Probing the "malate hypothesis" of differential aluminum tolerance in wheat by using other rhizotoxic ions as proxies for Al

Abstract

An Al-stimulated eux of malate from the root apex has been proposed as the primary mechanism whereby some wheat (Triticum aestivum L.) genotypes demonstrate marked resistance to the rhixotoxic metal Al. Appealing in its simplicity, the model has not been unequivocally validated, and suers from some signi®-cant discrepancies between estimated, steady-state concentrations of malate at the root surface and concentrations that are necessary to explain the resistance of the superior genotypes. Using two other rhizotoxic ions that are also chelated by malate, Cu(II) and La(III), we speci®cally probed whether the quantities of malate released by tolerant genotypes could eectively detoxify Al. Experiments with exogenous additions of malate to solution showed that ³200 lM malate is required to account for the dierence between Scout 66 (Al-sensitive) and Atlas 66 (Al-tolerant) wheats, and that this level of malate can also partially alleviate the toxicities of Cu and La. When simultaneously exposed to a mildly rhizotoxic level of Al (25 lM) to induce malate eux, Atlas exhibited a pronounced reduction in sensitivity to Cu. When, La was used as the proxy ion, however, no such Al-induced tolerance to La was observed, a result that refutes the signi®cance of malate eux to Al tolerance. Additional experiments using Al, Cu, and La in combination suggested that a trivalent ion can alleviate Cu toxicity directly (i.e. via competition for apoplastic binding), providing an alternative explanation for the ability of Al to detoxify Cu in Atlas. Using a weight-of-evidence approach, we argue that malate eux plays at most a minor role in the dierential Al tolerance of wheat, and that a more integrative, multifaceted model of tolerance is needed.

Polymeric Forms of Al13and Silicon Compounds as Unconventional Binding Agents for some Toxic Metals in Soils

“…the value at which the formation of tridecamer was the most efficient, the relative root growth reached its minimum level, which clearly provides the toxicity of this Al form. Similar conclusions were drawn by Parker and Pedler (1998) from tests with maize. Other authors (Wallace 1992;Wagatsuma et al 2001) reported the toxic influence of polymeric Al forms on oat tolerant towards mono-nucleus forms.…”

Possible Involvement of Protein Phosphorylation in Aluminum-Responsive Malate Efflux from Wheat Root Apex

“…Compared with citrate and oxalate, malate is suggested to bind to Al less effectively (Hue et al, 1986). This raises a question as to whether malate efflux is insufficient to explain the Al-resistance mechanism in wheat cultivars (Parker and Pedler, 1998). To examine the possible role of malate efflux in the Al-resistance mechanism, we asked if inhibition of malate efflux by K-252a would affect Al accumulation in root apexes and on Al-induced inhibition of root growth in cv Atlas.…”

The High Level of Aluminum Resistance in Signalgrass Is Not Associated with Known Mechanisms of External Aluminum Detoxification in Root Apices

“…Stoichiometric considerations would indeed suggest that the amount of organic acids secreted by root apices of Al resistant wheat and maize genotypes might only be adequate to detoxify Al at concentrations well below those inhibiting root growth of signalgrass (Delhaize et al, 1993;Pellet et al, 1995Pellet et al, , 1997Ryan et al, 1995b;Parker and Pedler, 1998). The effectiveness of Al resistance mechanisms based on external chelation of Al 3ϩ by chelating ligands may also be limited by other cell-surface ligands competing for Al ions (Parker and Pedler, 1998), the presence of other cations capable of forming complexes with organic acids (Jones and Darrah, 1994), adsorption of organic acids to the soil's exchange phase (Jones et al, 1996a), and rapid microbial degradation of organic acids in soils (Jones et al, 1996b). In addition, an Al exclusion mechanism based on the efflux of phosphate may be of questionable adaptive value in highly weathered acid soils where P is the principal limiting nutrient.…”