The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1

Plant Journal

Volumn 64, Issue 3, 2010, Pages 446-455

  Ryan, Peter R ^a   Raman, Harsh ^b   Gupta, Sanjay ^a,d   Sasaki, Takayuki ^c   Yamamoto, Yoko ^c   Delhaize, Emmanuel ^a  

^a CSIRO   (Australia)

^b NSW DEPARTMENT OF PRIMARY INDUSTRIES   (Australia)

^c OKAYAMA UNIVERSITY   (Japan)

^d Directorate of Soybean Research ICAR   (India)

Author keywords

Acid soil; Aegilops tauschii; Aluminium; Evolution; Resistance; Tolerance; Triticum aestivum

Indexed keywords

ACID SOILS; AEGILOPS; ALUMINIUM; EVOLUTION; RESISTANCE; TOLERANCE; TRITICUM AESTIVUM;

ACIDS; GENE EXPRESSION; NEGATIVE IONS; PLANTS (BOTANY); SOILS;

ALUMINUM;

ALUMINUM; MALIC ACID; MALIC ACID DERIVATIVE; ORGANIC ANION TRANSPORTER; VEGETABLE PROTEIN;

ALLELE; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MUTATION; PHYLOGENY; PLANT GENE; PROMOTER REGION; TANDEM REPEAT; TRANSGENIC PLANT; WHEAT;

ALLELES; ALUMINUM; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MALATES; MUTATION; ORGANIC ANION TRANSPORTERS; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; TANDEM REPEAT SEQUENCES; TRITICUM;

AEGILOPS TAUSCHII; EUKARYOTA; TRITICUM AESTIVUM;

EID: 78149423704     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04338.x     Document Type: Article

References (85)

