Role of dynamics of intracellular calcium in aluminium-toxicity syndrome

New Phytologist

Volumn 159, Issue 2, 2003, Pages 295-314

  Rengel, Z ^a   Zhang, W H ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Aluminium (Al); Calcium (Ca); Callose; Cytoplasmic Ca2+ homeostasis; Cytoskeleton; H+ ATPase; Plasma membrane; Secondary messenger system

Indexed keywords

ALUMINUM; CALCIUM; PHYTOTOXICITY;

EID: 0042463698     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1469-8137.2003.00821.x     Document Type: Review

References (227)

1. +-ATPase of cucumber root system in response to low root temperature. Plant Cell Reports 19: 831-835.
2. + across the plasma membrane in root apices of squash (Cucurbita pepo). Journal of Experimental Botany 53: 1959-1966.
3. +-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots. Plant Physiology 126: 1381-1390.
4. 3+ to phosphatidylcholine vesicles. Biochimica et Biophysica Acta 986: 33-40.
5. Alessa L, Oliveira L. 2001. Aluminum toxicity studies in Vaucheria longicaulis var. macounii (Xanthophyta, Tribophyceae). II. Effects on the F-actin array. Environmental and Experimental Botany 45: 223-237.
6. 2+ diffusion. Philosophical Transactions of the Royal Society of London, Series B 338: 53-61.
7. 2+-permeable slow vacuolar ion channel of stomatal guard cells. Plant Cell 7: 1473-1483.
8. Axelsen KB, Palmgren MG. 2001. Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiology 126: 696-706.
9. Barcelo J, Poschenrieder C. 2002. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environmental and Experimental Botany 48: 75-92.
10. Barcelo J, Poschenrieder C, Vazquez MD, Gunse B. 1996. Aluminium phytotoxicity: a challenge for plant scientists. Fertilizer Research 43: 217-223.
11. Bibikova TN, Zhigilei A, Gilroy S. 1997. Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203: 495-505.
12. Blamey FPC. 2001. The role of the root cell wall in aluminum toxicity. In: Ae N, Arihara J, Okada K, Srinivasan A, eds. Plant nutritent acquisition. New perspectives. Tokyo, Japan: Springer-Verlag, 201-226.
13. Blamey FPC, Dowling AJ. 1995. Antagonism between aluminium and calcium for sorption by calcium pectate. Plant and Soil 171: 137-140.
14. Blamey 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.
15. Blancaflor EB, Jones DL, Gilroy S. 1998. Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiology 118: 159-172.
16. 2+ by the carboxyl terminus of beta-tubulin. Plant, Cell & Environment 19: 539-548.
17. Bolan NS, Hedley MJ. 2003. Role of carbon, nitrogen and sulfur cycles in soil acidification. In: Rengel Z, ed. Handbook of soil acidity. New York, NY, USA: Marcel Dekker, 29-56.
18. Bolan NS, Hedley MJ, White RE. 1991. Processes of soil acidification during nitrogen cycling with emphasis on legume based pasture. Plant and Soil 134: 53-63.
19. Bowler C, Van Montagu M, Inze D. 1992. Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43: 83-116.
20. Bush DS. 1995. Calcium regulation in plant cells and its role in signalling. Annual Review of Plant Physiology and Plant Molecular Biology 46: 95-122.
21. Bush DS. 1996. Effects of gibberellic acid and environmental factors on cytosolic calcium in wheat aleurone cells. Planta 199: 89-99.
22. Cakmak I, Horst WJ. 1991. Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum 83: 463-468.
23. Caldwell CR. 1989. Analysis of aluminum and divalent cation binding to wheat root plasma membrane proteins using terbium phosphorescence. Plant Physiology 91: 233-241.
24. 3-mobilizable calcium in plant cells? Plant Science 90: 135-143.
25. Carpita NC, Gibeaut DM. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant Journal 3: 1-30.
26. 2+ from internal stores. Planta 214: 126-134.
27. Chang YC, Yamamoto Y, Matsumoto H. 1999. Enhancement of callose production by a combination of aluminum and iron in suspension-cultured tobacco (Nicotiana tabacum) cells. Soil Science and Plant Nutrition 45: 337-347.
28. Clarkson DT. 1984. Calcium transport between tissues and its distribution in the plant. Plant, Cell & Environment 7: 449-456.
