Abstract
The tryptophan decarboxylase (Tdc) gene from Catharanthus roseus (Madagascar periwinkle) encodes a key enzyme in biosynthesis of terpenoid indole alkaloids. The expression of the Tdc gene is transcriptionally induced by fungal elicitors. Tdc upstream sequences from −1818 to +198 relative to the transcriptional start site were functionally analysed to identify cis-acting elements that determine basal expression or respond to elicitor. In a loss-of-function analysis promoter derivatives with 5′ or internal deletions fused to the gusA reporter gene were analysed in transgenic tobacco plants. Whereas promoter activity dropped considerably following deletion down to −160, this short promoter derivative was still elicitor-responsive. Subsequently, the −160 to −37 region was further studied by gain-of-function experiments, in which subfragments were tested as tetramers cloned on two different truncated promoters. Combination of the data resulted in the identification of three functional regions in the −160 promoter. The region between −160 to −99 was shown to act as the main transcriptional enhancer. Two separable elicitor-responsive elements were found to reside between −99 and −87 and between −87 and −37. These two elements are not redundant in the Tdc promoter, since their combination gave a distinct elicitor response.
Similar content being viewed by others
References
Boller T: Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Mol Biol 46: 189–214 (1995).
Benfey PN, Ren L, Chua N-H: Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J 9: 1677–1684 (1990).
Chappell J, Hahlbrock K: Transcription of plant defence genes in response to UV light or fungal elicitor. Nature 311: 76–78 (1984).
Da Costa e Silva O, Klein L, Schmelzer E, Trezzini GF, Hahlbrock K: BPF-1, a pathogen-induced DNA-binding protein involved in the plant defense response. Plant J 4: 125–135 (1993).
Dixon RA, Paiva NL: Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085–1097 (1995).
Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon RA, Lamb C: Rapid stimulation of a soybean protein-serine kinase that phophorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16: 726–738 (1997).
Feldbrügge M, Sprenger M, Dinkelbach M, Yazaki K, Harter K, Weisshaar B: Functional analysis of a light-responsive plant bZIP transcriptional regulator. Plant Cell 6: 1607–1621 (1994).
Foster R, Izawa T, Chua N-H: Plant bZip proteins gather at ACGT elements. FASEB J 8: 192–200 (1994).
Fukuda Y, Shinshi H: Characterization of a novel cis-acting element that is responsive to a fungal elicitor in the promoter of a tobacco class I chitinase gene. Plant Mol Biol 24: 485–493 (1994).
Goddijn OJM, Lohman FP, de Kam RJ, Schilperoort RA, Hoge JHC: Nucleotide sequence of the tryptophan decarboxylase gene of Catharanthus roseus and expression of tdc-gusA gene fusions in Nicotiana tabacum. Mol Gen Genet 242: 217–225 (1994).
Hahlbrock K, Scheel D, Logemann E, Nürnberger T, Parniske m, Reinold S, Sacks WR, Schmelzer E: Oligopeptide elicitor-mediated defense gene activation in cultured parsley cells. Proc Natl Acad Sci USA 92: 4150–4157 (1995).
Hahn MG: Microbial elicitors and their receptors in plants. Annu Rev Phytopath 34: 387–412 (1996).
Hashimoto T, Yamada Y: Alkaloid biogenesis: molecular aspects. Annu Rev Plant Physiol Plant Mol Biol 45: 257–285 (1994).
Jefferson RA: Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol Biol Rep 5: 387–405 (1987).
Kim SY, Chung H-J, Thomas TL: Isolation of a novel class of bZIP transcription factors that interact with ABA-responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant J 11: 1237–1251 (1997).
Korfhage U, Trezzini GF, Meier I, Hahlbrock K, Somssich IE: Plant homeodomain protein involved in transcriptional regulation of a pathogen defense-related gene. Plant Cell 6: 695–708 (1994).
Lam E, Benfey PN, Gilmartin PM, Fang R-X, Chua N-H: Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci USA 86: 7890–7894 (1989).
Lam E, Chua N-H: GT-1 binding site confers light responsive expression in transgenic tobacco. Science 248: 471–473 (1990).
Lawton MA, Clouse SD, Lamb CJ: Glutathione-elicited changes in chromatin structure within the promoter of the defense gene chalcone synthase. Plant Cell Rep 8: 561–564 (1990).
Lois R, Dietrich A, Hahlbrock K, Schulz W: A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J 8: 1641–1648 (1989).
Marsh JL, Erfle M, Wykes EJ: The pIC plasmid and phage vectors with versatile cloning sites for recombinant selection by insertional inactivation. Gene 32: 481–485 (1984).
