Skip to main content

Assessment of silver nanoparticle-induced physiological and molecular changes in Arabidopsis thaliana

Environmental Science and Pollution Research volume 21, pages 8858–8869 (2014)Cite this article

Abstract

In this study, the effect of silver nanoparticles and silver ions on Arabidopsis thaliana was investigated at physiological and molecular levels. The seedlings were grown in sublethal concentrations of silver nanoparticles and silver ions (0.2, 0.5, and 1 mg/L) in 1/4 Hoagland’s medium for 14 days under submerged hydroponic conditions. Significantly higher reduction in the total chlorophyll and increase in anthocyanin content were observed after exposure to 0.5 and 1 mg/L silver nanoparticles as compared to similar concentrations of silver ions. Lipid peroxidation increased significantly after exposure to 0.2, 0.5, and 1 mg/L of silver nanoparticles and 0.5 and 1 mg/L of silver ions. Qualitative analysis with dichloro-dihydro-fluorescein diacetate and rhodamine 123 fluorescence showed a dose-dependent increase in reactive oxygen species production and changes in mitochondrial membrane potential in the roots of seedlings exposed to different concentrations of silver nanoparticles. Real-time PCR analysis showed significant upregulation in the expression of sulfur assimilation, glutathione biosynthesis, glutathione S-transferase, and glutathione reductase genes upon exposure to silver nanoparticles as compared with silver ions. Overall, based on the physiological and molecular level responses, it was observed that exposure to silver nanoparticles exerted more toxic response than silver ions in A. thaliana.

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

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

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

References

  • Almofti MR, Ichikawa T, Yamashita K, Terada H, Shinohara Y (2003) Silver ion induces a cyclosporine a-sensitive permeability transition in rat liver mitochondria and release of apoptogenic cytochrome c. J Biochem 134:43–49

    CAS  Article  Google Scholar 

  • Baek YW, An YJ (2011) Microbial toxicity of metal oxide nanoparticles (CuO, NiO, ZnO, and Sb2O3) to Escherichia coli, Bacillus subtilis, and Streptococcus aureus. Sci Total Environ 409:1603–1608

    CAS  Article  Google Scholar 

  • Benn TM, Westerhoff P (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–4139

    CAS  Article  Google Scholar 

  • Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510

    CAS  Article  Google Scholar 

  • Brar SK, Verma M, Tyagi RD, Surampalli RY (2010) Engineered nanoparticles in wastewater and wastewater sludge—evidence and impacts. Waste Manag 30:504–520

    CAS  Article  Google Scholar 

  • Carocho M, Ferreira IC (2013) A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food Chem Toxicol 51:15–25

    CAS  Article  Google Scholar 

  • Chalapathi Rao ASV, Reddy AR (2008) In: Khan NA, Singh S, Umar S (eds) Glutathione reductase: a putative redox regulatory system in plant cells. In sulfur assimilation and abiotic stresses in plants. Springer, The Netherlands, pp 111–147

    Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    CAS  Article  Google Scholar 

  • Colman BP, Arnaout CL, Anciaux S, Gunsch CK, Hochella MF Jr, Kim B, Lowry GV, McGill BM, Reinsch BC, Richardson CJ, Unrine JM, Wright JP, Yin L, Bernhardt ES (2013) Low concentrations of silver nanoparticles in biosolids cause adverse ecosystem responses under realistic field scenario. PLoS ONE 8:e57189

    CAS  Article  Google Scholar 

  • Colvin VL (2003) The potential environmental impact of engineered nanomaterials. Nat Biotechnol 21:1166–1170

    CAS  Article  Google Scholar 

  • Costa CS, Vieira Ronconi JV, Daufenbach JF, Goncalves CL, Rezin GT, Streck EL, da Silva Paula MM (2010) In vitro effects of silver nanoparticles on the mitochondrial respiratory chain. Mol Cell Biochem 342:51–56

    CAS  Article  Google Scholar 

  • David D, Abdullah O (2012) Silver nanoparticles toxicity effect on photosystem II photochemistry of the green alga Chlamydomonas reinhardtii treated in light and dark conditions. Toxicol Environ Chem 94:1536–1546

    Article  Google Scholar 

  • Derjaguin BV, Landau LD (1941) Theory of the stability of strongly charged lyophobic sols and of the adhesion of strongly charged particles in solutions of electrolytes. Acta Phys Chim URSS 14:633–662

