The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: A review

Annals of Botany

Volumn 106, Issue 1, 2010, Pages 185-197

  Horst, Walter J ^a   Wang, Yunxia ^a,b   Eticha, Dejene ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b YANGZHOU UNIVERSITY   (China)

Author keywords

Aluminium; Aluminum; Apoplast; Cell wall; Pectin; Resistance; Root elongation

Indexed keywords

ALUMINUM;

ACID SOIL; ALUMINUM; BIOACCUMULATION; CARBOHYDRATE; DEVELOPMENTAL BIOLOGY; INHIBITION; ION EXCHANGE; MATRIX; MEMBRANE; MOLECULAR ANALYSIS; ORGANIC ACID; PLANT COMMUNITY; PLASMA; ROOT SYSTEM; TOLERANCE; TOXICITY;

CELL WALL; CYTOLOGY; DRUG EFFECT; PHYSIOLOGY; PLANT ROOT; REVIEW; DRUG EFFECTS; TOXICITY;

ALUMINUM; CELL WALL; PLANT ROOTS;

EID: 77954156302     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcq053     Document Type: Review

References (189)

1. +-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots. Plant Physiology 126:1381-1390.
2. +-ATPase activity in near-isogenic wheat lines differing in tolerance to aluminum. New Phytologist 162:71-79.
3. 3+ to phosphatidylcholine vesicles. Biochimica et Biophysica Acta 986:33-40.
4. Amenós M, Corrales I, Poschenrieder C, Illés P, Baluska F, Barceló 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 and Cell Physiology 50:528-540.
5. Basu U, Good AG, Aung T, et al. 1999. A 23-kDa, root exudate polypeptide co-segregates with aluminum resistance in Triticum aestivum. Physionogia Plantarum 106:53-61.
6. Bennet RJ, Breen CM, Fey MV. 1985. Aluminium uptake sites in the primary root of Zea mays L. South African Journal of Plant and Soil 2:1-7.
7. Blamey FPC. 2003. A role for pectin in the control of cell expansion. Soil Science and Plant Nutrition 49:775-783.
8. 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.
9. Blamey 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.
10. Blamey FPC, Asher CJ, Edwards DG, Kerven GL. 1993. In vitro evidence of aluminium effects on solution movement through root cell walls. Journal of Plant Nutrition 16:555-562.
11. Blamey FPC, Nishizawa NK, Yoshimura E. 2004. Timing, magnitude, and location of initial soluble aluminum injuries to mungbean roots. Soil Science and Plant Nutrition 50:67-76.
12. Blamey FPC, Nishizawa NK, Yoshimura E. 2005. Digital microscopy: a useful technique for measuring root elongation in solution. Soil Science and Plant Nutrition 51:705-708.
13. 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.
14. Bordenave M. 1996. Analysis of pectin methyl esterases. In: Linskens H, Jackson J. eds. Plant cell wall analysis. Berlin: Springer, 165-180.
15. Boscolo PRS, Menossi M, Jorge RA. 2003. Aluminum-induced oxidative stress in maize. Phytochemistry 62:181-189.
16. Boyer JS. 2009. Cell wall biosynthesis and the molecular mechanism of plant enlargement. Functional Plant Biology 36:383-394.
17. Brown PH, Hu H. 1997. Does boron play only a structural role in the growing tissues of higher plants? Plant and Soil 196:211-215.
18. Brown PH, Bellaloui N, Wimmer MA, et al. 2002. Boron in plant biology. Plant Biology 4:205-223.
19. Büscher P, Koedam N, Van Speybroek D. 1990. Cation exchange properties and adaptation to soil acidity in bryophytes. New Phytologist 115:177-186.
20. Caldwell CR. 1989. Analysis of aluminum and divalent cation binding to wheat root plasma membrane proteins using Terbium phosphorescence. Plant Physiology 91:233-241.
21. 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.
22. 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. The Plant Journal 3:1-30.
