Abstract
Nitric oxide has been reported to enhance the tolerance of plants to biotic and abiotic stresses. Wheat is highly affected by heat stress at different stages of growth and development. Tolerance to heat stress (HS) at germination stage is important for wheat crop in Central and Peninsular India. Here, we studied the effect of pre-treatment of seeds with NO (150 µmol) on the activity of enzymes associated with germination and overall tolerance of seedlings of contrasting wheat cvs. Raj3765 and HD2932 under differential HS. NO was observed to self-regulate it’s biosynthesis through upregulation of NOS and NR in seedlings under NO and HS treatments. HSP90, HSP70, SOD and CAT showed very high expression in response to NO and HS, as compared to control. An increase in the activities of α/β-amylases were observed in response to NO and HS in seedlings. The NO effect was more pronounced in the seedlings of thermotolerance cv. Raj3765, as compared to thermosusceptible cv. HD2932. We observed an increase in the activities of antioxidant enzymes (SOD, CAT and POX) in response to NO. Enhancement of biochemical traits associated with thermotolerance were also observed in seedlings treated with NO under HS. NO mitigated the effect of HS by triggering the SAGs and antioxidant enzymes associated defence network and thus tolerance of wheat seedling to HS. This provides an easy and cheap method to mitigate the effect of HS on germination in wheat.
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References
Ahmad, P., Abdel Latef, A. A., Hashem, A., Abd Allah, E. F., Gucel, S., & Tran, L.-S. P. (2016). Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Frontiers in Plant Science, 7, 347. https://doi.org/10.3389/fpls.2016.00347.
Arora, D., Jain, P., Singh, N., Kaur, H., & Bhatla, S. C. (2016). Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants. Free Radical Research, 50(3), 291–303. https://doi.org/10.3109/10715762.2015.1118473.
Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205–207. https://doi.org/10.1007/BF00018060.
Bernfeld, P. (1955). Amylases, alpha and beta. Methods in Enzymology I. https://doi.org/10.1016/0076-6879(55)01021-5.
Besson-Bard, A., Pugin, A., & Wendehenne, D. (2008). New insights into nitric oxide signaling in plants. Annual Review of Plant Biology, 59, 21–39. https://doi.org/10.1146/annurev.arplant.59.032607.092830.
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254.
Briggs, D. E. (1967). Modified assay for amylase in germinating barley. Journal of the Institute of Brewing, 73(4), 361–370. https://doi.org/10.1002/j.2050-0416.1967.tb03055.x.
Chamizo-Ampudia, A., Sanz-Luque, E., Llamas, A., Galvan, A., & Fernandez, E. (2017). Nitrate reductase regulates plant nitric oxide homeostasis. Trends in Plant Science, 22(2), 163–174. https://doi.org/10.1016/j.tplants.2016.12.001.
Del Río, L. A., Corpas, F. J., & Barroso, J. B. (2004). Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry, 65(7), 783–792. https://doi.org/10.1016/j.phytochem.2004.02.001.
Domingos, P., Prado, A. M., Wong, A., Gehring, C., & Feijo, J. A. (2015). Nitric oxide: A multitasked signaling gas in plants. Molecular Plant, 8(4), 506–520. https://doi.org/10.1016/j.molp.2014.12.010.
Everse, J., Johnson, M. C., & Marini, M. A. (1994). Peroxidative activities of hemoglobin and hemoglobin derivatives. Methods in Enzymology, 231, 547–561. https://doi.org/10.1016/0076-6879(94)31038-6.
Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases: I occurrence in higher plants. Plant Physiology, 59(2), 309–314. https://doi.org/10.1104/pp.59.2.309.
Gross, F., Durner, J., & Gaupels, F. (2013). Nitric oxide, antioxidants and prooxidants in plant defence responses. Frontiers in Plant Science, 4, 419. https://doi.org/10.3389/fpls.2013.00419.
Guo, F.-Q., Okamoto, M., & Crawford, N. M. (2003). Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science, 302(5642), 100–103. https://doi.org/10.1126/science.1086770.
Hageman, R. H., & Hucklesby, D. P. (1971). Nitrate reductase from higher plants. Methods in Enzymology, 23, 491–503. https://doi.org/10.1016/S0076-6879(71)23121-9.
Klein, A., Hüsselmann, L., Keyster, M., & Ludidi, N. (2018). Exogenous nitric oxide limits salt-induced oxidative damage in maize by altering superoxide dismutase activity. South African Journal of Botany, 115, 44–49. https://doi.org/10.1016/j.sajb.2017.12.010.
