Skip to main content
Log in

Steviol glycosides profile in Stevia rebaudiana Bertoni hairy roots cultured under oxidative stress-inducing conditions

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The ability to synthesize particular steviol glycosides (SvGls) was studied in Stevia rebaudiana Bertoni hairy roots (HR) grown in the light or in the dark under the influence of different osmotic active compounds. Manipulation of culture conditions led to changes in the morphology and growth rate of HR, as well as to an increase in oxidative stress manifested as an enhancement in endogenous hydrogen peroxide concentration in the cultured samples. The highest level of H2O2 was noted in HR cultured under light or in the medium with the highest osmotic potential. This correlated with the highest increase in the expression level of ent-kaurenoic acid hydroxylase, responsible for the redirection of metabolic route to SvGls biosynthesis pathway. An analysis of transcriptional activity of some UDPglucosyltransferase (UGT85c2, UGT74g1, UGT76g1) revealed that all of them were upregulated due to the manipulation of culture conditions. However, the level of their upregulation depended on the type of stress factor used in our experiment. Analysis of SvGls content revealed that HR grown under all applied conditions were able to synthesize and accumulate several SvGls but their concentration differed between the samples across the different conditions. The level of rebaudioside A concentration exceeded the content of stevioside in HR in all tested conditions. Concomitantly, the presence of some minor SvGls, such as steviolbioside and rebaudioside F, was confirmed only in HR cultured in the lowest osmotic potential of the medium while rebaudioside D was also detected in the samples cultured in the media supplemented with NaCl or PEG.

Key Points

● Several steviol glycosides are synthesized in hairy roots of S. rebaudiana.

● Light or osmotic factors cause enhancement in oxidative stress level in hairy roots.

● It correlates with a significant increase in the level of KAH expression.

● UGTs expression and steviol glycosides content depends on culture conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

All the relevant data used to support the findings of this study are included within the article.

References

  • Ahrazem O, Rubio-Moraga A, Trapero-Mozos A, López Climent AF, Gómez-Cadenas A, Gómez-Gómez L (2015) Ectopic expression of a stress-inducible glycosyltransferase from saffron enhances salt and oxidative stress tolerance in Arabidopsis while alters anchor root formation. Plant Sci 234:60–73

    Article  CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Ashraf MA, Iqbal M, Rasheed R, Hussain I, Riaz M, Arif MS (2018) Environmental stress and secondary metabolites in plants: an overview. In: Ahmad P, Ahanger MA, Singh VP, Tripathi DK, Alam P, Alyemeni MN (eds) Plant metabolites and regulation under environmental stress. Academic Press, London, pp 153–167

    Chapter  Google Scholar 

  • Balmer Y, Vensel WH, DuPont FM, Buchanan BB, Hurkman WJ (2006) Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. J Exp Bot 57:1591–1602

    Article  CAS  PubMed  Google Scholar 

  • Bohnert HJ (1995) Adaptations to environmental stresses. Plant Cell Online 7:1099–1111

    Article  CAS  Google Scholar 

  • Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277:2022–2037

    Article  CAS  PubMed  Google Scholar 

  • Bondarev N, Nosov A, Kornienko A (1997) Influence of several cultural factors on the growth and efficiency of Stevia callus and suspension cultures. Biotechnology 7:30–37

    Google Scholar 

  • Bondarev N, Reshetnyak O, Nosov A (2001) Peculiarities of diterpenoid steviol glycoside production in in vitro cultures of Stevia rebaudiana Bertoni. Plant Sci 161:155–163

    Article  CAS  Google Scholar 

  • Bondarev N, Reshetnyak O, Nosov A (2003a) Effects of nutrient medium composition on development of Stevia rebaudiana shoots cultivated in the roller bioreactor and their production of steviol glycosides. Plant Sci 165:845–850

