Skip to main content
SpringerLink
Log in

Target sites of aluminum phytotoxicity

  • Review
  • Published:
Biologia Plantarum

Abstract

The primary phytotoxic effect of aluminum (Al) is confined to the root apex. It is a matter of debate whether the primary injury of Al toxicity is apoplastic or symplastic. This review paper summarizes our current understanding of the spatial and metabolic sites of Al phytotoxicity. At tissue level, the meristematic, distal transition, and apical elongation zones of the root apex are most sensitive to Al. At cellular and molecular level, many cell components are implicated in Al toxicity including DNA in nucleus, numerous cytoplastic compounds, the plasma membrane, and the cell wall. Although it is difficult to distinguish the primary targets from the secondary effects so far, understanding of the target sites of Al toxicity is helpful for elucidating the mechanisms by which Al exerts its deleterious effects on root growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CaM:

calmodulin

CEC:

cation exchange capacity

cMTs:

cortical microtubules

DTZ:

distal transition zone

EZ:

elongation zone

PIP2 :

phosphatidylinositol-4,5-bisphosphate

PM:

plasma membrane

ROS:

reactive oxygen species

References

  • Ahn, S.J., Sivaguru, M., Chung, G.C., Rengel, Z., Matsumoto, H.: Aluminium-induced growth inhibition is associated with impaired efflux and influx of H+ across the plasma membrane in root apixes of squash (Cucurbita pepo).-J. exp. Bot. 376: 1959–1966, 2002.

    Article  Google Scholar 

  • Ahn, S.J., Sivaguru, M., Osawa, H., Chung, G.C., Matsumoto, H.: Aluminum inhibits the H+-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots.-Plant Physiol. 126: 1381–1390, 2001.

    Article  PubMed  Google Scholar 

  • Akeson, M., Munns, D.N.: Lipid bilayer permeation by neutral aluminum citrate and by three alpha hydroxy carboxylic acids.-Biochem. biophys. Acta 984: 200–206, 1989.

    PubMed  Google Scholar 

  • Akeson, M., Munns, D.N., Burau, R.G.: Adsorption of Al3+ to phosphatidylcholine vesicles.-Biochem. biophys. Acta 986: 33–40, 1989.

    PubMed  Google Scholar 

  • Archambault, D.J., Zhang, G., Taylor, G.J.: Accumulation of Al in root mucilage of an Al-resistant and an Al-sensitive cultivar of wheat.-Plant Physiol. 112: 1471–1478, 1996.

    PubMed  Google Scholar 

  • Basu, A., Basu, U., Taylor, G. J.: Induction of microsomal membrane proteins in roots of an aluminum-resistant cultivar of Triticum aestivum L. under conditions of aluminum stress.-Plant Physiol. 104: 1007–1013, 1994.

    PubMed  Google Scholar 

  • Basu, U., Good, A.G., Taylor, G.J.: Transgenic Brassica napus plants overexpressing aluminium-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminium.-Plant Cell Environ. 24: 1269–1278, 2001.

    Article  Google Scholar 

  • Bennet, R.J., Breen, C.M.: The aluminium signal: new dimensions to mechanisms of aluminium tolerance.-In: Wright, R.J., Baligar, V.C., Murrmann, R.P. (ed.): Plant-Soil Interactions at Low pH. Pp. 703–716. Kluwer Academic Publ., Dordrecht 1991.

    Google Scholar 

  • Berridge, M.J.: Inositol trisphosphate and diacylglycerol: two interacting second messengers.-Ann. Biochem. 56: 159–193, 1987.

    Google Scholar 

  • Blamey, F.P.C.: The role of the root cell wall in aluminum toxicity.-In: Ae, N., Arihara, J., Okada, K., Srinivasan, A. (ed.): Plant Nutritent Acquisition. New Perspectives. Pp. 201–226. Springer-Verlag, Tokyo 2001.

    Google Scholar 

  • Blamey, F.P.C., Dowling, A.J.: Antagonism between aluminium and calcium for sorption by calcium pectate.-Plant Soil 171: 137–140, 1995.

