Proton and anion transport at the tonoplast in crassulacean-acid-metabolism plants: specificity of the malate-influx system in Kalanchoë daigremontiana

Planta - Tập 179 - Trang 265-274 - 1989
Philip J. White1, J. Andrew C. Smith1
1Department of Botany, University of Edinburgh, Edinburgh, UK

Tóm tắt

Tonoplast vesicles were prepared from leaf mesophyll homogenates of the crassulacean-acid-metabolism plant Kalanchoë daigremontiana Hamet et Perrier de la Bâthie to study the effects of anions on ATP- and inorganic-pyrophosphate (PPi)-dependent H+ transport. In the presence of gramicidin, substrate hydrolysis by the tonoplast ATPase was characteristically stimulated by chloride and inhibited by nitrate, but was unaffected by malate and a wide range of other organic-acid anions; the PPiase was anion-insensitive. Malate was more effective than chloride both in stimulating ATP- and PPi-dependent vesicle acidification (measured as quinacrine-fluorescence quenching) and in dissipating a pre-existing inside-positive membrane potential (measured as oxonol-V-fluorescence quenching), indicating that malate was more readily transported across the tonoplast. Certain other four-carbon dicarboxylates also supported high rates of vesicle acidification, their order of effectiveness being fumarate ≫ malate ∼-succinate > oxalacetate ∼- tartrate; the five-carbon dicarboxylates 2-oxoglutarate and glutarate were also transported, although at lower rates. Experiments with non-naturally occurring anions indicated that the malate transporter was not stereospecific, but that it required the trans-carboxyl configuration for transport. Shorter-chain or longer-chain dicarboxylates were not transported, and neither were monocarboxylates, the amino-acid anions aspartate and glutamate, nor the tricarboxylate isocitrate. The non-permeant anions maleate and tartronate appeared to be competitive inhibitors of malate transport but did not affect chloride transport, indicating that malate and chloride influx at the tonoplast might be mediated by separate transporters.

