Abstract
The impact of inorganic pollutants in the zone of industrial wastewater settling tanks (South of Russia) was studied. The levels of Mn, Cr, Ni, Cu, Zn, Pb, Cd were determined for Verbascum thapsus L., which are part of the mesophilic succession of wild plants in the studied technogenically polluted territory. The bioavailability of heavy metals (HM) for plants from transformed soils has been established. Anatomical and morphological features in the tissues of the plants affected by HM were analyzed using light-optical and electron microscopic methods. Contamination of the soil cover with Mn, Cr, Ni, Cu, Zn, Pb and Cd has been established with maximum content of Zn. It was revealed that the HM content in the V. thapsus plants exceeded the maximum permissible levels (Russian state standard): Zn by 23, Pb by 2, Cr by 31 and Cd by 3 times. The lower level of HM content in the inflorescences of mullein plants in comparison with the root system, stems and leaves indicates the resistance of generative organs to technogenic pollution. In the root and leaves of the V. thapsus, the anatomical and ultrastructural observation were carried out using light-optical and transmission electron microscopy. Changes in the ultrastructure of plants under the influence of anthropogenic impact have been revealed. The most significant changes of the ultrastructure of the polluted plants were found in the cell organelles of leaves (mitochondria, plastids, peroxisomes, etc.) including spatial transformation of the thylakoid system of plastids during the metal accumulation by plants, which may determine the mechanism of plant adaptation to technogenic pollution.
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References
Akpinar, A., Arslan, H., Güleryüz, G., Kırmızı, S., Erdemİr, Ü. S., & Güçer, Ş. (2015). Ni-induced changes in nitrate assimilation and antioxidant metabolism of verbascum olympicum boiss: could the plant be useful for phytoremediation or/and restoration purposes? International Journal of Phytoremediation, 17(6), 546–555. https://doi.org/10.1080/15226514.2014.922926
Ali, H., Khan, E., & Sajad, M. A. (2013). Phytoremediation of heavy metals—concepts and applications. Chemosphere, 91(7), 869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075
Alkorta, I., & Garbisu, C. (2001). Phytoremediation of organic contaminants in soils. Bioresource Technology, 79(3), 273–276. https://doi.org/10.1016/S0960-8524(01)00016-5
Ansari, S., & Daehler, C. C. (2000). Common mullein (Verbascum thapsus): A literature review. Honolulu (HI): Pacific Cooperative Studies Unit, University of Hawaii at Manoa, Department of Botany. PCSU Technical Report, 127.
Arslan, H., Güleryüz, G., Akpınar, A., Kırmızı, S., Erdemir, Ü. S., & Güçer, Ş. (2014). Responses of ruderal verbascum olympicum boiss (S crophulariaceae) growing under cadmium stress. Clean: Soil, Air, Water, 42(6), 824–835.
Bae, J., Byun, C., Watson, A. K., & Benoit, D. L. (2015). Ground cover species selection to manage common ragweed (Ambrosia artemisiifolia L.) in roadside edge of highway. Plant Ecology, 216, 263–271.
