Abstract
Aluminium (Al) stimulates the efflux of malate from the apices of wheat (Triticum aestivum L.) roots (Delhaize et al. 1993, Plant Physiol. 103, 695–702). The response was five to tenfold higher in Al-tolerant seedlings than Al-sensitive seedlings and the capacity for Al-stimulated malate efflux was found to co-segregate with Al tolerance in a pair of near-isogenic wheat lines differing in Al-tolerance at a single dominant locus. We have investigated this response further using excised root apices. Half-maximal efflux of malate from apices of Al-tolerant seedlings was measured with 30 μM Al in 0.2 mM CaCl2, pH 4.2, while saturating rates of 2.0 nmol·apex−1·h−1 occurred with concentrations above 100 μM Al. The stimulation of malate efflux by Al was accompanied by an increase in K+ efflux which appeared to account for electroneutrality. The greater stimulation of malate efflux from Al-tolerant apices compared to Al-sensitive apices could not be explained by differences in the activities of phosphoenolpyruvate carboxylase or NAD-malate dehydrogenase. Several other polyvalent cations, including gallium, indium and the tridecamer Al13, failed to elicit malate efflux. Aluminium-stimulated efflux of malate was correlated with the measured concentration of total monomeric Al present, and with the predicted concentrations of Al3+ and AlOH2+ ions in the solution. Several antagonists of anion channels inhibited Al-stimulated efflux of malate with the following order of effectiveness: niflumic acid≈NPPB>IAA-94≈A-9-C>ethacrynic acid. Lanthanum, chlorate, perchlorate, zinc and α-cyano-4-hydroxycinnamic acid inhibited malate release by less than 30% at 100 μM while 4,4′-diisothiocyanatostilbene-2,2′-disulphonate (DIDS) had no effect. These results suggest that the Al3+ cation stimulates malate efflux via anion channels in apical cells of Al-tolerant wheat roots.
Similar content being viewed by others
Abbreviations
- A-9-C:
-
anthracene-9-carboxylic acid
- DIDS:
-
4,4′-diisothiocyanatostilbene-2,2′-disulphonate
- ET3, ET8, ES3, and ES8:
-
Al-tolerant and Al-sensitive lines of wheat
- IAA-94:
-
[6, 7-dichloro-2-cyclopentyl-2, 3-dihydro-2-methyl-oxo-1H-inden-5-yloxy] acetic acid
- NPPB:
-
5-nitro-2-(3-phenylpropylamino)-benzoic acid
References
Arata, H., Iwasaki, I., Kusumi, K., Nishimura, M. (1992) Thermodynamics of malate transport across the tonoplast of leaf cells of CAM plants. Plant Cell Physiol. 33, 873–880
Brown, P.L. (1989) The hydrolysis of metal ions. Part 11. The ionic strength dependence of gallium (III). J. Chem. Soc. Dalton Trans. 399–402
Cerana, R., Giromini, L., Colombo, R. (1994) Malate-regulated channels permeable to anions in vacuoles of Arabidopsis thaliana Aust. J. Plant Physiol., in press
Coleman, H.A. (1986) Chloride currents in Chara — A patch-clamp study. J. Membr. Biol. 83, 109–118
Delhaize, E., Craig, S., Beaton, C.D., Bennet, R.J., Jagadish, V.C., Randall, P.J. (1993a) Aluminum tolerance in wheat (Triticum aestivum L.) I. Uptake and distribution of aluminum in root apices. Plant Physiol. 103, 685–693
Delhaize, E., Ryan, P.R., Randall, P.J. (1993b) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol. 103, 695–702
Foy, C.D., Chaney, R.L., White, M.C. (1978) The physiology of metal toxicity in plants. Annu. Rev. Plant Physiol. 29, 511–566
Hatch, M.D., Oliver, I.R. (1978) Activation and inactivation of phosphoenolpyruvate carboxylase in leaf extracts of C4 species. Aust. J. Plant Physiol. 5, 571–580
Haug, A. Shi, B., Vitorello, V. (1994) Aluminum interaction with phosphoinositide-associated signal transduction. Arch. Toxicol. 68, 1–7
Hedrich, R., Busch, H., Raschke, K. (1990) Ca2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells. EMBO J. 9, 3889–3892
Kerven, G.L., Edwards, D.G., Asher, C.J., Hallman, P.S., Kokot, S. (1989) Aluminium determination in soil solution. II. Short-term colorimetric procedures for the measurement of inorganic monomeric aluminium in the presence of organic acid ligands. Aust. J. Soil Res. 27, 91–102
Kinraide, T.B., Ryan, P.R., Kochian, L.V. (1992) Interactive effects of Al3+, H+ and other ca on root elongation considered in terms of cell-surface electrical potential. Plant Physiol. 99, 1461–1468
Landry, D.W., Reitman, M., Cragoe, JR., E.J., Al-Awqati, Q. (1987) Epithelial chloride channel: Development of inhibitory ligands. J. Gen. Physiol. 90, 779–798
Lüttge, U., Smith, J.A.C. (1984) Mechanism of passive malic-acid efflux from vacuoles of the CAM plant Kalanchoë daigremontiana. J. Memb. Biol. 81, 149–158
Macnicol, P.K., Jacobsen, J.V. (1992) Endosperm acidification and related metabolic changes in the developing barley grain. Plant Physiol. 98, 1098–1104
Miyasaka, S.C., Kochian, L.V., Shaff, J.E., Foy, C.D. (1989) Mechanisms of aluminum tolerance in wheat: An investigation of genotypic differences in rhizosphere pH, K+ and H+ transport, and root-cell membrane potentials. Plant Physiol. 91, 1188–1196
Osmond, C.B., Laties, G.G. (1969) Compartmentation of malate in relation to ion absorption in beet. Plant Physiol. 44, 7–14
Pantoja, O., Gelli, A., Blumwald, E. (1992) Characterization of vacuolar malate and K+ channels under physiological conditions. Plant Physiol. 100, 1137–1141
Parker, D.R., Bertsch, P.M. (1992) Formation of the “Al13” tridecamer under diverse synthesis conditions. Environ. Sci. Technol. 26, 914–921
Plant, P.J., Gelli, A., Blumwald, E. (1994) Vacuolar chloride regulation of an anion selective tonoplast channel. J. Memb. Biol. 140, 1–12.