Tài liệu tham khảo

Aoki, K., Nishida, K. (1984) ATPase activity associated with vacuoles and tonoplast vesicles isolated from the CAM plant, Kalanchoë daigremontiana. Physiol. Plant. 60, 21–25 Balsamo, R.A., Uribe, E.G. (1988) Plasmalemma- and tonoplast-ATPase activity in mesophyll protoplasts, vacuoles and microsomes of the Crassulacean-acid-metabolism plant Kalanchoë daigremontiana. Planta 173, 190–196 Bennett, A.B., Spanswick, R.M. (1983) Optical measurements of Δ pH and Δψ in corn root membrane vesicles: kinetic analysis of Cl- effects on a proton-translocating ATPase. J. Membr. Biol. 71, 95–107 Bradford, M.M., (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 72, 248–254 Bremberger, C., Haschke, H.-P., Lüttge, U. (1988) Separation and purification of the tonoplast ATPase and pyrophosphatase from plants with constitutive and inducible Crassulacean acid metabolism. Planta 175, 465–470 Buser-Suter, C., Wiemken, A., Matile, P. (1982) A malic acid permease in isolated vacuoles of a Crassulacean Acid Metabolism plant. Plant Physiol. 69, 456–459 Chanson, A., Fichmann, J., Spear, D., Taiz, L. (1985) Pyrophosphate-driven proton transport by microsomal membranes of corn coleoptiles. Plant Physiol. 79, 159–164 Churchill, K.A., Sze, H. (1983) Anion-sensitive, H+-pumping ATPase of oat roots. Direct effects of Cl-, NO3 -, and a disulfonic stilbene. Plant Physiol. 76, 490–497 Giannini, J.L., Briskin, D.P. (1987) Proton transport in plasma membrane and tonoplast vesicles from red beet (Beta vulgaris L.) storage tissue. A comparative study of ion effects on Δ pH and Δψ. Plant Physiol. 84, 613–618 Griffith, C.J., Rea, P.A., Blumwald, E., Poole, R.J. (1986) Mechanism of stimulation and inhibition of tonoplast H+-ATPase of Beta vulgaris by chloride and nitrate. Plant Physiol. 81, 120–125 Guern, J., Mathieu, Y., Kurkdjian, A., Manigault, P., Manigault, J., Gillet, B., Beloeil, J.-C., Lallemand, J.-Y. (1989) Regulation of vacuolar pH of plant cells. II. A 31P NMR study of the modifications of vacuolar pH in isolated vacuoles induced by proton pumping and cation/H+ exchanges. Plant Physiol. 89, 27–36 Guern, J., Renaudin, J.-P., Barbier-Brygoo, H. (1987) Accumulation of organic solutes in plant vacuoles: the interpretation of data is not so easy. In: Plant vacuoles: their importance in solute compartmentation in cells and their applications in plant biotechnology, pp. 305–314, Marin, B., ed. Plenum Press, New York Hager, A., Berthold, W., Biber, W., Edel, H.-G., Lanz, C., Schiebel, G. (1986) Primary and secondary energized ion translocating systems on membranes of plant cells. Ber. Deutsch. Bot. Ges. 99, 281–295 Hager, A., Biber, W. (1984) Functional and regulatory properties of H+ pumps at the tonoplast and plasma membranes of Zea mays coleoptiles. Z. Naturforsch. 39c, 927–937 Haschke, H.-P., Grötsch, S., Lüttge, U. (1988) Proton transporting enzymes at the tonoplast of leaf cells of the CAM plant Kalanchoë daigremontiana. III. Regulation of the ATPase. J. Plant Physiol. 132, 604–607 Hedrich, R., Schroeder, J.I. (1989) The physiology of ion channels and electrogenic pumps in higher plants. Annu. Rev. Plant Physiol. 40, 539–563 Heldt, H.W., Flügge, U.I. (1987) Subcellular transport of metabolites in a plant cell. In: The biochemistry of plants. A comprehensive treatise, vol. 12: Physiology of metabolism, pp. 49–85, Davies, D.D., ed. Academic Press, New York Jochem, P., Lüttge, U. (1987) Proton transporting enzymes at the tonoplast of leaf cells of the CAM plant Kalanchoë daigremontiana. I. The ATPase. J. Plant Physiol. 129, 251–268 Jochem, P., Rona, J.-P., Smith, J.A.C., Lüttge, U. (1984) Anion-sensitive ATPase activity and proton transport in isolated vacuoles of species of the CAM genus Kalanchoë. Physiol. Plant. 62, 410–415 Kaestner, K.H., Sze, H. (1987) Potential-dependent anion transport in tonoplast vesicles from oat roots. Plant Physiol. 83, 483–489 Kay, W.W., Sweet, G.D., Widenhorn, K., Somers, J.M. (1987) Transport of organic acids in prokaryotes. In: Ion transport in prokaryotes, pp. 269–302, Rosen, B.P., Silver, S., eds. Academic Press, London LaNoue, K.F., Schoolwerth, A.C. (1979), Metabolite transport in mitochondria. Annu. Rev. Biochem. 48, 871–922 Lew, R.R., Spanswick, R.M. (1985) Characterization of anion effects on the nitrate-sensitive ATP-dependent proton pumping activity of soybean (Glycine max L.) seedling root microsomes. Plant Physiol. 77, 352–357 Lüttge, U. (1987) Carbon dioxide and water demand: Crassulacean acid metabolism (CAM), a versatile ecological adaptation exemplifying the need for integration in ecophysiological work. New Phytol. 106, 593–629 Lüttge, U., Smith, J.A.C. (1988) CAM plants. In: Solute transport in plant cells and tissues, pp. 417–452, Baker, D.A., Hall, J.L., eds. Longman Scientific, Harlow, UK Marigo, G., Bouyssou, H., Laborie, D. (1988) Evidence for a malate transport into vacuoles isolated from Catharanthus roseus cells. Bot. Acta. 101, 187–191 Marin, B. (ed.) (1987) Plant vacuoles: their importance in solute compartmentation in cells and their applications in plant biotechnology Plenum Press, New York Marquardt, G., Lüttge, U. (1987) Proton transporting enzymes at the tonoplast of leaf cells of the CAM plant Kalanchoë daigremontiana. II. The pyrophosphatase. J. Plant Physiol. 