Aluminum toxicity and tolerance mechanism in cereals and legumes - A review

Journal of the Korean Society for Applied Biological Chemistry

Volumn 56, Issue 1, 2013, Pages 1-9

  Arunakumara, Kodithuwakku Kankanange Indika Upali ^a   Walpola, Buddhi Charana ^b   Yoon, Min Ho ^b  

^a UNIVERSITY OF RUHUNA   (Sri Lanka)

^b Chungnam National University   (South Korea)

Author keywords

exudation; ligands; metabolism; tolerance; toxicity

Indexed keywords

EID: 84874292599     PISSN: 17382203     EISSN: 2234344X     Source Type: Journal    
DOI: 10.1007/s13765-012-2314-z     Document Type: Review

References (89)

1. Ahn SJ and Matsumoto H (2006) The role of the plasma membrane in the response of plant roots to aluminum toxicity. Plant Signal Behav1, 37-45.
2. Amenós M, Corrales I, Poschenrieder C, Illéš P, and Baluška F (2009) Different effects of aluminum on the actin cytoskeleton and brefeldin asensitive vesicle recycling in root apex cells of two maize varieties differing in root elongation rate and aluminum tolerance. Plant Cell Physiol50, 528-540.
3. Barcelo J and Pochenrieder C (2002) Fast root growth response, root exudates, and internal detoxification as clues to the mechanisms of aluminum toxicity and resistance, a review. Environ Exp Bot48, 75-92.
4. Blair MW, López-Marín HD, and Rao MI (2009) Identification of aluminum resistant Andean common bean (Phaseolus vulgaris L.) genotypes. Braz J Plant Physiol21, 291-300.
5. Bose J, Babourina O, Shabala S, and Rengel Z (2010) Aluminum-induced ion transport in Arabidopsis: the relationship between Al tolerance and root ion flux. J Exp Bot61, 3163-3175.
6. Cai MZ, Wang FM, Li RF, Zhang SN, Wang N, and Xu GD (2011) Response and tolerance of root border cells to aluminum toxicity in soybean seedlings. J Inorg Biochem105, 966-971.
7. Chaudhary ML, Adu-Gyamfi JJ, Saneoka H, Nguyen NT, Suwa R, Kanai S et al. (2008) The effect of phosphorus deficiency on nutrient uptake, nitrogen fixation and photosynthetic rate in mashbean, mungbean and soybean. Acta Physiol Plant30, 537-544.
8. Ciamporova M (2002) Morphological and structural response of plant roots to aluminum at organ, tissue and cellular levels. Biol Plant45, 161-171.
9. Damialis A and Konstantinou GN (2011) Cereal pollen sensitisation in pollen allergic patients: to treat or not to treat? Eur Ann Allergy Clin Immunol 43, 36-44.
10. Darkó E, Ambrusa H, Stefanovits-Bányai E, Fodor J, Bakos F, and Barnabás B (2004) Aluminum toxicity, Al tolerance and oxidative stress in an Alsensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. Plant Sci166, 583-591.
11. da Silva ALS, Sperling P, Horst W, Franke S, Ott C, Becker D et al. (2006) A possible role of sphingolipids in the aluminum resistance of yeast and maize. J Plant Physiol163, 26-38.
12. Delhaize E, Gruber BD, and Ryan PR (2007) The roles of organic anion permeases in aluminum resistance and mineral nutrition. FEBS Lett581, 2255-2262.
13. Delhaize E, Ma JF, and Ryan PR (2012) Transcriptional regulation of aluminum tolerance genes. Trends in Plant Sci17, 341-348.
14. Doncheva S, Amenós M, Poschenrieder C, and Barceló J (2005) Root cell patterning: a primary target for aluminum toxicity in maize. J Exp Bot56, 1213-1220.
15. Doyle JJ and Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol131, 900-910.
16. Éva Darkó, Helga Ambrus, Éva Stefanovits-Bányai, József Fodor, Ferenc Bakos, and Beáta Barnabás (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 Sci166, 583-591.
17. Garzon T, Gunse B, Moreno AR, Tomos AD, Barcelo J, and Poschenrieder C (2011) Aluminium-induced alteration of ion homeostasis in root tip vacuoles of two maize varieties differing in Al tolerance. Plant Sci180, 709-715.
18. Gaume A, Mächler F, and Frossard E (2001) Aluminum resistance in two cultivars of Zea mays L., Root exudation of organic acids and influence of phosphorus nutrition. Plant Oil234, 73-81.
