Biologia plantarum 60:572-578, 2016 | DOI: 10.1007/s10535-016-0607-5
Citric acid secretion induced by aluminum in two Stylosanthes species
- 1 Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Brazil
Secretion of organic acids (OAs) by roots has been suggested to be an important mechanism of Al resistance in many species. In Stylosanthes, the participation of OAs in the mechanism of Al resistance is poorly understood. We aimed to study the production and secretion of OAs by two Brazilian Stylosanthes species with different Al resistance. Stylosanthes capitata and S. guianensis were treated with Al at different concentrations in 0.5 mM CaCl2 (pH 4.0), and then root elongation, Al and OA content, OA secretion into the external solution, and the activity of citrate synthase (CS) were measured. Al-induced secretion of citric acid was also evaluated in the presence of protein synthesis and anion channel inhibitors. S. guianensis accumulated lower amounts of Al in its roots and displayed less inhibition of root elongation compared to S. capitata. Citric and malic acids were the most abundant OAs in the roots, and their content decreased with the Al treatment, except for citric acid in S. guianensis. Citric acid was the only OA secreted into the nutrient solution by the Al-treated plants of both species, but more by S. guianensis. Citrase synthase activity decreased in S. capitata but increased in S. guianensis with the Al treatment, and it may have a crucial role in the maintenance of citric acid content in the roots of S. guianensis. The use of anion channel and protein synthesis inhibitors reveal that anion channels were likely involved in the secretion of citric acid, and channel protein transcription was up-regulated by exposure to Al in Stylosanthes.
Keywords: aluminum resistance; citrate synthase; malic acid; organic acids; Stylosanthes capitata; S. guianensis
Subjects: citric acid; aluminum; organic acid secretion; citrate synthase; malic acid
Received: August 12, 2015; Revised: December 3, 2015; Accepted: January 18, 2016; Published: September 1, 2016 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Andrade, L.R.M., Ikeda, M., Amaral, L.I.V., Ishizuka, J.: Organic acid metabolism and root excretion of malate in wheat cultivars under aluminium stress. - Plant Physiol. Biochem. 49: 55-60, 2011.
Go to original source... - Barceló, J., Poschenrieder, C.: Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. - Environ. exp. Bot. 48: 75-92, 2002.
Go to original source... - Botrel, M.A., Pereira, J.R., Xavier, D.F.: [Evaluation and selection of forage legumes for low fertility acid soils. 1: Stylosanthes] - Pesq. agropec. bras. 20: 35-43, 1985. [In Port.]
- Cambraia, J., Cambraia, M.C.: [Aluminum tolerance evaluation of maize hybrids in nutrient solution] - Rev. Ceres 42: 297-307, 1995. [In Port.]
- Cambraia, J., Galvani, F.R., Estevão, M.M., Sant'Anna, R.: Effects of aluminum on organic acid, sugar and amino acid composition of the root system of sorghum (Sorghum bicolor L. Moench). - J. Plant Nutr. 6: 313-322, 1983.
Go to original source... - Chaffai, R., Marzouk, B.: The role of organic acids in the short- and long-term aluminum tolerance in maize seedlings (Zea mays L.). - Acta Physiol. Plant. 31: 805-814, 2009.
Go to original source... - Clark, R.B.: Characterization of phosphatase of intact maize roots. - J. Agr. Food Chem. 23: 458-460, 1975.
Go to original source... - Costa, L.C., Sartori, A.L.B., Pott, A.: [Taxonomic study of Stylosanthes (Leguminosae-Papilionoideae-Dalbergieae) in Mato Grosso do Sul, Brazil] - Rodriguesia 59: 547-572, 2008. [In Port.]
Go to original source... - Delhaize, E., Ryan, P.R.: Aluminum toxicity and tolerance in plants. - Plant Physiol. 107: 315-321, 1995.
Go to original source... - Doncheva, S., Amenós, M., Poschenrieder, C., Barceló, J.: Root cell patterning: a primary target for aluminium toxicity in maize. - J. exp. Bot. 56: 1213-1220, 2005.
Go to original source... - Du, Y.M., Tian, J., Liao, H., Bai, C.J., Yan, X.L., Liu, G.D.: Aluminium tolerance and high phosphorus efficiency helps Stylosanthes better adapt to low-P acid soils. - Ann. Bot. 103: 1239-1247, 2009.
Go to original source... - Gonçalves, J.F.C., Cambraia, J., Mosquim, P.R., Araújo, E.F.: Aluminum effect on organic acid production and accumulation in Sorghum. - J. Plant Nutr. 28: 507-520, 2005.
Go to original source... - Hayes, J.E., Ma, J.F.: Al-induced efflux of organic acid anions is poorly associated with internal organic acid metabolism in triticale roots. - J. exp. Bot. 54: 1753-1759, 2003.
Go to original source... - Jham, G.N., Fernandes, S.A., Garcia, C.F., Silva, A.A.: Comparison of GC and HPLC for the quantification of organic acids in coffee. - Phytochem. Anal. 13: 99-104, 2002.
Go to original source... - Kochian, L.V., Hoekenga, O.A., Piñeros, M.A.: How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. - Annu. Rev. Plant Biol. 55: 459-493, 2004.
