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Biochemistry, Genetics and Molecular Biology » "Abiotic Stress in Plants - Mechanisms and Adaptations", book edited by Arun Shanker and B. Venkateswarlu, ISBN 978-953-307-394-1, Published: September 22, 2011 under CC BY-NC-SA 3.0 license. © The Author(s).

Chapter 6

Biotechnological Solutions for Enhancing the Aluminium Resistance of Crop Plants

By Gaofeng Zhou, Emmanuel Delhaize, Meixue Zhou and Peter R Ryan
DOI: 10.5772/25187

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Effect of Al3+ toxicity on roots. The scanning electronmicrographs show root apices of near-isogenic wheat plants, ET8 and ES8, that differ in Al3+ resistance at a single major locus. The plants were grown for 4 days growth in 0.2 mM CaCl2 (pH 4.3) with 5 µM AlCl3. The resistant line (ET8, on the left) is unaffected by the treatment whereas the sensitive line (ES8, on the right) shows considerable damage to its tissues. The greater Al3+ resistance of ET8 is controlled by the TaAMLT1 gene on chromosome 4DL. TaALMT1 encodes an Al3+-activated anion channel that facilitates malate efflux from the root apices. (Reprinted from Delhaize and Ryan 1995).
Figure 1. Effect of Al3+ toxicity on roots. The scanning electronmicrographs show root apices of near-isogenic wheat plants, ET8 and ES8, that differ in Al3+ resistance at a single major locus. The plants were grown for 4 days growth in 0.2 mM CaCl2 (pH 4.3) with 5 µM AlCl3. The resistant line (ET8, on the left) is unaffected by the treatment whereas the sensitive line (ES8, on the right) shows considerable damage to its tissues. The greater Al3+ resistance of ET8 is controlled by the TaAMLT1 gene on chromosome 4DL. TaALMT1 encodes an Al3+-activated anion channel that facilitates malate efflux from the root apices. (Reprinted from Delhaize and Ryan 1995).
Al3+-activated organic anion efflux. The Type I response illustrates the rapid activation of organic anion efflux in species such as wheat where the anion channel is constitutively expressed. Al3+ is able to rapidly activate efflux by interacting directly with the pre-existing proteins (red arrows). The Type II response occurs in maize and rye and shows a delay between the addition of Al3+ and the start of organic anion efflux. This delay is interpreted as Al3+ first inducing the expression of the transport protein via a signal transduction pathway possibly involving a specific receptor (“R”)(blue arrows). Once synthesized and inserted in the plasma membrane, Al3+ is thought to interact with the protein to activate efflux of organic anion (OA).
Figure 2. Al3+-activated organic anion efflux. The Type I response illustrates the rapid activation of organic anion efflux in species such as wheat where the anion channel is constitutively expressed. Al3+ is able to rapidly activate efflux by interacting directly with the pre-existing proteins (red arrows). The Type II response occurs in maize and rye and shows a delay between the addition of Al3+ and the start of organic anion efflux. This delay is interpreted as Al3+ first inducing the expression of the transport protein via a signal transduction pathway possibly involving a specific receptor (“R”)(blue arrows). Once synthesized and inserted in the plasma membrane, Al3+ is thought to interact with the protein to activate efflux of organic anion (OA).

Biotechnological Solutions for Enhancing the Aluminium Resistance of Crop Plants

Gaofeng Zhou1, 2, Emmanuel Delhaize1, Meixue Zhou2 and Peter R. Ryan1

1. Introduction

Acid soils limit crop yields around the world due to nutrient deficiencies and mineral toxicities. Non-adapted plants grown on acid soils typically have smaller root systems because high concentrations of soluble aluminium (Al3+) inhibit root elongation. This restricts their ability to acquire water and nutrients. Plants vary widely in their capacity to tolerate acid soils and even genotypes within species show significant variation. The physiology and genetics controlling this variability have been studied for many years. The analysis of segregating populations and mutants has helped identify the mechanisms and genes controlling aluminium resistance in many species including wheat, rice, Arabidopsis, barley and sorghum. The release of organic anions from roots is an important mechanism of resistance in a wide variety of species. This trait is controlled by genes from two distinct gene families that encode transport proteins. Sufficient information is now available for enhancing the aluminium resistance of important crop species using biotechnology. We will review progress in understanding the mechanisms of Al3+ resistance in plants, the genes controlling these mechanisms and the application of genetic engineering to increase the Al3+ resistance of important crop plants. This approach can help maintain and even increase food production on acid soils in the future.

2. Acid soils

2.1. What is acid soil?

Soil pH is an important consideration for agriculture production (Kochian et al. 2004, von Uexkull and Mutert 1995). Some plants are sensitive to high or low pH, nutrient availability and mineral toxicities are influenced by pH and soil microbial communities are significantly affected by pH (Fierer and Jackson 2006, Osborne et al. 2011). Acid soils present multiple stresses to plants including proton toxicity, nutrient deficiencies (especially calcium, magnesium and phosphorus) and metal-ion toxicities especially aluminium and manganese. The United States Department of Agriculture classifies acid soils into five levels: ultra acid soils (below pH 3.5), extremely acid (pH 3.5 to 4.4), very strongly acid (pH 4.5 to 5.0), strongly acid (pH 5.1 to 5.5), moderately acid (pH 5.6 to 6.0) and slightly acid (pH 6.1 to 6.5). Soils with pH≤5.5 can adversely affect the production of many major food crops.

The major limitation to crop growth in acid soils is soluble aluminium. Although aluminium is the third most abundant element in the earth’s crust most of it occurs in mineral forms which are harmless to plants (complexes with oxides and silicates). In acid conditions however these minerals dissolve more readily releasing aluminium into the soil solution. Soluble aluminium hydrolyses to form a range of species the prevalence of which depends on soil pH. When the pH is 4.5 or below, the Al3+ species predominates but as pH increases other mononuclear aluminium species are formed including Al(OH)2 + and Al(OH)2+. The insoluble Al(OH)3 (gibbsite) can also form at higher pH. Trivalent aluminium (Al3+) is highly toxic to many plants but uncertainty continues regarding the relative toxicity of the hydroxyaluminium species (Alva et al. 1986, Kinraide 1997, Noble et al. 1988, Wright et al. 1987). Al3+ is a reactive metal ion that forms complexes with a variety of organic and inorganic ligands including carboxylates, sulphate, and phosphate and many of these complexes are less toxic to plants than free Al3+ (Jones 1998, Kinraide 1997, Matsumoto 2000, Takita et al. 1999).

2.2. Formation and distribution of acid soils

Acid soils can develop naturally depending on characteristics of the parent rock but human intervention can accelerate the process (Rechcigl and Sparks 1985, Vanbreemen et al. 1983). Ancient and highly-weathered soils are often acid because the basic cations (calcium, magnesium, sodium and potassium) have been leached down the profile, often with nitrate, and replaced by hydrogen (H+). Other drivers of acidification include acid precipitation (Rechcigl and Sparks 1985, Vanbreemen et al. 1983) and nitrification. Microorganisms can also generate organic acids and nitrate from the decomposition of plant residues which also contribute the soil acidification. Conversely low pH and aluminium mobilization can affect the microbial populations (Fierer and Jackson 2006) which are required for stubble turnover and nutrient recycling.

Approximately 30% of total land area consists of acid soils, and almost 70% of the world’s potentially arable lands are acidic (Vonuexkull and Mutert 1995). The two main geographical belts of acid soils include the humid northern temperate zone mainly covered by coniferous forests and the humid tropics which support savanna and tropical rain-forests.

The American continent, Asia, Africa, Europe and Australia and New Zealand account for 40.9%, 26.4%, 16.7%, 9.9% and 6.1% of the world’s acid soil respectively. Most acid soils in Asia are distributed throughout Southeast Asia and the Pacific. In Africa large tracts of the acid soil cannot be used for cultivation because they are sandy, nutrient-deprived and water-limited (Vonuexkull and Mutert 1995).

Naturally acidic soils occupy about one third of Australia, but many agricultural soils in the intensive land-use regions have become more acidic as the result of removal of harvestable product, leaching of nitrate and calcium from nitrogen-producing pastures (Australia State of the Environment report, 2001), and high applications of nitrogen fertilizer (Juo et al. 1995, Matsuyama et al. 2005, Sirovy 1979). Rapid acidification associated with the overuse of nitrogen fertilizer is also an emerging problem in China (Guo et al. 2010). Extremely acid soils can mobilise and increase the bioavailability of other toxic metals such as, mercury, zinc, copper, cadmium, chromium, manganese, and vanadium. All these factors may affect plant growth as well as the ecology of soil bacteria, mosses, algae, fungi, and invertebrates.

3. Aluminium toxicity

Acid soils are often low in basic cations, prone to crusting, erosion and compaction but physical constraints and nutrient deficiencies are rarely the main reasons crop plants grow poorly on these soils. Instead, soluble Al3+ is the major factor limiting growth because it inhibits root growth at very low concentrations. Indeed the inhibition of root growth is the primary symptom of plant stress on acid soils (Munns 1965). There are exceptions because many plants endemic to tropical and sub-tropical regions cope well and even thrive on acid soils. The growth of these species can even be stimulated by Al3+ and some accumulate high concentrations in their leaves. These are discussed in more detail later.

