Research Article
BibTex RIS Cite
Year 2023, , 65 - 74, 31.12.2023
https://doi.org/10.38042/biotechstudies.1332145

Abstract

References

  • Ageeva-Kieferle, A., Georgii, E., Winkler, B., Ghirardo, A., Albert, A., Hüther, P., Mengel, A., Becker, C., Schnitzler, J. P., Durner, J., & Lindermayr, C. (2021). Nitric oxide coordinates growth, development, and stress response via histone modification and gene expression. Plant physiology, 187(1), 336-360.https://doi.org/10.1093/plphys/kiab222
  • Akinci, S., & Losel, D. M. (2009). The soluble sugars determination in Cucurbitaceae species under water stress and recovery periods. Advances in Environmental Biology, 3(2), 175-183. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., Carrasco, P. & Tiburcio A. F. (2010). Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta, 231, 1237-1249. https://doi.org/10.1007/s00425-010-1130-0
  • Álvarez-Robles, M. J., López-Orenes, A., Ferrer, M. A. & Calderón, A. A. (2016). Methanol elicits the accumulation of bioactive steviol glycosides and phenolics in Stevia rebaudiana shoot cultures. Industrial Crops and Products, 87, 273–279.https://doi.org/10.1016/j.indcrop.2016.04.054
  • Antonić, S., Milošević, A., Cingel, M., Lojić, M., Trifunović-Momčilov, M., Petrić, A., Subotić, A. & Simonović, A. (2016). Effects of exogenous salicylic acid on Impatiens walleriana L. grown in vitro under polyethylene glycol-imposed drought. South African Journal of Botany, 105, 226-233. https://doi.org/10.1016/j.sajb.2016.04.002
  • Asgher, M., Per, T.S., Masood, A., Fatma, M., Freschi, L., Corpas, C. F. & Khan, N.A. (2017). Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environmental Science and Pollution Research, 24(3), 2273-2285.https://doi.org/10.1007/s11356-016-7947-8
  • Arasimowicz, M., & Floryszak-Wieczorek, J. (2007). Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Science, 172, 876-887.https://doi.org/10.1016/j.plantsci.2007.02.005
  • Bidabadi, S.S., Mahmood, M., Baninasab, B. & Ghobadi, C. (2012). Influence of salicylic acid on morphological and physiological responses of banana (Musa acuminata cv. ‘Berangan’, AAA) shoot tips to in vitro water stress induced by polyethylene glycol. Plant Omics, 5, 33-39.
  • Bitrián, M., Zarza, X., Altabella, T., Tiburcio, A. F., & Alcázar, R. (2012). Polyamines under Abiotic Stress: Metabolic Crossroads and Hormonal Crosstalks in Plants. Metabolites, 2(3), 516–528. https://doi.org/10.3390/metabo2030516
  • Cardenas-Manríquez, G., Vega-Muñoz, I., Villagómez-Aranda, A., León-Galvan, M., Cruz-Hernandez, A., Torres-Pacheco, I., Rangel-Cano, R., Rivera-Bustamante, R. & Guevara-Gonzalez, R. (2016). Proteomic and metabolomic profiles in transgenic tobacco (N. tabacum xanthi nc) to CchGLP from Capsicum chinense BG-3821 resistant to biotic and abiotic stresses. Environmental and Experimental Botany, 130, 33-41. https://doi.org/10.1016/j.envexpbot.2016.05.005
  • Chance, B. & Maehly, A. (1955). Assay of catalases and peroxidases. Methods in Enzymology, 2, 764-775.
  • Chavoushi, M., Najafi, F., Salimi, A. & Angaji, S.A. (2020). Effect of salicylic acid and sodium nitroprusside on growth parameters, photosynthetic pigments and secondary metabolites of safflower under drought stress. Scientia Horticulturae, 259. https://doi.org/10.1016/j.scienta.2019.108823
  • Chavoushi, M., Najafi, F., Salimi, A. & Angaji, S.A. (2019). Improvement in drought stress tolerance of safflower during vegetative growth by exogenous application of salicylic acid and sodium nitroprusside. Industrial Crops and Products, 134, 168-176. https://doi.org/10.1016/j.indcrop.2019.03.071
  • M. de Agazio, M., Grego, S., Ciofi-Luzzatto, A. Rea, E., Zaccaria, M.L. & Federico R. (1995). Inhibition of maize primary root elongation by spermidine: Effect on cell shape and mitotic index. Journal of Plant Growth Regulation, 14, 85-89. https://doi.org/10.1007/bf00203118
  • Durner, J. & Klessig, D. F. (1999). Nitric oxide as a signal in plants. Current Opinion in Plant Biology, 2, 369-374. Gantait, S., Das, A. & Mandal, N. (2015). Stevia: a comprehensive review on ethno-pharmacological properties and in vitro regeneration. Sugar Technology, 17, 95-106. https://doi.org/10.1007/s12355-014-0316-3
  • Gao, H. J., Yang, H. Q. & Wang, J. X. (2009). Arginine metabolism in roots and leaves of apple (Malus domestica Borkh.): the tissue-specific formation of both nitric oxide and polyamines. Scientia Horticulturae, 119, 147-15.https://doi.org/10.1016/j.scienta.2008.07.034
  • Gémes, K., Poór P., Horváth E., Kolbert Z., Szopkó D., Szepesi Á. & Tari, I. (2011). Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiologia Plantarum, 142, 179-192. https://doi.org/10.1111/j.1399-3054.2011.01461.x
  • Gholami Zali, A., & Ehsanzadeh, P. (2018). Exogenous proline improves osmoregulation, physiological functions, essential oil, and seed yield of fennel. Industrial Crops and Products, 111, 133-140. https://doi.org/10.1016/j.indcrop.2017.10.020
  • Giannopolitis, C. N. & Ries, S. K. (1977). Superoxide dismutases I. Occurrence in higher plants. Plant Physiology, 59, 309-314.
  • Giri, C. C. & Zaheer, M. (2016). Chemical elicitors versus secondary metabolite production in vitro using plant cell, tissue and organ cultures: recent trends and a sky eye view appraisal. Plant Cell Tiss Organ Culture, 126, 1-18. https://doi.org/10.1007/s11240-016-0985-6
  • Gunes, A., Inal, A., Alpaslan, M., Eraslan, F., Bagci, E. G. & Cicek, N. (2007). Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Plant Physiology, 164, 728-736. https://doi.org/10.1016/j.jplph.2005.12.009
  • Hajihashemi, S. & Geuns, J. M. (2017). Steviol glycosides correlation to genes transcription revealed in gibberellin and paclobutrazol-treated Stevia rebaudiana. Journal of Plant Biochemistry and Biotechnology, 26, 387-394. https://doi.org/10.1007/s13562-017-0399-5
  • Hancock, J. T. (2020). Nitric Oxide Signaling in Plants. Plants, 9 (11), 1550. https://doi.org/10.3390/plants9111550
  • Heath, R. L. & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125, 189-198.
