Metal ion toxicity and tolerance mechanisms in plants growing in acidic soil
DOI:
https://doi.org/10.20961/stjssa.v18i1.51254Keywords:
Metal toxicity, Detoxification, Organic acid, Aluminum, Iron, ArsenicAbstract
The abiotic factors have a wide effect on the growth of plants along with the cultivation of staple crops. The concentration of both essential and non-essential elements is impacted by number of biogeochemical factors. The low pH (≤5.0) of the soil is one such factor which poses variation in the levels of metal ions and mostly it leads to metal toxicity. The excess concentrations of the elements in the soil affects the growth, yield and the metabolic activities of the plants making them susceptible. However, some of the genotypes adapt themselves to metal toxicity condition by regulating their homeostatic genes leading to develop different strategies to undergo detoxification method. In the present review we discuss about the toxicity of Al, Fe and As which is a non-essential metal, an essential metal and an unwanted heavy metal. In a broad picture, to escape the toxic effects, plants have the strategy to exclude the excess metal outside the plant or include it in its storage cells. The insight of the present review aims at understanding these strategies in details which can be put into agricultural applications for developing better crops.Downloads
References
Adamczyk-Szabela, D., Markiewicz, J., & Wolf, W. M. (2015). Heavy Metal Uptake by Herbs. IV. Influence of Soil pH on the Content of Heavy Metals in Valeriana officinalis L. Water, Air, & Soil Pollution, 226(4), 106. https://doi.org/10.1007/s11270-015-2360-3
Adeleke, R., Nwangburuka, C., & Oboirien, B. (2017). Origins, roles and fate of organic acids in soils: A review. South African Journal of Botany, 108, 393-406. https://doi.org/10.1016/j.sajb.2016.09.002
Agnello, A. C., Huguenot, D., Van Hullebusch, E. D., & Esposito, G. (2014). Enhanced Phytoremediation: A Review of Low Molecular Weight Organic Acids and Surfactants Used as Amendments. Critical Reviews in Environmental Science and Technology, 44(22), 2531-2576. https://doi.org/10.1080/10643389.2013.829764
Aguilera, J. G., Teodoro, P. E., da Silva Junior, J. P., Pereira, J. F., Zuffo, A. M., & Consoli, L. (2019). Selection of Aluminum-Resistant Wheat Genotypes Using Multienvironment and Multivariate Indices. Agronomy Journal, 111(6), 2804-2810. https://doi.org/10.2134/agronj2019.06.0470
Al-Huqail, A. A., Al-Rashed, S. A., Ibrahim, M. M., El-Gaaly, G. A., & Qureshi, M. I. (2017). Arsenic induced eco-physiological changes in Chickpea (Cicer arietinum) and protection by gypsum, a source of sulphur and calcium. Scientia Horticulturae, 217, 226-233. https://doi.org/https://doi.org/10.1016/j.scienta.2017.02.007
Anoop, V. M., Basu, U., McCammon, M. T., McAlister-Henn, L., & Taylor, G. J. (2003). Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant physiology, 132(4), 2205-2217. https://doi.org/10.1104/pp.103.023903
Aoyama, T., Kobayashi, T., Takahashi, M., Nagasaka, S., Usuda, K., Kakei, Y., Ishimaru, Y., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2009). OsYSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol Biol, 70(6), 681-692. https://doi.org/10.1007/s11103-009-9500-3
Arunakumara, K. K. I. U., Walpola, B. C., & Yoon, M.-H. (2013). Aluminum toxicity and tolerance mechanism in cereals and legumes — A review. Journal of the Korean Society for Applied Biological Chemistry, 56(1), 1-9. https://doi.org/10.1007/s13765-012-2314-z
Aung, M. S., & Masuda, H. (2020). How Does Rice Defend Against Excess Iron?: Physiological and Molecular Mechanisms [Mini Review]. Frontiers in Plant Science, 11(1102). https://doi.org/10.3389/fpls.2020.01102
Bashir, K., Hanada, K., Shimizu, M., Seki, M., Nakanishi, H., & Nishizawa, N. K. (2014). Transcriptomic analysis of rice in response to iron deficiency and excess. Rice, 7(1), 18. https://doi.org/10.1186/s12284-014-0018-1
