Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils

Plant Physiology

Volumn 161, Issue 3, 2013, Pages 1347-1361

  Liang, Cuiyue ^a,b   Piñeros, Miguel A ^b   Tian, Jiang ^a   Yao, Zhufang ^a   Sun, Lili ^c   Liu, Jiping ^b   Shaff, Jon ^b   Coluccio, Alison ^b   Kochian, Leon V ^b   Liao, Hong ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b Department of Obstetrics Gynecology   (United States)

^c INSTITUTE OF TROPICAL BIOSCIENCE AND BIOTECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874640804     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.208934     Document Type: Article

References (82)

1. Ackerman MJ, Wickman KD, Clapham DE (1994) Hypotonicity activates a native chloride current in Xenopus oocytes. J Gen Physiol 103: 153-179
2. Archambault DJ, Zhang GC, Taylor GJ (1997) Spatial variation in the kinetics of aluminium (Al) uptake in roots of wheat (Triticum aestivum L.) exhibiting differential resistance to Al: evidence for metabolism dependent exclusion of Al. J Plant Physiol 151: 668-674
3. Basu U, Good AG, Aung T, Slaski J, Basu A, Briggs KG, Taylor GJ (1999) A 23-kDa root exudates polypeptide co-segregates with aluminum resistance in Triticum aestivum. Physiol Plant 106: 53-61
4. Bertin C, Yang X, Weston L (2003) The role of root exudates and allelo chemicals in the rhizosphere. Plant Soil 256: 67-83
5. Cranados G, Pandey S, Ceballos H (1992) Response to selection for tolerance to acid soils in a tropical maize population. Crop Sci 33: 936-940
6. Davies DD (1973) Control of and by pH. Symp Soc Exp Biol 27: 513-529
7. Degenhardt J, Larsen PB, Howell SH, Kochian LV (1998) Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminuminduced increase in rhizosphere pH. Plant Physiol 117: 19-27
8. Delhaize E, Craig S, Beaton CD, Bennet RJ, Jagadish VC, Randall PJ (1993a) Aluminum tolerance in wheat (Triticum aestivum L.). I. Uptake and distribution of aluminum in root apices. Plant Physiol 103: 685-693
9. Delhaize E, Ryan PR, Randall PJ (1993b) Aluminium tolerance in wheat (Triticum aestivum L.). II. Aluminium-stimulated excretion of malic acid from root apices. Plant Physiol 103: 695-702
10. Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR, Richardson AE (2009) Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotechnol J 7: 391-400
11. Dong D, Peng X, Yan X (2004) Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes. Physiol Plant 122: 190-199
12. Elstner EF, Wagner GA, Schutz W (1988) Activated oxygen in green plants in relation to stress situations. Curr Top Plant Biochem Physiol 7: 159-187
13. Fukuda T, Saito A, Wasaki J, Shinano T, Osaki M (2007) Metabolic alterations proposed by proteome in rice roots grown under low P and high Al concentration under low pH. Plant Sci 172: 1157-1165
14. Gaume A, Machler F, Frossard E (2001) Aluminum resistance in two cultivars of Zea mays L: root exudation of organic acid and influence of phosphorus nutrition. Plant Soil 234: 73-81
15. Gruber BD, Ryan PR, Richardson AE, Tyerman SD, Ramesh S, Hebb DM, Howitt SM, Delhaize E (2010) HvALMT1 from barley is involved in the transport of organic anions. J Exp Bot 61: 1455-1467
16. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237: 173-195
17. Hoekenga OA, Maron LG, Piñeros MA, Cançado GMA, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, 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
18. Hoffland E, Findenegg GR, Nelemans JA (1989) Utilization of rock phosphate by rape. Plant Soil 113: 155-160
19. Hoffland E, Van den Boogard R, Nelemans J, Findenegg G (1992) Biosynthesis and root exudation of citric and malic acids in phosphatestarved rape plants. New Phytol 122: 675-680
20. Horst WJ, Schmoh N, Kollmeier M, Balulška F, Sivaguru M (1999) Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant Soil 215: 163-174
21. Huang CF, Yamaji N, Ma JF (2010) Knockout of a bacterial-type ATPbinding cassette transporter gene, AtSTAR1, results in increased aluminum sensitivity in Arabidopsis. Plant Physiol 153: 1669-1677
22. 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. Plant Cell 21: 655-667
23. 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
24. Jemo M, Abaidoo RC, Nolte C, Horst WJ (2007) Aluminum resistance of cowpea as affected by phosphorus-deficiency stress. J Plant Physiol 164: 442-451
