Oxidative stress in moss Bryum caespiticium (Bryaceae) under the influence of high temperature and light intensity in a technogenically transformed environment
AbstractMosses are pioneer plants in post-technogenic areas. Therefore, the question of adaptive reactions of mosses from these habitats represents a scientific interest. The research is devoted to the study of adaptive changes in the metabolism of the dominant moss species Bryum caespiticium Hedw., collected in the devastated territories of the Novoyavorivsk State Mining and Chemical Enterprise (SMCE) “Sirka (Sulfur)” exposed to hyperthermia and insolation, which cause oxidative stress in plants. The influence of these stressors on the activity and thermal stability of antioxidant enzymes, hydrogen peroxide content, anion radical generation and accumulation of prooxidant components in moss shoots was studied. The activity and thermal stability of peroxidase and superoxide dismutase (SOD) were analysed forB. caespiticium moss from different locations of northern exposure at the sulfur mining dump No 1 in summer and autumn. We established the dependence of the activity of antioxidant enzymes of moss on the intensity of light and temperature on the experimental plots of the dump No 1. In summer, the highest activity and thermal stability rates of peroxidase and SOD were observed. Under the conditions of the experiment in shoots of В. caespiticium from the northern peak of the dump under the influence of 2 hours temperature action (+ 42 ºС) the most significant increase in peroxidase activity was found by 1.78 times and SOD by 1.89 times, as well as increase in its thermal stability by 1.35–1.42 times, respectively. The increase in peroxidase and SOD activity, as well as the increase in their thermal stability caused by hyperthermia were negated by pre-processing with a protein biosynthesis inhibitor cyclohexamide, which may indicate the participation of the protein-synthesizing system in this process. The effect of increasing the thermal stability of enzymes can be considered as a mechanism of adaptation of the protein-synthesizing system to the action of high temperatures. Increase in the activity and thermal stability of antioxidant enzymes is caused primarily by changes in the expression of stress protein genes, which control the synthesis of specific adaptogens and protectors. The obtained results indicate that the extreme conditions of the anthropogenically transformed environment contribute to the development of forms with the highest potential abilities. The mechanism of action of high temperatures is associated with the development of oxidative stress, which is manifested in the intensification of lipid peroxidation and the generation of superoxide anion radical. It was found that temperature stress and high insolation caused an increased generation of superoxide anion radical as the main inducers of protective reactions in the samples of B. caespiticium from the experimental transect of the sulfur mining heap. It is known that the synthesis of Н2О2 occurs under stress and is a signal to start a number of molecular, biochemical and physiological processes of cells, including adaptation of plants to extreme temperatures. It is shown that high temperatures initiate the generation of hydrogen peroxide. Increased reactive oxygen species (ROS) formation, including Н2О2, under the action of extreme temperatures, can cause the activation of signaling systems. Therefore, the increase in the content of Н2О2 as a signaling mediator is a component of the antioxidant protection system. It is determined that adaptive restructuring of the metabolism of the moss В. caespiticium is associated with the accumulation of signaling prooxidant components (diene and triene conjugates and dienketones). The increase in primary lipid peroxidation products, detected by us, under the action of hyperthermia may indicate the intensification of free radical oxidation under adverse climatic conditions in the area of the sulfur production dump, which leads to the intensification of lipid peroxidation processes. The accumulation of radical and molecular lipid peroxidation products are signals for the activation of protective systems, activators of gene expression and processes that lead to increased resistance of plants.
Aleksandrov, V. Y. (1985). Reaktivnost’ kletok i belki [Cell reactivity and proteins]. Nauka, Leningrad (in Russian).
Alvarez, S., & Sanchez-Blanco, M. J. (2014). Long-term effect of salinity on plant quality, water relations, photosynthetic parameters and ion distribution in Callistemon citrinus. Plant Biology, 16, 757–764.
Apel, K., & Hirt, H. (2004). Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. The Annual Review of Plant Biology, 55, 373–399.
Ayala, A., Muñoz, M. F., & Argüelles, S. (2014). Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity, 360, 438.
Boychuk, M. A. (2021). Mosses (Bryophyta) of the Kostomuksha State Nature Reserve, Russia. Nature Conservation Research, 6(Suppl.1), 89–97.
Cavalcanti, F. R., Oliveira, J. T. A., Martins-Miranda, A. S., Viégas, R. A., & Silveira, J. A. G. (2004). Superoxide dismutase, catalase and peroxidase activities do not confer protection against oxidative damage in salt-stressed cowpea leaves. New Phytologist, 163, 563–571.
