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Antioxidant enzyme activity and osmolyte content in winter cereal seedlings under hardening and cryostress

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Abstract

Activities of antioxidant enzymes and the osmolyte contents in seedlings of winter rye (Secale cereale L.), soft (Triticum aestivum L.) and durum (T. durum L.) wheat, and barley (Hordeum vulgare L.) grown at 20°C (control) or after 7-day cold hardening at 2°C and/or 5-hour freezing at −6°C were investigated. It was found that nonhardened rye seedlings differed from those of other cereals by their ability to survival after freezing at −6°C and higher activity of guaiacol peroxidase (GPO) and high content of proline. Hardening induced the increase in the frost tolerance of all cereals under study, and the resistance of rye and soft wheat was found to be significantly higher than that of durum wheat and barley. Rye and soft wheat exhibited more profound tolerance to oxidative damages as well, and it was expressed in lesser increase in the MDA content after freezing. In the course of hardening, detectable increase in the activities of GPO and catalase (CAT), as well as the contents of proline and soluble carbohydrates, was observed in seedlings of all cereals under study. In barley, the activity of superoxide dismutase (SOD) increased to the highest extent under these conditions. After freezing of both hardened and nonhardened seedlings, higher activities of all tested antioxidant enzymes were revealed in rye and soft wheat as compared to those in durum wheat and barley. In this case, hardened rye and soft wheat seedlings after freezing displayed increased content of proline. All these results lead to the conclusion that the high content of proline and activity of GPO observed in rye seedlings may determine their increased constitutive frost tolerance, whereas high tolerance of hardened soft wheat seedlings is primarily associated with accumulation of low-molecular-weight protectors, such as sugars and proline, and, to some extent, with the increased activity of antioxidant enzymes.

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Abbreviations

GPO:

guiaicol peroxidase

CAT:

catalase

SOD:

superoxide dismutase

TBA:

2-thiobarbituric acid

References

  1. 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 

  2. Theocharis, A., Clement, C., and Barka, E.A., Physiological and molecular changes in plants grown at low temperatures, Planta, 2012, vol. 235, pp. 1091–1105.

    Article  CAS  PubMed  Google Scholar 

  3. Grabelnych, O.I., Sumina, O.N., Funderat, S.P., Pobezhimova, T.P., Voinikov, V.K., and Kolesnichenko, A.V., The distribution of electron transport between the main cytochrome and alternative pathways in plant mitochondria during short-term cold stress and cold hardening, J. Therm. Biol., 2004, vol. 29, pp. 165–175.

    Article  CAS  Google Scholar 

  4. Foyer, C.H. and Noctor, G., Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications, Antioxid. Redox Signal., 2009, vol. 11, pp. 861–906.

    Article  CAS  PubMed  Google Scholar 

  5. Pradedova, E.V., Isheeva, O.D., and Salyaev, R.K., Classification of the antioxidant defense system as the ground for reasonable organization of experimental studies of the oxidative stress in plants, Russ. J. Plant Physiol., 2011, vol. 58, pp. 210–217.

    Article  CAS  Google Scholar 

  6. Baek, K.H. and Skinner, D.Z., Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines, Plant Sci., 2003, vol. 165, pp. 1221–1227.

    Article  CAS  Google Scholar 

  7. 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 

  8. Janda, T., Szalai, G., Rios-Gonzalez, K., Veisz, O., and Paldi, E., Comparative study of frost tolerance and antioxidant activity in cereals, Plant Sci., 2003, vol. 164, pp. 301–306.

    Article  CAS  Google Scholar 

  9. Apostolova, P., Yordanova, R., and Popova, L., Response of antioxidative defence system to low temperature stress in two wheat cultivars, Gen. Appl. Plant Physiol., 2008, vol. 34, pp. 281–294.

    CAS  Google Scholar 

  10. Dzhavadian, N., Karimzade, G., Mafuzi, S., and Ganati, F., Cold-induced changes of enzymes, proline, carbohydrates, and chlorophyll in wheat, Russ. J. Plant Physiol., 2010, vol. 57, pp. 540–547.

    Article  Google Scholar 

  11. Lukatkin, A.S., Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants. 2. The activity of antioxidant enzymes during plant chilling, Russ. J. Plant Physiol., 2002, vol. 49, pp. 782–788.

    Article  CAS  Google Scholar 

  12. Sin’kevich, M.S., Deryabin, A.N., and Trunova, T.I., Characteristics of oxidative stress in potato plants with modified carbohydrate metabolism, Russ. J. Plant Physiol., 2009, vol. 56, pp. 168–174.

    Article  Google Scholar 

  13. Kolupaev, Yu.E. and Karpets, Yu.V., Formirovanie adaptivnykh reaktsii rastenii na deistvie abioticheskikh stressorov (Formation of Adaptive Responses of Plants to Abiotic Stressors), Kiev: Osnova, 2010.

