The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells

Plant Physiology

Volumn 142, Issue 3, 2006, Pages 1294-1303

  Ligaba, Ayalew ^a   Katsuhara, Maki ^a   Ryan, Peter R ^b   Shibasaka, Mineo ^a   Matsumoto, Hideaki ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM; CELLS; PLANTS (BOTANY); TOBACCO; TOXICITY;

CITRATE EFFLUX; MALATE EFFLUX; ORGANIC ANIONS; XENOPUS LAEVIS OOCYTES;

GENES;

ALUMINUM; CELLS; GENES; TOBACCO; TOXICITY; WHEAT;

BRASSICA NAPUS; NICOTIANA TABACUM; TRITICUM AESTIVUM; XENOPUS LAEVIS;

EID: 33751078302     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.106.085233     Document Type: Article

References (54)

1. Anoop VM, Basu U, McCammon MT, McAlister-Henn L, Taylor GJ (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol 132: 2205-2217
2. Chomezynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159
3. de la Fuente JM, Ramírez-Rodríguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276: 1566-1568
4. Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107: 315-321
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. Proc Natl Acad Sci USA 101: 15249-15254
6. Delhaize E, Ryan PR, Randall P (1993) Aluminium tolerance in wheat (Triticum aestivum L.). II. Aluminium-stimulated excretion of malic acid from root apices. Plant Physiol 103: 695-702
7. Ermolayev V, Weschki W, Manteuffel R (2003) Comparison of Al-induced gene expression in sensitive and tolerant soybean cultivars. J Exp Bot 54: 2745-2756
8. Ezaki B, Yamamoto Y, Matsumoto H (1995) Cloning and sequencing of the cDNAs induced by aluminium treatment and Pi starvation in tobacco cultured cells. Physiol Plant 93: 11-18
9. Foy CD, Chaney RL, White MC (1978) The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29: 511-566
10. Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil root interface is enhanced. Plant Soil 70: 107-124
11. Hoekenga OA, Maron LG, Cançado GMA, Piñeros MA, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, et al (2006) AtALMT1 (At1g08430) is a novel, essential factor for aluminum tolerance in Arabidopsis thaliana and encodes an aluminum-activated malate transporter. Proc Natl Acad Sci USA 103: 9734-9743
12. Hoekenga OA, Vision TJ, Shaff JE, Monforte AJ, Lee GP, Howell SH, Kochian LV (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
13. Hoffland E, Findenegg GR, Nelemans JA (1989) Utilization of rock phosphate by rape. Plant Soil 113: 155-160
14. Hoffland E, Van de Boogaard R, Nelemans JA, Findenegg GR (1992) Biosynthesis and root exudation of citric and malic acid in phosphate starved rape plants. New Phytol 122: 675-680
15. Horst WJ (1995) The role of the apoplast in aluminum toxicity and resistance of higher plants: a review. Z Pflanzenernaehr Bodenkd 158: 419-428
16. Kataoka T, Stekelenburg A, Nakanishi TM, Delhaize E, Ryan PR (2002) Several lanthanides activate malate efflux from roots of aluminium tolerant wheat. Plant Cell Environ 25: 453-460
17. Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant Cell Physiol 43: 885-893
18. Kinraide TB, Parker DR, Zobel RW (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
19. Kispal G, Rosenkrantz M, Guarente L, Srere PA (1988) Metabolic changes in Saccharomyces cerevisiae strains lacking citrate synthases. J Biol Chem 263: 11145-11149
20. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 46: 237-260
21. Kochian LV, Piñeros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274: 175-195
22. Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R (2001) Aluminum activates a citrate-permeable anion channel in the Al-sensitive zone of the maize root apex: a comparison between an Al-sensitive and an Al-tolerant cultivar. Plant Physiol 126: 397-410
23. Koyama H, Kawamura A, Kihara T, Hara T, Takita E, Shibata D (2000) Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphorus limited soil. Plant Cell Physiol 41: 1030-1037
24. Ligaba A, Shen H, Shibata K, Yamamoto Y, Tanakamaru S, Matsumoto H (2004) The role of phosphorus in aluminum-induced citrate and malate exudation in rape (Brassica napus L.). Physiol Plant 120: 575-584