    Google Scholar 

  • Dimkpa CO, McLean JE, Martineau N, Britt DW, Haverkamp R, Anderson AJ (2013) Silver nanoparticles disrupt Wheat (Triticum aestivum L.) growth in a sand matrix. Environ Sci Technol 47:1082–1090

    CAS  Article  Google Scholar 

  • Dominguez-Solis JR, Gutierrez-Alcala G, Romero LC, Gotor C (2001) The cytosolic O-acetylserine (thiol) lyase gene is regulated by heavy-metals and can function in cadmium tolerance. J Biol Chem 276:9297–9302

    CAS  Article  Google Scholar 

  • Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009) Silver nanoparticle impact on bacterial growth: effect of pH, concentration and organic matter. Environ Sci Technol 43:7285–7290

    CAS  Article  Google Scholar 

  • Farkas J, Peter H, Christian P, Urrea JAG, Hassellöv M, Tuoriniemi J, Gustafsson S, Olsson E, Hylland K, Thomas KV (2011) Characterization of the effluent from a nanosilver producing washing machine. Environ Int 37:1057–1062

    CAS  Article  Google Scholar 

  • Franklin KA, Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39:1410–1413

    CAS  Article  Google Scholar 

  • Geisler-Lee J, Wang Q, Yao Y, Zhang W, Geisler M, Li K, Huang Y, Chen Y, Kolmakov A, Ma X (2013) Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana. Nanotoxicol 7:323–337

    CAS  Article  Google Scholar 

  • Geranio L, Heuberger M, Nowack B (2009) The behavior of silver nanotextiles during washing. Environ Sci Technol 43:8113–8118

    CAS  Article  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  Article  Google Scholar 

  • Harada E, Choi EY, Tsuchisaka A, Obata H, Sano H (2001) Transgenic tobacco plants expressing a rice cysteine synthase gene are tolerant to toxic levels of cadmium. J Plant Physiol 158:655–699

    CAS  Article  Google Scholar 

  • Harada E, Yamaguchi Y, Koizumi N, Sano H (2002) Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathway in Arabidopsis. J Plant Physiol 159:445–448

    CAS  Article  Google Scholar 

  • Harris AT, Bali R (2008) On the formation and extent of uptake of silver nanoparticles by live plants. J Nanoparticle Res 10:691–695

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Herbette SL, Taconnat V, Hugouvieux L, Piette ML, Magniette M, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J, Renou JP, Vavasseur A, Leonhardt N (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88:1751–1765

    CAS  Article  Google Scholar 

  • Indo HP, Davidson M, Yen HC, Suenaga S, Tomita K, Nishii T, Higuchi M, Koga Y, Ozawa T, Majima HJ (2007) Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 7:106–118

    CAS  Article  Google Scholar 

  • Initiative TAG (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Jiang HS, Li M, Chang FY, Li W, Yin LY (2012) Physiological analysis of silver nanoparticles and AgNO3 toxicity to Spirodela polyrhiza. Environ Sci Technol 31:1880–1886

    CAS  Google Scholar 

  • Jie Z, Jin-Jun Z, Jian-wei G, Ying-ying W, Xian-zhi X (2013) Phytochrome B positively regulates chlorophyll biosynthesis and chloroplast development in rice. Rice Sci 20:243–248

    Article  Google Scholar 

  • Kaveh R, Li Y, Ranjbar S, Tehrani R, Brueck CL, Aken BV (2013) Changes in Arabidopsis thaliana gene expression in response to silver nanoparticles and silver ions. Environ Sci Technol 47:10637–10644

    CAS  Google Scholar 

  • Khan NA, Samiullah SS, Nazar R (2007) Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J Agron Crop Sci 193:435–444

    CAS  Article  Google Scholar 

  • Kjemtrup S, Boyes DC, Christensen C, McCaskill AJ, Hylton M, Davis K (2003) Growth stage-based phenotypic profiling of plants. Methods Mol Biol 236:427–442

    CAS  Google Scholar 

  • Lee S, Leustek T (1999) The effect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci 141:201–207

    CAS  Article  Google Scholar 

  • Lee CW, Mahendra S, Zodrow K, Li D, Tsai YC, Braam J, Alvarez PJJ (2010) Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem 29:669–675

