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

Aluminium tolerance in barley ( Hordeum vulgare L.): physiological mechanisms, genetics and screening methods 1 2 first-author 2 3 1 1 corresp ‡Corresponding Author ‡Corresponding Author †E-mail:mzhou@utas.edu.au †E-mail:mzhou@utas.edu.au mzhou@utas.edu.au Tasmanian Institute of Agricultural Research and School of Agricultural Science, University of Tasmania, P.O. Box, Kings Meadows, TAS 6249, Australia Tasmanian Institute of Agricultural Research and School of Agricultural Science, University of Tasmania, P.O. Box, Kings Meadows, TAS 6249, Australia NSW Department of Primary Industries, Wagga Wagga Agricultural Institute, PMB, Wagga Wagga, NSW 2650, Australia NSW Department of Primary Industries, Wagga Wagga Agricultural Institute, PMB, Wagga Wagga, NSW 2650, Australia Department of Agronomy, Zhejiang University, Hangzhou 310029, China Department of Agronomy, Zhejiang University, Hangzhou 310029, China 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. Barley Al toxicity Al tolerance INTRODUCTION 1 Aluminium (Al) toxicity is one of the major constraints on crop productivity on acid soils, which occur on up to 40% of the arable lands of the world (Kochian, 1995 1995 ). Al is the third most abundant element in the earth’s crust and is toxic to plants when solubilised into soil solution at acidic pH values (Kochian, 1995 1995 ). A total of 3950 million hectares of land is classed as having acidic soil, of which 15% is used for planting of annual and perennial crops (von Uexküll and Mutert, 1995 1995 ). Soils are becoming more acidic by certain farming practices, for example the application of ammonium-based fertilizers (Kochian et al., 2002 2002 ), and accumulation of organic matter (Williams, 1980 1980 ). In Australia, about 90 million hectares of agricultural land can be potentially affected and annually economic loss is estimated at more than USD 600 million ( http://www.science.org.au/nova/071/071box01.htm http://www.science.org.au/nova/071/071box01.htm ). At low pH, Al is solubilised as phytotoxic Al 3+ ions from non-toxic Al silicates and oxides (Hoekenga et al., 2003 2003 ). Although crop production on acid soils can be sustained by application of lime, runoff pollution is an undesirable effect (de la Fuente et al., 1997 1997 ). Liming is often not economic or practical because of the slow movement of lime especially in the deeper layers of subsoils (Foy et al., 1965 1965 ; Mugwira et al., 1976 1976 ). Furthermore, heavy application of lime may have adverse effects on some crops in the rotation or cause deficiencies of certain nutrients (Whitten, 1997 1997 ). Thus, developing cultivars with improved tolerance to acid soil stress is a solution to address this problem (Scott and Fisher, 1989 1989 ). In recent years, extensive research has been focused on this area, including evaluation of germplasm for Al tolerance, the biochemistry and physiology of Al toxicity and tolerance, and the genetics of Al tolerance. Barley is the fourth most important cereal crop globally. It is considered to be more sensitive to acidic soils than rye, oat, rice, and wheat (Bona et al., 1993 1993 ; Ishikawa et al., 2000 2000 ). This paper reviews advances in screening methods, mechanisms and genetics underlying Al tolerance especially in barley and related cereals. EFFECT OF Al TOXICITY ON GROWTH, DEVELOPMENT AND YIELD OF CROP PLANTS 1 Symptom of Al toxicity 2 Al toxicity is considered to be a complex of nutritional disorders of growth and development of plants, which may be manifested as a deficiency of essential nutrients like calcium, magnesium, iron or molybdenum; decreased availability of phosphorus or as toxicity of Mn and H + (Alam and Adams, 1980 1980 ; Foy, 1984 1984 ; 1988 1988 ; 1992 1992 ; Kamprath and Foy, 1985 1985 ; IRRI, 1974 1974 ; Clark et al., 1981 1981 ; Furlani and Clark, 1981 1981 ; Foy and Fleming, 1982 1982 ). The primary response to Al stress in plants occurs in roots, as reduced elongation at the tip, followed by swelling and distortion of differentiated cells, as well as root discolouration (Foy et al., 1978 1978 ; Bergmann, 1992 1992 ; Hossain et al., 2005 2005 ). Within meristematic and root cap cells, Al toxicity is associated with an increased vacuolation and turnover of starch grains (de Lima and Copeland, 1994 1994 ), as well as disruption of dictyosomes and their secretory function (Bennet et al., 1985 1985 ; Puthota et al., 1991 1991 ). The foliar symptoms in some plants resemble those of phosphorus deficiency manifested by overall stunting, small, dark green leaves, late maturity, purpling of stems, leaves and leaf veins, and yellowing and death of leaf tips (Foy, 1992 1992 ). Al stress decreases total chlorophyll concentration and photosynthetic rate, but the decline in transpiration rate is most severe (Ohki, 1986 1986 ). Al toxicity also appears as an induced calcium deficiency or as reduced Ca 2+ transport within plants, causing curling or rolling of young leaves, inhibited growth of lateral branches, or a collapse of growing points or petioles (Foy, 1992 1992 ). Effect of Al toxicity on plant growth and development 2 Al toxicity inhibits root cell division and elongation, thus reducing water and nutrient uptake, consequently resulting in poorer plant growth and yield (Alam, 1981 1981 ; Clarkson, 1966 1966 ; Foy, 1983 1983 ; Foy et al., 1967 1967 ; Gauthier, 1953 1953 ; Reid et al., 1969 1969 ; 1971 1971 ). Relative shoot and root dry weights in tolerant barley cultivars were two-fold and three-fold respectively compared to susceptible cultivars (Foy, 1996 1996 ). Al toxicity also limits both rooting depth and degree of root branching (Foy, 1992 1992 ). Parker ( 1995 1995 ) demonstrated that there are two responses to Al: an initial acute inhibition of growth that is followed by a later chronic Al effect on root growth. Al toxicity decreases drought tolerance and the use of subsoil nutrients (Carver and Ownby, 1995 1995 ). Gallardo et al.( 1999 1999 ) reported 50% and 30% reduction of grain yield, respectively for sensitive and tolerant cultivars of barley when they were grown in naturally acidic soil (pH 4.9) with a large amount of extractable Al compared to that grown in non acidic soil (pH 5.8). Oram ( 1983 1983 ) reported that Australian barley cultivars are generally tolerant to high soil manganese levels but sensitive to high Al levels. Australian cultivars did, however, outperform most tolerant lines introduced from Denmark in terms of grain and straw yield in a field trial experiment on soil with lime added (Oram, 1983 1983 ). Factors affecting Al toxicity 2 Al toxicity is affected by many factors such as pH, concentration of Al, temperature, and concentrations of cations and anions in culture solution. A pH 5.0 or above will reduce Al solubility (Reid et al., 1971 1971 ) thus reducing Al toxicity. Root elongation depended critically on the concentration of Ca 2+ , whether in the presence or absence of Al, with at least 0.2 mmol/L Ca 2+ being essential for optimum growth (Kinraide et al., 1985 1985 ). The concentration of Ca 2+ greatly influences the Al toxicity at a given pH and Al concentration. As the Ca 2+ concentration approached 1 mmol/L the inhibition by 1 μmol/L Al was nearly eliminated (Kinraide et al., 1985 1985 ). Increased concentrations of basic cations in solution of the root rhizosphere, particularly calcium, have been shown to ameliorate Al toxicity (Brady et al., 1993 1993 ). Mg 2+ at concentration of 0.5 mmol/L can also alleviate Al toxicity as did Ca 2+ (Kinraide et al., 1985 1985 ). Application of NH 4 Cl to a soil with a high exchangeable Al significantly reduced barley seedling emergence, shoot and root weights, spike numbers/m 2 and grain numbers/spike whereas NaNO 3 significantly increased all these parameters. At harvesting, soil analysis showed that NH 4 Cl significantly reduced soil pH and increased soil Al and Mn contents and this was confirmed by tissue analysis of shoots and roots (Stange et al., 1995 1995 ). NH 4 + -N induced release of H + from the roots particularly whilst NO 3 − -N significantly increased pH by release of OH − (Borie et al., 1994 1994 ). Adding excess P in nutrient solution will precipitate and detoxify Al (Kinraide et al., 1985 1985 ; Reid et al., 1971 1971 ). Field experiments identified that phosphate fertilizer allowed barley to withstand larger concentrations of soluble and exchangeable Al (Bache and Ross, 1991 1991 ). Silicon (as Na 2 SiO 3 ∙5H 2 O) significantly ameliorated the toxic effects of Al on root and shoot growth and decreased the Al concentration in the roots of barley seedlings under 25 and 50 μmol/L Al treatment (Hammond et al., 1995 1995 ), but exaggerated it at a higher concentration of Al (above 75 μmol/L) in barley (Liang et al., 2001 2001 ). In an Al-tolerant cultivar, Al-exposed plants pre-treated with Si exuded up to 15 times more phenolics than those plants not pre-treated with Si (Kidd et al., 2001 2001 ). However, Cocker et al.( 1998 1998 ) reported that Si does not reduce Al phytotoxicity as a result of Al/Si interactions in the external media, and that the mechanism of amelioration has an in planta component. SCREENING OF PLANTS FOR Al TOLERANCE 1 Genetic improvement of crops for acid soil tolerance has been accelerated by the availability of screening criteria for detecting Al tolerance. Laboratory- and greenhouse-based techniques are widely employed which are usually non-destructive, and can be applied in early developmental stages from seedlings only a few days old to flowering stage of the plants. Field-based screening techniques are more laborious, time consuming and expensive. Choice of a particular screening test is influenced by the kind of material under selection, i.e., germplasm collections for identifying suitable parents, segregating populations, or advanced breeding lines under consideration for release. Nutrient solution culture 2 Nutrient solution culture is the most common screening medium for Al tolerance, which provides easy access to root systems, tight control over nutrient availability and pH, and non-destructive measurement of tolerance (Carver and Ownby, 1995 1995 ). The experimental conditions including culture media, pH, Al concentration, and time of treatment used for screening barley germplasm are summarised in Table 1 1 . Because Al toxicity is affected by these factors, the experimental conditions need to be optimized. 2 Source pH Al (µmol/L) Temperature (°C) 2 Treatment time Light/dark (h) 3 Culture media 2 Material 2 Ma et al.( 1997 1997 ) 4.5 0, 5, 10, 20, 40 25/20 2 24 h 14/10 3 1 mmol/L CaCl 2 2 604 barley lines 2 Zhao et al.( 2003 2003 ) 5.0 10 25 2 24 h 3 Same as above 2 21 varieties 2 Gallardo et al.( 1999 1999 ) 4.8 0, 50, 100, 200 25 2 15 d 14/10 3 Ca 1270, K 750, NO 3 3710, NH 4 310, PO 4 100, SO 4 120, Fe 17.9, B 6.6, Mn 2.4, Zn 0.6, Cu 0.2, Mo 0.1 (µmol/L) 2 3 cultivars 2 Raman et al.( 2002 2002 ) 4.0, 4.3 100, 50, 10 24/18 2 Pulse treatment 1 d or 4 d, recovery 3 d 16/8 3 Ca 1000, Mg 400, K 1000, NO 3 3400, NH 4 600, PO 4 100, SO 4 401.1, Cl 78, Na 40.2, Fe 20, B 23, Mn 9, Zn 0.8, Cu 0.3, Mo 0.1 (µmol/L) 2 F 2 and F 3 2 Raman et al.( 2003 2003 ) 4.3 50, 25 24/18 2 Pulse treatment 1 d or 4 d, recovery 3 d 16/8 3 Same as above 2 F 3 2 Minella and Sorrells ( 1992 1992 ) 4.0 30, 60, 90 25 2 17 h 17/0 3 CaCl 2 4, KNO 3 6.5, MgCl 2 2.5, (NH 4 ) 2 SO 4 0.1, NH 4 NO 3 0.4 (mmol/L) 2 37 barley cultivars and F 2 s 2 2 Maxim and Duta ( 1996 1996 ) 3.9~4.1 30, 60, 90 22 2 17 h 17/0 3 Same as above 2 24 barley genoytpes 4.1, 4.2 74, 148 2 5 d for relative root elongation 3 2 2 Tang et al.( 2000 2000 ) 4.0 50 2 24 h 3 Same as above 2 F 2 , F 3 2 Reid et al.( 1971 1971 ) 4.8 4×10 −6 18~21 2 18 d 12/12 3 Ca 50.8, Mg 6.6, N 56, S 3.8, K 29.4, P 3, Na 0.01, Cl 0.34, Mn 0.13, Fe 1, B 0.07, Zn 0.04, Cu 0.0.1, Mo 0.005 (×10 −6 ) 2 30 varieties 2 Kinraide et al.( 1985 1985 ) 4.5 0, 0.25, 0.5, 0.75, 1.0 2 48 h 3 0.2 mmol/L CaSO 4 2 Dayton, Kearney 2 Lisitsyn ( 2000 2000 ) 4.3 1~2 mmol/L 21~23 2 5~7 d 3 Distilled water 2 75 barley cultivars 2 Hossain et al.