Skip to main content
Log in

Efficient uptake of flavonoids into parsley (Petroselinum hortense) vacuoles requires acylated glycosides

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Vacuoles were prepared from cultured parsley cells by polyamine-induced rupture of protoplasts. Acid-phosphatase activity, associated exclusively with the vacuoles, served for determination of vacuole yield in subsequent transport studies. Isolated vacuoles rapidly accumulated [2‴-14C]apigenin 7-O-(6-O-malonylglucoside) or 2″-14C]β-methyl D-6-O-malonylglucoside added at approximately 20 nM and 1.5 μM concentration, respectively, to the incubation mixture. The accumulation was linear with time and strongly dependent on alkaline buffer conditions as well as on the age of the vacuole preparation. Subsequent addition of a malonic hemiester esterase did not relase the label from the vacuoles. Moreover, neither [2-14C]apigenin 7-O-glucoside or [2-14C]malonic acid accumulated in the vacuoles under any assay conditions, nor did such compounds or β-methyl D-glucopyranoside, a malonic diester, and a succinic monoester inhibit transport of the acylated flavonoid. Transport was, however, inhibited by β-methyl D-6-O-malonylglucopyranoside. Vacuoles which had been incubated for more than 40 min at pH 8.0 did not stain any more with neutral-red dye and concomitantly lost the previously accumulated acylated glucoside. Our data confirm that malonylglucoside uptake by parsley vacuoles involves selective transport sites. It is suggested that changes in the molecular symmetry of the malonylglucosides are responsible for vacuolar trapping of flavonoids in parsley.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DEAE:

diethylamionethyl

References

  • Alibert, G., Boudet, A.M., Canut, H., Rataboul, P. (1985) Protoplasts in studies of vacuolar storage compounds. In: The physiological properties of plant protoplasts, pp. 105–115 Pilet, P.E., ed. Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • Alibert, G., Boudet, A.M., Rataboul, P. (1982) Transport of o-coumaric acid glucoside in isolated vacuoles of sweet clover. In: Plasmalemma and tonoplast transport: their functions in the plant cell. Developments in plant biology, vol. 7, pp. 193–200, Marmé, D., Marrè, E., Hertel, R., eds. Elsevier, Amsterdam New York Oxford

    Google Scholar 

  • Bergmeyer, H.U. (1974) Methoden der enzymatischen Analyse. Verlag Chemie, Weinheim

    Google Scholar 

  • Boller, T., Kende, H. (1979) Hydrolytic enzymes in the central vacuole of plant cells. Plant Physiol. 63, 1123–1132

    Google Scholar 

  • Boudet, A.M., Canut, H., Alibert, G. (1981) Isolation and characterization of vacuoles from Melilotus alba mesophyll. Plant Physiol. 68, 1354–1358

    Google Scholar 

  • Bridle, P., Loeffler, R.S.T., Timberlake, C.F., Self, R. (1984) Cyanidin 3-malonylglucoside in Cichorium intybus. Phytochemistry 23, 2968–2969

    Google Scholar 

  • Buser-Suter, C., Wiemken, A., Matile, Ph. (1982) A malic acid permease in isolated vacuoles of a crassulacean acid metabolism plant. Plant Physiol. 69, 456–459

    Google Scholar 

  • Deus-Neumann, B., Zenk, M.H. (1984) A highly selective alkaloid uptake system in vacuoles of higher plants. Planta 162, 250–260

    Google Scholar 

  • Doll, S., Rodier, F., Willenbrink, J. (1979) Accumulation of sucrose in vacuoles isolated from red beet tissue. Planta 144, 407–411

    Google Scholar 

  • Dürr, M., Boller, T., Wiemken, A. (1975) Polybase induced lysis of yeast sphaeroplasts. Arch. Microbiol. 105, 319–327

    Google Scholar 

  • Frehner, M., Keller, F., Wiemken, A. (1984) Localization of fructan metabolism in the vacuoles isolated from protoplasts of Jerusalem artichoke tissue. J. Plant Physiol. 116, 197–208

