Skip to main content

The Role of the Outer Surface of the Plasma Membrane in Aluminum Tolerance

  • Conference paper
Plant Nutrient Acquisition

Summary

Aluminum (Al) toxicity is the primary stress factor in acid soils. Al tolerance is suggested to be constitutional because of its rapid response. The cell wall of the root-tip acts as the adsorption site for Al ions, but its negativity and Al adsorption capacity cannot explain the differential Al tolerance among crop plant species and cultivars. Among several strategies to tolerate Al toxicity, much evidence has been accumulating on the specific exudation of organic acids (citric, oxalic, and malic acids) from root-tip cells. However, release of organic acids was suggested to be a partial strategy for tolerance to Al ions and not to be a general and satisfactory one. The role of phenolic compounds existing outside and/or inside of root cells under soil acidity stress should be clarified more in detail. Among the apoplastic components (mucilage, cell wall, and the outer surface of the plasma membrane), the plasma membrane is considered to be the determinant of Al tolerance. The structure, function, and genetic aspects of the plasma membrane of root-tip cells that control Al tolerance are future subjects for research. For better growth in acid soils, plants should also possess additional tolerances to low nutrients (phosphorus, calcium and others) under Al stress.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Akeson MA, Munns DN (1989) Lipid bilayer permeation by neutral aluminum citrate and by three a-hydroxy carboxylic acids. Biochim Biophys Acta 984: 200–206

    Article  PubMed  CAS  Google Scholar 

  • Allan DL, Shann JR, Bertsch PM (1990) Role of root cell walls in iron deficiency of soybean (Glycine max) and aluminium toxicity of wheat (Triticum aestivum). In: van Beusichem ML (Ed) Plant nutrition–physiology and applications. Kluwer Academic Publishers, Dordrecht, pp 345–349

    Chapter  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Blamey FPC, Dowling AJ (1995) Antagonism between aluminium and calcium for sorption by calcium pectate. Plant Soil 171: 137–140

    Article  CAS  Google Scholar 

  • Canny MJ (1995) Apoplastic water and solute movement: New rules for an old space. Annu Rev Plant Physiol Plant Mol Biol 46: 215–236

    Article  CAS  Google Scholar 

  • Cevc G (1982) Water and membranes: The interdependence of their physico-chemical properties in the case of phospholipid bilayers. Studia Biophysica 91: 45–52

    CAS  Google Scholar 

  • Chen J, Sucoff EI, Stadelmann EJ (1991) Aluminum and temperature alteration of cell membrane permeability of Quercus rubra. Plant Physiol 96: 644–649

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (1989) Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls. Planta 177: 121–130

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (1996) Plant cell enlargement and the action of expansins. BioEssays 18: 533–540

    CAS  Google Scholar 

  • Cosgrove DJ, Durachko DM (1994) Autolysis and extension of isolated walls from growing cucumber hypocotyls. J Exp Bot 45: 1711–1719

    PubMed  CAS  Google Scholar 

  • de la Fuente JM, Ramírez-Rodriguez V, Cabrela-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276: 1566–1568

    Article  PubMed  Google Scholar 

  • Deleers M, Servais J-P, Wulfert E (1985) Micromolar concentrations of Al“ induce phase separation, aggregation and dye release in phosphatidylserine-containing lipid vesicles. Biochim Biophys Acta 813: 195–200

    Article  PubMed  CAS  Google Scholar 

  • Deleers M, Servais J-P, Wulfert E (1986) Neurotoxic cations induce membrane rigidification and membrane fusion at micromolar concentrations. Biochim Biophys Acta 855: 271–276

    Article  PubMed  CAS  Google Scholar 

  • Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.). II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103: 695–702

    Google Scholar 

  • Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12: 285–292

    Article  CAS  Google Scholar 

  • Douglas TJ (1985) NaC1 effects on 4-desmethylsterol composition of plasma membrane-enriched preparations from citrus roots. Plant Cell Environ 8: 687–692

    Article  CAS  Google Scholar 

  • Esau K (1965) Plant anatomy. John Wiley and Sons, New York, pp 486, 712

    Google Scholar 

  • Flowers TJ,Yeo AR (1992) Solute transport in plants. Blackie Academic and Professional, London, pp 17–47

    Book  Google Scholar 

  • Hauser H, Phillips MC (1979) Interactions of the polar groups of phospholipid bilayer membranes. Prog Sur Mem Sci 13: 297–404

    CAS  Google Scholar 

  • Henderson M, Ownby JD (1991) The role of root cap mucilage secretion in aluminum tolerance in wheat. Curr Top Plant Biochem Physiol 10: 134–141

    CAS  Google Scholar 

  • Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape II. Local root exudation of organic acids as a response to P-starvation. Plant Soil 113: 161–165

    Google Scholar 

  • Horst WJ, Wagner A, Marschner H (1982) Mucilage protects root meristems from aluminum injury. Z Pflanzenphysiol 105: 435–444