23. Carr HP, Lombi E, Küpper H, McGrath SP, Wong MH. 2003. Accumulation and distribution of aluminium and other elements in tea (Camellia sinensis) leaves. Agronomie 23:705-710.
24. Chandran D, Sharopova N, Ivashuta S, Gantt J, VandenBosch K, Samac D. 2008a. Transcriptome profiling identified novel genes associated with aluminum toxicity, resistance and tolerance in Medicago truncatula. Planta 228:151-166.
25. Chandran D, Sharopova N, VandenBosch K, Garvin D, Samac D. 2008b. Physiological and molecular characterization of aluminum resistance in Medicago truncatula. BMC Plant Biology 8:89.
26. Chang YC, Yamamoto Y, Matsumoto H. 1999. Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron. Plant, Cell and Environment 22:1009-1017.
27. Cocker KM, Evans DE, Hodson MJ. 1998a. The amelioration of aluminium toxicity by silicon in higher plants: solution chemistry or an in planta mechanism? Physiologia Plantarum 104:608-614.
28. Cocker KM, Evans DE, Hodson MJ. 1998b. The amelioration of aluminium toxicity by silicon in wheat (Triticum aestivum L.): malate exudation as evidence for an in planta mechanism. Planta 204:318-323.
29. Collet L, Horst W. 2001. Characterisation of maize cultivars in their adaptation to acid soils on the single plant level. In: Horst WJ, Schenk MK, Bürckert A, et al. eds. Plant nutrition: food security and sustainability of agro-ecosystems through basic and applied research. Dordrecht: Kluwer Academic Publishers, 86-87.
30. Corrales I, Poschenrieder C, Barceló J. 2008. Boron-induced amelioration of aluminium toxicity in a monocot and a dicot species. Journal of Plant Physiology 165:504-513.
31. Da Silva ALS, Sperling P, Horst W, et al. 2006. A possible role of sphingolipids in the aluminium resistance of yeast and maize. Journal of Plant Physiology 163:26-38.
32. Delhaize E, Craig S, Beaton CD, Bennet RJ, Jagadish VC, Randall PJ. 1993. Aluminum tolerance in wheat (Triticum aestivum L.) (I. Uptake and distribution of aluminum in root apices). Plant Physiology 103:685-693.
33. Delhaize E, Gruber BD, Ryan PR. 2007. The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Letters 581:2255-2262.
34. Deng W, Luo K, Li D, et al. 2006. Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. Journal of Experimental Botany 57:4235-4243.
35. Ermolayev V, Weschke W, Manteuffel R. 2003. Comparison of Al-induced gene expression in sensitive and tolerant soybean cultivars. Journal of Experimental Botany 54:2745-2756.
36. Eticha D, Staß A, Horst WJ. 2005a. Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant, Cell and Environment 28:1410-1420.
37. Eticha D, Staß A, Horst WJ. 2005b. Localization of aluminium in the maize root apex: can morin detect cell wall-bound aluminium? Journal of Experimental Botany 56:1351-1357.
38. Eticha D, The C, Welcker C, Narro L, Staß A, Horst WJ. 2005c. Aluminium-induced callose formation in root apices: inheritance and selection trait for adaptation of tropical maize to acid soils. Field Crops Research 93:252-263.
39. Eticha D, Zahn M, Bremer M, Yang Z, Rangel AF, Rao IM, Horst WJ. 2010. Transcriptomic analysis reveals differential gene expression in response to aluminium in common bean (Phaseolus vulgaris) genotypes. Annals of Botany 105:1119-1128.
40. Ezaki B, Katsuhara M, Kawamura M, Matsumoto H. 2001. Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiology 127:918-927.
41. Ezaki B, Sasaki K, Matsumoto H, Nakashima S. 2005. Functions of two genes in aluminium (Al) stress resistance: repression of oxidative damage by the AtBCB gene and promotion of efflux of Al ions by the NtGDI1gene. Journal of Experimental Botany 56:2661-2671.
42. Fleischer A, O'Neill MA, Ehwald R. 1999. The pore size of nongraminaceous plant cell walls is rapidly decreased by borate ester crosslinking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiology 121:829-838.