    Google Scholar 

  • Garcia-Martinez, J.L., Ohlrogge, J.B., Rappaport, L. (1981) Differential compartmentation of gibberellin A1, and its metabolites in vacuoles of cowpea and barley leaves. Plant Physiol. 68, 865–867

    Google Scholar 

  • Ghisla, S., Mack, R., Blankenhorn, G., Hemmerich, P., Krienitz, E., Kuster, T. (1984) Structure of a novel flavin chromophore from Avena coleoptiles, the possible “blue light” photoreceptor. Eur. J. Biochem. 138, 339–344

    Google Scholar 

  • Guy, M., Reinhold, L., Michaeli, D. (1979) Direct evidence for a sugar transport mechanism in isolated vacuoles. Plant Physiol. 64, 61–64

    Google Scholar 

  • Holländer-Czytko, H., Amrhein, N. (1983) Subcellular compartmentation of shikimic acid and phenylalanine in buck-wheat cell suspension cultures grown in the presence of shkikmate pathway inhibitors. Plant Sci. Lett. 29, 89–96

    Google Scholar 

  • Hrazdina, G., Marx, G.A., Hoch, H.C. (1982) Distribution of secondary plant metabolites and their biosynthetic enzymes in pea (Pisum sativum L.) leaves. Plant Physiol. 70, 745–748

    Google Scholar 

  • Kaiser, G., Heber, U. (1984) Sucrose transport into vacuoles isolated from barley mesophyll protoplasts. Planta 161, 562–568

    Google Scholar 

  • Kasai, T., Okuda, M., Sakamura, S. (1981) 6-O-Malonyl-β-methyl-D-glucopyranoside from roots of Rumex obtusifolius. Phytochemistry, 20, 1131–1132

    Google Scholar 

  • Keller, F., Wiemken, A. (1982) Differential compartmentation of sucrose and gentianose in the cytosol and vacuoles of storage root protoplasts from Gentiana lutea L.. Plant Cell Rep. 1, 274–277

    Google Scholar 

  • Kenyon, W.H., Kringstad, R., Black, C.C. (1978) Diurnal changes in the malic content of vacuoles isolated from leaves of the Crassulacean acid metabolism plant, Sedum telephium. FEBS Lett. 94, 281–283

    Google Scholar 

  • Kesselmeier, J., Urban, B. (1983) Subcellular localization of saponins in green and etiolated leaves and green protoplasts of oat (Avena sativa L.). Protoplasma 114, 133–140

    Google Scholar 

  • Kleiner, D. (1981) The transport of NH3 and NH +4 across biological membranes. Biochim. Biophys. Acta 639, 41–52

    Google Scholar 

  • Knuth, M.E., Keith, B., Clark, C., Garcia-Martinez, J.L., Rappaport, L. (1983) Stabilization and transport capacity of cowpea and barley vacuoles. Plant Cell Physiol. 24, 423–432

    Google Scholar 

  • Koester, J., Bussmann, R., Barz, W. (1984) Malonyl-coenzyme A: isoflavone 7-O-glucoside-6″-malonyltransferase from roots of chick pea (Cicer arietinum L.). Arch. Biochem. Biophys. 234, 513–521

    Google Scholar 

  • Kurkdijan, A., Guern, J. (1981) Vacuolar pH measurement in higher plant cells. Plant Physiol. 67, 953–957

    Google Scholar 

  • Loeffelhardt, W., Kopp, B., Kubelka, W. (1979) Intracellular distribution of cardiac glycosides in leaves of Convallaria majalis. Phytochemistry 18, 1289–1291

    Google Scholar 

  • Lüttge, U., Smith, J.A.C., Marigo, G., Osmond, C.B. (1981) Energetics of malate accumulation in the vacuoles of Kalanchoe tubiflora cells. FEBS Lett. 126, 81–83

    Google Scholar 

  • Mäder, M. (1984) Die pflanzliche Vakuole aus biochemischer Sicht. Biol. Unserer Zeit 14, 171–176