29. Collet L, de Leon C, Kollmeier M, Schmohl N, Horst WJ. 2002. Assessment of aluminum sensitivity of maize cultivars using roots of intact plants and excised root tips. Journal of Plant Nutrition and Soil Science 165: 357-365.
30. Cosgrove DJ. 1997. Creeping walls, softening fruit, and penetrating pollen tubes: the growing roles of expansins. Proceedings of the National Academy of Sciences, USA 94: 5504-5505.
31. Coventry DR, Slattery WJ. 1991. Acidification of soil associated with lupins grown in a crop rotation in north-eastern Victoria. Australian Journal of Agricultural Research 42: 391-397.
32. + from the plasmalemma of root cells. A primary response to salt stress. Plant Physiology 79: 207-211.
33. Delhaize E. 1995. Genetic control and manipulation of root exudates. In: Johansen C, Lee KK, Sharma KK, Subbarao GV, Kueneman EA, eds. Genetic manipulation of crop plants to enhance integrated nutrient management in cropping systems. 1. Phosphorus. Proceedings of an FAO/ICRISAT Expert Consultancy Workshop, 15-18 March 1994. Patancheru, Andhra Pradesh, India: International Crops Research Institute for the Semi-Arid Tropics, 5-152.
34. 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.
35. Demidchik V, Bowen HC, Maathuis FJM, Shabala SN, Tester MA, White PJ, Davies JM. 2002a. Arabidopsis thaliana root nonselective cation channels mediate calcium uptake and are involved in growth. Plant Journal 32: 799-808.
36. Demidchik V, Davenport RJ, Tester M. 2002b. Nonselective cation channels in plants. Annual Review of Plant Biology 53: 67-107.
37. +-permeable channels in plant root cells. Journal of Cell Science 116: 81-88.
38. Dennison KL, Spalding EP. 2000. Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiology 124: 1511-1514.
39. DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, Thompson JE, Prestwich GD, Hama H. 2001. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiology 126: 759-769.
40. Ding JP, Badot P-M, Pickard BG. 1993. Aluminium and hydrogen ions inhibit a mechanosensory calcium-selective cation channel. Australian Journal of Plant Physiology 20: 771-778.
41. Ding JP, Pickard BG. 1993. Mechanosensory calcium-selective cation channels in epidermal cells. Plant Journal 3: 83-110.
42. Dobrovinskaya OR, Muniz J, Pottosin II. 1999. Inhibition of vacuolar ion channels by polyamines. Journal of Membrane Biology 167: 127-140.
43. DuPont FM, Bush DS, Winle JJ, Jones RL. 1990. Calcium and proton transport in membrane vesicles from barley roots. Plant Physiology 94: 179-188.
44. Evans DE, Briars SA, Williams LE. 1991. Active calcium transport by plant cell membranes. Journal of Experimental Botany 42: 285-303.
45. 2+-selective microelectrode tests and fura-dextran ratio imaging. Plant Physiology 114: 39-45.
46. Foy CD. 1988. Plant adaptation to acid, aluminum-toxic soils. Communications in Soil Science and Plant Analysis 19: 959-987.
47. Foyer CH, Descourvieres P, Kunert KJ. 1994. Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant, Cell & Environment 17: 507-523.
48. Frantzios G, Galatis B, Apostolakos P. 2000. Aluminium effects on microtubule organization in dividing root-tip cells of Triticum turgidum. I. Mitotic cells. New Phytologist 145: 211-224.
49. Frantzios G, Galatis B, Apostolakos P. 2001. Aluminium effects on microtubule organization in dividing root-tip cells of Triticum turgidum. II. Cytokinetic cells. Journal of Plant Research 114: 157-170.
50. Fricker MD, Oparka KJ. 1999. Imaging techniques in plant transport: meeting review. Journal of Experimental Botany 50: 1089-1100.
51. Gilroy S. 1997. Fluorescence microscopy of living plant cells. Annual Review of Plant Physiology and Plant Molecular Biology 48: 165-190.
52. Gilroy S, Bethke PC, Jones RL. 1993. Calcium homeostasis in plants. Journal of Cell Science 106: 453-462.
53. 2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiology 116: 429-437.
