Article pubs.acs.org/est
Copper Oxide Nanoparticle Foliar Uptake, Phytotoxicity, and Consequences for Sustainable Urban Agriculture TianTian Xiong,† Camille Dumat,‡,§ Vincent Dappe,∥ Hervé Vezin,∥ Eva Schreck,⊥ Muhammad Shahid,# Antoine Pierart,@ and Sophie Sobanska*,∥,∇ †
School of Life Science, South China Normal University, No. 55 Zhongshan Avenue West, Tianhe District, Guangzhou 510631, P. R. China ‡ Université de Toulouse, INP-ENSAT, Av. Agrobiopole, 31326 Castanet-Tolosan, France § Certop UMR5044-Centre d’Etude et de Recherche Travail Organisation Pouvoir, Université Toulouse J. Jaurès-Toulouse II, 5 allée Antonio Machado, 31058 Toulouse Cedex 9, France ∥ LASIR, UMR CNRS 8516, Université Lille 1, Bât. C5, 59655 Villeneuve d’Ascq, France ⊥ Géosciences Environnement Toulouse (GET), Observatoire Midi Pyrénées, Université de Toulouse, CNRS, IRD, 14 avenue E. Belin, F-31400 Toulouse, France # Department of Environmental Sciences, COMSATS Institute of Information Technology, Vehari 61100, Pakistan @ Environmental Science and Biochemistry Ecotoxicology Laboratory, University of Castilla-La Mancha, Toledo, Spain S Supporting Information *
ABSTRACT: Throughout the world, urban agriculture supplies fresh local vegetables to city populations. However, the increasing anthropogenic uses of metal-containing nanoparticles (NPs) such as CuO-NPs in urban areas may contaminate vegetables through foliar uptake. This study focused on the CuO-NP transfer processes in leafy edible vegetables (i.e., lettuce and cabbage) to assess their potential phytotoxicity. Vegetables were exposed via leaves for 5, 10, or 15 days to various concentrations of CuO-NPs (0, 10, or 250 mg per plant). Biomass and gas exchange values were determined in relation to the Cu uptake rate, localization, and Cu speciation within the plant tissues. High foliar Cu uptake occurred after exposure for 15 days for lettuce [3773 mg (kg of dry weight)−1] and cabbage [4448 mg (kg of dry weight)−1], along with (i) decreased plant weight, net photosynthesis level, and water content and (ii) necrotic Curich areas near deformed stomata containing CuO-NPs observed by scanning electron microscopy and energy dispersive X-ray microanalysis. Analysis of the CuO-NP transfer rate (7.8−242 μg day−1), translocation of Cu from leaves to roots and Cu speciation biotransformation in leaf tissues using electron paramagnetic resonance, suggests the involvement of plant Cu regulation processes. Finally, a potential health risk associated with consumption of vegetables contaminated with CuO-NPs was highlighted.
1. INTRODUCTION In urban agriculture (UA), plants are grown and animals are raised for food and other uses within and around cities and towns (i.e., intra- or peri-urban area). UA also includes related activities such as the production and delivery of inputs and the processing and marketing of products.1 UA has emerged and become popular with the rapid development of cities around the world and is an integral part of urban economical, social, and ecological systems. However, the contribution of UA to food security and healthy nutrition is probably its most important asset. The main health risk associated with UA is crop contamination with chemicals, including pesticides and metal(loid)s emitted by the numerous anthropogenic activities that have been performed in urban areas for centuries.2−5 Indeed, soil, water, and air pollution from traffic and/or industrial emissions as well as individual UA practices can seriously degrade cultivated plant quality. © XXXX American Chemical Society
CuO nanoparticles (CuO-NPs) are widely used in many agricultural applications such as pesticides, herbicides, fertilizers, additives for soil remediation, and growth regulators.6−9 Although copper is an essential element, the widespread use of CuO-NPs provides a significant gateway into the atmosphere, soil, and water, and there are concerns about the impacts that these materials might have on crops.10 Vegetables may be contaminated with CuO-NPs via roots in contaminated soils and/or foliar transfer. Most previous studies were focused on root or seed exposure.11,12 Although atmospheric pollution has recently been considered as a significant route for vegetable Received: Revised: Accepted: Published: A
January 3, 2017 March 13, 2017 April 6, 2017 April 6, 2017 DOI: 10.1021/acs.est.6b05546 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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Environmental Science & Technology
surfaces were estimated to be 0, 6.81 ± 0.9, and 218.75 ± 15 mg for 0, 10, and 250 mg, respectively, corresponding to a quantity of CuO-NPs per area of ∼0, ∼0.62, and ∼19.9 mg/ cm2 of leaf surface, respectively. During the exposure period of 3 weeks, a geotextile membrane was placed on the soil surface to prevent soil contamination and soil−plant transfer as previously described and validated.15,28 Five replicates were performed for each treatment. 2.2. Accumulation of Metal in Plant Tissues. Sample preparation for assessing metal transfer and accumulation within plants was explained elsewhere14,15,29,30 and is briefly summarized here. After being harvested, roots and shoots were separated and washed with deionized water to remove deposited particles. Plant tissues were oven-dried at 40 °C for 3 days, weighed, ground, and then sieved to TDI).79 On the other hand, other studies such as that conducted in the vicinity of an industrial zone in Jiangsu, China (16.9 μg kg−1 day−1 < TDI),80 found very low human levels of exposure to Cu. Regardless, adverse human health effects caused by Cu exposure are likely to happen in our study, even if no pronounced adverse effects on plant morphology were observed for L10 and C10. Lastly, the calculated MDI values for L10, L250, C10, and C250 ranged from 0.3 to 6.7 g od dry weight day−1, and these values can be easily reached by adult vegetable consumption. These results give slight insight into the current scenario of food crop contamination via foliar transfer in (peri)urban areas and possible health risks for high levels of Cu that have been accumulated in plants as nanoparticles. Several recent scientific reports about the bioaccessibility of microsized metal particles in plants found that only a portion of the total metal fraction was bioaccessible. Thus, further Cu bioaccessibility measurements on various vegetable samples could be used to refine the assessment of the potential risks associated with human exposure.
