Biotechnological Production of Natural Calorie Free Steviol Glycosides in Stevia rebaudiana: An Update on Current Scenario

Author(s): Abeer Kazmi, Mubarak Ali Khan*, Sher Mohammad, Amir Ali, Huma Ali.

Journal Name: Current Biotechnology

Volume 8 , Issue 2 , 2019

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Abstract:

Stevia rebaudiana is a vital medicinal plant of the genus Stevia and family Asteraceae. It is commonly used as a natural sweetener plant and its products are 300 times sweeter than the commonly used sugarcane. The sweetening potential is due to the presence of calorie-free steviol glycosides (SGs). The plant species has been extensively profiled to identify steviol glycosides (SGs) with intensity sweetening properties. However, the limited production of plant material is not fulfilling the higher market demand worldwide. Researchers are working worldwide to enhance the production of important SGs through the intervention of different biotechnological approaches in S. rebaudiana. In this review, the research work conducted in the last twenty years, on the different aspects of biotechnology to enhance the production of SGs has been precisely reviewed. Biotechnological methods such as micropropagation, callus and cell cultures, elicitation and the metabolomics and transcriptomic elucidation of the biosynthetic metabolic pathways for the production of steviol glycosides have been concisely reviewed and discussed.

Keywords: Stevia, steviol glycosides, cell culture, elicitor, adventitious roots, methyl jasmonate, stevioside, antioxidant, secondary metabolites, genetic engineering.

[1]
Bertoni MS. Le Ka’a he’e Sa nature et ses proprietes. An Cient Paraguay Ser I 1905; 5.
[2]
Skaria B, Joseph R, Mathew G, Malhew S, Joy P. Stevia: A sweet herb. Indian J Arecanut Spices Med Plants 2004; 6: 24-7.
[3]
Soejarto DD. Ethnobotany of Stevia and Stevia rebaudianaStevia. CRC Press 2001; pp. 53-80.
[4]
Grashoff JL. Systematic study of the North and Central American species of Stevia 1973.
[5]
Ogden EC. Contributions from the gray herbarium of harvard university—no. CXLVII. The broad-leaved species of potamogeton of north america north of mexico. Rhodora 1943; 45: 57-105.
[6]
Soejarto DD, Kinghorn AD, Farnsworth NR. Potential sweetening agents of plant origin. III. Organoleptic evaluation of Stevia leaf herbarium samples for sweetness. J Nat Prod 1982; 45(5): 590-9.
[http://dx.doi.org/10.1021/np50023a013] [PMID: 7153776]
[7]
Chauhan N, Lohani H, Andola HC. Quality evaluation of Stevia rebaudiana Cultivated in farmers field. Int J Res Ayurveda Pharm 2011; 2.
[8]
Kobus-Moryson M, Gramza-Michałowska A. Directions on the use of stevia leaves (Stevia Rebauidana) as an additive in food products. Acta Sci Pol Technol Aliment 2015; 14(1): 5-13.
[http://dx.doi.org/10.17306/J.AFS.2015.1.1] [PMID: 28068015]
[9]
Yadav AK, Singh S, Dhyani D, Ahuja PS. A review on the improvement of stevia [Stevia rebaudiana (Bertoni)]. Canadian journal of plant science 2011; 91: 1-27.
[http://dx.doi.org/10.4141/cjps10086]
[10]
Kumar R. Seed germination of Stevia rebaudiana influenced by various potting media. Octa Journal of Biosciences 2013; 1.
[11]
Abdullateef RA. M. bin Osman, Z. bint Zainuddin, Acclimatized apparatus enhanced seed germination in Stevia rebaudiana Bertoni. Int J Biol 2015; 7: 28.
[http://dx.doi.org/10.5539/ijb.v7n2p28]
[12]
Khalil SA, Zamir R, Ahmad N. Selection of suitable propagation method for consistent plantlets production in Stevia rebaudiana (Bertoni). Saudi J Biol Sci 2014; 21(6): 566-73.
[http://dx.doi.org/10.1016/j.sjbs.2014.02.005] [PMID: 25473365]
[13]
Khan MA, Khan T, Ali H. Plant Cell Culture Strategies for the Production of Terpenes as Green Solvents. Industrial Applications of Green Solvents 2019; I(50): 1-20.
[14]
Khan MA, Abbasi BH, Shah NA, Yücesan B, Ali H. Analysis of metabolic variations throughout growth and development of adventitious roots in Silybum marianum L.(Milk thistle), a medicinal plant. Plant Cell Tissue Organ Cult (PCTOC) 2015; 123: 501-10.
