Mechanisms Of Aluminum Toxicity In Plants

Controversy exists over mechanisms of aluminum phytotoxic effects (96-99). Researchers long have debated whether the primary toxic effect of aluminum is on inhibition of cell elongation or inhibition of cell division. Lazof and Holland (28) demonstrated in soybean, pea (Pisum sativum L.), and bean (Phaseolus vulgaris L.) that both effects occur, with rapid, largely reversible responses to aluminum toxicity due to cell extension effects and irreversible responses due to cell division effects.

Another question puzzling researchers is whether the primary injury due to aluminum in plants is symplasmic or apoplastic. Horst (100) and Horst et al. (101) reviewed the evidence supporting the apoplast as the site of the primary aluminum-toxic event. However, dividing aluminum effects into symplasmic or apoplastic can be arbitrary, because aluminum could enter the symplasm to produce effects in the cell wall or outer face of the plasma membrane.

Since cell walls occur in plants and not animals, aluminum injuries at this site are unique to plants. Possible mechanisms of aluminum injury in cell walls include: (a) aluminum binding to pectin; or (b) modification of synthesis or deposition of polysaccharides. Jones and Kochian (102) proposed that the plasma membrane is the most likely site of aluminum toxicity in plants. Possible mechanisms of toxicity in the plasma membrane are: (a) aluminum binding to phospho-lipids; (b) interference with proteins involved in transport; or (c) signal transduction. Once aluminum enters the symplasm, there are many possible interactions with molecules containing oxygen donor ligands (47,48). Probable mechanisms of aluminum toxicity within plant cells include: (a) disruption of the cytoskeleton, (b) disturbance of calcium homeostasis, (c) interaction with phytohormones, (d) oxidative stress, (e) binding to internal membranes in chloroplasts, or (f) binding to nuclei.

16.6.1 Cell Wall

Pectins are a mixture of heterogenous polysaccharides rich in D-galacturonic acid; one major function is to provide charged structures for ion exchange in cell walls (67). Under acidic conditions, aluminum binds strongly to negatively charged sites in the root apoplast, sites consisting mostly of free carboxyl groups on pectins. Klimashevskii and Dedov (103) isolated cell walls from pea roots, exposed them to aluminum, and found that aluminum decreased plasticity and elasticity of cell walls. Blamey et al. (104) demonstrated in vitro a rapid sorption of aluminum by calcium pectate and proposed that aluminum phytotoxicity is due to strong binding between aluminum and calcium pectate in cell walls. Reid et al. (105) proposed that aluminum could disrupt normal cell wall growth either by reducing Ca2+ concentration below that required for cross-linking of pectic residues or through formation of aluminum cross-linkages that alter normal cell wall structure. Using x-ray microanalysis, Godbold and

Jentschke (106) showed that aluminum displaced calcium and magnesium from root cortical cell walls of Norway spruce. Using a vibrating calcium-selective microelectrode, Ryan and Kochian (107) observed that addition of aluminum commonly resulted in an initial efflux of calcium from wheat roots, probably due to displacement of calcium from cell walls.

Pectin is secreted in a highly esterified form from the symplasm to the apoplast, where demethylation takes place by pectin methylesterase (PME), resulting in free carboxylic groups available to bind aluminum (108). Transgenic potato (Solanum tuberosum L.) overexpressing PME is more sensitive to aluminum based on inhibition of root elongation relative to unmodified control plants, indicating that increased binding sites for aluminum in the apoplast are associated with increased aluminum sensitivity (108).

16.6.1.1 Modification of Synthesis or Deposition of Polysaccharides

In addition to external binding to cell wall components, aluminum also could interfere with the internal synthesis or deposition of cell wall polysaccharides. Exposure of wheat seedlings to 10 |M Al for 6h decreased mechanical extensibility of subsequently isolated cell walls (109). Tabuchi and Matsumoto (109) showed that aluminum treatment modified cell wall components, increasing the molecular mass of hemicellulosic polysaccharides, thus decreasing the viscosity of cell walls, and perhaps restricting cell wall extensibility.

