Comparative study on the growth response and remediation potential of panicum maximum and axonopus compressus in lead contaminated soil
S. N. B. Ukoh, M. O. Akinola, K. L. Njoku
DOI: 10.5281/zenodo.2247129
Received: 17 October 2018
Accepted: 10 December 2018
Published online: 12 December 2018
ABSTRACT
The global problem concerning contamination of the environment as a consequence of heavy metals is on the increase. Soil contamination by heavy metals is a worldwide problem, therefore effective remediation approaches are necessary. Some plants can absorb these toxic metals and help to clean them up from the soil and sediment. This fact may be useful for developing rational forms of environmental safety management and innovative technology which more efficiently clean soils and improve their ecological condition with for agriculture. Phytoremediation is known as an eco-friendly and cost-effective way of reducing pollutants from the soil. Therefore, the present experiment was undertaken to investigate the comparative potential of two grasses, Panicum maximum and Axonopus compressus to bioremediate lead polluted soils. In addition, the impact of Pb on the antioxidant defense system of the plants was studied. Pb(NO3)2 salts were mixed with soil at various concentrations 5 mg/kg, 10 mg/kg, 20 mg/kg, 40 mg/kg and 80 mg/kg in triplicates and control experiment was also setup. After 4 months, the plants were removed and their parts (root, shoot and leaf) separated. They were analysed for morphological, biochemical parameters and Pb concentration. Soil samples were also analyzed for Pb. The root length of both P. maximum and A. compressus generally decreased as the concentration of Pb in the soil increased. The least shoot length inhibition of A. compressus was 7.13 % (5 mg/kg) while the highest shoot length inhibition was 36.29 % (40 mg/kg). The least shoot length inhibition of P. maximum was 10.51 % exposed to 5 mg/kg and the highest shoot length inhibition was 42.46 % (40 mg/kg). There was more significant reduction of the heavy metals in vegetated soils for both P. maximum and A. compressus at the end of the study compared to the to the heavy metals in the soils at the beginning of the study (p < 0.05). A. compressus is a better removal of Pb than P. maximum, however, it was not significant. Glutathione (GSH) levels varied significantly (p ≤ 0.05) with respect to concentration of heavy metals as well as different part of the plants. A. compressus has more effects on the Glutathione activities than P. maximum. Pb caused a decrease in the metallothionein level (10.11 %) in P. maximum while A. compressus metallothionein level increased by 116.10 % in 5 % treatment.
Keywords: contaminated soil; heavy metals; phytoremediation; environmental safety control.
REFERENCES
1. Adesuyi, A. A, Njoku, K. L, Akinola, M. O. (2015). Assessment of heavy metals pollution in soils and vegetation around selected industries in Lagos State, Nigeria. Journal of Geoscience and Environmental Protection, 3, 11–19. doi: 10.4236/gep.2015.37002.
2. Barsukova, G. (2018). Development of mathematical model of infiltration of iron sulfate acid solution. Technogenic and ecological safety, 4(2/2018), 99–104. doi: 10.5281/zenodo.1463022.
3. Vambol, S. O., Kondratenko, O. M. (2017). Calculated substantiation of choice of units of monetary equivalents of complex fuel and ecological criteria components. Technogenic and ecological safety, 2, 53–60. doi: 10.5281/zenodo.1182890.
4. Khalid, S., Shahid, M., Niazi, N. K. et al. (2017). A comparison of technologies for remediation of heavy metal contaminated soils. Journal of Geochemical Exploration, 182 (part B), 247–268.
5. Ziarati, P., Namvar, S., Sawicka, B. (2018). Heavy metals bio-adsorrption by Hibiscus Sabdariffa L. from contaminated weater. Technogenic and ecological safety, 4(2/2018), 22–32. doi: 10.5281/zenodo.1244568.
6. Najeeb, U., Jilani, G., Ali, S. et al. (2011). Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. Journal of Hazardous Materials, 186, 565–574.
7. Agency for Toxic Substance and Disease Registry (2012). Heavy Metals Toxicity and the Environment, Molecular, Clinical and Environmental Toxicology, 101, 133–164. doi: 10.1007/978-3-7643-8340-4_6.
