Differential Transcript Accumulation of Dhydrin and Beta-glucosidase Genes to Cold-induced Oxidative Stress in Chickpea

Authors
M. Khazaei 1
R. Maali-Amiri 1
A. R. Talei 1
S. Ramezanpour 2
1 Department of Agronomy and Plant Breeding, University College of Agriculture and Natural Resources, University of Tehran, Karaj, Islamic Republic of Iran.
2 Department of Plant Breeding and Biotechnology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Islamic Republic of Iran.
Abstract
In this study, accumulation of H2O2, malondialdehyde (MDA) (as cold-induced oxidative stress indicators), the transcript levels of dehydrin and beta-glucosidase genes (involved in metabolic responses) was evaluated in chickpea cv. Jam, using qRT-PCR during control, cold acclimation (CA), cold stress (CS), recovery, and freezing phases. Results showed the existence of wide range of genetic capacity in the cultivar to increase cold tolerance when environmental conditions change. Significant increase in H2O2 and MDA content during CA phase indicated that seedlings perceived cold signaling that resulted in remarkable increase in the transcript levels of dehydrin and beta-glucosidase genes as part of defense responses of plants. Balancing the expression of these genes and oxidative stress indicators showed the interplay between two major defense and injury pathways. During freezing phase, the higher transcript levels of these genes in acclimated plants compared to non-acclimated plants showed a more active role for plant cells. An incapability of defense machine in non-acclimated plants was a limiting factor determining the low potential of chickpea plants to freezing phase. It was suggested that adjustment and metabolic alterations like dehydrin and beta-glucosidase genes, especially after CA phase and, thereby, decrease in oxidative stress indicators, could be a reason for relative cold tolerance in chickpea.

