Фізіологія рослин і генетика 2026, том 58, № 2, 152-167, doi:

Вплив важких металів на проростання та розвиток коренів у Sorghum bicolor nothosubsp. drummondii f. alba

Матвєєва Н.А., Льошина Л.Г, Дуплій В.П., Богданович Т.А., Булко О.В., Кучук М.В.

Ключові слова: Sorghum bicolor nothosubsp. drummondii f. alba, toxic metals, phytoremediation, nickel, lead, copper, tolerance

Фізіологія рослин і генетика
2026, том 58, № 2, 152-167

Повний текст та додаткові матеріали

Цитована література

1.   Mustapha, L.S., Obayomi, O.V. & Obayomi, K.S. (2025). A comprehensive review on potential heavy metals in the environment: Persistence, bioaccumulation, ecotoxicology, and agricultural impacts. Ecol. Front., 46, pp. 434-449. https://doi.org/10.1016/ j.ecofro.2025.10.009

 2. Begum, W., Rai, S., Banerjee, S., Bhattacharjee, S., Mondal, M.H., Bhattarai, A. & Saha, B. (2022). A comprehensive review on the sources, essentiality and toxicological profile of nickel. RSC Advances., 12, pp. 9139-9153. https://doi.org/10.1039/ D2RA00378C

 3. Kumar, A. (2023). Nickel availability, deficiency and toxicity in soils and plants. Int. J. Appl. Res., 9, pp. 265-272. https://doi.org/10.22271/allresearch.2023.v9.i8d.11221

 4. Li, S., Yang, D., Tian, J., Wang, S., Yan, Y., He, X., Du, Z. & Zhong, F. (2022). Physiological and transcriptional response of carbohydrate and nitrogen metabolism in tomato plant leaves to nickel ion and nitrogen levels. Sci. Hort., 292, pp. 110620. https://doi.org/10.1016/j.scienta.2021.110620

 5. Miнkowiec, P. & Olech, Z. (2020). Searching for the correlation between the activity of urease and the content of nickel in the soil samples: The role of metal speciation. J. Soil Sci. Plant Nutr., 20, pp. 1904-1911. https://doi.org/10.1007/s42729-020-00261-7

 6. Patra, A., Singh, R.P., Singh, B.K. & Ram, R.M. (2024). Importance of nickel in plant nitrogen metabolism. Biotica Res. Today, 6, pp. 465-467.

 7. Lilay, H.G., Thiѕbaut, N., du Mee, D., Assunc±o, A.G.L., Schjoerring, J.K., Husted, S. & Persson, D.P. (2024). Linking the key physiological functions of essential micronutrients to deficiency symptoms in plants. New Phytol., 242(3), pp. 881-902. https://doi.org/10.1111/nph.19645

 8. Fabiano, C.C., Tezotto, T., Favarin, J.L., Polacco, J.C. & Mazzafera, P. (2015). Essentiality of nickel in plants: A role in plant stresses. Front. Plant Sci., 6, 754. https://doi.org/10.3389/fpls.2015.00754

 9. Ahmad, M.S.A. & Ashraf, M. (2012). Essential Roles and Hazardous Effects of Nickel in Plants. In: Whitacre, D. (eds) Reviews of Environmental Contamination and Toxicology. Reviews of Environmental Contamination and Toxicology, vol 214., pp. 125-167, Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0668-6_6

10. Kumar, U., Kumar, I., Singh, P.K., Dwivedi, A., Singh, P., Mishra, S., Seth, C.S. & Sharma, R.K. (2025). Nickel contamination in terrestrial ecosystems. Rev. Environ. Contamin. Toxicol., 263, article number 2. https://doi.org/10.1007/s44169-024-00075-z

11. Rizwan, M., Usman, K. & Alsafran, M. (2024). Ecological impacts and potential hazards of nickel. Chemosphere, 357, 142028. https://doi.org/10.1016/j.chemosphere.2024.142028

