The impact of heavy metals on plant organisms and methods of their analysis: an overview
DOI:
https://doi.org/10.31489/2025feb4/92-109Keywords:
heavy metals, aluminum, phytotoxicity, industrial pollution, acidic soils, environmental monitoring, bioavailability, phytoremediationAbstract
This review provides a detailed analysis of the impact of heavy metals on plant organisms, with a focus on the specific issue of aluminum toxicity in Kazakhstan’s industrial regions. The rapid expansion of mining and metallurgical industries has resulted in elevated pollutant emissions, with aluminum posing a significant environmental risk. Unlike other metals, its phytotoxicity manifests indirectly through soil acidification caused by acid rain (resulting from SO₂ and NOₓ emissions), which mobilizes toxic Al³⁺ ions from aluminosilicates. The Pavlodar region serves as a case study to examine secondary aluminum contamination and its major effects on plant roots, including growth inhibition, cytoskeleton disruption, mineral nutrient imbalance, and oxidative stress. The review compiles data on heavy metal accumulation in plants across Kazakhstan and critically evaluates advanced analytical techniques (ICP-MS, XAS, EXAFS) that are essential for determining aluminum bioavailability and toxicity. It also highlights the role of plants as bioindicators and the potential of phytoremediation technologies. Based on current research, the review recommends adaptive measures for Kazakhstan, including soil liming, the use of aluminum-tolerant plant species, and implementation of modern environmental monitoring to reduce ecological risks and maintain ecosystem productivity
References
1 Vareda, J.P., Valente, A.J.M.& Durães, L. (2019). Assessment of heavy metal pollution from anthropogenic activities and remediation strategies: A review. J. Environ. Manage, 246; 101-118. https://doi.org/10.1016/j.jenvman.2019.05.126 DOI: https://doi.org/10.1016/j.jenvman.2019.05.126
2 Tseshkovskaya, Y.A., Golubeva, E.I., Ibrayev, M.K., Oralova, A.T., Tsoy, N.K. &Issabayeva, M.B. (2019). Technogenic impact of mining industry on environment in karaganda region of republic of kazakhstan. News of the National Academy of Sciences of the Republic of Kazakhstan, Series of Geology and Technical Sciences, 6(438); 85-95. https://doi.org/10.32014/2019.2518-170X.159 DOI: https://doi.org/10.32014/2019.2518-170X.159
3 Singh, R., Gautam, N., Mishra, A. & Gupta, R. (2011). Heavy metals and living systems: An overview. Indian Journal of Pharmacology, 43(3); 246-53. https://doi.org/10.4103/0253-7613.81505 DOI: https://doi.org/10.4103/0253-7613.81505
4 Information bulletin on the state of the environment of the Republic of Kazakhstan. 1st half of 2024. Astana, 2024; 4-5. https://ecogosfond.kz/orhusskaja-konvencija/dostup-k-jekologicheskoj-informacii/jekologijaly-zha-daj/orsha-an-otrany-zhaj-k-ji-turaly-a-paratty-bjulletender/
5 Sushkova, S., Minkina, T., Dudnikova, T., Barbashev, A., Popov, Y., Rajput, V., Bauer, T., Nazarenko, O. & Kızılkaya, R. (2021). Reduced plant uptake of PAHs from soil amended with sunflower husk biochar. Eurasian Journal of Soil Science, 10(4); 269-277. https://doi.org/10.18393/ejss.935397 DOI: https://doi.org/10.18393/ejss.935397
6 Zhyrgalova, A., Yelemessov, S., Ablaikhan, B., Aitkhozhayeva, G. &Zhildikbayeva, A. (2024). Assessment of potential ecological risk of heavy metal contamination of agricultural soils in Kazakhstan. Brazilian Journal of Biology, 84. https://doi.org/10.1590/1519-6984.280583
7 Shomanova, Z., Nossenko, Y., Yerkibayeva, M., Yessimova, D., Kuspanova, A., Aldasheva, A., Kaimuldinova, K. & Safarov, R. (2025). Environmental risk assessment for sustainable industrial urban development: The case of northern industrial zone of Pavlodar, Kazakhstan. PLoS ONE, 20(4); e0320835. https://doi.org/10.1371/journal.pone.0320835 DOI: https://doi.org/10.1371/journal.pone.0320835
