Abstract
Silver nanoparticles (AgNP) have been extensively applied in different industrial areas, mainly due to their antibiotic properties. One of the environmental concerns with AgNP is its incorrect disposal, which might lead to severe environmental pollution. The interplay between AgNP and plants is receiving increasing attention. However, little is known regarding the phytotoxic effects of biogenic AgNP on terrestrial plants. This study aimed to compare the effects of a biogenic AgNP and AgNO3 in Sorghum bicolor seedlings. Seeds were germinated in increasing concentrations of a biogenic AgNP and AgNO3 (0, 10, 100, 500, and 1000 μM) in a growth chamber with controlled conditions. The establishment and development of the seedlings were evaluated for 15 days. Physiological and morpho-anatomical indicators of stress, enzymatic, and non-enzymatic antioxidants and photosynthetic yields were assessed. The results showed that both AgNP and AgNO3 disturbed germination and the establishment of sorghum seedlings. AgNO3 released more free Ag+ spontaneously compared to AgNP, promoting increased Ag+ toxicity. Furthermore, plants exposed to AgNP triggered more efficient protective mechanisms compared with plants exposed to AgNO3. Also, the topology and connectivity of the correlation-based networks were more impacted by the exposure of AgNO3 than AgNP. In conclusion, it is plausible to say that the biogenic AgNP is less toxic to sorghum than its matrix AgNO3.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- AgNP:
-
Silver nanoparticle
- AgNO3 :
-
Silver nitrate
- APX:
-
Ascorbate peroxidase
- ASC:
-
Ascorbate
- CAT:
-
Catalase
- Chl :
-
Chlorophyll
- ROS:
-
Reactive oxygen species
- PPFD:
-
Photosynthetic photon flux density
- rcf:
-
Relative centrifuge force
- RWC:
-
Relative water content
- TBARS:
-
Thiobarbituric acid-reactive substances
References
Agbedahin AV (2019) Sustainable development, Education for Sustainable Development, and the 2030 Agenda for Sustainable Development: Emergence, efficacy, eminence, and future. Sustainable Development 27(4):669–680
Anjum NA, Gill SS, Duarte AC, Pereira E, Ahmad I (2013) Silver nanoparticles in soil-plant systems. Journal of Nanoparticle Research 15. https://doi.org/10.1007/s11051-013-1896-7
Assenov Y, Ramírez F, Schelhorn SESE, Lengauer T, Albrecht M (2008) Computing topological parameters of biological networks. Bioinformatics 24:282–284. https://doi.org/10.1093/bioinformatics/btm554
Basu S, Duren W, Evans CR, Burant CF, Michailidis G, Karnovsky A (2017) Sparse network modeling and metscape-based visualization methods for the analysis of large-scale metabolomics data. Bioinformatics 33:1545–1553. https://doi.org/10.1093/bioinformatics/btx012
Benn TM, Westerhoff P (2008) Nanoparticle Silver Released into Water from Commercially Available Sock Fabrics. Environmental Science & Technology 42:4133–4139. https://doi.org/10.1021/es7032718
Bertolli SC, Vítolo HF, Souza GM (2013) Network connectance analysis as a tool to understand homeostasis of plants under environmental changes. Plants 2:473–488. https://doi.org/10.3390/plants2030473
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum 83:463–468. https://doi.org/10.1111/j.1399-3054.1991.tb00121.x
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. Environmental Pollution 253:578–598. https://doi.org/10.1016/j.envpol.2019.07.053
Cvjetko, P., Milosic, A., Domijan, A.M., Vinkovic Vrcek, I., Tolic, S., Peharec S?tefanic P, Letofsky-Papst I, Tkalec M, Balen B 2017. Toxicity of silver ions and differently coated silver nanoparticles in Allium cepa roots. Ecotoxicology and Environmental Safety 137, 18–28. https://doi.org/10.1016/j.ecoenv.2016.11.009
Dewez D, Goltsev V, Kalaji HM, Oukarroum A (2018) Inhibitory effects of silver nanoparticles on photosystem II performance in Lemna gibba probed by chlorophyll fluorescence. Current Plant Biology 16:15–21. https://doi.org/10.1016/j.cpb.2018.11.006
Dietz KJ, Herth S (2011) Plant nanotoxicology. Trends in Plant Science 16:582–589. https://doi.org/10.1016/j.tplants.2011.08.003
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. Environmental Science & Technology 47:1082–1090. https://doi.org/10.1021/es302973y