8. US EPA (2004). The US EPA reference dose for methylmercury Environ Res. 2004 Jul, 95(3), 406–413.
9. Shmandiy, V. M., Aleksyeyeva, T. M., Kharlamova, O. V. (2017). Kharaterystyka stanu ekolohichnoyi nebezpeky za pokazykamy dehradatsiyi hruntovo-roslynnoho pokryvu v urbosystemi. Technogenic and ecological safety, 2, 11–17.
10. Koloskov, V. (2018). Vyznachennya znachushchykh pokaznykiv kryteriyu ekolohichnoho rezervu terytoriy, prylehlykh do mistsʹ zberihannya vidkhodiv. Technogenic and ecological safety, 3(1/2018), 44–51. doi: 10.5281/zenodo.1182841.
11. Doncheva, S., Moustakas, M., Ananieva, K. et al. (2013). Plant response to lead in the presence or absence EDTA in two sunflower genotypes (cultivated H. annuus cv. 1114 and Interspecific line H. annuus x H. argophyllus). Environmental Sciences and Pollution Research, 20(2), 823–833. doi: 10.1007/s11356-012-1274-5.
12. Pant, P. P., Tripathi, A. K. (2014). Impact of heavy metals on morphological and biochemical parameters of Shorea robusta plant. Ekológia, 33(2), 116–126. doi: 10.2478/eko-2014-0012.
13. Majer, J. M., Jason, L. A., Ferrari, J. R. et al. (2002). Social support and self-efficacy for abstinence: is peer identification an issue? Journal of Substance Abuse Treatmen, 23, 209–215.
14. Aluko, T. S., Njoku, K. L., Adesuyi, A. A., Akinola, M. O. (2018). Health risk assessment of heavy metals in soil from Iron ore mining sites of Itakpe and Agbaja, Kogi State, Nigeria. Journal of Pollution, 4(3), 527–538. doi: 10.22059/poll.2018.243543.330.
15. Ziarati, P., Asgarpanah, J., Makki, F. M. M. (2015). Phytoremediation of heavy metal contaminated water using potential caspian sea wetland plant: nymphaeaceae. Biosciences Biotechnology Research Asia, 12(3), 2467–2473. doi: 10.13005/bbra/1925.
16. Henry, J. R. (2000). An overview of the phytoremediation of lead and mercury. U.S. Environmental Protection Agency Office of Solid Waste and Emergency Response Technology Innovation office Washington, D.C. Available: http://clu-in.org.
17. Njoku, K., Oboh, B., Akinola, M. (2016). Phytoremediation of crude oil contaminated soil using Glycine max (Merril); Through Phytoaccumulation or Rhizosphere Effect? Journal of Biological and Environmental Sciences, 10(30), 115–124.
18. Abioye, P. O. (2011). Biological remediation of hydrocarbon and heavy metals contaminated soil, soil contamination. ISBN: 978-953-307-647-8, InTech, Available: http://www.intechopen.com/books/soil-contamination/biologicalremediation-of-hydrocarbon-andheavymetals-contaminated-soil.
19. Dada, E. O., Njoku, K. L., Osuntoki, A. A., Akinola, M. O. (2015). A review of current techniques of in situ physico-chemical and biological remediation of heavy metals polluted soil. Ethiopian Journal of Environmental Studies and Management, 8(5), 606–615. doi: 10.4314/ejesm.v8i5.13.
20. Njoku, K. L., Akinola, M. O., Oboh, B. O. (2012). Phytoremediation of crude oil polluted soil: Effect of cow dung augmentation on the remediation of crude oil polluted soil by Glycine max. Journal of Applied Science Research, 8(1), 277–282. ISSN 1819-544X.
21. Dada, E. O., Njoku, K. L., Osuntoki, A. A., Akinola, M. O. (2016). Heavy metal remediation potential of a tropical wetland earthworm, Libyodrilus violaceus (Beddard). Iranica Journal of Energy and Environment, 7(3), 247–254. doi: 10.5829/idosi.ijee.2016.07.03.06.
22. Iheme, P. O., Akinola, M. O., Njoku, K. L. (2017). Evaluation on the growth response of Peanut (Arachis hypogaea) and Sorghum (Sorghum bicolor) to crude oil contaminated soil. Journal of Applied Science and Environmental Management, 21(6), 1169–1173. doi: 10.4314/jasem.v21i6.30.
23. Ali, M. S., Khandoker, Y. M., Afroz, M. A., Bhuiyan, A. K. (2012). Ovarian response to different dose levels of follicle stimulating hormone (FSH) in different genotypes of bangladeshi cattle. Asian-Australasian Journal of Animal Sciences, 25(1), 52–58.
