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Planta

, Volume 187, Issue 4, pp 445–454 | Cite as

Morphology and monoterpene biosynthetic capabilities of secretory cell clusters isolated from glandular trichomes of peppermint (Mentha piperita L.)

  • David McCaskill
  • Jonathan Gershenzon
  • Rodney Croteau
Article
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Accepted:

Abstract

Secretory cells were isolated from the monoterpene-producing glandular trichomes (peltate form) of peppermint as clusters of eight cells each. These isolated structures were shown to be non-specifically permeable to low-molecular-weight, water-soluble cofactors and substrates. Short incubation periods with the polar dye Lucifer yellow iodoacetamide (Mr=660) resulted in a uniform staining of the cytoplasm, with exclusion of the dye from the vacuole. The molecular-weight exclusion limit for this permeability was shown to be less than approx. 1800, based on exclusion of fluorescein-conjugated dextran (Mr ∼ 1800). Intact secretory cell clusters very efficiently incorporated [3H]geranyl pyrophosphate into monoterpenes. The addition of exogenous cofactors and redox substrates affected the distribution of monoterpenes synthesized from [3H]geranyl pyrophosphate, demonstrating that the cell clusters were permeable to these compounds and that the levels of endogenous cofactors and redox substrates were depleted in the isolated cells. When provided with the appropriate cofactors, such as NADPH, NAD+, ATP, ADP and coenzyme A, the isolated secretory cell clusters incorporated [14C]sucrose into monoterpenes, indicating that these structures are capable of the de-novo biosynthesis of monoterpenes from a primary carbon source, and that they maintain a high degree of metabolic competence in spite of their permeable nature.

