Skip to main content

The Role of the Root Cell Wall in Aluminum Toxicity

  • Conference paper
Plant Nutrient Acquisition

Summary

Aluminum (Al), the most common metal of the earth’s crust, is highly toxic to roots of many plant species when present in solution as monomeric cations (e.g., A13+, A1OH2+) at a concentration as low as 10 µM. Despite this long-known effect, there is little consensus on the biochemical basis of Al toxicity, which may be manifest either external to or within the symplasm. There is increasing evidence that the vast majority of Al in roots occurs in the walls of cells at the apex of plant roots;≥99% of the Al in Chara corallina nodal cells occurs in the cell wall, for example. The Al which accumulates at the apex of plant roots is bound both rapidly and strongly by negatively-charged pectic compounds (predominantly α-1,4 D-polygalacturonic acid). It is proposed that the accumulation of Al in the cell wall exerts a detrimental effect on root growth and function in three ways. First, the decrease in apoplastic sorption of basic cations, which have limited ability to displace bound Al, reduces nutrient acquisition per unit root length. Second, the Al sorbed in the cell wall reduces cell expansion, thus reducing root elongation (a major visible effect of soluble Al). This would also reduce nutrient uptake through decreased root proliferation through the soil. Third, sorption of Al in the cell wall reduces the movement of water and solutes through the apoplasm, directly decreasing nutrient acquisition by the root.

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

  • Adams F, Lund ZF (1966) Effect of chemical activity of soil solution aluminum on cotton root penetration of acid subsoils. Soil Sci 101: 193–198

    Article  CAS  Google Scholar 

  • Alva AK, Blarney FPC, Edwards DG, Asher CJ (1986) An evaluation of aluminum indices to predict aluminum toxicity in plants grown in nutrient solutions. Communications in Soil Science and Plant Analysis 17: 1271–1280

    Article  CAS  Google Scholar 

  • Ando T (1970) Cation absorption by excised barley roots in relation to root cation exchange capacity. Journal of the Faculty of Fisheries and Animal Husbandry, Hiroshima University 9: 83–121

    CAS  Google Scholar 

  • Asher CJ, Blarney FPC, Kerven GL (1992) Recent research on soil acidity: Identifying toxic aluminium in soils. In: Tovar SJL, Quintero L (Eds) La Investgacion Edafologica en Mexico 1991–1992. Memorias del 15 Congreso Nacional de la Sociedad Mexicana de la Ciencia del Suelo. Sociedad Mexicana de la Ciencia del Suelo, Acapulco, pp 61–68

    Google Scholar 

  • Barcelo J, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: A review. Journal of Plant Nutrition 13: 1–37

    Google Scholar 

  • Baron-Epel 0, Gharyal PK, Schindler M (1988) Pectins as mediators of wall porosity in soybean cells. Planta 175: 389–395

    Article  CAS  Google Scholar 

  • Bazzaz FA, Carlson RW, Rolfe GL (1974) The effect of heavy metals on plants: Part 1. Inhibition of gas exchange in sunflower by Pb, Cd, Ni, and Tl. Environmental Pollution 7: 241–252

    Google Scholar 

  • Bennet RJ, Breen CM (1991a) The aluminium signal: New dimensions to mechanisms of aluminum tolerance. In: Wright RJ, Baligar VC, Murrmann RP (Eds) Plant-Soil Interactions at Low pH. Developments in Plant and Soil Sciences. Kluwer Academic, Dordrecht, pp 703–716

    Google Scholar 

  • Bennet RJ, Breen CM (1991b) The recovery of roots of Zea mays L. from various aluminium treatments: Towards elucidating the regulatory processes that underlie root growth control. Environmental and Experimental Botany 31: 153–163

    Google Scholar 

  • Bennet RJ, Breen CM, Fey MV (1985) The primary site of aluminium injury in the root of Zea mays L. South African Journal of Plant and Soil 2: 8–17

    CAS  Google Scholar 

  • Bertsch PM, Parker DR (1996) Aqueous polynuclear aluminum species. In: Sposito G (Ed) The environmental chemistry of aluminum. CRC Lewis, Boca Raton, pp 117–168

    Google Scholar 

  • Blarney FPC, Dowling AJ (1995) Antagonism between aluminium and calcium for sorption by calcium pectate. In: Date RA, Grundon NJ, Rayment GE, Probert ME (Eds) Plant-soil interactions at low pH: Principles and management. Kluwer Academic, Dordrecht, pp 303–306

