Skip to main content
Log in

Marker-assisted breeding for TaALMT1, a major gene conferring aluminium tolerance to wheat

Biologia Plantarum

Cite this article


Aluminium toxicity in acid soils is the main limitation to crop production worldwide. In wheat (Triticum aestivum L.), the Al-activated malate transporter (TaALMT1) gene located on chromosome 4DL is associated with malate efflux and Al-tolerance. To introgress Al-tolerance from the breeding line CAR3911 into the high yielding Al-sensitive cultivar Kumpa-INIA, phenotypic and molecular characterizations of gene/QTL underlying Al-tolerance in CAR3911 followed by marker-assisted backcrossing (MAS-BC) were undertaken. Al-tolerant backcross (BC) lines were selected using the functional marker ALMT1-4 designed immediately upstream of the TaALMT1 coding region. Foreground and background selections using ALMT1-4 and microsatellite markers were conducted. Linkage and sequence analyses suggest that the TaALMT1 gene could underly the Al-tolerance in CAR3911, possessing the same promoter type (V) as the Al-tolerant genotypes Carazinho and ET8. The MAS-BC strategy allowed the selection of Al-tolerant lines with the smallest introgressed region (6 cM) on 4D and the highest recurrent parent genome (RPG) (98 %) covering 2 194 cM of the wheat genome. The homozygous BC3F2 line named Kumpa-INIA-TaALMT1 expressed a 3-fold higher Al-tolerance than its isogenic line Kumpa-INIA at 40 μM Al in the hydroponic solution, and similarly to CAR3911 and Carazinho. The MAS-BC strategy was successful for the introgression of the TaALMT1 gene into Kumpa-INIA in only three BC generations, shortening the breeding cycle to 24 months, which promises to increase wheat production and a greater yield stability in the acid soils of Southern Chile.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others



bulk segregant analysis


marker assisted backcrossing


quantitative trait loci


recurrent parent genome


relative root elongation


root regrowth


Al-activated malate transporter gene 1


  • Basu, U., McDonald, J., Archamhault, D., Good, A., Briggs, K., Aung, T., Taylor, G.: Genetic and physiological analysis of doubled-haploid, aluminium resistance lines of wheat provide evidence for the involvement of a 23 kD, root exudate polypeptide in mediating resistance. — Plant Soil 196: 283–288, 1997.

    Article  CAS  Google Scholar 

  • Bertrand, C., Collar, Y., Mackill, D.J.: Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. — Phil. Trans. roy. Soc. London B. 363: 557–572, 2008.

    Article  Google Scholar 

  • Cai, S., Bai, G.H., Zhang, D.: Quantitative trait loci for aluminium resistance in Chinese wheat landrace FSW. — Theor. appl. Genet. 117: 49–56, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Delhaize, E., Higgins, T.J.V., Randall, P.J.: Aluminium tolerance in wheat: analysis of polypeptides in the root apices of tolerant and sensitive genotypes. — In: Wright, R.J., Baligar, V.C., Murrmann, R.P. (ed.): Plant-Soil Interactions at Low pH. Developments in Plant and Soil Sciences. Vol. 45. Pp. 1071–1079. Springer, Dordrecht 1991.

    Chapter  Google Scholar 

  • Frisch, M., Bohn, M., Melchinger, A.: Comparison of selection strategies for marker-assisted backcrossing of a gene. — Crop Sci. 39: 1295–1301, 1999.

    Article  Google Scholar 

  • Gallardo, F., Borie, F., Alvear, L., Bae, E.V.: Evaluation of aluminium tolerance of three barley cultivars by two short-term screening methods and field experiments. — Soil Sci. Plant Nutr. 45: 713–719, 1999.

    Article  CAS  Google Scholar 

  • Gupta, P., Balyan, H., Edwards, K., Isaac, P., Korzun, V., Röder, M., Gautier, M., Joudrier, P., Schlatter, A., Dubcovsky, J., De la Peña, R., Khairallah, M., Penner, G., Hayden, M., Sharp, P., Keller, B., Wang, R., Hardouin, J., Jack, P., Leroy, P.: Genetic mapping of 66 new microsatellite (SSR) loci in bread wheat. — Theor. appl. Genet. 105: 413–422, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Hede, A.R., Skovmand, B., Ribaut, J.M., González de León, D., Stolen, O.: Evaluation of aluminium tolerance in a spring rye collection by hydroponic screening. — Plant Breed. 121: 241–248, 2002.