Bae, J., Benoit, D. L., & Watson, A. K. (2016). Effect of heavy metals on seed germination and seedling growth of common ragweed and roadside ground cover legumes. Environmental Pollution, 213, 112–118. https://doi.org/10.1016/j.envpol.2015.11.041
Barcelo, J., Vazquez, M. D., & Poschenrieder, C. H. (1988). Cadmium-induced structural and ultrastructural changes in the vascular system of bush bean stems. Botanica Acta, 101(3), 254–261. https://doi.org/10.1111/j.1438-8677.1988.tb00041.x
Basile, A., Sorbo, S., Cardi, M., Lentini, M., Castiglia, D., Cianciullo, P., Conte, B., Loppi, S., & Esposito, S. (2015). Effects of heavy metals on ultrastructure and Hsp70 induction in Lemna minor L. exposed to water along the Sarno River Italy. Ecotoxicology and Environmental Safety, 114, 93–101. https://doi.org/10.1016/j.ecoenv.2015.01.009
Bini, C., Wahsha, M., Fontana, S., & Maleci, L. (2012). Effects of heavy metals on morphological characteristics of Taraxacum officinale Web growing on mine soils in NE Italy. Journal of Geochemical Exploration, 123, 101–108. https://doi.org/10.1016/j.gexplo.2012.07.009
Chaplygin, V., Minkina, T., Mandzhieva, S., Burachevskaya, M., Sushkova, S., Poluektov, E., Antonenko, E., & Kumacheva, V. (2018). The effect of technogenic emissions on the heavy metals accumulation by herbaceous plants. Environmental Monitoring and Assessment, 190(3), 124. https://doi.org/10.1007/s10661-018-6489-6
Chaplygin, V., Mandzhieva, S., Minkina, T., Sushkova, S., Kizilkaya, R., Gülser, C., Zamulina, I., Kravtsova, N., Lobzenko, I., & Chernikova, N. (2019). Sustainability of agricultural and wild cereals to aerotechnogenic exposure. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-019-00411-6
Colzi, I., Rocchi, S., Rangoni, M., Del Bubba, M., & Gonnelli, C. (2014). Specificity of metal tolerance and use of excluder metallophytes for the phytostabilization of metal polluted soils: the case of Silene paradoxa L. Environmental Science and Pollution Research, 21(18), 10960–10969. https://doi.org/10.1007/s11356-014-3045-y
Danilovic, G., Morina, F., Satovic, Z., Prokic, L., & Pankovic, D. (2015). Genetic variability of Verbascum populations from metal polluted and unpolluted sites. Genetika, 47(1), 245–251. https://doi.org/10.2298/GENSR1501245D
de Freitas, T. A., França, M. G. C., de Almeida, A. A. F., de Oliveira, S. J. R., de Jesus, R. M., Souza, V. L., dos Santos Silva, J. V., & Mangabeira, P. A. (2015). Morphology, ultrastructure and mineral uptake is affected by copper toxicity in young plants of Inga subnuda subs luschnathiana (Benth) TD Penn. Environmental Science and Pollution Research, 22(20), 15479–15494.
Erdemir, U. S., Arslan, H., Guleryuz, G., Yaman, M., & Gucer, S. (2018). Manganese tolerance in Verbascum olympicum Boiss affecting elemental uptake and distribution: Changes in nicotinic acid levels under stress conditions. Environmental Science and Pollution Research, 25(29), 29129–29143.
Fedorenko, G. M., Fedorenko, A. G., Minkina, T. M., Mandzhieva, S. S., Rajput, V. D., Usatov, A. V., & Sushkova, S. N. (2018). Method for hydrophytic plant sample preparation for light and electron microscopy (studies on Phragmites australis Cav.). MethodsX, 5, 1213–1220.
Provisional Maximum Permissible Levels (MPL) for Some Chemical Elements and Gossypol in Forage for Farm Animals and Feed Additives (1987). USSR State Agriculture Committee. Moscow (in Russian).
GN 2.1.7.2041–06. (2006). Maximum permissible concentration (MPC) of chemicals in the soil. Moscow: Federal Center for Hygiene and Epidemiology of Rospotrebnadzor (in Russian).
GOST 17.4.3.01–83. (2004). Protection of Nature. Soils. General requirements for sampling. Moscow. IPK Standards Publishing House, 4 p. (in Russian).
GOST 17.4.4.02–84. (2008). Protection of Nature. Methods of sampling and preparation of samples for chemical, bacteriological, helminthological analysis. Moscow. Publishing house "Standartinform", 8 p. (in Russian).
GOST 26657–85. (1985). Feed, compound feed, compound feed raw materials. Methods for determination of phosphorus content (in Russian).
Gross, K. L. (1980). Colonization by Verbascum thapsus (mullein) of an old-field in Michigan: Experiments on the effects of vegetation. The Journal of Ecology. https://doi.org/10.2307/2259465
Gross, K. L., & Werner, P. A. (1978). The biology of canadian weeds: 28. Verbascum Thapsus L. and V. Blattaria L. Canadian Journal of Plant Science, 58(2), 401–413.