24. ISO 10390. (2005). Soil quality. Determnation of pH. International Organization for Standardization, Geneva, Switzerland.
25. Bernard, B. B., Bernard, H., Brooks, J. M. (2004). Determination of total carbon, total organic carbon & inorganic carbon in sediments. TDIBrooks International/B&B Lab Inc. Texas. Available: https://www.tdi-bi.com/analytical_services/environmental/NOAA_methods/TOC.pdf.
26. De Filippo, B. V., Ribeiro, A. C. (1997). Análise química do solo (Metodologia) 2 ed. Universidade Federal de Viçosa, Viçosa, MG, Brasil. 1997, 26 p.
27. Aldesuquy, H., Baka, Z., Mickky, B. (2014). Kinetin and spermine mediated induction of salt tolerance in wheat plants: Leaf area, photosynthesis and chloroplast ultrastructure of flag leaf at ear emergence. Egyptian Journal of Basic and Applied Sciences, 1, 77–87.
28. Akoto, O, Bruce, T. N., Darko, G. (2008). Heavy metals pollution profiles in streams serving the Owabi reservoir. African Journal of Environmental Science and Technology, 2(11), 354–359.
29. Cui, S., Zhou, Q., Chao, L. (2007). Potential hyperaccumulation of Pb, Zn, Cu and Cd in endurant plants distributed in an old smeltery, northeast China. Environmental Geology, 51, 1043–1048.
30. Bulaj, G., Kortemme, T., Goldenberg, D. P. (1998). Ionization-reactivity relationships for cysteine thiols in polypeptides. Biochemistry, 37, 8965–8972.
31. Scheuhammer, A. M., Cherian, M. G. (1991). Quantification of metallothionein by silver saturation. Methods in Enzymology, 205, 78–83.
32. Gornall, A. G., Bardawill, C. J., David, M. M. (1949). Determination of serum proteins by means of the biuret reaction. Journal of Biological Chemistry, 177, 751–766.
33. Habig, W. H., Pabst, M. J., Jakoby, W. B. (1974). Glutathione S-Transferases: The first enzymatic step in mercapturic acid formation. The Journal of Biological Chemistry, 249(22), 7130–7139.
34. Singh, G., Agnihotri, R. K., Singh, D. K., Sharma, R. (2013). Effect of Pb and Ni on root development and biomass production of black gram (Vigna Mungo L.): overcoming through exogenous nitrogen application. International Journal of Agriculture and Crop Sciences, 5(22), 2689–2696.
35. Pant, P. P., Tripathi, A. K. Gairola, S. (2011). Phytpremediation of arsenic using cassia fistula linn seedling. International Journal of Research in Chemistry and Environment, 1(1), 24–28. ISSN 2248-9649.
36. Arias, J. A., Peralta-Videa, J. R., Ellzey, J. T. et al. (2010). Effects of glomus deserticola inoculation on prosopis: enhancing chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and TEM techniques. Environmental and Experimental Botany, 68(2), 139–148.
37. Seyyedi, M., Timko, M. P., Sundqvist, C. (1999). Protochlorophylliden POR and chlorophyll formation in the Lip1 mutant of pea. Physiologia. Plantarum, 106, 344–354. doi: 10.1007/978-94-011-4788-0_33.
38. Ground-Water Remediation Technologies Analysis Center (GWRTAC). (1997). Remediation of Metal-Contaminated Soils and Groundwater. GWRTAC E Series. TE-97-01.
39. Kushwaha, A., Rani, R., Kumar, S., Gautam, A. (2015). Heavy metal detoxification and tolerance mechanisms in plants: Implications for phytoremediation. Environmental Reviews, 23, 1–13. doi: 10.1139/er-2015-0010.
40. Javed, M. T. (2011). Mechanisms behind pH changes by plant roots and shoots caused by elevated concentration of toxic elements. Doctoral Thesis in Plant Physiology at Stockholm University, Sweden, 2011. 40 pp.
41. Efe, S. I., Elenwo, E. I. (2014). Phytoremediation of crude oil contaminated soil with Axonopus compressus in the Niger Delta Region of Nigeria. Natural Resources, 5, 59–67. doi: 10.4236/nr.2014.52006.
