Abstract
The mature plant cell vacuole is a multifunctional organelle which is unique to higher plants. It constitutes a compartment which is thought to be anabolically inactive and a primary site for metabolite storage and sequestration.1, 2 Cytologists carried out extensive studies of plant vacuoles during the late 1800’s and early 1900’s which revealed many of the functions of this organelle. This chapter will consider the roles of the vacuole in solute storage and sequestration, and discuss methods now being used to isolate and investigate plant vacuoles. Recent studies which have utilized vacuoles to estimate the compartmentation of solutes and enzymes will be discussed. Possible mechanisms of tonoplast transport will be considered.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Zirkle, C. 1937. The Plant Vacuole. Bot. Rev. 3: 1–30.
Guilliermond, A. 1941. The Cytoplasm of the Plant Cell. Chronica Botanica Co., Waltham, MA. pp. 1–247.
Kramer, P. J. 1955. Physical chemistry of the vacuoles. In Encyclopedia of Plant Physiology (W. Ruhland, ed.). Springer-Verlag, Berlin, Vol 1, pp. 649–660.
Voeller, B. R. 1964. The plant cell: aspects of its form and function. In The Cell (J. Brachet, A. E. Mirsky, eds.) Academic Press, New York, Vol. VI, pp. 245–312.
De Robertis, E. D. P., W. W. Narinski, F. A. Salz. 1965. The plant vacuole. In Cell Biology, 4th Ed. W. B. Saunders Co., Philadelphia, Pa.
Pisek, A. 1955. Chemie des Zellsaftes. In Encyclopedia of Plant Physiology (W. Ruhland, ed.) Vol. I, Springer-Verlag, Berlin, pp. 614–626.
Matile, P. 1978. Biochemistry and function of vacuoles. Ann. Rev. Plant Physiol. 29: 193–213.
Marty, F., D. Branton, R. A. Leigh. 1980. Plant vacuoles. In The Biochemistry of Plants (P. K. Stumpf, E. E. Conn, eds.). Vol. I, Academic Press, New York, pp. 625–658.
Leigh, R. A. 1979. Do plant vacuoles degrade cytoplasmic components? Trends in Biol. Sci. N37-N38.
Nishimura, M., H. Beevers. 1979. Hydrolysis of protein in vacuoles isolated from higher plant tissue. Nature 277: 412–413.
Van der Wilden, W., E. M. Herman, M. J. Chrispeels. 1980. Protein bodies of mung bean cotyledons as autophagic organelles. Proc. Nat. Acad. Sci. Usa 77: 428–432.
Peoples, M. B., V. C. Beilharz, S. P. Waters, R. J. Simpson, M. J. Dalling. 1980. Nitrogen redistribution during grain growth in wheat. Planta 149: 241–251.
Heck, V., E. Martinoia, P. Matile. 1981. Subcellular localization of acid protease in barley mesophyll protoplasts. Planta 151: 198–200.
Ragster, L. E., M. J. Chrispeels. 1981. Autodigestion in crude extracts of soybean leaves and isolated chloroplasts as a measure of proteolytic activity. Plant Physiol. 67: 104–109.
Lin, W., V. A. Wittenbach. 1981. Subcellular localization of proteases in wheat corn mesophyll protoplasts. Plant Physiol. 67: 969–972.
Wagner, G. Isolation of higher plant vacuoles and tonoplast. In Isolation of Membranes and Organelles from Plant Cells (J. L. Hall, A. L. Moore, eds.). Academic Press, London (In press).
Wagner, G. J., H. C. Butcher, H. W. Siegelman. 1978. The plant protoplast. BioScience 28: 95–101.
Wagner, G. J. 1981. Enzymic and protein character of tonoplast from Hippeastrum vacuoles. Plant Physiol. 68: 499–503.
Wiebe, H. H. 1978. The significance of plant vacuoles. BioScience 28: 327–331.
