Skip to main content
SpringerLink
Log in

Chemogenic silver nanoparticles enhance lignans and neolignans in cell suspension cultures of Linum usitatissimum L.

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

Abstract

Cell suspension culture of Linum usitatissimum is a great source of the novel and multipurpose medicinal compounds lignans and neolignans. Conventional culturing practices usually result in low yield of plant secondary metabolites; therefore, we conceived a successful mechanism to elicit production of lignans and neolignans in cell suspension cultures, simply, by addition of chemogenic Ag-NPs into the culture medium. A three stage feeding strategy (day 10, 10 and 15, and 10 and 20, respectively, after inoculation) spanning the log growth phase (day 10–20), was implemented to elicit cell suspension cultures of Linum usitatissimum. Though enhancing effects of Ag-NPs were observed at each stage, feeding Ag-NPs at day 10 resulted in comparatively, highest production of lignans (secoisolariciresinol diglucoside, 252.75 mg/l; lariciresinol diglucoside, 70.70 mg/l), neolignans (dehydrodiconiferyl alcohol glucoside, 248.20 mg/l; guaiacylglycerol-β-coniferyl alcohol ether glucoside, 34.76 mg/l), total phenolic content (23.45 mg GAE/g DW), total flavonoid content (11.85 mg QUE/g DW) and biomass (dry weight: 14.5 g/l), respectively. Furthermore, a linear trend in accumulation of lignans and neolignans was observed throughout log phase as compared to control, wherein growth non-associated trend in biosynthesis of these metabolites was observed. Optimum production of both lignans and neolignans occurred on day 20 of culture; a ten fold increase in secoisolariciresinol diglucoside, 2.8 fold increase in lariciresinol diglucoside, five fold increase in dehydrodiconiferyl alcohol glucoside and 1.75 fold increase in guaiacylglycerol-β-coniferyl alcohol ether glucoside was observed in production levels compared to control treatments, respectively.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ahmad N, Fazal H, Abbasi BH, Anwar S, Basir A (2013) DPPH free radical scavenging activity and phenotypic difference in hepatoprotective plant (Silybum marianum L.). Toxicol Ind Health 29(5):460–467

    Article  Google Scholar 

  • Al-Huqail AA, Hatata MM, Al-Huqail AA, Ibrahim MM (2018) Preparation, characterization of silver phyto nanoparticles and their impact on growth potential of Lupinus termis L. seedlings. Saudi J Biol Sci 25(2):313–319

    Article  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  Google Scholar 

  • Corbin C, Fidel T, Leclerc EA, Barakzoy E, Sagot N, Falguiéres A, Renouard S, Blondeau J-P, Ferroud C, Doussot J (2015) Development and validation of an efficient ultrasound assisted extraction of phenolic compounds from flax (Linum usitatissimum L.) seeds. Ultrason Sonochem 26:176–185

    Article  CAS  Google Scholar 

  • Das P, Barua S, Sarkar S, Karak N, Bhattacharyya P, Raza N, Kim K-H, Bhattacharya SS (2018) Plant extract–mediated green silver nanoparticles: efficacy as soil conditioner and plant growth promoter. J hazard Mater 346:62–72

    Article  CAS  Google Scholar 

  • Farag MA, Al-Mahdy DA, Meyer A, Westphal H, Wessjohann LA (2017) Metabolomics reveals biotic and abiotic elicitor effects on the soft coral Sarcophyton ehrenbergi terpenoid content. Sci Rep 7(1):648

    Article  Google Scholar 

  • 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 

  • Gupta SD, Agarwal A, Pradhan S (2018) Phytostimulatory effect of silver nanoparticles (AgNPs) on rice seedling growth: an insight from antioxidative enzyme activities and gene expression patterns. Ecotoxicol Environ Saf 161:624–633

    Article  CAS  Google Scholar 

  • Heble M, Staba E (1980) Steroid metabolism in stationary phase cell suspensions of Dioscorea deltoidea. Planta Med 40(S 1):124–128

    Article  Google Scholar 

  • Karwasara VS, Jain R, Tomar P, Dixit V (2010) Elicitation as yield enhancement strategy for glycyrrhizin production by cell cultures of Abrus precatorius Linn. Vitro Cell Dev Biol Plant 46(4):354–362

    Article  CAS  Google Scholar 

  • Ketchum RE, Gibson DM, Croteau RB, Shuler ML (1999) The kinetics of taxoid accumulation in cell suspension cultures of Taxus following elicitation with methyl jasmonate. Biotechnol Bioeng 62(1):97–105

