Biosynthesis of NanoSilver and Its Effect on Key Genes of Flavonoids and Physicochemical Properties of Viola tricolor L.

Abstract

Wild pansy (Viola tricolor L.) is of the Violaceae plant family. Some of the medicinal properties of this plant are related to the ability to produce and biosynthesized a group of flavonoids. Silver nanoparticles are one of the most important and attractive nanomaterials among several metal nanoparticles.In the present study, plant-mediated nanosilver was produced from aqueous extract of Pansy flower as a good covering and stabilizing agent using the green synthesis method. Dynamic light scattering (DLS), transmission electron microscopy (TEM), and zeta potential methods were used to determine the specifications of synthesized nanoparticles. In this study, the effect of different concentrations of bio nanosilver 0, 10, 50, and 100 mg/l on phytochemical and physiological properties, and the expression of some key genes involved in flavonoids biosynthesis including phenylalanine ammonia-lyase (PAL), chalcone synthase (CHS), flavonoid 3′, 5′-hydroxylase (F3′5′H), and flavonoid 3-hydroxylase (F3′H) were determined in V. tricolor plant. The results showed nanosilver treatments cause the accumulation of manganese, zinc, and silver elements and increasing the content of phenolic, flavonoid, anthocyanin and antioxidant activity. Using AgNPs also causes the increase in activity of antioxidant enzymes such as superoxide dismutase (SOD), ascorbate peroxidase (APX), phenylalanine ammonia-lyase (PAL), and peroxidase (POD). Besides, treatment with a concentration of 10 mg/l of silver nanoparticles significantly causes an increase in flavonoids compounds such as rutin, apigenin, and quercetin. Our results suggest that bio nanosilver could increase secondary metabolites content in the V. tricolor plant.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Notes

  1. 1.

    SEM.

  2. 2.

    TEM.

  3. 3.

    Zeta potential.

  4. 4.

    DLS.

References

  1. Adefegha SA, Oyeleye SI, Dada FA et al (2018) Modulatory effect of quercetin and its glycosylated form on key enzymes and antioxidant status in rats penile tissue of paroxetine-induced erectile dysfunction. Biomed Pharmacother 107:1473–1479. https://doi.org/10.1016/j.biopha.2018.08.128

    Article  Google Scholar 

  2. Agarwal H, Venkat Kumar S, Rajeshkumar S (2018) Antidiabetic effect of silver nanoparticles synthesized using lemongrass (Cymbopogon citratus) through conventional heating and microwave irradiation approach. J MicrobiolBiotechnol Food Sci 7:371–376. https://doi.org/10.15414/jmbfs.2018.7.4.371-376

    Article  Google Scholar 

  3. Ali SW, Rajendran S, Joshi M (2011) Synthesis and characterization of chitosan and silver loaded chitosan nanoparticles for bioactive polyester. CarbohydrPolym 83:438–446. https://doi.org/10.1016/j.carbpol.2010.08.004

    Article  Google Scholar 

  4. Babu TS, Akhtar TA, Lampi MA et al (2003) Similar stress responses are elicited by copper and ultraviolet radiation in the aquatic plant Lemna gibba: implication of reactive oxygen species as common signals. Plant Cell Physiol 44:1320–1329. https://doi.org/10.1093/pcp/pcg160

    Article  Google Scholar 

  5. Bailly C, Benamar A, Corbineau F, Côme D (1996) Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol Plant 97:104–110. https://doi.org/10.1111/j.1399-3054.1996.tb00485.x

    Article  Google Scholar 

  6. Bais HP, Sudha GS, Ravishankar GA (2000) Putrescine and silver nitrate influences shoot multiplication, in vitro flowering and endogenous titers of polyamines in Cichorium intybus L. cv. Lucknow local. J Plant Growth Reg 19:238–248. https://doi.org/10.1007/s003440000012