  • Horváth, E., Pál, M., Szalai, G., Páldi, E., & Janda, T. (2007). Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. Biologia plantarum, 51(3), 480-487. https://doi.org/10.1007/s10535-007-0101-1
  • Iglesias, M. J., Terrile, M. C. & Casalongué, C. A. (2011). Auxin and salicylic acid signalings counteract the regulation of adaptive responses to stress. Plant Signal Behaviour, 6, 452-454. https://doi.org/10.4161/psb.6.3.14676
  • Jain, P., Kachhwah, S. & Kothari, S. (2014). Biotechnology and metabolic engineering of Stevia rebaudiana (Bert.) Bertoni: perspective and possibilities. International Journal of Life Sciences Biotechnology and Pharma Research, 3, 15.
  • JECFA (2007). Steviol glycosides. In: 68th JECFA-Chemical and Technical Assessment. Geneva, Switzerland.
  • Javed, R., Yücesan, B. & Gurel, E. (2018). Hydrogen peroxide-induced steviol glycosides accumulation and enhancement of antioxidant activities in leaf tissues of Stevia rebaudiana Bertoni. Sugar Technology, 20, 100-104. https://doi.org/10.1007/s12355-017-0521-y
  • Kazemi, N., Khavari-Nejad, R. A., Fahimi, H., Saadatmand, S. & Nejad-Sattari, T. (2010). Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Scientia Horticulturae, 126, 402-407.https://doi.org/10.1016/j.scienta.2010.07.037
  • Kevers, C., Gaspar, T. & Jacques, D. (2002). The beneficial role of different auxins and polyamines at successive stages of somatic embryo formation and development of Panax ginseng in vitro. Plant Cell Tissue Organ Culture, 70, 181-188.
  • Khan, M. I. R., Fatma, M., Per, T. S., Anjum, N. A., & Khan, N. A. (2015). Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Frontiers in Plant Science, 6, 462. https://doi.org/10.3389/fpls.2015.00462
  • Khokon, M., Okuma, E. I., Hossain, M. A., Munemasa, S., Uraji, M., Nakamura, Y., Mori, I. C. & Murata, Y. (2011). Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell Environment, 34, 434-443. https://doi.org/10.1111/j.1365-3040.2010.02253.x
  • Kolb, N., Herrera, J. L., Ferreyra, D. J. & Uliana, R. F. (2001). Analysis of Sweet Diterpene Glycosides from Stevia rebaudiana: Improved HPLC Method. Journal of Agricultural and Food Chemistry, 49, 4538-4541. https://doi.org/10.1021/jf010475p
  • Kong, J., Dong, Y., Xu, L., Liu, S. & Bai, X. (2014). Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of (Arachis hypogaea L.). Botanical Studuies, 55, 1-12. https://doi.org/10.1186/1999-3110-55-9
  • Kumar, D. & Klessig, D. F. (2000). Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Molecular Plant-Microbe Interact, 13, 347-351. https://doi.org/10.1094/mpmi.2000.13.3.347
  • Kumar, H., Kaul, K., Bajpai-Gupta, S., Kaul, V. K. & Kumar, S. (2012). A comprehensive analysis of fifteen genes of steviol glycosides biosynthesis pathway in Stevia rebaudiana (Bertoni). Gene, 492, 276-284. https://doi.org/10.1016/j.gene.2011.10.015
  • Li, Z., Zhang, Y., Zhang, X., Peng, Y., Merewitz, E., Ma, X., Huang, L. & Yan, Y. (2016). The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white clover. Environmental and Experimental Botany, 124, 22-38. https://doi.org/10.1016/j.envexpbot.2015.12.004
  • Lipton, S. A., Choi, Y. B., Pan, Z. H., Lei, S. Z. & Chen, H. S. (1993). A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature, 364, 626-632. https://doi.org/10.1038/364626a0
  • Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randal, R. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193, 65-75. https://doi.org/10.1016/s0021-9258(19)52451-6
  • Manjunatha, G., Lokesh, V. & Neelwarne, B (2010). Nitric oxide in fruit ripening: trends and opportunities. Biotechnology Advances 28, 489-499. https://doi.org/10.1016/j.biotechadv.2010.03.001
  • Mathur, S. & Shekhawat, G. S. (2013). Establishment and characterization of Stevia rebaudiana (Bertoni) cell suspension culture: an in vitro approach for production of stevioside. Acta Physiologia Plantarum, 35(3), 931-939. https://doi.org/10.1007/s11738-012-1136-2
  • Metwally, A., Finkemeier, I., Georgi, M. & Dietz, K. J. (2003). Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiology, 132, 272-281. https://doi.org/10.1104/pp.102.018457
  • Miura, K., & Tada, Y. (2014). Regulation of water, salinity, and cold stress responses by salicylic acid. Frontiers in Plant Science, 5, 4. https://doi.org/10.3389/fpls.2014.00004
  • Moharramnejad, S., Azam, A. T., Panahandeh, J., Dehghanian, Z. & Muhammad, A. (2019). Effect of Methyl Jasmonate and Salicylic Acid on In Vitro Growth, Stevioside Production, and Oxidative Defense System in Stevia rebaudiana. Sugar Technology, 21, 1031-1038. https://doi.org/10.1007/s12355-019-00727-8
  • Mora-Herrera, M. E., Lopez-Delgado, H., Castillo-Morales, A. & Foyer, C. H. (2005). Salicylic acid and H2O2 function by independent pathways in the induction of freezing tolerance in potato. Physiologia Plantarum, 125(4), 430-440.https://doi.org/10.1111/j.1399-3054.2005.00572.x
  • Nahar, K., Hasanuzzaman, M., Alam, M. M., Rahman, A., Suzuki, T. & Fujita, M. (2016). Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology and Environmental Safety, 126, 245-255. https://doi.org/10.1016/j.ecoenv.2015.12.026
  • Naser Alavi, S. M., Arvin, M. J. & Manoochehri Kalantari, K. (2014). Salicylic acid and nitric oxide alleviate osmotic stress in wheat (Triticum aestivum L.) seedlings. Journal of Plant Interactions, 9, 683-688. https://doi.org/10.1080/17429145.2014.900120
  • Nawaz, F., Shabbir, R. N., Shahbaz, M., Majeed, S., Raheel, M., Hassan, W. & Sohail, M. A. (2017). Cross talk between nitric oxide and phytohormones regulate plant development during abiotic stresses. In M. El-Esawi (Ed.), Phytohormones-signaling mechanisms and crosstalk in plant development and stress responses (1st ed., pp. 117-141). InTech. https://doi.org/10.5772/intechopen.69812
  • Pacheco, A. C., da Silva Cabral, C., da Silva Fermino, E. S. & Aleman, C. C. (2013). Salicylic acid induced changes to growth, flowering and flavonoids production in marigold plants. Medicinal Plants Research, 7, 3158-3163.
  • Popova, L. & Tuan, T. (2010). Nitric oxide in plants: Properties, biosynthesis, and physiological functions. Iranian Journal of Science and Technology Transaction A: Science, 34, 173-183.
