Abstract
Environmental concern related to Ag+ release from conventional AgNPs is expected to be prevented once contained into a magnetic core like magnetite or CoFe2O4. Accordingly, we obtained CoFe2O4 NPs by microwave-assisted synthesis, which AgNO3 addition rendered Ag@CoFe2O4 NPs. NPs were characterized, and before exploring potential applications, we carried out 7-day wheat toxicity assays. Seed germination and seedling growth were used as toxicity endpoints and photosynthetic pigments and antioxidant enzymes as oxidative stress biomarkers. Total Fe, Co, and Ag determination was initial indicative of Ag@CoFe2O4 NPs uptake by plants. Then NPs localization in seedling tissues was sought by scanning electron microscopy (SEM) and darkfield hyperspectral imaging (DF-HSI). Not any silver ion (Ag+) was detected into the ferrite structure, but results only confirmed the presence of metallic silver (Ag0) adsorbed on the CoFe2O4 NPs surface. Agglomerates of Ag@CoFe2O4 NPs (~10 nm) were fivefold smaller than CoFe2O4 NPs, and ferrimagnetic properties of the CoFe2O4 NPs were conserved after the formation of the Ag@CoFe2O4 composite NPs. Seed germination was not affected by NPs, but root and shoot lengths of seedlings diminished 50% at 54.89 mg/kg and 168.18 mg/kg NPs, respectively. Nonetheless, hormesis was observed in roots of plants exposed to lower Ag@CoFe2O4 NPs treatments. Photosynthetic pigments and the antioxidant enzymes catalase (CAT), superoxide dismutase (SOD), guaiacol peroxidase (GPX), and ascorbate peroxidase (APX) indicated oxidative damage by reactive oxygen species (ROS) generation. SEM suggested NPs presence in shoots and roots, whereas DF-HSI confirmed some Ag@CoFe2O4 NPs contained in shoots of wheat plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adhikari T, Kundu S, Corporation S, Biswas AK, Tarafdar JC (2012) Effect of copper oxide nano particle on seed germination of selected crops. J Agric Sci Technol A2(June):815–823
Aebi H (1984) Catalase in vitro. Methods Enzymol 105(1947):121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Avellan A, Schwab F, Masion A, Chaurand P, Borschneck D, Vidal V, Rose J, Santaella C, Levard C (2017) Nanoparticle uptake in plants: gold nanomaterial localized in roots of Arabidopsis thaliana by X-ray computed nanotomography and hyperspectral Imaging. Environ Sci Technol 51:8682–8691. https://doi.org/10.1021/acs.est.7b01133
Avellan A, Yun J, Zhang Y, Spielman-Sun E, Unrine JM, Thieme J, Li J, Lombi E, Bland G, Lowry GV (2019) Nanoparticle size and coating chemistry control foliar uptake pathways, translocation, and leaf-to-rhizosphere transport in wheat. ACS Nano 13(5):5291–5305. https://doi.org/10.1021/acsnano.8b09781
Bao D, Oh ZG, Chen Z (2016) Characterization of silver nanoparticles internalized by arabidopsis plants using single particle ICP-MS Analysis. Front Plant Sci 7(February):1–8. https://doi.org/10.3389/fpls.2016.00032
Bensebaa F, Zavaliche F, L’Ecuyer P, Cochrane RW, Veres T (2004) Microwave synthesis and characterization of co-ferrite nanoparticles. J Colloid Interface Sci 277(1):104–110. https://doi.org/10.1016/j.jcis.2004.04.016
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci TRPSC–1207:1–8. https://doi.org/10.1016/j.tplants.2014.07.005
Calabrese E, Baldwin L (1997) The dose determines the stimulation (and poison): development of a chemical hormesis database. Int J Toxicol 16:545–559. https://doi.org/10.1080/109158197226874
Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157(1):42–48. https://doi.org/10.1016/j.envpol.2008.07.028
Chaoui A, Mazhoudi S, Ghorbal MH, El Ferjani E (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127(2):139–147. https://doi.org/10.1016/S0168-9452(97)00115-5
Chapman PM (2002) Ecological risk assessment (ERA) and hormesis.pdf. Sci Total Environ 288(May 2001):131–140. https://doi.org/10.1016/S0048-9697(01)01120-2
