Plant Biotechnology
Molecular Biology and Genetics
Electronic Journal of Biotechnology ISSN: 0717-3458 Vol. 13 No. 4, Issue of July 15, 2010
© 2010 by Pontificia Universidad Católica de Valparaíso -- Chile Received November 3, 2009 / Accepted April 27, 2010
DOI: 10.2225/vol13-issue4-fulltext-4 How to reference this article

Mapping aluminum tolerance loci in cereals: A tool available for crop breeding

Claudio Inostroza-Blancheteau
Programa de Doctorado en Ciencias de Recursos Naturales,
Universidad de La Frontera,
Temuco, Chile

Braulio Soto
Centro de Genómica Nutricional Agro Acuícola
Unidad de Biotecnología de Plantas
Instituto de Investigaciones Agropecuarias
Temuco, Chile

Cristian Ibáñez#
Instituto de Biología Vegetal y Biotecnología
Universidad de Talca
Talca, Chile

Pilar Ulloa
Programa de Doctorado en Ciencias de Recursos Naturales
Universidad de La Frontera
Temuco, Chile  

Felipe Aquea
Facultad de Ciencias Biológicas
Pontificia Universidad Católica de Chile
Santiago, Chile

Patricio Arce-Johnson
Facultad de Ciencias Biológicas
Pontificia Universidad Católica de Chile
Santiago, Chile

Marjorie Reyes-Díaz*
Center of Plant, Soil Interaction and Natural Resources Biotechnology
Scientific and Technological Bioresource Nucleus
Universidad de La Frontera
Temuco, Chile

*Corresponding author

Present address: #Departamento de Biología, Facultad de Ciencias, Universidad de La Serena, La Serena, Chile.

Financial support: Fondecyt Project Nº11080231, C. Inostroza-Blancheteau was supported by a PhD fellowship from CONICYT-Chile and F. Aquea is supported by a Postdoctoral Project “Programa Bicentenario de Ciencia y Tecnología CONICYT Banco Mundial” PSD74 2006 and the Millennium Nucleus for Plant Functional Genomics (P06-009-F).

Keywords: ALMT1, aluminum tolerance, cereals, marker-assisted selection, organic acid.


AFLP: Amplified fragment length polymorphism
ALMT1: Aluminum Activated Malate Transporter 1
Alt: Al tolerance
GGT: graphical genotypes
HvAACT1: Hordeum vulgare Aluminum Activated Citrate Transporter 1
MAS: marker-assisted selection
MATE: multidrug and toxic compound extrusion
MM: Molecular markers
NILs: near isogenic lines
QTL: quantitative trait loci
RAPDs: Random Amplified Polymorphic DNAs
RFLP: Restriction Fragment length polymorphisms
SNP: Single Nucleotide Polymorphisms
SSR: Simple Sequence Repeats

Abstract   Reprint (PDF)

Aluminum (Al) toxicity is the main factor limiting crop productivity in acidic soils around the world. In cereals, this problem reduces crop yields by 30-40%. The use of DNA-based markers linked to phenotypic traits is an interesting alternative approach. Strategies such as molecular marker-assisted selection (MAS) in conjunction with bioinformatics-based tools such as graphical genotypes (GGT) have been important for confirming introgression of genes or genomic regions in cereals but also to reduce the time and cost of identifying them through genetic selection. These biotechnologies also make it possible to identify target genes or quantitative trait loci (QTL) that can be potentially used in similar crops to increase their productivity. This review presents the main advances in the genetic improvement of cereals for Al-tolerance.

Genetics of Al3+ tolerance in cereals
  • Molecular markers and marker-assisted selection applied to al-tolerance in cereals
    Genetic maps to improve Al-tolerance in cereals
    Concluding Remarks
    Figure 1
    Table 1
  • Aluminum (Al) is a light metal that makes up 7% of the earth’s crust, and is the third most abundant element after oxygen and silicon (Ma et al. 2001). Al is also one of the major factors that limits the productivity of acidic soils (Kochian, 1995) affecting almost 40% of soils used for agriculture around the world (Foy et al. 1978; Zheng et al. 1998; Delhaize et al. 2004). Most of the Al can be found in alumino silicates (Al2O3, SiO2) with only small amounts present in soluble forms in the rhizosphere. Acid soils (pH < 5) increase the phytotoxic levels of trivalent Al species (Al3+) whereas at higher pH other non-toxic forms such as Al(OH)2+ and Al(OH)2+ are more prevalent (Delhaize and Ryan, 1995). Al toxicity primarily affects the division and elongation of the root apex. When Al3+ penetrates into the roots, it binds to the negative charges of phospholipids in the plasma membrane leading to rigidification and disruption of membrane function and also enhancement of oxidative stress (Jones et al. 2006). These physiological changes in the root cell result in the poor uptake of nutrients and water that ultimately affect crop yields (Kochian, 1995; Ciamporová, 2002; Inostroza-Blancheteau et al. 2008). In response to Al stress, higher plants have evolved two main mechanisms to resist the effect of Al toxicity. The first is an exclusion mechanism in which Al is prevented from moving through the plasma membrane to the cytoplasm in the root cells (Kochian, 1995; Giaveno and Miranda, 2000). This is achieved by the secretion of organic acids from the radical apex to the rhizosphere which, in turn, modifies the pH and chelates the toxic Al3+ (Marschner, 1986; Miyasaka et al. 1989; Taylor, 1995; Degenhardt et al. 1998; Kinraide et al. 2005). The second mechanism involves chelation of Al by specific proteins, short-chain organic acids, phenolic compounds and tannins that can bind and form complexes with Al3+and subsequently compartmentalize it in the vacuole thus reducing Al-toxicity in the cell (Basu et al. 1994b; Jones, 1998; Jones and Ryan, 2004). In a species-specific manner, several studies have shown that there are differences in the type of organic acid involved in this Al3+ detoxification. For example, in Triticum aestivum (wheat), the organic acid involved in the Al exclusion mechanism is malate (Delhaize et al. 1993; Basu et al. 1994a; Ryan et al. 1995), in Fagopyrum esculentum (buckwheat) and Colocasia esculenta (taro) the organic acid uses is oxalate (Ma and Miyasaka, 1998, Zheng et al. 1998) whereas in Phaseolus vulgaris (snapbeans), Cassia tora (tora) and Zea mays (maize), citrate is employed (Miyasaka et al. 1991; Pellet et al. 1995; Ma et al. 1997; Piñeros et al. 2002). In Secale cereale (rye), exudation of both malate and citrate have been reported (Li et al. 2000). Citrate, malate and oxalate are organic acids with high affinity for Al3+ (Jones, 1998). Transport of these organic acids occurs via anionic channels, the opening of which may be activated by Al. Differences regarding the activation of these channels have been observed between tolerant and sensitive genotypes (Ryan et al. 1997; Zhang et al. 2001). The identification of a possible protein responsible for the transport of organic acids in wheat may indicate the existence of a new type of membrane transporter (Sasaki et al. 2004). This gene is called ALMT1 (Aluminum Activated Malate Transporter 1) and when expressed in transgenic rice seedlings and sensitive barley plants, ALMT1 activated malate exudation in roots (Delhaize et al. 2004). Recent studies in barley have identified another gene, HvAACT1 (Hordeum vulgare Aluminum Activated Citrate Transporter 1), which belongs to the multidrug and toxic compound extrusion family (MATE) and is responsible for citrate exudation in response to Al (Furukawa et al. 2007). Additionally, in Sorghum bicolor (sorghum) a MATE gene (SbMATE) was identified as an aluminum-activated citrate transporter (Magalhaes et al. 2007). The monogenic inheritance of genes encoding proteins responsible for transporting organic acids in cereals such as T. aestivum and Hordeum vulgare (barley) facilitates the prospects of improving these species for tolerance to Al in acidic soil. Knowledge of the molecular physiology of Al-tolerance and the genetics that control this trait, may allow significant advances in the development of tolerant varieties in sensitive cereals. Nevertheless, the complexity of this genetic control seems to vary among species. For instance, control of Al tolerance in Oryza sativa (rice) is polygenetic, thus making genetic improvement difficult for this trait (Nguyen et al. 2003). Although conventional breeding methods have been useful in identifying tolerant varieties of various crops (Riede and Anderson, 1996; Gallego and Benito, 1997; Tang et al. 2000), they do not guarantee per se an efficient transfer of these genes to other elite materials. Fortunately, it is possible to increase the efficiency of conventional breeding by combining it with marker-assisted selection (MAS) and gene mapping strategies, which reduces the costs and the selection time of developing Al-resistant varieties.

