Citrate exudation induced by aluminum is independent of plasma membrane H+-ATPase activity and coupled with potassium efflux from cluster roots of phosphorus-deficient white lupin
详细信息    查看全文
  • 作者:Houqing Zeng (1) (2)
    Xumeng Feng (1)
    Baolan Wang (3)
    Yiyong Zhu (1)
    Qirong Shen (1)
    Guohua Xu (1)
  • 关键词:Al tolerance ; Citrate exudation ; Plasma membrane H+ ; ATPase ; K+ efflux ; Cluster root ; White lupin (Lupinus albus)
  • 刊名:Plant and Soil
  • 出版年:2013
  • 出版时间:2 - May 2013
  • 年:2013
  • 卷:366
  • 期:1
  • 页码:389-400
  • 全文大小:458KB
  • 参考文献:1. Ahn SJ, Sivaguru M, Osawa H, Chung GC, Matsumoto H (2001) Aluminum inhibits the H+-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots. Plant Physiol 126:1381-390 CrossRef
    2. Ahn SJ, Rengel Z, Matsumoto H (2004) Aluminum-induced plasma membrane surface potential and H+-ATPase activity in near-isogenic wheat lines differing in tolerance to aluminum. New Phytol 162:71-9 CrossRef
    3. Bose J, Babourina O, Shabala S, Rengel Z (2010a) Aluminum-dependent dynamics of ion transport in / Arabidopsis: specificity of low pH and aluminum responses. Physiol Plant 139:401-12
    4. Bose J, Babourina O, Shabala S, Rengel Z (2010b) Aluminium-induced ion transport in / Arabidopsis: the relationship between Al tolerance and root ion flux. J Exp Bot 61:3163-175 CrossRef
    5. Cheng L, Bucciarelli B, Shen J, Allan D, Vance CP (2011) Update on white lupin cluster root acclimation to phosphorus deficiency. Plant Physiol 156:1025-032 CrossRef
    6. 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 Physiol 48:1081-091 CrossRef
    7. Gassmann W, Schroeder JI (1994) Inward-rectifying K+ channels in root hairs of wheat (a mechanism for aluminum-sensitive low-affinity K+ uptake and membrane-potential control). Plant Physiol 105:1399-408
    8. Hoekenga OA, Maron LG, Pi?eros MA, Can?ado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Koyama H, Kochian LV (2006) AtA / LMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in / Arabidopsis. Proc Natl Acad Sci USA 103:9738-743 CrossRef
    9. Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106:185-97 CrossRef
    10. Huang CF, Yamaji N, Chen Z, Ma JF (2012) A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J 69:857-67 CrossRef
    11. Kidd PS, Llugany M, Poschenrieder C, Gunse B, Barcelo J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize ( / Zea mays L.). J Exp Bot 52:1339-352 CrossRef
    12. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Mol Biol 46:237-60 CrossRef
    13. Kochian LV, Hoekenga OA, Pi?eros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459-93 CrossRef
    14. Kochian LV, Pi?eros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175-95 CrossRef
    15. Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R (2001) Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and aluminum-resistant cultivar. Plant Physiol 126:397-10 CrossRef
    16. Liao H, Wan HY, Shaff J, Wang XR, Yan XL, 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 141:674-84 CrossRef
    17. Ligaba A, Yamaguchi M, Shen H, Sakaki T, Yamamoto Y, Matsumoto H (2004) Phosphorus deficiency enhances plasma membrane H+-ATPase activity and citrate exudation in greater purple lupin ( / Lupinus pilosus). Funct Plant Biol 31:1075-083 CrossRef
    18. Liu K, Luan S (2001) Internal aluminum block of plant inward K+ channels. Plant Cell 13:1453-465
    19. Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41:257-68 CrossRef
    20. Ma JF (2000) Role of organic acids in detoxification of Al in higher plants. Plant Cell Physiol 44:383-90 CrossRef
    21. Ma JF, Zheng SJ, Matsumoto H (1997) Specific secretion of citric acid induced by Al stress in / Cassia tora L. Plant Cell Physiol 38:1019-025 CrossRef
    22. Ma JF, Ryan PR, Delhaize E (2001) Aluminum tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273-78 CrossRef
    23. Magalhaes JV, Liu J, Guimar?es CT, Lana UG, Alves VM, Wang YH, Schaffert RE, Hoekenga OA, Pi?eros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156-161 CrossRef
    24. Marschner H (1991) Mechanisms of adaptation of plants to acid soils. Plant Soil 134:1-0
    25. Matsumoto H (1988) Inhibition of proton transport activity of microsomal membrane vesicles of barley roots by aluminum. Soil Sci Plant Nut 34:499-06 CrossRef
    26. Meng ZB, Chen LQ, Suo D, Li GX, Tang CX, Zheng SJ (2012) Nitric oxide is the shared signalling molecule in phosphorus- and iron-deficiency-induced formation of cluster roots in white lupin ( / Lupinus albus). Ann Bot 109:1055-064 CrossRef