Cox A, Venkatachalam P, Sahi S, Sharma N (2016) Plant physiology and biochemistry silver and titanium dioxide nanoparticle toxicity in plants : a review of current research. Plant Physiol Biochem 107:147–163. https://doi.org/10.1016/j.plaphy.2016.05.022
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2(December):1–13. https://doi.org/10.3389/fenvs.2014.00053
Dazy M, Béraud E, Cotelle S, Meux E, Masfaraud JF, Férard JF (2008) Antioxidant enzyme activities as affected by trivalent and hexavalent chromium species in Fontinalis antipyretica Hedw. Chemosphere 73(3):281–290. https://doi.org/10.1016/j.chemosphere.2008.06.044
Dimkpa CO, McLean JE, Martineau N, Britt DW, Haverkamp R, Anderson AJ (2013) S Silver nanoparticles disrupt wheat (Triticum aestivum L.) growth in a sand matrix. Environ Sci Technol 47(2):1082–1090. https://doi.org/10.1021/es302973y
Du J, Tang J, Xu S, Ge J, Dong Y, Li H, Jin M (2018a) A review on silver nanoparticles-induced ecotoxicity and the underlying toxicity mechanisms. Regul Toxicol Pharmacol 98(July):231–239. https://doi.org/10.1016/j.yrtph.2018.08.003
Du W, Xu Y, Yin Y, Ji R, Guo H (2018b) Risk assessment of engineered nanoparticles and other contaminants in terrestrial plants. Curr Opin Environ Sci Health 6:21–28. https://doi.org/10.1016/j.coesh.2018.07.010
El-Temsah YS, Joner EJ (2012) Ecotoxicological effects on earthworms of fresh and aged nano-sized zero-valent iron (nZVI) in soil. Chemosphere 89(1):76–82. 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 Physiol Plant 39:155–113. https://doi.org/10.1007/s11738-017-2452-3
García-Limones C, Hervás A, Navas-Cortés JA, Jiménez-Daíz RM, Tena M (2002) Induction of an antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp.ciceris. Physiol Mol Plant Pathol 61:325–337. https://doi.org/10.1006/pmpp.2003.0445
Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, Reuel NF, Hilmer AJ, Sen F, Brew JA (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13(4):400–408. https://doi.org/10.1038/nmat3890
Hamilton MA, Russo RC, Thurston RV (1977) Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol 11(7):714–719. https://doi.org/10.1021/es60130a004
Hara S, Aisu J, Kato M, Aono T, Sugawa K, Takase K, Otsuki J, Shimizu S, Ikake H (2018) One-pot synthesis of monodisperse CoFe2O4@Ag core-shell nanoparticles and their characterization. Nanoscale Res Lett 13:176. https://doi.org/10.1186/s11671-018-2544-z
Kooti M, Saiahi S, Motamedi H (2013) Fabrication of silver-coated cobalt ferrite nanocomposite and the study of its antibacterial activity. J Magn Magn Mater 333:138–143. https://doi.org/10.1016/j.jmmm.2012.12.038
Kraemer SM, Crowley DE, Kretzschmar R (2006) Geochemical aspects of phytosiderophore-promoted iron acquisition by plants. Adv Agron 91:1–46. https://doi.org/10.1016/S0065-2113(06)91001-3
Kumar V, Sharma M, Khare T, Wani SH (2017) Impact of nanoparticles on oxidative stress and responsive antioxidative defense in Plants. Nanomater Plants Algae Microorganisms 1:393–406. https://doi.org/10.1016/B978-0-12-811487-2.00017-7
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(5):491–499. https://doi.org/10.1016/j.chemosphere.2011.10.013
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Liu D, Zou J, Wang M, Jiang W (2008) Hexavalent chromium uptake and its effects on mineral uptake, antioxidant defence system and photosynthesis in Amaranthus viridis L. Bioresour Technol 99(7):2628–2636. https://doi.org/10.1016/j.biortech.2007.04.045
López-Luna J, Silva-Silva MJ, Martinez-Vargas S, Mijangos-Ricardez OF, González-Chávez MC, Solís-Domínguez FA, Cuevas-Díaz MC (2016) Magnetite nanoparticle (NP) uptake by wheat plants and its effect on cadmium and chromium toxicological behavior. Sci Total Environ 565:941–950. https://doi.org/10.1016/j.scitotenv.2016.01.029