8 Balali-Mood, M., Naseri, K., Tahergorabi, Z., Khazdair, M.R. & Sadeghi, M. (2021). Toxic Mechanisms of Five Heavy Metals: Mercury, Lead, Chromium, Cadmium, and Arsenic. Front Pharmacol, 13; 12:643972. https://doi.org/10.3389/fphar.2021.643972 DOI: https://doi.org/10.3389/fphar.2021.643972
9 Faurat, A., Azhayev, G., Shupshibayev, K., Akhmetov, K., Boribay, E. &Abylkhassanov, T. (2024). Assessment of heavy metal contamination and health risks in "snow cover-soil cover-vegetation system" of urban and rural gardens of an industrial city in Kazakhstan. International Journal of Environmental Research and Public Health, 21(8); 1002. https://doi.org/10.3390/ijerph21081002 DOI: https://doi.org/10.3390/ijerph21081002
10 Kerimray, A., Assanov, D., Kenessov, B., Karaca, F. (2020). Trends and health impacts of major urban air pollutants in Kazakhstan. J Air Waste Manag Assoc, 70(11); 1148-1164. https://doi.org/10.1080/10962247.2020.1813837. DOI: https://doi.org/10.1080/10962247.2020.1813837
11 National report on the state of the environment and the use of natural resources of the Republic of Kazakhstan for 2022. Astana, 2023; 9-10. https://ecogosfond.kz/orhusskaja-konvencija/dostup-k-jekologicheskoj-informacii/jekologijaly-zha-daj/orsha-an-otrany-zhaj-k-ji-turaly-a-paratty-bjulletender/
12 National report on the state of the environment and the use of natural resources of the Republic of Kazakhstan for 2022. Astana, 2023; 10-11. https://ecogosfond.kz/orhusskaja-konvencija/dostup-k-jekologicheskoj-informacii/jekologijaly-zha-daj/orsha-an-otrany-zhaj-k-ji-turaly-a-paratty-bjulletender/
13 Order of the Minister of Health of the Republic of Kazakhstan dated August 2, 2022 No. KR DSM-70 "On approval of Hygienic standards for atmospheric air in urban and rural settlements, on the territories of industrial organizations". https://adilet.zan.kz/rus/docs/V2200029011
14 Beisenova, R., Kuanyshevich, B.Z., Turlybekova, G., Yelikbayev, B., Kakabayev, A.A., Shamshedenova, S. &Nugmanov, A. (2023). Assessment of atmospheric air quality in the region of Central Kazakhstan and Astana. Atmosphere, 14(11); 1601. https://doi.org/10.3390/atmos14111601 DOI: https://doi.org/10.3390/atmos14111601
15 Li, H., He, Q., & Liu, X. (2020). Identification of long-range transport pathways and potential source regions of pm2.5 and pm10 at akedala station, central asia. Atmosphere, 11(11). https://doi.org/10.3390/atmos11111183 DOI: https://doi.org/10.3390/atmos11111183
16 Wondimu, T & Forbes, Patricia. (2015). Metal and metalloid speciation in plants: Overview, instrumentation, approaches and commonly assessed elements. TrAC Trends in Analytical Chemistry. 77. 10.1016/j.trac.2015.10.007. DOI: https://doi.org/10.1016/j.trac.2015.10.007
17 He, C., Clifton, O., Felker-Quinn, E., Ryan Fulgham, S., JuncosaCalahorrano, J. F., Lombardozzi, D., … Steiner, A. L. (2021, March 1). Interactions between air pollution and terrestrial ecosystems perspectives on challenges and future directions. Bulletin of the American Meteorological Society. American Meteorological Society. https://doi.org/10.1175/BAMS-D-20-0066.1 DOI: https://doi.org/10.1175/BAMS-D-20-0066.1
18 He, S., Niu, Y., Xing, L., Liang, Z., Song, X., Ding, M. & Huang W. (2024) Research progress of the detection and analysis methods of heavy metals in plants. Front. Plant Sci., 15; 1310328. https://doi.org/10.3389/fpls.2024.1310328 DOI: https://doi.org/10.3389/fpls.2024.1310328
19 Fuhrer, J. &Bungener, P. (1999). Effects of air pollutants on plants. Analusis. John Wiley and Sons Inc., 27(4); 355-362. https://doi.org/10.1051/analusis:1999270355 DOI: https://doi.org/10.1051/analusis:1999270355
