Full Text:   <2342>

CLC number: S512

On-line Access: 

Received: 2006-06-02

Revision Accepted: 2006-07-28

Crosschecked: 0000-00-00

Cited: 24

Clicked: 6072

Citations:  Bibtex RefMan EndNote GB/T7714

-   Go to

Article info.
1. Reference List
Open peer comments

Journal of Zhejiang University SCIENCE B 2006 Vol.7 No.10 P.769-787


Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods

Author(s):  WANG Jun-ping, RAMAN Harsh, ZHANG Guo-ping, MENDHAM Neville, ZHOU Mei-xue

Affiliation(s):  Tasmanian Institute of Agricultural Research and School of Agricultural Science, University of Tasmania, P.O. Box, Kings Meadows, TAS 6249, Australia; more

Corresponding email(s):   mzhou@utas.edu.au

Key Words:  Barley, Al toxicity, Al tolerance

Share this article to: More |Next Article >>>

WANG Jun-ping, RAMAN Harsh, ZHANG Guo-ping, MENDHAM Neville, ZHOU Mei-xue. Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods[J]. Journal of Zhejiang University Science B, 2006, 7(10): 769-787.

@article{title="Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods",
author="WANG Jun-ping, RAMAN Harsh, ZHANG Guo-ping, MENDHAM Neville, ZHOU Mei-xue",
journal="Journal of Zhejiang University Science B",
publisher="Zhejiang University Press & Springer",

%0 Journal Article
%T Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods
%A WANG Jun-ping
%A RAMAN Harsh
%A ZHANG Guo-ping
%A MENDHAM Neville
%A ZHOU Mei-xue
%J Journal of Zhejiang University SCIENCE B
%V 7
%N 10
%P 769-787
%@ 1673-1581
%D 2006
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.2006.B0769

T1 - Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods
A1 - WANG Jun-ping
A1 - RAMAN Harsh
A1 - ZHANG Guo-ping
A1 - MENDHAM Neville
A1 - ZHOU Mei-xue
J0 - Journal of Zhejiang University Science B
VL - 7
IS - 10
SP - 769
EP - 787
%@ 1673-1581
Y1 - 2006
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.2006.B0769

Aluminium (Al) toxicity is one of the major limiting factors for barley production on acid soils. It inhibits root cell division and elongation, thus reducing water and nutrient uptake, consequently resulting in poor plant growth and yield. Plants tolerate Al either through external resistance mechanisms, by which Al is excluded from plant tissues or internal tolerance mechanisms, conferring the ability of plants to tolerate Al ion in the plant symplasm where Al that has permeated the plasmalemma is sequestered or converted into an innocuous form. barley is considered to be most sensitive to al toxicity among cereal species. al tolerance in barley has been assessed by several methods, such as nutrient solution culture, soil bioassay and field screening. Genetic and molecular mapping research has shown that al tolerance in barley is controlled by a single locus which is located on chromosome 4H. Molecular markers linked with al tolerance loci have been identified and validated in a range of diverse populations. This paper reviews the (1) screening methods for evaluating al tolerance, (2) genetics and (3) mechanisms underlying al tolerance in barley.

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article


[1] Aitken, R.L., Moody, P.W., Compton, B.L., 1990. A simple bioassay for the diagnosis of aluminium toxicity in soils. Commun. Soil. Sci. Plant Anal., 21:511-529.

[2] Alam, S.M., 1981. Influence of aluminium on plant growth and mineral nutrition of barley. Commun. Soil Sci. Plant Anal., 12:121-138.

[3] Alam, S.M., Adams, W.A., 1980. Effects of aluminium upon the growth and nutrition composition of oats. Pak. J. Sci. Res., 23:130-135.

[4] Aniol, A., 1995. Physiological aspects of aluminium tolerance associated with the long arm of chromosome 2D of the wheat (Triticum aestivum L.) genome. Theor. Appl. Genet., 91:510-516.

[5] Aniol, A., 1997. The Aluminium Tolerance in Wheat. In: Ruzgas, V., Lemezis, E., Apanaviciene, M., Basiulis, A., Bilis, J. (Eds.), Proceedings of the International Conference: Plant Breeding: Theories, Achievements and Problems. Kedainiai, Lithuania, p.4-22.

[6] Aniol, A., 2004. Chromosomal location of aluminium tolerance genes in rye. Plant Breeding, 123(2):132-136.

[7] Aniol, A., Gustafson, J.P., 1984. Chromosome location of genes controlling aluminium tolerance in wheat, rye and triticate. Can. J. Genet. Cytol., 26:701-705.

[8] Arumuganathan, K., Earle, E.D., 1991. Nuclear DNA content of some important plant species. Plant Mol. Bio. Rep., 9:208-219.

[9] Bache, B.W., Ross, J., 1991. Effect of phosphorus and aluminum in the response of spring barley to soil acidity. J. Agric. Sci., 117:299-305.