Chevari, S., Andyal, T., & Shtrenger, Y. (1991). Opredeleniye antioksidantnikh parametrov krovi i ikh diagnosticheskoye znacheniye v pozhilom vozdaste [Determination of antioxidant blood parameters and their diagnostic value in elderly patients]. Laboratornoe Delo, 18(2), 9–13 (in Russian).
Choudhury, F. K., Rivero, R. M., Blumwald, E., & Mittler, R. (2017). Reactive oxygen species, abiotic stress and stress combination. The Plant Journal, 90(5), 856–867.
Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Irize, D., & Van Breusegem, F. (2000). Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences, 57(5), 779–795.
Demidchik, V. (2015). Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environmental and Experimental Botany, 109, 212–228.
Dey, A., & De, J. N. (2012). Antioxidative potential of Bryophytes: Stress tolerance and commercial perspectives: A review. Pharmacologia, 3(6), 151–159.
Di cyclohexamidelo, L., Lambardi, M., & Pazzagli, L. (1999). Response to cadmium in carrot in vitro plants and cell suspension cultures. Plant Science, 137, 119–129.
Dubinina, E. E. (2001). Rol’ aktivnykh form kisloroda v kachestve signal’nykh molekul v metabolizme tkaney pri sostoyaniyakh okislitel’nogo stressa [The role of reactive oxygen species as signaling molecules in tissue metabolism under oxidative stress conditions]. Problems of Medicinal Chemistry, 47(6), 561–581 (in Russian).
Durand, E., Zhao, Y., Ruesgas-Ramón, M., Cruz Figueroa-Espinoza, M., Lamy, S., Coupland, J. N., Elias, R. J., & Villeneuve, P. (2019). Evaluation of antioxidant activity and interaction with radical species using the vesicle conjugated autoxidizable triene (VesiCAT). European Journal of Lipid Science and Technology, 121(5), 180–199.
Ermakov, A. I., Arasimovich, V. V., & Yarosh, N. P. (1987). Metody biokhimicheskogo issledovaniya rasteniy [Methods of biochemical research of plants]. Agropromizdat, Leningrad (in Russian).
Fan, X. W., Li, F. M., Song, L., Xiong, Y. C., An, L. Z., Jia, Y., & Fang, X. W. (2009). Defense strategy of old and modern spring wheat varieties during soil drying. Physiologia Plantarum, 136, 310–323.
Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909–930.
Grishutkin, O. G., Boychuk, M. A., Grishutkina, G. A., & Rukavishnikova, V. V. (2020). Check-list and ecology of Sphagnum mosses (Sphagnaceae) in the Republic of Mordovia (Russia). Nature Conservation Research, 5(3), 114–133.
Guan, L. M., & Scandalios, J. G. (2000). Hydrogen-peroxide-mediated catalase gene expression in response to wounding. Free Radical Biology and Medicine, 28(8), 1182–1190.
Gupta, K. J., & Igamberdiev, A. U. (2015). Compartmentalization of reactive oxygen species and nitric oxide production in plant cells: An overview. In: Gupta, K. J., & Igamberdiev, A. U. (Eds.). Reactive oxygen and nitrogen species signaling and communication in plants, signaling and communication in plants. Springer, Heidelberg, New York, Dordrecht, London. Pp. 1–14.
Hasanuzzaman, M., Borhannuddin Bhuyan, M. H. M., Zulfiqar, F., Raza, A., Mohsin, M. S., Mahmud, J. A., Fujita, M., & Fotopoulos, V. (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants, 9, 681.
Helena, M., & Carvalho, C. (2008). Drought stress and reactive oxygen species. Production, scavenging and signaling. Plant Signaling and Behavior, 3, 156–165.
Jiang, M., & Zhang, J. (2002). Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. The Journal of Experimental Botany, 53, 2401–2410.
Kacperska, A. (2004). Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: Do they depend on stress intensity? Physiologia Plantarum, 122(2), 159−168.
Karpets, Y. V. (2019). Donors of nitric oxide and their application for increase in plants resistance to action of abiotic stressors. The Bulletin of Kharkiv National Agrarian University, Series Biology, 48, 28–51.
Karpets, Y. V., & Kolupaev, Y. E. (2009). Otvet rastenyya na hypertermyyu: Molekulyarno-kletochnye protsessy [Plant response to hyperthermia: Molecular and cellular processes]. The Bulletin of Kharkiv National Agrarian University, Biological Series, 1, 19–39 (in Russian).
