Genetic Dissection of Aluminium Tolerance in the Triticeae


Aluminium (Al) toxicity is the major constraint to crop productivity on acidic soils worldwide. Members of the Triticeae such as wheat, barley, and rice, show a range of genetic variation within and between species. Among key cereals, rye displays the maximum level of Al tolerance, while barley shows the least. In the majority of species, genetic control for aluminium tolerance has been investigated using conventional genetic and molecular analyses. During the last decade, candidate and causative genes and mechanisms for Al tolerance have been identified in wheat, barley, rice and sorghum. New phenotypic and genotyping platforms were also developed in order to understand genes and their networks underlying Al tolerance comprehensively. In this chapter, we review the progress made on recent discoveries on genetic dissection of aluminium tolerance with special focus on wheat, barley, and rice.


  1. Akhunov ED, Goodyear AW, Geng S et al (2003) The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms. Genome Res 13:753–763PubMedGoogle Scholar
  2. Altshuler D, Pollara VJ, Cowles CR et al (2000) An SNP map of the human genome genome generated by reduced representation shotgun sequencing. Nature 407:513–516PubMedGoogle Scholar
  3. Baier AC, Somers DJ, Gustafson JP (1995) Aluminium tolerance in wheat: correlating hydroponic evaluations with field and soil performances. Plant Breed 114:291–296Google Scholar
  4. Baird NA, Etter PD, Atwood TS et al (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:e3376PubMedCentralPubMedGoogle Scholar
  5. Benito C, Silva-Navas J, Fontecha G et al (2009) From the rye Alt3 and Alt4 aluminum tolerance loci to orthologous genes in other cereals. Plant Soil 327:107–120Google Scholar
  6. Bennet RJ (1997) The response of lucerne and red clover roots to aluminium/Hematoxylin: How universal is the hematoxylin test for aluminium? S Afr J Plant Soil 14:120–125Google Scholar
  7. Berzonsky WA (1992) The genomic inheritance of aluminium tolerance in ‘Atlas 66’ wheat. Genome 35:689–693Google Scholar
  8. Bona L, Wright RJ, Baligar VC, Matuz J (1993) Screening wheat and other small grains for acid soil tolerance. Landsc Urban Plan 27:175–178Google Scholar
  9. Buckler ES, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111PubMedGoogle Scholar
  10. Buckler ES, Holland JB, Bradbury PJ et al (2009) The genetic architecture of maize flowering time. Science 325:714–718PubMedGoogle Scholar
  11. Cai SB, Bai GH, Zhang DD (2008) Quantitative trait loci for aluminum resistance in Chinese wheat landrace FSW. Theor Appl Genet 117:49–56PubMedGoogle Scholar
  12. Camargo CEdO, Felicio JC, Ferreira F (1989) Wheat breeding: XXI. Evaluation of inbred lines in different regions of the state of São Paulo, Brazil. Bragantia 48:53–71Google Scholar
  13. Camargo CEdO, Filho F, Penteado AW et al (1992) Wheat breeding: XXVII. Variance, heritability and correlations in hybrid populations for grain yield, tolerance to aluminum toxicity and plant height. Bragantia 51:21–30Google Scholar
  14. Cançado GMA, Loguercio LL, Martins PR et al (1999) Hematoxylin staining as a phenotypic index for aluminum tolerance selection in tropical maize (Zea mays L.). Theor Appl Genet 99:747–754Google Scholar
  15. Carver BF, Whitmore WE, Smith EL, Bona L (1993) Registration of four aluminum-tolerant winter wheat germplasms and two susceptible near-isolines. Crop Sci 33:1113–1114Google Scholar
  16. Collins NC, Shirley NJ, Saeed M et al (2008) An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179:669–682PubMedGoogle Scholar
