journal article Open Access Nov 01, 2023

Phytotoxic impact of bifunctionalized silver nanoparticles (AgNPs-Cit-L-Cys) and silver nitrate (AgNO3) on chronically exposed callus cultures of Populus nigra L.

View at Publisher Save 10.1007/s11356-023-30690-7
Abstract
AbstractOwing to the unique physicochemical properties and the low manufacturing costs, silver nanoparticles (AgNPs) have gained growing interest and their application has expanded considerably in industrial and agricultural sectors. The large-scale production of these nanoparticles inevitably entails their direct or indirect release into the environment, raising some concerns about their hazardous aspects. Callus culture represents an important tool in toxicological studies to evaluate the impact of nanomaterials on plants and their potential environmental risk. In this study, we investigated the chronic phytotoxic effects of different concentrations of novel bifunctionalized silver nanoparticles (AgNPs-Cit-L-Cys) and silver nitrate (AgNO3) on callus culture of Populus nigra L., a pioneer tree species in the riparian ecosystem. Our results showed that AgNPs-Cit-L-Cys were more toxic on poplar calli compared to AgNO3, especially at low concentration (2.5 mg/L), leading to a significant reduction in biomass production, accompanied by a decrease in protein content, a significant increase in both lipid peroxidation level, ascorbate peroxidase (APX), and catalase (CAT) enzymatic activities. In addition, these findings suggested that the harmful activity of AgNPs-Cit-L-Cys might be correlated with their physicochemical properties and not solely attributed to the released Ag+ ions and confirmed that AgNPs-Cit-L-Cys phytoxicity is associated to oxidative stress.
Topics

No keywords indexed for this article. Browse by subject →

References
65
[1]
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3 10.1016/s0076-6879(84)05016-3
[2]
The Effects of Copper and Silver Nanoparticles on Container-Grown Scots Pine (Pinus sylvestris L.) and Pedunculate Oak (Quercus robur L.) Seedlings

Marta Aleksandrowicz-Trzcińska, Magdalena Bederska-Błaszczyk, Adam Szaniawski et al.

Forests 2019 10.3390/f10030269
[3]
Al-Huqail AA, Hatata AA, 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 25:313–319. https://doi.org/10.1016/j.sjbs.2017.08.013 10.1016/j.sjbs.2017.08.013
[4]
Ali A, Mohammad S, Khan MA, Raja NI, Arif M, Kamil A, Mashwani ZU (2019) Silver nanoparticles elicited in vitro callus cultures for accumulation of biomass and secondary metabolites in Caralluma tuberculata. Artif Cells Nanomed Biotechnol 47(1):715–724. https://doi.org/10.1080/21691401.2019.1577884 10.1080/21691401.2019.1577884
[5]
Cytotoxicity and Genotoxicity of Silver Nanoparticles in Human Cells