43. Frantzios G, Galatis B, Apostolakos P. 2005. Aluminium causes variable responses in actin filament cytoskeleton of the root tip cells of Triticum turgidum. Protoplasma 225:129-140.
44. Gerendás J. 2007. Significance of polyamines for pectin methylesterase activity and the ion dynamics in the apoplast. In: Sattelmacher B, Horst W. eds. The apoplast of higher plants: compartment of storage, transport, and reactions. Dordrecht: Kluwer Academic Publishers, 67-83.
45. Goldbach HE, Wimmer MA. 2007. Boron in plants and animals: is there a role beyond cell-wall structure? Journal of Plant Nutrition and Soil Science 170:39-48.
46. Goodwin SB, Sutter TR. 2009. Microarray analysis of Arabidopsis genome response to aluminum stress. Biologia Plantarum 53:85-99.
47. Grauer UE. 1992. Faktoren der Aluminium-Toleranz bei verschiedenen Pflanzen. PhD Thesis, Universität Hohenheim, Germany.
48. Grauer UE, Horst WJ. 1992. Modeling cation amelioration of aluminum phytotoxicity. Soil Science Society of America Journal 56:166-171.
49. Guo P, Bai G, Carver B, Li R, Bernardo A, Baum M. 2007. Transcriptional analysis between two wheat near-isogenic lines contrasting in aluminum tolerance under aluminum stress. Molecular Genetics and Genomics 277:1-12.
50. Han Y, Zhang W, Zhang B, Zhang S, Wang W, Ming F. 2009. One novel mitochondrial citrate synthase from Oryza sativa L. can enhance aluminum tolerance in transgenic tobacco. Molecular Biotechnology 42:299-305.
51. Hartwell BL, Pember FR. 1918. The presence of aluminium as a reason for the difference in the effect of so-called acid soil on barley and rye. Soil Science 6:259-281.
52. Heim A, Luster J, Brunner I, Frey B, Frossard E. 1999. Effects of aluminium treatment on Norway spruce roots: aluminium binding forms, element distribution, and release of organic substances. Plant and Soil 216:103-116.
53. Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H. 2001. A large family of class III plant peroxidases. Plant and Cell Physiology 42:462-468.
54. Hodson MJ, Evans DE. 1995. Aluminium/silicon interactions in higher plants. Journal of Experimental Botany 46:161-171.
55. Horst WJ. 1995. The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Zeitschrift für Pflanzenernä hrung und Bodenkunde 158:419-428.
56. Horst WJ, Asher CJ, Cakmak I, Szulkiewicz P, Wissemeier AH. 1992. Short-term responses of soybean roots to aluminium. Journal of Plant Physiology. 140:174-178.
57. Horst WJ, Püschel A-K, Schmohl N. 1997. Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant and Soil 192:23-30.
58. 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.
59. Horst WJ, Kollmeier M, Schmohl N, et al. 2007. Significance of the root apoplast for aluminium toxicity and resistance of maize. In: Sattelmacher B, Horst W. eds. The apoplast of higher plants: compartment of storage, transport, and reactions. Dordrecht: Kluwer Academic Publishers, 49-66.
60. Hossain AKMZ, Asgar M, Hossain MA, Tosaki T, Koyama H, Hara T. 2005. Boron-calcium synergically alleviates aluminum toxicity in wheat plants (Triticum aestivum L.). Soil Science and Plant Nutrition 51:43-49.
61. Houde M, Diallo AO. 2008. Identification of genes and pathways associated with aluminum stress and tolerance using transcriptome profiling of wheat near-isogenic lines. BioMed Central Genomics 9:400.
62. Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF. 2009. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. The Plant Cell 21:655-667.
63. Illes P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluška 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 behavior, and nitric oxide production. Journal of Experimental Botany 57:4201-4213.
64. Ishikawa S, Wagatsuma T. 1998. Plasma membrane permeability of root-tip cells following temporary exposure to Al ions is a rapid measure of Al tolerance among plant species. Plant and Cell Physiology 39:516-525.
