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Physiological, metabolic, and transcriptional effects of biologically-synthesized silver nanoparticles in turnip (Brassica rapa ssp. rapa L.)

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Abstract

Silver nanoparticles (AgNPs) use has been increased in recent years, which has potentially antagonistic effects on living organisms, including microbes, human, and plants. The physiological and molecular responses of AgNPs have been reported for several plants; however, the detailed mechanism of action of AgNPs is not known in turnip. Accordingly, the aim of this study was determined to evaluate the impact of AgNPs exposure in turnip seedlings at concentrations up to 10.0 mg/l. The frequency of seed germination decreased with increasing AgNPs concentration. Moreover, while exposure to 1.0 mg/l AgNPs significantly increased plant fresh biomass. The plant growth, biomass, and chlorophyll content were decreased at 5.0 and 10.0 mg/l AgNPs. Anthocyanin, malondialdehyde, and hydrogen peroxide levels were significantly increased with higher concentrations of AgNPs. Furthermore, reactive oxygen species (ROS) production and DNA damage were significantly elevated in plants treated with higher concentrations of AgNPs. The DNA damage potential was confirmed in the experiment of DNA laddering, comet, and TUNEL assays. Consequently, the study confirms the phytotoxic, cytotoxic, and genotoxic potentials induced by AgNPs. Moreover, higher concentrations (5.0 and 10.0 mg/l) of AgNPs significantly induced expression of genes related to glucosinolates and phenolics biosynthesis as well as abiotic and biotic stresses whereas down-regulated the carotenoid gene expressions. To our knowledge, this is the first report to evaluate the physiological, metabolic, and transcriptional responses of turnip to biologically synthesized AgNPs.

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References

  • Albrecht MA, Evans CW, Raston CL (2006) Green chemistry and the health implications of nanoparticles. Green Chem 8:417–432

    Article  CAS  Google Scholar 

  • Borevitz JO, **a Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2394

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Donaldson K, Stone V, MacNee W (1999) The toxicology of ultrafine particles. In: Maynard RL, Howards CV (eds) Particulate matter: Properties and effects upon health. Bios, Oxford, pp 115–127

    Google Scholar 

  • Du YY, Wang PC, Chen J, Song CP (2008) Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J Integr Plant Biol 50:1318–1326

  • Duan Y, Zhang W, Li B, Wang Y, Li K, Sodmergen HC, Zhang Y, Li X (2010) An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytol 186:681–695

    Article  CAS  PubMed  Google Scholar 

  • Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: Behaviour and effects in the aquatic environment. Environ Int 37:517–531

    Article  CAS  PubMed  Google Scholar 

  • Faisal M, Saquib Q, Alatar AA, Al-Khedhairy AA, Hegazy AK, Musarrat J (2013) Phytotoxic hazards of NiO-nanoparticles in tomato: a study on mechanism of cell death. J Hazard Mater 250:318–332

    Article  PubMed  Google Scholar 

  • Fendrych M, Van Hautegem T, Van Durme M, Olvera-Carrillo Y, Huysmans M, Karimi M, Lippens S, Guérin CJ, Krebs M, Schumacher K, Nowack MK (2014) Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr Biol 24:931–940

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Descourvières P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism study in transgenic plants. Plant Cell Environ 17:507–523

    Article  CAS  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. Nanotoxicology 7:323–337

    Article  CAS  PubMed  Google Scholar 

  • Ghosh M, Bandyopadhyay M, Mukherjee A (2010) Genotoxicity of titanium dioxide (TiO2) nanoparticles at two trophic levels: Plant and human lymphocytes. Chemosphere 81:1253–1262

    Article  CAS  PubMed  Google Scholar 

  • Gigolashvili T, Yatusevich R, Berger B, Müller C, Flügge UI (2007) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 51:247–261

    Article  CAS  PubMed  Google Scholar 

  • Gigolashvili T, Engqvist M, Yatusevich R, Müller C, Flügge UI (2008) HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol 177:627–642

    Article  CAS  PubMed  Google Scholar 

  • Gould KS, McKelvie J, Markham KR (2002) Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury. Plant Cell Environ 25:1261–1269