Walter, H., E. Stadelmann. 1968. The physiological prerequisites for the transition of autotrophic plants from water to terrestrial life. BioScience 18: 694–701.
Dainty, J. 1968. The structure and possible function of the vacuole. In Plant Cell Organelles (J. B. Pridham, ed.). Academic Press, New York, pp. 40–46.
Hrazdina, G., G. J. Wagner, H. W. Siegelman. 1978. Subcellular localization of enzymes of anthocyanin biosynthesis in protoplasts. Phytochemistry 17: 53–56.
Schmeltz, I. 1971. Nicotine and other tobacco alkaloids. In Naturally Occurring Insecticides (J. Jacobson, D. G. Crosby, eds.). Dekker, New York, pp. 559–585.
Muller, C. H. 1969. The “co” in coevolution. Science 164: 197–198.
Fraenkel, G. S. 1959. The raison d’etre of secondary plant substances. Science 129: 1466–1470.
Rhoades, D. F., R. G. Cates. 1976. Toward a general theory of plant antiherbivore chemistry. In Biochemical Interaction between Plants and Insects (J. W. Wallace, R. L. Mansell, eds.). Recent Advances in Phytochemistry, Vol. 10. Plenum Press, New York, pp. 168–213.
Bell, A. O. 1981. Biochemical mechanisms of disease resistance. Annu. Rev. Plant Physiol. 32: 21–81.
Berenbaum, M., P. Feeny. 1981. Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race? Science 212: 927–929.
Franceschi, V. R., H. T. Horner. 1980. Calcium oxalate crystals in plants. Bot. Rev. 46: 361–427.
Oaks, A., R. G. S. Bidwell. 1970. Compartmentation of intermediary metabolites. Annu. Rev. Plant Physiol. 21: 43–66.
Osmond, G. B. 1976. Transport in plants. In Encyclopedia of Plant Physiology, New Series. U. Luttge, M. G. Pitman, eds. Vol. 2A Springer-Verlag, Berlin, pp. 347–372.
Kisaki, T., N. E. Tolbert. 1969. Glycolate and glyoxylate metabolism by isolated peroxisomes and chloroplasts. Plant Physiol. 44: 242–250.
Saunders, J. A. 1979. Investigations of vacuoles isolated from tobacco. Plant Physiol. 64: 74–78.
Saunders, J. A., E. E. Conn, C. H. Lin, C. R. Stocking. 1977. Subcellular localization of the cyanogenic glucoside of Sorghum by autoradiography. Plant Physiol. 59: 647–652.
Robinson, T. 1980. The Organic Constituents of Higher Plants. Edit. 4. Cordus Press, P. O. Box 587, North Amherst, MA, pp. 201–205.
Imai, K., K. Furuya. 1951. Study of the phytochemical component of Fagopyrum cymosum Meisn. J. Pharm. Soc. Japan 71: 266–273.
Asen, S., R. N. Stewart, K. H. Norris. 1977. Antho-cyanin and pH involved in the color of ‘heavenly blue’ morning glory. Phytochemistry 16: 1118–1119.
Burch, G. E. 1972. Experiments of nature: whole leaf and purified alkaloids. Am. Heart J. 83: 845–847.
Akahori, A., F. Yasuda, M. Togami, K. Kagawa, T. Okahishi. 1969. Variation in isodiotigenin and diosgenin content in aerial parts of Dioscorea tokoro. Phytochemistry 8: 2213–2217.
Feeny, P. P. 1968. Seasonal changes in the tannin content of oak leaves. Phytochemistry 7: 871–880.
Arnold, G. W., J. J. Hill. 1972. Chemical factors effecting selection of food plants by ruminants. In Phytochemical Ecology (J. Harborne, ed.). Academic Press, London and New York, pp. 71–101.
Fassett, D. W. 1973. Oxalates. In Toxicants Occurring Naturally in Foods, National Academcy of Sciences, 2101 Constitution Ave., N.W., Washington, D.C., pp. 346–362.