[http://dx.doi.org/10.1007/s11240-015-0854-8]
[15]
Kazmi A, Khan MA, Mohammad S, et al. Elicitation directed growth and production of steviol glycosides in the adventitious roots of Stevia rebaudiana Bertoni. Ind Crops Prod 2019. 139111530
[http://dx.doi.org/10.1016/j.indcrop.2019.111530]
[16]
Khan MA, Khan T, Riaz MS, Ullah N, Ali H, Nadhman A. Plant cell nanomaterials interaction: Growth, physiology and secondary metabolism Comprehensive Analytical Chemistry, Edition: Volume Number 84, Chapter: 2, Publisher. Elsevier 2019; pp. 23-54.
[17]
Kumar AA, Narayanan SB, Ravi S. Stevia the Ideal Sweetener: A Review. Res J Pharm Biol Chem Sci 2015; 6: 174-8.
[18]
Efsa P. Panel (2015), DRAFT Guidance Document Guidance to define protection goals for environmental risk assessment in relation to biodiversity and ecosystem services. Parma, Italy: European Food Safety Authority 2015. http://www. efsa. europa. eu/sites/default/files/assets/150622a. pdf [Verified 1 December 2015].
[19]
Jeppesen PB, Gregersen S, Poulsen CR, Hermansen K. Stevioside acts directly on pancreatic β cells to secrete insulin: actions independent of cyclic adenosine monophosphate and adenosine triphosphate-sensitive K+-channel activity. Metabolism 2000; 49(2): 208-14.
[http://dx.doi.org/10.1016/S0026-0495(00)91325-8] [PMID: 10690946]
[20]
Segura-Campos M, Barbosa-Martín E, Matus-Basto Á, et al. Comparison of chemical and functional properties of Stevia rebaudiana (Bertoni) varieties cultivated in Mexican Southeast. Am J Plant Sci 2014; 2014
[http://dx.doi.org/10.4236/ajps.2014.53039]
[21]
Aranda-González I, Segura-Campos M, Moguel-Ordoñez Y, Betancur-Ancona D. Stevia rebaudiana Bertoni. Un potencial adyuvante en el tratamiento de la diabetes mellitus. CYTA J Food 2014; 12: 218-26.
[http://dx.doi.org/10.1080/19476337.2013.830150]
[22]
Kim I-S, Yang M, Lee O-H, Kang S-N. The antioxidant activity and the bioactive compound content of Stevia rebaudiana water extracts. Lebensm Wiss Technol 2011; 44: 1328-32.
[http://dx.doi.org/10.1016/j.lwt.2010.12.003]
[23]
Konoshima T, Takasaki M. Cancer-chemopreventive effects of natural sweeteners and related compounds. Pure Appl Chem 2002; 74: 1309-16.
[http://dx.doi.org/10.1351/pac200274071309]
[24]
Jayaraman S, Manoharan MS, Illanchezian S. In-vitro antimicrobial and antitumor activities of Stevia rebaudiana (Asteraceae) leaf extracts. Trop J Pharm Res 2008; 7: 1143-9.
[http://dx.doi.org/10.4314/tjpr.v7i4.14700]
[25]
Kinghorn AD, Soejarto DD. Current status of stevioside as a sweetening agent for human use, Economic and medicinal plant research. Hiroshi Hikino, Norman R. Farnsworth 1985.
[26]
Sharangi AB, Bhutia PH. Stevia: Medicinal Miracles and Therapeutic Magic, Int J Crop. Sci Tech 2016; 2.
[27]
Ahmed B, Hossain M, Islam R, Kumar Saha A, Mandal A. A review on natural sweetener plant–Stevia having medicinal and commercial importance Agronomski glasnik: Glasilo Hrvatskog agronomskog društva. 73(2011): 75-91.
[28]
Martini A, Tavarini S, Macchia M, et al. Floral phenology, insect pollinators and seed quality of 36 genotypes of Stevia rebaudiana Bert. Cultivated in Italy, in: Stevia: growth in knowledge and taste EUSTAS. 2015; pp. 13-26.
[29]
Turgut K, Ucar E, Tutuncu B, Ozyigit Y. Stevia rebaudiana Bertoni could be an alternative crop in the Mediterranean region of Turkey in. Stevia: Growth in Knowledge and Taste, Proceedings of the 8th EUSTAS Stevia Symposium, EU, print Heverlee. 43-52.
[30]
Ijaz M, Pirzada AM, Saqib M, Latif M. Stevia rebaudiana: An alternative sugar crop in Pakistan-a review Journal of medicinal and spice plants 2015; 20: 88-96.
