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Influence of silver nanoparticles on the enhancement and transcriptional changes of glucosinolates and phenolic compounds in genetically transformed root cultures of Brassica rapa ssp. rapa

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Abstract

Glucosinolates (GSLs) and phenolic compounds (PCs) are biologically active and involved in the defense reaction of plants; these compounds have a beneficial effect on human health. In this study, we described the influence of biologically synthesized silver nanoparticles (Ag NPs) to enhance the phytochemicals (GSLs and PCs), their transcription levels, and their biological activities in genetically transformed root cultures (hairy root cultures) of Brassica rapa. The concentrations of silver and reactive oxygen species (malondialdehyde and hydrogen peroxide) were highly elevated in the Ag NP-elicited hairy roots (HRs). Glucosinolates (glucoallysin, glucobrassicanapin, sinigrin, progoitrin, gluconapin, 4-methoxyglucobrassicin, 4-hydroxyglucobrassicin, glucobrassicin, neoglucobrassicin, and gluconasturtiin) and their transcripts (MYB34, MYB51, MYB28, and MYB29) were significantly enhanced in the Ag NP-elicited HRs. Moreover, the phenolic compounds (flavonols, hydroxybenzoic, and hydroxycinnamic acids) were significantly enriched in the Ag NP-elicited HRs. Total phenolic and flavonoid concentrations and their transcripts (PAL, CHI, and FLS) were higher in the Ag NP-elicited HRs than in the non-elicited HRs. Additionally, biological (antioxidant, antimicrobial, and anticancer) activities were significantly higher in the Ag NP-elicited HRs than in the non-elicited HRs. The Ag NP-elicited HR cultures offered an efficient and promising in vitro method to increase the production of health-promoting bioactive compounds, which may be useful in nutraceutical and pharmaceutical industries.

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Abbreviations

Ag NPs:

Silver nanoparticles

DPPH:

1,1-Diphenyl-2-picrylhydrazyl

GSLs:

Glucosinolates

HRCs:

Hairy root cultures

HRs:

Hairy roots

IPCs:

Individual phenolic compounds

ICP-MS:

Inductively coupled plasma-mass spectrometry

MDA:

Malondialdehyde

H2O2 :

Hydrogen peroxide

MTT:

Thiazolyl blue tetrazolium bromide

PCs:

Phenolic compounds

ROS:

Reactive oxygen species

RT-PCR:

Real-time polymerase chain reaction

TFC:

Total flavonoid content

TPC:

Total phenolic content

UHPLC–TQMS:

Ultra-high-pressure liquid chromatography–triple quadrupole mass spectrometry

UHPLC:

Ultra-high-performance liquid chromatography

References

  1. Chung IM, Rekha K, Rajakumar G, Thiruvengadam M (2016) Production of glucosinolates, phenolic compounds and associated gene expression profiles of hairy root cultures in turnip (Brassica rapa ssp. rapa). 3 Biotech 6:175

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hassini I, Baenas N, Moreno DA, Carvajal M, Boughanmi N, Martinez Ballesta MDC (2017) Effects of seed priming, salinity and methyl jasmonate treatment on bioactive composition of Brassica oleracea var. capitata (white and red varieties) sprouts. J Sci Food Agric 97(8):2291–2299

    Article  CAS  Google Scholar 

  3. Ru M, An Y, Wang K, Peng L, Li B, Bai Z, Wang B, Liang Z (2016) Prunella vulgaris L. hairy roots: culture, growth, and elicitation by ethephon and salicylic acid. Eng Life Sci 16:494–502

    Article  CAS  Google Scholar 

  4. Zhang CH, Yan Q, Cheuk WK, Wu JY (2004) Enhancement of tanshinone production in Salvia miltiorrhiza hairy root culture by Ag+ elicitation and nutrient feeding. Planta Med 70:147–151