Al3+ can begin to inhibit root growth of wheat (Triticum aestivum L.) within minutes or hours in simple hydroponic solutions (Ryan et al. 1992). Longer exposures result in thickened roots, damaged root cap, and lesions in the epidermal and cortical tissues near the apices. The root system becomes small and damaged which limits water and nutrient acquisition. Root apices are the most sensitive part of the root and Al3+ must contact the apices directly for growth to be affected (Figure 1). Exposure of an entire maize root to Al3+ except the apical 5 mm has no affect on growth in the short term (Ryan et al. 1993). Within this region the zone between the meristematic and elongation zones (distal transition zone) appears to be the most sensitive part of the root (Sivaguru and Horst 1998). The concentration-dependent responses of root growth vary between species and even among genotypes. In some plants root growth remains unaffected at low concentrations of Al3+ but declines once a threshold is reached. This is called the threshold for toxicity response (Barcelo and Poschenrieder 2002). In other species root growth is stimulated by low concentrations of Al3+ but declines at higher concentrations. This hormesis-type response, is interpreted as Al3+ first alleviating H+ toxicity at low concentrations and then becoming toxic itself at higher concentrations. A third response observed shows growth inhibition at low concentrations of Al3+ (or short exposures) but little or no effect at higher concentrations (or longer exposures). This is called the threshold for tolerance model and is indicative of an acclimation response occurring.

For many crops including the cereals, most of the Al3+ absorbed by roots localises to the apoplast. The fixed negative charges on the membrane surfaces and pectin in the cell walls attract and bind cations, and especially highly-charged cations like Al3+. Nevertheless it is still uncertain whether this apoplastic Al3+ is toxic to plants or if Al3+ needs to enter the cytosol to cause injury. By binding to pectin in the cell walls Al3+ can rigidify the walls and restrict solute flow through the apoplast (Horst et al. 2010, Sivaguru et al. 2006). High concentrations of Al3+ in the apoplast can induce callose production (1,3 beta D-glucan) and affect membrane function by binding with lipids and proteins or by displacing calcium from critical sites on membranes (Foy et al. 1978). Al3+ can also directly inhibit nutrient uptake by blocking the function of ion channels involved in Ca2+ and K+ influx (Gassmann and Schroeder 1994, Pineros and Tester 1993).

Cytosolic levels of free Ca2+ ([Ca]c) are typically below 1.0 µM in most living cells but transient increases act as signals to control cellular functions and responses to hormones and stress. Ca2+-sensitive fluorescent compounds have detected transient increases in [Ca]c in root cells treated with Al3+ (Rincon-Zachary et al. 2010). The rapidity of these responses indicate that Al3+ is causing damage in the apoplast and that cytosolic Ca2+ could signal early responses to Al3+ stress. Al3+ can interfere with another signal transduction pathway involving inositol 1,4,5-trisphosphate (Jones and Kochian 1995) as well as actin and tubulin stability (Grabski and Schindler 1995, Sivaguru et al. 2003b).


Figure 1.

Effect of Al3+ toxicity on roots. The scanning electronmicrographs show root apices of near-isogenic wheat plants, ET8 and ES8, that differ in Al3+ resistance at a single major locus. The plants were grown for 4 days growth in 0.2 mM CaCl2 (pH 4.3) with 5 µM AlCl3. The resistant line (ET8, on the left) is unaffected by the treatment whereas the sensitive line (ES8, on the right) shows considerable damage to its tissues. The greater Al3+ resistance of ET8 is controlled by the TaAMLT1 gene on chromosome 4DL. TaALMT1 encodes an Al3+-activated anion channel that facilitates malate efflux from the root apices. (Reprinted from Delhaize and Ryan 1995).

Small but measureable amounts of Al3+ does enter the cytosol perhaps via non-specific cation channels (Lazof et al. 1994, Rengel and Reid 1997, Taylor et al. 2000). The combination of pH, ionic strength and availability of organic ligands in the cytosol maintain the soluble Al3+ concentrations to extremely low levels, perhaps less than 1 nM. However even these concentrations may cause damage because Al3+ can out-compete other cations like Mg2+ and Ca2+ for important binding sites and even bind with DNA (Martin 1992). Al3+ also triggers oxidative stress in root cells by triggering the production of reactive oxygen species (Yamamoto et al. 2001). Whether this response is induced by apoplastic Al3+ or symplastic Al3+ is unclear but these highly reactive compounds can rapidly damage membranes, proteins and nucleic acids. Oxidative stress induces callose production which in turn increases cell wall rigidity and decreases the symplastic flow of solutes via the plasmadesmata (Horst et al. 2010, Sivaguru et al. 2000).

In summary, Al3+ interferes with many cellular functions. The Al3+-induced changes to cytosolic Ca2+ concentration, oxidative stress and callose production are likely to signal the early signs of Al3+ injury.

4. Natural variations

Plant species vary widely in their ability to grow and yield on acid soils (Foy 1988). Mclean and Gibert (1927) investigated the relative Al3+ resistance of several crop plants. Sensitive crops included Lactuca sativa (lettuce), Beta vulgaris (beet), Phleum pratense (timothy), Hordeum vulgare (barley), moderately resistant crops were Raphanus sativus (radish), Sorghum bicolour (sorghum), Capitata var. alba L. (cabbage), Avena sativa (oat), Secale cereale (rye) and noticeably resistant species included Zea mays (maize), Brassica rapa (turnip) and Agrostis gigantean (redtop) (McLean and Gilbert 1927). Among the cereals rice is significantly more resistant than maize, wheat and sorghum, while barley and durum wheat are among the most sensitive cereal species (Famoso et al. 2010, Garvin and Carver 2003, Khatiwada et al. 1996).

Significant variation in Al3+ resistance occurs within many species as well including maize, wheat, barley, rice, sorghum, snapbean and Arabidopsis (Foy 1988, Foy et al. 1993, Furlani et al. 1987, Kochian et al. 2004, Koyama et al. 2003, Magalhaes et al. 2007, Ryan et al. 2011, Toda et al. 1999). This variation provides opportunities for breeders to develop new cultivars better suited to acid soils. Even barley, which is considered one of the most Al3+-sensitive of the small-grained Triticeae, displays significant genotypic variability. A seedling-based screen of barley lines in the South and East Asian Barley Core Collection identified Kearney and Golden Promise as sensitive to Al3+ while Dayton and several Japanese cultivars (Honen, Ohichi and Zairai Tanbo) were among the most resistant (Moroni et al. 2010).

A greater variation occurs in hexaploid or bread wheat where differences in root growth can vary by ten-fold or more in short-term growth assays or in field screens (Bona et al. 1993; Cosic et al. 1994, Dai et al. 2009, Foy 1996, Garvin and Carver 2003, Pinto-Carnide and Guedes-Pinto 1999, Raman et al. 2008, Rengel and Jurkic 1992, Ryan et al. 1995a, Tang et al. 2003). Highly Al3+-resistant genotypes of bread wheat commonly used in experiments include BH1146 and Carazinho from Brazil and Atlas 66 from the USA. In most cases enhanced Al3+ resistance is associated with reduced Al3+ accumulation in the roots. Therefore the more resistant genotypes of wheat, maize, barley, sorghum and rye are able to exclude Al3+ from their roots cells – especially from the root apices.

5. Genetics

The inheritance and genetics of Al3+ resistance have been widely studied in members of the Triticeae. In wheat, barley and sorghum Al3+ resistance is often consistent with a single genetic locus inheritance while in maize and rice it is a more complex multigenic trait.

5.1. Single or few genes: cases of simple inheritance

Crop improvement programs in Brazil and the US led to the development of highly-resistant cultivars of wheat such as BH1146 and Atlas66 which have been used for genetic mapping and quantitative trait loci (QTL) analyses. Many studies indicate a single locus controls most of the variation in Al3+ resistance. For instance, a population of recombinant inbred lines developed with BH 1146 and the sensitive cultivar Anahuac showed a bimodal distribution for Al tolerance, consistent with single gene inheritance. Similar results were obtained with other populations (Raman et al. 2005). The resistance locus in BH 1146, named Alt BH , was mapped to chromosome 4DL and explained 85% of the phenotypic variation (Riede and Anderson 1996). The location of Alt BH gene was further confirmed using 91 recombinant inbred lines and a set of wheat deletion lines (Milla and Gustafson 2001) and Luo et al. (1996) had also linked this chromosome to Al3+ resistance using Chinese Spring deletion lines. More recently a major aluminium resistance gene called TaALMT1 (Figure 1; see later) was mapped to the same locus on 4DL (Raman et al. 2005) while minor loci were mapped to 4BL and 3BL (Navakode et al. 2009; Ryan et al. 2009).

QTL analyses of 100 F2 barley seedlings derived from the Al3+-resistant cultivar (Murasakimochi) and the Al-sensitive cultivar (Morex) identified a single Al3+ resistance locus on chromosome 4H which explained more than 50% of the phenotypic variation (Ma et al. 2004). The Alp locus was also mapped to chromosome 4H in a high-resolution map generated from genotypes Dayton and Zhepi 2 (Wang et al. 2007).

Sorghum is closely related to maize and possesses the second smallest genome among cultivated grasses (Mullet et al. 2002). Like wheat and barley the genetics indicate that a single locus, Alt SB , on chromosome 3 controls most of the variation in resistance (Magalhaes et al. 2004).

5.2. Multiple genes: Cases of complex inheritance

Rye is generally regarded as a highly resistant cereal species. Unlike wheat, rye is self-incompatible, so co-segregation experiments in rye generally detect a number of Al3+ resistance loci. Using wheat-rye addition lines, Aniol and Gustafson (1984) identified at least three different Al3+ resistance loci on chromosome 6RS, Alt2 on 3R, and Alt3 on 4RL. Two major dominant and independent loci, Alt1 on chromosome 6RL and Alt3 were identified (Gallego and Benito 1997) and another on chromosome 7RS (Matos et al. 2005). More recently the 7RS locus was shown to include a cluster of ALMT-like genes in the resistant lines (see later) (Collins et al. 2008).