20 Cronin, P., Ryan, F. &Coughan, M. (2008). Undertaking a literature review: A step-by-step approach. British Journal of Nursing, 17(1); 38-43 DOI: https://doi.org/10.12968/bjon.2008.17.1.28059
21 Timothy, N., &Tagui W.E. (2019). Environmental Pollution by Heavy Metal: An Overview. International Journal of Environmental Chemistry, 3(2); 72. https://doi.org/10.11648/j.ijec.20190302.14 DOI: https://doi.org/10.11648/j.ijec.20190302.14
22 Saikia, A. & Thapa, P. (2022). Environmental Change in South Asia. Springer International Publishing, 8; 233 https://doi.org/10.1007/978-3-030-47660-1 DOI: https://doi.org/10.1007/978-3-030-47660-1
23 Vongdala, N., Tran, H.D., Xuan, T.D., Teschke, R. & Khanh, T.D. (2019). Heavy metal accumulation in water, soil, and plants of municipal solid waste landfill in Vientiane, Laos. International Journal of Environmental Research and Public Health, 16(1); 22. https://doi.org/10.3390/ijerph16010022 DOI: https://doi.org/10.3390/ijerph16010022
24 Alimbaev, T., Mazhitova, Z., Beksultanova, C. &Tentigulkyzy, N. (2020). Activities of mining and metallurgical industry enterprises of the Republic of Kazakhstan: Environmental problems and possible solutions. In E3S Web of Conferences. EDP Sciences, 175. https://doi.org/10.1051/e3sconf/202017514019 DOI: https://doi.org/10.1051/e3sconf/202017514019
25 Mukhamedzhanov, M.A., Kazanbayeva, L.M., Nurgaziyeva, A.A. &Rakhmetov, I.K. (2019). Environmental problems of south kazakhstan and pollution of drinking groundwater. In International Multidisciplinary Scientific GeoConference Surveying Geology and Mining Ecology Management, SGEM, 19; 207-214). https://doi.org/10.5593/sgem2019/1.2/S02.027 DOI: https://doi.org/10.5593/sgem2019/1.2/S02.027
26 Kalimoldina, L.M., Sultangazieva, G.S. &Suleimenova, M.Sh. (2022). Contamination of soils with heavy metal in the urban area of Almaty. Soil science and agrochemistry, (3); 38-45. https://cyberleninka.ru/article/n/contamination-of-soils-with-heavy-metal-in-the-urban-area-of-almaty DOI: https://doi.org/10.51886/1999-740X_2022_3_38
27 Zhyrgalova, A., Yelemessova, S., Ablaikhana, B., Aitkhozhayeva, G.& Zhildikbayeva, A. (2024). Assessment of potential ecological risk of heavy metal contamination of agricultural soils in Kazakhstan. Braz. J. Biol, 84; e280583. https://doi.org/10.1590/1519-6984.280583 DOI: https://doi.org/10.1590/1519-6984.280583
28 Matveyeva, I.V., Ponomarenko, O.I., Soltangaziyev, N.B., Nursapina, N.A., Nazarkulova, Sh.N. & Gurin, A.N. (2019). Heavy metals in soils of Almaty region (Kazakhstan). Chemical journal of Kazakhstan, 2(66); 62-68.
29 Tazitdinova, R.M., Beisenova, R.R., Grigoryev, A.I. &Issayenko, O.P. (2019). Contamination of soil with heavy metals in industrial districts of Kokshetau. Bulletin of the Karaganda university. Biology. Medicine. Geography series, 2(94)/2019; 93-98. DOI: https://doi.org/10.31489/2019bmg2/93-98
30 Kocjan, A., Kwasniewska, J. &Szurman-Zubrzycka, M. (2025). Understanding plant tolerance to aluminum: Exploring mechanisms and perspectives. Plant and Soil, 507; 195-219. https://doi.org/10.1007/s11104-024-06745-0 DOI: https://doi.org/10.1007/s11104-024-06745-0
31 Ofoe, R., Thomas, R.H., Asiedu, S.K., Wang-Pruski, G., Fofana, B. & Abbey, L. (2023). Aluminum in plant: Benefits, toxicity and tolerance mechanisms. Frontiers in Plant Science, 13; 1085998. https://doi.org/10.3389/fpls.2022.1085998 DOI: https://doi.org/10.3389/fpls.2022.1085998
32 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; 571-598. DOI: https://doi.org/10.1146/annurev-arplant-043014-114822
33 Islam, F., Yasmeen, T., Ali, Q., Ali, S., Arif, M.S., Hussain, S., et al. (2014). Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ. Saf., 104; 285-293. https://doi.org/10.1016/j.ecoenv.2014.03.008 DOI: https://doi.org/10.1016/j.ecoenv.2014.03.008