  17. Davey JW, Hohenlohe PA, Etter PD et al (2011) Genome-wide genetic marker discovery and genotyping using next generation sequencing. Nat Rev Genet 12:499–510PubMedGoogle Scholar
  18. Delhaize E, Craig S, Beaton CD et al (1993a) Aluminum tolerance in wheat (Triticum aestivum L.) I. Uptake and distribution of aluminum in root apices. Plant Physiol 103:685–693Google Scholar
  19. Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. PNAS 101: 15249–15254Google Scholar
  20. Delhaize E, Ryan PR, Randall PJ (1993b) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702Google Scholar
  21. Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Lett 581:2255–2262PubMedGoogle Scholar
  22. Delhaize E, James RA, Ryan PR (2012) Aluminium tolerance of root hairs underlies genotypic differences in rhizosheath size of wheat (Triticum aestivum) grown on acid soil. New Phytol 195:609–619PubMedGoogle Scholar
  23. Echart CL, Barbosa-Neto JF, Garvin DF et al (2002) Aluminum tolerance in barley: methods for screening and genetic analysis. Euphytica 126:309–313Google Scholar
  24. Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple Genotyping-by-Sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379PubMedCentralPubMedGoogle Scholar
  25. Famoso AN, Clark RT, Shaff JE et al (2010) Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol 153:1678–1691PubMedCentralPubMedGoogle Scholar
  26. Famoso AN, Zhao K, Clark RT et al (2011) Genetic architecture of aluminium tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet 7(8):e1002221PubMedCentralPubMedGoogle Scholar
  27. Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374PubMedGoogle Scholar
  28. Fontecha G, Silva-Navas J, Benito C et al (2007) Candidate gene identification of an aluminum-activated organic acid transporter gene at the Alt4 locus for aluminum tolerance in rye (Secale cereale L.). Theor Appl Genet 114:249–260PubMedGoogle Scholar
  29. Fujii M, Yamaji N, Sato K, Ma JF. 2009. Mechanism regulating HvAACT1 expression in barley. In: Liao H, Yan X, Kochian LV, eds. Plant–soil interactions at low pH: a nutriomic approach – Proceedings of the 7th International Symposium of Plant–Soil Interactions at Low pH. Guangzhou: South China University of Technology Press, 165–166.Google Scholar
  30. Fujii M, Yokosho K, Yamaji N et al (2012) Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun 3:713PubMedCentralPubMedGoogle Scholar
  31. Furukawa J, Yamaji N, Wang H et al (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091PubMedGoogle Scholar
  32. Gallego FJ, Benito C (1997) Genetic control of aluminium tolerance in rye (Secale cereale L.). Theor Appl Genet 95:393–399Google Scholar
  33. Gallego FJ, Calles B, Benito C (1998a) Molecular markers linked to the aluminium tolerance gene Alt1 in rye (Secale cereale L.). Theor Appl Genet 97:1104–1109Google Scholar
  34. Gallego FJ, Lopez-Solanilla ELÃ, Figueiras AM, Benito C (1998b) Chromosomal location of PCR fragments as a source of DNA markers linked to aluminium tolerance genes in rye. Theor Appl Genet 96:426–434Google Scholar
  35. Galvez L, Clark RB, Klepper LA, Hansen L (1991) Organic acid and free proline accumulation and nitrate reductase activity in sorghum (Sorghum bicolor) genotypes differing in aluminum tolerance. In: ‘Plant-Soil Interaction at Low PH’, Wright RJ, Baligar VC, Murrmann RP (eds) Kluwer Academic Publishers, Dordrecht, pp 859–867Google Scholar
  36. Garvin DF, Carver BF (2003) Role of the genotype in tolerance of acidity and aluminium toxicity. In: Rengel Z (ed) Handbook of soil acidity. Marcel Dekker, Inc., New York, pp 387–406Google Scholar
