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figure 16.1 Speciation of aluminum as affected by solution pH. (From R.B. Martin. Fe3+ and Al3+ hydrolysis equilibria. Cooperativity in Al3+ hydrolysis reactions. J. Inorg. Biochem. 44:141-147, 1991.)

16.4.2 Absorption

Since aluminum is a trivalent cation in its phytotoxic form in the external medium, it does not easily cross the plasma membrane. Akeson and Munns (40) calculated that the endocytosis of Al3+ could contribute to its absorption. Alternatively, it is possible that Al3+ could be absorbed through calcium channels (41) or nonspecific cation channels.

Our understanding of aluminum absorption across plant membranes has been limited by the complex speciation of Al, its binding to cell walls, lack of an affordable and available isotope, and lack of sensitive analytical techniques to measure low levels of aluminum in subcellular compartments (42). Aluminum absorption by excised roots of wheat, cabbage (Brassica oleracea L.), lettuce (Lactuca sativa L.), and kikuyu grass (Pennisetum clandestinum Hochst. ex Chiov.), and by cell suspensions of snapbean (Phaseolus vulgaris L.) followed biphasic kinetics (43-45). A rapid, nonlinear, nonmetabolic phase of uptake occurred during the first 20 to 30min. This nonsaturable phase was thought to be accumulation in the apoplastic compartment due to polymerization or precipitation of aluminum or binding to exchange sites in cell walls (44). A linear, metabolic phase of uptake was superimposed over the nonlinear phase and thought to be accumulation in the symplas-mic compartment (i.e., within the plasma membrane).

Using the rare 26Al isotope and accelerator mass spectrometry on giant algal cells of Chara corallina Klein ex Willd., Taylor et al. (42) provided the first unequivocal evidence that aluminum rapidly crosses the plasma membrane into the symplasm. Accumulation of 26Al in the cell wall was nonsaturable during 3 h of aluminum exposure and accounted for most of aluminum uptake. Absorption of aluminum into the protoplasm occurred immediately but accounted for less than 0.05% of the total accumulation (42). Accumulation in the vacuole occurred after a 30-min lag period (42).

16.4.3 Aluminum Speciation in Symplasm

The pH of the cytoplasmic compartment generally ranges from 7.3 to 7.6 (5). Once aluminum enters the symplasm, the aluminate ion, Al(OH)j or insoluble Al(OH)3 could form (Figure 16.1) (46). Alternatively, Al3+ could precipitate with phosphate as variscite, Al(OH)2H2PO4 (47). Based on higher stability constants, it is likely that Al3+ would be complexed by organic ligands, such as adenosine triphosphate (ATP) or citrate (47,48). Martin (47) hypothesized that based on their similar effective ionic radii and affinity for oxygen donor ligands, Al3+ would compete with Mg2+ rather than Ca2+ in metabolic processes.

16.4.4 Radial Transport

The main barrier to radial transport of aluminum across the root into the stele appears to be the endo-dermis. Rasmussen (49) used electron microprobe x-ray analysis to show little penetration of aluminum past the endodermis of corn (Zea mays L.) roots. Similarly, in Norway spruce (Picea abies H. Karst.) roots, a large aluminum concentration was detected outside the endodermis, but very low aluminum concentrations on the inner tangential wall (3,50). Using secondary-ion mass spectrometry, Lazof et al. (51) confirmed that the highest aluminum accumulation occurred at the root periphery of soybean root tips, with substantial aluminum in cortical cells, but very low aluminum in stellar tissues. Similar to calcium, aluminum is thought to bypass the endodermis, entering the xylem in maturing tissues where the endodermis is not fully suberized.

16.4.5 Mucilage

Aluminum must cross the root mucilage before it can penetrate to the root apical meristem. Mucilage is produced by the root cap and is a complex mixture of high-molecular-weight polysaccharides, a population of several thousand border cells, and an array of cell wall fragments (52). Archambault et al. (53) showed that aluminum binds tightly to wheat mucilage, with 25 to 35% of total aluminum remaining after citrate desorption.

16.5 ALUMINUM TOXICITY SYMPTOMS IN PLANTS 16.5.1 Short-Term Effects

Owing to the numerous biochemical processes with which aluminum can interfere, researchers have attempted to determine the primary phytotoxic event by searching for the earliest responses to aluminum. Symptoms of aluminum toxicity that occur within a few hours of aluminum exposure are inhibition of root elongation, disruption of root cap processes, callose formation, lignin deposition, and decline in cell division.