[10] Ball, S., Mulla, T., Konzak, C.F., 1993. Spatial heterogeneity affects variety trial interpretation. Crop Sci., 33:931-935.

[11] Becker, J., Heun, M., 1995. Barley microsatellite: allele variation and mapping. Plant Mol. Biol., 27(4):835-845.

[12] Bennet, R.J., Breen, C.M., Fey, M.V., 1985. The primary site of aluminium injury in the root of Zea mays L. South African J. Plant Soil, 2:8-17.

[13] Bergmann, W., 1992. Nutritional Disorders of Plants: Development, Visual and Analytical Diagnosis. Gustav Fisher Verlag, Jena, Germany.

[14] Blamey, F.C.P., Dowling, A.J., 1995. Antagonism between aluminium and calcium for sorption by calcium pectate. Plant Soil, 171(1):137-140.

[15] Blamey, F.C.P., Edmeades, D.C., Wheeler, D.M., 1990. Role of root cation-exchange capacity in differential aluminium tolerance of lotus species. J. Plant Nutr., 13:729-744.

[16] Blamey, F.C.P., Asher, C.J., Edwards, D.G., Kerven, G.L., 1993. In vitro evidence of aluminium effects on solution movement through root cell walls. J. Plant Nutr., 16:555-562.

[17] Bona, L., Wright, R.J., Baligar, V.C., Matuz, J., 1993. Screening wheat and other small grains for acid soil tolerance. Landscape and Urban Planning, 27(2-4):175-178.

[18] Bona, L., Wright, R.J., Carver, B.F., 1998. A proposed scale for quantifying aluminium tolerance levels in wheat and barley detected by hematoxylin staining. Cereal Res. Commun., 26(1):97-99.

[19] Borie, B.F., Stange, J.B., Morales, L.A., Pino, B.M., 1994. Effect of aluminium and acidity on root growth in barley (Hordeum vulgare L.) and oats (Avena sativa L.). Agricultura Tecnica (Santiago), 54:224-230.

[20] Brady, D.J., Edwards, D.G., Asher, C.J., Blamey, F.C.P., 1993. Calcium amelioration of aluminium toxicity effects on root hair development in soybean (Glycin max L.) Merr. New Phytol., 123(3):531-538.

[21] Büschges, R., Hokkricher, K., Panstruga, R., Simmons, G., Wolter, M., Frijters, A., van Dealen, R., van der Lee, T., Diergaarde, P., Groenendijk, J., et al., 1997. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell, 88(5):695-705.

[22] Caldwell, C., 1989. Analysis of aluminium and divalent cation binding to wheat root plasma membrane proteins using terbium phosphorescence. Plant Physiol., 91:233-241.

[23] Camargo, C.E.O., 1981. Wheat improvement. I. The heritability of tolerance to aluminium toxicity. Bragantia, 40:33-45.

[24] Carpita, N.C., Gibeaut, D.M., 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with physical properties of the walls during growth. Plant J., 3(1):1-30.

[25] Carver, B.F., Ownby, J.D., 1995. Acid soil tolerance in wheat. Adv. Agron., 54:117-173.

[26] Carver, B.F., Inskeep, W.P., Wilson, N.P., Westerman, R.L., 1988. Seedling tolerance to aluminium toxicity in hard red winter wheat germplasm. Crop Sci., 28:463-467.

[27] Carver, B.F., Whitmore, W.E., Smith, E.L., Bona, L., 1993. Registration of four aluminium-tolerant winter wheat germplasms two susceptible near-isolines. Crop Sci., 33:1113-1114.

[28] Clark, R.B., Pier, H.A., Knudsen, D., Maranville, J.W., 1981. Effect of trace element deficiencies and excesses on mineral nutrients in sorghum. J. Plant Nutr., 3:357-374.

[29] Clarkson, D.T., 1966. Effect of aluminium on the uptake and metabolism of phosphorus of barley seedlings. Plant Physiol., 41:165-172.

[30] Clarkson, D.T., 1967. Interaction between aluminium and phosphorus on root surface and cell wall materials. Plant Soil, 27(3):347-356.

[31] Cocker, K.M., Evans, D.E., Hodson, M.J., 1998. The amelioration of aluminium toxicity by silicon in wheat (Triticum aestivum L.): malate exudation as evidence for an in planta mechanism. Planta, 204(3):318-323.

[32] Cruz-Ortega, R., Cushman, J.C., Ownby, J.D., 1997. cDNA clones encoding 1,3-β-glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots. Plant Physiol., 114(4):1453-1460.

[33] de la Fuente, J.M., Ramírez-Rodríguez, V., Cabrera-Ponce, J.L., Herrera-Estrella, L., 1997. Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science, 276(5318):1566-1568.

[34] de Lima, M.L., Copeland, L., 1994. Changes in the ultrastructure of the root tip of wheat following exposure to aluminium. Aust. J. Plant Physiol., 21:85-94.

[35] Delhaize, E., Ryan, P.R., 1995. Aluminium toxicity and tolerance in plants. Plant Physiol., 107:315-321.