López-Luna J, Camacho-Martínez MM, Solís-Domínguez FA, González-Chávez MC, Carrillo-González R, Martinez-Vargas S, Mijangos-Ricardez OF, Cuevas-Díaz MC (2018) Toxicity assessment of cobalt ferrite nanoparticles on wheat plants. J Toxicol Environ Health A Curr Issues. https://doi.org/10.1080/15287394.2018.1469060
López-Moreno ML, Lugo L, Guzmán N, Álamo B, Perales O, Cedeno-Mattei Y, Román F (2016) Effect of cobalt ferrite (CoFe2O4) nanoparticles on the growth and development of Lycopersicon lycopersicum (tomato plants). Sci Total Environ 550:45–52. https://doi.org/10.1016/j.scitotenv.2016.01.063
Martinez-Vargas S, Martínez AI, Hernández-Beteta EE, Mijangos-Ricardez OF, Vázquez-Hipólito V, Patiño-Carachure C, Hernandez-Flores H, López-Luna J (2017) Arsenic adsorption on cobalt and manganese ferrite nanoparticles. J Mater Sci 52(11):6205–6215. https://doi.org/10.1007/s10853-017-0852-9
Massart R (1981) Preparation of aqueous magnetic liquids in alkaline and acidic media. IEEE Trans Magn 17(2):1247–1248. https://doi.org/10.1109/TMAG.1981.1061188
McClean RG, Schofield MA, Kean WF, Sommer CV, Robertson DP, Toth D, Gajdardziska-Josifovska M (2001) Botanical iron minerals correlation between nanocrystal structure and modes of biological self-assembly. Eur J Mineral 13:1235–1242. https://doi.org/10.1127/0935-1221/2001/0013-1235
Melegari SP, Perreault F, Costa RHR, Popovic R, Matias WG (2013) Evaluation of toxicity and oxidative stress induced by copper oxide nanoparticles in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 142–143:431–440. https://doi.org/10.1016/j.aquatox.2013.09.015
OECD (2003) OECD guideline for the testing of chemicals terrestrial plant test: vegetative vigour test. Terrestrial plant test: vegetative vigour test. OECD Guidelines for the Testing of Chemicals, (September), pp 1–21
Pradas Del Real AE, Vidal V, Carrière M, Castillo-Michel H, Levard C, Chaurand P, Sarret G (2017) A complex interplay. Environ Sci Technol 51(10):5774–5782. https://doi.org/10.1021/acs.est.7b00422
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 (China) 25(9):1947–1955. https://doi.org/10.1016/S1001-0742(12)60301-5
Qiu-Fang Z, Yuan-Yuan L, Cai-Hong P, Cong-Ming L, Bao-Shan W (2005) NaCl enhances thylakoid-bound SOD activity in the leaves of C3 halophyte Suaeda salsa L. Plant Sci 168(2):423–430. https://doi.org/10.1016/j.plantsci.2004.09.002
Rǎcuciu M, Creangǎ DE (2009) Biocompatible magnetic fluid nanoparticles internalized in vegetal tissue. Rom Rep Phys 54(1–2):115–124
Rezvani N, Sorooshzadeh A, Farhadi N (2012) Effect of nano-silver on growth of saffron in flooding stress. World Acad Sci Eng Technol 6(1):517–522
Rico CM, Peralta-Videa JR, Gardea-Torresdey JL (2015) Chemistry, biochemistry of nanoparticles, and their role in antioxidant defense system in plants. Nanotechnol Plant Sci:1–17. https://doi.org/10.1007/978-3-319-14502-0_1
Römheld V, Marschner H (1986) Mobilization of iron in the rhizosphere of different plant species. In: Tinker B, Läuchli A (eds) Advances in plant nutrition, vol 2. Praeger Scientific, New York, pp 155–204
Roy S, Sen CK, Hänninen O (1996) Monitoring of polycyclic aromatic hydrocarbons using ‘moss bags’: bioaccumulation and responses of antioxidant enzymes in Fontinalis antipyretica Hedw. Chemosphere 32(12):2305–2315. https://doi.org/10.1016/0045-6535(96)00139-7
Sarvendra-Kumar, Patra AK, Datta SC, Rosin KG, Purakayastha TJ (2015) Phytotoxicity of nanoparticles to seed germination of plants. Int J Adv Res 3(3):854–865
Shannahan HJ, Podila R, Brown MJ (2015) A hyperspectral and toxicological analysis of protein corona impact on silver nanoparticle properties, intracellular modifications, and macrophage activation. Int J Nanomedicine 10:6509–6521. https://doi.org/10.2147/IJN.S92570
Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Associates Inc, Sunderland 764 pp
Tripathi DK, Shweta, Singh S, Singh S, Pandey R, Singh VP, Sharma NC, Prasad SM, Dubey NK, Chauhan DK (2017) An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiol Biochem 110:2–12. https://doi.org/10.1016/j.plaphy.2016.07.030
