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Response of transgenic rape plants bearing the Osmyb4 gene from rice encoding a trans-factor to low above-zero temperature

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Abstract

Accumulation of soluble sugars (sucrose, fructose, and glucose), proline, phenols (total phenols and flavonoids), and antocyanins during adaptation to low-temperature stress (4°C) of two lines of spring rape (Brassica napus L., cv. Westar) characterized by weak (Bn-1) and strong (Bn-3) expression of the Osmyb4 transgene was studied. Vegetatively propagated transgenic and wild-type plants were grown in the hydroponic culture at 24°C; at the stage of 5–6 leaves, plants were exposed to 4°C for 5 days and then returned to the optimum temperature of 24°C for recovery. Transgenic plants were established to manifest improved cold and frost tolerance, which was evident from more active biomass accumulation at 4°C as compared with wild-type plants and from sustaining their viability after 2-day-long exposure to −6°C. Determination of MDA content showed that one of the reasons of their improved cold tolerance was their capability of maintaining oxidative homeostasis under low-temperature stress. This suggestion is supported by intense accumulation of phenols and antocyanins, manifesting pronounced antioxidant effects, by transgenic plants during their cold adaptation. Thus, during 2–5 days of plant exposure to 4°C, in transgenic plants the total content of phenols increased by 2.6–3.7 times, flavonoids — by 3.7–4.7 times, and antocyanins — by 3.5–5.3 times as compared with control plants growing at 24°C. Transgenic Bn-3 plants with strong expression of the Osmyb4 gene accumulated phenols and antocyanins at 4°C more actively than Bn-1 plants characterized by weak expression of this gene. Transgenic rape plants subjected to cold stress accumulated more proline, manifesting stress-protection effects, and lesser accumulation of soluble sugars. Before the beginning of experiment, the content of soluble sugars was approximately similar in wild-type plants and transgenic lines; at 4°C their level in transgenic plants was substantially lower than in control plants. As distinct from the process of cold adaptation, during recovery, the content of all tested stress-protection compounds dropped sharply. The results obtained indicate that active expression of the Osmyb4 gene from rice in the rape plants was accompanied not only by accumulation of compatible osmolytes but also by biosynthesis of antioxidants of phenolic nature.

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References

  1. Kuznetsov, Vl.V., Kimpel, J., Ki, J., and Gokdzhiyan, J., Elements of Genome Nonspecific Responses to Cold and Thermal Stresses, Sov. Plant Physiol., 1987, vol. 34, pp. 859–868.

    CAS  Google Scholar 

  2. Thomashow, M.F., Plant Cold Acclimation: Freezing Tolerance Genes and Regulatory Mechanisms, Annu. Rev. Plant Physiol., 1999, vol. 50, pp. 571–599.

    Article  CAS  Google Scholar 

  3. Kuznetsov, Vl.V., Physiological Mechanisms of Adaptation and Stress-Tolerant Plant Making, VII Kuprevichevskie chteniya (The 7th Kuprevich Lecture), Laman, N.A., Ed., Minsk: Tekhnologiya, 2009.

    Google Scholar 

  4. Gusta, L.V., Wilen, R.W., and Fu, P., Low Temperature Stress Tolerance: The Role of Abscisic Acid, Sugars, and Heat-Stable Proteins, HortScience, 1996, vol. 31, pp. 39–46.

    Google Scholar 

  5. 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 

  6. Amiri, R.M., Yur’eva, N.O., Shimshilashvili, K.R., Goldenkova-Pavlova, I.V., Pchelkin, V.P., Kuznetsova, E.I., Tsydendambaev, V.D., Trunova, T.I., Los, D.A., Jouzani, G.S., and Nosov, A.M., Expression of Acyl-Lipid delta-12-Desaturase Gene in Prokaryotic and Eukaryotic Cells and Its Effect on Cold Stress Tolerance of Potato, J. Integr. Plant Biol., 2010, vol. 52, pp. 289–297.

    Article  PubMed  CAS  Google Scholar 

  7. Kuznetsov, Vl.V. and Shevyakova, N.I., Proline under Stress: Biological Role, Metabolism, and Regulation, Russ. J. Plant Physiol., 1999, vol. 46, pp. 274–289.

    CAS  Google Scholar 

  8. Patton, A.J., Cunningham, S.M., Volenec, J.J., and Reicher, Z.J., Differences in Freeze Tolerance of Zoysiagrasses: II. Carbohydrate and Proline Accumulation, Crop Sci., 2007, vol. 47, pp. 2170–2181.

