Aluminum Stress Adaptation in Plants pp 229-251

Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 24) | Cite as

Specificity of Ion Uptake and Homeostasis Maintenance During Acid and Aluminium Stresses

  • Jayakumar Bose
  • Olga Babourina
  • Yanling Ma
  • Meixue Zhou
  • Sergey Shabala
  • Zed Rengel


Low pH (proton toxicity) and aluminium toxicity coexist in acid soils, affecting plant growth worldwide. Decades of research concluded that proton and aluminium toxicity mechanisms are complex and remain unclear. Among the Al tolerance mechanisms, exudation of organic acid anions received considerable attention, leading to the identification of novel genes involved in organic acid anion metabolism and transport. As a downside, the major focus on exudation of organic acid anions has overshadowed research on other potential Al tolerance mechanisms (e.g. reduced cell wall binding, rhizosphere alkalisation, phosphate exudation, enhanced uptake of essential nutrients) that may be operating. In this work, the current knowledge on how proton and aluminium toxicity and tolerance mechanisms are operating when plants are exposed to acid soils is reviewed. Special emphasis has been given to the question of how uptake and homeostasis of hydrogen, potassium, phosphorus, calcium, and magnesium ions in plants are affected and regulated during low-pH and aluminium stresses. There is enough evidence to suggest that low-pH and combined low-pH/aluminium stresses differentially affect root tissues and, consequently, the rhizosphere. Less disturbed phosphorus, calcium, and magnesium uptake and homeostasis maintenance help plants to cope with low-pH and combined low-pH/aluminium stresses.


H+ fluxes K+ fluxes Ca2+ fluxes Mg2+ fluxes Ion homeostasis Cytoplasmic pH Cytoplasmic Ca2+ Cytoplasmic Mg2+ 


  1. Ahn SJ, Matsumoto H (2006) The role of the plasma membrane in the response of plant roots to aluminum toxicity. Plant Signal Behav 1:37–45PubMedCentralPubMedCrossRefGoogle Scholar
  2. Ahn SJ, Sivaguru M, Osawa H, Chung GC, Matsumoto H (2001) Aluminum inhibits the H+-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots. Plant Physiol 126:1381–1390PubMedCentralPubMedCrossRefGoogle Scholar
  3. Ahn SJ, Sivaguru M, Chung GC, Rengel Z, Matsumoto H (2002) Aluminium-induced growth inhibition is associated with impaired efflux and influx of H+ across the plasma membrane in root apices of squash (Cucurbita pepo). J Exp Bot 53:1959–1966PubMedCrossRefGoogle Scholar
  4. Ahn SJ, Shin R, Schachtman DP (2004) Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol 134:1135–1145PubMedCentralPubMedCrossRefGoogle Scholar
  5. Akeson MA, Munns DN, Burau RG (1989) Adsorption of Al3+ to phosphatidylcholine vesicles. Biochim Biophys Acta 986:33–40PubMedCrossRefGoogle Scholar
  6. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1994) Molecular biology of the cell. Garland Publishing, New York, NYGoogle Scholar
  7. Amenos M, Corrales I, Poschenrieder C, Illes P, Baluska F, Barcelo J (2009) Different effects of aluminum on the actin cytoskeleton and brefeldin A-sensitive vesicle recycling in root apex cells of two maize varieties differing in root elongation rate and aluminum tolerance. Plant Cell Physiol 50:528–540PubMedCrossRefGoogle Scholar
  8. Andreev IM (2001) Functions of the vacuole in higher plant cells. Russ J Plant Physiol 48:672–680CrossRefGoogle Scholar
  9. Babourina O, Rengel Z (2009) Uptake of aluminium into Arabidopsis root cells measured by fluorescent lifetime imaging. Ann Bot 104:189–195PubMedCentralPubMedCrossRefGoogle Scholar
  10. Babourina O, Ozturk L, Cakmak I, Rengel Z (2006) Reactive oxygen species production in wheat roots is not linked with changes in H+ fluxes during acidic and aluminium stresses. Plant Signal Behav 1:71–76PubMedCentralPubMedCrossRefGoogle Scholar
  11. Baluška F, Mancuso S, Volkmann D, Barlow P (2004) Root apices as plant command centres: the unique ‘brain-like’ status of the root apex transition zone. Biologia (Bratislava) 59:7–19Google Scholar
  12. Bibikova T, Gilroy S (2002) Root hair development. J Plant Growth Regul 21:383–415CrossRefGoogle Scholar
  13. Blamey FPC (2001) The role of the root cell wall in aluminum toxicity. In: Ae N, Arihara J, Okada K, Srinivasan A (eds) Plant nutrient acquisition: new perspectives. Springer, Tokyo, pp 201–226CrossRefGoogle Scholar
  14. Bolan NS, Hedley MJ, White RE (1991) Processes of soil acidification during nitrogen cycling with emphasis on legume based pastures. Plant Soil 134:53–63CrossRefGoogle Scholar