  37. Gourley LM, Rogers SA, Ruiz-Gomez C, Clark RB (1990) Genetic aspects of aluminium tolerance in sorghum. Plant Soil 123:211–216Google Scholar
  38. Gruber B, Ryan P, Richardson A et al (2006) The identification and characterisation of ALMT1 homologs in the Triticeae. Proceedings of 8th International Congress of Plant Molecular Biology, Adelaide, Australia, p 185Google Scholar
  39. Hoekenga OA, Maron LG, Cancado GMA et al (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:9738–9743PubMedGoogle Scholar
  40. Horst WJ, Puschel AK, Schmohl N (1997) Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant Soil 192:23–30Google Scholar
  41. Hu SW, Bai GH, Carver BF, Zhang DD (2008) Diverse origins of aluminium-resistance sources in wheat. Theor Appl Genet 118:29–41PubMedGoogle Scholar
  42. Huang CF, Yamaji N, Mitani N et al (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667PubMedCentralPubMedGoogle Scholar
  43. Hue NV, Craddock GR, Adams F (1986) Effect of organic acids on aluminum toxicity in subsoils. Soil Sci Soc Am J 50:28–34Google Scholar
  44. Inostroza-Blancheteau C, Soto B, Ibáñez C et al (2010) Mapping aluminum tolerance loci in cereals: a tool available for crop breeding. Electron J Biotech 13:doi:10.2225/vol2213-issue2224-fulltext-2224Google Scholar
  45. Ishikawa S, Wagatsuma T, Sasaki R, Ofei-Manu P (2000) Comparison of the amount of citric and malic acids in Al media of seven plant species and two cultivars each in five plant species. Soil Sci Plant Nutr 46:751–758Google Scholar
  46. Iuchi S, Koyama H, Iuchi A et al (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Nat Acad Sci 104:9900–9905PubMedGoogle Scholar
  47. Johnson JP, Carver BF, Baligar VC (1997) Expression of aluminum tolerance transferred from Atlas 66 to hard winter wheat. Crop Sci 37:103–108Google Scholar
  48. Jones DL (1998) Organic acids in the rhizosphere—a crtitical review. Plant Soil 205:25–44Google Scholar
  49. Kerridge PC, Kronstad WE (1968) Evidence of genetic resistance to aluminium toxicity in wheat. Agronomy J 60:710–711Google Scholar
  50. Kinraide TB, Parker DR, Zobel RW (2005) Organic acid secretion as a mechanism of aluminium resistance: a model incorporating the root cortex, epidermis, and the external unstirred layer. J Exp Bot 56:1853–1865PubMedGoogle Scholar
  51. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260Google Scholar
  52. Krill AM, Kirst M, Kochian LV et al (2010) Association and linkage analysis of aluminium tolerance genes in maize. PLoS ONE 5:e9958PubMedCentralPubMedGoogle Scholar
  53. Krizek DT, Foy CD (1988) Role of water stress in differential aluminium tolerance of two barley cultivar in acid soil. J Plant Nutr 11:351–367Google Scholar
  54. Larsen PB, Degenhardt J, Tai CY et al (1998) Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol 117:9–18PubMedCentralPubMedGoogle Scholar
  55. Ligaba A, Katsuhara M, Ryan PR et al (2006) The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. Plant Physiol 142:1294–1303PubMedCentralPubMedGoogle Scholar
  56. Ligaba A, Maron L, Shaff J et al (2012) Maize ZmALMT2 is a root anion transporter that mediates constitutive root malate efflux. Plant Cell Environ 35:1185–1200PubMedGoogle Scholar
  57. Lima M, Furlani PR, Miranda-Filho JB de (1992) Divergent selection for aluminium tolerance in a maize (Zea mays L.) population. Maydica 37:123–132Google Scholar
  58. Liu J, Magalhaes JV, Shaff J et al (2008) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 389–399Google Scholar
  59. Loarce Y, Hueros G, Ferrer E (1996) A molecular linkage map of rye. Theor Appl Genet 93:1112–1118PubMedGoogle Scholar