More than 30 QTLs for Al3+ resistance have been reported in rice using populations derived from indica and japonica cultivars as well as wild relatives like Oryza rufiogon. (Ma et al. 2002; Nguyen et al. 2003; Nguyen et al. 2001, Nguyen et al. 2002, Wu et al. 2000; Xue et al. 2007, Xue et al. 2006a, Xue et al. 2006b). Resistance loci on chromosomes 1, 8 and 9 were consistently identified in these studies which confirms resistance is a multigenic trait in this species. Given the conservation of genetic locations among the Triticeae (synteny), it will be intriguing whether orthologous loci to the resistance loci from other cereals play a similar role in rice. For instance, a major resistance locus on rice chromosome 3 is homeologous to Triticeae 4L where the Al3+ resistance loci on wheat and barley are located (Nguyen et al. 2003). In maize, five QTLs on chromosomes 2, 6 and 8 contribute to Al3+ resistance and these explain 60% of the phenotypic variation. Dominant and additive effects were detected between these loci (Ninamango-Cardenas et al. 2003).

6. Mechanisms of Al3+ resistance

Some plants have evolved mechanisms that enable them to tolerate Al3+ toxicity and acid soils better than others. The identification and characterization of these mechanisms has been the focus of considerable research. Some very resistant species like tea (Camelia sinensis) and Hydragenea sp accumulate high concentrations of Al3+ in their roots and leaves while others, such as resistant members of the Triticeae, exclude Al3+ from their root and shoots. For instance the concentration of Al3+ in the root apices of an Al3+-sensitive wheat cultivar after 24 h in 50 μM Al3+ was 10-fold greater than a resistant cultivar (Rincon and Gonzales 1992) and similar results were reported in closely-related wheat lines that differed in Al3+ resistance (Delhaize et al. 1993a). Therefore two main mechanisms have been proposed to account for resistance: exclusion mechanisms and tolerance mechanisms, and evidence is now available for both of these. Exclusion mechanisms prevent Al3+ from entering the cytosol and minimize harmful interactions from occurring in the apoplast. Tolerance mechanisms allow plants to safely take-up and accumulate Al3+ within their cells. Both mechanisms may be operating in the same plant.

6.1. Mechanisms of Al3+ exclusion

There are several ways Al3+ could be prevented from accumulating in apoplastic and symplastic fractions of root tissues. Cell wall chemistry could affect Al3+ binding, the maintenance of a slightly higher rhizosphere pH could shift the hydrolysis of soluble aluminium from Al3+ to Al(OH)2+ which would reduce accumulation in the cell wall, compounds could be released from the root which bind the harmful Al3+ and limit other more damaging interactions from occurring and Al3+ could be actively exuded from the root cell by some active transport process. Charged residues on cell wall pectin will attract and accumulate cations but pectin content is not consistently correlated with either Al3+ sensitivity or resistance (Horst et al. 2010). Recent studies showing that methylation of the pectin residues is correlated with reduced Al3+ accumulation in the wall support the idea that modifications to cell walls can increase Al3+ resistance.

Currently there are no examples of resistance based on Al3+ exudation and nor are there convincing cases linking higher rhizospheric pH to genotypic variation in resistance despite detailed studies in wheat and maize (Pineros et al. 2005). However there are claims of an Al3+-resistant Arabidopsis mutant (alr-104) showing a pH dependent increase in resistance (Degenhardt et al. 1998). Measurements with micro-pH electrodes detected a 0.15 unit higher pH at the root surface of alr-104 plants compared to wildtype plants and subsequent experiments indicated this relatively small pH change could explain the increased resistance. The molecular biology of the alr-104 mutation has not been characterised in detail.

The importance of Al3+ exclusion to the very high resistance of rice was confirmed after characterizing two Al3+-sensitive mutations, als1 and c68, because both of these recessive mutations lead to increased accumulation of Al3+ in the roots (Huang et al. 2009, Ma et al. 2005). als1 carries a mutation in a gene encoding part of an ATP binding cassette (ABC) transporter (see later) while the c68 mutation remains uncharacterized at the genetic level.

The exclusion mechanism for which most supporting evidence is available is the release of organic anions from roots (Delhaize et al. 2007, Ma et al. 2001, Ryan et al. 2001). Malate and citrate are the two anions most commonly reported but oxalate efflux occurs from a few species. Once these anions are released from root cells they bind the Al3+ and prevent it from accumulating in the apoplast, damaging the cells and being absorbed by the roots. Efflux is largely restricted to the root apices and in nearly all cases it does not occur continuously but is activated by exposure to Al3+. The effectiveness of these anions in reducing Al3+ toxicity is demonstrated by adding them to solutions containing toxic concentrations of Al3+. Root growth improves as the anion concentration increases. This occurs for malate, citrate and oxalate additions but not for anions, such as succinate and acetate, which have lower stability constants for Al3+ (Ryan et al. 2001). This exclusion mechanism has now been reported in species from the Poaceae (e.g. wheat, barley, sorghum, maize and rye), Araceae (e.g. taro), Polygonaceae (e.g. buckwheat), Brassicaceae (e.g. Arabidopsis) and the Fabaceae (e.g. soybean, snapbean, common bean, Cassia tora).

The first study linking organic anion efflux with Al3+ resistance was described by Miyasaka et al. (1991). They showed that Al3+ activated citrate exudation from snapbean roots and that the efflux from a resistant cultivar was 10-fold greater than efflux from a sensitive cultivar. Another example was reported soon after in wheat by Delhaize et al.(1993b) and Ryan et al. (1995a) using near-isogenic wheat lines differing in Al3+ resistance. These studies showed that addition of Al3+ to a nutrient solution rapidly stimulated malate release from the root apices of the resistant iso-line but not from the sensitive line. This rapid activation of efflux is termed a Type I response (Figure 2). Type I responses are interpreted as Al3+ activating a transport protein already present in the plasma membrane so little or no delay occurs (Ma et al. 2001). An F2 population generated from these near-isogenic lines demonstrated that resistance co-segregates with malate efflux. Subsequent analyses revealed a strong positive correlation between malate efflux and Al3+ resistance in diverse germplasm which supports the importance of this major trait in wheat (Raman et al. 1995a, 1995b, Raman et al. 2005). Al3+ resistance in barley is correlated with citrate efflux from roots. Organic anion efflux does not appear to be important contributor to the high resistance of rice but it does appear to be a minor contributor in maize. Several maize genotypes display an Al3+-activated efflux of citrate but the efflux is delayed by several hours after Al3+ addition. This is referred to as a Type II response (Figure 2). The delay is interpreted as Al3+ first inducing expression of the transport protein before then activating anion efflux (Ma et al. 2001). Type II responses have also been reported for citrate efflux from Cassia tora, rice bean, and rye (Ma et al. 2001; Yang et al 2006). Some maize genotypes also show a slower Al3+-inducible increase of citrate content suggesting that Al3+ resistance may also rely on internal detoxification (Pineros et al. 2002). Nevertheless no clear correlation has been established between citrate exudation and Al3+ resistance among a large range of maize genotypes (Pineros et al. 2002) which supports a model where several different mechanisms contribute to Al3+ resistance in this species.

6.2. Mechanisms of Al3+ tolerance

Instead of excluding Al3+ from their tissues, many highly-tolerant species absorb Al3+ and store it in their leaves sometimes to concentrations exceeding 3000 mg/kg. This relies on quite different processes involving complexation, detoxification and transport of aluminium within the plant. Aluminium accumulator species are defined as those with 1000 mg/kg aluminium or more in their leaves. Some of these species include tea (Camelia sinensis), Hydrangea sp and buckwheat (Fagopyrum esculentum) as well as a range of tree and shrub species (Haridasan and Dearaujo 1988). Most of the aluminium in tea leaves resides in the apoplast (Tolra et al. 2011) whereas in the leaves of Hydrangea and buckwheat the aluminium is bound in vacuoles by citrate and oxalate anions, respectively. Hydrangea is an ornamental plant that changes the colour of its flowers from pink to blue when grown in acid soils with high Al3+ availability (Ma et al. 1997). This colour change is caused by the formation of aluminium delphinidin complexes or aluminium caffeolylquinate complexes (Takeda et al. 1985). Buckwheat can accumulate 15,000 mg/kg aluminium in its leaves when grown in acid soils (Ma et al. 1997).

High shoot accumulation of aluminium implies soluble aluminium is transported through the xylem and then stored safely in leaf vacuoles or in the apoplast. To protect the plant cells from damage aluminium is bound by organic ligands as it is transported throughout the plant. 27Al NMR studies identified aluminium oxalate complexes (1:3) in buckwheat leaves


Figure 2.

Al3+-activated organic anion efflux. The Type I response illustrates the rapid activation of organic anion efflux in species such as wheat where the anion channel is constitutively expressed. Al3+ is able to rapidly activate efflux by interacting directly with the pre-existing proteins (red arrows). The Type II response occurs in maize and rye and shows a delay between the addition of Al3+ and the start of organic anion efflux. This delay is interpreted as Al3+ first inducing the expression of the transport protein via a signal transduction pathway possibly involving a specific receptor (“R”)(blue arrows). Once synthesized and inserted in the plasma membrane, Al3+ is thought to interact with the protein to activate efflux of organic anion (OA).

(Ma et al. 2001), but aluminium citrate complexes in the xylem (Ma and Hiradate 2000). It appears that aluminium undergoes a ligand exchange with oxalate and citrate depending on whether it is transported into xylem or being sequestered in the leaves.