    Google Scholar 

  • Matern, U. (1983) Acylhydrolases from parsley (Petroselinum hortense). Relative distribution and properties of four esterases hydrolyzing malonic acid hemiesters of flavonoid glucosides. Arch. Biochem. Biophys. 224, 261–271

    Google Scholar 

  • Matern, U., Feser, C., Hammer, D. (1983b) Further characterization and regulation of malonyl-coenzyme A: flavonoid glucoside malonyltransferases from parsley cell suspension cultures. Arch. Biochem. Biophys. 226, 206–217

    Google Scholar 

  • Matern, U., Feser, C., Heller, W. (1984) N-Malonyltransferases from peanut. Arch. Biochem. Biophys. 235, 218–227

    Google Scholar 

  • Matern, U., Heller, W., Himmelspach, K. (1983a) Conformational changes of apigenin 7-O-(6-O-malonylglucoside), a vacuolar pigment from parsley, with solvent composition and proton concentration. Eur. J. Biochem. 133 439–448

    Google Scholar 

  • Matile, Ph. (1975) The lytic compartment of plant cells. Cell biology monographs, vol. 1, Alfert, M., Beermann, W., Rudkin, G., Sandritter, W., Sitte, P., eds. Springer, Wien New York

    Google Scholar 

  • Matile, Ph. (1984) Das toxische Kompartiment der Pflanzenzelle. Naturwissenschaften, 71, 18–24

    Google Scholar 

  • Moskowitz, A.H., Hrazdina, G. (1981) Vacuolar contents of fruit subepidermal cells from Vitis species. Plant Physiol. 68, 686–692

    Google Scholar 

  • Neumann, D., Krauss, G., Hieke, M., Gröger, D. (1983) Indole alkaloid formation and storage in cell suspension cultures of Catharanthus roseus. Planta Med. 48, 20–23

    Google Scholar 

  • Reinhold, L., Kaplan, A. (1984) Membrane transport of sugars and amino acids. Annu. Rev. Plant Physiol. 35, 45–83

    Google Scholar 

  • Saunders, J.A. (1979) Investigations of vacuoles isolated from tobacco. I. Quantitation of nicotine. Plant Physiol. 64, 74–78

    Google Scholar 

  • Schmitt, R., Sandermann, Jr., H. (1982) Specific localization of β-D-glucoside conjugates of 2,4-dichlorophenoxyacetic acid in soybean vacuoles. Z. Naturforsch. 37 Teil C, 772–777

    Google Scholar 

  • Sitte, P. (1972) Vitalfärbung nach dem Ionenfallen-Prinzip. Biol. Unserer Zeit. 2, 192–194

    Google Scholar 

  • Tamura, H., Kondo, T., Kato, Y., Goto, T. (1983) Structures of a succinyl anthocyanin and a malonyl flavone, two constituents of the complex blue pigment of cornflower Centaurea cyanus. Tetrahedron Lett. 24, 5749–5752

    Google Scholar 

  • Thom, M., Komor, E., Maretzki, A. (1982) Vacuoles from sugarcane suspension cultures. II. Characterization of sugar uptake. Plant Physiol. 69, 1320–1325

    Google Scholar 

  • Werner, C., Matile, Ph. (1985) Accumulation of coumaryl glucosides in vacuoles of barley mesophyll protoplasts. J. Plant Physiol. 118, 237–249

    Google Scholar 

  • Wöldecke, M., Herrmann, K. (1974) Flavonole und Flavone der Gemüsearten. IV. Flavonole und Flavone des Kopfsalates und der Endivien. Z. Lebensm. Unters. Forsch. 156, 153–157

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matern, U., Reichenbach, C. & Heller, W. Efficient uptake of flavonoids into parsley (Petroselinum hortense) vacuoles requires acylated glycosides. Planta 167, 183–189 (1986). https://doi.org/10.1007/BF00391413

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00391413

Key words

Navigation