54. Grabski S, Arnoys E, Busch B, Schindler M. 1998. Regulation of actin tension in plant cells by kinases and phosphatases. Plant Physiology 116: 279-290.
55. Grabski S, Schindler M. 1995. Aluminum induces rigor within the actin network of soybean cells. Plant Physiology 108: 897-901.
56. Grabski S, Xie XG, Holland JF, Schindler M. 1994. Lipids trigger changes in the elasticity of the cytoskeleton in plant cells: a cell optical displacement assay for live cell measurements. Journal of Cell Biology 126: 713-726.
57. Greulich KO, Pilarczyk G, Hoffmann A, Horste GMZ, Schafer B, Uhl V, Monajembashi S. 2000. Micromanipulation by laser microbeam and optical tweezers: from plant cells to single molecules. Journal of Microscopy 198: 182-187.
58. Hamilton CA, Good AG, Taylor GJ. 2001. Induction of vacuolar ATPase and mitochondrial ATP synthase by aluminum in an aluminum-resistant cultivar of wheat. Plant Physiology 125: 2068-2077.
59. Hanson JB. 1984. The functions of calcium in plant nutrition. Advances in Plant Nutrition 1: 149-208.
60. Haug A. 1984. Molecular aspects of aluminum toxicity. Critical Reviews in Plant Sciences 1: 345-373.
61. Haug A, Shi B, Vitorello V. 1994. Aluminum interaction with phosphoinositide-associated signal transduction. Archives of Toxicology 68: 1-7.
62. Hepler PK, Wayne RO. 1985. Calcium and plant development. Annual Review of Plant Physiology 36: 397-439.
63. 2+ and pH. New Phytologist 129: 523-533.
64. Heslop-Harrison J. 1987. Pollen germination and pollen tube growth. International Review of Cytology 107: 1-78.
65. 2+ transport: who's directing the traffic. Trends in Plant Science 6: 100-104.
66. Holdaway-Clarke TL, Feijo JA, Hackett GR, Kunkel JG, Hepler PK. 1997. Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9: 1999-2010.
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: 329-335.
68. Horst WJ. 1995. The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Zeitschrift für Pflanzenernährung und Bodenkunde 158: 419-428.
69. 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.
70. Horst WJ, Schmohl N, Kollmeier M, Baluska F, Sivaguru M. 1999. Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant and Soil 215: 163-174.
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 Physiology 110: 561-569.
72. 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 Physiology 98: 230-237.
73. +-ATPases in the plasma membrane: physiology and molecular biology. In: Rengel Z, ed. Handbook of plant growth. pH as the master variable. New York, NY, USA: Marcel Dekker, 1-22.
74. 2+-ATPase activity in plant cells under chilling stress: a comparative study between the chilling-sensitive maize and the chilling-insensitive winter wheat. Plant and Cell Physiology 40: 1061-1071.
75. 2+ homeostasis in root hairs of Arabidopsis thaliana (L). Planta 206: 378-387.
76. Jones DL, Kochian LV. 1995. Aluminum inhibition of the inositol 1,4,5-triphosphate signal transduction pathway in wheat roots: a role in aluminum toxicity? Plant Cell 7: 1913-1922.
77. Jones DL, Kochian LV. 1997. Aluminum interaction with plasma membrane lipids and enzyme metal binding sites and its potential role in Al cytotoxicity. FEBS Letters 400: 51-57.
78. Jones DL, Kochian LV, Gilroy S. 1998b. Aluminum induces a decrease in cytosolic calcium concentration in BY-2 tobacco cell cultures. Plant Physiology 116: 81-89.
79. Jones DL, Shaff JE, Kochian LV. 1995. Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. I. Inhibition of tip growth by aluminum. Planta 197: 672-680.
80. Jorge RA, Menossi M, Arruda P. 2001. Probing the role of calmodulin in Al toxicity in maize. Phytochemistry 58: 415-422.
81. Jorns AC, Hecht-Buchholz C, Wissemeier AH. 1991. Aluminium-induced callose formation in root tips of Norway spruce (Picea abies (L.) Karst.). Zeitschrift für Pflanzenernährung und Bodenkunde 154: 349-353.
82. Kauss H. 1987. Some aspects of calcium-dependent regulation in plant metabolism. Annual Review of Plant Physiology 38: 47-72.