    Article  CAS  Google Scholar 

  9. 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 

  10. Vannini, C., Locatelli, F., Bracale, M., Magnani, E., Marsoni, M., Osnato, M., Mattana, M., Baldoni, E., and Coraggio, I., Overexpression of the Rice Osmyb4 Gene Increases Chilling and Freezing Tolerance of Arabidopsis thaliana Plants, Plant J., 2004, vol. 37, pp. 115–127.

    Article  PubMed  CAS  Google Scholar 

  11. Yamaguchi-Shinozaki, K. and Shinozaki, K., Organization of cis-Acting Regulatory Elements in Osmotic and Cold Stress Responsive Promoters, Trends Plant Sci., 2005, vol. 10, pp. 88–94.

    Article  PubMed  CAS  Google Scholar 

  12. Chinnusamy, V., Zhu, J., and Zhu, J.K., Gene Regulation under Cold Acclimation in Plants, Physiol. Plant., 2006, vol. 126, pp. 52–61.

    Article  CAS  Google Scholar 

  13. Park, M.-R., Yun, K.-Y., Mohanty, B., Herath, V., Xu, F., Wijaya, E., Balic, V.B., Yun, S.-J., and Reyes, B.G., Supra-Optimal Expression of the Cold-Regulated OsMyb4 Transcription Factor in Transgenic Rice Changes the Complexity of Transcriptional Network with Major Effects on Stress Tolerance and Panicle Development, Plant Cell Environ., 2010, vol. 33, pp. 2209–2230.

    Article  PubMed  CAS  Google Scholar 

  14. Du, H., Zhang, L., Tang, X.-F., Yang, W.-J., Wu, Y.-M., Huang, Y.-B., and Tang, Y.-X., Biochemical and Molecular Characterization of Plant MYB Transcription Factor Family, Biochemistry (Moscow), 2009, vol. 74, pp. 1–11.

    Article  CAS  Google Scholar 

  15. Pandolfi, D., Solinas, G., Valle, G., and Coraggio, I., Cloning of a cDNA Encoding a Novel myb Gene (accession no. y11414) Highly Expressed in Cold Stressed Rice Coleoptiles (PGR PGR97-079), Plant Physiol., 1997, vol. 114, p. 747.

  16. Mattana, M., Biazzi, E., Consonni, R., Locatelli, F., Vannini, C., Provera, S., and Coraggio, I., Overexpression of Osmyb4 Enhances Compatible Solute Accumulation and Increases Stress Tolerance of Arabidopsis thaliana, Physiol. Plant., 2005, vol. 125, pp. 212–223.

    Article  CAS  Google Scholar 

  17. Pasquali, G., Biricolti, S., Locatelli, F., Baldoni, E., and Mattana, M., Osmyb4 Expression Improves Adaptive Responses to Drought and Cold Stress in Transgenic Apples, Plant Cell Rep., 2008, vol. 27, pp. 1677–1686.

    Article  PubMed  CAS  Google Scholar 

  18. Vannini, C., Iriti, M., Bracale, M., Locatelli, F., Faoro, F., Croce, P., Pirona, R., di Maro, A., Coraggio, I., and Genga, A., The Ectopic Expression of the Rice Osmyb4 Gene in Arabidopsis Increases Tolerance to Abiotic, Environmental and Biotic Stresses, Physiol. Mol. Plant Pathol., 2006, vol. 69, pp. 26–42.

    Article  CAS  Google Scholar 

  19. Vannini, C., Campa, M., Iriti, M., Genga, A., Faoro, F., Carraviere, S., Rotino, G.L., Rossoni, V., Spinardi, A., and Bracale, M., Evaluation of Transgenic Tomato Plants Ectopically Expressing the Rice Osmyb4 Gene, Plant Sci., 2007, vol. 173, pp. 231–239.

    Article  CAS  Google Scholar 

  20. Malyshenko, S.I., Tyul’kina, L.G., Zvereva, S.D., and Raldugina, G.N., Transgenic Brassica campestris Plants Expressing the gfp Gene, Russ. J. Plant Physiol., 2003, vol. 50, pp. 276–281.

    Article  CAS  Google Scholar 

  21. Fulton, T.M., Chunwongse, J., and Tanksley, S.D., Micropreparative Protocol for Extraction of DNA from Tomato and Other Herbaceous Plants, Plant Mol. Biol. Rep., 1995, vol. 13, pp. 207–209.

    Article  CAS  Google Scholar 

  22. Pawlowski, K., Kunze, R., Vries, S., and Bisseling, T., Isolation of Total, Poly(A) and Polysomal RNA from Plant Tissues, Plant Molecular Biology. Manual D5, Gelvin, S.B. and Schilperoort, R.A., Eds., Dordrecht: Kluwer, 1994, pp. 1–13.