    Article  Google Scholar 

  • Blancaflor, E.B., Jones, D.L., Gilroy, S.: Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize.-Plant Physiol. 118: 159–172, 1998.

    Article  PubMed  Google Scholar 

  • Boscolo, P.R.S., Menossi, M., Jorge, R.A.: Aluminum-induced oxidative stress in maize.-Phytochemistry 62: 181–189, 2003.

    Article  PubMed  Google Scholar 

  • Cakmak, L, Horst, W.J.: Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max).-Physiol. Plant. 83: 463–468, 1991.

    Article  Google Scholar 

  • Ciamporova, M.: Morphological and structure responses of plant roots to aluminium at organ, tissue, and cellular levels.-Biol. Plant. 45: 161–171, 2002.

    Article  Google Scholar 

  • Clarkson, D.T.: The effect of aluminium and some trivalent metal cations on cell division in the root apices of Allium cepa.-Ann. Bot. 29: 309–315, 1965.

    Google Scholar 

  • Cote, G.G., Crain, R.C.: Biochemistry of phosphoinositides.-Annu. Rev. Plant Physiol. Plant mol. Biol. 44: 333–356, 1993.

    Article  Google Scholar 

  • Cruz-Ortega, R., Cushman, J.C., Ownby, J.P.: cDNA clones encoding 1,3-(β-glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots.-Plant Physiol. 114: 1453–1460, 1997.

    Article  PubMed  Google Scholar 

  • Darnowski, D.W., Valenta, R., Parthasarathy, M.V.: Identification and distribution of profilin in tomato (Lycopersicon esculentum Mill.).-Planta 198: 158–161, 1996.

    Article  Google Scholar 

  • De la Fuente, J.M., Herrera-Estrella, L.: Advances in the understanding of aluminum toxicity and the development of aluminum-tolerant transgenic plants.-Adv. Agron. 66: 103–120, 1999.

    Google Scholar 

  • Delhaize, E., Ryan, P.R.: Aluminum toxicity and tolerance in plants.-Plant Physiol. 107: 315–321, 1995.

    PubMed  Google Scholar 

  • Devi, S.R., Yamamoto, Y., Matsumoto, H.: An intracellular mechanism of aluminum tolerance associated with high antioxidant status in cultured tobacco cells.-J. inorg. Biochem. 97: 59–68, 2003.

    Article  PubMed  Google Scholar 

  • Drobak, B.K., Watkins, P.A.C., Valenta, R., Dove, S.K., Lloyd, C.W., Staiger, C.J.: Inhibition of plant plasma membrane phosphoinositide phospholipase C by the actin-binding protein profiling.-Plant J. 6: 389–400, 1994.

    Article  Google Scholar 

  • Ezaki, B., Gardner, R.C., Ezaki, Y, Matsumoto, H.: Expression of aluminum-induced genes in transgenic arabidopsis plants can ameliorate aluminum stress and/or oxidative stress.-Plant Physiol. 122: 657–665, 2000.

    Article  PubMed  Google Scholar 

  • Ezaki, B., Tsugita, S., Matsumoto, H.: Expression of a moderately anionic peroxidase is induced by aluminum treatment in tobacco cells: Possible involvement of peroxidase isozymes in aluminum ion stress.-Physiol. Plant. 96: 21–28, 1996.

    Article  Google Scholar 

  • Ezaki, B., Yamamoto, Y., Matsumoto, H.: Cloning and sequencing of the cDNAs induced by aluminium treatment and Pi starvation in cultured tobacco cells.-Physiol. Plant. 93: 11–18, 1995.

    Article  Google Scholar 

  • Fiskesjo, G.: Occurrence and degeneration of “Al-structure” in root cap cells of Allium cepa L. after Al-treatment.-Hereditas 112: 193–202, 1990.

    Google Scholar 

  • Foy, C.D.: The physiology of plant adaptation to metal stress.-Iowa State J. Res. 57: 355–391, 1983.

