Abstract
Little is known about the mechanisms that couple regulation of secondary metabolic pathways to the synthesis of primary metabolic precursors. Camalexin, an indolic secondary metabolite, appears to be the major phytoalexin in Arabidopsis. It was previously shown that camalexin accumulation is caused by infection with plant pathogens, by abiotic elicitors, and in spontaneous lesions in the accelerated cell death mutant acd2. We demonstrate that the accumulation of this phytoalexin is accompanied by the induction of the mRNAs and proteins for all of the tryptophan biosynthetic enzymes tested. A strong correlation was observed between the magnitude of camalexin accumulation and the induction of tryptophan biosynthetic proteins, indicating coordinate regulation of these processes. Production of disease symptoms is not sufficient for the response because systemic infection with cauliflower mosaic virus or cucumber mosaic virus did not induce the tryptophan pathway enzymes or camalexin accumulation. Salicylic acid appears to be required, but unlike other documented pathogenesis-related proteins, it is not sufficient for the coordinate induction. Results with trp mutants suggest that the tryptophan pathway is not rate limiting for camalexin accumulation. Taken together, these results are consistent with the hypothesis that the regulation of the tryptophan pathway in plants responds to needs for biosynthesis of secondary metabolites.
Full Text
The Full Text of this article is available as a PDF (2.5 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Berlyn M. B., Last R. L., Fink G. R. A gene encoding the tryptophan synthase beta subunit of Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4604–4608. doi: 10.1073/pnas.86.12.4604. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bohlmann J., DeLuca V., Eilert U., Martin W. Purification and cDNA cloning of anthranilate synthase from Ruta graveolens: modes of expression and properties of native and recombinant enzymes. Plant J. 1995 Mar;7(3):491–501. doi: 10.1046/j.1365-313x.1995.7030491.x. [DOI] [PubMed] [Google Scholar]
- Bohlmann J., Lins T., Martin W., Eilert U. Anthranilate synthase from Ruta graveolens. Duplicated AS alpha genes encode tryptophan-sensitive and tryptophan-insensitive isoenzymes specific to amino acid and alkaloid biosynthesis. Plant Physiol. 1996 Jun;111(2):507–514. doi: 10.1104/pp.111.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cao H., Bowling S. A., Gordon A. S., Dong X. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. Plant Cell. 1994 Nov;6(11):1583–1592. doi: 10.1105/tpc.6.11.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chappell J., Nable R. Induction of sesquiterpenoid biosynthesis in tobacco cell suspension cultures by fungal elicitor. Plant Physiol. 1987 Oct;85(2):469–473. doi: 10.1104/pp.85.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Conklin P. L., Last R. L. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol. 1995 Sep;109(1):203–212. doi: 10.1104/pp.109.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Delaney T. P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut-Rella M., Kessmann H., Ward E., Ryals J. A central role of salicylic Acid in plant disease resistance. Science. 1994 Nov 18;266(5188):1247–1250. doi: 10.1126/science.266.5188.1247. [DOI] [PubMed] [Google Scholar]
- Dyer W. E., Henstrand J. M., Handa A. K., Herrmann K. M. Wounding induces the first enzyme of the shikimate pathway in Solanaceae. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7370–7373. doi: 10.1073/pnas.86.19.7370. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grimsley N., Hohn B., Hohn T., Walden R. "Agroinfection," an alternative route for viral infection of plants by using the Ti plasmid. Proc Natl Acad Sci U S A. 1986 May;83(10):3282–3286. doi: 10.1073/pnas.83.10.3282. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hellwald K. H., Palukaitis P. Viral RNA as a potential target for two independent mechanisms of replicase-mediated resistance against cucumber mosaic virus. Cell. 1995 Dec 15;83(6):937–946. doi: 10.1016/0092-8674(95)90209-0. [DOI] [PubMed] [Google Scholar]