P. V. AshaRani, Grace Low Kah Mun, Manoor Prakash Hande et al.

ACS Nano 2009 10.1021/nn800596w
[6]
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. https://doi.org/10.1007/s11738-016-2092-z 10.1007/s11738-016-2092-z
[7]
Behzadi Tayemeh M, Esmailbeigi M, Shirdel I, Joo HS, Johari SA, Banan A, Nourani H, Mashhadi H, Jami MJ, Tabarrok M (2020) Perturbation of fatty acid composition, pigments, and growth indices of Chlorella vulgaris in response to silver ions and nanoparticles: a new holistic understanding of hidden ecotoxicological aspects of pollutants. Chemosphere 238:124576. https://doi.org/10.1016/j.chemosphere.2019.124576 10.1016/j.chemosphere.2019.124576
[8]
Bell IR, Ives JA, Wayne BJ (2014) Nonlinear effects of nanoparticles: biological variability from hormetic doses, small particle size, and dynamic adaptive interactions. Dose Response 12:202–232. https://doi.org/10.2203/dose-response.13-025.Bell 10.2203/dose-response.13-025.bell
[9]
Bellingeri A, Scattoni M, Venditti I, Battocchio C, Protano G, Corsi I (2022) Ecologically based methods for promoting safer nanosilver for environmental applications. J Hazard Mat 438:129523. https://doi.org/10.1016/j.jhazmat.2022.129523 10.1016/j.jhazmat.2022.129523
[10]
Bernabè-Antonio A, Sánchez-Sánchez A, Romero-Estrada A, Meza-Contreras JC, Silva-Guzmán JA, Fuentes-Talavera FJ, Hurtado-Díaz I, Alvarez L, Cruz-Sosa F (2021) Establishment of a cell suspension culture of Eysenhardtia platycarpa: phytochemical screening of extracts and evaluation of antifungal activity. Plants 10:414. https://doi.org/10.3390/plants10020414 10.3390/plants10020414
[11]
Bertelà F, Marsotto M, Meneghini C, Burratti L, Valentin-Adrian M, Iucci G, Venditti I, Prosposito P, D’Ezio V, Persichini T, Battocchio C (2021) Biocompatible silver nanoparticles: study of the chemical and molecular structure, interaction to cadmium and arsenic in water and biological properties. Nanomaterials 11(10):2540. https://doi.org/10.3390/nano11102540 10.3390/nano11102540
[12]
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999 10.1006/abio.1976.9999
[13]
Budhani S, Egboluche NP, Arslan Z, Yu H, Deng H (2019) Phytotoxic effect of silver nanoparticles on seed germination and growth of terrestrial plants. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 37(4):330–355. https://doi.org/10.1080/10590501.2019.1676600 10.1080/10590501.2019.1676600
[14]
Chung I, 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 69:97–109. https://doi.org/10.1556/018.68.2018.1.8 10.1556/018.68.2018.1.8
[15]
Cocozza C, Perone A, Giordano C, Salvatici MC, Pignattelli S, Raio A, Schaub M, Sever K, Innes JL, Tognetti R, Cherubini P (2019) Silver nanoparticles enter the tree faster through leaves than through roots. Tree Physiol 39(7):1251–1261. https://doi.org/10.1093/treephys/tpz046 10.1093/treephys/tpz046
[16]
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(2):e57189. https://doi.org/10.1371/journal.pone.0057189 10.1371/journal.pone.0057189
[17]
Confalonieri M, Balestrazzi A, Bisoffi S, Carbonera D (2003) In vitro culture and genetic engineering of Populus spp.: synergy for forest tree improvement. Plant Cell Tissue Organ Cult 73:109–138. https://doi.org/10.1023/A:1022265504775 10.1023/a:1022265504775
[18]
Courtois P, Rorat A, Lemiere S, Guyoneaud R, Attard E, Levard C, Vandenbulcke F (2019) Ecotoxicology of silver nanoparticles and their derivatives introduced in soil with or without sewage sludge: a review of effects on microorganisms, plants and animals. Environ Pollut 253:578–598. https://doi.org/10.1016/j.envpol.2019.07.053 10.1016/j.envpol.2019.07.053
[19]
Cox A, Venkatachalam P, Sahi S, Sharma N (2017) Silver and titanium dioxide nanoparticle toxicity in plants: a review of current research. Plant Physiol Biochem 110:33–49. https://doi.org/10.1016/j.plaphy.2016.08.007 10.1016/j.plaphy.2016.08.007
[20]
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. Ecotoxicol Environ Saf 137:18–28. https://doi.org/10.1016/j.ecoenv.2016.11.009 10.1016/j.ecoenv.2016.11.009
[21]
Cvjetko P, Zovko M, Peharec Štefanić P, Biba R, Tkalec M, Domijan AM, Vinković Vrček I, Letofsky-Papst I, Šikić S, Balen B (2018) Phytotoxic effects of silver nanoparticles in tobacco plants. Environ Sci Pollut Res Int 25:5590–5602. https://doi.org/10.1007/s11356-017-0928-8 10.1007/s11356-017-0928-8
[22]
Donner E, Scheckel K, Sekine R, Popelka-Filcoff RS, Bennett JW, Brunetti G, Naidu R, McGrath SP, Lombi E (2015) Non-labile silver species in biosolids remain stable throughout 50 years of weathering and ageing. Environ Pollut 205:78–86. https://doi.org/10.1016/j.envpol.2015.05.017 10.1016/j.envpol.2015.05.017
[23]
Fiorati A, Bellingeri A, Punta C, Corsi I, Venditti I (2020) Silver nanoparticles for water pollution monitoring and treatments: ecosafety challenge and cellulose-based hybrids solution. Polymers 12(8):1635. https://doi.org/10.3390/polym12081635 10.3390/polym12081635
[24]
Ghorbanpour M, Khaltabadi Farahani AH, Hadian J (2018) Potential toxicity of nano-graphene oxide on callus of Plantago major L. under polyethylene glycol-induced dehydration. Ecotoxicol Environ Saf 148:910–922. https://doi.org/10.1016/j.ecoenv.2017.11.061 10.1016/j.ecoenv.2017.11.061
[25]
Grün AL, Straskraba S, Schulz S, Schloter M, Emmerling C (2018) Long-term effects of environmentally relevant concentrations of silver nanoparticles on microbial biomass, enzyme activity, and functional genes involved in the nitrogen cycle of loamy soil. J Environ Sci 69:12–22. https://doi.org/10.1016/j.jes.2018.04.013 10.1016/j.jes.2018.04.013
[26]
Photoperoxidation in isolated chloroplasts