    Article  CAS  PubMed  Google Scholar 

  5. Thiruvengadam M, Gurunathan S, Chung IM (2015) Physiological, metabolic, and transcriptional effects of biologically-synthesized silver nanoparticles in turnip (Brassica rapa ssp. rapa L.). Protoplasma 252(4):1031–1046

    Article  CAS  Google Scholar 

  6. Zhang B, Zheng LP, Li YW, Wang JW (2013) Stimulation of artemisinin production in Artemisia annua hairy roots by Ag-SiO2 core-shell nanoparticles. Curr Nanosci 9:363–370

    Article  CAS  Google Scholar 

  7. Shakeran Z, Keyhanfar M, Asghari G, Ghanadian M (2015) Improvement of atropine production by different biotic and abiotic elicitors in hairy root cultures of Datura metel. Turk J Biol 39:111–118

    Article  CAS  Google Scholar 

  8. Ghasemi B, Hosseini R, Nayeri FD (2015) Effects of cobalt nanoparticles on artemisinin production and gene expression in Artemisia annua. Turk J Bot 39:769–777

    Article  CAS  Google Scholar 

  9. Jamshidi M, Ghanati F, Rezaei A, Bemani E (2016) Change of antioxidant enzymes activity of hazel (Corylus avellana L.) cells by AgNPs. Cytotechnology 68(3):525–530

    Article  CAS  Google Scholar 

  10. Moharrami F, Hosseini BB, Sharafi A, Farjaminezhad M (2017) Enhanced production of hyoscyamine and scopolamine from genetically transformed root culture of Hyoscyamus reticulatus L. elicited by iron oxide nanoparticles. In Vitro Cell Develop Biol Plant 53(2):104–111

    Article  CAS  Google Scholar 

  11. Lin D, Xing B (2008) Root uptake and phytotoxicity of Zn nanoparticles. IJEST 42:5580–5582

    CAS  Google Scholar 

  12. Sharafi E, Khayam Nekoei SM, 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.). J Medicinal Plants By-Products 2:177–184

    Google Scholar 

  13. Murashige T, Skoog FA (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  14. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  15. Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in regulation of senescence in pear. Plant Physiol 59:411–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Singelton VR, Orthifer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Methods Enzymol 299:152–178

    Article  Google Scholar 

  17. Willet WC (2002) Balancing life-style and genomics research for disease prevention. Science 296:695–698

    Article  Google Scholar 

  18. Thiruvengadam M, Chung IM (2015) Selenium, putrescine, and cadmium influence health-promoting phytochemicals and molecular-level effects on turnip (Brassica rapa ssp. rapa). Food Chem 173:185–193

    Article  CAS  Google Scholar 

  19. Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT—Food Sci Technol 28(1):25–30

    Article  CAS  Google Scholar 

  20. Oyaizu M (1986) Studies on products of browning reactions: antioxidative activities of browning reaction prepared from glucosamine. Jpn J Nutr 44:307–315

    Article  CAS  Google Scholar 

  21. Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269:337–341

    Article  CAS  Google Scholar 

  22. Gabr AMM, Mabrok HB, Ghanem KZ, Blaut M, Smetanska I (2016) Lignan accumulation in callus and Agrobacterium rhizogenes mediated hairy root cultures of flax (Linum usitatissimum). Plant Cell Tissue Organ Cult 126:255–267

    Article  CAS  Google Scholar 

  23. Kalimuthu K, Babu RS, Venkataraman D, Bilal M, Gurunathan S (2008) Biosynthesis of silver nanocrystals by Bacillus licheniformis. Colloids Surf B: Biointerfaces 65:150–153

    Article  CAS  PubMed  Google Scholar 

  24. Fayez KA, El-Deeb BA, Mostafa NY (2017) Toxicity of biosynthetic silver nanoparticles on the growth, cell ultrastructure and physiological activities of barley plant. Acta Physiol Plant 39:155

    Article  Google Scholar 

  25. Xu QS, Hu JZ, Xie KB, Yang HY, Du KH, Shi GX (2010) Accumulation and acute toxicity of silver in Potamogeton crispus L. J Hazard Mater 173:186–193