[36] Delhaize, E., Craig, S., Beaton, C.D., Bennet, R.J., Jagadish, V.C., Randall, P.J., 1993. Aluminum tolerance in wheat (Triticum aestivum L.). I. Uptake and distribution of aluminum in root apices. Plant Physiol., 103:685-693.

[37] Delhaize, E., Hebb, D.M., Ryan, P.R., 2001. Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol., 125(4):2059-2067.

[38] Delhaize, E., Ryan, P.R., Hebb, D.M., Yamamoto, Y., Sasaki, T., Matsumoto, H., 2004. Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc. Natl. Acad. Sci. USA, 101(42):15249-15254.

[39] Duke, J.A., 1982. Plant Germplasm Resources for Breeding of Crops Adapted to Marginal Environments. In: Christiansen, M.N., Lews, C.F. (Eds.), Breeding Plants for Less Favourable Environments. John Wiley and Son, New York, p.339-433.

[40] Ezaki, B., Tsgita, S., Matsumoto, H., 1996. Expression of moderately anionic peroxidase is induced by aluminum treatment in tobacco cells: possible involvement of peroxidase isozymes in aluminium ion stress. Physiol. Plant., 96(1):21-28.

[41] Ezaki, B., Gardner, R.C., 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(3):657-665.

[42] Ezaki, B., Katsuhara, M., Kawamura, M., Matsumoto, H., 2001. Different mechanisim of four aluminum (Al)-resisitance transgenes for Al toxicity in Arabidopsis. Plant Physiol., 127(3):918-927.

[43] Fisher, J.A., Scott, B.J., 1987. Response to Selection for Aluminium Tolerance. In: Searle, P.G.E., Davey, B.G. (Eds.), Priorities in Soil/Plant Relations Research for Plant Production. Univ. of Sydney, Australia, p.135-137.

[44] Foy, C.D., 1976. General Principles Involved in Screening Plants from Aluminium and Manganese Tolerance. In: Wright, M.J., Ferrari, A.S. (Eds.), Plant Adaptation to Mineral Stress in Problem Soils. Cornel Univ. Press, Ithaca, p.255-267.

[45] Foy, C.D., 1983. The physiological of plant adaptation to mineral stress. Iowa State J. Res., 57:355-391.

[46] Foy, C.D., 1984. Physiological Effects of Hydrogen, Aluminium and Manganese Toxicities in Acid Soils. In: Adams, F. (Ed.), Soil Acidity and Liming, 2nd Ed. Soil Sci. Soc. Am., Amer. Soc. Agron., and Crop Sci. Soc. Am., Medison, Wisconsin, p.57-97.

[47] Foy, C.D., 1988. Plant adaptation to acid, aluminium-toxic soils. Commun. Soil Sci. Plant Anal., 19:959-987.

[48] Foy, C.D., 1992. Soil Chemical Factors Limiting Plant Root Growth. In: Hatfield, J.L., Stewart, B.A. (Eds.), Advances in Soil Science: Limitation to Plant Root Growth, Vol. 19. Springer-Verlag, New York, p.97-149.

[49] Foy, C.D., 1996. Tolerance of barley cultivars to an acid, aluminium-toxic subsoil related to mineral element concentrations in their shoots. J. Plant Nutr., 19:1361-1380.

[50] Foy, C.D., Fleming, A.L., 1982. Aluminium tolerance of two wheat cultivars related to nitrate reductase activities. J. Plant Nutr., 5:1313-1333.

[51] Foy, C.D., Armiger, W.H., Briggle, L.W., Reid, D.A., 1965. Differential aluminum tolerance of wheat and barley varieties in acid soils. Agron. J., 57:413-417.

[52] Foy, C.D., Fleming, A.L., Burns, G.R., Armiger, W.H., 1967. Characterisation of differential aluminium tolerance among varieties of wheat and barley. Soil Sci. Soc. Am. Proc., 31:513-521.

[53] Foy, C.D., Chaney, R.L., White, M.C., 1978. The physiology of metal toxicity in plants. Annu. Rev. Plant Physiol., 29(1):511-566.

[54] Foy, C.D., Scott, B., Fisher, J.A., 1988. Genetic Differences in Plant Tolerance to Manganese Toxicity. In: Graham, R.D., Hannam, R.J., Uren, N.C. (Eds.), Manganese in Soils and Plants. Kluwer Academic Publishers, the Netherlands, p.293-307.

[55] Furlani, R.R., Clark, R.B., 1981. Screening sorghum for aluminium tolerance in nutrient solution. Agron. J., 73:587-594.

[56] Gallardo, F., Borie, F., Alvear, L., Baer, E.V., 1999. Evaluation of aluminium tolerance of three barley cultivars by two short-term screening methods and field experiments. Soil Sci. Plant Nutr., 45:713-719.

