Metabolism of carbohydrates and activity of the antioxidant system in mosses on a post-technogenic salinized territory
AbstractAdaptive physiological and biochemical reactions of mosses Didymodon rigidulus Hedw., Barbula unguiculata Hedw. and Brachythecium campestre (Müll. Hal.) Schimp. to salt stress have been investigated from the territory of the tailings storage of the Stebnyk Mining and Chemical Enterprise “Polymineral” (Lviv region, Ukraine). The peculiarities of carbohydrate metabolism in mosses under salinity conditions have been studied. The content of soluble carbohydrates and proline, the antioxidant activity, the content of ascorbate and reduced glutathione as well as the activity of enzymes of their metabolism – ascorbate peroxidase and glutathione reductase at the initial stages of the stress (salt shock) and prolonged stress exposure (salt stress) have been evaluated. It has been found that the increase of α-amylase activity, enhancement of the hydrolysis of starch and the increase of the concentration of soluble carbohydrates under salt stress were the reactions of the studied species of mosses. It has been established that there was an increase in the concentration of soluble carbohydrates by 1.2–1.5 times in moss shoots under salinity conditions, compared with plants from the background area (vicinity of Stebnyk). Experimental studies have shown that under salinity conditions sucrose dominates in the pool of soluble carbohydrates (59.0–79.5% of the total sugars content). The sucrose content was 1.5–2.0 times higher in the plants B. unguiculata and D. rigidulus from the highly saline area of the tailings storage. It has been indicated that under stress conditions constitutive adaptive mechanisms are more expressed in resistant moss species, and plants with a lower level of resistance adapt to the stressor, mainly due to induced protective systems. Experimental studies have shown that plants B. unguiculata and D. rigidulus, which are resistant to abiotic stressors, have a high constitutive pool of soluble carbohydrates both at the beginning of the experiment and under prolonged exposure of the salt stress. In the shoots of the sensitive moss B. campestre the stress-induced character of the sugars accumulation has been revealed. The accumulation of proline in mosses cells under salt stress depended on their species characteristics. The stress-induced accumulation of proline can be considered as a part of the bryophytes’ protective system, but this osmolyte does not play a key role in the formation of the mosses’ resistance to salt stress. Obviously, soluble carbohydrates are the main osmolytes in the moss cells. It has been found that resistant moss species have a high constitutive antioxidant status, while in the sensitive moss B. campestre the increase in the antioxidant activity occurred during prolonged salt stress, which may indicate its induced nature. It has been shown that the resistant mosses B. unguiculata and D. rigidulus have 3–4 times higher levels of glutathione and ascorbate content and 1.6–2.5 times higher activity of enzymes of their metabolism – glutathione reductase and ascorbate peroxidase, compared to plants of the less tolerant moss species B. campestre, which provided reduction of the lipid peroxidation process in plasma membranes and decreased the content of TBA-active products under stress.
Aversi-Ferreira, T., Penha-Silva, N., Fonseca, A., Brito, A., & Penha, M. (2004). Rapid determination of reducing sugars with picric acid for biotechnological use. Bioscience Journal, 20, 183–188.
Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205–207.
Boots, M., & Best, A. (2018). The evolution of constitutive and induced defences to infectious disease. Proceedings of the Royal Society, Biological Series, 285, 20180658.
Boychuk, M. A. (2021). Mosses (Bryophyta) of the Kostomuksha State Nature Reserve, Russia. Nature Conservation Research, 6, 89–97.
Brand-Williams, W., Cuvelier, M. E., & Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. Food Science and Technology, 28, 25–30.
Ćosić, M., Vujićić, M., Sabovljević, M., & Sabovljević, A. (2018). What do we know about salt stress in bryophytes? Plant Biosystems, 9(4), 51–60.
DuBois, M., Hamilton, J. K., Rebers, P., & Smith, F. (2002). Calorimetric Dubois method for determination of sugar and related substances. Analytical Chemistry, 28, 350–356.
Durand, E., Zhao, Y., Ruesgas-Ramón, M., Figueroa-Espinoza, C. 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) assay. European Journal of Lipid Science and Technology, 121(5), 126–142.
Flowers, T. J., Munns, R., & Colmer, T. D. (2014). Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Annals of Botany, 115, 419–431.