[31]
Gupta P. Plant tissue culture of Stevia rebaudiana (Bertoni): A review. J Pharmacog Phytother 2013; 5: 26-33.
[32]
Gupta P, Sharma S, Saxena S. Callusing in Stevia rebaudiana (natural sweetener) for steviol glycoside production. International Journal of Agricultural and Biological Sciences 2010; 1: 30-4.
[33]
Golkar P, Moradi M, Garousi GA. Elicitation of Stevia glycosides using salicylic acid and silver nanoparticles under callus culture. Sugar Tech 2019; 21: 569-77.
[http://dx.doi.org/10.1007/s12355-018-0655-6]
[34]
Idrees M, Sania B, Hafsa B, et al. Spectral lights trigger biomass accumulation and production of antioxidant secondary metabolites in adventitious root cultures of Stevia rebaudiana (Bert.). C R Biol 2018; 341(6): 334-42.
[http://dx.doi.org/10.1016/j.crvi.2018.05.003] [PMID: 29859915]
[35]
Lucho SR, do Amaral MN, Milech C, et al. Elicitor-induced transcriptional changes of genes of the steviol glycoside biosynthesis pathway in Stevia rebaudiana Bertoni. J Plant Growth Regul 2018; 37: 971-85.
[http://dx.doi.org/10.1007/s00344-018-9795-x]
[36]
Gupta P, Sharma S, Saxena S. Effect of salts (NaCl and Na2CO3) on callus and suspension culture of Stevia rebaudiana for Steviol glycoside production. Appl Biochem Biotechnol 2014; 172(6): 2894-906.
[http://dx.doi.org/10.1007/s12010-014-0736-2] [PMID: 24449376]
[37]
Gupta P, Sharma S, Saxena S. Biomass yield and steviol glycoside production in callus and suspension culture of Stevia rebaudiana treated with proline and polyethylene glycol. Appl Biochem Biotechnol 2015; 176(3): 863-74.
[http://dx.doi.org/10.1007/s12010-015-1616-0] [PMID: 25940589]
[38]
Ali A, Mohammad S, Khan MA, et al. Silver nanoparticles elicited in vitro callus cultures for accumulation of biomass and secondary metabolites in Caralluma tuberculata. Artif Cells Nanomed Biotechnol 2019; 47(1): 715-24.
[http://dx.doi.org/10.1080/21691401.2019.1577884] [PMID: 30856344]
[39]
Ho T-T, Lee J-D, Jeong C-S, Paek K-Y, Park S-Y. Improvement of biosynthesis and accumulation of bioactive compounds by elicitation in adventitious root cultures of Polygonum multiflorum. Appl Microbiol Biotechnol 2018; 102(1): 199-209.
[http://dx.doi.org/10.1007/s00253-017-8629-2] [PMID: 29138909]
[40]
Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 1962; 15: 473-97.
[http://dx.doi.org/10.1111/j.1399-3054.1962.tb08052.x]
[41]
Banerjee M, Sarkar P. In vitro callusing in Stevia rebaudiana Bertoni using cyanobacterial media-a novel approach to tissue culture. Int J Integr Biol 2008; 3: 163.
[42]
Karim M, Jannat R, Rahman M, Haque M. Micropropagation of stevia plant from nodal segments. Progress Agric 2008; 19: 21-6.
[http://dx.doi.org/10.3329/pa.v19i2.16914]
[43]
Patel RM, Shah RR. Regeneration of stevia plant through callus culture. Indian J Pharm Sci 2009; 71(1): 46-50.
[http://dx.doi.org/10.4103/0250-474X.51954] [PMID: 20177455]
[44]
Debnath M. Clonal propagation and antimicrobial activity of an endemic medicinal plant Stevia rebaudiana. J Med Plants Res 2008; 2: 45-51.
[45]
Ibrahim I, Nasr M, Mohammedm B, El-Zefzafi M. Nutrient factors affecting in vitro cultivation of Stevia rebaudiana. Sugar Tech 2008; 10: 248-53.
[http://dx.doi.org/10.1007/s12355-008-0044-7]
[46]
Sivaram L, Mukundan U. In vitro culture studies on Stevia rebaudiana. In Vitro Cell Dev Biol Plant 2003; 39: 520-3.
[http://dx.doi.org/10.1079/IVP2003438]
[47]
Sridhar TM, Aswath CR. Influence of additives on enhanced in vitro shoot multiplication of Stevia Rebaudiana (Bert.)—an important anti diabetic medicinal plant. Am J Plant Sci 2014; 5: 192.
