Skip to main content
SpringerLink
Log in

Iron nano modulated growth and biosynthesis of steviol glycosides in Stevia rebaudiana

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Application of nanomaterials is becoming the most effective strategy of elicitation to produce a desirable level of plant biomass with complex medicinal compounds. This study was, designed to check the influence of commercial iron nanoparticles (FeNPs) on physical growth characteristics, antioxidant status and production of steviol glycosides of in vitro grown Stevia rebaudiana. Results indicated that lower concentrations of FeNPs (45 µg/L) had a positive influence on morphological growth parameters. At a higher dose (90, and 135 µg/L) FeNPs in culture media were found detrimental to growth characteristics and development. Furthermore, the stress caused by FeNPs at 135 µg/L in cultures produced higher levels of total phenolic content (3.2 ± 0.042 mg/g dry weight: DW), total flavonoid content (1.6 ± 0.022 mg/g DW and antioxidant activity (73 ± 4.6%). In addition, plants grown in the presence of FeNPs at 90 µg/L resulted in higher enzymatic antioxidant activities (SOD = 3.2 ± 0.042 U/mg; POD = 2.1 ± 0.026 U/mg; CAT = 2.6 ± 0.034 U/mg and APx = 3.3 ± 0.043 U/mg), respectively. Furthermore, exposure to a low dose of FeNPs (45 µg/L) exhibited the maximum amount of stevioside (stevioside: 4.2 ± 0.058 mg/g (DW) and rebaudioside A: 4.9 ± 0.068 mg/g DW) as compared to high doses. The current investigation confirms the effectiveness of FeNPs in growth media and offers a suitable prospect for commercially desirable production of S. rebaudiana biomass with higher sweet glycosides profiles in vitro.

Key message

Lower concentrations of Iron nano particles (FeNPs) had a positive influence on morphological growth parameters, production of antioxidant secondary metabolites and natural calorie free steviol glycosides in Stevia rebaudiana.

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

Access this article

Log in via an institution

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abbasi BH, Khan MA, Mahmood T, Ahmad M, Chaudhary MF, Khan MA (2010) Shoot regeneration and free-radical scavenging activity in Silybum marianum L. Plant Cell Tissue Organ Cult 101(3):371–376

    Article  CAS  Google Scholar 

  • Abeles FB, Biles CL (1991) Characterization of peroxidases in lignifying peach fruit endocarp. Plant Physiol 95(1):269–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akbar-Mozafari A, Havas F, Ghaderi N (2018) Application of iron nanoparticles and salicylic acid in in vitro culture of strawberries (Fragaria× ananassa Duch.) to cope with drought stress. Plant Cell Tissue Organ Cult 132(3):511–523

    Article  CAS  Google Scholar 

  • Ali H, Khan MA, Kayani WK, Khan T, Khan RS (2018) Thidiazuron regulated growth, secondary metabolism and essential oil profiles in shoot cultures of Ajuga bracteosa. Ind Crops Prod 121:418–427

    Article  CAS  Google Scholar 

  • Ali A, Mohammad S, Khan MA, Raja NI, Arif M, Kamil A, Z-u-R M (2019) Silver nanoparticles elicited in vitro callus cultures for accumulation of biomass and secondary metabolites in Caralluma tuberculata. Artif Cells Nanomed Biotechnol 47(1):715–724

    Article  CAS  PubMed  Google Scholar 

  • Arrigoni O, De Gara L, Tommasi F, Liso R (1992) Changes in the ascorbate system during seed development of Vicia faba L. Plant Physiol 99(1):235–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brittenham G (1994) New advances in iron metabolism, iron deficiency, and iron overload. Curr Opin Hematol 1(2):101–106

    CAS  PubMed  Google Scholar 

  • Castro-González CG, Sánchez-Segura L, Gómez-Merino FC, Bello-Bello JJ (2019) Exposure of stevia (Stevia rebaudiana B) to silver nanoparticles in vitro: transport and accumulation. Sci Rep 9(1):1–10

    Article  CAS  Google Scholar 

  • Chang CC, Yang MH, Wen HM, Chern JC (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10(3):178–182

    CAS  Google Scholar 

  • Chung I-M, Rajakumar G, Thiruvengadam M (2018) Effect of silver nanoparticles on phenolic compounds production and biological activities in hairy root cultures of Cucumis anguria. Acta Biol Hung 69(1):97–109

    Article  CAS  PubMed  Google Scholar 

  • Desai Heta B, Desai Charmi V, Suthar K, Singh D, Suthar H (2017) Effect of magnesium nanoparticles on physiology and stevioside in Stevia rebaudiana bertoni. European Journal of Biomedical 4(9):642–646