16.5.1.1 Inhibition of Root Elongation

The first, easily observable symptom of aluminum toxicity is inhibition of root elongation. Elongation of adventitious onion (Allium cepa L.) roots (54), and primary roots of soybean (55,56), corn (57,58), and wheat (59-61) were suppressed within 1 to 3 h of aluminum exposure. The shortest time of aluminum exposure required to inhibit elongation rates was observed in seminal roots of an aluminum-sensitive corn cultivar BR 201F after 30min (62).

Application of aluminum to the terminal 0 to 3 mm of corn root must occur for inhibition of root elongation to occur; however, the presence of the root cap was not necessary for aluminum-induced growth depression (63). Using further refinement of techniques, Sivaguru and Horst (58) determined that the most aluminum-sensitive site in corn was between 1 and 2 mm from the root apex, or the distal transition zone (DTZ), where cells are switching from cell division to cell elongation.

Lateral root growth of soybean was inhibited by aluminum-containing solutions to a greater extent than that of the taproot (64,65). Interestingly, Rasmussen (49) observed greater aluminum accumulation in lateral roots that emerged from the root surface, breaking through the endodermal layer. Similarly, root hair formation was more sensitive to aluminum toxicity than root elongation in white clover (Trifolium repens L.) (66).

16.5.1.2 Disruption of Root Cap Processes

The Golgi apparatus is the site of synthesis of noncellulosic polysaccharides targeted to the cell wall (67). Activity of the Golgi apparatus in the peripheral cap cells of corn was disrupted at 18 |M Al, a concentration below that necessary to inhibit root growth (68). In wheat, mucilage from the root cap disappeared within 1 h of aluminum exposure, and dictyosome volume and presence of endoplasmic reticulum decreased within 4h (69). Death of root border cells (a component of root mucilage) occurred within 1 h of exposure to aluminum in snapbean roots (70).

16.5.1.3 Callose Formation

Callose is a polysaccharide consisting of 1,3-0-glucan chains, which are formed naturally by cells at a specific stage of wall development or in response to wounding (67). An early symptom of aluminum toxicity is formation of callose in roots. Using fluorescence spectrometry, callose could be quantified in soybean root tips (0 to 3 cm from root apex) after 2h of exposure to 50 ||M Al (55). In root cells surrounding the meristem of Norway spruce roots, distinct callose deposits were observed after 3 h of exposure to 170 |M Al (71). Zhang et al. (72) showed that callose accumulated in roots of aluminum-sensitive wheat cultivars exposed to 75 | M Al and they proposed using callose synthesis as a rapid, sensitive marker for aluminum-induced injury. However, callose was not accumulated in two aluminum-sensitive arabidopsis (Arabidopsis thaliana Heynh.) mutants exposed to aluminum, indicating no obligatory relationship between callose deposition and aluminum-induced inhibition of root growth (73). Sivaguru et al. (74) showed that aluminum-induced callose deposition in plasmodesmata of epidermal and cortical cells of aluminum-sensitive wheat roots reduced movement of micro-injected fluorescent dyes between cells.

16.5.1.4 Lignin Deposition

Lignins are complex networks of aromatic compounds that are the distinguishing feature of secondary walls (67). Deposition of lignin in response to aluminum was found in wheat cortical cells located 1.4 to 4.5 mm from the root tip (elongating zone [EZ]) after 3h of exposure to 50 |M Al (75). Lignin occurred in cells with damaged plasma membranes as indicated by staining with propidium iodide, and Sasaki et al. (61) proposed that aluminum-induced lignification was a marker of aluminum injury and was closely associated with inhibition of root elongation. Interestingly, Snowden and Gardner (76) showed that a cDNA induced by aluminum treatment in wheat exhibited high homology with the gene for phenylalanine ammonia-lyase, a key enzyme in the pathway for biosynthesis of lignin.

16.5.1.5 Decline in Cell Division

A decrease in abundance of mitotic figures was observed in adventitious roots of onion after 5 h of exposure to 1 mM Al (54). Similarly, a decrease in the mitotic index of barley root tips was found within 1 to 4 hours of exposure to 5 to 20 |M AI (pH 4.2) (77).

16.5.2 Long-Term Effects

Although they may not be indicative of initial, primary phytotoxic events, long-term effects of aluminum are important for plants growing in aluminum-toxic soils or subsoils. Long-term exposure to aluminum over several days or weeks results in suppressed root and shoot biomass, abnormal root morphology, suppressed nutrient uptake and translocation, restricted water uptake and transport, suppressed photosynthesis, and inhibition of symbiosis with rhizobia.

