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A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum

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.

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Figure 1: Positional cloning of AltSB.
Figure 2: Expression and localization of SbMATE.
Figure 3: Correlation of SbMATE expression, root citrate exudation and aluminum tolerance in ten sorghum lines that harbor an allelic series at AltSB (BR012, BR007, IS8577, SC549, 3DX, SC175, 9DX, CMS225, SC283, SC566)10 exposed to {27} μM Al3+ in nutrient solution.
Figure 4: Expression of SbMATE in transgenic A. thaliana plants.

References

  1. Kochian, L.V. Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Biol. 46, 237–260 (1995).

    Article  CAS  Google Scholar 

  2. 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).

    Google Scholar 

  3. 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).

    Book  Google Scholar 

  4. 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).

    Article  CAS  Google Scholar 

  5. 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).

    Article  CAS  Google Scholar 

  6. 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).

    Article  CAS  Google Scholar 

  7. 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).

    Article  CAS  Google Scholar 

  8. Sasaki, T. et al. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37, 645–653 (2004).

    Article  CAS  Google Scholar 

  9. 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).

    Article  CAS  Google Scholar 

  10. Caniato, F.F. et al. Genetic diversity for aluminum tolerance in sorghum. Theor. Appl. Genet. 114, 863–876 (2007).

    Article  CAS  Google Scholar 

  11. 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).

    Article  Google Scholar 

  12. 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).

    Article  CAS  Google Scholar 

  13. 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).

    Article  CAS  Google Scholar 

  14. 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).

    Article  CAS  Google Scholar 

  15. Magalhaes, J.V. Molecular genetic and physiological investigations of aluminum tolerance in sorghum (Sorghum bicolor L. Moench). Ph.D. thesis, Cornell University, (2003).

  16. 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).

    Article  CAS  Google Scholar 

  17. 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).

    Article  CAS  Google Scholar 

  18. 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).

    Article  CAS  Google Scholar 

  19. 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).

    Article  CAS  Google Scholar 

  20. Hvorup, R.N. et al. The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur. J. Biochem. 270, 799–813 (2003).

    Article  CAS  Google Scholar 

  21. 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).

    Article  CAS  Google Scholar 

  22. 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).

    Article  CAS  Google Scholar 

  23. Green, L.S. & Rogers, E.E. FRD3 controls iron localization in Arabidopsis. Plant Physiol. 136, 2523–2531 (2004).

    Article  CAS  Google Scholar 

  24. 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).

    Article  CAS  Google Scholar 

  25. Yang, G. et al. A two-edged role for the transposable element Kiddo in the rice ubiquitin2 promoter. Plant Cell 17, 1559–1568 (2005).

    Article  CAS  Google Scholar 

  26. 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).

    Article  CAS  Google Scholar 

  27. Nguyen, V.T. et al. Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor. Appl. Genet. 102, 1002–1010 (2001).

    Article  CAS  Google Scholar 

  28. Paterson, A.H. et al. Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269, 1714–1718 (1995).

    Article  CAS  Google Scholar 

  29. 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).

    Article  Google Scholar 

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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.

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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.

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Correspondence to Jurandir V Magalhaes or Leon V Kochian.

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The authors declare no competing financial interests.

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Supplementary Methods, Supplementary Note, Supplementary Tables 1–2, Supplementary Figures 1–4 (PDF 692 kb)

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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

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