  15. Boscolo PRS, Menossi M, Jorge RA (2003) Aluminum-induced oxidative stress in maize. Phytochemistry 62:181–189PubMedCrossRefGoogle Scholar
  16. Bose J, Babourina O, Shabala S, Rengel Z (2010a) Aluminium-induced ion transport in Arabidopsis: the relationship between Al tolerance and root ion flux. J Exp Bot 61:3163–3175PubMedCentralPubMedCrossRefGoogle Scholar
  17. Bose J, Babourina O, Shabala S, Rengel Z (2010b) Aluminum dependent dynamics of ion transport in Arabidopsis: specificity of low pH and aluminum responses. Physiol Plant 139:401–412PubMedGoogle Scholar
  18. Bose J, Babourina O, Rengel Z (2011a) Role of magnesium in alleviation of aluminium toxicity in plants. J Exp Bot 62:2251–2264PubMedCrossRefGoogle Scholar
  19. Bose J, Pottosin I, Shabala SS, Palmgren MG, Shabala S (2011b) Calcium efflux systems in stress signalling and adaptation in plants. Front Plant Sci 2:85PubMedCentralPubMedCrossRefGoogle Scholar
  20. Bose J, Babourina O, Shabala S, Rengel Z (2013) Low-pH and aluminium resistance in Arabidopsis correlates with high cytosolic magnesium content and increased magnesium uptake by plant roots. Plant Cell Physiol 54:1093–1104PubMedCrossRefGoogle Scholar
  21. Brady NC, Weil RR (1990) Nature and properties of soils. Macmillan, New York, NYGoogle Scholar
  22. Brady DJ, Edwards DG, Asher CJ, Blamey FPC (1993) Calcium amelioration of aluminum toxicity effects on root hair development in soybean [Glycine max (L) Merr]. New Phytol 123:531–538CrossRefGoogle Scholar
  23. Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Biol 46:95–122CrossRefGoogle Scholar
  24. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468CrossRefGoogle Scholar
  25. Chen ZC, Ma JF (2013) Magnesium transporters and their role in Al tolerance in plants. Plant Soil 368:51–56CrossRefGoogle Scholar
  26. Chen JP, Sucoff EI, Stadelmann EJ (1991) Aluminum and temperature alteration of cell membrane permeability of Quercus rubra. Plant Physiol 96:644–649PubMedCentralPubMedCrossRefGoogle Scholar
  27. Chen ZC, Yamaji N, Motoyama R, Nagamura Y, Ma JF (2012) Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol 159:1624–1633PubMedCentralPubMedCrossRefGoogle Scholar
  28. Clarkson DT (1965) The effect of aluminium and some other trivalent metal cations on cell division in the root apices of Allium cepa. Ann Bot 29:309–315Google Scholar
  29. Clarkson DT (1984) Calcium transport between tissues and its distribution in the plant. Plant Cell Environ 7:449–456CrossRefGoogle Scholar
  30. Clarkson DT (1985) Factors affecting mineral nutrient acquisition by plants. Annu Rev Plant Biol 36:77–115CrossRefGoogle Scholar
  31. Darko E, Ambrus H, Stefanovits-Banyai E, Fodor J, Bakos F, Barnaba B (2004) Aluminium toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. Plant Sci 166:583–591CrossRefGoogle Scholar
  32. Davies DD (1986) The fine control of cytosolic pH. Physiol Plant 67:702–706CrossRefGoogle Scholar
  33. De Campos JMS, Viccini LF (2003) Cytotoxicity of aluminum on meristematic cells of Zea mays and Allium cepa. Caryologia 56:65–73CrossRefGoogle Scholar
  34. De Cnodder T, Vissenberg K, Van Der Straeten D, Verbelen JP (2005) Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid: a matter of apoplastic reactions. New Phytol 168:541–550PubMedCrossRefGoogle Scholar
  35. Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321PubMedCentralPubMedGoogle Scholar
  36. Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR, Richardson AE (2009) Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotech J 7:391–400CrossRefGoogle Scholar
  37. Demidchik V, Bowen HC, Maathuis FJM, Shabala SN, Tester MA, White PJ, Davies JM (2002) Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. Plant J 32:799–808PubMedCrossRefGoogle Scholar
  38. Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. J Cell Sci 116:81–88PubMedCrossRefGoogle Scholar
  39. Deng W, Luo K, Li D, Zheng X, Wei X, Smith W, Thammina C, Lu L, Li Y, Pei Y (2006) Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. J Exp Bot 57:4235–4243PubMedCrossRefGoogle Scholar
  40. Ding JP, Badot PM, Pickard BG (1993) Aluminium and hydrogen ions inhibit a mechanosensory calcium-selective cation channel. Aust J Plant Physiol 20:771–778PubMedCrossRefGoogle Scholar
  41. Dolan L, Davies J (2004) Cell expansion in roots. Curr Opin Plant Biol 7:33–39PubMedCrossRefGoogle Scholar
  42. Doncheva S, Amenos M, Poschenrieder C, Barcelo J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot 56:1213–1220PubMedCrossRefGoogle Scholar