  60. Luo MC, Dvorak J (1996) Molecular mapping of an aluminium tolerance locus on chromosome 4D of Chinese Spring wheat. Euphytica 91:31–35Google Scholar
  61. Ma HX, Bai GH, Carver B, Zhou LL (2005) Molecular mapping of a quantitative trait locus for aluminum tolerance in wheat cultivar Atlas 66. Theor Appl Genet 112:51–57PubMedGoogle Scholar
  62. Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278PubMedGoogle Scholar
  63. Ma JF, Shen R, Zhao Z et al (2002) Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol 43:652–659PubMedGoogle Scholar
  64. Ma JF, Nagao S, Sato K et al (2004) Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley. J Exp Bot 55:1335–1341PubMedGoogle Scholar
  65. Magalhaes JV, Garvin DF, Wang YH et al (2004) Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the Poaceae. Genetics 167:1905–1914PubMedGoogle Scholar
  66. Magalhaes JV, Liu J, Guimaraes CT et al (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161PubMedGoogle Scholar
  67. Maltais K, Houde M (2002) A new biochemical marker for aluminium tolerance in plants. Physiol Plant 115:81–86PubMedGoogle Scholar
  68. Maron LG, Pineros MA, Guimaraes CT et al (2010) Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J 61:728–740PubMedGoogle Scholar
  69. Masojć P, Mysków B, Milczarski P (2001) Extending a RFLP-based genetic map of rye using random amplified polymorphic DNA (RAPD) and isozyme markers. Theor Appl Genet 102:1273–1279Google Scholar
  70. Massot N, Poschenrieder C, Barcelo J (1992) Differential response of three beans (Phaselous vulagaris) cultivars to aluminium. Acta Botanica Neerlandica 41:293–298Google Scholar
  71. Massot N, Llugany M, Poschenrieder C, Barcelo J (1999) Callose production as indicator of aluminum toxicity in bean cultivars. J Plant Nutr 22:1–10Google Scholar
  72. Miftahudin T, Scoles GJ, Gustafson JP (2002) AFLP markers tightly linked to the aluminum-tolerance gene Alt3 in rye (Secale cereale L.). Theor Appl Genet 104:626–631Google Scholar
  73. Miftahudin T, Scoles GJ, Gustafson JP (2004) Development of PCR-based codominant markers flanking the Alt3 gene in rye. Genome 47:231–238PubMedGoogle Scholar
  74. Miftahudin T, Chikmawati T, Ross K et al (2005) Targeting the aluminum tolerance gene Alt3 region in rye, using rice/rye micro-colinearity. Theor Appl Genet 110:906–913PubMedGoogle Scholar
  75. Milla R, Gustafson JP (2001) Genetic and physical characterization of chromosome 4DL in wheat. Genome 44:883–892PubMedGoogle Scholar
  76. Minella E, Sorrells ME (1992) Aluminum tolerance in barley: Genetic relationships among genotypes of diverse origin. Crop Sci 32:593–598Google Scholar
  77. Minella E, Sorrells ME (1997) Inheritance and chromosome location of Alp, a gene controlling aluminium tolerance in ‘Dayton’ barley. Plant Breed 116:465–469Google Scholar
  78. Moroni JS, Briggs KG, Taylor GJ (1991) Pedigree analysis of the origin of manganese tolerance in Canadian spring wheat (Triticum aestivum L.) cultivars. Euphytica 56:107–120Google Scholar
  79. Navakode S, Weidner A, Lohwasser U et al (2009a) Molecular mapping of quantitative trait loci (QTLs) controlling aluminium tolerance in bread wheat. Euphytica 166:283–290Google Scholar
  80. Navakode S, Weidner A, Varshney RK et al (2009b) A QTL analysis of aluminium tolerance in barley, using gene-based markers. Cereal Res Commun 37:531–540Google Scholar
  81. Nguyen BD, Brar DS, Bui BC et al (2003) Identification and mapping of QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., to indica rice (Oryza sativa L.). Theor Appl Genet 106:583–593PubMedGoogle Scholar
