Abstract
There appears to be an emerging consensus that resistance to aluminium (Al) is mediated at the cellular level. Virtually all current hypotheses which seek to explain the basis of Al resistance have a cellular focus, including those which postulate that external mechanisms limit the rate of Al entry across the membrane and/or protect sensitive extracellular sites, as well as those which postulate that internal mechanisms detoxify Al in the cytoplasm. If Al resistance is a cellular phenomenon, it should be expressed in single cells. Attempts to demonstrate resistance in cell culture systems, however, have not been uniformly satisfying. Considerable uncertainty has arisen from use of experimental conditions which favour formation of insoluble or non-toxic Al species. This problem has plagued research which has attempted to select for Al resistance in cell culture systems, as well as research which has attempted to express existing patterns of differential resistance in cell culture systems. Despite technical problems such as this, work at the cellular level has provided some important contributions. Most importantly, we now know resistance to Al can be expressed at the cellular level. We have discovered also that plant cells accumulate Al much more rapidly in cell culture systems than in intact roots and that isolated cells are more sensitive to Al than complex tissues. While this type of research is still hampered by a number of technical barriers, it would appear that more rapid progress could be achieved if greater emphasis was placed on true “experimental” work. Furthermore, we need to begin evaluating experimental data in the context of an integrated Al stress response if we are to achieve a full understanding of the cellular basis of Al resistance.
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References
Arihara A, Kumagai R, Koyama H and Ojima K 1991 Aluminumtolerance of carrot (Daucus carota L.) plants regenerated from selected callus cultures. Soil Sci. Plant Nutr. 37, 699–705.
Basu A, Basu U and Taylor G J 1994a Induction of microsomal membrane proteins in roots of an Al-resistant-cultivar of Triticum aestivum L. in response to aluminum stress. Plant Physiol. 104, 1007–1013.
Basu U, Basu A and Taylor G J 1994b Differential exudation of polypepides by roots of aluminum-resistant and aluminum-sensitive cultivars of Triticum aestivum L. in response to aluminum stress. Plant Physiol. 106, 151–158.
Blamey F, Edwards D and Asher C 1983 Effects of aluminum, OH:Al and P:Al molar ratios, and ionic strength on soybean root elongation in solution culture. Soil Sci. 136, 197–207.
Clarkson D T 1967 Interactions between aluminium and phosphorus on root surfaces and cell wall material. Plant and Soil 27, 347–356.
Conner A J and Meredith C P 1985a Simulating the mineral environment of aluminium toxic soils in plant cell culture. J. Exp. Bot. 36, 870–880.
Conner A J and Meredith C P 1985b Strategies for the selection and characterization of aluminum-resistant variants from cell cultures of Nicotiana plumbaginifolia. Planta 166, 466–473.
Conner A J and Meredith C P 1985c Large scale selection of aluminum-resistant mutants from plant cell culture: expression and inheritance in seedlings. Theor. Appl. Genet. 71, 159–165.
Cumming J R, Buckelew Cumming A and Taylor G J 1992 Patterns of root respiration associated with the induction of aluminium tolerance in Phaseolus vulgaris L. J. Exp. Bot. 43, 1075–1081.
Cumming J R and Taylor G J 1990 Mechanisms of metal tolerance in plants: Physiological adaptations for exclusion of metal ions from the cytoplasm. In Stress Responses in Plants: Adaptation and Acclimation Mechanisms. Eds. R C Alscher and J R Cumming. pp 329–356. Wiley-Liss, Inc., New York.
Delhaize E, Craig S, Beaton C D, Bennet R J, Jagadish V C and Randall P J 1993a Aluminum tolerance in wheat (Triticum aestium L.) I. Uptake and distribution of aluminum in root apices. Plant Physiol. 103, 685–693.
Delhaize E, Higgins T J V and Randall P J 1991 Aluminium tolerance in wheat: analysis of polypeptides in the root apices of tolerant and sensitive genotypes. In Plant-Soil Interactions at low pH. Eds. R J Wright, V C Baligar and R P Murrmann. pp 1071–1079. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Delhaize E, Ryan P R 1993b Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol. 103, 695–702.
Hairiah K, van Noordwijk M, Stulen I and Kuiper P J C 1992 Aluminium avoidance by Mucuna pruriens. Physiol. Plant. 86, 17–24.
Hartel P and Bouton J 1989 Rhizobium meliloti inoculation of alfalfa selected for tolerance to acid, aluminium-rich soils. Plant and Soil 116, 283–285.
Haug A 1984 Molecular aspects of aluminum toxicity. C.R.C. Crit. Rev. Plant Sci. 1, 345–373.