25. Kereszt A, Li D, Indrasumunar A, Nguyen CD, Nontachaiyapoom S, Kinkema M, Gresshoff PM (2007) Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat Protoc 2: 948-952
26. Kinraide TB (1998) Three mechanisms for the calcium alleviation of mineral toxicities. Plant Physiol 118: 513-520
27. 2+upon root elongation. Eur J Soil Sci 54: 323-333
28. Kobayashi Y, Hoekenga OA, Itoh H, Nakashima M, Saito S, Shaff JE, Maron LG, Piñeros MA, Kochian LV, 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
29. Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55: 459-493
30. Kovermann P, Meyer S, Hörtensteiner 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. Plant J 52: 1169-1180
31. Koyama H, Toda T, Hara T (2001) Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin-Ca interaction may play an important role in proton rhizotoxicity. J Exp Bot 52: 361-368
32. 2reduction) with two cultivars of Sorghum mutants. Soil Biol Biochem 18: 201-207
33. 2reduction) with two cultivars of Sorghum mutants. Soil Biol Biochem 20: 157-162
34. Larsen PB, Degenhardt J, Tai CY, Stenzler LM, Howell SH, Kochian LV (1998) Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol 117: 9-18
35. Liang CY, Tian J, Lam HM, Lim BL, Yan XL, Liao H (2010) Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiol 152: 854-865
36. Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance: exudation of specific organic acids from different regions of the intact root system. Plant Physiol 141: 674-684
37. 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 Physiol 142: 1294-1303
38. Ligaba A, Maron LG, Shaff J, Kochian LV, Piñeros MA (2012) Maize ZmALMT2 is a root anion transporter that mediates constitutive root malate efflux. Plant Cell Environ 35: 1185-1200
39. Ligaba A, Shen H, Shibata K, Yamamoto Y, Tanakamaru S, Matsumoto H (2004) The role of phosphorus in aluminium-induced citrate and malate exudation from rape (Brassica napus). Physiol Plant 120: 575-584
40. Lipton DS, Blanchar RW, Blevins DG (1987) Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiol 85: 315-317
41. Liu J, 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. Plant J 57: 389-399
42. Lü J, Gao X, Dong Z, Yi J, An L (2012) Improved phosphorus acquisition by tobacco through transgenic expression of mitochondrial malate dehydrogenase from Penicillium oxalicum. Plant Cell Rep 31: 49-56
43. Ma JF (2000) Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol 41: 383-390
44. Ma JF, Taketa S, Yang ZM (2000) Aluminum tolerance genes on the short arm of chromosome 3R are linked to organic acid release in Triticale. Plant Physiol 122: 687-694
45. Maron LG, Piñeros MA, Guimarães 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. Plant J 61: 728-740
46. Martínez-Camacho JL, la Vara LG, Hamabata A, Mora-Escobedo R, Calderón-Salinas V (2004) A pH-stating mechanism in isolated wheat (Triticum aestivum) aleurone layers involves malic acid transport. J Plant Physiol 161: 1289-1298
47. McCormick LH, Borden FY (1972) Phosphate fixation by aluminium in plant roots. Soil Sci Soc Am J 36: 779-802
48. Meriga B, Reddy BK, Rao KR, Reddy LA, Kishor PB (2004) Aluminiuminduced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161: 63-68
49. Meyer S, Mumm P, Imes D, Endler A, Weder B, Al-Rasheid KAS, Geiger D, Marten I, Martinoia E, Hedrich R (2010) AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63: 1054-1062
50. Pellet DM, Papernik LA, Kochian LV (1996) Multiple aluminum resistance mechanisms in wheat: roles of root apical phosphate and malate exudation. Plant Physiol 112: 591-597
51. Piñeros MA, Cançado GMA, Kochian LV (2008a) 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
52. Piñeros MA, Cançado GMA, Maron LG, Lyi SM, Menossi M, Kochian LV (2008b) Not all ALMT1-type transporters mediate aluminum-activated organic acid responses: the case of ZmALMT1, an anion-selective transporter. Plant J 53: 352-367
53. Ramos-Díaz A, Brito-Argáez L, Munnik T, Hernández-Sotomayor SMT (2007) Aluminum inhibits phosphatidic acid formation by blocking the phospholipase C pathway. Planta 225: 393-401
54. Rao IM, Zeigler RS, Vera R, Sarkarung S (1993) Selection and breeding for acid-soil tolerance in crops. Bioscience 43: 454-465
55. Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148: 1547-1556
