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Molecular physiology of aluminum toxicity and tolerance in plants.

Abstract
Aluminum Chemistry in the Soil
Aluminum Toxicity
 Morphophysiological
 Cellular and Biochemical
Aluminum Tolerance
 Physiological and Biochemical
Molecular Genetics of Aluminum Toxicity and Tolerance
Remarks on the Future and Conclusions
Acknowledgment
Literature Cited


Aluminum Chemistry in the Soil

Aluminum, bound as oxides and complex aluminosilicates, ranks third in abundance among the elements in the Earth's crust. Despite much research since Hartwell and Pember first postulated, nearly 90 years ago, that soluble aluminum is a major inhibitor of plant growth in acid soils, the mechanism of aluminum phytotoxicity is not yet fully understood. Aluminum can inhibit root growth at the organ, tissue, and cellular levels at micromolecular concentrations (Ciamporova, 2002). Acid soils, present mostly in humid tropical and subtropical areas of the world, are characterized by having excess [H.sup.+], [Mn.sup.2+], and [Al.sup.3+], with deficiencies of [Ca.sup.2+], [Mg.sup.2+], and P[O.sub.4.sup.3-] (Foy, 1984). Additionally, sulfur dioxide and other air pollutants cause acid soil stress in areas other than the tropics. In acidic soils, hydroxyl-rich aluminum compounds solubilize to an extent in the soil solution. Forty percent of the arable land globally is acidic because of solubilization of the abundantly present aluminum, greatly limiting crop productivity.

Aluminum chemistry is quite complex. It has a high ionic charge and a small crystalline radius, which give it a level of reactivity that is unmatched by other soluble metals. When the pH of a solution is raised above 4.0, [Al.sup.3+] forms the mononuclear species AlO[H.sup.2+], Al[(OH).sub.2.sup.+], Al[(OH).sub.3], and Al[(OH).sub.4.sub.+], and soluble complexes with inorganic ligands such as sulfate and fluoride, that is, [AlF.sup.2+], [AlF.sup.3+], Al[(SO).sub.4.sup.+], and also with a host of organic compounds. Larger polynuclear hydroxyl aluminum species also form as metastable intermediates during Al[(OH).sub.3] precipitation. The mononuclear [Al.sup.3+] species seems to be most toxic at low pH, at which it exists as an octahedral hexahydrate. With increasing pH, Al[([H.sub.2]O).sup.3+.sub.6] undergoes repeated deprotonations to form insoluble Al[(OH).sub.3] at pH 7.0. At cytosolic pH, 7.4, Al[(OH).sub.4.sup.-], that is, aluminate ion, is formed. In near neutral solutions, polynuclear forms of aluminum, which contain more than one aluminum atom, form, one of the most important being triskaidekaaluminum, Al[O.sub.4][Al.sub.12][(OH).sub.24][([H.sub.2]O).sub.127+], referred to as [Al.sub.13] (Parker & Bertsch, 1992).

Aluminum Toxicity

MORPHOPHYSIOLOGICAL

The main aluminum toxicity symptom is inhibition of root elongation with simultaneous induction of [beta]-1,3-glucan (callose) synthesis, which is apparent after even a short exposure time. Aluminum causes extensive root injury, leading to poor ion and water uptake (for a review, see Barcelo & Poschenrieder, 2002). One hypothesis is that the sequence of toxicity starts with perception of aluminum by the root cap cells, followed by signal transduction and a physiological response within the root meristem (Bennet and Breen, 1991). However, recent work has ruled out a role of the root cap and emphasizes that the root meristem is the sensitive site. Root tips have been found to be the primary site of aluminum injury, and the distal part of the transition zone has been identified as the target site in maize (Zea mays) (Sivaguru & Horst, 1998). Division and elongation of root cells result in root elongation. Aluminum is known to induce a decrease in mitotic activity in many plants, and the aluminum-induced reduction in the number of proliferating cells is accompanied by the shortening of the region of cell division in maize (Ryan et al., 1993). The mechanism responsible for decreased cell division with root exposure to aluminum is uncertain. Aluminum can accumulate inside cells at the root tip within 30 minutes to several hours of exposure, and the intracellular aluminum then binds to cell nuclei and DNA (Matsumoto, 1991; Vasquez et al., 1999). However, most experiments have used higher aluminum concentrations than have agronomic significance, so the role of aluminum binding at the nucleus is unclear. Intracellular aluminum accumulates in nuclei of differentiated cells 1 to 2 mm behind the root tip, close to the undifferentiated meristematic zone. In experiments using aluminum-sensitive and aluminum-tolerant soybean (Glycine max) seedlings exposed to aluminum (1.45 [micro]M) showed substantial aluminum accumulation in the nuclei within 30 minutes, and the accumulation was higher in seedlings with the aluminum-sensitive genotype, as shown by confocal laser scanning microscopy (Silva et al., 2000). The production and development of root border cells also vary with genotype. Aluminum seriously inhibits the production and release of root border cells, resulting in clumping of border cells in Scout 66 but in less clustering of the cells in Atlas 66, both aluminum-tolerant wheat (Triticum aestivum) cultivars. Aluminum treatment also induced the death of detached border cells in vitro. The removal of border cells from root tips of both Atlas 66 and Scout 66 enhanced the aluminum-induced inhibition of root elongation, concomitant with increased aluminum accumulation in the root, suggesting a potential role of the border cells in protection from aluminum injury in wheat (Zhu et al., 2003). Auxin seems to play a major role in these aluminum effects on cell division. However, interaction with other hormonal factors cannot be excluded in view of the rapid effects of aluminum on root cytokinin and ethylene concentrations (Massot et al., 2002). Our understanding of the timing of aluminum toxicity responses has been improved by the development of computer-assisted devices based on linear displacement transducer systems and video monitoring (Llugany et al., 1995; Kidd et al., 2001). Such systems have helped to determine the response times of roots faced with environmentally feasible aluminum concentrations. Monitoring of root elongation inhibition, which occurs after 30 minutes to 2 hours of aluminum exposure, has suggested different response models, the toxicity curve threshold, hormesis, and tolerance threshold models. Earlier experiments have clearly shown that both apoplast and symplast are target sites of aluminum toxicity. Aluminum toxicity targeted to the apoplast invokes a rapid and irreversible displacement of calcium from cell-wall components such as calcium pectate (Blamey, 2001). Recent pressure probe experiments showed aluminum-induced cell-wall stiffening in root cells of aluminum-sensitive maize, and hemicellulosic polysaccharides accumulated in cell walls of root tips in aluminum-sensitive wheat (Gunse et al., 1997; Tabuchi & Matsumoto, 2001). In the root cap cells, Golgi bodies are sensitive to aluminum. Structural modifications after exposure to aluminum include a lower frequency of Golgi bodies in the cells, resulting in a decrease in mucilage secretion. Moreover, [Ca.sup.2+] is needed for the secretory functions of the cap cells, and aluminum is known to affect [Ca.sup.2+] homeostasis in cells, also leading to a reduction in mucilage secretion (Marschner, 1995; Kawano et al., 2003). The cytoskeleton appears to be extremely sensitive to aluminum. Experiments with inhibitors of actin cytoskeletons showed changes similar to those induced by aluminum, suggesting that growth inhibition by aluminum is a result of actin network distortion and rearrangement and depolymerization of microtubules, which are early symptoms of aluminum treatment of wheat and maize root apices (Sasaki et al., 1997a; Sivaguru et al., 1999a).