    Chapter  Google Scholar 

  • Blarney FPC, Edwards DG, Asher CJ (1983) Effect of aluminum, OH:Al and P:Al ratios, and ionic strength on soybean root elongation in solution culture. Soil Science 136: 197–207

    Article  Google Scholar 

  • Blarney FPC, Edmeades DC, Wheeler DM (1990) Role of root cation-exchange capacity in differential aluminum tolerance of Lotus species. Journal of Plant Nutrition 13: 729–744

    Article  Google Scholar 

  • Blarney FPC, Edmeades DC, Wheeler DM (1992) Empirical models to approximate calcium and magnesium ameliorative effects and genetic differences in aluminium tolerance in wheat. Plant and Soil 144: 281–287

    Article  Google Scholar 

  • Blarney FPC, Asher CJ, Edwards DG, Kerven GL (1993a) In vitro evidence of aluminum effects on solution movement through root cell walls. Journal of Plant Nutrition 16: 555–562

    Article  Google Scholar 

  • Blarney FPC, Asher CJ, Kerven GL, Edwards DG (1993b) Factors affecting aluminium sorption by calcium pectate. Plant and Soil 149: 87–94

    Article  Google Scholar 

  • Blarney FPC, Ostatek-Boczynski Z, Kerven GL (1997) Ligand effects on aluminium sorption by calcium pectate. Plant and Soil 192: 269–275

    Article  Google Scholar 

  • Brady DJ, Edwards DG, Asher CJ, Blarney FPC (1993) Calcium amelioration of aluminium toxicity effects on root hair development in soybean (Glycine max ( L.) Merr.). New Phytologist 123: 531–538

    Google Scholar 

  • Brett CT, Waldron KW (1996) Physiology and biochemistry of plant cell walls. 2nd ed. Chapman and Hall, London

    Google Scholar 

  • Cameron RS, Ritchie GSP, Robson AD (1986) Relative toxicities of inorganic aluminum complexes to barley. Soil Science Society of America Journal 50: 1231–1236

    Article  CAS  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls of flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant Journal 3: 1–30

    Article  PubMed  CAS  Google Scholar 

  • Carver BF, Ownby JD (1995) Acid soil tolerance in wheat. Advances in Agronomy 54: 117–173

    Article  CAS  Google Scholar 

  • Clarkson DT (1967) Interactions between aluminium and phosphorus on root surfaces and cell wall material. Plant and Soil 27: 347–356

    Article  CAS  Google Scholar 

  • Clarkson DT (1996) Root structure and sites of ion uptake. In: Waisel Y, Eshel A, Kafkafi U (Eds )

    Google Scholar 

  • Plant roots: The hidden half. 2nd ed. Marcell Dekker Inc, New York, pp 483–510

    Google Scholar 

  • Cosgrove DJ (1993) Wall extensibility: its nature, measurement and relationship to plant cell growth.

    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 Physiology 103: 695–702

    Google Scholar 

  • Ferris T (1988) Corning of age in the milky way. Morrow, New York

    Google Scholar 

  • Foy CD (1984) Physiological effects of hydrogen, aluminum, and manganese toxicities in acid soil. In: Adams F (Ed) Soil acidity and liming. 2nd ed, Agronomy No. 12, American Society of Agronomy, Madison, pp 57–97

    Google Scholar 

  • Foy CD, Fleming AL, Burns GE, Armiger WH (1967) Characterization of differential aluminum tolerance among varieties of wheat and barley. Soil Science Society of America Proceedings 31: 513–521

    Article  CAS  Google Scholar 

  • Grauer UE, Horst WJ (1992) Modeling cation amelioration of aluminum phytotoxicity. Soil Science Society of America Journal 56: 166–172

    Article  CAS  Google Scholar 

  • Haynes RJ (1980) Ion exchange properties of roots and ionic interactions within the root apoplasm: their role in ion accumulation by plants. Botanical Reviews 46: 75–99

    Article  CAS  Google Scholar 

  • Hecht-Buchholz C, Brady DJ, Asher CJ, Edwards DG (1990) Effects of low activities of aluminium on soybean (Glycine max) II. Root cell structure and root hair development. In: van Beusichem ML (Ed) Plant nutrition–physiology and applications. Kluwer Academic, Haren, pp 335–343