    Article  CAS  Google Scholar 

  • Guo N, Cheng F, Wu J, Liu B, Zheng S, Liang J, Wang X (2014) Anthocyanin biosynthetic genes in Brassica rapa. BMC Genomics 15:426

    Article  PubMed Central  PubMed  Google Scholar 

  • Gurunathan S, Lee KJ, Kalishwaralal K, Sheikpranbabu S, Vaidyanathan R, Eom SH (2009) Antiangiogenic properties of silver nanoparticles. Biomaterials 30:6341–6350

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Henglein A (1993) Physicochemical properties of small metal particles in solution: microelectrode reactions chemisorption, composite metal particles, and the atom to metal transition. J Phys Chem 97:5457–5471

    Article  CAS  Google Scholar 

  • Jeong SW, Das PK, Jeoung SC, Song JY, Lee HK, Kim YK, Kim WJ, Park YI, Yoo SD, Choi SB, Choi G, Park YI (2010) Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis. Plant Physiol 154:1514–1531

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jeong MJ, Choi BS, Bae DW, Shin SC, Park SU, Lim HS, Kim J, Kim JB, Cho BK, Bae H (2012) Differential expression of kenaf phenylalanine ammonia-lyase (PAL) ortholog during developmental stages and in response to abiotic stresses. Plant Omics 5:392–399

    CAS  Google Scholar 

  • 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 

  • Kalishwaralal K, Deepak V, Pandian SRK, Kottaisamy M, Kanth SB, Kartikeyan B, Gurunathan S (2010) Biosynthesis of silver and gold nanoparticles using Brevibacterium casei. Colloids Surf B: Biointerfaces 77:257–262

    Article  CAS  PubMed  Google Scholar 

  • Kaveh R, Li YS, 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  PubMed  Google Scholar 

  • Kim YB, Li X, Kim S-J, Kim HH, Lee J, Kim HR, Park SU (2013) MYB Transcription factors regulate glucosinolate biosynthesis in different organs of chinese cabbage (Brassica rapa ssp. pekinensis). Molecules 18:8682–8695

  • Kumari M, Mukherjee A, Chandrasekaran N (2009) Genotoxicity of silver nanoparticles in Allium cepa. Sci Total Environ 407:5243–5246

    Article  CAS  PubMed  Google Scholar 

  • Lee WM, Kwak JI, An YJ (2012) Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor: Media effect on phytotoxicity. Chemosphere 86:491–499

    Article  CAS  PubMed  Google Scholar 

  • Lee JG, Bonnema G, Zhang N, Kwak JH, de Vos RCH, Beekwilder J (2013) Evaluation of glucosinolate variation in a collection of turnip (Brassica rapa) germplasm by the analysis of intact and desulfo glucosinolates. J Agric Food Chem 61:3984–3993

    Article  CAS  PubMed  Google Scholar 

  • Lin TH, Huang YL, Huang SF (2006) Lipid peroxidation in liver of rats administrated with methyl mercuric chloride. Biol Trace Elem Res 54:33–41

    Article  Google Scholar 

  • Liu WX, Zhang FC, Zhang WZ, Song LF, Wu WH, Chen YF (2013) Arabidopsis Di19 functions as a transcription factor and modulates PR1, PR2, and PR5 expressions in response to drought stress. Mol Plant 6:1487–1502

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • López-Berenguer C, Martínez-Ballesta MC, García-Viguera C, Carvajal M (2008) Leaf water balance mediated by aquaporins under salt stress and associated glucosinolate synthesis in broccoli. Plant Sci 174:321–328

    Article  Google Scholar 

  • Lu Y, Li X, He M, Zhao X, Liu Y, Cui Y, Pan Y, Tan H (2010) Seedlings growth and antioxidative enzyme activities in leaves under heavy metal stress differ between two desert plants: a perennial (Peganum harmala) and an annual (Halogeton glomeratus) grass. Acta Physiol Plant 32:583–590

    Article  CAS  Google Scholar 

  • Maccarrone M, Veldink GA, Agro AF, Vliegenthart JF (1995) Modulation of soybean lipoxygenase expression and membrane oxidation by water deficit. FEBS Lett 371:223–226