42. Hasegawa, H., Ismail, M. D., Rahman, I., Rahman, M. A. (2016). The effects of soil properties to the extent of soil contamination with metals. Environmental Remediation Technologies for Metal-Contaminated Soils. Springer, Tokyo,1–19. doi: 10.1007/978-4-431-55759-3.
43. Fontes, F., Matos, M. P., Teixeira, A. et al. (2000). Competitive adsorption of zinc, cadmium, copper, and lead in three highly – weathered Brazilian soils. Communication in Soil Science and Plant Analysis, 31, 2939–2958. doi: 10.1080/00103620009370640.
44. Chijoke-Osuji, C. C., Ebenezer, B. (2017). Axonopus compressus: a resilient phytoremediatior of waste engine oil contaminated soil. International Journal of Plant and Soil Science, 14(2), 1–10.
45. U.S. Environmental Protection Agency (USEPA). (2004). Risk assessment guidance for superfund (Rags). Human Health Evaluation Manual (Part E, Supplemental Guidance for Dermal Risk Assessment) Interim. Available: http://www.epa.gov/oswer/ riskassessment/ragse/.
46. Mani, D., Kumar, C., Patel, N. K., Sivakumar, D. (2015). Enhanced clean-up of lead-contaminated alluvial soil through Chrysanthemum indicum L. International Journal of Environmental Science and Technology, 12(4), 1211–1222. doi: 10.1007/s13762-013-0488-5.
47. Liu, X., Peng, K., Wang, A. et al. (2010). Cadmium accumulation and distribution in populations of Phytolacca americana L. and the role of transpiration. Chemosphere, 78(9), 1136–1141. doi: 10.1016/j.chemosphere.2009.12.030.
48. Pourrut, B., Shahid, M., Dumat, C. et al. (2011). Lead uptake, toxicity, and detoxification in plants. Reviews of Environmental Contamination and Toxicology, 213, 113–136. doi: 10.1007/978-1-4419-9860-6_4.
49. Scott, N., Hatlelid, K. M., MacKenzie, N. E., Carter, D. E. (1993). Reactions of arsenic(III) and arsenic(V) species with glutathione. Chemical Research and Toxicology, 6, 102–106. doi: 10.1021/tx00031a016.
50. Sarma, H. (2011). Metal hyperaccumulation in plants: a review focusing on phytoremediation technology. Journal of Environmental Science and Technology, 4, 118–138.
51. Rosen, B. P. (2002). Biochemistry of arsenic detoxification. FEBS Letter, 529, 86–92.
52. Koricheva, J., Roy, S., Vranjic, J. A. et al. (1997). Antioxidants responses to stimulated acid rain and heavy metal deposition in birch seedlings. Environmental Pollution, 95, 249–258.
53. Gupta, D. K., Huang, H. G., Corpas, F. J. (2013). Lead tolerance in plants: strategies for phytoremediation. Environmental Sciences and Pollution Research, 20, 2150–2161.
54. Ruley, A. T., Sharma, N. C., Sahi, S. V. (2004). Antioxidant defense in a lead accumulating plant, Sesbania drummondii. Plant Physiology and Biochemistry, 42(11), 899–906.
55. Ojuederie, O. B., Babalola, O. O. (2017). Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. International Journal of Environmental Research and Public Health, 14(12), 1504. doi: 10.3390%2Fijerph14121504.
56. Grennan, A. K. (2011). Metallothioneins, a diverse protein family. Plant Physiology, 155, 1750–1751.
57. Guo, J., Xu, L., Su, Y. et al. (2013). ScMT2-1-3, a metallothionein gene of sugarcane, plays an important role in the regulation of heavy metal tolerance/accumulation. BioMed Research International, 904769. doi: 10.1155/2013/904769.
58. Emamverdian, A., Ding, Y., Mokhberdoran, F., Xie, Y. (2015). Heavy metal stress and some mechanisms of plant defense response. Science World Journal, 2015, article ID 756120. doi: 10.1155/2015/756120.
59. Street, N. R., Skogstro, M. O., Sjo din, A. et al. (2006). The genetics and genomics of the drought response in Populus. Plant Journal, 48, 321–341.
60. Bogeat-Triboulot, M. B., Brosche, M., Renaut, J. et al. (2007). Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiology, 143, 876–892.
61. Du, J., Yaang, J. L., Li, C. H. (2002). Advances in metallothionein studies in forest trees. Plant Omics Journal, 5(1), 46–51.
