Abstract
Crop yields are significantly reduced by aluminum toxicity on highly acidic soils, which comprise up to 50% of the world's arable land1,2,3. Candidate aluminum tolerance proteins include organic acid efflux transporters, with the organic acids forming non-toxic complexes with rhizosphere aluminum1,4. In this study, we used positional cloning to identify the gene encoding a member of the multidrug and toxic compound extrusion (MATE) family, an aluminum-activated citrate transporter, as responsible for the major sorghum (Sorghum bicolor) aluminum tolerance locus, AltSB5. Polymorphisms in regulatory regions of AltSB are likely to contribute to large allelic effects, acting to increase AltSB expression in the root apex of tolerant genotypes. Furthermore, aluminum-inducible AltSB expression is associated with induction of aluminum tolerance via enhanced root citrate exudation. These findings will allow us to identify superior AltSB haplotypes that can be incorporated via molecular breeding and biotechnology into acid soil breeding programs, thus helping to increase crop yields in developing countries where acidic soils predominate.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Kochian, L.V. Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Biol. 46, 237–260 (1995).
Wood, S., Sebastian, K. & Scherr, S.J. in Pilot Analysis of Global Ecosystems: Agroecosystems (ed. Rosen, C.) 45–54 (International Food Policy Research Institute and the World Resources Institute, Washington, D.C., 2000).
von Uexküll, H.R. & Mutert, E. in Plant-Soil Interactions at Low pH: Principles and Management (eds. Date, R.A. Grundon, N.J. Raymet, G.E. & Probert, M.E.) 5–19 (Kluwer Academic Publishers, Dordrecht, The Netherlands, 1995).
Kochian, L.V., Hoekenga, O.A. & Piñeros, M.A. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu. Rev. Plant Biol. 55, 459–493 (2004).
Magalhaes, J.V. et al. Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the Poaceae. Genetics 167, 1905–1914 (2004).
Ryan, P.R., DiTomaso, J.M. & Kochian, L.V. Aluminum toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44, 437–446 (1993).
Ma, J.F., Ryan, P.R. & Delhaize, E. Aluminum tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6, 273–278 (2001).
Sasaki, T. et al. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37, 645–653 (2004).
Raman, H. et al. Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48, 781–791 (2005).
Caniato, F.F. et al. Genetic diversity for aluminum tolerance in sorghum. Theor. Appl. Genet. 114, 863–876 (2007).
Brown, M.H., Paulsen, I.T. & Skurray, R.A. The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol. Microbiol. 31, 393–395 (1999).
Morita, Y. et al. NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob. Agents Chemother. 42, 1778–1782 (1998).
Diener, A.C., Gaxiola, R.A. & Fink, G.R. Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell 13, 1625–1637 (2001).
Li, L., He, Z., Pandey, G.K., Tsuchiya, T. & Luan, S. Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J. Biol. Chem. 277, 5360–5368 (2002).
Magalhaes, J.V. Molecular genetic and physiological investigations of aluminum tolerance in sorghum (Sorghum bicolor L. Moench). Ph.D. thesis, Cornell University, (2003).
Bureau, T.E. & Wessler, S.R. Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4, 1283–1294 (1992).
Wessler, S.R., Bureau, T.E. & White, S.E. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr. Opin. Genet. Dev. 5, 814–821 (1995).
Hoekenga, O.A. et al. 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, 9738–9743 (2006).
Lou, Y. et al. The highly charged region of plant beta-type phosphatidylinositol 4-kinase is involved in membrane targeting and phospholipid binding. Plant Mol. Biol. 60, 729–746 (2006).
Hvorup, R.N. et al. The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur. J. Biochem. 270, 799–813 (2003).
He, G-X. et al. An H+-coupled multidrug efflux pump, PmpM, a member of the MATE family of transporters, from Pseudomonas aeruginosa. J. Bact. 186, 262–265 (2004).
Uhde-Stone, C., Liu, J., Zinn, K.E., Allan, D.L. & Vance, C.P. Transgenic proteoid roots of white lupin: a vehicle for characterization and silencing root genes involved in adaptation to P stress. Plant J. 44, 840–853 (2005).
Green, L.S. & Rogers, E.E. FRD3 controls iron localization in Arabidopsis. Plant Physiol. 136, 2523–2531 (2004).
Durrett, T.P., Gassmann, W. & Rogers, E.E. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol. 144, 197–205 (2007).
Yang, G. et al. A two-edged role for the transposable element Kiddo in the rice ubiquitin2 promoter. Plant Cell 17, 1559–1568 (2005).
Raizada, M.N., Benito, M.-I. & Walbot, V. The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs. Plant J. 25, 79–91 (2001).
Nguyen, V.T. et al. Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor. Appl. Genet. 102, 1002–1010 (2001).
Paterson, A.H. et al. Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269, 1714–1718 (1995).
Piñeros, M.A., Magalhaes, J.V., Alves, V.M.C. & Kochian, L.V. The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation. Plant Physiol. 129, 1194–1206 (2002).
Acknowledgements
The authors thank J. Giovannoni and E. Buckler for critically reading the manuscript and J. Essig and M. Wohler for their technical support with wheat tissue culture and wheat genetic engineering. The work was supported by Generation Challenge Program grant IC69, US Department of Agriculture–National Research Initiative Competitive grant 2006-35301-16884, a McKnight Foundation Collaborative Crop Research Program grant and a FAPEMIG–Brazil grant.
Author information
Authors and Affiliations
Contributions
J.V.M. and L.V.K. shared equally in the work, including the direction and oversight of the research and writing of the paper and, thus, are both equally contributing first authors and corresponding authors. J.L., C.T.G., U.G.P.L., Y.-H.W. and P.E.K. contributed to the positional cloning of AltSB, and J.L. conducted the real-time PCR analysis and generation and characterization of transgenic A. thaliana. U.G.P.L. and C.M.C. conducted the RT-PCR analysis of AltSB expression in the diversity panel. V.M.C.A. and J.E.S. conducted the analysis of sorghum root organic acid exudation, and J.E.S. conducted the A. thaliana root organic acid analysis. R.E.S. generated the mapping populations and NILs. O.A.H. contributed to the analysis of A. thaliana Al tolerance and organic acid exudation, and M.A.P. conducted the AltSB-GFP protein localization and expression and electrophysiological characterization of SbMATE in Xenopus laevis oocytes.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Text and Figures
Supplementary Methods, Supplementary Note, Supplementary Tables 1–2, Supplementary Figures 1–4 (PDF 692 kb)
Rights and permissions
About this article
Cite this article
Magalhaes, J., Liu, J., Guimarães, C. et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39, 1156–1161 (2007). https://doi.org/10.1038/ng2074
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng2074
This article is cited by
-
The LRR receptor-like kinase ALR1 is a plant aluminum ion sensor
Cell Research (2024)
-
Aluminum Toxicity in Plants: Present and Future
Journal of Plant Growth Regulation (2023)
-
Integration of GWAS and transcriptome analyses to identify SNPs and candidate genes for aluminum tolerance in rapeseed (Brassica napus L.)
BMC Plant Biology (2022)
-
Molecular and physiological aspects of plant responses to aluminum: what do we know about Cerrado plants?
Brazilian Journal of Botany (2022)
-
Strategies to acquire and use phosphorus in phosphorus-impoverished and fire-prone environments
Plant and Soil (2022)