  • Pradhan, N., Singh, P., Dwivedi, P. & Pandey, D.K. (2020). Evaluation of sodium nitroprusside and putrescine on polyethylene glycol induced drought stress in Stevia rebaudiana Bertoni under in vitro condition. Industrial Crops and Products, 154. https://doi.org/10.1016/j.indcrop.2020.112754
  • Rahdari, P. & Hoseini, M. (2012). Drought stress: a review. International Journal of Agronomy and Plant Production, 10, 443-446.
  • Raskin, I. (1992). Role of salicylic acid in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 43, 439-463. https://doi.org/10.1146/annurev.pp.43.060192.002255
  • Razmi, N., Ebadi, A., Jahanfar Daneshian, J., & Soodabeh Jahanbakhsh (2017). Salicylic acid induced changes on antioxidant capacity, pigments, and grain yield of soybean genotypes in water deficit condition, Journal of Plant Interactions, 12, 457-464. https://doi.org/10.1080/17429145.2017.1392623
  • Sadeghipour, O. & Aghaei, P. (2012). Impact of exogenous salicylic acid application on sometraits of common bean (Phaseolus vulgaris L.) under water stress conditions. International Journal of Agriculture and Crop Sciences, 4, 685-690.
  • Safari, M., Mousavi-Fard, S., Rezaei Nejad, A., Sorkheh K. & Sofo A. (2022). Exogenous salicylic acid positively affects morpho-physiological and molecular responses of Impatiens walleriana plants grown under drought stress. International Journal of Environmental Science and Technology, 19, 969-984. https://doi.org/10.1007/s13762-020-03092-2
  • Sequera-Mutiozabal, M., Antoniou, C., Tiburcio, A. F., Alcázar R. & Fotopoulos V. (2017). Polyamines: Emerging Hubs Promoting Drought and Salt Stress Tolerance in Plants. Current Molecular Biology Reports, 3, 28-36. https://doi.org/10.1007/s40610-017-0052-z
  • Seyis, F., Yurteri, E. & Özcan, A. (2017). In Vitro Multiplication of Stevia rebaudiana (Bertoni) Genotypes Using Different Explants. International Journal of Crop Science and Technology, 3(2), 36-41. https://doi.org/10.26558/ijcst.326792
  • Shehab, G. G., Ahmed, O. K. & El-Beltagi, H. S. (2010). Effects of various chemical agents for alleviation of drought stress in rice plants (Oryza sativa L.). Notulae Botanicae Horti Agrobotanici Cluj, 38, 139-148.
  • Sichanova, M., Geneva, M., Petrova, M., Miladinova-Georgieva, K., Kirova, E., Nedev, T., Tsekova, D., Iwanov, I., Dochev, K., Ivanova, V., & Trendafilova, A. (2022). Improvement of Stevia rebaudiana Bertoni In Vitro Propagation and Steviol Glycoside Content Using Aminoacid Silver Nanofibers. Plants, 11(19), 2468. https://doi.org/10.3390/plants11192468
  • Singh, G., Singh, G., Singh, P., Parmar, R., Paul, N., Vashist, R., Swarnkar, M. K., Kumar, A., Singh, S. & Singh, A. K. (2017). Molecular dissection of transcriptional reprogramming of steviol glycosides synthesis in leaf tissue during developmental phase transitions in Stevia rebaudiana Bert. Scientific Reports, 7, 11835. https://doi.org/10.1038/s41598-017-12025-y
  • Szepesi, Á., Csiszár, J., Gémes, K., Horváth, E., Horváth, F., Simo, M.L. & Tari, I. (2009). Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. Journal of Plant Physiology, 9, 914-925. https://doi.org/10.1016/j.jplph.2008.11.012
  • Şahin, G. (2019). Effects of salicylic acid and heat acclimation on thermotolerance and withanolide accumulation under high temperature stress in the Cape gooseberry (Physalis peruviana L.) Turkish Journal of Botany, 43, 468-474. https://doi.org/10.3906/bot-1901-4
  • Tadhani, M., Patel, V. & Subhash, R. (2007). In vitro antioxidant activities of Stevia rebaudiana leaves and callus. Journal of Food Compostion and Analysis, 20, 323-329. https://doi.org/10.1016/j.jfca.2006.08.004
  • Tun, N. N., Santa-Catarina, C., Begum, T., Silveira, V., Handro, W., Floh, EIS, Scherer, G. F. (2006). Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiology, 47, 346-354. https://doi.org/10.1093/pcp/pci252
  • Uddin, M. S., Chowdhury, M. S. H., Khan, M. M. M. H., Uddin, M. B., Ahmed, R. & Baten, M. (2006). In vitro propagation of Stevia rebaudiana Bert in Bangladesh. African Journal of Biotechnology, 5, 1238-1240.
  • Vasquez-Hernandez, C., Feregrino-Perez, A. A., Perez-Ramirez, I., Ocampo-Velazqueza, R. V., Rico-García E., Torres-Pacheco I. & Guevara-Gonzaleza R. G. (2019). Controlled elicitation increases steviol glycosides (SGs) content and gene expression-associated to biosynthesis of SGs in Stevia rebaudiana B. cv. Morita II. Industrial Crops and Products, 139, 111479. https://doi.org/10.1016/j.indcrop.2019.111479
  • Vázquez-Hernández, M. C., Parola-Contreras, I., Montoya-Gómez, L. M., Torres-Pacheco, I., Schwarz, D. & Guevara-González, R. G. (2019). Eustressors: chemical and physical stress factors used to enhance vegetables production. Scientia Horticulture, 250, 223-229. https://doi.org/10.1016/j.scienta.2019.02.053
  • Yildiztugay, E., Ozfidan-Konakci, C. & Kucukoduk, M. (2014). Exogenous nitric oxide (as sodium nitroprusside) ameliorates polyethylene glycol induced osmotic stress in hydroponically grown maize roots. Plant Growth Regulation, 330, 683-696. https://doi.org/10.1007/s00344-014-9417-1
  • Yin, Z. P., Li S., Ren, J. & Song, X. S. (2014). Role of spermidine and spermine in alleviation of drought-induced oxidative stress and photosynthetic inhibition in Chinese dwarf cherry (Cerasus humilis) seedlings. Plant Growth Regulation, 74, 209-218. https://doi.org/10.1007/s10725-014-9912-1
  • Yoneda, Y., Shimizu, H., Nakashima, H., Miyasaka, J. & Ohdoi, K. (2018). Effect of treatment with gibberellin, gibberellin biosynthesis inhibitör, and auxin on steviol glycoside content in Stevia rebaudiana bertoni. Sugar Technology, 20(4), 482-491. https://doi.org/10.1007/s12355-017-0561-3
  • Zhu, J. K. (2001). Cell signaling under salt, water, and cold stresses. Current Opinion in Plant Biology, 4(5), 401–406. https://doi.org/10.1016/s1369-5266(00)00192-8
  • Zottini, M., Costa, A., De Michele, R., Ruzzene, M., Carimi, F. & Lo Schiavo, F. (2007). Salicylic acid activates nitric oxide synthesis in Arabidopsis. Journal of Experimental Botany, 58(6), 1397-1405. https://doi.org/10.1093/jxb/erm001