    Article  CAS  Google Scholar 

  • Hu, S.W., Bai, G.H., Carver, B., Zhang, D.: Diverse origins of aluminium-resistance sources in wheat. — Theor. appl. Genet. 118: 29–41, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Inostroza-Blancheteau, C., Rengel, Z., Alberdi, M., Mora, M.L., Aquea, F., Arce-Johnson, P., Reyes-Díaz, M.: Molecular and physiological strategies to increase aluminium resistance in plants. — Mol. Biol. Rep. 39: 2069–2079, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Jobet, C., Hewstone, C.: Kumpa-INIA: new winter wheat variety for Southern Chile. — Chil. J. agr. Res. 63: 81–86, 2003.

    Google Scholar 

  • Khan, I.A., Procunier, J.D., Humpreys, D.G., Tranquilli, G., Schlatter, A.R., Marcucci-Poltri, S., Frohberg, R., Dubcovsky, J.: Development of PCR-based markers for a high grain protein content gene from Triticum turgidum ssp. dicoccoides transferred to bread wheat. — Crop Sci. 40: 518–524, 2000.

    Article  CAS  Google Scholar 

  • Kosambi, D.D.: The estimation of map distance from recombination values. — Ann. Eugen. 12: 172–175, 1944.

    Article  Google Scholar 

  • Ma, J., Shen, R., Zhao, Z., Wissuwa, M., Takeuchi, Y., Ebitani, T., Yano, M.: Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. — Plant Cell Physiol. 43: 652–659, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Ma, H., Bai, G., Carver, B., Zhou, L.: Molecular mapping of a quantitative trait locus for aluminium tolerance in wheat cultivar Atlas 66. — Theor. appl. Genet. 112: 51–57, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Martins N., Gonçalves, S., Romano, A.: Metabolism and aluminum accumulation in Plantago almogravensis and P. algarbiensis in response to low pH and aluminum stress. — Biol. Plant. 57: 325–331, 2013.

    Article  CAS  Google Scholar 

  • Michelmore, R., Paran, I., Kesseli, V.: Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. — Proc. nat. Acad. Sci. USA 88: 9828–9832, 1991.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Papernik, L., Bethea, A., Singleton, T., Magalhaes, V., Garvin, D., Kochian, L.: Physiological basis of reduced Al tolerance in ditelosomic lines of Chinese Spring wheat. — Planta 212: 829–834, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Peñaloza, E., Martinez, J., Montenegro, A., Corcuera, L.: Response of two lupin species to phytotoxic aluminium. — Chil. J. agr. Res. 64: 127–138, 2004.

    Google Scholar 

  • Raman, H., Karakousis, A., Moroni, J., Raman, R., Read, B., Garvin, D., Kochian, L., Sorrells, M.: Development and allele diversity of microsatellite markers linked to the aluminium tolerance gene Alp in barley. — Aust. J. agr. Res. 54: 1315–1321, 2003.

    Article  CAS  Google Scholar 

  • Raman, H., Moroni, J., Sato, K., Read, B.: Identification of AFLP and microsatellite markers linked with an aluminium tolerance gene in barley (Hordeum vulgare L.). — Theor. appl. Genet. 105: 458–464, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Raman, H., Raman, R., Wood, R., Martin, P.: Repetitive indel markers within the ALMT1 gene conditioning aluminium tolerance in wheat (Triticum aestivum L.). — Mol. Breed. 18: 171–183, 2006.

    Article  CAS  Google Scholar 

  • Raman, H., Ryan, P.R., Raman, R., Stodart, B.J., Zhang, K., Martin, P., Wood, R., Sasaki, T., Yamamoto, Y., Mackay, M., Hebb, D.M., Delhaize, E.: Analysis of TaALMT1 traces the transmission of aluminium resistance in cultivated common wheat (Triticum aestivum L.). — Theor. appl. Genet. 116: 343–354, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Raman, H., Zhang, K., Cakir, M., Appels, R., Garvin, D., Maron, L., Kochian, L., Moroni, J., Raman, R., Imtiaz, M., Drake-Brockman, F., Waters, I., Martin, P., Sasaki, T., Yamamoto, Y., Matsumoto, H., Hebb, D., Delhaize, E., Ryan, P.: Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). — Genome 48: 781–791, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Raman, H., Stodart, B., Ryan, P.R., Delhaize, E., Emebiri, L., Raman, R., Coombes, N., Milgate, A.: Genome-wide association analyses of common wheat (Triticum aestivum L.) germoplasm identifies multiple loci for aluminum resistance. — Genome 53: 957–966, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Ribaut, J.M., Hoisington, D.: Marker-assisted selection: new tools and strategies. — Trends Plant Sci. 3: 236–239, 1998.