( 2005 2005 ) 4.5 50~100 22 2 24 h 3 CaCl 2 4, KNO 3 6.5, MgCl 2 2.5, (NH 4 ) 2 SO 4 0.1, NH 4 NO 3 0.4 (mmol/L) 2 6 barley varieties There are two major criteria for evaluation of Al tolerance in nutrient solution culture. First, root length measurement is the most suitable approach for genetic and molecular studies in which a precise quantitative response for Al stress is needed. It is also suitable for identifying genotypes with superior alleles for Al tolerance (Hede et al., 2002 2002 ). Second, root staining is quicker and more efficient. It is suitable for screening a large segregating population derived from improved germplasm (Hede et al., 2002 2002 ). Haematoxylin (Polle et al., 1978 1978 ; Minella and Sorrells, 1992 1992 ; Bona et al., 1998 1998 ; Tang et al., 2000 2000 ) and eriochrome cyanine R (Fig. 1 1 ) (Aniol, 1995 1995 ; Ma et al., 1997 1997 ; Wang et al., 2006 2006 ) stains have been used for evaluation of barley germplasm. Other parameters such as ratio of root to shoot fresh weight (Ma et al., 2004 2004 ), ultra-weak luminescence (UL) analysis (Hu et al., 2002 2002 ) and nitro blue tetrazolium (NBT) reduction (Maltais and Houde, 2002 2002 ) have also been used for assessment of germplasm for Al tolerance. Variation in temperature in the growth chamber and minor fluctuation of pH of the nutrient solution, as it affects effective Al concentration, can reduce repeatability of the results (Moore et al., 1977 1977 ). The concentration of Al and duration of exposure are varied inversely. A long exposure to Al for 3~4 weeks requires much lower (about one third) concentrations than brief exposure of 24 h. Shuman et al.( 1993 1993 ) found effective screening of wheat cultivars using very low Al levels in solution to minimize Al precipitation and to more closely represent actual environmental stresses compared to traditional short-term exposure with higher Al concentrations. The longer exposure makes solution culture technically more difficult, requiring constant adjustments of pH, water loss and nutrient loss. Other variables to consider in solution-based screening are nutrient composition and standards for measuring tolerance. Changes in nutrient composition can change the intensity of Al stress at a given concentration (Foy et al., 1988 1988 ; Little, 1988 1988 ; Scott and Fisher, 1989 1989 ). Higher concentration of phosphorus may lead to Al-phosphate precipitates in Al solution and protect plants against Al toxicity. Hence, phosphorus is often avoided in nutrient solution, particularly in short-term Al exposures when phosphorus needs are satisfied by seed reserves. Tamas et al.( 2006 2006 ), however, indicated several disadvantages of hydroponics. For example, the transfer of young germinated barley seedlings to hydroponics can cause significant stress and requires a long period for the onset of several mechanisms to adapt to hydroponics, especially in plants sensitive to hypoxia. They have developed a filter-paper-based system for cultivating germinating barley seeds for Al tolerance analysis (Tamas et al., 2006 2006 ). In their method, millimolar Al concentrations were used to cause similar Al toxicity symptoms on roots as micromolar Al concentrations in hydroponics due to the high affinity of filter paper to Al monomeric forms. Measurements of shoot and root growth as total dry weight for long-term culture also provide good separation of Al-tolerant and sensitive genotypes. The hematoxylin staining method which was originally described by Polle et al.( 1978 1978 ) with applications to genotypic classification (Takagi et al., 1981 1981 ; Ma et al., 1997 1997 ; Carver et al., 1988 1988 ), genetic characterization (Ruiz-Torres and Carver, 1992 1992 ), and selection (Fisher and Scott, 1987 1987 ; Carver et al., 1993 1993 ) has been widely used in wheat and other species with higher levels of Al tolerance. Polle et al.( 1978 1978 ) recommended a qualitative scale to rate genotypes as completely, partially, or unstained for 3 different concentrations of Al in solution. These rating parameters are applicable when the seminal roots have a consistent stain pattern, but some genotypes show a differential staining pattern (none vs complete) among roots on the same plants, or between plants of a single genotype, making genotypic/individual plant classification confusing and difficult (Ruiz-Torres and Carver, 1992 1992 ; Hossain et al., 2005 2005 ). A modified method was developed by Hossain et al.( 2005 2005 ) as follows: pre-germinated seedlings (2 d at 22 °C) were cultured for 3 d in nutrient solution (Al free) followed by 24 h growing in a solution with 50 or 100 μmol/L Al, and then 48 h regrowth in Al free nutrient solution. A particular feature of this method involves the culture of individual plants in small tubes rather than in bulk tanks, to avoid cross contamination. Following this method, seminal root regrowth length (SRRL) and relative seminal root regrowth length (RSRRL) showed significant differences between tolerant and sensitive cultivars. Screening with soil bioassay 2 The use of soil media has received less attention than solution media because of the complications of creating a soil environment with a specific type and amount of phytotoxicity (Foy, 1976 1976 ). Mitigating effects of other nutrients (e.g., Ca, P, or Mg) or organic matter must be considered as well as other factors like variability at the soil collection site, time of collection, and soil storage condition (Scott and Fisher, 1989 1989 ). Results from soil bioassays may lack consistency when the same soil is used repeatedly due to the effects of continuous wetting and drying on soil chemistry. There has been some attention to the development of rapid soil bioassays in screening for acid soil tolerance. Fundamental to such an assay is that reduction in length of the primary root is the first visual indicator of Al sensitivity and that reduction in primary root length only two days after germination under dark conditions is equally effective in discriminating genotypes as root lengths measured later under light conditions (Aitken et al., 1990 1990 ). Early root growth under dark conditions is primarily supported by the seed reserves without possible confounding effects of nutrient uptake. Screening in soils representative of the targeted production area where soil acidity is a yield limiting factor provides a critical intermediate step in selection of tolerant genotypes after preliminary screening in nutrient solution but before more lengthy and costly screening under natural field conditions (Carver and Ownby, 1995 1995 ). Field screening 2 The most direct screening for acid soil tolerance is the measurement of yield of both grain and total biomass under field conditions. The result is an integrated measurement of tolerance expressed throughout development. The procedure is to conduct tests in unamended and lime added blocks to allow a direct measurement of tolerance and to ensure that acid soil tolerance is not related to low yield potential in the absence of stress. Soil management practices are otherwise equal between blocks. The data from the field experiments are often reported as the ratio of grain yield in the unamended block to that in the lime-amended block to adjust for differences in yield potential without acid soil stress. However, Scott and Fisher ( 1989 1989 ) showed that equally responsive genotypes may have equal absolute tolerances (yield differential between blocks) but appear quite different in their yield ratios. Thus, the ratios should be interpreted with caution, or at least not reported alone. The major obstacle for field screening is the inherent spatial variability for pH or plant nutrients (e.g., P) in soil, which influences Al stress severity. Spatial variability can greatly bias the interpretation of the field screening results (Ball et al., 1993 1993 ) and, in turn, lead to an inefficient selection response if not considered in the experimental design or in the statistical analysis by use of a covariate or nearest-neighbour method. Adjustments must also be made in field data, either statistically or intuitively, for a variable response to other environmental factors, such as disease or insect pressures and water supply. MECHANISMS OF Al TOLERANCE IN PLANTS 1 During the past two decades there have been many hypotheses to explain the mechanisms to cope with Al stress among plants. In general, strategies that various plants use to tolerate Al fall into two categories: (1) external resistance mechanisms, by which Al is excluded from plant tissues, especially the symplastic portion of the root meristem; and (2) 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 (Kochian, 1995 1995 ). The possible external resistance or exclusion mechanisms of Al tolerance are: immobilisation of Al at the cell wall or low cell wall cation exchange capacity, selective permeability of the plasma membrane, formation of a plant induced pH barrier in the rhizosphere or root apoplasm, exudation of chelate ligands, exudation of phosphate, and Al efflux (Kochian, 1995 1995 ; Taylor, 1991 1991 ), Al 3+ -induced changes in the membrane protein, and ATPase activity of the microsomal membrane function (Matsumoto et al., 1992 1992 ; Wagatsuma et al., 1995 1995 ). A metabolism-dependent exclusion of Al from root apical meristem has been described, which involves inhibition of Al accumulation in root tips (Rincon and Gonzales, 1992 1992 ). Foy ( 1996 1996 ) also reported that when barley plants were grown at pH 4.4, the accumulation of Al and phosphorus in shoots of susceptible cultivars were three times and two times higher, respectively, than in that of the tolerant cultivars. Accumulation of such high concentrations of Al and P in the aerial parts of the plants are considered to be toxic to growth and development of the plants. The internal resistance mechanisms are those which operate within the symplasm and are mediated at the cellular level either by detoxification or immobilisation of Al ions that have penetrated into plant cells (Taylor, 1995 1995 ). The possible mechanisms for internal resistance are: chelation of Al in the cytosol, compartmentation in the vacuole, evolution of Al-tolerance enzymes and elevated tolerance of enzyme activity. Exudation of organic acids 2 The mechanism(s) of Al tolerance in plants have not been fully elucidated, but the suggestion that the release of various di- and tricarboxylic acids can form strong complexes with Al has lead to various studies attempting to show that plants use this as a defence mechanism against Al toxicity (Ishikawa et al., 2000 2000 ; Kochian et al., 2005 2005 ). Exudation of organic acids, mainly citric and malic acids appears to be one of the main mechanisms for Al tolerance (Carver and Ownby, 1995 1995 ; Gallardo et al., 1999 1999 ; Ishikawa et al., 2000 2000 ). Ma et al.( 2001 2001 ) proposed two patterns of Al-stimulated efflux of organic acids: (1) the pattern where no discernible delay is observed between the addition of Al and the onset of organic acid efflux (Delhaize et al., 2001 2001 ; Ryan et al., 1995 1995 ; Zheng et al., 1998 1998 ) and (2) the pattern where the efflux of organic acids is delayed for several hours (Li et al., 2000 2000 ; Ma et al., 2001 2001 ; Yang et al., 2006 2006 ). At sufficient concentrations, these organic acids can form complexes with Al ions, prevent the Al ions from binding to the fixed negative sites of the cell wall and plasma membrane, and confer Al tolerance to plants to maintain the normal functions of the cell wall and plasma membrane (Ishikawa et al., 2000 2000 ). Wagatsuma and Yamasaku ( 1985 1985 ) reported that Al tolerant barley cultivars exclude Al actively outside the plasmalemma of root cells, and excluded Al may be polymerised and/or react with phosphorus to form Al precipitates, resulting in low Al content in the root cell protoplast. Zhu et al.( 2003 2003 ) reported an Al-exclusion mechanism in Al-tolerant mutant cell lines of barley by exudation of malate and citrate. A negative correlation between accumulation of Al in cells and release of citrate and malate in the medium was observed (Zhu et al., 2003 2003 ), however, the authors did not find any positive correlation between synthesis of citrate and malate in the cells and the amount of these organic acids released in the medium. Citrate secretion from the root apices of barley plays an important role in excluding Al and thereby detoxifying Al based on a positive correlation between citrate secretion and Al resistance in 21 barley varieties (Zhao et al., 2003 2003 ). Miyasaka et al.