Liener, I. E., J. E. Rose. 1953. Soyin, a toxic protein from the soybean III. Immunochemical properties. Proc. Soc. Exp. Biol. Med. 83: 539–547.
Vinson, C. G., F. B. Cross. 1942. Vitamin C contentof persimmon leaves and fruits. Science 96: 430–431.
Fassett, D. W. 1973. Nitrates and Nitrites. In Toxicants Occurring Naturally in Foods, National Academy of Sciences, 2101 Constitution Ave., N. W., Washington, D.C., pp. 7–25.
Allaway, W. H., H. A. Laitinen, H. W. Lakin, O. H. Muth. 1974. Selenium. In Geochemistry and The Environment, Vol. 1. National Academy of Sciences, 2101 Constitution Ave., Washington, D.C., pp. 57–63.
Brooks, R. R., J. Lee, R. D. Reeves. 1976. Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193: 579–580.
Page, A. L., F. T. Bingham, C. Nelson. 1972. Cadmium absorption and growth of various plant species as influenced by solution cadmium concentration. J. Environ. Quality 1: 288–291.
Finlayson, D. G., H. R. MacCarthy. 1973. Pesticide residues in plants. In Environmental Pollution by Pesticides (C. A. Edwards, ed.). Plenum Press, New York, pp. 57–86.
Martinoia, E., U. Heck, A. Wiemken. 1981. Vacuoles as storage compartments for nitrate in barley leaves. Nature 289: 292–294.
Wagner, G. J. 1979. The subcellular site and nature for intracellular cadmium in plants. In Trace Substances in Environmental Health — XIII (D. D. Hemphill, ed.). Univ. of Missouri Press, Columbia, Missouri, pp. 115–123.
Wagner, G. J., H. W. Siegelman. 1975. Large-scale isolation of intact vacuoles and isolation of choloroplasts from mature plant tissues. Science 190: 1298–1299.
Leigh, R. A., D. Branton. 1976. Isolation of vacuoles from root storage tissue of Beta vulgaris L. Plant Physiol. 58: 656–662.
Lorz, H. C., T. Harms, I. Potrykus. 1976. Isolation of “Vacuoplasts” from protoplasts of higher plants. Biochem. Physiol. Pflanzen 169: 617–620.
Leigh, R. A., D. Branton, F. Marty. 1979. Methods of isolation of intact vacuoles and fragments of tono-plast. In Plant Organelles, Methodological Surveys (B) Biochemistry, Vol. 9 (E. Reid, ed.). Ellis Harwood LTD., Publishers, Chichester, West Sussex, England, pp. 69–80.
Ohlrogge, J. B., J. L. Garcia-Martinez, D. Adams, L. Rappaport. 1980. Uptake and subcellular compart-mentation of gibberellin Ax applied to leaves of barley and cowpea. Plant Physiol. 66: 422–427.
Leigh, R. A., T. Rees, W. A. Fuller, J. Banfield. 1979. The location of acid invertase activity and sucrose in the vacuoles of storage of roots of beet root (Beta vulgaris). Biochem. J. 178: 539–547.
Grob, K., P. Matile. 1980. Compartmentation of ascorbic acid in vacuoles of horseradish root cells. Z. Pflanzenphysiol. 98: 235–243.
Buser, C., P. Matile. 1977. Malic acid in vacuoles isolated from Bryophyllum leaf cells. Z. Pflanzenphysiol. 82: 462–466.
Boller, T., H. Kende. 1979. Hydrolytic enzymes in the central vacuole of plant cells. Plant Physiol. 63: 1123–1132.
Taylor, A. R. D., J. L. Hall. 1976. Some physiological properties of protoplasts isolated from maize and tobacco tissues. J. Exp. Bot. 27: 383–391.
Hall, J. L. 1979. Methods for isolation of protoplasts and plasma membranes. In Plant Organelles, Methodological Surveys (B) Biochemistry, Vol. 9 (E. Reid, ed.). Ellis Horwood Ltd. Publisher, Chichester, West Sussex, England, pp. 69–80.
