Abstract
The role of gene of proline dehydrogenase (PDH) in the maintenance of stress tolerance was investigated using the model transgenic plants of tobacco (Nicotiana tabacum L.) carrying an antisense suppressor of PDH gene (a fragment of Arabidopsis PDH gene under the control of cauliflower mosaic virus 35S promoter in antisense orientation) and notable for a low activity of PDH and elevated content of proline. The progeny of transgenic plants belonging to the 5th generation (T5) with partially suppressed PDH activity was more resistant to various types of stress as compared with the control plants of tobacco, cv. Petit Havana SR-1 (SR1). The seedlings of transgenic lines cultured in Petri dishes on agar media supplemented with stress agents were resistant to high NaCl concentrations (200–300 mM) and water deficit simulated by an increased agar content in the medium (14 g/l) as compared to the control seedlings of cv. SR1. Juvenile plants of transgenic lines grown in pots filled with a mixture of vermiculite and perlite also manifested the higher resistance to water deficit and low temperatures (2°C and −2°C) than the control plants. Thus, the partial PDH suppression correlated with an increase in nonspecific resistance to different types of abiotic stress: salinity, water deficit, and low temperatures. Such transgenic lines of tobacco are promising genetic models for thorough investigation of molecular mechanisms of stress resistance in plants.
Similar content being viewed by others
Abbreviations
- BA:
-
benzyladenine
- Km:
-
kanamycin
- PDH:
-
proline dehydrogenase
References
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.
Verbruggen, N. and Hermans, C., Proline Accumulation in Plants: A Review, Amino Acids, 2008, vol. 35, pp. 753–759.
Radyukina, N.L., Shashukova, A.V., Shevyakova, N.I., and Kuznetsov, Vl.V., Effects of Various Iron Supply on Oxidative Stress Development and Ferritin Formation in the Common Ice Plants, Russ. J. Plant Physiol., 2008, vol. 55, pp. 649–656.
Szabados, L. and Savoure, A., Proline: A Multifunctional Amino Acid, Trends Plant Sci., 2010, vol. 15, pp. 89–97.
Lehmann, S., Funck, D., Szabados, L., and Rentsch, D., Proline Metabolism and Transport in Plant Development, Amino Acids, 2010, vol. 39, pp. 949–962.
Sreenivasulu, N., Sopory, S.K., and Kavi, Kishor, P.B., Deciphering the Regulatory Mechanisms of Abiotic Stress Tolerance in Plants by Genomic Approaches, Gene, 2007, vol. 388, pp. 1–13.
Kavi Kishor, P.B., Hong, Z., Miao, G.-H., Hu, C.-A.A., and Verma, D.P.S., Overexpression of a Delta-1-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants, Plant Physiol., 1995, vol. 108, pp. 1387–1394.
Xin, Z. and Browse, J., Eskimo1 Mutants of Arabidopsis Are Constitutively Freezing-Tolerant, Proc. Natl. Acad. Sci. USA., 1998, vol. 95, pp. 7799–7804.
Nanjo, T., Kobayashi, M., Yoshiba, Y., Kakubari, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K., Antisense Suppression of Proline Degradation Improves Tolerance to Freezing and Salinity in Arabidopsis thaliana, FEBS Lett., 1999, vol. 461, pp. 205–210.
Konstantinova, T., Parvanova, D., Atanassov, A., and Djilianov, D., Freezing Tolerant Tobacco, Transformed to Accumulate Osmoprotectants, Plant Sci., 2002, vol. 163, pp. 157–164.
Verdoy, D., Coba de la Peña, T., Redondo, F.J., Lucas, M.M., and Pueyo, J.J., Transgenic Medicago truncatula Plants That Accumulate Proline Display Nitrogen-Fixing Activity with Enhanced Tolerance to Osmotic Stress, Plant Cell Environ., 2006, vol. 29, pp. 1913–1923.
Mokhamed, A.M., Raldugina, G.N., Kholodova, V.P., and Kuznetsov, Vl.V., Osmolyte Accumulation in Different Rape Genotypes under Sodium Chloride Salinity, Russ. J. Plant Physiol., 2006, vol. 53, pp. 649–655.
Mokhamed, A.M., Titov, S.E., Kochetov, A.V., Raldugina, G.N., Kholodova, V.P., and Kuznetsov, Vl.V., Physiological and Molecular Characteristics of Transgenic Rape Plants with Antisense Suppressor of Proline Dehydrogenase Gene, Mater. IX Mezhd. konf. molodykh botanikov v Sankt-Peterburge (Proc. IX Int. Conf. of Young Botanists, St. Petersburg), St. Petersburg, 2006, pp. 201–202.