    Article  Google Scholar 

  7. Baskar V, Venkatesh J, Park SW (2015) Impact of biologically synthesized silver nanoparticles on the growth and physiological responses in Brassica rapa ssp. pekinensis. Environ SciPollut Res 22:17672–17682. https://doi.org/10.1007/s11356-015-4864-1

    Article  Google Scholar 

  8. Bhakya S, Muthukrishnan S, Sukumaran M, Muthukumar M (2016) Biogenic synthesis of silver nanoparticles and their antioxidant and antibacterial activity. ApplNanosci 6:755–766. https://doi.org/10.1007/s13204-015-0473-z

    Article  Google Scholar 

  9. Binder BM (2020) Ethylene signaling in plants. J BiolChem 295:7710–7725

    Google Scholar 

  10. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Ann Rev Plant Biol 54:519–546. https://doi.org/10.1146/annurev.arplant.54.031902.134938

    Article  Google Scholar 

  11. Casillas-figueroa F, Arellano-garcía ME, Leyva-aguilera C et al (2020) ArgovitTM silver nanoparticles effects on allium cepa: plant growth promotion without cytogenotoxic damage. Nanomaterials 10:1–20. https://doi.org/10.3390/nano10071386

    Article  Google Scholar 

  12. Chand K, Cao D, Fouad DE et al (2020) Green synthesis, characterization and photocatalytic application of silver nanoparticles synthesized by various plant extracts. Arab J Chem. https://doi.org/10.1016/j.arabjc.2020.01.009

    Article  Google Scholar 

  13. Ebrahimzadeh MA, Nabavi SM, Nabavi SF et al (2010) Antioxidant and free radical scavenging activity of H. officinalis L. var. angustifolius, V. odorata, B. hyrcana and C. speciosum. Pak J Pharm Sci 23:29–34. https://doi.org/10.1080/14786419.2012.658799

    Article  Google Scholar 

  14. Gan Q, Wang T, Cochrane C, McCarron P (2005) Modulation of surface charge, particle size and morphological properties of chitosan–TPP nanoparticles intended for gene delivery. Coll Surf B Biointerf 44:65–73. https://doi.org/10.1016/j.colsurfb.2005.06.001

    Article  Google Scholar 

  15. Garcia-Brugger A, Lamotte O, Vandelle E et al (2006) Early signaling events induced by elicitors of plant defenses. Molecul Plant Microbe Interact 19:711–724. https://doi.org/10.1094/MPMI-19-0711

    Article  Google Scholar 

  16. Ghorbani A, Razavi SM, Omran VOG, Pirdashti H (2018) Piriformosporaindica alleviates salinity by boosting redox poise and antioxidative potential of tomato. Russ J Plant Physiol 65:898–907. https://doi.org/10.1134/S1021443718060079

    Article  Google Scholar 

  17. Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309

    Article  Google Scholar 

  18. Gokce Y, Cengiz B, Yildiz N et al (2014) Ultrasonication of chitosan nanoparticle suspension: influence on particle size. Coll Surf APhysicochemEng Aspects 462:75–81. https://doi.org/10.1016/j.colsurfa.2014.08.028

    Article  Google Scholar 

  19. Guardia T, Rotelli AE, Juarez AO, Pelzer LE (2001) Anti-inflammatory properties of plant flavonoids. Effects of rutin, quercetin and hesperidin on adjuvant arthritis in rat. Il Farmaco 56:683–687. https://doi.org/10.1016/S0014-827X(01)01111-9

    Article  Google Scholar 

  20. Hong J, Rico CM, Zhao L et al (2015) Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa). Environ Sci Process Impacts 17:177–185. https://doi.org/10.1039/c4em00551a

    Article  Google Scholar 

  21. Janbaz KH, Saeed SA, Gilani AH (2002) Protective effect of rutin on paracetamol-and CCl4-induced hepatotoxicity in rodents. Fitoterapia 73:557–563. https://doi.org/10.1016/S0367-326X(02)00217-4