Karpets, Y. V., Kolupaev, Y. E., & Vayner, A. A. (2015a). Functional interaction between nitric oxide and hydrogen peroxide during formation of wheat seedling induced heat resistance. Russian Journal of Plant Physiology, 62(1), 65–70.
Karpets, Y. V., Kolupaev, Y. E., Grigorenko, D. O., & Firsova, K. M. (2016). Reaktsiya rasteniy yachmenya razlichnykh genotipov na pochvennuyu zasukhu i deystviye donora oksida azota [Response of barley plants of various genotypes to soil drought and influence of nitric oxide donor]. The Bulletin of Kharkiv National Agrarian University, Series Biology, 38, 94–105 (in Russian).
Karpets, Y. V., Kolupaev, Y. E., Yastreb, T. O., & Lugova, G. A. (2017). Activity of antioxidant enzymes in leaves of barley plants of various genotypes under influence of soil drought and sodium nitroprusside. Plant Physiology and Genetics, 49(1), 71–81.
Karpets, Y. V., Kolupaev, Y. E., Yastreb, T. O., & Oboznyi, A. I. (2015b). Effects of NO-status modification, heat hardening, and hydrogen peroxide on the activity of antioxidant enzymes in wheat seedlings. Russian Journal of Plant Physiology, 62(3), 292–298.
Khan, M. N., Mobin, M., & Abbas, Z. K. (2015). Nitric oxide and high temperature stress: A physiological perspective. In: Khan, M. N. (Ed.). Nitric oxide action in abiotic stress responses in plants. Springer, Heidelberg, New York, Dordrecht, London, 7, 77–94.
Khan, T. A., Fariduddin, Q., & Yusuf, M. (2017). Low-temperature stress: Is phytohormones application a remedy? Environmental Science and Pollution Research, 24(27), 21574–21590.
Khorkavtsiv, Y. D., Ripetskyj, R. T., & Baik, O. L. (2009). Phenotypic and epigenetic adaptation of the moss clone to mercury. Cytology and Genetics, 43(5), 311–315.
Khorobrykh, A. (2019). Hydrogen peroxide and superoxide anion radical photoproduction in PSII preparations at various modifications of the water-oxidizing complex. Plants, 8(9), 329.
Kimura, M., Umemoto, Y., & Kawano, T. (2014). Hydrogen peroxide-independent generation of superoxide by plant peroxidase: Hypotheses and supportive data employing ferrous ion as a model stimulus. Frontiers in Plant Science, 5, 285.
Kimura, S., Waszczak, C., Hunter, K., & Wrzaczek, M. (2017). Bound by fate: The role of reactive oxygen species in receptor-like kinase signaling. Plant Cell, 29, 638–654.
Kolupaev, Y. E. (2016). Antioksidanty rastitelnoy kletki, ikh rol v AFK-signalinge i ustoychivosti rasteniy [Plant cell antioxidants and their role in ROS signaling and plant resistance]. Uspekhi Sovremennoy Biologii, 136(2), 181–198 (in Russian).
Kolupaev, Y. E., & Karpets, Y. V. (2009). Aktivnyye formy kisloroda pri adaptatsii rasteniy k stressovym temperaturam [Reactive oxygen species during plant adaptation to stress temperatures]. Fiziologiya i Biokhimiya Kulturnykh Rasteniy, 41(2), 95–108 (in Russian).
Kolupaev, Y. E., & Karpets, Y. V. (2010). Formirovaniye adaptativnykh reaktsiy rasteniy na deystviye abioticheskikh stressorov [Formation of adaptive responses of plants to the action of abiotic stressors]. Osnova, Kiev (in Russian).
Kolupaev, Y. E., & Obozny, A. I. (2013). Aktyvni formy kysnyu i antyoksydantna systema pry perekhresniy adaptatsiyi roslyn do diyi abiotychnykh stresoriv [Reactive forms of oxygen and antioxidant system in cross-adaptation of plants to the action of abiotic stressors]. The Bulletin of Kharkiv National Agrarian University, Series Biology, 30, 18–31 (in Ukrainian).
Kolupaev, Y. E., & Oboznyi, A. I. (2012). Uchastiye aktivnykh form kisloroda v indutsirovanii askorbatperoksidazy i gvayakolperoksidazy pri teplovom zakalivanii prorostkov pshenitsy [Participation of reactive oxygen species in the induction of ascorbate peroxidase and guaiacol peroxidase during heat hardening of wheat seedlings]. The Ukrainian Biochemical Journal, 84(6), 131–138 (in Russian).