    Article  CAS  Google Scholar 

  • Bondarev N, Sukhanova M, Reshetnyak OV, Nosov AM (2003b) Steviol glycoside content in different organs of Stevia rebaudiana and its dynamics during ontogeny. Biol Plant 47:261–264

    Article  CAS  Google Scholar 

  • Bowles D, Isayenkova J, Lim EK, Poppenberger B (2005) Glycosyltransferases: managers of small molecules. Curr Opin Plant Biol 8:254–263

    Article  CAS  PubMed  Google Scholar 

  • Brandle JE, Telmer PG (2007) Steviol glycoside biosynthesis. Phytochemistry 68:1855–1863

    Article  CAS  PubMed  Google Scholar 

  • Brandle J, Richman A, Swanson AK, Chapman BP (2002) Leaf ESTs from Stevia rebaudiana: a resource for gene discovery in diterpene synthesis. Plant Mol Biol 50:613–622

    Article  CAS  PubMed  Google Scholar 

  • Bulgakov VP (2008) Functions of rol genes in plant secondary metabolism. Biotechnol Adv 26:318–324

    Article  CAS  PubMed  Google Scholar 

  • Cantabella D, Piqueras A, Acosta-Motos JR, Bernal-Vicente A, Hernández JA, Díaz-Vivancos P (2017) Salt-tolerance mechanisms induced in Stevia rebaudiana Bertoni: effects on mineral nutrition, antioxidative metabolism and steviol glycoside content. Plant Physiol Biochem 115:484–496

    Article  CAS  PubMed  Google Scholar 

  • Carneiro JWP, Muniz AS, Guedes TA (1997) Greenhouse bedding plant production of Stevia rebaudiana (Bert) Bertoni. Can J Plant Sci 77:473–474

    Article  Google Scholar 

  • Ceunen S, Geuns JM (2013) Steviol glycosides: chemical diversity, metabolism, and function. J Nat Prod 76:1201–1228

    Article  CAS  PubMed  Google Scholar 

  • Chen JM, Ding L, Sui XC, Xia YM, Wan HD, Lu T (2016) Production of a bioactive sweetener steviolbioside via specific hydrolyzing ester linkage of stevioside with a b-galactosidase. Food Chem 196:155–160

    Article  CAS  PubMed  Google Scholar 

  • Chomczynski P (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform. Anal Biochem 162:156–159

    Article  CAS  PubMed  Google Scholar 

  • Cramer B, Ikan R (1986) Sweet glycosides from the Stevia plant. Chem Br 22:915–917

    Google Scholar 

  • Debnath M, Ashwath N, Hill CB, Callahan DL, Dias DA, Jayasinghe NS, Midmore DJ, Roessner U (2018) Comparative metabolic and ionomic profiling of two cultivars of Stevia rebaudiana Bert. (Bertoni) grown under salinity stress. Plant Physiol Biochem 129:56–70

    Article  CAS  PubMed  Google Scholar 

  • Edreva A, Velikova V, Tsonev T, Dagnon S, Gürel A, Aktaş L, Gesheva E (2008) Stress-protective role of secondary metabolites: diversity of functions and mechanisms. Gen Appl Plant Physiol 34:67–78

    CAS  Google Scholar 

  • Esmaeili F, Ghaheri M, Kahrizi D, Mansouri M, Safavi SM, Ghorbani T, Muhammadi S, Rahmanian E, Vaziri S (2018) Effects of various glutamine concentrations on gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni. Cell Mol Biol 64:1–5

    Article  PubMed  Google Scholar 

  • Fallah F, Nokhasi F, Ghaheri M, Kahrizi D, Agha AB, Ghorbani T, Kazemi E, Ansarypour Z (2017) Effect of salinity on gene expression, morphological and biochemical characteristics of Stevia rebaudiana Bertoni under in vitro conditions. Cell Mol Biol 63:102–106