    Genetics of Al3+ tolerance in cereals

    The genetic control of Al tolerance has only been studied for a limited number of species of agronomic interest. In cereals such as T. aestivum, H. vulgare, S. cereale, S. bicolor and Avena sativa (oat), different members of the ALMT and MATE families have been found to control Al tolerance traits (Gallego and Benito, 1998; Raman et al. 2002; Miftahudin et al. 2002; Tang et al. 2002; Magalhaes et al. 2004; Nava et al. 2006). In T. aestivum, the major locus that defines Al tolerance has been mapped on the long arm of chromosome 4D (4DL), and has been mapped in many different segregating populations and is linked to known molecular markers (Luo and Derorak, 1996; Riede and Anderson, 1996; Rodríguez-Milla and Gustafson, 2001; Raman et al. 2005; Raman et al. 2008). Recently Ryan et al. (2009) identified a major locus on chromosome 4BL that accounts for 50% of the phenotypic variation in citrate efflux. This suggests that citrate could be acting as a second mechanism for Al resistance in T. aestivum (in conjunction with malate). This locus, Xcec, was mapped within 6.3 cM of the Simple Sequence Repeats (SSR) marker Xgwm495. Nevertheless, studies in the Atlas 66 cultivar of T. aestivum determined that not all genes were located on the 4DL chromosome suggesting that Al-tolerance is inherited polygenically in this cultivar (Berzonsky, 1992). Zhou et al. (2007) identified a minor quantitative trait loci (QTL) for Al tolerance in Atlas 66 on chromosome 3BL in a population of recombinant inbred lines derived from the Chisholm cultivar of T. aestivum. Raman et al. (2005) identified a major QTL on chromosome 4DL that accounts for approximately 55% of the genetic variation for Al-resistance (chromosome 4DL accounts for approximately 45% and chromosome 3BL accounts for approximately 11%) in this Atlas 66 cultivar. Recently, other genes that encode membrane transporters have been identified and characterized (Sasaki et al. 2004; Furukawa et al. 2007). These genes confer resistance to toxicity for Al in different cereals such as T. aestivum, H. vulgare, S. bicolor and other species (Table 1). Sasaki et al. (2004) identified a malate transporter, encoded by the major gene ALMT1, in near isogenic lines (NILs) of wheat. This gene might be constitutively expressed in both tolerant and sensitive genotypes although higher levels were observed in the plasma membrane of roots of ET8 lines (Al-tolerant). Location of this malate transporter was also confirmed by transiently-expressing ALMT1 fused to green fluorescent protein in onion epidermal cells and suspension cultured tobacco cells (Yamaguchi et al. 2005). In addition, heterologous expression of ALMT1 conferred Al-resistance to barley plants whereas, in O. sativa, the expression of this gene resulted in a significant increase in the efflux of Al-activated malate, but not in Al tolerance itself (Delhaize et al. 2004; Kikui et al. 2007). This may be due to the intrinsic properties of malate as this organic acid has a lower Al ion-chelating capacity in comparison to oxalate or citrate (Ma et al. 1998; Ma et al. 2001). ALMT1 cosegregates with Al tolerance in F2 and F3 populations derived from crossing isogenic T. aestivum lines (Sasaki et al. 2004; Zhou et al. 2007). In this way, genes that are differentially expressed between two NILs of wheat (Chisholm-T, tolerant and Chisholm-S, sensitive) have also been identified using suppression subtractive hybridization libraries. In this case, root tips from plants exposed during seven days to different Al concentrations were compared with non-treated control plants. Of a total of 1065 possible genes, 57 were differentially expressed during the first Al exposure period. Among these, 28 genes, including ALMT1, ent-kaurenoic, β-glucosidase, lectin, histidine kinase and phosphoenolpyruvate carboxylase, exhibited high amounts of transcripts in Chisholm-T, thus correlating with Al tolerance (Guo et al. 2007). These results suggest that Al-tolerance can be co-regulated not only by specific genes (such as ALMT1) but also by multiple genes with diverse functions in the plant. In addition, recent research using microarrays and NILs of wheat, identified 83 candidate genes associated with Al stress, such as pyruvate dehydrogenase, alternative oxidase and galactonolactone oxidase. In addition, 25 candidate genes which correlate with Al tolerance were identified, including ALMT1 as well as some unexpected genes such as glutathione S-transferase, germin/oxalate oxidase, fructose 1.6-bisphosphatase, cysteine-rich proteins, cytochrome P450 monooxygenase, cellulose synthase, zinc finger transcription factor, disease resistance response protein and F-box containing domain proteins (Houde and Oury Diallo, 2008), although no direct relation among them and the Al-resistance phenotype was established.

    ALMT1, the most recurrent gene observed in Al-tolerant T. aestivum cultivars is 3968 bp long, and is composed of six exons with a coding region of 1388 bp (Raman et al. 2005). The first 1000 base pairs upstream of the ALMT1 coding region is more variable, and six different patterns or alleles have been distinguished (Types I to VI). Moreover, all non Japanese cereal cultivars correlated positively with different levels of Al resistance (Sasaki et al. 2006). In addition, Raman et al. (2006) identified molecular markers targeting insertions/deletions (indels) within the intron-3 region of the ALMT1 gene. These ALMT1-SSR3a and ALMT1-SSR3b markers exhibited complete co-segregation with Al-resistance and malate efflux. Thus, these markers located in an intron and in the promoter region of TaALMT1 are useful tools to monitor the inheritance of the Al tolerance locus within specific T. aestivum populations.