  43. DuPont FM, Bush DS, Windle JJ, Jones RL (1990) Calcium and proton transport in membrane vesicles from barley roots. Plant Physiol 94:179–188PubMedCentralPubMedCrossRefGoogle Scholar
  44. Evans DE, Briars SA, Williams LE (1991) Active calcium transport by plant cell membranes. J Exp Bot 42:285–303CrossRefGoogle Scholar
  45. Exley C (2004) The pro-oxidant activity of aluminum. Free Rad Biol Med 36:380–387PubMedCrossRefGoogle Scholar
  46. Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–666PubMedCentralPubMedCrossRefGoogle Scholar
  47. Facanha AR, Okorokova-Facanha AL (2002) Inhibition of phosphate uptake in corn roots by aluminum-fluoride complexes. Plant Physiol 129:1763–1772PubMedCentralPubMedCrossRefGoogle Scholar
  48. Ferguson IB, Clarkson DT (1975) Ion transport and endodermal suberization in the roots of Zea mays. New Phytol 75:69–79CrossRefGoogle Scholar
  49. Ferguson IB, Clarkson DT (1976) Simultaneous uptake and translocation of magnesium and calcium in barley (Hordeum vulgare L.) roots. Planta 128:267–269PubMedCrossRefGoogle Scholar
  50. Ferrufino A, Smyth TJ, Israel DW, Carter TE Jr (2000) Root elongation of soybean genotypes in response to acidity constraints in a subsurface solution compartment. Crop Sci 40:413CrossRefGoogle Scholar
  51. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  52. Foy CD (1988) Plant adaptation to acid, aluminum-toxic soils. Commun Soil Sci Plant Anal 19:959–987CrossRefGoogle Scholar
  53. Foy CD, Duke JA, Devine TE (1992) Tolerance of soybean germplasm to an acid Tatum subsoil. J Plant Nutr 15:527–547CrossRefGoogle Scholar
  54. Frensch J (1997) Primary responses of root and leaf elongation to water deficits in the atmosphere and soil solution. J Exp Bot 48:985–999Google Scholar
  55. Fukuda T, Saito A, Wasaki J, Shinano T, Osaki M (2007) Metabolic alterations proposed by proteome in rice roots grown under low P and high Al concentration under low pH. Plant Sci 172:1157–1165CrossRefGoogle Scholar
  56. Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (P-32) uptake from soil. Plant Soil 198:147–152CrossRefGoogle Scholar
  57. Galloway JN (1989) Atmospheric acidification: projections for the future. Ambio 18:161–166Google Scholar
  58. Gassmann W, Schroeder JI (1994) Inward-rectifying K+ channels in root hairs of wheat – a mechanism for aluminum-sensitive low-affinity K+ uptake and membrane-potential control. Plant Physiol 105:1399–1408PubMedCentralPubMedGoogle Scholar
  59. Gerendas J, Ratcliffe RG, Sattelmacher B (1990) 31P nuclear magnetic resonance evidence for differences in intracellular pH in the roots of maize seedlings grown with nitrate or ammonium. J Plant Physiol 137:125–128CrossRefGoogle Scholar
  60. Godbold DL, Jentschke G (1998) Aluminium accumulation in root cell walls coincides with inhibition of root growth but not with inhibition of magnesium uptake in Norway spruce. Physiol Plant 102:553–560CrossRefGoogle Scholar
  61. Göransson A, Eldhuset TD (1995) Effects of aluminium ions on uptake of calcium, magnesium and nitrogen in Betula pendula seedlings growing at high and low nutrient supply rates. Water Air Soil Pollut 83:351–361CrossRefGoogle Scholar
  62. Goulding KWT, Bailey NJ, Bradbury NJ, Hargreaves P, Howe M, Murphy DV, Poulton PR, Willison TW (1998) Nitrogen deposition and its contribution to nitrogen cycling and associated soil processes. New Phytol 139:49–58CrossRefGoogle Scholar
  63. Grimme H (1983) Aluminium induced magnesium deficiency in oats. Zeitsch Pflanzenern Bodenk 146:666–676CrossRefGoogle Scholar
  64. Guo KM, Babourina O, Christopher DA, Borsic T, Rengel Z (2010) The cyclic nucleotide-gated channel AtCNGC10 transports Ca2+ and Mg2+ in Arabidopsis. Physiol Plant 139:303–312PubMedGoogle Scholar
  65. Haynes R, Mokolobate M (2001) Amelioration of Al toxicity and P deficiency in acid soils by additions of organic residues: a critical review of the phenomenon and the mechanisms involved. Nutr Cycl Agroecosyst 59:47–63CrossRefGoogle Scholar
  66. Hirschi K (2001) Vacuolar H+/Ca2+ transport: who’s directing the traffic? Trends Plant Sci 6:100–104PubMedCrossRefGoogle Scholar
  67. Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL (2000) Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210:329–335PubMedCrossRefGoogle Scholar
  68. Horst WJ, Asher CJ, Cakmak I, Szulkiewicz P, Wissemeier AH (1992) Short-term responses of soybean roots to aluminum. J Plant Physiol 140:174–178CrossRefGoogle Scholar