[http://dx.doi.org/10.4236/ajps.2014.51025]
[48]
Thiyagarajan M, Venkatachalam P. Large scale in vitro propagation of Stevia rebaudiana (bert) for commercial application: Pharmaceutically important and antidiabetic medicinal herb. Ind Crops Prod 2012; 37: 111-7.
[http://dx.doi.org/10.1016/j.indcrop.2011.10.037]
[49]
Das A, Gantait S, Mandal N. Micropropagation of an elite medicinal plant: Stevia rebaudiana Bert. Int J Agric Res 2011; 6: 40-8.
[http://dx.doi.org/10.3923/ijar.2011.40.48]
[50]
Hwang SJ. Rapidin Vitro propagation and enhanced stevioside accumulation in Stevia rebaudiana Bert. J Plant Biol 2006; 49: 267-70.
[http://dx.doi.org/10.1007/BF03031153]
[51]
Khan T, Abbasi BH, Khan MA, Azeem M. Production of biomass and useful compounds through elicitation in adventitious root cultures of Fagonia indica. Ind Crops Prod 2017; 108: 451-7.
[http://dx.doi.org/10.1016/j.indcrop.2017.07.019]
[52]
Reis RV, Borges APPL, Chierrito TPC, et al. Establishment of adventitious root culture of Stevia rebaudiana Bertoni in a roller bottle system. Plant Cell Tissue Organ Cult (PCTOC) 2011; 106: 329-35.
[http://dx.doi.org/10.1007/s11240-011-9925-7]
[53]
Sanches Lopes SM, Francisco MG, Higashi B, et al. Chemical characterization and prebiotic activity of fructo-oligosaccharides from Stevia rebaudiana (Bertoni) roots and in vitro adventitious root cultures. Carbohydr Polym 2016; 152: 718-25.
[http://dx.doi.org/10.1016/j.carbpol.2016.07.043] [PMID: 27516323]
[54]
Ghazal B, Saif S, Farid K, et al. Stimulation of secondary metabolites by copper and gold nanoparticles in submerge adventitious root cultures of Stevia rebaudiana (Bert.) IET nanobiotechnology 2018; 12: 569-73.
[55]
Reis RV, Chierrito TP, Silva TF, et al. Morpho-anatomical study of Stevia rebaudiana roots grown in vitro and in vivo. Rev Bras Farmacogn 2017; 27: 34-9.
[http://dx.doi.org/10.1016/j.bjp.2016.08.007]
[56]
Tahmasi S, Garoosi G, Ahmadi J, Farjaminezhad R. Effect of salicylic acid on stevioside and rebaudioside A production and transcription of biosynthetic genes in in vitro culture of Stevia rebaudiana. Iranian Journal of genetics and plant breeding 2017; 6: 1-8.
[57]
Bayraktar M, Naziri E, Karabey F, et al. Enhancement of stevioside production by using biotechnological approach in in vitro culture of Stevia rebaudiana. Int J Sec Metab 2018; 5: 362-74.
[http://dx.doi.org/10.21448/ijsm.496724]
[58]
Hendawey M, Abo El Fadl R. Biochemical studies on the production of active constituents in Stevia rebaudiana L. callus. Global J Biotechn Biochem 2014; 9: 76-93.
[59]
Vafadar F, Amooaghaie R, Otroshy M. Effects of plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungus on plant growth, stevioside, NPK, and chlorophyll content of Stevia rebaudiana. J Plant Interact 2014; 9: 128-36.
[http://dx.doi.org/10.1080/17429145.2013.779035]
[60]
Das K, Dang R. Influence of biofertilizers on stevioside content in Stevia rebaudiana grown in acidic soil condition. Arch Appl Sci Res 2010; 2: 44-9.
[61]
Punja ZK. Genetic engineering of plants to enhance resistance to fungal pathogens—a review of progress and future prospects. Can J Plant Pathol 2001; 23: 216-35.
[http://dx.doi.org/10.1080/07060660109506935]
[62]
Khan RS, Iqbal A, Malak R, et al. Plant defensins: types, mechanism of action and prospects of genetic engineering for enhanced disease resistance in plants. 3 Biotech 2019; 9: 192.
[63]
Mubarak M, El Halmouch Y, Belal A, Elfadeel MT. EL-Din, S. Mahmoud, M. El Sharnouby, E. El Sarag, Improving sweet leaf (‘Stevia rebaudiana’var. Bertoni) resistance to bialaphos herbicide via’bar’gene transfer. Plant Omics 2015; 8: 232.
[64]
Kazmi A, Khan MA, Ali H. Biotechnological approaches for production of bioactive secondary metabolites in Nigella sativa: an up-to-date review. International Journal of Secondary Metabolite 2019; 6: 172-95.
