The convergent evolution of aluminium resistance in plants exploits a convenient currency

Functional Plant Biology

Volumn 37, Issue 4, 2010, Pages 275-284

  Ryan, Peter R ^a   Delhaize, Emmanuel ^a  

^a CSIRO   (Australia)

Author keywords

Acid soil; Aluminum; Anion channel; Citrate; Malate; Tolerance; Toxicity

Indexed keywords

ACID SOILS; ACIDIC SOILS; ALUMINIUM RESISTANCES; ALUMINUM ANIONS; APOPLASTS; ARABIDOPSIS; BRASSICA NAPUS; CONVERGENT EVOLUTION; GENE CONTROLLING; HORDEUM VULGARE; IN-PLANTS; OIL SEED RAPE; ORGANIC ANIONS; ORYZA SATIVA; PLANT GROWTH; PLANT PRODUCTION; PROTEIN EXPRESSIONS; PROTEIN FUNCTIONS; RHIZOTOXICITY; SECALE CEREALE; SOLUBLE ALUMINIUM; TRANSPORT PROTEINS; WHEAT (TRITICUM AESTIVUM L.);

BIOCHEMISTRY; GENES; MOLECULAR BIOLOGY; NEGATIVE IONS; PLANT LIFE EXTENSION; PLANTS (BOTANY); PROTEINS; SOILS; TOXICITY;

ALUMINUM;

ALUMINUM; CONVERGENT EVOLUTION; CROP PLANT; DETOXIFICATION; GENE EXPRESSION; GROWTH RATE; PHYTOTOXICITY; PROTEIN; TOLERANCE;

ARABIDOPSIS; BRASSICA NAPUS; HORDEUM; HORDEUM VULGARE SUBSP. VULGARE; ORYZA SATIVA; SECALE CEREALE; TRITICUM AESTIVUM;

EID: 77950236896     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP09261     Document Type: Article

References (76)