83. 2+ uptake and callose synthesis in suspension-cultured cells of Catharanthus roseus are decreased by the protein phosphatase inhibitor okadaic acid. Physiologia Plantarum 81: 309-312.
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 Journal 21: 225-229.
85. Kinraide TB. 1998. Three mechanisms for the calcium alleviation of mineral toxicides. Plant Physiology 118: 513-520.
86. Kinraide TB, Parker DR. 1987. Cation amelioration of aluminum toxicity in wheat. Plant Physiology 83: 546-551.
87. +, and other cations on root elongation considered in terms of cell-surface electrical potential. Plant Physiology 99: 1461-1468.
88. 2+-displacement hypothesis. Planta 192: 104-109.
89. Kinraide TB, Yermiyahu U, Rytwo G. 1998. Computation of surface electrical potentials of plant cell membranes. Correspondence published zeta potentials from diverse plant sources. Plant Physiology 118: 505-512.
90. Klusener B, Weiler EW. 1999. A calcium-selective channel from root-tip endomembranes of garden cress. Plant Physiology 119: 1399-1405.
91. Klusener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugouvieux V, Schroeder JI. 2002. Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiology 130: 2152-2163.
92. Klyubin I, Kirpichnikova KM, Gamaley IA. 1996. Hydrogen peroxide-induced chemotaxis of mouse peritoneal neutrophils. European Journal of Cell Biology 70: 347-351.
93. Knight H. 2000. Calcium signalling during abiotic stress in plants. International Review of Cell Biology 195: 269-324.
94. Knight MR. 2002. Signal transduction leading to low-temperature tolerance in Arabidopsis thaliana. Philosophical Transactions of the Royal Society of London, Series B 357: 871-875.
95. Knight H, Brandt S, Knight MR. 1998. A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant Journ 16: 681-687.
96. Knight MR, Campbell AK, Smith SM, Trewavas AJ. 1991. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352: 524-526.
97. Knight MR, Read ND, Campbell AK, Trewavas AJ. 1993. Imaging calcium dynamics in living plants using semi-synthetic recombinant aequorins. Journal of Cell Biology 121: 83-90.
98. Knight MR, Smith SM, Trewavas AJ. 1992. Wind-induced plant motion immediately increases cytosolic calcium. Proceedings of the National Academy of Sciences, SA 89: 4967-4971.
99. Knight H, Trewavas AJ, Knight MR. 1996. Cold calcium signalling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8: 489-503.
100. Knight H, Trewavas AJ, Knight MR. 1997. Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant Journal 12: 1067-1078.
101. Kochian LV. 1995. Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 46: 237-260.
102. Kochian LV, Jones DL. 1997. Aluminum toxicity and resistance in plants. In: Yokel RA, Golub MS, eds. Research issues in aluminum toxicity. London, UK: Taylor & Francis, 69-89.
103. Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R. 2001. Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum-resistant cultivar. Plant Physiology 126: 397-410.
104. 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 Physiology 122: 945-956.
105. Larkindale J, Knight MR. 2002. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology 128: 682-695.
106. Lazof DB, Holland MJ. 1999. Evaluation of the aluminium-induced root growth inhibition in isolation from low pH effects in Glycine max, Pisum sativum and Phaseolus vulgaris. Australian Journal of Plant Physiology 26: 147-157.
107. - influx in roots of two soybean genotypes differing in Al tolerance. Plant and Soil 164: 291-297.
108. Le Van H, Kuraishi S, Sakurai N. 1994. Aluminum-induced rapid root inhibition and changes in cell-wall components of squash seedlings. Plant Physiology 106: 971-976.
109. Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A. 2002. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14: 2627-2641.
110. 2+ in Arabidopsis roots changes in response to touch but not gravity. Plant Physiology 114: 789-800.
111. 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). Physiologia Plantarum 99: 405-414.
112. Lindberg S, Szynkier K, Greger M. 1991. Aluminum effects on transmembrane potential in cells of fibrous roots of sugar beet. Physiologia Plantarum 83: 54-62.
113. Loneragan JF, Snowball K. 1969. Calcium requirement of plants. Australian Journal of Agricultural Research 20: 465-478.
114. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W. 2002. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14: s389-s400.
115. Ma JF. 2000. Role of organic acids in detoxification of aluminum in higher plants. Plant and Cell Physiology 41: 383-390.