7. Identification of Al3+-resistance genes in plants

Several Al3+ resistance genes have now been mapped and cloned from a range of species (Table 1). Ryan et al. (2011) classifies these resistance genes into three groups: (1) those isolated by analysing segregating populations and therefore explain genotypic variation, (2) those identified from mutant analysis and therefore do not necessarily explain genotypic variation, and (3) likely resistance genes which require additional supporting information.

SpeciesGenesProtein FunctionReference
Organic transporters
WheatTaALMT1Malate transporter(Sasaki et al. 2004)
ArabidopsisAtALMT1Malate transporter(Hoekenga et al. 2006)
SorghumSbMATECitrate transporter(Magalhaes et al. 2007)
BarleyHvAACT1Citrate transporter(Furukawa et al. 2007)
RyeScALMT1 gene clusterMalate transporter(Collins et al. 2008)
ArabidopsisAtMATE1Citrate transporter(Liu et al. 2009)
MaizeZmMATE1Citrate transporter(Maron et al. 2010)
ABC transporters and other proteins
ArabidopsisAtSTOP1C2H2-type Zn finger transcription factor(Iuchi et al. 2007)
ArabidopsisAtSTAR1ABC transporter-basic detoxification of Al(Huang et al. 2010)
ArabidopsisALS1Half ABC transporter(Larsen et al. 2007)
ArabidopsisALS3Half ABC transporter(Larsen et al. 2005)
RiceART1C2H2-type Zn finger transcription factor(Yamaji et al. 2009)
RiceSTAR1,STAR2ABC transporter- UDP-glucose transport(Huang et al. 2009)
Likely Al3+ resistance gene
WheatTaMATE1Citrate transporter(Ryan et al. 2009)
RyeScMATE2Citrate transporter(Yokosho et al. 2010)
Brassica napusBnALMT1Malate transporter(Ligaba et al. 2006)
BnALMT2Malate transporter

Table 1.

Al3+ resistance genes in plants

7.1 Organic anion transporters

The genes controlling organic anion efflux from roots were the first Al3+ resistance genes to be isolated from plants. Those controlling malate efflux belong to the ALMT (aluminium activated malate transporter) family of genes and those controlling citrate efflux belong to the MATE (multi-drug and toxic compound extrusion) family of genes. The genes controlling oxalate efflux are still unknown. The first aluminium resistance gene cloned from plants was the wheat gene TaALMT1 which encodes an Al3+-activated malate channel (Sasaki et al. 2004). TaALMT1 was identified by cDNA subtractive hybridization using near-isogenic wheat lines ET8 (resistant) and ES8 (sensitive). TaALMT1 was identified for being more highly expressed in root tips of ET8 than of ES8 and its expression co-segregated with Al3+ resistance in a segregating population. Heterologus expression of TaALMT1 in Xenopus laevis oocytes, tobacco suspension cells, barley, wheat and Arabidopsis all generate the same phenotype: an Al3+-activated efflux of malate (Sasaki et al. 2004, Delhaize et al. 2004, Pereira et al. 2010, Ryan et al. 2011). Al3+ resistance was not related to the coding alleles of TaALMT1, but to the level of expression (Raman et al. 2005). Polymorphisms detected in the promoter of TaALMT1 are correlated with Al3+ resistance. Tandem repeats in the promoter of resistance genotypes explain the higher expression in resistant plants such that the larger the number of repeats the higher the expression and this is correlated with greater malate efflux (Ryan et al. 2010, Sasaki et al. 2006). Homologues of TaALMT1 also control Al3+ resistance in Arabidopsis (Hoekenga et al. 2006) and rye (Collins et al. 2008). However not all ALMT genes confer Al3+ resistance because members of this family in barley and Arabidopsis (HvALMT, AtALMT9 and AtALMT12) have other functions on the tonoplast of leaves and in guard cells (Gruber et al. 2011, Kovermann et al. 2007; Sasaki et al. 2010).

The first MATE gene involved in Al3+ resistance was cloned in sorghum by positional cloning (Magalhaes et al. 2007). SbMATE encodes a transport protein located on the plasma membrane that facilitates citrate release from the root cells. SbMATE is constitutively expressed in the root apices of resistant sorghum lines but Al3+ treatment increases expression over hours and days and this change parallels the increase in citrate efflux. Interestingly, the coding regions of SbMATE in the sensitive and resistant genotypes are identical, with polymorphisms in one of the introns only. It will be interesting to discover how SbMATE expression is controlled in sorghum.

MATE genes also control the citrate efflux from Al3+-resistant barley plants and Arabidopsis. The HvAACT1 gene from barley (also known as HvMATE) was also isolated by positional cloning (Furukawa et al. 2007). Like TaALMT1 in wheat, HvAACT1 is constitutively expressed in roots but Al3+ is still required to activate citrate efflux. Unlike TaALMT1 and SbMATE, HvAACT1 expression is higher slightly behind the root apices which may influence its effectiveness. Liu et al. (2009) showed that knock-out mutations in AtMATE prevent the Al3+-activated efflux of citrate but the contribution of AtMATE to the resistance of this species is relatively small compared to the malate channel AtALMT1.

Al3+ resistance in maize is likely to involve several mechanisms. Nevertheless citrate efflux does contribute and Maron et al. (2010) isolated a MATE gene called ZmMATE1 which co-localizes with a major QTL for Al3+ resistance. ZmMATE1 is mainly expressed in roots, is up-regulated by Al3+ and shows higher expression in Al3+-resistant genotypes. ZmMATE1 elicits anion efflux when expressed in Xenopus oocytes and measurements with labeled [14C]-citrate confirmed ZmMATE1 transports citrate (Maron et al. 2010).

Other candidate genes are likely to control Al3+ resistance but need confirmation. For instance, TaMATE1 expression in wheat segregates with citrate efflux in some Brazillian genotypes but it needs to be demonstrated directly that TaMATE is a citrate transporter (Ryan et al. 2009). The citrate efflux from these few genotypes of wheat differs from other species in one important way: it occurs constitutively and does not require Al3+ to activate it. Two genes from Brassica napus, BnALMT1 and BnALMT2, encode functional malate transporters in Xenopus oocytes and their expression is induced by Al3+ but no genetic analysis or knockout mutants have confirmed that they contrbute to Al3+ resistance.

7.2 Other resistance genes

A different set of Al3+ resistance genes was identified using mutant analysis (Table 1). This approach requires no prior knowledge regarding genetics or mechanisms involved. Mutagenized seed is generated by chemical treatments, radiation or the random insertion of a DNA fragment (T-DNA or transposon) into the genome. M2 seedlings are screened and those that grow similar to wild-type plants under control conditions, but show altered responses to Al3+ stress, are selected for further analysis. Candidate genes can be isolated by mapping or obtaining the sequence flanking the T-DNA region and analysed further. The candidate genes can be characterized by overexpression studies, knockout studies, mutant analysis or association analysis. These genes need not show allelic variation within natural populations.

Using this approach Huang et al. (2009) cloned two genes from rice called STAR1 and STAR2 (sensitive to Al rhizotoxicity) which cause plants to be hypersensitive to Al3+ toxicity when knocked out. Both genes are expressed in roots and induced by Al3+ treatment. STAR1 encodes a nucleotide binding domain of bacterial-type ATP binding cassette (ABC) transporter and STAR2 encodes the transmembrane domain for an ABC transporter. Huang et al (2009) demonstrated that STAR1 and STAR2 interact to form a functional ABC transporter which localizes to vesicles of most root cells except for those in the epidermal layer of the mature zone. Xenopus laevis oocytes expressing STAR1/STAR2 can transport UDP-glucose but a more recent study shows that STAR1 is also involved in nicotianamine transport, a secondary metabolite used for the long-distance transport of Fe3+ in plants. The role of STAR1/STAR2 in Al3+ resistance remains unclear but it could be involved with releasing compounds that modify the cell wall during Al3+ stress.

A homologue of STAR1 in Arabidopsis, called AtSTAR1, also encodes an ATP-binding domain of a bacterial-type ABC transporter (Huang et al. 2010). A line carrying a knockout mutation showed increased sensitivity to Al3+ and early flowering. Unlike OsSTAR1, AtSTAR1 is expressed in both the roots and shoots, and its expression is not induced by Al3+ stress. AtSTAR1 may interact with another protein called ALS3 to form a functional ABC transporter. ALS3 had been identified previously in similar screens in Arabidopsis because plants carrying loss-of-function mutations are more sensitive to Al3+ stress (Larsen et al. 2005; Larsen et al. 2007).

STOP1 (sensitive to protons) encodes a transcription factor identified by analysing Arabidopisis mutants which are hypersensitive to H+ toxicity. STOP1 belongs to C2H2-type zinc finger family of proteins. stop1 mutants are more sensitive to Al3+ but not to a range of other cations including cadmium, copper, lanthanum, manganese and sodium. STOP1 is required for the induction of a range of genes including AtALMT1 which encodes the malate transporter. STOP1 plays a critical role in enabling Arabidopsis to resist stress induced by low pH and Al3+ toxicity (Iuchi et al. 2007).