Blake, L., & Goulding, K. W. T. (2002). Effects of atmospheric deposition, soil pH and acidification on heavy metal contents in soils and vegetation of semi-natural ecosystems at Rothamsted Experimental Station, UK. Plant and Soil, 240(2), 235-251. https://doi.org/10.1023/A:1015731530498
Bojórquez-Quintal, E., Escalante-Magaña, C., EchevarrÃa-Machado, I., & MartÃnez-Estévez, M. (2017). Aluminum, a Friend or Foe of Higher Plants in Acid Soils [Review]. Frontiers in Plant Science, 8(1767). https://doi.org/10.3389/fpls.2017.01767
Bonneau, J., Baumann, U., Beasley, J., Li, Y., & Johnson, A. A. (2016). Identification and molecular characterization of the nicotianamine synthase gene family in bread wheat. Plant Biotechnol J, 14(12), 2228-2239. https://doi.org/10.1111/pbi.12577
Chen, L., Liu, Y., Liu, H., Kang, L., Geng, J., Gai, Y., Ding, Y., Sun, H., & Li, Y. (2015). Identification and expression analysis of MATE genes involved in flavonoid transport in blueberry plants. PLoS One, 10(3), e0118578. https://doi.org/10.1371/journal.pone.0118578
Chibuike, G. U., & Obiora, S. C. (2014). Heavy Metal Polluted Soils: Effect on Plants and Bioremediation Methods. Applied and Environmental Soil Science, 2014, 752708. https://doi.org/10.1155/2014/752708
Connorton, J. M., Balk, J., & RodrÃguez-Celma, J. (2017). Iron homeostasis in plants - a brief overview. Metallomics : integrated biometal science, 9(7), 813-823. https://doi.org/10.1039/c7mt00136c
Conte, S. S., & Walker, E. L. (2011). Transporters contributing to iron trafficking in plants. Mol Plant, 4(3), 464-476. https://doi.org/10.1093/mp/ssr015
Delhaize, E., Ryan, P. R., Hebb, D. M., Yamamoto, Y., Sasaki, T., & Matsumoto, H. (2004). Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proceedings of the National Academy of Sciences of the United States of America, 101(42), 15249-15254. https://doi.org/10.1073/pnas.0406258101
Dey, S., Regon, P., Kar, S., & Panda, S. K. (2020). Chelators of iron and their role in plant’s iron management. Physiology and Molecular Biology of Plants, 26(8), 1541-1549. https://doi.org/10.1007/s12298-020-00841-y
Dufey, I., Hiel, M.-P., Hakizimana, P., Draye, X., Lutts, S., Koné, B., Dramé, K. N., Konaté, K. A., Sie, M., & Bertin, P. (2012). Multienvironment Quantitative Trait Loci Mapping and Consistency across Environments of Resistance Mechanisms to Ferrous Iron Toxicity in Rice. Crop Science, 52(2), 539-550. https://doi.org/https://doi.org/10.2135/cropsci2009.09.0544
Durrett, T. P., Gassmann, W., & 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
Eekhout, T., Larsen, P., & De Veylder, L. (2017). Modification of DNA Checkpoints to Confer Aluminum Tolerance. Trends in Plant Science, 22(2), 102-105. https://doi.org/https://doi.org/10.1016/j.tplants.2016.12.003
Fageria, N. K., Santos, A. B., Barbosa Filho, M. P., & Guimarães, C. M. (2008). Iron Toxicity in Lowland Rice. Journal of Plant Nutrition, 31(9), 1676-1697. https://doi.org/10.1080/01904160802244902
Famoso, A. N., Clark, R. T., Shaff, J. E., Craft, E., McCouch, S. R., & Kochian, L. V. (2010). Development of a Novel Aluminum Tolerance Phenotyping Platform Used for Comparisons of Cereal Aluminum Tolerance and Investigations into Rice Aluminum Tolerance Mechanisms Plant physiology, 153(4), 1678-1691. https://doi.org/10.1104/pp.110.156794
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
Hell, R., & Stephan, U. W. (2003). Iron uptake, trafficking and homeostasis in plants. Planta, 216(4), 541-551. https://doi.org/10.1007/s00425-002-0920-4
Huang, C. F., Yamaji, N., Mitani, N., Yano, M., Nagamura, Y., & Ma, J. F. (2009). A bacterial-type ABC transporter is involved in aluminum tolerance in rice. The Plant cell, 21(2), 655-667. https://doi.org/10.1105/tpc.108.064543
Inoue, H., Kobayashi, T., Nozoye, T., Takahashi, M., Kakei, Y., Suzuki, K., Nakazono, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2009). Rice OsYSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem, 284(6), 3470-3479. https://doi.org/10.1074/jbc.M806042200