    27. Miyasaka SC, Buta JG, Howell RK, Foy CD (1991) Mechanism of aluminum tolerance in snapbean, root exudation of citric acid. Plant Physiol 96:737-43 CrossRef
    28. Murphy AS, Eisinger WR, Shaff JE, Kochian LV, Taiz L (1999) Early copper-induced leakage of K+ from / Arabidopsis seedlings is mediated by ion channels and coupled to citrate efflux. Plant Physiol 121:1375-382 CrossRef
    29. Neumann G, Martinoia E (2002) Cluster roots—an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162-67 CrossRef
    30. Neumann G, Massonneau A, Martinoia E, R?mheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373-82 CrossRef
    31. Ohno T, Koyama H, Hara T (2003) Characterization of citrate transport through the plasma membrane in a carrot mutant cell line with enhanced citrate excretion. Plant Cell Physiol 44:156-62 CrossRef
    32. Olivetti GP, Cumming JR, Etherton B (1995) Membrane-potential depolarization of root cap cells precedes aluminum tolerance in snapbean. Plant Physiol 109:123-29
    33. Osawa H, Matsumoto H (2002) Aluminium triggers malate-independent potassium release via ion channels from the root apex in wheat. Planta 215:405-12 CrossRef
    34. Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an Al-tolerance mechanism in maize ( / Zea mays L.). Planta 196:788-95 CrossRef
    35. Rangel AF, Rao IM, Braun HP, Horst WJ (2010) Aluminum resistance in common bean ( / Phaseolus vulgaris) involves induction and maintenance of citrate exudation from root apices. Physiol Plant 138:176-90 CrossRef
    36. Roelofs RFR, Rengel Z, Cawthray GR, Dixon KW, Lambers H (2001) Exudation of carboxylates in Australian / Proteaceae: chemical composition. Plant Cell Environ 24:891-03 CrossRef
    37. Ryan PR, Delhaize E, Randall PJ (1995) Characteristic of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103-10 CrossRef
    38. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Mol Biol 52:527-60 CrossRef
    39. 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 Physiol 149:340-51 CrossRef
    40. Shen R, Ma J, Kyo M, Iwashita T (2002) Compartmentation of aluminium in leaves of an Al-accumulator, / Fagopyrum esculentum Moench. Planta 215:394-98 CrossRef
    41. Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287-96 CrossRef
    42. Shen H, Chen J, Wang Z, Yang C, Sasaki T, Yamamoto Y, Matsumoto H, Yan X (2006) Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 57:1353-362 CrossRef
    43. Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 138:2475-482 CrossRef
    44. Tanoi K, Junko H, Kazutoshi S, Yoshitake H, Hiroki N, Tomoko MN (2005) Analysis of potassium uptake by rice roots treated with aluminum using a positron emitting nuclide, 38K. Soil Sci Plant Nut 51:715-17 CrossRef
    45. Tomasi N, Kretzschmar T, Espen L, Weisskopf L, Fuglsang AT, Palmgren MG, Neumann G, Varanini Z, Pinton R, Martinoia E, Cesco S (2009) Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32:465-75 CrossRef
    46. Wang B, Shen J, Zhang W, Zhang F, Neumann G (2007) Citrate exudation from white lupin induced by phosphorus deficiency differs from that induced by aluminum. New Phytol 176:581-89 CrossRef
    47. Wherrett T, Ryan PR, Delhaize E, Shabala S (2005) Effect of aluminium on membrane potential and ion fluxes at the apices of wheat roots. Funct Plant Biol 32:199-08 CrossRef
    48. Yan F, Zhu Y, Müller C, Z?rb C, Schubert S (2002) Adaptation of H+-pumping and plasma membrane H+ ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiol 129:50-3 CrossRef
    49. Yang ZM, Sivaguru M, Horst WJ, Matsumoto H (2000) Aluminium tolerance is achieved by exudation of citric acid from roots of soybean ( / Glycine max). Physiol Plant 110:72-7 CrossRef
    50. 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 56:1197-203 CrossRef
    51. Yang JL, Zhang L, Li YY, You JF, Wu P, Zheng SJ (2006) Citrate transporters play a critical role in aluminium-stimulated citrate efflux in rice bean ( / Vigna umbellata) roots. Ann Bot 97:579-84 CrossRef
    52. Yang JL, You JF, Li YY, Wu P, Zheng SJ (2007) Magnesium enhances aluminum-induced citrate secretion in rice bean roots ( / Vigna umbellata) by restoring plasma membrane H+-ATPase activity. Plant Cell Physiol 48:66-3 CrossRef
    53. Yang JL, Zhu XF, Peng YX, Zheng C, Ming F, Zheng SJ (2011) Aluminum regulates oxalate secretion and plasma membrane H+-ATPase activity independently in tomato roots. Planta 234:281-91 CrossRef