El-Temsah YS, Joner EJ (2012) Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environmental Toxicology 27:42–49. https://doi.org/10.1002/tox.20610
Fayez KA, El-Deeb BA, Mostafa NY (2017) Toxicity of biosynthetic silver nanoparticles on the growth, cell ultrastructure and physiological activities of barley plant. Acta Physiologiae Plantarum 39. https://doi.org/10.1007/s11738-017-2452-3
Geranio L, Heuberger M, Nowack B (2009) The Behavior of Silver Nanotextiles during Washing. Environmental Science & Technology 43:8113–8118. https://doi.org/10.1021/es9018332
Giannopolotis CN, Ries SK (1977) Superoxide dismutases: Occurrence in higher plants. Plant Physiology 59:309–314
Goh C-H, Ko S-M, Koh S, Kim Y-J, Bae H-J (2011) Photosynthesis and Environments: Photoinhibition and Repair Mechanisms in Plants. Journal of Plant Biology 55:93–101. https://doi.org/10.1007/s12374-011-9195-2
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry 106:207–212. https://doi.org/10.1016/0003-2697(80)90139-6
Havir EA, McHale NA (1987) Biochemical and Developmental Characterization of Multiple Forms of Catalase in Tobacco Leaves. PLANT PHYSIOLOGY 84:450–455. https://doi.org/10.1104/pp.84.2.450
Inamine G, Baker J (1989) A catalase from tomato fruit. Phytochemistry 28:345–348
Jiang HS, Li M, Chang FY, Li W, Yin LY (2012) Physiological analysis of silver nanoparticles and AgNO3 toxicity to Spirodela polyrhiza. Environmental Toxicology and Chemistry 31:1880–1886. https://doi.org/10.1002/etc.1899
Jiang HS, Yin LY, Ren NN, Zhao ST, Li Z, Zhi Y, Shao H, Li W, Gontero B (2017) Silver nanoparticles induced reactive oxygen species via photosynthetic energy transport imbalance in an aquatic plant. Nanotoxicology 11:157–167. https://doi.org/10.1080/17435390.2017.1278802
Johansen DA (1940) Plant Microtechnique. McGraw-Hill, New York, NY
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). International journal of environmental research and public health 16:1–17. https://doi.org/10.3390/ijerph16132261
Lardinois OM, Mestdagh MM, Rouxhet PG (1996) Reversible inhibition and irreversible inactivation of catalase in presence of hydrogen peroxide. Biochimica et biophysica acta 1295:222–238
Larue C, Castillo-Michel H, Sobanska S, Cécillon L, Bureau S, Barthès V, Ouerdane L, Carrière M, Sarret G (2014) Foliar exposure of the crop Lactuca sativa to silver nanoparticles: Evidence for internalization and changes in Ag speciation. Journal of Hazardous Materials 264:98–106. https://doi.org/10.1016/j.jhazmat.2013.10.053
Li W-Q, Qing T, Li C-C, Li F, Ge F, Fei J-J, Peijnenburg WJGM (2020) Integration of subcellular partitioning and chemical forms to understand silver nanoparticles toxicity to lettuce (Lactuca sativa L.) under different exposure pathways. Chemosphere 258:127349. https://doi.org/10.1016/j.chemosphere.2020.127349
Lichtenthaler H, Wellburn A, Lichtentharler HK, Welburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11:591–592. https://doi.org/10.1042/bst0110591
Lima Neto MC, Silveira JAG, Cerqueira JVA, Cunha JR (2017) Regulation of the photosynthetic electron transport and specific photoprotective mechanisms in Ricinus communis under drought and recovery. Acta Physiologiae Plantarum 39:183. https://doi.org/10.1007/s11738-017-2483-9
Lin D, Xing B (2007) Phytotoxicity of nanoparticles: Inhibition of seed germination and root growth. Environmental Pollution 150:243–250. https://doi.org/10.1016/j.envpol.2007.01.016
Liu J, Hurt RH (2010) Ion Release Kinetics and Particle Persistence in Aqueous Nano-Silver Colloids. Environmental Science & Technology 44:2169–2175. https://doi.org/10.1021/es9035557
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence--a practical guide. Journal of experimental botany 51:659–668
Mueller NC, Nowack B (2008) Exposure Modeling of Engineered Nanoparticles in the Environment. Environmental Science & Technology 42:4447–4453. https://doi.org/10.1021/es7029637
