Content of Enzymatic and Nonenzymatic Antioxidants in Salix viminalis L. Grown on the Stebnyk Tailing

Anastasiia Fetsiukh, Liubov Bunio, Ostap Patsula, Salme Timmusk, Olga Terek

Abstract


Currently, the problem of environmental pollution, especially in contaminated areas, is highly important. The study of the defense mechanisms of plants under salt stress (high salinity) is of considerable importance, given the conditions of current agricultural development and climate change. The aim of this study was to reveal the effect of salinity on Salix viminalis L. under field conditions at the Stebnyk tailing site in Ukraine. After 120 days of growth, the leaves, stems, and roots of S. viminalis were harvested to measure the antioxidant defense system of plants under salinity. Inhibition of S. viminalis growth was observed. We found that peroxidase, ascorbic acid, and proline mainly accumulated in the stems of S. viminalis under salinity conditions. However, in the roots, an increase in catalase activity and soluble sugars content was observed under salinity stress. Thus, the increase in the amount and changes in the activity of enzymes showed the involvement of the antioxidant system in the adaptation of S. viminalis to salinity. The data obtained in this study serve as a starting point for understanding the adaptive mechanisms of S. viminalis to salinity, particularly at the Stebnyk tailing. We believe our findings will support the use of plants in nature-based solutions and eco-engineering projects on saline and industrially polluted lands.

Keywords


willow; catalase; peroxidase; soluble sugars; proline; ascorbic acid; salinity

Full Text:

PDF XML (JATS)

References


Akyol, T. Y., Yilmaz, O., Uzilday, B., Uzilday, R. Ö., & Türkan, İ. (2020). Plant response to salinity: An analysis of ROS formation, signaling, and antioxidant defense. Turkish Journal of Botany, 44(1), 1–13. https://doi.org/10.3906/bot-1911-15

Alencar, N. L. M., Oliveira, A. B., Alvarez-Pizarro, J. C., Marques, E. C., Prisco, J. T., & Gomes-Filho, E. (2021). Differential responses of dwarf cashew clones to salinity are associated to osmotic adjustment mechanisms and enzymatic antioxidative defense. Anais da Academia Brasileira de Ciências, 93, Article e20180534. https://doi.org/10.1590/0001-3765202120180534

Arsenov, D., Zupunski, M., Borisev, M., Nikolic, N., Orlovic, S., Pilipovic, A., & Pajevic, S. (2017). Exogenously applied citric acid enhances antioxidant defense and phytoextraction of cadmium by willows (Salix spp.). Water, Air, & Soil Pollution, 228(6), Article 221. https://doi.org/10.1007/s11270-017-3405-6

Babeanu, C., & Dodocioiu, A. M. (2018). Antioxidant enzymes activities and proline content in leaves of Salix species grown on fly ash dumps. Annals of the University of Craiova-Agriculture, Montanology, Cadastre Series, 47(2), 20–24.

Babeanu, C., Soare, M., Corneanu, M., & Dragoi, M. (2017). Effects of drought stress on some oxidoreductase enzymes and proline content in leaves of Salix genotypes. In 17th International Multidisciplinary Scientific GeoConference SGEM 2017, 29 June – 5 July, 2017 (pp. 665–671). STEF92 Technology. https://doi.org/10.5593/sgem2017/61/S25.087

Bandurska, H. (2001). Does proline accumulated in leaves of water deficit stressed barley plants confine cell membrane injuries? II. Proline accumulation during hardening and its involvement in reducing membrane injuries in leaves subjected to severe osmotic stress. Acta Physiologiae Plantarum, 23(4), 483–490. https://doi.org/10.1007/s11738-001-0059-0

Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205–207. https://doi.org/10.1007/BF00018060

Bhattacharya, A., Routh, J., Jacks, G., Bhattacharya, P., & Mörth, M. (2006). Environmental assessment of abandoned mine tailings in Adak, Västerbotten District (northern Sweden). Applied Geochemistry, 21(10), 1760–1780. https://doi.org/10.1016/j.apgeochem.2006.06.011

Bilek, M. A., Soolanayakanahally, R. Y., Guy, R. D., & Mansfield, S. D. (2020). Physiological response of Populus balsamifera and Salix eriocephala to salinity and hydraulic fracturing wastewater: Potential for phytoremediation applications. International Journal of Environmental Research and Public Health, 17(20), Article 7641. https://doi.org/10.3390/ijerph17207641

Білоніжка [Bilonizhka], Р. [P.], & Дяків [Diakiv], В. [V.]. (2009). Хімічний та мінеральний склад відходів збагачення калійних руд Стебницького родовища та їхній вплив на довкілля [Chemical and mineral composition of the enrichment wastes of the Stebnyk deposit potassium ores and its influence on the environment]. Вісник Львівського університету. Cерія геологічна [Visnyk of the Lviv University. Geology Series], 2009(23), 162–174.