Cocking E. C. Isolation of Plant Protoplasts. In Isolation of Membranes and Organelles from Plant Cells (J. L. Hall, A. L. Moore, eds.). Academic Press, London (In Press).
Wagner, G. J., P. Mulready, J. Cutt. 1981. Vacuole/ extravacuole distribution of soluble protease in Hippeastrum petal and Triticum leaf protoplasts. Plant Physiol. 68: 1081–1089.
Wagner, G. J. 1979. Content and vacuole/extravacuole distribution of neutral sugars, free amino acids and anthocyanin in protoplasts. Plant Physiol. 64: 88–93.
Nishimura, M., H. Beevers. 1978. Hydrolases in vacuoles from castor bean endosperm. Plant Physiol. 62: 44–48.
Wagner, G. J. 1981. Vacuolar deposition of ascorbate-derived oxalic acid in barley. Plant Physiol. 67: 591–593.
Lin, W., G. J. Wagner, H. W. Siegelman, G. Hind. 1977. Membrane-bound ATPase of intact vacuoles and tono-plasts isolated from mature plant tissue. Biochim. Biophys. Acta 465: 110–117.
Saunders, J. A., E. E. Conn. 1978. Presence of the cyanogenic glucoside dhurrin in isolated vacuoles from Sorghum. Plant Physiol. 61: 154–157.
Galun, E. 1981. Plant protoplasts as physiological tools. Annu. Rev. Plant Physiol. 32: 237–266.
Walker-Simmons, M., C. A. Ryan. 1977. Immunologicalidentification of protease inhibitors I and II in isolated tomato leaf vacuoles. Plant Physiol. 60: 61–63.
Beevers, L. 1976. Nitrogen Metabolism in Plants. Arnold Press, London.
Holleman, J. M., J. L. Key. 1967. Inactive and protein precursor pools of amino acids in the soybean hypocotyl. Plant Physiol. 42: 29–36.
Giaquinta, R. 1978. Source of sink leaf metabolism in relation to phloem translocation. Plant Physiol. 61: 380–385.
Outlaw, W. H., D. B. Fisher, A. L. Christy. 1975. Compartmentation in Vica faba leaves. Plant Physiol. 55: 704–711.
Moskowitz, A. H., G. Hrazdina. 1981. Vacuolar contents of fruit subepidermal cells from Vitis species. Plant Physiol. 68: 686–692.
Kenyon, W. H., R. Kringstad, C. C. Black. 1978. Diurnal changes in the malic acid content of vacuoles isolated from leaves of the crassulacean acid metabolism plant, Sedum telephium. FEBS Lett. 94: 281–283.
Reijngoud, D. J., J. M. Tager. 1977. The permeability properties of the lysosomal membrane. Biochim. Biophys. Acta 472: 419–449.
Matile, P. 1975. The Lytic Compartment of Plant Cells. Springer-Verlag, New York, pp. 1–175.
Butcher, H. C., G. J. Wagner, H. W. Siegelman. 1977. Localization of acid hydrolases in protoplasts. Plant Physiol. 59: 1098–1103.
Swain, T. 1976. Nature and properties of flavonoids. In Chemistry and Biochemistry of Plant Pigments (T. W. Goodwin, ed.). Edit. 2, Vol. 1, Academic Press, New York, pp. 425–463.
Conn, E. E. 1973. Biosynthesis of cyanogenic gluco-sides. Biochem. Soc. Symp. 38: 277–302.
Quail, P. H. 1979. Plant cell fractionation. Annu. Rev. Plant Physiol. 30: 425–484.
Saunders, J. A., E. E. Conn, C. H. Lin, M. Shimada. 1977. Localization of cinnamic acid 4-monoxygenase and the membrane-bound enzyme system for dhurrin biosynthesis in Sorghum seedlings. Plant Physiol. 60: 629–634.
