Skip to main content
Log in

Activities of Hydrogen Peroxide-Scavenging Enzymes during Low-Temperature Hardening of Potato Plants Transformed by the desA Gene of Δ12-Acyl-Lipid Desaturase

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Activities of enzymes decomposing hydrogen peroxide (H2O2) under long exposure to hardening low temperatures and the effect of Δ12-acyl-lipid desaturase on these processes were studied on potato (Solanum tuberosum L., cv. Desnitsa), which typically represents cold-tolerant plants. We compared nontransformed plants (control) and the line transformed with the construction carrying the target desA gene of the mentioned desaturase from cyanobacterium Synechocystis sp. PCC (desA-licBM3 plants). The plants were hardened at 5°C for six days under illumination of 50 μmol/(m2 s). The hardening was found to favor plant tolerance to the subsequent frost, and the desA-licBM3 plants exceed the controls in this property. Of the studied H2O2-scavenging enzymes, soluble type III peroxidases (guaiacol peroxidases) displayed the most activity, and type I peroxidase (ascorbate peroxidase) was the least active in the two potato lines over the hardening period. The activity of catalase increased twofold in the control and fourfold in the transformed plants in the first day of the hardening. However, the doubled catalase activity did not appear to compensate the H2O2 accumulation over this period. The recorded rise in catalase activity in the desA-licBM3 plants, together with the high activity of guaiacol peroxidases, favored lowering the hydrogen peroxide level in comparison with the initial values. For the first time, electrophoresis revealed two catalase isoforms, CAT1 and CAT2, in leaves of both potato lines. The significance of CAT1 was greater than that of CAT2 in the total catalase activity during the hardening period. It is concluded that, under the long-term cold hardening of potato plants, the content of hydrogen peroxide is determined by highly active guaiacol peroxidases and Class I catalase exerting energy-independent H2O2 decomposing. In this case, in the transformants that are rich in membrane lipids, where polyunsaturated fatty acids predominate, the activity of H2O2-scavenging enzymes increased significantly more than in the control, which is why the hardening of the transformants is more effective.

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.

Similar content being viewed by others

Abbreviations

CAT1 and CAT2:

isoforms of catalase

FA:

fatty acids

SOD:

superoxide dismutase

References

  1. Tumanov, I.I., Fiziologiya zakalivaniya i zimostoikosti rastenii (Physiology of Hardening and Winter Hardiness of Plants), Moscow: Nauka, 1979.

    Google Scholar 

  2. Titov, A.F., Akimova, T.V., Talanova, V.V., and Topchieva, L.V., Ustoichivost’ rastenii v nachal’nyi period deistviya neblagopriyatnykh temperatur (Plant Resistance in the Initial Period of Extreme Temperatures), Moscow: Nauka, 2006.

    Google Scholar 

  3. Voinikov, V.K., Energeticheskaya i informatsionnaya sistemy rastitel’nykh kletok pri gipotermii (Energy and Information Systems of Plant Cells under Hypothermia), Novosibirsk: Nauka, 2013.

    Google Scholar 

  4. Lukatkin, A.S., Kholodovoe povrezhdenie teplolyubivykh rastenii i okislitel’nyi stress (Cold Damage of Heat-Loving Plants and Oxidative Stress), Saransk: Izd. Mord. Univ., 2002.

    Google Scholar 

  5. Levitt, J., Responses of plants to environmental stresses: chilling, freezing and high temperature stresses, in Physiological Ecology, New York: Academic, 1980, vol. 1.

  6. Trunova, T.I., Rastenie i nizkotemperaturnyi stress. 64-e Timiryazevskoe chtenie (Plant and Low Temperature Stress, the 64th Timiryazev Lecture), Moscow: Nauka, 2007.

    Google Scholar 

  7. Demin, I.N., Deryabin, A.N., Sin’kevich, M.S., and Trunova, T.I., Insertion of cyanobacterial desA gene coding for Δ12-acyl-lipid desaturase increases potato plant resistance to oxidative stress induced by hypothermia, Russ. J. Plant Physiol., 2008, vol. 55, pp. 639–648.

    Article  CAS  Google Scholar 

  8. Mittler, R., Oxidative stress, antioxidants and stress tolerance, Trends Plant Sci., 2002, vol. 7, pp. 405–410.

    Article  PubMed  CAS  Google Scholar 

  9. Naraikina, N.V., Sin’kevich, M.S., Demin, I.N., Selivanov, A.A., Moshkov, I.E., and Trunova, T.I., Changes in the activity of superoxide dismutase isoforms in the course of low-temperature adaptation in potato plants of wild type and transformed with Δ12-acyl-lipid desaturase gene, Russ. J. Plant Physiol., 2014, vol. 61, pp. 332–338.

    Article  CAS  Google Scholar 

  10. Sin'kevich, M.S., Naraikina, N.V., and Trunova, T.I., Processes hindering activation of lipid peroxidation in cold-tolerant plants under hypothermia, Russ. J. Plant Physiol., 2011, vol. 58, pp. 1020–1026.

    Article  CAS  Google Scholar 

  11. Demin, I.N., Shimshilashvili, C.R., Yur’eva, N.O., Naraykyna, N., Goldenkova-Pavlova, I.V., Los, D.A., Nosov, A.M., and Trunova, T.I., Overexpression of the acyl-lipid Δ12-desaturase gene protects potato plants from low temperature damage, Acta Agron. Hung., 2011, vol. 59, pp. 87–99.

