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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Effect of aluminium on membrane potential and ion fluxes at the apices of wheat roots

Tim Wherrett A , Peter R. Ryan B , Emmanuel Delhaize B and Sergey Shabala A C
+ Author Affiliations
- Author Affiliations

A School of Agricultural Science, University of Tasmania, Private Bag 54, Hobart, Tas. 7001, Australia.

B CSIRO Plant Industry, PO Box 1600, Canberra, ACT 2601, Australia.

C Corresponding author. Email: Sergey.Shabala@utas.edu.au

Functional Plant Biology 32(3) 199-208 https://doi.org/10.1071/FP04210
Submitted: 12 November 2004  Accepted: 16 February 2005   Published: 5 April 2005

Abstract

Aluminium (Al) tolerance in wheat (Triticum aestivum L.) is associated with the Al-activated efflux of malate and K+ from the root apices. We tested the hypothesis that these Al-activated ion fluxes would induce changes in the membrane potential (Vm) and that these responses would differ between wheat genotypes that differ in Al tolerance. Within minutes of exposing wheat roots to 50 μm AlCl3, a significant depolarisation was measured in the Al-tolerant ET8 genotype but not in a near-isogenic, Al-sensitive genotype, ES8. We investigated the ion movements that may be responsible for these changes in Vm by measuring real-time fluxes of Cl, H+ and K+ at the root apices of wheat seedlings using the non-invasive microelectrode ion flux estimation (MIFE) technique. Addition of 50 μm AlCl3 to the bathing solution stimulated an increase in K+ efflux and H+ influx in ET8 but not in ES8. The differences between the genotypes were sustained for 24 h and were observed only at the elongating zone and not the meristematic zone. After 24 h Al increased Cl influx in ET8 but inhibited ES8 influx in a dose-dependent manner. These results provide new temporal and spatial information on the Al-activated ion fluxes from intact wheat plants.

Keywords: charge balance, ion channels, malate, Triticum aestivum.


Acknowledgments

This work was supported by ARC and GRDC grants to Dr S. Shabala. T. Wherrett is a recipient of the University of Tasmania Cuthbertson Scholarship.


References


Ahn SJ, Sivaguru M, Chung GC, Rengel Z, Matsumoto H (2002) Aluminium-induced growth inhibition is associated with impaired efflux and influx of H+ across the plasma membrane in root apices of squash (Cucurbita pepo). Journal of Experimental Botany 53, 1959–1966.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chen J, Sucoff EI, Stadelmann EJ (1991) Aluminum and temperature alteration of cell membrane permeability of Quercus rubra. Plant Physiology 96, 644–649. open url image1

Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiology 107, 315–321.
PubMed |
open url image1

Delhaize E, Craig S, Beaton CD, Bennet RJ, Jagadish VC, Randall PJ (1993a) Aluminum tolerance in wheat (Triticum aestivum L). 1. Uptake and distribution of aluminum in root apices. Plant Physiology 103, 685–693.
PubMed |
open url image1

Delhaize E, Ryan PR, Randall PJ (1993b) Aluminum tolerance in wheat (Triticum aestivum L). 2. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiology 103, 695–702.
PubMed |
open url image1

Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proceedings of the National Academy of Sciences USA 101, 15249–15254.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ding JP, Badot PM, Pickard BG (1993) Aluminium and hydrogen ions inhibit a mechanosensory calcium-selective cation channel. Australian Journal of Plant Physiology 20, 771–778.
PubMed |
open url image1

Gassmann W, Schroeder JI (1994) Inward-rectifying K+ channels in root hairs of wheat. A mechanism for aluminum-sensitive low-affinity K+ uptake and membrane-potential control. Plant Physiology 105, 1399–1408.
PubMed |
open url image1

Horst WJ (1995) The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Zeitschrift für Pflanzenernährung Bodenkunde 158, 419–428. open url image1

Kataoka T, Stekelenburg A, Nakanishi TM, Delhaize E, Ryan PR (2002) Several lanthanides activate malate efflux from roots of aluminium-tolerant wheat. Plant, Cell and Environment 25, 453–460.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kinraide TB (1988) Proton extrusion by wheat roots exhibiting severe aluminum toxicity symptoms. Plant Physiology 88, 418–423. open url image1

Kinraide TB (1993) Aluminium enhancement of plant growth in acid rooting media. A case of reciprocal alleviation of toxicity by two toxic cations. Physiologia Plantarum 88, 619–625.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kinraide TB (2001) Ion fluxes considered in terms of membrane-surface electrical potentials. Australian Journal of Plant Physiology 28, 605–616. open url image1

Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Physiology 46, 237–260.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kochian LV, Shaff JE, Ryan PR (1991) Microelectrode-based investigations into the relationship between Al toxicity and root-cell membrane transport processes. Current Topics in Plant Biochemistry and Physiology 10, 117–133. open url image1

Lindberg S, Strid H (1997) Aluminium induces rapid changes in the cytosolic pH and free calcium and potassium concentrations in root protoplasts of wheat (Triticum aestivum). Physiologia Plantarum 99, 405–414.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lindberg S, Szynkier K, Greger M (1991) Aluminium effects on transmembrane potential in cells of fibrous roots of sugar beet. Physiologia Plantarum 83, 54–62.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6, 273–278.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Marschner, H (1995). ‘Mineral nutrition of higher plants.’ 2nd edn . (Academic Press: London)

Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. International Review of Cytology 200, 1–46.
Crossref | PubMed |
open url image1

Miller AL, Gow NAR (1989) Correlation between profile of ion current circulation and root development. Physiologia Plantarum 75, 102–108. open url image1

Miyasaka SC, Kochian LV, Shaff JE, Foy CD (1989) Mechanisms of aluminium tolerance in wheat: an investigation of genotypic differences in rhizosphere pH, K+, and H+ transport, and root-cell membrane potentials. Plant Physiology 91, 1188–1196. open url image1

Miyasaka SC, Buta JG, Howell RK, Foy CD (1991) Mechanism of aluminium tolerance in snapbeans: root exudation of citric acid. Plant Physiology 96, 737–743. open url image1

Newman IA, Kochian LV, Grusak MA, Lucas WJ (1987) Fluxes of H+ and K+ in corn roots. Characterisation and stoichiometries using ion-selective microelectrodes. Plant Physiology 84, 1177–1184. open url image1

Olivetti GP, Cumming JR, Etherton B (1995) Membrane-potential depolarization of root cap cells precedes aluminum tolerance in snapbean. Plant Physiology 109, 123–129. open url image1

Osawa H, Matsumoto H (2002) Aluminium triggers malate-independent potassium release via ion channels from the root apex in wheat. Planta 215, 405–412.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Papernik LA, Kochian LV (1997) Possible involvement of Al-induced electrical signals in Al tolerance in wheat. Plant Physiology 115, 657–667.
PubMed |
open url image1

Pavlovkin J, Mistrik I (1999) Phytotoxic effect of aluminium on maize root membranes. Biologia 54, 473–479. open url image1

Piñeros M, Tester M (1993) Plasma-membrane Ca2+ channels in roots of higher-plants and their role in aluminum toxicity. Plant and Soil 156, 119–122.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reid RJ, Walker NA (1984) The energetics of Cl– active transport in Chara. Journal of Membrane Biology 78, 157–162. open url image1

Ryan PR, Newman IA, Shields B (1990) Ion fluxes in corn roots measured by microelectrodes with ion-specific liquid membranes. Journal of Membrane Science 53, 59–67.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ryan PR, Shaff JE, Kochian LV (1992) Aluminium toxicity in roots: correlation among ionic currents, ion fluxes, and root elongation in aluminum-sensitive and aluminium-tolerant wheat cultivars. Plant Physiology 99, 1193–1200. open url image1

Ryan PR, Delhaize E, Randall PJ (1995a) Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Australian Journal of Plant Physiology 22, 531–536. open url image1

Ryan PR, Delhaize E, Randall PJ (1995b) Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103–110.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman SD (1997) Aluminum activates an anion channel in the apical cells of wheat roots. Proceedings of the National Academy of Sciences USA 94, 6547–6552.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527–560.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sanders D (1980) The mechanism of Cl– transport at the plasma membrane of Chara corallina. I. Co-transport with H+. Journal of Membrane Biology 53, 129–142. open url image1

Sasaki M, Kasai M, Yamamoto Y, Matsumoto H (1995) Involvement of plasma-membrane potential in the tolerance mechanism of plant-roots to aluminum toxicity. Plant and Soil 171, 119–124.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. The Plant Journal 37, 645–653.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Scott BIH (1962) Electricity in plants. Scientific American 136, 3–11. open url image1

Shabala S (2000) Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll. Plant, Cell and Environment 23, 825–838.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shabala S (2003) Physiological implications of ultradian oscillations in plant roots Plant and Soil 255, 217–226.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shabala S, Knowles A (2002) Rhythmic patterns of nutrient acquisition by wheat roots. Functional Plant Biology 29, 595–605. open url image1

Shabala SN, Newman IA, Morris J (1997) Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiology 113, 111–118.
PubMed |
open url image1

Takabatake R, Shimmen T (1997) Inhibition of electrogenesis by aluminium in characean cells. Plant & Cell Physiology 38, 1264–1271. open url image1

Taylor, GJ (1988). The physiology of aluminum phytotoxicity. In ‘Metal ions in biological systems. Vol 24’. pp. 123–163. (Marcel Dekker: New York)

von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant and Soil 171, 1–15.
Crossref | GoogleScholarGoogle Scholar | open url image1

Walker NA, Beilby MJ, Smith FA (1979) Amine uniport at the plasmalemma of Charophyte cells. I. Current–voltage curves, saturation kinetics and the effect of unstirred layers. The Journal of Membrane Biology 49, 21–55. open url image1

Weisenseel MH, Beck HF, Ehlgotz JG (1992) Growth, gravitropism, and endogenous ion currents of cress root (Lepidium sativum L.). Measurements using a novel three-dimensional recording probe. Plant Physiology 100, 16–25. open url image1

Zhang W-H, Ryan PR, Tyerman SD (2001) Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. Plant Physiology 125, 1459–1472.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1