Gao, B., Li, X., Zhang, D., Liang, Y., Yang, H., Chen, M., Zhang, Y., Zhang, J., & Wood, A. J. (2017). Desiccation tolerance in bryophytes: The dehydration and rehydration transcriptomes in the desiccation-tolerant bryophyte Bryum argenteum. Scientific Reports, 7, 117–126.
Garbary, D. J., Miller, A. G., Scrosati, R., Kim, K., & Schofield, W. B. (2008). Distribution and salinity tolerance of intertidal mosses from Nova Scotia. The Bryologist, 111, 282–291.
Glime, G. M. (2007). Bryophyte ecology. Biological Sciences, Michigan Technological University.
González-Orenga, S., Marius-Nicusor, G., Boscaiu, M., & Vicente, O. (2021). Constitutive and induced salt tolerance mechanisms and potential uses of Limonium Mill. species. Agronomy, 11(3), 413–422.
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.
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 defence regulator. Antioxidants, 9(8), 2–52.
Hatanaka, R., & Sugawara, Y. (2010). Development of desiccation tolerance and vitrification by preculture treatment in suspension-cultured cells of the liverwort Marchantia polymorpha. Planta, 231(4), 965–976.
He, M., He, C.-Q., & Ding, N.-Z. (2018). Abiotic stresses: General defences of land plants and chances for engineering multistress tolerance. Frontiers in Plant Sciences, 9, 1771.
Isayenkov, S. V. (2012). Physiological and molecular aspects of salt stress in plants. Cytology and Genetics, 46(5), 302–318.
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.
Ketehouli, T., Idrice Carther, K. F., Noman, M., Wang, F.-W., Li, X.-W., & Li, H.-Y. (2019). Adaptation of plants to salt stress: Characterization of Na+ and K+ transporters and role of CBL gene family in regulating salt stress response. Agronomy, 9(11), 687.
Kolupaev, Y. E., & Karpets, Y. V. (2009). Aktivnye formy kisloroda pri adaptatsii rastenii k stressovym temperaturam [Reactive oxygen species during plants’ adaptation to thermal stress]. Fiziologiya i Biokhimiya Kul’turnych Rastenii, 41(2), 95–104 (in Russian).
Kolupaev, Y. E., Karpets, Y. V., & Yastreb, T. O. (2017). Funktsionirovanie antioksidantnoj sistemy rastenij pri solevom stresse [Functioning of the antioxidant system of plants under salt stress]. Bulletin of Kharkiv National Agrarian University, Series: Biology, 3, 23–45 (in Russian).
Kolupaev, Y. E., Shklyarevskiy, M. A., Karpets, Y. V., Shvidenko, N. V., & Lugovaya, A. A. (2021). AFK-zavisimoe indutsirovanie geminom antioksidantnoy sistemy i teploustoychivosti prorostkov pshenitsy [ROS-dependent hemin induction of the antioxidant system and heat tolerance in wheat seedlings]. Fiziologiya Rasteniy, 68(2), 177–186 (in Russian).
Kolupaev, Y. E., Vayner, A. A., & Yastreb, T. O. (2014). Prolin: Fiziologicheskie funktsii i regulyatsiya soderzhaniya v rasteniyakh v stressovykh usloviyakh [Proline: Physiological functions and regulation of the content in plants under stress conditions]. Bulletin of Kharkiv National Agrarian University, Series: Biology, 32, 6–22 (in Russian).
Kovács, Z., Simon-Sarkadi, L., Vashegyi, I., & Kocsy, G. (2012). Different accumulation of free amino acids during short- and long-term osmotic stress in wheat. The Scientific Word Journal, 8(3). 243–258.
Kyyak, N. Y., & Khorkavtsiv, Y. D. (2016). Otsinka okysniuvalnoho stresu mokhu Pohlia nutans (Hedw.) Lindb. zalezhno vid vplyvu hravitatsiyi [Estimation of the oxidative stress in moss Pohlia nutans (Hedw.) Lindb. depending on the influence of gravity]. Space Science and Technology, 22(4), 58–66 (in Ukrainian).