Kosakivska, I. B., Yarotska, K. M., Voytenko, L. V., & Babenko, L. M. (2016). Effect of hyperthermia on cytokinin and pigments content of Glycine max (L.) Merr. varieties differed in thermotolerance. Plant Physiology and Genetics, 48(1), 56–64.
Kosakivska, I. V., Voytenko, L. V., & Likhnyovskiy, R. V. (2015). Effect of temperature on Triticum aestivum L. seedlings growth and phytohormone balance. The Journal of Stress Physiology and Biochemistry, 11(4), 91–99.
Kosakivska, I. V., Voytenko, L. V., & Yarotska, K. M. (2017). Effect of hyperthermia on accumulation and localization of abscisic acid in varieties of Glycine max (L.) Merr. differing in resistance to abiotic stressors. The Bulletin of Kharkiv National Agrarian University, Series Biology, 42, 62–71.
Kosakivska, I. V., Voytenko, L. V., Likhnyovskiy, R. V., & Ustinova, A. Y. (2014). Effect of temperature on accumulation of abscisic acid and indole-3-acetic acid in Triticum aesticum L. seedling. Genetics and Plant Physiology, 4, 201–208.
Kurganova, L. N., Veselov, A. P., & Goncharova, T. A. (1997). Perekisnoye okisleniye lipidov i antioksidantnaya sistema zashchity v khloroplastakh gorokha pri teplovom shoke [Lipid peroxidation and antioxidant defense system in pea chloroplasts under heat shock]. Plant Physiology, 44(5), 725–730 (in Russian).
Kusvuran, S., Kiran, S., & Ellialtioglu, S. (2016). Antioxidant enzyme activities and abiotic stress tolerance relationship in vegetable crops. In: Shanker, A., & Shanker, C. (Eds.). Abiotic and biotic stress in plants – Recent advances and future perspectives. IntechOpen, London.
Kyyak, N. Y., & Baik, O. L. (2016). Role of the bryophyte cover in accumulation of organic carbon and biogenic elements in technogenic substrate on the territory of sulfur deposit. Biologichni Studii, 10(3), 48–55.
Kyyak, N. Y., Baik, O. L., & Kit, N. A. (2017). Morfo-fiziolohichna adaptatsiia briofitiv do ekolohichnykh faktoriv na devastovanykh terytoriiakh vydobutku sirky [Morpho-physiological adaptation of bryophytes to environmental factors on the devastated territories of sulphur extraction]. ScienceRise: Biological Science, 5(8), 33–38 (in Ukrainian).
Kyyak, N., & Bunіo, L. (2017). Mekhanizmy prystosuvannia briofitiv do sol’ovogo stresu na terytoriji khvostoskhovyshha Stebnytckogo girnycho-khimichnogo pidpryjemstva “Polimineral” [Mechanisms of adaptation of bryophytes to salt stress on the territory of tailing of Stebnyk Mining and Chemical Enterprise “Polimineral”]. Visnyk of the Lviv University, Series Biology, 76, 87–96 (in Ukrainian).
Legostayeva, T. V., & Volyanyk, K. O. (2017). Dynamika aktyvnosti peroksydazy u lystkakh Ailanthus altissima za aerotekhnohennoho zabrudnennia [Dynamics of peroxidase activity in Ailanthus altissima leaves under aerotechnogenic pollution]. Issues of Steppe Forestry and Forest Land Reclamation, 46, 81–86 (in Ukrainian).
Li, P., Cai, Q., Wang, H., Li, S., Cheng, J., Li, H., Yu, Q., & Wu, S. (2020). Hydrogen peroxide homeostasis provides beneficial micro-environment for SHR-mediated periclinal division in Arabidopsis root. New Phytologist, 228(6), 1926–1938.
Lobachevska, O., Kyjak, N., Khorkavtsiv, O., Dovgalyuk, A., Kit, N., Klyuchivska, O., Stoika, R., Ripetsky, R., & Cove, D. (2005). Influence of metabolic stress on the inheritance of cell determination in the moss, Pottia intermedia. Cell Biology International, 29(3), 181–186.
Lyutova, M. I., & Kamentseva, I. E. (2001). Termoindutsirovannoye uvelicheniye ustoychivosti nitratreduktazy iz list’jev pshenitsy k inaktivirujushchim vozdeystvijam [Thermal-induced increase in the resistance of nitrate reductase from wheat leaves to inactivating influences]. Plant Physiology, 48(1), 100–105 (in Russian).
