A REVIEW ON PHYSIOLOGICAL BASIS OF Al TOXICITY TOLERANCE IN CROPS


1.   Introduction

Aluminium is one of the most abundant metals in the earth’s crust. Approximately 50% of the world’s potentially arable soils are acidic, and aluminium (Al) toxicity has been recognizedas one of the most prominent growth limiting factors (Kochian et al., 2005). At soil pH bellow 5.0, Al speciates into its various soluble forms, among which Al3+and Al(OH)2+are the most predominant form that are highly toxic to plants resulting in a poorly developed root system and thus susceptible to drought stress, lodging nutrient deficiencies. These ions of Al cause inhibition of root elongation by destroying the cell structure of the root apex and thus affecting water and nutrient uptake in the roots which results into suppression of plants growth and development (Zheng et al., 2010). At mildly acidic or neutral soils, it occurs primarily as insoluble deposits and is essentially biologically inactive (Yang et al., 2013). Al toxicity is reported to be a major factor limiting crop productivity in acidic soils (Kochian et al., 2004).

2.   Tolerance Mechanism

Many plants have evolved mechanisms for detoxifying Al through secretion of Al chelating substances from the roots (Yang et al 2013). Exclusion of Al from the root tip by root released organic acids (OA) which chelate Al3+ is well documented mechanism of Al tolerance in crop plants (Yang et al., 2006) . Plants differ in the species of OA anions secreted, secretion patterns, temperature sensitivity, response to inhibitors, and dose response to Al (Ma 2007). Since the first report on the Al-induced secretion of malate from wheat (Triticumaestivum) roots (Kitagawa et al.,  1986), increasing evidence shows that many Al-tolerant species or cultivars are able to secrete high levels of citrate, malate, and/or oxalate from roots when exposed to Al, including barley (Hordeumvulgare) (Zhao et al,  2007), spinach (Yang et al, 2006), maize (Zea mays) (Pellet et al,  2003), soybean (Glycine max) (Liao, 2006) Citrus junos (Deng et al., 2009), sorghum (Sorghum bicolor) (Kochian, 2005),triticale (Triticosecale Wittmark) (Ma et al., 2001), Lespedeza bicolor (Dong, 2008), Citrus grandis, and Citrus sinensis (Yang et al.,  2012).All these OA anions (citrate, oxalate, and malate) secreted from plant roots can form stable, nontoxic complexes with Al in the rhizosphere, thereby preventing the binding of Al to cellular components, resulting in detoxification of Al (Ma, 2007). Of the three OA anions, citrate has the highest chelating activity for Al followed by oxalate and malate (Ma, 2007). Citric acid is specifically secreted by Cassia tora L under Al stress (Ma, 2007). The Al-induced secretion of OA anions is localized to the root apex, which is in agreement with the targeting site for Al toxicity and their secretion is highly specific to Al, neither phosphorus (P) deficiency nor other polyvalent cations result in the secretion of OA anions. Based on the timing of secretion, two patterns of Al-induced OA anion secretion have been proposed (Ma, 2001). In Pattern I plants, no discernible delay is observed between the addition of Al and the onset of OA anion secretion such as buckwheat (Yang et al., 2006), tobacco (Nicotianatabacum) (Delhaize et al., 2004), and wheat (Ryan et al., 2011). In this case, Al may simply activate a transporter in the plasma membrane (PM) to initiate OA anion secretion, and the induction of genes is not required (Ma, 2007). In Pattern II plants, OA anion secretion is delayed for several hours after exposure to Al such as in rye and Cassia tora (Yang et al., 2006), C. Junos (Deng et al., 2009), soybean (Liao 2006), L. bicolor (Dong 2008), and triticale (Ma 2001). In this case, Al may induce the expression of genes and the synthesis of proteins involved in OA metabolism or in the transport of OA anions (Ma 2001). Yang et al. investigated the effects of a protein-synthesis inhibitor (cycloheximide, CHM) on the Al-induced secretion of OA anions from the roots of buckwheat, a typical Pattern I plant, and C. tora, a typical Pattern II plants, suggesting that both de novo synthesis and activation of an anion channel are needed for the Al-activated secretion of citrate in C. tora, but in buckwheat the PM protein responsible for oxalate secretion preexisted (Yang et al, 2006). Although the Al-induced secretion of OA anions has been well documented, there is a lack of correlation between OA anion secretion and Al tolerance in some plant species. For example, the Al-induced secretion of OA anions (citrate and oxalate) cannot account for the genotypic differences in Al tolerance in maize, soybean, and buckwheat cultivars (Nian et al., 2004). Wenzl et al. observed that the secretion of OA anions from Al-treated signal grass (Brachiariadecumbens) apices was three- to 30-times smaller than that from Al-treated apices of buckwheat, maize, and wheat (all much more sensitive to Al than signal grass) (Wenzl et al.,  2001). Ishikawa et al. investigated the amount of malate and citrate in Al media of seven plant species (Al tolerance order: Brachiariabrizantha, rice (Oryzasativa), and tea (Camellia sinensis) > maize > pea (Pisumsativum) and C. tora> barley) and of two cultivars with differential Al tolerance each in five plant species (rice, maize, wheat, pea, and sorghum). They did not observe any correlation of Al tolerance among some plant species or between two cultivars in some plant species with the amount of citrate and malate in Al media (Ishikawa et al, 2000). Yang et al. showed that eight oxalate accumulator cultivars from four species including Amaranthus spp., buckwheat, spinach (Spinaciaoleracea), and tomato (Lycopersiconesculentum) secreted oxalate rapidly under Al stress, but oxalate secretion was not related to their Al tolerance (Yang et al., 2012). Therefore, it is reasonable to assume that some plant species may contain other (stronger) mechanisms, which mask the effect of OA anions and/or that the Al-induced secretion of OA anions is too low to be an effective mechanism (Yang et al., 2013). In this section, we will discuss several aspects that have been implicated in the regulation of the Al-induced OA anion secretion.

