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. 1995 Nov;7(11):1787–1799. doi: 10.1105/tpc.7.11.1787

Creation of a Metabolic Sink for Tryptophan Alters the Phenylpropanoid Pathway and the Susceptibility of Potato to Phytophthora infestans.

K Yao 1, V De Luca 1, N Brisson 1
PMCID: PMC161038  PMID: 12242360

Abstract

The creation of artificial metabolic sinks in plants by genetic engineering of key branch points may have serious consequences for the metabolic pathways being modified. The introduction into potato of a gene encoding tryptophan decarboxylase (TDC) isolated from Catharanthus roseus drastically altered the balance of key substrate and product pools involved in the shikimate and phenylpropanoid pathways. Transgenic potato tubers expressing the TDC gene accumulated tryptamine, the immediate decarboxylation product of the TDC reaction. The redirection of tryptophan into tryptamine also resulted in a dramatic decrease in the levels of tryptophan, phenylalanine, and phenylalanine-derived phenolic compounds in transgenic tubers compared with nontransformed controls. In particular, wound-induced accumulation of chlorogenic acid, the major soluble phenolic ester in potato tubers, was found to be two- to threefold lower in transgenic tubers. Thus, the synthesis of polyphenolic compounds, such as lignin, was reduced due to the limited availability of phenolic monomers. Treatment of tuber discs with arachidonic acid, an elicitor of the defense response, led to a dramatic accumulation of soluble and cell wall-bound phenolics in tubers of untransformed potato plants but not in transgenic tubers. The transgenic tubers were also more susceptible to infection after inoculation with zoospores of Phytophthora infestans, which could be attributed to the modified cell wall of these plants. This study provides strong evidence that the synthesis and accumulation of phenolic compounds, including lignin, could be regulated by altering substrate availability through the introduction of a single gene outside the pathway involved in substrate supply. This study also indicates that phenolics, such as chlorogenic acid, play a critical role in defense responses of plants to fungal attack.

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Selected References

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  1. Bate N. J., Orr J., Ni W., Meromi A., Nadler-Hassar T., Doerner P. W., Dixon R. A., Lamb C. J., Elkind Y. Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-determining step in natural product synthesis. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7608–7612. doi: 10.1073/pnas.91.16.7608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bentley R. The shikimate pathway--a metabolic tree with many branches. Crit Rev Biochem Mol Biol. 1990;25(5):307–384. doi: 10.3109/10409239009090615. [DOI] [PubMed] [Google Scholar]
  3. Bolwell G. P., Robbins M. P., Dixon R. A. Metabolic changes in elicitor-treated bean cells. Enzymic responses associated with rapid changes in cell wall components. Eur J Biochem. 1985 May 2;148(3):571–578. doi: 10.1111/j.1432-1033.1985.tb08878.x. [DOI] [PubMed] [Google Scholar]
  4. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  5. Bradley D. J., Kjellbom P., Lamb C. J. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell. 1992 Jul 10;70(1):21–30. doi: 10.1016/0092-8674(92)90530-p. [DOI] [PubMed] [Google Scholar]
  6. Brisson L. F., Tenhaken R., Lamb C. Function of Oxidative Cross-Linking of Cell Wall Structural Proteins in Plant Disease Resistance. Plant Cell. 1994 Dec;6(12):1703–1712. doi: 10.1105/tpc.6.12.1703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chavadej S., Brisson N., McNeil J. N., De Luca V. Redirection of tryptophan leads to production of low indole glucosinolate canola. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2166–2170. doi: 10.1073/pnas.91.6.2166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Constabel C. P., Bertrand C., Brisson N. Transgenic potato plants overexpressing the pathogenesis-related STH-2 gene show unaltered susceptibility to Phytophthora infestans and potato virus X. Plant Mol Biol. 1993 Aug;22(5):775–782. doi: 10.1007/BF00027364. [DOI] [PubMed] [Google Scholar]
  9. De Luca V., Fernandez J. A., Campbell D., Kurz W. G. Developmental Regulation of Enzymes of Indole Alkaloid Biosynthesis in Catharanthus roseus. Plant Physiol. 1988 Feb;86(2):447–450. doi: 10.1104/pp.86.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. De Luca V., Marineau C., Brisson N. Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal dopa decarboxylases. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2582–2586. doi: 10.1073/pnas.86.8.2582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Elkind Y., Edwards R., Mavandad M., Hedrick S. A., Ribak O., Dixon R. A., Lamb C. J. Abnormal plant development and down-regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. Proc Natl Acad Sci U S A. 1990 Nov;87(22):9057–9061. doi: 10.1073/pnas.87.22.9057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ely B., Pittard J. Aromatic amino acid biosynthesis: regulation of shikimate kinase in Escherichia coli K-12. J Bacteriol. 1979 Jun;138(3):933–943. doi: 10.1128/jb.138.3.933-943.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Farmer E. E. Effects of fungal elicitor on lignin biosynthesis in cell suspension cultures of soybean. Plant Physiol. 1985 Jun;78(2):338–342. doi: 10.1104/pp.78.2.338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ferguson I. B., Lurie S., Bowen J. H. Protein Synthesis and Breakdown during Heat Shock of Cultured Pear (Pyrus communis L.) Cells. Plant Physiol. 1994 Apr;104(4):1429–1437. doi: 10.1104/pp.104.4.1429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Iiyama K., Lam TBT., Stone B. A. Covalent Cross-Links in the Cell Wall. Plant Physiol. 1994 Feb;104(2):315–320. doi: 10.1104/pp.104.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kato Y., Yamanouchi H., Hinata K., Ohsumi C., Hayashi T. Involvement of Phenolic Esters in Cell Aggregation of Suspension-Cultured Rice Cells. Plant Physiol. 1994 Jan;104(1):147–152. doi: 10.1104/pp.104.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Klee H. J., Hayford M. B., Kretzmer K. A., Barry G. F., Kishore G. M. Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. Plant Cell. 1991 Nov;3(11):1187–1193. doi: 10.1105/tpc.3.11.1187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maher E. A., Bate N. J., Ni W., Elkind Y., Dixon R. A., Lamb C. J. Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7802–7806. doi: 10.1073/pnas.91.16.7802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Maina G., Allen R. D., Bhatia S. K., Stelzig D. A. Phenol metabolism, phytoalexins, and respiration in potato tuber tissue treated with Fatty Acid. Plant Physiol. 1984 Nov;76(3):735–738. doi: 10.1104/pp.76.3.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Matton D. P., 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. 1993 May;22(2):279–291. doi: 10.1007/BF00014935. [DOI] [PubMed] [Google Scholar]
  21. SRINIVASAN P. R., SHIGEURA H. T., SPRECHER M., SPRINSON D. B., DAVIS B. D. The biosynthesis of shikimic acid from D-glucose. J Biol Chem. 1956 May;220(1):477–497. [PubMed] [Google Scholar]
  22. Songstad D. D., De Luca V., Brisson N., Kurz W. G., Nessler C. L. High levels of tryptamine accumulation in transgenic tobacco expressing tryptophan decarboxylase. Plant Physiol. 1990 Nov;94(3):1410–1413. doi: 10.1104/pp.94.3.1410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. van der Krol A. R., Mur L. A., Beld M., Mol J. N., Stuitje A. R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell. 1990 Apr;2(4):291–299. doi: 10.1105/tpc.2.4.291. [DOI] [PMC free article] [PubMed] [Google Scholar]

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