Chiappero, J., del Rosario Cappellari, L., Palermo, T. B., Giordano, W., Khan, N., & Banchio, E. (2021). Antioxidant status of medicinal and aromatic plants under the influence of growth-promoting rhizobacteria and osmotic stress. Industrial Crops and Products, 167, Article 113541. https://doi.org/10.1016/j.indcrop.2021.113541

Chutipaijit, S. (2016). Changes in physiological and antioxidant activity of indica rice seedlings in response to mannitol-induced osmotic stress. Chilean Journal of Agricultural Research, 76(4), 455–462. https://doi.org/10.4067/S0718-58392016000400009

Das, S., Jahiruddin, M., Islam, M. R., Mahmud, A. A., Hossain, A., & Laing, A. M. (2020). Zinc biofortification in the grains of two wheat (Triticum aestivum L.) varieties through fertilization. Acta Agrobotanica, 73(1), Article 7312. https://doi.org/10.5586/aa.7312

Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28(3), 350–356. https://doi.org/10.1021/ac60111a017

Eljebbawi, A., Guerrero, Y. D. C. R., Dunand, C., & Estevez, J. M. (2021). Highlighting reactive oxygen species as multitaskers in root development. Iscience, 24(1), Article 101978. https://doi.org/10.1016/j.isci.2020.101978

Фецюх [Fetsiukh], A. [A.], Буньо [Bun′o], Л. [L.], Пацула [Patsula], О. [O.], & Терек [Terek], О. [O]. (2018). Екологічні проблеми, спричинені розробкою Прикарпатського pодовища полімінеральних калійних руд у м. Стебник [Environmental problems caused by the development of the Precarpathian deposit of polymineral potassium ores in Stebnyk]. Біологічні студії [Studia Biologica], 12(2), 157–166. https://doi.org/10.30970/sbi.1202.537

Фецюх [Fetsiukh], A. [A.], Буньо [Bun′o], Л. [L.], Пацула [Patsula], О. [O.], & Терек [Terek], О. [O]. (2019). Накопичення важких металів рослинами S. viminalis за росту на субстраті зі Стебницького хвостосховища [Accumulation of heavy metals by Salix viminalis plants under growing at the substrate from Stebnyk tailings]. Вісник Львівського університету. Серія біологічна [Visnyk of the Lviv University. Biological Series], 2019(81), 96–110. https://doi.org/10.30970/vlubs.2019.81.11

Gajić, G., Djurdjević, L., Kostić, O., Jarić, S., Mitrović, M., & Pavlović, P. (2018). Ecological potential of plants for phytoremediation and ecorestoration of fly ash deposits and mine wastes. Frontiers in Environmental Science, 6, Article 124. https://doi.org/10.3389/fenvs.2018.00124

Гавриленко [Gavrilenko], В. Ф. [V. F.], Ладышна [Ladyshna], М. Е. [M. E.], & Хандобина [Handobina], Л. М. [L. M.]. (1975). Большой практикум по физиологии растений: Фотосинтез. Дыхание [Plant physiology: Photosynthesis and respiration]. Высшая школа [Vysshaia shkola].