Keywords

1. Amara, I., Odena, A., Oliveira, E., Moreno, A., Masmoudi, K., Pagès, M. and Goday, A. 2012. Insights into Maize LEA Proteins: From Proteomics to Functional Approaches. Plant Cell Physiol., 53: 312–329.
2. Baron, K. N., Schroeder, D. F. and Stasolla, C. 2012. Transcriptional Response of Abscisic Acid (ABA) Metabolism and Transport to Cold and Heat Stress Applied at the Reproductive Stage of Development in Arabidopsis thaliana. Plant Sci., 188–189: 48–59.
3. Bräutigam, K., Dietzel, L., Kleine, T., Ströher, E., Wormuth, D., Dietz, K. J., Radke, D., Wirtz, M., Hell, R., Dörmann, P., Nunes-Nesi, A., Schauer, N., Fernie, A. R., Oliver, S. N., Geigenberger, P., Leister, D. and Pfannschmidt, T. 2009. Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis. Plant Cell, 21: 2715–2732.
4. Byun, Y. J., Kim, J. K. and Dong, H. L. 2009. Long SAGE Analysis of the Early Response to Cold Stress in Arabidopsis Leaf. Planta, 229: 1181–1200.
5. Deryabin, A. N., Dubinina, I. M., Burakhanova, E. A., Astakhova, N. V., Sabel’nikova, E. P. and Trunova, T. I. 2005. Influence of Yeast-derived Invertase Gene Expression in Potato Plants on Membrane Lipid Peroxidation at Low Temperature. J. Thermal Biol., 30: 73–77.
6. Dietz, K. J., Sauter, R. A., Wichert, K., Messdaghi, D. and Hartung, W. 2000. Extracellular Beta-Glucosidase Activity in Barley Involved in the Hydrolysis of ABA Glucose Conjugate in Leaves. J. Exp. Bot., 51: 937–944.
7. Habibpour Mehraban, F., Maali Amiri, R., Nazari, M. R. and Zeinali, H. 2012. Genotypic Variability and Physio-Biochemical Characteristics of Iranian Black Chickpea to Cold Stress. Romanian Agric. Res., 29: 121–130.
8. Hara, M., Fujinaga, M. and Kuboi, T. 2005. Metal Binding by Citrus Dehydrin with Histidine-Rich Domains. J. Exp. Bot., 56: 2695–2703.
9. Heath, R. L. and Packer, L. 1968. Photoperoxidation in Isolated Chloroplasts. i. Kinetics and Stoichoimetry of Fatty Acid Peroxidation. Arch. Biochem. Biophys., 125: 189–215.
10. Heidarvand, L. and Maali Amiri, R. 2010. What Happens in Plant Molecular Responses to Cold Stress?. Acta Physiol. Plant., 32: 419–431.
11. Heidarvand, L., and Maali-Amiri, R. 2013. Physio-biochemical and Proteome Analysis of Chickpea in Early Phases of Cold Stress. J. Plant Physiol., 170: 459–469.
12. Heidarvand, L., Maali-Amiri, R., Naghavi, M. R., Farayedi, Y., Sadeghzadeh, B. and Alizadeh, K. 2011. Physiological and Morphological Characteristics of Chickpea Accessions under Low Temperature Stress. Russ. J. Plant Physiol., 58: 157–163.
13. Kazemi Shahandashti, S. S., Maali-Amiri, R., Zeinali, H. and Ramezanpour, S. S. 2013. Change in Membrane Fatty Acid Compositions and Cold-Induced Responses in Chickpea. Mol. Biol. Rep., 40: 893–903.
14. Ketudat Cairns, J. R. and Esen, A. 2010. β-glucosidases. Cell. Mol. Life Sci., 67: 3389–3405.
15. Kreps, J. A., Wu, Y., Chang, H. S., Zhu, T., Wang, X. and Harper, J. F. 2002. Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress. Plant Physiol., 130: 2129–2141.
16. Lee, K. H., Piao, H. L., Kim, H. Y., Choi, S. M., Jiang, F., Hartung, W., Hwang, I., Kwak, J. M., Lee, I. J. and Hwang, I. 2006. Activation of Glucosidase via Stress-induced Polymerization Rapidly Increases Active Pools of Abscisic Acid. Cell, 126: 1109–1120.
17. Loreto, F. and Velikova, V. 2001. Isoprene Production by Leave Protects the Photosynthetic Apparatus against Ozone Damage, Aquenches Ozone Products, and Reduces Lipid Proxidation of Cellular Membranes. Plant Physiol., 127: 1781–1787.
18. Maali-Amiri, R., Goldenkova-Pavlova, I. V., Pchelkin, V. P., Tsydendambaev, V. D., Vereshchagin, A. G., Deryabin, A. N., Trunova, T. I., Los, D. A. and Nosov, A. M. 2007. Lipid Fatty Acid Composition of Potato Plants Transformed with the Δ12-Desaturase Gene from Cyanobacterium. Russ. J. Plant Physiol., 54: 600–606.
19. Maali Amiri, R., Yur’eva, N. O., Shimshilashvili, K. R., Goldenkova-Pavlova, I. V., Pchelkin, V. P., Kuznitsova, E. I., Tsydendambaev, V. D., Trunova, T. I., Los, D. A., Salehi Jouzani, G. R. and Nosov, A. M. 2010. Expression of Acyl-lipid Δ12-desaturase Gene in Prokaryotic and Eukaryotic Cells and its Effect on Cold Stress Tolerance of Potato. J. Integr. Plant Biol., 52: 289–297.
20. Millan, T., Clarke, H. J., Siddique, K. H. M., Buhariwalla, H. K., Gaur, P. M., Kumar, J., Gil, J., Kahl, G. and Winter, P. 2006. Chickpea Molecular Breeding: New Tools and Concepts. Euphytica, 147: 81–103.
21. Nayyar, H., Bains, T. S. and Sanjeev, K. 2005. Chilling Stressed Chickpea Seedlings: Effect of Cold Acclimation, Calcium and Abscisic Acid on Cryoprotective Solutes and Oxidative Damage. Environ. Exp. Bot., 54: 275–285.
22. Pfaffl, M. W., Horgan, G. W. and Dempfle, L. 2002. Relative Expression Software Tool (REST) for Group-wise Comparison and Statistical Analysis of Relative Expression Results in Real-Time PCR. Nucleic Acids Res., 30: 36–46.
23. Puhakainen, T., Hess, M. W., Makela, P., Svensson, J., Heino, P. and Palva, E. T. 2004. Overexpression of Multiple Dehydrin Genes Enhances Tolerance to Freezing Stress in Arabidopsis. Plant Mol. Biol., 54: 743–753.
24. Vanacker, H., Carver, T. L. W. and Foyer, C. H. 2000. Early H2O2 Accumulation in Mesophyll Cells Leads to Induction of Glutathione during the Hyper-sensitive Response in the Barley-Powdery Mildew Interaction. Plant Physiol., 123: 1289–1300.
25. Sperotto, R. A., Ricachenevsky, F. K. and Fett, J. P. 2007. Deficiency in Rice Shoots: Identification of Novel Induced Genes Using RDA and Possible Relation to Leaf Senescence. Plant Cell Rep., 26: 1399–1411.
26. Zhu, J., Dong, C. H. and Zhu, J. K. 2007. Interplay between Cold-responsive Gene Regulation, Metabolism and RNA Processing during Plant Cold Acclimation. Curr. Opin. Plant Biol., 10: 290–295.
Journal of Agricultural Science and Technology
Volume 17, Issue 3
May and June 2015
Pages 725-734