The role of organic acids in heavy metal tolerance in plants
DOI:
https://doi.org/10.21638/spbu03.2018.103Abstract
Organic acid metabolism is of fundamental importance at the cellular and at the whole plant level. In recent years there has been increased attention in the role of organic acids in modulating adaptation to the environment, including organic acids participation in the detoxification of heavy metals. The basis of the phenomenon is the ability of acids such as citrate, malate, oxalate, malonate, aconitate and tartrate to form strong bonds with heavy metal ions through metal chelatation with carboxyl groups carrying the function of donor oxygen in metal-ligands. This review deals with aspects of extracellular and intracellular chelation of heavy metal ions with the involvement of organic acids. We consider the role of metal-induced secretion of malate, citrate and oxalate by roots of various plant species in extracellular complexation of heavy metals and in the reduction of their bioavailability for plants. We also review the possible mechanisms of stimulation of metals uptake by plants under the influence of exogenous application of organic acids in the soil. The efficiency of intracellular chelation of heavy metal ions with the participation of organic acids is considered due to the importance of this strategy in hyperaccumulators and non-hyperaccumulators to improve metal tolerance in plants.
Keywords:
organic acids, heavy metals, plant tolerance, organic acid secretion, chelation, malate, citrate, oxalate
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Anjum, N. A., Hasanuzzaman, M., Hossain, M. A., Thangavel, P., Roychoudhury, A., Gill, S. S., Rodrigo, M. A. M., Adam, V., Fujita, M., Kizek, R., Duarte, A. C., Pereir, E., and Ahmad, I. 2015. Jacks of metal/metalloid chelation trade in plants — an overview. Frontiers in Plant Science 6:192. https://doi.org/10.3389/fpls.2015.00192" target="_blank">https://doi.org/10.3389/fpls.2015.00192
Chaffai, R., Tekitek, A., and El Ferjani, E. 2006. A comparative study on the organic acid content and exudation in maize (Zea mays L.) seedlings under conditions of copper and cadmium stress. Asian Journal of Plant Sciences 5(4):598–606. https://doi.org/10.3923/ajps.2006.598.606" target="_blank">https://doi.org/10.3923/ajps.2006.598.606
Chai, M. W., Li, R. L., Shi, F. C., Liu, F. C., Pan, X., Cao, D., and Wen, X. 2012. Effects of cadmium stress on growth, metal accumulation and organic acids of Spartina alterniflora Loisel. African Journal of Biotechnology 11(22):6091–6099. https://doi.org/10.5897/AJB11.2804" target="_blank">https://doi.org/10.5897/AJB11.2804
Chirkova, T. V. 2002. Physiologicheskiie osnovy ustojchivosti rastenii [Physiological basis of plant tolerance]. 240 pp. Izdatelstvo Sankt-Peterburgskogo Universiteta, Saint Petersburg.
Choi, Y. E., Harada, E., Wada, M., Tsuboi, H, Morita, Y., Kusano, T., and San, H. 2001. Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213(1):45–50. https://doi.org/10.1007/s004250000487" target="_blank">https://doi.org/10.1007/s004250000487
Cosio, C., Martinoia, E., and Keller, C. 2004. Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiology 134(2):716–725. https://doi.org/10.1104/pp.103.031948" target="_blank">https://doi.org/10.1104/pp.103.031948
Degryse, F., Smolders, E., and Parker, D. R. 2006. Metal complexes increase uptake of Zn and Cu by plants: implications for uptake and deficiency studies in chelator buffered solutions. Plant and Soil 289(1/2):171–185. https://doi.org/10.1007/s11104-006-9121-4" target="_blank">https://doi.org/10.1007/s11104-006-9121-4
Delhaize, E., Gruber, B. D., and Ryan, P. R. 2007. The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Letters 581(12):2255–2262. https://doi.org/10.1016/j.febslet.2007.03.057" target="_blank">https://doi.org/10.1016/j.febslet.2007.03.057
Delhaize, E., Ryan, P. R., and Randall, P. J. 1993. Aluminum tolerance in wheat (Triticum aestivum L.): II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiology 103(3):695–702. https://doi.org/10.1104/pp.103.3.695" target="_blank">https://doi.org/10.1104/pp.103.3.695