Effects of nitric oxide, spermidine, and salicylic acid signaling and their crosstalk with each other in the production of commercially important stevioside content and drought stress responses in Stevia rebaudiana bertoni

Year 2023, , 65 - 74, 31.12.2023
https://doi.org/10.38042/biotechstudies.1332145

Abstract

The leaves of Stevia rebaudiana Bertoni contain steviol glycosides (SGs), which provide the sweet taste of stevia. However, drought can have a negative impact on the plant's growth and development. To address this issue, signaling molecules such as sodium nitroprusside (SNP), spermidine (SPD), and salicylic acid (SA) are often applied to increase plant tolerance. However, the combined effects of these molecules have not been extensively studied. This research aimed to investigate the effects of controlled elicitation with SA, SNP, SPD, and their combinations on plant performance, SG content, and drought stress mitigation in Stevia rebaudiana under drought stress. The elicitor treatments were found to result in a significant increase in SG content, with 0.1 mM SA being the most effective treatment. Additionally, the treatments were able to reduce the stress effects on growth parameters to non-stress levels. The use of SPD, SA+SNP, and SPD+SNP on stressed plants significantly increased CAT and SOD activity, resulting in a more active antioxidant defense system that lowered MDA contents and H2O2 generation. These findings suggest that stevia cultivation with controlled elicitation could be used to improve plant growth, tolerance, and SG production under drought stress conditions.