    CAS  Google Scholar 

  • Ishikawa S, Wagatsuma T (1998) 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

    Article  CAS  Google Scholar 

  • Ishikawa S, Wagatsuma T, Ikarashi T (1996) Comparative toxicity of Al3+,Yb3*, and Lai to root-tip cells differing in tolerance to high Al“ in terms of ionic potentials of dehydrated trivalent cations. Soil Sci Plant Nutr 42: 613–625

    Article  CAS  Google Scholar 

  • Jones DL, Prabowo AM, Kochian LV (1996a) Aluminum-organic acid interactions in acid soils. II. Influence of solid phase sorption on organic acid -Al complexation and Al rhizotoxicity. Plant Soil 182: 229–237

    Google Scholar 

  • Jones DL, Prabowo AM, Kochian LV (1996b) Kinetics of malate transport and decomposition in acid soils and isolated bacterial populations: The effects of microorganisms on root exudation of malate under Al stress. Plant Soil 182: 239–247

    Google Scholar 

  • Jones DL, Kochian LV (1997) Aluminum interaction with plasma membrane lipids and enzyme metal binding sites and its potential role in Al cytotoxicity. FEBS Lett 400: 51–57

    Article  PubMed  CAS  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46: 237–260

    Article  CAS  Google Scholar 

  • Kochian LV, Jones DL (1996) 4. Aluminum toxicity and resistance in plants. In: Yokel RA, Golub MS (Eds) Research issues in aluminum toxicity. Taylor and Francis, Washington, pp 69–89

    Google Scholar 

  • Larsson C, Willer IM (1990) The plant plasma membrane. Springer-Verlag, Berlin Heidelberg, pp 16–75

    Chapter  Google Scholar 

  • Larsson C, Widell S, Kjellbom P (1987) Preparation of high-purity plasma membranes. Methods Enzymol 148: 558–568

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Luo HM, Osaki M, Tadano T (1997) Mechanisms of differential tolerance of crop plants to high aluminum and low phosphorus growth conditions. In: Ando T et al. (Eds) Plant nutrition–for sustainable food production and environment. Kluwer Academic Publishers, Dordrecht, pp 473–474

    Chapter  Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H (1997a) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 38: 1019–1025

    Article  CAS  Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H, Hiradate S (1997b) Detoxifying aluminum with buckwheat. Nature 390: 569–570

    Article  Google Scholar 

  • Ma JF, Hiradate S, Matsumoto H (1998) High aluminum resistance in buckwheat. II. Oxalic acid detoxifies aluminum internally. Plant Physiol 117: 753–759

    Google Scholar 

  • Masion A, Bertsch PM (1997) Aluminum speciation in the presence of wheat root cell walls: a wet chemical study. Plant Cell Environ 20: 504–512

    Article  CAS  Google Scholar 

  • McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4: 1425–1433

    PubMed  CAS  Google Scholar 

  • Mugwira LM, Elgawhary SM (1979) Aluminum accumulation and tolerance of triticale and wheat in relation to root cation exchange capacity. Soil Sci Soc Am J 43: 736–740

    Article  CAS  Google Scholar 

  • Munch E (1930) Die Stoffbewegungen in der Pflanze. p 73 Jena. Fischer 234 pp

    Google Scholar 

  • Munn DA, McCollum RE (1976) Solution culture evaluation of sweet potato cultivar tolerance to aluminum. Agron J 68: 989–991

    Article  CAS  Google Scholar 

  • Nordstrom DK, May HM (1989) 2. Aqueous equilibrium data for mononuclear aluminum species. In:. Sposito G (Ed) The environmental chemistry of aluminum. CRC Press, Boca Raton, pp 29–53

    Google Scholar 

  • Obi I, Ichikawa Y, Kakutani T, Senda M (1989) Electrophoretic studies on plant protoplasts. I. pH dependence of zeta potentials of protoplasts from various sources. Plant Cell Physiol 30: 439–444

    Google Scholar 

  • Ohwaki Y, Hirata H (1992) Differences in carboxylic acid exudation among P-starved leguminous crops in relation to carboxylic acid contents in plant tissues and phospholipid level in roots. Soil Sci Plant Nutr 38: 235–243

    Article  CAS  Google Scholar 

  • Orvig C (1993) The aqueous coordination chemistry of aluminum. In: Robinson GH (Ed) Coordination chemistry of aluminum. VCH Publishers, New York, pp 85–122

    Google Scholar 

  • Osawa H, Kojima K, Sasaki S (1997) Excretion of citrate as an aluminum-tolerance mechanism in tropical leguminous trees. In: Ando T et al. (Eds) Plant nutrition - for sustainable food production and environment. Kluwer Academic Publishers, Dordrecht, pp 455–456

