Improving Photosynthetic Responses during Recovery from Heat Treatments with Brassinosteroid and Calcium Chloride in Indian Bread Wheat Cultivars


Climate change is expected to unleash severe and frequent heat waves in future, adversely affecting crop productivity. The aim of this study was to examine the effect of two separate episodes of heat stress, mimicking heat wave conditions on the physiology of four Indian bread wheat cultivars and to study the ameliorating effects of epibrassinolide (BR) and calcium chloride on the recovery of these cultivars. The two thermo-tolerant cultivars C306 and K7903 suffered less inhibition of photosystem II efficiency as compared to the two thermo-susceptible cultivars HD2329 and PBW343. Application of BR and calcium chloride resulted in faster recovery in all the four cultivars. Measurement of the minimum fluorescence (Fo) versus temperature curves revealed a higher inflection temperature of Fo (Ti) for the two tolerant cultivars as compared to the susceptible cultivars, emphasizing greater thermo stability of the photosynthetic apparatus. The two thermo-tolerant cultivars showed higher photochemistry (ΦPSII) relative to the two susceptible cultivars. An increase in the steady state fluorescence was observed in both the susceptible cultivars as compared to the tolerant cultivars. Expression analysis revealed faster recovery of the transcripts involved in photosynthesis in tolerant cultivars as compared to susceptible cultivars. Exogenous application of the ameliorating compounds resulted in faster recovery of transcripts in all the cultivars. The result suggested that under severe stress conditions tolerant cultivars showed faster recovery and a better thermo-stability of its photosynthetic apparatus as compared to susceptible cultivars and application of epibrassinolide and calcium chloride could ameliorate the damaging effect of severe temperature stress to a considerable level in all the four cultivars under study.

Share and Cite:

Hairat, S. and Khurana, P. (2015) Improving Photosynthetic Responses during Recovery from Heat Treatments with Brassinosteroid and Calcium Chloride in Indian Bread Wheat Cultivars. American Journal of Plant Sciences, 6, 1827-1849. doi: 10.4236/ajps.2015.611184.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] IPCC (2007) Summary for Policymakers. In: Solomon. S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M. and Miller, H.L., Eds., Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge.
[2] Wagner, D. (1996) Scenarios of Extreme Temperature Events. Climate Change, 33, 385-407.
[3] White, T.A., Campbell, B.D., Kemp, P.D. and Hunt, C.L. (2001) Impacts of Extreme Climatic Events on Competition during Grassland Invasions. Global Change Biology, 7, 1-13.
[4] Garcia-Plazaola, J.I., Esteban, R., Hormaetxe, K., Fernandez-Marin, B. and Becerri, J.M. (2008) Photoprotective Responses of Mediterranean and Atlantic Trees to the Extreme Heat-Wave of Summer 2003 in Southwestern Europe. Trees, 22, 385-392.
[5] Wang, D., Heckathorn, S.A., Mainali, K. and Hamilton, E.W. (2008) Effects of N on Plant Response to Heat-Wave: A Field Study with Prairie Vegetation. Journal of Integrative Plant Biology, 50, 1416-1425.
[6] Luo, H.B., Ma, L., Xi, H.F., Duan, W., Li, S.H., Loescher, W., Wang, J.F. and Wang, L.J. (2011) Photosynthetic Responses to Heat Treatments at Different Temperatures and Following Recovery in Grapevine (Vitis amurensis L.) Leaves. PloS ONE, 6, 8.
[7] Koves, P.K., Biro, B., Voros, I., Takacs, T., Osztoics, E. and Strasser, R.J. (1998) Enhanced Activity of Microsymbiont-Alfalfa System Probed by the Fast Fluorescence Rise OJIP. In: Garab, P., Ed., Proceedings of the International Congress on Photosynthesis, Kluwer Academic Publishers, Dordrecht, 2765-2768.
[8] Percival, G.C. (2005) The Use of Chlorophyll Fluorescence to Identify Chemical and Environmental Stress in Leaf Tissue of Three Oak (Quercus) Species. Journal of Arboriculture, 31, 215-227.
[9] Georgieva, K. and Yordanov, I. (1993) Temperature Dependence of Chlorophyll Fluorescence Parameters of Pea Seedlings. Journal of Plant Physiology, 142, 151-155.
[10] Fujioka, S. and Yokota, T. (2003) Biosynthesis and Metabolism of Brassinosteroids. Annual Review Plant Biology, 5, 137-164.
[11] Sasse, J.M. (2003) Physiological Actions of Brassinosteroids: An Update. Journal of Plant Growth Regulation, 22, 276-288.
[12] Feldmann, K. (2006) Steroid Regulation Improves Crop Yield. Nature Biotechnology, 24, 46-47.