    Recently, in H. vulgare, a dominant gene for Al tolerance (named Alt) has been mapped by amplified fragment length polymorphism (AFLP) and restriction fragment length polymorphisms (RFLP) markers. RFLP analysis has located this gene on the long arm of chromosome 4H (4HL), 2.1 cM proximally from the Xbcd1117 marker and 2.1 cM distal from the Xwg464 and the Xcdo1395 markers (Tang et al. 2000; Raman et al. 2002). On the other hand, Wang et al. (2007) using a high resolution map, identified the Alp locus, which is very close (0.2 cM) to the ABG715 and HvGABP markers. In addition, using double haploid and F2 populations from crosses between Dayton (tolerant) and elite sensitive cultivars, the HvMATE gene was identified as a gene belonging to the MATE family, which accounts for the Al tolerance in barley. In this same species, Furukawa et al. (2007) using both mapping and microarray analyses, identified the same gene (HvAACT1) in the Al-tolerant cultivar Murasakimochi. The gene product is responsible for citrate exudation and it is activated by Al. In this same study, a very high correlation was observed between HvAACT1 expression and citrate secretion in 10 H. vulgare cultivars with differing Al tolerance. Thus HvAACT1, as an Al-activated citrate transporter, is responsible for Al tolerance in H. vulgare (Furukawa et al. 2007). In other studies performed in rye, the most Al-tolerant cereal, four different genes related to Al-tolerance (Alt1, Alt2, Alt3 and Alt4) were discovered. These genes are located on chromosome 6RS, 3RS, 4RL and 7RS, respectively (Ma et al. 2000; Aniol, 2004; Fontecha et al. 2007; Matos et al. 2007). Another Al-tolerant species is X Triticosecale Wittmack (triticale), a hybrid resulting from the cross between T. aestivum and S. cereale. This cereal contains a complete genome copy of the rye chromosomes (AABBRR) that has given it the potential to grow and produce high yields in marginal soils such as those containing toxic levels of Al (Kim et al. 2001). Al tolerance was analyzed in two sets of hexaploid X Triticosecale Wittmack lines with disomic substitution of the D-genome of the T. aestivum chromosome. Of 20 substitution lines developed in winter X Triticosecale Wittmack (Presto) and 18 lines generated in spring X Triticosecale Wittmack (Rhino), six (30%) and nine (50%) lines, respectively, showed an increase in Al tolerance when they were compared with control lines (Budzianowski and Wos, 2004).

    Based on relative root growth (RRG) and mapping approaches, several QTLs for Al-tolerance have been identified in O. sativa. The lines were derived from crosses between the Al-tolerant Asominori and the Al-sensitive IR24 cultivars. The qRRE-1, qRRE-9 and qRRE-11 QTLs were detected on chromosomes 1, 9 and 11, respectively and the phenotypic variance ranged between 13.5% and 17.7% (Xue et al. 2006; Xue et al. 2007). The alleles of the Asominori cultivar from these three QTLs were all associated with an increase in Al tolerance. qRRE-9 was expressed in the genetic backgrounds of both IR24 and Asominori/IR24 (Xue et al. 2007). On the other hand, for two of the Al-tolerant sorghum cultivars, a unique locus named AltSB has been found to control this trait (Magalhaes et al. 2004). This locus might result in Al-tolerance through citrate exudation from roots. Consequently, by using positional cloning, a MATE gene conferring Al-tolerance in S. bicolor, has been identified (Magalhaes et al. 2007). Hoekenga et al. (2003) identified two major loci in Arabidopsis thaliana (arabidopsis), which account for approximately 40% of the phenotypic variance in Al tolerance observed among recombinant inbred lines derived from Landsberg erecta (sensitive) and Columbia (tolerant) ecotypes.

    Molecular markers and marker-assisted selection applied to Al-tolerance in cereals

    Molecular markers (MM) play an important role in the identification of desirable genes or alleles enabling genotype improvement. They also allow the structure and organization of the entire genome to be studied, as well as the physical mapping of BAC clones (Somers, 2004). In recent years, different dominant and co-dominant marker systems have been used. The dominant markers include Random Amplified Polymorphic DNAs (RAPDs) and Amplified Fragment Length Polymorphisms (AFLPs), whereas Restriction Fragment Length Polymorphisms (RFLPs), Simple Sequence Repeats (SSRs) and Single Nucleotide Polymorphisms (SNPs) are codominant markers. These markers have been developed for use with a range of crop species including cereals (Korzun, 2002; Korzun, 2003). Each type of molecular marker presents advantages and disadvantages. For instance, MMs based on PCR such as RAPDs, AFLPs, SSRs and SNPs require very small amounts of DNA, and are fast and easy to use, which facilitates the process of genotyping (Somers, 2004; Chao, 2006). On the other hand, other MMs such as RFLPs require large amounts of highly purified DNA, making the process more laborious. The Polymorphic Information Content (PIC), which gives account of the resolution power of a MM to distinguish different genotypes within populations, is another important feature of MMs. Currently, AFLPs and SSRs are the most popular MMs used in cereals because they provide a suitable genome coverage and PIC, respectively, at a reasonable cost. Nevertheless, with the advent of economically viable sequencing projects in model and economically important plants, SNP markers that represent sequence polymorphisms occurring at the single nucleotide level between varieties of the same species will be the markers of choice (Gupta et al. 2001). Using the current knowledge of SNP markers in cereals, it is possible to implement a high-throughput approach based on oligonucleotide arrays. The polymorphisms discovered from array hybridizations have been referred to as Single Feature Polymorphisms (SFPs) (Borevitz et al. 2003). Array-based SFP detection has been applied to several plant species including H. vulgare (Rostoks et al. 2005), O. sativa (Kumar et al. 2007), Solanum lycopersicum (tomato) (Sim et al. 2009) and Vigna unguiculata (cowpea) (Das et al. 2008). SFP discovery using an oligonucleotide array would be an efficient way to develop a large number of markers that may be used for high-resolution genetic mapping and marker-assisted breeding.

    The widespread use of DNA polymorphisms along with the growing technology of MMs has had a significant impact on plant improvement with regards to genetic diversity and genotyping studies, linkage map construction, trait tagging, gene cloning, and Marker-Assisted Selection (MAS). The MAS procedure is based on the concept of genetic linkage between two loci located close together on the same chromosome, resulting in co-inheritance or co-transmission to the progeny. Thus, by identifying the genotype of a specific marker, the phenotype of a linked locus might be deduced (Stam, 2003). The application of MMs for the selection of superior genotypes in plant breeding is most beneficial for those traits that are difficult to select phenotypically, are subject to high experimental error, or are expensive to assess (Kuchel et al. 2007), such as Al resistance. Since one of the aims of plant breeding is the introgression of one or more favorable alleles from a donor line into an elite variety, MAS enables the breeder to accelerate the recovery of the elite or recurrent parent genome (RPG) by backcrossing where only few rounds are necessary to introgress the target gene. Reductions in the time and expense of the whole process are additional positive aspects of MAS (Frisch et al. 1999; Tang et al. 2005). Comparison between conventional improvement and MAS are shown in Figure 1. Perhaps one of the most studied species regarding Al resistance is wheat. Riede and Anderson, (1996) established the association between the RFLP marker bcd1230 and the Al tolerance gene (AltBH) on 4DL at 1.1 cM. Subsequently, this information allowed SSR markers to be linked, which have facilitated the identification and introgression of this gene. Thus, the SSR markers WMC331, WMC457 and GWM165 have been tightly linked to the ALMT1 gene in different Al tolerant cultivars (Ma et al. 2004; Inostroza-Blancheteau et al. 2005; Raman et al. 2005; Zhou et al. 2007). By cloning the ALMT1 gene and analyzing the promoter region, Sasaki et al. (2004) and Sasaki et al. (2006) designed the marker ALMT1-4, which was used to identify six different alleles correlating 100% with levels of Al tolerance. In rye, efforts to identify MMs useful for the selection of Al tolerant genotypes have been reported by Gallego et al. (1998) using the SCAR markers ScR01600 and ScB157900, linked at 2.1 and 5.5 cM from the Alt1 locus, respectively. On the other hand, Collins et al. (2008) showed that the Alt4 Al-tolerance locus identified in the M39A-1-63/M77A-1 cross is located on the short arm of rye chromosome 7R. This agrees with the claim by Benito et al. (2005) that this locus was on 7RS, but disagrees with the chromosome 4R location originally determined by Miftahudin et al. (2002). The identification of an Alt locus on 4R has been recently reported by Benito et al. (2010). Matos et al. (2005) linked the RAPD markers SCIM8111376, SCIM812626, SCIM8121138 to the Alt4 locus. Using primers designed against the wheat TaALMT1 gene, Fontecha et al. (2007) amplified, cloned and sequenced an ALMT1 gene in rye located on chromosome 7RS that they named ScALMT1. Polymorphisms detected by SNP markers for this gene were detected among the parents of three F2 rye populations for the Alt4 locus. In H. vulgare, the most sensitive species of the Triticeae family, SSR markers such as Bmag353, Bmac310, HVM68, HVMCABG and ABG715 have been identified that are closely linked to the HvMATE gene (Raman et al. 2002; Furukawa et al. 2007; Wang et al. 2007) and represent a good set of putative molecular markers for use in identifying Al-tolerant plants. In diploid Avena strigosa (oat), RFLP markers linked to Al-tolerance have been identified through comparative mapping and QTL analysis, indicating that these QTLs are orthologous for Al-tolerance in other species (Wight et al. 2006).