    Article  CAS  PubMed  Google Scholar 

  • Gasmalla MAA, Yang R, Hua X (2014) Stevia rebaudiana Bertoni: an alternative sugar replacer and its application in food industry. Food Eng Rev 6:150–162

    Article  CAS  Google Scholar 

  • Ghaheri M, Kahrizi D, Bahrami G, Mohammadi-Motlagh H-R (2019) Study of gene expression and steviol glycosides accumulation in Stevia rebaudiana Bertoni under various mannitol concentrations. Mol Biol Rep 46:7–16

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Subudhi E, Nayak S (2008) Antimicrobial assay of Stevia rebaudiana Bertoni leaf extracts against 10 pathogens. Int J Integr Biol 2:27–31

    Google Scholar 

  • Guleria P, Yadav SK (2013) Agrobacterium mediated transient gene silencing (AMTS) in Stevia rebaudiana: insights into steviol glycoside biosynthesis pathway. PLoS One 8:e74731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta E, Purwar S, Sundaram S, Rai GK (2013) Nutritional and therapeutic values of Stevia rebaudiana: a review. J Med Plant Res 7:3343–3353

    CAS  Google Scholar 

  • Gupta P, Sharma S, Saxena S (2014) Effect of salts (NaCl and Na2CO3) on callus and suspension culture of Stevia rebaudiana for steviol glycoside production. Appl Biochem Biotechnol 172:2894–2906

    Article  CAS  PubMed  Google Scholar 

  • Gupta P, Sharma S, Saxena S (2015) Biomass yield and steviol glycoside production in callus and suspension culture of Stevia rebaudiana treated with proline and polyethylene glycol. Appl Biochem Biotechnol 176:863–874

    Article  CAS  PubMed  Google Scholar 

  • Gupta E, Purwar S, Sundaram S, Prashasti Tripathi P, Rai G (2016) Stevioside and rebaudioside A – predominant ent-kaurene diterpene glycosides of therapeutic potential: a review. Czech J Food Sci 34:281–299

    Article  CAS  Google Scholar 

  • Hajihashemi S, Ehsanpour AA (2014) Antioxidant response of Stevia rebaudiana B. to polyethylene glycol and paclobutrazol treatments under in vitro culture. Appl Biochem Biotechnol 172:4038–4052

    Article  CAS  PubMed  Google Scholar 

  • Hajihashemi S, Geuns JM (2016) Gene transcription and steviol glycoside accumulation in Stevia rebaudiana under polyethylene glycol-induced drought stress in greenhouse cultivation. FEBS Open Biol 6:937–944

    Article  CAS  Google Scholar 

  • Hajihashemi S, Geuns JMC, Ehsanpour AA (2013) Gene transcription of steviol glycoside biosynthesis in Stevia rebaudiana Bertoni under polyethylene glycol, paclobutrazol and gibberellic acid treatments in vitro. Acta Physiol Plant 35:2009–2014

    Article  CAS  Google Scholar 

  • Helliwell CA, Poole A, Peacock WJ, Dennis ES (1999) Arabidopsis ent-kaurene oxidase catalyzes three steps of gibberellin biosynthesis. Plant Physiol 119:507–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong SY, Roze LV, Linz JE (2013) Oxidative stress-related transcription factors in the regulation of secondary metabolism. Toxins 5:683–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horvath DM, Chuai NH (1996) Identification of an immediate-early salicylic acid-inducible tobacco gene and characterization of induction by other compounds. Plant Mol Biol 31:1061–1072

    Article  CAS  PubMed  Google Scholar 

  • Hsing YI, Su WF, Chang WC (1983) Accumulation of stevioside and rebaudioside A in callus culture of Stevia rebaudiana Bertoni. Bot Bull Acad Sin 24:115–119

    CAS  Google Scholar 

  • Humphrey T, Menassa R, Brandle J (2006) Spatial organisation of four nzymes from Stevia rebaudiana that are involved in steviol glycoside synthesis. Plant Mol Biol 61:47–62