[http://dx.doi.org/10.21448/ijsm.575075]
[65]
Richman AS, Gijzen M, Starratt AN, Yang Z, Brandle JE. Diterpene synthesis in Stevia rebaudiana: recruitment and up-regulation of key enzymes from the gibberellin biosynthetic pathway. Plant J 1999; 19(4): 411-21.
[http://dx.doi.org/10.1046/j.1365-313X.1999.00531.x] [PMID: 10504563]
[66]
Kim KK, Sawa Y, Shibata H. Hydroxylation of ent-kaurenoic acid to steviol in Stevia rebaudiana Bertoni--purification and partial characterization of the enzyme. Arch Biochem Biophys 1996; 332(2): 223-30.
[http://dx.doi.org/10.1006/abbi.1996.0336] [PMID: 8806729]
[67]
Brandle JE, Telmer PG. Steviol glycoside biosynthesis. Phytochemistry 2007; 68(14): 1855-63.
[http://dx.doi.org/10.1016/j.phytochem.2007.02.010] [PMID: 17397883]
[68]
Yoneda Y, Nakashima H, Miyasaka J, Ohdoi K, Shimizu H. Impact of blue, red, and far-red light treatments on gene expression and steviol glycoside accumulation in Stevia rebaudiana. Phytochemistry 2017; 137: 57-65.
[http://dx.doi.org/10.1016/j.phytochem.2017.02.002] [PMID: 28215607]
[69]
Richman A, Swanson A, Humphrey T, et al. Functional genomics uncovers three glucosyltransferases involved in the synthesis of the major sweet glucosides of Stevia rebaudiana. Plant J 2005; 41(1): 56-67.
[http://dx.doi.org/10.1111/j.1365-313X.2004.02275.x] [PMID: 15610349]
[70]
Yang Y, Huang S, Han Y, Yuan H, Gu C, Wang Z. Environmental cues induce changes of steviol glycosides contents and transcription of corresponding biosynthetic genes in Stevia rebaudiana. Plant Physiol Biochem 2015; 86: 174-80.
[http://dx.doi.org/10.1016/j.plaphy.2014.12.004] [PMID: 25500454]
[71]
Modi A, Litoriya N, Prajapati V, Rafalia R, Narayanan S. Transcriptional profiling of genes involved in steviol glycoside biosynthesis in Stevia rebaudiana bertoni during plant hardening. Dev Dyn 2014; 243(9): 1067-73.
[http://dx.doi.org/10.1002/dvdy.24157] [PMID: 24975237]
[72]
Ceunen S, Werbrouck S, Geuns JM. Stimulation of steviol glycoside accumulation in Stevia rebaudiana by red LED light. J Plant Physiol 2012; 169(7): 749-52.
[http://dx.doi.org/10.1016/j.jplph.2012.01.006] [PMID: 22341569]
[73]
Maryam NN, Nangyal H, Ali L, Rashid A. Screening of Leaf Extracts of Stevia rebaudiana for Antibacterial Activity. Phytotoxic and Haemagglutination Activities Am Eur Agric Sci 2015; 15: 2035-8.
[74]
Sunitha V. Irene wilsy J, Reginold M. Antibacterial activity in medicinal plant (Stevia rebaudiana) using two solvents. Int J Recent Sci Res 2015; 6: 5070-1.
[75]
Tomita T, Sato N, Arai T, et al. Bactericidal activity of a fermented hot-water extract from Stevia rebaudiana Bertoni towards enterohemorrhagic Escherichia coli O157:H7 and other food-borne pathogenic bacteria. Microbiol Immunol 1997; 41(12): 1005-9.
[http://dx.doi.org/10.1111/j.1348-0421.1997.tb01961.x] [PMID: 9492187]
[76]
Curi R, Alvarez M, Bazotte RB, Botion LM, Godoy JL, Bracht A. Effect of Stevia rebaudiana on glucose tolerance in normal adult humans. Braz J Med Biol Res 1986; 19(6): 771-4.
[PMID: 3651629]
[77]
Suzuki H, Kasai T, Sumihara M, Sugisawa H. Influence of oral administration of stevioside on levels of blood glucose and liver glycogen of intact rats. Nippon Nogeikagaku Kaishi 1977.
[78]
Chen T-H, Chen S-C, Chan P, Chu Y-L, Yang H-Y, Cheng J-T. Mechanism of the hypoglycemic effect of stevioside, a glycoside of Stevia rebaudiana. Planta Med 2005; 71(2): 108-13.