CELLULAR AND BIOCHEMICAL

The plasma membrane, which is rich in phospholipids, is a potential target of aluminum. Aluminum has been shown to alter the surface charge of liposome vesicles and to affect the fluidity of membranes in the extremophile Thermoplasma acidophilum (Viestra & Haug, 1978; Akeson et al., 1989). Aluminum binds to phospholipids in the microsomal fractions of root plasma membrane of barley (Hordeum vulgare), and has toxic effects on membrane proteins (Caldwell, 1989). Aluminum induces an increase in membrane permeability, allowing nonelectrolytes as well as lipid permeators to pass (Zhao et al., 1987). Aluminum has also been shown to reduce membrane fluidity and to increase the packing density of lipids (Chen et al., 1991). Though a decrease in [H.sup.+]-ATPase and [H.sup.+]-pump activity of wheat root plasma membrane was observed under aluminum treatment, the response did not significantly differ between sensitive and tolerant cultivars (Sasaki et al., 1995). Experiments with barley suggest the development of a positively charged layer that allows anions to be transported across by proteins (Nichol et al., 1993). A stronger depolarization of membrane potential was seen in an aluminum-tolerant wheat cultivar than in an aluminum-sensitive one with increasing aluminum concentrations. Aluminum caused depolarization of the transmembrane potential and a simultaneous increase in cytosolic [Ca.sup.2+] contents, measured in the same cells. (Zheng & Yang, 2005). A similar inhibition of potassium efflux from the cytosol was observed in these same wheat cultivars (Olivetti et al., 1995). In pea (Pisum sativum) and barley, considerable permeability of root membranes was seen after a 30-minute aluminum pretreatment (Ishikawa & Wagatsuma, 1998). Aluminum toxicity also affects plasma membrane-associated microtubules (Collings et al., 1992). Plasma membrane vesicles isolated from roots pretreated with aluminum showed a lower depolarization response to added aluminum in vitro than control roots, suggesting that tight binding of aluminum to plasma membrane target sites occurs in the first 5 mm of the root apex, possibly causing irreversible alteration of membrane properties. Immunolocalization of [H.sup.+]-ATPase showed a decrease in tissue-specific [H.sup.+]-ATPase in epidermal and cortical cells (2-3 mm) after aluminum exposure, and zone-specific depolarization of surface potential coupled to [H.sup.+]-ATPase activity, in squash (Cucurbita pepo) roots (Ahn et al., 2001). Impairment of [H.sup.+] transport with a decrease in [H.sup.+]-ATPase activity was also seen in aluminum-exposed squash roots (Ahn et al., 2002). Recently Ahn et al. (2004) reported aluminum-induced changes in the plasma membrane surface potential and [H.sup.+]-ATPase activity in near isogenic wheat lines differing in aluminum tolerance. After 4 hours of vivo treatment with aluminum (2.6 [micro]M), [H.sup.+]-ATPase activity and the [H.sup.+] transport rate were decreased and surface potential was depolarized in plasma membrane vesicles from root tips of the aluminum-sensitive ES8 cultivar but not in those of the aluminum-tolerant cultivar ET8. Malate was shown to alleviate the toxic effects of aluminum on [H.sup.+]-ATPase activity and surface potentials. In vitro treatment with aluminum did not affect [H.sup.+]-ATPase activity in plasma membrane vesicles from a region distal to the root tips in aluminum-sensitive ES8, but it activated [H.sup.+]-ATPase in aluminum-tolerant ET8. Aluminum-induced exudation of malate was accompanied by changes in plasma membrane surface potential and [H.sup.+]-ATPase activation. An increase in ATP- and pyrophosphate ([PP.sub.i])-dependent [H.sup.+]-pumps of the tonoplast vesicles was observed in barley roots under aluminum stress, possibly because of an increase in [H.sup.+]-ATPase and [H.sup.+]-Ppiase, as seen by immunoblot analysis (Matsumoto et al., 1996). Aluminum-sensitive wheat genotypes accumulate more aluminum in root tissues than aluminum-resistant ones (Collet et al., 2002). A transient increase in cytosolic [[H.sup.+]] in aluminum-tolerant and -sensitive wheat cultivars subjected to aluminum treatment has been observed. However, though normal pH is regained in tolerant cultivars, repeated addition of aluminum causes a decline in cytosolic pH in sensitive ones (for a review, see Matsumoto, 2000). The degree of aluminum toxicity is affected by cytosolic pH because of the solubility dependence of aluminum on pH. Thus, aluminum-induced tonoplast [H.sup.+]-pumps may be an adaptive response to aluminum to maintain pH homeostasis in the cytosol, thus decreasing aluminum toxicity. Progressive vacuolations in the cells of barley roots (Ikeda & Tadano, 1993), in meristematic tissue of oat (Avena sativa) (Marienfeld et al., 1995), and also in tobacco (Nicotiana tabacum) cells (Panda et al., submitted) have been seen under aluminum stress.