12. Maheshwari, R. & Dubey, R.S. (2009). Nickel-induced oxidative stress in rice seedlings. Plant Growth Regul., 59, pp. 37-49. https://doi.org/10.1007/s10725-009-9386-8

13. Amjad, M., Raza, H., Murtaza, B., Abbas, G., Imran, M., Shahid, M., Naeem, M.A., Zakir, A. & Iqbal, M.M. (2020). Nickel toxicity induced changes in nutrient dynamics and antioxidant profiling in two maize (Zea mays L.) hybrids. Plants, 9, 5. https://doi.org/10.3390/plants9010005

14. Baran, U. & Ekmekci, Y. (2022). Physiological, photochemical, and antioxidant responses of wild and cultivated Carthamus species exposed to nickel toxicity and evaluation of their usage potential in phytoremediation. Environ. Sci. Pollution Res.,. 29, pp. 29513-29527. https://doi.org/10.1007/s11356-021-15493-y

15. Hassan, M.U., Chattha, M.U., Khan, I., Chattha, M.B., Aamer, M., Nawaz, M., Ali, A., Khan, M. & Khan, T.A. (2019). Nickel toxicity in plants: Reasons, toxic effects, tolerance mechanisms, and remediation possibilities. Environ. Sci. Pollution Res., 26, pp. 12673-12688. https://doi.org/10.1007/s11356-019-04892-x

16. Sengar, R.S., Gautam, M., Garg, S.K., Sengar, R.S., Garg, S.K., Sengar, K. & Chaudhary, R. (2008). Lead Stress Effects on Physiobiochemical Activities of Higher Plants. In: Whitacre, D. (eds) Reviews of Environmental Contamination and Toxicology Vol. 196, pp. 73-93. Reviews of Environmental Contamination and Toxicology, vol 196. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78444-1_3

17. Romanowska, E., WrЩblewska, B., Droьak, A., Zienkiewicz, M. & Siedlecka, M. (2008). Effect of Pb ions on antioxidant enzymes. Biol. Plant., 52, pp. 80-86. https://doi.org/ 10.1007/s10535-008-0012-9

18. Reddy, A.M., Kumar, S.G., Jyothsnakumari, G., Thimmanaik, S. & Sudhakar, C. (2005). Lead-induced changes in antioxidant metabolism. Chemosphere, 60, pp. 97-104. https://doi.org/10.1016/j.chemosphere.2004.11.092

19. Qufei, L. & Fashui, H. (2009). Effects of Pb2+ on the structure and function of Photosystem II of Spirodela polyrrhiza. Biol. Trace Element Res., 129, pp. 251-260. https://doi.org/10.1007/s12011-008-8283-8

20. Meyers, D.E. R., Auchterlonie, G.J., Webb, R.I., & Wood, B. (2008). Uptake and localisation of lead in the root system of Brassica juncea. Environ. Poll., 153, pp. 323-332. https://doi.org/10.1016/j.envpol.2007.08.029

21. Liu, D., Li, T., Jin, X., Yang, X., Islam, E. & Mahmood, Q. (2008). Lead-induced changes in the growth and antioxidant metabolism of the lead-accumulating and non-accumulating ecotypes of Sedum alfredii. J. Integr. Plant Biol., 50, pp. 129-140. https://doi.org/10.1111/j.1744-7909.2007.00608.x

22. Pourrut, B., Shahid, M., Dumat, C., Winterton, P. & Pinelli, E. (2011). Lead uptake, toxicity, and detoxification in plants. Rev. Environ. Contamin. Toxicol., 213, pp. 113-136. https://doi.org/10.1007/978-1-4419-9860-6_4

23. Liu, Y., Du, C., Lin, C., Gao, X., Zhu, J. & Zhang, C. (2022) Characterization of Copper/Zinc Superoxide Dismutase Activity on Phascolosoma esculenta (Sipuncula: Phascolosomatidea) and Its Protection from Oxidative Stress Induced by Cadmium. Int. J. Mol. Sci., 23, pp. 12136. https://doi.org/10.3390/ijms232012136