    Google Scholar 

  • Grabski, S., Schindler, M.: Aluminum induces rigor within the actin network of soybean cells.-Plant Physiol. 108: 897–901, 1995.

    PubMed  Google Scholar 

  • Gunse, B., Poschenrieder, C., Barcelo, J.: Water transport properties of roots and root cortical cells in proton-and Alstressed maize varieties.-Plant Physiol. 113: 595–602, 1997.

    PubMed  Google Scholar 

  • Hartwell, B.L., Pember, F.R.: The presence of aluminium as a reason for the difference in the effect of so-called acid soil on barley and rye.-Soil Sci. 6: 259–279, 1918.

    Google Scholar 

  • Haug, A., Vitorello, V.: Aluminium coordination to calmodulin: thermodynamic and kinetic aspects.-Coordination Chem. Rev. 149: 113–124, 1996.

    Google Scholar 

  • Horst, W.J.: The role of the apoplast in aluminium toxicity and resistance of higher pants: A review.-Z. Pflanzenernahr. Bodenk. 158: 419–428, 1995.

    Google Scholar 

  • Horst, W.J., Asher, C.J., Cakmak, I., Szulkiewica, P., Wissemeier, A.H.: Short-term responses of soybean roots to Al.-J. Plant Physiol. 140: 174–178, 1992.

    Google Scholar 

  • Horst, W.J., Poschel, A.K., Schmohl, N.: Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize.-Plant Soil 192: 23–30, 1997.

    Article  Google Scholar 

  • Horst, W.J., Schmohl, N., Baluska, F., Sivaguru, M.: Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum?-Plant Soil 215: 163–174, 1999.

    Article  Google Scholar 

  • Horst, W.J., Wanger, A., Marschner, H.: Mucilage protects roots from aluminum injury.-Z. Pflanzenphysiol. 105: 435–444, 1982.

    Google Scholar 

  • Huang, J.W., Grunes, D.L., Kochian, L.V.: Aluminum effects on the kinetics of calcium uptake into cells of the wheat root apex.-Planta 188: 414–421, 1992a.

    Article  Google Scholar 

  • Huang, J.W., Shaff, J.E., Grunes, D.L., Kochian, L.V.: Aluminum effects on calcium fluxes at the root apex of aluminum-tolerant and aluminum-sensitive wheat cultivars.-Plant Physiol. 98: 230–237, 1992b.

    Google Scholar 

  • Huck, M.G.: Impairment of sucrose utilization for cell wall formation in the roots of aluminum-damaged cotton seedlings.-Plant Cell Physiol. 13: 7–14, 1972.

    Google Scholar 

  • Ishikawa, S., Wagatsuma, T.: Plasma membrane permeability of root-tip cells following temporary exposure to Al ions is a rapid measure of Al tolerance among plant species.-Plant Cell Physiol. 39: 516–525, 1998.

    Google Scholar 

  • Ishikawa, S., Wagatsuma, T., Takano, T., Tawaraya, K., Oomata, K.: The plasma membrane intactness of root-tip cell is a primary factor for Al-tolerance in cultivars of five species.-Soil Sci. Plant Nutr. 47: 489–501, 2001.

    Google Scholar 

  • Jones, D.L., Gilroy, S., Larsen, P.B., Howell, S.H., Kochian, L.V.: Effect of aluminum on cytoplasmic Ca2+ homeostasis in root hairs of Arabidopsis thaliana (L.).-Planta 206: 378–387, 1998.

    Article  PubMed  Google Scholar 

  • Jones, D.L., Kochian, L.V.: Aluminium inhibition of the inositol 1,4,5-triphosphate signal transduction pathway in wheat roots: a role in aluminium toxicity?-Plant Cel1 7: 1931–1922, 1995.

    Google Scholar 

  • Jones, D.L., Shaff, J.E., Kochian, L.V.: Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. I. Inhibition of tip growth by aluminum.-Planta 197: 672–680, 1995.