19. Godbold DL and Brunner I (2007) The platform for European root science, COST action E38: an introduction and overview. Plant Biosyst141, 390-393.
20. Graham PH and Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol131, 872-877.
21. Gunsé B, Poschenrieder C, and Barcelo J (2000) The role of ethylene metabolism in the short-term responses to aluminium by roots of two maize cultivars different in Al-resistance. Environ Exp Bot43, 73-81.
22. Gunsé B, Garzón T, and Barceló J (2003) Study of aluminum toxicity by means of vital staining profiles in four cultivars of Phaseolus vulgaris L. J Plant Physiol160, 1447-1450.
23. Guo TR, Yao PC, Zhang ZD, Wang JJ, and Wang M (2012) Devolvement of antioxidative defense system in rice growing seedlings exposed to Aluminum toxicity and Phosphorus deficiency. Rice Sci19, 179-185.
24. Hiradate S, Ma JF, and Matsumoto H (2007) Strategies of plants to adapt to mineral stresses in problem soils. In Advances in Agronomy. Donald, LS (ed.), pp. 65-132, Academic Press, New York, USA.
25. Hirano Y and Brunner I (2006) Quantitative determination of callose in tree roots. J Plant Physiol163, 1333-1336.
26. Horst WJ, Wang YX, and Eticha D (2010). The role of root apoplasm in aluminum induced inhibition of root elongation and aluminum resistance of plants: a review. Ann Bot106, 185-197.
27. 2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res65, 151-164.
28. Ismail M (2005) Aluminum-phosphorus interactions on growth and some physiological traits of carrot and radish plants. Acta Agron Hung53, 293-301.
29. Kidd PS, Llugany M, Poschenrieder CH, Gunse B, and Barcelo 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.). J Exp Bot52, 1339-1352.
30. Kikui S, Sasaki T, Maekawa M, Mryao A, Hirochika H, Matsumoto H et al. (2005) Physiological and genetic analyses of aluminum tolerance in rice, focusing on root growth during germination. J Inorg Biochem99, 1837-1844.
31. Kikui S, Sasaki T, Osawa H, Matsumoto H, and Yamamoto Y (2007) Malate enhances recovery from aluminum-caused inhibition of root elongation in wheat. Plant Soil290, 1-15.
32. Klug B and Horst WJ (2010) Oxalate exudation into the root-tip water free space confers protection against aluminum toxicity and allows aluminum accumulation in the symplast in buckwheat (Fagopyrum esculentum). New Phytol187, 380-391.
33. Kochian LV (2004) How do crop plants tolerate acid soils? Mechanisms of aluminium tolerance and phosphorus efficiency. Annu Rev Plant Biol55, 459-493.
34. Kochian LV, Piñeros MA, and Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminium resistance and toxicity. Plant Soil274, 175-195.
35. Kollmeier M, Felle HH, and 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? J Plant Physiol122, 945-956.
36. Kuo MC and Kao CH (2003) Aluminum effects on lipid peroxidation and antioxidative enzyme activated in rice leaves. Biol Plant46, 149-152.
37. León-Ruiz E, Alcázar P, Domínguez-Vilches E, and Galán C (2011) Study of Poaceae phenology in a Mediterranean climate. Which species contribute most to airborne pollen counts? Aerobiologia27, 37-50.
38. Li CS, Liu P, Xu GD, and Lin HJ (2006) Ameliorating effects of exogenous organic acids on aluminum toxicity in buckwheat seedlings. J Acta Agronomica Sinica32, 532-539.
39. Li CS, Liu P, Xu GD, He WB, and Zhu J (2004) Effect of acid-Al on the germination of soaked buckwheat seeds. J Seed23, 9-11.
40. Li XF, Ma JF, and Matsumoto H (2000) Pattern of Aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol123, 1537-1543.
41. Lilienfein J, Qualls RG, Uselman SM, and Bridgham SD (2003) Soil formation and organic matter accretion in a young andesitic chronosequence at Mt. Shasta, California. Geoderma116, 249-264.
42. Liu J, Magalhaes JV, Shaff J, and Kochian LV (2009) Aluminum activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J57, 389-399.
43. Ma FJ, Ryan PR, and Delhaize E (2001) Aluminum tolerance in plants and the complexing role of organic acids. Trends Plant Sci6, 273-278.