    Article  CAS  Google Scholar 

  12. Astakhova, N.V., Demin, I.N., Naraikina, N.V., and Trunova, T.I., Effect of the desA gene encoding Δ12 acyl-lipid desaturase on the chloroplast structure and tolerance to hypothermia of potato plants, Russ. J. Plant Physiol., 2011, vol. 58, pp. 18–23.

    Article  CAS  Google Scholar 

  13. Hepburn, H.A., Nayllor, F.L., and Strokes, D.I., Electrolyte leakage from winter barley tissue as indicator of winter hardiness, Ann. Appl. Biol., 1986, vol. 108, pp. 164–165.

    Article  Google Scholar 

  14. Kumar, G.N. and Knowles, N.R., Changes in lipid peroxidation and lipolytic and free-radical scavenging enzyme during aging and sprouting of potato (Solanum tuberosum L.) seed-tubers, Plant Physiol., 1993, vol. 102, pp. 115–124.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Nakano, Y. and Asada, K., Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts, Plant Cell Physiol., 1981, vol. 22, pp. 867–880.

    CAS  Google Scholar 

  16. Nelson, D.P. and Kiesow, L.A., Enthalpy of decomposition of hydrogen peroxide by catalase at 25 degrees C (with molar extinction coefficients of H2O2 solutions in the UV), Anal. Biochem., 1972, vol. 49, pp. 474–478.

    Article  PubMed  CAS  Google Scholar 

  17. Davis, B.J., Disc electrophoresis. II. Method and application to human serum proteins, Ann. New York Acad. Sci., 1964, vol. 121, pp. 404–427.

    Article  CAS  Google Scholar 

  18. Candiano, G., Bruschi, M., Musante, L., Santucci, L., Ghiggeri, G.M., Carnemolla, B., Orecchia, P., Zardi, L., and Righetti, P.G., Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis, Electrophoresis, 2004, vol. 25, pp. 1327–1333.

    Article  PubMed  CAS  Google Scholar 

  19. Zimmermann, P., Heinlein, Ch., Orendi, G., and Zentgraf, U., Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh., Plant Cell Environ., 2006, vol. 29, pp. 1049–1060.

    Article  PubMed  CAS  Google Scholar 

  20. Miller, G., Shulaev, V., and Mittler, R., Reactive oxygen signaling and abiotic stress, Physiol. Plant., 2008, vol. 133, pp. 481–489.

    Article  PubMed  CAS  Google Scholar 

  21. Cosio, C. and Dunand, C., Specific function of individual class III peroxidase genes, J. Exp. Bot., 2009, vol. 60, pp. 391–408.

    Article  PubMed  CAS  Google Scholar 

  22. Shigeto, J. and Tsutsumi, Y., Diverse functions and reactions of class III peroxidases, New Phytol., 2016, vol. 209, pp. 1395–1402.

    Article  PubMed  CAS  Google Scholar 

  23. Wyrwicka, A. and Sklodowska, M., Influence of repeated acid rain treatment on antioxidative enzyme activities and on lipid peroxidation in cucumber leaves, Environ. Exp. Bot., 2006, vol. 56, pp. 198–204.

    Article  CAS  Google Scholar 

  24. Maksimov, I.V., Cherepanova, E.A., Burkhanova, G.F., Sorokan’, A.V., and Kuz’mina, O.I., Structural-functional features of plant isoperoxidases, Biochemistry (Moscow), 2011, vol. 76: 609.

    Article  CAS  Google Scholar 

  25. Kolupaev, Yu.E. and Karpets, Yu.V., Formirovanie adaptivnykh reaktsii rastenii na deistvie abioticheskikh stressorov (Formation of Adaptive Reactions of Plants to the Action of Abiotic Stressors), Kiev: Osnova, 2016.

    Google Scholar 

  26. Miroshnichenko, O.S., Biogenesis, physiological role and properties of catalase, Biopolim. Kletka, 1992, vol. 8, pp. 2–25.

    Google Scholar 

  27. Feierabend, J., Catalases in plants: molecular and functional properties and role in stress defence, in Antioxidants and Reactive Oxygen Species in Plants, Smirnoff, N., Ed., Oxford: Blackwell Sci., 2005, pp. 101–140.

    Google Scholar 

  28. Scandalios, J.G., Guan, L., and Polidoros, A.N., Catalases in plant: gene structure, properties, regulation and expression, in Oxidative Stress and the Molecular Biology of Antioxidant Defenses, 1997, pp. 343–406.

    Google Scholar 

  29. Willekens, H., Villarroel, R., Inze, D., van Montagu, M., and van Camp, W., Molecular identification of catalases from Nicotiana plumbaginifolia, FEBS Lett., 1994, vol. 352, pp. 79–83.

    Article  PubMed  CAS  Google Scholar 

  30. Mhamdi, A., Queval, G., Chaouch, S., Vanderauwera, S., van Breusegem, F., and Noctor, G., Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models, J. Exp. Bot., 2010, vol. 61, pp. 41–97.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. S. Sin’kevich.

Additional information

Original Russian Text © N.V. Naraikina, M.S. Sin’kevich, A.N. Deryabin, T.I. Trunova, 2018, published in Fiziologiya Rastenii, 2018, Vol. 65, No. 5, pp. 340–347

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Naraikina, N.V., Sin’kevich, M.S., Deryabin, A.N. et al. Activities of Hydrogen Peroxide-Scavenging Enzymes during Low-Temperature Hardening of Potato Plants Transformed by the desA Gene of Δ12-Acyl-Lipid Desaturase. Russ J Plant Physiol 65, 667–673 (2018). https://doi.org/10.1134/S1021443718040064

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443718040064

Keywords

Navigation