34 Ahammed, G.J., Wu, M.-J., Wang, Y.-Q., Yan, Y.-R., Mao, Q. Ren, J.-J., et al. (2020). Melatonin alleviates iron stress by improving iron homeostasis, antioxidant defense and secondary metabolism in cucumber. Sci. Hortic., 265; 109205. https://doi.org/10.1016/j.scienta.2020.109205 DOI: https://doi.org/10.1016/j.scienta.2020.109205
35 Rahman, S.U., Nawaz, M.F., Gul, S., Yasin, G., Hussain, B., Li, Y.-L., et al. (2022). State-of-the-art OMICS strategies against toxic effects of heavy metals in plants: A review. Ecotoxicol Environ. Saf., 242; 113952. https://doi.org/10.1016/j.ecoenv.2022.113952 DOI: https://doi.org/10.1016/j.ecoenv.2022.113952
36 El-Jaoual, T. & Cox, D.A. (1998). Manganese toxicity in plants. J. Plant Nutr., 21 (2); 353-386. https://doi.org/10.1080/01904169809365409 DOI: https://doi.org/10.1080/01904169809365409
37 Kaur, H., & Garg, N. (2021). Zinc toxicity in plants: a review. Planta. Springer Science and Business Media Deutschland GmbH, 253. https://doi.org/10.1007/s00425-021-03642-z DOI: https://doi.org/10.1007/s00425-021-03642-z
38Li, G., Kronzucker, H.J. & Shi, W. (2016). The response of the root apex in plant adaptation to iron heterogeneity in soil. Frontiers in Plant Science. Frontiers Media S.A., 7; 344. https://doi.org/10.3389/fpls.2016.00344 DOI: https://doi.org/10.3389/fpls.2016.00344
39 Veliksar, S., Lemanova, N., Gladei, M. & David, T. (2019). The Impact of Trace Elements Applied with PGPB on the Vitis vinifera L Seedlings Resistance to the Copper Excess in Soil. International Journal of Agriculture and Environmental Science, 6(4); 43-47. https://doi.org/10.14445/23942568/ijaes-v6i4p108 DOI: https://doi.org/10.14445/23942568/IJAES-V6I4P108
40 Ahmed, S., Sameen & Sardar, R. (2023). Improvement in growth and physiochemical attributes of Raphanus sativus L. through exogenous application of 28-Homobrassinolide under nickel stress. Sci. Hortic., 311; 111791. https://doi.org/10.1016/j.scienta.2022.111791 DOI: https://doi.org/10.1016/j.scienta.2022.111791
41 Shetty, R., Vidya, C.S.-N., Prakash, N.B., Lux, A. & Vaculík, M. (2021). Aluminum toxicity in plants and its possible mitigation in acid soils by biochar: A review. Sci. Total Environ., 765; 142744. https://doi.org/10.1016/j.scitotenv.2020.142744 DOI: https://doi.org/10.1016/j.scitotenv.2020.142744
42 Zulfiqar, U., Farooq, M., Hussain, S., Maqsood, M., Hussain, M., Ishfaq, M., et al. (2019). Lead toxicity in plants: Impacts and remediation. J. Environ. Manage, 250; 109557. https://doi.org/10.1016/j.jenvman.2019.109557 DOI: https://doi.org/10.1016/j.jenvman.2019.109557
43 Banerjee, S., Islam, J., Mondal, S., Saha, A., Saha, B. & Sen, A. (2023). Proactive attenuation of arsenic-stress by nano-priming: Zinc Oxide Nanoparticles in Vigna mungo (L.) Hepper trigger antioxidant defense response and reduce root-shoot arsenic translocation. J. Hazard Mater., 446; 130735. https://doi.org/10.1016/j.jhazmat.2023.130735 DOI: https://doi.org/10.1016/j.jhazmat.2023.130735
44 Haider, F.U., Liqun, C., Coulter, J.A., Cheema, S.A., Wu, J., Zhang, R., … Farooq, M. (2021). Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicology and Environmental Safety, 211; 111887. https://doi.org/10.1016/j.ecoenv.2020.111887 DOI: https://doi.org/10.1016/j.ecoenv.2020.111887
45 Ali, S., Mir, R. A., Tyagi, A., Manzar, N., Kashyap, A.S., Mushtaq, M., et al. (2023). Chromium toxicity in plants: signaling, mitigation, and future perspectives. Plants, 12 (7); 1502. https://doi.org/10.3390/plants12071502 DOI: https://doi.org/10.3390/plants12071502
