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Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots

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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.

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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

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Authors and Affiliations

  1. CSIRO Division of Plant Industry, GPO Box 1600, 2601, Canberra, ACT, Australia

    Peter R. Ryan, Emmanuel Delhaize & Peter J. Randall

Authors
  1. Peter R. Ryan
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  2. Emmanuel Delhaize
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  3. Peter J. Randall
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Corresponding author

Correspondence to Emmanuel Delhaize.

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.

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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

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