16.5.2.1 Suppressed Root and Shoot Biomass

Increasing aluminum concentrations in solution, sand, or soil decreased fine root biomass of red spruce (Picea rubens Sarg.) (78). Typically, aluminum reduces root biomass to a greater degree than shoot biomass, resulting in a decreased root/shoot ratio (78-80). In contrast, in 3-year-old Scots pine (Pinus sylvestris L.), increasing solution of aluminum up to 5.6mM produced no obvious aluminum toxicity symptoms on roots but decreased needle length and whole shoot length, resulting in increased needle density (81).

16.5.2.2 Abnormal Root Morphology

Often, one symptom of aluminum toxicity is 'coralloid' root morphology with inhibited lateral root formation and thickened primary roots (54). Cells in the elongation zone of primary wheat roots exposed to aluminum had decreased length and increased diameter, resulting in appearance of lateral swelling (61). This abnormal root morphology combined with reduced root length could result in decreased nutrient uptake and multiple deficiencies.

16.5.2.3 Suppressed Nutrient Uptake and Translocation

Increasing aluminum levels in the medium have been reported to decrease uptake and translocation of calcium, magnesium, and potassium (78,82). Forest declines in North America and Europe have been proposed to be due to aluminum-induced reductions in calcium and magnesium concentrations of tree roots and needles (3). Excess aluminum reduced magnesium concentration of Norway spruce needles to a level considered to be critical for magnesium deficiency (3). Also, aluminum toxicity reduced calcium and magnesium leaf concentrations in beech (Fagus sylvatica L.) (83). In sorghum (Sorghum bicolor Moench), magnesium deficiency was a source of acid-soil stress (84).

In the case of phosphorus, concentrations increased in roots but typically decreased in shoots. In roots of red spruce, 32P accumulation increased but 32P translocation to shoots decreased (85). Clarkson (86) proposed that there were two interactions between aluminum and phosphorus: (a) an adsorption-precipitation reaction in the apoplast; and (b) reaction with various organic phosphorus compounds within the symplasm of the cell. Aluminum and phosphorus were shown to be copre-cipitated in the apoplast of corn roots, using x-ray microprobe analysis (49). Excised corn roots exposed to 20 h of 0.1 to 0.5 mM Al had decreased mobile inorganic phosphate (40%), ATP (65%), and uridine diphosphate glucose (UDGP) (65%) as shown by 31P-NMR (nuclear magnetic resonance), indicating aluminum interference with phosphorus metabolism within the symplasm (87,88).

16.5.2.4 Restricted Water Uptake and Transport

Typically, aluminum toxicity decreases water uptake and movement in plants. Stomatal closure of arabidopsis occurred after 9h of exposure to 100 |M Al at pH 4.0 (89). In wheat, transpiration decreased after 28 days of exposure to 148 |M Al (90). Treatment of 1-year-old black spruce (Picea mariana Britton) with 290 |M Al resulted in wilting and reduced water uptake within 7 days (91). Hydraulic conductivity of red oak roots was reduced after 48 to 63 days of exposure to aluminum, although no effect was observed after only 4 days (92). In contrast, transpiration in sorghum increased after 28 days of aluminum treatment (90).

16.5.2.5 Suppressed Photosynthesis

Net photosynthesis is reported to decrease with excess aluminum relative to normal rates. Exposure to 250 |M Al for 6 to 8 weeks reduced the photosynthetic rate of red spruce, and McCanny et al. (79) attributed this effect to an aluminum-induced decrease in root/shoot ratio. Similarly, exposure of beech seedlings to 0.37 mM Al for 2 months significantly decreased net CO2 assimilation rates (83).

16.5.2.6 Inhibition of Symbiosis with Rhizobia

Biological nitrogen fixation results in release of H+, acidification of legume pastures, and increased solubilization of aluminum (2). Excess aluminum has an inhibitory effect on rhizobial symbiosis. In an Australian pasture, the percentage of plant nitrogen derived from the atmosphere declined in subterranean clover (Trifolium subterraneum L.) as foliar concentration of aluminum increased (93). In four tropical pasture legumes, aluminum at >25 |M for 28 days delayed appearance of nodules, decreased percentage of plants that nodulated, and decreased number and dry weight of nodules (94). In phasey-bean (Macroptilium lathyroides Urb.) and centro (Centrosema pubescens Benth.), nodulation was more sensitive to aluminum toxicity than host plant growth (94).

Aluminum also inhibited the multiplication and nodulating ability of the symbiotic bacterium, Rhizobium leguminosarum bv. trifolii Frank (66). Recent research efforts have focused on identifying aluminum-tolerant rhizobial strains. For example, strains of Bradyrhizobium spp. that were isolated from acid soils were found to more tolerant of 50 ||M Al at pH 4.5 than commercial strains (95).

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