1. BerzonskyWA,KimberG(1986) Tolerance of Triticum species to aluminum. Plant Breeding 97, 275-278. doi:10.1111/j.1439-0523.1986.tb01066.x
2. Collins NC, Shirley NJ, Saeed M, Pallotta M, Gustafson JP (2008)An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179, 669-682. doi:10.1534/genetics. 107.083451
3. Cosic T, Poljak M, Custic M, Rengel Z (1994) Aluminum tolerance of durum-wheat germplasm. Euphytica 78, 239-243. doi:10.1007/ BF00027522
4. Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiology 103, 695-702.
5. Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proceedings of the National Academy of Sciences of the United States of America 101, 15249-15254. doi:10.1073/pnas. 0406258101
6. Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Letters 581, 2255-2262. doi:10.1016/j.febslet.2007.03.057 (Pubitemid 46726299)
7. Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316, 1862-1866. doi:10.1126/science.1143986 (Pubitemid 47025777)
8. Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiology 144, 197-205. doi:10.1104/pp.107.097162 (Pubitemid 46941624)
9. Felsenstein J (1985) Confidence-limits on phylogenies - an approach using the bootstrap. Evolution 39, 783-791. doi:10.2307/2408678
10. Fernie AR, Martinoia E (2009) Malate. Jack of all trades or master of a few? Phytochemistry 70, 828-832. doi:10.1016/j.phytochem.2009.04.023
11. Foy CD (1988) Plant adaptation to acid, aluminum-toxic soils. Communications in Soil Science and Plant Analysis 19, 959-987. doi:10.1080/00103628809367988
12. Fujii M, Yamaji N, Sato K, Ma JF (2009) Mechanism regulating HvAACT1 expression in barley. In 'Plant-soil interactions at low pH: a nutriomic approach. Proceedings of the 7th international symposium of plant-soil interactions at low pH'. (Eds H Liao, X Yan, LV Kochian) pp. 165-166. (South China University of Technology Press: Guangzhou
13. Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant & Cell Physiology48, 1081-1091. doi:10.1093/pcp/pcm091 (Pubitemid 47283661)
14. Garvin DF, Carver BF (2003) Role of the genotype in tolerance to acidity and aluminum toxicity. In 'Handbook of soil acidity'. (Ed. Z. Rengel) pp. 387-406. (Marcel Dekker Inc.: New York
15. Gruber BD (2009) Characterisation of the HvALMT1 gene from barley. PhD Thesis. The Australian National University, Canberra, ACT.
16. Hiradate S, Ma JF, Matsumoto H (2007) Strategies of plants to adapt to mineral stresses in problem soils. Advances in Agronomy 96, 65-132. doi:10.1016/S0065-2113(07)96004-6
17. HoekengaOA,MaronLG,PiñerosMA,CaņcadoGMA,Shaff JE, et al. (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 9738-9743. doi:10.1073/pnas.0602868103 (Pubitemid 43955894)
18. Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. The Plant Cell 21, 655-667. doi:10.1105/tpc.108.064543
19. Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou XF, Saier MH (2003) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. European Journal of Biochemistry 270, 799-813. doi:10.1046/j.1432-1033.2003. 03418.x (Pubitemid 36315323)
20. Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nature Genetics 33, 102-106. doi:10.1038/ng1063 (Pubitemid 36068691)
21. Kataoka T, Stekelenburg A, Nakanishi TM, Delhaize E, Ryan PR (2002) Several lanthanides activate malate efflux from roots of aluminiumtolerant wheat. Plant, Cell & Environment 25, 453-460. doi:10.1046/ j.0016-8025.2001.00821.x
22. Kinraide TB (1991) Identity of the rhizotoxic aluminium species. Plant and Soil 134, 167-178.
23. Kinraide TB (1994) Use of a Gouy-Chapman-Stern model for membranesurface electrical potential to interpret some features of mineral rhizotoxicity. Plant Physiology 106, 1583-1592.
24. Kobayashi Y, Hoekenga OA, Itoh H, Nakashima M, Saito S, Shaff JE, Maron LG, PiñerosMA,Kochian LV, KoyamaH(2007) Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiology 145, 843-852. doi:10.1104/pp.107.102335 (Pubitemid 350127620)
25. Kochian LV, Hoekenga OA, PiñerosMA(2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annual Review of Plant Biology 55, 459-493. doi:10.1146/ annurev.arplant.55. 031903.141655 (Pubitemid 38940940)
26. Konishi S, Ferguson IB, Putterill J (1988) Effect of acidic polypeptides on aluminiumtoxicityintubegrowthofpollenfromtea (CamelliasinensisL.). Plant Science 56, 55-59. doi:10.1016/0168-9452(88)90185-9
27. Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. The Plant Journal 52, 1169-1180.
28. Lance C, Rustin P (1984) The central role of malate in plant-metabolism. Physiologie Vegetale 22, 625-641.