Kumar, R.R., Goswami, S., Sharma, S.K., et al. (2012) Protection against heat stress in wheat involves change in cell membrane stability, antioxidant enzymes, osmolyte, H2O2 and transcript of heat shock protein. International Journal of Plant Physiology and Biochemistry, 4, 83–91. https://doi.org/10.5897/IJPPB12.008
Kumar, R. R., Goswami, S., Gadpayle, K.A., et al. (2013) Ascorbic acid at pre-anthesis modulate the thermotolerance level of wheat (Triticum aestivum) pollen under heat stress. Journal of Plant Biochemistry and Biotechnology, 23, 293–306. https://doi.org/10.1007/s13562-013-0214-x
Kumar, R. R., Goswami, S., Shamim, M., Mishra, P., Jain, M., Singh, K., et al. (2017). Biochemical defense response: Characterizing the plasticity of source and sink in spring wheat under terminal heat stress. Frontiers in Plant Science, 8, 1603. https://doi.org/10.3389/fpls.2017.01603.
Kumar, R. R., Goswami, S., Singh, K., Dubey, K., Rai, G. K., Singh, B., et al. (2018). Characterization of novel heat-responsive transcription factor (TaHSFA6e) gene involved in regulation of heat shock proteins (HSPs)—A key member of heat stress-tolerance network of wheat. Journal of Biotechnology, 279, 1–12. https://doi.org/10.1016/j.jbiotec.2018.05.008.
Kumar, R. R., Goswami, S., Singh, K., Dubey, K., Singh, S., Sharma, R., et al. (2016). Identification of putative RuBisCo Activase (TaRca1)—the catalytic chaperone regulating carbon assimilatory pathway in wheat (Triticum aestivum) under the heat stress. Frontiers in Plant Science, 7, 986. https://doi.org/10.3389/fpls.2016.00986.
Kumar, R. R., Sharma, S. K., Goswami, S., Verma, P., Singh, K., Dixit, N., et al. (2015). Salicylic acid alleviates the heat stress-induced oxidative damage of starch biosynthesis pathway by modulating the expression of heat-stable genes and proteins in wheat (Triticum aestivum). Acta Physiologiae Plantarum, 37(8), 1–12.
Kumar, R. R., Sharma, S. K., Rai, G. K., Singh, K., Choudhury, M., Dhawan, G., et al. (2014). Exogenous application of putrescine at pre-anthesis enhances the thermotolerance of wheat (Triticum aestivum L.). Indian Journal of Biochemistry and Biophysics, 51(5), 396–406.
Lamattina, L., García-Mata, C., Graziano, M., & Pagnussat, G. (2003). Nitric oxide: The versatility of an extensive signal molecule. Annual Review of Plant Biology, 54(1), 109–136. https://doi.org/10.1146/annurev.arplant.54.031902.134752.
Palavan-Unsal, N., & Arisan, D. (2009). Nitric oxide signalling in plants. Botanical Review, 75(2), 203–229. https://doi.org/10.1007/s12229-009-9031-2.
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleid Acids Research, 29(9), e45–e45.
Radi, R., Beckman, J. S., Bush, K. M., & Freeman, B. A. (1991). Peroxynitrite-induced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide. Archives of Biochemistry and Biophysics, 288(2), 481–487. https://doi.org/10.1016/0003-9861(91)90224-7.
Rockel, P., Strube, F., Rockel, A., Wildt, J., & Kaiser, W. M. (2002). Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. Journal of Experimental Botany, 53(366), 103–110. https://doi.org/10.1093/jxb/53.366.103.
Song, L., Ding, W., Zhao, M., Sun, B., & Zhang, L. (2006). Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Science, 171(4), 449–458. https://doi.org/10.1016/j.plantsci.2006.05.002.
Suriyasak, C., Harano, K., Tanamachi, K., Matsuo, K., Tamada, A., Iwaya-Inoue, M., et al. (2017). Reactive oxygen species induced by heat stress during grain filling of rice (Oryza sativa L.) are involved in occurrence of grain chalkiness. Journal of Plant Physiology, 216, 52–57. https://doi.org/10.1016/j.jplph.2017.05.015.
Uchida, A., Jagendorf, A. T., Hibino, T., Takabe, T., & Takabe, T. (2002). Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science, 163(3), 515–523. https://doi.org/10.1016/S0168-9452(02)00159-0.
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We duly acknowledge the financial assistance received from Indian Council of Agricultural Research (ICAR) under NICRA Project (TG3079).
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Kumar, R.R., Tasleem, M., Singh, K. et al. NO protect the wheat embryo from oxidative damage by triggering the biochemical defence network and amylolytic activity. Plant Physiol. Rep. 24, 35–45 (2019). https://doi.org/10.1007/s40502-019-0439-3
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DOI: https://doi.org/10.1007/s40502-019-0439-3