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Planta

, Volume 197, Issue 1, pp 49–56 | Cite as

Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha x piperita) rely exclusively on plastid-derived isopentenyl diphosphate

  • David McCaskill
  • Rodney Croteau
Article
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Accepted:

Abstract

The subcellular compartmentation of isopentenyl diphosphate (IPP) synthesis was examined in secretory cells isolated from glandular trichomes of peppermint (Mentha x piperita L. cv. Black Mitcham). As a consequence of their anatomy and the conditions of their isolation, the isolated secretory cells are non-specifically permeable to low-molecular-weight water-soluble metabolites. Thus, the cytoplasm is readily accessible to the exogenous buffer whereas the selective permeability of subcellular organelles is maintained. With the appropriate choice of exogenous substrates, this feature allows the assessment of cytoplasmic and organellar (e.g. plastidic) metabolism in situ. Glycolytic substrates such as [14C]glucose-6-phosphate and [14C]pyruvic acid are incorporated into both monoterpenes and sesquiterpenes with a monoterpene:sesquiterpene ratio that closely mimics that observed in vivo, indicating that the correct subcellular partitioning of these substrates is maintained in this model system. Additionally, exogenous [14C]mevalonic acid and [14C]IPP, which are both intitially metabolized in the cytoplasm, produce an abnormally high proportion of sesquiterpenes. In contrast, incubation with either [14C]citrate or [14C]acetyl-CoA results in the accumulation of 3-hydroxy-3-methylglutaryl-CoA (HMG-CoA) with no detectable isoprenoids formed. Taken together, these results indicate that the cytoplasmic mevalonic acid pathway is blocked at HMG-CoA reductase and that the IPP utilized for both monoterpene and sesquiterpene biosynthesis is synthesized exclusively in the plastids.

Key words

Isopentenyl diphosphate Isoprenoid biosynthesis Leucoplast Mentha Mevalonic acid pathway 