  82. Nguyen VT, Burrow MD, Nguyen HT et al (2001) Molecular mapping of genes conferring aluminium tolerance in rice (Oryza sativa L.). Theor Appl Genet 102:1002–1010Google Scholar
  83. Nguyen VT, Nguyen BD, Sarkarung S et al (2002) Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds. Mol Genet Gen 267:772–780Google Scholar
  84. Niedziela A, Bednarek P, Cichy H et al (2012) Aluminum tolerance association mapping in triticale. BMC Genomics 13:67PubMedCentralPubMedGoogle Scholar
  85. Ninamango-Cardenas FE, Guimaraes CT, Martins PR et al (2003) Mapping QTLs for aluminum tolerance in maize. Euphytica 130:223–232Google Scholar
  86. Omote H, Hiasa M, Matsumoto T et al (2006) The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci 27:587–593PubMedGoogle Scholar
  87. Pan W, Hopkins A, Jackson W (1989) Aluminum inhibition of shoot lateral branches of Glycine max and reversal by exogenous cytokinin. Plant Soil 120:1–9Google Scholar
  88. Pellet DM, Papernik LA, Kochian LV (1996) Multiple aluminum-resistance mechanisms in wheat. Roles of root apical phosphate and malate exudation. Plant Physiol 112:591–597PubMedCentralPubMedGoogle Scholar
  89. Pereira JF, Zhou GF, Delhaize E et al (2010) Engineering greater aluminium resistance in wheat by over-expressing TaALMT1. Ann Bot 106:205–214PubMedGoogle Scholar
  90. Philipp U, Wehling P, Wricke G (1994) A linkage map of rye. Theor Appl Genet 88:243–248PubMedGoogle Scholar
  91. Pineros MA, Cancado GMA, Maron LG et al (2008) Not all ALMT1-type transporters mediate aluminum-activated organic acid responses: the case of ZmALMT1—an anion-selective transporter. Plant J 53:352–367PubMedGoogle Scholar
  92. Polle E, Konzak CF (1985) A single scale for determining Al tolerance levels in cereals. Agronomy Abstracts 67, ASA, Madison, USAGoogle Scholar
  93. Polle E, Konzak CF, Kittrick JA (1978) Visual detection of aluminum tolerance levels in wheat by hematoxylin staining of seedling roots. Crop Sci 18:823–827Google Scholar
  94. Raman H, Gustafson P (2010) Molecular breeding for aluminium tolerance in cereals. In: Root Genomics (A Costa de Oliveira and R.K. Varshney eds). Springer, pp 251–288Google Scholar
  95. Raman H, Moroni S, Raman R et al (2001) A genomic region associated with aluminium tolerance in barley. Proceedings of the 10th Australian Barley Technical Symposium. (http://wwwregionalorgau/au/abts/2001/t3/indexhtm#TopOfPage), CanberraGoogle Scholar
  96. Raman H, Moroni JS, Sato K et al (2002) Identification of AFLP and microsatellite markers linked with an aluminium tolerance gene in barley (Hordeum vulgare L.). Theor Appl Genet 105:458–464PubMedGoogle Scholar
  97. Raman H, Karakousis A, Moroni JS et al (2003) Development and allele diversity of microsatellite markers linked to the aluminium tolerance gene Alp in barley. Aust J Agric Res 54:1315–1321Google Scholar
  98. Raman H, Wang JP, Read B et al (2005a) Molecular mapping of resistance to aluminium toxicity in barley. Proceedings of Plant and Animal Genome XIII Conference, San Diego, p 154Google Scholar
  99. Raman H, Zhang K, Cakir M et al (2005b) Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48:781–791Google Scholar
  100. Raman H, Raman R, Wood R, Martin P (2006) Repetitive indel markers within the ALMT1 gene conditioning aluminium tolerance in wheat (Triticum aestivum L.). Mol Breed 18:171–183Google Scholar
  101. Raman H, Ryan PR, Raman R et al (2008) Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). Theor Appl Genet 116:343–354PubMedGoogle Scholar
  102. Raman H, Raman R, Luckett D et al (2009) Characterisation of genetic variation for aluminium resistance and polyphenol oxidase activity in genebank accessions of spelt wheat. Breed Sci 59:373–381Google Scholar