  69. Horst WJ, Kollmeier M, Schmohl N, Sivaguru M, Wang Y, Felle HH, Hedrich R, Schröder W, Staß A (2007) Significance of the root apoplast for aluminium toxicity and resistance of maize. In: Sattelmacher B, Horst WJ (eds) The apoplast of higher plants: compartment of storage, transport and reactions. Springer, Dordrecht, pp 49–66CrossRefGoogle Scholar
  70. Huang JW, Shaff JE, Grunes DL, Kochian LV (1992) Aluminum effects on calcium fluxes at the root apex of aluminum-tolerant and aluminum-sensitive wheat cultivars. Plant Physiol 98:230–237PubMedCentralPubMedCrossRefGoogle Scholar
  71. Huang JW, Pellet DM, Papernik LA, Kochian LV (1996) Aluminum interactions with voltage-dependent calcium transport in plasma membrane vesicles isolated from roots of aluminum-sensitive and-resistant wheat cultivars. Plant Physiol 110:561–569PubMedCentralPubMedCrossRefGoogle Scholar
  72. Illes P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluska F, Ovecka M (2006) Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production. J Exp Bot 57:4201–4213PubMedCrossRefGoogle Scholar
  73. Ishikawa S, Adu-Gyamfi J, Nakamura T, Yoshihara T, Watanabe T, Wagatsuma T (2002) Genotypic variability in phosphorus solubilizing activity of root exudates by pigeonpea grown in low-nutrient environments. In: Adu-Gyamfi JJ (ed) Food security in nutrient-stressed environments: exploiting plants’ genetic capabilities. Kluwer Academic, Dordrecht, pp 111–121. doi:10.1007/978-94-017-1570-6_13 CrossRefGoogle Scholar
  74. Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S, Kobayashi Y, Ikka T, Hirayama T, Shinozaki K, Kobayashi M (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci U S A 104:9900–9905PubMedCentralPubMedCrossRefGoogle Scholar
  75. Jemo M, Abaidoo RC, Nolte C, Horst WJ (2007) Aluminum resistance of cowpea as affected by phosphorus-deficiency stress. J Plant Physiol 164:442–451PubMedCrossRefGoogle Scholar
  76. Johnson VJ, Tsunoda M, Murray TF, Sharma RP (2005) Decreased membrane fluidity and hyperpolarization in aluminum-treated PC-12 cells correlates with increased production of cellular oxidants. Environ Toxicol Pharmacol 19:221–230PubMedCrossRefGoogle Scholar
  77. Jones DL, Shaff JE, Kochian LV (1995) Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. Planta 197:672–680CrossRefGoogle Scholar
  78. Jones DL, Gilroy S, Larsen PB, Howell SH, Kochian LV (1998a) Effect of aluminum on cytoplasmic Ca2+ homeostasis in root hairs of Arabidopsis thaliana (L.). Planta 206:378–387PubMedCrossRefGoogle Scholar
  79. Jones DL, Kochian LV, Gilroy S (1998b) Aluminum induces a decrease in cytosolic calcium concentration in BY-2 tobacco cell cultures. Plant Physiol 116:81–89PubMedCentralCrossRefGoogle Scholar
  80. Jones DL, Blancaflor EB, Kochian LV, Gilroy S (2006) Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ 29:1309–1318PubMedCrossRefGoogle Scholar
  81. Keltjens WG (1988) Short-term effects of Al on nutrient uptake, H+ efflux, root respiration and nitrate reductase activity of two sorghum genotypes differing in Al-susceptibility. Commun Soil Sci Plant Anal 19:1155–1163CrossRefGoogle Scholar
  82. Keltjens WG, Tan K (1993) Interactions between aluminium, magnesium and calcium with different monocotyledonous and dicotyledonous plant species. Plant Soil 155–156:485–488CrossRefGoogle Scholar
  83. Kidd PS, Proctor J (2001) Why plants grow poorly on very acid soils: are ecologists missing the obvious? J Exp Bot 52:791–799PubMedCrossRefGoogle Scholar
  84. Kiegle E, Gilliham M, Haseloff J, Tester M (2000) Hyperpolarisation-activated calcium currents found only in cells from the elongation zone of Arabidopsis thaliana roots. Plant J 21:225–229PubMedCrossRefGoogle Scholar
  85. Kinraide TB (1990) Assessing the rhizotoxicity of the aluminate ion, Al(OH)4 -. Plant Physiol 93:1620–1625PubMedCentralPubMedCrossRefGoogle Scholar
  86. Kinraide TB (1991) Identity of the rhizotoxic aluminium species. Plant Soil 134:167–178Google Scholar
  87. Kinraide TB (1993) Aluminum enhancement of plant growth in acid rooting media – a case of reciprocal alleviation of toxicity by 2 toxic cations. Physiol Plant 88:619–625CrossRefGoogle Scholar
  88. Kinraide TB (1994) Use of a Gouy-Chapman-Stern model for membrane-surface electrical potential to interpret some features of mineral rhizotoxicity. Plant Physiol 106:1583–1592PubMedCentralPubMedGoogle Scholar
  89. Kinraide TB (2001) Ion fluxes considered in terms of membrane-surface electrical potentials. Aust J Plant Physiol 28:605–616Google Scholar
  90. Kinraide TB, Ryan PR, Kochian LV (1992) Interactive effects of Al3+, H+, and other cations on root elongation considered in terms of cell-surface electrical potential. Plant Physiol 99:1461–1468PubMedCentralPubMedCrossRefGoogle Scholar