Key words

Glandular trichome Isoprenoid biosynthesis Mentha Monoterpene biosynthesis 

Abbreviations

GLC

gas liquid chromatography

LSCM

laser scanning confocal microscopy

LY-IA

Lucifer yellow iodoacetamide

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References

  1. Amelunxen, F. (1964) Elektronenmikroskopische Untersuchungen an den Drüsenhaaren von Mentha piperita L. Planta Med. 12, 121–139Google Scholar
  2. Amelunxen, F. (1965) Elektronenmikroskopische Untersuchungen an den Drüsenschuppen von Mentha piperita L. Planta Med. 13, 457–473Google Scholar
  3. 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
  4. Battaile, J., Burbott, A.J., Loomis, W.D. (1968) Monoterpene interconversions: Metabolism of pulegone by a cell-free system from Mentha piperita. Phytochemistry 7, 1159–1163Google Scholar
  5. de Belder, A.N., Granath, K. (1973) Preparation and properties of fluorescein-labelled dextrans. Carbohydr. Res. 30, 375–378Google Scholar
  6. Burbott, A.J., Loomis, W.D. (1967) Effects of light and temperature on the monoterpenes of peppermint. Plant Physiol. 42, 20–28Google Scholar
  7. Clegg, J.S., Jackson, S.A. (1988) Glycolysis in permeabilized L-929 cells. Biochem. J. 255, 335–344Google Scholar
  8. Clegg, J.S., Jackson, S.A. (1989) Evidence for intermediate channeling in the glycolytic pathway of permeabilized L-929 cells. Biochem. Biophys. Res. Comm. 160, 1409–1414Google Scholar
  9. 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
  10. Croteau, R. (1987) Biosynthesis and catabolism of monoterpenoids. Chem. Rev. 87, 929–954Google Scholar
  11. Croteau, R., Venkatachalam, K.V. (1986) Metabolism of monoterpenes: Demonstration that (+)-cis-isopulegone, not piperitenone, is the key intermediate in the conversion of (−)-isopiperitenone to (+)-pulegone in peppermint (Mentha piperita). Arch. Biochem. Biophys. 249, 306–315Google Scholar
  12. Dennis, D.T., Miernyk, J.A. (1982) Compartmentation of non-photosynthetic carbohydrate metabolism. Annu. Rev. Plant Physiol. 33, 27–50Google Scholar
  13. Fahn, A. (1979) Secretory tissues in plants. London, Academic PressGoogle Scholar
  14. Gershenzon, J., Duffy, M.A., Karp, F., Croteau, R. (1987) Mechanized techniques for the selective extraction of enzymes from plant epidermal glands. Anal. Biochem. 163, 159–164Google Scholar
  15. Gershenzon, J., Maffei, M., Croteau, R. (1989) Biochemical and histochemical localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata). Plant Physiol. 89, 1351–1357Google Scholar
  16. 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
  17. Gordon, W.P., Huitric, A.C., Seth, C.L., McClanahan, R.H., Nelson, S.D. (1987) The metabolism of the abortifacient terpene, (R)-(+)-pulegone, to a proximate toxin, menthofuran. Drug Metab. Disp. 15, 589–594Google Scholar
  18. Greenspan, P., Fowler, S.D. (1985) Spectrofluorometric studies of the lipid probe, nile red. J. Lipid Res. 26, 781–789Google Scholar
  19. Greenspan, P., Mayer, E.P., Fowler, S.D. (1985) Nile red: A selective fluorescent stain for intracellular lipid droplets. J. Cell Biol. 100, 965–973Google Scholar
  20. Kandra, L., Wagner, G.J. (1988) Studies of the site and mode of biosynthesis of tobacco trichome exudate components. Arch. Biochem. Biophys. 265, 425–432Google Scholar
  21. Karp, F., Mihaliak, C.A., Harris, J.L., Croteau, R. (1990) Monoterpene biosynthesis: Specificity of the hydroxylations of (−)-limonene by enzyme preparations from peppermint (Mentha piperita), spearmint (Mentha spicata), and perilla (Perilla frutescens) leaves. Arch. Biochem. Biophys. 276, 219–226Google Scholar
  22. Keene, C.K., Wagner, G.J. (1985) Direct demonstration of duvatrienediol biosynthesis in glandular heads of tobacco trichomes. Plant Physiol. 79, 1026–1032Google Scholar
  23. Kelsey, R.G., Reynolds, G.W., Rodriguez, E. (1984) The chemistry of biologically active constituents secreted and stored in plant glandular trichomes. In: Biology and chemistry of plant trichomes, pp. 187–241, Rodriguez, E., Healy, P.L., Mehta, I., eds. Plenum Press, New YorkGoogle Scholar
  24. Kjonaas, R., Martinkus-Taylor, C., Croteau, R. (1982) Metabolism of monoterpenes: Conversion of l-menthone to l-menthol and d-neomenthol by stereospecific dehydrogenases from peppermint (Mentha piperita) leaves. Plant Physiol. 69, 1013–1017Google Scholar
  25. Kleinig, H. (1989) The role of plastids in isoprenoid biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 39–59Google Scholar
  26. 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
  27. Liedvogel, B. (1986) Acetyl coenzyme A and isopentenylpyrophosphate as lipid precursors in plant cells-biosynthesis and compartmentation. J. Plant Physiol. 124, 211–222Google Scholar
  28. Lüttge, U. (1971) Structure and function of plant glands. Annu. Rev. Plant Physiol. 22, 23–44Google Scholar
  29. Maffei, M., Chialva, F., Sacco, T. (1989) Glandular trichomes and essential oils in developing peppermint leaves. New Phytol. 111, 707–716Google Scholar
  30. Oparka, K.J. (1991) Uptake and compartmentation of fluorescent probes by plant cells. J. Exp. Bot. 42, 565–579Google Scholar
  31. Peterson, R.L., Vermeer, J. (1984) Histochemistry of Trichomes. In: Biology and chemistry of plant trichomes, pp. 71–94, Rodriguez, E., Healy, P.L., Mehta, I., eds. Plenum Press, New YorkGoogle Scholar
  32. Robards, A.W., Lucas, W.J. (1990) Plasmodesmata. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 369–419Google Scholar
  33. Sauer, H., Pratsch, L., Peters, R. (1991) A microassay for the pore-forming activity of complement, perforin, and other cytolytic proteins based on confocal laser scanning microscopy. Anal. Biochem. 194, 418–424Google Scholar
  34. Schnepf, E. (1974) Gland cells. In: Dynamic aspects of plant ultrastructure, pp. 331–357, Robards, A. W., ed. McGraw-Hill, New YorkGoogle Scholar
  35. Schulze-Siebert, D., Schultz, G. (1987) β-Carotene synthesis in isolated spinach chloroplasts. Plant Physiol. 84, 1233–1237Google Scholar
  36. Slone, J.H., Kelsey, R.G. (1985) Isolation and purification of glandular secretory cells from Artemisia tridentata (ssp. vaseyana) by Percoll density gradient centrifugation. Am. J. Bot. 72, 1445–1451Google Scholar
  37. Thompson, ST., Stellwagen, E. (1976) Binding of Cibacron blue F3GA to proteins containing the dinucleotide fold. Proc. Nat. Acad. Sci. USA. 73, 361–365Google Scholar
  38. Valle, E.M., Heldt, H.W. (1991) Alanine synthesis by bundle sheath cells of maize. Plant Physiol. 95, 839–845Google Scholar
  39. Voirin, B., Brun, N., Bayet, C. (1990) Effects of daylength on the monoterpene composition of leaves of Mentha piperita. Phytochemistry 29, 749–755Google Scholar
  40. Weiner, H., Burnell, J.N., Woodrow, I.E., Heldt, H.W., Hatch, M.D. (1988) Metabolite diffusion into bundle sheath cells from C4 plants. Relation to C4 photosynthesis and plasmodesmatal function. Plant Physiol. 88, 815–822Google Scholar
  41. 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 1992

Authors and Affiliations

  • David McCaskill
    • 1
  • Jonathan Gershenzon
    • 1
  • Rodney Croteau
    • 1
  1. 1.Institute of Biological ChemistryWashington State UniversityPullmanUSA

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