    Currently, the availability of gene sequences related to Al tolerance have enabled the cloning of genes with similar functions in different cereals such as Triticum urartu (wheat), Aegilops speltoides (goatgrass), A. sativa, Z. mays and P. vulgaris, all sharing at least 72.3% similarity with the TaALMT1 sequences (Jardim, 2007). The knowledge of these sequences will substantially improve the potential to develop polymorphic molecular markers and apply them for breeding.

    Genetic maps to improve Al-tolerance in cereals

    A major use of MMs in cereals is for constructing genetic maps by analyzing the co-segregation of markers and traits in defined populations (Korzun, 2002). Genetic maps match the positioning of markers in different linkage groups or chromosomes based on the percentage of genetic recombination that exists between two loci or markers observed in a segregating population (Dear, 2002). Since map distances are somewhat additive, the combination of distances for various genes or genetic marker loci for assembling maps is possible, so that the order of these genes/marker loci along chromosomes can be elucidated and therefore genetic maps can be constructed. Although genetic maps are crucial in the localization of genes and the estimation of the proportion of parental genomes present in the progenies, it is difficult to visualize simultaneously the whole genome for hundreds of plants and MMs across backcross populations. Fortunately, van Berloo, (1999) designed the software named Graphical Genotype (GGT) which allows the rapid visualization of molecular marker data in a user-friendly color format. The GGT concept was described by Young and Tanksley, (1989), and it has speeded up the modern genetic improvement for Al tolerance in cereals (Figure 1). Currently, the availability of well-saturated genetic maps facilitates the introgression of Al resistance in many cereals. For instance, a genetic map for wheat based on SSR markers has been developed (Röder et al. 1998; Gupta et al. 2002; Somers et al. 2004), and used to associated markers to the TaALMT1 gene on 4DL (Raman et al. 2005; Zhou et al. 2007; Cai et al. 2008). In H. vulgare, genetic maps based on SSR markers are also available (Liu et al. 1996; Ramsay et al. 2000). These maps have led to the localization of the HvMATE gene on 4H (Tang et al. 2000; Raman et al. 2002; Ma et al. 2004; Furukawa et al. 2007; Wang et al. 2007). More recently, a linkage map was developed in rye where locus Alt4 and the ScALMT1 gene for Al tolerance were located on chromosome 7R (Matos et al. 2005; Matos et al. 2007). In addition, several QTLs have been mapped in O. sativa (Nguyen et al. 2003) and Z. mays (Ninamango-Cardenas et al. 2003) which account for the Al tolerance observe in segregating populations. Today this valuable information could propel breeding programs around the world in order to satisfy the current demands for new Al tolerant cultivars of crops and cereals.

    Concluding Remarks

    Conventional plant breeding is primarily based on the phenotypic selection of superior individuals among segregating populations. Although significant progress has been made in crop improvement through phenotypic selection, considerable difficulties are encountered during this process. The problem of genotype-environment interactions might generate unreliable data or expensive field experiments due to the nature of the target trait, for example, evaluation of abiotic stress such as Al toxicity.

    In the last 20 years, advances in molecular plant biology and more recently, in plant genomics have generated what some scientists call the new Green Revolution (Dubcovsky, 2004), which has lead to the development of molecular markers, genetic linkage maps and comparative mapping among related species such as T. aestivum, H. vulgare, S. cereale and O. sativa. This allows a much better understanding of their genomic organization, gene functions and helps to identify homologous genes with the same or similar effect, thus simplifying their cloning and fine mapping, and facilitating the application of marker (gene) assisted selection. The recent cloning of TaALMT1 (Sasaki et al. 2004) and HvAACT1 (Furukawa et al. 2007) that control the exudation of malate and citrate in Al-stressed T. aestivum and H. vulgare, respectively, are examples of these useful marker-trait associations. However, studies detailing successful implementation of molecular markers in pragmatic breeding programs are limited and they are often restricted to examples where the selection has focused on only one or two traits at a time (Kuchel et al. 2007). The current molecular information available regarding TaALMT1, AtALMT1, HvAACT1, ScALMT1 and ZmALMT1 and well-known in wheat, A. thaliana, H. vulgare, S. cereale and Z. mays Al-tolerant germoplasm, making it possible to generate new Al-tolerant varieties. Moreover, exploiting wild relatives or by using landraces as donor alleles would allow researchers and breeders to take advantage of polymorphisms between parent lines, identifying easily the target gene and the undesirable genomic regions coming from the donor parent, by using current molecular markers in conjunction with currently-available linkage maps.

    In conclusion, the next step should be the application of this knowledge in pragmatic breeding programs to overcome the Al toxicity problem in crops worldwide. Complementation between molecular technologies and conventional breeding is a crucial step for developing comprehensive research strategies aimed towards more efficient crop improvement in the near future (Figure 1). With the current rate of human population growth, cultivation of acidic soils will soon be necessary to satisfy the increasing food demand around the world. This issue concerns all important economic crops, therefore the extrapolation of the advances achieved in related species using genomic approaches, comparative mapping and bioinformatics, will be vital to accelerate the production of superior varieties for Al toxicity and other important traits.


    The authors would like to thank J. Larraín-Linton, Loreto Muñoz and Michael Handford for their assistance in language support.


    ANIOL, A. Chromosomal location of aluminum tolerance genes in rye. Plant Breeding, April 2004, vol. 123, no. 2, p. 132-136. [CrossRef]

    BASU, U.; GODBOLD, D. and TAYLOR, G.J. Aluminum resistance in Triticum aestivum associated with enhanced exudation of malate. Journal of Plant Physiology, May 1994a, vol. 144, no. 6, p. 747-753.

    BASU, U.; BASU, A. and TAYLOR, G.J. Differential exudation of polypeptides by roots of aluminum-resistant and aluminum-sensitive cultivars of Triticum aestivum L. in response to aluminum stress. Plant Physiology, September 1994b, vol. 106, no. 1, p. 151-158.