X-ray microanalysis has shown localization of aluminum in the peripheral cell walls of oat. The negative charge of the cell wall binds aluminum, followed by precipitation as Al[(OH).sub.3] and aluminum phosphate, which helps to regulate the further entry of aluminum into the vascular cylinder (Marienfeld & Stelzer, 1993). Calcium pectate, present in the apoplast, helps in the initial adsorption of aluminum, and controls its further movement to the cytosol across the plasma membrane. Aluminum causes an increase in pectin content, which helps to traps aluminum, resulting in diminished aluminum toxicity (Le et al., 1994). Callose is rapidly synthesized in the plasma membrane as an early response to aluminum, and then released into the apoplast. Adhesion between the cell wall and plasma membrane via the cytoskeleton may help to channel the aluminum signal from the apoplasm to the symplasm (Horst et al., 1999). Changes in apoplastic aluminum during initial growth of aluminum-tolerant maize was observed (Vazquez et al., 1999). As already mentioned, aluminum affects the cytoskeletal architecture of plant cells. Plant cells require dynamic cytoskeleton-based networks for various cell activities such as differentiation, cell division, and cell-wall biosynthesis (Sivaguru et al., 1999a). Microtubules are closely related to longitudinal cell expansion, and when they are disrupted, lateral expansion may result. The disappearance of cortical microtubules in elongating wheat roots was observed under aluminum stress (Sasaki et al., 1997b). Because the orientation of cellulose microfibrils tends to reflect that of microtubules, disruption of the microtubules causes reduced root growth. A significant increase in tension within the transvascular actin network has been observed in soybean under aluminum stress. The effect of aluminum was confirmed by crosschecking with inhibitors of calmodulin and calmodulin-dependent kinases (Grabski et al., 1998). Aluminum has been found to reorganize the microtubules in the inner cortex, but not in the outer cortex or epidermis of the elongation zone of maize (Blancaflor et al., 1998). In aluminum-sensitive maize cultivars, prominent aluminum-mediated alterations of microtubules and actin microfilaments were found in cells of the distal transition zone (Sivaguru et al., 1999a). Within an hour, aluminum (90 [micro]M) caused a depletion of microtubules in the distal transition zone. However, no such response was seen in elongating cells under aluminum stress. Tissue- and development-specific alterations to the cytoskeleton were accompanied by aluminum-induced plasma membrane depolarization and callose formation in the outer cortical cells of the distal transition zone. After treatment of log-phase tobacco cells for 6 hours, large, faint phragmoplasts and unusually large daughter nuclei were observed. No phragmoplasts or spindle microtubules were seen in metaphasic cells after 24 hours of aluminum treatment, which might block cell division, thus affecting the progression of the cell cycle. With an increase in aluminum concentration, progressive depolymerization of cortical microtubules in log-phase cells was observed, different from stationary-phase cells, where aluminum induced stabilization of the cortical microtubules (Sivaguru et al., 1999b). Minocha et al. (2001) reported toxic effects of aluminum on the growth, viability, and mitochondrial activity of red spruce (Picea rubens) cells, and they also observed changes at the subcellular level. Exposure to aluminum for 24 to 48 hours caused a loss of cell viability, growth inhibition, and a decrease in mitochondrial activity, measured by MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) reduction. A marked increase in soluble protein content occurred in aluminum-treated cells. Energy dispersive X-ray microanalysis of sections of freeze-substituted cells showed the presence of aluminum in dense regions in the cell walls, cytoplasm, plastids, and vacuoles after 48 hours of exposure to aluminum. A 24-hour aluminum treatment caused an increase in vacuolar and total cell volume without a change in nuclear volume. A marked increase in the surface area of Golgi membranes and endoplasmic reticulum was also observed under aluminum treatment. Minocha et al. (2001) conclude from their data that aluminum movement occurred across the plasma membrane without major cellular disruption. However, the mechanism of aluminum entry into cells remains to be elucidated. As with other metals and abiotic stress factors, possible signal transduction pathways of aluminum toxicity in plants have been analyzed. A decrease in inositol triphosphate ([IP.sub.3]), a common second messenger, and an imbalance in [Ca.sup.2+] homeostasis has been observed in aluminum toxicity (Rengel, 1992). Jones and Kochian (1997) found that aluminum inhibited phospholipase C in association with [Ca.sup.2+] signaling. Rengel and Zhang (2003) reported that a disruption of cytosolic [Ca.sup.2+] homeostasis was the primary trigger of aluminum toxicity. The increase in cytosolic [Ca.sup.2+] due to aluminum toxicity arises partly from the aluminum-resistant portion of the flux through depolarization-activated [Ca.sup.2+] channels and from fluxes through [Ca.sup.2+]-permeable nonselective cation channels in the plasma membrane, which are extracellular, and partly from increased cytosolic [Ca.sup.2+] activity that enhances the [Ca.sup.2+] release channels in the tonoplast and endoplasmic reticulum, which is intracellular. One recent report suggests that an imbalance in [Ca.sup.2+] homeostasis arises as a result of an oxidative burst in tobacco BY-2 cells under aluminum stress (Kawano et al., 2003). However, little is known about the signaling pathways of aluminum toxicity and its relationships with cytosolic [Ca.sup.2+] homeostasis.

Microinjection of a dye, lucifer yellow carbohydrazide, into peripheral root cells of aluminum-sensitive wheat (Scout 66) before or after aluminum treatment showed that aluminum-induced root growth inhibition was caused by aluminum-induced blockage of cell-to-cell trafficking via the plasmodesmata. Immunofluorescence combined with immunoelectron microscopy with a monoclonal antibody against callose showed that aluminum-induced callose deposition is responsible for the plasmodesmata blockade, which was further substantiated with the use of an inhibitor of callose synthesis. Aluminum-induced expression of calreticulin and unconventional myosin VIII showed enhanced fluorescence and colocalization with callose deposits. These results showed that the aluminum-induced imbalance in [Ca.sup.2+] homeostasis produces callose, which significantly blocks the plasmodesmata, closing off symplastic traffic (Sivaguru et al., 2000).