Uridine diphosphate glucose (UDGP) is the substrate for cellulose synthesis. Using 31P-NMR, Pfeffer et al. (87) demonstrated that a 20-h exposure of excised corn roots to 0.1 mM Al decreased UDGP by 65%, and they speculated that such suppression could limit production of cell wall poly-saccharides. In barley, one of the most aluminum-sensitive cereals, callose was excreted from the junction between the root cap and the root epidermis after 38min of exposure to 37 |M Al, and Kaneko et al. (110) proposed that aluminum-induced inhibition of root elongation could be due to reduced cell wall synthesis caused by a shortage of substrate to form polysaccharides.

16.6.2 Plasma Membrane 16.6.2.1 Binding to Phospholipids

Biological membranes are composed of phospholipids that contain a phosphate group (67), and aluminum can bind to this negatively charged group. Using electron paramagnetic resonance spec-troscopy, Vierstra and Haug (111) demonstrated that 100 mM Al at pH 4 decreased fluidity in membrane lipids of a thermophilic microorganism (Thermoplasma acidophilum Darland, Brock, Samsonoff and Conti). Using physiologically significant concentrations of aluminum, Deleers et al. (112) showed that 25 |M Al increased rigidity of membrane vesicles as indicated by the increased temperature required to maintain a specific polarization value. In addition, aluminum at < 30 |M could induce phase separation of phosphatidylserine (PS; a negatively charged phospholipid) vesicles, as shown by leakage of a fluorescent compound (113).

Phosphatidylcholine (PC) is the most abundant phospholipid in plasma membranes of eukary-otes, and Akeson et al. (114) showed that in vitro, Al3+ has a 560-fold greater affinity for the surface of PC than Ca2+. Further, Jones and Kochian (102) found that lipids with net negatively charged head groups such as phosphatidyl inositol (PI) had a much greater affinity for aluminum than PC with its net neutral head group. Interestingly, Delhaize et al. (115) found that expression of a wheat cDNA (TaPSS1) encoding for phosphatidylserine synthase (PSS) increased in response to excess aluminum in roots. Overexpression of this cDNA conferred aluminum resistance in one strain of yeast (Saccharomyces cerevisiae) but not in another. In addition, a disruption mutant of the endogenous yeast CHO1 gene that encodes for PSS was sensitive to aluminum (115).

Aluminum reduced membrane permeability to water as shown by a plasmometric method on root disks of red oak (116). To remove the confounding effect of aluminum binding to cell walls, Lee et al. (117) used protoplasts of red beet (Beta vulgaris L.). Within 1 min of exposure to 0.5 mM

Al, volumetric expansion of red beet cells was reduced under hypotonic conditions, and Lee et al. (117) hypothesized that aluminum could bridge neighboring negatively charged sites on the plasma membrane, stabilizing the membrane.

Binding of Al3+ to the exterior of phospholipids reduces the surface negative charge of membranes. Kinraide et al. (27) proposed that accumulation of aluminum at the negatively charged cell surface plays a role in rhizotoxicity and that amelioration of aluminum toxicity by cations is due to reduced negativity of the cell-surface electrical potential by charge screening or cation binding. Kinraide et al. (27) found a good correlation between the reduction in relative root length of an aluminum-sensitive wheat cultivar with aluminum activity as calculated at the membrane surface, but not in the bulk external solution. Ahn et al. (118) measured the zeta potential (an estimate of surface potential) of plasma membrane vesicles from squash (Cucurbita pepo L.) roots and showed that aluminum exposure resulted in a less negative surface potential. Measuring uptake of radioisotopes by barley roots, Nichol et al. (119) showed that influx of cations (K+, NH4", and Ca2+) decreased whereas influx of anions (NO3-, HPO42 ) increased in the presence of aluminum. They speculated that binding of Al3+ to the exterior of a plasma membrane forms a positively charged layer that retards movement of cations to the membrane surface and increases movement of anions to the surface.

In contrast, Silva et al. (120) demonstrated that Mg2+ was 100-fold more effective than Ca2+ in alleviating aluminum-induced inhibition of soybean taproot elongation. They (120) suggested that such an effect could not be explained by changes in membrane surface potential and proposed that the protective effects of Mg could be due to alleviation of aluminum binding to G-protein.

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