Abstract
Soil contamination by lead (Pb) is a problem due to the persistence of this element on soil. High amounts of Pb in soil impair plant establishment, however some plants may increase tolerance to heavy metals when colonized by arbuscular mycorrhizal fungi (AMF). The leguminous plant, Calopogonium mucunoides, is Pb-sensitive that is tolerant to Pb when associated to AMF. We performed a chromatographic analysis of foliar free-amino acid in non-mycorrhizal and mycorrhizal plants to determine its relation with Pb tolerance. Mycorrhization caused drastic increase in aspartate, glutamine, glycine, threonine, alanine, isoleucine and gamma-aminobutiric acid (GABA), while depletion of asparagine, histidine and arginine was observed in AMF-associated plants. When grouped according to common metabolic precursor, it was found that amino acids derived from 3-phosphoglicerate and pyruvate was higher in mycorrhizal plants while amino acids derived from glucose-6-phosphate and 2-oxoglutarate were higher in non-mycorrhizal plants; phosphoenolpyruvate and oxaloacetate pathways were not influenced by mycorrhization. Summarizing, mycorrhization changed soluble amino acids profile in C. mucunoides leaves, especially aspartate, alanine and GABA, which may be involved in tolerance to abiotic stress. Additionally the depletion of asparagine, histidine and arginine may be related to a deviation for metabolic pathways not related to protein biosynthesis but to the synthesis of polyamines, especially in the case of arginine. Therefore, we suggest that mycorrhization influence on soluble free amino acid profile in leaves can be one of the factors involved with the attenuation of Pb toxicity in AMF-associated C. mucunoides plants.
This is a preview of subscription content, log in via an institution to check access.
References
Ahmad MSA, Ashraf M, Tabassam Q, Hussain M, Firdous H (2011) Lead (Pb)-induced regulation of growth, photosynthesis, and mineral nutrition in maize (Zea mays L.) plants at early growth stages. Biol Trace Elem Res 144:1229–1239
Akçay N, Bor M, Karabudak T, Özdemir F, Türkan İ (2012) Contribution of Gamma amino butyric acid (GABA) to salt stress responses of Nicotiana sylvestris CMSII mutant and wild type plants. J Plant Physiol 169:452–458
Aloui A, Recorbet G, Robert F, Schoefs B, Bertrand M, Henry C, Gianinazzi-Pearson V, Dumas-Gaudot E, Aschi-Smiti S (2011) Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant Biol 11:75
Amarante L, Sodek L (2006) Waterlogging effect on xylem sap glutamine of nodulated soybean. Biol Plant 50:405–410
Andrade SAL, Gratao PL, Schiavinato MA, Silveira APD, Azevedo RA, Mazzafera P (2009) Zn uptake, physiological response and stress attenuation in mycorrhizal jack bean growing in soil with increasing Zn concentrations. Chemosphere 75:1363–1370
Andrade SAL, Gratão PL, Azevedo RA, Silveira APD, Schiavinato MA, Mazzafera P (2010) Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ Exp Bot 68:198–207
Arbona V, Manzi M, de Ollas C, Gomez-Cadenas A (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 14:4885–4911
Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317
Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect of cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Funct Plant Biol 30:57–64
Bieleski RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Anal Biochem 17:278–293
Bolton MD (2009) Primary metabolism and plant defense-fuel for the fire. Mol Plant Microbe Interact 22:487–497
de Souza LA, de Andrade SAL, de Souza SCR, Schiavinato MA (2012) Arbuscular mycorrhiza confers Pb tolerance in Calopogonium mucunoides. Acta Physiol Plant 34:523–531
Freitas EV, Nascimento CW, Souza A, Silva FB (2013) Citric acid-assisted phytoextraction of lead: a field experiment. Chemosphere 92:213–217
Galli U, Schuepp H, Brunold C (1994) Heavy metal binding by mycorrhizal fungi. Physiol Plant 92:364–368
Garg N, Aggarwal N (2011) Effects of interactions between cadmium and lead on growth, nitrogen fixation, phytochelatin, and glutathione production in mycorrhizal Cajanus cajan (L.) Millsp. J Plant Growth Regul 30:286–300
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Irtelli B, Petrucci WA, Navari-Izzo F (2009) Nicotianamine and histidine/proline are, respectively, the most important copper chelators in xylem sap of Brassica carinata under conditions of copper deficiency and excess. J Exp Bot 60:269–277
Jarrett HW, Cooksy KD, Ellis B, Anderson JM (1986) The separation of o-phthalaldehyde derivatives of amino acids by reversed-phase chromatography on octylsilica columns. Anal Biochem 153:189–198
Krämer U, CotterHowells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638
Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1353
Lanfranco L, Guether M, Bonfante P (2011) Arbuscular mycorrhizas and N acquisition by plants. In: Pollaco JC, Todd CD (eds) Ecological aspects of nitrogen metabolism in plants. Wiley, New Jersey, pp 52–68
Queiroz HM, Sodek L, Haddad CRB (2012) Effect of salt on the growth and metabolism of Glycine max. Braz Arch Biol Technol 55:809–817
Rabe E, Lovatt CJ (1986) Increased arginine biossynthesis during phosphorus deficiency: a response to the increased ammonia content of leaves. Plant Physiol 81:774–779
Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45:481–487
Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574
Ruzicka DR, Hausmann NT, Barrios-Masias FH, Jackson LE, Schachtman DP (2012) Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions. Plant Soil 350:145–162
Salvioli A, Zouari I, Chalot M, Bonfante P (2012) The arbuscular mycorrhizal status has an impact on the transcriptome profile and amino acid composition of tomato fruit. BMC Plant Biol 12:1–12
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52
Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446–452
Willis A, Rodrigues BF, Harris PJC (2012) The ecology of arbuscular mycorrhizal fungi. Crit Rev Plant Sci 32:1–20
Wu QS, He XH, Zou YN, Liu CY, Xiao J, Li Y (2012) Arbuscular mycorrhizas alter root system architecture of Citrus tangerine through regulating metabolism of endogenous polyamines. Plant Growth Regul 68:27–35
Acknowledgments
The authors thank CAPES for the financial support and Prof. Dr. Ladaslav Sodek for sharing the HPLC equipment.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Souza, L.A., Camargos, L.S., Schiavinato, M.A. et al. Mycorrhization alters foliar soluble amino acid composition and influences tolerance to Pb in Calopogonium mucunoides . Theor. Exp. Plant Physiol. 26, 211–216 (2014). https://doi.org/10.1007/s40626-014-0019-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-014-0019-x