  103. Raman H, Stodart B, Ryan PR et al (2010) Genome wide association analyses of common wheat (Triticum aestivum L) germplasm identifies multiple loci for aluminium resistance. Genome 53:957–966PubMedGoogle Scholar
  104. Reid DA (1971) Genetic control of reaction to aluminum in winter barley. In: Nilan RA (ed) Proceedings of the 2nd International Barley Genetics Symposium (1969). Washington State University Press, Pullman, WA, pp 409–413Google Scholar
  105. Reid DA, Fleming AL, Foy CD (1971) A method for determining aluminum response of barley in nutrient solution in comparison to response in Al-toxic soil. Agronomy J 63:600–603Google Scholar
  106. Rhue RD, Grogan CO, Stockmeyer EW, Everett HL (1978) Genetic control of aluminium tolerance in corn. Crop Sci 18:1063–1067Google Scholar
  107. Riede CR, Anderson JA (1996) Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Sci 36:905–909Google Scholar
  108. Ryan P, Raman H, Gupta S et al (2010) The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and from more recent cis mutations to TaALMT1. Plant J 64:446–455PubMedGoogle Scholar
  109. Ryan PR, Delhaize E, Randall PJ (1995a) Characterization of Al-stimulated efflux of malate from apices of Al-tolerant wheat roots. Planta 196:103–110Google Scholar
  110. Ryan PR, Delhaize E, Randall PJ (1995b) Malate efflux from root apices and tolerance to aluminium are highly correlated in wheat. Aust J Plant Physiol 22:531–536Google Scholar
  111. Ryan PR, Raman H, Gupta S et al (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149:340–351PubMedCentralPubMedGoogle Scholar
  112. Saal B, Wricke G (1999) Development of simple sequence repeat markers in rye (Secale cereale L.). Genome 42:964–972PubMedGoogle Scholar
  113. Sasaki T, Yamamoto Y, Ezaki B et al (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653PubMedGoogle Scholar
  114. Sasaki T, Ryan PR, Delhaize E et al (2006) Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant Cell Physiol 47:1343–1354PubMedGoogle Scholar
  115. Senft P, Wricke G (1996) An extended genetic map of rye (Secale cereale L.). Plant Breed 115:508–510Google Scholar
  116. Smith AV, Thomas DJ, Munro HM, Abecasis GR (2005) Sequence features in regions of weak and strong linkage disequilibrium. Genome Res 15:1519–1534PubMedGoogle Scholar
  117. Somers DJ, Briggs KG, Gustafson JP (1996) Aluminum stress and protein synthesis in near isogenic lines of Triticum aestivum differing in aluminum tolerance. Physiol Plant 97:694–700Google Scholar
  118. Soto-Cerda BJ, Cloutier S (2012) Association Mapping in Plant Genomes. Genetic Diversity in Plants. Prof Mahmut Caliskan (Ed), ISBN: 978–953-51–0185-7, InTec. http://wwwintechopencom/books/genetic-diversity-in-plants/association-mapping-in-plant-genomesGoogle Scholar
  119. Stich B, Melchinger AE, Piepho HP et al (2007) Potential causes of linkage disequilibrium in a European maize breeding program investigated with computer simulations. Theor Appl Genet 115:529–536PubMedGoogle Scholar
  120. Stich B, Mohring J, Piepho HP et al (2008) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754PubMedGoogle Scholar
  121. Stodart BJ, Raman H, Coombes N, Mackay M (2007) Evaluating landraces of bread wheat Triticum aestivum L. for tolerance to aluminium under low pH conditions. Genet Res Crop Evol 54:759–766Google Scholar
  122. Tang Y, Sorrells ME, Kochian LV, Garvin DF (2000) Identification of RFLP markers linked to the barley aluminum tolerance gene Alp. Crop Sci 40:778–782Google Scholar