Gonzalez-Ollauri, A., & Mickovski, S. B. (2020). The effect of willow (Salix sp.) on soil moisture and matric suction at a slope scale. Sustainability, 12(23), Article 9789. https://doi.org/10.3390/su12239789

Hangs, R. D., Schoenau, J. J., Van Rees, K. C. J., & Steppuhn, H. (2011). Examining the salt tolerance of willow (Salix spp.) bioenergy species for use on salt-affected agricultural lands. Canadian Journal of Plant Science, 91, 509–517. https://doi.org/10.4141/cjps10135

Harris, M. M., & Jurgensen, M. F. (1977). Development of Salix and Populus mycorrhizae in metallic mine tailings. Plant and Soil, 47(2), 509–517. https://doi.org/10.1007/BF00011507

Hernandez, S., Deleu, C., & Larher, F. (2000). Accumulation de proline dans les tissus foliaires de tomate en réponse à la salinité [Proline accumulation by tomato leaf tissue in response to salinity]. Comptes rendus de l’Academie des sciences. Serie III, Sciences de la vie, 323(6), 551–557. https://doi.org/10.1016/s0764-4469(00)00167-0

Huang, X., Soolanayakanahally, R. Y., Guy, R. D., Shunmugam, A. S., & Mansfield, S. D. (2020). Differences in growth and physiological and metabolic responses among Canadian native and hybrid willows (Salix spp.) under salinity stress. Tree Physiology, 40(5), 652–666. https://doi.org/10.1093/treephys/tpaa017

Гузар [Huzar], О. [O.]., Буньо [Bunio], Л. [L.], & Микієвич [Mykiyevych], І. [I.]. (2016). Вплив сольового забруднення хвостосховища на накопичення Карбону у субстраті та в рослинах Salix viminalis L. [Effect of tailing contamination with salt on the accumulation of carbon in the substrate and in Salix viminalis L. plants]. In Сборник статей XIV Междунар. заочн. научно-практ. конф. «Развитие науки в XXI веке», г. Харьков, 16 июня 2016 г [Proceedings of the XIV International Conference “Development of science in the twenty-first century,” Kharkiv, June 16, 2016] (pp. 38–42). Serenity-Group.

Іващенко [Ivashchenko], О. Л. [O. L.]. (2013). Визначення вмісту проліну в галофітах куяльницького лиману [Determination of proline content in halophytes of Kuyalnytsya estuary]. Одеський національний університет імені І. І. Мечникова [Odessa I. I. Mechnikov National University]. http://dspace.onu.edu.ua:8080/handle/123456789/5048

Jahantigh, O., Najafi, F., Badi, H. N., Khavari-Nejad, R. A., & Sanjarian, F. (2016). Changes in antioxidant enzymes activities and proline, total phenol and anthocyanine contents in Hyssopus officinalis L. plants under salt stress. Acta Biologica Hungarica, 67(2), 195–204. https://doi.org/10.1556/018.67.2016.2.7

Janicka, M., Kutkowska, A., & Paderewski, J. (2021). Diversity of segetal flora in Salix viminalis L. crops established on former arable and fallow lands in central Poland. Agriculture, 11(1), Article 25. https://doi.org/10.3390/agriculture11010025

Jia, H., Wang, L., Li, J., Sun, P., Lu, M., & Hu, J. (2020). Physiological and metabolic responses of Salix sinopurpurea and Salix suchowensis to drought stress. Trees, 34(2), 563–577. https://doi.org/10.1007/s00468-019-01937-z

Karmakar, D., Deb, K., & Padhy, P. K. (2021). Ecophysiological responses of tree species due to air pollution for biomonitoring of environmental health in urban area. Urban Climate, 35, Article 100741. https://doi.org/10.1016/j.uclim.2020.100741

Khaleghi, A., Naderi, R., Brunetti, C., Maserti, B. E., Salami, S. A., & Babalar, M. (2019). Morphological, physiochemical and antioxidant responses of Maclura pomifera to drought stress. Scientific Reports, 9(1), Article 19250. https://doi.org/10.1038/s41598-019-55889-y

Колупаєв [Kolupaiev], Ю. Є. [Iu. Ie.], & Обозний [Oboznyĭ], О. І. [O. I.]. (2013). Активні форми кисню і антиоксидантна система при перехресній адаптації рослин до дії абіотичних стресорів [Reactive oxygen species and antioxidative system at cross adaptation of plants to activity of abiotic stressors]. Вісник Харківського національного аграрного університету. Серія: Біологія [Bulletin of Kharkiv National Agrarian University. Biology Series], 2013(3), 18–31.

Королюк [Koroliuk], М. А. [M. A.], Иванова [Ivanova], Л. К. [L. K.], Майорова [Maĭorova], И. Г. [I. G.], & Токарева [Tokareva], В. А. [V. A.]. (1988). Метод определения активности каталазы [Method for determination of catalase activity]. Лабораторное дело [Laboratornoe delo], 1988(4), 44–47.

Кригер [Kriger], Н. В. [N. V.], Козлов [Kozlov], М. А. [M. A.], & Баранов [Baranov], Е. С. [E. S.]. (2013). Влияние техногенной нагрузки на содержание аскорбиновой кислоты в листьях древесных растений, произрастающих в разных районах города Красноярска [The anthropogenic load influence on the ascorbic acid content in wood plant leaves growing in the Krasnoyarsk City different districts]. Вестник Красноярского государственного аграрного университета [Bulletin of the Krasnoyarsk State Agrarian University], 2013(10), 116–119.

Кияк [Kyiak], Н. [N.]. (2018). Фотосинтетична активність бріофітів в умовах засолення на території хвостосховища Стебницького ГХП «Полімінерал» [Photosynthetic activity of bryophytes under the conditions of salinity on the territory of tailing of Stebnyk state mining and chemical enterprise Polimineral]. Вісник Львівського університету. Серія біологічна [Visnyk of the Lviv University. Biological Series], 2018(79), 184–194. https://doi.org/10.30970/vlubs.2018.79.20

Li, B., Ouyang, J., Li, C., Shang, X., & Zou, J. (2018). Response to NaCl stress in Salix matsudana Koidz seedlings. Polish Journal of Environmental Studies, 27(2), 753–762. https://doi.org/10.15244/pjoes/75820

Lu, Y., Zeng, F. J., Li, X. Y., & Zhang, B. (2021). Physiological changes of three woody plants exposed to progressive salt stress. Photosynthetica, 59(1), 171–184. https://doi.org/10.32615/ps.2021.007

Munawar, W., Hameed, A., & Khan, M. K. R. (2021). Differential morphophysiological and biochemical responses of cotton genotypes under various salinity stress levels during early growth stage. Frontiers in Plant Science, 12, Article 622309. https://doi.org/10.3389/fpls.2021.622309

Mushtaq, Z., Faizan, S., & Gulzar, B. (2020). Salt stress, its impacts on plants and the strategies plants are employing against it: A review. Journal of Applied Biology & Biotechnology, 8(3), 81–91. https://doi.org/10.7324/JABB.2020.80315

Мусієнко [Musiienko], М. М. [M. M.], Паршикова [Parshikova], Т. В. [T. V.], & Славний [Slavnyĭ], П. С. [P. S.]. (2001). Спектрофотометричні методи в практиці фізіології, біохімії та екології рослин [Spectrophotometric methods in the practice of physiology, biochemistry, and ecology of plants]. Фітосоціоцентр [Phytocenter].

Nemati, I., Moradi, F., Gholizadeh, S., Esmaeili, M. A., & Bihamta, M. R. (2011). The effect of salinity stress on ions and soluble sugars distribution in leaves, leaf sheaths and roots of rice (Oryza sativa L.) seedlings. Plant, Soil and Environment, 57(1), 26–33. https://doi.org/10.17221/71/2010-PSE

Павлюк [Pavliuk], Ю. Е. [Iu. E.], Ференц [Ferents], Н. А. [N. A.], & Мелько [Mel′ko], В. М. [V. M.]. (2013). Техногенна небезпека гірничих виробок калійних мінеральних добрив [Technogenic danger of excavations of potash mineral fertilizers]. Вісник ЛДУ БЖД [Visnyk of Lviv State University of Life Safety], 2013(7), 199–202.

Qaseem, M. F., Qureshi, R., Shaheen, H., & Waheed, A. (2021). Multivariate analysis for yield and proline content in wheat under lab and field conditions. Pakistan Journal of Botany, 53(1), 227–239. https://doi.org/10.30848/PJB2021-1(30)

Rasheed, F., Gondal, A., Kudus, K. A., Zafar, Z., Nawaz, M. F., Khan, W. R., Abdullah, M., Ibrahim, F. H., Depardieu, C., Pazi, A. M. M., Anjum, K., Afzal, S., Akram, S., & Nazre, M. (2021). Effects of soil water deficit on three tree species of the arid environment: Variations in growth, physiology, and antioxidant enzyme activities. Sustainability, 13(6), Article 3336. https://doi.org/10.3390/su13063336

Rosa, M., Prado, C., Podazza, G., Interdonato, R., González, J. A., Hilal, M., & Prado, F. E. (2009). Soluble sugars: Metabolism, sensing and abiotic stress: A complex network in the life of plants. Plant Signaling & Behavior, 4(5), 388–393. https://doi.org/10.4161/psb.4.5.8294

Shi, X., Wang, S., Sun, H., Chen, Y., Wang, D., Pan, H., Zou, Y., Liu, J., Zheng, L., Zhao, X., & Jiang, Z. (2017). Comparative of Quercus spp. and Salix spp. for phytoremediation of Pb/Zn mine tailings. Environmental Science and Pollution Research, 24(4), 3400–3411. https://doi.org/10.1007/s11356-016-7979-0

Снітинський [Snityns′kyĭ], В. [V.], Зелізко [Zelizko], О. [O.], Хірівський [Khirivs′kyĭ], П. [P.], Бучко [Buchko], A. [A.], & Корінець [Korinets′], Ю. [Iu.]. (2015). Екологічнa оцінкa гідрогеологічних пaрaметрів території Стебницького родовищa кaлійних солей Дрогобицького рaйону Львівської облaсті [Environmental assessment of hydrogeological parameters territory of Stebnyk deposits of potassium salts of Drohobych District Lviv region]. Вісник Львівського нaціонального аграрного університету. Серія Aгрономія [Visnyk of Lviv National Agrarian University. Agronomy Series], 2015(19), 3–7.

Song, H. J., & Su, K. M. (2017). Physiological responses against salt stress of Salix gracilistyla. Journal of Agriculture & Life Science, 51(3), 1–10. https://doi.org/10.14397/jals.2017.51.3.1

Stolarska, A., & Klimek, D. (2008). Free proline synthesis in leaves of three clones of basket willow (Salix viminalis) as a response to substrate salinity. Environment Protection Engineering, 34(4), 97–101.

Stoltz, E., & Greger, M. (2002). Accumulation properties of As, Cd, Cu, Pb and Zn by four wetland plant species growing on submerged mine tailings. Environmental and Experimental Botany, 47, 271–280. https://doi.org/10.1016/S0098-8472(02)00002-3

Vahdati, K., & Lotfi, N. (2013). Abiotic stress tolerance in plants with emphasizing on drought and salinity stresses in walnut. In K. Vahdati & C. Leslie (Eds.), Abiotic stress – Plant responses and applications in agriculture (pp. 307–365). InTech. https://doi.org/10.5772/56078

Varga, C., Marian, M., Mihaly-Cozmuta, L., Mihaly-Cozmuta, A., & Mihalescu, L. (2009). Evaluation of the phytoremediation potential of the Salix caprea in tailing ponds. Analele Universităţii din Oradea, Fascicula Biologie, 16(1), 141–149.

Wang, Y., Yuan, H., Li, M., Li, Y., Ma, X., Tan, F., & Zhang, J. (2013). Phenotypic and physiological responses of two willow varieties to salt stress. Israel Journal of Plant Sciences, 61(1–4), 73–82. https://doi.org/10.1080/07929978.2014.977548

Wilcox, E. (2013). Survival and growth of willows on biosolid covers over Ni–Cu tailings [Unpublished doctoral dissertation]. Laurentian University Sudbury.

Wróbel, J., & Mikiciuk, M. (2010). Water and ionic balance in the leaves of basket willow (Salix viminalis L.) cultivated in hydroponics with different salinity levels. Ecological Chemistry and Engineering A, 17(10), 1315–1321.

Yang, J., Yang, J., Zhao, L., Gu, L., Wu, F., Tian, W., Sun, Y., Zhang, S., Su, H., & Wang, L. (2021). Ectopic expression of a Malus hupehensis Rehd. myo-inositol oxygenase gene (MhMIOX2) enhances tolerance to salt stress. Scientia Horticulturae, 281, Article 109898. https://doi.org/10.1016/j.scienta.2021.109898

Zhou, M., Li, D., Li, Z., Hu, Q., Yang, C., Zhu, L., & Luo, H. (2013). Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiology, 161(3), 1375–1391. https://doi.org/10.1104/pp.112.208702




DOI: https://doi.org/10.5586/aa.752

Journal ISSN:
  • 2300-357X (online)
  • 0065-0951 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society