D., Ward, E.W.B. (1985) Temperature-induced susceptibility of soybeans to Phytophthora megasperma f. sp. glycinea: production and activity of elicitors of glyceollin. Physiol. Plant Pathol. 26, 289–296
Colhoun, J. (1973) Effects of environmental factors on plant disease. Annu. Rev. Phytopathol. 1, 343–364
Findly, R.C., Pederson, T. (1981) Regulated transcription of the genes for actin and heat shock proteins in cultured Drosophila cells. J. Cell Biol. 88, 323–328
Hadwiger, L.A., Wagoner, W. (1983) Effects of heat shock on the mRNA-directed disease resistance response of peas. Plant Physiol. 72, 553–556
Hahlbrock, K. (1981) Flavonoids. In: The biochemistry of plants, vol. 7: Secondary plant products, pp. 425–456, Stumpf, P.K., Conn, E.E., eds. Academic Press, New York
Hahlbrock, K., Grisebach, H. (1979) Enzymic controls in the biosynthesis of lignins and flavonoids. Annu. Rev. Plant Physiol. 30, 105–130
Hahlbrock, K., Scheel, D. (1987) Biochemical responses of plants to pathogens. In: Innovative approaches to plant disease control, pp. 229–254, Chet, I., ed. John Wiley and Sons, Chichester, New York
Hahlbrock, K., Lamb, C.J., Purwin, C., Ebel, J., Fautz, E., Schäfer, E. (1981) Rapid response of suspension-cultured parsley cells to the elicitor from Phytophthora megasperma var. sojae. Induction of the enzymes of general phenylpropanoid metabolism. Plant Physiol. 67, 768–773
Hahlbrock, K., Chappell, J., Jahnen, W., Walter, M. (1985) Early defense reactions of plants to pathogens. In: Molecular form and function of the plant genome, pp. 129–140, Van Vloten-Doting, L., Groot, G., Hall, T., eds. Plenum Publishing Corporation, New York London
Hauffe, K.D., Hahlbrock, K., Scheel, D. (1986) Elicitor-stimulated furanocoumarin biosynthesis in cultured parsley cells. S-adenosyl-L-methionine: bergaptol and S-adenosyl-L-methionine: xanthotoxol O-methyltransferases. Z. Naturforsch. 41 c, 228–239
Hultmark, D., Klemenz, R., Gehring, W.J. (1986) Translational and transcriptional control elements in the untranslated leader of the heat shock gene HSP 22. Cell 4, 429–438
Ingolia, T.D., Craig, E.A. (1982) Drosophila gene related to the major heat shock induced gene is transcribed at normal temperatures and not induced by heat shock. Proc. Natl. Acad. Sci. USA 79, 525–529
Kimpel, J.A., Key, J.L. (1985) Heat shock in plants. Trends Biochem. Sci. 10, 353–357
Klemenz, R., Hultmark, D., Gehring, W.J. (1985) Selective translation of heat shock mRNA in Drosophila melanogaster depends on sequence information in the leader. EMBO J. 4, 2053–2060
Kreuzaler, F., Ragg, H., Fautz, E., Kuhn, D.N., Hahlbrock, K. (1983) UV-induction of chalcone synthase mRNA in cell suspension cultures of Petroselinum hortense. Proc. Natl. Acad. Sci. USA 80, 2591–2593
Krüger, C., Benecke, B.J. (1981) In vitro translation of Drosophila heat shock and non-heat shock mRNAs in heterologous and homologous cell-free systems. Cell 23, 595–603
Kuhn, D.N., Chappell, J., Boudet, A., Hahlbrock, K. (1984) Induction of phenylalanine ammonia-lyase and 4-coumarate: CoA ligase mRNAs in cultured plant cells by UV light or fungal elicitor. Proc. Natl. Acad. Sci. USA 81, 1102–1106
Li, G.C., Werb, Z., (1982) Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibrolasts. Proc. Natl. Acad. Sci. USA 79, 3218–3222