( 1991 1991 ) observed that Al-tolerant snapbean cultivars when grown under sterile conditions for relatively long periods (8 d) exuded citric acid to a level that reached 26% of initial Al (mol/mol). This response was not seen in an Al-sensitive cultivar and the authors concluded that exudation of citric acid into the medium provides Al tolerance, either by chelating external Al and thus preventing its entry into the roots or by mobilizing phosphate that had been precipitated with Al in the root apoplast (Millard et al., 1990 1990 ). It has been reported that the accumulation of Al phosphate on the root surface of the tolerant barley cultivar Dayton was about two times higher than that on the susceptible cultivar Kearney as revealed by X-ray photoelectron spectroscopy, and that the tolerant cultivars create a barrier to the transport of Al to the interior of the roots. Binding Al in the cell wall 2 The interaction of Al with cell wall constituents remains a relatively unexplored aspect of Al phytotoxicity. Binding of Al to charge sites on the cell wall surface is a prerequisite for uptake and toxicity. Plants with a higher root cation exchange capacity are generally more sensitive to Al than similar lines with lower cation exchange capacity (Blamey et al., 1990 1990 ). In terms of a specific interaction with Al, Blamey et al.( 1993 1993 ) have provided evidence that Al displaces Ca 2+ from pectic acid in the cell wall, which reduces the movement of water and mineral nutrients through the cell wall interstices. In the presence of Al, an increase in Ca 2+ concentration in the root environment reduced the porosity of the root cell wall, which is regulated by the arrangement of Ca 2+ pectate, thereby regulating the movement of solutes and limiting the uptake of Al in the root cell (Blamey and Dowling, 1995 1995 ; Carpita and Gibeaut, 1993 1993 ). However, Kinraide et al.( 1992 1992 ) have concluded that negative charges on the cell wall pectins as well as the charge sites on membrane lipids and proteins, do not play a significant role in differential Al tolerance. An association between Al toxicity and accumulation of Al phosphate precipitates in the apoplasm was reported (Clarkson, 1967 1967 ). It is still unclear, however, whether Al-tolerant plants actively release phosphate to immobilize Al in the apoplast. Evidence for active efflux of cell phosphate in Al-tolerant sugar beet was reported (Lindberg, 1990 1990 ). However, it should be noted that cellular phosphate often leaks into the cell wall region as part of the Al stress effect (Ownby, 1993 1993 ). Various studies have suggested that tolerance of low phosphate, and high efficiency in uptake and distribution of phosphate, may be characteristics of Al-tolerant cultivars (Foy et al., 1978 1978 ). There is evidence that Al-tolerant wheat cultivars are able to absorb and translocate phosphate to shoots in the presence of Al. Production of root-cap mucilage 2 The mucilage exudates from root tips, predominantly comprising pectin and D-polygalacturonic acid were found to protect roots from toxic Al, and removal of root cap mucilage caused an increase in Al uptake and phytotoxicity (Horst et al., 1982 1982 ). Henderson and Ownby ( 1991 1991 ) noted a strong correlation between root mucilage volume and Al tolerance in winter wheat cultivars. The mechanism of protection by mucilage is not clear yet. It has been assumed that a mucilage droplet would create a boundary layer in which diffusion of Al to the root surface is slowed and where the organic acid/Al ratio would likely be much more favourable than in the rhizosphere as a whole (Henderson and Ownby, 1991 1991 ). Exclusion of Al in the plasmalemma 2 There is circumstantial evidence that the constituents of the cell wall and plasma membrane are directly involved in an exclusion mechanism, however, details are yet to be explored. The plasmalemma has an essential role in cell metabolism and growth, and is the primary target site of selective Al toxicity. The effect of Al on membrane integrity and function includes binding of Al to membrane lipids (Haug and Shi, 1991 1991 ), as well as inhibition of ATPase activity (Matsumoto and Yamaya, 1986 1986 ), NADH-linked electron transfer (Loper et al., 1993 1993 ) and ion channel functions (Rengel and Elliott, 1992 1992 ). Al toxicity was associated with an increase in the ratio of phosphatidylcholine to phosphatidylethanolamine, which could increase membrane permeability (Lindberg and Griffiths, 1993 1993 ). Caldwell ( 1989 1989 ) observed that a root membrane isolated from an Al-sensitive cultivar appeared to bind more Al than did a tolerant cultivar and inferred that Al could displace Ca 2+ from membrane protein-binding sites. GENETICS OF Al TOLERANCE 1 Genotypic difference in Al tolerance 2 Tolerance to Al toxicity or acidic soils differs greatly among cereal species, and barley is usually considered the most susceptible member of the Poaceae (Garvin and Carver, 2003 2003 ). The Al tolerance order as reported is maize > rye > triticale > wheat > barley (Polle and Konzak, 1985 1985 ), rye > oats > millet > bread wheat > barley > durum wheat (Bona et al., 1993 1993 ), and rice > maize > pea > barley (Ishikawa et al., 2000 2000 ). Al tolerance has been evaluated by different methods around the world (Foy et al., 1965 1965 ; Maxim and Duta, 1996 1996 ; Ma et al., 1997 1997 ; Minella and Sorrells, 1992 1992 ; Foy, 1996 1996 ; Xu et al., 1991 1991 ; Read and Scott, 1983 1983 ; Read and Oram, 1995 1995 ; Hossain et al., 2005 2005 ). Some barley varieties with high Al tolerance were identified, although most of them were sensitive (Foy et al., 1965 1965 ; Minella and Sorrells, 1992 1992 ; Maxim and Duta, 1996 1996 ). In general, 6-row cultivars were more tolerant than 2-row and 4-row types, husked more tolerant than naked, and winter cultivars more tolerant than spring ones (Xu et al., 1991 1991 ). All eight tolerant barley cultivars ranked by Minella and Sorrells ( 1992 1992 ) were six-row cultivars. Two row barleys having Al tolerance have also been reported (Raman et al., 2002 2002 ). A wide range of genetic variation for Al tolerance exists in barley (Reid et al., 1969 1969 ) and has been exploited to develop varieties with increased Al tolerance (Foy et al., 1965 1965 ). In Australia, some breeding lines outperformed significantly better on acid soils than Al sensitive lines (Oram, 1983 1983 ) and have been released for commercial cultivation on acid soils, for example Brindabella, Yambla, and Tulla. Inheritance of Al tolerance in barley 2 Al tolerance in barley has been assessed by root staining using hematoxylin (Minella and Sorrells, 1992 1992 ; Tang et al., 2000 2000 ) and eriochrome cyanine (Ma et al., 1997 1997 ; Wang et al., 2006 2006 ). These qualitative variations have been assessed as stained, unstained and partially stained to represent Al-sensitive, tolerant and intermediate genotypes respectively. Al tolerance on the basis of relative root regrowth in barley has also been assessed as a quantitative trait (Raman et al., 2005a 2005a ). In some cases continuous quantitative phenotypic variations could be grouped into discrete classes. Raman et al.( 2002 2002 ) classified tolerant, sensitive and intermediate genotypes in an F 2 segregating population for Al tolerance, evaluated on the basis of root growth rate. Similarly, Ma et al.( 2004 2004 ) classified Al tolerant and Al sensitive genotypes by root/shoot ratio, with ratios > 0.24 being classified as tolerant, and < 0.24 being classified as sensitive. Previous work carried out by Tang et al.( 2000 2000 ) and Raman et al.( 2002 2002 ) highlighted the need to use F 3 populations for Al tolerance evaluations. Both the studies reported phenotypic misclassifications at F 2 stage, thus it was recommended to perform F 3 family testing to confirm the genetic constitution of an individual F 2 . Research to date has shown that the Al tolerance in barley is under a single locus control. The earliest work was with the barley cultivar Dayton, which was reported to have Al tolerance conferred by a single dominant gene, designated as Alp (Reid, 1970 1970 ). Stфlen and Anderson ( 1978 1978 ) reported a dominant allele Pht at one locus which controls high tolerance to acidic soil conditions. The single locus model was confirmed by Minella and Sorrells ( 1992 1992 ), based on extensive crosses. The results further indicated that the expression of the tolerance (dominant or recessive) was dependent on the Al concentration. Al tolerance segregation in F 2 populations from crosses between Dayton (Al tolerant)/Harlan Hybrid (Al sensitive), Harrington (Al sensitive)/Brindabella (Al tolerant), Yambla (moderate Al tolerant)/WB229 (Al tolerant), and F6ant28B48-16 (Al sensitive)/Honen were in a monogenic fashion (Raman et al., 2001 2001 ; 2002 2002 ; Tang et al., 2000 2000 ; Wang et al., 2006 2006 ). Oram ( 1983 1983 ), however, obtained Al tolerant genotypes in an F 4 population of a cross between two of the most susceptible cultivars (CI7115/Weeah) of barley and suggested that transgressive segregation might be due to more than one locus which determines Al tolerance. Minella and Sorrells ( 1992 1992 ) did not find any transgressive segregation in segregating populations derived from crosses between tolerant/susceptible and moderately tolerant/tolerant using 37 barley genotypes of diverse genetic and geographical origin. Duke ( 1982 1982 ) suggested additive genetic effects in a composite cross of winter barley varieties from all over the world grown on Al-toxic soils resulted in considerable increase in tolerance within one generation. Location of the gene conferring Al tolerance 2 The locus Pht conferring tolerance to low soil pH was located on chromosome 4H (Stфlen and Anderson, 1978 1978 ). The locus Alp conferring Al tolerance of Dayton was located on the long arm of chromosome 4H by crossing Dayton with trisomic Shin Ebisu 16 (Minella and Sorrells, 1997 1997 ). This result was later on confirmed by restriction fragment length polymorphism (RFLP) mapping analysis (Tang et al., 2000 2000 ) and simple sequence repeat (SSR) marker linkage analysis (Raman et al., 2003 2003 ). The same chromosomal location (4H) of other proposed Al tolerance loci was confirmed including Alt from WB229 by amplified fragment length polymorphism (AFLP), SSR and analysis of wheat-barley chromosome addition lines (Raman et al., 2002 2002 ) and Alp3 from Brindabella (Raman et al., 2001 2001 ). However, it is not known whether Alp , Pht , Alt , and Alp3 are allelic. Recently, Raman et al.( 2005a 2005a ) identified several quantitative trait loci (QTLs) for root elongation under Al stress on 3H, 4H, 5H and 6H in an F 2 population from Ohichi/F6ant28B48-16. These additional indicative QTLs require further validation in different genetic backgrounds. Identification of molecular markers linked with the Al tolerance gene(s) 2 Molecular markers are highly regarded as an efficient selection tool to indirectly select traits linked to Al tolerance loci (Raman et al., 2002 2002 ). In recent years, a significant effort has been made in developing molecular markers for agronomic traits for efficient marker-assisted selection (MAS) in breeding programs. Table 2 2 shows the results from studies of molecular markers linked with the Al tolerance gene(s) in barley, and closely related cereals such as wheat and rye. 2 Species 2 Crosses 2 Ranking Al tolerance 2 Gene/QTLs 2 Designation and chromosome location 2 Contribution 2 Mapping population 2 Marker species 2 Flanking markers 2 Distance (cM) 2 Reference Al stress Criteria Hordeum vulgare Yambla/WB229 100 μmol/L 4 d+50μmol/L 5 d Root regrowth Gene Alt (4H) Single major Wheat-barley chromosome addition lines 67 F 2 AFLP and SSR Bmag353,HVM68/HVM3 1.6/1.6 Raman et al.( 2002 2002 ) Hordeum vulgare Dayton/Harlan 50 μmol/L 24 h Hematoxylin stain Gene Alp (4HL) Single 48 F 2 RFLP Xbcd1117/Xwg464, Xcdo1395 2.1/2.1 Tang et al.( 2000 2000 ) Hordeum vulgare Dayton/Harlan 50 μmol/L 24 h Hematoxylin stain Gene Alp (4HL) Single 48 F 2 SSR HVM68/Bmag353 5.3/3.1 Raman et al.