62. Gupta, D., Huang, H., Yang, X. et al. (2010). The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. Journal of Hazardous Materials, 177(1–3), 437–444.
63. Hayes, J. D., Flanagan, J. U., Jowsey, I. R. (2005). Glutathione transferases. Annual Review of Pharmacology and Toxicology, 45, 51–88.
64. He, G., Guan, C., Chen, Q. X. et al. (2016). Genome-wide analysis of the glutathione S-transferase gene family in Capsella rubella: identification, expression, and biochemical functions. Frontier in Plant Science, 1325. doi: 10.3389%2Ffpls.2016.01325.
65. Kaviani, E., Niazi, A., Heydarian, Z. et al. (2017). Phytoremediation of Pb-contaminated soil by Salicornia iranica: key physiological and molecular mechanisms involved in Pb detoxification. Clean–Soil Air Water, 45(5). doi: 10.1002/clen.201500964.
ЛІТЕРАТУРА
1. Adesuyi A. A, Njoku K. L, Akinola M. O. Assessment of heavy metals pollution in soils and vegetation around selected industries in Lagos State, Nigeria // Journal of Geoscience and Environmental Protection. 2015. Vol. 3. P. 11–19. doi: 10.4236/gep.2015.37002.
2. Barsukova G. Development of mathematical model of infiltration of iron sulfate acid solution // Technogenic and ecological safety. 2018. Vol. 4(2/2018). P. 99–104. doi: 10.5281/zenodo.1463022.
3. Vambol S. O., Kondratenko O. M. Calculated substantiation of choice of units of monetary equivalents of complex fuel and ecological criteria components // Technogenic and ecological safety. 2017. Vol. 2. P. 53–60. doi: 10.5281/zenodo.1182890.
4. A comparison of technologies for remediation of heavy metal contaminated soils / Khalid S., Shahid M., Niazi N. K. et al. // Journal of Geochemical Exploration. 2017. Vol. 182 (part B). P. 247–268.
5. Ziarati P., Namvar S., Sawicka B. Heavy metals bio-adsorrption by Hibiscus Sabdariffa L. from contaminated weater // Technogenic and ecological safety. 2018. Vol. 4(2/2018). P. 22–32. doi: 10.5281/zenodo.1244568.
6. Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid / Najeeb U., Jilani G., Ali S. et al. // Journal of Hazardous Materials. 2011. Vol. 186. P. 565–574.
7. Agency for Toxic Substance and Disease Registry. Heavy Metals Toxicity and the Environment, Molecular, Clinical and Environmental Toxicology. 2012. Vol. 101. P. 133–164. doi: 10.1007/978-3-7643-8340-4_6.
8. US EPA. The US EPA reference dose for methylmercury Environ Res. 2004 Jul, Vol. 95, Issue 3. P. 406–413.
9. Shmandiy V. M., Aleksyeyeva T. M., Kharlamova O. V. Kharaterystyka stanu ekolohichnoyi nebezpeky za pokazykamy dehradatsiyi hruntovo-roslynnoho pokryvu v urbosystemi // Technogenic and ecological safety. 2017. Vol. 2. P. 11–17.
10. Koloskov V. Vyznachennya znachushchykh pokaznykiv kryteriyu ekolohichnoho rezervu terytoriy, prylehlykh do mistsʹ zberihannya vidkhodiv // Technogenic and ecological safety. 2018. Vol. 3(1/2018). P. 44–51. doi: 10.5281/zenodo.1182841.
11. Plant response to lead in the presence or absence EDTA in two sunflower genotypes (cultivated H. annuus cv. 1114 and Interspecific line H. annuus x H. argophyllus) / Doncheva S., Moustakas M., Ananieva K. et al. // Environmental Sciences and Pollution Research. 2013. Vol. 20, Issue 2. P. 823–833. doi: 10.1007/s11356-012-1274-5.
12. Pant P. P., Tripathi A. K. Impact of heavy metals on morphological and biochemical parameters of Shorea robusta plant // Ekológia. 2014. Vol. 33, Issue 2. P. 116–126. doi: 10.2478/eko-2014-0012.
13. Social support and self-efficacy for abstinence: is peer identification an issue? / Majer J. M., Jason L. A., Ferrari J. R. et al. // Journal of Substance Abuse Treatmen. 2002. Vol. 23. P. 209–215.