129, 269–286 Martell, A.E., Smith, R.M. (1977) Critical stability constants. Vol. 3: Other organic ligands. Plenum Press, New York Martinoia, E., Flügge, U.I., Kaiser, G., Heber, U., Heldt, H.-W. (1985) Energy-dependent uptake of malate into vacuoles isolated from barley mesophyll protoplasts. Biochim. Biophys. Acta 806, 311–319 Martinoia, E., Schramm, M.J., Kaiser, G., Kaiser, W.M., Heber, U. (1986) Transport of anions in isolated barley vacuoles. I. Permeability to anions and evidence for a Cl--uptake system. Plant Physiol. 80, 895–901 Mellman, I., Fuchs, R., Helenius, A. (1986) Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55, 663–700 Mettler, I.J., Mandala, S., Taiz, L. (1982) Characterization of in vitro proton pumping by microsomal vesicles isolated from corn coleoptiles. Plant Physiol. 70, 1738–1742 Nishida, K., Tominaga, O. (1987) Energy-dependent uptake of malate into vacuoles isolated from CAM plant, Kalanchoë daigremontiana. J. Plant Physiol. 127, 385–393 Poole, R.J. (1988) Plasma membrane and tonoplast. In: Solute transport in plant cells and tissues, pp. 83–105. Baker, D.A., Hall, J.L., eds. Longman Scientific, Harlow, UK Pope, A.J., Leigh, R.A. (1987) Some characteristics of anion transport at the tonoplast of oat roots, determined from the effects of anions on pyrophosphate-dependent proton transport. Planta 172, 91–100 Pope, A.J., Leigh, R.A. (1988) The use of a chloride-sensitive fluorescent probe to measure chloride transport in isolated tonoplast vesicles. Planta 176, 451–460 Rea, P.A., Poole, R.J. (1985) Proton-translocating inorganic pyrophosphatase in red beet (Beta vulgaris L.) tonoplast vesicles. Plant Physiol. 77, 46–52 Rea, P.A., Sanders, D. (1987) Tonoplast energization: two H+ pumps, one membrane. Physiol. Plant. 71, 131–141 Rona, J.-P., Pitman, M.G., Lüttge, U., Ball, E. (1980) Electrochemical data on compartmentation into cell wall, cytoplasm and vacuole of leaf cells in the CAM genus Kalanchoë. J. Membr. Biol. 57, 25–35 Scherman, D., Henry, J.P. (1980) Oxonol-V as a probe of chromaffin granule membrane potentials. Biochim. Biophys. Acta 599, 150–166 Schumaker, K.S., Sze, H. (1987) Decrease of pH gradients in tonoplast vesicles by NO -3 and Cl-: evidence for H+-coupled anion transport. Plant Physiol. 83, 490–496 Smith, J.A.C. (1987) Vacuolar accumulation of organic acids and their anions in CAM plants. In: Plant vacuoles: their importance in solute compartmentation in cells and their applications in plant biotechnology, pp. 79–87, Marin, B., ed. Plenum Press, New York Smith, J.A.C., Uribe, E.G., Ball, E., Heuer, S., Lüttge, U. (1984a) Characterization of the vacuolar ATPase activity of the crassulacean-acid-metabolism plant Kalanchoë daigremontiana. Eur. J. Biochem. 141, 415–420 Smith, J.A.C., Uribe, E.G., Ball, E., Lüttge, U. (1984b) ATPase activity associated with isolated vacuoles of the crassulacean acid metabolism plant Kalanchoë daigremontiana. Planta 162, 299–304 Struve, I., Lüttge, U. (1987) Characteristics of MgATP2--dependent electrogenic proton transport in tonoplast vesicles of the facultative crassulacean-acid-metabolism plant Mesembryanthemum crystallinum L. Planta 170, 111–120 Sze, H. (1985) H+-translocating ATPases: advances using membrane vesicles. Annu. Rev. Plant Physiol. 36, 175–208 Udvardi, M.K., Price, G.D., Gresshof, P.M., Day, D.A. (1988) A dicarboxylate transporter on the peribacterial membrane of soybean nodules. FEBS Lett. 231, 36–40 Van Dyke, R.W. (1988) Proton pump-generated electrochemical gradients in rat liver multivesicular bodies. Quantitation and effects of chloride. J. Biol. Chem. 263, 2603–2611 Walker, R.R., Leigh, R.A. (1981a) Characterisation of a saltstimulated ATPase activity associated with vacuoles isolated from storage roots of red beet (Beta vulgaris L.). Planta 153, 140–149 Walker, R.R., Leigh, R.A. (1981b) Mg2+-dependent, cationstimulated inorganic pyrophosphatase associated with vacuoles isolated from storage roots of red beet (Beta vulgaris L.). Planta 153, 150–155 Walmsley, A.R., Lowe, A.G. (1986) Multifit — A flexible nonlinear regression program in BASIC. Comput. Methods Programs Biomed. 21, 113–118 Wang, Y., Leigh, R.A., Kaestner, K.H., Sze, H. (1986) Electrogenic H+-pumping pyrophosphatase in tonoplast vesicles of oat roots. Plant Physiol. 81, 497–502 Woo, K.C., Flügge, U.I., Heldt, H.W. (1987) A two-translocator model for the transport of 2-oxoglutarate and glutamate in chloroplasts during ammonia assimilation in the light. Plant Physiol. 84, 624–632 Zoglowek, C., Krömer, S., Heldt, H.W. (1988) Oxaloacetate and malate transport by plant mitochondria. Plant Physiol. 87, 109–115