  91. Kinraide TB, Pedler JF, Parker DR (2004) Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH. Plant Soil 259:201–208CrossRefGoogle Scholar
  92. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260CrossRefGoogle Scholar
  93. Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493PubMedCrossRefGoogle Scholar
  94. Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195CrossRefGoogle Scholar
  95. Kollmeier M, Felle HH, Horst WJ (2000) Genotypical differences in aluminum resistance 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 122:945–956PubMedCentralPubMedCrossRefGoogle Scholar
  96. Kurkdjian A, Guern J (1989) Intracellular pH: measurement and importance in cell activity. Annu Rev Plant Biol 40:271–303CrossRefGoogle Scholar
  97. Lee J, Pritchard M (1984) Aluminium toxicity expression nutrient uptake, growth and root morphology of Trifolium repens L. cv. ‘Grasslands Huia’. Plant Soil 82:101–116CrossRefGoogle Scholar
  98. Lenoble ME, Blevins DG, Sharp RE, Cumbie BG (1996) Prevention of aluminium toxicity with supplemental boron. I. Maintenance of root elongation and cellular structure. Plant Cell Environ 19:1132–1142CrossRefGoogle Scholar
  99. Li L, Tutone AF, Drummond RSM, Gardner RC, Luan S (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13:2761–2775PubMedCentralPubMedCrossRefGoogle Scholar
  100. Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. Exudation of specific organic acids from different regions of the intact root system. Plant Physiol 141:674–684PubMedCentralPubMedCrossRefGoogle Scholar
  101. Ligaba A, Yamaguchi M, Shen H, Sasaki T, Yamamoto Y, Matsumoto H (2004) Phosphorus deficiency enhances plasma membrane H+-ATPase activity and citrate exudation in greater purple lupin(Lupinus pilosus). Funct Plant Biol 31:1075–1083CrossRefGoogle Scholar
  102. Lindberg S (1990) Aluminium interactions with K+ (86Rb+) and 45Ca2+ fluxes in three cultivars of sugar beet (Beta vulgaris). Physiol Plant 79:275–282CrossRefGoogle Scholar
  103. Lindberg S, Strid H (1997) Aluminium induces rapid changes in cytosolic pH and free calcium and potassium concentrations in root protoplasts of wheat (Triticum aestivum). Physiol Plant 99:405–414CrossRefGoogle Scholar
  104. Liu K, Luan S (2001) Internal aluminum block of plant inward K+ channels. Plant Cell 13:1453–1465PubMedCentralPubMedCrossRefGoogle Scholar
  105. Lopez-Bucio J, Nieto-Jacobo MF, Ramırez-Rodrıguez V, Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160:1–13PubMedCrossRefGoogle Scholar
  106. Ma JF (2007) Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int Rev Cytol 264:225–253PubMedCrossRefGoogle Scholar
  107. Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278PubMedCrossRefGoogle Scholar
  108. Ma Q, Rengel Z, Kuo J (2002) Aluminium toxicity in rye (Secale cereale): root growth and dynamics of cytoplasmic Ca2+ in intact root tips. Ann Bot 89:241–244PubMedCentralCrossRefGoogle Scholar
  109. Ma JF, Shen R, Nagao S, Tanimoto E (2004) Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. Plant Cell Physiol 45:583–589PubMedCrossRefGoogle Scholar
  110. MacDiarmid CW, Gardner RC (1998) Overexpression of the Saccharomyces cerevisiae magnesium transport system confers resistance to aluminum ion. J Biol Chem 273:1727–1732PubMedCrossRefGoogle Scholar
  111. Maguire ME, Cowan JA (2002) Magnesium chemistry and biochemistry. Biometals 15:203–210PubMedCrossRefGoogle Scholar
  112. Mannion AM (1998) Global environmental change: the causes and consequences of disruption to biogeochemical cycles. Geogr J 164:168–182CrossRefGoogle Scholar
  113. Mariano ED, Keltjens WG (2005) Long-term effects of aluminum exposure on nutrient uptake by maize genotypes differing in aluminum resistance. J Plant Nutr 28:323–333CrossRefGoogle Scholar
  114. Marschner H (1991) Mechanisms of adaptation of plants to acid soils. Plant Soil 134:1–20Google Scholar
  115. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  116. Marty F (1999) Plant vacuoles. Plant Cell 11:587–600PubMedCentralPubMedCrossRefGoogle Scholar
  117. Matsumoto H (1988) Inhibition of proton transport activity of microsomal membrane vesicles of barley roots by aluminum. Soil Sci Plant Nutr 34:499–506CrossRefGoogle Scholar
  118. Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46PubMedCrossRefGoogle Scholar
  119. Matsumoto H, Yamaya T (1986) Inhibition of potassium uptake and regulation of membrane-associated Mg2+-ATPase activity of pea roots by aluminum. Soil Sci Plant Nutr 32:179–188CrossRefGoogle Scholar