[57] Gallego, F.J., Calles, B., Benito, C., 1998a. Molecular markers linked to the aluminium tolerance gene Alt1 in rye (Secale cereale L.). Theor. Appl. Genet., 97(7):1104-1109.

[58] Gallego, F.J., Lopez-Solanilla, E., Figueiras, A.M., Benito, C., 1998b. Chromosomal location of PCR fragments as a source of DNA markers linked to aluminium tolerance genes in rye. Theor. Appl. Genet., 96(3-4):426-434.

[59] Garvin, D.F., Carver, B.F., 2003. The Role of the Genotype in Tolerance to Acidity and Aluminum Toxicity. In: Rengel, Z. (Ed.), Handbook of Soil Acidity. Marcel Dekker, New York, p.387-406.

[60] Gauthier, F.M., 1953. Tolerance of barley varieties to soil acidity. Cereal Newsl., 3:12.

[61] Hamel, F., Breton, C., Houde, M., 1998. Isolation and characterization of wheat aluminum-regulated genes: possible involvement of aluminum as a pathogenesis response elicitor. Planta, 205(4):531-538.

[62] Hammond, K.E., Evans, D.E., Hodson, M.J., 1995. Aluminium silicon interactions in barley (Hordeum vulgare L.) seedlings. Plant Soil, 173(1):89-95.

[63] Haug, A., Shi, B., 1991. Biochemical Basis of Aluminium Tolerance in Plant Cells. In: Wright, R.J., Baligar, V.C., Murrmann, R.P. (Eds.), Plant-Soil Interactions at Low pH. Kluwer Academic Publishers, Dordrecht, the Netherlands, p.839-850.

[64] Hede, A.R., Skovmand, B., Ribaut, J.M., Gonzalez-de-leon, D., Stфlen, O., 2002. Evaluation of aluminium tolerance in a spring rye collection by hydroponic screening. Plant Breeding, 121(3):241-248.

[65] Henderson, M., Ownby, J.D., 1991. The role of root cap mucilage secretion in aluminium tolerance in wheat. Curr. Topics Plant Biochem. Physiol., 10:134-141.

[66] Hoekenga, O.A., Vision, T.J., Shaff, J.E., Monforte, A.J., Lee, G.P., Howell, S.H., Kochian, L.V., 2003. Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta×Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol., 132(2):936-948.

[67] Hoekenga, O.A., Maron, L.G., Piñeros, M.A., Cançado, G.M., Shaff, J., Kobayashi, Y., Ryan, P.R., Dong, B., Delhaize, E., Sasaki, T., et al., 2006. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc. Natl. Acad. Sci. USA, 103(25):9738-9743.

[68] Horst, W.J., Wagner, A., Marschner, H., 1982. Mucilage protects root meristems from aluminium injury. Z. Pflanzenphysiol., 105:435-444.

[69] Hossain, M., Zhou, M.X., Mendham, N.J., 2005. A reliable screening system for aluminium tolerance in barley cultivars. Aust. J. Agric. Res., 56(5):475-482.

[70] Hu, X.M., Pan, J.W., Chen, H., Zhu, M.Y., 2002. Aluminum-induced ultraweak luminescence changes in root-tip cells of barley. J. Zhejiang Univ. (Agric. Life Sci.), 18:383-386 (in Chinese).

[71] IRRI, 1974. International Rice Research Institute Report for 1973. IRRI, Los Banos, Philippines.

[72] Ishikawa, S., Wagamatsu, T., Sasaki, R., Manu, P.O., 2000. Comparison of the amount of citric and malic acids in Al media of seven plant species and two cultivars each in five plant species. Soil Sci. Plant Nutr., 46:751-758.

[73] Kamprath, E.J., Foy, C.D., 1985. Lime-fertilizer-plant Interactions in Acid Soils. Fertilizer Technology and Use, p.91-151.

[74] Kidd, P.S., Llugany, M., Poschenrieder, C., Gunse, B., 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. Bot., 52(359):1339-1352.

[75] Kinraide, T.B., Arnold, R.C., Baligar, V.C., 1985. A rapid assay for aluminium phytotoxicity at submicromolar concentrations. Physiol. Plant., 65(3):245-250.

[76] Kinraide, T.B., Ryan, P.R., Kochian, L.V., 1992. Interactive effects of Al3+, H+, and other cations on root elongation considered in terms of cell-surface electrical potential. Plant Physiol., 99:1461-1468.

[77] Kochian, L.V., 1995. Cellular mechanism of aluminium toxicity and resistance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 46(1):237-260.

[78] Kochian, L.V., Pence, N.S., Letham, D.L.D., Pineros, M.A., Magalhaes, J.V., Hoekenga, O.A., Garvin, D.F., 2002. Mechanisms of metal resistance in plants: aluminum and heavy metals. Plant Soil, 247(1):109-119.

[79] Kochian, L.V., Piñeros, M.A., Hoekenga, O.A., 2005. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil, 274(1-2):175-195.

[80] Li, X.F., Ma, J.F., Matsumoto, H., 2000. Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol., 123(4):1537-1543.