1. Adiloglu, A., and, Adiloglu, S., (2003) The investigation of some available trace element contents of acid soils in Turkey. Arch. Agron. Soil Sci. 49, 179-185.
2. Aniol, A., and, Gustafson, J.P., (1984) Chromosome location of genes controlling aluminum tolerance in wheat, rye and triticale. Can. J. Genet. Cytol. 26, 701-705.
3. Berzonsky, W.A., and, Kimber, G., (1986) Tolerance of Triticum species to aluminum. Plant Breed. 97, 275-278.
4. Blackwood, E.M., and, Kadonaga, J.T., (1998) Going the distance: a current view of enhancer action. Science, 281, 60-63.
5. Cai, S.B., Bai, G.H., and, Zhang, D.D., (2008) Quantitative trait loci for aluminum resistance in Chinese wheat landrace FSW. Theor. Appl. Genet. 117, 49-56.
6. Caldwell, K.S., Dvorak, J., Lagudah, E.S., Akhunov, E., Luo, M.C., Wolters, P., and, Powell, W., (2004) Sequence polymorphism in polyploid wheat and their D-genome diploid ancestor. Genetics, 167, 941-947.
7. Chan, Y.F., Marks, M.E., Jones, F.C., etal. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science, 327, 302-305.
8. Collins, N.C., Shirley, N.J., Saeed, M., Pallotta, M., and, Gustafson, J.P., (2008) An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics, 179, 669-682.
9. Cosic, T., Poljak, M., Custic, M., and, Rengel, Z., (1994) Aluminum tolerance of durum-wheat germplasm. Euphytica, 78, 239-243.
10. Delhaize, E., Ryan, P.R., and, Randall, P.J., (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol. 103, 695-702. (Pubitemid 2023261)
11. Delhaize, E., Ryan, P.R., Hebb, D.M., Yamamoto, Y., Sasaki, T., and, Matsumoto, H., (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc. Natl Acad. Sci. USA, 101, 15249-15254.
12. Delhaize, E., Gruber, B.D., and, Ryan, P.R., (2007) The roles of organic anion permeases in aluminum resistance and mineral nutrition. FEBS Lett. 581, 2255-2262.
13. Dubcovsky, J., and, Dvorak, J., (2007) Genome plasticity: a key factor in the success of polyploid wheat under domestication. Science, 316, 1862-1866.
14. Dvorak, J., Luo, M.C., Yang, Z.L., and, Zhang, H.B., (1998) The structure of the Aegilops tauschii genepool and the evolution of hexaploid wheat. Theor. Appl. Genet. 97, 657-670.
15. Espley, R.V., Brendolise, C., Chagne, D., etal. (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell, 21, 168-183.
16. Feldman, M., and, Levy, A.A., (2005) Allopolyploidy-a shaping force in the evolution of wheat genomes. Cytogenet. Genome Res. 109, 250-258.
17. Felsenstein, J., (1989) PHYLIP-Phylogeny Inference Package, version 3.2. Cladistics, 5, 164-166.
18. Fitch, W.M., (1971) Toward defining course of evolution-minimum change for a specific tree topology. Syst. Zool. 20, 406-416.
19. Furukawa, J., Yamaji, N., Wang, H., Mitani, N., Murata, Y., Sato, K., Katsuhara, M., Takeda, K., and, Ma, J.F., (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol. 48, 1081-1091.
20. Garvin, D.F., and, Carver, B.F., (2003) Role of the genotype in tolerance to acidity and aluminum toxicity. In Handbook of Soil Acidity (, Rengel, Z., ed). Boca Ration, FL: CRC Press, pp. 387-406.
21. Hamamoto, H., Hasegawa, K., Nakaune, R., Lee, Y.J., Makizumi, Y., Akutsu, K., and, Hibi, T., (2000) Tandem repeat of a transcriptional enhancer upstream of the sterol 14-demethylase gene (CYP51) in Penicillium digitatum. Appl. Environ. Microbiol. 66, 3421-3426.
22. Hanikenne, M., Talke, I.N., Haydon, M.J., Lanz, C., Nolte, A., Motte, P., Kroymann, J., Weigel, D., and, Kramer, U., (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature, 453, 391-395.
23. Hiradate, S., Ma, J.F., and, Matsumoto, H., (2007) Strategies of plants to adapt to mineral stresses in problem soils. Adv. Agron. 96, 65-132.
24. Hoekenga, O.A., Vision, T.J., Shaff, J.E., Monforte, A.J., Lee, G.P., Howell, S.H., and, Kochian, L.V., (2003) Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta x Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol. 132, 936-948.
25. Hoekenga, O.A., Maron, L.G., Canaado, G.M.A., etal. (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.
26. Horst, W.J., (1995) The role of the apoplasm in aluminum toxicity and resistance of higher plants. A review. Z. Pflanzenernahrung Bodenkunde, 158, 419-428.
27. Hu, S.W., Bai, G.H., Carver, B.F., and, Zhang, D.D., (2008) Diverse origins of aluminium-resistance sources in wheat. Theor. Appl. Genet. 118, 29-41.
28. Huang, C.F., Yamaji, N., Mitani, N., Yano, M., Nagamura, Y., and, Ma, J.F., (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell, 21, 655-667.
29. Iuchi, S., Koyama, H., Iuchi, A., Kobayashi, Y., Kitabayashi, S., Kobayashi, Y., Ikka, T., Hirayama, T., Shinozaki, K., and, 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.
