Does plant growing condition affects biodistribution and biological effects of silver nanoparticles?

Keywords: phytotoxicity, pepper, plant uptake


Among the many different types, silver nanoparticles (AgNPs) are the most commercialized and applied engineered nanoparticles in a wide range of areas, including agriculture. Despite numerous studies on their safety and toxicity of AgNPs, data on their effect and interactions with terrestrial plants are largely unknown. This study aimed to investigate the effect of growing conditions on the response of pepper plants (Capsicum annuum L.) to citrate-coated AgNPs. Growth parameters, biodistribution, and defence response were examined in peppers grown hydroponically or in soil substrate. In addition, the effects of nano and ionic form of silver were compared. The leaves and stems of peppers grown in substrate showed a higher bioaccumulation compared to hydroponically cultivated plants. The nano form of silver accumulated to a higher extent than ionic form in both leaves and stems. Both silver forms inhibited pepper growth to a very similar extent either through hydroponic or substrate growing settings. Unlike other studies, which investigated the effects of unrealistically high doses of AgNPs on different plant species, this study revealed that vascular plants are also susceptible to very low doses of AgNPs. Both silver forms affected all parameters used to evaluate oxidative stress response in pepper leaves; plant pigment and total phenolics contents were decreased, while lipid peroxidation and hydrogen peroxide lever were increased in treated plants. Similar biological effects of both nano and ionic Ag forms were observed for both substrate and hydroponic growing systems.


Download data is not yet available.


Adani F, Genevini P, Zaccheo P, Zocchi G, 1998. The effect of commercial humic acid on tomato plant growth and mineral nutrition. J Plant Nutr 21 (3): 561-575.

Barbasz A, Kreczmer B, Oćwieja M, 2016. Effects of exposure of callus cells of two wheat varieties to silver nanoparticles and silver salt (AgNO3). Acta Physiol Plant 38 (3): 76.

Bernhardt ES, Colman BP, Hochella M, Cardinale B, Nisbet R, Richardson C, Yin L, 2010. Emerging environmental crisis or part of the Green Revolution: the ecological impacts of nanomaterials in the environment. J Environ Qual 39: 1954-1965.

Biemelt S, Keetman U, Mock HP, Grimm B, 2000. Expression and activity of isoenzymes of superoxide dismutase in wheat roots in response to hypoxia and anoxia. Plant Cell Environ 23: 135-144.

Blokhina O, Virolainen E, Fagerstedt KV, 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179-194.

Chen Z, Porcher C, Campbell PGC, Fortin C, 2013. Influence of humic acid on algal uptake and toxicity of ionic silver. Environ Sci Technol 47 (15): 8835-8842.

Chirkova TV, Novitskaya LO, Blokhina OB, 1998. Lipid peroxidation and antioxidant systems under anoxia in plants differing in their tolerance to oxygen deficiency. Russ J Plant Physiol 45: 55-62.

Cvjetko P, Milošić A, Domijan AM, Vinković Vrček I, Tolić S, Peharec Štefanić P, Letofsky-Papst I, Tkalec M, Balen B, 2017. Toxicity of silver ions and differently coated silver nanoparticles in Allium cepa roots. Ecotox Environ Safe 137: 18-28.

Cvjetko P, Zovko M, Peharec Štefanić P, Biba R, Tkalec M, Domijan A-M, Vinković Vrček I, Letofsky-Papst I, Šikić S, Balen B, 2018. Phytotoxic effects of silver nanoparticles in tobacco plants. Environ Sci Pollut Res 25 (6): 5590-5602.

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

EC, 2014. Considerations on information needs for nanomaterials in consumer products. European Commission, Joint Research Centre, Institute for Health and Consumer Protection, Ispra, Italy. [21 Jan 2018].

Eyheraguibel B, Silvestre J, Morard P, 2008. Effects of humic substances derived from organic waste enhancement on the growth and mineral nutrition of maize. Bioresour Technol 99: 4206-4212.

Fabrega J, Luoma SN, Tyler CR, Galloway TS, Leadet JR, 2011. Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37: 517-531.

Ferrante A, Quattrini E, Martinetti L, Schiavi M, Maggiore T, 2005. Per la quarta gamma. Colture Protette 12: 72.

Gardea-Torresdey JL, Gomez E, Peralta-Videa J, Parsons JG, Troiani HE, Yacaman MJ, 2003. Alfalfa sprouts: a natural source for the synthesis of silver nanoparticles. Langmuir 19: 1357-1361.

Gubbins EJ, Batty LC, Lead JR, 2011. Phytotoxicity of silver nanoparticles to Lemna minor L. Environ Pollut 159: 1551-1559.

Harris AT, Bali RJ, 2008. On the formation and extent of uptake of silver nanoparticles by live plants. J Nanopart Res 10: 691-695.

Heath RL, Packer L, 1968. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archiv Biochem Biophys 125: 189-198.

Jiang H, Li M, Chang F, Li W, Yin L, 2012. Physiological analysis of silver nanoparticles and AgNO3 toxicity to Spirodela polyrrhiza. Environ Toxicol Chem 31: 1880-1996.

Jiang HS, Qiu XN, Li GB, Li W, Yin LY, 2014. Silver nanoparticles induced accumulation of reactive oxygen species and alteration of antioxidant systems in the aquatic plant Spirodela polyrhiza. Environ Toxicol Chem 33 (6): 1398-1405.