    Article  Google Scholar 

  • Jorge, R.A., Menossi, M., Arruda, P.: Probing the role of calmodulin in Al toxicity in maize.-Phytochemistry 58: 415–422, 2001.

    Article  PubMed  Google Scholar 

  • Jorns, A.C., Hecht-Buchholz, C., Wisseier, A.H.: Aluminum-induced callose formation in root tips of Norway spruce [Picea abies (L.) Karst.].-Z. Pflanzenernahr. Bodenk. 154: 349–353, 1991.

    Google Scholar 

  • Kataoka, T., Furukawa, J., Nakanishi, T.M.: The decrease of extracted apoplast protein in soybean root tip by aluminium treatment.-Biol. Plant. 46: 445–449, 2003.

    Article  Google Scholar 

  • Kenzhebaeva, S.S., Yamamoto, Y., Matsumoto, H.: Aluminum-induced changes in cell-wall glycoproteins in the root tips of Al-tolerant and Al-sensitive wheat lines.-Russ. J. Plant Physiol. 48: 441–447, 1999.

    Article  Google Scholar 

  • Kinraide, T.B.: Use of Gouy-Chapman-Stern model for membrane-surface-electrical potential to interpret some feature of mineral rhizotoxicity.-Plant Physiol. 106: 1583–1592, 1994.

    PubMed  Google Scholar 

  • Kochian, L.V.: Cellular mechanisms of aluminum toxicity and resistance in plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 46: 237–260, 1995.

    Article  Google Scholar 

  • Kochian, L.V., Jones, D.L.: Aluminum toxicity and resistence in plants.-In: Yokel, R., Golub, M.S. (ed.): Research Issues in Aluminum Toxicity. Pp. 69–90. Taylor and Francis Publ., Washington 1997.

    Google Scholar 

  • Kollmeier, M., Felle, H.H., Horst, W.J.: Genotypical differences in aluminum resistence of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum?-Plant Physiol. 122: 945–956, 2000.

    Article  PubMed  Google Scholar 

  • Kuo, M.C., Kao, C.H.: Aluminum effects on lipid peroxidation and antioxidative enzyme activities in rice leaves.-Biol. Plant. 46: 149–152, 2003.

    Article  Google Scholar 

  • Lazof, D.B., Goldsmith, J.G, Rufty, T.W., Linton, R.W.: Rapid uptake of aluminum into cells of intact soybean root tips: a microanalytical study using secondary ion mass spectrometry.-Plant Physiol. 106: 1107–1114, 1994.

    PubMed  Google Scholar 

  • Le Van, H., Kuraishi, S., Sakurai, N.: Aluminum-induced rapid root inhibition and changes in cell-wall components of squash seedlings.-Plant Physiol. 106: 971–976, 1994.

    PubMed  Google Scholar 

  • Li, X.F., Ma, J.F., Syuntaro, S., Matsumoto, H.: Mucilage strongly binds aluminum but dose not prevent roots from aluminum in Zea mays.-Physiol. Plant. 108: 152–160, 2000.

    Article  Google Scholar 

  • Lindberg, S., Strid, H.: Aluminum induces rapid changes in cytosolic pH and free calcium and potassium concentrations in root protoplasts of wheat (Triticum aestivum).-Physiol. Plant. 99: 405–414, 1997.

    Article  Google Scholar 

  • Lindberg, S., Szynkier, K., Greger, M.: Aluminium effects on transmembrane potential in cells of fibrous roots of sugar beet.-Physiol. Plant. 83: 54–62, 1991.

    Article  Google Scholar 

  • Llugany, M., Massot, N., Wisseier, A.H., Poschenrieder, C., Horst, W.J., Barcelo, J.: Aluminum tolerance of maize cultivars as assessed by callose production and root elongation.-Z. Pflanzenernahr. Bodenk. 157: 447–451, 1994.