29. Larsen PB, Geisler MJB, Jones CA, Williams KM, Cancel JD (2005) ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. The Plant Journal 41, 353-363. doi:10.1111/j.1365-313X.2004.02306.x (Pubitemid 40252755)
30. Larsen PB, Cancel J, Rounds M, 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. doi:10.1007/s00425-006- 0452-4 (Pubitemid 46632368)
31. Ligaba A, Katsuhara M, Ryan PR, Shibasaka M, Matsumoto H (2006) The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. Plant Physiology 142, 1294-1303. doi:10.1104/pp.106.085233.
32. Liu JP, Magalhaes JV, Shaff J, Kochian LV (2009) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. The Plant Journal 57, 389-399. doi:10.1111/j.1365-313X.2008.03696.x
33. Luttge U (1987) Carbon-dioxide and water demand- crassulacean acid metabolism (CAM), a versatile ecological adaptation exemplifying the need for integration in ecophysiological work. New Phytologist 106, 593-629. doi:10.1111/j.1469-8137.1987.tb00163.x
34. Ma JF, Hiradate S, Matsumoto H (1998) High aluminum resistance in buckwheat. II. Oxalic acid detoxifies aluminum internally. Plant Physiology 117, 753-759. doi:10.1104/pp.117.3.753
35. Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6, 273-278. doi:10.1016/S1360-1385(01)01961-6 (Pubitemid 33141638)
36. Magalhaes JV (2006) Aluminum tolerance genes are conserved between monocots and dicots. Proceedings of the National Academy of Sciences of the United States of America 103, 9749-9750. doi:10.1073/pnas. 0603957103
37. Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VMC, et al. (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genetics 39, 1156-1161. doi:10.1038/ng2074 (Pubitemid 47340643)
38. Maron LG, Pineros MA, Guimaraes CT, Magalhaes JV, Pleiman JK, Mao C, Shaff JE, Belicuas SNJ, Kochian LV (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. The Plant Journal 61, 728-740. doi:10.1111/ j.1365-313x.2009.04103.x
39. Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. Journal of Experimental Botany 58, 83-102. doi:10.1093/jxb/erl183 (Pubitemid 46026250)
40. Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. International Review of Cytology 200, 1-46. doi:10.1016/ S0074-7696(00)00001-2
41. Osmond CB (1976) Ion absorption and carbon metabolism in cells of higher plants. In 'Encyclopedia of plant physiology. New series. Vol.2'.(EdsULuttge, MGPitman)pp.347-372.(Springer-Verlag:Berlin
42. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annual Review of Genetics 34, 401-437. doi:10.1146/annurev.genet.34.1.401 (Pubitemid 32065927)
43. Piffanelli P, Ramsay L, Waugh R, Benabdelmouna A, D'Hont A, Hollricher K, Jorgensen JH, Schulze-Lefert P, Panstruga R (2004) A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430, 887-891. doi:10.1038/nature02781 (Pubitemid 39119215)
44. Piñeros MA, Caņcado GMA, Maron LG, Lyi SM, Menossi M, Kochian LV (2008) Not all ALMT1-type transporters mediate aluminum-activated organic acid responses: the case of ZmALMT1 - an anion-selective transporter. The Plant Journal 53, 352-367. doi:10.1111/j.1365-313X. 2007.03344.x
45. Poschenrieder C, Tolrà RP, Barcelo J (2005) A role for cyclic hydroxamates in aluminium resistance in maize? Journal of Inorganic Biochemistry 99, 1830-1836. doi:10.1016/j.jinorgbio.2005.05.017 (Pubitemid 41253770)
46. Putterill JJ, Gardner RC (1988) Proteins with the potential to protect plants from Al3+ toxicity. Biochimica et Biophysica Acta 1988, 137-145.
47. Raman H, Ryan PR, Raman R, Stodart BJ, Zhang K, et al. (2008) Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). Theoretical and Applied Genetics 116, 343-354. doi:10.1007/s00122-007-0672-4
48. Reumann S, Weber APM (2006) Plant peroxisomes respire in the light: some gaps of the photorespiratory C-2 cycle have become filled - others remain. Biochimica et Biophysica Acta - Molecular. Cell Research 1763, 1496-1510.
49. Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. The Plant Cell 14, 1787-1799. doi:10.1105/tpc.001495
50. Rudrappa T,CzymmekKJ, ParePW,BaisHP(2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiology 148, 1547-1556. doi:10.1104/pp.108.127613 (Pubitemid 352847518)
51. Ryan PR, DiTomaso JM, Kochian LV (1993) Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. Journal of Experimental Botany 44, 437-446. doi:10.1093/jxb/44.2.437
52. Ryan PR, Delhaize E, Randall PJ (1995) Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103-110. doi:10.1007/BF00193223
53. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527-560. doi:10.1146/ annurev.arplant.52.1.527
54. Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiology 149, 340-351. doi:10.1104/ pp.108.129155
55. Saitou N, Nei M (1987) The neighbour-joining method - a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406-425. SakanoK(1998) Revision of biochemical pH-stat: involvement of alternative pathway metabolisms. Plant & Cell Physiology 39, 467-473.
56. Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. The Plant Journal 37, 645-653. doi:10.1111/j.1365- 313X.2003.01991.x
57. Sasaki T, Ryan PR, Delhaize E, Hebb DM, Ogihara Y, et al. (2006) Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant & Cell Physiology 47, 1343-1354. doi:10.1093/pcp/pcl002 (Pubitemid 44684533)
58. Sawaki Y, Iuchi S, Kobayashi Y, Kobayashi Y, Ikka T, et al. (2009) STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiology 150, 281-294. doi:10.1104/ pp.108.134700
59. Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone of Zea mays L. Plant Physiology 116, 155-163. doi:10.1104/pp.116.1.155
60. Slootmaker LAJ (1974) Tolerance to high soil acidity in wheat related species, rye and triticale. Euphytica 23, 505-513. doi:10.1007/ BF00022471
61. TamuraK,DudleyJ, NeiM,KumarS(2007)MEGA4:molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596-1599. doi:10.1093/molbev/msm092 (Pubitemid 47236692)
62. Taylor GJ (1988a) The physiology of aluminum phytotoxicity. In 'Metal ions in biological systems. Vol. 24'. (Eds H Sigel, A Sigel) pp. 123-163. (Marcell Dekker: New York
63. Taylor GJ (1988b) The physiology of aluminum tolerance in higher plants. Communications in Soil Science and Plant Analysis 19, 1179-1194. doi:10.1080/00103628809368004
64. Taylor GJ (1991) Current views of the aluminum stress response: the physiological basis of tolerance. Current Topics in Plant Biochemistry and Physiology 10, 57-93.
65. Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiology 101, 339-344.
66. Wang JP, Raman H, Zhou MX, Ryan PR, Delhaize E, Hebb DM, Coombes N, Mendham N (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 115, 265-276. doi:10.1007/s00122- 007-0562-9 (Pubitemid 47012431)
67. Weber APM, Fischer K (2007) Making the connections - the crucial role of metabolite transporters at the interface between chloroplast and cytosol. FEBS Letters 581, 2215-2222. doi:10.1016/j.febslet.2007. 02.010 (Pubitemid 46726292)
68. Wicker T, Yahiaoui N, Keller B (2007) Illegitimate recombination is a major evolutionary mechanism for initiating size variation in plant resistance genes. The Plant Journal 51, 631-641. doi:10.1111/j.1365-313X.2007. 03164.x (Pubitemid 47231186)
69. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA (2003) The evolution of transcriptional regulation in eukaryotes. Molecular Biology and Evolution 20, 1377-1419. doi:10.1093/molbev/msg140 (Pubitemid 37086669)
70. Yamaguchi M, Sasaki T, Sivaguru M, Yamamoto Y, Osawa H, Ahn SJ, Matsumoto H (2005) Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). Plant & Cell Physiology 46, 812-816. doi:10.1093/pcp/pci083 (Pubitemid 40793829)
71. Yamaji N, Huan CF, Nagao S, Yano M, Sato Y, Nagamura Y, Ma JF (2009) A zinc finger transcription factor ART1 regulates multiple genes involved in aluminum tolerance in rice. The Plant Cell 21, 3339-3349. doi:10.1105/tpc.109. 070771
72. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2003) Oxidative stress triggered by aluminum in plant roots. Plant and Soil 255, 239-243. doi:10.1023/A:1026127803156 (Pubitemid 37399610)
73. Yokosho K, Yamaji N, Ma JF (2009a) Functional analysis of OsFRDL4, a citrate transporter gene induced by aluminum. In 'Plant-soil interactions at low pH: a nutriomic approach. Proceedings of the 7th international symposium of plant-soil interactions at low pH'. (EdsHLiao,XYan, LV Kochian) pp. 161-162. (South China University of Technology Press: Guangzhou
74. Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF (2009b) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiology 149, 297-305. doi:10.1104/pp.108.128132
75. Zhang W, Ryan PR, Sasaki T, Yamamoto Y, Sullivan W, Tyerman SD (2008) Characterization of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. Plant & Cell Physiology 49, 1316-1330. doi:10.1093/pcp/pcn107
76. Zheng SJ, Ma JF, Matsumoto H (1998) High aluminum resistance in buckwheat. 1. Al-induced specific secretion of oxalic acid from root tips. Plant Physiology 117, 745-751. doi:10.1104/pp.117.3.745