( 2003 2003 ) Triticum aestivum BH 1146/Anahuac 1.7 mmol/L 17 h+0 mmol/L 24 h Root regrowth Gene Alt BH (4DL) 85% 101 F 5 RILs RFLP Xbcd1230/Xcdo1395 1.1/11.3 Riede and Anderson ( 1996 1996 ) Triticum aestivum BH 1146/Anahuac 37 μmol/L 72 h Root tolerance index Gene Alt BH (4DL) Single dominant 91 F 5 RILs RFLP SSR AFLP Xgdm125/Xpsr914 4.8/1.1 Milla and Gustafson ( 2001 2001 ) Secale cereale Ailes/Riodeva 150 μmol/L 24 h Root regrowth Gene Alt1 (6RS) Dominant F 2 RAPD & SCARs ScR01600/ScB15790 2.1/5.5 Gallego et al.( 1998a 1998a ) Secale cereale M39A-1-6/M77A1 2×10 −6 72 h Root tolerance index Gene Alt3 (4RL) Single F 6 RILs AFLP AMAL5/AMAL5 0.4/0.7 Miftahudin et al.( 2002 2002 ) 5 Oryza sativa 5 IR64/ Oryza rufipogon 5 1.48 mmol/L 14 d 5 Relative root length 5 QTLs QAlRr1.1 (1) 9.0% 5 171 F 6 RILs 5 RFLP SSR Nguyen et al.( 2003 2003 ) QAlRr3.1 (3) 24.9% QAlRr7.1 (7) 22.5% QAlRr8.1 (8) 20.8% QAlRr9.1 (9) 9.9% 10 Oryza sativa 10 CT9993/IR62266 10 30×10 −6 10 d 10 Relative root length 10 QTLs qALRR-1 -1 24.1% 10 146 DH lines 10 RFLP AFLP SSR Nguyen et al.( 2002 2002 ) qALRR-1 -2 18.5% qALRR -2 13.4% qALRR -3 12.8% qALRR -4 20.1% qALRR -7 10.3% qALRR -8 28.7% qALRR -9 19.3% qALRR -10 17.7% qALRR -12 19.7% 8 Oryza sativa 8 IR1552/Azucena 8 1 mmol/L 2 and 4 weeks 8 Relative root length 8 QTLs QTLs 2 weeks 8 150 F 9 RILs 8 AFLP RFLP Wu et al.( 2000 2000 ) (1) 19% (3) 9% (12) 10% QTLs 4 weeks (1) 15% (9) 9% (12) 20% 3 Oryza sativa 3 Koshihikari/Kasalath 3 50 μmol/L 24 h 3 Relative root elongation 3 QTLs QTL (1) 11.1% 3 183 backcross inbred lines 3 RFLP 3 C86 R2460 G200 Ma et al.( 2002 2002 ) QTL (2) 7.3% QTL (6) 8.7% 2 Zea mays 2 Cat-100-6/S1587 2 31×10 −6 7 d 2 Net root length 2 Genes Alm1 (10S) 24.2 ( F -test value) 2 56 Inbred lines 2 RFLP 2 CSU70 UMC130 Sibov et al.( 1999 1999 ) Alm2 (6S) 7.67 ( F -test value) 5 Zea mays 5 L53/L1327 5 222 μmol/L 7 d 5 Net root length 5 QTLs QTL1 (2) 10.9% 5 168 F 3:4 5 RFLP SSR Ninamango-Cárdenas et al.( 2003 2003 ) QTL2 (6) 5.3% QTL3 (6) 15.6% QTL4 (8) 7.4% QTL5 (8) 8.6% Different molecular marker systems such as RFLP, AFLP, SSR, sequence tagged site (STS), and diversity array platform have been used to identify Al tolerance alleles in barley (Fig. 2 2 ). Tang et al.( 2000 2000 ) reported three RFLP markers flanking the Al tolerance gene Alp , which was 2.1 cM proximal to the marker BCD1117 and 2.1 cM distal to the markers WG464 and CDO1395. RFLP-based marker-assisted selection (MAS) of the Alp is both time-consuming and labour intensive and generally involves radioactive isotopes and hence is not suitable for high throughput analysis in breeding programs (Raman et al., 2003 2003 ). Therefore, SSR markers (e.g. Bmag353, Bmac186 and Bmac310) were identified that showed tight linkage with the Alp locus (Raman et al., 2003 2003 ). A: Dayton/Harlan hybrid (Tang et al., 2000 2000 ; Raman et al., 2003 2003 ); B: Murasakimochi/Morex (Ma et al., 2004 2004 ); C: F6ant28B48-16/Honen (Wang et al., 2006 2006 ); D: Yambla/WB229 (Raman et al., 2002 2002 ) In an independent study, markers Bmac310, Bmag353, HVM68 and HVRCABG were found to be tightly linked to a major Al tolerance locus Alt in a F 2 population from Yambla (moderately tolerant of Al)/WB229 (tolerant of Al) (Raman et al., 2002 2002 ). The Alt gene was 1.6 cM proximal to marker Bmag353 and HVM68 and 1.6 cM distal to HVM3. Two SSR markers (Bmac310 and HVRCABG) and six AFLP markers co-segregated with Alt (Raman et al., 2002 2002 ). These SSR markers were used to distinguish other source for Al tolerance in different populations derived from Harrington (Al sensitive)/Brindabella (Raman et al., 2001 2001 ), Ohichi/F6ant28B48-16 (Raman et al., 2005a 2005a ) and F6ant28B48-16/Honen (Wang et al., 2006 2006 ). These markers have enabled fast tracking Al tolerance alleles in different breeding programs in Australia. Molecular mapping especially with the SSR markers has allowed validating the ‘hypothesised’ mechanism for Al tolerance in barley (Zhao et al., 2003 2003 ). For example, Ma et al.( 2004 2004 ) reported that tightly linked marker Bmag353 explained 51.3% of phenotypic variance for citrate excretion in an intercross population from Murasakimochi/Morex. Most of the mapping studies employed smaller population comprising 48~100 individuals. It is clear that improved mapping resolution is needed. Firstly, the Al tolerant cultivar Dayton possesses blue aleurone colour which is not desirable for malting barley varieties. The marker Bmag353, which is linked with Al tolerance, could also explain about 54% of phenotypic variation for blue aleurone colour (Li et al., 2003 2003 ; Read et al., 2003 2003 ), indicating the possible tight linkage between these loci. Secondly, barley has a large genome of about 4800 Mb (Arumuganathan and Earle, 1991 1991 ) and the genetic map covers about 1800 cM (Becker and Heun, 1995 1995 ), so the mapping interval of 1 cM should correspond to a DNA segment of several megabases. Higher resolution mapping is not only very important to reduce genetic drag during the marker-assisted introgression process but also useful in positional cloning of the Al tolerance gene and may lead to genetic engineering of crops. This strategy has been used to isolate the Mlo gene for powdery mildew resistance in barley (Büschges et al., 1997 1997 ; Simons et al., 1997 1997 ). Comparison of genetics of Al tolerance in cereals 2 The major gene conferring Al tolerance in barley, wheat and rye seems to be due to orthologous loci on the long arm of the group 4 chromosome. Al tolerance in-wheat cultivars has been found to be under the control of a single dominant gene (Delhaize et al., 1993 1993 ; Riede and Anderson, 1996 1996 ; Luo and Dvorak, 1996 1996 ). However, there was also evidence to suggest that more than one Al tolerance gene might exist in certain wheat cultivars (Aniol and Gustafson, 1984 1984 ; Camargo, 1981 1981 ; Aniol, 1997 1997 ). Riede and Anderson ( 1996 1996 ) used RFLP markers to map the gene Alt BH conferring Al tolerance in Brazilian wheat cv BH1146 on the long arm of chromosome 4D (4DL). RFLP markers BCD1230 and CDO1395 were 1.1 and 11.3 cM from the Alt BH locus respectively. Milla and Gustafson ( 2001 2001 ) used AFLP and SSR markers and mapped this locus to a 5.9 cM interval between markers GDM125 and PSR914, while marker BCD1230 co-segregated with Alt BH . However, CDO1395 and BCD1230 were 2.1 cM and 33.5 cM respectively from the Al tolerance locus Alp in barley (Tang et al., 2000 2000 ). The different relative position of the same markers and Al tolerance locus suggested that this chromosome segment has been subject to structural changes in these two species (Tang et al., 2000 2000 ). In rye, Al tolerance was reported to be controlled by a single gene on chromosome 4R (Miftahudin et al., 2002 2002 ), 7R (Matos et al., 2005 2005 ), three major genes on 3RL, 4RL, and 6RS (Aniol and Gustafson, 1984 1984 ; Gallego et al., 1998b 1998b ), and the major locus on 3RS (Aniol, 2004 2004 ). Gallego et al.( 1998a 1998a ) mapped a gene conferring Al tolerance, designated as Alt1 , on the short arm of chromosome 6R by RAPD (random amplified polymorphic DNA) and SCAR (sequence characterized amplified regions) markers. Miftahudin et al.( 2002 2002 ) mapped Alt3 on 4RL with AFLP and RFLP markers using an F 6 rye recombinant inbred line (RIL) population. They found that the RFLP marker BCD1230 co-segregated with Alt3 . This marker had previously showed co-segregation with Alt BH locus in wheat (Milla and Gustafson, 2001 2001 ) or was tightly linked with this gene (1.1 cM) (Riede and Anderson, 1996 1996 ) in wheat. Molecular mapping of genes conferring Al tolerance in rice suggested that Al tolerance was a complex multigenic trait. The major QTLs were detected by different molecular markers on chromosomes 1 and 12 (Wu et al., 2000 2000 ), on chromosomes 1, 2 and 6 (Ma et al., 2002 2002 ), or on chromosomes 1 and 8 (Nguyen et al., 2002 2002 ). The common chromosome 1 did not seem to correspond to most of the genes that had been mapped for Al tolerance in other species (Nguyen et al., 2001 2001 ) because homeologous chromosome 4 of the Triticeae generally corresponds to chromosome 3 in rice. However, in later work a major QTL explaining 24.9% of the phenotype variation was found on chromosome 3 of rice, which is conserved across cereal species (Nguyen et al., 2003 2003 ). In sorghum, a major Al tolerance locus has been mapped on chromosome 3, which is not a syntenic region of group 4 chromosomes of wheat, barley and rye. Instead, it maps to a homeologous region of Triticeae chromosome 3, rice chromosome 1 and maize chromosomes 3 and 8. QTLs associated with Al tolerance in maize and rice have also been mapped on these chromosomes (Ninamango-Cárdenas et al., 2003 2003 ). These studies indicate evolutional inheritance of Al tolerance genes in different cereals. Genes or proteins regulated by Al stress 2 Studies on genes regulated by Al stress have indicated the complexity of Al toxicity. In rye, Al-regulated genes were found belonging to 13 major functional categories involved in cell elongation and division, oxidative stress, iron metabolism and other cellular mechanisms. The transcripts of two different genes coding for tonoplast intrinsic proteins (TIPs) decreased under Al stress, which would suggest generation of a lower turgor pressure in the cell elongation zone resulting in reduced root growth (Milla et al., 2002 2002 ). Watt ( 2003 2003 ) indicated that 14 of the 50 cDNAs up-regulated by Al stress in sugarcane were involved in signalling events and the regulation of gene expression. Mao et al.( 2003 2003 ) identified several Al-regulated genes related to the metabolism of cell wall components in rice. The expression of Al-induced genes in a transgenic Arabidopsis plant could ameliorate Al stress and/or oxidative stress (Ezaki et al., 2000 2000 ). The four transgenic lines ( AtBCB - Arabidopsis blue copper-binding protein, parB -tobacco GST, NtPox -tobacco peroxidase, NtGDI1 -tobacco GDP dissociation inhibitor) ameliorate Al toxicity through different mechanisms. AtBCB may suppress Al absorption, NtGDI1 promotes a release of Al in the root tip region, whereas parB and NtPox enhance the enzyme activities which diminish oxidative damage caused by Al. More resistant transgenic plants could be produced by combination of these four genes (Ezaki et al., 2001 2001 ). Cruz-Ortega et al.( 1997 1997 ) suggested that synthesis of 1,3-β-glucanase during Al stress in wheat could be as a protective response against pathogen attack. TaMDR1 encoding multidrug resistance-like protein was induced in both Al sensitive and Al-tolerant wheat cultivars but the concentration for the induction was lower in the Al sensitive cultivar than in the Al-tolerant one (Sasaki et al., 2002 2002 ). A clone OsAR28 coding for an unknown protein could be a candidate gene for Al tolerance in rice (Mao et al., 2003 2003 ). Isolation and cloning of genes for Al tolerance 2 More than 50 genes with expression induced by Al stress have been isolated from a range of plant species. However, most of these genes are general stress-inducible genes, whose expressions are turned on by oxidative stress (Ezaki et al., 1996 1996 ; Richards et al., 1998 1998 ; Watt, 2003 2003 ), pathogen infection (Hamel et al., 1998 1998 ; Cruz-Ortega et al., 1997 1997 ; Watt, 2003 2003 ), other metal ions (Snowden et al., 1995 1995 ), and water-stress and cold stress (Watt, 2003 2003 ). They are correlated with Al toxicity rather than tolerance to Al stress. Most recently, an ALMT1 gene, which encoded for an Al-activated malate transporter was isolated and characterised (Sasaki et al., 2004 2004 ; Raman et al., 2005b 2005b ). This gene co-segregated with Al tolerance in wheat and increased the tolerance of tobacco cells (Sasaki et al., 2004 2004 ). This discovery gave an explanation of a physiological mechanism of Al exclusion in wheat. The gene was induced in rice and was expressed in the transgenic lines. However, the Al tolerance of these transgenic plants was not increased (Sasaki et al., 2004 2004 ). Transgenic barley with expression of the ALMT1 gene displayed a capacity for Al-activated malate efflux which was not observed in control plants. Plants expressing ALMT1 were also more tolerant