    Google Scholar 

  • Llugany, M., Poschenrieder, C., Barcelo, J.: Monitoring of aluminium-induced inhibition of root elongation in four maize cultivars differing in tolerance to aluminium and proton toxicity.-Physiol. Plant. 93: 265–271, 1995.

    Article  Google Scholar 

  • MacDonald, T.L., Humphreys, W.G., Martin, B.R.: Promotion of tubulin assembly by aluminum ion in vitro.-Science 236: 183–186, 1987.

    PubMed  Google Scholar 

  • MacDonald, T.L., Martin, R.B.: Aluminum ion in biological systems.-Trends biol. Sci. 13: 15–19, 1988.

    Article  Google Scholar 

  • Marienfeld, S., Stelzer, R.: X-ray microanalyses in roots of Al-treated Avena sativa plants.-J. Plant Physiol. 141: 569–573, 1993.

    Google Scholar 

  • Marschner, H.: Mechanisms of adaptation of plants to acid soils.-Plant Soil 134: 1–20, 1991.

    Google Scholar 

  • Masaoka, Y., Saito, A., Arakawa, Y., Matsuzaki, H., Miyazaki, C., Kobayashi, K.: Al26 microanalysis in the leaf cell organelles of ryegrass and barley by accelerator mass spectrometry (AMS).-J. Plant Nutr. 25: 343–354, 2002.

    Article  Google Scholar 

  • Massot, N., Llugany, M., Poschenrieder, C., Barcelo, J.: Callose production as indicator of aluminum toxicity in bean cultivars.-J. Plant Nutr. 22: 1–10, 1999.

    Google Scholar 

  • Matsumoto, H.: Changes of the structure of pea chromatin by aluminum.-Plant Cell Physiol. 29: 281–287, 1988.

    Google Scholar 

  • Matsumoto, H.: Biochemical mechanism of the toxicity of aluminium and the sequestration of aluminum in plant cells.-In: Wright, R.J., Baligar, V.C., Murrmann, R.P. (ed.): Plant-Soil Interactions at Low pH. Pp. 825–838. Kluwer Academic Publ., Dordrecht 1991.

    Google Scholar 

  • Matsumoto, H.: Cell biology of aluminum toxicity and tolerance in higher plants.-Int. Rev. Cytol. 200: 1–46, 2000.

    Article  PubMed  Google Scholar 

  • Matsumoto, H.: Plant roots under aluminum stress: Toxicity and tolerance.-In: Waisel, Y., Eshel, A., Kaflcaf, U. (ed.): Plant Roots. Pp. 821–838. Marcel Dekker, New York 2002.

    Google Scholar 

  • Matsumoto, H., Hirasawa, E., Torikai, H., Takahashi. E.: Localization of absorbed aluminum in pea root and its binding to nucleic acids.-Plant Cell Physiol. 17: 127–137, 1976.

    Google Scholar 

  • Matsumoto, H., Morimura, S.: Repressed template activity of chromatin of pea roots treated by aluminum.-Plant Cell Physiol. 21: 951–959, 1980.

    Google Scholar 

  • May, H.M., Nordsrom, D.K.: Assessing the solubilities and reaction kinetics of aluminuous minerals in soils.-In: Ulrich, B., Sumner, M.E. (ed.): Soil Acidity. Pp. 125–148. Springer-Verlag, Berlin-Heidelberg 1991.

    Google Scholar 

  • Miyasaka, S.C., Hawes, M.: Possible role of root border cells in detection and avoidance of aluminum toxicity.-Plant Physiol. 125: 1978–1987, 2001.

    Article  PubMed  Google Scholar 

  • Moody, S.F., Clark, A.E., Bacic, A.: Structure analysis of secreted slime from wheat and cowpea roots.-Phytochemistry 27: 2864–2875, 1988.

    Article  Google Scholar 

  • Nichol, B.E., Oliveira, L.A.: Effects of aluminum on the growth and distribution of calcium in roots of an aluminum-sensitive cultivar of barley (Hordeum vulgare).-Can. J. Bot. 73: 1849–1858, 1995.