References

  • Ageeva-Kieferle, A., Georgii, E., Winkler, B., Ghirardo, A., Albert, A., Hüther, P., Mengel, A., Becker, C., Schnitzler, J. P., Durner, J., & Lindermayr, C. (2021). Nitric oxide coordinates growth, development, and stress response via histone modification and gene expression. Plant physiology, 187(1), 336-360.https://doi.org/10.1093/plphys/kiab222
  • Akinci, S., & Losel, D. M. (2009). The soluble sugars determination in Cucurbitaceae species under water stress and recovery periods. Advances in Environmental Biology, 3(2), 175-183. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., Carrasco, P. & Tiburcio A. F. (2010). Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta, 231, 1237-1249. https://doi.org/10.1007/s00425-010-1130-0
  • Álvarez-Robles, M. J., López-Orenes, A., Ferrer, M. A. & Calderón, A. A. (2016). Methanol elicits the accumulation of bioactive steviol glycosides and phenolics in Stevia rebaudiana shoot cultures. Industrial Crops and Products, 87, 273–279.https://doi.org/10.1016/j.indcrop.2016.04.054
  • Antonić, S., Milošević, A., Cingel, M., Lojić, M., Trifunović-Momčilov, M., Petrić, A., Subotić, A. & Simonović, A. (2016). Effects of exogenous salicylic acid on Impatiens walleriana L. grown in vitro under polyethylene glycol-imposed drought. South African Journal of Botany, 105, 226-233. https://doi.org/10.1016/j.sajb.2016.04.002
  • Asgher, M., Per, T.S., Masood, A., Fatma, M., Freschi, L., Corpas, C. F. & Khan, N.A. (2017). Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environmental Science and Pollution Research, 24(3), 2273-2285.https://doi.org/10.1007/s11356-016-7947-8
  • Arasimowicz, M., & Floryszak-Wieczorek, J. (2007). Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Science, 172, 876-887.https://doi.org/10.1016/j.plantsci.2007.02.005
  • Bidabadi, S.S., Mahmood, M., Baninasab, B. & Ghobadi, C. (2012). Influence of salicylic acid on morphological and physiological responses of banana (Musa acuminata cv. ‘Berangan’, AAA) shoot tips to in vitro water stress induced by polyethylene glycol. Plant Omics, 5, 33-39.
  • Bitrián, M., Zarza, X., Altabella, T., Tiburcio, A. F., & Alcázar, R. (2012). Polyamines under Abiotic Stress: Metabolic Crossroads and Hormonal Crosstalks in Plants. Metabolites, 2(3), 516–528. https://doi.org/10.3390/metabo2030516
  • Cardenas-Manríquez, G., Vega-Muñoz, I., Villagómez-Aranda, A., León-Galvan, M., Cruz-Hernandez, A., Torres-Pacheco, I., Rangel-Cano, R., Rivera-Bustamante, R. & Guevara-Gonzalez, R. (2016). Proteomic and metabolomic profiles in transgenic tobacco (N. tabacum xanthi nc) to CchGLP from Capsicum chinense BG-3821 resistant to biotic and abiotic stresses. Environmental and Experimental Botany, 130, 33-41. https://doi.org/10.1016/j.envexpbot.2016.05.005
  • Chance, B. & Maehly, A. (1955). Assay of catalases and peroxidases. Methods in Enzymology, 2, 764-775.
  • Chavoushi, M., Najafi, F., Salimi, A. & Angaji, S.A. (2020). Effect of salicylic acid and sodium nitroprusside on growth parameters, photosynthetic pigments and secondary metabolites of safflower under drought stress. Scientia Horticulturae, 259. https://doi.org/10.1016/j.scienta.2019.108823
  • Chavoushi, M., Najafi, F., Salimi, A. & Angaji, S.A. (2019). Improvement in drought stress tolerance of safflower during vegetative growth by exogenous application of salicylic acid and sodium nitroprusside. Industrial Crops and Products, 134, 168-176. https://doi.org/10.1016/j.indcrop.2019.03.071
  • M. de Agazio, M., Grego, S., Ciofi-Luzzatto, A. Rea, E., Zaccaria, M.L. & Federico R. (1995). Inhibition of maize primary root elongation by spermidine: Effect on cell shape and mitotic index. Journal of Plant Growth Regulation, 14, 85-89. https://doi.org/10.1007/bf00203118
  • Durner, J. & Klessig, D. F. (1999). Nitric oxide as a signal in plants. Current Opinion in Plant Biology, 2, 369-374. Gantait, S., Das, A. & Mandal, N. (2015). Stevia: a comprehensive review on ethno-pharmacological properties and in vitro regeneration. Sugar Technology, 17, 95-106. https://doi.org/10.1007/s12355-014-0316-3
  • Gao, H. J., Yang, H. Q. & Wang, J. X. (2009). Arginine metabolism in roots and leaves of apple (Malus domestica Borkh.): the tissue-specific formation of both nitric oxide and polyamines. Scientia Horticulturae, 119, 147-15.https://doi.org/10.1016/j.scienta.2008.07.034
  • Gémes, K., Poór P., Horváth E., Kolbert Z., Szopkó D., Szepesi Á. & Tari, I. (2011). Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiologia Plantarum, 142, 179-192. https://doi.org/10.1111/j.1399-3054.2011.01461.x
  • Gholami Zali, A., & Ehsanzadeh, P. (2018). Exogenous proline improves osmoregulation, physiological functions, essential oil, and seed yield of fennel. Industrial Crops and Products, 111, 133-140. https://doi.org/10.1016/j.indcrop.2017.10.020