65. Jansen S, Broadley MR, Robbrecht W, Smets E. 2002. Aluminum hyperaccumulation in angiosperms: a review of its phylogenetic significance. Botanical Review 68:235-269.
66. 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.
67. 2+ homeostasis in root hairs of Arabidopsis thaliana (L.). Planta 206:378-387.
68. 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 and Environment 29:1309-1318.
69. 2+ is an important but not the only signal in callose synthesis induced by chitosan, saponins and polyene antibiotics. In: Lugtenberg BJJ. ed. Signal molecules in plant and plant-microbe interactions. Berlin: Springer-Verlag. 107-116.
70. Kerven GL, Edwards DG, Asher CJ, Hallman PS, Kobot S. 1989. Aluminium determination in soil solution. I. Evaluation of existing colorimetric and separation methods for the determination of inorganic monomeric aluminium in the presence of organic acid ligands. Australian Journal of Soil Research 27:79-90.
71. 5-sterols in plasma membrane lipids of root-tip cells correlates with aluminum tolerance of rice. Physiologia Plantarum 135:73-83.
72. Kidd PS, Llugany M, Poschenrieder C, Gunsé B, Barceló J. 2001. The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). Journal of Experimental Botany 52:1339-1352.
73. +, and other cations on root elongation considered in terms of cell-surface electrical potential. Plant Physiology 99:1461-1468.
74. Kinraide TB. 2006. Plasma membrane surface potential ('psi' PM) as a determinant of ion bioavailability: a critical analysis of new and published toxicological studies and a simplified method for the computation of plant 'psi' PM. Environmental Toxicology and Chemistry 25:3188-3198.
75. Kinraide TB. 2009. Improved scales for metal ion softness and toxicity. Environmental Toxicology and Chemistry 28:525-533.
76. Klimashevskii EL, Dedov VM. 1975. Localization of growth inhibiting action of aluminum ions in elongating cell walls. Fiziologiia Rastenii 22:1183-1190.
77. Klug B, Horst WJ. 2010. Spatial characteristics of aluminium uptake and translocation in roots of buckwheat (Fagopyrum esculentum Moench). Physiologia Plantarum (in press).
78. Kochian LV, Hoekenga OA, Piñeros MA. 2004. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annual Review of Plant Biology 55:459-493.
79. Kollmeier M, Horst WJ. 2001. Aluminium-induced exudation of citrate from the root tip of Zea mays (L.): are differential impacts of Al on citrate metabolism involved in genotypical differences? In: Horst WJ, Schenk MK, Bürckert A, et al. eds. Plant nutrition: food security and sustainability of agro-ecosystems through basic and applied research. Dordrecht: Kluwer Academic Publishers, 492-493.
80. 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.
81. Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R. 2001. Aluminum activates a citrate-permeable anion channel in the aluminumsensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum-resistant cultivar. Plant Physiology 126:397-410.
82. Kopittke PM, Blamey FPC, Menzies NW. 2008. Toxicities of soluble Al, Cu, and La include ruptures to rhizodermal and root cortical cells of cowpea. Plant and Soil 303:217-227.
83. Kopittke PM, McKenna BA, Blamey FPC, Wehr JB, Menzies NW. 2009. Metal-induced cell rupture in elongating roots is associated with metal ion binding strengths. Plant and Soil 322:303-315.
84. Kumari M, Taylor GJ, Deyholos MK. 2008. Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. Molecular Genetics and Genomics 279:339-357.
85. 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.
86. LeNoble ME, Blevins DG, Sharp RE, Cumbie BG. 1996a. Prevention of aluminium toxicity with supplemental boron. I. Maintenance of root elongation and cellular structure. Plant, Cell and Environment 19:1132-1142.
87. LeNoble ME, Blevins DG, Miles RJ. 1996b. Prevention of aluminium toxicity with supplemental boron. II. Stimulation of root growth in an acidic, high-aluminium subsoil. Plant, Cell and Environment 19:1143-1148.