[http://dx.doi.org/10.1055/s-2005-837775] [PMID: 15729617]
[79]
Savita S, Sheela K, Sunanda S, Shankar A, Ramakrishna P, Sakey S. Health implications of Stevia rebaudiana. J Hum Ecol 2004; 15: 191-4.
[http://dx.doi.org/10.1080/09709274.2004.11905691]
[80]
Ghanta S, Banerjee A, Poddar A, Chattopadhyay S. Oxidative DNA damage preventive activity and antioxidant potential of Stevia rebaudiana (Bertoni) Bertoni, a natural sweetener. J Agric Food Chem 2007; 55(26): 10962-7.
[http://dx.doi.org/10.1021/jf071892q] [PMID: 18038982]
[81]
Stoyanova S, Geuns J, Hideg E, Van den Ende W. The food additives inulin and stevioside counteract oxidative stress. Int J Food Sci Nutr 2011; 62(3): 207-14.
[http://dx.doi.org/10.3109/09637486.2010.523416] [PMID: 21043580]
[82]
Shukla S, Mehta A, Bajpai VK, Shukla S. In vitro antioxidant activity and total phenolic content of ethanolic leaf extract of Stevia rebaudiana Bert. Food Chem Toxicol 2009; 47(9): 2338-43.
[http://dx.doi.org/10.1016/j.fct.2009.06.024] [PMID: 19540900]
[83]
Nakamura Y, Sakiyama S, Takenaga K. Suppression of syntheses of high molecular weight nonmuscle tropomyosins in macrophages. Cell Motil Cytoskeleton 1995; 31(4): 273-82.
[http://dx.doi.org/10.1002/cm.970310404] [PMID: 7553914]
[84]
Mizushina Y, Akihisa T, Ukiya M, et al. Structural analysis of isosteviol and related compounds as DNA polymerase and DNA topoisomerase inhibitors. Life Sci 2005; 77(17): 2127-40.
[http://dx.doi.org/10.1016/j.lfs.2005.03.022] [PMID: 15935396]
[85]
Raskovic A, Jakovljevic V, Mikov M, Gavrilovic M. Joint effect of commercial preparations of Stevia rebaudiana Bertoni and sodium monoketocholate on glycemia in mice. Eur J Drug Metab Pharmacokinet 2004; 29(2): 83-6.
[http://dx.doi.org/10.1007/BF03190580] [PMID: 15230334]
[86]
Yasukawa K, Kitanaka S, Seo S. Inhibitory effect of stevioside on tumor promotion by 12-O-tetradecanoylphorbol-13-acetate in two-stage carcinogenesis in mouse skin. Biol Pharm Bull 2002; 25(11): 1488-90.
[http://dx.doi.org/10.1248/bpb.25.1488] [PMID: 12419967]
[87]
Wang T, Song X, Zhang Z, et al. Stevioside inhibits inflammation and apoptosis by regulating TLR2 and TLR2-related proteins in S. aureus-infected mouse mammary epithelial cells. Int Immunopharmacol 2014; 22(1): 192-9.
[http://dx.doi.org/10.1016/j.intimp.2014.06.015] [PMID: 24975657]
[88]
Bayraktar M, Naziri E, Akgun IH, et al. Elicitor induced stevioside production, in vitro shoot growth, and biomass accumulation in micropropagated Stevia rebaudiana. Plant Cell Tissue Organ Cult (PCTOC) 2016; 127: 289-300.
[http://dx.doi.org/10.1007/s11240-016-1049-7]
[89]
Fakhrul R, Norrizah J, Jaapar S, Noor A. The effect of nitrogen concentrations on the growth and development of Stevia rebaudiana (Bertoni) and production of stevioside and rebaudioside A. Aust J Basic Appl Sci 2014; 8: 500-9.
[90]
Ahmed M, Salahin M, Karim R, et al. An efficient method for in vitro clonal propagation of a newly introduced sweetener plant (Stevia rebaudiana Bertoni.) in Bangladesh. Am-Eur J Sci Res 2007; 2: 121-5.
[91]
Singh M, Saharan V, Rajpurohit D, Kumar R. Direct organogenesis from cold treated in vitro leaf explants of Stevia rebaudiana Bertoni. Journal of Pharmacognosy and Phytochemistry 2017; 6: 1561-4.
[92]
Singh P, Dwivedi P. Two-stage culture procedure using thidiazuron for efficient micropropagation of Stevia rebaudiana, an antidiabetic medicinal herb. 3 Biotech 2014; 4: 431-7.
[93]
Radić S, Vujčić V, Glogoški M, Radić-Stojković M. Influence of pH and plant growth regulators on secondary metabolite production and antioxidant activity of Stevia rebaudiana (Bert). Period Biol 2016; 118: 9-19.