    Google Scholar 

  • Dilshad E, Ismail H, Khan MA, Cusido RM, Mirza B (2020) Metabolite profiling of Artemisia carvifolia Buch transgenic plants and estimation of their anticancer and antidiabetic potential. Biocatal Agric Biotechnol 25:101539

    Article  Google Scholar 

  • El-Temsah YS, Joner EJ (2012) Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environ Toxicol 27(1):42–49

    Article  CAS  PubMed  Google Scholar 

  • Ghazal B, Saif S, Farid K, Khan A, Rehman S, Reshma A, Fazal H, Ali M, Ahmad A, Rahman L (2018) Stimulation of secondary metabolites by copper and gold nanoparticles in submerge adventitious root cultures ofStevia rebaudiana (Bert). IET Nanobiotechnol 12(5):569–573

    Article  PubMed  PubMed Central  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59(2):309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golkar P, Moradi M, Garousi GA (2019) Elicitation of Stevia glycosides using salicylic acid and silver nanoparticles under callus culture. Sugar Technol 21(4):569–577

    Article  CAS  Google Scholar 

  • Jamzad Fard M, Mousavi M, Ghafarian Mogharab M (2013) Investigation on effect of Fe oxide nanoparticles on shoot proliferation and rooting in miniature rose in vitro. In: The 1st national conference on solution to access sustainable development in agriculture, natural resources and environment, vol 10, p 7

  • Javed R, Mohamed A, Yücesan B, Gürel E, Kausar R, Zia M (2017a) CuO nanoparticles significantly influence in vitro culture, steviol glycosides, and antioxidant activities of Stevia rebaudiana Bertoni. Plant Cell Tissue Organ Cult 131(3):611–620

    Article  CAS  Google Scholar 

  • Javed R, Usman M, Yücesan B, Zia M, Gürel E (2017b) Effect of zinc oxide (ZnO) nanoparticles on physiology and steviol glycosides production in micropropagated shoots of Stevia rebaudiana Bertoni. Plant Physiol Biochem 110:94–99

    Article  CAS  PubMed  Google Scholar 

  • Jhinjer RK, Verma L, Wani SH, Gosal SS (2016) Molecular farming using transgenic approaches. Advances in plant breeding strategies: agronomic, abiotic and biotic stress traits. Springer, Berlin, pp 97–145

    Book  Google Scholar 

  • Kazmi A, Khan MA, Mohammad S, Ali A, Ali H (2019a) Biotechnological production of natural calorie free Steviol glycosides in stevia Rebaudiana: an update on current scenario. Curr Biotechnol 8(2):70–84

    Article  Google Scholar 

  • Kazmi A, Khan MA, Mohammad S, Ali A, Kamil A, Arif M, Ali H (2019b) Elicitation directed growth and production of steviol glycosides in the adventitious roots of Stevia rebaudiana Bertoni. Ind Crops Prod 139:111530

    Article  CAS  Google Scholar 

  • Keller AA, Lazareva A (2014) Predicted releases of engineered nanomaterials: from global to regional to local. Environ Sci Technol Lett 1(1):65–70

    Article  CAS  Google Scholar 

  • Khan MA, Abbasi BH, Ahmed N, Ali H (2013) Effects of light regimes on in vitro seed germination and silymarin content in Silybum marianum. Ind Crops Prod 46:105–110

    Article  CAS  Google Scholar 

  • Khan MA, Khan T, Ali H (2019a) Plant cell culture strategies for the production of terpenes as green solvents. Ind Appl Green Solv I 50:1–20

    CAS  Google Scholar 

  • Khan MA, Riaz MS, Ullaha N, Alid H, Nadhmane A (2019b) Plant cell nanomaterials interaction: growth, physiology and secondary metabolism. Analysis, fate, and toxicity of engineered nanomaterials in plants. Compr Anal Chem 84:23–54. https://doi.org/10.1016/bs.coac.2019.04.005

    Article  CAS  Google Scholar 

  • Kim J-H, Oh Y, Yoon H, Hwang I, Chang Y-S (2015) Iron nanoparticle-induced activation of plasma membrane H+-ATPase promotes stomatal opening in Arabidopsis thaliana. Environ Sci Technol 49(2):1113–1119

    Article  CAS  PubMed  Google Scholar 

  • Ladygin V, Bondarev N, Semenova G, Smolov A, Reshetnyak O, Nosov A (2008) Chloroplast ultrastructure, photosynthetic apparatus activities and production of steviol glycosides in Stevia rebaudiana in vivo and in vitro. Biol Plant 52(1):9–16