Miller, G., Shulaev, V., & Mittler, R. (2008). Reactive oxygen signaling and abiotic stress. Physiologia Plantarum, 133(3), 481–492.
Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K., Gollery, M., Shulaev, V., & Breusegem, F. V. (2011). ROS signaling: The new wave? Trends in Plant Science, 16, 300–309.
Moyo, C. E., Beckett, R. P., Trifonova, T. V., & Minibayeva, F. V. (2017). Extracellular redox cyclingand hydroxyl radical production occurs widely in lichenized Ascomycetes. Fungal Biology, 121, 582–588.
Nakamura, A., Ohori, Y., & Watanabe, K. (2000). Peroxidative formation of lipid hydroperoxides in etiolated leaves. Pesticide Biochemistry and Physiology, 66, 206–212.
Neill, S. J., Desikan, R., Clarke, A., Hurst, R. D., & Hancock, J. T. (2002b). Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany, 53(372), 1237–1247.
Neill, S. J., Gould, K. S., & Kilmartin, P. A. (2002c). Antioxidant activities on red versus green leaves in Elatostema rugosum. Plant, Cell and Environment, 25, 539–547.
Neill, S., Desikan, R., & Hancock, J. (2002a). Hydrogen peroxide signaling. Current Opinion in Plant Biology, 5, 388–395.
Noctor, G., Mhamdi, A., & Foyer, C. H. (2016). Oxidative stress and antioxidative systems: Recipes for successful data collection and interpretation. Plant, Cell and Environment, 39, 1140–1160.
Oboznyi, A. I., Kolupaev, E. Y., & Shvidenko, N. V. (2012). Dinamika aktivnosti antioksidantnykh fermentov pri kross-adaptatsii prorostkov pshenitsy k gipertermii i osmoticheskomu shoku [Dynamics of the activity of antioxidant enzymes during cross-adaptation of wheat seedlings to hyperthermia and osmotic shock]. The Bulletin of Kharkiv National Agrarian University, Series Biology, 26, 71–84 (in Russian).
Oboznyi, A. I., Yastreb, T. O., Kolupaev, Y. E., Popov, V. N., & Krivoruchko, R. V. (2010). Vliyaniye kratkovremennogo nagreva na aktivnost’ i termostabil’nost’ rastvorimoy peroksidazy korney pshenitsy raznykh ekotipov [Influence of short-term heating on the activity and thermal stability of soluble peroxidase of wheat roots of different ecotypes]. The Bulletin of Kharkiv National Agrarian University, Series Biology, 20, 61–68 (in Russian).
Onele, A. O., Chasov, A., Viktorova, L., Beckettc, R. P., Trifonova, T., & Minibayeva, F. (2018). Biochemical characterization of peroxidases from the moss Dicranum scoparium. South African Journal of Botany, 119, 132–141.
Pavlovskaya, N. E., & Grinblat, A. I. (2010). Aktivnyye formy kisloroda i apoptoz u pshenitsy i gorokha [Active forms of oxygen and apoptosis in wheat and pea]. Sel’skokhozyaistvennaya Biologiya, 1, 51–55 (in Russian).
Prasad, T. K., Anderson, M. D., & Stewart, C. R. (1994). Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiology, 105, 619–627.
Proctor, M. C., Oliver, M. J., Wood, A. J., Alpert, P., Stark, L. R., Cleavitt, N. L., & Mishler, B. D. (2007). Desiccation-tolerance in bryophytes: A review. Bryologist, 110, 595–621.
Pyatygin, S. S. (2008). Stress u rasteniy: Fiziologicheskiy podkhod [Stress in plants: A physiological approach]. Zhurnal Obshchei Biologii, 69(4), 294–298 (in Russian).
Rampitsch, C., & Srinivasan, M. (2011). The application of proteomics to plant biology: A review. Canadian Journal of Botany, 84(6), 883–892.
Ren, X., Wang, M., Wang, Y., & Huang, A. (2021). Superoxide anion generation response to wound in Arabidopsis hypocotyl cutting. Plant Signaling and Behavior, 16(2), 27–58.
Richards, S., Wilkins, K., Swarbreck, S., Anderson, A., Habib, N., Smith, A., McAinsh, M., & Davies, J. (2015). The hydroxyl radical in plants: From seed to seed. Journal of Experimental Botany, 66(1), 37–46.