  • Giannopolitis, C. N. & Ries, S. K. (1977). Superoxide dismutases I. Occurrence in higher plants. Plant Physiology, 59, 309-314.
  • Giri, C. C. & Zaheer, M. (2016). Chemical elicitors versus secondary metabolite production in vitro using plant cell, tissue and organ cultures: recent trends and a sky eye view appraisal. Plant Cell Tiss Organ Culture, 126, 1-18. https://doi.org/10.1007/s11240-016-0985-6
  • Gunes, A., Inal, A., Alpaslan, M., Eraslan, F., Bagci, E. G. & Cicek, N. (2007). Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Plant Physiology, 164, 728-736. https://doi.org/10.1016/j.jplph.2005.12.009
  • Hajihashemi, S. & Geuns, J. M. (2017). Steviol glycosides correlation to genes transcription revealed in gibberellin and paclobutrazol-treated Stevia rebaudiana. Journal of Plant Biochemistry and Biotechnology, 26, 387-394. https://doi.org/10.1007/s13562-017-0399-5
  • Hancock, J. T. (2020). Nitric Oxide Signaling in Plants. Plants, 9 (11), 1550. https://doi.org/10.3390/plants9111550
  • Heath, R. L. & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125, 189-198.
  • Horváth, E., Pál, M., Szalai, G., Páldi, E., & Janda, T. (2007). Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. Biologia plantarum, 51(3), 480-487. https://doi.org/10.1007/s10535-007-0101-1
  • Iglesias, M. J., Terrile, M. C. & Casalongué, C. A. (2011). Auxin and salicylic acid signalings counteract the regulation of adaptive responses to stress. Plant Signal Behaviour, 6, 452-454. https://doi.org/10.4161/psb.6.3.14676
  • Jain, P., Kachhwah, S. & Kothari, S. (2014). Biotechnology and metabolic engineering of Stevia rebaudiana (Bert.) Bertoni: perspective and possibilities. International Journal of Life Sciences Biotechnology and Pharma Research, 3, 15.
  • JECFA (2007). Steviol glycosides. In: 68th JECFA-Chemical and Technical Assessment. Geneva, Switzerland.
  • Javed, R., Yücesan, B. & Gurel, E. (2018). Hydrogen peroxide-induced steviol glycosides accumulation and enhancement of antioxidant activities in leaf tissues of Stevia rebaudiana Bertoni. Sugar Technology, 20, 100-104. https://doi.org/10.1007/s12355-017-0521-y
  • Kazemi, N., Khavari-Nejad, R. A., Fahimi, H., Saadatmand, S. & Nejad-Sattari, T. (2010). Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Scientia Horticulturae, 126, 402-407.https://doi.org/10.1016/j.scienta.2010.07.037
  • Kevers, C., Gaspar, T. & Jacques, D. (2002). The beneficial role of different auxins and polyamines at successive stages of somatic embryo formation and development of Panax ginseng in vitro. Plant Cell Tissue Organ Culture, 70, 181-188.
  • Khan, M. I. R., Fatma, M., Per, T. S., Anjum, N. A., & Khan, N. A. (2015). Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Frontiers in Plant Science, 6, 462. https://doi.org/10.3389/fpls.2015.00462
  • Khokon, M., Okuma, E. I., Hossain, M. A., Munemasa, S., Uraji, M., Nakamura, Y., Mori, I. C. & Murata, Y. (2011). Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell Environment, 34, 434-443. https://doi.org/10.1111/j.1365-3040.2010.02253.x
  • Kolb, N., Herrera, J. L., Ferreyra, D. J. & Uliana, R. F. (2001). Analysis of Sweet Diterpene Glycosides from Stevia rebaudiana: Improved HPLC Method. Journal of Agricultural and Food Chemistry, 49, 4538-4541. https://doi.org/10.1021/jf010475p
  • Kong, J., Dong, Y., Xu, L., Liu, S. & Bai, X. (2014). Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of (Arachis hypogaea L.). Botanical Studuies, 55, 1-12. https://doi.org/10.1186/1999-3110-55-9
  • Kumar, D. & Klessig, D. F. (2000). Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Molecular Plant-Microbe Interact, 13, 347-351. https://doi.org/10.1094/mpmi.2000.13.3.347
  • Kumar, H., Kaul, K., Bajpai-Gupta, S., Kaul, V. K. & Kumar, S. (2012). A comprehensive analysis of fifteen genes of steviol glycosides biosynthesis pathway in Stevia rebaudiana (Bertoni). Gene, 492, 276-284. https://doi.org/10.1016/j.gene.2011.10.015
  • Li, Z., Zhang, Y., Zhang, X., Peng, Y., Merewitz, E., Ma, X., Huang, L. & Yan, Y. (2016). The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white clover. Environmental and Experimental Botany, 124, 22-38. https://doi.org/10.1016/j.envexpbot.2015.12.004
  • Lipton, S. A., Choi, Y. B., Pan, Z. H., Lei, S. Z. & Chen, H. S. (1993). A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature, 364, 626-632. https://doi.org/10.1038/364626a0
  • Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randal, R. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193, 65-75. https://doi.org/10.1016/s0021-9258(19)52451-6