8. Transgenic approaches for increasing Al3+ resistance

The increasing demands for food from a growing world population highlight the need to overcome the major soil constraints currently limiting crop yields. For acid soils, the application of lime (calcium carbonate) can increase the soil pH but this usually only changes the surface pH in the year of application and it can take decades for acidity to be neutralized at depth. Additionally, in third world countries it can be prohibitively expensive to apply sufficient lime to neutralize soil acidity. Increasing the acid soil tolerance by conventional breeding has been successfully applied to several crop species and this complements liming practices as a way of managing acid soils. However, some species lack sufficient variation in their germplasm and genetic modification provides another avenue for increasing their acid soil tolerance. As described above the mechanisms of Al3+ resistance in species, such as wheat, sorghum and barley have been elucidated and the genes underlying these mechanisms have been isolated. These genes have been used to generate transgenic plants with enhanced Al3+ resistance. A range of other genes, not necessarily responsible for natural variation in Al3+ resistance, have also been used to enhance the Al3+ resistance of plants. The following discussion summarises these recent attempts to enhance Al3+ resistance using biotechnology (see Table 2).

8.1 Over-expression of genes involved in organic anion biosynthesis

The important role of organic anion efflux in Al3+ resistance was established 20 years ago, more than a decade before the genes controlling this trait were cloned. Therefore the first attempts to increase organic anion efflux to improve Al3+ resistance focused on increasing organic anion synthesis because the key enzymes and genes involved in those pathways were well known (Table 2). This approach was based on the idea that an increased concentration of organic anions in the cytosol would result in increased organic anion transport across the plasma membrane. The underlying assumption was that transport of organic anions across the plasma membrane is not the rate-limiting step for efflux. Citrate synthase was a sensible starting point due to the known role of citrate in the Al3+ resistance of Cassia tora, maize, rye and snapbean (Ryan et al., 2001; Ma et al., 2001). Citrate synthase is the first enzyme involved in the tricarboxylic acid and glyoxylate cycles. De la Fuente et al. (1997) transformed tobacco and papaya with the citrate synthase gene (CS) from the bacterium Pseudomonas aeruginosa to increase the biosynthesis and efflux of citrate for enhanced Al3+ resistance. When homozygous lines of tobacco expressing the CS gene were analyzed they were found to accumulate up to 10 fold more citrate than the wildtype plants. Citrate efflux of the transgenics was increased four fold over wildtype and this was associated with enhanced Al3+ resistance. Similar results were reported for transgenic papaya expressing the same transgene. However, subsequent work by Delhaize et al. (2001) was not able to repeat these findings on the same tobacco lines or even when the gene was expressed to a much greater level. More recently other groups have reported enhanced Al3+ resistance when CS expression was increased in alfalfa (Barone et al. 2008), Arabidopsis (Koyama et al. 2000, Koyama et al. 1999) and tobacco (Han et al. 2009). In most of these cases the increases in Al3+ resistance were marginal except for tobacco transformed with a rice CS gene where transgenic lines showed up to 4.5-fold greater Al3+ resistance than the wildtype.

Malate dehydrogenase (MDH) which oxidises oxaloacetate to form malate is another enzyme involved in organic anion biosynthesis and this gene has now been over-expressed in several species. An MDH gene highly expressed in root nodules of alfalfa (neMDH ) was over-expressed in alfalfa and this was associated with enhanced malate efflux and greater Al3+ resistance (Tesfaye et al. 2001). Similarly, when MDH genes from Arabidopsis and Escherichia coli were expressed in tobacco, the transgenic plants showed enhanced malate efflux and improved Al3+ resistance (Wang et al. 2010).

8.2. Over-expression of genes involved in organic anion transport

Once the Al3+ resistance genes controlling organic anion efflux were identified and cloned they were transformed into plants (Table 2). These genes belong to the MATE or ALMT gene families and they encode transport proteins that mediate organic anion movement across the plasma membrane to the external medium.

TaALMT1 has now been expressed in several species and in nearly all cases the transgenic plants showed Al3+-activated malate efflux and enhanced Al3+ resistance. The one exception was rice, where TaALMT1 expression conferred Al3+-activated malate efflux but not

Gene functionSource of geneSpecies
Organic anion metabolism
Citrate synthasePseudomonas aeruginosaTobacco and papaya2-fold(De la Fuente et al. 1997)
Citrate synthase (AtCS)ArabidopsisCarrot1.3-fold(Koyama et al. 1999)
Citrate synthase (DcCS)CarrotArabidopsis1.2-fold(Koyama et al. 2000)
Citrate synthase (OsCS1)RiceTobacco4.5-fold(Han et al. 2009)
Citrate synthasePseudomonas aeruginosaAlfalfa2.5-fold(Barone et al. 2008)
Citrate synthase (AtmtCS)ArabidopsisCanola2-fold(Anoop et al. 2003)
Malate dehydrogenaseAlfalfaAlfalfa2-fold(Tesfaye et al. 2001)
Malate dehydrogenaseArabidospis E coli.Tobacco2.4-fold(Wang et al. 2010)
Blue-copper-binding protein gene (AtBCB)ArabidopsisArabidopsis1.7-fold(Ezaki et al. 2000)
Stress response
Glutathione S-transferase gene (parB)TobaccoArabidopsis1.7-fold(Ezaki et al. 2000)
Peroxidase gene (NtPox)TobaccoArabidopsis1.7-fold(Ezaki et al. 2000)
GDP-dissociation inhibitor gene (NtGDI1)TobaccoArabidopsis1.7-fold(Ezaki et al. 2000)
Dehydroascorbate reductaseArabidopsistobacco1.5-fold(Yin et al. 2010)
Manganese superoxide dismutasewheatBrassica napus2.5-fold(Basu et al. 2001)
Organic anion transporter
TaALMT1wheatwheat8-fold(Pereira et al. 2010)
TaALMT1wheatbarley20-fold(Delhaize et al. 2004)
TaALMT1wheatArabidopsis4-fold(Ryan et al. 2011)
SbMATEsorghumArabidopsis2.5-fold(Magalhaes et al. 2007)
Frd3ArabidopsisArabidopsis2-fold(Durrett et al. 2007)
ZmMATE1maizeArabidopsis3-fold(Maron et al. 2010)
HvAACT1barleytobacco2-fold(Furukawa et al. 2007)

Table 2.

Phenotype (RRG) shows the reported increase in Al3+ resistance of the transgenic plants based on measurement of relative root growth (RRG).

Table 2. Studies which have used biotechnology to increase Al3+ resistance in plants.

enhanced Al3+ resistance (Sasaki et al. 2004). The inability of TaALMT1 to increase resistance in this case was attributed to the very high endogenous level of Al3+ resistance of rice.

Barley is among the most Al3+-sensitive cereal crops but the small genotypic variation in resistance that does occur is correlated with low rates of citrate release, but not malate efflux (see above). Expression of TaALMT1 in barley was associated with increased Al3+-activated malate efflux and a significant increase in Al3+ resistance when compared to wildtype plants and null segregant lines (Delhaize et al. 2004). The transgenic barley showed enhanced Al3+ resistance when grown in both hydroponic culture and in acid soil. In hydroponic culture root growth of transgenics was more than 10-fold greater than wildtype (Delhaize et al. 2004). More recently it was shown that these transgenic barley had enhanced phosphorus-use efficiency and improved grain yield when grown on an acid soil (Delhaize et al. 2009).

Similarly Al3+-activated malate efflux and Al3+ resistance were enhanced when TaALMT1 was over-experessed in wheat (Pereira et al. 2010) and Arabidopsis (Ryan et al. 2011). Some of the transgenic wheat lines displayed greater Al3+ resistance than ET8 (the source of the TaALMT1 gene) in both hydroponic and soil experiments (Pereira et al. 2010).

MATE genes encoding citrate transporter proteins in sorghum (SbMATE), barley (HvAACT1), maize (ZmMATE1) and Arabidopsis (AtMATE and Frd3) were transformed into Arabidopsis or tobacco plants (Durrett et al. 2007, Furukawa et al. 2007,Magalhaes et al. 2007, Maron et al. 2010). Frd3 is not an Al3+-resistance gene but it does encode a transporter which releases citrate into the xylem to assist iron movement to the shoots. In all cases these genes increased citrate efflux and enhanced Al3+ resistance of the transgenic plants.

These findings indicate that the MATE and ALMT genes can be effectively used to enhance the Al3+ resistance of not only model species, but also important crop species. The observation that organic anion efflux can be increased by expression of a transport protein suggests that biosynthesis of organic anions is not a limiting factor for many plant species. To date, the transport proteins, and TaALMT1 in particular, have provided the most effective means to increase the Al3+ resistance of plants.

8.3 Genes not associated with organic anions

One of the first biotechnological strategies to increase Al3+ resistance sought to over-express genes induced by Al3+ stress, and especially those involved in combating oxidative stress.

Ezaki et al. (2000) first identified a range of genes whose expression is induced by Al and then overexpressed these genes in Arabidopsis. They found that an Arabidopsis blue-copper-binding protein gene (AtBCB), a tobacco glutathione S-transferase gene (parB), a tobacco peroxidase gene (NtPox) and a tobacco GDP-dissociation inhibitor gene (NtGDI1) conferred a degree of tolerance to Al3+ when over-expressed. In particular, overexpression of the parB gene simultaneously conferred resistance to both Al3+ and oxidative stresses. Other stress-related genes, such as dehydroascorbate reductase from Arabidopsis and manganese superoxide dismutase from wheat, were expressed in tobacco and Brassica napus, respectively with the transgenic plants showing enhanced Al3+ tolerance (Basu et al. 2001; Yin et al. 2010). Overexpression of these stress-related genes in transgenic plants exhibited a 1.5-2.5-fold increase in relative root growth compared to wildtype.