    Google Scholar 

  • Nichol, B.E., Oliveira, L.A., Glass, A.D.M., Siddiqi, M.Y.: The effects of aluminum on the influx of calcium, potassium, ammonium, nitrate, and phosphate in an aluminum-sensitive cultivar of barley (Hordeum vulgare L.).-Plant Physiol. 101: 1263–1266, 1993.

    PubMed  Google Scholar 

  • Obi, I., Ichikawa, Y., Kakutani, T., Senda, M.: Electrophoresis, zeta potential and potential and surface charges of barley mesophyll protoplasts.-Plant Cell Physiol. 30: 129–135. 1989a.

    Google Scholar 

  • Obi, I., Ichikawa, Y., Kakutani, T., Senda, M.: Electrophoretic studies on plant protoplasts from various sources.-Plant Cell Physiol. 30: 439–444, 1989b.

    Google Scholar 

  • Olivetti, G.P., Cumming, J.R., Etherton, B.: Membrane potential depolarization of root cap cells precedes aluminum tolerance in snap bean.-Plant Physiol. 109: 123–129, 1995.

    Google Scholar 

  • Ono, K., Yamamoto, Y., Hachiya, A., Matsumoto, H.: Synergistic inhibition of growth by aluminum and iron of tobacco (Nicotiana tabacum L.) cells in suspension culture.-Plant Cell Physiol. 36: 115–125, 1995.

    Google Scholar 

  • Osawa, H., Matsumoto, H.: Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex.-Plant Physiol. 126: 411–420, 2001.

    Article  PubMed  Google Scholar 

  • Oteiza, P.L.: A mechanism for the stimulatory effect of aluminum on iron-induced lipid peroxidation.-Arch. Biochem. Biophys. 308: 374–379, 1994.

    Article  PubMed  Google Scholar 

  • Pineros, M., Tester, M.: Plasma-membrane Ca2+ channels in roots of higher plants and their role in aluminum toxicity.-Plant Soil 155: 119–122, 1993.

    Article  Google Scholar 

  • Rengel, Z.: Role of calcium in aluminum toxicity.-New Phytol. 121: 199–513, 1992a.

    Google Scholar 

  • Rengel, Z.: Disturbance of cell Ca2+ homeostasis as a primary trigger of Al toxicity syndrome.-Plant Cell Environ. 15: 931–938, 1992b.

    Google Scholar 

  • Rengel, Z.: Uptake of aluminium by plant cells.-New Phytol. 134: 389–406, 1996.

    Google Scholar 

  • Rengel, Z.: Relationship between cytosolic calcium activity and toxicity of aluminium to plant cells.-In: International Symposium on Impact of Potential Tolerance of Plants on the Increased Productivity under Aluminum Stress. Pp. 15–18. Institute of Bioresources, Okayama University, Kurashiki 2000.

    Google Scholar 

  • Rengel, Z., Elliott, D.C.: Mechanism of aluminum inhibition of net 45Ca2+ uptake by Amaranthus protoplants.-Plant Physiol. 98: 632–638, 1992.

    Google Scholar 

  • Rengel, Z., Zhang, W.H.: Role of dynamics of intracellular calcium in aluminium toxicity syndrome.-New Phytol. 159: 295–314, 2003.

    Article  Google Scholar 

  • Richardt, G., Federolf, G., Habermann, E.: The interaction of aluminum and other metal ions with calcium-calmodul-independent phosphodiesterase.-Arch. Toxicol. 57: 257–259, 1985.

    Article  PubMed  Google Scholar 

  • Rincon, M., Gonzales, A.: Aluminum partitioning in intact roots of aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars.-Plant Physiol. 99: 1021–1028, 1992.

    Google Scholar 

  • Ryan, P.R., Delhaize, E., Jones, D.L.: Function and mechanism of organic anion exudation from plant roots.-Annu. Rev. Plant Physiol. Plant mol. Biol. 52: 527–560, 2001.

