Agrobacterium rhizogenes-Mediated Transformation Enhances Steviol Glycosides Production and Growth in Stevia rebaudiana Plantlets

Sugar Tech

Volumn 21, Issue 3, 2019, Pages 398-406

  Sanchéz Cordova, Ángel de Jesús ^a   Capataz Tafur, Jacqueline ^a   Barrera Figueroa, Blanca Estela ^a   López Torres, Adolfo ^a   Sanchez Ocampo, Paul Mauricio ^a   García López, Edgar ^a   Huerta Heredia, Ariana Arlene ^a  

^a UNIVERSIDAD DEL PAPALOAPAN   (Mexico)

Author keywords

Agrobacterium; Genetic transformation; Rebaudioside A; Stevia rebaudiana; Stevioside

Indexed keywords

EID: 85060610203     PISSN: 09721525     EISSN: 09740740     Source Type: Journal    
DOI: 10.1007/s12355-018-0681-4     Document Type: Article

References (47)

1. Amselem, J., and M. Tepfer. 1992. Molecular basis of novel root phenotypes induced by Agrobacterium rhizogenes A4 on cucumber. Plant Molecular Biology 19: 421–432.
2. Anbazhagan, M., M. Kalpana, R. Rajendran, V. Natarajan, and D. Dhanavel. 2010. In vitro production of Stevia rebaudiana Bertoni. Emirates Journal of Food Agriculture 2: 216–222.
3. Bayraktar, M., E. Naziri, I. Hakki, A. Fatih, K. Esra, I. Begum, A. Erdal, and B.A. Gurel. 2016. Elicitor induced stevioside production, in vitro shoot growth, and biomass accumulation in micropropagated Stevia rebaudiana. Plant Cell, Tissue and Organ Culture 127: 289–300.
4. Bender, C., S. Graziano, and B.F. Zimmermann. 2015. Study of Stevia rebaudiana Bertoni antioxidant activities and cellular properties. International Journal of Food Sciences and Nutrition 66: 553–558.
5. Bonhomme, V., D. Laurain-Mattar, and M.A. Fliniaux. 2000. Effects of the rolC gene on hairy root: Induction development and tropane alkaloid production by Atropa belladonna. Journal of Natural Products 63: 1249–1252.
6. Bulgakov, V.P. 2008. Functions of rol genes in plant secondary metabolism. Biotechnolgy Advances 26: 318–324.
7. Calderón-Gabriel, L., A. Jiménez-Brigada, A.A. Huerta-Heredia, J. Capataz-Tafur, and E. García-López. 2016. Effect of three strains of Agrobacterium rhizogenes and explant type on genetic transformation of Stevia rebaudiana. Mexican Journal of Biotechnology 1: 34–41.
8. Choi, P.S., Y.D. Kim, K.M. Choi, H.J. Chung, D.W. Choi, and J.R. Liu. 2004. Plant regeneration from hairy-root cultures transformed by infection with Agrobacterium rhizogenes in Catharanthus roseus. Plant Cell Reports 22: 828–831.
9. Christey, M.C. 2001. Use of Ri-mediated transformation for production of transgenic plants. Vitro Cellular & Developmental Biology-Plant 37: 687–700.
10. David, C., M.D. Chilton, and J. Tempé. 1984. Conservation of T-DNA in plants regenerated from hairy root cultures. Nature Biotechnology 2: 73–76.
11. Dilshad, E., H. Ismail, R.M. Cusido, J. Palazon, K. Ramirez-Estrada, and B. Mirza. 2016. Rol genes enhance the biosynthesis of antioxidants in Artemisia carvifolia Buch. BMC Plant Biology 16: 125.
12. Edwards, K., C. Johnstone, and C. Thompson. 1991. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Research 19: 1349.
13. Fallah, F., F. Nokhasi, M. Ghaheri, D. Kahrizi, A. Beheshti Ale Agha, T. Ghorbani, E. Kazemi, and Z. Ansarypour. 2017. Effect of salinity on gene expression, morphological and biochemical characteristics of Stevia rebaudiana Bertoni under in vitro conditions. Cellular and Molecular Biology 63: 102–106.
14. Fu, X., Z.P. Yin, J.G. Chen, X.C. Shangguan, X. Wang, Q.F. Zhang, and D.Y. Peng. 2015. Production of chlorogenic acid and its derivatives in hairy root cultures of Stevia rebaudiana. Journal Agricultural and Food Chemistry 63: 262–268.
15. Gamboa, F., and M. Chaves. 2012. Antimicrobial potential of extracts from Stevia rebaudiana leaves against bacteria of importance in dental caries. Acta Odontológica Latinoamericana 25: 171–175.
