Evaluation of secondary metabolites and antioxidant activity in Dracocephalum polychaetum Bornm. cell suspension culture under magnetite nanoparticles and static magnetic field elicitation

  • Marzieh Taghizadeh
  • Fatemeh NasibiEmail author
  • Khosrow Manouchehri Kalantari
  • Faezeh Ghanati
Original Article


Suspension-cultured Dracocephlum polychaetum Bornm. is a wild medicinal herb native to Iran, treated with a static magnetic field (SMF) and Fe2O3 magnetic nanoparticles (MNP). The effect of SMF (30 mT), Fe2O3 MNP (100 ppm) and the combination of these treatments on phenolic metabolism and the medicinal compounds were examined by high performance liquid chromatography and UV–Vis spectrophotometer. The activity of polyphenol oxidase and phenylalanine ammonialyase, as well as the content of total phenolics, flavonoid, anthocyanins, lignin and malondialdehyde in all treated cells, showed a significant difference with control. The intracellular content of rosmarinic acid, naringin, apigenin, thymol, carvacrol, quercetin and rutin, in all treated cells increased considerably. Their quantities also increased significantly in the treated cell culture media. These results suggest this increase is due to the increased production and secretion of the medicinal compounds from cells to the culture media upon application of SMF and Fe2O3 MNP.


Suspension cultured cells Magnetite nanoparticles Medicinal compounds Static magnetic field Antioxidant activity Secondary metabolite 



Fe2O3 magnetic nanoparticles


Static magnetic field


Polyphenol oxidase


Phenylalanine ammonia lyase





This study was supported by Shahid Bahonar University of Kerman and Tarbiat Modares University of Tehran, Iran.