116. 2+ in intact root tips. Annals of Botany 89: 241-244.
117. Ma JF, Ryan PR, Delhaize E. 2001. Aluminium tolerance in plants and the complexing role of organic adds. Trends in Plant Science 6: 273-278.
118. Mahler RL, Halvorson AR, Koehler FE. 1985. Long-term acidification of farmland in northern Idaho and eastern Washington. Communications in Soil Science and Plant Analysis 16: 83-95.
119. Malho R, Trewavas AJ. 1996. Localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8: 1935-1949.
120. Massot N, Llugany M, Poschenrieder C, Barcelo J. 1999. Callose production as indicator of aluminum toxicity in bean cultivars. Journal of Plant Nutrition 22: 1-10.
121. Matsumoto H. 1988. Inhibition of proton transport activity of microsomal membrane vesicles of barley roots by aluminum. Soil Science and Plant Nutrition 34: 499-506.
122. Matsumoto H. 2000. Cell biology of aluminum toxicity and tolerance in higher plants. International Review of Cytology 200: 1-46.
123. 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 Science and Plant Nutrition 38: 411-419.
124. May HM, Nordstrom DK. 1991. Assessing the solubilities and reaction kinetics of aluminous minerals in soils. In: Ulrich B, Sumner ME, eds. Soil acidic. Berlin, Germany: Springer Verlag, 125-148.
125. McAinsh MR, Clayton H, Mansfield TA, Hetherington AM. 1996. Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiology 111: 1031-1042.
126. Miedema H, Bothwell JHF, Brownlee C, Davies JM. 2001. Calcium uptake by plant cells - channels and pumps acting in concert. Trends in Plant Science 6: 514-519.
127. + transport, and root-cell membrane potentials. Plant Physiology 91: 1188-1196.
128. 2+ elevations in root endodermal cells subjected to cooling. Plant Journal 30: 457-465.
129. +-ATPase: structure, function and regulation. Biochimica et Biophysica Acta 1645: 1-16.
130. 2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abil-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13: 2513-2523.
131. Nakamura C, Van Telgen HJ, Mennes AM, Ono H, Libbenga KR. 1988. Correlation between auxin resistance and the lack of a membrane-bound auxin binding protein and a root-specific peroxidase in Nicotiana tabacum. Plant Physiology 88: 845-849.
132. Nichol BE, Oliveira LA. 1995. Effects of aluminum on the growth and distribution of calcium in roots of an aluminum-sensitive cultivar of barley (Hordeum vulgare) . Canadian Journal of Botany 73: 1849-1858.
133. 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 Physiology 101: 1263-1266.
134. Ozaki S, DeWald DB, Shope JC, Chen J, Prestwich GD. 2000. Intracellular delivery of phosphoinositides and inositol phosphates using polyamine carriers. Proccedings of the National Academy of Sciences, USA 97: 11286-11291.
135. +-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Physiology and Plant Molecular Biology 52: 817-845.
136. Pandey S, Tiwari SB, Upadhyaya KC, Sopory SK. 2000. Calcium signalling: linking environmental signals to cellular functions. Critical Reviews in Plant Sciences 19: 291-318.
137. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731-734.
138. Pellet DM, Grunes DL, Kochian LV. 1995. Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L). Planta 196: 788-795.
139. Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C. 2002. Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant Journal 32: 539-548.
140. Pierson ES, Miller DD, Callaham DA, Shipley AM, Rivers BA, Cresti M, Hepler PK. 1994. Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell 6: 1815-1828.
141. 3+-induced anion channels. Plant Physiology 125: 292-305.
142. 2+-selective channel from wheat roots. Planta 195: 478-488.
143. Piñeros M, Tester M. 1997. Calcium channels in higher plant cells: selectivity, regulation and pharmacology. Journal of Experimental Botany 48: 551-577.
144. Plieth C. 2001. Plant calcium signaling and monitoring: pros and cons and recent experimental approaches. Protoplasma 218: 1-23.
145. 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 Journal 18: 643-650.
146. Poovaiah BW, Reddy ASN. 1987. Calcium messenger system in plants. Critical Reviews in Plant Sciences 6: 47-103.
147. Poovaiah BW, Reddy ASN. 1993. Calcium and signal transduction in plants. Critical Reviews in Plant Sciences 12: 185-211.
148. Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ, Knight MR. 1994. Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6: 1301-1310.
149. Read ND, Allan WTG, Knight H, Knight MR, Malho R, Russell A, Shaddock PS, Trewavas AJ. 1992. Imaging and measurement of cytosolic free calcium in plant and fungal cells. Journal of Microscopy 166: 57-86.
150. Reid RJ, Tester MA, Smith FA. 1995. Calcium/aluminium interactions in the cell wall and plasma membrane of Chara. Planta 195: 362-368.
151. 2+ homeostasis as a primary trigger in the Al toxicity syndrome. Plant, Cell & Environment 15: 931-938.
152. Rengel Z. 1992b. Role of calcium in aluminium toxicity. New Phytologist 121: 499-513.
153. Rengel Z. 1992c. The role of calcium in salt toxicity. Plant, Cell & Environment 15: 625-632.
154. 2+ uptake by Amaranthus protoplasts. Journal of Plant Physiology 143: 47-51.
155. Rengel Z. 1996. Tansley Review, 89: Uptake of aluminium by plant cells. New Phytologist 134: 389-406.
156. Rengel Z. 2000. Relationship between cytosolic calcium activity and toxicity of aluminium to plant cells. In: International Symposium on Impact of Potential Tolerance of Plants on the Increased Productivity under Aluminum Stress. Institute for Bioresources, Okayama University, Kurashiki, Japan, 15-18.
157. 2+ uptake by Amaranthus protoplasts. Biochemie und Physiologie der Pflanzen 188: 177-186.
158. 2+ uptake by Amaranthus protoplasts. Plant Physiology 98: 632-638.
159. Rengel Z, Piñeros M, Tester M. 1995. Transmembrane calcium fluxes during Al stress. Plant and Soil 171: 125-130.
160. Rengel Z, Robinson DL. 1989a. Aluminum and plant age effects on adsorption of cations in the Donnan free space of ryegrass roots. Plant and Soil 116: 223-227.
161. Rengel Z, Robinson DL. 1989b. Aluminum effects on growth and macronutrient uptake by annual ryegrass. Agronomy Journal 81: 208-215.
162. Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC. 1998. Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiology 116: 409-418.
163. Rincón M, Gonzales RA. 1992. Aluminum partitioning in intact roots of aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars. Plant Physiology 99: 1021-1028.
164. Roos W. 2000. Ion mapping in plant cells - methods and applications in signal transduction research. Planta 210: 347-370.
165. Roy SJ, Holdaway-Clarke TL, Hackett GR, Kunkel JG, Lord EM, Hepler PK. 1999. Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis. Plant Journal 19: 379-386.
166. Rudd JJ, Franklin-Tong VE. 1999. Calcium signaling in plants. Cellular and Molecular Life Sciences 55: 214-232.
167. Runge M, Rode MW. 1991. Effects of soil acidity on plant association. In: Ulrich B, Sumner ME, eds. Soil acidity. Berlin/Heidelberg, Germany: Springer-Verlag, 183-202.
168. Ryan PR, Delhaize E, Randall PJ. 1995a. Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196: 103-110.
169. Ryan PR, Delhaize E, Randall PJ. 1995b. Malate efflux from root apices and tolerance to aluminium are highly correlated in wheat. Australian Journal of Plant Physiology 22: 531-536.
170. 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.
171. 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 Physiology 102: 975-982.
172. 2+-displacement hypothesis for Al toxicity. Plant Physiology 113: 1351-1357.
173. Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman SD. 1997b. Aluminum activates an anion channel in the apical cells of wheat roots. Proceedings of the National Academy of Sciences, USA 94: 6547-6552.
174. Samuels TD, Kucukakyuz K, Rincon ZM. 1997. Al partitioning patterns and root growth as related to Al sensitivity and Al tolerance in wheat. Plant Physiology 113: 527-534.
175. Sanders D, Pelloux J, Brownlee C, Harper JF. 2002. Calcium at the crossroads of signaling. Plant Cell 14: s401-s417.
176. Sasaki M, Kasai M, Yamamoto Y, Matsumoto H. 1995. Involvement of plasma membrane potential in the tolerance mechanism of plant roots to aluminium toxicity. Plant and Soil 171: 119-124.