    Article  CAS  Google Scholar 

  • Lee SK, Mbwambo Z, Chung H, Luyengi L, Gamez E, Mehta R, Kinghorn A, Pezzuto J (1998) Evaluation of the antioxidant potential of natural products. Comb Chem High throughput Screen 1(1):35–46

    CAS  PubMed  Google Scholar 

  • Lee W-M, Kwak JI, An Y-J (2012) Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor: media effect on phytotoxicity. Chemosphere 86(5):491–499

    Article  CAS  Google Scholar 

  • Li X, Ke M, Zhang M, Peijnenburg W, Fan X, Xu J, Zhang Z, Lu T, Fu Z, Qian H (2018) The interactive effects of diclofop-methyl and silver nanoparticles on Arabidopsis thaliana: growth, photosynthesis and antioxidant system. Environ Pollut 232:212–219

    Article  CAS  Google Scholar 

  • Mahendran D, PB KK, Sreeramanan S, Venkatachalam P (2018) Enhanced biosynthesis of colchicine and thiocolchicoside contents in cell suspension cultures of Gloriosa superba L. exposed to ethylene inhibitor and elicitors. Ind Crops Prod 120:123–130

    Article  CAS  Google Scholar 

  • Moreno PR, Poulsen C, van der Heijden R, Verpoorte R (1996) Effects of elicitation on different metabolic pathways in Catharanthus roseus (L.) G. Don cell suspension cultures. Enzyme Microb Technol 18(2):99–107

    Article  CAS  Google Scholar 

  • Muir AD, Westcott ND (2003) Flax: the genus Linum. CRC Press, Boca Raton

    Book  Google Scholar 

  • Mulabagal V, Tsay H-S (2004) Plant cell cultures-an alternative and efficient source for the production of biologically important secondary metabolites. Int J Appl Sci Eng 2(1):29–48

    Google Scholar 

  • Murthy HN, Lee E-J, Paek K-Y (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tissue Organ Cult 118(1):1–16

    Article  CAS  Google Scholar 

  • Nadeem M, Abbasi BH, Garros L, Drouet S, Zahir A, Ahmad W, Giglioli-Guivarc’h N, Hano C (2018) Yeast-extract improved biosynthesis of lignans and neolignans in cell suspension cultures of Linum usitatissimum L. Plant Cell Tissue Organ Cult 135:347–355

    Article  Google Scholar 

  • Nair R (2016) Effects of nanoparticles on plant growth and development. In: Plant nanotechnology. Springer, Berlin, p 95–118

    Google Scholar 

  • Namdeo A (2007) Plant cell elicitation for production of secondary metabolites: a review. Pharmacogn Rev 1(1):69–79

    CAS  Google Scholar 

  • Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao A-J, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17(5):372–386

    Article  CAS  Google Scholar 

  • Osman NI, Sidik NJ, Awal A (2018) Efficient enhancement of gallic acid accumulation in cell suspension cultures of Barringtonia racemosa L. by elicitation. Plant Cell Tissue Organ Cult 135: 203–212

    Article  Google Scholar 

  • Phillips R, Henshaw G (1977) The regulation of synthesis of phenolics in stationary phase cell cultures of Acer pseudoplatanus L. J Exp Bot 28(4):785–794

    Article  CAS  Google Scholar 

  • Ramirez-Estrada K, Vidal-Limon H, Hidalgo D, Moyano E, Golenioswki M, Cusidó RM, Palazon J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21(2):182

    Article  Google Scholar 

  • Sharma P, Bhatt D, Zaidi M, Saradhi PP, Khanna P, Arora S (2012) Silver nanoparticle-mediated enhancement in growth and antioxidant status of Brassica juncea. Appl Biochem Biotechnol 167(8):2225–2233

    Article  CAS  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent Methods in enzymology. Elsevier, Amsterdam, 299, 152–178

    Google Scholar 

  • Thuesombat P, Hannongbua S, Akasit S, Chadchawan S (2014) Effect of silver nanoparticles on rice (Oryza sativa L. cv. KDML 105) seed germination and seedling growth. Ecotoxicol Environ Saf 104:302–309