  120. Matsumoto H, Hirasawa E, Torikai H, Takahashi E (1976) Localization of absorbed aluminium in pea root and its binding to nucleic acids. Plant Cell Physiol 17:127–137Google Scholar
  121. Matsumoto H, Yamamoto Y, Kasai M (1992) Changes of some properties of the plasma membrane-enriched fraction of barley roots related to aluminum stress: membrane-associated ATPase, aluminum and calcium. Soil Sci Plant Nutr 38:411–419CrossRefGoogle Scholar
  122. Meriga B, Krishna Reddy B, Rajender Rao K, Ananda Reddy L, Kavi Kishor PB (2004) Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161:63–68PubMedCrossRefGoogle Scholar
  123. Miedema H, Bothwell JHF, Brownlee C, Davies JM (2001) Calcium uptake by plant cells–channels and pumps acting in concert. Trends Plant Sci 6:514–519PubMedCrossRefGoogle Scholar
  124. Miyasaka SC, Kochian LV, Shaff JE, Foy CD (1989) Mechanisms of aluminum tolerance in wheat – an investigation of genotypic differences in rhizosphere pH, K+, and H+ transport, and root cell membrane potentials. Plant Physiol 91:1188–1196PubMedCentralPubMedCrossRefGoogle Scholar
  125. Morimura E, Takahashi E, Matsumoto H (1978) Association of aluminium with nuclei and inhibition of cell division in onion (Allium cepa) roots. Zeitschr Pflanzenphysiol 88:395–408CrossRefGoogle Scholar
  126. Mugwira LM, Patel SU, Fleming AL (1980) Aluminium effects on growth and Al, Ca, Mg, K and P levels in triticale, wheat and rye. Plant Soil 57:467–470CrossRefGoogle Scholar
  127. Newman IA (2001) Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant Cell Environ 24:1–14PubMedCrossRefGoogle Scholar
  128. Nichol BE, Oliveira LA, Glass ADM, Siddiqi MY (1993) 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 101:1263–1266PubMedCentralPubMedGoogle Scholar
  129. Olivetti GP, Cumming JR, Etherton B (1995) Membrane-potential depolarization of root cap cells precedes aluminum tolerance in snapbean. Plant Physiol 109:123–129Google Scholar
  130. Ono K, Yamamoto Y, Hachiya A, Matsumoto H (1995) Synergistic inhibition of growth by aluminum and iron of tobacco (Nicotiana tabacum L.) cells in suspension culture. Plant Cell Physiol 36:115–125Google Scholar
  131. Osawa H, Matsumoto H (2002) Aluminium triggers malate-independent potassium release via ion channels from the root apex in wheat. Planta 215:405–412PubMedCrossRefGoogle Scholar
  132. Parker JS, Cavell AC, Dolan L, Roberts K, Grierson CS (2000) Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 12:1961–1974PubMedCentralPubMedCrossRefGoogle Scholar
  133. Pineros M, Tester M (1993) Plasma-membrane Ca2+ channels in roots of higher plants and their role in aluminum toxicity. Plant Soil 156:119–122CrossRefGoogle Scholar
  134. Pineros M, Tester M (1997) Calcium channels in higher plant cells: selectivity, regulation and pharmacology. J Exp Bot 48:551–577PubMedCrossRefGoogle Scholar
  135. Plieth C, Sattelmacher B, Hansen UP, Knight MR (1999) Low-pH-mediated elevations in cytosolic calcium are inhibited by aluminium: a potential mechanism for aluminium toxicity. Plant J 18:643–650PubMedCrossRefGoogle Scholar
  136. Poschenrieder C, Gunsé B, Corrales I, Barceló J (2008) A glance into aluminum toxicity and resistance in plants. Sci Total Environ 400:356–368PubMedCrossRefGoogle Scholar
  137. Poschenrieder C, Amenos M, Corrales I, Doncheva S, Barcelo J (2009) Root behavior in response to aluminum toxicity. In: Baluska F (ed) Plant-environment interactions. Springer, Berlin, pp 21–43CrossRefGoogle Scholar
  138. Reid RJ, Tester MA, Smith FA (1995) Calcium/aluminium interactions in the cell wall and plasma membrane of Chara. Planta 195:362–368Google Scholar
  139. Rengel Z (1990) Competitive Al3+ inhibition of net Mg2+ uptake by intact Lolium multiflorum roots: II. Plant age effects. Plant Physiol 93:1261–1267PubMedCentralPubMedCrossRefGoogle Scholar
  140. Rengel Z (1992) Role of calcium in aluminium toxicity. New Phytol 121:499–513CrossRefGoogle Scholar
  141. Rengel Z (1994) Effects of Al, rare earth elements, and other metals on net 45Ca2+ uptake by Amaranthus protoplasts. J Plant Physiol 143:47–51CrossRefGoogle Scholar
  142. Rengel Z (1996) Uptake of aluminium by plant cells. New Phytol 134:389–406CrossRefGoogle Scholar
  143. Rengel Z (2004) Aluminium cycling in the soil-plant-animal-human continuum. Biometals 17:669–689PubMedCrossRefGoogle Scholar
  144. Rengel Z, Elliott DC (1992) Mechanism of aluminum inhibition of net 45Ca2+ uptake by Amaranthus protoplasts. Plant Physiol 98:632–638PubMedCentralPubMedCrossRefGoogle Scholar