    BENITO, C.; FONTECHA, G.; SILVA-NAVAS, J.; HERNÁNDEZ-RIQUER, V.; EGUREN, M.; ESCRIBANO, R.M.; MESTRES, M.A. and GALLEGO, F.J. Chromosomal location of molecular markers linked to Aluminum tolerance genes in rye. In: International Triticeae Symposium. 2005 Prague, Czech Republic. p. 288.

    BENITO, C.; SILVA-NAVAS, J.; FONTECHA, G.; HERNÁNDEZ-RIQUER, M.V.; EGUREN, M.; SALVADOR, N. and GALLEGO, F.J. From the rye Alt3 and Alt4 aluminum tolerance loci to orthologous genes in other cereals. Plant and Soil, February 2010, vol. 327, no. 1-2, p. 107-120. [CrossRef]

    BERZONSKY, William A. The genomic inheritance of aluminum tolerance in “Atlas 66” wheat. Genome, August 1992, vol. 35, no. 4, p. 689-693.

    BOREVITZ, Justin O.; LIANG, David; PLOUFFE, David; CHANG, Hur-Song; ZHU, Tong; WEIGEL, Detlef; BERRY, Charles C.; WINZELER, Elizabeth and CHORY, Joanne. Large-scale identification of single-feature polymorphisms in complex genomes. Genome Research, March 2003, vol. 13, no. 3, p. 513-523. [CrossRef]

    BUDZIANOWSKI, Grzegorz and WOS, Henryk. The effect of single D-genome chromosomes on aluminum tolerance of triticale. Euphytica, May 2004, vol. 137, no. 2, p. 165-172. [CrossRef]

    CAI, Shibin; BAI, Gui-Hua and ZHANG, Dadong. Quantitative trait loci for aluminium resistance in Chinese wheat landrace FSW. Theoretical and Applied Genetics, June 2008, vol. 117, no. 1, p. 49-56. [CrossRef]

    CHAO, S. Application of molecular marker technologies on cereal crops improvement. In: American Oat Workers Conference. (23rd-25th July, 2006, Fargo, ND.,USA).

    CIAMPOROVÁ, M. Morphological and structural responses of plant roots to aluminum at organ, tissue and cellular levels. Biologia Plantarum, June 2002, vol. 45, no. 2, p. 161-171. [CrossRef]

    COLLINS, N.C.; SHIRLEY, N.J.; SAEED, M.; PALLOTTA, M. and GUSTAFSON, J.P. An ALMT1 gene cluster controlling Aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics, May 2008, vol. 179, no. 1, p. 669-682. [CrossRef]

    DAS, Sayan; BHAT, Prasanna R.; SUDHAKAR, Chinta; EHLERS, Jeffrey D.; WANAMAKER, Steve; ROBERTS, Philip A.; CUI, Xinping and CLOSE, Timothy J. Detection and validation of single feature polymorphisms in cowpea (Vigna unguiculata L. Walp) using a soybean genome array. BMC Genomics, February 2008, vol. 9, no. 107. [CrossRef]

    DEAR, P. Genome mapping: A practical approach. Oxford University Press, UK, 2002, 359 p. ISBN 0-19-963631-1.

    DEGENHARDT, Jörg; LARSEN, Paul; HOWELL, Stephen H. and KOCHIAN, Leon V. Aluminum resistance in the arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiology, May 1998, vol. 117, no. 1, p. 19-27. [CrossRef]

    DELHAIZE, E.; RYAN, P. and RANDALL, P. Aluminum tolerance in wheat (Triticum aestivum L.), II. Aluminum-Stimulated excretion of malic acid from root apices. Plant Physiology, November 1993, vol. 103, no. 3, p. 695-702.

    DELHAIZE, E. and RYAN, P.R. Aluminum toxicity and tolerance in plant. Plant Physiology, February 1995, vol. 107, no. 2, p. 315-321.

    DELHAIZE, Emmanuel; RYAN, Peter R.; HEBB, Diane M.; YAMAMOTO, Yoko; SASAKI, Takayuki and MATSUMOTO, Hideaki. Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proceedings of the National Academy of Sciences of the United States of America, October 2004, vol. 101, no. 42, p. 15249-15254. [CrossRef]

    DUBCOVSKY, Jorge. Marker-assisted selection in public breeding programs: The wheat experience. Crop Science, November 2004, vol. 44, no. 6, p. 1895-1898.

    FONTECHA, G.; SILVA-NAVAS, J.; BENITO, C.; MESTRES, M.A.; ESPINO, F.J.; HERNÁNDEZ-RIQUER, M.V. and GALLEGO, F.J. 2007. Candidate gene identification of an aluminum-activated organic acid transporter gene at the Alt4 locus for aluminum tolerance in rye (Secale cereale L.). Theoretical and Applied Genetics, January 2007, vol. 114, no. 2, p. 249-260. [CrossRef]

    FOY, C.D.; CHANEY, R.L. and WHITE, M.C. The physiology of metal toxicity in plants. Annual Review of Plant Physiology, June 1978, vol. 29, p. 511-566.

    FRISCH, Matthias; BOHN, Martin and MELCHINGER, Albrecht E. Comparison of selection strategies for markers assisted backcrossing of a gene. Crop Science, November 1999, vol. 39, no. 5, p. 1295-1301.

    FURUKAWA, Jun; YAMAJI, Naoki; WANG, Hua; MITANI, Namiki; MURATA, Yoshiko; SATO, Kazuhiro; KATSUHARA, Maki, TAKEDA, Kazuyoshi and MA, Jian Feng. An Aluminum-activated citrate transporter in barley. Plan Cell Physiology, August 2007, vol. 48, no. 8, p. 1081-1091. [CrossRef]

    GALLEGO, F. and BENITO, C. Genetic control of aluminum tolerance in rye (Secale cereale L.). TAG Theoretical and Applied Genetics, August 1997, vol. 95, no. 3, p. 393-399. [CrossRef]

    GALLEGO, F.J.; CALLES, B. and BENITO, C. Molecular markers linked to the aluminum tolerance gene Alt1 in rye (Secale cereale L). TAG Theoretical and Applied Genetics, November 1998, vol. 97, no. 7, p. 1104-1109. [CrossRef]

    GIAVENO, Carlos Daniel and MIRANDA, José B. Rapid screening for aluminum tolerance in maize (Zea mays L.). Genetics and Molecular Biology, December 2000, vol. 23, no. 4, p. 847-850. [CrossRef]

    GUO, P.; BAI, G.; CARVER, B.; LI, R.; BERNARDO, A. and BAUM, M. Transcriptional analysis between two wheat near-isogenic lines contrasting in aluminum tolerance under aluminum stress. Molecular Genetics and Genomics, January 2007, vol. 277, no. 1, p. 1-12.

    GUPTA, P.K.; ROY, J.K. and PRASAD, M. Single nucleotide polymorphisms: a new paradigm for molecular marker technology and DNA polymorphism detection with emphasis on their use in plants. Current Science, February 2001, vol. 80, no. 4, p. 524-535.