[81] Li, C.D., Lance, R.M.C., Collins, H.M., Tarr, A., Roumeliotis, S., Harasymow, S., Cakir, M., Fox, G.P., Grime, C.R., Broughton, S., et al., 2003. Quantitative trait loci controlling kernel discoloration in barley (Hordeum vulgare L.). Aust. J. Agric. Res., 54(12):1251-1259.

[82] Liang, Y.C., Yang, C.G., Shi, H.H., 2001. Effects of silicon on growth and mineral composition of barley grown under toxic levels of aluminum. J. Plant Nutr., 24(2):229-243.

[83] Lindberg, S., 1990. Aluminium interaction with K+ (86Rb+) and 45Ca+ fluxes in three cultivars of sugar beet (Beta vulgaris). Physiol. Plant., 79(2):275-282.

[84] Lindberg, S., Griffiths, G., 1993. Aluminium effects on ATPase activity and lipid composition of plasma membrane of sugar beet roots. J. Exp. Bot., 44(10):1543-1550.

[85] Little, R., 1988. Plant soil interactions at low pH: problem solving—the genetic approach. Commun. Soil Sci. Plant Anal., 19:1239-1257.

[86] Lisitsyn, E.M., 2000. Intravarietal level of aluminum resistance in cereal crops. J. Plant Nutr., 23:793-804.

[87] Loper, M., Brauer, D., Patterson, D., Tu, S.I., 1993. Aluminium inhibition of NADH-linked electron transfer by corn root plasma membrane. J. Plant Nutr., 16:507-514.

[88] Luo, M.C., Dvorak, J., 1996. Molecular mapping of an aluminum tolerance locus on chromosome 4D of Chinese Spring wheat. Euphytica, 91:31-35.

[89] Ma, J.F., Zheng, J.S., Li, X.F., Takeda, K., Matsumoto, H., 1997. A rapid hydroponic screening for aluminium tolerance in barley. Plant Soil, 191(1):133-137.

[90] Ma, J.F, Ryan, P.R., Delhaize, E., 2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci., 6(6):273-278.

[91] Ma, J.F., Shen, R., Zhao, Z., Wissuwa, M., Takeuchi, Y., Ebitani, T., Yano, M., 2002. Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol., 43(6):652-659.

[92] Ma, J.F., Nagao, S., Sato, K., Ito, H., Furukawa, J., Tekeda, K., 2004. Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley. J. Exp. Bot., 55(401):1335-1341.

[93] Maltais, K., Houde, M., 2002. A new biochemical markers for aluminium tolerance in plants. Physiol. Plant., 115(1):81-87.

[94] Mao, C., Yi, K., Yang, L., Zheng, B., Wu, Y., Liu, F., Wu, P., 2003. Identification of aluminium-regulated genes by cDNA-AFLP in rice (Oryza sativa L.): Al-regulated genes for the metabolism of cell wall components. J. Exp. Bot., 55(394):137-143.

[95] Matos, M., Camacho, M.V., Pérez-Flores, V., Pernaute, B., Pinto-Carnide, O., Benito, C., 2005. A new aluminum tolerance gene located on rye chromosome arm 7RS. Theor. Appl. Genet., 111:360-369.

[96] Matsumoto, H., Yamaya, T., 1986. Inhibition of potassium uptake and regulation of membrane-associated Mg2+-ATPase activity of pea roots by aluminium. Soil Sci. Plant Nutr., 32:179-188.

[97] Matsumoto, H., Yamamoto, Y., Kasai, M., 1992. Change of some properties of the plasma membrane-enhanced fraction of barley roots related to aluminium stress: membrane-associated ATPase, aluminium and calcium. Soil Sci. Plant Nutr., 38:411-419.

[98] Maxim, P., Duta, Z., 1996. Aluminium tolerance of barley 1. Efficiency of in vivo procedure in estimation of genotypic differences. Romanian Agric. Res., (5-6):21-28.

[99] Miftahudin, G., Scoles, J., Gustafson, J.P., 2002. AFLP markers tightly linked to the aluminum-tolerance gene Alt3 in rye (Secale cereale L.). Theor. Appl. Genet., 104(4):626-631.

[100] Milla, M.A.R., Gustafson, J.P., 2001. Genetic and physical characterization of chromosome 4DL in wheat. Genome, 44(5):883-892.

[101] Milla, M.A.R., Butler, E., Huete, A.R., Wilson, C.F., Anderson, O., Gustafson, J.P., 2002. Expressed sequence tag-based gene expression analysis under aluminum stress in rye. Plant Physiol., 130(4):1706-1716.

[102] Millard, M.M., Foy, C.D., Coradetti, C.A., Reinsel, M.D., 1990. X-ray photoelectron spectroscopy surface analysis of aluminium ion stress in barley roots. Plant Physiol., 93:578-583.

[103] Minella, E., Sorrells, M.E., 1992. Aluminium tolerance in barley: genetic relationships among genotypes of diverse origin. Crop Sci., 32:593-598.