Matton DP, Prescott G, Bertrand C, Camirand A, Brisson N: Identification of cis-acting elements involved in the regulation of the pathogenesis-related gene STH-2 in potato. Plant Mol Biol 22: 279–291 (1993).
Meier I, Hahlbrock K, Somssich IE: Elicitor-inducible and constitutive in vivo DNA footprints indicate novel cisacting elements in the promoter of a parsley gene encoding pathogenesis-related protein 1. Plant Cell 3: 309–315 (1991).
Meijer AH, Verpoorte R, Hoge JHC: Regulation of enzymes and genes involved in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. J Plant Res 3: 145–164 (1993).
Menkens AE, Schindler U, Cashmore AR: The G-box: a ubiquitous regulatory element in plants bound by the GBF family of bZip proteins. Trends Biochem Sci 20: 506–510 (1995).
Moreno PRH, van der Heijden R, Verpoorte R: Cell and tissue cultures of Catharanthus roseus: a literature survey. Plant Cell Tiss Org Cult 42: 1–25 (1995).
Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D: High affinity binding of a fungal oligopeptide elicitor to parsley membranes triggers multiple defense responses. Cell 78: 449–460 (1994).
Oeda K, Salinas J, Chua N-H: A tobacco bZip transcription activator (TAF-1) binds to a G-box-like motif conserved in plant genes. EMBO J 7: 1793–1802 (1991).
Ouwerkerk PBF, Memelink J: A simple method for directional multimerization of DNA sequences. Trends Genet 13: 207 (1997).
Pasquali G, Goddijn OJM, de Waal A, Verpoorte R, Schilperoort RA, Hoge JHC, Memelink J: Coordinated regulation of two indole alkaloid biosynthetic genes from Catharanthus roseus by auxin and elicitors. Plant Mol Biol 18: 1121–1131 (1992).
Pasquali G, Ouwerkerk PBF, Memelink J: Versatile transformation vectors to assay the promoter activity of DNAelements in plants. Gene 149: 373–374 (1994).
Puente P, Wei N, Deng XW: Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J 15: 3732–3743 (1996).
Roewer IA, Clottier N, Nessler CL, De Luca V: Transient induction of tryptophan decarboxylase (TDC) and strictosidine synthase (SS) genes in cell suspension cultures of Catharanthus roseus. Plant Cell Rep 11: 86–89 (1992).
Rushton PJ, Tovar Torres J, Parniske M, Wernert P, Hahlbrock K, Somssich IE: Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15: 5690–5700 (1997).
Schulze-Lefert P, Becker-André M, Schulz W, Hahlbrock K, Dangl JL: Functional architecture of the light-responsive chalcone synthase promoter from parsley. Plant Cell 1: 707–714 (1989).
Somssich IE: Regulatory elements governing pathogenesisrelated (PR) gene expression. In: Nover L (eds) Results and problems in Cell Differentiation, vol. 20, pp. 163–179. Springer-Verlag, Berlin/Heidelberg, Germany (1994).
Suzuki K, Shinshi H: Transient activation and tyrosine phosphorylation of a protein kinase in tobacco cells treated with a fungal elicitor. Plant Cell 7: 639–647 (1995).
Wang MM, Reed RR: Molecular cloning of the olfactory neuronal transcription factor Olf-1 by genetic selection in yeast. Nature 364: 121–126 (1993).
Weisshaar B, Armstrong GA, Block A, da Costa e Silva O, Hahlbrock K: Light-inducible and constitutively expressed DNA-binding proteins recognizing a plant promoter element with functional relevance in light responsiveness. EMBO J 10: 1777–1786 (1991).
Wingender R, Röhrig H, Höricke C, Schell J: Cis-regulatory elements involved in ultraviolet light regulation and plant defense. Plant Cell 2: 1019–1026 (1990).
Yang Y, Shah J, Klessig DF: Signal perception and transduction in plant defense responses. Genes Dev 11: 1621–1639 (1997).
Yu LM, Lamb CJ, Dixon RA: Purification and biochemical characterization of proteins which bind to the H-box cis-element implicated in transcriptional activation of plant defense genes. Plant J 3: 805–816 (1993).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ouwerkerk, P.B., Memelink, J. Elicitor-responsive promoter regions in the tryptophan decarboxylase gene from Catharanthus roseus. Plant Mol Biol 39, 129–136 (1999). https://doi.org/10.1023/A:1006138601744
Issue Date:
DOI: https://doi.org/10.1023/A:1006138601744