3.Internal mechanisms for tolerance
                                                                     
Internal mechanisms refer to cell internal components or structures that chelate Al to form non-toxic components. These include the chelating of Al in the cytosol, compartmentalization in the vacuole, Al-binding proteins and Al-tolerant isoenzymes (Kochian et al., 2004). Little is known about the internal mechanism that alleviates Al toxicity since it is very complicated and there are numerous chemicals and targets responding to Al toxicity. For example, Watanabe and Osaki (Watanabe and Osaki, 2001) reported that the melastoma could accumulate high concentrations of Al in leaves. When Al was translocated from roots to leaves, it formed different chemicals including Al-citrate and Al-oxalate complexes. Flavonoid-type phenolics can possibly detoxify Al inside plant cells. Kidd et al. (Kidd et al., 2001) found that phenolics including catechol and quercetin were released in maize treated with Al and Si, and the release was dependent on Al concentration. However, due to a lack of efficient methodologies, our understanding of internal mechanisms of Al tolerance in plants is still fragmentary.

4.Al resistance mechanism and transporters

Secretion of OA anions from roots induced by Al have been reported by many researchers in different plants because it is a major mechanism leading to Al tolerance in higher plants, but the mechanisms which lead to the accumulation and secretion of OA anions are not fully understood (fig 8). Al 3+ resistance genes of several species have been isolated and found to encode membrane proteins that facilitate organic anions efflux from roots. These proteins belong to the Al3+ activated malate transporter (ALMT) and multidrug and toxin extrusion (MATE) families (Magalhaes JV, 2010). The gene named aluminium activated malate transporter (ALMT) belonged to a previously uncharacterized gene fa and was the first Al3+ resistant gene identified in any plant species. The identification of aluminium resistance genes provides opportunities for improving crop productivity on acid soils (Ryan et al., 2011). Al activated secretion of OA anions is mediated through anion channels and carriers (Yang et al., 2013). Inhibitors of anion channels inhibit the Al activated secretion of malate from the roots of wheat plants providing evidence that Al might activate malate secretion in a channel in the plasma membrane in the apical cells of wheat variety tolerant to Al. Inhibition of anion channel and thus inhibiting OA anion is a species dependent and inhibitior concentration dependent process (You et al., 2010). Two citrate carrier inhibitors (pyridoxal 5 phosphate (PP) and phenylisothiocyanate (PITC) effectively inhibited citrate secretion, confirming that the Al activated citrated from rye roots is mediated by citrate carrier (Li et al, 2000). Al activated secretion of citrate from rice bean (Vignaumbellata) and stylosanthessps roots was inhibited by both anion channels and carrier inhibitorsindicating the possible involvement of both the citrate carrier and anion channel in the Al activated citrate secretion. Evidence shows that plant growth hormone ABA is involved in the secretion of oxalate (Ma 2001). ABA activates the anion channels in guard cells of stomata and may play a similar role in the roots and may induce Al tolerance in plants. Both ALMT1 proteins from wheat- rye, A thaliana and rape and Mate proteins from barley and sorghum require Al to activate their function (Ryan et.al. 2011). However the mechanisms of their activation remain unclear, although evidence shows that induction of ALMT 1 expression by Al may involve reversible phosphorylation.