    CAS  Article  Google Scholar 

  • Liu JY, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–2175

    CAS  Article  Google Scholar 

  • Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061

    CAS  Article  Google Scholar 

  • Ma C, Chhikara S, Xing B, Musante C, White JC, Dhankher OP (2013) Physiological and molecular response of Arabidopsis thaliana (L.) to nanoparticle cerium and indium oxide exposure. ACS Sustain Chem Eng 1:768–778

    CAS  Google Scholar 

  • Maynard, Michelson (2009) Woodrow Wilson International Center for Scholars: analysis-consumer products-nanotechnology project

  • Miralles P, Church TL, Harris AT (2012) Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. Environ Sci Technol 46:9224–9239

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Nazar R, Iqbal N, Syeed S, Khan NA (2010) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mung bean cultivars. J Plant Physiol 168:807–1575

    Article  Google Scholar 

  • Oleszczuk P, Josko I, Xing BS (2011) The toxicity to plants of the sewage sludges containing multiwalled carbon nanotubes. J Hazard Mater 186:436–442

    CAS  Article  Google Scholar 

  • Oukarroum A, Barhoumi L, Pirastru L, Dewez D (2013) Silver nanoparticles toxicity effect on growth and cellular viability of the aquatic plant Lemma gibba. Environ Toxicol Chem 32:902–907

    CAS  Article  Google Scholar 

  • Park HJ, Kim JY, Kim J, Lee JH, Hahn JS, Gu MB, Yoon J (2009) Silver-ion-mediated reactive oxygen species generation affecting bacterial activity. Water Res 43:1027–1032

    CAS  Article  Google Scholar 

  • Park M, Neigh AM, Vermeulen JP, de la Fonteyne LJJ, Verharen HW, Briede JJ, van Loveren H, de Jong WH (2011) The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. Biomaterials 32:9810–9817

    CAS  Article  Google Scholar 

  • Peralta-Videa JR, Zhao L, Lopez-Moreno ML, de la Rosa G, Hong J, Gardea-Torresdey JL (2011) Nanomaterials and the environment: a review for the biennium 2008–2010. J Hazard Mater 186:1–15

    CAS  Article  Google Scholar 

  • Piao MJ, Kang KA, Lee IK, Kim HS, Kim S, Choi JY, Choi J, Hyun JW (2011) Silver nanoparticles induce oxidative cell damage in human liver cells through inhibition of reduced glutathione and induction of mitochondrial-involved apoptosis. Toxicol Lett 201:92–100

    CAS  Article  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 25:1947–1956

    CAS  Article  Google Scholar 

  • Rabino I, Mancinelli AL (1986) Light, temperature and anthocyanin production. Plant Physiol 81:922–924

    CAS  Article  Google Scholar 

  • Rico CM, Majumdar S, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem 27:3485–3498

    Article  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2006) Cd effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544

    Article  Google Scholar 

  • Saito K (2000) Regulation of sulfate transport and synthesis of sulfur containing amino acids. Curr Opin Plant Biol 3:188–195

    CAS  Article  Google Scholar 

  • Schiavona M, Zhang L, Abdel-Ghany SE, Pilon M, Malagoli M, Pilon-Smits EAH (2007) Variation in copper tolerance in Arabidopsis thaliana accessions Columbia, Landsberg erecta and Wassilewskija. Physiol Plant 129:342–350

    Article  Google Scholar 

  • Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646

    CAS  Article  Google Scholar 

  • Sotiriou GA, Pratsinis SE (2010) Antibacterial activity of nanosilver ions and particles. Environ Sci Technol 44:5649–5654

    CAS  Article  Google Scholar 

  • Sun Q, Wang XR, Ding SM, Yuan XF (2005) Effects of interactions between cadmium and zinc on phytochelatin and glutathione production in wheat (Triticum aestivum L.). Environ Toxicol 20:195–201

    CAS  Article  Google Scholar 

  • Szalai G, Kellos T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80

    CAS  Article  Google Scholar 

  • Tahara S (2007) A journey of twenty-five years through the ecological biochemistry of flavonoids. Biosci Biotechnol Biochem 71:1387–1404

    CAS  Article  Google Scholar 

  • Verwey EJW, Overbeek JTG (1948) Theory of the stability of lyophobic colloids. Elsevier, Amsterdam