Guiamet, J. J., Pichersky, E., & Nooden, L. D. (1999). Mass exodus from senescing soybean chioroplasts. Plant and Cell Physiology, 40(9), 986–992. https://doi.org/10.1093/oxfordjournals.pcp.a029632
Güleryüz, G., Arslan, H., İzgi, B., & Güçer, Ş. (2006). Element content (Cu, Fe, Mn, Ni, Pb, And Zn) of the ruderal plant verbascum olympicum boiss from east mediterranean. Zeitschrift Für Naturforschung C, 61(5–6), 357–362.
Güleryüz, G., Erdemir, Ü. S., Arslan, H., Akpinar, A., Çiçek, A., & Güçer, Ş. (2015). Variation in trace element mobility and nitrogen metabolism of Verbascum olympicum Boiss under copper stress. Chemistry and Ecology, 31(6), 494–509.
Hinkle, P. C., & McCarty, R. E. (1978). How cells make ATP. Scientific American, 238(3), 104–123.
ISO 10390. (2005) Soil Quality – Determination of pH.
ISO 10693. (1995). Soil Quality – Determination of Carbonate Content-Volumetric Method.
ISO 14235. (1998). Soil Quality – Determination of Organic Carbon by Sulfochromic Oxidation.
ISO 13317–2. (2001). Determination of Particle Size Distribution by Gravitational Liquid Sedimentation Methods – Part 2: Fixed Pipette Method.
ISO 23470 (2011). Soil Quality – Determination of Effective Cation Exchange Capacity (CEC) and Exchangeable Cations.
IUSS Working Group WRB. (2015). World reference base for soil resources 2014, update 2015: International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106.
Jaca, T. P. (2017). Two Verbascum L species naturalised in South Africa. South African Journal of Botany, 100(109), 338–339.
Jin, X. F., Yang, X. E., Islam, E., Liu, D., Mahmood, Q., Li, H., & Li, J. (2008). Ultrastructural changes, zinc hyperaccumulation and its relation with antioxidants in two ecotypes of Sedum alfredii Hance. Plant Physiology and Biochemistry, 46(11), 997–1006. https://doi.org/10.1016/j.plaphy.2008.06.012
Jovanovic, L. J., Morina, F., Kukavica, B., & Veljovic-Jovanovic, S. (2007). High antioxidative capacity of Verbascum thapsus L. from a metal-contaminated area is induced upon treatment with Zn. Biogeochemistry of Trace Elements in the Environment: Environmental Protection, Remediation, and Human Health. Proceedings of the Ninth ICOBTE (pp 184–185). Beijing: Tsinghua University Press.
Kabata-Pendias, A., & Pendias, H. (2001). Trace elements in soils and plants CRC Press Inc. Florida: Boca Raton.
Kfayatullah, Q., Shah, M. T., & Arfan, M. (2001). Biogeochemical and environmental study of the chromite-rich ultramafic terrain of Malakand area Pakistan. Environmental Geology, 40(11–12), 1482–1486. https://doi.org/10.1007/s002540100374
Kozhevnikova, A. D., Seregin, I. V., Gosti, F., & Schat, H. (2017). Zinc accumulation and distribution over tissues in Noccaea caerulescens in nature and in hydroponics: a comparison. Plant and Soil, 411(1–2), 5–16. https://doi.org/10.1007/s11104-016-3116-6
Kozubov, G. M., & Danilova, M. F. (1972). Atlas of the ultrastructure of plant cells. Karelia : Petrozavodsk. (in Russian).
Kranner, I., & Colville, L. (2011). Metals and seeds: biochemical and molecular implications and their significance for seed germination. Environmental and Experimental Botany, 72, 93–105.
Kuznetsov, V. V., & Dmitrieva, G. A. (2005). Plant Physiology. Vysshaya shkola. (in Russian).
Ladonin, D. V. (2002). Heavy metal compounds in soils: problems and methods of study. Eurasian Soil Science, 35(6), 605–613. (in Russian).
Linnik, V. G., Bauer, T. V., Minkina, T. M., Mandzhieva, S. S., & Mazarji, M. (2020). Spatial distribution of heavy metals in soils of the flood plain of the Seversky Donets River (Russia) based on geostatistical methods. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-020-00688-y
Mashansky, V, F., Komissarchik, Y. Y., Vinnichenko, L. N., Mosevich, T. N., & Dunaeva, S. E. (1971). Various changes of ultrastructure of mitochondria related with specific functions of the cells. In Mitochondria: Structure and Functions in Norm and Pathology (pp 9-18). Moscow: Nauka (in Russian).