    Article  CAS  PubMed  Google Scholar 

  26. Dietz KJ, Baier M, Kramer U (1999) Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants: from molecules to ecosystems. Springer, Berlin, pp 73–97

    Chapter  Google Scholar 

  27. Nair PMG, Chung IM (2014) Physiological and molecular level effects of silver nanoparticles exposure in rice (Oryza sativa L.) seedlings. Chemosphere 112:105–113

    Article  CAS  PubMed  Google Scholar 

  28. Nair PMG, Chung IM (2015) Physiological and molecular level studies on the toxicity of silver nanoparticles in germinating seedlings of mung bean (Vigna radiata L.). Acta Physiol Plant 37(1):1–11

    Article  CAS  Google Scholar 

  29. Fazal H, Abbasi BH, Ahmad N, Ali M (2016) Elicitation of medicinally important antioxidant secondary metabolites with silver and gold nanoparticles in callus cultures of Prunella vulgaris L. Appl Biochem Biotechnol 180(6):1076–1092

    Article  CAS  Google Scholar 

  30. Spinoso-Castillo JL, Chavez-Santoscoy RA, Bogdanchikova N, Pérez-Sato JA, Morales-Ramos V, Bello-Bello JJ (2017) Antimicrobial and hormetic effects of silver nanoparticles on in vitro regeneration of vanilla (Vanilla planifolia Jacks. ex Andrews) using a temporary immersion system. Plant Cell Tiss Org Cult 129(2):195–207

    Article  CAS  Google Scholar 

  31. Ghanati F, Bakhtiarian S (2013) Changes of natural compounds of Artemisia annua L. by methyl jasmonate and silver nanoparticles. Adv Env Biol 7(9):2251–2258

    Google Scholar 

  32. Xing B, Yang D, Guo W, Liang Z, Yan X, Zhu Y, Liu Y (2015) Ag+ as a more effective elicitor for production of tanshinones than phenolic acids in Salvia miltiorrhiza hairy roots. Molecules 20:309–324

    Article  Google Scholar 

  33. Tuan PA, Kim YS, Kim Y, Thwe AA, Li X, Park CH, Lee SY, Park SU (2016) Molecular characterization of flavonoid biosynthetic genes and accumulation of baicalin, baicalein, and wogonin in plant and hairy root of Scutellaria lateriflora. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2016.08.011

    Article  Google Scholar 

  34. Krishnaraj C, Jagan G, Ramachandran R, Abirami SM, Mohan N, Kalaichelvan PT (2012) Effect of biologically synthesized silver nanoparticles on Bacopa monnieri L. Wettst. plant growth metabolism. Process Biochem 47(4):651–658

    Article  CAS  Google Scholar 

  35. Ghanati F, Bakhtiarian S, Parast BM, Behrooz MK (2014) Production of new active phytocompounds by Achillea millefolium L. after elicitation with silver nanoparticles and methyl jasmonate. Biosci Biotechnol Res Asia 11(2):391–399

    Article  Google Scholar 

  36. Zakaria ZA, Rofiee MS, Mohamed AM, Teh LK, Salleh MZ (2011) In vitro antiproliferative and antioxidant activities and total phenolic contents of the extracts of Melastoma malabathricum leaves. J Acupunct Meridian Stud 4:248e256

    Article  Google Scholar 

Download references

Acknowledgements

This paper was supported by the KU Research Professor Program of Konkuk University, Seoul, South Korea.

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Correspondence to Muthu Thiruvengadam.

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Chung, IM., Rekha, K., Rajakumar, G. et al. Influence of silver nanoparticles on the enhancement and transcriptional changes of glucosinolates and phenolic compounds in genetically transformed root cultures of Brassica rapa ssp. rapa. Bioprocess Biosyst Eng 41, 1665–1677 (2018). https://doi.org/10.1007/s00449-018-1991-3

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  • DOI: https://doi.org/10.1007/s00449-018-1991-3

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