25. Lipton D, Blanchar R, Blevins D (1987) Citrate, malate and succinate concentration in exudates from P sufficient and P stressed Medicago sativa L. seedlings. Plant Physiol 85: 315-317
26. Ma JF, Ryan PR, Delhaize E (2001) Aluminum tolerance in plants and the complexing role of organic acids. Trends Plant Sci 66: 273-278
27. Ma JF, Zheng SJ, Matsumoto H (1997a) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 38: 1019-1025
28. Ma JF, Zheng SJ, Matsumoto H, Hiradate S (1997b) Detoxifying aluminum with buckwheat. Nature 390: 569-570
29. Ma Z, Miyasaka SC (1998) Oxalate exudation by taro in response to Al. Plant Physiol 118: 861-865
30. Magalhaes JV, Garvin DF, Wang Y, Sorrells ME, Klein PE, Schaffert RE, Li L, Kochian LV (2004) Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the poaceae. Genetics 167: 1905-1914
31. Matsumoto H (2002) Metabolism of organic acids and metal tolerance in plants exposed to aluminum. In MNV Prasad, K Strzalka, eds, Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Kluwer Academic Publisher, Dordrecht, The Netherlands, pp 95-109
32. Miyasaka SC, Buta JG, Howell RK, Foy CD (1991) Mechanism of aluminium tolerance in snapbeans: root exudates of citric acid. Plant Physiol 96: 737-743
33. Neumann G, Massonneau A, Maritinoia E, Roemheld V (1999) Physiological adaptation of phosphorous deficiency during proteoid root development in white lupin. Planta 208: 373-382
34. Osawa H, Matsumoto H (2002) Aluminum triggers malate independent potassium release via ion channels from the root apex in wheat. Planta 215: 405-412
35. Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminium-tolerance mechanism in maize (Zea mays L.). Planta 196: 788-795
36. 3+-induced anion channels. Plant Physiol 125: 292-305
37. Piñeros MA, Magalhaes JV, Alve VMC, Kochian LV (2002) The physiology and biophysics of Al tolerance mechanism based on root citrate exudation in maize. Plant Physiol 129: 1194-1206
38. Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256: 385-387
39. Raman H, Zhang K, Cakir M, Appels R, Garvin DF, Maron LG, Kochian LV, Moroni JS, Raman R, Imtiaz M, et al (2005) Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48: 781-791
40. Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116: 409-418
41. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52: 527-560
42. Ryan PR, Delhaize E, Randall PJ (1995a) Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196: 103-110
43. Ryan PR, Delhaize E, Randall PJ (1995b) Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Aust J Plant Physiol 22: 531-536
44. Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman S (1997) Aluminum activates an anion channel in the apical cells of wheat roots. Proc Natl Acad Sci USA 94: 6547-6552
45. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467
46. 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. Plant J 37: 645-653
47. Snowden KC, Richards KD, Gardner RC (1995) Aluminum-induced genes (induction by toxic metals, low calcium, and wounding and pattern of expression in root tips). Plant Physiol 107: 341-348
48. Taylor GJ (1991) Current views of the aluminum stress response; the physiological basis of tolerance. Curr Top Plant Biochem Physiol 10: 57-93
49. Tesfaye M, Temple SJ, Allan DJ, Vance CP, Samac DA (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol 127: 1836-1844
50. 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 Physiol 46:812-816
51. Yamamoto Y, Rikiishi S, Chang YC, Ono K, Kasai M, Matsumoto H (1994) Quantitative estimation of aluminum toxicity in cultured tobacco cells: correlation between aluminum uptake and growth inhibition. Plant Cell Physiol 35: 575-583
52. Yang ZM, Sivaguru M, Horst JW, Matsumoto H (2000) Aluminium tolerance is achieved by exudation of citric acid from roots of soybean (Glycine max). Physiol Plant 110: 72-77
53. Zhang W-H, Ryan PR, Tyerman S (2001) Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. Plant Physiol 125: 1459-1472
54. Zheng SJ, Ma JF, Matsumoto H (1998) High aluminium resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol 117: 745-751