Go to original source... - Li, X.F., Zuo, F.H., Ling, G.Z., Li, Y.Y., Yu, Y.X., Yang, P.Q., Tang, X. L.: Secretion of citrate from roots in response to aluminum and low phosphorus stresses in Stylosanthes. - Plant Soil 325: 219-229, 2009.
Go to original source... - Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J.: Protein measurement with the Folin phenol reagent. - J. biol. Chem. 193: 265-275, 1951
Go to original source... - Ma, J.F.: Role of organic acids in detoxification of aluminum in higher plants. - Plant Cell Physiol. 41: 383-390, 2000.
Go to original source... - Ma, J.F.: Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. - Int. Rev. Cyt. 264: 225-253, 2007.
Go to original source... - Ma, J.F., Ryan, P.R, Delhaize, E.: Aluminium tolerance in plants and the complexing role of organic acids. - Trends Plant Sci. 6: 273-278, 2001.
Go to original source... - Ma, J.F., Shen, R., Nagao, S., Tanimoto, E.: Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. - Plant Cell Physiol. 45: 583-589, 2004.
Go to original source... - Ma, J.F., Zheng, S.J., Matsumoto, H.: Specific secretion of citric acid induced by Al stress in Cassia tora L. - Plant Cell 38: 1019-1025, 1997.
Go to original source... - Martins, N., Gonçalves, S., Andrade, P.B., Valentão, P., Romano, A.: Changes on organic acid secretion and accumulation in Plantago almogravensis Franco and Plantago algarbiensis Samp. under aluminum stress. - Plant Sci. 198: 1-6, 2013.
Go to original source... - Poschenrieder, C., Gunsé, B., Corrales, I., Barceló, J.: A glance into aluminum toxicity and resistance in plants. - Sci. total Environ. 400: 356-68, 2008.
Go to original source... - Ryan, P.R., Delhaize, E.: The convergent evolution of aluminium resistance in plants exploits a convenient currency. - Funct. Plant Biol. 37: 275-284, 2010.
Go to original source... - Ryan, P.R., Delhaize, E., Jones, D.: Function and mechanism of organic anion exudation from plant roots. - Annu. Rev. Plant Physiol. 52: 527-560, 2001.
Go to original source... - Shen, H., Yan, X., Cai, K., Matsumoto, H.: Differential Al resistance and citrate secretion in the tap and basal roots of common bean seedlings. - Physiol. Plant. 121: 595-603, 2004.
Go to original source... - Singh, D., Chauhan, S.K.: Organic acids of crop plants in aluminium detoxification. - Curr. Sci. 100: 1509-1515, 2011.
- Sun, L., Liang, C., Chen, Z., Liu, P., Tian, J., Liu, G., Liao, H.: Superior aluminium (Al) tolerance of Stylosanthes is achieved mainly by malate synthesis through an Al-enhanced malic enzyme, SgME1. - New Phytol. 202: 209-216, 2014.
Go to original source... - Yang, J.L., Zhang, L., Li, Y.Y., You, J.F., Wu, P., Zheng, S.J.: Citrate transporters play a critical role in aluminium-stimulated citrate efflux in rice bean (Vigna umbellata) roots. - Ann. Bot. 97: 579-584, 2006a.
Go to original source... - Yang, J.L., Zheng, S.J., He, Y.F., You, J.F., Zhang, L., Yu, X.H.: Comparative studies on the effect of a protein-synthesis inhibitor on aluminium-induced secretion of organic acids from Fagopyrum esculentum Moench and Cassia tora L. roots. - Plant Cell Environ. 29: 240-246, 2006b.
Go to original source... - Yang, L.T., Jiang, H.X., Tang, N., Chen, L.S.: Mechanisms of aluminum-tolerance in two species of citrus: Secretion of organic acid anions and immobilization of aluminum by phosphorus in roots. - Plant Sci. 180: 521-530, 2011.
Go to original source... - Yang, L.T., Qi, Y.P., Jiang, H.X., Chen, L.S.: Roles of organic acid anion secretion in aluminium tolerance of higher plants. - BioMed Res. Int. Article ID 173682, 2013.
Go to original source... - Yang, Z.M., Nian, H., Sivaguru, M., Tanakamaru, S., Matsumoto, H.: Characterization of aluminium-induced citrate secretion in aluminium-tolerant soybean (Glycine max) plants. - Physiol. Plant. 113: 64-71, 2001.
Go to original source... - Yang, Z.M., Yang, H., Wang, J., Wang, Y.S.: Aluminum regulation of citrate metabolism for Al-induced citrate efflux in the roots of Cassia tora L. - Plant Sci. 166: 1589-1596, 2004.
Go to original source... - Yu, L., Yan, J., Guo, S., Zhu, W.: Aluminum-induced secretion of organic acid by cowpea (Vigna unguiculata L.) roots. - Sci. Hort. 135: 52-58, 2012.
Go to original source... - Zuo, F.-H., Ling, G.-Z., Tang, X.-L., Yu, Y.-X., Li, Y.-Y., Li, X.-F.: Al stress-induced citrate secretion from roots in Stylosanthes. - Sci. Agr. Sin. 43: 59-64, 2010.