[104] Minella, E., Sorrells, M.E., 1997. Inheritance and chromosome location of Alp, a gene controlling aluminium tolerance in ‘Dayton’ barley. Plant Breeding, 116(5):465-469.

[105] Miyasaka, S.C., Buta, J.G., Howell, R.K., Foy, C.D., 1991. Mechanism of aluminium tolerance in snapbeans: root exudation of citric acid. Plant Physiol., 96:737-743.

[106] Moore, D.P., Kronstad, W.E., Metzger, R.J., 1977. Screening Wheat for Aluminium Tolerance. In: Wright, M.J., Ferrari, S.A. (Eds.), Plant Adaptation to Mineral Stress in Problem Soils. Special Publ., Cornell Univ. Agr. Exp. Sta., Ithaca, New York, p.287-295.

[107] Mugwira, L.M., Elgawhary, S.M., Patel, K.I., 1976. Differential tolerances of Triticale, wheat, rye and barley to aluminium in nutrient solution. Agron. J., 68:782-787.

[108] Nguyen, V.T., Burrow, M.D., Nguyen, H.T., Le, B.T., Le, T.D., Paterson, A.H., 2001. Molecular mapping of genes conferring aluminium tolerance in rice (Oryza sativa L.). Theor. Appl. Genet., 102(6-7):1002-1010.

[109] Nguyen, V.T., Nguyen, B.D., Sarkarung, S., Martinez, C., Paterson, A.H., Nguyen, H.T., 2002. Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds. Mol. Genet. Genomics, 267(6):772-780.

[110] Nguyen, B.D., Brar, D.S., Bui, B.C., Nguyen, T.V., Pham, L.N., Nguyen, H.T., 2003. Identification and mapping of QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., to indica rice (Oryza sativa L.). Theor. Appl. Genet., 106:583-593.

[111] Ninamango-Cárdenas, F.E., Guimaraes, C.T., Martins, P.R., Parentoni, S.N., Carneiro, N.P., Lopes, M.A., Moro, J.R., Paiva, E., 2003. Mapping QTLs for aluminum tolerance in maize. Euphytica, 130(2):223-232.

[112] Ohki, K., 1986. Photosynthesis, chlorophyll and transpiration responses in aluminium stressed wheat and sorghum. Crop Sci., 26:572-575.

[113] Oram, R.N., 1983. Breeding Barley Tolerant to High Soil Acidity and Waterlogging. In: Driscoll, C.J. (Ed.), Proc. Aust. Plant Breed. Conf. Adelaide, South Australia, p.71-73.

[114] Ownby, J.D., 1993. Mechanisms of reaction of hematoxylin with aluminium-treated wheat roots. Physiol. Plant., 87: (3)371-380.

[115] Parker, D.R., 1995. Root growth analysis: an underutilization approach to understanding aluminium rhizotoxicity. Plant Soil, 171(1):151-157.

[116] Polle, E., Konzak, C.F., 1985. A single scale for determining Al tolerance levels in cereals. Agron. Abstr., p.67.

[117] Polle, E., Konzak, C.F., Kittrick, A.J., 1978. Visual detection of aluminium tolerance levels in wheat by hematoxylin staining of seedling roots. Crop Sci., 18:823-827.

[118] Puthota, V., Cruz-Ortega, R., Johnson, J., Ownby, J., 1991. An Ultrastructural Study of the Inhibition of Mucilage Secretion in Wheat Root Cap by Aluminium. In: Wright, R.J., Baligar, V.C., Murrmann, R.P. (Eds.), Plant-Soil Interactions at Low Soil pH. Kluwer Academic Publishers, Dordrecht, the Netherlands, p.779-787.

[119] Raman, H., Moroni, S., Raman, R., Karakousis, A., Read, B., Sato, K., Scott, B.J., 2001. A Genomic Region Associated with Aluminium Tolerance in Barley. Proceedings of the 10th Australian Barley Technical Symposium. Http://www.regional.org.au/au/abts/2001/t3/raman.htm

[120] Raman, H., Moroni, J.H., Saito, K., Read, B.J., Scott, B.J., 2002. Identification of AFLP and microsatellite markers linked with an aluminium tolerance gene in barley (Hordeum vulgare L.). Theor. Appl. Genet., 105(2-3):458-464.

[121] Raman, H., Karakousis, A., Moroni, J.S., Raman, R., Read, B., Garvin, D.F., Kochian, L.V., Sorrells, M.E., 2003. Development and allele diversity of microsatellite markers linked to the aluminium tolerance gene Alp in barley. Aust. J. Agric. Res., 54(12):1315-1321.

