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2001 | 48 | 3 | 673-686
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Effect of aluminium on plant growth and metabolism.

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Aluminium toxicity is one of the major factors that limit plant growth and development in many acid soils. Root cells plasma membrane, particularly of the root apex, seems to be a major target of Al toxicity. However, strong interaction of Al3+, the main Al toxic form, with oxygen donor ligands (proteins, nucleic acids, polysaccharides) results in the inhibition of cell division, cell extension, and transport. Although the identification of Al tolerance genes is under way, the mechanism of their expression remains obscure.Soil chemical factors that limit root growth in acid soils, diminish crop production, include Al, Mn and various cations, and also deficiency or unavailability of Ca, Mg, P, Mo, and Si. These effects are further complicated by interactions of Al with other ions in different plant genotypes and under stress conditions (Foy, 1992). Cytotoxicity of Al has been well documented in plants (Delhaize & Ryan, 1995; Horst et al., 1999; Kollmeier et al., 2000; Marienfeld et al., 2000). It is generally known that plants grown in acid soils due to Al solubility at low pH have reduced root systems and exhibit a variety of nutrient-deficiency symptoms, with a consequent decrease in yield. In many countries with naturally acid soils, which constitute about 40% of world arable soil (LeNoble et al., 1996), Al toxicity is a major agricultural problem, and is intensively studied in plant systems.The effects of aluminium on plant growth, crop yield, uptake and nutrients distribution in vegetative and reproductive parts are still not fully understood. This review discusses recent information on aluminium toxicity with an emphasis on plant response to Al stress.

Physical description
  • Department of Biochemistry, Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University of Poznań, Poznań, Poland
  • Aniol, A. (1995) Physiological aspects of aluminum tolerance associated with long arm of chromosome 2D of the wheat (Triticum aestivum L.) genome. Theor. Appl. Genet. 91, 510-516.
  • Aniol, A. & Gustafson, J.P. (1984) Chromosome location of genes controlling aluminum tolerance in wheat, rye and triticale. Can. J. Genet. Cytol. 26, 701-705.
  • Baker, A.J.M., McGrath, S.P., Reeves, R.D. & Smith, J.A.C. (2000) Metal hyperaccumulator plants: A review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils; in Phytoremediation of Contaminated Soil and Water (Terry, N. & Banuelos, G., eds.) pp. 85-107, Lewis Publisher, Boca Raton.
  • Basu, U., Good, A.G., Aung, T., Slaski, J.J., Basu, A., Briggs, K.G. & Taylor, G.J. (1999) A 23-kDa, root exudate polypeptide co-segregates with aluminum resistance in Triticum aestivum. Physiol. Plant. 106, 53-61
  • Bianchi-Hall, C.M., Carter, T.E., Rufty, T.W., Arellano, C., Boerma, H.R., Ashley, D.A. & Burton, J.W. (1998) Heritability and resource allocation of aluminum tolerance derived from soybean PI 416937. Crop Sci. 38, 513-522.
  • Blancaflor, E.B., Jones, D.L. & Gilroy, S. (1998) Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol. 118, 159-172.
  • Chang, Y.-C., Yamamoto, Y. & Matsumoto, H. (1999) Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron. Plant Cell Environ. 22, 1009-1017.
  • Cobbet, C.S. (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 123, 825-832.
  • Cocker, K.M., Evans, D.E. & Hodson, M.J. (1998) The amelioration of aluminium toxicity by silicon in higher plants: Solution chemistry or an in planta mechanism? Physiol. Plant. 104, 608-614.
  • Crawford, S.A. & Wilkens, S. (1997) Ultrastructural changes in root cap cells of two Australian native grass species following exposure to aluminum. Aust. J. Plant Physiol. 24, 165-174.
  • Cruz-Ortega, R. & Ownby, J.D. (1993) A protein similar to PR (pathogenesis related) proteins is elicited by metal toxicity in wheat roots. Physiol. Plant. 89, 211-219.
  • Degenhardt, J., Larsen, P.B., Howell, S.H. & Kochian, L.V. (1998) Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiol. 117, 19-27.