Figure 4. Experimental EPR spectra of (a) L0, (b) L10 at T5 and (c) T15, and L250 at (d) T5 and (E) T15. Lettuce exposed to CuO-NPs (0, 10, and 250 mg) is defined as L0, L10, and L250, respectively, and at exposure times (5 and 15 days) is defined as T5 and T15, respectively.
reported that CuO-NPs are expected to dissolve in an undersaturated solution at neutral to basic pH,67 which would then favor the formation of organic complexes such as Cu(II)− organic complexes when the exposure time and dose increase. This suggests that CuO-NP internalization, likely through stomatal openings, would result from biological processes, which would first induce CuO-NP solubilization and Cu complex formation, which is clearly observed by EPR. Thus, in cultivated vegetable leaves exposed to atmospheric CuO-NPs, they may accumulate as CuO that is partially transformed as Cu(II)−organic complexes in the plant tissues. Finally, EPR analysis demonstrated the relationship between quinoid radicals at decreasing Mn levels together with increasing growth times and Cu(II) concentrations. The radical decrease accompanied by the decrease in the Mn signal intensity reflects the photosynthetic inhibiting effect of Cu(II) because Cu2+ inhibited photosynthetic evolution through the replacement of Mn ions.68 Moreover, EPR analysis suggests electron transfer involving Mn together with a Cu(II)-to-Cu(I) reduction, which indirectly shows the CuO-NP-induced oxidative stress. However, further unambiguous assignments could not be made from our EPR data. Overall, excess Cu has a high threat score (CdOCdCl2 > CuO > PbO > ZnO > PbSO4 > Sb2O3), cytotoxicity, and oxidative potential, despite being an essential element.24 Indeed, CuO-NPs could significantly accumulate in plants and then influence plant growth, the net photosynthesis rate, the content of nutritional elements, and antioxidant enzyme activities and even lead to DNA damage.10,69,70 Cu can transfer G
DOI: 10.1021/acs.est.6b05546 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.6b05546. Typical Raman spectra of particles observed on a leaf surface (Figure S1), optical images of CuO-NPs within stomata and necrosis (Figures S2 and S3), EPR parameters, i.e., A∥/g∥, measured for contaminated leaves and compared to the values reported in the literature (Figure S4), composition of the nutrient solution (Table S1), partial correlation coefficients between growth parameters and exposure conditions (Table S2), mean Cu concentrations in leaves and roots of lettuce and cabbage as a function of exposure time and CuO-NP content deposited on leaves and the corresponding translocation factors (TFs) (Table S3), and estimated daily intake of pollutant (EDI) and maximal allowable daily intake of contaminated plants (MDI) (Table S4) (PDF)
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Phone: +33 5 4000 31 88. ORCID
Hervé Vezin: 0000-0002-7282-2703 Sophie Sobanska: 0000-0002-3264-3938 Present Address ∇
S.S.: Institut des Sciences Moleculaires, UMR CNRS 5255, Université de Bordeaux, 351 cours de la liberation, A12, 33405 Talence, France. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was supported by the National Research Agency (ANR-12-0011-VBDU), the French Agency of Sustainable Development and Energy (ADEME, DIMENSION Project), the Institut de REcherche en ENvironnement Industriel (IRENI) program, and Region Hauts de France-Nord Pas de Calais Picardie.
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DOI: 10.1021/acs.est.6b05546 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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DOI: 10.1021/acs.est.6b05546 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