    Article  Google Scholar 

  • Riede, C., Anderson, J.: Linkage of RFLP markers to an aluminium tolerance gene in wheat. — Crop Sci. 36: 905–909, 1996.

    Article  Google Scholar 

  • Röder, M., Korzun, V., Wendehake, K., Plaschke, J., Tixier, M., Leroy, P., Ganal, M.: A microsatellite map of wheat. — Genetics 149: 2007–2023, 1998.

    PubMed Central  PubMed  Google Scholar 

  • Ryan, P., Raman, H., Gupta, S., Horst, W., Delhaize, E.: A second mechanism for aluminium resistance in wheat relies on the constitutive efflux of citrate from roots. — Plant Physiol. 149: 340–351, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ryan, P.R, Raman, H., Gupta, S., Sasaki, T., Yamamoto, Y., Delhaize, E.: The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1. — Plant J. 64: 446–455, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Sasaki, T., Yamamoto, Y., Ezaki, B., Katsuhara, M., Ahn, S.J., Ryan, P., Delhaize, E.: A wheat gene encoding an aluminium-activated malate transporter. — Plant J. 37: 645–653, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Sasaki, T., Ryan, P., Delhaize, E., Hebb, D., Ogihara, Y., Kawaura, K., Noda, K., Kojima, T., Toyoda, A., Matsumoto, H., Yamamoto, Y.: Sequence upstream of the wheat (Triricum aestivum L.) ALMT1 gene and its relationship to aluminium resistance. — Plant Cell Physiol. 47: 1343–1354, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Servin, B., Hospital, F.: Optimal positioning of markers to control genetic background in marker assisted backcrossing. — J. Hered. 93: 214–217, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Somers, D., Gustafson, J.: The expression of aluminium stress induced polypeptides 1 in a population segregating for aluminium tolerance in wheat (Triticum aestivum L.). — Genome 38: 1213–1220, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Somers, D., Isaac, P., Edwards, K.: A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). — Theor. appl. Genet. 109: 1105–1114, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Sourdille, P., Charmet, G., Trottet, M., Tixier, H., Boeuf, C.: Linkage between RFLP molecular markers and the dwarfing genes Rtht and Rht-D1 in wheat. — Hereditas 128: 41–46, 1998.

    Article  CAS  Google Scholar 

  • Tester, M., Langridge, P.: Breeding technologies to increase crop production in a changing world. — Science 327: 818–822, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Torada, A., Koike, M., Mochida, K., Ogihara, Y.: SSR-based linkage map with new markers using intraspecific population of common wheat. — Theor. appl. Genet. 112: 1042–1051, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Van Berloo, R.: GGT 2.0: versatile software for visualization and analysis of genetic data. — J. Hered. 99: 232–236, 2008.

    Article  PubMed  Google Scholar 

  • Van Ooijen, J.W.: JoinMap® Versión 4.0: Software for the Calculation of Genetic Linkage Maps in Experimental Populations. — Kyazma BV, Wageningen 2006.

    Google Scholar 

  • Wood, S., Sebastian, K., Scherr, S.J.: Pilot Analysis of Global Ecosystems: Agroecosystems. — Rosen, Washington 2000.

    Google Scholar 

  • Zheng, S., Ma, J., Matsumoto, H.: High aluminium resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tips. — Plant Physiol. 117: 745–751, 1998.

    Article  PubMed Central  Google Scholar 

  • Zheng, S.J.: Crop production on acidic soils: overcoming aluminium toxicity and phosphorus deficiency. — Ann. Bot. 106: 183–184, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou, L., Bai, G., Ma, H., Carver, B.: Quantitative trait loci for aluminium resistance in wheat. — Mol. Breed. 9: 153–161, 2007.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations


Corresponding author

Correspondence to H. Salvo-Garrido.

Additional information

Acknowledgments: The authors acknowledge the financial support from the Fundación para la Innovación Agraría FIA-PI-C-2005-3-A-064, CGNA and the CONICYT Regional/GORE Araucanía/CGNA/R10C100, and the INIA fo r providing infrastructure. We are grateful to Dr. Emmanuel Delhaize, CSIRO Plant Industry, Canberra, Australia, for providing Carazinho, ET8, and ES8 wheat genotypes. The authors wish to thank Dr. Adriano Nunes-Nesi of the Departamento de Biologia Vegetal, Universidade Federal de Viçosa, MG, Brazil, for his contribution in the critical review of this manuscript. First two authors contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soto-Cerda, B.J., Inostroza-Blancheteau, C., Mathías, M. et al. Marker-assisted breeding for TaALMT1, a major gene conferring aluminium tolerance to wheat. Biol Plant 59, 83–91 (2015).

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

Additional key words