Plant Mechanisms of Aluminum Tolerance

Mechanisms of internal tolerance of aluminum involve: (a) complexation with organic acids, (b) complexation with phenolics, (c) complexation with silicon, (d) sequestration in the vacuole or other storage organs, and (e) trapping of aluminum in cells.

Complexation with Organic Acids

In the leaves of aluminum-accumulating hydrangea, Ma et al. (257) used molecular sieve chromatography to determine that citrate eluted at the same time as aluminum and that the molar ratio of aluminum to citric acid was approximately 1:1. In the aluminum accumulator, buckwheat, aluminum was complexed with citrate in the xylem (258), but with oxalic acid in vacuoles of leaf cells (259,260). In the aluminum accumulator, Melastoma malabathricum L., aluminum citrate occurred in the xylem sap and was then transformed into aluminum oxalate for storage in leaves (261,262).

Complexation with Phenolics

In aluminum-accumulating tea, Nagata et al. (263) used 27Al-NMR to demonstrate that aluminum was bound to catechin in young leaves and buds; in mature leaves, aluminum-phenolic acid and aluminum-organic acid complexes were found. Interestingly, Ofei-Manu et al. (227) showed that at pH 7 (cytoplasmic pH), aluminum binding capacity is in the order: quercetin>catechin, chlorogenic acid, morin>organic acids. Among ten woody plant species and two marker crop species, a positive linear correlation was found between root phenolic compounds and aluminum tolerance, based on aluminum-inhibited root elongation (227).

Complexation with Silicon

Cocker et al. (229) proposed that amelioration of aluminum toxicity by silicon is due to formation of an aluminosilicate compound in the root apoplast. Hodson and Sangster (264) proposed that codeposition of aluminum and silicon in needles of conifers is responsible for aluminum detoxification by silicon. Hodson and Evans (228) reviewed the evidence in support of various mechanisms of silicon amelioration of aluminum toxicity, and they divided plants into four groups: (a) aluminum accumulators in arborescent dicots, (b) silicon accumulators in grasses, (c) gymnosperms and arborescent dicots with moderate amounts of aluminum and silicon, and (d) herbaceous dicots that exclude aluminum and silicon. Obviously, aluminum can codeposit with silicon only in plants that accumulate both elements. Aluminum was deposited in phytoliths (hydrated silica deposits) of conifers, graminaceous plants, and dicots in the Ericaceae family (265,266). Using x-ray microanalysis, Hodson and Sangster (267) found codeposition of aluminum and silicon in the outer tangential wall of the endodermis of sorghum. In Faramea marginata Cham., a woody member of the Rubiaceae family that is known to accumulate aluminum and silicon in leaves, colocalization of aluminum and silicon in a molar ratio of 1:2 occurred in the cortex of stem sections and throughout leaves (268). A good review of aluminum and silicon interactions can be found in Hodson and Evans (228), Cocker et al. (229), and Hodson and Sangster (264).

Sequestration in the Vacuole or in Other Organelles

Aluminum ions could be sequestered in vacuoles or other storage organelles where they would not affect metabolism in the cytoplasm adversely. The presence of 50 µM Al increased pyrophosphatedependent and ATP-dependent H⁺ pump activity in tonoplast membrane vesicles isolated from barley roots, and Kasai et al. (269) hypothesized that Al³⁺ was sequestered in the vacuole perhaps by an Al/nH⁺ exchange reaction. Interestingly, expression of two 51 kDa proteins is strongly induced in an aluminum-tolerant wheat cultivar, and only weakly expressed in an aluminum-sensitive wheat cultivar (270). Sequence analysis of the purified peptides showed that one is homologous to the B subunit of the vacuolar H⁺-ATPase (V-ATPase) (270).

In an aluminum-tolerant unicellular red alga (Cyanidium caldarium Geitler), aluminum accumulated in spherical electron-dense bodies in the cytoplasm near the nucleus (271). These bodies contained high levels of iron and phosphorus, and the researchers speculated that they might be iron-storage sites under normal culture conditions. Interestingly, transferrin, an iron carrier, is the main protein that binds Al³⁺ in the blood plasma of animals (47).

Trapping of Aluminum in Cells

Fiskesjo (272) proposed that aluminum could be trapped in root border cells, which were then detached and sloughed away from roots. Consistent with this hypothesis, detached root border cells of snap bean were killed by aluminum within 2 h of aluminum exposure (70). A punctated pattern of cell death was observed in aluminum-tolerant wheat roots after 8 h of exposure to aluminum, with an increase in oxalate oxidase activity and H₂O2 production after 24 h (273). Delisle et al. (273) speculated that cell death could be a means for root tip cells to trap or exclude aluminum from live tissues. Interestingly, a hypersensitive cell death response is a common means for plants to trap pathogens, not allowing them to spread to other cells. Many genes up-regulated by aluminum in wheat are similar to pathogenesis-related genes (274).