    Chapter  Google Scholar 

  • Horst WJ (1995) The role of the apoplast in aluminum toxicity and resistance of higher plants: a review. Zeitschrift für Pflanzenerährung and Bodenkunde 158: 419–428

    Article  CAS  Google Scholar 

  • Horst WJ, Wagner A, Marschner H (1982) Mucilage protects root meristems from aluminium in-jury. Proceedings of the 9th International Plant Nutrition Colloquium, Warwick, 238–243

    Google Scholar 

  • Horst WJ, Asher CJ, Cakmak I, Szulkiewicz P, Wissemeier AH (1992) Short-term responses of soy-bean roots to aluminum. Journal of Plant Nutrition 140: 174–178

    CAS  Google Scholar 

  • Horst WJ, Puschel AK, Schmohl N (1997) Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant and Soil 192: 23–30

    Article  CAS  Google Scholar 

  • Ishikawa H, Evans ML (1995) Specialized zones of development in roots. Plant Physiology 109: 725–727

    PubMed  CAS  Google Scholar 

  • Jackson ML (1963) Aluminum bonding in soils: A unifying principle in soil science. Soil Science Society of America Proceedings 27: 1–10

    Article  CAS  Google Scholar 

  • Jardine PM, Zelazny LW (1986) Mononuclear and polynuclear aluminum speciation through dif-ferential kinetic reactions with ferron. Soil Science Society of America Journal 50: 895–900

    Article  CAS  Google Scholar 

  • Jones DL, Shaff JE, Kochian LV (1995) Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. Planta 197: 672–680

    Article  CAS  Google Scholar 

  • Keltj ens WG (1995) Magnesium uptake by Al-stressed maize plants with special emphasis on cation interactions at root exchange sites. Plant and Soil 171: 141–146

    Article  CAS  Google Scholar 

  • Kerridge PC (1969) Aluminum toxicity in wheat (Triticum aestivum Vill. Host) Ph. D. Thesis, Oregon State University (Dissertation Abstracts B29, 3159 )

    Google Scholar 

  • Kerven GL, Edwards DG, Asher CJ, Hallman PS, Kokot S (1988) Aluminium determination in soil solution. II. Short term colorimetric procedures for the measurement of inorganic monomeric aluminum in the presence of organic acid ligands.Australian Journal of Soil Research 27: 91–102

    Google Scholar 

  • Kerven GL, Larsen PL, Blarney FPC (1995) Detrimental sulfate effects on formation of Al-13 tridecameric polycation in synthetic soil solutions. Soil Science Society of America Journal 59: 765–771

    Article  CAS  Google Scholar 

  • Kinraide TB (1988) Proton extrusion by wheat roots exhibiting severe Al toxicity symptoms. Plant Physiology 88: 418–423

    Article  PubMed  CAS  Google Scholar 

  • Kinraide TB (1990) Assessing the rhizotoxicity of the aluminate ion, Al(OH)4. Plant Physiology 93: 1620–1625

    Article  PubMed  CAS  Google Scholar 

  • Kinraide TB (1991) Identity of the rhizotoxic aluminium species. In: Wright RJ, Baligar VC, Murrmann RP (Eds) Plant-soil Interactions at Low pH. Developments in Plant and Soil Sciences. Kluwer Academic, Dordrecht, pp 717–728

    Google Scholar 

  • Kinraide TB (1993) Aluminium enhancement of plant growth in acid rooting media. A case of reciprocal alleviation of toxicity by two toxic cations. Physiologia Plantarum 88: 619–625

    Article  CAS  Google Scholar 

  • Kinraide TB (1997) Reconsidering the rhizotoxicity of hydroxyl, sulfate, and fluoride complexes of aluminium. Journal of Experimental Botany 48: 1115–1124

    Article  CAS  Google Scholar 

  • Kinraide TB, Parker DR (1987) Non-phytotoxicity of the aluminum sulphate ion,A1SO4’. Physiologia Plantarum 71: 207–212

    Article  CAS  Google Scholar 

  • Kinraide TB, Parker DR (1990) Apparent phytotoxicity of mononuclear hydroxy-aluminum to four dicotyledonous species. Physiologia Plantarum 79: 283–288