177. Schmohl N, Horst WJ. 2000. Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant, Cell & Environment 23: 735-742.
178. Schofield RMS, Pallon J, Fiskesjo 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: 175-180.
179. Schwarzerova K, Zelenkova S, Nick P, Opatrny Z. 2002. Aluminum-induced rapid changes in the microtubular cytoskeleton of tobacco cell lines. Plant and Cell Physiology 43: 207-216.
180. 2+ responses to anoxia in Arabidopsis thaliana seedlings. Plant Physiology 111: 243-257.
181. Serrano R. 1990. Plasma membrane ATPase. In: Larsson C, Møller IM, eds The plant plasma membrane. Berlin, Germany: Springer-Verlag, 127-153.
182. Shi B, Chou K, Haug A. 1993. Aluminum impacts elements of the phosphoinositide signalling pathway in neuroblastoma cells. Molecular and Cellular Biochemistry 121: 109-118.
183. 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 Physiology 123: 543-552.
184. Sivaguru M, Baluska F, Volkmann D, Felle HH, Horst WJ. 1999a. Impacts of aluminum on the cytoskeleton of the maize root apex. Short-term effects on the distal part of the transition zone. Plant Physiology 119: 1073-1082.
185. Sivaguru M, Fujiwara T, Samaj J, Baluska F, Yang ZM, 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 Physiology 124: 991-1005.
186. 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.
187. Sivagurn M, Yamamoto Y, Matsumoto H. 1999b. Differential impacts of aluminium on microtubule organisation depends on growth phase in suspension-cultured tobacco cells. Physiologia Plantarum 107: 110-119.
188. Snedden WA, Fromm H. 1998. Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends in Plant Science 3: 299-304.
189. Snedden WA, Fromm H. 2001. Calmodulin as a versatile calcium signal transducer in plants. New Phytologist 151: 35-66.
190. Suhayda CG, Giannini JL, Briskin DP, Shannon MC. 1990. Electrostatic changes in Lycopersicon esculentum root plasma membrane resulting from salt stress. Plant Physiology 93: 471-478.
191. Tang C, Rengel Z. 2003. Role of plant cation/anion uptake ratio in soil acidification. In: Rengel Z, ed. Handbook of soil acidity. New York, NY, USA: Marcel Dekker, 57-81.
192. Taylor LP, Hepler PK. 1997. Pollen germination and tube growth. Annual Review of Plant Physiology and Plant Molecular Biology 48: 461-491.
193. 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 Physiology 123: 987-996.
194. Thion L, Mazars C, Nacry P, Bouchez D, Moreau M, Ranjeva R, Thuleau P. 1998. Plasma membrane depolarization-activated calcium channels, stimulated by microtubule-depolymerizing drugs in wild-type Arabidopsis thaliana protoplasts, display constitutively large activities and a longer half-life in ton 2 mutant cells affected in the organization of cortical microtubules. Plant Journal 13: 603-610.
195. Thion L, Mazars C, Thuleau P, Graziana A, Rossignol M, Moreau M, Ranjeva R. 1996. Activation of plasma membrane voltage-dependent calcium-permeable channels by disruption of microtubules in carrot cells. FEBS Letters 393: 13-18.
196. Thuleau P, Ward JM, Ranjeva R, Schroeder JI. 1994. Voltage-dependent calcium-permeable channels in the plasma membrane of a higher plant cell. EMBO Journal 13: 2970-2975.
197. Tice KR, Parker DR, DeMason A. 1992. Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. Plant Physiology 100: 309-318.
198. Trewavas A. 1999. Le calcium, c'est la vie: Calcium makes waves. Plant Physiology 120: 1-6.
199. Trewavas AJ, Malho R. 1997. Signal perception and transduction: the origin of the phenotype. Plant Cell 9: 1181-1195.
200. Van Oene H. 1998. A mechanistic model for the inhibiting effects of aluminium on the uptake of cations. Zeitschrift für Pflanzenernährung und Bodenkunde 161: 661-670.
201. Van Praag HJ, Weissen F, Dreze P, Cogneau M. 1997. Effects of aluminium on calcium and magnesium uptake and translocation by root segments of whole seedlings of Norway spruce (Picea abies Karst.). Plant and Soil 189: 267-273.
202. Vazquez MD, Poschenrieder C, Corrales I, Barcelo J. 1999. Change in apoplastic aluminum during the initial growth response to aluminum by roots of a tolerant maize variety. Plant Physiology 119: 435-444.