    Article  Google Scholar 

  22. Jiang H-S, Qiu X-N, Li G-B et al (2014) Silver nanoparticles induced accumulation of reactive oxygen species and alteration of antioxidant systems in the aquatic plant Spirodela polyrhiza. Environ ToxicolChem 33:1398–1405. https://doi.org/10.1002/etc.2577

    Article  Google Scholar 

  23. Jurca T, Pallag A, Marian E, Eugenia M (2019) The histo-anatomical investigation and the polyphenolic profile of antioxidant complex active ingredients from three viola species. Farmacia 67:634–640. https://doi.org/10.31925/farmacia.2019.4.12

    Article  Google Scholar 

  24. Kamalakkannan N, Prince PSM (2006) Antihyperglycaemic and antioxidant effect of rutin, a polyphenolic flavonoid, in streptozotocin-induced diabetic wistar rats. Basic ClinPharmacolToxicol 98:97–103. https://doi.org/10.1111/j.1742-7843.2006.pto_241.x

    Article  Google Scholar 

  25. Keshari AK, Srivastava R, Singh P et al (2020) Antioxidant and antibacterial activity of silver nanoparticles synthesized by Cestrum nocturnum. J Ayurveda Integr Med 11:37–44. https://doi.org/10.1016/j.jaim.2017.11.003

    Article  Google Scholar 

  26. Kim J-E, Joo S-I, Seo J-H, Lee S-P (2009) Antioxidant and α-glucosidase inhibitory effect of tartary buckwheat extract obtained by the treatment of different solvents and enzymes. J Korean Soc Food SciNutr 38:989–995. https://doi.org/10.3746/jkfn.2009.38.8.989

    Article  Google Scholar 

  27. Koda T, Kuroda Y, Imai H (2008) Protective effect of rutin against spatial memory impairment induced by trimethyltin in rats. Nutr Res 28:629–634. https://doi.org/10.1016/j.nutres.2008.06.004

    Article  Google Scholar 

  28. Kosyk OI, Khomenko IM, Batsmanova LM, Taran NY (2017) Phenylalanine ammonia-lyase activity and anthocyanin content in different varieties of lettuce under the cadmium influence. UkrBiochem J. https://doi.org/10.17721/1728_2748.2018.75.37-45

    Article  Google Scholar 

  29. Krizek DT, Britz SJ, Mirecki RM (1998) Inhibitory effects of ambient levels of solar UV-A and UV-B radiation on growth of cv. New Red Fire lettuce Physiol Plant 103:1–7. https://doi.org/10.1034/j.1399-3054.1998.1030101.x

    Article  Google Scholar 

  30. La Casa C, Villegas I, De La Lastra CA et al (2000) Evidence for protective and antioxidant properties of rutin, a natural flavone, against ethanol induced gastric lesions. J Ethnopharmacol 71:45–53. https://doi.org/10.1016/S0378-8741(99)00174-9

    Article  Google Scholar 

  31. Matsui K, Walker AR (2020) Biosynthesis and regulation of flavonoids in buckwheat. Breed Sci 70:74–84. https://doi.org/10.1270/jsbbs.19041

    Article  Google Scholar 

  32. Mattioli R, Francioso A, Mosca L, Silva P (2020) Anthocyanins: a comprehensive review of their chemical properties and health effects on cardiovascular and neurodegenerative diseases. Molecules 25:3809. https://doi.org/10.3390/molecules25173809

    Article  Google Scholar 

  33. Mehrian SK, Heidari R, Rahmani F (2015) Effect of silver nanoparticles on free amino acids content and antioxidant defense system of tomato plants. Indian J Plant Physiol 20:257–263. https://doi.org/10.1007/s40502-015-0171-6

    Article  Google Scholar 

  34. Munné-Bosch S, Peñuelas J, Asensio D, Llusià J (2004) Airborne ethylene may alter antioxidant protection and reduce tolerance of holm oak to heat and drought stress. Plant Physiol 136:2937–2947. https://doi.org/10.1104/pp.104.050005