  • de la Fuente, J.M., Ramirez-Rodriguez, V., Cabrera-Ponce, J.L. & Herrera-Estrella, L. (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthase. Science 276, 1566-1568.
  • Delhaize, E. & Ryan, P.R. (1995) Aluminum toxicity and tolerance in plants. Plant Physiol. 107, 315-321.
  • Delhaize, E., Hebb, D.M., Richards, K.D., Lin, J.M., Ryan, P.R. & Gardner, R.C. (1999) Cloning and expression of a wheat (Triticum aestivum L.) phosphatidylserine synthase cDNA: Overexpression in plants alters the composition of phospholipids. J. Biol. Chem. 274, 7082-7088.
  • Ezaki, B., Koyanagi, M., Gardner, R.C. & Matsumoto, H. (1997) Nucleotide sequence of a cDNA for GDP dissociation inhibitor (GDI) which is induced by aluminum (Al) ion stress in tobacco cell culture (accession no. AF012823) (PGR 97-133). Plant Physiol. 115, 314.
  • Ezaki, B., Sivaguru, M., Ezaki, Y., Matsumoto, H. & Gardner, R.C. (1999) Acquisition of aluminum tolerance in Saccharomyces cerevisiae by expression of the BCB or NtGDI1 gene derived from plants. FEMS Microbiol. Lett. 171, 81-87.
  • Ezaki, B., Gardner, R.C., Ezaki, Y. & Matsumoto, H. (2000) Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol. 122, 657-665.
  • Foy, C.D. (1988) Plant adaptation to acid, aluminum-toxic soils. Commun. Soil Sci. Plant Anal. 19, 959-987.
  • Foy, C.D. (1992) Soil chemical factors limiting plant root growth. Adv. Soil Sci. 19, 97-149.
  • Gallego, F.J. & Benito, C. (1997) Genetic control of aluminium tolerance in rye (Secale cereale L.). Theor. Appl. Genet. 95, 393-399.
  • Gallego, F.J., Lopez-Solanilla, Figueiras, A.M. & Benito, C. (1998) Chromosomal location of PCR fragments as a source of DNA markers linked to aluminium tolerance genes in rye. Theor. Appl. Genet. 96, 426-434.
  • Grabski, S., Arnoys, E., Bush, B. & Schindler, M. (1998) Regulation of actin tension in plant cells by kinases and phosphatases. Plant Physiol. 116, 279-290.
  • Gunsé, B., Poschenrieder, Ch. & Barceló, J. (1997) Water transport properties of roots and root cortical cells in proton- and Al-stressed maize varieties. Plant Physiol. 113, 595-602.
  • Hamilton, C.A., Good, A.G. & Taylor, G.J. (2001) Induction of vacuolar ATPase and mitochondrial ATP synthase by aluminum in an aluminum-resistant cultivar of wheat. Plant Physiol. 125, 2068-2077.
  • Hare, P.D. & Cress, W.A. (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 21, 79-102.
  • Horst, W.J. (1995) The role of the apoplast in aluminum toxicity and resistance of higher plants: A review. Z. Pflanzenernaehr Bodenkd. 158, 419-428.
  • Horst, W.J., Püschel, A.-K. & Schmohl, N. (1997) Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant Soil 192, 23-30.
  • Horst, W.J. Schmohl, N., Kollmeier, M., Baluska, F. & Sivaguru, M. (1999) Does aluminium inhibit root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant Soil 215, 163-174.
  • Huang, J.W., Pellet, D.M., Papernik, L.A. & Kochian, L.V. (1996) Aluminum interactions with voltage-dependent calcium transport on plasma membrane vesicles isolated from roots of aluminum-sensitive and -resistance wheat cultivars. Plant Physiol. 110, 561-569.
  • Hue, N.V., Croddock, G.R. & Adams, F. (1986) Effect of organic acids on Al toxicity in subsoils. Soil Sci. Soc. Am. J. 50, 28-34.