    54. Yokosho K, Yamaji N, Ma JF (2011) An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J 68:1061-069 CrossRef
    55. You JF, He YF, Yang JL, Zheng SJ (2005) A comparison of aluminum resistance among / Polygonum species originating on strongly acidic and neutral soils. Plant Soil 276:143-51 CrossRef
    56. Zeng H, Liu G, Kinoshita T, Zhang R, Zhu Y, Shen Q, Xu G (2012) Stimulation of phosphorus uptake by ammonium nutrition involves plasma membrane H+ ATPase in rice roots. Plant Soil 357:205-14 CrossRef
    57. Zhang WH, Ryan PR, Tyerman SD (2004) Citrate-permeable channels in the plasma membrane of cluster roots of white lupin. Plant Physiol 136:3771-783 CrossRef
    58. Zhang R, Liu G, Wu N, Gu M, Zeng H, Zhu Y, Xu G (2011) Adaptation of plasma membrane H+ ATPase and H+ pump to P deficiency in rice roots. Plant Soil 349:3-1 CrossRef
    59. Zhao Z, Ma JF, Sato K, Takeda K (2003) Differential Al resistance and citrate secretion in barley ( / Hordeum vulgare L.). Planta 217:794-00 CrossRef
    60. Zheng SJ (2010) Crop production on acidic soils: overcoming aluminium toxicity and phosphorus deficiency. Ann Bot 106:183-84 CrossRef
    61. Zheng SJ, Ma JF, Matsumoto H (1998) High aluminum resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol 117:745-51 CrossRef
    62. Zheng SJ, Yang JL, He YF, Yu XH, Zhang L, You JF, Shen RF, Matsumoto H (2005) Immobilization of aluminum with phosphorous in roots is associated with high aluminum resistance in buckwheat. Plant Physiol 138:297-03 CrossRef
    63. Zhu Y, Yan F, Z?rb C, Schubert S (2005) A link between citrate and proton release by proteoid roots of white lupin ( / Lupinus albus L.) grown under phosphorus-deficient conditions? Plant Cell Physiol 46:892-01 CrossRef
    64. Zhu Y, Di T, Xu G, Chen X, Zeng H, Yan F, Shen Q (2009) Adaptation of plasma membrane H+-ATPase of rice roots to low pH as related to ammonium nutrition. Plant Cell Environ 32:1428-440 CrossRef
  • 作者单位:Houqing Zeng (1) (2)
    Xumeng Feng (1)
    Baolan Wang (3)
    Yiyong Zhu (1)
    Qirong Shen (1)
    Guohua Xu (1)

    1. Key Laboratory of Plant Nutrition and Fertilization in Low-Middle Reaches of the Yangtze River, Ministry of Agriculture, College of Resource and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China
    2. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, 310036, People’s Republic of China
    3. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, the Chinese Academy of Sciences, Beijing, 100093, People’s Republic of China
  • ISSN:1573-5036
文摘
Aims Exudation of organic acid anions is one of the mechanisms responsible for aluminum (Al) tolerance. The plasma membrane (PM) H+-ATPase is involved in the exudation of organic acid anions. However, the relationship between organic acid exudation and PM?H+-ATPase under Al toxicity remains unclear. This study aims to investigate the correlation among Al-induced citrate exudation, PM?H+-ATPase activity and counterions for citrate release from cluster roots of phosphorus-deficient (?P) white lupin. Methods Al and various pharmacological agents were applied to incubate the cluster roots of P-deficient white lupin; the citrate exudation rate, PM?H+-ATPase activity and ion exudation of cluster roots were examined. Results Citrate exudation from cluster roots of P-deficient white lupin was induced by 50?μM Al treatment within 1.5?h, but no extra increase was found when the duration of Al treatment increased. The PM?H+-ATPase activity of cluster roots was insensitive to Al treatment, irrespective of Al concentration and duration of Al treatment. Al treatment increased K+ efflux but not H+ efflux from cluster roots. After application of pharmacological agents to P-deficient cluster roots under Al treatment or not, vanadate decreased H+ efflux and increased K+ efflux, but had no inhibitory effect on citrate exudation; fusicoccin increased H+ efflux and citrate exudation, but decreased K+ efflux; tetraethylammonium (TEA) chloride, a K+-channel inhibitor, inhibited K+ efflux and increased H+ efflux. Conclusions These results indicate that citrate exudation induced by combined treatment with P-deficiency and Al is independent of PM?H+-ATPase activity, and is coupled with K+ efflux, which may compensate H+ efflux for keeping the charge balance for Al-induced citrate exudation from cluster roots of P-deficient white lupin.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700