16. Ghorbani, T., D. Kahrizi, M. Saeidi, and I. Arji. 2017. Effect of sucrose concentrations on Stevia rebaudiana Bertoni tissue culture and gene expression. Cellular and Molecular Biology 63: 33–37.
17. Gunjan, S.K., J. Lutz, A. Bushong, D.T. Rogers, and J. Littleton. 2013. Hairy root cultures and plant regeneration in Solidago nemoralis transformed with Agrobacterium rhizogenes. American Journal of Plant Sciences 4: 1675–1678.
18. Gupta, E., S. Kaushik, S. Purwar, R. Sharma, A.K. Balapure, and S. Sundaram. 2017. Anticancer potential of steviol in MCF-7 human breast cancer cells. Pharmacognosy Magazine 13: 345–350.
19. Gupta, E., S. Purwar, S. Sundaram, and G.K. Rai. 2013. Nutritional and therapeutic values of Stevia rebaudiana: A review. Journal of Medicinal Plants Research 7: 3343–3353.
20. Gurusamy, P.D., H. Schäfer, S. Ramamoorthy, and M. Wink. 2017. Biologically active recombinant human erythropoietin expressed in hairy root cultures and regenerated plantlets of Nicotiana tabacum L. PLoS ONE 12 (8): e0182367.
21. Ishizaki, T., Y. Hoshino, K. Masuda, and K. Oosawa. 2002. Explants of Ri-transformed hairy roots of spinach can develop embryogenic calli in the absence of gibberellic acid, an essential growth regulator for induction of embryogenesis from non-transformed roots. Plant Science 163: 223–231.
22. Javed, R., A. Mohamed, B. Yücesan, E. Gurel, R. Kausar, and M. Zia. 2017a. CuO nanoparticles significantly influence in vitro culture, steviol glycosides, and antioxidant activities of Stevia rebaudiana Bertoni. Plant Cell, Tissue and Organ Culture 131: 611–620.
23. Javed, R., M. Usman, B. Yücesan, M. Zia, and E. Gürel. 2017b. Effect of zinc oxide (ZnO) nanoparticles on physiology and steviol glycosides production in micropropagated shoots of Stevia rebaudiana Bertoni. Plant Physiology and Biochemistry 110: 94–99.
24. Khan, S.A., L.U. Rahman, K. Shanker, and M. Singh. 2014. Agrobacterium tumefaciens mediated transgenic plant and somaclone production through direct and indirect regeneration from leaves in Stevia rebaudiana with their glycoside profile. Protoplasma 251: 661–670.
25. Khan, S.A., L.U. Rahman, R. Verma, and K. Shanker. 2016. Physical and chemical mutagenesis in Stevia rebaudiana: Variant generation with higher UGT expression and glycosidic profile but with low photosynthetic capabilities. Acta Physiologiae Plantarum 38: 1–12.
26. Ladygin, V.G., N.I. Bondarev, G.A. Semenova, A.A. Smolov, O.V. Reshetnyak, and A.M. Nosov. 2008. Chloroplast ultrastructure, photosynthetic apparatus activities and production of steviol glycosides in Stevia rebaudiana in vivo and in vitro. Biologia Plantarum 52: 9–16.
27. Libik-Konieczny, M., E. Capecka, E. Kąkol, M. Dziurka, A. Grabowska-Joachimiak, E. Sliwinska, and L. Pistelli. 2018. Growth, development and steviol glycosides content in the relation to the photosynthetic activity of several Stevia rebaudiana Bertoni strains cultivated under temperate climate conditions. Scientia Horticulturae 234: 10–18.
28. Lichtenthaler, H.K., and A.R. Wellburn. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11: 591–592.
29. López-Laredo, A.R., F.D. Ramírez-Flores, G. Sepúlveda-Jiménez, and G. Trejo-Tapia. 2009. Comparison of metabolite levels in callus of Tecoma stans (L.) Juss. ex Kunth. cultured in photoperiod and darkness. Vitro Cellular & Developmental Biology-Plant 45: 550–558.
30. Magangana, T.P., M.A. Stander, and N.P. Makunga. 2018. Effect of nitrogen and phosphate on in vitro growth and metabolite profiles of Stevia rebaudiana Bertoni (Asteraceae). Plant Cell, Tissue and Organ Culture 134: 141–151.