Any condition that disrupts the cellular redox homeostasis can be defined as oxidative stress. Oxygen in the atmosphere is mainly utilized as a hydrogen acceptor, yielding water in aerobic organisms, and an inevitable result of mitochondria-, chloroplast-, and plasma membrane-linked electron transport is the univalent reduction of molecular oxygen in plant cells with the resultant production of toxic reactive oxygen species (ROS) (Asada, 1994). Toxic hydrogen peroxide, which is a product of organellar oxidative reactions, can act both as oxidant and reductant. It is the most stable of the ROS and is capable of rapid diffusion across cell membranes (del Rio et al., 1992). ROS include the superoxide radical ([O.sup.-.sub.2]), the hydroxyl radical (x OH), the alkoxyl radical (RO x), hydrogen peroxide ([H.sub.2][O.sub.2]), and singlet oxygen ([sup.1][O.sub.2]). These ROS have the capacity to oxidize cellular components such as lipids, proteins, enzymes, and nucleic acids, leading to cell death (Hagar et al., 1996). The enzymatic sources of ROS are both extracellular and intracellular (Bolwell et al., 2002). Peroxidases and amine oxidases in cell walls, NADPH oxidase in the plasma membrane, intracellular oxidases, and peroxidases in the mitochondria, chloroplasts, peroxisomes, and nuclei are the chief sources of ROS (Laurenzi et al., 2001; del Rio et al., 2002). Highly reactive lipid hydroperoxides are produced nonenzymatically by direct ROS lipid oxidation, and enzymatically by lipoxygenase (Jalloul et al., 2002). Plant cells are well equipped with complex nonenzymatic antioxidants such as ascorbate, glutathione, [alpha]-tocopherol, and carotenoid, and with enzymatic antioxidants such as catalase, ascorbate peroxidase, guaiacol peroxidase, superoxide dismutase (SOD), monodehydroascorbate reductase, dehydroascorbate reductase, glutathione-S-transferase (GST), and glutathione reductase, which help to detoxify the ROS (Scandalios, 1993; Alscher et al., 1997; Panda & Patra, 2000). The imposition of biotic and abiotic stresses can give rise to further increases in ROS levels. Metals, including aluminum, are known to act as catalysts in ROS production and to induce oxidative damage in plants (Dietz et al., 1999; Panda & Patra, 2000; Yamamoto et al., 2002; Panda et al., 2003a).

As early as 1991, Cakmak and Horst (1991) identified aluminum as a cause of lipid peroxidation, affecting antioxidative enzyme activity in soybean root tips. Aluminum ions cause membrane rigidification, which facilitates radical chain reactions mediated by iron and causes lipid peroxidation (Deleers et al., 1986). Oteiza (1994) reported aluminum-enhanced iron-mediated nonenzymatic lipid peroxidation in phospholipids of liposomes. Aluminum increased the iron-mediated loss of plasma membrane integrity, membrane lipid peroxidation, and apoptosis-like cell death in tobacco cells, which have proved to be good model system for aluminum toxicity studies (Ono et al., 1995; Yamamoto et al., 1997; Yamaguchi et al., 1999). A similar result has been observed in soybean cells (Rath & Barz, 2000). Pan et al. (2001) suggested a correlation between ROS production and cell death in root tips of barley under aluminum stress. Long-term treatment of green gram (Vigna radiata) with aluminum resulted in greatly increased levels of peroxide and lipid peroxidation in the leaves (Panda et al., 2003a). A transient increase in the superoxide radical level with high aluminum concentrations was seen in tobacco cells (Kawano et al., 2003). In a whole-root system in pea, aluminum caused enhancement of lipid peroxidation. It has been shown histochemically that aluminum accumulation, lipid peroxidation, and callose production are uniformly distributed over the entire surface of the root apex. However, histochemical analysis of the loss of plasma membrane integrity showed exclusive localization at the periphery of cracks in the root surface, suggesting that the plasma membrane maintains its integrity under aluminum treatment. Studies with the lipophilic antioxidant butylated hydroxyanisole showed that aluminum-caused lipid peroxidation is an early symptom of aluminum toxicity, leading to callose production but not root-growth inhibition (Yamamoto et al., 2001). It has been shown that pea seedlings treated with aluminum in a calcium solution at pH 4.75 produce ROS in the elongating zone of the root apex after only 2 hours of exposure to aluminum, as studied by dihydroethidium staining, which becomes intercalated in the DNA where it emits fluorescence (Yamamoto et al., 2002). Aluminum toxicity is well known to be related to lipid peroxidation (Yamamoto et al., 2002, 2003). Recently, Kobayashi et al. (2004) reported a similar degree of root-growth inhibition, organic acid release, and aluminum accumulation in the aluminum-tolerant pea cultivar Alaska and the aluminum-sensitive cultivar Hyogo, suggesting that aluminum tolerance is not related to organic acid exclusion. An increase in ROS in the root elongation zone was seen in both cultivars, and a strong correlation was obtained between root-growth inhibition and ROS production in time-course experiments. A 20% decrease in root (apex) respiration in the tolerant cultivar, and a 30% inhibition in the sensitive cultivar, was observed under 10 [micro]M aluminum treatment. Though the ATP content in the tolerant pea was double that in the sensitive one without aluminum stress, under aluminum treatment a decrease in the ATP content in the tolerant cultivar, Alaska, was seen, with no change in the ATP content in the sensitive cultivar, Hyogo. In nonphotosynthetic cells, the mitochondrial electron transport system is the major site of ROS production, and experiments were conducted on the effect of aluminum on superoxide and hydrogen peroxide production in isolated mitochondria. The results showed that both the superoxide radical and hydrogen peroxide contents are significantly elevated under aluminum treatment. Further experiments using mitochondrial complex I and II inhibitors showed that both are potential generators of ROS in tobacco cell mitochondria under aluminum treatment (Panda et al., submitted). These results demonstrate that aluminum potentially triggers ROS production via the mitochondria, resulting in growth inhibition and cell death. Similar redox changes accompanied by ROS production, respiration inhibition, callose formation, and growth inhibition have been observed in tobacco cells and the meristematic root tip cells of pea under aluminum treatment (Yamamoto et al., 2002). Experiments with isolated mitochondria of tobacco ceils showed inhibition of coupled respiration (state III), state IV respiration, alternative oxidase pathway capacity, and cytochrome pathway capacity under aluminum treatment. However, mitochondrial ATP did not show much change compared with respiratory inhibition and ROS production (Panda et al., submitted). A novel mechanism of aluminum toxicity that results in programmed cell death via the mitochondria in tobacco cells has been observed. An increase in ROS production in mitochondria under aluminum treatment resulted in the opening of mitochondrial permeability transition pores in isolated mitochondria of log-phase tobacco cells. This was followed by a collapse of mitochondrial transmembrane potential without a simultaneous release of cytochrome c into the cytosol. This result was further confirmed by transmission electron microscopy of mitochondria from control and aluminum-treated cells, which showed a great difference in the volume, with high-amplitude swelling, and the surface architecture of the mitochondria (Fig. 1). Great numbers of swollen mitochondria with many vacuoles, blebbing out of plasma membrane from the cell wall, and preapoptotic nuclear structures were some of the characteristic features of aluminum-treated cells, confirming that aluminum signaling follows the mitochondrial pathway of cell death in tobacco cells (Panda et al., submitted).