The best characterized Al-resistance mechanism is the transporter responsible for malate efflux, which was firstly cloned in 2004 by a Japanese research group (Sasaki et al 2004). Three years later, two transporters belonging to the MATE family responsible for citrate efflux were near-simultaneously cloned in sorghum by a group from Cornell University (Magalhaes et al 2007) and in barley by a group from Okayama University (Furukawa et al., 2007). In a review paper, (Magalhaes 2010) examines the major characteristics of the transporters in the MATE family and tries to relate this knowledge to Al resistance in plants. However, the MATE family is highly flexible with respect to substrate specificity, which raises the possibility that Al resistance as encoded by MATE proteins may not be restricted to Al-activated citrate release in plant species. There are also indications that regulatory loci may be of pivotal importance in fully exploring the potential for improvement of Al resistance based on MATE genes.

Following the first cloning of the TaALMT1 gene in wheat (Sasaki et al., 2004), it was successfully transferred into an Al-sensitive barley cultivar, conferring Al resistance (Delhaize et al., 2004); however, it still remains unknown as to whether Al resistance can be improved in Al-sensitive wheat cultivars by expressing the TaALMT1gene. In the paper by Pereira et al. (2010), particle bombardment is employed to transform wheat with TaALMT1, using the maize ubiquitin promoter to drive expression. The results showed that TaALMT1 expression, malate efflux and Al3+ resistance in nine T2 lines were significantly increased when compared to untransformed controls and null-segregant lines. Some T2 lines displayed greater Al3+ resistance than the Al-resistant reference genotype, ET8, in both hydroponic and soil experiments. This is the first report of a major food crop being stably transformed for greater Al3+ resistance: so a transgenic strategy has been shown to be an effective option for increasing food production on acid soils. (Zheng et al., 2010)

5. Solutions to overcome Al toxicity

5.1   Breeding for tolerance to soil acidity

Al toxicity is favoured by low pH under reducible soil conditions. Therefore, agronomic practices to overcome this problem are primarily based on increasing soil pH. Application of lime has been the most common practice for many years. The addition of lime increases root cell growth, lowers absorption of Al and enhances the protective ability of the cell (Guo et al., 2006) However, this practice has disadvantages (Tolta et al., 2009) including Zn and Mn deficiency. It has been reported that more efficient than lime in alleviating Al toxicity is Mg and K respectively (Wang et al., 2009).  However, when Mg is present in excess, it becomes toxic (Venkatesan and Jayaganesh, 2010). Other substances, such as boron (B) and silicon (Si), also help to alleviate Al toxicity. These strategies were reported to be dependent on species or even genotypes. Nevertheless, of all practices, improving plant tolerance to acid soil through breeding is still the best solution to cope with Al toxicity. Traditional breeding methods, such as backcrossing, intercrossing, single seed descent and topcrossing can be used in breeding cereals for acid soil tolerance. With advances in molecular techniques, such as marker-assisted selection (MAS), breeding for acid soil tolerance becomes more effective. However, the effectiveness of using MAS relies on the closeness of markers linked to the tolerance genes.

5.2   Molecular approaches to reveal mechanisms of Al tolerance

5.2.1Molecular marker development and their application in studies of Al tolerance and marker-assisted selection (MAS):

Genetic markers are useful tools to reveal Al tolerance mechanisms in higher plants following their detection by inheritance studies and identification of relevant genes or loci (Yang et al., 2012). During the last two decades, molecular markers based on DNA sequence variations were widely used to study Al tolerance. By detecting molecular markers, the gene or trait could be easily identified and traced (Inostroza et al., 2010). Based on the techniques used, molecular markers could be classified as PCR-based or hybridization-based. DArT (Diversity Arrays Technology) and RFLP (restriction fragment length polymorphism) are hybridization-based markers, whereas AFLP (amplified fragment length polymorphism), RAPD (randomly amplified of polymorphic DNA), SSR (simple sequence repeat) and SNP (single nucleotide polymorphism) are based on polymerase chain reaction (PCR) techniques. PCR-based markers are preferred and widely used as they are highly efficient, uses less DNA, is less labour intensive and amenable to automation and avoidance of autoradiography (Nagaraju et al., 2001). The use of molecular markers in Al-tolerance studies includes Al-tolerance gene/loci identification and molecular mapping as well as MAS. One RFLP marker bcd1230, co-segregating with a major gene for Al tolerance, on wheat chromosome 4DL, explained 85% of the phenotypic variation in Al tolerance (Riede and Anderson, 1996).