  • Jones, D.L., Kochian, L.V. & Gilroy, S. (1998) Aluminum induces a decrease in cytosolic calcium concentration in BY-2 tobacco cell cultures. Plant Physiol. 116, 81-89.
  • Kinraide, T.B. (1997) Reconsidering the rhizotoxicity of hydroxyl, sulphate, and fluoride complexes of aluminum. J. Exp. Bot. 48, 1115-1124.
  • Knight, H. & Knight, M.R. (2001) Abiotic stress signaling pathways: Specificity and cross-talk. Trends Plant Sci. 6, 262-267.
  • Kochian, L.V. (1995) Cellular mechanism of aluminum toxicity and resistance in plants. Annu. Rev. Plant Physiol. Mol. Biol. 46, 237-260.
  • Kollmeier, M., Felle, H.H. & Horst, W.J. (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduce basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol. 122, 945-956.
  • Larsen, P.B., Tai, C.Y., Kochian, L.V. & Howell, S.H. (1996) Arabidopsis mutants with increased sensitivity to aluminum. Plant Physiol. 110, 743-751.
  • Larsen, P.B., Degenhard, J., Tai, C., Stenzler, L.M., Howell, S.H. & Kochian, L.V. (1998) Aluminum-resistance Arabidopsis mutants that exhibit altered pattern of aluminum accumulation and organic acid release from roots. Plant Physiol. 117, 9-18.
  • Lazof, D.B., Goldsmith, J.G., Rufty, T.W. & Linton, R.W. (1994) Rapid uptake of aluminum into cells of intact soybean root tips. A microanalytical study using secondary ion mass spectroscopy. Plant Physiol. 106, 1107-1114.
  • LeNoble, M.E., Blevins, D.G., Sharp, R.E. & Cumbie, B.G. (1996) Prevention of aluminium toxicity with supplemental boron. I. Maintenance of root elongation and cellular structure. Plant. Cell Environ. 19, 1132-1142.
  • Li, K.F., Ma, J.F. & Matsumoto, H. (2000) Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol. 123, 1537-1543.
  • Ligterink, W. & Hirt, H. (2001) Mitogen-activated protein (MAP) kinase pathways in plants: Versatile signalling tools. Int. Rev. Cytol. 201, 209-275.
  • Little, R. (1988) Plant soil interaction at low pH: Problem solving genetic approach. Commun. Soil Sci. Plant Anal. 19, 1239-1257.
  • Lorenc-Plucińska, G. & Ziegler, H. (1996) Changes in ATP levels in Scots pine needles during aluminium stress. Photosynthetica 32, 141-144.
  • Lukaszewski, K.M. & Blevins, D.G. (1996) Root growth inhibition in boron-deficient in aluminum stressed squash may be a result of impaired ascorbate metabolism. Plant Physiol. 112, 1135-1140.
  • Ma, J.F. (2000) Role of organic acids on detoxification of aluminum in higher platns. Plant Cell Physiol. 41, 383-390.
  • Ma, J.F., Zheng, S.J., Matsumoto, H. & Hiradate, S. (1997a) Detoxifying aluminum with buckwheat. Nature 390, 569-570.
  • Ma, J.F., Hiradate, S., Nomoto, K., Iwoshita, T. & Matsumoto, H. (1997b) Internal detoxification mechanism of Al in hydrangea: Identification of Al forms in the root apices. Plant Physiol. 113, 1033-1039.
  • Ma, J.F., Taketa, S. & Yang, Z.M. (2000) Aluminum tolerance genes on the short arm of chromosome 3R are linked to organic acid release in triticale. Plant Physiol. 122, 687-694.
  • Ma, X.-F., Ross, K. & Gustafson, J.P. (2001) Physical mapping of restriction fragment length polymorphism (RFLP) markers in homoeologous groups 1 and 3 chromosomes of wheat by in situ hybridization. Genome 44, 401-412.
  • Marienfeld, S., Schmohl, N., Klein, M., Schröder, W.H., Kuhn, A.J. & Horst, W.J. (2000) Localisation of aluminium in root tips of Zea mays and Vicia faba. J. Plant Physiol. 156, 666-671.