[FIGURE 1 OMITTED]

Aluminum Tolerance

PHYSIOLOGICAL AND BIOCHEMICAL

Plants, being immobile, develop specific mechanisms for withstanding stress. For aluminum, two possible mechanisms have been observed: first, exclusion of aluminum from the root apex, not allowing it to enter the symplasm; and second, intracellular tolerance once aluminum is in the symplast (Kochian, 1995). Exclusion of aluminum can be brought about by modification of the rhizospheric environment by formation of a pH gradient, exudation of aluminum-chelating ligands, or immobilization of aluminum in the cell wall itself. As the solubility of aluminum is strongly pH dependent, developing a high rhizospheric pH may help the plant to tolerate aluminum (Taylor & Foy, 1985). Dagenhardt et al. (1998) reported more substantive evidence than had been obtained from earlier experiments, showing a clear increase in pH very near the root tip in aluminum-tolerant Arabidopsis (air-104) by using a vibrating microelectrode. A twofold increase in the net proton efflux was also recorded, which increased the pH by 0.15 units. No similar effect was detected in aluminum-sensitive cultivars. A role for the mucilage coating of root caps in aluminum tolerance has also been proposed (Horst et al., 1982). The kinetics of aluminum binding to mucilage was biphasic, with a rapid phase in the first half hour of exposure. Though a good correlation exists between the mucilage droplet volume and aluminum tolerance, no binding with aluminum was seen with hematoxylin staining. The mucilage may also be a site of accumulation of concentrated organic acid effluxed from the root apex, which subsequently complexes with aluminum, reducing its toxicity. An aluminum-induced mucilage release from the root cap border cells can protect root tips from aluminum-induced cellular damage (Miyasaka & Hawes, 2001). The aluminum concentration that triggers the release appears to depend upon the genetics and controls of organic acid secretion (Kochian et al., 2004; Kinraide et al., 2005).