[http://dx.doi.org/10.18054/pb.2016.118.1.3420]
[94]
Pandey H, Pandey P, Pandey SS, Singh S, Banerjee S. Meeting the challenge of stevioside production in the hairy roots of Stevia rebaudiana by probing the underlying process. Plant Cell Tissue Organ Cult (PCTOC) 2016; 126: 511-21.
[http://dx.doi.org/10.1007/s11240-016-1020-7]
[95]
Röck-Okuyucu B, Bayraktar M, Akgun IH, Gurel A. Plant growth regulator effects on in vitro propagation and stevioside production in Stevia rebaudiana Bertoni. HortScience 2016; 51: 1573-80.
[http://dx.doi.org/10.21273/HORTSCI11093-16]
[96]
Tadhani M, Patel V, Subhash R. In vitro antioxidant activities of Stevia rebaudiana leaves and callus. J Food Compos Anal 2007; 20: 323-9.
[http://dx.doi.org/10.1016/j.jfca.2006.08.004]
[97]
Ahmad N, Rab A, Ahmad N. Light-induced biochemical variations in secondary metabolite production and antioxidant activity in callus cultures of Stevia rebaudiana (Bert). J Photochem Photobiol B 2016; 154: 51-6.
[http://dx.doi.org/10.1016/j.jphotobiol.2015.11.015] [PMID: 26688290]
[98]
Dheeranupattana S, Wangprapa M, Jatisatienr A. Effect of sodium acetate on stevioside production of Stevia rebaudiana in. Int Workshop Med Aromatic Plants 2008.
[http://dx.doi.org/10.17660/Actahortic.2008.786.31]
[99]
Babu P, Chikkasubbanna V, Prasad T, Radhakrishna D. In vitro studies on the bearing ability of stevia for stevioside biosynthesis. Biosci Biotech Res Comm 2011; 4: 19-22.
[100]
Das K, Dang R, Rajasekharan P. Establishment and maintenance of callus of Stevia rebaudiana Bertoni under aseptic environment. 2006.
[101]
Dey A, Kundu S, Bandyopadhyay A, Bhattacharjee A. Efficient micropropagation and chlorocholine chloride induced stevioside production of Stevia rebaudiana Bertoni. C R Biol 2013; 336(1): 17-28.
[http://dx.doi.org/10.1016/j.crvi.2012.11.007] [PMID: 23537766]
[102]
Guruchandran V, Sasikumar C. Effect of polyamines on in vitro organogenesis using shoot tip explants of Stevia Rebaudiana Bert, International Journal. Curr Biotechnol 2013; 1: 16-8.
[103]
Jain P, Kachhwaha S, Kothari S. Improved micropropagation protocol and enhancement in biomass and chlorophyll content in Stevia rebaudiana (Bert.) Bertoni by using high copper levels in the culture medium. Sci Hortic (Amsterdam) 2009; 119: 315-9.
[http://dx.doi.org/10.1016/j.scienta.2008.08.015]
[104]
Khan SA, Ur Rahman L, Shanker K, Singh M. Agrobacterium tumefaciens-mediated transgenic plant and somaclone production through direct and indirect regeneration from leaves in Stevia rebaudiana with their glycoside profile. Protoplasma 2014; 251(3): 661-70.
[PMID: 24154495]
[105]
Singh P, Dwivedi P, Atri N. In vitro shoot multiplication of Stevia and assessment of stevioside content and genetic fidelity of the regenerants. Sugar Tech 2014; 16: 430-9.
[http://dx.doi.org/10.1007/s12355-013-0292-z]
[106]
Ramírez-Mosqueda MA, Iglesias-Andreu LG. Direct organogenesis of Stevia rebaudiana Bertoni using thin cell layer (TCL) method. Sugar Tech 2016; 18: 424-8.
[http://dx.doi.org/10.1007/s12355-015-0391-0]
[107]
Javed R, Usman M, Yücesan B, Zia M, Gürel E. Effect of zinc oxide (ZnO) nanoparticles on physiology and steviol glycosides production in micropropagated shoots of Stevia rebaudiana Bertoni. Plant Physiol Biochem 2017; 110: 94-9.
[http://dx.doi.org/10.1016/j.plaphy.2016.05.032] [PMID: 27246994]
[108]
Javed R, Yücesan B, Gurel E. Hydrogen peroxide-induced steviol glycosides accumulation and enhancement of antioxidant activities in leaf tissues of Stevia rebaudiana Bertoni. Sugar Tech 2018; 20: 100-4.