88. Lewis TE. 1989. Environmental chemistry and toxicology of aluminium. Michigan: Lewis Publishers.
89. Li YY, Yang JL, Zhang YJ, Zheng SJ. 2009a. Disorganized distribution of homogalacturonan epitopes in cell walls as one possible mechanism for aluminium-induced root growth inhibition in maize. Annals of Botany 104:235-241.
90. Li YY, Zhang YJ, Zhou Y, Yang JL, Zheng SJ. 2009b. Protecting cell walls from binding aluminum by organic acids contributes to aluminum resistance. Journal of Integrative Plant Biology 51:574-580.
91. 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.
92. Lindberg S, Szynkier K, Greger M. 1991. Aluminium effects on transmembrane potential in cells of fibrous roots of sugar beet. Physiologia Plantarum 83:54-62.
93. Liu Q, Yang JL, He LS, Li YY, Zheng SJ. 2008. Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale. Biologia Plantarum 52:87-92.
94. Llugany M, Poschenrieder C, Barceló J. 1995. Monitoring of aluminium-induced inhibition of root elongation in four maize cultivars differing in tolerance to aluminium and proton toxicity. Physiologia Plantarum 93:265-271.
95. Lukaszewski KM, Blevins DG. 1996. Root growth inhibition in borondeficient or aluminum-stressed squash may be a result of impaired ascorbate metabolism. Plant Physiology 112:1135-1140.
96. Ma JF. 2007. Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. International Review of Cytology 264:225-252.
97. Ma JF, Hiradate S, Nomoto K, Iwashita T, Matsumoto H. 1997. Internal detoxification mechanism of Al in hydrangea (identification of Al form in the leaves). Plant Physiology 113:1033-1039.
98. Ma JF, Hiradate S, Matsumoto H. 1998. High aluminum resistance in buckwheat. II. Oxalic acid detoxifies aluminum internally. Plant Physiology 117:753-759.
99. Ma JF, Ryan PR, Delhaize E. 2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6:273-278.
100. Ma JF, Shen R, Zhao Z, et al. 2002. Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant and Cell Physiology 43:652-659.
101. Ma JF, Shen RF, Nagao S, Tanimoto E. 2004. Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. Plant and Cell Physiology 45:583-589.
102. Maltais K, Houde M. 2002. A new biochemical marker for aluminium tolerance in plants. Physiologia Plantarum 115:81-86.
103. Marienfeld S, Stelzer R. 1993. X-ray microanalyses in roots of Al-treated Avena sativa plants. Journal of Plant Physiology 141:569-573.
104. Marienfeld S, Schmohl N, Klein M, Schröder WH, Kuhn AJ, Horst WJ. 2000. Localization of aluminium in root tips of Zea mays and Vicia faba. Journal of Plant Physiology 156:666-671.
105. Maron LG, Kirst M, Mao C, Milner MJ, Menossi M, Kochian LV. 2008. Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytologist 179:116-128.
106. Matsumoto H. 2000. Cell biology of aluminium toxicity and tolerance in higher plants. International Review of Cytology 200:1-46.
107. Morita A, Fujii Y, Yokota H. 2001. Effect of aluminium on exudation of organic acid anions in tea plants. In: Horst WJ, Schenk MK, Bürckert A, et al. eds. Plant nutrition: food security and sustainability of agro-ecosystems through basic and applied research. Dordrecht: Kluwer Academic Publishers, 508-509.
108. Morita A, Yanagisawa O, Takatsu S, Maeda S, Hiradate S. 2008. Mechanism for the detoxification of aluminum in roots of tea plant (Camellia sinensis (L.) Kuntze). Phytochemistry 69:147-153.
109. Naumann A. 2001. Aufnahme und Verlagerung von Aluminium bei Hortensie (Hydrangea macrophylla) in Beziehung zur Aluminiumtoleranz und zur Blaufärbung der Sepalen. PhD Thesis, Leibniz Universität Hannover, Germany.
110. Naumann A, Horst WJ. 2003. Effect of aluminium supply on aluminium uptake, translocation and blueing of Hydrangea macrophylla (Thunb.) ser. cultivars in a peat-clay substrate. Journal of Horticultural Science and Biotechnology 78:463-469.