14. Health risk assessment of heavy metals in soil from Iron ore mining sites of Itakpe and Agbaja, Kogi State, Nigeria / Aluko T. S., Njoku K. L., Adesuyi A. A., Akinola, M. O. // Journal of Pollution. 2018. Vol. 4, Issue 3. P. 527–538. doi: 10.22059/poll.2018.243543.330.
15. Ziarati P., Asgarpanah J., Makki F. M. M. Phytoremediation of heavy metal contaminated water using potential caspian sea wetland plant: nymphaeaceae // Biosciences Biotechnology Research Asia. 2015. Vol. 12, Issue 3. P. 2467–2473. doi: 10.13005/bbra/1925.
16. Henry J. R. An overview of the phytoremediation of lead and mercury // U.S. Environmental Protection Agency Office of Solid Waste and Emergency Response Technology Innovation office Washington, D.C. 2000. Available: http://clu-in.org.
17. Njoku K., Oboh B., Akinola M. Phytoremediation of crude oil contaminated soil using Glycine max (Merril); Through Phytoaccumulation or Rhizosphere Effect? // Journal of Biological and Environmental Sciences. 2016. Vol. 10, Issue 30. P. 115–124.
18. Abioye P. O. Biological remediation of hydrocarbon and heavy metals contaminated soil, soil contamination. 2011. ISBN: 978-953-307-647-8, InTech, Available: http://www.intechopen.com/books/soil-contamination/biologicalremediation-of-hydrocarbon-andheavymetals-contaminated-soil.
19. A review of current techniques of in situ physico-chemical and biological remediation of heavy metals polluted soil / Dada E. O., Njoku K. L., Osuntoki A. A., Akinola M. O // Ethiopian Journal of Environmental Studies and Management. 2015. Vol. 8, Issue 5. P. 606–615. doi: 10.4314/ejesm.
v8i5.13.
20. Njoku K. L., Akinola M. O., Oboh B. O. Phytoremediation of crude oil polluted soil: Effect of cow dung augmentation on the remediation of crude oil polluted soil by Glycine max // Journal of Applied Science Research. 2012. Vol. 8, Issue 1. P. 277–282. ISSN 1819-544X.
21. Heavy metal remediation potential of a tropical wetland earthworm, Libyodrilus violaceus (Beddard) / Dada E. O., Njoku K. L., Osuntoki A. A., Akinola M. O. // Iranica Journal of Energy and Environment. 2016. Vol. 7, Issue 3. P. 247–254. doi: 10.5829/idosi.ijee.2016.07.03.06.
22. Iheme P. O., Akinola M. O., Njoku K. L. Evaluation on the growth response of Peanut (Arachis hypogaea) and Sorghum (Sorghum bicolor) to crude oil contaminated soil // Journal of Applied Science and Environmental Management. 2017. Vol. 21, Issue 6. P. 1169–1173. doi: 10.4314/jasem.
v21i6.30.
23. Ovarian response to different dose levels of follicle stimulating hormone (FSH) in different genotypes of bangladeshi cattle / Ali M. S., Khandoker Y. M., Afroz M. A., Bhuiyan A. K. // Asian-Australasian Journal of Animal Sciences. 2012. Vol. 25, Issue 1. P. 52–58.
24. ISO 10390. Soil quality. Determnation of pH. International Organization for Standardization, Geneva, Switzerland. 2005.
25. Bernard B. B., Bernard H., Brooks J. M. Determination of total carbon, total organic carbon & inorganic carbon in sediments. TDIBrooks International/B&B Lab Inc. Texas. 2004. Available: https://www.tdi-bi.com/analytical_services/environmental/NOAA_methods/TOC.pdf.
26. De Filippo B. V., Ribeiro A. C. Análise química do solo (Metodologia) 2 ed. Universidade Federal de Viçosa, Viçosa, MG, Brasil. 1997, 26 p.
27. Aldesuquy H., Baka Z., Mickky B. Kinetin and spermine mediated induction of salt tolerance in wheat plants: Leaf area, photosynthesis and chloroplast ultrastructure of flag leaf at ear emergence // Egyptian Journal of Basic and Applied Sciences. 2014. Vol. 1. P. 77–87.
28. Akoto O, Bruce T. N., Darko G. Heavy metals pollution profiles in streams serving the Owabi reservoir // African Journal of Environmental Science and Technology. 2008. Vol. 2, Issue 11. P. 354–359.