Nakano Y, Asada K (1981a) Hydrogen Peroxide is Scavenged by Ascorbate-specific Peroxidase in Spinach Chloroplasts. Plant and Cell Physiology 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nakano Y, Asada K (1981b) Hydrogen peroxide is scavenged by ascorbato specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nallanthighal S, Chan C, Bharali DJ, Mousa SA, Vásquez E, Reliene R (2017) Particle coatings but not silver ions mediate genotoxicity of ingested silver nanoparticles in a mouse model. NanoImpact 5:92–100. https://doi.org/10.1016/j.impact.2017.01.003
Noori A, Donnelly T, Colbert J, Cai W, Newman LA, White JC (2020) Exposure of tomato ( Lycopersicon esculentum ) to silver nanoparticles and silver nitrate: physiological and molecular response. International Journal of Phytoremediation 22:40–51. https://doi.org/10.1080/15226514.2019.1634000
Ogbaga CC, Stepien P, Johnson GN (2014) Sorghum ( Sorghum bicolor ) varieties adopt strongly contrasting strategies in response to drought. Physiologia Plantarum 152:389–401. https://doi.org/10.1111/ppl.12196
Ottoni CA, Simões MF, Fernandes S, dos Santos JG, Silva ES, de Souza RFB, Maiorano AE (2017) Screening of filamentous fungi for antimicrobial silver nanoparticles synthesis. AMB Express 7:31. https://doi.org/10.1186/s13568-017-0332-2
Ottoni CA, Lima Neto MC, Léo P, Ortolan BD, Barbieri E, De Souza AO (2020) Environmental impact of biogenic silver nanoparticles in soil and aquatic organisms. Chemosphere 239:124698. https://doi.org/10.1016/j.chemosphere.2019.124698
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman WD, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556. https://doi.org/10.1038/nature07723
Pereira SPP, Jesus F, Aguiar S, de Oliveira R, Fernandes M, Ranville J, Nogueira AJA (2018) Phytotoxicity of silver nanoparticles to Lemna minor: Surface coating and exposure period-related effects. Science of The Total Environment 618:1389–1399. https://doi.org/10.1016/j.scitotenv.2017.09.275
Pradas del Real AE, Vidal V, Carrière M, Castillo-Michel H, Levard C, Chaurand P, Sarret G (2017) Silver Nanoparticles and Wheat Roots: A Complex Interplay. Environmental Science & Technology 51:5774–5782. https://doi.org/10.1021/acs.est.7b00422
Rani PU, Yasur J, Loke KS, Dutta D (2016) Effect of synthetic and biosynthesized silver nanoparticles on growth, physiology and oxidative stress of water hyacinth: Eichhornia crassipes (Mart) Solms. Acta Physiologiae Plantarum 38:1–9. https://doi.org/10.1007/s11738-016-2074-1
Rastogi, Anshu, Zivcak, M., Tripathi, D.K., 2019a. Phytotoxic effect of silver nanoparticles in Triticum aestivum : Improper regulation of photosystem I activity as the reason for oxidative damage in the chloroplast Phytotoxic effect of silver nanoparticles in Triticum aestivum : Improper regulation of ph. https://doi.org/10.32615/ps.2019.019
Rastogi, A., Zivcak, M., Tripathi, D.K., Yadav, S., Kalaji, H.M., 2019b. Phytotoxic effect of silver nanoparticles in Triticum aestivum: Improper regulation of photosystem I activity as the reason for oxidative damage in the chloroplast. Photosynthetica 57, 209–216. 10.32615/ps.2019.019
Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S., Mittler, R., 2004. When Defense Pathways Collide . The Response of Arabidopsis to a Combination of Drought and Heat Stress 1 [ w ]. Stress: The International Journal on the Biology of Stress 134, 1683–1696. https://doi.org/10.1104/pp.103.033431.1
Rodrigues AG, Ping LY, Marcato PD, Alves OL, Silva MCP, Ruiz RC, Melo IS, Tasic L, De Souza AO (2013) Biogenic antimicrobial silver nanoparticles produced by fungi. Applied Microbiology and Biotechnology 97:775–782. https://doi.org/10.1007/s00253-012-4209-7
Roy A, Bulut O, Some S, Mandal AK, Yilmaz MD (2019) Green synthesis of silver nanoparticles: biomolecule-nanoparticle organizations targeting antimicrobial activity. RSC Adv 9:2673–2702. https://doi.org/10.1039/C8RA08982E
Salem SS, Fouda A (2020) Green synthesis of metallic nanoparticles and their prospective biotechnological applications: An overview. Biol Trace Elem Res 199:344–370. https://doi.org/10.1007/s12011-020-02138-3
Schrader M, Fahimi HD (2006) Peroxisomes and oxidative stress. Biochimica et biophysica acta 1763:1755–1766. https://doi.org/10.1016/j.bbamcr.2006.09.006