    Google Scholar 

  23. Turkina, M.V. and Sokolova, S.V., Methods for Monosaccharides and Oligosaccharide Determination, Biokhimicheskie metody v fiziologii rastenii (Biochemical Methods for Plant Physiology), Pavlinova, O.A., Ed., Moscow: Nauka, 1971, pp. 7–34.

    Google Scholar 

  24. Bates, L.S., Waldren, R.P., and Teare, I.D., Rapid Determination of Free Proline for Water Stress Studies, Plant Soil, 1973, vol. 39, pp. 205–207.

    Article  CAS  Google Scholar 

  25. Zagoskina, N.V., Dubravina, G.A., Alyavina, A.K., and Goncharuk, E.A., Effect of Ultraviolet (UV-B) Radiation on the Formation and Localization of Phenolic Compounds in Tea Plant Callus Cultures, Russ. J. Plant Physiol., 2003, vol. 50, pp. 270–275.

    Article  CAS  Google Scholar 

  26. Gage, T.B. and Wendei, S.H., Quantitative Determination of Certain Flavonol 3-Glycosides, Anal. Chem., 1950, vol. 22, pp. 708–711.

    Article  CAS  Google Scholar 

  27. Mabry, T.J., Markham, K.R., and Thomas, M.B., The Systematic Identification of Flavonoids, New York: Springer-Verlag, 1970, pp. 261–266.

    Google Scholar 

  28. Heath, R.L. and Packer, L., Photoperoxidation in Isolated Chloroplasts. Kinetics and Stoichiometry of Fatty Acid Peroxidation, Arch. Biochem. Biophys., 1968, vol. 125, pp. 189–198.

    Article  PubMed  CAS  Google Scholar 

  29. Radionov, N.V., Vagun, I.V., Paskarel, N.K., Kislova, U.L., Raldugina, G.N., Mattana, M., Vannini, K., and Kuznetsov, Vl.V., Transformation of Brassica napus and Nicotiana tabacum Plants with Osmyb4 Trans-Factor Gene for Production of Transgenic Plants Resistant to Unfavorable Conditions, Sovremennaya fiziologiya rastenii: ot molekul do ekosistem, Mater. Mezhd. konf. Ch. 2 (Current Plant Physiology: From Molecules to Ecosystems. Proc. Int. Conf., part 2), Syktyvkar: Komi Nauch. Tsentr Ural. Otd. Ros. Akad. Nauk, 2007, p. 337.

    Google Scholar 

  30. Hare, P.D., Cress, W.A., and van Staden, J., Dissecting the Roles of Osmolytes Accumulation during Stress, Plant Cell Environ., 1998, vol. 21, pp. 535–553.

    Article  CAS  Google Scholar 

  31. Michalak, A., Phenolic Compounds and Their Antioxidant Activity in Plants Growing under Heavy Metal Stress, Pol. J. Environ. Stud., 2006, vol. 15, pp. 523–530.

    CAS  Google Scholar 

  32. Chalker-Scott, L., Environmental Significance of Anthocyanins in Plant Stress Responses, Photochem. Photobiol., 1999, vol. 70, pp. 1–9.

    Article  CAS  Google Scholar 

  33. Sasaki, H. and Ishimura, K., and Odo, M., Changes in Sugar Content during Cold Acclimation and Deacclimation of Cabbage Seedlings, Ann. Bot., 1996, vol. 78, pp. 365–369.

    Article  CAS  Google Scholar 

  34. Burbulis, N., Kupriene, R., and Blinstrubiene, A., Investigation of Cold Resistance of Winter Rapeseed In Vitro, Sodinink. Darznink, 2008, vol. 27, pp. 223–232.

    Google Scholar 

  35. Bolouri-Moghaddam, M.R., Roy, K.L., Xiang, L., Rolland, F., and Ende, W.V., Sugar Signalling and Antioxidant Network Connections in Plant Cells, FEBS J., 2010, vol. 277, pp. 2022–2037.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to A. M. Gomaa.

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Original Russian Text © A.M. Gomaa, G.N. Raldugina, N.A. Burmistrova, N.V. Radionov, Vl.V. Kuznetsov, 2012, published in Fiziologiya Rastenii, 2012, Vol. 59, No. 1, pp. 118–128.

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Gomaa, A.M., Raldugina, G.N., Burmistrova, N.A. et al. Response of transgenic rape plants bearing the Osmyb4 gene from rice encoding a trans-factor to low above-zero temperature. Russ J Plant Physiol 59, 105–114 (2012). https://doi.org/10.1134/S1021443711060070

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