    Article  CAS  Google Scholar 

  • Li J, Hu J, Ma C, Wang Y, Wu C, Huang J, Xing B (2016) Uptake, translocation and physiological effects of magnetic iron oxide (γ-Fe2O3) nanoparticles in corn (Zea mays L.). Chemosphere 159:326–334

    Article  CAS  PubMed  Google Scholar 

  • Liu R, Lal R (2015) Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Sci Total Environ 514:131–139

    Article  CAS  PubMed  Google Scholar 

  • Ma C, Liu H, Guo H, Musante C, Coskun SH, Nelson BC, White JC, Xing B, Dhankher OP (2016) Defense mechanisms and nutrient displacement in Arabidopsis thaliana upon exposure to CeO2 and In2O3 nanoparticles. Environ Sci Nano 3(6):1369–1379

    Article  CAS  Google Scholar 

  • Magangana TP, Stander MA, Makunga NP (2018) Effect of nitrogen and phosphate on in vitro growth and metabolite profiles of Stevia rebaudiana Bertoni (Asteraceae). Plant Cell Tissue Organ Cult 134(1):141–151

    Article  CAS  Google Scholar 

  • Maurel C, Boursiac Y, Luu D-T, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95(4):1321–1358

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Shinzaki Y, Nishioka M, Horiguchi S, Tomizawa K-I (2006) Photoinactivation of ascorbate peroxidase in isolated tobacco chloroplasts: Galdieria partita APX maintains the electron flux through the water–water cycle in transplastomic tobacco plants. Plant Cell Physiol 47(2):200–210

    Article  CAS  PubMed  Google Scholar 

  • Mohammad S, Khan MA, Ali A, Khan L, Khan MS (2019) Feasible production of biomass and natural antioxidants through callus cultures in response to varying light intensities in olive (Olea europaea L.) cult. Arbosana. J Photochem Photobiol B 193:140–147

    Article  CAS  PubMed  Google Scholar 

  • Parisi C, Vigani M, Rodríguez-Cerezo E (2015) Agricultural nanotechnologies: what are the current possibilities? Nano Today 10(2):124–127

    Article  CAS  Google Scholar 

  • Poborilova Z, Opatrilova R, Babula P (2013) Toxicity of aluminium oxide nanoparticles demonstrated using a BY-2 plant cell suspension culture model. Environ Exp Bot 91:1–11

    Article  CAS  Google Scholar 

  • Pokhrel LR, Dubey B (2013) Evaluation of developmental responses of two crop plants exposed to silver and zinc oxide nanoparticles. Sci Total Environ 452:321–332

    Article  PubMed  CAS  Google Scholar 

  • Qian H, Peng X, Han X, Ren J, Sun L, Fu Z (2013) Comparison of the toxicity of silver nanoparticles and silver ions on the growth of terrestrial plant model Arabidopsis thaliana. J Environ Sci 25(9):1947–1956

    Article  CAS  Google Scholar 

  • Rui M, Ma C, Hao Y, Guo J, Rui Y, Tang X, Zhao Q, Fan X, Zhang Z, Hou T (2016) Iron oxide nanoparticles as a potential iron fertilizer for peanut (Arachis hypogaea). Front Plant Sci 7:815

    Article  PubMed  PubMed Central  Google Scholar 

  • Saeed S, Ali H, Khan T, Kayani W, Khan MA (2017) Impacts of methyl jasmonate and phenyl acetic acid on biomass accumulation and antioxidant potential in adventitious roots of Ajuga bracteosa Wall ex Benth., a high valued endangered medicinal plant. Physiol Mol Biol Plants 23(1):229–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salehi B, López MD, Martínez-López S, Victoriano M, Sharifi-Rad J, Martorell M, Rodrigues CF, Martins N (2019) Stevia rebaudiana Bertoni bioactive effects: from in vivo to clinical trials towards future therapeutic approaches. Phytotherapy Res 33(11):2904–2917

    Article  Google Scholar 

  • Sarmast M, Niazi A, Salehi H, Abolimoghadam A (2015) Silver nanoparticles affect ACS expression in Tecomella undulata in vitro culture. Plant Cell Tissue Organ Cult 121(1):227–236

    Article  CAS  Google Scholar 

  • Sharafi E, Khayam Nekoei S, Fotokian MH, Davoodi D, Hadavand Mirzaei H, Hasanloo T (2013) Improvement of hypericin and hyperforin production using zinc and iron nano-oxides as elicitors in cell suspension culture of St John’s wort (Hypericum perforatum L.). JMPB 2:177–184