Kyyak, N. Y., Lobachevska, O. V., & Khorkavtsiv, Y. D. (2021). Morfo-fiziolohichni reaktsii hravichutlyvosti ta adaptatsiyi do UF-vyprominiuvannia mokhu Bryum caespiticium Hedw. iz Antarktyky [Morpho-physiological reactions of gravisensitivity and adaptation to UV irradiation of the moss Bryum caespiticium Hedw. from Antarctica]. Space Science and Technology, 27(5), 47–59 (in Ukrainian).
Kyyak, N. Y., Lobachevska, O. V., Rabyk, I. V., & Kyyak, V. H. (2020). Role of the bryophytes in substrate revitalization on a post-technogenic salinized territory. Biosystems Diversity, 28(4), 419–425.
Kyyak, V. H., & Kyyak, N. Y. (2019). Mechanisms of maintenance of cytoplasmic osmotic homeostasis in bryophytes cells under salinity stress. Studia Biologica, 13(2), 55–66.
Lavrenko, S. O., Lavrenko, N. M., & Lykhovyd, P. V. (2019). Effect of degree of salinity on seed germination and initial growth of chickpea (Cicer arietinum). Biosystems Diversity, 27(2), 101–105.
Li, J., Li, X., & Chen, C. (2014). Degradation and reorganization of thylakoid protein complexes of Bryum argenteum in response to dehydration and rehydration. The Bryologist, 117(2), 110–118.
Liu, B.-Y., Lei, C.-Y., Jin, J.-H., Guan, Y.-Y., Li, S., Zhang, Y.-S., & Liu, W.-Q. (2016). Physiological responses of two moss species to the combined stress of water deficit and elevated N deposition (II): Carbon and nitrogen metabolism. Ecology and Evolution, 6, 7596–7609.
Liu, W., Xu, J., Fu, W., Wang, X., Lei, C., & Chen, Y. (2019). Evidence of stress imprinting with population-level differences in two moss species. Ecology and Evolution, 9(11), 6329–6341.
Lobachevska, O. V. (2008). Vmist vilnoho prolinu ta aktyvnist antyoksydantnoho zakhystu u mokhopodibnykh za stresovykh umov [Content of free proline and antioxidant protection activity in mosses under stress conditions]. Chornomorski Botanical Journal, 4(2), 230–236 (in Ukrainian).
Lobachevska, O. V., Kyyak, N. Y., & Rabyk, I. V. (2019). Ecological and physiological peculiarities of bryophytes on a post-technogenic salinized territory. Biosystems Diversity, 27(4), 342–348.
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.
Lushchak, V. I., Bahniukova, T. V., & Lushchak, O. V. (2004). Tiobarbiturataktyvni produkty i karbonilni hrupy bilkiv [Thiobarbituric acid-active products and carbonyl groups of proteins]. The Ukrainian Biochemical Journal, 76(3), 136–141 (in Ukrainian).
MacGregor, A. W., MacDougall, F. H., Mayer, C., & Daussant, J. (1984). Changes in levels of a-amylase components in barley tissues during germination and early seedling growth. Plant Physiology, 75, 203–206.
Mehta, N., Patani, P., & Singhvi, I. (2018). Colorimetric estimation of ascorbic acid from different varities of tomatoes cultivated in Gujarat. World Journal of Pharmaceutical Research, 7(4), 1376–1384.
Monsigny, M., Petit, C., & Roche, A. C. (1988). Colorimetric determination of neutral sugars by a resorcinol sulfuric acid micromethod. Analytical Biochemistry, 175, 525–530.
Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59, 651–681.
Nagao, M., Minami, A., Arakawa, K., Fujikawa, S., & Takezawa, D. (2005). Rapid degradation of starch in chloroplasts and concomitant accumulation of soluble sugars associated with ABA-induced freezing tolerance in the moss Physcomitrella patens. Journal of Plant Physiology, 162(2), 169–180.
Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22(5), 867–880.
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.
Oke, T. A., Turetsky, M. R., Weston, D. J., & Shaw, J. A. (2020). Tradeoffs between phenotypic plasticity and local adaptation influence the ecophysiology of the moss, Sphagnum magellanicum. Oecologia, 193(4), 867–877.
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.
Paciolla, C., & Tomassi, F. (2003/2004). The ascorbate system in two bryophytes: Brachytecium velutinum and Marchantia polymorpha. Biologia Plantarum, 47(3), 387–393.