Matthews, D. J., Moran, B. M., & Otte, M. L. (2005). Screening the wetland plant species Alisma plantago-aquatica, Carex rostrata and Phalaris arundinacea for innate tolerance to zinc and comparison with Eriophorum angustifolium and Festuca rubra Merlin. Environmental Pollution, 134(2), 343–351.
Maximum permissible concentration (MPC) of chemicals in soils (Goskompriroda of the USSR, № 02–2333 of 10.12.90) (in Russian).
Methodological guidelines on determination of heavy metals in agricultural soils and crop produce (1992). Moscow: TsINAO (in Russian).
Minkina, T. M., Nevidomskaya, D. G., Pol’shina, T. N., Fedorov, Y. A., Mandzhieva, S. S., Chaplygin, V. A., Bauer, T. V., & Burachevskaya, M. V. (2017). Heavy metals in the soil–plant system of the Don River estuarine region and the Taganrog Bay coast. Journal of Soils and Sediments, 17(5), 1474–1491. https://doi.org/10.1007/s11368-016-1381-x
Minkina, T., Fedorenko, G., Nevidomskaya, D., Fedorenko, A., Chaplygin, V., & Mandzhieva, S. (2018). Morphological and anatomical changes of Phragmites australis Cav. due to the uptake and accumulation of heavy metals from polluted soils. Science of the Total Environment, 636, 392–401. https://doi.org/10.1016/j.scitotenv.2018.04.306
Minkina, T. M., Mandzhieva, S. S., Burachevskaya, M. V., Bauer, T. V., & Sushkova, S. N. (2018). Method of determining loosely bound compounds of heavy metals in the soil. MethodsX, 5, 217–226. https://doi.org/10.1016/j.mex.2018.02.007
Minkina, T. M., Fedorenko, G. M., Nevidomskaya, D. G., Pol’shina, T. N., Fedorenko, A. G., Chaplygin, V. A., Mandzhieva, S. S., Sushkova, S. N., & Hassan, T. M. (2019). Bioindication of soil pollution in the delta of the Don River and the coast of the Taganrog Bay with heavy metals based on anatomical, morphological and biogeochemical studies of macrophyte Typha australis Schum & Thonn. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-019-00379-3
Minkina, T., Rajput, V., Fedorenko, G., Fedorenko, A., Mandzhieva, S., Sushkova, S., Morin, T., & Yao, J. (2020). Anatomical and ultrastructural responses of Hordeum sativum to the soil spiked by copper. Environmental Geochemistry and Health, 42(1), 45–58.
Molas, J. (2002). Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni (II) complexes. Environmental and Experimental Botany, 47(2), 115–126. https://doi.org/10.1016/S0098-8472(01)00116-2
Morina, F., Jovanović, L., Prokić, L., & Veljović-Jovanović, S. (2016). Physiological basis of differential zinc and copper tolerance of Verbascum populations from metal-contaminated and uncontaminated areas. Environmental Science and Pollution Research, 23(10), 10005–10020. https://doi.org/10.1007/s11356-016-6177-4
Motuzova, G. V., Minkina, T. M., Karpova, E. A., Barsova, N. U., & Mandzhieva, S. S. (2014). Soil contamination with heavy metals as a potential and real risk to the environment. Journal of Geochemical Exploration, 144, 241–246. https://doi.org/10.1016/j.gexplo.2014.01.026
Muszynska, E., Labudda, M., Różańska, E., Hanus-Fajerska, E., & Znojek, E. (2018). Heavy metal tolerance in contrasting ecotypes of Alyssum montanum. Ecotoxicology and Environmental Safety, 161, 305–317. https://doi.org/10.1016/j.ecoenv.2018.05.075
Nascimento, C. W. A. D., & Xing, B. (2006). Phytoextraction: A review on enhanced metal availability and plant accumulation. Scientia Agricola, 63(3), 299–311. https://doi.org/10.1590/S0103-90162006000300014
Ntantiso, Z., & Jaca, T. P. (2015). Assessment of potential invasiveness of Verbascum thapsus L. in South Africa. South African Journal of Botany, 98, 214–215. https://doi.org/10.1016/j.sajb.2015.03.171
Ouzounidou, G., Eleftheriou, E. P., & Karataglis, S. (1992). Ecophysical and ultrastructural effects of copper in Thlaspi ochroleucum (Cruciferae). Canadian Journal of Botany, 70(5), 947–957. https://doi.org/10.1139/b92-119
Panou-Filotheou, H., Bosabalidis, A. M., & Karataglis, S. (2001). Effects of copper toxicity on leaves of oregano (Origanum vulgare subsp. hirtum). Annals of Botany, 88(2), 207–214.