  • Matsumoto, H. (1991) Biochemical mechanism of the toxicity of aluminum and the sequestration of aluminum in plant cells; in Plant-Soil Interactions at Low pH (Wright, R.J., Baligar, V.C. & Murrmann, R.P., eds.) pp. 825-838, Kluwer Academic Publishers, Dordrecht, Netherlands.
  • Matsumoto, H. (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int. Rev. Cytol. 200, 1-46.
  • Matsumoto, H., Hiraseva, E., Morimura, S. & Takahashi, E. (1976) Localization of aluminum in tea leaves. Plant Cell Physiol. 17, 627-631.
  • May, H.M. & Nordstrom, D.K. (1991) Assessing the solubilities and reaction kinetics of aluminous minerals in soil; in Soil Acidity (Urlich, B. & Sumner, M.E., eds.) pp. 125-148, Springer-Verlag, Berlin.
  • Miller, D., Hable, W., Gottwald, J., Ellard-Ivey, M., Demura, T., Lomax, T. & Carpita, N. (1997) Connections: The hard wiring of the plant cell for perception, signaling and response. Plant Cell 9, 2105-2117.
  • Mossor-Pietraszewska, T., Kwit, M. & Łęgiewicz, M. (1997) The influence of aluminium ions on activity changes of some dehydrogenases and aminotransferases in yellow lupine. Biol. Bull. Poznań 34, 47-48.
  • Nguyen, V.T., Burow, M.D., Nguyen, H.T., Le, B.T., Le, T.D. & Paterson, A.H. (2001) Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor. Appl. Genet. 102, 1002-1010.
  • Nosko, P., Brassard, P., Kramer, J.R. & Kershaw, K.A. (1988) The effect of aluminum on seed germination and early seedling establishment, growth and respiration of white spruce (Picea glauca). Can. J. Bot. 66, 2305-2310.
  • Osawa, H. & Matsumoto, H. (2001) Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex. Plant Physiol. 126, 411-420.
  • Pellet, D.M., Grunes, D.L. & Kochian, L.V. (1995) Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196, 788-795.
  • Pellet, D.M., Papernik, L.A. & Kochian, L.V. (1996) Multiple aluminum-resistance mechanisms in wheat: Roles of root apical phosphate and malate exudation. Plant Physiol. 112, 591-597.
  • Piñeros, M.A. & Kochian, L.V. (2001) A patch- clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al3+-induced anion channels. Plant Physiol. 125, 292-305.
  • Rengel, Z. (1996) Uptake of aluminium by plant cells. New Phytol. 134, 389-406.
  • Rengel, Z. & Robinson, D.L. (1989) Aluminum effects on growth and macronutrient uptake by annual ryegrass. Agron. J. 81, 208-215.
  • Rengel, Z. & Reid, R.J. (1997) Uptake of Al across the plasma membrane of plant cells. Plant Soil 192, 31-35.
  • Richards, K.D., Schott, E.J., Sharma, Y.K., Davis, K.R. & Gardner, R.C. (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol. 116, 409-418.
  • Roy, A.K., Sharma, A. & Talukder, G. (1988) Some aspects of aluminum toxicity in plants. Bot. Rev. 54, 145-177.
  • Ryan, P.R., Delhaize, E. & Randall, P.J. (1995) Characterization of Al-stimulated efflux of malate from apices of Al-tolerant wheat roots. Planta 196, 103-110.
  • Schott, E.J. & Gardner, R.C. (1997) Aluminum- sensitive mutants of Saccharomyces cerevisiae. Mol. Gen. Genet. 254, 63-72.
  • Silva, J.R., Smyth, T.J., Moxley, D.F., Carter, T.E., Allen, N.S. & Rufty, T.W. (2000) Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol. 123, 543-552.
  • Sivaguru, M., Baluška, F., Volkman, D., Felle, H.H. & Horst, W.J. (1999) Impacts of aluminum on the cytoskeleton of the maize root apex. Short-term effects on the distal part of the transition zone. Plant Physiol. 119, 1073- 1082.