    Article  CAS  Google Scholar 

  • Klimashevskii EL, Dedov VM (1980) Characteristics of an elastic cell wall of the root in relation to genotypic variance of plant resistance to aluminum ions. Izv Sib. Otd. Akad. Nauk SSSR, Ser. Biol. Nauk 1:108–112 (Chemical Abstracts 93 (15): 416–417 )

    Google Scholar 

  • Knight AH, Crooke WM, Inkson RHE (1961) Cation-exchange capacities of tissues of higher and lower plants and their related uronic acid contents. Nature 192: 142–143

    Article  PubMed  CAS  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 46: 237–260

    Article  CAS  Google Scholar 

  • Lance JC, Pearson RW (1969) Effect of low concentrations of aluminum on growth and water and nutrient uptake by cotton roots. Soil Science Society of America Proceedings 33: 95–98

    Article  CAS  Google Scholar 

  • Larsen PL, Kerven GL, Bell LC, Edwards DG (1995) Effects of silicic acid on the chemistry of monomeric and polymeric (A113) aluminium species in solutions. In: Date RA, Grundon NJ, Rayment GE, Probert ME (Eds) Plant-soil interactions at low pH: Principles and management. Kluwer Academic, Dordrecht, pp 617–621

    Chapter  Google Scholar 

  • Lazof DB, Goldsmith JG, Rufty TW, Linton RW (1994) Rapid uptake of aluminum into cells of intact soybean root tips. A microanalytical study using secondary ion mass spectrometry. Plant Physiology 106: 1107–1114

    Google Scholar 

  • Lindsay WL (1979) Chemical equilibria in soils. John Wiley and Sons, New York

    Google Scholar 

  • Macdonald TL, Martin RB (1988) Aluminum ion in biological systems. Trends in Biochemical Sciences 13: 15–19

    Article  PubMed  CAS  Google Scholar 

  • Martin RB (1994) Aluminum: A neurotoxic product of acid rain. Accounts of Chemical Research. 27: 204–210

    Article  CAS  Google Scholar 

  • Matsumoto H (1994) Comparison of the early response to aluminum stress between tolerant and sensitive wheat cultivars: Root growth, aluminum content and efflux of K *. Journal of Plant Nutrition 17: 1257–1288

    Article  Google Scholar 

  • Matsumoto H, Hirasawa E, Morimura S, Takahashi E (1976) Localization of aluminum in tea leaves. Plant and Cell Physiology 17: 627–631

    CAS  Google Scholar 

  • Menzies NW (1991) Solution phase aluminium in highly weathered soils: evaluation and relation- ship to aluminum toxicity to plants. PhD Thesis. The University of Queensland, Brisbane

    Google Scholar 

  • Menzies NW, Bell LC, Edwards DG (1991a) A simple positive pressure apparatus for the ultra- filtration of soil solution. Communications in Soil Science and Plant Analysis 22: 137–145

    Article  CAS  Google Scholar 

  • Menzies NW, Bell LC, Edwards DG (1991b) Characteristics of membrane filters in relation to aluminium studies in soil solutions and natural waters. Journal of Soil Science 42: 585–597

    Article  CAS  Google Scholar 

  • Menzies NW, Bell LC, Edwards DG (1991c) Effects of incubation time and filtration technique on soil solution composition with particular reference to inorganic and organically complexed Al. Australian Journal of Soil Research 29: 223–238

    Article  CAS  Google Scholar 

  • Nieboer E, Richardson DHS (1980) The replacement of the nondescript term `heavy metals’ by a biologically and chemically significant classification of metal ions. Environmental Pollution 1: 3–26

    CAS  Google Scholar 

  • Noble AD, Sumner ME (1988) Calcium and Al interactions and soybean growth in nutrient solutions. Communications in Soil Science and Plant Analysis 19: 1119–1131

    Article  CAS  Google Scholar 

  • Ostatek-Boczynski Z, Kerven GL, Blamey FPC (1995) Aluminium reactions with polygalacturonate and related organic ligands. Plant and Soil 171: 41–45

    Article  CAS  Google Scholar 

  • Parker DR, Bertsch PM (1992) Identification and quantification of the “A113” tridecameric polycation using ferron. Environmental Science and Technology 26: 908–914

    Article  CAS  Google Scholar 

  • Parker DR, Kinraide TB, Zelazny LW (1989) On the phytotoxicity of polynuclear hydroxy-aluminum complexes. Soil Science Society of America Journal 53: 789–796