[13] Li, J.M. and Chory, J. (1997) A Putative Leucine Rich Repeat Receptor Kinase Involved in Brassinosteroid Signal Transduction. Cell, 90, 929-38.
[14] Yamamuro, C., Ihara, Y., Wu, X., Noguchi, T., Fujioka, S., Takatsuto, S., Ashikari, M., Kitano, H. and Matsuoka, M. (2000) Loss of Function of a Rice Brassinosteroid Insensitive 1 Homolog Prevents Internode Elongation and Bending of the Lamina Joint. The Plant Cell, 12, 1591-1605.
[15] Montoya, T., Nomura, T., Farrar, K., Kaneta, T., Yokota, T. and Bishop, G.J. (2002) Cloning the Tomato Curl3 Gene Highlights the Putative Dual Role of the Leucine-Rich Repeat Receptor Kinase tBRI1/SR160 in Plant Steroid Hormone and Peptide Hormone Signaling. The Plant Cell, 14, 3163-3176.
[16] Nomura, T., Bishop, G., Kaneta, T., Reid, J.B., Chory, J. and Yokota, T. (2003) The LKA Gene Is a BRASSINOSTEROID INSENSITIVE 1 Homolog of Pea. The Plant Journal, 36, 291-300.
[17] Sairam, R.K. (1994) Effect of Homobrasssinolide Application on Plant Metabolism and Grain Yield under Irrigated and Moisture-Stress Conditions of Two Wheat Cultivars. Journal of Plant Growth Regulation, 14, 173-181.
[18] Wang, B. and Zeng, G. (1993) Effect of Epibrassinolide on the Resistance of Rice Seedlings to Chilling Injury. Acta Phytophysiologica Sinica, 19, 38-42.
[19] Krishna, P. (2003) Brassinosteroid-Mediated Stress Resistance. Journal of Plant Growth Regulator, 22, 265-275.
[20] Kagale, S., Divi, U.K., Krochko, J.E., Keller, W.A. and Krishna, P. (2007) Brassinosteroid Confers Tolerance in Arabidopsis thaliana and Brassica napus to a Range of Abiotic Stresses. Planta, 225, 353-364.
[21] Dhaubhadel, S., Browning, K.S., Gallie, D.R. and Krishna, P. (2002) Brassinosteroid Functions to Protect the Translational Machinery and Heat-Shock Protein Synthesis Following Thermal Stress. The Plant Journal, 29, 681-691.
[22] Dhaubhadel, S., Chaudhary, S., Dobinson, K.F. and Krishna, P. (1999) Treatment with 24-Epibrassinolide, a Brassinosteroid, Increases the Basic Thermotolerance of Brassica napus and Tomato Seedlings. Plant Molecular Biology, 40, 333-342.
[23] Nayyar, H. and Kaushal, S.K. (2002) Alleviation of Negative Effects of Water Stress in Two Contrasting Wheat Genotypes by Calcium and Abscisic acid. Biology of Plant, 45, 65-70.
[24] Rentel, M.C. and Knight, M.R. (2004) Oxidative Stress-Induced Calcium Signaling in Arabidopsis. Plant Physiology, 135, 1471-1479.
[25] Sanders, D., Pelloux, J., Brownlee, C. and Harper, J.F. (2002) Calcium at the Crossroads of Signaling. The Plant Cell, 14, S401-S417.
[26] Noctor, G. (2006) Metabolic Signalling in Defence and Stress: The Central Roles of Soluble Redox Couples. The Plant Cell and Environment, 29, 409-425.
[27] Kaya, C. and Higgs, D. (2002) Calcium Nitrate as a Remedy for Salt-Stressed Cucumber Plants. Journal Plant Nutrition, 25, 861-871.
[28] Jaleel, C.A., Manivannan, P., Sankar, B., Kishorekumar, A., Gopi, R., Somasundaram, R. and Panneerselvam, R. (2007) Water Deficit Stress Mitigation by Calcium Chloride in Catharanthus roseus: Effects on Oxidative Stress, Proline Metabolism and Indole Alkaloid Accumulation. Colloids Surfaces B: Biointerfaces, 60, 110-116.
[29] Shao, H.B., Song, W.Y. and Chu, L.Y. (2008) Advances of Calcium Signals Involved in Plant Anti-Drought. Comptes Rendus Biologies, 331, 587-596.
[30] Wang, C.Q. and Song, H. (2009) Calcium Protects Trifolium repens L. Seedlings against Cadmium Stress. The Plant Cell Reports, 28, 1341-1349.