46 Azevedo, R., Rodriguez, E., Mendes, R.J., Mariz-Ponte, N., Sario, S., Lopes, J.C., … Santos, C. (2018). Inorganic Hg toxicity in plants: A comparison of different genotoxic parameters. Plant Physiology and Biochemistry, 125; 247-254. https://doi.org/10.1016/j.plaphy.2018.02.015 DOI: https://doi.org/10.1016/j.plaphy.2018.02.015
47 Kiran, B.R., Sharma, R. (2022). Effect of heavy metals: An overview. Materials Today: Proc., 51; 880-885. https://doi.org/10.1016/j.matpr.2021.06.278 DOI: https://doi.org/10.1016/j.matpr.2021.06.278
48 Liang, J., Fang, H.-L., Zhang, T.-L., Wang, X.-X. & Liu, Y.-D. (2017). Heavy metal in leaves of twelve plant species from seven different areas in Shanghai, China. Urban For Urban Gree, 27; 390-398. https://doi.org/10.1016/j.ufug.2017.03.006 DOI: https://doi.org/10.1016/j.ufug.2017.03.006
49 Shahid, M., Dumat, C., Khalid, S., Schreck, E., Xiong, T.-T. & Niazi, N. K. (2017). Foliar heavy metal uptake, toxicity and detoxification in plants: A comparison of foliar and root metal uptake. J. Hazard Mater., 325; 36-58. https://doi.org/10.1016/j.jhazmat.2016.11.063 DOI: https://doi.org/10.1016/j.jhazmat.2016.11.063
50Vetchinnikova, L.V., Kuznetsova, T.Yu. & Titov, A.F. (2013). Features of the accumulation of heavy metals in the leaves of woody plants in urban areas in the North. Proceedings of the Karelian Scientific Center of the Russian Academy of Sciences, 3; 68-73.
51Hrotkó, K., Gyeviki, M., Sütöriné, D.M., Magyar, L., Mészáros, R., Honfi, P. & Kardos, L. (2021). Foliar dust and heavy metal deposit on leaves of urban trees in Budapest (Hungary). Environmental Geochemistry and Health, 43(5); 1927-1940. https://doi.org/10.1007/s10653-020-00769-y DOI: https://doi.org/10.1007/s10653-020-00769-y
52Ghuge, S.A., Nikalje, G.C., Kadam, U.S., Suprasanna, P. & Hong, J.-C. (2023). Comprehensive mechanisms of heavy metal toxicity in plants, detoxification, and remediation. J. Hazard Mater., 450; 131039. https://doi.org/10.1016/j.jhazmat.2023.131039 DOI: https://doi.org/10.1016/j.jhazmat.2023.131039
53 Souri, Z., Karimi, N. & Sandalio, L. M. (2017). Arsenic hyperaccumulation strategies: an overview. Front. Cell Dev. Biol., 5. https://doi.org/10.3389/fcell.2017.00067 DOI: https://doi.org/10.3389/fcell.2017.00067
54 Zhang, D.-Y., Yang, S.-W., Ma, Q.-F., Sun, J.-N., Cheng, H.-Y., Wang, Y.-C., et al. (2020). Simultaneous multi-elemental speciation of As, Hg and Pb by inductively coupled plasma mass spectrometry interfaced with high-performance liquid chromatography. Food Chem., 313; 126119. https://doi.org/10.1016/j.foodchem.2019.126119 DOI: https://doi.org/10.1016/j.foodchem.2019.126119
55 El-Khatib, A.A., Youssef, N.A., Barakat, N.A. & Samir, N.A. (2020). Responses of Eucalyptus globulus and Ficus nitida to different potential of heavy metal air pollution. International Journal of Phytoremediation, 22(10); 986-999. https://doi.org/10.1080/15226514.2020.1719031 DOI: https://doi.org/10.1080/15226514.2020.1719031
56 Salt, D.E., Blaylock, M., Kumar, N.P.B.A., Dushenkov, V., Ensley, B.D., Chet, I. & Raskin, I. (1995). Phytoremediation: A novel strategy for the removal of toxic metals from the environment using plants. Bio/Technology, 13(5), 468-474. https://doi.org/10.1038/nbt0595-468 DOI: https://doi.org/10.1038/nbt0595-468
57 Wei, Z., Van Le, Q., Peng, W., Yang, Y., Yang, H., Gu, H., … Sonne, C. (2021). A review on phytoremediation of contaminants in air, water and soil. Journal of Hazardous Materials, 403; https://doi.org/10.1016/j.jhazmat.2020.123658 DOI: https://doi.org/10.1016/j.jhazmat.2020.123658
58 Guo, C.-Y., Lv, L.-J., Liu, Y.-C., Ji, M.-Y., Zang, E.-H., Liu, Q., et al. (2023). Applied analytical methods for detecting heavy metals in medicinal plants. Crit. Rev. Anal. Chem., 53 (2); 339-359. https://doi.org/10.1080/10408347.2021.1953371 DOI: https://doi.org/10.1080/10408347.2021.1953371