    Article  CAS  PubMed  Google Scholar 

  • Hussain MS, Rahman MA, Fareed S, Ansari S, Ahmad IZ, Mohd S (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioapllied Sci 4:10–20

    Article  CAS  Google Scholar 

  • Hussin S, Geissler N, El-Far MMM, Koyro H-W (2017) Effects of salinity and short-term elevated atmospheric CO2 on the chemical equilibrium between CO2 fixation and photosynthetic electron transport of Stevia rebaudiana Bertoni. Plant Physiol Biochem 118:178–186

    Article  CAS  PubMed  Google Scholar 

  • Jadeja RP, Tadhani MB, Rema S, Parekh LJ (2005) Qualitative studies on the production of stevioside in in vitro callus culture of Stevia rebaudiana Bertoni. Analele ştiinţifice ale Universitaţii “Al. I. Cuza” Iaşi Tomul LI, s. II a. Biologie Vegetala 51:139–140

    Google Scholar 

  • Janarthanam B, Gopalakrishnan M, Sekar T (2010) Secondary metabolite production in callus cultures of Stevia rebaudiana Bertoni. Bangladesh J Sci Ind Res 45:243–248

    Article  CAS  Google Scholar 

  • Javed R, Gürel E (2019) Salt stress by NaCl alters the physiology and biochemistry of tissue culture-grown Stevia rebaudiana Bertoni. Turk J Agric For 43:11–20

    Article  CAS  Google Scholar 

  • Kang KH, Lee EW (1981) Physio-ecological studies on stevia (Stevia rebaudiana Bertoni). Korean J Crop Sci 26:69–89

    Google Scholar 

  • Khalil SA, Zamir R, Ahmad N (2014) Selection of suitable propagation method for consistent plantlets production in Stevia rebaudiana (Bertoni). Saudi J Biol Sci 21:566–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim MJ, Zheng J, Liao MH, Jang I-C (2019) Overexpression of SrUGT76G1 in Stevia alters major steviol glycosides composition towards improved quality. Plant Biotechnol J 17:1037–1047

    Article  CAS  PubMed  Google Scholar 

  • Kohda H, Kasai R, Yamasaki K, Murakami K, Tanaka O (1976) New sweet diterpene glucosides from Stevia rebaudiana. Phytochem 15:981–983

    Article  CAS  Google Scholar 

  • Królicka A, Staniszewska I, Bielawski K, Maliński E, Szafranek J, Łojkowska E (2001) Establishment of hairy root cultures of Ammi majus. Plant Sci 160:259–264

    Article  PubMed  Google Scholar 

  • Kumari M, Chandra S (2015) Phytochemical studies and estimation of major steviol glycosides in varied parts of Stevia rebaudiana. Int J Pharm Pharm Sci 7:62–65

    CAS  Google Scholar 

  • Ladygin VG, Bondarev NI, Semenova GA, Smolov AA, Reshetnyak OV, Nosov AM (2008) Chloroplast ultrastructure, photosynthetic apparatus activities and production of steviol glycosides in Stevia rebaudiana in vivo and in vitro. Biol Plant 52:9–16

    Article  CAS  Google Scholar 

  • Langlois-Meurinne M, Gachon CM, Saindrenan P (2005) Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv tomato in Arabidopsis. Plant Physiol 139:1890–1901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Roy J, Huss B, Creach A, Hawkins S, Neutelings G (2016) Glycosylation is a major regulator of phenylpropanoid availability and biological activity in plants. Front Plant Sci 7:735

    PubMed  PubMed Central  Google Scholar 

  • Lee KR, Park JR, Choi BS (1982) Studies on the callus culture of stevia as a new sweetening source and the formation of stevioside. Korean J Food Sci Technol 14:179–183