Czichi, V., H. Kindl. 1977. Phenylalanine ammonia lyase and cinnamic acid hydroxylases as assembled consecutive enzymes on microsomal membranes of cucumber cotyledons: cooperation and subcellular distribution. Planta 134: 133–143.
McClure, J. W. 1977. The physiology of phenolic compounds in plants. Recent Advan. Phytochem. 12: 525–556.
Stafford, H. A. 1974. Possible multienzyme complexes regulating the formation of Cß-Ca phenolic compounds and lignins in higher plants. Recent Advan. Phytochem. 8: 53–79.
Diers, L., F. Schotz, B. Meyer. 1973. Uber die Ausbildung von Gerbsstoffvakuolen bei Oenothera. Cytobiologie 7: 10–19.
Chafe, S. C., D. J. Durzan. 1973. Tannin inclusions in cell suspension cultures of white spruce. Planta 113: 251–262.
Baur, P. S., C. H. Walkinshaw. 1974. Fine structure of tannin accumulation in callus cultures of Pinus elliotti (slash pine). Can. J. Bot. 52: 615–619.
Ginsberg, C. 1967. The relation of tannins to the differentiation of the root tissues in Reaumuria palastina. Bot. Gaz. 128: 1–10.
Pecket, R. C., C. J. Small. 1980. Occurrence, localization and development of anthocyanoplasts. Phytochemistry 19: 2571–2576.
Haghiri, F. 1973. Cadmium uptake by plants. J. Environ. Qual. 2: 93–96.
Bartlof, M., E. Brennan, C. A. Price. 1980. Partial characterization of cadmium-binding protein from the roots of cadmium-treated tomato. Plant Physiol. 66: 438–441.
Weigel, H. J., H. J. Jager. 1980. Subcellular distribution and chemical form of cadmium in bean plants. Plant Physiol. 65: 480–482.
Wagner, G. J., M. M. Trotter. Inducible cadmium binding complexes of cabbage and tobacco. Plant Physiol. (In Press).
Cherian, M. G. 1979. Metabolism and potential toxic effects of metallothionein. In Metallothionein (J. H. R. Kagi, M. Nordberg, eds.). Birkhauser Verlag, Basel, Boston, Stuttgart, pp. 337–345.
Smith, F. A., J. A. Raven. 1979. Intracellular pH and its regulation. Annu. Rev. Plant Physiol. 30: 289–311.
Kurkdjian, À., J. Guern. 1978. Intracellular pH in higher plant cells. Plant Sci. Lett. 11: 337–344.
Drawert, H. 1955. Der pH-Wert des Zellsaftes. In Encyclopedia of Plant Physiology (W. Ruhland, ed.). Springer-Verlag, Berlin, Vol. 1, pp. 627–639.
Wagner, G. J., P. Mulready. 1981. Solubilization and characterization of tonoplasts ATPase. Plant Physiol. Supp. 67: 8.
Leigh, R. A., R. R. Walker. 1980. ATPase and acid phosphatase activities associated with vacuoles isolated from storage roots of red beet (Beta vulgaris L.). Planta 150: 222–229.
Walker, R. R., R. A. Leigh. 1981. Characterization of a salt-stimulated ATPase activity associated with vacuoles isolated from storage roots of red beet (Beta vulgaris L.). Planta (In Press).
d’Auzac, J. 1975. Characterisation d’une ATPase membranaire en presence d’une phosphatase acide dans les lutoides du latex d’Hevea brasiliensis. Phytochemistry 14: 671–675.
d’Auzac, J. 1977. ATPase membranaire de vacuoles lysosomales: les lutoides du latex d1 Hevea brasiliensis. Phytochemistry 16: 1881–1885.
Lin, W., G. J. Wagner, G. Hind. 1977. The proton pump and membrane potential of vacuoles isolated from Tulipa petals. Plant Physiol. Supp. 59: 85.