- Henstrand J. M., McCue K. F., Brink K., Handa A. K., Herrmann K. M., Conn E. E. Light and Fungal Elicitor Induce 3-Deoxy-d-arabino-Heptulosonate 7-Phosphate Synthase mRNA in Suspension Cultured Cells of Parsley (Petroselinum crispum L.). Plant Physiol. 1992 Feb;98(2):761–763. doi: 10.1104/pp.98.2.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kutchan T. M. Alkaloid Biosynthesis[mdash]The Basis for Metabolic Engineering of Medicinal Plants. Plant Cell. 1995 Jul;7(7):1059–1070. doi: 10.1105/tpc.7.7.1059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Landry L. G., Chapple C. C., Last R. L. Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol. 1995 Dec;109(4):1159–1166. doi: 10.1104/pp.109.4.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Last R. L., Fink G. R. Tryptophan-Requiring Mutants of the Plant Arabidopsis thaliana. Science. 1988 Apr 15;240(4850):305–310. doi: 10.1126/science.240.4850.305. [DOI] [PubMed] [Google Scholar]
- Li J., Last R. L. The Arabidopsis thaliana trp5 mutant has a feedback-resistant anthranilate synthase and elevated soluble tryptophan. Plant Physiol. 1996 Jan;110(1):51–59. doi: 10.1104/pp.110.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Niyogi K. K., Fink G. R. Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway. Plant Cell. 1992 Jun;4(6):721–733. doi: 10.1105/tpc.4.6.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Niyogi K. K., Last R. L., Fink G. R., Keith B. Suppressors of trp1 fluorescence identify a new arabidopsis gene, TRP4, encoding the anthranilate synthase beta subunit. Plant Cell. 1993 Sep;5(9):1011–1027. doi: 10.1105/tpc.5.9.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Radwanski E. R., Zhao J., Last R. L. Arabidopsis thaliana tryptophan synthase alpha: gene cloning, expression, and subunit interaction. Mol Gen Genet. 1995 Oct 25;248(6):657–667. doi: 10.1007/BF02191705. [DOI] [PubMed] [Google Scholar]
- Rose A. B., Casselman A. L., Last R. L. A Phosphoribosylanthranilate Transferase Gene Is Defective in Blue Fluorescent Arabidopsis thaliana Tryptophan Mutants. Plant Physiol. 1992 Oct;100(2):582–592. doi: 10.1104/pp.100.2.582. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ryals J., Lawton K. A., Delaney T. P., Friedrich L., Kessmann H., Neuenschwander U., Uknes S., Vernooij B., Weymann K. Signal transduction in systemic acquired resistance. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4202–4205. doi: 10.1073/pnas.92.10.4202. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsuji J., Jackson E. P., Gage D. A., Hammerschmidt R., Somerville S. C. Phytoalexin Accumulation in Arabidopsis thaliana during the Hypersensitive Reaction to Pseudomonas syringae pv syringae. Plant Physiol. 1992 Apr;98(4):1304–1309. doi: 10.1104/pp.98.4.1304. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., Chandler D., Slusarenko A., Ward E., Ryals J. Acquired resistance in Arabidopsis. Plant Cell. 1992 Jun;4(6):645–656. doi: 10.1105/tpc.4.6.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vögeli U., Chappell J. Induction of sesquiterpene cyclase and suppression of squalene synthetase activities in plant cell cultures treated with fungal elicitor. Plant Physiol. 1988 Dec;88(4):1291–1296. doi: 10.1104/pp.88.4.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yalpani N., Silverman P., Wilson T. M., Kleier D. A., Raskin I. Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell. 1991 Aug;3(8):809–818. doi: 10.1105/tpc.3.8.809. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhao J., Last R. L. Immunological characterization and chloroplast localization of the tryptophan biosynthetic enzymes of the flowering plant Arabidopsis thaliana. J Biol Chem. 1995 Mar 17;270(11):6081–6087. doi: 10.1074/jbc.270.11.6081. [DOI] [PubMed] [Google Scholar]