Simões MF, Ottoni CA, Antunes A (2020) Biogenic Metal Nanoparticles: A New Approach to Detect Life on Mars? Life 10(3):28. https://doi.org/10.3390/life10030028
Sheth BP, Thaker VS (2014) Plant systems biology: Insights, advances and challenges. Planta 240:33–54. https://doi.org/10.1007/s00425-014-2059-5
Thuesombat P, Hannongbua S, Akasit S, Chadchawan S (2014) Effect of silver nanoparticles on rice (Oryza sativa L. cv. KDML 105) seed germination and seedling growth. Ecotoxicology and Environmental Safety. https://doi.org/10.1016/j.ecoenv.2014.03.022
Tripathi, A., Liu, S., Singh, P.K., Kumar, N., Pandey, A.C., Tripathi, D.K., Chauhan, D.K., Sahi, S., 2017. Differential phytotoxic responses of silver nitrate (AgNO 3 ) and silver nanoparticle (AgNps) in Cucumis sativus L. Plant Gene 0–1. https://doi.org/10.1016/j.plgene.2017.07.005, 11, 255
Verma DK, Patel S, Kushwah KS (2020) Green biosynthesis of silver nanoparticles and impact on growth, chlorophyll, yield and phytotoxicity of Phaseolus vulgaris L. Vegetos. 33:648–657. https://doi.org/10.1007/s42535-020-00150-5
Vishwakarma K, Shweta, Upadhyay N, Singh J, Liu S, Singh VP, Prasad SM, Chauhan DK, Tripathi DK, Sharma S (2017) Differential Phytotoxic Impact of Plant Mediated Silver Nanoparticles (AgNPs) and Silver Nitrate (AgNO3) on Brassica sp. Frontiers in Plant Science 8:1501. https://doi.org/10.3389/fpls.2017.01501
Wu B, Li L, Qiu T, Zhang X, Cui S (2018) Cytosolic APX2 is a pleiotropic protein involved in H2O2homeostasis, chloroplast protection, plant architecture and fertility maintenance. Plant Cell Reports 37:833–848. https://doi.org/10.1007/s00299-018-2272-y
Yan A, Chen Z (2019) Impacts of silver nanoparticles on plants: A focus on the phytotoxicity and underlying mechanism. International Journal of Molecular Sciences 20:23–25. https://doi.org/10.3390/ijms20051003
Zhang CL, Jiang HS, Gu SP, Zhou XH, Lu ZW, Kang XH, Yin L, Huang J (2019) Combination analysis of the physiology and transcriptome provides insights into the mechanism of silver nanoparticles phytotoxicity. Environmental Pollution 252:1539–1549. https://doi.org/10.1016/j.envpol.2019.06.032
Zhang L, Wei Y, Wang H, Wu F, Zhao Y, Liu X, Wu H, Wang L, Su H (2020) Green synthesis of silver nanoparticles using mushroom Flammulina velutipes extract and their antibacterial activity against aquatic pathogens. Food Bioprocess Techn 13:1908–1917. https://doi.org/10.1007/s11947-020-02533-7
Zhou M, Diwu Z, Panchuk-Voloshina N, Haugland RP (1997) A Stable Nonfluorescent Derivative of Resorufin for the Fluorometric Determination of Trace Hydrogen Peroxide: Applications in Detecting the Activity of Phagocyte NADPH Oxidase and Other Oxidases. Analytical Biochemistry 253:162–168. https://doi.org/10.1006/abio.1997.2391
Funding
This work was supported by grant #2018/0458-6 and #2010/50186-5, São Paulo Research Foundation (FAPESP) and grant #404707/2018-1 National Council for Scientific and Technological Development (CNPq) and also for the scholarship granted to ABSZ by CAPES.
Author information
Authors and Affiliations
Contributions
ABSZ: conducting the experiments, analysis and interpretation of the data. CAO: conception and design, drafting the manuscript, provision of materials. CNC: analysis and data interpretation, technical support, collection and assembly data. OJGA: drafting of the article, data analysis and interpretation of morpho-anatomical analysis, AOS: critical revision of the article, obtaining of funding, provision of study materials. MCLN: conception and design, analysis and interpretation, obtaining funding, provision of materials, writing-reviewing, and editing. All authors approved the manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Competing interests
The authors declare that they have no competing interests.
Additional information
Responsible Editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ziotti, A.B.S., Ottoni, C.A., Correa, C.N. et al. Differential physiological responses of a biogenic silver nanoparticle and its production matrix silver nitrate in Sorghum bicolor. Environ Sci Pollut Res 28, 32669–32682 (2021). https://doi.org/10.1007/s11356-021-13069-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-13069-4