    Article  PubMed  Google Scholar 

  • Ryan, P.R., Ditomaso, J.M., Kochian, L.V.: Aluminium toxicity in roots: An investigation of spatial sensitivity and the role of the root cap.-J. exp. Bot. 44: 437–446, 1993.

    Google Scholar 

  • Ryan, P.R., Kinraide, T.B., Kochian, L.V.: Al3+-Ca2+ interactions in aluminum rhizotoxicity I. Inhibition of root growth is not caused by reduction of calcium uptake.-Planta 192: 98–103, 1994.

    Google Scholar 

  • Ryan, P.R., Reid, R.J., Smith, F.A.: Direct evaluation of the Ca2+-displacement hypothesis for Al toxicity.-Plant Physiol. 113: 1351–1357, 1997.

    PubMed  Google Scholar 

  • Schaeffer, H.J., Walton, J.D.: Aluminum ions induce oat protoplasts to produce an extracellular (1,3)(β-D-glucan.-Plant Physiol. 94: 13–19, 1990.

    Google Scholar 

  • Schildknecht, P.H.P.A., Vidal, B.C.: A role for the cell wall in Al3+ resistance and toxicity: crystallinity and availability of negative charges.-Int. Arch. Biosci. 2002: 1087–1095, 2002.

    Google Scholar 

  • Schmohl, N., Pilling, J., Horst, W.J.: Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum.-Physiol. Plant. 109: 419–427, 2000.

    Article  Google Scholar 

  • Schofield, R.M.S., Pallon, J., Fiskesjo, G., Karlsson, G., Malmqvist, K.G.: Aluminum and calcium distribution patterns in aluminum-intoxicated roots of Allium cepa do not support the calcium-displacement hypothesis and indicated signal-mediated inhibition of root growth.-Planta 205: 175–180, 1998.

    Article  Google Scholar 

  • Schwarzerova, K., Zelenkova, S., Nick, P., Opatrny, Z.: Aluminum-induced rapid changes in the microtubular cytoskeleton of tobacco cell lines.-Plant Cell Physiol. 43: 207–216, 2002.

    Article  PubMed  Google Scholar 

  • Silva, L.R., Smith, J., Moxley, D.F., Carter, T.E., Allen, N.S., Rufty, T.W.: Aluminum accumulation at nuclei of cells in root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy.-Plant Physiol. 123: 543–552, 2000.

    Article  PubMed  Google Scholar 

  • Simonovicova, M., Tamas, L., Huttova, J., Mistrik, I.: Effect of aluminium on oxidative stress related enzyme activities.-Biol. Plant. 48: 261–266, 2004.

    Article  Google Scholar 

  • Sivaguru, M., Baluska, F., Volkmann, D., Felle, H.H., Horst, WJ.: 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, 1999a.

    Article  PubMed  Google Scholar 

  • Sivaguru, M., Fujiwara, T., Samaj, J., Baluska, F., Yang, Z., Osawa, H., Maeda, T., Mori, T., Volkmann, D., Matsumoto, H.: Aluminum-induced 1,3-β-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata: a new mechanism of Al toxicity in plants.-Plant Physiol. 124: 991–1005, 2000.

    Article  PubMed  Google Scholar 

  • Sivaguru, M., Horst, W.J.: The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize.-Plant Physiol. 116: 155–163, 1998.

    Article  Google Scholar 

  • Sivaguru, M., Yamamoto, Y, Matsumoto, H.: Differential impacts of aluminium on microtubule organization depends on growth phase in suspension-cultured tobacco cells.-Physiol. Plant. 107: 110–119, 1999b.

    Article  Google Scholar 

  • Tabuchi, A., Matsumoto, H.: Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition.-Physiol. Plant. 112: 353–358, 2001.

    Article  PubMed  Google Scholar 

  • Taylor, G.J.: The physiology of aluminium phytotoxicity.-In: Siegel, H. (ed.): Metal Ions in Biological Systems. Pp. 123–163. Marcel Dekker, New York 1990.