    Chapter  Google Scholar 

  • Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as a mechanism of Al-tolerance in maize (Zea mays L.). Planta 197: 788–795

    Article  Google Scholar 

  • Puthota V, Cruz-Ortega R, Johnson J, Ownby J (1991) An ultrastructural study of the inhibition of mucilage secretion in the wheat root cap by aluminum. In: Wright RI et al. (Eds) Plant-soil interactions at low pH. Kluwer Academic Publishers, Dordrecht, pp 779–789

    Chapter  Google Scholar 

  • Rengel Z (1992) Role of calcium in aluminium toxicity. New Phytol 121: 499–513

    Article  CAS  Google Scholar 

  • Rengel Z, Robinson DL (1989) Determination of cation exchange capacity of ryegrass roots by summing exchangeable cations. Plant Soil 116: 217–222

    Article  CAS  Google Scholar 

  • Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminum toxicity in roots: An investigation of spacial sensitivity and the role of the root cap. J Exp Bot 44: 437–446

    Google Scholar 

  • Ryan PR, Delhaize E, Randall P (1995) Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Aust J Plant Physiol 22: 531–536

    Article  CAS  Google Scholar 

  • Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman SD (1997) Aluminum activates an anion channel in the apical cells of wheat roots. Proc Natl Acad Sci USA 94: 6547–6552

    Article  PubMed  CAS  Google Scholar 

  • Sonobe S, Takahashi S (1994) Association of microtubules with the plasma membrane of tobacco BY-2 cells in vitro. Plant Cell Physiol 35: 451–460

    CAS  Google Scholar 

  • Ström L, Olsson T, Tyler G (1994) Differences between calcifuge and acidifuge plants in root exudation of low-molecular organic acids. Plant Soil 167: 239–245

    Article  Google Scholar 

  • Takabatake R, Shimmen T (1997) Inhibition of electrogenesis by aluminum in characean cells. Plant Cell Physiol 38: 1264–1271

    Article  CAS  Google Scholar 

  • Tam SC, McColl JG (1990) Aluminum-and calcium-binding affinities of some organic ligands in acidic conditions. J Environ Qual 19: 514–520

    Article  CAS  Google Scholar 

  • Vierstra R, Haug A (1978) The effects of A13+ on the physical properties of membrane lipids in Thermoplasma acidophilum. Biochim Biophys Res Commun 84: 138–144

    Article  CAS  Google Scholar 

  • Wagatsuma T (1983) Characterization of absorption sites for aluminum in the roots. Soil Sci Plant Nutri 29: 499–515

    Article  CAS  Google Scholar 

  • Wagatsuma T,Akiba R (1989) Low surface negativity of root protoplasts from aluminum-tolerant plant species. Soil Sci Plant Nutr 35: 443–452

    Article  Google Scholar 

  • Wagatsuma T, Ishikawa S, Obata H, Tawaraya K, Katohda S (1995a) Plasma membrane of younger and outer cells is the primary specific site for aluminum toxicity in roots. Plant Soil 171: 105–112

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Wagatsuma T, Hitomi H, Ishikawa S, Tawaraya K (1997) Al-binding capacity of plasma membrane of root-tip portion in relation to Al tolerance. In: Ando T et al. (Eds) Plant nutrition–for sustainable food production and environment. Kluwer Academic Publishers, Dordrecht, pp 467–468

    Chapter  Google Scholar 

  • Yermiyahu U, Brauer DK, Kinraide TB (1997) Sorption of aluminum to plasma membrane vesicles isolated from roots of Scout 66 and Atlas 66 cultivars of wheat. Plant Physiol 115: 1119–1125

    PubMed  CAS  Google Scholar 

  • Zhang G, Taylor GJ (1989) Kinetics of aluminum uptake by excised roots of aluminum-tolerant and aluminum-sensitive cultivars of Triticum aestivum L. Plant Physiol 91: 1094–1099

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Slaski JJ, Archambault DJ, Taylor GJ (1997) Alteration of plasma membrane lipids in aluminum-resistant and aluminum-sensitive wheat genotypes in response to aluminum. Physiol Plant 99: 302–308

    Article  CAS  Google Scholar 

  • Zheng SJ, Ma JF, Matsumoto H (1998) High aluminum resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tip. Plant Physiol 117: 745–751

    Article  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2001 Springer Japan

About this paper

Cite this paper

Wagatsuma, T., Ishikawa, S., Ofei-Manu, P. (2001). The Role of the Outer Surface of the Plasma Membrane in Aluminum Tolerance. In: Ae, N., Arihara, J., Okada, K., Srinivasan, A. (eds) Plant Nutrient Acquisition. Springer, Tokyo. https://doi.org/10.1007/978-4-431-66902-9_7

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-66902-9_7

  • Publisher Name: Springer, Tokyo

  • Print ISBN: 978-4-431-66904-3

  • Online ISBN: 978-4-431-66902-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics