vestibИзвестия Национальной академии наук Беларуси. Серия биологических наукProceedings of the National Academy of Sciences of Belarus, Biological Series1029-89402524-230XThe Republican Unitary Enterprise Publishing House "Belaruskaya Navuka"10.29235/1029-8940-2025-70-4-304-315vestib-987Research ArticleСтатьиИзменение уровня экспрессии генов, кодирующих системы стрессового ответа, в корнях Arabidopsis thaliana (L.) Heynh. под действием токсических уровней Ni2+ в среде и влияние на него экзогенного L-гистидинаAlterations in expression of stress-responsive genes in Arabidopsis thaliana (L.) Heynh. roots induced by toxic Ni2+ levels and joint application of Ni2+ and L-histidinehttps://orcid.org/0000-0002-5116-0157МацкевичВ. С.MackievicV. S.

Мацкевич Вера Сергеевна – старший преподаватель, науч. сотрудник.

пр. Независимости, 4, 220030, Минск

Viera S. Mackievic – Senior Lecturer, Researcher, Belarusian State University.

4, Nezavisimosti Ave., 220030, Minsk

mackievic@bsu.byhttps://orcid.org/0000-0003-3765-8386ДемидчикВ. В.DemidchikV. V.

Демидчик Вадим Викторович – член-корреспондент, д-р биол. наук, профессор, гл. науч. сотрудник.

ул. Академическая, 27, 220072, Минск

Vadim V. Demidchik – Corresponding Member, D. Sc. (Biol.), Professor, Chief Researcher, V.F. Kuprevich Institute of Experimental Botany of the National Academy of Sciences of Belarus.

27, Akademicheskaya Str., 220072, Minsk

demidchik@botany.byБелорусский государственный университетBelarusian State UniversityИнститут экспериментальной ботаники имени В.Ф. Купревича Национальной академии наук БеларусиV.F. Kuprevich Institute of Experimental Botany of the National Academy of Sciences of Belarus202507112025704304315Copyright © Мацкевич В.С., Демидчик В.В., 20252025Мацкевич В.С., Демидчик В.В.Mackievic V.S., Demidchik V.V.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://vestibio.belnauka.by/jour/article/view/987

Никель является для высших растений эссенциальным трэйс-элементом, входящим в состав уреазы, глиоксилаз и ряда гидрогеназ. Однако в высоких концентрациях данный металл подавляет рост и развитие растений. Токсичные для растений уровни Ni2+ (>10–5 М) характерны для почв, сформированных из вулканических пород, вблизи горнодобывающих и металлургических комбинатов, свалок, мест захоронения отходов. Повышенное содержание уровня никеля в почвах зарегистрировано и на некоторых территориях Беларуси. В представленной работе исследовано воздействие диапазона токсических концентраций Ni2+ (0,3–2 ммоль/л NiCl2) на экспрессию ряда важнейших генов стрессового ответа у модельных растений Arabidopsis thaliana (L.) Heynh., а также влияние на этот процесс природного защитного агента растений – L-гистидина (Гис), усиленно синтезируемого растениями при никелевом стрессе и способного связывать Ni2+. В ходе проведенных опытов с использованием метода полимеразной цепной реакции в реальном времени (ПЦР-РВ) было обнаружено, что введение Ni2+ в культивационную среду вызывало дозозависимое увеличение относительной экспрессии генов, кодирующих глутатионредуктазу (GR1), НАДФН-оксидазу (RBOHC), Са2+-зависимую протеинкиназу (CPK6), каталазу (CAT2) и наружу-выпрямляющий К+-канал (GORK1). Максимальное увеличение наблюдалось при обработке 2 ммоль/л Ni2+ и составляло 5,9; 5,0; 3,0; 2,8 и 2,2 раза для транскриптов RBOHC, GR1, CPK6, CAT2 и GORK1 соответственно. В случае генов поли(АДФ-рибоза)-полимеразы (PARP1), циклина В2 (CYCB2) и Cu/Zn-супероксиддисмутазы (CSD2) уровень транскриптов возрастал при низких уровнях Ni2+, а затем снижался при его более высоких уровнях в среде. Введение Гис совместно с Ni2+ предотвращало Ni2+-индуцированное изменение экспрессии генов. Таким образом, в работе продемонстрировано, что растения A. thaliana отвечают на избыток Ni2+ индукцией экспрессии ферментативных антиоксидантов, белков редокс- и Са2+-опосредуемой клеточной сигнализации, а также модификацией систем контроля деления и репликации ДНК; данный эффект находится под контролем экзогенного Гис.

Nickel (Ni) is an essential trace element for higher plants, being a part of urease, glyoxylases and hydrogenases. However, in high concentrations, this metal exerts a pronounced toxic effect. Levels of Ni2+ that are toxic to plants (>10–5 M) are typical for soils formed from volcanic rocks, near mining and metallurgical plants, landfills, waste disposal sites. Elevated nickel levels are also recorded in the soils of Belarus. In the presented work, we examined the effect of a range of toxic Ni2+ concentrations (0.3–2 mM NiCl2) on the expression of a number of important stress response genes in model plants Arabidopsis thaliana (L.) Heynh., as well as the effect of a natural plant protective agent, L-histidine (His), which is intensively synthesized by plants under nickel stress and is able to bind Ni2+, on this process. In the experiments conducted using the Real-Time Polymerase Chain Reaction (RT-PCR) method, it was found that the introduction of Ni2+ into the culture medium caused a dose-dependent increase in the relative expression of genes encoding glutathione reductase (GR1), NADPH oxidase (RBOHC), Ca2+-dependent protein kinase (CPK6), catalase (CAT2) and outward-rectifying K+ channel (GORK1). The maximum increase was observed upon treatment with 2 mM Ni2+, relative transcript levels were 5.9, 5.0, 3.0, 2.8 and 2.2 times higher than in control for RBOHC, GR1, CPK6, CAT2 and GORK1 respectively. In the case of the genes encoding poly(ADP-ribose)-polymerase (PARP1), cyclin B2 (CYCB2), and Cu/Zn-superoxide dismutase (CSD2), the transcript levels increased at low Ni2+ concentrations and then decreased at higher Ni2+ concentrations in the medium. The introduction of His, in conjunction with Ni2+, prevented the Ni2+-induced change in gene expression. Thus, it was demonstrated that A. thaliana plants respond to excess Ni2+ by inducing the expression of enzymatic antioxidants, proteins involved in redox- and Ca2+-mediated cellular signaling. This response is accompanied by alterations in the systems of control cell division and DNA replication, which can be regulated by exogenous His.

тяжелые металлыникельфизиология стрессаL-гистидинактивные формы кислородакальциевая сигнализацияредокс-регуляцияэкспрессия геновArabidopsis thalianaheavy metalsnickelstress physiologyL-histidinereactive oxygen speciescalcium signalingredox regulationgene expressionArabidopsis thalianaРабота была выполнена в рамках заданий БРФФИ (№ Б25КИ-086 «Установление механизмов снижения токсичности тяжелых металлов в высших растениях под действием квантовых точек, содержащих микроэлементы» (совместно с КНР) и Б24-060-1 «Роль транспортеров малата в устойчивости высших растений к высоким уровням тяжелых металлов и алюминия в среде»); ГПНИ «Исследование мембранных механизмов модификации ростовых, сигнальных и транспортных процессов в клетках корня при взаимодействии высших растений с редокс-активными тяжелыми металлами» (№ госрегистрации 20241163); подпрограммы «Молекулярные и клеточные биотехнологии-2» государственной программы научных исследований «Биотехнологии-2» на 2021–2025 гг., а также гранта Европейского Союза «Адаптация растений к тяжелым металлам и радиоактивному загрязнению» (PIRSES-GA-2013-612587).This work was supported by projects of the BRFFR (No. B25KI-086 “Establishment of mechanisms for reducing the toxicity of heavy metals in higher plants under the influence of quantum dots containing trace elements” (joint with China) and B24-060-1 “The role of malate transporters in the resistance of higher plants to high levels of heavy metals and aluminum in the environment”), and also supported by the State Scientific Research Institute “Study of membrane mechanisms of modification of growth, signaling and transport processes in root cells during interaction of higher plants with redox-active heavy metals” (state registration No. 20241163), subprogram “Molecular and Cellular Biotechnologies 2” of the state research program “Biotechnologies 2” for 2021–2025. This work was also supported by the grant EU PIRSES-GA-2013-612587 (“Plant DNA tolerance – Plant adaptation to heavy metal and radioactive pollution”).ReferencesBergmann, W. Nutritional Disorders of Plants: Development, Visual and Analytical Diagnosis / W. Bergman. – Stuttgart: Gustav Fischer Verlag, 1992. – 741 p.Bergmann W. Nutritional Disorders of Plants: Development, Visual and Analytical Diagnosis. Stuttgart, Gustav Fischer Verlag, 1992. 741 p.Nagajyoti, P. C. Heavy metals, occurrence and toxicity for plants: a review / P. C. Nagajyoti, K. D. Lee, T. V. M. Sreekanth // Environmental Chemistry Letters. – 2010. – Vol. 8, N 3. – P. 199–216. https://doi.org/10.1007/s10311-010-0297-8Nagajyoti P. C., Lee K. D., Sreekanth T. V. M. Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters, 2010, vol. 8, no. 3, pp. 199–216. http://doi.org/10.1007/s10311-010-0297-8Barker, A. V. Handbook of Plant Nutrition / A. V. Barker, D. J. Pilbeam. – 2nd ed. – Boca Raton: CRC Press, 2015. – 773 p.Barker A. V., Pilbeam D. J. Handbook of Plant Nutrition. 2nd ed. Boca Raton, CRC Press, 2015. 773 p.Nickel; whether toxic or essential for plants and environment – A review / B. Shahzad, M. Tanveer, A. Rehman [et al.] // Plant Physiology and Biochemistry. – 2018. – Vol. 132. – P. 641–651. https://doi.org/10.1016/j.plaphy.2018.10.014Shahzad B., Tanveer M., Rehman A., Cheema S. A., Fahad S., Rehman S., Sharma A. Nickel; whether toxic or essential for plants and environment – A review. Plant Physiology and Biochemistry, 2018, vol. 132, pp. 641–651. https://doi.org/10.1016/j.plaphy.2018.10.014Dalir, N. Root uptake and translocation of nickel in wheat as affected by histidine / N. Dalir, A. H. Khoshgoftarmanesh // Journal of Plant Physiology. – 2015. – Vol. 184. – P. 8–14. https://doi.org/10.1016/j.jplph.2015.05.017Dalir N., Khoshgoftarmanesh A. H. Root uptake and translocation of nickel in wheat as affected by histidine. Journal of Plant Physiology, 2015, vol. 184, pp. 8–14. https://doi.org/10.1016/j.jplph.2015.05.017Мацкевич, В. С. Механизм трансмембранного и дальнего транспорта никеля в высших растениях / В. С. Мацкевич, В. В. Демидчик // Экспериментальная биология и биотехнология. – 2023. – № 2. – С. 4–29.Matskevich V. S., Demidchik V. V. Mechanism of transmembrane and long-distance transport of nickel in higher plants. Eksperimental’naya biologiya i biotekhnologiya [Experimental Biology and Biotechnology], 2023, no. 2, pp. 4–29 (in Russian).Welch, R. M. Breeding for micronutrients in staple food crops from a human nutrition perspective / R. M. Welch, R. D. Graham // Journal of Experimental Botany. – 2004. – Vol. 55, N 396. – P. 353–364. https://doi.org/10.1093/jxb/erh064Welch R. M., Graham R. D. Breeding for micronutrients in staple food crops from a human nutrition perspective. Journal of Experimental Botany, 2004, vol. 55, no. 396, pp. 353–364. https://doi.org/10.1093/jxb/erh064Состояние природной среды Беларуси: экологич. бюл. / Е. И. Громадская, Д. В. Цубленок, М. В. Водейко [и др.]; под общ. ред. Е. И. Громадской. – Мн.: РУП «ЦНИИКИВР», 2024. – 196 с.Gromadskaya E. I., Tsublenok D. V., Vodeiko M. V., Buko I. Yu., Khomich V. S., Zhivnach S. G., Struk M. I. State of the natural environment of Belarus: ecological bulletin. Minsk, RUE “TsNIIKIVR”, 2024. 196 p. (in Russian).Состояние природной среды Беларуси: экол. бюл. 2013 г. / под ред. В. Ф. Логинова. – Мн.: Ин-т природопользования Нац. акад. наук Беларуси, 2014. – 361 с.Loginov V. F. (ed.). State of the natural environment of Belarus: ecological bulletin. 2013. Minsk, Institute of Nature Management of the National Academy of Sciences of Belarus, 2014. 361 p. (in Russian).Толкач, Г. В. Содержание химических элементов в почвах на территории фермерских (крестьянских) хозяйств Брестского района / Г. В. Толкач, С. С. Позняк // Экологический вестник. – 2015. – № 3. – С. 79–88.Tolkach G. V., Poznyak S. S. Contents of chemical elements in soil in the farms of Brest region. Ekologicheskii vestnik [Ecological Bulletin], 2015, no. 3, pp. 79–88 (in Russian).Состояние природной среды Беларуси: экол. бюл. / Е. И. Громадская, Д. В. Цубленок, М. В. Водейко [и др.]; под общ. ред. Е. И. Громадской. – Мн.: ЦНИИКИВР, 2023. – 151 с.Gromadskaya E. I., Tsublenok D. V., Vodeiko M. V., Khomich V. S., Zhivnach S. G., Struk M. I. State of the natural environment of Belarus: ecological bulletin. Minsk, Central research institute for integrated use of water resources, 2023. 151 p. (in Russian).Национальная система мониторинга окружающей среды в Республике Беларусь: результаты наблюдений, 2021 год / под общ. ред. М. И. Лемутовой. – Мн.: Респ. центр по гидрометеорологии, контролю радиоактив. загрязнения и мониторингу окружающей среды, 2022. – 556 с.Lemutova M. I. (ed.). National environmental monitoring system in the Republic of Belarus: observation results, 2021. Minsk, Belhydromet, 2022. 556 p. (in Russian).Marschner, H. Mineral Nutrition of Higher Plants. / H. Marschner; ed. P. Marschner. – 3rd ed. – London: Academic Press, 2012. – 684 p.Marschner H. Mineral nutrition of higher plants. 3rd ed. London, Academic Press, 2012. 684 p.Alfalahi, A. O. Nanonutrients: Plant Nutritive and Possible Antioxidant Regulators / A. O. Alfalahi, F. W. Abdulqahar // Nanobiotechnology / eds.: J. M. Al-Khayri, M. I. Ansari, A. K. Singh. – Cham, 2021. – Ch. 21. – P. 471–498. https://doi.org/10.1007/978-3-030-73606-4_21Alfalahi A. O., Abdulqahar F. W. Nanonutrients: Plant Nutritive and Possible Antioxidant Regulators. Nanobiotechnology, Cham, 2021, ch. 21, pp. 471–498. https://doi.org/10.1007/978-3-030-73606-4_21Hanikenne, M. Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics / M. Hanikenne, C. Nouet // Current Opinion in Plant Biology. – 2011. – Vol. 14, N 3. – P. 252–259. https://doi.org/10.1016/j.pbi.2011.04.003Hanikenne M., Nouet C. Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Current Opinion in Plant Biology, 2011, vol. 14, no. 3, pp. 252–259. https://doi.org/10.1016/j.pbi.2011.04.003Nickel in Soils and Plants / eds.: C. Tsadilas, J. Rinklebe, M. Selim. – Boca Raton: CRC Press, 2018. – 432 p.Tsadilas C., Rinklebe J., Selim M. (eds.). Nickel in Soils and Plants. Boca Raton, CRC Press, 2018. 432 p. https://doi.org/10.1201/9781315154664Ингибирование ростовых процессов и индукция запрограммированной клеточной гибели в корне Helianthus annuus L. под действием ионов никеля и никель-гистидиновых комплексов / В. С. Мацкевич, А. А. Шикер, С. Н. Звонарев [и др.] // Журнал Белорусского государственного университета. Биология. – 2020. – № 1. – С. 11–19.Matskevich V. S., Shiker A. A., Zvonarev S. N., Litskevich K. S., Turovets O. A., Smolich, I. I., Sokolik A. I., Demidchik V. V. Growth inhibition and induction of programmed cell death in the root of Helianthus annuus L. triggered by nickel ions and nickel-histidine complexes. Zhurnal Belorusskogo gosudarstvennogo universiteta. Biologiya [Journal of the Belarusian State University. Biology], 2020, no. 1, pp. 11–19 (in Russian).L-histidine makes Ni2+ ‘visible’ for plant signalling systems: Shading the light on Ni2+-induced Ca2+ and redox signalling in plants / V. Mackievic, Y. Li, P. Hryvusevich [et al.] // Plant Physiology and Biochemistry. – 2025. – Vol. 220. – Art. 109227. https://doi.org/10.1016/j.plaphy.2024.109227Mackievic V., Li Y., Hryvusevich P., Svistunenko D., Seregin I., Kozhevnikova A., Kartashov A. [et al.]. L-histidine makes Ni2+ ‘visible’ for plant signalling systems: Shading the light on Ni2+-induced Ca2+ and redox signalling in plants. Plant Physiology and Biochemistry, 2025, vol. 220, art. 109227. https://doi.org/10.1016/j.plaphy.2024.109227Physiological, biochemical and transcriptomic responses of Medicago sativa to nickel exposure / S. Helaoui, I. Boughattas, S. Hattab [et al.] // Chemosphere. – 2020. – Vol. 249. – Art. 126121. https://doi.org/10.1016/j.chemosphere.2020.126121Helaoui S., Boughattas I., Hattab S., Mkhinini M., Alphonse V., Livet A., Bousserrhine N., Banni M. Physiological, biochemical and transcriptomic responses of Medicago sativa to nickel exposure. Chemosphere, 2020, vol. 249, art. 126121. https://doi.org/10.1016/j.chemosphere.2020.126121Transient influx of nickel in root mitochondria modulates organic acid and reactive oxygen species production in nickel hyperaccumulator Alyssum murale / B. Agrawal, K. J. Czymmek, D. L. Sparks, H. P. Bais // Journal of Biological Chemistry. – 2013. – Vol. 288, N 10. – P. 7351‒7362. https://doi.org/10.1074/jbc.m112.406645Agrawal B., Czymmek K. J., Sparks D. L., Bais H. P. Transient Influx of Nickel in Root Mitochondria Modulates Organic Acid and Reactive Oxygen Species Production in Nickel Hyperaccumulator Alyssum murale. Journal of Biological Chemistry, 2013, vol. 288, no. 10, pp. 7351‒7362. https://doi.org/10.1074/jbc.M112.406645Yemets, A. Cadmium, nickel, copper, and zinc influence on microfilament organization in Arabidopsis root cells / A. Yemets, I. Horiunova, Y. Blume // Cell Biology International. – 2021. – Vol. 45, N 1. – P. 211–226. https://doi.org/10.1002/cbin.11485Yemets A., Horiunova I., Blume Y. Cadmium, nickel, copper, and zinc influence on microfilament organization in Arabidopsis root cells. Cell Biology International, 2021, vol. 45, no, 1, pp. 211‒226. https://doi.org/10.1002/cbin.11485Nickel Toxicity Targets Cell Wall-Related Processes and PIN2-Mediated Auxin Transport to Inhibit Root Elongation and Gravitropic Responses in Arabidopsis / A. Lešková, M. Zvarík, T. Araya, R. F. H. Giehl // Plant Cell Physiology. – 2020. – Vol. 61, N 3. – Р. 519–535. https://doi.org/10.1093/pcp/pcz217Lešková A., Zvarík M., Araya T., Giehl R. F. H. Nickel Toxicity Targets Cell Wall-Related Processes and PIN2-Mediated Auxin Transport to Inhibit Root Elongation and Gravitropic Responses in Arabidopsis. Plant Cell Physiology, 2020, vol. 61, no. 3, pp. 519‒535. https://doi.org/10.1093/pcp/pcz217Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis / T. Czechowski, M. Stitt, T. Altmann [et al.] // Plant Physiology. – 2005. – Vol. 139, N 1. – Р. 5–17. https://doi.org/10.1104/pp.105.063743Czechowski T., Stitt M., Altmann T., Udvardi M. K., Scheible W. R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology, 2005, vol. 139, no. 1, pp. 5‒17. https://doi.org/10.1104/pp.105.063743The combined effect of uranium and gamma radiation on biological responses and oxidative stress induced in Arabidopsis thaliana / N. Vanhoudt, H. Vandenhove, N. Horemans [et al.] // Journal of Environmental Radioactivity. – 2010. – Vol. 101, N 11. – Р. 923–930. https://doi.org/10.1016/j.jenvrad.2010.06.008Vanhoudt N., Vandenhove H., Horemans N., Wannijn J., Van Hees M., Vangronsveld J., Cuypers A. The combined effect of uranium and gamma radiation on biological responses and oxidative stress induced in Arabidopsis thaliana. Journal of Environmental Radioactivity, 2010, vol. 101, no. 11, pp. 923–30. https://doi.org/10.1016/j.jenvrad.2010.06.008Differential innate immune signalling via Ca2+ sensor protein kinases / M. Boudsocq, M. R. Willmann, M. McCormack [et al.] // Nature. – 2010. – Vol. 464, N 7287. – Р. 418–422. https://doi.org/10.1038/nature08794Boudsocq M., Willmann M. R., McCormack M., Lee H., Shan L., He P., Bush J., Cheng Sh.-H., Sheen J. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature, 2010, vol. 464, no. 7287, pp. 418–22. https://doi.org/10.1038/nature08794Seregin, I. V. Physiological role of nickel and its toxic effects on higher plants / I. V. Seregin, A. D. Kozhevnikova // Russian Journal of Plant Physiology. – 2006. – Vol. 53, N 2. – P. 257–277. https://doi.org/10.1134/s1021443706020178Seregin I. V., Kozhevnikova A. D. Physiological role of nickel and its toxic effects on higher plants. Russian Journal of Plant Physiology, 2006, vol. 53, no. 2, pp. 257–277. https://doi.org/10.1134/S1021443706020178A Comprehensive Review on the Heavy Metal Toxicity and Sequestration in Plants / R. Riyazuddin, N. Nisha, B. Ejaz [et al.] // Biomolecules. – 2022. – Vol. 12, N 1. – Art. 43. https://doi.org/10.3390/biom12010043Riyazuddin R., Nisha N., Ejaz B., Khan M. I. R., Kumar M., Ramteke P. W., Gupta R. A comprehensive review on the heavy metal toxicity and sequestration in plants. Biomolecules, 2021, vol. 12, no. 1, art. 43. https://doi.org/10.3390/biom12010043Histidine as a metal chelator in plants that accumulate nickel / U. Krämer, J. D. Cotter-Howells, J. M. Charnock [et al.] // Nature. – 1996. – Vol. 379, N 6566. – P. 635‒638. https://doi.org/10.1038/379635a0Krämer U., Cotter-Howells J. D., Charnock J. M., Baker A. J. M., Smith J. A. C. Histidine as a metal chelator in plants that accumulate nickel. Nature, 1996, vol. 379, no. 6566, pp. 635‒638. https://doi.org/10.1038/379635a0Constitutively High Expression of the Histidine Biosynthetic Pathway Contributes to Nickel Tolerance in Hyperaccumulator Plants / R. A. Ingle, S. T. Mugford, J. D. Rees [et al.] // Plant Cell. – 2005. – Vol. 17, N 7. – P. 2089–2106. https://doi.org/10.1105/tpc.104.030577Ingle R. A., Mugford S. T., Rees J. D., Campbell M. M., Smith J. A. C. Constitutively High Expression of the Histidine Biosynthetic Pathway Contributes to Nickel Tolerance in Hyperaccumulator Plants. Plant Cell, 2005, vol. 17, no. 7, pp. 2089‒2106. https://doi.org/10.1105/tpc.104.030577Demidchik, V. Mechanisms of oxidative stress in plants: From classical chemistry to cell biology / V. Demidchik // Environmental and Experimental Botany. – 2015. – Vol. 109. – P. 212–228. https://doi.org/10.1016/j.envexpbot.2014.06.021Demidchic, V. Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environmental and Experimental Botany, 2015, vol. 109, pp. 212-228. https://doi.org/10.1016/j.envexpbot.2014.06.021Reactive oxygen species produced by NADPH oxidase regulate plant cell growth / J. Foreman, V. Demidchik, J. H. F. Bothwell [et al.] // Nature. – 2003. – Vol. 422, N 6930. – P. 442–446. https://doi.org/10.1038/nature01485Foreman J., Demidchik V., Bothwell J. H. F., Mylona P., Miedema H., Torres M. A., Linstead P., Costa S., Brownlee C., Jones J. D. G., Davies J. M., Dolan L. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 2003, vol. 422, no. 6930, pp. 442–446. https://doi.org/10.1038/nature01485Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment / V. Demidchik, D. Straltsova, S. S. Medvedev [et al.] // Journal of Experimental Botany. – 2014. – Vol. 65, N 5. – P. 1259–1270. https://doi.org/10.1093/jxb/eru004Demidchik V., Straltsova D., Medvedev S. S., Pozhvanov G. A., Sokolik A., Yurin V. Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany, 2014, vol. 65, no. 5, pp. 1259–1270. https://doi.org/10.1093/jxb/eru004Arabidopsis calcium-dependent protein kinase CPK6 regulates drought tolerance under high nitrogen by the phosphorylation of NRT1.1 / Q. Ma, Ch. Zhao, Sh. Hu, K. Zuo // Journal of Experimental Botany. – Vol. 74, N 18. – P. 5682–5693. https://doi.org/10.1093/jxb/erad277Ma Q., Zhao Ch., Hu Sh., Zuo K. Arabidopsis calcium-dependent protein kinase CPK6 regulates drought tolerance under high nitrogen by the phosphorylation of NRT1.1. Journal of Experimental Botany, 2023, vol. 74, no. 18, pp. 5682–5693. https://doi.org/10.1093/jxb/erad277Evidence of a significant role of glutathione reductase in the sulfur assimilation pathway / A. Cohen, Y. Hacham, Y. Welfe [et al.] // The Plant Journal. – 2020. – Vol. 102, N 2. – P. 246–261. https://doi.org/10.1111/tpj.14621Cohen A., Hacham Y., Welfe Y., Khatib S., Avice J.-Ch., Amir R. Evidence of a significant role of glutathione reductase in the sulfur assimilation pathway. The Plant Journal, 2020, vol. 102, no. 2, pp. 246–261. https://doi.org/10.1111/tpj.14621Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase / J. Lee, A. Das, M. Yamaguchi [et al.] // The Plant Journal. – 2003. – Vol. 34, N 4. – P. 417–425. https://doi.org/10.1046/j.1365-313x.2003.01736.xLee J., Das A., Yamaguchi M., Hashimoto J., Tsutsumi N., Uchimiya H., Umeda M. Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase. The Plant Journal, 2003, vol. 34, no. 4, pp. 417–425. https://doi.org/10.1046/j.1365-313x.2003.01736.xThe role of NADPH oxidases in regulating leaf gas exchange and ion homeostasis in Arabidopsis plants under cadmium stress / C. Hafsi, A. M. Collado-Arenal, H. Wang [et al.] // Journal of Hazardous Materials. – 2022. – Vol. 429. – Art. 128217. https://doi.org/10.1016/j.jhazmat.2022.128217Hafsi C., Collado-Arenal A. M., Wang H., Sanz-Fernández M., Sahrawy M., Shabala S., Romero-Puertas M. C., Sandalio L. M. The role of NADPH oxidases in regulating leaf gas exchange and ion homeostasis in Arabidopsis plants under cadmium stress. Journal of Hazardous Materials, 2022, vol. 429, art. 128217. https://doi.org/10.1016/j.jhazmat.2022.128217Glutathione Is a Key Player in Metal-Induced Oxidative Stress Defenses / M. Jozefczak, T. Remans, J. Vangronsveld, A. Cuypers // International Journal of Molecular Sciences. – 2012. – Vol. 13, N 3. – P. 3145–3175. https://doi.org/10.3390/ijms13033145Jozefczak M., Remans T., Vangronsveld J., Cuypers A. Glutathione Is a Key Player in Metal-Induced Oxidative Stress Defenses. International Journal of Molecular Sciences, 2012, vol. 13, no. 3, pp. 3145–3175. https://doi.org/10.3390/ijms13033145Arabidopsis GLUTATHIONE REDUCTASE1 Plays a Crucial Role in Leaf Responses to Intracellular Hydrogen Peroxide and in Ensuring Appropriate Gene Expression through Both Salicylic Acid and Jasmonic Acid Signaling Pathways / A. Mhamdi, J. Hager, S. Chaouch [et al.] // Plant Physiology. – 2010. – Vol. 153, N 3. – P. 1144–1160. https://doi.org/10.1104/pp.110.153767Mhamdi A., Hager J., Chaouch S., Queval G., Han Y., Taconnat L., Saindrenan P., Gouia H., Issakidis-Bourguet E., Renou J. P., Noctor G. Arabidopsis GLUTATHIONE REDUCTASE1 Plays a Crucial Role in Leaf Responses to Intracellular Hydrogen Peroxide and in Ensuring Appropriate Gene Expression through Both Salicylic Acid and Jasmonic Acid Signaling Pathways. Plant Physiology, 2010, vol. 153, no. 3, pp. 1144–1160. https://doi.org/10.1104/pp.110.153767Grill, E. Phytochelatins: The Principal Heavy-Metal Complexing Peptides of Higher Plants / E. Grill, E.-L. Winnacker, M. H. Zenk // Science. – 1985. – Vol. 230, N 4726. – P. 674–676. https://doi.org/10.1126/science.230.4726.674Grill E., Winnacker E.-L., Zenk M. H. Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science, 1985, vol. 230, no. 4726, pp. 674–676. https://doi.org/10.1126/science.230.4726.674Chen, J. Characterization of phytochelatin synthase from tomato / J. Chen, J. Zhou, P. B. Goldsbrough // Physiologia Plantarum. – 1997. – Vol. 101, N 1. – P. 165–172. https://doi.org/10.1111/j.1399-3054.1997.tb01833.xChen J., Zhou J., Goldsbrough P. B. Characterization of phytochelatin synthase from tomato. Physiologia Plantarum, 1997, vol. 101, no. 1, pp. 165–172. https://doi.org/10.1111/j.1399-3054.1997.tb01833.x

The authors declare that there are no conflicts of interest present.