5.2.2 QTL mapping and inheritance of Al tolerance in plants:

Genetic mapping refers to the mapping of gene/loci to specific chromosome locations using linked genetic markers (Semagn et al., 2006). Some cereal crops, such as wheat, barley, sorghum (Sorghum bicolor L.) and oat were reported to have simple genetic mechanisms of Al tolerance, whereas rice and maize (Zea mays L.) have more complicated inheritance with numerous genes/loci involved. Generally, a single dominant gene is responsible for Al tolerance in wheat (Delhize et al, 2004) however; there are exceptions in some cultivars (Tang et al., 2002). Using different populations, genes/loci for Al tolerance were mapped on different wheat chromosomes.

Single loci for Al tolerance were identified on chromosomes 4DL, 4D, 4BL or 3BL, which had phenotypic contributions as high as 85% (locus on 4DL), 50% (4D), 50% (4BL) and 49% (3BL) (Riede and Anderson, 1996).  In addition, genes/loci on chromosomes 6AL, 7AS, 2DL, 5AS, 3DL and 7D had roles in Al tolerance in wheat (Aniol, 1990). Complex inheritance of Al tolerance was found in wheat. Zhou et al .(2007) identified a secondary QTL for Al resistance on chromosome 3BL in Atlas 66, which was effective only when the epistatic gene on 4DL was absent. Cai et al. (2008) mapped three QTL responsible for Al tolerance on wheat chromosomes 4DL, 3BL and 2A, which collectively explained 80% of the phenotypic variation. Magalhaes et al. (2004) reported a major locus AltSB on chromosome 3 for Al tolerance using comparative mapping. In rye, Al tolerance was reported to be controlled by several loci; at least four independent loci, Alt1 on 6RS (Gallego et al., 1998), Alt2 on 3RS (Aniol, 1990) Alt3 on 4RL ((Riede and Anderson, 1996) and Alt4 on 7RS (Matos et al., 2005) were validated by QTL analysis.

The genes on 3R, 6RS and 4R were validated using wheat addition and substitution lines with rye chromosomes (Aniol, 1990) Gallego and Benito (Gallego et al., 1998) reported that Al tolerance in rye was controlled by dominant loci Alt1 and Alt3; the latter on chromosome 4RL was validated using recombinant inbred lines (Miftahudin et al., 2002) Alt4 on chromosome 7RS was identified in three different F2 populations (Matos et al, 2005).

In Arabidopsis, Al tolerance seems to be multi-genetically controlled. Two major QTL accounting for approximately 40% of the phenotypic variance in Al tolerance were identified using recombinant inbred lines derived from the sensitive ecotype Landsbergerecta and tolerant ecotype Columbia (Hoekenga et al., 2003).

5.3   Transgenic approaches

Transgenic methods are very efficient for validating gene function in Al-tolerance studies. The first report on a transgenic approach to increasing Al tolerance in plants was in 1997 when De La Fuente et al. (1997) reported that an over expressed citrate synthase gene enhanced citrate efflux and led to improved root Al tolerance in transgenic tobacco. Nodule enhanced malate dehydrogenase and phosphoenolpyruvate carboxylase expression in alfalfa caused increased organic acid exudation in transgenic alfalfa. ALMT1 is a single major gene for Al tolerance in wheat. Delhaize et al. (2004) reported that wheat malate transporter gene ALMT1 significantly improved Al tolerance in transgenic barley. Transgenic plants showed robust root growth and unaffected root apices under certain levels of Al stress. Similar results were also reported by Pereira et al. (2010) who transformed TaALMT1 into wheat line ET8 using particle bombardment. T-2 lines showed increased gene expression, malate efflux andAl3+ resistance. HvALMT, a barley malate transporter gene, on chromosome 2H is mainly expressed in stomatal guard cells and expanding root cells (Gruber et al., 2011). When this gene was over expressed in transgenic barley plants there was enhanced exudation of organic compounds and improved Al resistance. The efflux was validated to be independent of Al3+ (Gruber et al., 2011).