to Al stress based on root growth in both hydroponic culture and acid soil experiments. This indicated that a higher level of Al tolerance can be achieved by promoting malate efflux in barley (Delhaize et al., 2004 2004 ; Ryan et al., 2004 2004 ). A homolog of the wheat ALMT1 named AtALMT1 in Arabidopsis was the best candidate from the 14 member AtALMT family to be involved with Al tolerance (Hoekenga et al., 2006 2006 ). Genetic analysis of Al tolerance in highly diverse barley genotypes (Minella and Sorrells, 1992 1992 ; Tang et al., 2000 2000 ; Raman et al., 2001 2001 ; 2002 2002 ; 2003 2003 ; 2005a 2005a ; Ma et al., 2004 2004 ; Wang et al., 2006 2006 ) indicates that the genetic base for Al tolerance is very narrow. The genetic variation in Al tolerance may be due to mutations in the Al tolerance gene in barley, that may lead to variation in Al tolerance levels (e.g. highly/moderately tolerant). Minella and Sorrells ( 1992 1992 ) reported that there is a little chance for barley improvement for Al tolerance. More research is required to screen barley germplasm, in order to identify better sources for Al tolerance. Alternatively, genetic manipulation can be used to improve the Al tolerance levels in barley. So far, there is no gene conditioning Al tolerance which has been isolated and characterised in barley. Since Al could have diverse effects and act differently in different species (Delhaize and Ryan, 1995 1995 ), the Al-induced gene expression change of barley deserves further study. Furthermore, the mechanisms of Al tolerance include Al exclusion and tissue tolerance (Taylor, 1988 1988 ; Kochian, 1995 1995 ). It is still unknown whether any gene relates to a tissue tolerance mechanism, or if it exists. References RL Aitken , PW Moody , BL Compton . A simple bioassay for the diagnosis of aluminium toxicity in soils . Commun Soil Sci Plant Anal , 1990 . 21 511 - 529 . . A simple bioassay for the diagnosis of aluminium toxicity in soils SM Alam . Influence of aluminium on plant growth and mineral nutrition of barley . Commun Soil Sci Plant Anal , 1981 . 12 121 - 138 . . Influence of aluminium on plant growth and mineral nutrition of barley SM Alam , WA Adams . Effects of aluminium upon the growth and nutrition composition of oats . Pak J Sci Res , 1980 . 23 130 - 135 . . Effects of aluminium upon the growth and nutrition composition of oats A Aniol . Physiological aspects of aluminium tolerance associated with the long arm of chromosome 2D of the wheat ( Triticum aestivum L.) genome . Theor Appl Genet , 1995 . 91 510 - 516 . . Physiological aspects of aluminium tolerance associated with the long arm of chromosome 2D of the wheat (Triticum aestivum L.) genome A Aniol . V Ruzgas , E Lemezis , M Apanaviciene , 等 . The Aluminium Tolerance in Wheat . Proceedings of the International Conference: Plant Breeding: Theories, Achievements and Problems , 1997 . 4 - 22 . Kedainiai, Lithuania . The Aluminium Tolerance in Wheat A Aniol . Chromosomal location of aluminium tolerance genes in rye . Plant Breeding , 2004 . 123 ( 2 ): 132 - 136 . DOI: 10.1046/j.1439-0523.2003.00958.x http://doi.org/10.1046/j.1439-0523.2003.00958.x . Chromosomal location of aluminium tolerance genes in rye A Aniol , JP Gustafson . Chromosome location of genes controlling aluminium tolerance in wheat, rye and triticate . Can J Genet Cytol , 1984 . 26 701 - 705 . . Chromosome location of genes controlling aluminium tolerance in wheat, rye and triticate K Arumuganathan , ED Earle . Nuclear DNA content of some important plant species . Plant Mol Bio Rep , 1991 . 9 208 - 219 . . Nuclear DNA content of some important plant species BW Bache , J Ross . Effect of phosphorus and aluminum in the response of spring barley to soil acidity . J Agric Sci , 1991 . 117 299 - 305 . . Effect of phosphorus and aluminum in the response of spring barley to soil acidity S Ball , T Mulla , CF Konzak . Spatial heterogeneity affects variety trial interpretation . Crop Sci , 1993 . 33 931 - 935 . . Spatial heterogeneity affects variety trial interpretation J Becker , M Heun . Barley microsatellite: allele variation and mapping . Plant Mol Biol , 1995 . 27 ( 4 ): 835 - 845 . DOI: 10.1007/BF00020238 http://doi.org/10.1007/BF00020238 . Barley microsatellite: allele variation and mapping RJ Bennet , CM Breen , MV Fey . The primary site of aluminium injury in the root of Zea mays L. . South African J Plant Soil , 1985 . 2 8 - 17 . . The primary site of aluminium injury in the root of Zea mays L. W Bergmann . Nutritional Disorders of Plants: Development, Visual and Analytical Diagnosis , 1992 . : Jena, Germany Gustav Fisher Verlag , . Nutritional Disorders of Plants: Development, Visual and Analytical Diagnosis FCP Blamey , AJ Dowling . Antagonism between aluminium and calcium for sorption by calcium pectate . Plant Soil , 1995 . 171 ( 1 ): 137 - 140 . DOI: 10.1007/BF00009576 http://doi.org/10.1007/BF00009576 . Antagonism between aluminium and calcium for sorption by calcium pectate FCP Blamey , DC Edmeades , DM Wheeler . Role of root cation-exchange capacity in differential aluminium tolerance of lotus species . J Plant Nutr , 1990 . 13 729 - 744 . . Role of root cation-exchange capacity in differential aluminium tolerance of lotus species FCP Blamey , CJ Asher , DG Edwards , GL Kerven . In vitro evidence of aluminium effects on solution movement through root cell walls . J Plant Nutr , 1993 . 16 555 - 562 . . In vitro evidence of aluminium effects on solution movement through root cell walls L Bona , RJ Wright , VC Baligar , J Matuz . Screening wheat and other small grains for acid soil tolerance . Landscape and Urban Planning , 1993 . 27 ( 2-4 ): 175 - 178 . DOI: 10.1016/0169-2046(93)90046-G http://doi.org/10.1016/0169-2046(93)90046-G . Screening wheat and other small grains for acid soil tolerance L Bona , RJ Wright , BF Carver . A proposed scale for quantifying aluminium tolerance levels in wheat and barley detected by hematoxylin staining . Cereal Res Commun , 1998 . 26 ( 1 ): 97 - 99 . . A proposed scale for quantifying aluminium tolerance levels in wheat and barley detected by hematoxylin staining BF Borie , JB Stange , LA Morales , BM Pino . Effect of aluminium and acidity on root growth in barley ( Hordeum vulgare L.) and oats ( Avena sativa L.) . Agricultura Tecnica (Santiago) , 1994 . 54 224 - 230 . . Effect of aluminium and acidity on root growth in barley (Hordeum vulgare L.) and oats (Avena sativa L.) DJ Brady , DG Edwards , CJ Asher , FCP Blamey . Calcium amelioration of aluminium toxicity effects on root hair development in soybean ( Glycin max L.) Merr . New Phytol , 1993 . 123 ( 3 ): 531 - 538 . DOI: 10.1111/j.1469-8137.1993.tb03765.x http://doi.org/10.1111/j.1469-8137.1993.tb03765.x . Calcium amelioration of aluminium toxicity effects on root hair development in soybean (Glycin max L.) Merr R Büschges , K Hokkricher , R Panstruga , G Simmons , M Wolter , A Frijters , R van Dealen , T van der Lee , P Diergaarde , J Groenendijk , 等 . The barley Mlo gene: a novel control element of plant pathogen resistance . Cell , 1997 . 88 ( 5 ): 695 - 705 . DOI: 10.1016/S0092-8674(00)81912-1 http://doi.org/10.1016/S0092-8674(00)81912-1 . The barley Mlo gene: a novel control element of plant pathogen resistance C Caldwell . Analysis of aluminium and divalent cation binding to wheat root plasma membrane proteins using terbium phosphorescence . Plant Physiol , 1989 . 91 233 - 241 . . Analysis of aluminium and divalent cation binding to wheat root plasma membrane proteins using terbium phosphorescence CEO Camargo . Wheat improvement. I. The heritability of tolerance to aluminium toxicity . Bragantia , 1981 . 40 33 - 45 . . Wheat improvement. I. The heritability of tolerance to aluminium toxicity NC Carpita , DM Gibeaut . Structural models of primary cell walls in flowering plants: consistency of molecular structure with physical properties of the walls during growth . Plant J , 1993 . 3 ( 1 ): 1 - 30 . DOI: 10.1046/j.1365-313X.1993.00999.x http://doi.org/10.1046/j.1365-313X.1993.00999.x . Structural models of primary cell walls in flowering plants: consistency of molecular structure with physical properties of the walls during growth BF Carver , JD Ownby . Acid soil tolerance in wheat . Adv Agron , 1995 . 54 117 - 173 . . Acid soil tolerance in wheat BF Carver , WP Inskeep , NP Wilson , RL Westerman . Seedling tolerance to aluminium toxicity in hard red winter wheat germplasm . Crop Sci , 1988 . 28 463 - 467 . . Seedling tolerance to aluminium toxicity in hard red winter wheat germplasm BF Carver , WE Whitmore , EL Smith , L Bona . Registration of four aluminium-tolerant winter wheat germplasms two susceptible near-isolines . Crop Sci , 1993 . 33 1113 - 1114 . . Registration of four aluminium-tolerant winter wheat germplasms two susceptible near-isolines RB Clark , HA Pier , D Knudsen , JW Maranville . Effect of trace element deficiencies and excesses on mineral nutrients in sorghum . J Plant Nutr , 1981 . 3 357 - 374 . . Effect of trace element deficiencies and excesses on mineral nutrients in sorghum DT Clarkson . Effect of aluminium on the uptake and metabolism of phosphorus of barley seedlings . Plant Physiol , 1966 . 41 165 - 172 . . Effect of aluminium on the uptake and metabolism of phosphorus of barley seedlings DT Clarkson . Interaction between aluminium and phosphorus on root surface and cell wall materials . Plant Soil , 1967 . 27 ( 3 ): 347 - 356 . DOI: 10.1007/BF01376328 http://doi.org/10.1007/BF01376328 . Interaction between aluminium and phosphorus on root surface and cell wall materials KM Cocker , DE Evans , MJ Hodson . The amelioration of aluminium toxicity by silicon in wheat ( Triticum aestivum L.): malate exudation as evidence for an in planta mechanism . Planta , 1998 . 204 ( 3 ): 318 - 323 . DOI: 10.1007/s004250050262 http://doi.org/10.1007/s004250050262 . The amelioration of aluminium toxicity by silicon in wheat (Triticum aestivum L.): malate exudation as evidence for an in planta mechanism R Cruz-Ortega , JC Cushman , JD Ownby . cDNA clones encoding 1,3-β-glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots . Plant Physiol , 1997 . 114 ( 4 ): 1453 - 1460 . DOI: 10.1104/pp.114.4.1453 http://doi.org/10.1104/pp.114.4.1453 . cDNA clones encoding 1,3-β-glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots JM de la Fuente , V Ramírez-Rodríguez , JL Cabrera-Ponce , L Herrera-Estrella . Aluminum tolerance in transgenic plants by alteration of citrate synthesis . Science , 1997 . 276 ( 5318 ): 1566 - 1568 . DOI: 10.1126/science.276.5318.1566 http://doi.org/10.1126/science.276.5318.1566 . Aluminum tolerance in transgenic plants by alteration of citrate synthesis ML de Lima , L Copeland . Changes in the ultrastructure of the root tip of wheat following exposure to aluminium . Aust J Plant Physiol , 1994 . 21 85 - 94 . . Changes in the ultrastructure of the root tip of wheat following exposure to aluminium E Delhaize , PR Ryan . Aluminium toxicity and tolerance in plants . Plant Physiol , 1995 . 107 315 - 321 . . Aluminium toxicity and tolerance in plants E Delhaize , S Craig , CD Beaton , RJ Bennet , VC Jagadish , PJ Randall . Aluminum tolerance in wheat ( Triticum aestivum L.). I. Uptake and distribution of aluminum in root apices . Plant Physiol , 1993 . 103 685 - 693 . . Aluminum tolerance in wheat (Triticum aestivum L.). I. Uptake and distribution of aluminum in root apices E Delhaize , DM Hebb , PR Ryan . Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux . Plant Physiol , 2001 . 125 ( 4 ): 2059 - 2067 . DOI: 10.1104/pp.125.4.2059 http://doi.org/10.1104/pp.125.4.2059 . Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux E Delhaize , PR Ryan , DM Hebb , Y Yamamoto , T Sasaki , H Matsumoto . Engineering high-level aluminum tolerance in barley with the ALMT1 gene . Proc Natl Acad Sci USA , 2004 . 101 ( 42 ): 15249 - 15254 . DOI: 10.1073/pnas.0406258101 http://doi.org/10.1073/pnas.0406258101 . Engineering high-level aluminum tolerance in barley with the ALMT1 gene JA Duke . MN Christiansen , CF Lews . Plant Germplasm Resources for Breeding of Crops Adapted to Marginal Environments . Breeding Plants for Less Favourable Environments , 1982 . : New York John Wiley and Son , 339 - 433 . . Plant Germplasm Resources for Breeding of Crops Adapted to Marginal Environments B Ezaki , S Tsgita , H Matsumoto . Expression of moderately anionic peroxidase is induced by aluminum treatment in tobacco cells: possible involvement of peroxidase isozymes in aluminium ion stress . Physiol Plant , 1996 . 