29. Cui S., Zhou Q., Chao L. Potential hyperaccumulation of Pb, Zn, Cu and Cd in endurant plants distributed in an old smeltery, northeast China // Environmental Geology. 2007. Vol. 51. P. 1043–1048.
30. Bulaj G., Kortemme T., Goldenberg D. P. Ionization-reactivity relationships for cysteine thiols in polypeptides // Biochemistry. 1998. Vol. 37. P. 8965–8972.
31. Scheuhammer A. M., Cherian M. G. Quantification of metallothionein by silver saturation // Methods in Enzymology. 1991. Vol. 205. P. 78–83.
32. Gornall A. G., Bardawill C. J., David M. M. Determination of serum proteins by means of the biuret reaction // Journal of Biological Chemistry. 1949. Vol. 177. P. 751–766.
33. Habig W. H., Pabst M. J., Jakoby W. B. Glutathione S-Transferases: The first enzymatic step in mercapturic acid formation // The Journal of Biological Chemistry. 1974. Vol. 249, Issue 22. P. 7130–7139.
34. Effect of Pb and Ni on root development and biomass production of black gram (Vigna Mungo L.): overcoming through exogenous nitrogen application / Singh G., Agnihotri R. K., Singh D. K., Sharma R. // International Journal of Agriculture and Crop Sciences. 2013. Vol. 5, Issue 22. P. 2689–2696.
35. Pant P. P., Tripathi A. K. Gairola S. Phytpremediation of arsenic using cassia fistula linn seedling // International Journal of Research in Chemistry and Environment. 2011. Vol. 1, Issue 1. P. 24–28. ISSN 2248-9649.
36. Effects of glomus deserticola inoculation on prosopis: enhancing chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and TEM techniques / Arias J. A., Peralta-Videa J. R., Ellzey J. T. et al. // Environmental and Experimental Botany. 2010. Vol. 68, Issue 2. P. 139–148.
37. Seyyedi M., Timko M. P., Sundqvist C. Protochlorophylliden POR and chlorophyll formation in the Lip1 mutant of pea // Physiologia. Plantarum. 1999. Vol. 106. P. 344–354. doi: 10.1007/978-94-011-4788-0_33.
38. Ground-Water Remediation Technologies Analysis Center (GWRTAC). (1997). Remediation of Metal-Contaminated Soils and Groundwater. GWRTAC E Series. TE-97-01.
39. Heavy metal detoxification and tolerance mechanisms in plants: Implications for phytoremediation / Kushwaha A., Rani R., Kumar S., Gautam A. // Environmental Reviews. 2015. Vol. 23. P. 1–13. doi: 10.1139/er-2015-0010.
40. Javed M. T. Mechanisms behind pH changes by plant roots and shoots caused by elevated concentration of toxic elements. Doctoral Thesis in Plant Physiology at Stockholm University, Sweden, 2011. 40 pp.
41. Efe S. I., Elenwo E. I. Phytoremediation of crude oil contaminated soil with Axonopus compressus in the Niger Delta Region of Nigeria // Natural Resources. 2014. Vol. 5. P. 59–67. doi: 10.4236/nr.2014.52006.
42. The effects of soil properties to the extent of soil contamination with metals / Hasegawa H., Ismail M. D., Rahman I., Rahman M. A. // Environmental Remediation Technologies for Metal-Contaminated Soils. Springer, Tokyo. 2016. P. 1–19. doi: 10.1007/978-4-431-55759-3.
43. Competitive adsorption of zinc, cadmium, copper, and lead in three highly – weathered Brazilian soils / Fontes F., Matos M. P., Teixeira A. et al. // Communication in Soil Science and Plant Analysis. 2000. Vol. 31. P. 2939–2958. doi: 10.1080/00103620009370640.
44. Chijoke-Osuji C. C., Ebenezer B. Axonopus compressus: a resilient phytoremediatior of waste engine oil contaminated soil // International Journal of Plant and Soil Science. 2017. Vol. 14, Issue 2. P. 1–10.
45. U.S. Environmental Protection Agency (USEPA). Risk assessment guidance for superfund (Rags). Human Health Evaluation Manual (Part E, Supplemental Guidance for Dermal Risk Assessment) Interim. 2004. Available: http://www.epa.gov/oswer/ riskassessment/ragse/.