USEPA (1994). Determination of metals and trace elements in water and wastes by inductively coupled plasma-atomic spectrometry. EPA Method 200.7. U.S. Environmental Protection Agency., 4, 1–58
USEPA (1996a). Ecological effects test guidelines. Seed germination/root elongation toxicity test. U.S. Environmental Protection Agency, 712-C-96–1 (April)
USEPA (1996b) Method 3052, Microwave assisted acid digestion of siliceous and organically based matrices. U.S. Environmental Protection Agency, 1–20 (December)
Wang H, Kou X, Pei Z, Xiao JQ, Shan X, Xing B (2011) Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L.) and pumpkin (Cucurbita mixta) plants. Nanotoxicology 5(1):30–42. https://doi.org/10.3109/17435390.2010.489206
Wang WP, Yang H, Xian T, Jiang JL (2012) XPS and magnetic properties of CoFe2O4 nanoparticles synthesized by a polyacrylamide gel route. Mater Trans 53:1586–1589. https://doi.org/10.2320/matertrans.M2012151
Wu H, Tito N, Giraldo JP (2017) Anionic cerium oxide nanoparticles protect plant photosynthesis from abiotic stress by scavenging reactive oxygen species. ACS Nano 11(11):11283–11297. https://doi.org/10.1021/acsnano.7b05723
Xu J, Chang Y, Zhang Y, Mab S, Qub Y, Xu C (2008) Effect of silver ions on the structure of ZnO and photocatalytic performance of Ag/ZnO composites. Appl Surf Sci 255:1996–1999. https://doi.org/10.1016/j.apsusc.2008.06.130
Yang J, Cao W, Rui Y (2017) Interactions between nanoparticles and plants: phytotoxicity and defense mechanisms. J Plant Interact 12(1):158–169. https://doi.org/10.1080/17429145.2017.1310944
Zhang S, Niu H, Cai Y, Zhao X, Shi Y (2010) Arsenite and arsenate adsorption on coprecipitated bimetal oxide magnetic nanomaterials: MnFe2O4 and CoFe2O4. Chem Eng J 158(3):599–607. https://doi.org/10.1016/j.cej.2010.02.013
Zia-ur-Rehman M, Naeem A, Khalid H, Rizwan M, Ali S, Azhar M (2017) Responses of plants to iron oxide nanoparticles. In: Nanomaterials in plants, algae, and microorganisms. Elsevier Inc., Amsterdam. https://doi.org/10.1016/B978-0-12-811487-2.00010-4
Acknowledgments
The authors gratefully acknowledge Miguel Bautista for ICP-OES technical support and Omar López for graphical help.
Funding
This work was financially supported by SEP-CONACYT CB-2012-01-181592.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict(s) of interest.
Additional information
Responsible editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Fig. S1
Hyperspectral Microscopy Imaging and Analysis of shoot transverse sections of wheat seedlings exposed to Ag@CoFe2O4 NPs. a) Enhanced Darkfield Optical Image (60X) of the NPs sample. b) Spectral library of Ag@CoFe2O4 NPs. c) Enhanced Darkfield Optical Image (60X) of control wheat seedling where the Ag@CoFe2O4 NPs spectral library was applied. d) Hyperspectral Image (60X) of control wheat seedling. (PNG 4076 kb)
Fig. S2
Hyperspectral Microscopy Imaging and Analysis of shoot transverse sections of wheat seedlings exposed to Ag@CoFe2O4 NPs. a) Enhanced Darkfield Optical Image (60X) of wheat seedling under NPs exposure. b) Hyperspectral Image (60X) of wheat seedling under NPs exposure where the Ag@CoFe2O4 spectral library was applied. c) Hyperspectral Image (60X) of wheat seedling under NPs exposure where pixels that matched the Ag@CoFe2O4 spectral library are mapped in red. d) Hyperspectral Image (60X) of wheat seedling under NPs exposure with sample layer removed, where the pixels mapped in red can be easily visualized. (PNG 3802 kb)
Rights and permissions
About this article
Cite this article
López-Luna, J., Cruz-Fernández, S., Mills, D.S. et al. Phytotoxicity and upper localization of Ag@CoFe2O4 nanoparticles in wheat plants. Environ Sci Pollut Res 27, 1923–1940 (2020). https://doi.org/10.1007/s11356-019-06668-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-06668-9