  145. Rengel Z, Robinson DL (1989) Competitive Al3+ inhibition of net Mg2+ uptake by intact Lolium multiflorum roots: I. Kinetics. Plant Physiol 91:1407–1413PubMedCentralPubMedCrossRefGoogle Scholar
  146. Rengel Z, Zhang WH (2003) Role of dynamics of intracellular calcium in aluminium toxicity syndrome. New Phytol 159:295–314CrossRefGoogle Scholar
  147. Rengel Z, Pineros M, Tester M (1995) Transmembrane calcium fluxes during Al stress. Plant Soil 171:125–130CrossRefGoogle Scholar
  148. Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418PubMedCentralPubMedCrossRefGoogle Scholar
  149. Rincon-Zachary M, Teaster ND, Sparks JA, Valster AH, Motes CM, Blancaflor EB (2010) Fluorescence resonance energy transfer-sensitized emission of Yellow Cameleon 3.60 reveals root zone-specific calcium signatures in Arabidopsis in response to aluminum and other trivalent cations. Plant Physiol 152:1442–1458PubMedCentralPubMedCrossRefGoogle Scholar
  150. Ritchey KD, Carter TE (1993) Emergence and growth of two non-nodulated soybean genotypes (Glycine max (L.) Merr.) in response to soil acidity. Plant Soil 151:175–183CrossRefGoogle Scholar
  151. Roos W, Viehweger K, Dordschbal B, Schumann B, Evers S, Steighardt J, Schwartze W (2006) Intracellular pH signals in the induction of secondary pathways – the case of Eschscholzia californica. J Plant Physiol 163:369–381PubMedCrossRefGoogle Scholar
  152. Rowell DL, Wild A (1985) Causes of soil acidification: a summary. Soil Use Manag 1:32–33CrossRefGoogle Scholar
  153. Ryan PR, Kochian LV (1993) Interaction between aluminum toxicity and calcium uptake at the root apex in near-isogenic lines of wheat (Triticum aestivum L.) differing in aluminum tolerance. Plant Physiol 102:975–982PubMedCentralPubMedGoogle Scholar
  154. Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44:437–446CrossRefGoogle Scholar
  155. Ryan PR, Delhaize E, Randall PJ (1995) Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103–110CrossRefGoogle Scholar
  156. Ryan PR, Reid RJ, Smith FA (1997) Direct evaluation of the Ca2+-displacement hypothesis for Al toxicity. Plant Physiol 113:1351–1357PubMedCentralPubMedGoogle Scholar
  157. Sano T, Becker D, Ivashikina N, Wegner LH, Zimmermann U, Roelfsema MRG, Nagata T, Hedrich R (2007) Plant cells must pass a K+ threshold to re-enter the cell cycle. Plant J 50:401–413PubMedCrossRefGoogle Scholar
  158. Sasaki M, Kasai M, Yamamoto Y, Matsumoto H (1995) Involvement of plasma membrane potential in the tolerance mechanism of plant roots to aluminum toxicity. Plant Soil 171:119–124CrossRefGoogle Scholar
  159. Sawaki Y, Iuchi S, Kobayashi Y, Kobayashi Y, Ikka T, Sakurai N, Fujita M, Shinozaki K, Shibata D, Kobayashi M, Koyama H (2009) STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol 150:281–294PubMedCentralPubMedCrossRefGoogle Scholar
  160. Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–427CrossRefGoogle Scholar
  161. Schofield RMS, Pallon J, Fiskesjö G, Karlsson G, Malmqvist KG (1998) Aluminum and calcium distribution patterns in aluminum-intoxicated roots of Allium cepa do not support the calcium-displacement hypothesis and indicate signal-mediated inhibition of root growth. Planta 205:175–180CrossRefGoogle Scholar
  162. Scholz-Starke J, Gambale F, Carpaneto A (2005) Modulation of plant ion channels by oxidizing and reducing agents. Arch Biochem Biophys 434:43–50PubMedCrossRefGoogle Scholar
  163. Shen H, Yan X, Zhao M, Zheng S, Wang X (2002) Exudation of organic acids in common bean as related to mobilization of aluminum-and iron-bound phosphates. Environ Exp Bot 48:1–9CrossRefGoogle Scholar
  164. Shen J, Tang C, Rengel Z, Zhang F (2004) Root-induced acidification and excess cation uptake by N2-fixing Lupinus albus grown in phosphorus-deficient soil. Plant Soil 260:69–77CrossRefGoogle Scholar
  165. Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296PubMedCentralPubMedCrossRefGoogle Scholar
  166. Silva IR, Smyth TJ, Moxley DF, Carter TE, Allen NS, Rufty TW (2000) Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol 123:543–552PubMedCentralPubMedCrossRefGoogle Scholar
  167. Šimonovicová M, Huttova J, Mistrik I, Široká B, Tamas L (2004a) Peroxidase mediated hydrogen peroxide production in barley roots grown under stress conditions. Plant Growth Regul 44:267–275CrossRefGoogle Scholar
  168. Šimonovicová M, Huttová J, Mistrik I, Široká B, Tamas L (2004b) Root growth inhibition by aluminum is probably caused by cell death due to peroxidase-mediated hydrogen peroxide production. Protoplasma 224:91–98PubMedGoogle Scholar