  • Manjunatha, G., Lokesh, V. & Neelwarne, B (2010). Nitric oxide in fruit ripening: trends and opportunities. Biotechnology Advances 28, 489-499. https://doi.org/10.1016/j.biotechadv.2010.03.001
  • Mathur, S. & Shekhawat, G. S. (2013). Establishment and characterization of Stevia rebaudiana (Bertoni) cell suspension culture: an in vitro approach for production of stevioside. Acta Physiologia Plantarum, 35(3), 931-939. https://doi.org/10.1007/s11738-012-1136-2
  • Metwally, A., Finkemeier, I., Georgi, M. & Dietz, K. J. (2003). Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiology, 132, 272-281. https://doi.org/10.1104/pp.102.018457
  • Miura, K., & Tada, Y. (2014). Regulation of water, salinity, and cold stress responses by salicylic acid. Frontiers in Plant Science, 5, 4. https://doi.org/10.3389/fpls.2014.00004
  • Moharramnejad, S., Azam, A. T., Panahandeh, J., Dehghanian, Z. & Muhammad, A. (2019). Effect of Methyl Jasmonate and Salicylic Acid on In Vitro Growth, Stevioside Production, and Oxidative Defense System in Stevia rebaudiana. Sugar Technology, 21, 1031-1038. https://doi.org/10.1007/s12355-019-00727-8
  • Mora-Herrera, M. E., Lopez-Delgado, H., Castillo-Morales, A. & Foyer, C. H. (2005). Salicylic acid and H2O2 function by independent pathways in the induction of freezing tolerance in potato. Physiologia Plantarum, 125(4), 430-440.https://doi.org/10.1111/j.1399-3054.2005.00572.x
  • Nahar, K., Hasanuzzaman, M., Alam, M. M., Rahman, A., Suzuki, T. & Fujita, M. (2016). Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology and Environmental Safety, 126, 245-255. https://doi.org/10.1016/j.ecoenv.2015.12.026
  • Naser Alavi, S. M., Arvin, M. J. & Manoochehri Kalantari, K. (2014). Salicylic acid and nitric oxide alleviate osmotic stress in wheat (Triticum aestivum L.) seedlings. Journal of Plant Interactions, 9, 683-688. https://doi.org/10.1080/17429145.2014.900120
  • Nawaz, F., Shabbir, R. N., Shahbaz, M., Majeed, S., Raheel, M., Hassan, W. & Sohail, M. A. (2017). Cross talk between nitric oxide and phytohormones regulate plant development during abiotic stresses. In M. El-Esawi (Ed.), Phytohormones-signaling mechanisms and crosstalk in plant development and stress responses (1st ed., pp. 117-141). InTech. https://doi.org/10.5772/intechopen.69812
  • Pacheco, A. C., da Silva Cabral, C., da Silva Fermino, E. S. & Aleman, C. C. (2013). Salicylic acid induced changes to growth, flowering and flavonoids production in marigold plants. Medicinal Plants Research, 7, 3158-3163.
  • Popova, L. & Tuan, T. (2010). Nitric oxide in plants: Properties, biosynthesis, and physiological functions. Iranian Journal of Science and Technology Transaction A: Science, 34, 173-183.
  • Pradhan, N., Singh, P., Dwivedi, P. & Pandey, D.K. (2020). Evaluation of sodium nitroprusside and putrescine on polyethylene glycol induced drought stress in Stevia rebaudiana Bertoni under in vitro condition. Industrial Crops and Products, 154. https://doi.org/10.1016/j.indcrop.2020.112754
  • Rahdari, P. & Hoseini, M. (2012). Drought stress: a review. International Journal of Agronomy and Plant Production, 10, 443-446.
  • Raskin, I. (1992). Role of salicylic acid in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 43, 439-463. https://doi.org/10.1146/annurev.pp.43.060192.002255
  • Razmi, N., Ebadi, A., Jahanfar Daneshian, J., & Soodabeh Jahanbakhsh (2017). Salicylic acid induced changes on antioxidant capacity, pigments, and grain yield of soybean genotypes in water deficit condition, Journal of Plant Interactions, 12, 457-464. https://doi.org/10.1080/17429145.2017.1392623
  • Sadeghipour, O. & Aghaei, P. (2012). Impact of exogenous salicylic acid application on sometraits of common bean (Phaseolus vulgaris L.) under water stress conditions. International Journal of Agriculture and Crop Sciences, 4, 685-690.
  • Safari, M., Mousavi-Fard, S., Rezaei Nejad, A., Sorkheh K. & Sofo A. (2022). Exogenous salicylic acid positively affects morpho-physiological and molecular responses of Impatiens walleriana plants grown under drought stress. International Journal of Environmental Science and Technology, 19, 969-984. https://doi.org/10.1007/s13762-020-03092-2
  • Sequera-Mutiozabal, M., Antoniou, C., Tiburcio, A. F., Alcázar R. & Fotopoulos V. (2017). Polyamines: Emerging Hubs Promoting Drought and Salt Stress Tolerance in Plants. Current Molecular Biology Reports, 3, 28-36. https://doi.org/10.1007/s40610-017-0052-z
  • Seyis, F., Yurteri, E. & Özcan, A. (2017). In Vitro Multiplication of Stevia rebaudiana (Bertoni) Genotypes Using Different Explants. International Journal of Crop Science and Technology, 3(2), 36-41. https://doi.org/10.26558/ijcst.326792