    CAS  Google Scholar 

  • Lee SG, Salomon E, Yu O, Jez JM (2019) Molecular basis for branched steviol glucoside biosynthesis. PNAS 116:13131–13136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Libik-Konieczny M, Capecka E, Kąkol E, Dziurka M, Grabowska-Joachimiak A, Sliwinska E, Pistelli L (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. Sci Hortic (Amsterdam) 23:10–18

    Article  CAS  Google Scholar 

  • Lucho SR, do Amaral MN, Auler PA (2019) Salt stress-induced changes in in vitro cultured Stevia rebaudiana Bertoni: effect on metabolite contents, antioxidant capacity and expression of steviol glycosides-related biosynthetic genes. J Plant Growth Regul 38:1341–1353

    Article  CAS  Google Scholar 

  • Luwańska A, Perz A, Mańkowska G, Wielgus K (2015) Application of in vitro stevia (Stevia rebaudiana Bertoni) cultures in obtaining steviol glycoside rich material. Herba Polonica 61:50–63

    Article  Google Scholar 

  • Mathur S, Shekhawat GS (2013) Establishment and characterization of Stevia rebaudiana (Bertoni) cell suspension culture: an in vitro approach for production of stevioside. Acta Physiol Plant 35:1–9

    Article  CAS  Google Scholar 

  • Mathur S, Bulchandani N, Parihar S, Shekhawat GS (2017) Critical review on steviol glycosides: pharmacological, toxicological and therapeutic aspects of high potency zero caloric sweetener. Int J Pharmacol 13:916–928

    Article  CAS  Google Scholar 

  • Mazel A, Levine A (2002) Induction of glucosyltransferase transcription and activity during superoxide-dependent cell death in Arabidopsis plants. Plant Physiol Biochem 40:133–140

    Article  CAS  Google Scholar 

  • Meissner D, Albert A, Bottcher C, Strack D, Milkowski C (2008) The role of UDP glucose: hydroxycinnamate glucosyltransferases in phenylpropanoid metabolism and the response to UV-B radiation in Arabidopsis thaliana. Planta 228:663–674

    Article  CAS  PubMed  Google Scholar 

  • Michalec-Warzecha Ż, Pistelli L, D’Angiolillo F, Libik-Konieczny M (2016) Establishment of highly efficient agrobacterium rhizogenes-mediated transformation for Stevia rebaudiana Bertoni explants. Acta Biol Cracoviensia Ser Bot 58:113–118

    Article  CAS  Google Scholar 

  • Mohamed AAA, Ceunen S, Geuns JMC, Van den Ende W, De Ley M (2011) UDP-dependent glycosyltransferases involved in the biosynthesis of steviol glycosides. J Plant Physiol 168:1136–1141

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee C, Sircar D, Chatterjee M, Das S, Mitra A (2014) Combating photooxidative stress in green hairy roots of Daucus carota cultivated under light irradiation. J Plant Physiol 171:179–187

    Article  CAS  PubMed  Google Scholar 

  • Pandey M, Chikara SK (2015) Effect of salinity and drought stress on growth parameters, glycoside content and expression level of vital genes in steviol glycosides biosynthesis pathway of Stevia rebaudiana (Bertoni). Int J Genet 7:153–160

    CAS  Google Scholar 

  • Pandey H, Pandey P, Pandey SS, Singh S, Banerjee S (2016) Meeting the challenge of stevioside production in the hairy roots of Stevia rebaudiana by probing the underlying process. Plant Cell Tissue Organ Cult 126:511–521

    Article  CAS  Google Scholar 

  • Pazuki A, Aflaki F, Yücesan B, Gürel S (2019) Effects of cytokinins, gibberellic acid 3, and gibberellic acid 4/7 on in vitro growth, morphological traits, and content of steviol glycosides in Stevia rebaudiana. Plant Physiol Biochem 137:154–161

    Article  CAS  PubMed  Google Scholar 

  • Pistelli L, Giovannini A, Ruffoni B, Bertoli A, Pistelli L (2010) Hairy root cultures for secondary metabolites production. Adv Exp Med Biol 698:167–182