[122] Raman, H., Wang, J.P., Read, B., Zhou, M.X., Venkataganappa, S., Moroni, J.S., O'Bree, B., Mendham, N., 2005a. Molecular Mapping of Resistance to Aluminium Toxicity in Barley. Proceedings of Plant and Animal Genome XIII Conference. San Diego, USA, p.154. Http://www.intl-ag.org/13/abstracts/PAG13_P328.htm

[123] Raman, H., Zhang, K., Cakir, M., Appels, R., Moroni, J.S., Maron, L.G., Kochian, L.V., Raman, R., Imtiaz, M., Drake-Brockman, F., et al., 2005b. Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome, 48:781-791.

[124] Read, B.J., Scott, B.J., 1983. Tolerance of Barley to Aluminium and Manganese. Proceedings of the 8th Australasian Plant Breeding Conference. Adelaide, p.333-334.

[125] Read, B.J., Oram, R.N., 1995. Hordeum vulgare (Barley) cv. Brindabella. Aust. J. Exp. Agric., 35(3):425.

[126] Read, B., Raman, H., McMichael, G., Chalmers, K., Ablett, G., Platz, G.J., Raman, R., Genger, R., Boyd, R., Park, R.F., et al., 2003. Mapping and QTL analysis of the barley population Sloop/Halcyon. Aust. J. Agric. Res., 54(12):1145-1153.

[127] Reid, D.A., 1970. Genetic Control of Reaction to Aluminum in Winter Barley. In: Nilan, R.A. (Ed.), Proceedings of the 2nd International Barley Genetics Symposium. Washington State University Press, Pullman, WA, p.409-413.

[128] Reid, D.A., Jones, G.D., Armiger, W.H., Foy, C.D., Hoch, E.J., Sterling, T.M., 1969. Differential aluminium tolerance of winter barley varieties and selections in associated greenhouse and field experiment. Agron. J., 61:218-222.

[129] Reid, D.A., Fleming, A.I., Foy, C.D., 1971. A method for determining aluminium response of barley in nutrient solution in comparison to response in Al-toxic soil. Agron. J., 63:600-603.

[130] Rengel, Z., Elliott, D.C., 1992. Mechanism of aluminium inhibition of net 45Ca2+ uptake by Amaranthus protoplasts. Plant Physiol., 98:632-638.

[131] Richards, K.D., Schott, E.J., Sharma, Y.K., Davis, K.R., Gardner, R.C., 1998. Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol., 116(1):409-418.

[132] Riede, C.R., Anderson, J.A., 1996. Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Sci., 36:905-909.

[133] Rincon, M., Gonzales, R., 1992. Aluminium partitioning in intact roots of aluminium-tolerant and aluminium-sensitive wheat (Triticum aestivum L.) cultivars. Plant Physiol., 99:1021-1028.

[134] Ruiz-Torres, N.A., Carver, B.F., 1992. Genetic expression of aluminium tolerance in hard red winter wheat. Cereal Res. Com., 20:233-240.

[135] Ryan, P.R., Delhaize, E., Randall, P.J., 1995. Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta, 196(1):103-111.

[136] Ryan, P.R., Raman, H., Zhang, K., Moroni, J.S., Appels, R., Sasaki, T., Matsumoto, H., Hebb, D., Delhaize, E., 2004. Molecular Mapping of Wheat ALMT1 Gene for Aluminium Tolerance and Its Function in Heterologous Expression Systems. VI. International Symposium on Plant-Soil Interaction at Low pH. Sendai, Japan.

[137] Sasaki, T., Ezaki, B., Matsumoto, H., 2002. A gene encoding multidrug resistance (MDR)-like protein is induced by aluminum and inhibitors of calcium flux in wheat. Plant Cell Physiol., 43(2):177-185.

[138] Sasaki, T.Y.Y., Ezaki, B., Katsuhara, M., Ahn, S.J., Ryan, P.R., Delhaize, E., Matsumoto, H., 2004. A wheat gene encoding an aluminium-activated malate transporter. Plant J., 37(5):645-653.

[139] Scott, B.J., Fisher, J.A., 1989. Selection of Genotypes Tolerant of Aluminium and Manganese. In: Robson, A.D. (Ed.), Soil Acidity and Plant Growth. Academic Press, Australia, p.167-203.

[140] Shuman, L.M., Wilson, D.O., Duncan, R.R., 1993. Screening wheat and sorghum cultivars for aluminium sensitivity at low aluminium levels. J. Plant Nutr., 16:2383-2395.

[141] Sibov, S.T., Gaspar, M., Silva, M.J., Ottoboni, L.M.M., Arruda, P., Souza, A.P., 1999. Two genes control aluminum tolerance in maize: genetic and molecular mapping analyses. Genome, 42(3):475-482.

[142] Simons, G., van der Lee, T., Diergaarde, P., van Dealen, R., Groenendijk, J., Frijters, A., Büschges, R., Hollricher, K., Töpsch, S., Schulze-Lefert, P., et al., 1997. AFLP-based fine mapping of the Mlo gene to a 30-kb DNA segment of the barley genome. Genomics, 44(1):61-70.