Dong, J., Mao, W. H., Zhang, G. P., Wu, F. B., and Cai, Y. 2007. Root excretion and plant tolerance to cadmium toxicity — a review. Plant, Soil and Environment 53(5):193–200. https://doi.org/10.17221/2205-PSE" target="_blank">https://doi.org/10.17221/2205-PSE
Durrett, T. P., Gassmann, W., and Rogers, E. E. 2007. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiology 144(1):197–205. https://doi.org/10.1104/pp.107.097162" target="_blank">https://doi.org/10.1104/pp.107.097162
Ehsan, S., Ali, S., Noureen, S., Mahmood, K., Farid, M., Ishaque, W., Shakoor, M. B., and Rizwan, M. 2014. Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicology and Environmental Safety 106(7):164–172. https://doi.org/10.1016/j.ecoenv.2014.03.007" target="_blank">https://doi.org/10.1016/j.ecoenv.2014.03.007
Evangelou, M. W. H., Ebel, M., and Schaeffer, A. 2007. Chelate assisted phytoextraction of heavy metals from soil: effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68(6):989–1003. https://doi.org/10.1016/j.chemosphere.2007.01.062" target="_blank">https://doi.org/10.1016/j.chemosphere.2007.01.062
Faheed, F., Mazen, A. M. A., and Elmohsen, S. 2013. Physiological and ultrastructural studies on calcium oxalate crystal formation in some plants. Turkish Journal of Botany 37:139–152. https://doi.org/10.3906/bot-1112-19" target="_blank">https://doi.org/10.3906/bot-1112-19
Fan, W., Xu, J. M., Lou, H. Q., Xiao, C., Chen, W. W., and Yang, J. L. 2016. Physiological and molecular analysis of aluminium-induced organic acid anion secretion from grain amaranth (Amaranthus hypochondriacus L.) roots. International Journal of Molecular Sciences 17(5):608. https://doi.org/10.3390/ijms17050608" target="_blank">https://doi.org/10.3390/ijms17050608
Guo, H., Feng, X., Hong, C., Chen, H., Zeng, F., Zheng, B., and Jiang, D. 2017. Malate secretion from the root system is an important reason for higher resistance of Miscanthus sacchariflorus to cadmium. Physiologia Plantarum 159(3):340–353. https://doi.org/10.1111/ppl.12526" target="_blank">https://doi.org/10.1111/ppl.12526
Hall, J. L. 2002. Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany 53(366):1–11. https://doi.org/10.1093/jexbot/53.366.1" target="_blank">https://doi.org/10.1093/jexbot/53.366.1
Igamberdiev, A. U., and Eprintsev, A. T. 2016. Organic acids: the pools of fixed carbon involved in redox regulation and energy balance in higher plants. Frontiers in Plant Science 7:1042. https://doi.org/10.3389/fpls.2016.01042" target="_blank">https://doi.org/10.3389/fpls.2016.01042
Jones, D. L. 1998. Organic acids in the rhizosphere — a critical review. Plant and Soil 205:25–44. https://doi.org/10.1023/A:1004356007312" target="_blank">https://doi.org/10.1023/A:1004356007312
Kochian, L. V., Pineros, M. A., Liu, J., and Magalhaes, J. V. 2015. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annual Review of Plant Biology 66:571–598. https://doi.org/10.1146/annurev-arplant-043014-114822" target="_blank">https://doi.org/10.1146/annurev-arplant-043014-114822
Kurilenko, V. V., and Osmolovskaya, N. G. 2015. Heavy metal pollution of Kotlin Island in the Gulf of Finland. Baltica 28(1):1–10. https://doi.org/10.5200/baltica.2015.28.01" target="_blank">https://doi.org/10.5200/baltica.2015.28.01
Küpper, H., Mijovilovich, A., Meyer-Klaucke, W., and Kroneck, P. M. H. 2004. Tissue- and age-dependent differences in the complexation of cadmium and zinc in the Cd/Zn hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiology 134(2):748–775. https://doi.org/10.1104/pp.103.032953" target="_blank">https://doi.org/10.1104/pp.103.032953
Li, X., Chen, X., and Cui, X. 2012. Zinc chemical forms and organic acid exudation in non-heading Chinese cabbages under zinc stress. Agricultural Sciences 3(4):562-566. https://doi.org/10.4236/as.2012.34067" target="_blank">https://doi.org/10.4236/as.2012.34067
Lopez-Bucio, J., Nieto-Jacobo, M. F., Ramırez-Rodriguez, V., and Herrera-Estrella, L. 2000. Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Science 160(1):1–13. https://doi.org/10.1016/S0168-9452(00)00347-2" target="_blank">https://doi.org/10.1016/S0168-9452(00)00347-2