    Article  Google Scholar 

  35. Nabavi SM, Šamec D, Tomczyk M et al (2020) Flavonoid biosynthetic pathways in plants: versatile targets for metabolic engineering. BiotechnolAdv 38:107316. https://doi.org/10.1016/j.biotechadv.2018.11.005

    Article  Google Scholar 

  36. Nair PMG, Chung IM (2014) Physiological and molecular level effects of silver nanoparticles exposure in rice (Oryza sativa L.) seedlings. Chemosphere 112:105–113. https://doi.org/10.1016/j.chemosphere.2014.03.056

    Article  Google Scholar 

  37. Nijveldt RJ, Van Nood ELS, Van Hoorn DEC et al (2001) Flavonoids: a review of probable mechanisms of action and potential applications. Am J ClinNutr 74:418–425. https://doi.org/10.1093/ajcn/74.4.418

    Article  Google Scholar 

  38. Papadimitriou S, Bikiaris D, Avgoustakis K et al (2008) Chitosan nanoparticles loaded with dorzolamide and pramipexole. CarbohydrPolym 73:44–54. https://doi.org/10.1016/j.carbpol.2007.11.007

    Article  Google Scholar 

  39. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:e45–e45. https://doi.org/10.1093/nar/29.9.e45

    Article  Google Scholar 

  40. Raei M, Angaji SA, Omidi M, et al (2014) Effect of abiotic elicitors on tissue culture of Aloe vera. Int J Biosci 5:74–81. https://doi.org/10.12692/ijb/5.1.74-81.

  41. Rice-Evans C, Miller N, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159. https://doi.org/10.1016/S1360-1385(97)01018-2

    Article  Google Scholar 

  42. Saunders JA, McClure JW (1974) The suitability of a quantitative spectrophotometric assay for phenylalanine ammonia-lyase activity in barley, buckwheat, and pea seedlings. Plant Physiol 54:412–413. https://doi.org/10.1104/pp.54.3.412

    Article  Google Scholar 

  43. Servin AD, Morales MI, Castillo-Michel H et al (2013) Synchrotron verification of TiO2 accumulation in cucumber fruit: a possible pathway of TiO2 nanoparticle transfer from soil into the food chain. Environ SciTechnol 47:11592–11598. https://doi.org/10.1021/es403368j

    Article  Google Scholar 

  44. Shahzad A, Saeed H, Iqtedar M et al (2019) Size-controlled production of silver nanoparticles by aspergillusfumigatus BTCB10: likely antibacterial and cytotoxic effects. J Nanomater. https://doi.org/10.1155/2019/5168698

    Article  Google Scholar 

  45. Sharma P, Bhatt D, Zaidi MGH et al (2012) Silver nanoparticle-mediated enhancement in growth and antioxidant status of brassica juncea. ApplBiochemBiotechnol 167:2225–2233. https://doi.org/10.1007/s12010-012-9759-8

    Article  Google Scholar 

  46. Smirnoff N (1996) Botanical briefing: the function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669. https://doi.org/10.1006/anbo.1996.0175

    Article  Google Scholar 

  47. Sohal JK, Saraf A, Shukla K, Shrivastava M (2019) Determination of antioxidant potential of biochemically synthesized silver nanoparticles using Aloe vera gel extract. Plant Sci Today 6:208–217. https://doi.org/10.14719/pst.2019.6.2.532

    Article  Google Scholar 

  48. Song JY, Kim BS (2009) Rapid biological synthesis of silver nanoparticles using plant leaf extracts. Bioprocess BiosystEng 32:79. https://doi.org/10.1007/s00449-008-0224-6

    Article  Google Scholar 

  49. Song JY, Jang H-K, Kim BS (2009) Biological synthesis of gold nanoparticles using Magnolia kobus and Diopyros kaki leaf extracts. Process Biochem 44:1133–1138. https://doi.org/10.1016/j.procbio.2009.06.005