Johnson, J. F., Vance, C. P., & Allan, D. L. (1996). Phosphorus Deficiency in Lupinus albus (Altered Lateral Root Development and Enhanced Expression of Phosphoenolpyruvate Carboxylase). Plant physiology, 112(1), 31-41. https://doi.org/10.1104/pp.112.1.31
Khalid, S., Shahid, M., Niazi, N. K., Rafiq, M., Bakhat, H. F., Imran, M., Abbas, T., Bibi, I., & Dumat, C. (2017). Arsenic behaviour in soil-plant system: Biogeochemical reactions and chemical speciation influences. In Enhancing cleanup of environmental pollutants (pp. 97-140). Springer. https://doi.org/10.1007/978-3-319-55423-5_4
Kobayashi, T., & Nishizawa, N. K. (2012). Iron Uptake, Translocation, and Regulation in Higher Plants. Annual Review of Plant Biology, 63(1), 131-152. https://doi.org/10.1146/annurev-arplant-042811-105522
Kochian, L. V., Hoekenga, O. A., & Piñeros, M. A. (2004). HOW DO CROP PLANTS TOLERATE ACID SOILS? MECHANISMS OF ALUMINUM TOLERANCE AND PHOSPHOROUS EFFICIENCY. Annual Review of Plant Biology, 55(1), 459-493. https://doi.org/10.1146/annurev.arplant.55.031903.141655
Kochian, L. V., Piñeros, M. A., Liu, J., & Magalhaes, J. V. (2015). Plant Adaptation to Acid Soils: The Molecular Basis for Crop Aluminum Resistance. Annual Review of Plant Biology, 66(1), 571-598. https://doi.org/10.1146/annurev-arplant-043014-114822
Larsen, P. B., Geisler, M. J., Jones, C. A., Williams, K. M., & Cancel, J. D. (2005). ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J, 41(3), 353-363. https://doi.org/10.1111/j.1365-313X.2004.02306.x
Li, G., Kronzucker, H. J., & Shi, W. (2016). Root developmental adaptation to Fe toxicity: Mechanisms and management. Plant Signaling & Behavior, 11(1), e1117722. https://doi.org/10.1080/15592324.2015.1117722
Li, J.-Y., Liu, J., Dong, D., Jia, X., McCouch, S. R., & Kochian, L. V. (2014). Natural variation underlies alterations in Nramp aluminum transporter (<em>NRAT1</em>) expression and function that play a key role in rice aluminum tolerance. Proceedings of the National Academy of Sciences, 111(17), 6503. https://doi.org/10.1073/pnas.1318975111
Likar, M., Vogel-MikuÅ¡, K., Potisek, M., HanÄević, K., Radić, T., NeÄemer, M., & Regvar, M. (2015). Importance of soil and vineyard management in the determination of grapevine mineral composition. Science of The Total Environment, 505, 724-731. https://doi.org/10.1016/j.scitotenv.2014.10.057
López-Bucio, J., Nieto-Jacobo, M. a. F., RamıÌrez-RodrıÌguez, V., & 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
Montiel-Rozas, M. M., Madejón, E., & Madejón, P. (2016). Effect of heavy metals and organic matter on root exudates (low molecular weight organic acids) of herbaceous species: An assessment in sand and soil conditions under different levels of contamination. Environmental Pollution, 216, 273-281. https://doi.org/10.1016/j.envpol.2016.05.080
Muller, N. C., & Nowack, B. (2010). Nano zero valent iron – THE solution for water and soil remediation? Observatory NANO Focus Report, Netherlands. https://www.yumpu.com/en/document/read/6104945/nano-zero-valent-iron-the-solution-for-water-and-soil-remediation
Neina, D. (2019). The Role of Soil pH in Plant Nutrition and Soil Remediation. Applied and Environmental Soil Science, 2019, 5794869. https://doi.org/10.1155/2019/5794869
Nozoye, T., von Wirén, N., Sato, Y., Higashiyama, T., Nakanishi, H., & Nishizawa, N. K. (2019). Characterization of the Nicotianamine Exporter ENA1 in Rice [Original Research]. Frontiers in Plant Science, 10(502). https://doi.org/10.3389/fpls.2019.00502
OveÄka, M., & TakáÄ, T. (2014). Managing heavy metal toxicity stress in plants: Biological and biotechnological tools. Biotechnology Advances, 32(1), 73-86. https://doi.org/10.1016/j.biotechadv.2013.11.011
Pourrut, B., Shahid, M., Dumat, C., Winterton, P., & Pinelli, E. (2011). Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol, 213, 113-136. https://doi.org/10.1007/978-1-4419-9860-6_4