56. Runge-Metzger A (1995) Closing the cycle: obstacles to efficient P management for improved global security. In H Tiessen, ed, Phosphorus in the Global Environment: Transfers, Cycles and Management. John Wiley & Sons, New York, pp 27-42
57. Ryan PR, Delhaize E, Jones D (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52: 527-560
58. Ryan PR, Shaff JE, Kochian LV (1992) Aluminum toxicity in roots: correlation among ionic currents, ion fluxes, and root elongation in aluminumsensitive and aluminum-tolerant wheat cultivars. Plant Physiol 99: 1193-1200
59. Sas L, Rengel Z, Tang C (2001) Excess cation uptake, and extrusion of protons and organic acid anions by Lupinus albus under phosphorus deficiency. Plant Sci 160: 1191-1198
60. 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
61. Sawaki Y, Iuchi S, Kobayashi Y, Kobayashi Y, Ikka T, Sakurai N, Fujita M, Shinozaki K, Shibata D, Kobayashi M, et al (2009) STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol 150: 281-294
62. Schubert S, Schubert E, Mengel K (1990) Effect of low pH of the root medium on proton release, growth, and nutrient uptake of field beans (Vicia faba). Plant Soil 124: 239-244
63. Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330: 207-214
64. Sivaguru M, Baluška F, Volkmann D, Felle HH, Horst WJ (1999) Impacts of aluminum on the cytoskeleton of the maize root apex: short-term effects on the distal part of the transition zone. Plant Physiol 119: 1073-1082
65. Sivaguru M, Fujiwara T, Šamaj J, Baluska F, Yang Z, Osawa H, Maeda T, Mori T, Volkmann D, Matsumoto H (2000) Aluminum-induced 1-3-β-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata: a new mechanism of aluminum toxicity in plants. Plant Physiol 124: 991-1006
66. Sun QB, Shen RF, Zhao XQ, Chen RF, Dong XY (2008) Phosphorus enhances Al resistance in Al-resistant Lespedeza bicolor but not in Al-sensitive L. cuneata under relatively high Al stress. Ann Bot (Lond) 102: 795-804
67. Tan K, Keltjens WG (1990a) Interaction between aluminium and phosphorus in sorghum plants. I. Studies with the aluminium sensitive sorghum genotype TAM428. Plant Soil 124: 15-23
68. Tan K, Keltjens WG (1990b) Interaction between aluminium and phosphorus in sorghum plants. II. Studies with the aluminium tolerant sorghum genotype SCO283. Plant Soil 124: 25-32
69. Tokimasa T, North RA (1996) Effects of barium, lanthanum and gadolinium on endogenous chloride and potassium currents in Xenopus oocytes. J Physiol 496: 677-686
70. Tzfira T, Tian GW, Lacroix B, Vyas S, Li JX, Leitner-Dagan Y, Krichevsky A, Taylor T, Vainstein A, Citovsky V (2005) pSAT vectors: a modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol Biol 57: 503-516
71. Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants securing a nonrenewable resource. New Phytol 157: 423-447
72. von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171: 1-15
73. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132: 44-51
74. 2+concentrations. J Plant Nutr 12: 1379-1394
75. Yamaguchi Y, Yamamoto Y, Matsumoto H (1999) Cell death process initiated by a combination of aluminium and iron in suspension cultures of tobacco cells (Nicotiana tabacum): apoptosis-like cell death mediated by calcium and proteinase. Soil Sci Plant Nutr 45: 647-657
76. Yamaji N, Huang CF, Nagao S, Yano M, Sato Y, Nagamura Y, Ma JF (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21: 3339-3349
77. Yan F, Schubert S, Mengel K (1992) Effect of low root medium pH on net proton release, root respiration, and root growth of corn (Zea mays L.) and broad bean (Vicia faba L.). Plant Physiol 99: 415-421
78. Yan X, Lynch JP, Beebe SE (1995) Genetic variation for phosphorus efficiency of common bean in contrasting soil types. I. Vegetative response. Crop Sci 35: 1086-1093
79. Yang JL, Zheng SJ, He YF, Matsumoto H (2005) Aluminium resistance requires resistance to acid stress: a case study with spinach that exudes oxalate rapidly when exposed to Al stress. J Exp Bot 56: 1197-1203
80. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
81. Zhao J, Fu J, Liao H, HuMY, Nian H, Hu Y, Qiu L, Dong Y, Yan X (2004) Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm. Chin Sci Bull 49: 1611-1620
82. Zheng SJ, Yang JL, He YF, Yu XH, Zhang L, You JF, Shen RF, Matsumoto H (2005) Immobilization of aluminum with phosphorus in roots is associated with high aluminum resistance in buckwheat. Plant Physiol 138: 297-303