46. Enhanced clean-up of lead-contaminated alluvial soil through Chrysanthemum indicum L. / Mani D., Kumar C., Patel N. K., Sivakumar D. // International Journal of Environmental Science and Technology. 2015. Vol. 12, Issue 4. P. 1211–1222. doi: 10.1007/s13762-013-0488-5.
47. Cadmium accumulation and distribution in populations of Phytolacca americana L. and the role of transpiration / Liu X., Peng K., Wang A. et al. // Chemosphere. 2010. Vol. 78, Issue 9. P. 1136–1141. doi: 10.1016/j.chemosphere.2009.12.030.
48. Lead uptake, toxicity, and detoxification in plants / Pourrut B., Shahid M., Dumat C. et al. // Reviews of Environmental Contamination and Toxicology. 2011. Vol. 213. P. 113–136. doi: 10.1007/978-1-4419-9860-6_4.
49. Reactions of arsenic(III) and arsenic(V) species with glutathione / Scott N., Hatlelid K. M., MacKenzie N. E., Carter,D. E. // Chemical Research and Toxicology. 1993. Vol. 6. P. 102–106. doi: 10.1021/tx00031a016.
50. Sarma H. Metal hyperaccumulation in plants: a review focusing on phytoremediation technology // Journal of Environmental Science and Technology. 2011. Vol. 4. P. 118–138.
51. Rosen B. P. Biochemistry of arsenic detoxification // FEBS Letter. 2002. Vol. 529. P. 86–92.
52. Antioxidants responses to stimulated acid rain and heavy metal deposition in birch seedlings / Koricheva J., Roy S., Vranjic J. A. et al. // Environmental Pollution. 1997. Vol. 95. P. 249–258.
53. Gupta D. K., Huang H. G., Corpas F. J. Lead tolerance in plants: strategies for phytoremediation // Environmental Sciences and Pollution Research. 2013. Vol. 20. P. 2150–2161.
54. Ruley A. T., Sharma N. C., Sahi S. V. Antioxidant defense in a lead accumulating plant, Sesbania drummondii // Plant Physiology and Biochemistry. 2004. Vol. 42, Issue 11. P. 899–906.
55. Ojuederie O. B., Babalola O. O. Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review // International Journal of Environmental Research and Public Health. 2017. Vol. 14. Issue 12. P. 1504. doi: 10.3390%2Fijerph14121504.
56. Grennan A. K. Metallothioneins, a diverse protein family // Plant Physiology. 2011. Vol. 155. P. 1750–1751.
57. ScMT2-1-3, a metallothionein gene of sugarcane, plays an important role in the regulation of heavy metal tolerance/accumulation / Guo J., Xu L., Su Y. et al. // BioMed Research International. 2013. P. 904769. doi: 10.1155/2013/904769.
58. Heavy metal stress and some mechanisms of plant defense response / Emamverdian A., Ding Y., Mokhberdoran F., Xie Y. // Science World Journal. 2015. Vol. 2015. Article ID 756120. doi: 10.1155/2015/756120.
59. The genetics and genomics of the drought response in Populus / Street N. R., Skogstro M. O., Sjo din A. et al. // Plant Journal. 2006. Vol. 48. P. 321–341.
60. Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions / Bogeat-Triboulot, M. B., Brosche, M., Renaut, J. et al. // Plant Physiology. 2007. Vol. 143. P. 876–892.
61. Du J., Yaang J. L., Li C. H. Advances in metallothionein studies in forest trees // Plant Omics Journal. 2002. Vol. 5, Issue 1. P. 46–51.
62. The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione / Gupta D., Huang H., Yang X. et al. // Journal of Hazardous Materials. 2010. Vol. 177, Issue 1–3. P. 437–444.
63. Hayes J. D., Flanagan J. U., Jowsey I. R. Glutathione transferases // Annual Review of Pharmacology and Toxicology. 2005. Vol. 45. P. 51–88.
64. Genome-wide analysis of the glutathione S-transferase gene family in Capsella rubella: identification, expression, and biochemical functions /
He G., Guan C., Chen Q. X. et al. // Frontier in Plant Science. 2016. P. 1325. doi: 10.3389%2Ffpls.2016.01325.
65. Phytoremediation of Pb-contaminated soil by Salicornia iranica: key physiological and molecular mechanisms involved in Pb detoxification / Kaviani E., Niazi A., Heydarian Z. et al. // Clean–Soil Air Water. 2017. Vol. 45, Issue 5. doi: 10.1002/clen.201500964.