  • Shehab, G. G., Ahmed, O. K. & El-Beltagi, H. S. (2010). Effects of various chemical agents for alleviation of drought stress in rice plants (Oryza sativa L.). Notulae Botanicae Horti Agrobotanici Cluj, 38, 139-148.
  • Sichanova, M., Geneva, M., Petrova, M., Miladinova-Georgieva, K., Kirova, E., Nedev, T., Tsekova, D., Iwanov, I., Dochev, K., Ivanova, V., & Trendafilova, A. (2022). Improvement of Stevia rebaudiana Bertoni In Vitro Propagation and Steviol Glycoside Content Using Aminoacid Silver Nanofibers. Plants, 11(19), 2468. https://doi.org/10.3390/plants11192468
  • Singh, G., Singh, G., Singh, P., Parmar, R., Paul, N., Vashist, R., Swarnkar, M. K., Kumar, A., Singh, S. & Singh, A. K. (2017). Molecular dissection of transcriptional reprogramming of steviol glycosides synthesis in leaf tissue during developmental phase transitions in Stevia rebaudiana Bert. Scientific Reports, 7, 11835. https://doi.org/10.1038/s41598-017-12025-y
  • Szepesi, Á., Csiszár, J., Gémes, K., Horváth, E., Horváth, F., Simo, M.L. & Tari, I. (2009). Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. Journal of Plant Physiology, 9, 914-925. https://doi.org/10.1016/j.jplph.2008.11.012
  • Şahin, G. (2019). Effects of salicylic acid and heat acclimation on thermotolerance and withanolide accumulation under high temperature stress in the Cape gooseberry (Physalis peruviana L.) Turkish Journal of Botany, 43, 468-474. https://doi.org/10.3906/bot-1901-4
  • Tadhani, M., Patel, V. & Subhash, R. (2007). In vitro antioxidant activities of Stevia rebaudiana leaves and callus. Journal of Food Compostion and Analysis, 20, 323-329. https://doi.org/10.1016/j.jfca.2006.08.004
  • Tun, N. N., Santa-Catarina, C., Begum, T., Silveira, V., Handro, W., Floh, EIS, Scherer, G. F. (2006). Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiology, 47, 346-354. https://doi.org/10.1093/pcp/pci252
  • Uddin, M. S., Chowdhury, M. S. H., Khan, M. M. M. H., Uddin, M. B., Ahmed, R. & Baten, M. (2006). In vitro propagation of Stevia rebaudiana Bert in Bangladesh. African Journal of Biotechnology, 5, 1238-1240.
  • Vasquez-Hernandez, C., Feregrino-Perez, A. A., Perez-Ramirez, I., Ocampo-Velazqueza, R. V., Rico-García E., Torres-Pacheco I. & Guevara-Gonzaleza R. G. (2019). Controlled elicitation increases steviol glycosides (SGs) content and gene expression-associated to biosynthesis of SGs in Stevia rebaudiana B. cv. Morita II. Industrial Crops and Products, 139, 111479. https://doi.org/10.1016/j.indcrop.2019.111479
  • Vázquez-Hernández, M. C., Parola-Contreras, I., Montoya-Gómez, L. M., Torres-Pacheco, I., Schwarz, D. & Guevara-González, R. G. (2019). Eustressors: chemical and physical stress factors used to enhance vegetables production. Scientia Horticulture, 250, 223-229. https://doi.org/10.1016/j.scienta.2019.02.053
  • Yildiztugay, E., Ozfidan-Konakci, C. & Kucukoduk, M. (2014). Exogenous nitric oxide (as sodium nitroprusside) ameliorates polyethylene glycol induced osmotic stress in hydroponically grown maize roots. Plant Growth Regulation, 330, 683-696. https://doi.org/10.1007/s00344-014-9417-1
  • Yin, Z. P., Li S., Ren, J. & Song, X. S. (2014). Role of spermidine and spermine in alleviation of drought-induced oxidative stress and photosynthetic inhibition in Chinese dwarf cherry (Cerasus humilis) seedlings. Plant Growth Regulation, 74, 209-218. https://doi.org/10.1007/s10725-014-9912-1
  • Yoneda, Y., Shimizu, H., Nakashima, H., Miyasaka, J. & Ohdoi, K. (2018). Effect of treatment with gibberellin, gibberellin biosynthesis inhibitör, and auxin on steviol glycoside content in Stevia rebaudiana bertoni. Sugar Technology, 20(4), 482-491. https://doi.org/10.1007/s12355-017-0561-3
  • Zhu, J. K. (2001). Cell signaling under salt, water, and cold stresses. Current Opinion in Plant Biology, 4(5), 401–406. https://doi.org/10.1016/s1369-5266(00)00192-8
  • Zottini, M., Costa, A., De Michele, R., Ruzzene, M., Carimi, F. & Lo Schiavo, F. (2007). Salicylic acid activates nitric oxide synthesis in Arabidopsis. Journal of Experimental Botany, 58(6), 1397-1405. https://doi.org/10.1093/jxb/erm001
There are 73 citations in total.

Details

Primary Language English
Subjects Plant Biochemistry, Plant Biotechnology, Plant Physiology
Journal Section Research Articles
Authors

Günce Şahin This is me 0000-0003-0060-259X

Early Pub Date July 24, 2023
Publication Date December 31, 2023
Published in Issue Year 2023

Cite

APA Şahin, G. (2023). Effects of nitric oxide, spermidine, and salicylic acid signaling and their crosstalk with each other in the production of commercially important stevioside content and drought stress responses in Stevia rebaudiana bertoni. Biotech Studies, 32(2), 65-74. https://doi.org/10.38042/biotechstudies.1332145


ULAKBIM TR Index, Scopus, Google Scholar, Crossref, Scientific Indexing Services