Abbreviations

DMAPP

dimethylallyl diphosphate

FPP

farnesyl diphosphate

GLC

gas liquid chromatography

GPP

geranyl diphosphate

HMG-CoA

3-hydroxy-3-methylglutaryl-CoA

IPP

isopentenyl diphosphate

PEP

phosphoenolpyruvic acid

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References

  1. Amelunxen, F. (1965) Elektronenmikroskopische Untersuchungen an den Drüsenschuppen von Mentha piperita L. Planta Med. 13, 457–473Google Scholar
  2. Amelunxen, F., Wahlig, T., Arbeiter, H. (1969) Über den Nachweis des ätherischen Öls in isolierten Drüsenhaaren und Drüsenschuppen von Mentha piperita L. Z. Pflanzenphysiol. 61, 68–72Google Scholar
  3. Burden R.S., Cooke, D.T., Carter, G.A. (1989) Inhibitors of sterol biosynthesis and growth in plants and fungi. Phytochemistry 28, 1791–1804Google Scholar
  4. Cheniclet, C., Carde, J.-P. (1985) Presence of leucoplasts in secretory cells and of monoterpenes in the essential oil: a correlative study. Isr. J. Bot. 34, 219–238Google Scholar
  5. Coates, R.M., Denissen, J.F., Croteau, R.B., Wheeler, C.J. (1987) Geminal dimethyl stereochemistry in the enzymatic cylization of geranyl pyrophosphate to (+)- and (−)-α-pinene. J. Am. Chem. Soc. 109, 4399–4401Google Scholar
  6. Connolly, J.D., Hill, R.A. (1992) Dictionary of Terpenoids, Chapman and Hall, New YorkGoogle Scholar
  7. Croteau, R. (1987) Biosynthesis and catabolism of monoterpenoids. Chem. Rev. 87, 929–954Google Scholar
  8. Croteau, R., Martinkus, C. (1979) Metabolism of monoterpenes. Demonstration of (+)-neomenthyl-β-d-glucoside as a major metabolite of (−)-menthone in peppermint (Mentha piperita). Plant Physiol. 64 169–175Google Scholar
  9. Croteau, R.B., Satterwhite, D.M. (1990) Method for radio-capillary gas chromatography employing a modified oxidation-reduction train and flow-through detector. J. Chromatogr. 500, 349–54Google Scholar
  10. Gershenzon, J., Croteau, R. (1991) Terpenoids. In: Herbivores: Their interactions with secondary plant metabolites. The Chemical Participants. Vol. I, pp. 165–219, Rosenthal, G.A., Berenbaum, M.R. eds. Academic Press, San DiegoGoogle Scholar
  11. Gershenzon, J., Croteau, R. (1993) Terpenoid biosynthesis: The basic pathway and formation of monoterpenes, sesquiterpenes and diterpenes. In: Lipid Metabolism in Plants, pp. 340–388, Moore, Jr. T.S. ed. CRC Press, Boca Raton, Fla.Google Scholar
  12. Gershenzon, J., McCaskill, D., Rajaonarivony, J.I.M., Mihaliak, C., Karp, F., Croteau, R. (1992) Isolation of secretory cells from plant glandular trichomes and their use in biosynthetic studies of monoterpenes and other gland products. Anal. Biochem. 200, 130–138Google Scholar
  13. Gray, J.C. (1987) Control of isoprenoid biosynthesis in higher plants. Adv. Bot. Res. 14, 25–91Google Scholar
  14. Hanson, J.B. (1985) Membrane transport systems of plant mitochondria. In: Encyclopedia of plant physiology. N.S. Vol. 18: Higher plant cell respiration, pp. 248–280, Douce, R., Day, D.A. eds. Springer-Verlag, New YorkGoogle Scholar
  15. Heintze, A., Görlach, J., Leuschner, C., Hoppe, P., Hagelstein, P., Schulze-Siebert, D, Schultz, G. (1990) Plastidic isoprenoid synthesis during chloroplast development. Plant Physiol. 93, 1121–1127Google Scholar
  16. Huang, L.-S., Romani, R.J. (1991) Metabolically driven self-restoration of energy-linked functions by avocado mitochondria. Plant Physiol. 95, 1096–1105Google Scholar
  17. Kaethner, T.M., ap Rees, T. (1985) Intracellular location of ATP citrate lyase in leaves of Pisum sativum L. Planta 163, 290–294Google Scholar
  18. Kleinig, H. (1989) The role of plastids in isoprenoid biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 39–59Google Scholar
  19. Lawrence, B.M., Hogg, J.W., Terhune, S.J. (1972) Essential oils and their trace constituents. X. Some new trace constituents in the oil of Mentha piperita L. Flav. Indust. 3, 467–472Google Scholar
  20. Liedvogel, B. (1986) Acetyl coenzyme A and isopentenylpyrophosphate as lipid precursors in plant cells — biosynthesis and compartmentation. J. Plant Physiol. 124, 211–222Google Scholar
  21. McCaskill, D., Croteau, R. (1993) Procedures for the isolation and quantification of the intermediates of the mevalonic acid pathway. Anal. Biochem. 215, 142–149Google Scholar
  22. McCaskill, D., Gershenzon, J., Croteau, R. (1992) Morphology and monoterpene biosynthetic capabilities of secretory cell clusters isolated from glandular trichomes of peppermint (Mentha piperita L.). Planta 187, 445–454Google Scholar
  23. Munck, S.L., Croteau, R. (1990) Purification and characterization of the sesquiterpene cyclase patchoulol synthase from Pogostemon cablin. Arch. Biochem. Biophys. 282, 58–64Google Scholar
  24. Ohlrogge, J.B., Jaworski, J.G., Post-Beittenmiller, D. (1993) De novo fatty acid biosynthesis. In: Lipid metabolism in plants, pp. 3–32, Moore, Jr., T.S., ed. CRC Press, Boca RatonGoogle Scholar
  25. Peterson, J.A., Prough, R.A. (1986) Cytochrome P-450 reductase and cytochrome b5 in cytochrome P-450 catalysis. In: Cytochrome P-450. Structure, mechanism and biochemistry, pp. 89–117, Ortiz de Montellano P.R., ed. Plenum Press, New YorkGoogle Scholar
  26. Randall, D.D., Miernyk, J.A., Fang, T.K., Budde, R.J.A., Schuller, K.A. (1989) Regulation of the pyruvate dehydrogenase complexes in plants. In: Annals of the New York Academy of Sciences, pp. 192–205, Roche, T.E., Patel, M.S., eds. New YorkGoogle Scholar
  27. Rohmer, M., Knani, M., Simonin, P., Sutter, B., Sahm, H. (1993) Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem. J. 295, 517–524Google Scholar
  28. Schneider, M.M., Hampp, R., Ziegler, H. (1977) Envelope permeability to possible precursors of carotenoid biosynthesis during chloroplast-chromoplast transformation. Plant Physiol. 60, 518–520Google Scholar
  29. Srivastava, D.K., Bernhard, S.A. (1987) Biophysical chemistry of metabolic reaction sequences in concentrated enzyme solution and in the cell. Annu. Rev. Biophys. Biophys. Chem. 16, 175–204Google Scholar
  30. Stermer, B.A., Bianchini, G.M., Korth, K.L. (1994) Regulation of HMG-CoA reductase acitivity in plants. J. Lipid Res. 35, 1133–1140Google Scholar
  31. Wagner, K.G., Backer, A.I. (1992) Dynamics of nucleotides in plants studied on a cellular basis. In: International reviews of cytology, pp. 1–84, Jeon, K.W., Friedlander, M., eds. Academic Press, New YorkGoogle Scholar
  32. Wellburn, A.R., Hampp, R. (1976) Uptake of mevalonate and acetate during plastid developmentf. Biochem. J. 158, 231–233Google Scholar
  33. Werker, E., Ravid, U., Putievsky, E. (1985) Structure of glandular hairs and identification of the main components of their secreted material in some species of the Labiatae. Isr. J. Bot. 34, 31–45Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  1. 1.Institute of Biological Chemistry, Washington State UniversityPullmanUSA

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