Marin, B., M. Marin-Lanza, E. Komor. 1981. The proton motive potential difference across the vacuo-lysosornai membrane of Hevea brasiliensis (rubber tree) and its modification by a membrane-bound adenosine triphosphatase. Biochem. J. 98: 365–372.
d’Auzac, J., C. Lioret. 1974. Mise en evidence d’un mecanisme d’accumulation du citrate dans les lutoides du latex d’Hevea brasiliensis. Physiol. Veg. 12: 617–635.
Guy, M., L. Reinhold, D. Michaeli. 1979. Direct evidence for a sugar transport mechanism in isolated vacuoles. Plant Physiol. 64: 61–64.
Doll, S., F. Rodier, J. Willenbrink. 1979. Accumulation of sucrose in vacuoles isolated from red beet tissue. Planta 144: 407–411.
Willenbrink, J., S. Doll. 1979. Characteristics of the sucrose uptake system of vacuoles isolated from red beet tissue. Planta 147: 159–162.
Doll, S., R. Hauer. 1981. Determination of the membrane potential of vacuoles isolated from red beet storage tissue. Planta 152: 153–158.
Briskin, D. P., R. T. Leonard. 1980. Isolation of tonoplast vesicles from tobacco protoplasts. Plant Physiol. 66: 684–687.
Rosen, B. P., E. R. Kashket. 1978. Energetics of active transport. In Bacterial Transport (B. P. Rosen, ed.). Chap. 12, Marcel Dekker, Inc., New York. pp. 559–620.
Hays, J. B. 1978. Group translocation transport systems. In Bacterial Transport (B. P. Rosen, ed.). Chap. 2, Marcel Dekker, Inc., New York. pp. 43–102.
Goto, K., H. Kirata, Y. Kagawa. 1980. A stable Na /H antiporter of thermophylic bacterium PS3. J. Bioenerget. Biomembran. 12: 297–308.
Mertz, S. M., N. Higinbotham. 1976. Transmembrane electropotential in barley roots as related to cell type, cell location, and cutting and aging effects. Plant Physiol. 57: 123–128,
Goldsmith, M. H. M., R. E. Clealand. 1978. The contribution of tonoplast and plasmamembrane to the electrical properties of higher plant cells. Planta 143: 261–265.
Saftner, R. A., R. E. Wyse. 1980. Alkali cation/sucrose cotransport in the root sink of sugar beet. Plant Physiol. 66: 884–889.
Luttge, U., E. Ball. 1979. Electrochemical investigation of active malic acid transport at the tonoplast into the vacuoles of the CAM plant Kalanchoe daigremontiana. J. Membrane Biol. 47: 401–422.
Boller, T., M. Durr, A. Wiemken. 1975. Characterization of a specific transport system for arginine in isolated yeast vacuoles. Eur. J. Biochem. 54: 81–91.
Ohsumi, Y., Y. Anraku. 1981. Active transport of basic amino acids driven by a proton motive force in vacuolar membrane vesciles of Saccharomyces cerevisiae. J. Biol. Chem. 256: 2079–2082.
Kakinuma, Y., Y. Ohsumi, Y. Anraku. 1981. Properties of H translocating adenosine triphosphatase in vacuolar membranes of Saccharomyces cerevisiae. J. Biol. Chem. 256: 10859–10863.
Blobel, G., B. Dobberstein. 1975. Transfer of proteins across membranes. J. Cell. Biol. 67:852–862.
Blobel, G. 1980. Intracellular protein topogenesis. Proc. Natl. Acad. Sci. USA 77: 1496–1500.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1982 Springer Science+Business Media New York
About this chapter
Cite this chapter
Wagner, G.J. (1982). Compartmentation in Plant Cells: The Role of the Vacuole. In: Creasy, L.L., Hrazdina, G. (eds) Cellular and Subcellular Localization in Plant Metabolism. Recent Advances in Phytochemistry, vol 16. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-4727-0_1
Download citation
DOI: https://doi.org/10.1007/978-1-4757-4727-0_1
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4757-4729-4
Online ISBN: 978-1-4757-4727-0
eBook Packages: Springer Book Archive