96 ( 1 ): 21 - 28 . DOI: 10.1111/j.1399-3054.1996.tb00178.x http://doi.org/10.1111/j.1399-3054.1996.tb00178.x . Expression of moderately anionic peroxidase is induced by aluminum treatment in tobacco cells: possible involvement of peroxidase isozymes in aluminium ion stress B Ezaki , RC Gardner , Y Ezaki , H Matsumoto . Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress . Plant Physiol , 2000 . 122 ( 3 ): 657 - 665 . DOI: 10.1104/pp.122.3.657 http://doi.org/10.1104/pp.122.3.657 . Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress B Ezaki , M Katsuhara , M Kawamura , H Matsumoto . Different mechanisim of four aluminum (Al)-resisitance transgenes for Al toxicity in Arabidopsis . Plant Physiol , 2001 . 127 ( 3 ): 918 - 927 . DOI: 10.1104/pp.127.3.918 http://doi.org/10.1104/pp.127.3.918 . Different mechanisim of four aluminum (Al)-resisitance transgenes for Al toxicity in Arabidopsis JA Fisher , BJ Scott . PGE Searle , BG Davey . Response to Selection for Aluminium Tolerance . Priorities in Soil/Plant Relations Research for Plant Production , 1987 . : Australia Univ. of Sydney , 135 - 137 . . Response to Selection for Aluminium Tolerance CD Foy . MJ Wright , AS Ferrari . General Principles Involved in Screening Plants from Aluminium and Manganese Tolerance . Plant Adaptation to Mineral Stress in Problem Soils , 1976 . : Ithaca Cornel Univ. Press , 255 - 267 . . General Principles Involved in Screening Plants from Aluminium and Manganese Tolerance CD Foy . The physiological of plant adaptation to mineral stress . Iowa State J Res , 1983 . 57 355 - 391 . . The physiological of plant adaptation to mineral stress CD Foy . F Adams . Physiological Effects of Hydrogen, Aluminium and Manganese Toxicities in Acid Soils . Soil Acidity and Liming , 1984 . 2nd Ed : Medison, Wisconsin Soil Sci. Soc. Am., Amer. Soc. Agron., and Crop Sci. Soc. Am. , 57 - 97 . . Physiological Effects of Hydrogen, Aluminium and Manganese Toxicities in Acid Soils CD Foy . Plant adaptation to acid, aluminium-toxic soils . Commun Soil Sci Plant Anal , 1988 . 19 959 - 987 . . Plant adaptation to acid, aluminium-toxic soils CD Foy . JL Hatfield , BA Stewart . Soil Chemical Factors Limiting Plant Root Growth . Advances in Soil Science: Limitation to Plant Root Growth , 1992 . Vol. 19 : New York Springer-Verlag , 97 - 149 . . Soil Chemical Factors Limiting Plant Root Growth CD Foy . Tolerance of barley cultivars to an acid, aluminium-toxic subsoil related to mineral element concentrations in their shoots . J Plant Nutr , 1996 . 19 1361 - 1380 . . Tolerance of barley cultivars to an acid, aluminium-toxic subsoil related to mineral element concentrations in their shoots CD Foy , AL Fleming . Aluminium tolerance of two wheat cultivars related to nitrate reductase activities . J Plant Nutr , 1982 . 5 1313 - 1333 . . Aluminium tolerance of two wheat cultivars related to nitrate reductase activities CD Foy , WH Armiger , LW Briggle , DA Reid . Differential aluminum tolerance of wheat and barley varieties in acid soils . Agron J , 1965 . 57 413 - 417 . . Differential aluminum tolerance of wheat and barley varieties in acid soils CD Foy , AL Fleming , GR Burns , WH Armiger . Characterisation of differential aluminium tolerance among varieties of wheat and barley . Soil Sci Soc Am Proc , 1967 . 31 513 - 521 . . Characterisation of differential aluminium tolerance among varieties of wheat and barley CD Foy , RL Chaney , MC White . The physiology of metal toxicity in plants . Annu Rev Plant Physiol , 1978 . 29 ( 1 ): 511 - 566 . DOI: 10.1146/annurev.pp.29.060178.002455 http://doi.org/10.1146/annurev.pp.29.060178.002455 . The physiology of metal toxicity in plants CD Foy , B Scott , JA Fisher . RD Graham , RJ Hannam , NC Uren . Genetic Differences in Plant Tolerance to Manganese Toxicity . Manganese in Soils and Plants , 1988 . : the Netherlands Kluwer Academic Publishers , 293 - 307 . . Genetic Differences in Plant Tolerance to Manganese Toxicity RR Furlani , RB Clark . Screening sorghum for aluminium tolerance in nutrient solution . Agron J , 1981 . 73 587 - 594 . . Screening sorghum for aluminium tolerance in nutrient solution F Gallardo , F Borie , L Alvear , EV Baer . Evaluation of aluminium tolerance of three barley cultivars by two short-term screening methods and field experiments . Soil Sci Plant Nutr , 1999 . 45 713 - 719 . . Evaluation of aluminium tolerance of three barley cultivars by two short-term screening methods and field experiments FJ Gallego , B Calles , C Benito . Molecular markers linked to the aluminium tolerance gene Alt1 in rye ( Secale cereale L.) . Theor Appl Genet , 1998 . 97 ( 7 ): 1104 - 1109 . DOI: 10.1007/s001220050997 http://doi.org/10.1007/s001220050997 . Molecular markers linked to the aluminium tolerance gene Alt1 in rye (Secale cereale L.) FJ Gallego , E Lopez-Solanilla , AM Figueiras , C Benito . Chromosomal location of PCR fragments as a source of DNA markers linked to aluminium tolerance genes in rye . Theor Appl Genet , 1998 . 96 ( 3-4 ): 426 - 434 . DOI: 10.1007/s001220050759 http://doi.org/10.1007/s001220050759 . Chromosomal location of PCR fragments as a source of DNA markers linked to aluminium tolerance genes in rye DF Garvin , BF Carver . Z Rengel . The Role of the Genotype in Tolerance to Acidity and Aluminum Toxicity . Handbook of Soil Acidity , 2003 . : New York Marcel Dekker , 387 - 406 . . The Role of the Genotype in Tolerance to Acidity and Aluminum Toxicity FM Gauthier . Tolerance of barley varieties to soil acidity . Cereal Newsl , 1953 . 3 12 . Tolerance of barley varieties to soil acidity F Hamel , C Breton , M Houde . Isolation and characterization of wheat aluminum-regulated genes: possible involvement of aluminum as a pathogenesis response elicitor . Planta , 1998 . 205 ( 4 ): 531 - 538 . DOI: 10.1007/s004250050352 http://doi.org/10.1007/s004250050352 . Isolation and characterization of wheat aluminum-regulated genes: possible involvement of aluminum as a pathogenesis response elicitor KE Hammond , DE Evans , MJ Hodson . Aluminium silicon interactions in barley ( Hordeum vulgare L.) seedlings . Plant Soil , 1995 . 173 ( 1 ): 89 - 95 . DOI: 10.1007/BF00155521 http://doi.org/10.1007/BF00155521 . Aluminium silicon interactions in barley (Hordeum vulgare L.) seedlings A Haug , B Shi . RJ Wright , VC Baligar , RP Murrmann . Biochemical Basis of Aluminium Tolerance in Plant Cells . Plant-Soil Interactions at Low pH , 1991 . : Dordrecht, the Netherlands Kluwer Academic Publishers , 839 - 850 . . Biochemical Basis of Aluminium Tolerance in Plant Cells AR Hede , B Skovmand , JM Ribaut , D Gonzalez-de-leon , O Stфlen . Evaluation of aluminium tolerance in a spring rye collection by hydroponic screening . Plant Breeding , 2002 . 121 ( 3 ): 241 - 248 . DOI: 10.1046/j.1439-0523.2002.00706.x http://doi.org/10.1046/j.1439-0523.2002.00706.x . Evaluation of aluminium tolerance in a spring rye collection by hydroponic screening M Henderson , JD Ownby . The role of root cap mucilage secretion in aluminium tolerance in wheat . Curr Topics Plant Biochem Physiol , 1991 . 10 134 - 141 . . The role of root cap mucilage secretion in aluminium tolerance in wheat OA Hoekenga , TJ Vision , JE Shaff , AJ Monforte , GP Lee , SH Howell , LV Kochian . 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 , 2003 . 132 ( 2 ): 936 - 948 . DOI: 10.1104/pp.103.023085 http://doi.org/10.1104/pp.103.023085 . Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta×Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait OA Hoekenga , LG Maron , MA Piñeros , GM Cançado , J Shaff , Y Kobayashi , PR Ryan , B Dong , E Delhaize , T Sasaki , 等 . AtALMT1 , which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis . Proc Natl Acad Sci USA , 2006 . 103 ( 25 ): 9738 - 9743 . DOI: 10.1073/pnas.0602868103 http://doi.org/10.1073/pnas.0602868103 . AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis WJ Horst , A Wagner , H Marschner . Mucilage protects root meristems from aluminium injury . Z Pflanzenphysiol , 1982 . 105 435 - 444 . . Mucilage protects root meristems from aluminium injury M Hossain , MX Zhou , NJ Mendham . A reliable screening system for aluminium tolerance in barley cultivars . Aust J Agric Res , 2005 . 56 ( 5 ): 475 - 482 . DOI: 10.1071/AR04191 http://doi.org/10.1071/AR04191 . A reliable screening system for aluminium tolerance in barley cultivars XM Hu , JW Pan , H Chen , MY Zhu . Aluminum-induced ultraweak luminescence changes in root-tip cells of barley . J Zhejiang Univ (Agric Life Sci) , 2002 . 18 383 - 386 . (in Chinese) . Aluminum-induced ultraweak luminescence changes in root-tip cells of barley IRRI International Rice Research Institute Report for 1973 , 1974 . : Los Banos, Philippines IRRI , . International Rice Research Institute Report for 1973 S Ishikawa , T Wagamatsu , R Sasaki , PO Manu . 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 , 2000 . 46 751 - 758 . . Comparison of the amount of citric and malic acids in Al media of seven plant species and two cultivars each in five plant species EJ Kamprath , CD Foy . Lime-fertilizer-plant Interactions in Acid Soils , 1985 . Fertilizer Technology and Use , 91 - 151 . . Lime-fertilizer-plant Interactions in Acid Soils PS Kidd , M Llugany , C Poschenrieder , B Gunse , J Barcelo . 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 , 2001 . 52 ( 359 ): 1339 - 1352 . DOI: 10.1093/jexbot/52.359.1339 http://doi.org/10.1093/jexbot/52.359.1339 . The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.) TB Kinraide , RC Arnold , VC Baligar . A rapid assay for aluminium phytotoxicity at submicromolar concentrations . Physiol Plant , 1985 . 65 ( 3 ): 245 - 250 . DOI: 10.1111/j.1399-3054.1985.tb02390.x http://doi.org/10.1111/j.1399-3054.1985.tb02390.x . A rapid assay for aluminium phytotoxicity at submicromolar concentrations TB Kinraide , PR Ryan , LV Kochian . Interactive effects of Al 3+ , H + , and other cations on root elongation considered in terms of cell-surface electrical potential . Plant Physiol , 1992 . 99 1461 - 1468 . . Interactive effects of Al3+, H+, and other cations on root elongation considered in terms of cell-surface electrical potential LV Kochian . Cellular mechanism of aluminium toxicity and resistance in plants . Annu Rev Plant Physiol Plant Mol Biol , 1995 . 46 ( 1 ): 237 - 260 . DOI: 10.1146/annurev.pp.46.060195.001321 http://doi.org/10.1146/annurev.pp.46.060195.001321 . Cellular mechanism of aluminium toxicity and resistance in plants LV Kochian , NS Pence , DLD Letham , MA Pineros , JV Magalhaes , OA Hoekenga , DF Garvin . Mechanisms of metal resistance in plants: aluminum and heavy metals . Plant Soil , 2002 . 247 ( 1 ): 109 - 119 . DOI: 10.1023/A:1021141212073 http://doi.org/10.1023/A:1021141212073 . Mechanisms of metal resistance in plants: aluminum and heavy metals LV Kochian , MA Piñeros , OA Hoekenga . The physiology, genetics and molecular biology of plant aluminum resistance and toxicity . Plant Soil , 2005 . 274 ( 1-2 ): 175 - 195 . DOI: 10.1007/s11104-004-1158-7 http://doi.org/10.1007/s11104-004-1158-7 . The physiology, genetics and molecular biology of plant aluminum resistance and toxicity XF Li , JF Ma , H Matsumoto . Pattern of aluminum-induced secretion of organic acids differs between rye and wheat . Plant Physiol , 2000 . 123 ( 4 ): 1537 - 1543 . DOI: 10.1104/pp.123.4.1537 http://doi.org/10.1104/pp.123.4.1537 . Pattern of aluminum-induced secretion of organic acids differs between rye and wheat CD Li , RMC Lance , HM Collins , A Tarr , S Roumeliotis , S Harasymow , M Cakir , GP Fox , CR Grime , S Broughton , 等 . Quantitative trait loci controlling kernel discoloration in barley ( Hordeum vulgare L.) . Aust J Agric Res , 2003 . 54 ( 12 ): 1251 - 1259 . DOI: 10.1071/AR03002 http://doi.org/10.1071/AR03002 . Quantitative trait loci controlling kernel discoloration in barley (Hordeum vulgare L.) YC Liang , CG Yang , HH Shi . Effects of silicon on growth and mineral composition of barley grown under toxic levels of aluminum . J Plant Nutr , 2001 . 