Rudrappa, T., Czymmek, K. J., PareÌ, P. W., & Bais, H. P. (2008). Root-Secreted Malic Acid Recruits Beneficial Soil Bacteria Plant physiology, 148(3), 1547-1556. https://doi.org/10.1104/pp.108.127613
Sahrawat, K. L. (2005). Iron Toxicity in Wetland Rice and the Role of Other Nutrients. Journal of Plant Nutrition, 27(8), 1471-1504. https://doi.org/10.1081/PLN-200025869
Santos, A. L. d., Chaves-Silva, S., Yang, L., Maia, L. G. S., Chalfun-Júnior, A., Sinharoy, S., Zhao, J., & Benedito, V. A. (2017). Global analysis of the MATE gene family of metabolite transporters in tomato. BMC Plant Biology, 17(1), 185. https://doi.org/10.1186/s12870-017-1115-2
Sasaki, T., Yamamoto, Y., Ezaki, B., Katsuhara, M., Ahn, S. J., Ryan, P. R., Delhaize, E., & Matsumoto, H. (2004). A wheat gene encoding an aluminum-activated malate transporter. Plant J, 37(5), 645-653. https://doi.org/10.1111/j.1365-313x.2003.01991.x
Sharma, T., Dreyer, I., Kochian, L., & Piñeros, M. A. (2016). The ALMT Family of Organic Acid Transporters in Plants and Their Involvement in Detoxification and Nutrient Security [Review]. Frontiers in Plant Science, 7(1488). https://doi.org/10.3389/fpls.2016.01488
Singh, P. K., Indoliya, Y., Chauhan, A. S., Singh, S. P., Singh, A. P., Dwivedi, S., Tripathi, R. D., & Chakrabarty, D. (2017). Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress. Scientific Reports, 7(1), 3592. https://doi.org/10.1038/s41598-017-03923-2
Singh, S., Parihar, P., Singh, R., Singh, V. P., & Prasad, S. M. (2016). Heavy Metal Tolerance in Plants: Role of Transcriptomics, Proteomics, Metabolomics, and Ionomics [Review]. Frontiers in Plant Science, 6(1143). https://doi.org/10.3389/fpls.2015.01143
Srivastava, S., Suprasanna, P., & D’Souza, S. F. (2012). Mechanisms of Arsenic Tolerance and Detoxification in Plants and their Application in Transgenic Technology: A Critical Appraisal. International Journal of Phytoremediation, 14(5), 506-517. https://doi.org/10.1080/15226514.2011.604690
Wan, J. L., Zhai, H. Q., & Wan, J. M. (2005). Mapping of QTLS for ferrous iron toxicity tolerance in rice (Oryza sativa L.). Yi Chuan Xue Bao, 32(11), 1156-1166.
Wu, L.-B., Shhadi, M. Y., Gregorio, G., Matthus, E., Becker, M., & Frei, M. (2014). Genetic and physiological analysis of tolerance to acute iron toxicity in rice. Rice (New York, N.Y.), 7(1), 8-8. https://doi.org/10.1186/s12284-014-0008-3
Wu, L., Kobayashi, Y., Wasaki, J., & Koyama, H. (2018). Organic acid excretion from roots: a plant mechanism for enhancing phosphorus acquisition, enhancing aluminum tolerance, and recruiting beneficial rhizobacteria. Soil Science and Plant Nutrition, 64(6), 697-704. https://doi.org/10.1080/00380768.2018.1537093
Xu, X. Y., McGrath, S. P., & Zhao, F. J. (2007). Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol, 176(3), 590-599. https://doi.org/10.1111/j.1469-8137.2007.02195.x
Yang, Z. B., You, J. F., Xu, M. Y., & Yang, Z. M. (2009). Interaction between aluminum toxicity and manganese toxicity in soybean (Glycine max). Plant and Soil, 319(1), 277-289. https://doi.org/10.1007/s11104-008-9869-9
Zhang, X., Zhang, D., Sun, W., & Wang, T. (2019). The Adaptive Mechanism of Plants to Iron Deficiency via Iron Uptake, Transport, and Homeostasis. International journal of molecular sciences, 20(10), 2424. https://doi.org/10.3390/ijms20102424
Zheng, L., Fujii, M., Yamaji, N., Sasaki, A., Yamane, M., Sakurai, I., Sato, K., & Ma, J. F. (2011). Isolation and Characterization of a Barley Yellow Stripe-Like Gene, HvYSL5. Plant and Cell Physiology, 52(5), 765-774. https://doi.org/10.1093/pcp/pcr009
Downloads
Additional Files
Published
Issue
Section
License
Authors who publish with this journal agree to the following terms:- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution-NonCommercial License that allows others to Share (copy and redistribute the material in any medium or format) and Adapt (remix, transform, and build upon the material) the work non-commercially with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).


.png)