The complexing ability of organic acids with aluminum is well known. The first evidence for this came from snapbean (Phaseolus vulgaris), in which eightfold more citric acid effluxed from aluminum-tolerant cultivars than from aluminum-sensitive cultivars (Miyasaka et al., 1991). Delhaize et al. (1993) reported that in wheat the release of malate, encoded by alt1 locus, from the root apex conferred aluminum tolerance. A very specific efflux of malate in response to aluminum, protection of sensitive wheat from aluminum toxicity by adding malate to a nutrient solution, and association of a high malate efflux with the alt1 locus in populations exhibiting aluminum tolerance are some of the experimental findings that support malate's function in aluminum tolerance. It has been further shown in near-isogenic lines of wheat that aluminum activates malate release within minutes, and that the malate is localized within the first few millimeters of the root apex in aluminum-tolerant near-isogenic wheat (Ryan et al., 1995a, 1995b). Since these initial experiments, a correlation has been shown in a number of plant species between organic acid release and aluminum tolerance. A similar association of aluminum tolerance with malate secretion has been reported in Arabidopsis (Hoekenga et al., 2003). In all cases, a dose-dependent and exogenous supply of aluminum activates the release of carboxylate organic acids, which complex with the aluminum, and the aluminum-organic acid complex cannot be transported into the symplasm (Ma et al., 1997a; Pineros et al., 2002; Ma & Furukawa, 2003). In some cases, overexpression of genes encoding enzymes for organic acid synthesis has also proved to enhance aluminum tolerance (Tesfaye et al., 2001). Electrophysiological experiments with maize and wheat root tip protoplasts have revealed an aluminum-gated anion channel for carboxylate transport (Zhang et al., 2001; Pineros et al., 2002). Questions remain as to whether organic acid secretion activated by aluminum is inducible at the gene level. In species such as wheat, a rapid and consistent malate efflux has been recorded, whereas in species such as rye (Secale cereale), triticale (Triticale hexaploide), and Cassia sp., an increase in malate exudation occurs after a lag in 12- to 24-h aluminum treatment. In one model, aluminum triggers the opening of a malate-permeable channel by changing its conformation, accounting for the activated malate efflux in wheat, and then the aluminum interacts with a membrane receptor, which subsequently transduces the signal through a series of secondary messages, allowing the aluminum to enter the cytosol (Delhaize & Ryan, 1995). Ma et al. (1997a) obtained insight into the role of organic acids in intra- and extracellular aluminum tolerance. In Hydrangea sp., of the total aluminum uptake, about 77% was in the cell sap. A molecular ratio of 1:1 between aluminum and the citrate ligand in this case was determined by [sup.27]Al-nuclear magnetic resonance spectroscopy. In aluminum-tolerant Cassia tora, secretion of citric acid was low during the initial 4h of exposure. Buckwheat (Fagopyrum esculentum) with high aluminum tolerance effluxed oxalic acid after aluminum exposure, and the absorbed aluminum exists as an aluminum:oxalate (1:3) complex, which is completely detoxified in the roots and leaves (Ma et al., 1997c). The organic acids are possibly secreted to the outside via ion channels, which are the ion transporters. Anion channels activated by aluminum have been identified in patch-clamp studies with aluminum-resistant wheat root-tip protoplasts (Zhang et al., 2001) and in maize (Pineros & Kochian, 2001; Pineros et al., 2002), suggesting that these anion channels are involved in aluminum resistance. From the analysis of root tips, membrane patches, and whole cells, a putative mechanism has emerged by which aluminum may activate a plasma membrane-bound anion channel. Aluminum might directly bind and then activate a membrane protein or an associated receptor, or it might indirectly activate the channel via cytosolic components. The two most important families of channel proteins are the chloride channel family and a subset of the ATP-binding cassette (ABC) protein superfamily. In yeast (Saccharomyces cerevisiae), Pdr12, an ABC protein, assists the carboxylate efflux. Some circumstantial evidence suggests that the carboxylate transporter involved in aluminum resistance may be an ABC transporter. Guard cell plasma membranes containing slow anion channels seem to have several similarities with anion channels in aluminum-resistant wheat and maize, and both are inhibited by the ABC transporter antagonist diphenylamine-2-carboxylic acid. Recently, Sasaki et al. (2004) reported the cloning of a wheat gene, ALMT1 (aluminum-activated malate transporter), which encodes a membrane protein that is constitutively expressed in the root apices of aluminum-tolerant wheat lines. Heterologous expression of ALMT1 in Xenopus oocytes, rice (Oryza sativa), and cultured tobacco cells showed an aluminum-activated malate efflux. These findings open up a path for cloning of the ALMT1 gene, which can be regarded as the first identified major aluminum-resistance gene, into aluminum-sensitive crops, which will increase their productivity in acid soils. In species in which a gradual increase in organic acid efflux is observed, it is possible that aluminum-resistance genes are being induced, but the mechanism is not known. Possible mechanisms include an abundance of a membrane-bound carboxylate transporter, or an increase in activity of enzymes involved in organic acid synthesis (however, no correlation between organic acid efflux and increased enzyme activity has been found), or better internal compartmentation of organic acids, so that the maximum concentration of organic acids is available for effective transport (Hayes & Ma, 2003). Though in many cases organic acid efflux and aluminum resistance are correlated, no such correlation was observed in rye, suggesting that in some plants other intracellular mechanisms operate to induce aluminum tolerance. The use of confocal microscopy and other microanalytical tools may help us achieve better understanding of the probable mechanisms of tolerance conferred by organic acids and how efflux amounts vary in response to aluminum treatments of different duration. Osawa and Matsumoto (2001) proposed that protein phosphorylation may have a role in aluminum-induced malate efflux from the root apex of wheat. An aluminum-tolerant wheat cultivar (Atlas) showed a malate efflux after 5 minutes of aluminum treatment. K-252a, a protein kinase inhibitor effectively blocked the aluminum-induced malate efflux, resulting in a high aluminum accumulation and root growth inhibition. Transient activation of a 48-kDa protein kinase and irreversible repression of a 42-kDa protein kinase were observed preceding the beginning of the malate efflux, and K-252a exhibited an antagonistic effect. Though a decrease in other organic anions was observed, no changes in inorganic anions such as chloride, nitrate, or phosphate were seen. Rama Devi et al. (2003) reported an intracellular mechanism of aluminum tolerance in tobacco cells, which showed a high antioxidant status in an aluminum-tolerant line under aluminum treatment. ROS production in a sensitive cell line (SL) was very high compared with that in an aluminum-tolerant line, ALT301, under a 24-h aluminum treatment (Yamamoto et al., 2002). The rate of citrate efflux was similar, however, in both cell lines. The rate of MnSOD gene expression was significantly higher in SL than in ALT301, whereas the MnSOD activity enhancement remained similar, suggesting the exclusion of a possible role of organic acid and MnSOD in the aluminum tolerance mechanism of ALT301. Higher amounts of ascorbate and glutathione were observed in ALT301 than in SL during normal growth. Cross-tolerance to other oxidants such as [H.sup.2][O.sub.2], [Fe.sup.2+], and [Cu.sup.2+] was seen in ALT301, which maintained a lower peroxide content along with the higher amounts of ascorbate and glutathione. During post-aluminum treatment growth, lipid peroxidation was very high in SL compared with that in ALT301. The high antioxidant status may be responsible for the aluminum tolerance in ALT301 by protecting the cells from oxidative damage under aluminum and other oxidative stress. Darko et al. (2004) developed aluminum-sensitive and aluminum-tolerant wheat by in vitro microspore selection and showed better root growth, low aluminum accumulation, and less ROS in the aluminum-tolerant wheat. ROS production was observed in the root elongation zone, whereas aluminum accumulated in the root apex. SOD, ascorbate peroxidase, catalase, and GST activities were induced. Among these, catalase and GST have been suggested to have an antioxidant function in aluminum-tolerant wheat.

Molecular Genetics of Aluminum Toxicity and Tolerance

Most molecular genetics research on aluminum stress focuses on development of aluminum-resistant cultivars that will show greater crop yield in acid soils; the preferred species include rice, wheat, and maize. Unlike wheat, both rice and maize show a quantitative inheritance pattern of aluminum tolerance. The goal of molecular genetics research on aluminum stress is to discover more aluminum-resistance genes by using a modern genomics approach in Arabidopsis and in important dietary crops. In the most exhaustively studied species, wheat, aluminum tolerance has been found to be regulated by a single dominant locus, and in some crosses, two loci have been identified (Garvin & Carver, 2003). Some additional loci have also been inferred from chromosomal mutation analyses.

In earlier experiments done in wheat (Ryan et al., 1995a), a strong correlation was shown between relative root length and the activated release of malate. Recently, Sasaki et al. (2004), working in wheat, isolated, characterized, and cloned for the first time an aluminum-tolerance gene, ALMT1, which encodes an aluminum-activated malate transporter. ALMTI-1 expression is associated with aluminum tolerance in wheat, and cultured tobacco cells overexpressing this gene also show an increase in aluminum tolerance, which suggests that ALMT1-1 is a strong candidate for the Alt1 gene of wheat. Two alleles of ALMT1 are found in wheat (ALMT1-1 and ALMT1-2), and expression of these alleles in Xenopus oocytes and cultured tobacco cells showed that both products are malate transporters, with ALMT1-1 being more effective. However, in a moderately aluminum-tolerant wheat, Chinese Spring, a high level of ALMT1-2 expression was observed. These results show that the relative greater aluminum tolerance conferred by ALMT1 in different wheat cultivars is not determined by the two amino acids difference between the two alleles but primarily relates to the expression level. From previous physiological experiments and the present results, it can be inferred that ALMT1 may be the first member of a new family of plant anion channels, or it may encode for a receptor that can activate a malate transporter protein. In an aluminum-tolerant maize line that exhibits aluminum-activated root citrate release, aluminum activated an anion channel that mediates a [Cl.sup.-] efflux in root tip protoplasts (Pineros et al., 2002).

