Abstract
Lespedeza bicolor (Lespedeza bicolor Turcz. cv. Jiangxi) is a leguminous shrub that is well adapted to acid infertile soils. However, the mechanisms of aluminum resistance in this species have not been established. This study aimed to assess the possible resistance mechanisms of this plant to Al. An Al-sensitive species of Lespedeza, sericea lespedeza [Lespedeza cuneata (Dum.-Cours.) G. Don cv. Zhejiang], was used as a reference. The roots of L. bicolor secreted both malate and citrate after exposure to Al, but roots of L. cuneata did not. The secretion of organic acids from L. bicolor was specific to Al; neither 15-day P starvation nor 50 μM lanthanum induced the secretion of these organic acid anions. Secretion of organic acid anions in L. bicolor was detected after 3–6 h exposure to Al, and the amount increased significantly after 6 h exposure, suggesting that this plant shows a pattern II-type organic acid secretion. This is supported by the finding that the secretion was significantly inhibited by a protein-synthesis inhibitor, cycloheximide. Two kinds of anion-channel inhibitors had different effects on Al-induced secretion of organic acids: 9-anthracene carboxylic acid completely inhibited secretion, phenylglyoxal had no effect. Root elongation in L. bicolor was more severely inhibited by Al in the presence of 9-anthracene carboxylic acid. All these results indicated that the secretion of malate and citrate is a specialized response to Al stress in L. bicolor roots, which might be one of the Al-resistance mechanisms in this species.
This is a preview of subscription content, log in to check access.








References
Campbell TA, Nuernberg NJ, Foy CD (1991) Differential responses of sericea lespedeza to aluminum stress. J Plant Nutr 14:1057–1066
Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.): aluminum stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702
Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321
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 48:1081–1091
Heim A, Brunner I, Frey B, Frossard E, Luster J (2001) Root exudation, organic acids, and element distribution in roots of Norway spruce seedlings treated with aluminum in hydroponics. J Plant Nutr Soil Sci 164:519–526
Hyland HL (1938) Comparison of legume growth in different soil types at varying acidity levels. J Am Soc Agron 30:111–121
Kitagawa T, Morishita T, Tachibana Y, Namai H, Ohta Y (1986) Differential aluminum resistance of wheat varieties and secretion of organic acids. Jpn J Soil Sci Plant Nutr 57:352–358
Kochian LV (1995) Cellular mechanism of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol 46:237–260
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
Li YA, Jia LM, Yang L (2004) A review of the research and development of the utilization value and cultivation techniques for high output of Lespedeza. Hebei Journal of Forestry and Orchard Research 19:185–152 (in Chinese)
Li XF, Ma JF, Matsumoto H (2000) Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol 123:1537–1543
Li XF, Ma JF, Matsumoto H (2002) Aluminum-induced secretion of both citrate and malate in rye. Plant Soil 242:235–243
Ma JF (2000) Role of organic acids in detoxification of Al in higher plant. Plant Cell Physiol 41:383–390
Ma JF (2005) Physiological mechanisms of Al resistance in higher plants. Soil Sci Plant Nutr 51:609–612
Ma Z, Miyasaka SC (1998) Oxalate exudation by taro in response to Al. Plant Physiol 118:861–865
Ma JF, Hiradate S, Nomoto K, Iwashita T, Matsumoto H (1997a) Internal detoxification mechanism of Al in hydrangea. Identification of Al form in the leaves. Plant Physiol 113:1033–1039
Ma JF, Zheng SJ, Hiradate S, Matsumoto H (1997b) Detoxifying aluminum with buckwheat. Nature 390:569–570
Ma JF, Zheng SJ, Matsumoto H (1997c) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 38:1019–1025
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
Ma JF, Ryan PR, Delhaize E (2001) Aluminum tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278
Magalhaes JV, Liu J, Guimarães CT, Lana UGP, Alves VMC, Wang YH, Schaffert RE, Hoekenga OA, Piñeros 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 39:1156–1161
Miyasaka SC, Buta JG, Howell RK, Foy CD (1991) Mechanism of aluminum tolerance in snapbean: root exudation of citric acid. Plant Physiol 96:737–743
Osawa H, Kojima K (2006) Citrate-release-mediated aluminum resistance is coupled to the inducible expression of mitochondrial citrate synthase gene in Paraserianthes falcataria. Tree Physiol 26:565–574
Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196:788–795
Ryan PR, Delhaize E, Randall PJ (1995) Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103–110
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
Shen RF, Ma JF (2001) Distribution and mobility of aluminum in an Al-accumulating plant, Fagopyrum esculentum Moench. J Exp Bot 52:1683–1687
Shen RF, Iwashita T, Ma JF (2004) Form of Al changes with Al concentration in leaves of buckwheat. J Exp Bot 55:131–136
Silva IR, Novais RF, Jham GN, Barros NF, Gebrim FO, Nunes FN, Neves JCL, Leite FP (2004) Responses of eucalypt species to aluminum: the possible involvement of low molecular weight organic acids in the Al tolerance mechanism. Tree Physiol 24:1267–1277
Taylor GJ (1991) Current views of the aluminum stress response: the physiological basis of tolerance. Curr Topics Plant Biochem Physiol 10:57–95
Watanabe T, Osaki M (2002) Mechanisms of adaptation to high aluminum condition in native plant species growing in acid soils: a review. Commun Soil Sci Plant Anal 33:1247–1260
Wenzl P, Chaves AL, Patino GM, Mayer JE, Rao IM (2002) Aluminum stress stimulates the accumulation of organic acids in root apices of Brachiaria species. J Plant Nutr Soil Sci 165:582–588
Yang YS, Liu BG, Sha JS (1994) Study on the cultivation of Lespedeza bicolor for water–soil resources restoration. Resources and Environment in the Yangtze Valley 3:330–334 (in Chinese)
Yang ZM, Nian H, Sivaguru M, Tanakamaru S, Matsumoto H (2001) Characterization of aluminum-induced citrate secretion in aluminum-tolerant soybean (Glycine max) plants. Physiol Plant 113:64–71
Zhao ZQ, Ma JF, Sato K, Takeda K (2003) Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). Planta 217:794–800
Zheng SJ, Ma JF, Matsumoto H (1998) High aluminum resistance in buckwheat: I. Al-induced special secretion of oxalic acid from root tips. Plant Physiol 117:745–751
Acknowledgement
This study was supported by the CAS International Partnership Project (CXTD-Z2005-04), the National Natural Science Foundation of China (40621001, 30571114) and by a Joint Research Project from the Japanese Society for the Promotion of Science.
Author information
Additional information
Responsible Editor: Juan Barcelo.
Rights and permissions
About this article
Cite this article
Dong, X.Y., Shen, R.F., Chen, R.F. et al. Secretion of malate and citrate from roots is related to high Al-resistance in Lespedeza bicolor . Plant Soil 306, 139–147 (2008). https://doi.org/10.1007/s11104-008-9564-x
Received:
Accepted:
Published:
Issue Date:
Keywords
- Al resistance
- Anion-channel inhibitors
- Citrate
- Lespedeza bicolor
- Malate
- Specific secretion