111. Olivetti GP, Cumming JR, Etherton B. 1995. Membrane potential depolarization of root cap cells precedes aluminum tolerance in snapbean. Plant Physiology 109:123-129.
112. Osaki M, Nursyamsi D, Begum HH, Watanabe T. 2001. Study on aluminium resistance in relation to organic-acid anion exudation from roots of PEPC transgenic rice plants. In: Horst WJ, Schenk MK, Bürckert A, et al. eds. Plant nutrition: food security and sustainability of agro-ecosystems through basic and applied research. Dordrecht: Kluwer Academic Publishers, 514-515.
113. Osawa H, Kojima K. 2006. Citrate-release-mediated aluminum resistance is coupled to the inducible expression of mitochondrial citrate synthase gene in Paraserianthes falcataria. Tree Physiology 26:565-574.
114. Panda S, Matsumoto H. 2007. Molecular physiology of aluminum toxicity and tolerance in plants. Botanical Review 73:326-347.
115. Passardi F, Longet D, Penel C, Dunand C. 2004. The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65:1879-1893.
116. 3+-induced anion channels. Plant Physiology 125:292-305.
117. Piñeros MA, Shaff JE, Manslank HS, Carvalho Alves VM, Kochian LV. 2005. Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiology 137:231-241.
118. 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. The Plant Journal 18:643-650.
119. Ramachandran S, Christensen HEM, Ishimaru Y, et al. 2000. Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiology 124:1637-1647.
120. Rangel AF, Rao IM, Horst WJ. 2007. Spatial aluminium sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminium resistance. Journal of Experimental Botany 58:3895-3904.
121. Rangel AF, Rao IM, Horst WJ. 2009a. Intracellular distribution and binding state of aluminum in root apices of two common bean (Phaseolus vulgaris) genotypes in relation to Al toxicity. Physiologia Plantarum 135:162-173.
122. Rangel AF, Rao IM, Braun H-P, Horst WJ. 2009b. Aluminium resistance in common bean (Phaseolus vulgaris L.) involves induction and maintenance of citrate exudation from root apices. Physiologia Plantarum 138:176-190.
123. Rengel Z. 1996. Uptake of aluminium by plant cells. New Phytologist 134:389-406.
124. Rengel Z, Reid RJ. 1997. Uptake of Al across the plasma membrane of plant cells. Plant and Soil 192:31-35.
125. Rengel Z, Zhang WH. 2003. Role of dynamics of intracellular calcium in aluminium-toxicity syndrome. New Phytologist 159:295-314.
126. Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC. 1998. Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiology 116:409-418.
127. 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.
128. Ryan PR, Delhaize E, Randall PJ. 1995. Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103-110.
129. Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman SD. 1997. Aluminum activates an anion channel in the apical cells of wheat roots. Proceedings of the National Academy of Sciences, USA 94:6547-6552.
130. Ryan PR, Delhaize E, Jones DL. 2001. Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Biology 52:527-560.
131. 8 sphingolipid desaturase with a preference for (Z)-isomer formation confers aluminum tolerance to yeast and plants. Plant Physiology 144:1968-1977.
132. Ryan PR, Delhaize E. 2010. The convergent evolution of aluminium resistance in plants exploits a convenient currency. Functional Plant Biology (in press).
133. Sarkar P, Bosneaga E, Auer M. 2009. Plant cell walls throughout evolution: towards a molecular understanding of their design principles. Journal of Experimental Botany 60:3615-3635.
134. 3+ resistance and toxicity: crystallinity and availability of negative charges. International Archives of Biosciences 2000:1087-1095.
135. Schmohl N, Horst WJ. 2000. Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant, Cell and Environment 23:735-742.
136. Schmohl N, Horst WJ. 2002. Effect of aluminium on the activity of apoplastic acid phosphatase and the exudation of macromolecules by roots and suspension-culture cells of Zea mays L. Journal of Plant Physiology 159:1213-1218.
137. Schmohl N, Pilling J, Fisahn J, Horst WJ. 2000. Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiologia Plantarum 109:419-427.