5.4     Transcriptional approaches

Transcriptional approaches, such as transcriptional profiling, RT-PCR, RNAi, Northern blotting, and RNA sequencing (Wang et al., 2009) facilitated the identification of pathway-related genes and verification of gene function in Al tolerance. Northern analysis of ALS3, which was reported to encode an ABC transporter-like protein related to Al tolerance in Arabidopsis, revealed that gene expression occurred in all organs and expression increased in roots treated with Al. Chandran et al. (2008) reported over 3000 genes by transcription profiling in an Al-sensitive Medicagotruncatula cultivar under Al treatment. These genes were involved in cell wall modification, cell metabolism, protein synthesis and processing, and abiotic and biotic stress responses. RNA-induced silencing also proved that two of these genes, pectinacetylesterase and annexin, increased sensitivity to Al. Using a suppression subtractive hybridization technique, Chen et al. (2011)  identified 229 functional ESTs in the roots of Al-sensitive alfalfa cultivar YM1 after treatment with 5 μ mol L−1 Al stress. Of them, 137 were known Al-response genes, while the other 92 were novel genes potentially related to Al tolerance. The author also noticed that some novel genes related to metabolism and energy were up-regulated and RT-PCR validated the same result.

6. Conclusion

Fe and Al toxicity is a serious problem for sustainable crop productivity in low land rice soils and in acid soils of India and other parts of the World. Higher concentrations of Fe and Al are found to be toxic to crop plants, particularly rice and upland crops. The last decade has seen rapid progress in our understanding of Fe and Al toxicity mechanisms and plants’ tolerance to soil acidity. Development of tolerant varieties of crops to Fe and Al toxicity for sustainable agriculture in toxic soils can be the best solution to these physiological problems. Understanding both morphological and genetic diversity of a germplasm collection provides a basis for improvement of crops and development of resistant varieties. Finally, these cultivars must be targeted to the Fe and Al toxic environment in which their adaptation mechanism will actually be translated into higher or more robust yields and may need to be supplemented with the appropriate agronomic management interventions. Only such an integrated approach seems to effectively address the problem of Fe toxicity in lowland rice and Al toxicity in acid soils.

Research on molecular basis for Al3+ resistance mechanisms in plants that rely on the effect of organic anions opened up new vistas in the field of acid soil tolerance in crops. Further study in protein structure and function to determine which residues define substrate specificity and to identify those critical for Al3+ activation might be more useful for Al tolerance study in field conditions. Research on genetic engineering, transgenic and implementation of molecular markers to facilitate breeding for Fe2+ and Al3+ tolerance / resistance may bring out complete solution to the problem of yield loss and sustainability of lowland and acid soil agriculture. Physiological response of crop varieties specially at field conditions in iron or aluminium toxic soils will probably shed light on other associated plant nutrition related problems and can give new directions for future research.


Fig 8: A diagram showing the reactions and process involved in the accumulation and secretion of organic acid (OA) anions in aluminium (Al) treated plants. Ac-CoA : acetyl-CoA :ALMT, Al-activated malate transporter ; CS: citrate synthase ; Dpi : diphosphate; MATE : multidrug and toxin compounds extrusion; NAD-ME : NADP malic enzyme; OAA: oxaloacetate; PDH : pyruvate dehydrogenase; PEP : phosphoenolpyruvate ; PEPC : PEP carboxylase; Pi: phosphate ;PK: pyruvate kinase; PPDK : pyruvate Pi dikinase; PPi : pyrophosphate; TCAC : tricarboxylic acid cycle;V-ATPase: tonoplast adenosine triphosphatase; V-PPiase, tonoplastpyrophosphatase; 1,aconitase(ACO); 2,NAD-isocitrate dehydrogenase (NAD-IDH) ; 3,α-ketoglutarate dehydrogenase ; 4,succinate thiokinase; 5, succinate dehydrogenase; 6,fumarase; 7,NAD-MDH ; 8,NAD – malic enzyme (NAD-ME) ; 9,NADP –IDH ----- Redrawn from (Anoop et al., 2003), (Mariano et al., 2005), (Bose et al., 2011), (Lin et al., 2011), and (Yang et al., 2013).

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About the author: The author, Mr. Tarun Saikia is serving as Associate professor, Department of Chemistry at Devi Charan Baruah Girls’ College, Jorhat, Assam, India. A good number of research papers of the author have been published by different esteemed journals. He is associated as life member with different scientific bodies. [Read More]



1 comment:

  1. Plant can grow with soil and water but some plants required specific environmental conditions so they store in plant growth chamber to know that condition and grow that plant.

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