[http://dx.doi.org/10.1007/s12355-017-0521-y]
[109]
Javed R, Zia M, Yücesan B, Gürel E. Abiotic stress of ZnO-PEG, ZnO-PVP, CuO-PEG and CuO-PVP nanoparticles enhance growth, sweetener compounds and antioxidant activities in shoots of Stevia rebaudiana Bertoni IET nanobiotechnology 2017; 11: 898-902.
[110]
Javed R, Mohamed A, Yücesan B, Gürel E, Kausar R, Zia M. CuO nanoparticles significantly influence in vitro culture, steviol glycosides, and antioxidant activities of Stevia rebaudiana Bertoni. Plant Cell Tissue Organ Cult (PCTOC) 2017; 131: 611-20.
[http://dx.doi.org/10.1007/s11240-017-1312-6]
[111]
Mejía-Espejel L, Robledo-Paz A, Lozoya-Gloria E, Peña-Valdivia CB, Carrillo-Salazar JA. Elicitors on steviosides production in Stevia rebaudiana Bertoni calli. Sci Hortic (Amsterdam) 2018; 242: 95-102.
[http://dx.doi.org/10.1016/j.scienta.2018.07.023]
[112]
Kilam D, Saifi M, Abdin M, Agnihotri A, Varma A. Endophytic root fungus Piriformospora indica affects transcription of steviol biosynthesis genes and enhances production of steviol glycosides in Stevia rebaudiana. Physiol Mol Plant Pathol 2017; 97: 40-8.
[http://dx.doi.org/10.1016/j.pmpp.2016.12.003]
[113]
Ramírez-Mosqueda MA, Iglesias-Andreu LG, Bautista-Aguilar JR. The effect of light quality on growth and development of in vitro plantlet of Stevia rebaudiana Bertoni. Sugar Tech 2017; 19: 331-6.
[http://dx.doi.org/10.1007/s12355-016-0459-5]
[114]
Esmaeili F, Ghaheri M, Kahrizi D, et al. Effects of various glutamine concentrations on gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni. Cell Mol Biol 2018; 64(2): 1-5.
[http://dx.doi.org/10.14715/cmb/2018.64.2.1] [PMID: 29433620]
[115]
Akbari F, Arminian A, Kahrizi D, Fazeli A. Effect of nitrogen sources on some morphological characteristics of in vitro stevia rebaudiana Bertoni. Cell Mol Biol 2017; 63(2): 107-11.
[http://dx.doi.org/10.14715/cmb/2017.63.2.17] [PMID: 28364791]
[116]
Gerami M, Abbaspour H, Ghasemiomran V, Pirdashti H. Effects of Ethyl Methanesulfonate on Morphological and Physiological Traits of Plants Regenerated from Stevia (Stevia rebaudiana Bertoni) Calli. Appl Ecol Environ Res 2017; 15: 373-85.
[http://dx.doi.org/10.15666/aeer/1503_373385]
[117]
Kumari M, Chandra S. Secondary Metabolite Production in Transformed Cultures: Stevioside Glycosides Production from Stevia rebaudiana. Hairy Root Cultures. Transgenesis and Secondary Metabolism 2017; pp. 103-21.
[http://dx.doi.org/10.1007/978-3-319-28669-3_1]
[118]
de Jesús Sanchéz-Cordova Á, Capataz-Tafur J, Barrera-Figueroa BE, et al. Agrobacterium rhizogenes-Mediated Transformation Enhances Steviol Glycosides Production and Growth in Stevia rebaudiana Plantlets. Sugar Tech 2019; 21: 398-406.
[http://dx.doi.org/10.1007/s12355-018-0681-4]
[119]
Ghaheri M, Kahrizi D, Bahrami G, Mohammadi-Motlagh H-R. Study of gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni under various mannitol concentrations. Mol Biol Rep 2019; 46(1): 7-16.
[http://dx.doi.org/10.1007/s11033-018-4250-4] [PMID: 30506508]
[120]
Ahmad N, Rab A, Ahmad N, Fazal H. Differential pH-Induced Biosynthesis of Steviol Glycosides and Biochemical Parameters in Submerge Root Cultures of Stevia rebaudiana (Bert.). Sugar Tech 2018; 20: 734-44.
[http://dx.doi.org/10.1007/s12355-018-0589-z]
[121]
Gerami M, Abbaspour H, Omran G, Alah V, Pirdashti HA, Majidian P. Effect of Chemical Mutagen on Some Biochemical Properties of Stevia rebaudiana Bertoni. J Gen Res 2017; 3: 26-35.


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VOLUME: 8
ISSUE: 2
Year: 2019
Page: [70 - 84]
Pages: 15
DOI: 10.2174/2211550108666191210100751

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