[31] Senthil-Kumar, M., Srikanthbabu, V., Mohan Raju, B., Ganeshkumar, Shivaprakash, N. and Udayakumar, M. (2003) Screening of Inbred Lines to Develop a Thermo-Tolerant Sunflower Hybrid Using the Temperature Induction Response (TIR) Technique: A Novel Approach by Exploiting Residual Variability. Journal of Experimental Botany, 54, 2569-2578.
[32] Hiscox, J.D. and Israelstam, G.F. (1979) A Method for Extraction of Chlorophyll from Leaf Tissue without Maceration. Canadian Journal of Botany, 57, 1332-1334.
[33] Almeselmani, M., Deshmukh, P.S., Sairam, R.K., Kushwaha, S.R. and Singh, T.P. (2006) Protective Role of Antioxidant Enzymes under High Temperature Stress. Plant Science, 171, 382-388.
[34] Fisher, R.A. and Maurer, R. (1978) Drought Resistance in Wheat Cultivars. I. Grain Yield Response. Journal of Agricultural Research, 29, 898-907.
[35] Mamedov, M., Hayashi, H. and Murata, N. (1993) Effects of Glycinebetaine and Unsaturation of Membrane Lipids on Heat Stability of Photosynthetic Electron-Transport and Phosphorylation Relations in Synechocystis PCC6803. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1142, 1-5.
[36] Demmig-Adams, B., Adams, W.W., Barker, D.H., Logan, B.A., Verhoeven, A.S. and Bowling, D.R. (1996) Using Chlorophyll Fluorescence to Assess the Fraction of Absorbed Light Allocated to Thermal Dissipation of Excess Excitation. Physiologia Plantarum, 98, 253-264.
[37] Muller, P., Li, X.P. and Niyogi, K.K. (2001) Non-Photochemical Quenching. A Response to Excess Light Energy. Plant Physiology, 125, 1558-1566.
[38] Kramer, D.M., Johnson, G., Kiirats, O. and Edwards, G.E. (2004) New Fluorescence Parameters for the Determination of Q (A) Redox State and Excitation Energy Fluxes. Photosynthesis Research, 79, 209-218.
[39] Anderson, J.M., Chow, W.S and Park, Y.I. (1995) The Grand Design of Photosynthesis: Acclimation of the Photosynthetic Apparatus to Environmental Cues. Photosynthesis Research, 46, 129-139.
[40] Schreiber, U. and Berry, J.A. (1977) Heat-Induced Changes of Chlorophyll Fluorescence in Intact Leaves Correlated with Damage of the Photosynthetic Apparatus. Planta, 136, 233-238.
[41] Srikanthbabu, V., Ganeshkumar, Krishnaprasad, B.T., Gopalakrishna, R., Savitha, M. and Udayakumar, M. (2002) Identification of Pea Genotypes with Enhanced Thermotolerance Using Temperature Induction Response Technique (TIR). Journal of Plant Physiology, 159, 535-545.
[42] Natu, P.S., Savitha, M., Babu, S. and Udayakumar, M. (2007) Heat Shock Response of Wheat Cultivars Differing in Thermotolerance. Indian Journal of Plant Physiology, 12, 327-336.
[43] Mangelsen, E., Kilian, J., Harter, K., Jansson, C., Wanke, D. and Sundberg, E. (2011) Transcriptome Analysis of High-Temperature Stress in Developing Barley Caryopses: Early Stress Responses and Effects on Storage Compound Biosynthesis. Molecular Plant, 4, 97-115.
[44] Chauhan, H., Khurana, N., Nijhavan, A., Khurana, J.P. and Khurana, P. (2012) The Wheat Chloroplastic Small Heat Shock Protein (sHSP26) Is Involved in Seed Maturation and Germination and Imparts Tolerance to Heat Stress. Plant, Cell and Environment, 35, 1912-1931.
[45] Ruban, A. and Murchie, E.H. (2012) Assessing the Photoprotective Effectiveness of Non-Photochemical Chlorophyll Fluorescence Quenching: A New Approach. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1817, 977-982.
[46] Schreiber, U. and Bilger, W. (1987) Rapid Assessment of Stress Effects on Plant Leaves by Chlorophyll Fluoreecence Measurements. In: Tenhunen, J.D., Catarino, F.M., Lange, O.L. and Oechel, W.C., Eds., Plant Response to Stress: Functional Analysis in Mediterranean Ecosystems, Springer-Verlag, Berlin, 27-53.
[47] Froux, F., Ducrey, M., Epron, D. and Dreyer, E. (2004) Seasonal Variations and Acclimation Potential of the Thermos- tability of Photochemistry in Four Mediterranean Conifers. Annals of Forest Science, 61, 235-241.
[48] Weng, J.H. and Lai, M.F. (2005) Estimating Heat Tolerance among Plant Species by Two Chlorophyll Fluorescence Parameters. Photosynthetica, 43, 439-444.