44. Ma JF and Furukawa J (2003) Recent progress in the research of external Al detoxification in higher plants: a mini review. J Inorg Biochem97, 46-51.
45. Ma JF, She RF, Nagao S, and Tanimoto E (2004) Aluminium targets elongating cells by reducing cell wall extensibility in wheat roots. Plant Cell Physiol45, 583-589.
46. Maron LG, Piñeros MA, Guimaraes CT, Magalhaes JV, Pleiman JK, Mao CZ et al. (2010) Two functionally distinct members of the MATE (multidrug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J61, 728-740.
47. Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol200, 1-46.
48. Matsumoto H and Motoda H (2012) Aluminum toxicity recovery processes in root apices; possible association with oxidative stress. Plant Sci186, 1-8.
49. Meda AR and Furlani PR (2005) Tolerance to aluminum toxicity by tropical leguminous plants used as cover crops. Braz Arch Biol Technol48, 309-317.
50. Meriga B, Attitalla IH, Ramgopal M, Ediga A, and Kavikishor PB (2010) Differential tolerance to Aluminum toxicity in rice cultivars: Involvement of antioxidative enzymes and possible role of Aluminum resistant locus. Acad J Plant Sci3, 53-63.
51. Motoda H, Kano Y, Hiragami F, Kawamura K, and Matsumoto H (2010) Morphological changes in the apex of pea roots during and after recovery from aluminum treatment. Plant Soil333, 49-58.
52. Motoda H, Kano Y, Hiragami F, Kawamura K, and Matsumoto H (2011) Changes in rupture formation and zonary region stained with Evans blue during the recovery process from aluminum toxicity in the pea root apex. Plant Signal Behav6, 98-100.
53. Nagy NE, Dalen LS, Jones DL, Swensen B, Fossdal CG, and Eldhuset TD (2004) Cytological and enzymatic responses to aluminum stress in root tips of Norway spruce seedlings. New Phytol163, 595-607.
54. Nasr N, Carapetian J, Heidari R, Asri Rezaei S, Abbaspour N, and Darvishzadeh R (2011) Differential effects of aluminum on the seedling parameters of wheat. African J Biotechnol10, 3345-3353.
55. Osawa H and Matsumoto H (2001) Possible involvement of protein phosphorylation in aluminium-responsive malate efflux from wheat root apex. Plant Physiol126, 411-420.
56. Peixoto PHP, Cambraia J, Sant'Anna R, Mosquim PR, and Moreira MA (2001) Aluminum effects on fatty acid composition and lipid peroxidation of a purified plasma membrane fraction of root apices of two sorghum cultivars. J Plant Nutr24, 1061-1070.
57. Piñeros MA, Magalhaes JV, Alves VMC, and Kochian LV (2005) Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiol137, 231-241.
58. Poozesh V, Cruz P, Choler P, and Bertoni G (2007) Relationship between the Al resistance of grasses and their adaptation to an unfertile habitat. Ann Bot99, 947-954.
59. Poschenrieder C, Tolra' RP, and Barcelo J (2005) A role for cyclic hydroxamates in aluminium resistance in maize? J Inorg Biochem99, 1830-1836.
60. Poschenrieder C, Gunsé B, Corrales I, and Barceló J (2008) A glance into aluminum toxicity and resistance in plants. Sci Total Environ400, 356-368.
61. Purcino AAC, Alves VMC, Parentoni SN, Belele CL, and Loguercio LL (2003) Aluminum effects on nitrogen uptake and nitrogen assimilating enzymes in maize genotypes with contrasting tolerance to aluminum toxicity. J Plant Nutr26, 31-61.
62. Rangel AF, Mobin M, Rao IM, and Horst WJ (2005) Proton toxicity interferes with the screening of common bean (Phaseolus vulgaris L.) genotypes for aluminium resistance in nutrient solution. J Plant Nutr Soil Sci168, 607-616.
63. Rangel AF, Rao IM, and Horst WJ (2009) Intracellular distribution and binding state of aluminum in root apices of two common bean (Phaseolus vulgaris) genotypes in relation to Al toxicity. Physiol Plant135, 162-173.
64. Ruf M and Brunner I (2003) Vitality of tree fine roots: reevaluation of the tetrazolium test. Tree Physiol23, 257-263.
65. Ryan PR, Delhaize E, and Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Ann Rev Plant Physiol Plant Molec Biol52, 527-560.