  123. Uhde-Stone C, Liu J, Zinn KE et al (2005) Transgenic proteiod roots of white lupin: a vehicle for characterisation and silencing root genes involved in adapation to P stress. Plant J 44:840–853PubMedGoogle Scholar
  124. von Uexkull HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15Google Scholar
  125. Wang JP, Raman H, Read B et al (2004) Comparison of root staining and root elongation in predicting aluminium tolerance using SSR markers in barley. Proceeding of 4th International Crop ScienceCongress. http://wwwcropscienceorgau/icsc2004/poster/3/6/4/1168_wangjhtm, BrisbaneGoogle Scholar
  126. Wang J, Raman H, Zhang G-P et al (2006a) Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms and screening methods. J Zhejiang Univ Sci 7:769–787Google Scholar
  127. Wang JP, Raman H, Read B et al (2006b) Validation of an Alt locus for aluminium tolerance scored with eriochrome cyanine R staining method in barley cultivar Honen (Hordeum vulgare L.). Aust J Agric Res 57:113–118Google Scholar
  128. Wang JP, Raman H, Zhou MX et al (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 115:265–276PubMedGoogle Scholar
  129. Wenzl P, Li H, Carling J et al (2006) A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genomics 7:206PubMedCentralPubMedGoogle Scholar
  130. Wight CP, Kibite S, Tinker NA, Molnar SJ (2006) Identification of molecular markers for aluminium tolerance in diploid oat through comparative mapping and QTL analysis. Theor Appl Genet 112:222–231PubMedGoogle Scholar
  131. Wu P, Liao CY, Hu B, Yi et al (2000) QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genet 100:1295–1303Google Scholar
  132. Xia J, Yamaji N, Kasai T, Ma JF (2010) Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci USA 107:18381–18385PubMedGoogle Scholar
  133. Xue Y, Jiang L, Su N et al (2007) The genetic basic and fine-mapping of a stable quantitative-trait loci for aluminium tolerance in rice. Planta 227:255–262PubMedGoogle Scholar
  134. Yamaguchi M, Sasaki T, Sivaguru M et al (2005) Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). Plant Cell Physiol 46:812–816PubMedGoogle Scholar
  135. Yamajia N, Huang CF, Nagao S et al (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21:3339–3349Google Scholar
  136. Yan J, Shah T, Warburton ML et al (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4:e8451PubMedCentralPubMedGoogle Scholar
  137. Yokosho K, Yamaji N, Ma JF (2010) Isolation and characterisation of two MATE genes in rye. Funct Plant Biol 37:296–303Google Scholar
  138. Yokosho K, Yamaji N, Ma JF (2011) An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J 68:1061–1069PubMedGoogle Scholar
  139. Yu J, Pressoir G, Briggs WH et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208PubMedGoogle Scholar
  140. Yu JM, Holland JB, McMullen MD, Buckler ES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178:539–551PubMedGoogle Scholar
  141. Zhang X, Jessop RS (1998) Analysis of genetic variability of aluminium tolerance response in triticale. Euphytica 102:177–182Google Scholar
  142. Zhou LL, Bai G-H, Ma HX, Carver BF (2007a) Quantitative trait loci for aluminum resistance in wheat. Mol Breed 19:153–161Google Scholar
  143. Zhou LL, Bai GH, Carver BF, Zhang DD (2007b) Identification of new sources of aluminium resistance in wheat. Plant Soil 297:105–118Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Graham Centre for Agricultural Innovation (an alliance between Charles Sturt University and NSW Department of Department of Primary Industries)Wagga Wagga Agricultural InstituteWagga WaggaAustralia
  2. 2.Division of Plant SciencesUniversity of MissouriColumbiaUSA

Personalised recommendations