    Google Scholar 

  • Wang J, Koo Y, Alexander A, Yang Y, Westerhof S, Zhang Q, Schnoor JL, Colvin VL, Braam J, Alvarez PJJ (2013) Phytostimulation of poplars and Arabidopsis exposed to silver nanoparticles and Ag+ at sublethal concentrations. Environ Sci Technol 47:5442–5449

    CAS  Article  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    CAS  Article  Google Scholar 

  • Xia T, Zhao Y, Sager T, George S, Pokhrel S, Li N, Schoenfeld D, Meng H, Lin S, Wang X, Wang M, Ji Z, Zink JI, Madler L, Castranova V, Lin S, Nel AE (2011) Decreased dissolution of ZnO by iron doping yields nanoparticles with reduced toxicity in the rodent lung and zebrafish embryos. ACS Nano 5:1223–1235

    CAS  Article  Google Scholar 

  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    CAS  Article  Google Scholar 

  • Xu L, Takemura T, Xu M, Hanagata N (2011) Toxicity of silver nanoparticles as assessed by global gene expression analysis. Mater Exp 1:74–79

    Article  Google Scholar 

  • Yin L, Colman BP, McGill BM, Wright JP, Bernhard ES (2012) Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS ONE 7:1–7

    Article  Google Scholar 

  • Zechmann B, Müller M, Zellnig G (2008) In: Khan NA, Singh S, Umar S (eds) Modified levels of cysteine affect glutathione metabolism in plant cells. In sulfur assimilation and abiotic stresses in plants, vol 51. Springer, The Netherlands, pp 193–206

    Chapter  Google Scholar 

  • Zhang W, Yao Y, Sullivan N, Chen Y (2011) Modeling the primary size effects of citrate-coated silver nanoparticles on their ion release kinetics. Environ Sci Technol 45:4422–4428

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the SMART Research Professor Program of Konkuk University, Seoul, South Korea to Prakash M. Gopalakrishnan Nair. This work was supported by a grant from the Next-Generation BioGreen 21 Program (Plant Molecular Center No. PJ009053), Rural Development Administration, Republic of Korea.

Conflict of interest

The authors declare no conflict of interest.

Author information

Affiliations

  1. Department of Applied Biosciences, College of Life and Environmental Sciences, Konkuk University, 120 Neungdong-ro, Gwangjin-gu, Seoul, 143-701, South Korea

    Prakash M. Gopalakrishnan Nair & Ill Min Chung

Authors
  1. Prakash M. Gopalakrishnan Nair
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ill Min Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ill Min Chung.

Additional information

Responsible editor: Markus Hecker

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Figure 1
figure 9

(A) Phenotypes of Arabidopsis thaliana seedlings grown in the presence of silver nanoparticles for fourteen days. (Left to right:- control, 0.2, 0.5 and 1 mg/L silver nanoparticles exposed seedlings). Dark squares indicate the root tip browning caused by exposure to different concentrations of silver nanoparticles. (B) Enlarged view of the root of control (Arrow marks indicates root hairs) and (C) 1 mg/L silver nanoparticles (Arrow marks indicates root tip browning) exposed seedlings. (GIF 307 kb)

Full size image
Supplementary Figure 2
figure 10

Mean fluorescence intensity of the control, AgNPs (0.2, 0.5 and 1 mg/L) and Ag+ ions (1 mg/L) exposed roots of plants stained with 2′,7′-dichlorofluorescin diacetate and Rhodamine 123. The mean fluorescence intensities were calculated using image-Pro Plus 6.0 software. The results were mean values of three replications. (GIF 83 kb)

Full size image

High resolution image (TIFF 702 kb)

High resolution image (TIFF 75 kb)

Supplementary Table 1

Details of primer sequence (5’-3’) (DOC 54 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nair, P.M.G., Chung, I.M. Assessment of silver nanoparticle-induced physiological and molecular changes in Arabidopsis thaliana . Environ Sci Pollut Res 21, 8858–8869 (2014). https://doi.org/10.1007/s11356-014-2822-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-2822-y

Keywords

  • Arabidopsis thaliana
  • Silver nanoparticles
  • Lipid peroxidation
  • Mitochondrial membrane potential
  • Gene expression