Abstract
Effects of anoxia and subsequent reaeration on formation of hydrogen peroxide, and activities of catalase (EC 1.11.1.6) and guaiacol peroxidase (EC 1.11.1.7) were studied in wheat and rice plants that are contrasting in their tolerance to hypoxia. It was found that anoxia and reaeration, especially long-term, strongly increased the H2O2 production in hypoxia-intolerant wheat plants. Meanwhile, such treatment did not significantly entail peroxide production in rice, which is tolerant to oxygen lack. In these tolerant plants, the activities of catalase, as well as intra- and extracellular guaiacol peroxidases, rapidly increased under anoxia and the following oxidative stress. By contrast, wheat did not display stimulation of catalase activity; activation of its peroxidase occurred only in the shoots after a short anoxia and long reaeration. The increased or stable activities of catalase and peroxidase in the rice seedlings, under anoxia and reaeration, were inhibited by cycloheximide and, to smaller extent, actinomycin D. In rice, the stimulation of catalase activity was accompanied by the increased expression of the corresponding genes, in particular, OsCatB and OsCatС. The activities of apoplastic peroxidases were suppressed by brefeldin A. Electrophoresis did not reveal the emergence of new isoforms of guaiacol peroxidase under anoxia and post-anoxic aeration. Meanwhile, the activities of the majority of preexisting isoforms in rice and individual isoforms in wheat were considerably stimulated under these conditions. It is suggested that, in the tolerant plants subjected to anoxia and post-anoxic aeration, the activation of apoplastic peroxidases fulfills an adaptive function decomposing hydrogen peroxide in the cell wall and preventing its penetration into the cytosol. Under long-term reaeration, detoxification of ROS in the rice cytosol may be favored by activation of catalase and intracellular peroxidase. Unlike rice, the absence of activation of the antioxidant enzymes in the wheat cell wall allows ROS to penetrate inside the cell where they are deactivated by cytoplasmic forms of guaiacol peroxidase. The efficient work of antioxidant enzymes under anoxia, followed by post-anoxic aeration, prevents ROS accumulation in the tolerant plant and, thus, represents an important adaptation to both lack of oxygen and subsequent oxidative stress.
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REFERENCES
Chirkova, T.V., Ways of plant adaptation to hypoxia and anoxia, L.: Publishing house of the Leningrad University, 1988, 244 p.
Crawford, R.M.M., Studies in Plant Survival. Ecological Case Histories of Plant Adaptation to Adversity, Oxford: Blackwell Scientific Publications, 1989, 296 p.
Kennedy, R.A., Rumpho, M.E., and Fox, T.C., Anaerobic metabolism in plants, Plant Physiol., 1992, vol. 100, p. 1, https://doi.org/10.1104/pp.100.1.1
Vartapetian, B.B. and Jackson, B.M., Plant adaptations to anaerobic stress, Ann. Bot., 1997, vol. 79, p. 3, https://doi.org/10.1093/oxfordjournals.aob.a010303
Chirkova, T.V., Plant and anaerobiosis, Bulletin of St. Petersburg University, ser. 3, 1998, issue 2, p. 41.
Kende, H., van der Knaap, E., and Cho, H.T., Deepwater rice: A model plant to study stem elongation, Plant Physiol., 1998, vol. 118, p. 1105, https://doi.org/10.1104/pp.118.4.1105
Bailey-Serres, J. and Voesenek, L.A.C.J., Flooding stress: Acclimations and genetic diversity, Annu. Rev. Plant Biol., 2008, vol. 59, p. 313, https://doi.org/10.1146/annurev.arplant.59.032607.092752
Voesenek, L.A.C.J. and Bailey-Serres, J., Flood adaptive traits and processes: An overview, New Phytol., 2015, vol. 206, p. 57, https://doi.org/10.1111/nph.13209
Chirkova, T. and Yemelyanov, V., The Study of plant adaptation to oxygen deficiency in Saint Petersburg university, Biol. Commun., 2018, vol. 63, p. 17. https://doi.org/10.21638/spbu03.2018.104
Tamang, B.G. and Fukao, T., Plant adaptation to multiple stresses during submergence and following desubmergence, Int. J. Mol. Sci., 2015, vol. 16, p. 30164, https://doi.org/10.3390/ijms161226226
Shikov, A.E., Chirkova, T.V., and Yemelyanov, V.V., Post-anoxia in plants: reasons, consequences, and possible mechanisms, Russ. J. Plant Physiol., 2020, vol. 67, p. 45, https://doi.org/10.1134/S1021443720010203
Blokhina, O.B., Fagerstedt, K.V., and Chirkova, T.V., Relationships between lipid peroxidations and anoxia tolerance in a range of species during post-anoxic reaeration, Plant. Physiol., 1999, vol. 105, p. 625, https://doi.org/10.1034/j.1399-3054.1999.105405.x
Chirkova, T.V., Novitskaya, L.O., and Blokhina, O.B., Lipid peroxidation and antioxidant systems under anoxia in plants differing in their tolerance to oxygen deficiency, Russ. J. Plant Physiol., 1998, vol. 45, p. 55.