  • Nagata T, Todoriki S, Masumizu T, Suda I, Furuta S, Du Z, Kikuchi S (2003) Levels of active oxygen species are controlled by ascorbic acid and anthocyanin in Arabidopsis. J Agric Food Chem 51:2992–2999

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Safe 78:80–85

    Article  CAS  Google Scholar 

  • Panda KK, Achary VMM, Krishnaveni R, Padhi BK, Sarangi SN, Sahu SN, Panda BB (2011) In vitro biosynthesis and genotoxicity bioassay of silver nanoparticles using plants. Toxicol In Vitro 25:1097–1105

    Article  CAS  PubMed  Google Scholar 

  • Poynton HC, Lazorchak JM, Impellitteri CA, Blalock BJ, Rogers K, Allen HJ, Loguinov A, Heckman JL, Govindasmawy S (2012) Toxicogenomic responses of nanotoxicity in Daphnia magna exposed to silver nitrate and coated silver nanoparticles. Environ Sci Technol 46:6288–6296

  • Qian H, Peng X, Han X, Ren J, Sun L, Fu Z (2013) Comparison of the toxicity of silver nanoparticles and silver ion on the growth of terrestrial plant model Arabidopsis thaliana. J Environ Sci 25:1947–1955

    Article  CAS  Google Scholar 

  • Ruffini Castiglione M, Giorgetti L, Cremonini R, Bottega S, Spanò C (2014) Impact of TiO2 nanoparticles on Vicia narbonensis L.: Potential toxicity effects. Protoplasma. doi:10.1007/s00709-014-0649-5

    PubMed  Google Scholar 

  • Sastry M, Mayya KS, Bandyopadhyay K (1997) pH Dependent changes in the optical properties of carboxylic acid derivatized silver colloidal particles. Colloid Surf A127:221–228

    Article  Google Scholar 

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

    Article  CAS  PubMed  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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sperdouli I, Moustakas M (2012) Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. J Plant Physiol 169:577–585

    Article  CAS  PubMed  Google Scholar 

  • Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473–9479

    Article  CAS  PubMed  Google Scholar 

  • Thakkar KN, Mhatre SS, Parikh RY (2010) Biological synthesis of metallic nanoparticles. Nanomedicine 6:257–262

    Article  CAS  PubMed  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Torre-Roche RDL, Hawthorne J, Musante C, **ng B, Newman LA, Ma X, White JC (2013) Impact of Ag nanoparticle exposure on p, p′-DDE bioaccumulation by Cucurbita pepo (Zucchini) and Glycine max (Soybean). Environ Sci Technol 47:718–725

  • Vidhyavathi R, Venkatachalam L, Sarada R, Ravishankar GA (2008) Regulation of carotenoid biosynthetic genes expression and carotenoid accumulation in the green alga Haematococcus pluvialis under nutrient stress conditions. J Exp Bot 59:1409–1418

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Joseph JA (1999) Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 27:612–616

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, **e X, Zhao J, Liu X, Feng W, White JC, **ng B (2012) Xylem and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ Sci Technol 46:4434–4441

    Article  CAS  PubMed  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

  • Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opinion Plant Biol 5:218–223

  • Yin L, Colman BP, McGill BM, Wright JP, Bernhardt ES (2012) Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS One 7:e47674

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Acknowledgments

This paper was supported by the KU Research Professor Program of Konkuk University, Seoul, South Korea to Muthu Thiruvengadam. This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (2014R1A2A2A01002202).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Applied Bioscience, College of Life and Environmental Sciences, Konkuk University, Seoul, 143 701, Republic of Korea

    Muthu Thiruvengadam & Ill-Min Chung

  2. Department of Animal Biotechnology, Konkuk University, Seoul, 143701, Republic of Korea

    Sangiliyandi Gurunathan

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  1. Muthu Thiruvengadam
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Correspondence to Ill-Min Chung.

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Handling Editor: Liwen Jiang

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Thiruvengadam, M., Gurunathan, S. & Chung, IM. Physiological, metabolic, and transcriptional effects of biologically-synthesized silver nanoparticles in turnip (Brassica rapa ssp. rapa L.). Protoplasma 252, 1031–1046 (2015). https://doi.org/10.1007/s00709-014-0738-5

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