Genes encoding proteins involved in various stress responses, endocytosis, lipid biosynthesis or Al-induced programmed cell death have also conferred a degree of Al3+ tolerance when over-expressed in Arabidopsis or tobacco. These genes encode WAK1, a auxilin-like protein, a ∆8 sphingolipid desaturase and a Ced-2 protein (Ezaki et al. 2000, Ryan et al. 2007, Sivaguru et al. 2003a, Wang et al. 2009). The details of how these genes function to confer Al3+ resistance are not well understood and it is not yet clear that they would be sufficiently effective to enhance the Al3+ resistance of crop species.

9. Conclusions

Much information has been gathered on the mechanisms of Al3+ toxicity and tolerance over the last 20 years. Our understanding of the mechanisms involving organic anion release is more complete than other mechanisms operating in species like rice and maize. Genes belonging to the MATE and ALMT families encode organic anion transport proteins that facilitate anion efflux from the roots. Transgenic plants expressing these genes show increased organic efflux and significantly greater resistance to Al3+ stress. Strategies based on enhanced efflux of organic anions appear to be effective and combining them with Al3+ tolerance mechanisms that act within the plant could provide even greater protection from Al3+ toxicity. These advances pave the way for biotechnological approaches to enhance the acid-soil tolerance of important food crops through genetic engineering and by marker-assisted selection in traditional breeding programs.