24. Zhang, S. (2023) Recent Advances of Polyphenol Oxidases in Plants. Molecules, 28, p. 2158. https://doi.org/10.3390/molecules28052158

25. Milrad, Y., Wegemann, D., Kuhlgert, S., Scholz, M., Younas, M., Vidal-Meireles, A. & Hippler, M. (2025) Insights into plastocyanin-cytochrome b6f complex formation: The role of plastocyanin phosphorylation. Plant Physiol., 198, kiaf269. https://doi.org/ 10.1093/plphys/kiaf269

26. Mansilla, N., Racca, S., Gras, D.E., Gonzalez, D.H. & Welchen, E. (2018) The Complexity of Mitochondrial Complex IV: An Update of Cytochrome c Oxidase Biogenesis in Plants. Int. J. Mol. Sci., 19, p. 662. https://doi.org/10.3390/ijms19030662

27. Xu, E., Liu, Y., Gu, D., Zhan, X., Li, J., Zhou, K., Zhang, P. & Zou, Y. (2024) Molecular Mechanisms of Plant Responses to Copper: From Deficiency to Excess. Int. J. Mol. Sci., 25, p. 6993. https://doi.org/10.3390/ijms25136993

28. Panagos, P., Ballabio, C., Lugato, E., Jones, A., Borrelli, P., Scarpa, S., Orgiazzi, A. & Montanarella, L. (2018) Potential Sources of Anthropogenic Copper Inputs to European Agricultural Soils. Sustainability, 10, p. 2380. https://doi.org/10.3390/su10072380

29. Adrees, M., Ali, S., Rizwan, M., Ibrahim, M., Abbas, F., Farid, M., Zia-ur-Rehman, M., Irshad, M.K. & Bharwana, S.A. (2015) The Effect of Excess Copper on Growth and Physiology of Important Food Crops: A Review. Environ. Sci. Pollut Res, 22, pp. 8148-8162. https://doi.org/10.1007/s11356-015-4496-5

30. Kapoor, D., Singh, S., Kumar, V., Romero, R., Prasad, R. & Singh, J. (2019) Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Plant Gene, 19, p. 100182. https://doi.org/10.1016/j.plgene.2019.100182

31. P¬tsikk¬, E., Kairavuo, M., ћerлen, F., Aro, E.M. & Tyystj¬rvi, E. (2002) Excess Copper Predisposes Photosystem II to Photoinhibition in Vivo by Outcompeting Iron and Causing Decrease in Leaf Chlorophyll. Plant Physiol., 129, pp. 1359-1367. https://doi.org/10.1104/pp.004788

32. Arredondo, M., MartНnez, R., NуФez, M.T., Ruz, M. & Olivares, M. (2006) Inhibition of iron and copper uptake by iron, copper and zinc. Biol. Res., 39, pp. 95-102. https://doi.org/10.4067/s0716-97602006000100011

33. Tang, X., Huang, Y., Li, Y., Wang, L., Pei, X., Zhou, D., He, P. & Hughes, S.S. (2021). Chromium detoxification by microorganisms. Ecotoxicol. Environ. Safety, 208, pp. 111699. https://doi.org/10.1016/j.ecoenv.2020.111699

34. Awa, S.H. & Hadibarata, T. (2020). Removal of heavy metals in contaminated soil by phytoremediation mechanism: A review. Water, Air, Soil Pollut., 231, 47. https://doi.org/10.1007/s11270-020-4426-0

35. Dijoux, J., Gigante, S., Lecellier, G., Guentas, L. & Burtet-Sarramegna, V. (2025). Plant nickel-exclusion versus hyperaccumulation: A microbial perspective. Microbiome, 13, 110. https://doi.org/10.1186/s40168-025-02098-7

36. Bolan, N.S., Park, J.H., Robinson, B., Naidu, R. & Huh, K.Y. (2011). Phytostabilization: A green approach to contaminant containment. Advances in Agronomy, 112, pp. 145-204. https://doi.org/10.1016/B978-0-12-385538-1.00004-4