    GUPTA, P.; BALYAN, H.; EDWARDS, K.; ISAAE, P.; KORZUN, V.; RODER, M.; GAUTIER, M.; JOUDRIER, P.; SCHLATTER, A.; DUBCOVKY, J.; DE LA PEÑA, T.; KHAIRALLAH, M.; PENNER, G.; HAYDEN, M.; SHARP, P.; KELLER, B.; WANG, R.; HARDOUIN, J.; JACK, P. and LEROY, P. Genetic mapping of 66 new micro-satellite (SSR) loci in bread wheat. TAG Theoretical and Applied Genetics, August 2002, vol. 105, no. 2-3, p. 413-422. [CrossRef]

    HOEKENGA, Owen A.; VISION, Todd J.; SHAFF, Jom E.; MONFORTE, Antonio J.; LEE, Gung Pyo; HOWELL, Stephen H. and KOCHIAN, Leon V. Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiology, June 2003, vol. 132, no. 2, p. 936-948. [CrossRef]

    HOEKENGA, Owen A.; MARON, Lyza G.; PIÑEROS, Miguel A.; CANCADO, Geraldo M.A.; SHAFF, Jon; KOBAYASHI, Yuriko; RYAN, Peter R.; DONG, Bei; DELHAIZE, Emmanuel; SASAKI, Takayuki; MATSUMOTO, Hideaki; YAMAMOTO, Yoko; KOYAMA, Hiroyuki and KOCHIAN, Leon V. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, June 2006, vol. 103, no. 25, p. 9738-9743. [CrossRef]

    HOUDE, Mario and OURY DIALLO, Amadou. Identification of genes and pathways associated with aluminum stress and tolerance using transcriptome profiling of wheat near isogenic lines. BMC Genomics, August 2008, vol. 9, no. 400. [CrossRef]

    INOSTROZA-BLANCHETEAU, C.; SOTO, B.; PEÑALOZA, E. and SALVO-GARRIDO, H. Introgresión de genes que confieren tolerancia a aluminio (Al3+) en trigo Triticum aestivum L. In: Congreso Internacional de Biotecnología-Grupo Biotecnología. (VI, Simposio Nacional de Biotecnología. REDBIO-Argentina, 7-10 de Junio. Encuentro Trinacional REDBIO Argentina-Chile-Uruguay, Buenos Aires, Argentina, 2005. p. 269-270.

    INOSTROZA-BLANCHETEAU, Claudio; SOTO, Braulio; ULLOA, Pilar; AQUEA, Felipe and REYES-DÍAZ, Marjorie. Resistance mechanisms of aluminum (Al3+) phytotoxicity in cereals: physiological, genetic and molecular bases. Revista de la Ciencia del Suelo y Nutrición Vegetal, October 2008, vol. 8, no. 3, p. 57-71.

    JARDIM, S.N. Comparative genomics of grasses tolerant to aluminum. Genetics and Molecular Research, December 2007, vol. 6, no. 4, p. 1178-1189.

    JONES, David L. Organic acids in the rhizosphere - a critical review. Plant and Soil, August 1998, vol. 205, no. 1, p. 25-44. [CrossRef]

    JONES, D.L. and RYAN, P.R. Nutrition. Aluminum Toxicity. Encyclopedia of Applied Plant Science, October 2004, p. 656-664. [CrossRef]

    JONES, D.L.; BLANCAFLOR, E.B.; KOCHIAN, L.V. and GILROY, S. Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environment, April 2006, vol. 29, no. 7, p. 1309-1318. [CrossRef]

    KIKUI, Satoshi; SASAKI, Takayuki; OSAWA, Hiroki; MATSUMOTO, Hideaki and YAMAMOTO, Yoko. Malate enhances recovery from aluminum-caused inhibition of root elongation in wheat. Plant and Soil, January 2007, vol. 290, no .1-2, p. 1-15. [CrossRef]

    KIM, B.Y.; BAIER, A.C.; SOMERS, D.J. and GUSTAFSON, J.P. Aluminum tolerance in triticale, wheat, and rye. Euphytica, August 2001, vol. 120, no. 3, p. 329-337. [CrossRef]

    KINRAIDE, Thomas B.; PARKER, David R. and ZOBEL, Richard W. Organic acid secretion as a mechanism of aluminium resistance: a model incorporating the root cortex, epidermis, and the external unstirred layer. Journal of Experimental Botany, July 2005, vol. 56, no. 417, p. 1853-1865. [CrossRef]

    KOCHIAN, Leon V. Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Physiology and Plant Molecular Biology, June 1995, vol. 46, p. 237-260. [CrossRef]

    KORZUN, V. Use of molecular markers in cereal breeding. Cellular and Molecular Biology Letters, 2002, vol. 7, no. 2B, p. 811-820.

    KORZUN, V. Molecular markers and their applications in cereals 1 breeding. In: Markers Assisted Selection: A fast track to increase genetic gain in plant and animal breeding. Session I: MAS in plant, 2003, p. 18-22.

    KUCHEL, Haydn; FOX, Rebecca; REINHEIMER, Jason; MOSIONEK, Lee; WILLEY, Nicholas; BARIANA, Harbans and JEFFERIES, Stephen. The successful application of a marker-assisted wheat breeding strategy. Molecular Breeding, November 2007, vol. 20, no. 4, p. 295-308. [CrossRef]

    KUMAR, Rajesh; QIU, Jing; JOSHI, Trupti; VALLIYODAN, Babu; XU, Dong and NGUYEN, Henry T. Single feature polymorphism discovery in rice. PLoS One, March 2007, vol. 2, no. 3, e284. [CrossRef]

    LI, Xiao Feng; MA, Jian Feng and MATSUMOTO Hideaki. Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiology, August 2000, vol. 123, no. 4, p. 1537-1543. [CrossRef]

    LIGABA, Ayalew; KATSUHARA, Maki; RYAN, Peter R.; SHIBASAKA, Mineo and MATSUMOTO, Hideaki. The BnALMT1 and BnALMT2 genes from Brassica napus L. encode aluminum-activated malatetransporters that enhance the aluminum resistance of plant cells. Plant Physiology, November 2006, vol. 142, no. 3, p. 1294-1303. [CrossRef]

    LIU, Jiping; MAGALHAES, Jurandir V.; SHAFF, Jon and KOCHIAN, Leon V. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. The Plant Journal, February 2008, vol. 57, no. 3, p. 389-399.[CrossRef]

    LIU, Z.; BIYASHEV, R. and SAGHAI MARROF, M. Development of simple sequence repeat DNA markers and their integration into a barley linkage map. TAG Theoretical and Applied Genetics, October 1996, vol. 93, no. 5-6, p. 869-876. [CrossRef]

    LUO, M.C. and DVORAK, J. Molecular mapping of an aluminum tolerance locus on chromosome 4D of Chinese Spring wheat. Euphytica, January 1996, vol. 91, no. 1, p. 31-35. [CrossRef]

    MA, Jian Feng; ZHENG, Shao Jian and MATSUMOTO, Hideaki. Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiology, 1997, vol. 38, no. 9, p. 1019-1025.