24 ( 2 ): 229 - 243 . DOI: 10.1081/PLN-100001384 http://doi.org/10.1081/PLN-100001384 . Effects of silicon on growth and mineral composition of barley grown under toxic levels of aluminum S Lindberg . Aluminium interaction with K + ( 86 Rb + ) and 45 Ca + fluxes in three cultivars of sugar beet ( Beta vulgaris ) . Physiol Plant , 1990 . 79 ( 2 ): 275 - 282 . DOI: 10.1111/j.1399-3054.1990.tb06742.x http://doi.org/10.1111/j.1399-3054.1990.tb06742.x . Aluminium interaction with K+ (86Rb+) and 45Ca+ fluxes in three cultivars of sugar beet (Beta vulgaris) S Lindberg , G Griffiths . Aluminium effects on ATPase activity and lipid composition of plasma membrane of sugar beet roots . J Exp Bot , 1993 . 44 ( 10 ): 1543 - 1550 . . Aluminium effects on ATPase activity and lipid composition of plasma membrane of sugar beet roots EM Lisitsyn . Intravarietal level of aluminum resistance in cereal crops . J Plant Nutr , 2000 . 23 793 - 804 . . Intravarietal level of aluminum resistance in cereal crops R Little . Plant soil interactions at low pH: problem solving—the genetic approach . Commun Soil Sci Plant Anal , 1988 . 19 1239 - 1257 . . Plant soil interactions at low pH: problem solving—the genetic approach M Loper , D Brauer , D Patterson , SI Tu . Aluminium inhibition of NADH-linked electron transfer by corn root plasma membrane . J Plant Nutr , 1993 . 16 507 - 514 . . Aluminium inhibition of NADH-linked electron transfer by corn root plasma membrane MC Luo , J Dvorak . Molecular mapping of an aluminum tolerance locus on chromosome 4D of Chinese Spring wheat . Euphytica , 1996 . 91 31 - 35 . . Molecular mapping of an aluminum tolerance locus on chromosome 4D of Chinese Spring wheat JF Ma , JS Zheng , XF Li , K Takeda , H Matsumoto . A rapid hydroponic screening for aluminium tolerance in barley . Plant Soil , 1997 . 191 ( 1 ): 133 - 137 . DOI: 10.1023/A:1004257711952 http://doi.org/10.1023/A:1004257711952 . A rapid hydroponic screening for aluminium tolerance in barley JF Ma , PR Ryan , E Delhaize . Aluminium tolerance in plants and the complexing role of organic acids . Trends Plant Sci , 2001 . 6 ( 6 ): 273 - 278 . DOI: 10.1016/S1360-1385(01)01961-6 http://doi.org/10.1016/S1360-1385(01)01961-6 . Aluminium tolerance in plants and the complexing role of organic acids JF Ma , R Shen , Z Zhao , M Wissuwa , Y Takeuchi , T Ebitani , M Yano . Response of rice to Al stress and identification of quantitative trait loci for Al tolerance . Plant Cell Physiol , 2002 . 43 ( 6 ): 652 - 659 . DOI: 10.1093/pcp/pcf081 http://doi.org/10.1093/pcp/pcf081 . Response of rice to Al stress and identification of quantitative trait loci for Al tolerance JF Ma , S Nagao , K Sato , H Ito , J Furukawa , K Tekeda . Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley . J Exp Bot , 2004 . 55 ( 401 ): 1335 - 1341 . DOI: 10.1093/jxb/erh152 http://doi.org/10.1093/jxb/erh152 . Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley K Maltais , M Houde . A new biochemical markers for aluminium tolerance in plants . Physiol Plant , 2002 . 115 ( 1 ): 81 - 87 . DOI: 10.1034/j.1399-3054.2002.1150109.x http://doi.org/10.1034/j.1399-3054.2002.1150109.x . A new biochemical markers for aluminium tolerance in plants C Mao , K Yi , L Yang , B Zheng , Y Wu , F Liu , P Wu . 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 , 2003 . 55 ( 394 ): 137 - 143 . DOI: 10.1093/jxb/erh030 http://doi.org/10.1093/jxb/erh030 . Identification of aluminium-regulated genes by cDNA-AFLP in rice (Oryza sativa L.): Al-regulated genes for the metabolism of cell wall components M Matos , MV Camacho , V Pérez-Flores , B Pernaute , O Pinto-Carnide , C Benito . A new aluminum tolerance gene located on rye chromosome arm 7RS . Theor Appl Genet , 2005 . 111 360 - 369 . DOI: 10.1007/s00122-005-2029-1 http://doi.org/10.1007/s00122-005-2029-1 . A new aluminum tolerance gene located on rye chromosome arm 7RS H Matsumoto , T Yamaya . Inhibition of potassium uptake and regulation of membrane-associated Mg 2+ -ATPase activity of pea roots by aluminium . Soil Sci Plant Nutr , 1986 . 32 179 - 188 . . Inhibition of potassium uptake and regulation of membrane-associated Mg2+-ATPase activity of pea roots by aluminium H Matsumoto , Y Yamamoto , M Kasai . 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 , 1992 . 38 411 - 419 . . Change of some properties of the plasma membrane-enhanced fraction of barley roots related to aluminium stress: membrane-associated ATPase, aluminium and calcium P Maxim , Z Duta . Aluminium tolerance of barley 1. Efficiency of in vivo procedure in estimation of genotypic differences . Romanian Agric Res , 1996 . ( 5-6 ): 21 - 28 . . Aluminium tolerance of barley 1. Efficiency of in vivo procedure in estimation of genotypic differences G Miftahudin , J Scoles , JP Gustafson . AFLP markers tightly linked to the aluminum-tolerance gene Alt3 in rye ( Secale cereale L.) . Theor Appl Genet , 2002 . 104 ( 4 ): 626 - 631 . DOI: 10.1007/s00122-001-0782-3 http://doi.org/10.1007/s00122-001-0782-3 . AFLP markers tightly linked to the aluminum-tolerance gene Alt3 in rye (Secale cereale L.) MAR Milla , JP Gustafson . Genetic and physical characterization of chromosome 4DL in wheat . Genome , 2001 . 44 ( 5 ): 883 - 892 . DOI: 10.1139/gen-44-5-883 http://doi.org/10.1139/gen-44-5-883 . Genetic and physical characterization of chromosome 4DL in wheat MAR Milla , E Butler , AR Huete , CF Wilson , O Anderson , JP Gustafson . Expressed sequence tag-based gene expression analysis under aluminum stress in rye . Plant Physiol , 2002 . 130 ( 4 ): 1706 - 1716 . DOI: 10.1104/pp.009969 http://doi.org/10.1104/pp.009969 . Expressed sequence tag-based gene expression analysis under aluminum stress in rye MM Millard , CD Foy , CA Coradetti , MD Reinsel . X-ray photoelectron spectroscopy surface analysis of aluminium ion stress in barley roots . Plant Physiol , 1990 . 93 578 - 583 . . X-ray photoelectron spectroscopy surface analysis of aluminium ion stress in barley roots E Minella , ME Sorrells . Aluminium tolerance in barley: genetic relationships among genotypes of diverse origin . Crop Sci , 1992 . 32 593 - 598 . . Aluminium tolerance in barley: genetic relationships among genotypes of diverse origin E Minella , ME Sorrells . Inheritance and chromosome location of Alp , a gene controlling aluminium tolerance in ‘Dayton’ barley . Plant Breeding , 1997 . 116 ( 5 ): 465 - 469 . DOI: 10.1111/j.1439-0523.1997.tb01032.x http://doi.org/10.1111/j.1439-0523.1997.tb01032.x . Inheritance and chromosome location of Alp, a gene controlling aluminium tolerance in ‘Dayton’ barley SC Miyasaka , JG Buta , RK Howell , CD Foy . Mechanism of aluminium tolerance in snapbeans: root exudation of citric acid . Plant Physiol , 1991 . 96 737 - 743 . . Mechanism of aluminium tolerance in snapbeans: root exudation of citric acid DP Moore , WE Kronstad , RJ Metzger . MJ Wright , SA Ferrari . Screening Wheat for Aluminium Tolerance . Plant Adaptation to Mineral Stress in Problem Soils , 1977 . : Ithaca, New York Cornell Univ. Agr. Exp. Sta. , 287 - 295 . Special Publ. . Screening Wheat for Aluminium Tolerance LM Mugwira , SM Elgawhary , KI Patel . Differential tolerances of Triticale, wheat, rye and barley to aluminium in nutrient solution . Agron J , 1976 . 68 782 - 787 . . Differential tolerances of Triticale, wheat, rye and barley to aluminium in nutrient solution VT Nguyen , MD Burrow , HT Nguyen , BT Le , TD Le , AH Paterson . Molecular mapping of genes conferring aluminium tolerance in rice ( Oryza sativa L.) . Theor Appl Genet , 2001 . 102 ( 6-7 ): 1002 - 1010 . DOI: 10.1007/s001220000472 http://doi.org/10.1007/s001220000472 . Molecular mapping of genes conferring aluminium tolerance in rice (Oryza sativa L.) VT Nguyen , BD Nguyen , S Sarkarung , C Martinez , AH Paterson , HT Nguyen . Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds . Mol Genet Genomics , 2002 . 267 ( 6 ): 772 - 780 . DOI: 10.1007/s00438-002-0686-1 http://doi.org/10.1007/s00438-002-0686-1 . Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds BD Nguyen , DS Brar , BC Bui , TV Nguyen , LN Pham , HT Nguyen . 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 , 2003 . 106 583 - 593 . . Identification and mapping of QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., to indica rice (Oryza sativa L.) FE Ninamango-Cárdenas , CT Guimaraes , PR Martins , SN Parentoni , NP Carneiro , MA Lopes , JR Moro , E Paiva . Mapping QTLs for aluminum tolerance in maize . Euphytica , 2003 . 130 ( 2 ): 223 - 232 . DOI: 10.1023/A:1022867416513 http://doi.org/10.1023/A:1022867416513 . Mapping QTLs for aluminum tolerance in maize K Ohki . Photosynthesis, chlorophyll and transpiration responses in aluminium stressed wheat and sorghum . Crop Sci , 1986 . 26 572 - 575 . . Photosynthesis, chlorophyll and transpiration responses in aluminium stressed wheat and sorghum RN Oram . CJ Driscoll . Breeding Barley Tolerant to High Soil Acidity and Waterlogging . Proc. Aust. Plant Breed Conf. , 1983 . Adelaide, South Australia 71 - 73 . . Breeding Barley Tolerant to High Soil Acidity and Waterlogging JD Ownby . Mechanisms of reaction of hematoxylin with aluminium-treated wheat roots . Physiol Plant , 1993 . 87 ( 3 ): 371 - 380 . DOI: 10.1111/j.1399-3054.1993.tb01744.x http://doi.org/10.1111/j.1399-3054.1993.tb01744.x . Mechanisms of reaction of hematoxylin with aluminium-treated wheat roots DR Parker . Root growth analysis: an underutilization approach to understanding aluminium rhizotoxicity . Plant Soil , 1995 . 171 ( 1 ): 151 - 157 . DOI: 10.1007/BF00009579 http://doi.org/10.1007/BF00009579 . Root growth analysis: an underutilization approach to understanding aluminium rhizotoxicity E Polle , CF Konzak . A single scale for determining Al tolerance levels in cereals . Agron Abstr , 1985 . 67 . A single scale for determining Al tolerance levels in cereals E Polle , CF Konzak , AJ Kittrick . Visual detection of aluminium tolerance levels in wheat by hematoxylin staining of seedling roots . Crop Sci , 1978 . 18 823 - 827 . . Visual detection of aluminium tolerance levels in wheat by hematoxylin staining of seedling roots V Puthota , R Cruz-Ortega , J Johnson , 等 . RJ Wright , VC Baligar , RP Murrmann . An Ultrastructural Study of the Inhibition of Mucilage Secretion in Wheat Root Cap by Aluminium . Plant-Soil Interactions at Low Soil pH , 1991 . : Dordrecht, the Netherlands Kluwer Academic Publishers , 779 - 787 . . An Ultrastructural Study of the Inhibition of Mucilage Secretion in Wheat Root Cap by Aluminium H Raman , S Moroni , R Raman , 等 . A Genomic Region Associated with Aluminium Tolerance in Barley. Proceedings of the 10th Australian Barley Technical Symposium . 2001 . (Available from: Http://www.regional.org.au/au/abts/2001/t3/raman.htm Http://www.regional.org.au/au/abts/2001/t3/raman.htm ) . A Genomic Region Associated with Aluminium Tolerance in Barley. Proceedings of the 10th Australian Barley Technical Symposium H Raman , JH Moroni , K Saito , BJ Read , BJ Scott . Identification of AFLP and microsatellite markers linked with an aluminium tolerance gene in barley ( Hordeum vulgare L.) . Theor Appl Genet , 2002 . 105 ( 2-3 ): 458 - 464 . DOI: 10.1007/s00122-002-0934-0 http://doi.org/10.1007/s00122-002-0934-0 . Identification of AFLP and microsatellite markers linked with an aluminium tolerance gene in barley (Hordeum vulgare L.) H Raman , A Karakousis , JS Moroni , R Raman , B Read , DF Garvin , LV Kochian , ME Sorrells . Development and allele diversity of microsatellite markers linked to the aluminium tolerance gene Alp in barley . Aust J Agric Res , 2003 . 54 ( 12 ): 1315 - 1321 . DOI: 10.1071/AR02226 http://doi.org/10.1071/AR02226 . Development and allele diversity of microsatellite markers linked to the aluminium tolerance gene Alp in barley H Raman , JP Wang , B Read , 等 . Molecular Mapping of Resistance to Aluminium Toxicity in Barley . Proceedings of Plant and Animal Genome XIII Conference , 2005 . San Diego, USA 154 (Available from: Http://www.intl-ag.org/13/abstracts/PAG13_P328.htm Http://www.intl-ag.org/13/abstracts/PAG13_P328.htm ) . Molecular Mapping of Resistance to Aluminium Toxicity in Barley H Raman , K Zhang , M Cakir , R Appels , JS Moroni , LG Maron , LV Kochian , R Raman , M Imtiaz , F Drake-Brockman , 等 . Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat ( Triticum aestivum L.) . Genome , 2005 . 