    Article  CAS  Google Scholar 

  • Tripathi DK, Singh S, Singh S, Srivastava PK, Singh VP, Singh S, Prasad SM, Singh PK, Dubey NK, Pandey AC (2017) Nitric oxide alleviates silver nanoparticles (AgNps)-induced phytotoxicity in Pisum sativum seedlings. Plant Physiol Biochem 110:167–177

    Article  CAS  Google Scholar 

  • Ul-Haq I, Ullah N, Bibi G, Kanwal S, Ahmad MS, Mirza B (2012) Antioxidant and cytotoxic activities and phytochemical analysis of Euphorbia wallichii root extract and its fractions. Iran J Pharm Res 11(1):241

    PubMed  PubMed Central  Google Scholar 

  • Verma N, Shukla S (2015) Impact of various factors responsible for fluctuation in plant secondary metabolites. J Appl Res Med Aromat Plants 2(4):105–113

    Google Scholar 

  • Wallis A (1998) Structural diversity in lignans and neolignans. Lignin Lignan Biosynth

  • Yin L, Cheng Y, Espinasse B, Colman BP, Auffan M, Wiesner M, Rose J, Liu J, Bernhardt ES (2011) More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ Sci Technol 45(6):2360–2367

    Article  CAS  Google Scholar 

  • Zahir A, Abbasi BH, Adil M, Anjum S, Zia M (2014) Synergistic effects of drought stress and photoperiods on phenology and secondary metabolism of Silybum marianum. Appl Biochem Biotechnol 174(2):693–707

    Article  CAS  Google Scholar 

  • Zahir A, Ahmad W, Nadeem M, Giglioli-Guivarc’h N, Hano C, Abbasi BH (2018) In vitro cultures of Linum usitatissimum: synergistic effects of mineral nutrients and photoperiod regimes on growth and biosynthesis of lignans and neolignans. Photochem Photobiol B 187:141–150

    Article  CAS  Google Scholar 

  • Zaka M, Abbasi BH, Rahman L-u, Shah A, Zia M (2016) Synthesis and characterisation of metal nanoparticles and their effects on seed germination and seedling growth in commercially important Eruca sativa. IET Nanobiotechnol 10(3):134–140

    Article  Google Scholar 

  • Zhao J-L, Zhou L-G, Wu J-Y (2010a) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87(1):137–144

    Article  CAS  Google Scholar 

  • Zhao J-L, Zhou L-G, Wu J-Y (2010b) Promotion of Salvia miltiorrhiza hairy root growth and tanshinone production by polysaccharide–protein fractions of plant growth-promoting rhizobacterium Bacillus cereus. Process Biochem 45(9):1517–1522

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Dr. Bilal Haider Abbasi acknowledges research fellowship of Le Studium-Institute for Advanced Studies, Loire Valley, Orléans, France. This research was in part supported by Cosmetosciences, a global training and research program dedicated to the cosmetic industry. Located in the heart of the cosmetic valley, this program led by University of Orléans, France is funded by the Region Centre-Val de Loire. Adnan Zahir acknowledges the financial assistance of Higher Education Commission of Pakistan for his indigenous PhD scholarship.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Quaid-i-Azam University, Islamabad, 45320, Pakistan

    Adnan Zahir, Muhammad Nadeem, Waqar Ahmad & Bilal Haider Abbasi

  2. EA2106 Biomolecules et Biotechnologies Vegetales, Universite Francois-Rabelais de Tours, Tours, France

    Nathalie Giglioli-Guivarc’h & Bilal Haider Abbasi

  3. Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Plant Lignans Team, INRA USC1328, Université d’Orléans, 28000, Chartres, France

    Christophe Hano & Bilal Haider Abbasi

Authors
  1. Adnan Zahir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muhammad Nadeem
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Waqar Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nathalie Giglioli-Guivarc’h
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christophe Hano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bilal Haider Abbasi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AZ did the research work, data analyses and manuscript write-up. WA and MN assisted AZ with experiments. BHA conceived the idea, supervised the research work and reviewed the manuscript. NGG helped with experimental design and critically reviewed the manuscript. CH performed chemical synthesis of standards and HPLC analysis.

Corresponding author

Correspondence to Bilal Haider Abbasi.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Silvia Moreno.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zahir, A., Nadeem, M., Ahmad, W. et al. Chemogenic silver nanoparticles enhance lignans and neolignans in cell suspension cultures of Linum usitatissimum L.. Plant Cell Tiss Organ Cult 136, 589–596 (2019). https://doi.org/10.1007/s11240-018-01539-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-018-01539-6

Keywords

Search

Navigation