66. Ryan PR, Tyerman SD, Sasaki T, Furuichi T, Yamamoto Y, Zhang WH et al. (2011) The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot62, 9-20.
67. Sarker BC and Karmoker JL (2011) Effects of phosphorus deficiency on accumulation of biochemical compounds in lentil (Lensculinaris medik.). Bangladesh J Bot40, 23-27.
68. Sharma P and Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep26, 2027-2038.
69. Silva S (2012) Aluminum toxicity targets in plants. J Bot2012, 219-262.
70. Singh NB, Yadav K, and Amist N (2011) Phytotoxic effects of Aluminum on growth and metabolism of Pisum sativum L. Int J Innov Biol Chem Sci2, 10-21.
71. Smith E, Naik D, and Cumming JR (2011) Genotypic variation in aluminum resistance, cellular aluminum fractions, callose and pectin formation and organic acid accumulation in roots of Populus hybrids. Environ Expl Bot72, 182-193.
72. Sun P, Tian QY, Chen J, and Zhang WH (2010) Aluminum-induced inhibition of root elongation in Arabidopsis is mediated by Ethylene and Auxin. J Exp Bot61, 346-356.
73. Sun P, Tian QY, Zhao MG, Dai XY, Huang JH and Zhang WH (2007) Aluminum-induced ethylene production is associated with inhibition of root elongation in Lotus japonicus L. Plant Cell Physiol48, 1229-1235.
74. Teraoka T, Kaneko M, Mori S, and Yoshimura E (2002) Aluminum rapidly inhibits cellulose synthesis in roots of barley and wheat seedlings. J Plant Physiol159, 17-23.
75. Tewari RK, Kumar P, Tewari N, Srivastava S, and Sharma PN (2004) Macronutrient deficiencies and differential antioxidant responsesinfluence on the activity and expression of superoxide dismutase in maize. Plant Sci66, 687-694.
76. Tolra R, Barcelo J, and Poschenrieder C (2009) Constitutive and aluminiuminduced patterns of phenolic compounds in two maize varieties differing in aluminium tolerance. J Inorg Biochem103, 1486-1490.
77. Tolra R, Poschenrieder C, Lupi B, and Barcelo J (2005) Aluminium-induced changes in the profiles of both organic acids and phenolic substances underlie Al tolerance in Rumex acetosa L. Environ Exp Bot54, 231-238.
78. van Wyk BE (2005) Food plants of the world. Identification, culinary uses and nutritional value. Briza Publications, Pretoria, South Africa.
79. Vanguelova EI, Hirano Y, Eldhuset TD, Sas-Paszt L, Bakker MR, Püttsepp Ü et al. (2007) Tree fine root Ca/Al molar ratioindicator of Al and acidity stress. Plant Biosyst141, 460-480.
80. Wang JW and Kao CH (2004) Reduction of aluminum-inhibited root growth of rice seedlings with supplemental calcium, magnesium and organic acids. Crop Environ Bioinform1, 191-198.
81. Wang P, BI S, and Han W (2006) Aluminum tolerance of two wheat cultivars (Brevor and Atlas66) in relation to their rhizosphere pH and organic acids exuded from roots. J Agric Food Chem54, 10033-10039.
82. Xiao XX, Yang ZW, Zhong R, and Chen L (2003) Effect of aluminum stress on cell ultrastructure of leaf and root of longan. Scientia Silvae Sinicae23, 58-63.
83. Ying XF, Liu P, Xu GD, Lu QD, and Zhu SL (2005) Screening of soybean genotypes with tolerance to aluminum toxicity and study of the screening indices. Chin J Oil Crop Sci27, 46-51.
84. Yu HN, Liu P, Wang ZY, Chen WR, and Xu GD (2011) The effect of aluminum treatments on the root growth and cell ultrastructure of two soybean genotypes. Crop Protection30, 323-328.
85. Zakir H, Koyama H, and Hara T (2003) Growth and cell wall properties of two wheat cultivars differing in their sensitivity to aluminum stress. J Plant Physiol163, 39-47.
86. Zhang WH, Ryan PR, and Tyerman SD (2001) Malate-permeable channels and cation channels activated by aluminium in the apical cells of wheat roots. Plant Physiol125, 1459-1472.
87. Zheng SJ and Yang JL (2005) Target sites of aluminum Phytotoxicity. Biol Plant49, 321-331.
88. Zhou S, Sauvé R, and Thannhauser TW (2009) Proteome changes induced by aluminum stress in tomato roots. J Exp Bot57 4201-4213.
89. Zobel RW and Kinraide TB (2007) Fine root diameters can change in response to nutrient concentrations. Plant Soil297, 243-254.