Lu, L., Tian, S., Yang, X., Peng, H., and Li, T. 2013. Improved cadmium uptake and accumulation in the hyperaccumulator Sedum alfredii: the impact of citric acid and tartaric acid. Journal of Zhejiang University-SCIENCE B 14(2):106–114. https://doi.org/10.1631/jzus.B1200211" target="_blank">https://doi.org/10.1631/jzus.B1200211
Lux, A., Martinka, M., Vaculik, M., and White, P. J. 2011. Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany 62(1):21–37. https://doi.org/10.1093/jxb/erq281" target="_blank">https://doi.org/10.1093/jxb/erq281
Ma, J. F. 2000. Role of organic acids in detoxification of aluminum in higher plants. Plant and Cell Physiol. 41(4):383–390. https://doi.org/10.1093/pcp/41.4.383" target="_blank">https://doi.org/10.1093/pcp/41.4.383
Ma, J. F., Ryan, P. R., and Delhaize, E. 2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6(6):273–278. https://doi.org/10.1016/S1360-1385(01)01961-6" target="_blank">https://doi.org/10.1016/S1360-1385(01)01961-6
Ma, J. F., Zheng, S. J., Matsumoto, H., and Hiradate, S. 1997. Detoxifying aluminium with buckwheat. Nature 390(6660):569–570. https://doi.org/10.1038/37518" target="_blank">https://doi.org/10.1038/37518
Mazen A. M. A. 2004. Calcium oxalate deposits in leaves of Corchorus olitorius as related to accumulation of toxic metals. Russian Journal of Plant Physiology 51(2):281–285. https://doi.org/10.1023/B:RUPP.0000019226.03536.21" target="_blank">https://doi.org/10.1023/B:RUPP.0000019226.03536.21
Mazen, A. M. A., and El Maghraby, O. M. O. 1997. Accumulation of cadmium, lead and strontium, and a role of calcium oxalate in water hyacinth tolerance. Biologia Plantarum 40(3):411–417. https://doi.org/10.1023/A:1001174132428" target="_blank">https://doi.org/10.1023/A:1001174132428
Meychik, N. R., Nikolaeva, Y. I., Komarynets, O. V., and Ermakov I. P. 2011. Barrier function of the cell wall during uptake of nickel ions. Russian Journal of Plant Physiology 58(3):409–414. https://doi.org/10.1134/S1021443711030137" target="_blank">https://doi.org/10.1134/S1021443711030137
Meyer S, De Angeli, A, Fernie, A. R., and Martinoia, E. 2010. Intra- and extra-cellular excretion of carboxylates. Trends in Plant Sciences 15:40–47. https://doi.org/10.1016/j.tplants.2009.10.002" target="_blank">https://doi.org/10.1016/j.tplants.2009.10.002
Nigam, R., and Srivastava, M. M. 2005. Effects of carboxylic and amino acids on Cd uptake by Lycopersicum esculentum. Chemical Speciation and Bioavailability 17(1):19–26. https://doi.org/10.3184/095422905782774973" target="_blank">https://doi.org/10.3184/095422905782774973
Osmolovskaya, N. G., Kuchaeva, L. N., and Novak, V. A. 2007. Role of organic acids in the formation of the ionic composition in developing glycophyte leaves. Russian Journal of Plant Physiology 54(3):336–342. https://doi.org/10.1134/S1021443707030077" target="_blank">https://doi.org/10.1134/S1021443707030077
Panfili, F., Schneider, A., Vives, A., Perro, F., Hubert, P., Pellerin, S., and Hale, B. 2009. Cadmium uptake by durum wheat in presence of citrate. Plant and Soil 316(1-2):299–309. https://doi.org/10.1007/s11104-008-9782-2" target="_blank">https://doi.org/10.1007/s11104-008-9782-2
Pellet, D. M., Grunes, D. L., and Kochian, L. V. 1995. Organicacid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196(4):788–795. https://doi.org/10.1007/BF01106775" target="_blank">https://doi.org/10.1007/BF01106775
Pineros, M. A., Shaff, J. E., Manslank, H. S., Alves, V. M. C., and Kochian, L. V. 2005. Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiology 137(1):231–241. https://doi.org/10.1104/pp.104.047357" target="_blank">https://doi.org/10.1104/pp.104.047357
Rauser, W. E. 1999. Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin, and metallothioneins. Cell Biochemistry and Biophysics 31:19–48. https://doi.org/10.1007/BF02738153" target="_blank">https://doi.org/10.1007/BF02738153