    MA, Jian Feng; TAKETA, Shin and YANG, Zhen Ming. Aluminum tolerance genes on the short arm of chromosome 3R are linked to organic acid release in triticale. Plant Physiology, March 2000, vol. 122, no. 3, p. 687-694. [CrossRef]

    MA, Jian Feng; RYAN, Peter R. and DELHAIZE, Emmanuel. Aluminum tolerance in plants and the complexing role of organic acids. Trends in Plant Science, June 2001, vol. 6, no. 6, p. 273-278. [CrossRef]

    MA, Jian Feng; NAGAO, Sakiko; SATO, Kazuhiro; ITO, Hiroyuki; FURUKAWA, Jun and TAKAEDA, Kazuyoshi. Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley. Journal of Experimetal Botany, June 2004, vol. 55, no. 401, p. 1335-1341. [CrossRef]

    MA, Zhong and MIYASAKA, Susan C. Oxalate exudation by taro in response to Al. Plant Physiology, November 1998, vol. 118, no. 3, p. 861-865. [CrossRef]

    MAGALHAES, Jurandir V.; GARVIN, David F.; WANG, Yihong; SORRELLS, Mark E.; KLEIN, Patricia E.; SHAFFERT, Robert E.; LI, Li and KOCHIAN, Leon V. Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the poaceae. Genetics, August 2004, vol. 167, no. 4, p. 1905-1914. [CrossRef]

    MAGALHAES, Jurandir V.; LIU, Jiping; GUIAMARAES, Claudia T.; LANA, Ubiraci G.P.; ALVES, Vera M.C.; WANG, Yi-Hong; SHAFFERT, Robert E.; HOEKENGA, Owen A.; PIÑEROS, Miguel A.; SHAFF, Jon E.; KLEIN, Patricia A.; CARNEIRO, Newton P.; COELHO, Cintia M.; TRICK, Harold N. and KOCHIAN, Leon V. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genetics, September 2007, vol. 39, no. 9, p. 1156-1161. [CrossRef]

    MARSCHNER, H. Mineral nutrition of higher plants. Academic Press, London, UK., 1986. 657 p. ISBN 0-12473543-6.

    MATOS, M.; CAMACHO, M.V.; PÉREZ-FLORES, V.; PERNAUTE, B. and PINTO-CARNIDE, O. A new aluminum tolerance gene located on rye chromosome arm 7RS. TAG Theoretical and Applied Genetics, July 2005, vol. 111, no. 2, p. 360-369. [CrossRef]

    MATOS, M.; PÉREZ-FLORES, V.; CAMACHO, M.V.; PERNAUTE, B.; PINTO-CARNIDE, O. and BENITO, C. Detection and mapping of SSRs in rye ESTs from aluminum-stressed roots. Molecular Breeding, September 2007, vol. 20, no. 2, p. 103-115. [CrossRef]

    MIFTAHUDIN, J.; SCOLES, G. and GUSTAFSON, J.P. AFLP markers tightly linked to the aluminum-tolerance gene Alt3 in rye (Secale cereale L.). TAG Theoretical and Applied Genetics, March 2002, vol. 104, no. 4, p. 626-631. [CrossRef]

    MIYASAKA, Susan C.; KOCHIAN, Leon V.; SHAFF, Jon E. and FOY, Charles D. Mechanisms of aluminium tolerance in wheat. An investigation of genotypic differences in rhizosphere pH, K+ and H+ transport, and root cell membranes potentials. Plant Physiology, November 1989, vol. 91, no. 3, p. 1188-1196. [CrossRef]

    MIYASAKA, Susan C.; BUTA, J. George; HOWELL, Robert K. and FOY, Charles D. Mechanism of aluminum tolerance in snapbeans. Root exudation of citric acid. Plant Physiology, July 1991, vol. 96, no. 3, p. 737-743. [CrossRef]

    NAVA, Itamar C.; DELATORRE, Carla A.; DE LIMA DUARTE, Ismael T.; PACHECO, Marcelo T. and FEDEREZZI, Luiz C. Inheritance of aluminum tolerance and its effects on grain yield and grain quality in oats (Avena sativa L.). Euphytica, April 2006, vol. 148, no. 3, p. 353-358. [CrossRef]

    NGUYEN, Bay D.; BRAR, Darshan S.; BUI, Buu C.; NGUYEN, Tao V.; PHAM, Luong N. and NGUYEN, Henry T. Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff, into indica rice (Oryza sativa L.). TAG Theoretical and Applied Genetics, February 2003, vol. 106, no. 4, p. 583-593. [CrossRef]

    NINAMANGO-CÁRDENAS, Fernando E.; TEIXEIRA GUIMARÃES, Claudia; MARTINS, Paulo R.; PARENTONI, Sidney N.; CARNEIRO, Newton P.; LOPEZ, Mauricio A.; MORO, Jose Roberto and PAIVA, Edilson. Mapping QTLs for aluminum tolerance in maize. Euphytica, March 2003, vol. 130, no. 2, p. 223-232. [CrossRef]

    PELLET, Didier M.; GRUNES, David L. and KOCHIAN, Leon V. Organic acid exudation as an aluminium tolerance mechanism in maize (Zea mays L.). Planta, July 1995, vol. 196, no. 4, p. 788-795.[CrossRef]

    PIÑEROS, Miguel A.; MAGALHAES, Jurandir V.; CARVALHO, Vera M. and KOCHIAN, Leon V. The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiology, July 2002, vol. 129, no. 3, p. 1194-1206.

    RAMAN, H.; MORONI, J.S.; SATO, K.; READ, B.J. and SCOTT, B.J. Identification of AFLP and micro-satellite markers linked with an aluminum tolerance gene in barley (Hordeum vulgare L.). TAG Theoretical and Applied Genetics, August 2002, vol. 105, no. 2-3, p. 458-464. [CrossRef]

    RAMAN, Harsh; ZHANG, Kerong; CAKIR, Mehmet; APPELS, Rudi; GARVIN, David F.; MARON, Lyza G.; KOCHIAN, Leon V.; MORONI, J. Sergio; RAMAN, Rosy; IMTIAZ, Muhammad; DRAKE-BROCKMAN, Fiona; WATERS, Irene; MARTIN, Peter; SASAKI, Takayuki; YAMAMOTO, Yoko; MATSUMOTO, Hideaki; HEBB, Diane M.; DELHAIZE, Emmanuel and RYAN, Peter R. Molecular characterization and of ALMT1, the aluminum-tolerance gene of bread wheat (Triticum aestivum L.). Genome, October 2005, vol. 48, no. 5, p. 781-791.

    RAMAN, Harsh; RAMAN, Rosy; WOOD, Rachel and MARTIN, Peter. Repetitive indel markers within the ALMT1 gene conditioning aluminum tolerance in wheat (Triticum aestivum L.). Molecular Breeding, September 2006, vol. 18, no. 2, p. 171-183. [CrossRef]

    RAMAN, Harsh; RYAN, Peter R.; RAMAN, Rosy; STODART, Benjamin J.; ZHANG, Kerong; MARTIN, Peter; WOOD, Rachel; SASAKI, Takayuki; YAMAMOTO, Yoko; MACKAY, Michael; HEBB, Diane M. and DELHAIZE, Emmanuel. Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). TAG Theoretical and Applied Genetics, February 2008, vol. 116, no. 3, p. 343-354. [CrossRef]

    RAMSAY, L.; MACAULAY, M.; IVANISSEVICH, S.; MACLEAN, K.; CARDLE, L.; FULLER, J.; EDWARDS, K.; TUVESSON, S.; MORGANTE, M.; MASSARI, A.; MAESTRI, E.; MARMIROLI, N.; SJAKSTE, T.; GANAL, M.; POWELL, W. and WAUGH, R. A simple sequence repeat-based linkage map of barley. Genetics, December 2000, vol. 156, no. 4, p. 1997-2005.

    RIBAUT, Jean-Marcel and HOISINGTON, David. Marker-assisted selection: new tools and strategies. Trends in Plant Science, June 1998, vol. 3, no. 6, p. 236-239. [CrossRef]

    RIEDE, C. and ANDERSON, J. Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Science, July 1996, vol. 36, no. 4, p. 905-909.