48 781 - 791 . . Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.) BJ Read , BJ Scott . Tolerance of Barley to Aluminium and Manganese . Proceedings of the 8th Australasian Plant Breeding Conference , 1983 . Adelaide 333 - 334 . . Tolerance of Barley to Aluminium and Manganese BJ Read , RN Oram . Hordeum vulgare (Barley) cv. Brindabella . Aust J Exp Agric , 1995 . 35 ( 3 ): 425 DOI: 10.1071/EA9950425 http://doi.org/10.1071/EA9950425 . Hordeum vulgare (Barley) cv. Brindabella B Read , H Raman , G McMichael , K Chalmers , G Ablett , GJ Platz , R Raman , R Genger , R Boyd , RF Park , 等 . Mapping and QTL analysis of the barley population Sloop/Halcyon . Aust J Agric Res , 2003 . 54 ( 12 ): 1145 - 1153 . DOI: 10.1071/AR03037 http://doi.org/10.1071/AR03037 . Mapping and QTL analysis of the barley population Sloop/Halcyon DA Reid . RA Nilan . Genetic Control of Reaction to Aluminum in Winter Barley . Proceedings of the 2nd International Barley Genetics Symposium , 1970 . : Pullman, WA Washington State University Press , 409 - 413 . . Genetic Control of Reaction to Aluminum in Winter Barley DA Reid , GD Jones , WH Armiger , CD Foy , EJ Hoch , TM Sterling . Differential aluminium tolerance of winter barley varieties and selections in associated greenhouse and field experiment . Agron J , 1969 . 61 218 - 222 . . Differential aluminium tolerance of winter barley varieties and selections in associated greenhouse and field experiment DA Reid , AI Fleming , CD Foy . A method for determining aluminium response of barley in nutrient solution in comparison to response in Al-toxic soil . Agron J , 1971 . 63 600 - 603 . . A method for determining aluminium response of barley in nutrient solution in comparison to response in Al-toxic soil Z Rengel , DC Elliott . Mechanism of aluminium inhibition of net 45 Ca 2+ uptake by Amaranthus protoplasts . Plant Physiol , 1992 . 98 632 - 638 . . Mechanism of aluminium inhibition of net 45Ca2+ uptake by Amaranthus protoplasts KD Richards , EJ Schott , YK Sharma , KR Davis , RC Gardner . Aluminum induces oxidative stress genes in Arabidopsis thaliana . Plant Physiol , 1998 . 116 ( 1 ): 409 - 418 . DOI: 10.1104/pp.116.1.409 http://doi.org/10.1104/pp.116.1.409 . Aluminum induces oxidative stress genes in Arabidopsis thaliana CR Riede , JA Anderson . Linkage of RFLP markers to an aluminum tolerance gene in wheat . Crop Sci , 1996 . 36 905 - 909 . . Linkage of RFLP markers to an aluminum tolerance gene in wheat M Rincon , R Gonzales . Aluminium partitioning in intact roots of aluminium-tolerant and aluminium-sensitive wheat ( Triticum aestivum L.) cultivars . Plant Physiol , 1992 . 99 1021 - 1028 . . Aluminium partitioning in intact roots of aluminium-tolerant and aluminium-sensitive wheat (Triticum aestivum L.) cultivars NA Ruiz-Torres , BF Carver . Genetic expression of aluminium tolerance in hard red winter wheat . Cereal Res Com , 1992 . 20 233 - 240 . . Genetic expression of aluminium tolerance in hard red winter wheat PR Ryan , E Delhaize , PJ Randall . Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots . Planta , 1995 . 196 ( 1 ): 103 - 111 . DOI: 10.1007/BF00193223 http://doi.org/10.1007/BF00193223 . Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots PR Ryan , H Raman , K Zhang , 等 . Molecular Mapping of Wheat ALMT1 Gene for Aluminium Tolerance and Its Function in Heterologous Expression Systems . International Symposium on Plant-Soil Interaction at Low pH , 2004 . : Sendai, Japan VI . Molecular Mapping of Wheat ALMT1 Gene for Aluminium Tolerance and Its Function in Heterologous Expression Systems T Sasaki , B Ezaki , H Matsumoto . A gene encoding multidrug resistance (MDR)-like protein is induced by aluminum and inhibitors of calcium flux in wheat . Plant Cell Physiol , 2002 . 43 ( 2 ): 177 - 185 . DOI: 10.1093/pcp/pcf025 http://doi.org/10.1093/pcp/pcf025 . A gene encoding multidrug resistance (MDR)-like protein is induced by aluminum and inhibitors of calcium flux in wheat TYY Sasaki , B Ezaki , M Katsuhara , SJ Ahn , PR Ryan , E Delhaize , H Matsumoto . A wheat gene encoding an aluminium-activated malate transporter . Plant J , 2004 . 37 ( 5 ): 645 - 653 . DOI: 10.1111/j.1365-313X.2003.01991.x http://doi.org/10.1111/j.1365-313X.2003.01991.x . A wheat gene encoding an aluminium-activated malate transporter BJ Scott , JA Fisher . AD Robson . Selection of Genotypes Tolerant of Aluminium and Manganese . Soil Acidity and Plant Growth , 1989 . : Australia Academic Press , 167 - 203 . . Selection of Genotypes Tolerant of Aluminium and Manganese LM Shuman , DO Wilson , RR Duncan . Screening wheat and sorghum cultivars for aluminium sensitivity at low aluminium levels . J Plant Nutr , 1993 . 16 2383 - 2395 . . Screening wheat and sorghum cultivars for aluminium sensitivity at low aluminium levels ST Sibov , M Gaspar , MJ Silva , LMM Ottoboni , P Arruda , AP Souza . Two genes control aluminum tolerance in maize: genetic and molecular mapping analyses . Genome , 1999 . 42 ( 3 ): 475 - 482 . DOI: 10.1139/gen-42-3-475 http://doi.org/10.1139/gen-42-3-475 . Two genes control aluminum tolerance in maize: genetic and molecular mapping analyses G Simons , T van der Lee , P Diergaarde , R van Dealen , J Groenendijk , A Frijters , R Büschges , K Hollricher , S Töpsch , P Schulze-Lefert , 等 . AFLP-based fine mapping of the Mlo gene to a 30-kb DNA segment of the barley genome . Genomics , 1997 . 44 ( 1 ): 61 - 70 . DOI: 10.1006/geno.1997.4844 http://doi.org/10.1006/geno.1997.4844 . AFLP-based fine mapping of the Mlo gene to a 30-kb DNA segment of the barley genome KC Snowden , KD Richards , RC Gardner . Aluminum-induced genes: induction by toxic metals, low calcium, and wounding and pattern of expression in root tips . Plant Physiol , 1995 . 107 341 - 348 . . Aluminum-induced genes: induction by toxic metals, low calcium, and wounding and pattern of expression in root tips MB Stange , ME Beratto , BA Montenegro , CA Peyrelongue , BF Borie . Effect of nitrogen source on growth of barley on a soil with a high aluminium content . Agricultura Tecnica (Santiago) , 1995 . 55 118 - 126 . . Effect of nitrogen source on growth of barley on a soil with a high aluminium content O Stϕlen , S Anderson . Inheritance of tolerance to low soil pH in barley . Heriditas , 1978 . 88 101 - 105 . . Inheritance of tolerance to low soil pH in barley H Takagi , H Namai , K Murakami . Evaluation of the hematoxylin staining method for detecting wheat tolerance to aluminium . Japan J Breed , 1981 . 31 152 - 160 . . Evaluation of the hematoxylin staining method for detecting wheat tolerance to aluminium L Tamas , S Budikova , M Simonovicova , J Huttova , B Siroka , I Mistrik . Rapid and simple method for Al-toxicity analysis in emerging barley roots during germination . Biologia Plantarum , 2006 . 50 ( 1 ): 87 - 93 . DOI: 10.1007/s10535-005-0079-5 http://doi.org/10.1007/s10535-005-0079-5 . Rapid and simple method for Al-toxicity analysis in emerging barley roots during germination Y Tang , ME Sorrells , LV Kochian , DF Gravan . Identification of RFLP markers linked to the barley aluminium tolerance gene Alp . Crop Sci , 2000 . 40 778 - 782 . . Identification of RFLP markers linked to the barley aluminium tolerance gene Alp GJ Taylor . H Sigel , A Sigel . The Physiology of Al Tolerance . Metal Ions in Biological Systems: Aluminium and Its Role in Biology , 1988 . : NY Marcel Dekker , 165 - 199 . . The Physiology of Al Tolerance GJ Taylor . Current views of the aluminium stress response: the physiological basis of tolerance . Curr Top Plant Biochem Physiol , 1991 . 10 57 - 93 . . Current views of the aluminium stress response: the physiological basis of tolerance GJ Taylor . Overcoming barriers to understanding the cellular basis of aluminium resistance . Plant Soil , 1995 . 171 ( 1 ): 89 - 103 . DOI: 10.1007/BF00009570 http://doi.org/10.1007/BF00009570 . Overcoming barriers to understanding the cellular basis of aluminium resistance HR von Uexküll , E Mutert . Global extent, development and economic impact of acid soils . Plant Soil , 1995 . 171 ( 1 ): 1 - 15 . DOI: 10.1007/BF00009558 http://doi.org/10.1007/BF00009558 . Global extent, development and economic impact of acid soils T Wagatsuma , K Yamasaku . Relationship between differential aluminium tolerance and plant induced pH change of medium among barley cultivars . Soil Sci Plant Nutr , 1985 . 31 521 - 535 . . Relationship between differential aluminium tolerance and plant induced pH change of medium among barley cultivars T Wagatsuma , S Ishikawa , H Obata , K Tawaraya , S Katohda . Plasma membrane of younger and outer cells is the primary specific site for aluminium toxicity in roots . Plant Soil , 1995 . 171 ( 1 ): 105 - 112 . DOI: 10.1007/BF00009571 http://doi.org/10.1007/BF00009571 . Plasma membrane of younger and outer cells is the primary specific site for aluminium toxicity in roots JP Wang , H Raman , B Read , MX Zhou , NJ Mendham , S Venkatanagappa . 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 , 2006 . 57 ( 1 ): 113 - 118 . DOI: 10.1071/AR05202 http://doi.org/10.1071/AR05202 . Validation of an Alt locus for aluminium tolerance scored with eriochrome cyanine R staining method in barley cultivar Honen (Hordeum vulgare L.) DA Watt . Aluminium-responsive genes in sugarcane: identification and analysis of expression under oxidative stress . J Exp Bot , 2003 . 54 ( 385 ): 1163 - 1174 . DOI: 10.1093/jxb/erg128 http://doi.org/10.1093/jxb/erg128 . Aluminium-responsive genes in sugarcane: identification and analysis of expression under oxidative stress M Whitten . DR Williamson . Subsurface Acdidification: Estimation Lime Requirements from Lime Dissolution Rates in the Field . Proceedings of the Fourth Triennial Western Australian Soil Science Conference , 1997 . : Geraldton, Western Australia African Reef Resort , 128 - 131 . . Subsurface Acdidification: Estimation Lime Requirements from Lime Dissolution Rates in the Field CH Williams . Soil acidification under clover pasture . Aust J Exp Agric , 1980 . 20 ( 106 ): 561 - 567 . DOI: 10.1071/EA9800561 http://doi.org/10.1071/EA9800561 . Soil acidification under clover pasture P Wu , CY Liao , B Hu , KK Yi , WZ Jin , JJ Ni , C He . QTLs and epistasis for aluminum tolerance in rice ( Oryza sativa L.) at different seedling stages . Theor Appl Genet , 2000 . 100 ( 8 ): 1295 - 1303 . DOI: 10.1007/s001220051438 http://doi.org/10.1007/s001220051438 . QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages AB Xu , BY Dang , MY Zhu , MB Yuan , CN Huang , JJ Yu , Q Huang , YL Wu , ZY Ni . Screening barley varieties for tolerance of acidic aluminium . Crop genet Res , 1991 . 3 17 - 19 . . Screening barley varieties for tolerance of acidic aluminium JL Yang , SJ Zheng , YF He , JF You , L Zhang , XH Yu . 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 , 2006 . 29 ( 2 ): 240 - 246 . DOI: 10.1111/j.1365-3040.2005.01416.x http://doi.org/10.1111/j.1365-3040.2005.01416.x . 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 ZQ Zhao , JF Ma , K Sato , K Takeda . Differential Al resistance and citrate secretion in barley ( Hordeum vulgare L.) . Planta , 2003 . 217 ( 5 ): 794 - 800 . DOI: 10.1007/s00425-003-1043-2 http://doi.org/10.1007/s00425-003-1043-2 . Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.) SJ Zheng , JF Ma , H Matsumoto . High aluminum resistance in buckwheat: I. Al-induced special secretion of oxalic acid from root tips . Plant Physiol , 1998 . 117 ( 3 ): 745 - 751 . DOI: 10.1104/pp.117.3.745 http://doi.org/10.1104/pp.117.3.745 . High aluminum resistance in buckwheat: I. Al-induced special secretion of oxalic acid from root tips MY Zhu , J Pana , L Wanga , Q Gua , C Huangd . Mutation induced enhancement of Al tolerance in barley cell lines . Plant Sci , 2003 . 164 ( 1 ): 17 - 23 . DOI: 10.1016/S0168-9452(02)00317-5 http://doi.org/10.1016/S0168-9452(02)00317-5 . Mutation induced enhancement of Al tolerance in barley cell lines 10.1631/jzus.2006.B0769 Project supported by NSW Agricultural Genomic Centre and the Grains Research and Development Corporation (GRDC) of Australia (UT8) 2006-06-02 2006-07-28 2006-09-14 2022-01-05 Copyright © 2006, Journal of Zhejiang University Science 2006 Journal of Zhejiang University-SCIENCE B (Biomedicine and Biotechnology) 10 07