37. Li, Y.M., Chaney, R.L., Brewer, E.P., Angle, J.S. & Nelkin, J. (2003). Phytoextraction of nickel and cobalt by hyperaccumulator Alyssum species grown on nickel-contaminated soils. Environ. Sci. Technol., 37, pp. 1463-1468. https://doi.org/10.1021/es0208963

38. Kumar, A., Jigyasu, D.K., Kumar, A., Subrahmanyam, G., Mondal, R., Shabnam, A.A., Cabral-Pinto, M.M.S., Malyan, S.K., Chaturvedi, A.K., Gupta, D.K., Fagodiya, R.K., Khan, S.A. & Bhatia, A. (2021). Nickel in terrestrial biota: Comprehensive review on contamination, toxicity, tolerance and its remediation approaches. Chemosphere, 275, p. 129996. https://doi.org/10.1016/j.chemosphere.2021.129996

39. Giordani, C., Cecchi, S. & Zanchi, C. (2005). Phytoremediation of soil polluted by nickel using agricultural crops. Environ. Manag., 36, pp. 675-681. https://doi.org/ 10.1007/s00267-004-0171-1

40. Al Chami, Z., Amer, N., Al Bitar, L. & Cavoski, I. (2015). Potential use of Sorghum bicolor and Carthamus tinctorius in phytoremediation of nickel, lead and zinc. Int. J. Environ. Sci. Technol., 12, pp. 3957-3970. https://doi.org/10.1007/s13762-015-0823-0

41. Anguilano, L., Onwukwe, U., Dekhli, A., Venditti, S., Aryani, D. & Reynolds, A. (2022). Hyperaccumulation of lead using Agrostis tenuis. Environ. Syst. Res., 11, 30. https://doi.org/10.1186/s40068-022-00279-z

42. Kтpper, H., Lombi, E., Zhao, F., Wieshammer, G., & McGrath, S.P. (2001). Cellular compartmentation of nickel in the HA Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J. Exp. Bot., 52, pp. 2291-2300. https://doi.org/10.1093/jexbot/ 52.365.2291

43. Zhang, L., Zhu, Y., Gu, H., Lam, S.S., Chen, X., Sonne, C. & Peng, W. (2024). A review of phytoremediation of environmental lead (Pb) contamination. Chemosphere, 362, 142691. https://doi.org/10.1016/j.chemosphere.2024.142691

44. Collin, S., Baskar, A., Geevarghese, D.M., Ali, M.N.V.S., Bahubali, P., Choudhary, R., Lvov, V., Tovar, G.I., Senatov, F., Koppala, S. & Swamiappan, S. (2022). Bioaccumulation of lead (Pb) and its effects in plants: A review. J. Hazardous Materials Lett., 3, 100064. https://doi.org/10.1016/j.hazl.2022.100064

45. Elik, U. & Gul, Z. (2025). Accumulation potential of lead and cadmium metals in maize (Zea mays L.) and effects on physiological-morphological characteristics. Life, 15, 310. https://doi.org/10.3390/life15020310

46. Yao, X., Saikawa, E., Warner, S., D’Souza, P.E., Ryan, P.B. & Barr, D.B. (2023). Phytoremediation of lead-contaminated soil in the Westside of Atlanta, GA. GeoHealth, 7, e2022GH000752. https://doi.org/10.1029/2022GH000752

47. Thompson, D., Bush, E. & Kirk-Ballard, H. (2021). Lead phytoremediation in contaminated soils using ornamental landscape plants. J. Geosci. Environ. Protect., 9, pp. 152-164. https://doi.org/10.4236/gep.2021.95011

48. Moln«r, E., Bobek-Nagy, J., Juzsakova, T., Kurdi, R. & Rauch, R. (2025). Tagetes erecta as a nickel phytoremediator: Insights into accumulation and growth response. Circular Econ. Sustainabil., 5, pp. 6483-6498. https://doi.org/10.1007/s43615-025-00603-6