Ryan, P. R., Delhaize, E., and Jones, D. 2001. Function and mechanism of organic anion exudation from plant roots. Annual review of plant physiology and plant molecular biology 52:527–560. https://doi.org/10.1146/annurev.arplant.52.1.527" target="_blank">https://doi.org/10.1146/annurev.arplant.52.1.527
Ryan, P. R., Tyerman, S. D., Sasaki, T., Yamamoto, Y., Zhang, W. H., and Delhaize E. 2011. The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. Journal of Experimental Botany 62(1):9–20. https://doi.org/10.1146/annurev.arplant.52.1.527" target="_blank">https://doi.org/10.1146/annurev.arplant.52.1.527
Salt, D. E., Prince, R. C., Baker, A. J. M., Raskin, I., and Pickering, I. J. 1999. Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environmental Science and Technology 33(5):713–717. https://doi.org/10.1021/es980825x" target="_blank">http://doi.org/10.1021/es980825x
Sarret, G., Saumitou-Laprade, P., Bert, V., Proux, O., Hazemann, J.-L., Traverse, A., Marcus, M. A., and Manceau, A. 2002. Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiology 130(4):1815–1826. https://doi.org/10.1104/pp.007799" target="_blank">https://doi.org/10.1104/pp.007799
Sazanova, K., Osmolovskaya, N., Schiparev S., Jakkonen K., Kuchaeva L., and Vlasov D. 2015. Organic acids induce tolerance to zinc- and copper-exposed fungi under various growth conditions. Current Microbiology 70(4):520–527. https://doi.org/10.1007/s00284-014-0751-0" target="_blank">https://doi.org/10.1007/s00284-014-0751-0
Schwab, A. P., Zhu, D. S., and Banks, M. K. 2008. Influence of organic acids on the transport of heavy metals in soil. Chemosphere 72(6):986–994. https://doi.org/10.1016/j.chemosphere.2008.02.047" target="_blank">https://doi.org/10.1016/j.chemosphere.2008.02.047
Senden, M. H. M. N., Van Paassen, F. J. M., Van der Meer, A. J. G. M., and Wolterbeek, H. T. 1992. Cadmium–citric acid–xylem cell wall interactions in tomato plants. Plant, Cell and Environment 15(1):71–79. https://doi.org/10.1111/j.1365-3040.1992.tb01459.x" target="_blank">https://doi.org/10.1111/j.1365-3040.1992.tb01459.x
Senden M. H. M. N., van der Meer A. J. G. M., Verburg, T. G., and Wolterbeek, H. T. 1995. Citric acid in tomato plant roots and its effect on cadmium uptake and distribution. Plant and Soil 171(2): 333–339. https://doi.org/10.1007/BF00010289" target="_blank">https://doi.org/10.1007/BF00010289
Shen, R., Iwashita, T., and Ma, J. F. 2004. Form of Al changes with Al concentration in leaves of buckwheat. Journal of Experimental Botany 55(394):131–136. https://doi.org/10.1093/jxb/erh016" target="_blank">https://doi.org/10.1093/jxb/erh016
Sun, R. L., Zhou, Q. X., and Jin, C. X. 2006. Cadmium accumulation in relation to organic acids in leaves of Solanum nigrum L. as a newly found cadmium hyperaccumulator. Plant and Soil 285(1–2):125–134. https://doi.org/10.1007/s11104-006-0064-6" target="_blank">https://doi.org/10.1007/s11104-006-0064-6
Titov, A. F., Kaznina, N. M., and Talanova, V. V. 2014. Tyazelye metally v rastenijah. [Heavy metals in plants]. 194 pp. Karelian research center of RAS. Petrozavodsk. https://doi.org/10.17076/eco112" target="_blank">https://doi.org/10.17076/eco112
Tolrà, R. P., Poschenrieder, C., and Barceló, J. 1996. Zinc hyperaccumulation in Thlaspi caerulescens. II. Influence on organic acids. Journal of Plant Nutrition 19(12):1541–1550. https://doi.org/10.1080/01904169609365220" target="_blank">https://doi.org/10.1080/01904169609365220
Turgut, C., Pepe, M. K., and Cutright, T. J. 2004. The effect of EDTA and citric acid on phytoremediation of Cd, Cr, and Ni from soil using Helianthus annuus. Environmental Pollution 131(1):147–154. https://doi.org/10.1016/j.envpol.2004.01.017" target="_blank">https://doi.org/10.1016/j.envpol.2004.01.017
Wójcik, M., Skórzynska-Polit, E., and Tukiendorf, A. 2006. Organic acids accumulation and antioxidant enzyme activities in Thlaspi caerulescens under Zn and Cd stress. Plant Growth Regulation 48(2):145–155. https://doi.org/10.1007/s10725-005-5816-4" target="_blank">https://doi.org/10.1007/s10725-005-5816-4