    RÖDER, Marion; KORZUN, Victor; WENDEHAKE, Katja; PLASCHKE, Jens; TIXIER, Marie- Hélène;; LEROY, Philippe and GANAL, Martin. A microsatellite map of wheat. Genetics, August 1998, vol. 149, no. 4, p. 2007-2023.

    RODRÍGUEZ-MILLA, M.A. and GUSTAFSON, J.P. Genetic and physical characterization of chromosome 4DL in wheat. Genome, October 2001, vol. 44, no. 5, p. 883-892. [CrossRef]

    ROSTOKS, Nils; BOREVITZ, Justin O.; HEDLEY, Peter E.; RUSSELL, Joanne; MUDIE, Sharon; MORRIS, Jenny; CARDLE, Linda; MARSHALL, David F. and WAUGH, Robbie. Single-feature polymorphism discovery in the barley transcriptome. Genome Biology, May 2005, vol. 6, no. 6, r54. [CrossRef]

    RYAN, Peter; DELHAIZE, Emmanuel and RANDALL, Peter. Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta, March 1995, vol. 196, no. 1, p. 103-110.[CrossRef]

    RYAN, Peter; SKERRETT, Martha; FINDLAY, Geoffrey; DELHAIZE, Emmanuel and TYERMAN, Stephen. Aluminum activates an anion channel in the apical cells of wheat roots. Proceedings of the National Academy of Science of the United States of America, June 1997, vol. 94, no. 12, p. 6547-6552. [CrossRef]

    RYAN, Peter; RAMAN, Harsh; GUPTA, Sanjay; HORST, Walter and DELHAIZE, Emmanuel. A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiology, January 2009, vol. 149, no. 1, p. 340-351. [CrossRef]

    SASAKI, Takayuki; YAMAMOTO, Yoko; EZAKI, Bunichi; KATSUHARA, Maki; JU AHN Sung; RYAN, Peter R.; DELHAIZE, Emmanuel and MATSUMOTO, Hideaki. A wheat gene encoding an aluminum-activated malate transporter. The Plant Journal, March 2004, vol. 37, no. 5, p. 645-653. [CrossRef]

    SASAKI, Takayuki; RYAN, Peter R.; DELHAIZE, Emmanuel; HEBB, Diane M.; OGIHARA, Yasunari; KAWAURA, Kanako; NODA, Kazuhiro; KOJIMA, Toshio; TOYODA, Atsushi; MATSUMOTO, Hideaki and YAMAMOTO, Yoko. Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant and Cell Physiology, October 2006, vol. 47, no. 10, p. 1343-1354. [CrossRef]

    SIM, Sung-Chur; ROBBINS, Matthew D.; CHILCOTT, Charles; ZHU, Tong and FRANCIS, David M. Oligonucleotide array discovery of polymorphisms in cultivated tomato (Solanum lycopersicum L.) reveals patterns of SNP variation associated with breeding. BMC Genomics, October 2009, vol. 10, p. 466. [CrossRef]

    SOMERS, D.J. Molecular marker systems and their evaluation for cereal genetics. In: GUPTA, P.K. and VARSHNEY, R.K. eds. Cereal genomics. Kluwer Academic Publishing, 2004. p. 19-34.

    SOMERS, Daryl; ISAAC, Peter and EDWARDS, Keith. A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). TAG Theoretical and Applied Genetics, October 2004, vol. 109, no. 6, p. 1105-1114. [CrossRef]

    STAM, P. Marker-assisted introgression: Speed at any cost? Eucarpia Leafy Vegetables, 2003 [cited June 7 2009]. Available from Internet:

    TANG, Y.; SORRELLS, M.; KOCHIAN, L.V. and GARVIN, D. Identification of RFLP markers linked to the barley aluminum tolerance gene Alp. Crop Science, May 2000, vol. 40, no. 3, p. 778-782.

    TANG, Y.; GARVIN, D.; KOCHIAN, L.V.; SORRELLS, M. and CARVER, F. Physiological genetics of aluminum tolerance in the wheat cultivar Atlas 66. Crop Science, September 2002, vol. 42, no. 5, p. 1541-1546.

    TANG, Qilin; RONG, Tingzhao; SONG, Yunchun; YANG, Junpin; PAN, Guangtang; LI, W.; HUANG, Yubi and CAO, Moju. Introgression of perennial teosinte genome into maize and identification of genomic in situ hybridization and microsatellite markers. Crop Science, March 2005, vol. 45, no. 2, p. 717-721.

    TAYLOR, Gregory J. Overcoming barriers to understanding the cellular basis of aluminium resistance. Plant and Soil, April 1995, vol. 171, no. 1, p. 89-103. [CrossRef]

    VAN BERLOO, R. GGT: software for the display of graphical genotypes. Journal of Heredity, March 1999, vol. 90, no. 2, p. 328-329. [CrossRef]

    WANG, Junping; RAMAN, Harsh; ZHOU, Meixue; RYAN, Peter; DELHAIZE, Emmanuel; HEBB, Diane M.; COOMBES, Neil and MENDHAM, Neville. High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminum tolerance in barley (Hordeum vulgare L.). TAG Theoretical and Applied Genetics, July 2007, vol. 115, no. 2, p. 265-276. [CrossRef]

    WIGHT, C.P.; KIBITE, S.; TINKER, N.A. and MOLNAR, J.S. Identification of molecular markers for aluminum tolerance in diploid oat through comparative mapping and QTL analysis. TAG Theoretical and Applied Genetics, January 2006, vol. 112, no. 2, p. 222-231. [CrossRef]

    XUE, Y.; WAN, J.M.; JIANG, L.; LIU, L.; SU, N.; ZHAI, H.Q. and MA, J.F. QTLs analysis of aluminum resistance in rice (Oryza sativa L.). Plant and Soil, September 2006, vol. 287, no. 1-2, p. 375-383. [CrossRef]

    XUE, Y.; JIANG, L.; SU, N.; WANG, J.K.; DENG, P.; MA, J.F.; ZHAI, H.Q. and WAN, J.M. The genetic basic and fine-mapping of a stable quantitative-trait loci for aluminum tolerance in rice. Planta, August 2007, vol. 227, no. 1, p. 255-262. [CrossRef]

    YAMAGUCHI, Mineo; SASAKI, Takayuki; SIVAGURU, Mayandi; YAMAMOTO, Yoko; OSAWA, Hiroki; JU AHN, Sung and MATSUMOTO, Hideaki. Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). Plant and Cell Physiology, May 2005, vol. 46, no. 5, p. 812-816. [CrossRef]

    YOUNG, N.D. and TANKSLEY, S.D. Restriction fragment length polymorphism maps and the concept of graphical genotypes. Theoretical and Applied Genetics, January 1989, vol. 77, no. 1, p. 95-101. [CrossRef]

    ZHANG, Wen-Hao; RYAN, Peter and TYERMAN, Stepehn D. Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. Plant Physiology, March 2001, vol. 125, no. 3, p. 1459-1472. [CrossRef]

    ZHENG, Shao Jian; MA, Jian Feng and MATSUMOTO, Hideaki. High aluminum resistance in buckwheat. I. Al induced specific secretion of oxalic acid from root tips. Plant Physiology, July 1998, vol. 117, no. 3, p. 745-751. [CrossRef]

    ZHOU, Li-Li; BAI, Gui-Hua; MA, Hong-Xiang and CARVER, Brett F. Quantitative trait loci for aluminium resistance in wheat. Molecular Breeding, February 2007, vol. 19, no. 2, p. 153-161. [CrossRef]

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