Huang J W, Grunes D L and Kochian L V 1993 Aluminum effects on calcium (45Ca2+) translocation in aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars. Plant Physiol. 102, 85–93.
Huett D O and Menary R C 1979 Aluminium uptake by excised roots of cabbage, lettuce and kikuyu grass. Aust. J. Plant Physiol. 6, 643–653.
Kinraide T B 1990 Assessing the rhizotoxicity of the aluminate ion Al(OH)4 -. Plant Physiol. 94, 1620–1625.
Kinraide T B 1991 Identity of the rhizotoxic aluminium species. Plant and Soil 134, 167–178.
Kinraide T B and Parker D R 1989 Assessing the phytotoxicity of mononuclear hydroxy-aluminum. Plant Cell Environ. 12, 479–487.
Kinraide T B and Parker D R 1990 Apparent phytotoxicity of mononuclear hydroxy-aluminum to four dicotyledonous species. Physiol. Plant. 79, 283–288.
Kinraide T B and Ryan P R 1991 Cell surface charge may obscure the identity of the rhizotoxic aluminum species. In Current Topics in Plant Biochemistry and Physiology 1991. Ultraviolet-B Radiation Stress, Aluminum, Stress, Toxicity and Tolerance, Boron Requirements, Stress and Toxicity. Volume 10. Eds. D D Randall, D G Blevins and C D Miles. pp 94–106. Interdisciplinary Plant Biochemistry and Physiology Program, University of Missouri-Columbia, USA.
Koyama H, Ojima K and Yamaya T 1990 Utilization of anhydrous aluminum phosphate as a sole source of phosphorus by a selected carrot cell line. Plant Cell Physiol. 31, 173–177.
Koyama H, Ojima K and Yamaya T 1992 Characteristics of aluminum-phosphate-adapted carrot cells: uptake and utilization of the phosphate. Plant Cell Physiol. 33, 171–176.
Koyama H, Okawara R, Ojima K and Yamaya T 1988 Re-evaluation of characteristics of a carrot cell line previously selected as aluminum-tolerant cells. Physiol. Plant. 74, 683–687.
McDonald-Stephens J L and Taylor G J 1994 Kinetics of aluminum uptake by cell suspensions of Phaseolus vulgaris. J. Plant Physiol. (In press).
Meredith C P 1978a Response of cultivated tomato cells to aluminum. Plant Sci. Lett. 12, 17–24.
Meredith C P 1978b Selection and characterization of aluminum-resistant variants from tomato cell cultures. Plant Sci. Lett. 12, 25–34.
Miyasaka S, Buta J, Howell R and Foy C 1991 Mechanism of aluminum tolerance in snapbeans. Root exudation of citric acid. Plant Physiol. 96, 737–743.
Ojima K, Abe H and Ohira K 1984 Release of citric acid into the medium by aluminum-tolerant carrot cells. Plant Cell Physiol. 25, 855–858.
Ojima K, Koyama H, Suzuki R and Yamaya T 1989 Characterization of two tobacco cell lines selected to grow in the presence of either ionic Al or insoluble Al-phosphate. Soil Sci. Plant Nutr. 35, 545–551.
Ojima K and Ohira K 1983 Characterization of aluminum and manganese tolerant cell lines selected from carrot cell cultures. Plant Cell Physiol. 24, 789–797.
Ojima K and Ohira K 1985 Reduction of aluminum toxicity by addition of a conditioned medium from aluminum-tolerant cells of carrot. Plant Cell Physiol. 26, 281–286.
Ojima K and Ohira K 1988 Aluminum-tolerance and citric acid release from a stress-selected cell line of carrot. Commun. Soil Sci. Plant Anal. 19, 1229–1236.
Ownby J D and Hruschka W R 1991 Quantitative changes in cytoplasmic and microsomal proteins associated with aluminum toxicity in two cultivars of winter wheat. Plant Cell Environ. 14, 303–309.
Parker D R and Bertsch P M 1992 Formation of the “Al13” tridecameric polycation under diverse synthesis condition. Environ. Sci. Technol. 26, 914–921.
Parrot W A and Bouton J H 1990 Aluminum tolerance in alfalfa as expressed in tissue culture. Crop Sci. 30, 387–389.
Peterson C A 1988 Exodermal Casparian bands: their significance for ion uptake by roots. Physiol. Plant. 72, 204–208.