1 - A. K. Alva, D. G. Edwards, C. J. Asher, F. P. C. Blamey, 1986 Relationships between root length of soybean and calculated activities of aluminum monomers in nutrient solution. Soil Sci Soc Am J 50 959 962
2 - A. Aniol, J. P. Gustafson, 1984 Chromosome location of genes-controlling aluminum tolerance in wheat, rye, and triticale. Can J Genet Cytol 26 701 705
3 - V. M. Anoop, U. Basu, M. T. Mc Cammon, L. Mc Alister-Henn, G. J. Taylor, 2003 Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol 132 2205 2217
4 - J. Barcelo, c. Poschenrieder, 2002 Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot 48 75 92
5 - P. Barone, D. Rosellini, P. La Fayette, J. Bouton, F. Veronesi, w. Parrott, 2008 Bacterial citrate synthase expression and soil aluminum tolerance in transgenic alfalfa. Plant Cell Rep 27 893 901
6 - U. Basu, A. G. Good, G. J. Taylor, 2001 Transgenic Brassica napus plants overexpressing aluminium-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminium. Plant Cell Environ 24 1269 1278
7 - L. Bona, R. J. Wright, V. C. Baligar, J. Matuz, 1993 Screening wheat and other small grains for acid soil tolerance. Landscape Urban Plan 27 175 178
8 - N. C. Collins, N. J. Shirley, M. Saeed, M. Pallotta, J. P. Gustafson, 2008 An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179 669 682
9 - T. Cosic, M. Poljak, M. Custic, z. Rengel, 1994Aluminum tolerance of durum-wheat germplasm. Euphytica 78 239 243
10 - S. F. Dai, Z. H. Yan, D. C. Liu, L. Q. Zhang, Y. M. Wei, Y. L. Zheng, 2009 Evaluation on chinese bread wheat landraces for low pH and aluminum tolerance using hydroponic screening. Agr Sci China 8 285 292
11 - J. M. De la Fuente, Rodriguez. V. Ramirez, Ponce. J. L. Cabrera, L. Herrera-Estrella, 1997 Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276 1566 1568
12 - J. Degenhardt, P. B. Larsen, S. H. Howell, L. V. Kochian, 1998 Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiol 117 19 27
13 - E. Delhaize, S. Craig, C. D. Beaton, R. J. Bennet, V. C. Jagadish, P. J. Randall, 1993a Aluminum tolerance in wheat (Triticum-aestivum L).1. uptake and distribution of aluminum in root apices. Plant Physiol 103 685 693
14 - E. Delhaize, P. R. Ryan, 1995 Aluminum toxicity and tolerance in plants. Plant Physiol 107 315 321
15 - E. Delhaize, B. D. Gruber, P. R. Ryan, 2007 The roles of organic anion permeases in aluminium resistance and mineral nutrition. Febs Lett 581 2255 2262
16 - E. Delhaize, D. M. Hebb, P. R. Ryan, 2001 Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125 2059 2067
17 - E. Delhaize, P. R. Ryan, D. M. Hebb, Y. Yamamoto, T. Sasaki, h. Matsumoto, 2004 Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci USA: 15249 15254
18 - E. Delhaize, P. R. Ryan, P. J. Randall, 1993b Aluminum tolerance in wheat (Triticum-aestivum L).2. aluminum-stimulated excretion of malic-acid from root apices. Plant Physiol 103 695 702
19 - E. Delhaize, P. Taylor, P. J. Hocking, R. J. Simpson, P. R. Ryan, A. E. Richardson, 2009 Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotechnol J 7 391 400
20 - T. P. Durrett, W. Gassmann, E. E. Rogers, 2007 The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol144 197 205
21 - B. Ezaki, R. C. Gardner, Y. Ezaki, h. Matsumoto, 2000 Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122 657 665
22 - A. N. Famoso, R. T. Clark, J. E. Shaff, E. Craft, S. R. Mc Couch, L. V. Kochian, 2010 Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol 153 1678 1691
23 - N. Fierer, R. B. Jackson, 2006 The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103 626 631
24 - C. D. Foy, 1988 Plant adaptation to acid, aluminum-toxic soils. Commun Soil Sci Plan19 959 987
25 - C. D. Foy, 1996 Tolerance of durum wheat lines to an acid, aluminum-toxic subsoil. J Plant Nutr 19 1381 1394
26 - C. D. Foy, R. L. Chaney, M. C. White, 1978 Physiology of metal toxicity in plants. Annu Rev Plant Phys 29 511 566
27 - C. D. Foy, R. R. Duncan, R. M. Waskom, D. R. Miller, 1993 Tolerance of sorghum genotypes to an acid, aluminum toxic tatum subsoil. J Plant Nutr 16 97 127
28 - P. R. Furlani, C. R. Bastos, R. A. Borgonovi, R. E. Schaffert, 1987 Differential responses of sorghum genotypes for tolerance to aluminum in nutrient solutions. Pesqui Agropecu Bras 22 323 330
29 - J. Furukawa, N. Yamaji, H. Wang, N. Mitani, Y. Murata, K. Sato, M. Katsuhara, K. Takeda, Ma J. F. , 2007 An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48 1081 1091
30 - F. J. Gallego, c. Benito, 1997 Genetic control of aluminium tolerance in rye (Secale cereale L.). Theor Appl Genet 95 393 399
31 - D. F. Garvin, B. F. Carver, 2003 Role of the genotype in tolerance to acidity and aluminum toxicity. Handbook of soil acidity [Ed. Z. Rengel]: 387 406
32 - W. Gassmann, J. I. Schroeder, 1994 Inwardly-rectifying K+ channels in roots hairs of wheat- a mechanism for aluminum-sensitive low-affinity K+ uptake amd membrane potential control. Plant Physiol 105 1399 1408
33 - S. Grabski, m. Schindler, 1995 (Aluminum induces rigor within the actin network of soybean cells. Plant Physiol 108 897 901
34 - B. D. Gruber, E. Delhaize, A. E. Richardson, U. Roessner, R. A. James, S. M. Howitt, P. R. Ryan, 2011 Characterisation of HvALMT1 function in transgenic barley plants. Funct Plant Biol 38 163 175
35 - J. H. Guo, X. J. Liu, Y. Zhang, J. L. Shen, W. X. Han, W. F. Zhang, P. Christie, K. W. T. Goulding, P. M. Vitousek, F. S. Zhang, 2010 Significant acidification in major Chinese croplands. Science 327 1008 1010
36 - Y. Y. Han, W. Z. Zhang, B. L. Zhang, S. S. Zhang, W. Wang, f. Ming, 2009 One novel mitochondrial citrate synthase from Oryza sativa L. can enhance aluminum tolerance in transgenic tobacco. Mol Biotechnol 42 299 305
37 - M. Haridasan, G. M. Dearaujo, 1988 Aluminium-accumulating species in 2 forest communities in the cerrado region of central Brazil. Forest Ecol Manag 24 15 26
38 - O. A. Hoekenga, L. G. Maron, MA Cancado. G. M. A. Pineros, J. Shaff, Y. Kobayashi, P. R. Ryan, B. Dong, E. Delhaize, T. Sasaki, H. Matsumoto, Y. Yamamoto, H. Koyama, L. V. Kochian, 2006 AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA 103: 9738 9743
39 - W. J. Horst, Y. X. Wang, D. Eticha, 2010 The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106 185 197
40 - C. F. Huang, N. Yamaji, J. F. mA, 2010 Knockout of a bacterial-type atp-binding cassette transporter gene, AtSTAR1, results in increased aluminum sensitivity in Arabidopsis. Plant Physiol 153 1669 1677
41 - C. F. Huang, N. Yamaji, N. Mitani, M. Yano, Y. Nagamura, J. F. mA, 2009 A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21 655 667
42 - S. Iuchi, H. Koyama, A. Iuchi, Y. Kobayashi, S. Kitabayashi, Y. Kobayashi, T. Ikka, T. Hirayama, K. Shinozaki, m. Kobayashi, 2007 Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci USA 104 9900 9905
43 - D. L. Jones, 1998 Organic acids in the rhizosphere- a critical review. Plant Soil 205 25 44
44 - D. L. Jones, L. V. Kochian, 1995 Aluminum inhibition of the inositol 145 -Trisphosphate signal-transduction pathway in wheat roots- a role in aluminum toxicity. Plant Cell 7: 1913-1922
45 - A. S. R. Juo, A. Dabiri, k. Franzluebbers, 1995 Acidification of a kaolinitic alfisol under continuous cropping with nitrogen-fertilization in West-Africa. Plant Soil 171: 245 253
46 - S. P. Khatiwada, D. Senadhira, A. L. Carpena, R. S. Zeigler, P. G. Fernandez, 1996 Variability and genetics of tolerance for aluminum toxicity in rice (Oryza sativa L). Theor Appl Genet 93 738 744
47 - T. B. Kinraide, 1997 Reconsidering the rhizotoxicity of hydroxyl, sulphate, and fluoride complexes of aluminium. J Exp Bot 48 1115 1124
48 - L. V. Kochian, O. A. Hoekenga, M. A. Pineros, 2004 How do crop plants tolerate acid soils?- Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55 459 493
49 - P. Kovermann, S. Meyer, S. Hortensteiner, C. Picco, J. Scholz-Starke, S. Ravera, Y. Lee, E. Martinoia, 2007 The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52 1169 1180
50 - H. Koyama, T. Ikka, Y. Kobayashi, M. Hasegawa, 2003 Comparison of aluminum-tolerance and other stress factors associated with acid soil between Arabidopsis accessions. Plant Cell Physiol 44: S164 -S164
51 - H. Koyama, A. Kawamura, T. Kihara, T. Hara, E. Takita, D. Shibata, 2000 Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphorus-limited soil. Plant Cell Physiol 41 1030 1037
52 - H. Koyama, E. Takita, A. Kawamura, T. Hara, D. Shibata, 1999 Over expression of mitochondrial citrate synthase gene improves the growth of carrot cells in Al-phosphate medium. Plant Cell Physiol 40 482 488
53 - P. B. Larsen, J. Cancel, M. Rounds, Ochoa, 2007 Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225: 1447 EOF 1458 EOF -1458
54 - P. B. Larsen, M. J. B. Geisler, C. A. Jones, K. M. Williams, J. D. Cancel, 2005 ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J 41 353 363
55 - D. B. Lazof, J. G. Goldsmith, T. W. Rufty, R. W. Linton, 1994 Rapid uptake of aluminum into cells of intact soybean root tips- a microanalytical study using secondary-ion mass-spectrometry. Plant Physiol 106 1107 1114
56 - A. Ligaba, M. Katsuhara, P. R. Ryan, M. Shibasaka, h. Matsumoto, 2006 The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. Plant Physiol 142 1294 1303
57 - J. P. Liu, J. V. Magalhaes, J. Shaff, L. V. Kochian, 2009 Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57 389 399
58 - M. C. Luo, J. Dvorak, 1996 Molecular mapping of an aluminum tolerance locus on chromosome 4D of Chinese Spring wheat. Euphytica 91 31 35
59 - J. F. Ma, S. Hiradate, 2000 Form of aluminium for uptake and translocation in buckwheat (Fagopyrum esculentum Moench). Planta 211 355 360
60 - J. F. Ma, S. Hiradate, K. Nomoto, T. Iwashita, H. Matsumoto, 1997 Internal detoxification mechanism of Al in hydrangea- Identification of Al form in the leaves. Plant Physiol 113 1033 1039
61 - Ma J. F. , S. Nagao, C. F. Huang, M. Nishimura, 2005 .Isolation and characterization of a rice mutant hypersensitive to Al. Plant Cell Physiol 46 1054 1061
62 - J. F. Ma, S. Nagao, K. Sato, H. Ito, J. Furukawa, K. Takeda, 2004, Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley. J Exp Bot 55 1335 1341
63 - J. F. Ma, P. R. Ryan, 2010 Understanding how plants cope with acid soils. Funct PlantBiol 37: iii-vi
64 - J. F. Ma, P. R. Ryan, E. Delhaize, 2001 Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6 273 278
65 - J. F. Ma, R. F. Shen, Z. Q. Zhao, M. Wissuwa, Y. Takeuchi, T. Ebitani, M. Yano, 2002 Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol 43 652 659
66 - J. V. Magalhaes, D. F. Garvin, Y. H. Wang, M. E. Sorrells, P. E. Klein, R. E. Schaffert, L. Li, L. V. Kochian, 2004 Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the Poaceae. Genetics 167 1905 1914
67 - J. V. Magalhaes, J. Liu, C. T. Guimaraes, U. G. P. Lana, V. M. C. Alves, Y. H. Wang, R. E. Schaffert, O. A. Hoekenga, M. A. Pineros, J. E. Shaff, P. E. Klein, N. P. Carneiro, C. M. Coelho, H. N. Trick, L. V. Kochian, 2007 A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39 1156 1161
68 - L. G. Maron, M. A. Pineros, C. T. Guimaraes, J. V. Magalhaes, J. K. Pleiman, C. Z. Mao, J. Shaff, S. N. J. Belicuas, L. V. Kochian, 2010 Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J 61 728 740
69 - R. B. Martin, 1992 Aluminum speciation in biology. Ciba Foundation Symposia 169 5 25
70 - M. Matos, M. V. Camacho, V. Perez-Flores, B. Pernaute, O. Pinto-Carnide, C. Benito, 2005 A new aluminum tolerance gene located on rye chromosome arm 7RS. Theor Appl Genet 111 360 369
71 - H. Matsumoto, 2000 Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200 1 46