Robert L. Heath, Lester Packer

Archives of Biochemistry and Biophysics 1968 10.1016/0003-9861(68)90654-1
[27]
Homaee MB, Ehsanpour AA (2015) Physiological and biochemical responses of potato (Solanum tuberosum) to silver nanoparticles and silver nitrate treatments under in vitro conditions. Indian J Plant Physiol 20:353–359. https://doi.org/10.1007/s40502-015-0188-x 10.1007/s40502-015-0188-x
[28]
Homaee MB, Ehsanpour AA (2016) Silver nanoparticles and silver ions: oxidative stress responses and toxicity in potato (Solanum tuberosum L.) grown in vitro. Hortic Environ Biotechnol 57(6):544–553. https://doi.org/10.1007/s13580-016-0083-z 10.1007/s13580-016-0083-z
[29]
Iannelli MA, Bellini A, Venditti I, Casentini B, Battocchio C, Scalici M, Ceschin S (2022) Differential phytotoxic effect of silver nitrate (AgNO3) and bifunctionalized silver nanoparticles (AgNPs-Cit-L-Cys) on Lemna plants (duckweeds). Aquat Toxicol 250:106260. https://doi.org/10.1016/j.aquatox.2022.106260 10.1016/j.aquatox.2022.106260
[30]
Iqbal M, Raja Iqbal N, Ali A, Rashid H, Hussain M, Ejaz M, Iqbal R, Khan AU, Shaheen N, Rauf A, Satti Hassan S, Saira H (2019) Silver nanoparticles and silver salt (AgNO3) elicits morphogenic and biochemical variations in callus culturesof sugarcane. IET Nanobiotechnol 13(9):896–904. https://doi.org/10.1049/iet-nbt.2018.5122 10.1049/iet-nbt.2018.5122
[31]
Ihtisham M, Noori A, Yadav S, Sarraf M, Kumari P, Brestic M, Imran M, Jiang F, Yan X, Rastogi A (2021) Silver nanoparticle’s toxicological effects and phytoremediation. Nanomaterials 11:2164. https://doi.org/10.3390/nano11092164 10.3390/nano11092164
[32]
Iori V, Pietrini F, Massacci A, Zacchini M (2012a) Induction of metal binding compounds and antioxidative defence in callus cultures of two black poplar (P. nigra) clones with different tolerance to cadmium. Plant Cell Tiss Org Cult 108:17–26. https://doi.org/10.1007/s11240-011-0006-8 10.1007/s11240-011-0006-8
[33]
Iori V, Pietrini F, Zacchini M (2012b) Assessment of ibuprofen tolerance and removal capability in Populus nigra L. by in vitro culture. J Hazard Mat 229–230:217–223. https://doi.org/10.1016/j.jhazmat.2012.05.097 10.1016/j.jhazmat.2012.05.097
[34]
Jadczak P, Kulpa D, Drozd R, Przewodowski W, Przewodowska A (2020) Effect of AuNPs and AgNPs on the antioxidant system and antioxidant activity of lavender (Lavandula angustifolia Mill.) from in vitro cultures. Molecules 25:5511. https://doi.org/10.3390/molecules25235511 10.3390/molecules25235511
[35]
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. https://doi.org/10.1002/etc.2577 10.1002/etc.2577
[36]
Ke M, Qu Q, Peijnenburg WJGM, Li X, Zhang M, Zhang Z, Lu T, Pan X, Qian H (2018) Phytotoxic effects of silver nanoparticles and silver ions to Arabidopsis thaliana as revealed by analysis of molecular responses and of metabolic pathways. Sci Total Environ 644:1070–1079. https://doi.org/10.1016/j.scitotenv.2018.07.061 10.1016/j.scitotenv.2018.07.061
[37]
Khan I, Raza MA, Khalid MHB, Awan SA, Raja NI, Zhang X, Min S, Wu BC, Hassan MJ, Huang L (2019) Physiological and biochemical responses of pearl millet (Pennisetum glaucum L.) seedlings exposed to silver nitrate (AgNO3) and silver nanoparticles (AgNPs). Int J Environ Res Public Health 16:2261. https://doi.org/10.3390/ijerph16132261 10.3390/ijerph16132261
[38]
Lv QZ, Long JT, Gong ZF, Nong KY, Liang XM, Qin T, Huang W, Yang L (2021) Current state of knowledge on the antioxidant effects and mechanisms of action of polyphenolic compounds. Nat Prod Commun 16:1–13. https://doi.org/10.1177/1934578X211027745 10.1177/1934578x211027745
[39]
Metal-Based Nanotoxicity and Detoxification Pathways in Higher Plants

Chuanxin Ma, Jason C. White, Om Parkash Dhankher et al.