30. Kochian, L.V., Hoekenga, O.A., and, 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.
31. Lagudah, E.S., Appels, R., and, McNeil, D., (1991) The Nor-D3 locus of Triticum tauschiinatural variation and genetic linkage to markers in chromosome 5. Genome, 34, 387-395.
32. Larsen, P.B., Tai, C.Y., Kochian, L.V., and, Howell, S.H., (1996) Arabidopsis mutants with increased sensitivity to aluminium. Plant Physiol. 110, 743-751.
33. Larsen, P.B., Geisler, M.J.B., Jones, C.A., Williams, K.M., and, Cancel, J.D., (2005) ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J. 41, 353-363.
34. Larsen, P.B., Cancel, J., Rounds, M., and, Ochoa, V., (2007) Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta, 225, 1447-1458.
35. Lelley, T., Stachel, M., Grausgruber, H., and, Vollmann, J., (2000) Analysis of relationships between Aegilops tauschii and the D genome of wheat utilizing microsatellites. Genome, 43, 661-668.
36. Luo, M., and, Dvorak, J., (1996) Molecular mapping of an aluminum tolerance locus on chromosome 4D of Chinese Spring wheat. Euphytica, 91, 31-35.
37. Ma, H.X., Bai, G.H., Carver, B., and, Zhou, L.L., (2005) Molecular mapping of a quantitative trait locus for aluminum tolerance in wheat cultivar Atlas 66. Theor. Appl. Genet. 112, 51-57.
38. Magalhaes, J.V., (2006) Aluminum tolerance genes are conserved between monocots and dicots. Proc. Natl Acad. Sci. USA, 103, 9749-9750.
39. Magalhaes, J.V., Garvin, D.F., Wang, Y.H., Sorrells, M.E., Klein, P.E., Schaffert, R.E., Li, L., and, Kochian, L.V., (2004) Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the Poaceae. Genetics, 167, 1905-1914.
40. Magalhaes, J.V., Liu, J., Guimaraes, C.T., etal. (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat. Genet. 39, 1156-1161.
41. Maron, L.G., Kirst, M., Mao, C., Milner, M.J., Menossi, M., and, Kochian, L.V., (2008) Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytol. 179, 116-128.
42. Maron, L.G., Pineros, M.A., Guimaraes, C.T., Magalhaes, J.V., Pleiman, J.K., Mao, C.Z., Shaff, J., Belicuas, S.N.J., and, Kochian, L.V., (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, 728-740.
43. Matos, M., Camacho, M.V., Perez-Flores, V., Pernaute, B., Pinto-Carnide, O., and, Benito, C., (2005) A new aluminum tolerance gene located on rye chromosome arm 7RS. Theor. Appl. Genet. 111, 360-369.
44. Matsumoto, H., (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int. Rev. Cytol. 200, 1-46.
45. McFadden, E.S., and, Sears, E.R., (1946) The origin of Triticum spelta and its free-threshing hexaploid relatives. J. Hered. 37, 81-89.
46. Miller, T.E., Reader, S.M., and, Ambrose, M.J., (2000) The Watkins wheat collection. Ann. Wheat Newsl. 46, 172.
47. Nguyen, B.D., Brar, D.S., Bui, B.C., Nguyen, T.V., Pham, L.N., and, Nguyen, H.T., (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, 583-593.
48. Ninamango-Carenas, F.E., Guimara, C.T., Martins, P.R., Parentoni, S.N., Carniero, N.P., Lopes, M.A., Moro, J.R., and, Paiva, E., (2003) Mapping QTLs for aluminum tolerance in maize. Euphytica, 130, 223-232.
49. Ogbonnaya, F.C., Halloran, G.M., and, Lagudah, E.S., (2005) D genome of wheat-60 years on from Kihara, Sears and McFadden. In Frontiers of Wheat Bioscience. Wheat Information Service Memorial Issue No. 100 (, Tsunewaki, K., ed). Yokohama, Japan: Kihara Memorial Yokohama Foundation for the Advancement of Life Sciences, pp. 205-220.
50. Papernik, L.A., Bethea, A.S., Singleton, T.E., Magalhaes, J.V., Garvin, D.F., and, Kochian, L.V., (2001) Physiological basis of reduced Al tolerance in ditelosomic lines of Chinese Spring wheat. Planta, 212, 829-834.
51. Pennisi, E., (2008) Deciphering the genetics of evolution. Science, 321, 760-763.
52. Pereira, J., Zhou, G., Delhaize, E., Richardson, T., and, Ryan, P.R., (2010) Engineering greater aluminum resistance in wheat by over-expressing TaALMT1. Ann. Bot. 106, 205-214.
53. Piffanelli, P., Ramsay, L., Waugh, R., Benabdelmouna, A., DHont, A., Hollricher, K., Jorgensen, J.H., Schulze-Lefert, P., and, Panstruga, R., (2004) A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature, 430, 887-891.
54. Pineros, M.A., Cancado, G.M.A., and, Kochian, L.V., (2008) Novel properties of the wheat aluminum tolerance organic acid transporter (TaALMT1) revealed by electrophysiological characterization in Xenopus oocytes: functional and structural implications. Plant Physiol. 147, 2131-2146.
55. Raman, H., Zhang, K., Cakir, M., etal. (2005) Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome, 48, 781-791.
56. Raman, H., Ryan, P.R., Raman, R., etal. (2008) Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). Theor. Appl. Genet. 116, 343-354.