Aluminum-tolerance genes in the moderately tolerant wheat Chinese Spring are located in chromosome arms 6AL, 7AS, 2DL, 3DL, 4DL, and 4BL and in chromosome 7D. In self-incompatible rye, the long arm of chromosome 4 contains a major aluminum-resistance locus called Alt3 (Gallego & Benito, 1997). On the short arm of chromosome 6, a second locus, Alt1, has been mapped. In barley, a major aluminum-resistance locus, Alp, has been found on the long arm of chromosome 4 (Minella & Sorrells, 1992). Rye, barley, and sorghum (Sorghum bicolor), like wheat, have an inheritance pattern with a single locus explaining the genotypic differences. The aluminum-resistance mechanisms of rice and maize are different from those in Triticeae species, which are inducible and whose manifestation requires more time (Magalhaes, 2002). In rice, a locus called Rice 1 has been found to be responsible for aluminum tolerance and is in a region homologous to that of sorghum linkage group G, which contains [Alt.sub.SB] (Nguyen et al., 2003). In studies of various parental rice varieties, 'indica' parents have been shown to have aluminum-sensitive alleles (Nguyen et al., 2003). Though some researchers consider aluminum tolerance to be a qualitative trait, most reports suggest that it is a quantitative trait. A single quantitative trait locus (QTL) mapping data set is available for maize, which shows five genomic regions related to aluminum tolerance (Ninamango-Cardenas et al., 2003). With the advancement of maize genomics, more aluminum-responsive QTLs will be identified in the future. In studies with Arabidopsis thaliana (Landsberg erecta x Columbia RIL mapping population), the principal QTL, found at the top of chromosome 1, explained at least 30% of the variance (Kobayashi & Koyama, 2002; Hoekenga et al., 2003).

A number of genes have been found to be induced by aluminum treatment. Richards et al. (1994) cloned seven genes induced by aluminum in wheat roots. The highly induced genes included genes encoding a metallothionein-like protein and two Bowman-Birk protease inhibitors. An acidic pathogenesis-related (PR) protein, PR-2 was found to be induced in wheat not only by aluminum but also by a wide range of other stresses (Cruz-Ortega & Ownby, 1993). A second PR protein, [beta]-glucanase, was also shown to be induced in wheat (Cruz-Ortega et al., 1997). De la Fuente et al. (1997) produced transgenic tobacco and papaya (Carica papaya) carrying the citrate synthase (CS) gene from Pseudomonas aeruginosa with the 35S CaMV promoter. Transgenic plants containing the CS gene exuded more citrate into the rhizosphere under aluminum stress than wild-type plants, and perhaps the protection from aluminum toxicity resulted from the chelation of aluminum with citrate. This efflux of citrate in transgenic plants would be more beneficial if it were regulated in response to aluminum exposure. Ezaki et al. (1995, 1996) identified three genes in tobacco cell cultures induced by a combination of aluminum and iron: the anionic peroxidase gene and the auxin-induced genes parA and parB. Richards et al. (1998) constructed a cDNA library from A rabidopsis thaliana treated for 2 hours with aluminum and found five cDNA clones that showed transient induction of mRNA, four cDNA clones that showed a longer induction period, and two in which mRNA was downregulated. The expression level of the four long-term-induced genes remained elevated for 48 hours; these genes encode for peroxidase, GST, blue copper-binding protein, and oxygen oxidoreductase, which is a protein homologous to reticulin. The gene for the oxidative stress protein SOD and that for the Bowman-Birk protease inhibitor were also induced by aluminum in Arabidopsis thaliana. Because most of the genes induced by aluminum are also induced by oxidative stress, it could be concluded that aluminum induces oxidative stress. To study the role of aluminum stress-induced genes, Ezaki et al. (2000) derived nine genes from Arabidopsis, tobacco, wheat, and yeast and expressed them in the Arabidopsis ecotype Landsberg erecta. A normal phenotype was observed in lines containing eight of these genes tested by using root elongation assays for their sensitivity to aluminum, other metals, and oxidative stress. The tobacco GST (parB) gene, the Arabidopsis blue copper-binding protein gene (AtBCB), tobacco peroxidase gene (NtPox), and a tobacco guanosine diphosphate-dissociation inhibitor gene (NtGDI1) conferred a degree of resistance to aluminum. Aluminum content in the root tips was also found to be reduced in four aluminum-resistant plant lines compared with the wild type. Reduced staining of roots with 2',7'-dichlorofluorescein diacetate ([H.sub.2]DCFDA), an indicator of oxidative stress, was also observed. These results suggest that aluminum-induced genes can ameliorate aluminum toxicity and that there is a link between aluminum stress and oxidative stress in plants. Ezaki et al. (2001) studied the mechanism of action of four transgenes (AtBCB, parB, NtPox, and NtGDI1) that conferred aluminum resistance in transgenic Arabidopsis. All of the transgenic lines showed lower callose deposition in response to aluminum stress compared with the wild type, suggesting the ameliorative functions of these four genes against aluminum toxicity. Aluminum influx and efflux experiments showed that the AtBCB gene may suppress aluminum absorption, whereas the NtGDI1 gene promotes the release of aluminum in the root tip of Arabidopsis. Aluminum stress increased significantly GST and peroxidase activities in transgenic parB and NtPox plants compared with in the wild-type Landsberg erecta ecotype of Arabidopsis. A decrease in lipid peroxidation was seen in these two transgenic lines under aluminum stress, which suggested that amelioration of oxidative stress may be possible with overexpression of these genes. Repression of cell death was also observed in the NtPox line. An [F.sub.1] hybrid analysis of these transgenic lines suggests that more resistant transgenics might result from the combination of these four genes. Basu et al. (2001) overexpressed MnSOD in Canola (Brassica napus) and found a modest aluminum resistance. Felix et al. (2001) and the Sugarcane Expressed Sequence Tag project generated around 50,000 genes from several tissues and confirmed the hypothesis that sugarcane (Saccharum spp.) microarrays can be successfully used to identify aluminum-induced genes in maize. Schultz et al. (2002) showed that aluminum treatment differentially affected members of the cell wall arabinogalactan protein family, though the exact role of this protein on cell-wall architecture is not known. Watt (2003) used suppression subtractive hybridization (SSH) technology to study aluminum-induced gene expression in sugarcane. A 43% inhibition of root growth was seen in hydroponically growing the sugarcane hybrid N19 challenged with 221 [micro]M aluminum. Database comparison revealed that a subset of 50 cDNAs are upregulated in root tips under aluminum stress: 14 cDNAs are involved in signaling and the regulation of gene expression, and 28 are of unknown function. All of the 50 cDNAs sequenced showed significant similarity to uncharacterized plant expressed sequence tags, and approximately 23 showed similarity to expressed sequence tags from other graminaceous crop species subjected to various types of stress. By using SSH, the characteristics of the genes expressed under aluminum stress could be identified, which will make it possible to further manipulate them in the future to develop aluminum-tolerant crops. In a recent work on aluminum-resistance genes in soybean, differential gene expression pattern between aluminum-stressed and nonstressed tolerant and sensitive cultivars was studied. Enhanced expression of phosphoenolpyruvate carboxylase in roots of aluminum-tolerant cultivars was observed and found to be related to mechanisms of aluminum stress. Additionally, two novel full-length cDNA sequences, homologous to translationally controlled tumor protein and inosine-5'-monophosphate dehydrogenase (IMPDH), with enhanced expression in roots of aluminum-tolerant soybean cultivars under aluminum stress were characterized. Compared with the wild type, transgenic plants showed less aluminum penetration. Numerous lateral roots with low callose accumulation formed in the transgenic plants under aluminum stress, which showed the role of the IMPDH homolog in conferring aluminum tolerance to the transgenic plants (Ermolayev et al., 2003). In Arabidopsis, aluminum-induced organ-specific expression of a cell wall-associated receptor kinasel (WAK1) gene was reported by Sivaguru et al. (2003). A short- and long-term analysis of gene expression in root showed a typical "on" and "off" pattern and also defined WAK1 to be a typical early aluminum-induced gene. However, in shoots, stable WAK1 gene expression was seen. Aluminum-induced closure of stomata was marked, suggesting root-shoot aluminum signaling. A high level of WAK1 protein in root cells showed a lag between aluminum-induced transcription and translation. In the peripheries of cortical cells in the root elongation zone, an abundance of WAK protein and disintegration of microtubules were revealed through immunolocalization and confocal laser scanning microscopy under aluminum treatment. Evidence for the accumulation of WAK proteins in plasma membrane domains was also found. Overexpression of WAK1 showed more aluminum tolerance, making it a suitable candidate gene for aluminum tolerance. Modulation of citrate metabolism by overexpression of mitochondrial citrate synthase (CS) in yeast and Canola showed tolerance to aluminum (Anoop et al., 2003). Overexpressing Arabidopsis mitochondrial CS in Canola via Agrobacterium tumefaciens showed high CS activity in transgenic lines with better root growth showing aluminum tolerance. When exposed to a 150 [micro]M of aluminum, a twofold increase in citrate exudation was observed. Anoop et al. (2003) suggested that modulation of different enzymes involved in citrate synthesis and turnover could be utilized for gene manipulation to produce aluminum tolerance in crops in which citrate metabolism plays a role. The mechanism of expression of two GST genes in Arabidopsis, AtGST1 and AtGST11, under aluminum stress was recently elucidated by Ezaki et al. (2004). In their experiments, an approximately 1-kb DNA fragment of the 5'-upstream region of each gene was fused to a [beta]-glucuronidase (GUS) reporter gene and put into the Arabidopsis ecotype Landsberg erecta. Time-dependent gene expression of varying degree was seen in the root and leaf under aluminum stress in the transgenics. Short-term aluminum treatment resulted in the expression of the pAtGSTI::GUS gene, whereas pAtGST11::GUS was expressed only after longer exposure. Possible signaling was suggested between root and shoot, which was supported by GUS staining in adult transgenic line carrying the pAtGSTI::GUS gene. Enhancement of pAtGST11::GUS expression was seen in shoots under aluminum stress, along with calcium depletion. A common response of increased GUS activity was observed in the transgenic lines under aluminum stress, cold stress, metal toxicity, and oxidative stress.