Picton S J, Richards K D and Gardner R C 1991 Protein profiles in root-tips of two wheat (Triticum aestivum L.) cultivars with differential tolerance to aluminium. In Plant-Soil Interactions at low pH. Eds. R J Wright, V C Baligar and R P Murrmann. pp 1063–1070. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Rengel Z 1992 Disturbance of cell Ca2+ homeostasis as a primary trigger of Al toxicity syndrome. Plant Cell Environ. 15, 931–938.
Rincon M and Gonzales R A 1991 Induction of protein synthesis by aluminium in wheat (Triticum aestivum L.) root tips. In Plant-Soil Interactions at low pH. Eds. R J Wright, V C Baligar and R P Murrmann. pp 851–858. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Rincon M and Gonzales R A 1992 Aluminum partitioning in intact roots of aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars. Plant Physiol. 99, 1021–1028.
Ryan P R, DiTomaso J M and Kochian L V 1993 Aluminium toxicity and calcium uptake at the root apex in near-isogenic lines of wheat (Triticum aestivum L.) differing in aluminum tolerance. Plant Physiol. 102, 975–982.
Schaeffer H J and Walton J D 1990 Aluminum ions induce oat protoplasts to produce an extracellular (1–3) β-d-glucan. Plant Physiol. 94, 13–19.
Shann J R and Bertsch P M 1993 Differential cultivar response to polynuclear hydroxo-aluminum complexes. Soil Sci. Soc. Am. J. 57, 116–120.
Shi B and Haug A 1990 Aluminum uptake by neuroblastoma cells. J. Neurochem. 55, 551–558.
Smith R H, Bhaskaran S and Schertz K 1983 Sorghum plant regeneration from aluminum selection media. Plant Cell Rep. 2, 129–132.
Taylor G J 1988a The physiology of aluminum tolerance. In Aluminum and its Role in Biology. Metal Ions in Biological Systems. Volume 24. Ed. H Sigel. pp 165–198. Marcel Dekker, Inc., New York, USA.
Taylor J 1988b Mechanisms of aluminum tolerance in Triticum aestivum L. (wheat). V. Nitrogen nutrition, plant-induced pH, and tolerance to aluminum; correlation without causality? Can. J. Bot. 66, 694–699.
Taylor G J 1991 Current views of the aluminum stress response; the physiological basis of tolerance. In Current Topics in Plant Biochemistry and Physiology 1991. Ultraviolet-B Radiation Stress, Aluminum Stress, Toxicity and Tolerance, Boron Requirements, Stress and Toxicity. Volume 10. Eds. D D Randall, D G Blevins and C D Miles. pp 57–93. Interdisciplinary Plant Biochemistry and Physiology Program, University of Missouri-Columbia, USA.
Taylor G J and Foy C D 1985a Mechanisms of aluminum tolerance in Triticum aestivum L. (wheat) I. Differential pH induced by winter cultivars in nutrient solutions. Am. J. Bot. 72, 695–701.
Taylor G J and Foy C D 1985b Mechanisms of aluminum tolerance in Triticum aestivum L (wheat) II. Differential pH induced by spring cultivars in nutrient solutions. Am. J. Bot. 72, 702–706.
Taylor G J and Foy C D 1985c Mechanisms of aluminum tolerance in Triticum aestivum L. (wheat). IV. The role of ammonium and nitrate nutrition. Can. J. Bot. 63, 2181–2186.
Tice K R, Parker D R and De Mason D A 1992 Operationally defined apoplastic and symplastic aluminum fractions in root tips of Al-intoxicated wheat. Plant Physiol. 100, 309–318.
Wissemeier A H, Diening A., Hergenroder A, Horst W J and Mix-Wagner G 1992 Callose formation as parameter for assessing genotypical plant tolerance of aluminium and manganese. Plant and Soil 146, 67–75.
Zhang G and Taylor G J 1989 Kinetics of aluminum uptake by excised roots of aluminum-tolerant and aluminum-sensitive cultivars of Triticum aestivum L. Plant Physiol. 91, 1094–109.
Zhang G and Taylor G J 1990 Kinetics of aluminum uptake in Triticum aestivum L. Identity of the linear phase of aluminum uptake by excised roots of aluminum-tolerant and aluminum-sensitive cultivars. Plant Physiol. 94, 577–584.
Zhang G and Taylor G J 1991 Effects of biological inhibitors on kinetics of aluminium uptake by excised roots and purified cell wall material of aluminium-tolerant and aluminium-sensitive cultivars of Triticum aestivum L. J. Plant Physiol. 138, 533–539.
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Taylor, G.J. Overcoming barriers to understanding the cellular basis of aluminium resistance. Plant Soil 171, 89–103 (1995). https://doi.org/10.1007/BF00009570
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DOI: https://doi.org/10.1007/BF00009570