Parker, I. M., Rodriguez, J., & Loik, M. E. (2003). An evolutionary approach to understanding the biology of invasions: Local adaptation and general-purpose genotypes in the weed Verbascum thapsus. Conservation Biology, 17(1), 59–72. https://doi.org/10.1046/j.1523-1739.2003.02019.x
Privalenko, V. V., Mazurenko, V. T., Panaskov, V. I., Moshkin, V. M., Mukhin, N. V., & Senin, B. K. (2000). Environmental problems of the city of Kamensk-Shakhtinsky. Color Printing Publishing House. (in Russian).
Raskin, I., & Ensley, B. D. (2000). Phytoremediation of toxic metals. Wiley.
Ratushnyak, A. Y., Chakhirev, I. V., Andreeva, M. G., & Trushin, M. V. (2014). Features of the formation of morphological structures and production of Typha angustifolia under load on lead. Biosciences Biotechnology Research Asia, 11, 365–369.
Reinartz, J. A. (1984). Life history variation of common mullein (Verbascum thapsus): I. Latitudinal differences in population dynamics and timing of reproduction. The Journal of Ecology. https://doi.org/10.2307/2259539
Salt, D. E., Blaylock, M., Kumar, N. P., 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
Selseleh, M., Ebrahimi, S. N., Aliahmadi, A., Sonboli, A., & Mirjalili, M. H. (2020). Metabolic profiling, antioxidant, and antibacterial activity of some Iranian Verbascum L. species. Industrial Crops and Products, 153, 112609.
Seregin, I. V., & Kozhevnikova, A. D. (2008). Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium. Russian Journal of Plant Physiology, 55(1), 1–22. https://doi.org/10.1134/S1021443708010019
Seregin, I. V., Kozhevnikova, A. D., Zhukovskaya, N. V., & Schat, H. (2015). Cadmium tolerance and accumulation in excluder Thlaspi arvense and various accessions of hyperaccumulator Noccaea caerulescens. Russian Journal of Plant Physiology, 62(6), 837–846.
Shah, M. T., Kifayattullah, Q., & Arfan, M. (2004). Pedo and biogeochemical study of Zinc-Lead deposits of the Besham area, northern Pakistan: its implication in mineral exploration and environmental degradation. Environmental Geology, 45(4), 544–549.
Siedlecka, A., & Krupa, Z. (1999). Cd/Fe interaction in higher plants-its consequences for the photosynthetic apparatus. Photosynthetica, 36(3), 321–331. https://doi.org/10.1023/A:1007097518297
Skorzynska-Polit, E., & Baszynski, T. (1997). Differences in sensitivity of the photosynthetic apparatus in Cd-stressed runner bean plants in relation to their age. Plant Science, 128(1), 11–21.
Sokolov, S. Y. (2000). Phytotherapy and Phytopharmacology. Medical News Agency. (in Russian).