    Google Scholar 

  • Sher Khan R, Iqbal A, Malak R, Shehryar K, Attia S, Ahmed T, Ali Khan M, Arif M, Mii M (2019) Plant defensins: types, mechanism of action and prospects of genetic engineering for enhanced disease resistance in plants. 3 Biotech 26:1015–1017

    Google Scholar 

  • Sheykhbaglou R, Sedghi M, Shishevan MT, Sharifi RS (2010) Effects of nano-iron oxide particles on agronomic traits of soybean. Not Sci Biol 2(2):112–113

    Article  Google Scholar 

  • Taghizadeh M, Nasibi F, Kalantari KM, Ghanati F (2019) Evaluation of secondary metabolites and antioxidant activity in Dracocephalum polychaetum Bornm. cell suspension culture under magnetite nanoparticles and static magnetic field elicitation. Plant Cell Tissue Organ Cult 136(3):489–498

    Article  CAS  Google Scholar 

  • Taj F, Khan MA, Ali H, Khan RS (2019) Improved production of industrially important essential oils through elicitation in the adventitious roots of Artemisia amygdalina. Plants 8(10):430

    Article  CAS  PubMed Central  Google Scholar 

  • Tavakoli H, Tavakoli N, Moradi F (2019) The effect of the elicitors on the steviol glycosides biosynthesis pathway in Stevia rebaudiana. Funct Plant Biol 46(9):787–795

    Article  CAS  PubMed  Google Scholar 

  • Thiyagarajan M, Venkatachalam P (2012) Large scale in vitro propagation of Stevia rebaudiana (bert) for commercial application: pharmaceutically important and antidiabetic medicinal herb. Ind Crops Prod 37(1):111–117

    Article  CAS  Google Scholar 

  • Vazquez-Hernandez C, Feregrino-Perez AA, Perez-Ramirez I, Ocampo-Velazquez RV, Rico-García E, 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 Crops Prod 139:111479

    Article  CAS  Google Scholar 

  • Villagarcia H, Dervishi E, de Silva K, Biris AS, Khodakovskaya MV (2012) Surface chemistry of carbon nanotubes impacts the growth and expression of water channel protein in tomato plants. Small 8(15):2328–2334

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Qian J, Yao L, Lu Y (2015) Enhanced production of flavonoids by methyl jasmonate elicitation in cell suspension culture of Hypericum perforatum. Bioresour Bioprocess 2(1):5

    Article  Google Scholar 

  • Wölwer-Rieck U (2012) The leaves of Stevia rebaudiana (Bertoni), their constituents and the analyses thereof: a review. J Agric Food Chem 60(4):886–895

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Yousaf R, Khan MA, Ullah N, Khan I, Hayat O, Shehzad MA, Khan I, Taj F, Ud Din N, Khan A (2019) Biosynthesis of anti-leishmanial natural products in callus cultures of Artemisia scoparia. Artif Cells Nanomed Biotechnol 47(1):1122–1131

    Article  CAS  PubMed  Google Scholar 

  • Zuverza-Mena N, Armendariz R, Peralta-Videa JR, Gardea-Torresdey JL (2016) Effects of silver nanoparticles on radish sprouts: root growth reduction and modifications in the nutritional value. Front Plant Sci 7:90

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biotechnology, Faculty of Chemical and Life Sciences, Abdul Wali Khan University Mardan (AWKUM), Mardan, 23390, Pakistan

    Mubarak Ali Khan

  2. Biotechnology Lab, Agricultural Research Institute (ARI), Tarnab Peshawar, Peshawar, Pakistan

    Amir Ali & Sher Mohammad

  3. Department of Biotechnology, Bacha Khan University, Charsadda, KP, Pakistan

    Huma Ali

  4. Department of Biotechnology, University of Malakand, Chakdara, KP, Pakistan

    Tariq Khan

  5. Department of Botany, PMAS Arid Agriculture University, Rawalpindi, Pakistan

    Zia-ur-Rehman Mashwani

  6. Department of Pharmacy, University of Peshawar, Peshawar, Pakistan

    Asif Jan

  7. Botany and Microbiology Department, College of Science, King Saud University, Riyadh, 11362, Saudi Arabia

    Pervaiz Ahmad

Authors
  1. Mubarak Ali Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amir Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sher Mohammad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huma Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tariq Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zia-ur-Rehman Mashwani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Asif Jan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pervaiz Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mubarak Ali Khan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Mohammad Faisal.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, M.A., Ali, A., Mohammad, S. et al. Iron nano modulated growth and biosynthesis of steviol glycosides in Stevia rebaudiana. Plant Cell Tiss Organ Cult 143, 121–130 (2020). https://doi.org/10.1007/s11240-020-01902-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-020-01902-6

Keywords

Search

Navigation