Skip to main content
Log in

Activities of Catalase and Peroxidase in Wheat and Rice Plants under Conditions of Anoxia and Post-Anoxic Aeration

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

REFERENCES

  1. Chirkova, T.V., Ways of plant adaptation to hypoxia and anoxia, L.: Publishing house of the Leningrad University, 1988, 244 p.

  2. Crawford, R.M.M., Studies in Plant Survival. Ecological Case Histories of Plant Adaptation to Adversity, Oxford: Blackwell Scientific Publications, 1989, 296 p.

    Google Scholar 

  3. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  CAS  Google Scholar 

  5. Chirkova, T.V., Plant and anaerobiosis, Bulletin of St. Petersburg University, ser. 3, 1998, issue 2, p. 41.

  6. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  Google Scholar 

  10. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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

    Article  CAS  Google Scholar 

  12. 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

    Article  CAS  Google Scholar 

  13. 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.

    CAS  Google Scholar 

  14. 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

    Article  CAS  Google Scholar 

  15. 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

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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.

    CAS  Google Scholar 

  18. 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

    Article  CAS  PubMed  Google Scholar 

  19. 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

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. 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

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  CAS  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. Andreeva, V.A., Peroxidase enzyme: Participation in the defense mechanism of plants, Moscow: Nauka, 1988, 128 p.

    Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  27. Rubin, B.A. and Loginova, L.N., Final stages of oxidation in the leaves of semi-submerged plants, Biochem., 1965, vol. 30, p. 681.

    CAS  Google Scholar 

  28. 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.

    CAS  Google Scholar 

  29. 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.

  30. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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.

  33. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. 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

    Article  CAS  Google Scholar 

  36. 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

    Article  CAS  PubMed  Google Scholar 

  37. Aebi, H., Catalase in vitro, Methods Enzymol., 1984, vol. 105, p. 121, https://doi.org/10.1016/S0076-6879(84)05016-3

    Article  CAS  PubMed  Google Scholar 

  38. 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

    Article  CAS  PubMed  Google Scholar 

  39. 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

    Article  CAS  PubMed  Google Scholar 

  40. 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

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

The basic equipment of the Research Park of the Center for Molecular and Cell Technologies (St. Petersburg State University) was used.

Funding

The work was supported by the Russian Science Foundation, project no. 22-24-00484.

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to V. V. Yemelyanov.

Ethics declarations

The authors declare that they have no conflicts of interest. This article does not contain any work conducted on animal or human participants.

Additional information

Translated by A. Aver’yanov

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1134/S1021443722060036

Keywords:

Navigation