Author contributions

MT and FN devised the project, the main conceptual ideas and proof outline. MT and FGh developed the theory. MT carried out the experiment and collected data. MT verified the analytical methods, and. analyzed and interpreted the data. MT wrote the manuscript. FN and KhMK. contributed to the final version of the manuscript. All authors supervised the project and discussed the results and contributed to the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aladjadjiyan A (2010) Influence of stationary magnetic field on lentil seeds. Int Agrophys 24:321–324Google Scholar
  2. Araji S et al (2014) Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut. Plant Physiol 164:1191–1203CrossRefGoogle Scholar
  3. Barreca D, Laganà G, Leuzzi U, Smeriglio A, Trombetta D, Bellocco E (2016) Evaluation of the nutraceutical, antioxidant and cytoprotective properties of ripe pistachio (Pistacia vera L., variety Bronte). Hulls Food Chem 196:493–502CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  5. Çelik Ö, Büyükuslu N, Atak Ç, Rzakoulieva A (2009) Effects of magnetic field on activity of superoxide dismutase and catalase in Glycine max (L.) Merr. Roots. Pol J Environ Stud 18:175–182Google Scholar
  6. Chandra S, Chakraborty N, Dasgupta A, Sarkar J, Panda K, Acharya K (2015) Chitosan nanoparticles: a positive modulator of innate immune responses in plants. Sci Rep 5:15195CrossRefGoogle Scholar
  7. Chua LS, Latiff NA, Lee SY, Lee CT, Sarmidi MR, Aziz RA (2011) Flavonoids and phenolic acids from Labisia pumila (Kacip Fatimah). Food Chem 127:1186–1192CrossRefGoogle Scholar
  8. Dias MI, Sousa MJ, Alves RC, Ferreira IC (2016) Exploring plant tissue culture to improve the production of phenolic compounds: a review. Ind Crops Prod 82:9–22CrossRefGoogle Scholar
  9. Dimkpa CO et al (2012) CuO and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sand-grown wheat. J Nanopart Res 14:1125CrossRefGoogle Scholar
  10. Dong J, Ma X, Wei Q, Peng S, Zhang S (2011) Effects of growing location on the contents of secondary metabolites in the leaves of four selected superior clones of Eucommia ulmoides. Ind Crops Prod 34:1607–1614CrossRefGoogle Scholar
  11. Galland P, Pazur A (2005) Magnetoreception in plants. J Plant Res 118:371–389CrossRefGoogle Scholar
  12. Gamborg O, Murashige T, Thorpe T, Vasil I (1976) Plant tissue culture media In vitro 12:473–478CrossRefGoogle Scholar
  13. Ghanati F, Morita A, Yokota H (2005) Effects of aluminum on the growth of tea plant and activation of antioxidant system. Plant Soil 276:133–141CrossRefGoogle Scholar
  14. Hara M, Oki K, Hoshino K, Kuboi T (2003) Enhancement of anthocyanin biosynthesis by sugar in radish (Raphanus sativus). Hypocotyl Plant Sci 164:259–265CrossRefGoogle Scholar
  15. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  16. Heidarabadi MD, Ghanati F, Fujiwara T (2011) Interaction between boron and aluminum and their effects on phenolic metabolism of Linum usitatissimum L. roots. Plant Physiol Biochem 49:1377–1383CrossRefGoogle Scholar
  17. Iiyama K, Wallis AF (1990) Determination of lignin in herbaceous plants by an improved acetyl bromide procedure. J Sci Food Agric 51:145–161CrossRefGoogle Scholar
  18. Jamshidi M, Ghanati F, Rezaei A, Bemani E (2016) Change of antioxidant enzymes activity of hazel (Corylus avellana L.) cells by AgNPs. Cytotechnology 68:525–530CrossRefGoogle Scholar
  19. Kahn V (1975) Polyphenol oxidase activity and browning of three avocado varieties. J Sci Food Agric 26:1319–1324CrossRefGoogle Scholar
  20. Khodami M, Abbasnejad M, Sheibani V, Mobasher M, Mehrabani M, Anaie Goodary A, Salari S (2011) Evaluation of the analgesic and anxiolytic effects of Dracocephalum polychaetum. Physiol Pharmacol 15:444–454Google Scholar
  21. Krishnaraj C, Jagan E, Ramachandran R, Abirami S, Mohan N, Kalaichelvan P (2012) Effect of biologically synthesized silver nanoparticles on Bacopa monnieri. (Linn.) Wettst plant growth metabolism. Process Biochem 47:651–658CrossRefGoogle Scholar
  22. Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061CrossRefGoogle Scholar
  23. Maffei ME (2014) Magnetic field effects on plant growth, development, and evolution. Front Plant Sci 5:445CrossRefGoogle Scholar
  24. Morita A, Yokota H, Ishka MR, Ghanati F (2006) Changes in peroxidase activity and lignin content of cultured tea cells in response to excess manganese. Soil Sci Plant Nutr 52:26–31CrossRefGoogle Scholar
  25. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  26. Pandya SR, Singh M (2015) Dispersion and optical activities of newly synthesized magnetic nanoparticles with organic acids and dendrimers in DMSO studied with UV/vis spectrophotometry. J Mol Liq 211:146–156CrossRefGoogle Scholar
  27. Payez A, Ghanati F, Behmanesh M, Abdolmaleki P, Hajnorouzi A, Rajabbeigi E (2013) Increase of seed germination, growth and membrane integrity of wheat seedlings by exposure to static and a 10-KHz. Electromagn Field Electromagn Biol Med 32:417–429CrossRefGoogle Scholar
  28. Peñuelas J, Llusià J (1997) Effects of carbon dioxide, water supply, and seasonality on terpene content and emission by Rosmarinus officinalis. J Chem Ecol 23:979–993CrossRefGoogle Scholar
  29. Petrussa E, Braidot E, Zancani M, Peresson C, Bertolini A, Patui S, Vianello A (2013) Plant flavonoids—biosynthesis, transport and involvement in stress responses. Int J Mol Sci 14:14950–14973CrossRefGoogle Scholar
  30. Poinapen D, Toppozini L, Dies H, Brown DC, Rheinstädter MC (2013) Static magnetic fields enhance lipid order in native plant plasma membrane. Soft Matter 9:6804–6813CrossRefGoogle Scholar
  31. Pouraboli I, Nazari S, Sabet N, Sharififar F, Jafari M (2016) Antidiabetic, antioxidant, and antilipid peroxidative activities of Dracocephalum polychaetum shoot extract in streptozotocin-induced diabetic rats: in vivo and in vitro studies. Pharm Biol 54:272–278CrossRefGoogle Scholar
  32. Rezaei A, Ghanati F, Behmanesh M (2010) Static magnetic field improved salicylic acid effect on taxol production in suspension-cultured hazel (Corylus avellana) cells. In: 6th International workshop on biological effects of electromagnetic fields pp 70–71Google Scholar
  33. Sahebjamei H, Abdolmaleki P, Ghanati F (2007) Effects of magnetic field on the antioxidant enzyme activities of suspension-cultured. Tob Cells Bioelectromagn 28:42–47CrossRefGoogle Scholar
  34. Shalaby S, Horwitz BA (2015) Plant phenolic compounds and oxidative stress: integrated signals in fungal–plant interactions. Curr Genet 61:347–357CrossRefGoogle Scholar
  35. Shang G-M, Wu J-C, Yuan Y-J (2004) Improved cell growth and Taxol production of suspension-cultured Taxus chinensis var. mairei in alternating direct current magnetic fields. Biotechnol Lett 26:875–878CrossRefGoogle Scholar
  36. Shokrollahi S, Ghanati F, Sajedi RH, Sharifi M (2018) Possible role of iron containing proteins in physiological responses of soybean to static magnetic field. J Plant Physiol 226:163–171CrossRefGoogle Scholar
  37. Simaei M, Khavari-Nejad R, Bernard F (2012) Exogenous application of salicylic acid and nitric oxide on the ionic contents and enzymatic activities in NaCl-stressed soybean plants American. J Plant Sci 3:1495CrossRefGoogle Scholar
  38. Tahsili J, Sharifi M, Safaie N, Esmaeilzadeh-Bahabadi S, Behmanesh M (2014) Induction of lignans and phenolic compounds in cell culture of Linum album by culture filtrate of Fusarium graminearum. J Plant Interact 9:412–417CrossRefGoogle Scholar
  39. Wang JW, Zheng LP, Wu JY, Tan RX (2006) Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and Taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide 15:351–358CrossRefGoogle Scholar
  40. Zhang B, Zheng LP, Yi Li W, Wen Wang J (2013) Stimulation of artemisinin production in Artemisia annua hairy roots by Ag-SiO2 core-shell nanoparticles. Curr Nanosci 9:363–370CrossRefGoogle Scholar
  41. Złotek U, Świeca M, Jakubczyk A (2014) Effect of abiotic elicitation on main health-promoting compounds, antioxidant activity and commercial quality of butter lettuce (Lactuca sativa L.). Food Chem 148:253–260CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Marzieh Taghizadeh
    • 1
  • Fatemeh Nasibi
    • 1
    • 2
    Email author
  • Khosrow Manouchehri Kalantari
    • 1
  • Faezeh Ghanati
    • 3
  1. 1.Department of Plant BiologyShahid Bahonar University of KermanKermanIran
  2. 2.Research and Technology Institute of Plant Production (RTIPP)Shahid Bahonar University of KermanKermanIran
  3. 3.Department of Plant Biology, Faculty of Biological ScienceTarbiat Modares UniversityTehranIran

Personalised recommendations