Amor, Y., Chevion, M., and Levine, A., Anoxia pretreatment protects soybean cells against H2O2-induced cell death: Possible involvement of peroxidases and of alternative oxidase, FEBS Lett., 2000, vol. 477, p. 175, https://doi.org/10.1016/s0014-5793(00)01797-x
Garnczarska, M., Bednarski, W., and Morkunas, I., Re-aeration-induced oxidative stress and antioxidative defenses in hypoxically pretreated lupine roots, J. Plant Physiol., 2004, vol. 161, p. 415, https://doi.org/10.1078/0176-1617-01073
Yemelyanov, V.V., Shikov, A.E., Lastochkin, V.V., and Chirkova, T.V., Oxidative stress under the action of reaeration and ROS generators in wheat and rice seedlings, Ecobiotech., 2020, vol. 3, p. 229, https://doi.org/10.31163/2618-964X-2020-3-2-229-238
Kalashnikov, Yu.E., Balakhnina, T.I., and Zakrzhevsky, D.A., The effect of soil hypoxia on oxygen activation and the defense system against oxidative degradation in the roots and leaves of Hordeum vulgare, Plant Phys., 1994, vol. 41, p. 583.
Blokhina, O.B., Chirkova, T.V., and Fagerstedt, K.V., Anoxic stress leads to hydrogen peroxide formation in plant cells, J. Exp. Bot., 2001, vol. 52, p. 1179, https://doi.org/10.1093/jexbot/52.359.1179
Paradiso, A., Caretto, S., Leone, A., Bove, A., Nisi, R., and De Gara, L., ROS Production and scavenging under anoxia and re-oxygenation in Arabidopsis cells: A balance between redox signaling and impairment, Front. Plant Sci., 2016, vol. 7, p. 1803, https://doi.org/10.3389/fpls.2016.01803
Parveen, M., Miyagi, A., Kawai-Yamada, M., Rashid, M.H., and Asaeda, T., Metabolic and biochemical responses of Potamogeton anguillanus Koidz. (Potamogetonaceae) to low oxygen conditions, J. Plant Physiol., 2019, vol. 232, p. 171, https://doi.org/10.1016/j.jplph.2018.11.023
Garnczarska, M. and Bednarski, W., Effect of a short-term hypoxic treatment followed by re-aeration on free radicals level and antioxidative enzymes in lupine roots, Plant Physiol. Biochem., 2004, vol. 42, p. 233, https://doi.org/10.1016/j.plaphy.2004.01.005
Ushimaru, T., Kanematsu, S., Katayama, M., and Tsujid, H., Antioxidative enzymes in seedlings of Nelumbo nucifera germinated under water, Physiol. Plant., 2001, vol. 112, p. 39, https://doi.org/10.1034/j.1399-3054.2001.1120106.x
Ushimaru, T., Shibasaka, M., and Tsuji, H., Development of O2 −-detoxification system during air adaptation of submerged rice seedlings, Plant Cell Physiol., 1992, vol. 33, p. 1065, https://doi.org/10.1093/oxfordjournals.pcp.a078357
Monk, L.S., Braendle, R., and Crawford, R.M.M., Catalase activity and post-anoxic injury in monocotyledonous species, J. Exp. Bot., 1987, vol. 38, p. 233, https://doi.org/10.1093/jxb/38.2.233
Andreeva, V.A., Peroxidase enzyme: Participation in the defense mechanism of plants, Moscow: Nauka, 1988, 128 p.
Cosio, C. and Dunand, C., Specific functions of individual class III peroxidase genes, J. Exp. Bot., 2009, vol. 60, p. 391, https://doi.org/10.1093/jxb/ern318
Rubin, B.A. and Loginova, L.N., Final stages of oxidation in the leaves of semi-submerged plants, Biochem., 1965, vol. 30, p. 681.