Maggio, A., Bressan, R.A., Hasegawa, P.M., and Locy, R.D., Moderately Increased Proline Level Does Not Alter Osmotic Stress Tolerance, Physiol. Plant., 1997, vol. 101, pp. 240–246.
Mani, S., van de Cotte, B., van Montagu, M., and Verbruggen, N., Altered Level of Proline Dehydrogenase Causes Hypersensitivity to Proline and Its Analogs in Arabidopsis, Plant Physiol., 2002, vol. 128, pp. 73–83.
Ribarits, A., Abdullaev, A., Tashpulatov, A., Richter, A., Heberle-Bors, E., and Touraev, A., Two Tobacco Proline Dehydrogenases Are Differentially Regulated and Play a Role in Early Plant Development, Planta, 2007, vol. 225, pp. 1313–1324.
Ueda, A., Shi, W., Shimada, T., Miyake, H., and Takabe, T., Altered Expression of Barley Proline Transporter Causes Different Growth Responses in Arabidopsis, Planta, 2008, vol. 227, pp. 277–286.
Hare, P.D. and Cress, W.A., Metabolic Implications of Stress-Induced Proline Accumulation in Plants, Plant Growth Regul., 1997, vol. 21, pp. 79–102.
Peng, Z., Lu, Q., and Verma, D.P., Reciprocal Regulation of Delta-1-Pyrroline-5-Carboxylate Synthetase and Proline Dehydrogenase Genes Controls Proline Levels during and after Osmotic Stress in Plants, Mol. Gen. Genet., 1996, vol. 253, pp. 334–341.
Kiyosue, T., Yoshiba, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K., A Nuclear Gene Encoding Mitochondrial Proline Dehydrogenase, an Enzyme Involved in Proline Metabolism, Is Upregulated by Proline but Downregulated by Dehydration in Arabidopsis, Plant Cell, 1996, vol. 8, pp. 1323–1335.
Kochetov, A.V., Titov, S.E., Kolodyazhnaya, Ya.S., Komarova, M.L., Koval, V.S., Makarova, N.N., Ilinskii, Yu.Yu., Trifonova, E.A., and Shumny, V.K., Tobacco Transformants Bearing Antisense Suppressor of Proline Dehydrogenase Gene Are Characterized by Higher Proline Content and Cytoplasm Osmotic Pressure, Genetika, 2004, vol. 40, pp. 282–285.
Kolodyazhnaya, Ya.S., Titov, S.E., Kochetov, A.V., Komarova, M.L., Romanova, A.V., Koval, V.S., and Shumny, V.K., Evaluation of Salt Tolerance in Nicotiana tabacum Plants Bearing an Antisense Suppressor of the Proline Dehydrogenase Gene, Genetika, 2006, vol. 42, pp. 278–281.
Kolodyazhnaya, Ya.S., Titov, S.E., Kochetov, A.V., Trifonova, E.A., Romanova, A.V., Komarova, M.L., Koval, V.S., and Shumny, V.K., Tobacco Transformants Expressing Antisense Sequence of Proline Dehydrogenase Gene Possess Tolerance to Heavy Metals, Genetika, 2007, vol. 43, pp. 994–998.
Gopal, J., Iwama, K., and Jitsuyama, Y., Effect of Water Stress Mediated through Agar In Vitro Growth of Potato, In Vitro Cell Dev. Biol. Plant, 2008, vol. 44, pp. 221–228.
Titov, S.E., Generation of Genetically Modified Nicotiana tabacum L. Plants Expressing Antisense Suppressor of Proline Dehydrogenase Gene, Abst. Cand. Sci. (Biol.) Diss., Novosibirsk: Inst. Cytol. Genet., Sib. Otd. Russ. Acad. Sci., 2008.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © S.S. Ibragimova, Ya.S. Kolodyazhnaya, S.V. Gerasimova, A.V. Kochetov, 2012, published in Fiziologiya Rastenii, 2012, Vol. 59, No. 1, pp. 99–107.
Rights and permissions
About this article
Cite this article
Ibragimova, S.S., Kolodyazhnaya, Y.S., Gerasimova, S.V. et al. Partial suppression of gene encoding proline dehydrogenase enhances plant tolerance to various abiotic stresses. Russ J Plant Physiol 59, 88–96 (2012). https://doi.org/10.1134/S1021443712010086
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443712010086