Pouliot, R., Rochefort, L., & Graf, M. (2012). Impacts of oil sands process water on fen plants: Implication for plant selection in required reclamation projects. Environmental Pollution, 167, 132–137.
Pressel, S., Ligrone, R., & Duckett, J. (2006). Effects of de- and rehydration on food-conducting cells in the moss Polytrichum formosum: A cytological study. Annals of Botany, 98, 67–76.
Proctor, M. C. F., & Tuba, Z. (2002). Poikilohydry and homiohydry: Antithesis or spectrum of possibilities? New Phytologist, 156, 327–349.
Proctor, M. C. F., Oliver, M. J., Wood, A. J., Alpert, P. R., Stark, L., Cleavitt, N. L., & Mishler, B. D. (2007). Desiccations-tolerance in bryophytes: A review. Bryologist, 110(4), 595–621.
Rabyk, I. V., Lobachevska, O. V., Kyyak, N. Y., & Shcherbachenko, O. I. (2018). Bryophytes on the devastated territories of sulphur deposits and their role in restoration of dump substrate. Biosystems Diversity, 26(4), 339–353.
Sabovljević, M. S., & Sabovljević, A. D. (2020). Bryophytes. IntechOpen, London.
Sabovljević, M., & Sabovljević, A. (2007). Contribution to the coastal bryophytes of the Northern Mediterranean: Are there halophytes among bryophytes? Phytologia Balcanica, 13(2), 131–135.
Sadasivam, S., & Manickam, A. (2007). Biochemical methods. New Age International, New Delhi.
Seel, W. E., Hendry, G. A. F., & Lee, J. A. (1992). The combined effects of desiccation and irradiance on mosses from xeric and hydric habitats. The Journal of Experimental Botany, 43, 1023–1030.
Smirnoff, N. (2005). Antioxidants and reactive oxygen species in plants. Blackwell Publishing Ltd., Oxford.
Smith, I. K., Vierheller, T. L., & Thorne, C. A. (1988). Assay of glutathione reductase in crude tissue homogenates using 5,5’-dithiobis(2-nitrobenzoic acid). Analytical Biochemistry, 175, 408–413.
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.
Stark, L. R. (2017). Ecology of desiccation tolerance in bryophytes: A conceptual framework and methodology. The Bryologist, 120(2), 129–164.
Venegas-Molina, J., Proietti, S., Pollier, J. Orozco-Freire, W., Ramirez-Villacis, D., & Leon-Reyes, A. (2020). Induced tolerance to abiotic and biotic stresses of broccoli and Arabidopsis after treatment with elicitor molecules. Scientific Reports, 10, 10319.
Wang, X., Liu, Z., & He, Y. (2008). Responses and tolerance to salt stress in bryophytes. Plant Signaling and Behavior, 3(8), 516–518.
Westbrook, R. L., Bridges, E., Roberts, J., Escribano-Gonzalez, C., Eales, K. L., Vettore, L. A., Walker, P. D., Vera-Siguenza, E., Rana, H., Cuozzo, F., Eskla, K.-L., Vellama, H., Shaaban, A., Nixon, C., Luuk, H., Lavery, G. G., Hodson, D. J., Harris, A. L., & Tennant, D. A. (2022). Proline synthesis through PYCR1 is required to support cancer cell proliferation and survival in oxygen-limiting conditions. Cell Reports, 38(5), 110320.
Wu, N., Zhang, Y. M., Downing, A., Zachary, T. Aanderud, C., Ye Tao, A., & Williams, S. (2014). Rapid adjustment of leaf angle explains how the desert moss, Syntrichia caninervis, copes with multiple resource limitations during rehydration. Functional Plant Biology, 41, 168–177.
Yan, L., Li, S., Riaz, M., & Jiang, C. (2021). Proline metabolism and biosynthesis behave differently in response to boron-deficiency and toxicity in Brassica napus. Plant Physiology and Biochemistry, 167, 529–540.
Yenne, S. P., & Hatzios, K. (1990). Influence of oxime ether on glutathione content and glutathione-related enzyme activity in seeds and seedlings of grain sorghum. Zeitschrift für Naturforschung, 45, 96–106.
Zhu, J.-K. (2002). Salt and drought stress signal transduction in plants. Annual Review of Plant Biology, 53, 247–273.
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