Environmental Science & Technology 2015 10.1021/acs.est.5b00685
[40]
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. https://doi.org/10.1016/j.scitotenv.2010.03.031 10.1016/j.scitotenv.2010.03.031
[41]
McShan D, Ray PC, Yu H (2014) Molecular toxicity mechanism of nanosilver. J Food Drug Anal 22:116–127. https://doi.org/10.1016/j.jfda.2014.01.010 10.1016/j.jfda.2014.01.010
[42]
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures

Toshio Murashige, Folke Skoog

Physiologia Plantarum 1962 10.1111/j.1399-3054.1962.tb08052.x
[43]
Mustafa HS, Oraibi AG, Ibrahim KM, Ibrahim NK (2017) Influence of silver and copper nanoparticles on physiological characteristics of Phaseolus vulgaris L. in vitro and in vivo. Int J Curr Microbiol Appl Sci 6: 834–843. https://doi.org/10.20546/ijcmas.2017.601.098 10.20546/ijcmas.2017.601.098
[44]
Physiological and molecular level studies on the toxicity of silver nanoparticles in germinating seedlings of mung bean (Vigna radiata L.)

Prakash M. Gopalakrishnan Nair, Ill Min Chung

Acta Physiologiae Plantarum 2015 10.1007/s11738-014-1719-1
[45]
Hydrogen Peroxide is Scavenged by Ascorbate-specific Peroxidase in Spinach Chloroplasts

Yoshiyuki Nakano, Kozi Asada

Plant and Cell Physiology 1981 10.1093/oxfordjournals.pcp.a076232
[46]
Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants and fungi. Ecotoxicology 17:372–386. https://doi.org/10.1007/s10646-008-0214-0 10.1007/s10646-008-0214-0
[47]
Peharec Štefanić P, Cvjetko P, Biba R, Domijan AM, Letofsky-Papst I, Tkalec M, Šikić S, Cindrić M, Balen B (2018) Physiological, ultrastructural and proteomic responses of tobacco seedlings exposed to silver nanoparticles and silver nitrate. Chemosphere 209:640–653. https://doi.org/10.1016/j.chemosphere.2018.06.128 10.1016/j.chemosphere.2018.06.128
[48]
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):1–15. https://doi.org/10.1016/j.jhazmat.2010.11.020 10.1016/j.jhazmat.2010.11.020
[49]
Pokhrel LR, Silva T, Dubey B, El Badawy AM, Tolaymat TM, Scheuerman PR (2012) Rapid screening of aquatic toxicity of several metal-based nanoparticles using the MetPLATETMbioassay. Sci Total Environ 426:414–422. https://doi.org/10.1016/j.scitotenv.2012.03.049 10.1016/j.scitotenv.2012.03.049
[50]
Powers CM, Slotkin TA, Seidler FJ, Badireddy AR, Padilla S (2011) Silver nanoparticles alter zebrafisher development and larval behavior: distinct roles for particle size, coating and composition. Neurotoxicol Teratol 33:708–714. https://doi.org/10.1016/j.ntt.2011.02.002 10.1016/j.ntt.2011.02.002

Showing 50 of 65 references

Cited By
11
Plant Cell, Tissue and Organ Cultur...
Journal of Nanobiotechnology
Metrics
11
Citations
65
References
Details
Published
Nov 01, 2023
Vol/Issue
30(54)
Pages
116175-116185
License
View
Funding
Ministero dell’Istruzione, dell’Università e della Ricerca Award: FOE-2021
Consiglio Nazionale delle Ricerche
Regione Lazio Award: A0375–2020-36521
Cite This Article
Valentina Iori, Valerio Giorgio Muzzini, Iole Venditti, et al. (2023). Phytotoxic impact of bifunctionalized silver nanoparticles (AgNPs-Cit-L-Cys) and silver nitrate (AgNO3) on chronically exposed callus cultures of Populus nigra L.. Environmental Science and Pollution Research, 30(54), 116175-116185. https://doi.org/10.1007/s11356-023-30690-7