Judy JD, Unrine JM, Bertsch PM, 2011. Evidence for biomagnification of gold nanoparticles within a terrestrial food chain. Environ Sci Technol 45: 776-781.

Kalashnikov JuE, Balakhnina TI, Zakrzhevsky DA, 1994. Effect of soil hypoxia on activation of oxygen and the system of protection from oxidative destruction in roots and leaves of Hordeum vulgare. Russ J Plant Physiol 41: 583-588.

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

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

Le VN, Rui Y, Gui X, Li X, Liu S, Han Y, 2014. Uptake, transport, distribution and bio-effects of SiO2 nanoparticles in Bt-transgenic cotton. J Nanobiotechnol 12: 50.

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.

Lenzi A, Baldi A, Tesi R, 2008. Effect of hypoxia on yield and quality of leafy vegetables grown in floating system. Abstracts Book "First Symposium on Horticulture in Europe", Vienna, 17-20 Feb, pp: 212-213.

Lenzi A, Baldi A, Tesi R, 2011. Growing spinach in a floating system with different volumes of aerated or non-aerated nutrient solution. Adv Hortic Sci 25 (1): 21-25.

Li R, Zhou Z, Xie X, Li Y, Zhang Y, Xu X, 2016. Effects of dissolved organic matter on uptake and translocation of lead in Brassica chinensis and potential health risk of Pb. Int J Environ Res Public Health 13 (7): 687.

Lichtenthaler HK, Wellburn AR, 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11: 591-592.

Lin D, Xing B, 2007. Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 150: 243-250.

Lin D, Xing B, 2008. Root uptake and phytotoxicity of ZnO nanoparticles. Environ Sci Technol 42: 5580-5585.

Michalak A, 2006. Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15 (4): 523-530.

Milić M, Leitinger G, Pavičić I, Zebić Avdičević M, Dobrović S, Goessler W, Vinković Vrček I, 2015. Cellular uptake and toxicity effects of silver nanoparticles in mammalian kidney cells. J Appl Toxicol 35 (6): 581-592.

Monica RC, Crenomini R, 2009. Nanoparticles and higher plants. Caryologia 62 (2): 161-165.

Mukherjee SP, Choudhuri MA, 1983. Implications of water stress-induced changes in the level of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plantarum 58: 166-170.

Nagajyoti PC, Lee KD, Sreekanth TVM, 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8: 199-216.

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

Piqueras A, Olmos E, Martinez-Solano JR, Hellin E, 1999. Cd-induced oxidative burst in tobacco BY2 cells: time-course, subcellular location and antioxidant response. Free Radical Res 31: 33-38.

Pokhrel LR, Dubey B, 2013. Evaluation of developmental responses of two crop plants exposed to silver and zinc oxide nanoparticles. Sci Total Environ 452-453: 321-332.

Reinsch BC, Levard C, Li Z, Ma R, Wise A, Gregory KB, Brown Jr GE, Lowry GV, 2012. Sulfidation of silver nanoparticles decreases Escherichia coli growth inhibition. Environ Sci Technol 46: 6992-7000.

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 Agr Food Chem 59: 3485-3489.

Sakihama Y, Cohen MF, Grace SC, Yamasaki H, 2002. Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177 (1): 67-80.

Schützendübel A, Polle A, 2002. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53 (372): 1351-1365.

Sharma P, Jha AB, Dubey RS, Pessarakli M, 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012: 1-26.

Shukla D, Krishnamurthy S, Sahi SV, 2014. Genome wide transcriptome analysis reveals ABA mediated response in Arabidopsis during gold (AuCl−4) treatment. Front Plant Sci 5: 652.

Singleton VL, Rossi JA, 1965. Colorimetry of total phenolics with phosphomolybdic- phosphotungstic acid reagents. Am J Enol Viticult 16: 144-158.

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

USEPA, 1996. Ecological effects test guidelines: terrestrial plant toxicity — vegetative vigor. OPPTS 850.4250, EPA 712-C-96-163 and Early Seedling Toxicity Test, OPPTS 850.4130, EPA 712–C–96–347, United States Environmental Protection Agency, Washington DC.

Vannini C, Domingo G, Onelli E, Prinsi B, Marsoni M, Espen L, Bracale M, 2013. Morphological and proteomic responses of Eruca sativa exposed to silver nanoparticles or silver nitrate. PLoS One 8 (7): e68752.

Vinković T, Novák O, Strnad M, Goessler W, Domazet Jurašin D, Parađiković N, Vinković Vrček I, 2017. Cytokinin response in pepper plants (Capsicum annuum L.) exposed to silver nanoparticles. Environ Res 156: 10-18.

Yan B, Dai Q, Liu X, Huang S, Wang Z, 1996. Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves. Plant Soil 179: 261-268.

Yasur J, Rani PU, 2013. Environmental effects of nanosilver: impact on castor seed germination, seedling growth, and plant physiology. Environ Sci Pollut Res 20: 8636-8648.

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: 2360-2367.

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 (10): e47674.

How to Cite
VinkovićT., Štolfa-ČamagajevacI., TkalecM., GoesslerW., Domazet-JurašinD., & Vinković-VrčekI. (2019). Does plant growing condition affects biodistribution and biological effects of silver nanoparticles?. Spanish Journal of Agricultural Research, 16(4), e0803.
Plant physiology