138. 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.
139. Shi BJ, Gustafson JP, Button J, et al. 2009. Physical analysis of the complex rye (Secale cereale L.) Alt4 aluminium (aluminum) tolerance locus using a whole-genome BAC library of rye cv. Blanco. Theoretical and Applied Genetics 119:695-704.
140. 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.
141. 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.
142. Sivaguru 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.
143. Sivaguru M, Fujiwara T, Samaj J, et al. 2000a. Aluminum-induced 1-3-β-D-glucan inhibits cell-to-cell traffiking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiology 124:991-1005.
144. Sivaguru M, Matsumoto H, Horst WJ. 2000b. Control of the response to aluminium stress. In: Nick P. ed. Plant microtubules: potential for biotechnology. Berlin: Springer Verlag, 103-120.
145. Sivaguru M, Horst WJ, Eticha D, Matsumoto H. 2006. Aluminum inhibits apoplastic flow of high-molecular weight solutes in root apices of Zea mays L. Journal of Plant Nutrition and Soil Science 169:679-690.
146. Staß A, Horst WJ. 1995. Effect of aluminium on membrane properties of soybean (Glycine max) cells in suspension culture. Plant and Soil 171:113-118.
147. Staß A, Horst WJ. 2009. Callose in abiotic stress. In: Bacic A, Fincher GB, Stone BA. eds. Chemistry, biochemistry, and biology of (1→3)-β-glucans and related polysaccharides. Burlington, MA: Academic Press, 499-524.
148. Staß A, Kotur Z, Horst WJ. 2007. Effect of boron on the expression of aluminium toxicity in Phaseolus vulgaris. Physiologia Plantarum 131:283-290.
149. Sun P, Tian Q-Y, Chen J, Zhang W-H. 2010. Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. Journal of Experimental Botany 61:347-356.
150. Tabuchi A, Matsumoto H. 2001. Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiologia Plantarum 112:353-358.
151. Taylor GJ, Macfie SM. 1994. Modeling the potential for boron amelioration of aluminum toxicity using the Weibull function. Canadian Journal of Botany 72:1187-1196.
152. Taylor GJ, McDonald-Stephens JL, Hunter DB, et al. 2000. Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiology 123:987-996.
153. Teraoka T, Kaneko M, Mori S, Yoshimura E. 2002. Aluminum rapidly inhibits cellulose synthesis in roots of barley and wheat seedlings. Journal of Plant Physiology 159:17-23.
154. Tesfaye M, Temple SJ, Allan DL, Vance CP, Samac DA. 2001. Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiology 127:1836-1844.
155. Tice KR, Parker DR, DeMason DA. 1992. Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. Plant Physiology 100:309-318.
156. Tognolli M, Penel C, Greppin H, Simon P. 2002. Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129-138.
157. von Uexküll HR, Mutert E. 1995. Global extent, development and economic impact of acid soils. Plant and Soil 171:1-15.
158. Van HL, Kuraishi S, Sakurai N. 1994. Aluminum-induced rapid root inhibition and changes in cell-wall components of squash seedlings. Plant Physiology 106:971-976.
159. Vàzquez MD, Poschenrieder C, Corrales I, Barcelò 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.
160. 3+ on the physical properties of membrane lipids in Thermoplasma acidophilum. Biochemical and Biophysical Research Communications 84:138-143.
161. Wagatsuma T, Akiba R. 1989. Low surface negativity of root protoplasts from aluminum-tolerant plant species. Soil Science and Plant Nutrition 35:443-452.
162. Wagatsuma T, Nakashima T, Twaraya K. 1991. Identification of aluminiumtolerant protoplasts in the original root protoplast population from several plant species differing in aluminium tolerance. In: Wright RJ, Baligar VC, Murrmann RP. eds. Plant-soil interactions at low pH. Dordrecht: Kluwer Academic Publishers, 789-793.
163. Wagatsuma T, Ishikawa S, Uemura M, et al. 2005a. Plasma membrane lipids are the powerful components for early stage aluminum tolerance in triticale. Soil Science and Plant Nutrition 51:701-704.
