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

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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.

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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

References

  • Amelunxen, F. (1965) Elektronenmikroskopische Untersuchungen an den Drüsenschuppen von Mentha piperita L. Planta Med. 13, 457–473

    Google Scholar 

  • 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, 68–72

    Google Scholar 

  • Burden R.S., Cooke, D.T., Carter, G.A. (1989) Inhibitors of sterol biosynthesis and growth in plants and fungi. Phytochemistry 28, 1791–1804

    Google Scholar 

  • 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, 219–238

    Google Scholar 

  • 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, 4399–4401

    Google Scholar 

  • Connolly, J.D., Hill, R.A. (1992) Dictionary of Terpenoids, Chapman and Hall, New York

    Google Scholar 

  • Croteau, R. (1987) Biosynthesis and catabolism of monoterpenoids. Chem. Rev. 87, 929–954

    Google Scholar 

  • 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. 64 169–175

    Google Scholar 

  • 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, 349–54

    Google Scholar 

  • 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 Diego

    Google Scholar 

  • 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 

  • 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, 130–138

    Google Scholar 

  • Gray, J.C. (1987) Control of isoprenoid biosynthesis in higher plants. Adv. Bot. Res. 14, 25–91

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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, 1121–1127

    Google Scholar 

  • Huang, L.-S., Romani, R.J. (1991) Metabolically driven self-restoration of energy-linked functions by avocado mitochondria. Plant Physiol. 95, 1096–1105

    Google Scholar 

  • Kaethner, T.M., ap Rees, T. (1985) Intracellular location of ATP citrate lyase in leaves of Pisum sativum L. Planta 163, 290–294

    Google Scholar 

  • Kleinig, H. (1989) The role of plastids in isoprenoid biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 39–59

    Google Scholar 

  • 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, 467–472

    Google Scholar 

  • Liedvogel, B. (1986) Acetyl coenzyme A and isopentenylpyrophosphate as lipid precursors in plant cells — biosynthesis and compartmentation. J. Plant Physiol. 124, 211–222

    Google Scholar 

  • McCaskill, D., Croteau, R. (1993) Procedures for the isolation and quantification of the intermediates of the mevalonic acid pathway. Anal. Biochem. 215, 142–149

    Google Scholar 

  • 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, 445–454

    Google Scholar 

  • Munck, S.L., Croteau, R. (1990) Purification and characterization of the sesquiterpene cyclase patchoulol synthase from Pogostemon cablin. Arch. Biochem. Biophys. 282, 58–64

    Google Scholar 

  • 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 Raton

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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 York

  • 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, 517–524

    Google Scholar 

  • Schneider, M.M., Hampp, R., Ziegler, H. (1977) Envelope permeability to possible precursors of carotenoid biosynthesis during chloroplast-chromoplast transformation. Plant Physiol. 60, 518–520

    Google Scholar 

  • 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, 175–204

    Google Scholar 

  • Stermer, B.A., Bianchini, G.M., Korth, K.L. (1994) Regulation of HMG-CoA reductase acitivity in plants. J. Lipid Res. 35, 1133–1140

    Google Scholar 

  • 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 York

    Google Scholar 

  • Wellburn, A.R., Hampp, R. (1976) Uptake of mevalonate and acetate during plastid developmentf. Biochem. J. 158, 231–233

    Google Scholar 

  • 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, 31–45

    Google Scholar 

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Authors and Affiliations

  1. Institute of Biological Chemistry, Washington State University, 99164-6340, Pullman, WA, USA

    David McCaskill & Rodney Croteau

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  1. David McCaskill
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  2. Rodney Croteau
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Correspondence to Rodney Croteau.

Additional information

This investigation was supported in part by U.S. Department of Energy Grant DE-FG06-88ER 13869, the Mint Industry Research Council, and Project 0268 from the Agricultural Research Center, Washington State University. We thank Jonathan Gershenzon for helpful criticisms of the manuscript and Greg Wichelns for growing the plants.

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McCaskill, D., Croteau, R. Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha x piperita) rely exclusively on plastid-derived isopentenyl diphosphate. Planta 197, 49–56 (1995). https://doi.org/10.1007/BF00239938

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  • DOI: https://doi.org/10.1007/BF00239938

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