Lin, C.-Y., Roberts, J.K., Key, J.L. (1984) Acquisition of thermotolerance in soybean seedlings. Synthesis and accumulation of heat shock proteins and their cellular localization. Plant Physiol. 74, 152–160
Lindquist, S. (1986) The heat shock response. Annu. Rev. Biochem. 55, 1151–1191
Lowe, D.G., Moran, L.A. (1984) Proteins related to the mouse L-cell major heat shock protein are synthesized in the absence of heat shock gene expression. Proc. Natl. Acad. Sci. USA 81, 2317–2321
Nover, L. (ed.) (1984) Heat shock response of eucaryotic cells. Springer, Berlin
Nover, L., Scharf, K.D. (1984) Synthesis, modification and structural binding of heat shock proteins in tomato cell cultures. Eur. J. Biochem. 139, 303–313
O'Farrell, P.H. (1975) High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007–4021
Palter, K.B., Watanabe, M., Stinson, L., Mahowald, A.P., Craig, E.A. (1986) Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Mol. Cell. Biol. 6, 1187–1203
Pelham, H., (1985) Activation of heat shock genes in eucaryotes. Trends Genet. 1, 31–35
Ragg, H., Kuhn, D.N., Hahlbrock, K. (1981) Coordinated regulation of 4-coumarate: CoA ligase and phenylalanine ammonia-lyase mRNAs in cultured plant cells. J. Biol. Chem. 256, 10061–10065
Schlesinger, M.J., Aliperti, G., Kelley, P.M. (1982) The response of cells to heat shock. Trends Biochem. Sci. 7, 220–225
Schröder, J., Betz, B., Hahlbrock, K. (1976) Light induced enzyme synthesis in cell suspension cultures of Petroselinum hortense. Demonstration in a heterologous cell-free system of rapid changes in the rate of phenylalanine ammonia-lyase synthesis. Eur. J. Biochem. 67, 527–541
Schröder, J., Heller, W., Hahlbrock, K. (1979) Flavanone synthase: Simple and rapid assay for the key enzyme of flavonoid biosynthesis. Plant Sci. Lett. 14, 281–286
Storti, R.V., Scott, M.P., Rich, A., Pardue, M.L. (1980) Translational control of protein synthesis in response to heat shock in Drosophila melanogaster cells. Cell 22, 825–834
Tietjen, K.G., Hunkler, D., Matern, U. (1983) Differential response of cultured parsley cells to elicitors from two nonpathogenic strains of fungi. 1. Identification of induced products as coumarin derivatives. Eur. J. Biochem. 131, 401–407
Vierling, E., Key, J.L. (1985) Ribulose 1,5 bisphosphate carboxylase during heat shock. Plant Physiol. 78, 155–162
Walter, M.H. (1984) Untersuchungen zur Regulation der Phenylalanin Ammonium-Lyase und verschiedener Stressproteine in Zellsuspensionskulturen der Petersilie (Petroselinum hortense). Doctoral Dissertation, University of Freiburg, FRG
Walter, M.H., Hahlbrock, K. (1985) Synthesis of characteristic proteins in nutrient depleted cell suspension cultures of parsley. Planta 166, 194–200
Ward, E.W.B., Lazarovits, G. (1982) Temperature-induced changes in specificity in the interaction of soybeans with Phytophthora megasperma f. sp. glycinea. Phytopathology 72, 826–830
Wolffe, A.P., Perlman, A.J., Tata, J.R. (1984) Transient paralysis by heat shock of hormonal regulation of gene expression. EMBO J. 3, 2763–2770
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Walter, M.H. The induction of phenylpropanoid biosynthetic enzymes by ultraviolet light or fungal elicitor in cultured parsley cells is overriden by a heat-shock treatment. Planta 177, 1–8 (1989). https://doi.org/10.1007/BF00392148
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DOI: https://doi.org/10.1007/BF00392148