203. Very AA, Davies JM. 2000. Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proceedings of the National Academy of Sciences, USA 97: 9801-9806.
204. Wallace SU, Anderson IC. 1984. Aluminum toxicity and DNA synthesis in wheat roots. Agronomy Journal 76: 5-8.
205. Ward JM, Pei ZM, Schroeder JI. 1995. Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 7: 833-844.
206. Webb AAR, McAinsh MR, Taylor JE, Hetherington AM. 1996. Calcium ions as intracellular second messengers in higher plants. Advances in Botanical Research 22: 45-96.
207. Weber A. 1976. Synopsis of the presentations. Symposia of the Society for Experimental Biology 30: 445-456.
208. White PJ. 1994. Characterization of a voltage-dependent cation-channel from the plasma membrane of rye (Secale cereale L.) roots in planar lipid bilayers. Planta 193: 186-193.
209. White PJ. 1997. Cation channels in the plasma membrane of rye roots. Journal of Experimental Botany 48: 499-514.
210. White PJ. 1998. Calcium channels in the plasma membrane of root cells. Annals of Botany 81: 173-183.
211. 2+ homeostasis. Plant Physiology 130: 1386-1395.
212. White PJ, Piñeros M, Tester M, Ridout MS. 2000. Cation permeability and selectivity of a root plasma membrane calcium channel. Journal of Membrane Biology 174: 71-83.
213. Wissemeier AH, Horst WJ. 1995. Effect of calcium supply on aluminium-induced callose formation, its distribution and persistence in roots of soybean (Glycine max (L.) Merr.). Journal of Plant Physiology 145: 470-476.
214. Wymer CL, Bibikova TN, Gilroy S. 1997. Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant Journal 12: 427-439.
215. Yamamoto Y, Hachiya A, Matsumoto H. 1997. Oxidative damage to membranes by a combination of aluminum and iron in suspension-cultured tobacco cells. Plant and Cell Physiology 38: 1333-1339.
216. Yamamoto Y, Kobayashi Y, Devi SR, Rildishi S, Matsumoto H. 2002. Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiology 128: 63-72.
217. Yamamoto Y, Masamoto K, Rikiishi S, Hachiya A, Yamaguchi Y, Matsumoto H. 1996. Aluminum tolerance acquired during phosphate starvation in cultured tobacco cells. Plant Physiology 112: 217-227.
218. Yamamoto Y, Rikiishi S, Chang Y-C, Ono K, Kasai M, Matsumoto H. 1994. Quantitative estimation of aluminium toxicity in cultured tobacco cells: correlation between aluminium uptake and growth inhibition. Plant and Cell Physiology 35: 575-583.
219. Yan F, Schubert S, Mengel K. 1992. Effect of low root medium pH on net proton release, root respiration, and root growth of corn (Zea mays L.) and broad bean (Vicia faba L.). Plant Physiology 99: 415-421.
220. Yermiyahu U, Brauer DK, Kinraide TB. 1997a. Sorption of aluminum to plasma membrane vesicles isolated from roots of Scout 66 and Adas 66 cultivars of wheat. Plant Physiology 115: 1119-1125.
221. Yermiyahu U, Nir S, Ben-Hayyim G, Kafkafi U, Kinraide TB. 1997b. Root elongation in saline solution related to calcium binding to root cell plasma membranes. Plant and Soil 191: 67-76.
222. 3+) to wheat root plasma membranes. Journal of Membrane Biology 159: 239-252.
223. Zhang G, Hoddinott J, Taylor GJ. 1994. Characterization of 1,3-β-D-glucan (callose) synthesis in roots of Triticum aestivum in response to aluminum toxicity. Journal of Plant Physiology 144: 229-234.
224. Zhang W-H, Rengel Z. 1999. Aluminium induces an increase in cytoplasmic calcium in intact wheat root apical cells. Australian Journal of Plant Physiology 26: 401-409.
225. 2+ in cells of intact wheat roots: Loading of acetoxymethyl ester of Fluo-3 under low temperature. Plant Journal 15: 147-151.
226. 2+ antagonists. Annals of Botany 84: 559-564.
227. Zhang WH, Ryan PR, Tyerman SD. 2001. Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. Plant Physiology 125: 1459-1472.