164. Wagatsuma T, Khan M, Rao IM, et al. 2005b. Methylene blue stainability of root-tip protoplasts as an indicator of aluminum tolerance in a wide range of plant species, cultivars and lines. Soil Science and Plant Nutrition 51:991-998.
165. Wang Y, Staß A, Horst WJ. 2004. Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiology 136:3762-3770.
166. Watanabe T, Osaki M, Yano H, Rao I. 2006. Internal mechanisms of plant adaptation to aluminum toxicity and phosphorus starvation in three tropical forages. Journal of Plant Nutrition 29:1243-1255.
167. Wehr JB, Menzies NW, Blamey FPC. 2003. Model studies on the role of citrate, malate and pectin esterification on the enzymatic degradation of Al-and Ca-pectate gels: possible implications for Al-tolerance. Plant Physiology and Biochemistry 41:1007-1010.
168. Wehr JB, Menzies NW, Blamey FPC. 2004. Inhibition of cell-wall autolysis and pectin degradation by cations. Plant Physiology and Biochemistry 42:485-492.
169. Wenzl P, Patino GM, Chaves AL, Mayer JE, Rao IM. 2001. The high level of aluminum resistance in signalgrass is not associated with known mechanisms of external aluminum detoxification in root apices. Plant Physiology 125:1473-1484.
170. Wissemeier AH, Klotz F, Horst WJ. 1987. Aluminium induced callose synthesis in roots of soybean (Glycine max L.). Journal of Plant Physiology 129:487-492.
171. Wissemeier AH, Diening A, Hergenröder A, Horst WJ, Mix-Wagner G. 1992. Callose formation as parameter for assessing genotypical plant tolerance of aluminium and manganese. Plant and Soil 146:67-75.
172. 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.
173. Wojcik P. 2003. Impact of boron on biomass production and nutrition of aluminium-stressed apple rootstocks. Journal of Plant Nutrition 26:2439-51.
174. Xue YJ, Ling T, Yang ZM. 2008. Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. Journal of Agricultural and Food Chemistry 56:9676-9684.
175. 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.
176. Yamamoto Y, Kobayashi Y, Matsumoto H. 2001. Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiology 125:199-208.
177. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H. 2003. Oxidative stress triggered by aluminum in plant roots. Plant and Soil 255:239-243.
178. Yang JL, Zheng SJ, He YF, Tang CX, Zhou GD. 2005. Genotypic differences among plant species in response to aluminum stress. Journal of Plant Nutrition 28:949-961.
179. Yang JL, Li YY, Zhang YJ, et al. 2008. Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiology 146:602-611.
180. 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 Physiology 115:1119-1125.
181. Yu M, Shen R, Xiao H, et al. 2009. Boron alleviates aluminum toxicity in pea (Pisum sativum). Plant and Soil 314:87-98.
182. 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.
183. Zhang G, Taylor GJ. 1990. Kinetics of aluminum uptake in Triticum aestivum L. Identity of the linear phase of Al uptake by excised roots of aluminum-tolerant and aluminum-sensitive cultivars. Plant Physiology 94:577-584.
184. Zhang J, He Z, Tian H, Zhu G, Peng X. 2007. Identification of aluminiumresponsive genes in rice cultivars with different aluminium sensitivities. Journal of Experimental Botany 58:2269-2278.
185. Zhang WH, Rengel Z. 1999. Aluminium induces an increase in cytoplasmic calcium in intact wheat root apical cells. Australian Journal of Plant Physiology 26:401-409.
186. 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.
187. Zheng SJ, Yang JL. 2005. Target sites of aluminum phytotoxicity. Biologia Plantarum 49:321-331.
188. Zheng SJ, Ma JF, Matsumoto H. 1998. High aluminum resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiology 117:745-751.
189. Zheng SJ, Lin X, Yang J, Liu Q, Tang C. 2004. The kinetics of aluminum adsorption and desorption by root cell walls of an aluminum resistant wheat (Triticum aestivum L.) cultivar. Plant and Soil 261:85-90.