Rincón, M., Gonzales, R.A. (1992) Aluminum partitioning in intact roots of aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars. Plant Physiol. 99, 1021–1028
Ryan, P.R., Shaff, J.E., Kochian, L.V. (1992) Aluminum toxicity in roots: Correlation among ionic currents, ion fluxes and root elongation in aluminum-sensitive and aluminum-tolerant wheat cultivars. Plant Physiol. 99, 1193–1200
Ryan, P.R., DiTomaso, J.M., Kochian, L.V. (1993) Aluminium toxicity in roots: An investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44, 437–446
Schauf, C.L., Wilson, K.J. (1987) Properties of single K+ and Cl− channels in Asclepias tuberosa protoplasts. Plant Physiol. 85, 413–418
Schroeder, J.I., Keller, B.U. (1992) Two types of anion channel currents in guard cells with distinct voltage regulation. Proc. Natl. Acad. Sci. USA 89, 5025–5029
Skerrett, M., Tyerman, S.D. (1994) A channel that allows inwardly directed fluxes of anions in protoplasts derived from wheat roots. Planta 192, 295–305
Taylor, G.J. (1988) The physiology of aluminum phytotoxicity. In: Metal ions in biological systems. Aluminum and its role in biology, vol. 24, pp. 123–163, Sigel, H., ed. Marcel Dekker, New York
Terry, B.R., Tyerman, S.D., Findlay, G.P. (1991) Ion channels in the plasma membrane of Amaranthus protoplasts: one cation and one anion channel dominate the conductance. J. Membr. Biol. 121, 223–236
Tester, M. (1990) Plant ion channels: whole-cell and single-channel studies. New Phytol. 114, 305–340
Tice, K.R., Parker, D.R., DeMason, D.A. (1992) Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. Plant Physiol. 100, 309–318
Tyerman, S.D. (1992) Anion channels in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 351–373
Tyerman, S.D., Findlay, G.P., Patterson, G.J. (1986) Inward membrane current in Chara inflata: I. A voltage- and time dependent Cl-component. J. Membr. Biol. 89, 139–152
Wheeler, D.M., Power, I.L., Edmeades, D.C. (1993) Effect of various metal ions on growth of two wheat lines known to differ in aluminium tolerance. In: Plant nutrition — from genetic engineering to field practice. pp. 723–726, Barrow, N.J., ed. Kluwer Academic Publishers Dordrecht, Boston, Lancaster
White, P.J., Smith, J.A.C. (1989) Proton and anion transport at the tonoplast in crassulacean- acid-metabolism plants: specificity of the malate-influx system in Kalanchoë daigremontiana Planta 179, 265–274
Author information
Authors and Affiliations
Corresponding author
Additional information
The authors are grateful to Dr. David Parker (Soil and Environmental Science Department, University of California, USA) and Dr. Andrew Noble (Plant Industry, CSIRO, Canberra, Australia) for assistance in preparing the Al13 solution and to Dr. Andrew Noble for performing the pyrocatechol-violet measurements. The computer program used for estimating the speciation of Al in solution was provided by Dr. Thomas Kinraide (USDA-ARS Research Laboratory, Beckley, W. Va, USA) and salts of scandium, gallium and indium were supplied by Dr. John Thompson (Research School of Chemistry, Australian National University, Canberra, Australia). The authors are especially grateful to Dr. D.W. Landry (Columbia University, N.Y., USA) for providing samples of IAA 94 and to Dr. Stephan Tyerman (School of Biological Sciences, The Flinders University of South Australia, Adelaide) for comments on the manuscript. Technical support was provided by Kirsty McAlister.
Rights and permissions
About this article
Cite this article
Ryan, P.R., Delhaize, E. & Randall, P.J. Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103–110 (1995). https://doi.org/10.1007/BF00193223
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00193223