    Article  Google Scholar 

  50. Tang L, Kwon S-Y, Kim S-H et al (2006) Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep 25:1380–1386. https://doi.org/10.1007/s00299-006-0199-1

    Article  Google Scholar 

  51. Trujillo-Reyes J, Majumdar S, Botez CE et al (2014) Exposure studies of core: shell Fe/Fe3O4 and Cu/CuO NPs to lettuce (Lactuca sativa) plants: are they a potential physiological and nutritional hazard? J Hazard Mater 267:255–263. https://doi.org/10.1016/j.jhazmat.2013.11.067

    Article  Google Scholar 

  52. Umashankari J, Inbakandan D, Ajithkumar TT, Balasubramanian T (2012) Mangrove plant, Rhizophoramucronata (Lamk, 1804) mediated one pot green synthesis of silver nanoparticles and its antibacterial activity against aquatic pathogens. AquatBiosyst 8:1–7. https://doi.org/10.1186/2046-9063-8-11

    Article  Google Scholar 

  53. Velioglu YS, Mazza G, Gao L, Oomah BD (1998) Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. J Agric Food Chem 46:4113–4117. https://doi.org/10.1021/jf9801973

    Article  Google Scholar 

  54. Vukics V, Kery A, Bonn GK, Guttman A (2008) Major flavonoid components of heartsease (Viola tricolor L.) and their antioxidant activities. Anal BioanalChem 390:1917–1925. https://doi.org/10.1007/s00216-008-1885-3

    Article  Google Scholar 

  55. Wagner GJ (1979) Content and vacuole/extravacuole distribution of neutral sugars, free amino acids, and anthocyanin in protoplasts. Plant Physiol 64:88–93. https://doi.org/10.1104/pp.64.1.88

    Article  Google Scholar 

  56. Yi TG, Yeoung YR, Choi I-Y, Park N-I (2019) Transcriptome analysis of Asparagus officinalis reveals genes involved in the biosynthesis of rutin and protodioscin. PLoS ONE 14:e0219973. https://doi.org/10.1371/journal.pone.0219973

    Article  Google Scholar 

  57. Zaeem A, Drouet S, Anjum S, et al (2020) Effects of biogenic zinc oxide nanoparticles on growth and oxidative stress response in flax seedlings vs. in vitro cultures: a comparative analysis. Biomolecules 10:918. doi:https://doi.org/10.3390/biom10060918.

  58. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. BiotechnolAdv 23:283–333. https://doi.org/10.1016/j.biotechadv.2005.01.003

    Article  Google Scholar 

  59. 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. https://doi.org/10.3389/fpls.2016.00090

    Article  Google Scholar 

Download references

Acknowledgments

The author thanks the Razi Herbal Medicine Research Center of the Lorestan University of Medical Science for their contribution to implementing the project.

Funding

There are no known competing financial interests or personal relationships that could have appeared to influence the work reported in this article.

Author information

Affiliations

Authors

Contributions

AH was involved in data curation, writing—original draft, conceptualization, methodology, resources, formal analysis. SS contributed to review and editing, supervision, project administration. HLY was involed in validation, supervision, project administration. AI contributed to software, supervision, project administration.

Corresponding author

Correspondence to Sara Saadatmand.

Ethics declarations

Conflict of interest

The authors report no declarations of interest.

Ethical Statement

I testify on behalf of all co-authors that our article submitted to Iranian Journal of Science and Technology, Transactions A: Science:

Data availability statement

The data that support the findings of this study are available from the corresponding author, [S.saadatmand], upon reasonable request.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hassanvand, A., Saadatmand, S., Lari Yazdi, H. et al. Biosynthesis of NanoSilver and Its Effect on Key Genes of Flavonoids and Physicochemical Properties of Viola tricolor L.. Iran J Sci Technol Trans Sci 45, 805–819 (2021). https://doi.org/10.1007/s40995-021-01091-7

Download citation

Keywords

  • Anthocyanin
  • Antioxidant enzymes
  • Phytochemical properties
  • Phenolic
  • Rutin