    Google Scholar 

  • Taylor, G.J.: Overcoming barriers to understanding the cellular basis of aluminum resistance.-Plant Soil 171: 89–103, 1995.

    Article  Google Scholar 

  • Taylor, G.J., McDonald-Stephens, J.L., Hunter, D.B., Bertsch, P.M., Elmore, D., Rengel, Z., Reid, R.J.: Direct measurement of aluminum uptake and distribution in single cells of Chara corallina.-Plant Physiol. 123: 987–996, 2000.

    Article  PubMed  Google Scholar 

  • Tice, K.R., Parker, D.R., DeMason, D.A.: Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat.-Plant Physiol. 100: 309–318, 1992.

    Google Scholar 

  • Van Breemen, N.: Acidification and decline of Central European forests.-Nature 315: 16, 1985.

    Article  PubMed  Google Scholar 

  • Vazquez, M., Poschenrieder, C., Corrales, L, Barcelo, J.: Changes in apoplastic aluminum during the initial growth response to aluminum by roots of tolerant maize variety.-Plant Physiol. 119: 435–444, 1999.

    Article  PubMed  Google Scholar 

  • Wagatsuma, T.: Characterization of absorption sites for aluminum in the roots.-Soil Sci. Plant Nutr. 29: 499–515, 1983.

    Google Scholar 

  • Wagatsuma, T., Jujo, K., Ishikawa, S., Nakashima, T.: Aluminum-tolerant protoplasts from roots can be collected with positively charged silica microbeads: A method based on differences in surface negativity.-Plant Cell Physiol. 36: 1493–1502, 1995.

    Google Scholar 

  • Wissemeier, A.H., Dieming, A., Hergenroder, A., Horst, W.J., Mix-Wanger, G.: Callose formation as parameter for assessing genotypical plant tolerance of aluminium and manganese.-Plant Soil 146: 67–75, 1992.

    Article  Google Scholar 

  • Wissemeier, A.H., Klotz, F., Horst, W.J.: Aluminum induced callose synthesis in roots of soybean (Glycine max L.).-J. Plant Physiol. 129: 487–492, 1987.

    Google Scholar 

  • Yamamoto, Y., Kobayashi, Y., Devi, S.R., Rikiishi, S., Matsumoto, H.: Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells.-Plant Physiol. 128: 63–72, 2002.

    Article  PubMed  Google Scholar 

  • Yamamoto, Y., Kobayashi, Y., Devi, S.R., Rikiishi, S., Matsumoto, H.: Oxidative stress triggered by aluminum in plant roots.-Plant Soil 255: 239–243, 2003.

    Article  Google Scholar 

  • Yermiyahu, U., Rytwo, G, Brauer, D.K., Kinraide, T.B.: Binding and electrostatic attraction of lanthanum (La3+) and aluminum (Al3+) to wheat root plasma membranes.-J. Membr. Biol. 159: 239–252, 1997.

    Article  PubMed  Google Scholar 

  • You, G, Nelson, D.J.: Al3+ versus Ca2+ ion binding to methionine and tyrosine spin-labeled bovine brain calmodulin.-J. inorg. Biochem. 41: 283–291, 1991.

    Article  PubMed  Google Scholar 

  • Zhang, W.H., Rengel, Z.: Aluminium induces an increase in cytoplasmic calcium in intact wheat root apical cells.-Aust. J. Plant Physiol. 26: 401–409, 1999.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Environmental and Resource Science, Zhejiang University, Hangzhou, 310029, P.R. China

    S. J. Zheng & J. L. Yang

Authors
  1. S. J. Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. L. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. J. Zheng.

Additional information

This work was partly supported by fund from the Huoyingdong Foundation, Education Ministry of China and Natural Science Foundation of China (Contact No. 30170548).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zheng, S.J., Yang, J.L. Target sites of aluminum phytotoxicity. Biol Plant 49, 321–331 (2005). https://doi.org/10.1007/s10535-005-0001-1

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-005-0001-1

Additional key words

Search

Navigation