Budilova, E.V., Rubin, B.A., Ivanova, M.A., and Semenova, N.A., Peroxidase isoenzymes in egg-pod leaves, Doklady AN SSSR, 1971, vol. 200, p. 980.
Chirkova, T.V., Sokolovskaya, E.A., and Khazova, I.V., Activity and isozyme composition of plant root peroxidase depending on the conditions of temporary anaerobiosis, Plant Phys., 1973, vol. 20, p. 1236. 1973.
Jayawardhane, J., Goyali, J.C., Zafari, S., and Igamberdiev, A.U., The response of cowpea (Vigna unguiculata) plants to three abiotic stresses applied with increasing intensity: Hypoxia, salinity, and water deficit, Metabolites, 2022, vol. 12, p. 38, https://doi.org/10.3390/metabo12010038
Lee, T.M. and Lin, Y., Changes in soluble and cell wall-bound peroxidase activities with growth in anoxia-treated rice (Oryza sativa L.) coleoptiles and roots, Plant Sci., 1995, vol. 1, p. 1, https://doi.org/10.1016/0168-9452(94)04053-j
Lastochkin, V.V., Yemelyanov, V.V., and Chirkova, T. V., Peroxidase activity in wheat and rice seedlings in relation to exposure to anoxia, Bulletin of St. Petersburg Univ., ser. 3., 2000, vol. 3, p. 59.
Yemelyanov, V.V., Lastochkin, V.V., Chirkova, T.V., Lindberg, S.M., and Shishova, M.F., Indoleacetic acid levels in wheat and rice seedlings under oxygen deficiency and subsequent reoxygenation, Biomolecules, 2020, vol. 10, 276, https://doi.org/10.3390/biom10020276
Gay, C. and Gebicki, J.M., A Critical evaluation of the effect of sorbitol on the ferric xylenol orange hydroperoxide assay, Anal. Biochem., 2000, vol. 284, p. 217, https://doi.org/10.1006/abio.2000.4696
Otter, T. and Polle, A., Characterisation of acidic and basic apoplastic peroxidases from needles of norway spruce (Picea abies L., Karsten) with respect to lignifying substrates, Plant Cell Physiol., 1997, vol. 38, p. 595, https://doi.org/10.1093/oxfordjournals.pcp.a029209
Bradford, M., A Rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, p. 248, https://doi.org/10.1006/abio.1976.9999
Aebi, H., Catalase in vitro, Methods Enzymol., 1984, vol. 105, p. 121, https://doi.org/10.1016/S0076-6879(84)05016-3
Davis, B., Disc electrophoresis. II. Method and application for human serum proteins, Ann. N. Y. Acad. Sci., 1964, vol. 121, p. 404, https://doi.org/10.1111/j.1749-6632.1964.tb14213.x
Livak, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method, Methods, 2001, vol. 25, p. 402, https://doi.org/10.1006/meth.2001.1262
Duarte, V.P., Pereira, M.P., Corrêa, F.F., de Castro, E.M., and Pereira, F.J., Aerenchyma, gas diffusion, and catalase activity in Typha domingensis: A complementary model for radial oxygen loss, Protoplasma, 2021, vol. 258, p. 765, https://doi.org/10.1007/s00709-020-01597-8
ACKNOWLEDGMENTS
The basic equipment of the Research Park of the Center for Molecular and Cell Technologies (St. Petersburg State University) was used.
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The work was supported by the Russian Science Foundation, project no. 22-24-00484.
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The authors V.V. Yemelyanov and T.V. Chirkova devised and worked out the experimental design. V.V. Lastochkin and E.G. Prikaziuk cultivated plant material. The experiments on hydrogen peroxide production and enzymatic activities were carried out by V.V. Lastochkin, those on isozymic spectrum of peroxidases by V.V. Lastochkin and V.V. Yemelyanov, and those on catalase gene expression by E.G. Prikaziuk and V.V. Yemelyanov. The data processing was performed by V.V. Lastochkin, E.G. Prikaziuk, and V.V. Yemelyanov. The text of the paper was written by V.V. Yemelyanov and T.V. Chirkova. All the authors were involved in discussions of the results.
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Translated by A. Aver’yanov
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Yemelyanov, V.V., Lastochkin, V.V., Prikaziuk, E.G. et al. Activities of Catalase and Peroxidase in Wheat and Rice Plants under Conditions of Anoxia and Post-Anoxic Aeration. Russ J Plant Physiol 69, 117 (2022). https://doi.org/10.1134/S1021443722060036
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DOI: https://doi.org/10.1134/S1021443722060036