Scarpeci, T. E., Zanor, M. I., Carrillo, N., Mueller-Roeber, B., & Valle, E. M. (2008). Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: A focus on rapidly induced genes. Plant Molecular Biology, 66(4), 361–378.
Schmitt, F. J., Renger, G., Friedrich, T., Kreslavski, V. D., Zharmukhamedov, S. K., Los, D. A., Kuznetsov, V. V., & Allakhverdiev, S. I. (2014). Reactive oxygen species: Re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochimica et Biophysica Acta – Bioenergetics, 1837(6), 835–848.
Seel, W. E., Hedry, G. A. F., & Lee, J. A. (1992). Effects of desiccation on some activated oxygen processing enzymes and antioxidants in mosses. Journal of Experimental Botany, 43, 1031–1037.
Shevyakova, N. I., Bakulina, Y. A., & Kuznetsov, V. V. (2009). Antioksidantnaya rol’ prolina u galofita khrustal’noy travki pri deystvii zasoleniya i parakvata, indutsiruyushchikh okislitel’nyy stress [Antioxidant role of proline in halophyte of crystal grass under the action of salinity and paraquat, inducing oxidative stress]. Plant Physiology, 56, 736–742 (in Russian).
Sidana, S., Bose, J., Shabala, L., & Shabala, S. (2015). Nitric oxide in drought stress signalling and tolerance in plants. In: Khan, M. N. (Ed.). Nitric oxide action in abiotic stress responses in plants. Springer, Heidelberg, New York, Dordrecht, London. Pp. 95–114.
Siddiqui, M. H., Al-Whaibi, M. H., & Basalah, M. O. (2011). Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma, 248, 447–455.
Smirnoff, N. (2005). Ascorbate, tocopherol and carotenoids: Metabolism, pathway engineering and functions. In: Smirnoff, N. (Ed.). Antioxidants and reactive oxygen species in plants. Blackwell Publishing Ltd., Oxford. Pp. 53–86.
Smirnoff, N., & Arnaud, D. (2019). Hydrogen peroxide metabolism and functions in plants. New Phytologist, 221, 1197–1214.
Sofo, A., Scopa, A., Nuzzaci, M., & Vitti, A. (2015). Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences, 16, 13561–13578.
Song, J., Wu, W., & Hu, B. (2020). Light and temperature receptors and their convergence in plants. Biologia Plantarum, 64, 159–166.
Sung, D.-Y., Kaplan, F., Lee, K.-J., & Guy, C. L. (2003). Acquired tolerance to temperature extremes. Trends in Plant Science, 8(4), 179–187.
Thakur, S., & Kapila, S. (2017). Seasonal changes in antioxidant enzymes, polyphenoloxidase enzyme, flavonoids and phenolic content inthree leafy liverworts. Lindbergia, 40(5), 39–44.
Uchida, A., Jagendorf, A. T., Hibino, T., Takabe, T., & Takabe, T. (2002). Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sciences, 163, 515–523.
Wadavkar, D. S., Murumkar, C. V., Deokule, S. S., & Chavan, S. J. (2017). Secondary metabolite and enzyme activity on some moss species from Western Ghats, Maharashtra, India. Bioscience Discovery, 8(4), 716–719.
Wahid, A., & Close, T. J. (2007). Expression of degidrins under heat stress and their relationship with water relations of sugarcane leaves. Biologia Plantarum, 51, 104–109.
Wani, K. I., Naeem, M., Castroverde, C. D. M., Kalaji, H. M., Albaqami, M., & Aftab, T. (2021). Molecular mechanisms of nitric oxide (NO) signaling and reactive oxygen species (ROS) homeostasis during abiotic stresses in plants. International Journal of Molecular Sciences, 22(17), 56–96.
Yurina, N. P., & Odintsova, M. S. (2007). Signal’nyye sistemy rasteniy. Plastidnyje signaly i ikh rol’ v ekspressii yadernykh genov [Plant signaling systems. Plastid signals and their role in the expression of nuclear genes]. Plant Physiology, 54(4), 485–498 (in Russian).
Zhang, X., Zhao, Y., & Wang, S. (2017). Responses of antioxidant defense system of epilithic mosses to drought stress in karst rock desertified areas. The Acta Geochimica, 36(2), 205–212.
Zyn, A. (2012). Prooksudantno-antuoksudantnuj homeostas i membrannuj transport u zuvuh organizmah [Prooxidant and antioxidant homeostasis and membrane transport in living organisms]. Visnyk of Lviv University, Series Biology, 60, 21–39 (in Ukrainian).
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.