72 - N. Matsuyama, M. Saigusa, E. Sakaiya, K. Tamakawa, Z. Oyamada, K. Kudo, 2005, Acidification and soil productivity of allophanic andosols affected by heavy application of fertilizers. Soil Sci Plant Nutr 51 117 123
73 - F. T. Mc Lean, B. E. Gilbert, 1927 The relative aluminum tolerance of crop plants. Soil Sci 24 163 175
74 - M. A. R. Milla, J. P. Gustafson, 2001 Genetic and physical characterization of chromosome 4DL in wheat. Genome 44 883 892
75 - S. C. Miyasaka, J. G. Buta, R. K. Howell, C. D. Foy, 1991 Mechanism of aluminum tolerance in snapbeans- root exudation of citric-acid. Plant Physiol 96 737 743
76 - J. S. Moroni, K. Sato, B. J. Scott, M. Conyers, B. J. Read, R. Fisher, G. Poile, 2010 (2010) Novel barley (Hordeum vulgare L.) germplasm resistant to acidic soil. Crop Pasture Sci 61 540 553
77 - J. E. Mullet, R. R. Klein, P. E. Klein, 2002 Sorghum bicolor- an important species for comparative grass genomics and a source of beneficial genes for agriculture. Curr Opin Plant Biol 5 118 121
78 - D. N. Munns, 1965 Soil acidity and growth of a legume.2. Reactions of aluminium and phosphate in solution and effects of aluminium phosphate calcium and Ph on Medicago sativa L and Trifolium subterraneum L in solution culture. Aust J Agr Res 16 743 -&
79 - S. Navakode, A. Weidner, U. Lohwasser, M. S. Roder, A. Borner, 2009, Molecular mapping of quantitative trait loci (QTLs) controlling aluminium tolerance in bread wheat. Euphytica 166 283 290
80 - B. D. Nguyen, D. S. Brar, B. C. Bui, T. V. Nguyen, L. N. Pham, H. T. Nguyen, 2003 Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., into indica rice (Oryza sativa L.). Theor Appl Genet 106:583 593
81 - V. T. Nguyen, M. D. Burow, H. T. Nguyen, B. T. Le , T. D. Le , A. H. Paterson, 2001 Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor Appl Genet 102 1002 1010
82 - V. T. Nguyen, B. D. Nguyen, S. Sarkarung, C. Martinez, A. H. Paterson, H. T. Nguyen, 2002 Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds. Mol Genet Genomics 267 772 780
83 - F. E. Ninamango-Cardenas, C. T. Guimaraes, P. R. Martins, S. N. Parentoni, N. P. Carneiro, M. A. Lopes, J. R. Moro, E. Paiva, 2003 Mapping QTLs for aluminum tolerance in maize. Euphytica 130 223 232
84 - A. D. Noble, M. V. Fey, M. E. Sumner, 1988 Division S-4- soil fertility and plant nutrition- calcium-aluminum balance and the growth of soybean roots in nutrient solutions. Soil Sci Soc Am J 52 1651 1656
85 - C. Osborne, A. Zwart, L. Broadhurst, A. Young, A. Richardson, 2011, The influence of sampling strategies and spatial variation on the detected soil bacterial communities under three different land-use types. Microbial Ecology (In press)
86 - J. F. Pereira, G. F. Zhou, E. Delhaize, T. Richardson, M. X. Zhou, P. R. Ryan, 2010 Engineering greater aluminium resistance in wheat by over-expressing TaALMT1. Ann Bot-106 205 214
87 - M. Pineros, M. Tester, 1993, Plasma-membrane Ca2+ channels in roots of higher roots and their role in aluminum toxicity. Plant Soil 156 119 122
88 - M. A. Pineros, J. V. Magalhaes, V. M. C. Alves, L. V. Kochian, 2002 The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiol 129 1194 1206
89 - M. A. Pineros, J. E. Shaff, H. S. Manslank, V. M. C. Alves, L. V. Kochian, 2005 Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiol 137 231 241
90 - O. Pinto-Carnide, H. Guedes-Pinto, 1999 Aluminum tolerance variability in rye and wheat Portuguese germplasm. Genet Resour Crop Ev 46 81 85
91 - H. Raman, P. R. Ryan, R. Raman, B. J. Stodart, K. Zhang, P. Martin, R. Wood, T. Sasaki, Y. Yamamoto, M. Mackay, D. M. Hebb, E. Delhaize, 2008 Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). Theor Appl Genet 116 343 354
92 - H. Raman, K. R. Zhang, M. Cakir, R. Appels, D. F. Garvin, L. G. Maron, L. V. Kochian, J. S. Moroni, R. Raman, M. Imtiaz, F. Drake-Brockman, I. Waters, P. Martin, T. Sasaki, Y. Yamamoto, H. Matsumoto, D. M. Hebb, E. Delhaize, P. R. Ryan, 2005 Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48 781 791
93 - J. E. Rechcigl, D. L. Sparks, 1985 Effect of acid-rain on the soil environment- a review. Commun Soil Sci Plan 16 653 680
94 - Z. Rengel, V. Jurkic, 1992 Genotypic differences in wheat Al-tolerance. Euphytica 62: 111 117 -117
95 - Z. Rengel, R. J. Reid, 1997 Uptake of Al across the plasma membrane of plant cells. Plant Soil 192 31 35
96 - C. R. Riede, J. A. Anderson, 1996 Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Sci 36 905 909
97 - M. Rincon-Zachary, N. D. Teaster, J. A. Sparks, A. H. Valster, C. M. Motes, E. B. Blancaflor, 2010 Fluorescence resonance energy transfer-sensitized emission of yellow cameleon 3.60 reveals root zone-specific calcium signatures in Arabidopsis in response to aluminum and other trivalent cations. Plant Physiol 152 1442 1458
98 - P. R. Ryan, E. Delhaize, D. L. Jones, 2001 Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Phys 52 527 560
99 - P. R. Ryan, E. Delhaize, P. J. Randall, 1995a Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196 103 110
100 - P. R. Ryan, E. Delhaize, P. J. Randall, 1995b Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Aust J Plant Physiol 22 531 536
101 - P. R. Ryan, J. M. Ditomaso, L. V. Kochian, 1993 Aluminum toxicity in roots- an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44 437 446
102 - P. R. Ryan, Q. Liu, P. Sperling, B. Dong, S. Franke, E. Delhaize, 2007A higher plant Delta 8 sphingolipid desaturase with a preference for (Z)-isomer formation confers aluminum tolerance to yeast and plants. Plant Physiol 144 1968 1977
103 - P. R. Ryan, H. Raman, S. Gupta, W. J. Horst, E. Delhaize, 2009 A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149 340 351
104 - P. R. Ryan, H. Raman, S. Gupta, T. Sasaki, Y. Yamamoto, E. Delhaize, 2010 The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1. Plant J 64 446 455
105 - P. R. Ryan, J. E. Shaff, L. V. Kochian, 1992 Aluminum toxicity in roots- correlation among ionic currents, ion fluxes, and root elongation in aluminum-sensitive and aluminum-tolerant wheat cultivars. Plant Physiol 99 1193 1200
106 - P. R. Ryan, S. D. Tyerman, T. Sasaki, T. Furuichi, Y. Yamamoto, W. H. Zhang, E. Delhaize, 2011 The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot 62 9 20
107 - T. Sasaki, I. C. Mori, T. Furuichi, S. Munemasa, K. Toyooka, K. Matsuoka, Y. Murata, Y. Yamamoto, 2010, Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant Cell Physiol 51 354 365
108 - T. Sasaki, P. R. Ryan, E. Delhaize, D. M. Hebb, Y. Ogihara, K. Kawaura, K. Noda, T. Kojima, A. Toyoda, H. Matsumoto, Y. Yamamoto, 2006, Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant Cell Physiol 47 1343 1354
109 - T. Sasaki, Y. Yamamoto, B. Ezaki, M. Katsuhara, S. J. Ahn, P. R. Ryan, E. Delhaize, H. Matsumoto, 2004 A wheat gene encoding an aluminum-activated malate transporter. Plant J 37 645 653
110 - V. Sirovy, 1979 Effect of high fertilizer doses on the acidification of soils. Rost Vyroba 25 755 762
111 - M. Sivaguru, B. Ezaki, Z. H. He, H. Y. Tong, H. Osawa, F. Baluska, D. Volkmann, H. Matsumoto, 2003a Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in arabidopsis. Plant Physiol 132 2256 2266
112 - M. Sivaguru, T. Fujiwara, J. Samaj, F. Baluska, Z. M. Yang, H. Osawa, T. Maeda, T. Mori, D. Volkmann, H. Matsumoto, 2000, Aluminum-induced 1-> 3-beta-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol 124 991 1005
113 - M. Sivaguru, W. J. Horst, 1998 The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol 116 155 163
114 - M. Sivaguru, W. J. Horst, D. Eticha, H. Matsumoto, 2006 Aluminum inhibits apoplastic flow of high-molecular weight solutes in root apices of Zea mays L. J Plant Nutr Soil Sci 169 679 690
115 - M. Sivaguru, S. Pike, W. Gassmann, T. I. Baskin, 2003b Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: Evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44 667 675
116 - K. Takeda, M. Kariuda, H. Itoi, 1985 Blueing of sepal color of hydrangea-macrophylla. Phytochemistry 24 2251 2254
117 - E. Takita, H. Koyama, T. Hara, 1999 Organic acid metabolism in aluminum-phosphate utilizing cells of carrot (Daucus carota L.). Plant Cell Physiol 40 489 495
118 - C. Tang, M. Nuruzzaman, Z. Rengel, 2003 Screening wheat genotypes for tolerance of soil acidity. Aust J Agr Res 54 445 452
119 - G. J. Taylor, J. L. Mc Donald-Stephens, D. B. Hunter, P. M. Bertsch, D. Elmore, Z. Rengel, R. J. Reid, 2000 Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol 123 987 996
120 - M. Tesfaye, S. J. Temple, D. L. Allan, C. P. Vance, D. A. Samac, 2001 Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol 127 1836 1844
121 - T. Toda, H. Koyama, T. Hori, T. Hara, 1999 Aluminum tolerance of Arabidopsis thaliana under hydroponic and soil culture conditions. Soil Sci Plant Nutr 45 419 425
122 - R. Tolra, K. Vogel-Mikus, R. Hajiboland, P. Kump, P. Pongrac, B. Kaulich, A. Gianoncelli, V. Babin, J. Barcelo, M. Regvar, C. Poschenrieder, 2011 Localization of aluminium in tea (Camellia sinensis) leaves using low energy X-ray fluorescence spectro-microscopy. J Plant Res 124 165 172
123 - N. Vanbreemen, J. Mulder, C. T. Driscoll, 1983 Acidification and alkalinization of soils. Plant Soil 75 283 308
124 - H. R. von Uexkull., E. Mutert, 1995 Golbal extent, development and economic-impact of acid soils. Plant Soil 171 1 15
125 - J. P. Wang, H. Raman, M. X. Zhou, P. R. Ryan, E. Delhaize, D. M. Hebb, N. Coombes, N. Mendham, 2007., High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 115 265 276
126 - Q. F. Wang, Y. Zhao, Q. O. Yi, K. Z. Li, Y. X. Yu, L. M. Chen, 2010 Overexpression of malate dehydrogenase in transgenic tobacco leaves: enhanced malate synthesis and augmented Al-resistance. Acta Physiol Plant 32 1209 1220
127 - W. Z. Wang, J. W. Pan, K. Zheng, H. Chen, H. H. Shao, Y. J. Guo, H. W. Bian, N. Han, J. H. Wang, M. Y. Zhu, 2009 Ced-9 inhibits Al-induced programmed cell death and promotes Al tolerance in tobacco. Biochem Bioph Res Co 383 141 145
128 - R. J. Wright, V. C. Baligar, S. F. Wright, 1987 Estimation of phytotoxic aluminum in soil solution using 3 spectrophotometric methods. Soil Sci 144 224 232
129 - P. Wu, C. Y. Liao, B. Hu, K. K. Yi, W. Z. Jin, J. J. Ni, C. He, 2000 QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genet 100 1295 1303
130 - Y. Xue, L. Jiang, N. Su, J. K. Wang, P. Deng, Ma J. F. , H. Q. Zhai, J. M. Wan, 2007 The genetic basic and fine-mapping of a stable quantitative-trait loci for aluminium tolerance in rice. Planta 227 255 262
131 - Y. Xue, J. M. Wan, L. Jiang, L. L. Liu, N. Su, H. Q. Zhai, J. F. Ma, 2006a QTL analysis of aluminum resistance in rice (Oryza sativa L.). Plant Soil 287 375 383
132 - Y. Xue, J. M. Wan, L. Jiang, C. M. Wang, L. L. Liu, Y. M. Zhang, H. Q. Zhai, 2006b Identification of quantitative trait loci associated with aluminum tolerance in rice (Oryza sativa L.). Euphytica 150 37 45
133 - N. Yamaji, C. F. Huang, S. Nagao, M. Yano, Y. Sato, Y. Nagamura, J. F. Ma, 2009 A zinc finger transcription factor art1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21 3339 3349
134 - Y. Yamamoto, Y. Kobayashi, H. Matsumoto, 2001 Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125 199 208
135 - J. L. Yang, L. Zhang, Y. Y. Li, J. F. You, P. Wu, S. J. Zheng, 2006 Citrate transporters play a critical role in aluminium-stimulated citrate efflux in rice bean (Vigna umbellata) roots. Ann Bot 97 579 584
136 - L. N. Yin, S. W. Wang, A. E. Eltayeb, M. I. Uddin, Y. Yamamoto, W. Tsuji, Y. Takeuchi, K. Tanaka, 2010 Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231 609 621
137 - K. Yokosho, N. Yamaji, J. F. Ma, 2010 Isolation and characterisation of two MATE genes in rye. Funct Plant Biol 37 296 303
138 - Z. Q. Zhao, J. F. Ma, K. Sato, K. Takeda, 2003 Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). Planta 217 794 800