31. Matveeva, T.V., S.V. Sokornova, and L.A. Lutova. 2015. Influence of Agrobacterium oncogenes on secondary metabolism of plants. Phytochemistry Reviews 14: 541–554.
32. Murashige, T., and F. Skoog. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15: 473–497.
33. Namdari, N., L. Shooshtari, and A. Qaderi. 2015. In vitro micropropagation of Stevia rebaudiana Bertoni. Biological Forum—An International Journal 7: 1750–1754.
34. Pandey, H., P. Pandey, S.S. Pandey, S. Singh, and S. Banerjee. 2016. Meeting the challenge of stevioside production in the hairy roots of Stevia rebaudiana by probing the underlying process. Plant Cell, Tissue and Organ Culture 126: 511–521.
35. Ramos-Tovar, E., E. Hernández-Aquino, S. Casas-Grajales, L.D. Buendia-Montaño, S. Galindo-Gómez, J. Camacho, V. Tsutsumi, and P. Muriel. 2018. Stevia prevents acute and chronic liver injury induced by carbon tetrachloride by blocking oxidative stress through Nrf2 upregulation. Oxidative Medicine Cellular Longevity 2018: 3823426. 10.1155/2018/3823426.
36. Razak, U.N.A.A., C.B. Ong, T.S. Yu, and L.K. Lau. 2014. In vitro micropropagation of Stevia rebaudiana Bertoni in Malaysia. Brazilian Archives of Biology Technology 57: 23–28.
37. Roychowdhury, D., A. Majumder, and S. Jha. 2013. Agrobacterium rhizogenes-mediated transformation in medicinal plants: Prospects and challenges. In Biotechnology for medicinal plants: Micropropagation and improvement, ed. S. Chandra, H. Lata, and A. Varma, 29–68. Berlin/Heidelberg: Springer.
38. Ruiz-Ruiz, J.C., Y.B. Moguel-Ordoñez, and M.R. Segura-Campos. 2017. Biological activity of Stevia rebaudiana Bertoni and their relationship to health. Critical Reviews in Food Science and Nutrition 57: 2680–2690.
39. Sarkar, S., I. Ghosh, D. Roychowdhury, and S. Jha. 2018. The Effects of rol genes of Agrobacterium rhizogenes on morphogenesis and secondary metabolite accumulation in medicinal plants. In Biotechnological approaches for medicinal and aromatic plants, ed. N. Kumar, 27–51. Singapore: Springer.
40. Shkryl, Y.N., G.N. Veremeichik, V.P. Bulgakov, G.K. Tchernoded, N.P. Mischenko, S.A. Fedoreyev, and Y.N. Zhuravlev. 2007. Individual and combined effects of the rolA, B and C genes on anthraquinone production in Rubia cordifolia transformed calli. Biotechnology and Bioengineering 100: 118–125.
41. Tada, A., K. Ishizuki, J. Iwamura, H. Mikami, Y. Hirao, I. Fujita, T. Yamazaki, H. Akiyama, and Y. Kawamura. 2013. Improvement of the assay method for steviol glycosides in the JECFA specifications. American Journal of Analytical Chemistry 4: 190–196.
42. Tepfer, D. 1984. Genetic transformation of several species of higher plants by Agrobacterium rhizogenes: Phenotypic consequences and sexual transmission of transformed genotype and phenotype. Cell 37: 959–967.
43. Tzfira, T., and V. Citovsky. 2006. Agrobacterium-mediated genetic transformation of plants: Biology and biotechnology. Current Opinion in Biotechnology 17: 147–154.
44. Yadav, S.K., and P. Guleria. 2012. Steviol glycosides from Stevia: Biosynthesis pathway review and their application in foods and medicine. Critical Reviews in Food Science and Nutrition 52: 988–998.
45. Yamazaki, T., H.E. Flores, K. Shimomura, and K. Yoshihira. 1991. Examination of steviol glucosides production by hairy root and shoot cultures of Stevia rebaudiana. Journal of Natural Products 54: 986–992.
46. Yang, D.C., and Y.E. Choi. 2000. Production of transgenic plants via Agrobacterium rhizogenes mediated transformation of Panax ginseng. Plant Cell Reports 19: 491–496.
47. Zhou, M.L., X.M. Zhu, J.R. Shao, Y.X. Tang, and Y.M. Wu. 2011. Production and metabolic engineering of bioactive substances in plant hairy root culture. Applied Microbiology and Biotechnology 90: 1229–1239.