    Article  CAS  PubMed  Google Scholar 

  • Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reis RV, Silva TFO, Chierrito TPC, Albiero ALM, Souza LA, Goncalves JE, Oliveira AJB, Goncalves RAC (2017) Morpho-anatomical study of Stevia rebaudiana roots grown in vitro and in vivo. Br J Pharmacogn 27:34–39

    Article  Google Scholar 

  • Richman A, Swanson A, Humphrey T, Chapman R, McGarvey B, Pocs R, Brandle J (2005) Functional genomics uncovers three glucosyltransferases involved in the synthesis of the major sweet glucosides of Stevia rebaudiana. Plant J 41:56–67

    Article  CAS  PubMed  Google Scholar 

  • Selmar D, Kleinwächter M (2013) Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation of natural products. Plant Cell Physiol 54:817–826

    Article  CAS  PubMed  Google Scholar 

  • Sepúlveda-Jiménez G, Rueda-Benítez P, Porta H, Rocha-Sosa M (2005) A red beet (Beta vulgaris) UDP-glucosyltransferase gene induced by wounding, bacterial infiltration and oxidative stress. J Exp Bot 56:605–611

    Article  PubMed  CAS  Google Scholar 

  • Shahverdi MA, Omidi H, Tabatabaei SJ (2018) Morpho-physiological responces of Stevia (Stevia rebaudiana ) to salinity under hydroponic culture conditions (a case of study in Iran). Appl Ecol Environ Res 16:17–28

    Article  Google Scholar 

  • Shkryl YN, Veremeichik GN, Bulgakov VP, Tchernoded GK, Mischenko NP, Fedoreyev SA, Zhuravlev YN (2008) Individual and combined effects of the rolA, B, and C genes on anthraquinone production in Rubia cordifolia transformed calli. Biotechnol Bioeng 100:118–125

    Article  CAS  PubMed  Google Scholar 

  • Sivaram L, Mukundan U (2003) In vitro culture studies on Stevia rebaudiana. In Vitro Cell Dev Biol Plant 39:520–523

    Article  Google Scholar 

  • Srivastava S, Srivastava AK (2007) Hairy root culture for mass-production of high-value secondary metabolites. Crit Rev Biotechnol 27:29–43

    Article  CAS  PubMed  Google Scholar 

  • Stoyanova S, Geuns J, Hideg É, Van Den Ende W (2011) The food additives inulin and stevioside counteract oxidative stress. Int J Food Sci Nutr 62:207–214

    Article  CAS  PubMed  Google Scholar 

  • Sun YG, Wang B, Jin SH, Qu XX, Li YJ, Hou BK (2013) Ectopic expression of Arabidopsis glycosyltransferase UGT85A5 enhances salt stress tolerance in tobacco. PLoS One 8:e59924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swanson SM, Mahady GB, Beecher CWW (1992) Stevioside biosynthesis by callus, root, shoot and rooted shoot cultures in vitro. Plant Cell Tissue Organ Cult 28:151–157

    Article  CAS  Google Scholar 

  • Tanaka O (1997) Improvement of taste of natural sweeteners. Pure Appl Chem 69:675–683

    Article  CAS  Google Scholar 

  • Tattini M, Loreto F, Fini A, Guidi L, Brunetti C, Velikova V, Gori A, Ferrini F (2015) Isoprenoids and phenylpropanoids are part of the antioxidant defense orchestrated daily by drought-stressed Platanus × acerifolia plants during Mediterranean summers. New Phytol 207:613–626

    Article  CAS  PubMed  Google Scholar 

  • Taware AS, Mukadam DS, Chavan AM, Taware SD (2010) Comparative studies of in vitro and in vivo grown plants and callus of Stevia rebaudiana (Bertoni). Int J Integr Biol 9:10–15

    Google Scholar 

  • Tognetti VB, van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, de Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W, Genty B, Stubbs KA, Inze D, van Breusegem F (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22:2660–2679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Totté N, Charon L, Rohmer M, Compernolle F, Baboeuf I, Geuns JMC (2000) Biosynthesis of the diterpenoid steviol, an ent-kaurene derivative from Stevia rebaudiana Bertoni, via the methylerythritol phosphate pathway. Tetrahedron Lett 41:6407–6410

    Article  Google Scholar 

  • Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inze D, Van Breusegem F (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vazquez-Hernandez C, Feregrino-Perez AA, Perez-Ramirez I, Ocampo-Velazquez RV, García R, Torres-Pacheco I, Guevara-Gonzalez RG (2019) Controlled elicitation increases steviol glycosides (SGs) content and gene expression-associated to biosynthesis of SGs in Stevia rebaudiana B. cv. Morita II. Ind Crop Prod 139:111479

    Article  CAS  Google Scholar 

  • Vogt T, Jones P (2000) Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci 5:380–386

    Article  CAS  PubMed  Google Scholar 

  • White FF, Garfinkel DJ, Huffman GA, Gordon MP, Nester EW (1983) Sequence homologous to Agrobacterium rhizogenes TDNA in the genome of uninfected plants. Nature 301:348–350

    Article  CAS  Google Scholar 

  • Woźniak L, Marszałek K, Skąpska S (2014) Influence of steviol glycosides on the stability of vitamin C and anthocyanins. J Agric Food Chem 62:11264–11269

    Article  PubMed  CAS  Google Scholar 

  • Yadav AS, Singh S, Dhyani D, Ahuja PS (2011) A review on the improvement of stevia Stevia rebaudiana (Bertoni). Can J Plant Sci 91:1–27

    Article  Google Scholar 

  • Yamazaki T, Flores HE (1991) Examination of steviol glycoside production by hairy root and shoot cultures of Stevia rebaudiana. J Nat Prod 54:986–992

    Article  CAS  Google Scholar 

  • Yang YW, Chang CW (1979) In vitro plant regeneration from leaf explants of Stevia rebaudiana Bertoni. Z Pflanzen Physiol 93:337–343

    Article  Google Scholar 

  • Yang Y, Huang S, Han Y, Yuan H, Gu C, Wang Z (2015) Environmental cues induce changes of steviol glycosides contents and transcription of corresponding biosynthetic genes in Stevia rebaudiana. Plant Physiol Biochem 86:174–180

    Article  CAS  PubMed  Google Scholar 

  • Zeng J, Chen A, Li D, Yi B, Wu W (2013) Effects of salt stress on the growth, physiological responses, and glycoside contents of Stevia rebaudiana Bertoni. J Agric Food Chem 61:5720–5726

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Barbara Coulter for English language corrections.

Funding

This work was supported in part by projects funded by the National Science Centre (no. 2012/05/B/NZ9/01035 and no. 2013/09/N/NZ9/01650.

Author information

Authors and Affiliations

Authors

Contributions

MLK designed the experiment, ŻMW, PR, MD, OZ, RK, and LP performed the experiments and the data analysis. MLK prepared the manuscript. All authors approved the final version of the manuscript.

Corresponding author

Correspondence to Marta Libik-Konieczny.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Ethical approval

All the required ethical approvals have been taken before performing the experiments.

Consent to participate

All the authors have given consent to participate in the manuscript.

Consent for publication

All the authors have given consent for the publication of the manuscript.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary materials

ESM 1

(PDF 797 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Libik-Konieczny, M., Michalec-Warzecha, Ż., Dziurka, M. et al. Steviol glycosides profile in Stevia rebaudiana Bertoni hairy roots cultured under oxidative stress-inducing conditions. Appl Microbiol Biotechnol 104, 5929–5941 (2020). https://doi.org/10.1007/s00253-020-10661-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10661-5

Keywords

Navigation