Speranza, L., Franceschelli, S., Pesce, M., Reale, M., Menghini, L., Vinciguerra, I., De Lutiis, M. A., Felaco, M., & Grilli, A. (2010). Antiinflammatory effects in THP-1 cells treated with verbascoside. Phytotherapy Research, 24(9), 1398–1404. https://doi.org/10.1002/ptr.3173
Sresty, T. V. S., & Rao, K. M. (1999). Ultrastructural alterations in response to zinc and nickel stress in the root cells of pigeonpea. Environmental and Experimental Botany, 41(1), 3–13. https://doi.org/10.1016/S0098-8472(98)00034-3
Sridhar, B. M., Diehl, S. V., Han, F. X., Monts, D. L., & Su, Y. (2005). Anatomical changes due to uptake and accumulation of Zn and Cd in Indian mustard (Brassica juncea). Environmental and Experimental Botany, 54(2), 131–141. https://doi.org/10.1016/j.envexpbot.2004.06.011
Titov, A. F., Akimova, T. V., & Venzhik, Y. V. (2007). Effect of root heating on the tolerance of barley leaf cells and ultrastructure of chloroplasts and mitochondria. Doklady Biological Sciences, 415(1), 324–327. https://doi.org/10.1134/S0012496607040229
Tognacchini, A., Salinitro, M., Puschenreiter, M., & van der Ent, A. (2020). Root foraging and avoidance in hyperaccumulator and excluder plants: A rhizotron experiment. Plant and Soil, 450(1), 287–302. https://doi.org/10.1007/s11104-020-04488-2
Turgeon, R., Beebe, D. U., & Gowan, E. (1993). The intermediary cell: Minor-vein anatomy and raffinose oligosaccharide synthesis in the Scrophulariaceae. Planta, 191(4), 446–456. https://doi.org/10.1007/BF00195746
Turker, A. U., & Camper, N. D. (2002). Biological activity of common mullein, a medicinal plant. Journal of Ethnopharmacology, 82(2–3), 117–125. https://doi.org/10.1016/S0378-8741(02)00186-1
Turker, A. U., & Gurel, E. (2005). Common mullein (Verbascum thapsus L.): Recent advances in research. Phytotherapy Research, 19(9), 733–739.
Tyler, V. E. (1994). Herbs of Choice: The Therapeutic Use of Phytomedicinals. Pharmaceutical Products Press.
Upadhyay, R. K., & Panda, S. K. (2009). Copper-induced growth inhibition, oxidative stress and ultrastructural alterations in freshly grown water lettuce (Pistia stratiotes L). Comptes Rendus Biologies, 332(7), 623–632.
Vinogradov, A. P. (1957). Geochemistry of rare and trace elements in soils. Publishing house of the USSR Academy of Sciences. (in Russian).
Yildirim, D., & Sasmaz, A. (2017). Phytoremediation of As, Ag, and Pb in contaminated soils using terrestrial plants grown on Gumuskoy mining area (Kutahya Turkey). Journal of Geochemical Exploration, 182, 228–234. https://doi.org/10.1016/j.gexplo.2016.11.005
Zamulina, I. V., Gorovtsov, A. V., Minkina, T. M., Mandzhieva, S. S., Bauer, T. V., & Burachevskaya, M. V. (2021). The influence of long-term Zn and Cu contamination in Spolic technosols on water-soluble organic matter and soil biological activity. Ecotoxicology and Environmental Safety. https://doi.org/10.1016/j.ecoenv.2020.111471
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This research was supported by the RFBR and SC RA, project no. 20-55-05014 arm_a, and Russian Academy of Sciences, project no. AAAA-A19-119011190176-7.
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This research was supported by the RFBR and SC RA, project no. 20–55-05014 arm_a, and Russian Academy of Sciences, project no. AAAA-A19-119011190176–7.
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Victor Chaplygin, Natalia Chernikova: Formal analysis, Investigation, Visualization, Writing—original draft preparation—review & editing; Aleksei Fedorenko: Data curation, Investigation, Visualization, Writing—original draft preparation—review & editing; Grigorii Fedorenko, Tatiana Minkina: Conceptualization, Supervision, Writing—original draft preparation—review & editing; Dina Nevidomskaya, Saglara Mandzhieva: Methodology, Writing—review & editing; Karen Ghazaryan, Hasmik Movsesyan: Conceptualization, Writing—review & editing; Vladimir Beschetnikova: Data curation.
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Chaplygin, V., Chernikova, N., Fedorenko, G. et al. Influence of soil pollution on the morphology of roots and leaves of Verbascum thapsus L. Environ Geochem Health 44, 83–98 (2022). https://doi.org/10.1007/s10653-021-00975-2
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DOI: https://doi.org/10.1007/s10653-021-00975-2