[49] Osmond, C.B. (1994) What Is Photoinhibition? Some Insights from Comparisons of Shade and Sun Plants. In: Baker, N.R. and Bowyer, J.R., Eds., Photoinhibition of Photosynthesis. From Molecular Mechanisms to the Field, BIOS Scientific Publishers, Oxford, 1-24.
[50] Blum, A. (1988) Plant Breeding for Stress Environments. CRC Press Inc., Boca Raton, 223.
[51] Quartacci, M.F., Pinzino, C., Sgherri, C.L.M., Vecchia, F.D. and Navari-Izzo, F. (2000) Growth in Excess Copper Induces Changes in the Lipid Composition and Fluidity of PSII-Enriched Membranes in Wheat. Physiologia Plantarum, 108, 87-93.
[52] Falcone, D.L., Ogas, J.P. and Somerville, C.R. (2004) Regulation of Membrane Fatty Acid Composition by Temperature in Mutants of Arabidopsis with Alterations in Membrane Lipid Composition. BMC Plant Biology, 4, 17.
[53] Mittler, R. and Poulos, T.L. (2005) Ascorbate Peroxidase. In: Smirnoff, N., Ed., Antioxidants and Reactive Oxygen Species in Plants, Blackwell Publishing, Oxford, 87-100.
[54] Rosa, S.B., Caverzan, A., Teixeira, F.K., Lazzarotto, F., Silveira, J.A.G., Ferreira-Silva, S.L., Abreu-Neto, J., Margis, R. and Margis-Pinheiro, M. (2010) Cytosolic APX Knockdown Indicates an Ambiguous Redox Responses in Rice. Phytochemistry, 71, 548-558.
[55] Khripach, V., Zhabinskii, V. and De Groot, A. (2000) Twenty Years of Brassinosteroids: Steroidal Plant Hormones Warrant Better Crops for the XXI Century. Annals of Botany, 86, 441-447.
[56] Nakashita, H., Yasuda, M., Nitta, T., Asami, T., Fujioka, S., Arai, Y., Sekimata, K., Takatsuto, S., Yamaguchi, I. and Yoshida, S. (2003) Brassinosteroid Functions in a Broad Range of Disease Resistance in Tobacco and Rice. The Plant Journal, 33, 887-898.
[57] Bishop, G.J. and Koncz, C. (2002) Brassinosteroids and Plant Steroid Hormone Signaling. The Plant Cell, 14, S97-S110.
[58] Mussig, C., Fischer, S. and Altmann, T. (2002) Brassinosteroid-Regulated Gene Expression. Plant Physiology, 129, 1241-1251.
[59] Cao, S.Q., Xu, Q.T., Cao, Y.J., Qian, K., An, K., Zhu, Y., Hu, B.Z., Zhao, H.F. and Kuai, B.K. (2005) Loss-of-Function Mutations in DET2 Gene Lead to an Enhanced Resistance to Oxidative Stress in Arabidopsis. Physiology Plant, 123, 57-66.
[60] Goda, H., Shimada, Y., Asami, T., Fujioka, S. and Yoshida, S. (2002) Microarray Analysis of Brassinosteroid-Regulated Genes in Arabidopsis. Plant Physiology, 130, 1319-1334.
[61] Gong, M., Van der Luit, A., Knight, M. and Trewavas, A. (1998) Heat-Shock Induces Changes in Intracellular Ca2+ Level in Tobacco Seedlings in Relation to Thermotolerance. Plant Physiology, 116, 429-437.
[62] Liu, H.T., Gao, F., Cui, S.J., Han, J.L., Sun, D.Y. and Zhou, R.G. (2006) Primary Evidence for Involvement of IP3 in Heat-Shock Signal Transduction in Arabidopsis. Cell Research, 16, 394-400.
[63] Saidi, Y., Finka, A., Muriset, M., Bromberg, Z., Weiss, Y.G., Maathuis, F.J., et al. (2009) The Heat Shock Response in Moss Plants is Regulated by Specific Calcium-Permeable Channels in the Plasma Membrane. The Plant Cell, 21, 2829-2843.
[64] Wu, H.C. and Jinn, T.L. (2010) Ethylesterase Activity and Cytosolic Ca2+ Oscillation Are Crucial for Plant Thermotolerance. Plant Signaling Behaviour, 5, 1252-1256.
[65] Zhang, W., Zhou, R.G., Gao, Y.J., Zheng, S.Z., Xu, P., Zhang, S.Q., et al. (2009) Molecular and Genetic Evidence for the Key Role of AtCaM3 in Heat-Shock Signal Transduction in Arabidopsis. Plant Physiology, 149, 1773-1784.

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.