    Google Scholar 

  14. Liang, X., Zhang, L., Natarajan, S.K., and Becker, D.F., Proline mechanisms of stress survival, Antioxid. Redox Signal., 2013, vol. 19, pp. 998–1011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Vagujfalvi, A., Kerepesi, I., Galiba, G., Tischner, T., and Sutka, J., Frost hardiness depending on carbohydrate changes during cold acclimation in wheat, Plant Sci., 1999, vol. 144, pp. 85–92.

    Article  CAS  Google Scholar 

  16. Burbulis, N., Jonytiene, V., Kupriene, R., and Blinstrubiene, A., Changes in proline and soluble sugars content during cold acclimation of winter rapeseed shoots in vitro, J. Food Agricult. Environ., 2011, vol. 9, pp. 371–374.

    Google Scholar 

  17. Radyukina, N.L., Shashukova, A.V., Makarova, S.S., and Kuznetsov, Vl.V., Exogenous proline modifies differential expression of superoxide dismutase genes in UV-B-irradiated Salvia officinalis plants, Russ. J. Plant Physiol., 2011, vol. 58, pp. 51–59.

    Article  CAS  Google Scholar 

  18. Carvalho, K., Campos, M.K., Domingues, D.S., Pereira, L.F., and Vieira, L.G., The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo, Mol. Biol. Rep., 2013, vol. 40, pp. 3269–3279.

    Article  CAS  PubMed  Google Scholar 

  19. Kartashov, A.V., Radyukina, N.L., Ivanov, Yu.V., Pashkovskii, P.P., Shevyakova, N.I., and Kuznetsov, Vl.V., Role of antioxidant systems in wild plant adaptation to salt stress, Russ. J. Plant Physiol., 2008, vol. 55, pp. 463–468.

    Article  CAS  Google Scholar 

  20. Samygin, G.A., Rapid determination of the relative hardiness of wheat samples by freezing of germinated seeds, Metody opredeleniya morozostoikosti rastenii (Methods for Determination of Frost Resistance), Moscow: Nauka, 1967, pp. 77–84.

    Google Scholar 

  21. Merzlyak, M.N., Pogosyan, S.I., Yuferova, S.G., and Shevyreva, V.A., The Use of 2-Thiobarbituric Acid in the Study of Lipid Peroxidation in Plant Tissues, Biol. Nauki, 1978, no. 9, pp. 86–94.

    Google Scholar 

  22. Karpets, Yu.V., Kolupaev, Yu.E., Lugovaya, A.A., and Oboznyi, A.I., Effect of jasmonic acid on the pro-/antioxidant system of wheat coleoptiles as related to hyperthermia tolerance, Russ. J. Plant Physiol., 2014, vol. 61, pp. 339–346.

    Article  CAS  Google Scholar 

  23. Alscher, R.G., Erturk, N., and Heath, L.S., Role of superoxide dismutases (SODs) in controlling oxidative stress in plants, J. Exp. Bot., 2002, vol. 53, pp. 1331–1341.

    Article  CAS  PubMed  Google Scholar 

  24. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.

    Article  CAS  PubMed  Google Scholar 

  25. Zhao, K., Fan, H., Zhou, S., and Song, J., Study on the salt and drought tolerance of Suaeda salsa and Kalanchoe claigremontiana under iso-osmotic salt and water stress, Plant Sci., 2003, vol. 165, pp. 837–844.

    Article  CAS  Google Scholar 

  26. Bates, L.S., Walden, R.P., and Tear, G.D., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, pp. 205–210.

    Article  CAS  Google Scholar 

  27. Wanner, L.A. and Junttila, O., Cold-induced freezing tolerance in Arabidopsis, Plant Physiol., 1999, vol. 120, pp. 391–399.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Radyukina, N.L., Kartashov, A.V., Ivanov, Yu.V., Shevyakova, N.I., and Kuznetsov, Vl.V., Functioning of defense systems in halophytes and glycophytes under progressing salinity, Russ. J. Plant Physiol., 2007, vol. 54, pp. 806–815.

    Article  CAS  Google Scholar 

  29. Michaeli, R., Philosoph-Hadas, S., Riov, J., Shahak, Y., Ratner, K., and Meir, S., Chilling-induced leaf abscission of Ixora coccinea plants. III. Enhancement by high light via increased oxidative processes, Physiol. Plant., 2001, vol. 113, pp. 338–345.

    Article  CAS  PubMed  Google Scholar 

  30. Konstantinova, T., Parvanova, D., Atanassov, A., and Djilianov, D., Freezing tolerant tobacco, transformed to accumulate osmoprotectants, Plant Sci., 2002, vol. 163, pp. 157–164.

    Article  CAS  Google Scholar 

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Correspondence to Yu. E. Kolupaev.

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Original Russian Text © Yu.E. Kolupaev, N.I. Ryabchun, A.A. Vayner, T.O. Yastreb, A.I. Oboznyi, 2015, published in Fiziologiya Rastenii, 2015, Vol. 62, No. 4, pp. 533–541.

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Kolupaev, Y.E., Ryabchun, N.I., Vayner, A.A. et al. Antioxidant enzyme activity and osmolyte content in winter cereal seedlings under hardening and cryostress. Russ J Plant Physiol 62, 499–506 (2015). https://doi.org/10.1134/S1021443715030115

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