  • Sivaguru, M., Fujiwara, T., Šamaj, J., Baluška, F., Yang, Z., Osawa, H., Maeda, T., Mori, T., Volkmann, D. & Matsumoto, H. (2000) Aluminum-induced 1→3-β-D-glucan inhibits cell-to- cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol. 124, 991-1005.
  • Ślaski, J.J., Zhang, G., Basu, U., Stephens, J.L. & Taylor, G.J. (1996) Aluminum resistance in wheat (Triticum aestivum) is associated with rapid Al-induced changes in activities of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase in root apices. Physiol. Plant. 98, 477-484.
  • Snowden, K.C., Richards, K.D. & Gardner, R.C. (1995) Aluminum-induced genes. Introduction of toxic metals, low calcium, and wounding and pattern of expression in root tips. Plant Physiol. 107, 341-348.
  • Somers, D.J., Gustafson, J.P. (1995) The expression of aluminum stress induced polypeptides in a population of wheat (Triticum aestivum L.). Genome 38, 1213-1220.
  • Takabatake, R. & Shimmen, T. (1997) Inhibition of electrogenesis by aluminum in characean cells. Plant Cell Physiol. 38, 1264-1271.
  • Taylor, G.J. (1988) The physiology of aluminum tolerance; in Metals Ions in Biological Systems (Sigel, H., ed.) vol. 24, Aluminum and Its Role in Biology, pp. 165-198, Marcel-Dekker, New York.
  • Taylor, G.J. (1991) Current views of the aluminum stress response; The physiological basis of tolerance. Curr. Top. Plant Biochem. Physiol. 10, 57-93.
  • Taylor, G.J. (1995) Overcoming barriers to understanding the cellular basis of aluminum resistance. Plant Soil 171, 89-103.
  • Taylor, G.J., Blamey, F.P.C. & Edwards, D.G. (1998) Antagonistic and synergistic interactions between aluminum and manganese on growth of Vigna unguiculata at low ionic strenght. Physiol. Plant. 104, 183-194.
  • Taylor, G.J., McDonald-Stephens, J.L., Hunter, D.B., Bertsch, P.M., Elmore, D., Rengel, Z. & Reid, R.J. (2000) Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol. 123, 987-996.
  • Thornton, F.C., Schaedle, M. & Raynal, D.L. (1986) Effect of aluminum on the growth of sugar maple in solution culture. Can. J. For. Res. 16, 892-896.
  • Turnau, K. (1996) Role of arbuscular mycorrhiza in plant resistance to heavy metals. Biol. Bull. Poznań 33 (Suppl.), 65.
  • Wagatsuma, T. & Akiba, R. (1989) Low surface negativity of root protoplasts from aluminum-tolerant plant species. Soil Sci. Plant Nutr. 35, 443-452.
  • Wu, P., Liao, C.Y., Hu, B., Yi, K.K., Jin, W.Z., Ni, J.J. & He, C. (2000) QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor. Appl. Genet. 100, 1295-1303.
  • Xiong, L. & Zhu, J.-K. (2001) Abiotic stress signal trandsuction in plant: Molecular and genetic perspectives. Physiol. Plant. 112, 152-166.
  • Yamamoto, Y., Kobayashi, Y. & Matsumoto, H. (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol. 125, 199-208.
  • Yang, Z.M., Sivaguru, M., Horst, W.J. & Matsumoto, H. (2000) Aluminum tolerance is achieved by exudation of citric acid from roots of soybean (Glycine max L. Merr.). Physiol. Plant. 110, 72-77.
  • Zhang, G., Slaski, J.J., Archambault, D.J. & Taylor, G.J. (1997) Alteration of plasma membrane lipids in aluminum-resistant and aluminum-sensitive wheat genotypes in response to aluminum stress. Physiol. Plant. 99, 302-308.
  • Zhang, W.H. & Rengel, Z. (1999) Aluminum induces an increase in cytoplasmic calcium in intact wheat root apical cells. Aust. J. Plant Physiol. 26, 401-409.
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