    Article  CAS  Google Scholar 

  • Parker DR, Norvell WA, Chaney RL (1995) GEOCHEM-PC: A chemical speciation program for IBM and compatible personal computers. In: Loeppert RH, Schwab AP, Goldberg S (Eds) Soil chemical equilibrium and reaction models. Soil Science Society of America, Inc, Madison, pp 253–269

    Google Scholar 

  • Passioura JB, Stirzaker RJ (1993) Feedforward responses of plants to physically inhospitable soil. In: Buxton DR, Shibles R, Forsberg RA, Blad BL,Asay KH, Paulsen GM, Wilson RF (Eds) International crop science I. Crop Science Society of America, Inc., Madison, pp 715–719

    Google Scholar 

  • Pritchard J (1994) The control of cell expansion in roots. New Phytologist 127: 2–26

    Article  Google Scholar 

  • Rengel Z (1990) Competitive Al“ inhibition of net Mg” uptake by intact Lolium multiforum roots. II. Plant age effects. Plant Physiology 93: 1261–1267

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rengel Z, Reid RJ (1997) Uptake of Al across the plasma membrane of plant cells. Plant and Soil 192: 31–35

    Article  CAS  Google Scholar 

  • Rengel Z, Robinson DL (1989) Aluminum and plant age effects on adsorption of cations in the Donnan free space of ryegrass roots. Plant and Soil 116: 223–227

    Article  CAS  Google Scholar 

  • Rengel Z, Robinson DL (1990) Competitive Al’ inhibition of net Mgt uptake by intact Lolium multiflorum roots. I. Kinetics. Plant Physiology 91: 1407–1413

    Google Scholar 

  • Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminium toxicity in roots: An investigation of spatial sensitivity and the role of the root cap. Journal of Experimental Botany 44: 437–446

    Google Scholar 

  • Sasaki K, Nagahashi G (1989) Autolysis-like release of pectic polysaccharides from regions of cell walls other than the middle lamella. Plant and Cell Physiology 30: 1159–1169

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sposito G (1995) The environmental chemistry of aluminum. 2nd ed, CRC Lewis, Boca Raton Steudle E, French J (1996) Water transport in plants: Role of the apoplast. Plant and Soil 187: 67–79

    Google Scholar 

  • Tan K, Keltjens WG (1995) Analysis of acid-soil stress in sorghum genotypes with emphasis on aluminium and magnesium interactions. Plant and Soil 171: 147–150

    Article  CAS  Google Scholar 

  • Tan K, Keltjens WG, Findenegg GR (1992) Acid soil damage in sorghum genotypes: Role of magnesium deficiency and root impairment. Plant and Soil 139: 149–155

    Google Scholar 

  • Taylor GJ (1991) Current views of the aluminum stress response; the physiological basis of tolerance. Current Topics in Plant Biochemistry and Physiology 10: 57–93

    CAS  Google Scholar 

  • Tice KR, Parker DR, DeMason DA (1992) Operationally defined apoplastic and symplastic alumi-num fractions in root tips of aluminum-intoxicated wheat. Plant Physiology 100: 309–318

    Article  PubMed  CAS  Google Scholar 

  • Vose PB, Randall PJ (1962) Resistance to aluminium and manganese toxicities in plants related to variety and cation exchange capacity. Nature 196: 85–86

    Article  CAS  Google Scholar 

  • Wissemeier AH, Horst WJ (1995) Effect of calcium supply on aluminum-induced callose formation, its distribution and persistence in roots of soybean (Glycine max ( L.) Merr.). Journal of Plant Physiology 145: 470–476

    Google Scholar 

  • Wissemeier AH, Klotz F, Horst WJ (1987) Aluminum induced callose synthesis in roots of soybean (Glycine max L.). Journal of Plant Physiology 129: 487–492

    Article  CAS  Google Scholar 

  • Wood M, Cooper JE (1984) Aluminium toxicity and multiplication of Rhizobium trifolii in a defined growth medium. Soil Biology and Biochemistry 16: 571–576

    Article  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 Physiology 91: 1094–1099

    Article  PubMed  CAS  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

Blamey, F.P.C. (2001). The Role of the Root Cell Wall in Aluminum Toxicity. 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_9

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-66902-9_9

  • 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