Remarks on the Future and Conclusions

Acid soils threaten crop productivity of almost 40% of the arable land of the world. Much information has been gathered on the mechanisms of aluminum toxicity and tolerance. The toxic effects of aluminum begin in plant roots within minutes of exposure and include root growth inhibition, callose accumulation, cytoskeletal damage, plasma membrane rigidification, alterations of the membrane surface charge, membrane lipid peroxidation, imbalance in [Ca.sup.2+] homeostasis, induction of oxidative stress in plant mitochondria, opening of mitochondrial membrane permeability transition pores causing high-amplitude swelling of mitochondria, collapse of inner membrane potential, and several other bioenergetic alterations resulting in cell death.

Many questions remain to be answered about the possible signaling of aluminum across the plasma membrane and how, without the release of cytochrome c intracellularly, cell death ultimately occurs. The appearance of numerous vacuoles under aluminum toxicity, observed by transmission electron microscopy, suggest that a possible role of vacuoles in accomplishing cell death.

With regard to aluminum tolerance, experimental results suggest that various mechanisms involving extracellular and intracellular carboxylate ion production help sequester and detoxify aluminum. Many oxidative stress and other metabolically significant genes that have been found to be induced in response to aluminum confer some degree of tolerance to aluminum stress in various other plants in which these genes are overexpressed. There is still some question, however, as to why different plants exude different kinds of organic acids and what the signaling mechanism is that is involved in conferring tolerance via organic acids. However, the research on aluminum toxicity and tolerance at physiological, biochemical, and molecular levels has helped us better understand this complicated phenomenon and has also opened up new areas of research. For example, the identification of more constitutive and also inducible candidate genes that can confer aluminum resistance on crop plants grown in acid soils might rescue large populations from food insecurity in the future. Although we have come a long way in aluminum research, the famous lines, "And miles to go before I sleep, And miles to go before I sleep," penned by Robert Frost, remind us to continue our quest to explicate the mechanisms of aluminum stress.

Acknowledgement

The Japan Society for Promotion of Science (JSPS) is duly acknowledged for providing a postdoctoral fellowship to Dr. S. K. Panda

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SANJIB KUMAR PANDA

Plant Biochemistry and Molecular Biology Laboratory, Department of Life Science, Assam (Central) University, Silchar-788011, Assam, India

AND

HIDEAKI MATSUMOTO

Research Institute for Bioresources, Okayama University, Kurashiki 710 0046, Japan
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