  169. Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol 116:155–163PubMedCentralCrossRefGoogle Scholar
  170. Sivaguru M, Baluska F, Volkmann D, Felle HH, Horst WJ (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 119:1073–1082PubMedCentralPubMedCrossRefGoogle Scholar
  171. Sivaguru M, Fujiwara T, Samaj J, Baluska 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 124:991–1006PubMedCentralPubMedCrossRefGoogle Scholar
  172. Sivaguru M, Pike S, Gassmann W, Baskin TI (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44:667–675PubMedCrossRefGoogle Scholar
  173. Street HE (1966) The physiology of root growth. Annu Rev Plant Physiol 17:315–344CrossRefGoogle Scholar
  174. Subbarao GV, Ae N, Otani T (1997) Genotypic variation in iron-, and aluminum-phosphate solubilizing activity of pigeonpea root exudates under P deficient conditions. Soil Sci Plant Nutr 43:295–305CrossRefGoogle Scholar
  175. Tabuchi A, Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol Plant 112:353–358PubMedCrossRefGoogle Scholar
  176. Tahara K, Yamanoshita T, Norisada M, Hasegawa I, Kashima H, Sasaki S, Kojima K (2008) Aluminum distribution and reactive oxygen species accumulation in root tips of two Melaleuca trees differing in aluminum resistance. Plant Soil 307:167–178CrossRefGoogle Scholar
  177. Tamás L, Šimonoviová M, Huttová J, Mistrik I (2004) Aluminium stimulated hydrogen peroxide production of germinating barley seeds. Environ Exp Bot 51:281–288CrossRefGoogle Scholar
  178. Tang C, Raphael C, Rengel Z, Bowden JW (2000) Understanding subsoil acidification: effect of nitrogen transformation and nitrate leaching. Austr J Soil Res 38:837–850CrossRefGoogle Scholar
  179. Tanoi K, Junko H, Kazutoshi S, Yoshitake H, Hiroki N, Tomoko MN (2005) Analysis of potassium uptake by rice roots treated with aluminum using a positron emitting nuclide, 38K. Soil Sci Plant Nutr 51:715–717CrossRefGoogle Scholar
  180. Taylor GJ, McDonald-Stephens JL, Hunter DB, Bertsch PM, Elmore D, Rengel Z, Reid RJ (2000) Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol 123:987–996PubMedCentralPubMedCrossRefGoogle Scholar
  181. Valadez-Gonzalez N, Colli-Mull JG, Brito-Argaez L, Muñoz-Sánchez JA, Aguilar JJZ, Castano E, Hernández-Sotomayor SMT (2007) Differential effect of aluminum on DNA synthesis and CDKA activity in two Coffea arabica cell lines. J Plant Growth Regul 26:69–77CrossRefGoogle Scholar
  182. Very A-A, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci U S A 97:9801–9806PubMedCentralPubMedCrossRefGoogle Scholar
  183. Vries W, Breeuwsma A (1987) The relation between soil acidification and element cycling. Water Air Soil Poll 35:293–310CrossRefGoogle Scholar
  184. Wang H, Inukai Y, Yamauchi A (2006) Root development and nutrient uptake. Crit Rev Plant Sci 25:279–301CrossRefGoogle Scholar
  185. Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26:1515–1523CrossRefGoogle Scholar
  186. Webb AAR, McAinsh MR, Taylor JE, Hetherington AM (1996) Calcium ions as intracellular second messengers in higher plants. Adv Bot Res 22:45–96CrossRefGoogle Scholar
  187. Wherrett T, Ryan PR, Delhaize E, Shabala S (2005) Effect of aluminium on membrane potential and ion fluxes at the apices of wheat roots. Funct Plant Biol 32:199–208CrossRefGoogle Scholar
  188. White PJ (1998) Calcium channels in the plasma membrane of root cells. Ann Bot 81:173–183CrossRefGoogle Scholar
  189. Yamamoto Y, Hachiya A, Matsumoto H (1997) Oxidative damage to membranes by a combination of aluminum and iron in suspension-cultured tobacco cells. Plant Cell Physiol 38:1333–1339CrossRefGoogle Scholar
  190. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72PubMedCentralPubMedCrossRefGoogle Scholar
  191. Yan X, Lynch JP, Beebe SE (1995) Genetic variation for phosphorus efficiency of common bean in contrasting soil types: I. Vegetative response. Crop Sci 35:1086CrossRefGoogle Scholar
  192. 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 115:1119–1125PubMedCentralPubMedGoogle Scholar
  193. Zhang WH, Rengel Z (1999) Aluminium induces an increase in cytoplasmic calcium in intact wheat root apical cells. Austr J Plant Physiol 26:401–410CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Jayakumar Bose
    • 1
    • 2
  • Olga Babourina
    • 1
  • Yanling Ma
    • 2
  • Meixue Zhou
    • 2
  • Sergey Shabala
    • 2
  • Zed Rengel
    • 1
  1. 1.School of Earth and EnvironmentUniversity of Western AustraliaCrawleyAustralia
  2. 2.School of Land and FoodUniversity of TasmaniaHobartAustralia

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