[143] Snowden, K.C., Richards, K.D., Gardner, R.C., 1995. Aluminum-induced genes: induction by toxic metals, low calcium, and wounding and pattern of expression in root tips. Plant Physiol., 107:341-348.

[144] Stange, M.B., Beratto, M.E., Montenegro, B.A., Peyrelongue, C.A., Borie, B.F., 1995. Effect of nitrogen source on growth of barley on a soil with a high aluminium content. Agricultura Tecnica (Santiago), 55:118-126.

[145] Stϕlen, O., Anderson, S., 1978. Inheritance of tolerance to low soil pH in barley. Heriditas, 88:101-105.

[146] Takagi, H., Namai, H., Murakami, K., 1981. Evaluation of the hematoxylin staining method for detecting wheat tolerance to aluminium. Japan J. Breed, 31:152-160.

[147] Tamas, L., Budikova, S., Simonovicova, M., Huttova, J., Siroka, B., Mistrik, I., 2006. Rapid and simple method for Al-toxicity analysis in emerging barley roots during germination. Biologia Plantarum, 50(1):87-93.

[148] Tang, Y., Sorrells, M.E., Kochian, L.V., Gravan, D.F., 2000. Identification of RFLP markers linked to the barley aluminium tolerance gene Alp. Crop Sci., 40:778-782.

[149] Taylor, G.J., 1988. The Physiology of Al Tolerance. In: Sigel, H., Sigel, A. (Eds.), Metal Ions in Biological Systems: Aluminium and Its Role in Biology. Marcel Dekker, NY, p.165-199.

[150] Taylor, G.J., 1991. Current views of the aluminium stress response: the physiological basis of tolerance. Curr. Top. Plant Biochem. Physiol., 10:57-93.

[151] Taylor, G.J., 1995. Overcoming barriers to understanding the cellular basis of aluminium resistance. Plant Soil, 171(1):89-103.

[152] von Uexküll, H.R., Mutert, E., 1995. Global extent, development and economic impact of acid soils. Plant Soil, 171(1):1-15.

[153] Wagatsuma, T., Yamasaku, K., 1985. Relationship between differential aluminium tolerance and plant induced pH change of medium among barley cultivars. Soil Sci. Plant Nutr., 31:521-535.

[154] Wagatsuma, T., Ishikawa, S., Obata, H., Tawaraya, K., Katohda, S., 1995. Plasma membrane of younger and outer cells is the primary specific site for aluminium toxicity in roots. Plant Soil, 171(1):105-112.

[155] Wang, J.P., Raman, H., Read, B., Zhou, M.X., Mendham, N.J., Venkatanagappa, S., 2006. Validation of an Alt locus for aluminium tolerance scored with eriochrome cyanine R staining method in barley cultivar Honen (Hordeum vulgare L.). Aust. J. Agric. Res., 57(1):113-118.

[156] Watt, D.A., 2003. Aluminium-responsive genes in sugarcane: identification and analysis of expression under oxidative stress. J. Exp. Bot., 54(385):1163-1174.

[157] Whitten, M., 1997. Subsurface Acdidification: Estimation Lime Requirements from Lime Dissolution Rates in the Field. In: Williamson, D.R. (Ed.), Proceedings of the Fourth Triennial Western Australian Soil Science Conference. African Reef Resort, Geraldton, Western Australia, p.128-131.

[158] Williams, C.H., 1980. Soil acidification under clover pasture. Aust. J. Exp. Agric., 20(106):561-567.

[159] Wu, P., Liao, C.Y., Hu, B., Yi, K.K., Jin, W.Z., Ni, J.J., He, C., 2000. QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor. Appl. Genet., 100(8):1295-1303.

[160] Xu, A.B., Dang, B.Y., Zhu, M.Y., Yuan, M.B., Huang, C.N., Yu, J.J., Huang, Q., Wu, Y.L., Ni, Z.Y., 1991. Screening barley varieties for tolerance of acidic aluminium. Crop genet. Res., 3:17-19.

[161] Yang, J.L., Zheng, S.J., He, Y.F., You, J.F., Zhang, L., Yu, X.H., 2006. Comparative studies on the effect of a protein-synthesis inhibitor on aluminum-induced secretion of organic acids from Fagopyrum esculentum Moench and Cassia tora L. roots. Plant Cell Environ., 29(2):240-246.

[162] Zhao, Z.Q., Ma, J.F., Sato, K., Takeda, K., 2003. Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). Planta, 217(5):794-800.

[163] Zheng, S.J., Ma, J.F., Matsumoto, H., 1998. High aluminum resistance in buckwheat: I. Al-induced special secretion of oxalic acid from root tips. Plant Physiol., 117(3):745-751.

[164] Zhu, M.Y., Pana, J., Wanga, L., Gua, Q., Huangd, C., 2003. Mutation induced enhancement of Al tolerance in barley cell lines. Plant Sci., 164(1):17-23.

Open peer comments: Debate/Discuss/Question/Opinion


Please provide your name, email address and a comment

Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2022 Journal of Zhejiang University-SCIENCE