57. Raman, H., Stodart, B., Ryan, P.R., Delhaize, E., Emebiri, L., Raman, R., Coombes, N., and, Milgate, A., (2010) Genome wide association analyses of common wheat (Triticum aestivum L) germplasm identifies multiple loci for aluminum resistance. Genome (in press).
58. Riede, C.R., and, Anderson, J.A., (1996) Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Sci. 36, 905-909.
59. Rockman, M.V., Hahn, M.W., Soranzo, N., Zimprich, F., Goldstein, D.B., and, Wray, G.A., (2005) Ancient and recent positive selection transformed opioid cis-regulation in humans. PLoS Biol. 3, 2208-2219.
60. Ryan, P.R., and, Delhaize, E., (2010) The convergent evolution of aluminum resistance in plants exploits a convenient currency. Funct. Plant Biol. 37, 275-284.
61. Ryan, P.R., DiTomaso, J.M., and, Kochian, L.V., (1993) Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44, 437-446.
62. Ryan, P.R., Delhaize, E., and, Randall, P.J., (1995a) Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Aust. J. Plant Physiol. 22, 531-536.
63. Ryan, P.R., Delhaize, E., and, Randall, P.J., (1995b) Characterisation ofAl-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta, 196, 103-110.
64. Ryan, P.R., Raman, H., Gupta, S., Horst, W.J., and, Delhaize, E., (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol. 149, 340-351.
65. Salamini, F., Ozkan, H., Brandolini, A., Schafer-Pregl, R., and, Martin, W., (2002) Genetics and geography of wild cereal domestication in the Near East. Nat. Rev. Genet. 3, 429-441.
66. Sasaki, T., Yamamoto, Y., Ezaki, B., Katsuhara, M., Ahn, S.J., Ryan, P.R., Delhaize, E., and, Matsumoto, H., (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37, 645-653.
67. Sasaki, T., Ryan, P.R., Delhaize, E., etal. (2006) Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant Cell Physiol. 47, 1343-1354.
68. Schunmann, P.H.D., Richardson, A.E., Vickers, C.E., and, Delhaize, E., (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol. 136, 4205-4214.
69. Shabalina, S.A., Ogurtsov, A.Y., Kondrashov, V.A., and, Kondrashov, A.S., (2001) Selective constraint in intergenic regions of human and mouse genomes. Trends Genet. 17, 373-376.
70. Sivaguru, M., and, Horst, W.J., (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone of Zea mays L. Plant Physiol. 116, 155-163.
71. Slootmaker, L.A.J., (1974) Tolerance to high soil acidity in wheat related species, rye and triticale. Euphytica, 23, 505-513.
72. Tang, Y., Sorrells, M.E., Kochian, L.V., and, Garvin, D.F., (2000) Identification of RFLP markers linked to the barley aluminum tolerance gene Alp. Crop Sci. 40, 778-782.
73. Taylor, G.J., (1988) The physiology of aluminum tolerance in higher plants. Commun. Soil Sci. Plant Anal. 19, 1179-1194.
74. Taylor, G.J., (1991) Current views of the aluminum stress response: the physiological basis of tolerance. Curr. Top. Plant Biochem. Physiol. 10, 57-93.
75. Toki, S., Hara, N., Ono, K., Onodera, H., Tagiri, A., Oka, S., and, Tanaka, H., (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J. 47, 969-976.
76. Tung, J., Primus, A., Bouley, A.J., Severson, T.F., Alberts, S.C., and, Wray, G.A., (2009) Evolution of a malaria resistance gene in wild primates. Nature, 460, 388-391.
77. Von Uexküll, H.R., and, Mutert, E., (1995) Global extent, development and economic impact of acid soils. Plant Soil, 171, 1-15.
78. Vinces, M.D., Legendre, M., Caldara, M., Hagihara, M., and, Verstrepen, K.J., (2009) Unstable tandem repeats in promoters confer transcriptional evolvability. Science, 324, 1213-1216.
79. Wang, J.P., Raman, H., Zhou, M.X., Ryan, P.R., Delhaize, E., Hebb, D.M., Coombes, N., and, Mendham, N., (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminum tolerance in barley (Hordeum vulgare L.). Theor. Appl. Genet. 115, 265-276.
80. Wittkopp, P.J., (2006) Evolution of cis-regulatory sequence and function in Diptera. Heredity, 97, 139-147.
81. Wray, G.A., Hahn, M.W., Abouheif, E., Balhoff, J.P., Pizer, M., Rockman, M.V., and, Romano, L.A., (2003) The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 20, 1377-1419.
82. Yamaji, N., Huang, C.F., Nagao, S., Yano, M., Sato, Y., Nagamura, Y., and, Ma, J.F., (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell, 21, 3339-3349.
83. 3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. Plant Cell Physiol. 49, 1316-1330.
84. Zhou, L.L., Bai, G.H., and, Ma, H.X., (2007) Quantitative trait loci for aluminum resistance in wheat. Mol Breed. 19, 153-161.
85. Zimprich, A., Kraus, J., Woltje, M., Mayer, P., Rauch, E., and, Hollt, V., (2000) An allelic variation in the human prodynorphin gene promoter alters stimulus-induced expression. J. Neurochem. 74, 472-477.