49. De Bernardi, A., Casucci, C., Businelli, D., D’Amato, R., Beone, G.M., Fontanella, M.C. & Vischetti, C. (2020). Phytoremediation potential of crop plants in countering nickel contamination in carbonation lime coming from the sugar industry. Plants, 9, 580. https://doi.org/10.3390/plants9050580

50. AdiloИlu, S., Turgut SaИlam, M., AdiloИlu, A. & Sтme, A. (2016). Phytoremediation of nickel (Ni) from agricultural soils using canola (Brassica napus L.). Desalinat. Water Treatment, 57, pp. 2383-2388. https://doi.org/10.1080/19443994.2014.994110

51. An, Y.-J. (2006). Assessment of comparative toxicities of lead and copper using plant assay. Chemosphere, 62, pp. 1359-1365. https://doi.org/10.1016/j.chemosphere. 2005.07.044

52. †evik, B., Arslan, H. & Ekinci, D. (2025). Effects of heavy metal stress on seedling growth and antioxidant system in sorghum (Sorghum bicolor (L.) Moench). Protein J., 44, pp. 308-316. https://doi.org/10.1007/s10930-025-10258-9

53. Jiang, J., Zhang, N., Srivastava, A.K., He, G., Tai, Z., Wang, Z., Yang, S., Xie, X. & Li, X. (2024). Superoxide dismutase positively regulates Cu/Zn toxicity tolerance in Sorghum bicolor by interacting with Cu chaperone for superoxide dismutase. J. Hazardous Materials, 480, 135828. https://doi.org/10.1016/j.jhazmat.2024.135828

54. Roy, S.K., Cho, S.W., Kwon, S.J., Kamal, A.H.M., Lee, D.G., Sarker, K., Lee, M.S., Xin, Z. & Woo, S.H. (2017). Proteome characterization of copper stress responses in the roots of sorghum. Biometals, 30, pp. 765-785. https://doi.org/10.1007/s10534-017-0045-7

55. Sagimbayeva, A.M., Tomlekova, N.B., Saparov, G.A., Abduraimov, Y.O., Kerimbayev, A.A., Nurabayev, S.S., Assanzhanova, N.N., Akmyrzayev, N.Z., Iskakova, K.M., Omarova, A.S. & Anapiyayev, B.B. (2025). Phytoremediation of heavy metal-contaminated soil using drought-adapted sweet sorghum (Sorghum bicolor L.) in arid regions of Kazakhstan. Plants, 14, 3627. https://doi.org/10.3390/plants14233627

56. Lima, L.R., Silva, H.F., Brignoni, A.S., Silva, F.G., Camargos, L.S. & Souza, L.A. (2019). Characterization of biomass sorghum for copper phytoremediation: Photosynthetic response and possibility as a bioenergy feedstock from contaminated land. Physiol. Mol. Biol. Plants, 25, pp. 433-441. https://doi.org/10.1007/s12298-018-00638-0

57. Kovrov, O., Koveria, A., Shemet, V., Ovcharenko, A., Cherdantseva, K., Panteleieva, O., Malichenko, V. (2026). Ecological assessment of soil quality affected by the Shahed-136 drone strike: Case study in Kirovograd region, Ukraine. Sustainable Environ., 12, 2615531. https://doi.org/10.1080/27658511.2026.2615531

58. TЮzsѕr, D., Osazuwa, J.D., Elias, J.S., Idehen, D.O., Gutiѕrrez Pѕrez, D.I., Ragy«k, A.Z., Sajtos, Z. & Magura, T. (2025). Comparative analysis of the short-term germination and metal accumulation patterns of two sorghum hybrids. Environ. Geochem. Health, 47, 178. https://doi.org/10.1007/s10653-025-02485-x

59. Perlein, A., Bert, V., Desannaux, O., Fernandes de Souza, M., Papin, A., Gaucher, R., Zdanevitch, I. & Meers, E. (2021). The use of sorghum in a phytoattenuation strategy: A field experiment on a TE-contaminated site. Appl. Sci., 11, 3471. https://doi.org/ 10.3390/app11083471