Al3+ resistance genes in plants
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,
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:
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 (
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).
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
Significant variation in Al3+ resistance occurs within many species as well including maize, wheat, barley, rice, sorghum, snapbean and
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
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
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
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,
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,
More than 30 QTLs for Al3+ resistance have been reported in rice using populations derived from
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 (
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
The importance of Al3+ exclusion to the very high resistance of rice was confirmed after characterizing two Al3+-sensitive mutations,
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.
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
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 (
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
(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.
Species | Genes | Protein Function | Reference |
Organic transporters | |||
Wheat | TaALMT1 | Malate transporter | (Sasaki et al. 2004) |
Arabidopsis | AtALMT1 | Malate transporter | (Hoekenga et al. 2006) |
Sorghum | SbMATE | Citrate transporter | (Magalhaes et al. 2007) |
Barley | HvAACT1 | Citrate transporter | (Furukawa et al. 2007) |
Rye | ScALMT1 gene cluster | Malate transporter | (Collins et al. 2008) |
Arabidopsis | AtMATE1 | Citrate transporter | (Liu et al. 2009) |
Maize | ZmMATE1 | Citrate transporter | (Maron et al. 2010) |
ABC transporters and other proteins | |||
Arabidopsis | AtSTOP1 | C2H2-type Zn finger transcription factor | (Iuchi et al. 2007) |
Arabidopsis | AtSTAR1 | ABC transporter-basic detoxification of Al | (Huang et al. 2010) |
Arabidopsis | ALS1 | Half ABC transporter | (Larsen et al. 2007) |
Arabidopsis | ALS3 | Half ABC transporter | (Larsen et al. 2005) |
Rice | ART1 | C2H2-type Zn finger transcription factor | (Yamaji et al. 2009) |
Rice | STAR1,STAR2 | ABC transporter- UDP-glucose transport | (Huang et al. 2009) |
Likely Al3+ resistance gene | |||
Wheat | TaMATE1 | Citrate transporter | (Ryan et al. 2009) |
Rye | ScMATE2 | Citrate transporter | (Yokosho et al. 2010) |
Brassica napus | BnALMT1 | Malate transporter | (Ligaba et al. 2006) |
BnALMT2 | Malate transporter |
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
The first
Al3+ resistance in maize is likely to involve several mechanisms. Nevertheless citrate efflux does contribute and Maron et al. (2010) isolated a
Other candidate genes are likely to control Al3+ resistance but need confirmation. For instance,
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
A homologue of
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
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 (
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
Gene function | Source of gene | Species transformed |
Phenotype (RRG) |
Reference |
Organic anion metabolism | ||||
Citrate synthase | Pseudomonas aeruginosa | Tobacco and papaya | 2-fold | (De la Fuente et al. 1997) |
Citrate synthase (AtCS) | Arabidopsis | Carrot | 1.3-fold | (Koyama et al. 1999) |
Citrate synthase (DcCS) | Carrot | Arabidopsis | 1.2-fold | (Koyama et al. 2000) |
Citrate synthase (OsCS1) | Rice | Tobacco | 4.5-fold | (Han et al. 2009) |
Citrate synthase | Pseudomonas aeruginosa | Alfalfa | 2.5-fold | (Barone et al. 2008) |
Citrate synthase (AtmtCS) | Arabidopsis | Canola | 2-fold | (Anoop et al. 2003) |
Malate dehydrogenase | Alfalfa | Alfalfa | 2-fold | (Tesfaye et al. 2001) |
Malate dehydrogenase | Arabidospis E coli. | Tobacco | 2.4-fold | (Wang et al. 2010) |
Blue-copper-binding protein gene (AtBCB) | Arabidopsis | Arabidopsis | 1.7-fold | (Ezaki et al. 2000) |
Stress response | ||||
Glutathione S-transferase gene (parB) | Tobacco | Arabidopsis | 1.7-fold | (Ezaki et al. 2000) |
Peroxidase gene (NtPox) | Tobacco | Arabidopsis | 1.7-fold | (Ezaki et al. 2000) |
GDP-dissociation inhibitor gene (NtGDI1) | Tobacco | Arabidopsis | 1.7-fold | (Ezaki et al. 2000) |
Dehydroascorbate reductase | Arabidopsis | tobacco | 1.5-fold | (Yin et al. 2010) |
Manganese superoxide dismutase | wheat | Brassica napus | 2.5-fold | (Basu et al. 2001) |
Organic anion transporter | ||||
TaALMT1 | wheat | wheat | 8-fold | (Pereira et al. 2010) |
TaALMT1 | wheat | barley | 20-fold | (Delhaize et al. 2004) |
TaALMT1 | wheat | Arabidopsis | 4-fold | (Ryan et al. 2011) |
SbMATE | sorghum | Arabidopsis | 2.5-fold | (Magalhaes et al. 2007) |
Frd3 | Arabidopsis | Arabidopsis | 2-fold | (Durrett et al. 2007) |
ZmMATE1 | maize | Arabidopsis | 3-fold | (Maron et al. 2010) |
HvAACT1 | barley | tobacco | 2-fold | (Furukawa et al. 2007) |
enhanced Al3+ resistance (Sasaki et al. 2004). The inability of
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
Similarly Al3+-activated malate efflux and Al3+ resistance were enhanced when
These findings indicate that the
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
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
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.
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