Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance

Plant Journal

Volumn 57, Issue 3, 2009, Pages 389-399

  Liu, Jiping ^a   Magalhaes, Jurandir V ^b   Shaff, Jon ^a   Kochian, Leon V ^a  

^a Department of Obstetrics Gynecology   (United States)

^b EMBRAPA MILHO E SORGO   (Brazil)

Author keywords

ALMT; Aluminum tolerance; Aluminum toxicity; Multi drug and toxic compound extrusion; Organic acid exudation; Plasma membrane protein; Transporter protein

Indexed keywords

ALMT1 PROTEIN, ARABIDOPSIS; ALUMINUM; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; CITRATE BINDING TRANSPORT PROTEIN; CITRATE-BINDING TRANSPORT PROTEIN; CITRIC ACID; MALIC ACID; MALIC ACID DERIVATIVE; ORGANIC ANION TRANSPORTER; PLANT RNA; STOP1 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLANT ROOT; SEQUENCE ALIGNMENT;

ALUMINUM; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CITRIC ACID; GENE EXPRESSION REGULATION, PLANT; MALATES; MOLECULAR SEQUENCE DATA; ORGANIC ANION TRANSPORTERS; PHYLOGENY; PLANT ROOTS; RNA, PLANT; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS;

ARABIDOPSIS; HORDEUM;

EID: 58849124631     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03696.x     Document Type: Article

References (37)

1. Carver, B.F. Ownby, J.D. (1995) Acid soil tolerance in wheat. Adv. Agron. 54, 117 172.
2. Debeaujon, I., Peeters, A.J.M., Léon-Kloosterziel, K.M. Koornneef, M. (2001) The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 13, 853 871.
3. Delhaize, E., Ryan, P.R. Randall, P.J. (1993b) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol. 103, 695 702.
4. Delhaize, E. Ryan, P.R. (1995) Aluminum toxicity and tolerance in plants. Plant Physiol. 107, 315 321.
5. Delhaize, E., Craig, S., Beaton, C.D., Bennet, R.J., Jagadish, V.C. Randall, P.J. (1993a) Aluminum tolerance in wheat (Triticum aestivum L.) I. Uptake and distribution of aluminum in root apices. Plant Physiol. 103, 685 693.
6. Delhaize, E., Ryan, P.R., Hebb, D.M., Yamamoto, Y., Sasaki, T. Matsumoto, H. (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc. Natl Acad. Sci. USA, 101, 15249 15254.
7. Delhaize, E., Gruber, B.D. Ryan, P.R. (2007) The roles of organic anion permeases in aluminum resistance and mineral nutrition. FEBS Lett. 581, 2255 2262.
8. Diener, A.C., Gaxiola, R.A. Fink, G.R. (2001) Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell 13, 1625 1637.
9. Duncan, R.R. (1988) Sequential development of acid soil tolerant sorghum genotypes under field stress conditions. Commun. Soil Sci. Plant Anal. 19, 1295 1305.
10. Durrett, T.P., Gassmann, W. Rogers, E.E. (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol. 144, 197 205.
11. Furukawa, J., Yamaji, N., Wang, H., Mitani, N., Murata, Y., Sato, K., Katsuhara, M., Takeda, K. Ma, J.F. (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol. 48, 1081 1091.
12. Gerhardt, R., Stitt, M. Heldt, H.W. (1987) Subcellular metabolite levels in spinach leaves. Plant Physiol. 83, 399 407.
13. Green, L.S. Rogers, E.E. (2004) FRD3 controls iron localization in Arabidopsis. Plant Physiol. 136, 2523 2531.
14. Hoekenga, O.A., Maron, L.G., Piñeros, M.A. 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 9743.
15. Hvorup, R.N., Winnen, B., Chang, A.B., Jiang, Y., Zhou, X.F. Saier, M.H. (2003) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur. J. Biochem. 270, 799 813.
16. Iuchi, S., Koyama, H., Iuchi, A., Kobayashi, Y., Kitabayashi, S., Kobayashi, Y., Ikka, T., Hirayama, T., Shinozaki, K. Kobayashi, M. (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc. Natl Acad. Sci. USA, 104, 9900 9905.
17. Kinraide, T.B., Parker, D.R. Zobel, R.W. (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 1865.
18. Kobayashi, Y., Hoekenga, O.A., Itoh, H., Nakashima, M., Saito, S., Shaff, J.E., Maron, L.M., Piñeros, M.A., Kochian, L.V. Koyama, H. (2007) Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol. 145, 843 852.
19. Kochian, L.V., Hoekenga, O.A. Piñeros, M.A. (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu. Rev. Plant Biol. 55, 459 493.
20. Li, L., He, Z., Pandey, G.K., Tsuchiya, T. Luan, S. (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J. Biol. Chem. 277, 5360 5368.
21. Ma, J.F. (2000) Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol. 41, 383 390.
22. Ma, J.F., Ryan, P.R. Delhaize, E. (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6, 273 278.
23. Magalhaes, J.V. (2006) Aluminum tolerance genes are conserved between monocots and dicots. Proc. Natl Acad. Sci. USA, 104, 9749 9750.
24. Magalhaes, J.V., Garvin, D.F., Wang, Y., Sorrells, M.E., Klein, P.E., Schaffert, R.E., Li, L. Kochian, L.V. (2004) Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the Poaceae. Genetics, 167, 1905 1914.
25. Magalhaes, J.V., Liu, J., Guimarães, C.T. et al. (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genet. 39, 1156 1161.
26. Marinova, K., Pourcel, L., Weder, B., Schwarz, M., Barron, D., Routaboul, J.-M., Debeaujon, I. Klein, M. (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin- accumulating cells of the seed coat. Plant Cell, 19, 2023 2038.
27. Matsumoto, H. (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int. Rev. Cytol. 200, 1 46.
28. Nawrath, C., Heck, S., Parinthawong, N. Métraux, J.-P. (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell, 14, 275 286.
29. Nguyen, V.T., Burrow, M.D., Nguyen, H.T., Le, T.D. Paterson, A.H. (2001) Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor. Appl. Genet. 102, 1002 1010.
30. Nguyen, V.T., Nguyen, B.D., Sakarung, S., Matinez, C. Paterson, A.H. (2002) Mapping genes controlling Al tolerance in rice: comparing different genetic backgrounds. Mol. Genet. Genomics, 267, 772 780.
31. Pandey, S., Ceballos, H., Magbavaca, R. et al. (1994) Genetics of tolerance to soil acidity in tropical maize. Crop Sci. 34, 1511 1514.
32. Piñeros, M.A., Magalhaes, J.V., Alves, V.M.C. Kochian, L.V. (2002) The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation. Plant Physiol. 129, 1194 1206.
33. Rogers, E.E. Guerinot, M.L. (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell, 14, 1787 1799.
34. Ryan, P.R., Delhaize, E. Randall, P.J. (1995) Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta, 196, 103 110.
35. Ryan, P.R., Delhaize, E. Jones, D.L. (2001) Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 527 560.
36. Sasaki, T., Yamamoto, Y., Ezaki, B., Katsuhara, M., Ahn, S.J., Ryan, P.R., Delhaize, E. Matsumoto, H. (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37, 645 653.
37. Wu, P., Liao, C.D., Hu, B., Yi, K.K., Jin, W.Z., Ni, J.J. He, C. (2000) QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor. Appl. Genet. 100, 1295 1303.