Wu, L. H., Luo, Y. M., Xing, X. R., and Christie, P. 2004. EDTA-enhanced phytoremediation of heavy metal contaminated soil with Indian mustard and associated potential leaching risk. Agriculture, Ecosystems and Environment 102(3):307–318. https://doi.org/10.1016/j.agee.2003.09.002" target="_blank">https://doi.org/10.1016/j.agee.2003.09.002
Wu, X., Li, R., Shi, J., Wang, J., Su,n Q., Zhang, H., Xing, Y., Qi, Y., Zhang, N., and Guo, Y-D. 2014. Brassica oleracea MATE encodes a citrate transporter and enhances aluminum tolerance in Arabidopsis thaliana. Plant and Cell Physiology 55(8):1426–1436. https://doi.org/10.1093/pcp/pcu067" target="_blank">https://doi.org/10.1093/pcp/pcu067
Yang, J. L., Zhang, L., and Zheng, S. J. 2008. Aluminum-activated oxalate secretion does not associate with internal content among some oxalate accumulators. Journal of Integrative Plant Biology 50(9):1103–1107. https://doi.org/10.1111/j.1744-7909.2008.00687.x" target="_blank">https://doi.org/10.1111/j.1744-7909.2008.00687.x
Yang, L. T., Jiang, H. X., Qi, Y. P., and Chen, L. S. 2012. Differential expression of genes involved in alternative glycolytic pathways, phosphorus scavenging and recycling in response to aluminum and phosphorus interactions in citrus roots. Molecular Biology Reports 39(5):6353–6366. https://doi.org/10.1007/s11033-012-1457-7" target="_blank">https://doi.org/10.1007/s11033-012-1457-7
Yang, L. T., Qi, Y. P., Jiang ,H. X., and Chen, L. S. 2013. Roles of organic acid anion secretion in aluminium tolerance of higher plants. BioMed Research International Volume 2013. Article ID 173682. https://doi.org/10.1155/2013/173682" target="_blank">https://doi.org/10.1155/2013/173682
Yang, L., Zheng, S. J., He, Y. F., and Matsumoto, H. 2005. Aluminium resistance requires resistance to acid stress: a case study with spinach that exudes oxalate rapidly when exposed to Al stress. Journal of Experimental Botany 56(414):1197–1203. https://doi.org/10.1093/jxb/eri113" target="_blank">https://doi.org/10.1093/jxb/eri113
Yang, X. E., Baligar, V. C., Foster, J. C., and Marten, D. C. 1997. Accumulation and transport of nickel in relation to organic acid in ryegrass and maize grown with different nickel levels. Plant and Soil 196(2):271–276. https://doi.org/10.1023/A:1004270528532" target="_blank">https://doi.org/10.1023/A:1004270528532
Yang, X., Feng, Y., He, X. L., and Stoffella, P. J. 2005. Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. Journal of Trace Elements in Medicine and Biology 18(4):339–353. https://doi.org/10.1016/j.jtemb.2005.02.007" target="_blank">https://doi.org/10.1016/j.jtemb.2005.02.007
Yang, X. E., Li, T. Q., Yang, J. C., He, Z. L., Lu, L. L., and Meng, F. H. 2006. Zinc compartmentation in root, transport into xylem, and absorption into leaf cells in the hyperaccumulating species of Sedum alfredii Hance. Planta 224(1):185–195. https://doi.org/10.1007/s00425-005-0194-8" target="_blank">https://doi.org/10.1007/s00425-005-0194-8
Yang, Y. Y., Jung, J. Y., Song, W. Y., Suh, H. S., and Lee, Y. 2000. Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiology 124(3):1019–1026. https://doi.org/10.1104/pp.124.3.1019" target="_blank">https://doi.org/10.1104/pp.124.3.1019
Zhao, F. J., Lombi, E., Breedon, T., and McGrath, S. P. 2000. Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant, Cell and Environment 23(5):507–514. https://doi.org/10.1046/j.1365-3040.2000.00569.x" target="_blank">https://doi.org/10.1046/j.1365-3040.2000.00569.x
Zhu, X. F, Zheng, C., Hu, Y. T., Jiang, T., Liu, Y., Dong, N. Y., Yang J. L, and Zheng, S. J. 2011. Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant, Cell and Environment 34(7):1055–1064. https://doi.org/10.1111/j.1365-3040.2011.02304.x" target="_blank">https://doi.org/10.1111/j.1365-3040.2011.02304.x
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2018-06-08
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Osmolovskaya, N., Vu, D. V., & Kuchaeva, L. (2018). The role of organic acids in heavy metal tolerance in plants. Biological Communications, 63(1), 9–16. https://doi.org/10.21638/spbu03.2018.103
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