Copper oxide nanoparticle foliar uptake, phytotoxicity and

1School of Life Science, South China Normal University, No.55 Zhongshan ... 3Certop UMR5044-Centre d'Etude et de Recherche Travail Organisation ... 2...
0 downloads 0 Views 4MB Size
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

Article

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 (CdOCdCl2 > 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

Article

Environmental Science & Technology



(6) Weitz, I. S.; Maoz, M.; Panitz, D.; Eichler, S.; Segal, E. Combination of CuO nanoparticles and fluconazole: preparation, characterization, and antifungal activity against Candida albicans. J. Nanopart. Res. 2015, 17 (8), 342. (7) Gogos, A.; Knauer, K.; Bucheli, T. D. Nanomaterials in Plant Protection and Fertilization: Current State, Foreseen Applications, and Research Priorities Foreseen Applications, and Research Priorities. J. Agric. Food Chem. 2012, 60, 9781−9792. (8) Du, W.; Tan, W.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L.; Ji, R.; Yin, Y.; Guo, H. Interaction of metal oxide nanoparticles with higher terrestrial plants: Physiological and biochemical aspects. Plant Physiol. Biochem. 2017, 110, 210−225. (9) Zhu, Q.; Zhang, M.; Ma, Q. Copper-based foliar fertilizer and controlled release urea improved soil chemical properties, plant growth and yield of tomato. Sci. Hortic. (Amsterdam, Neth.) 2012, 143, 109− 114. (10) Hong, J.; Wang, L.; Sun, Y.; Zhao, L.; Niu, G.; Tan, W.; Rico, C. M.; Peralta-videa, J. R.; Gardea-torresdey, J. L. Foliar applied nanoscale and microscale CeO2 and CuO alter cucumber (Cucumis sativus) fruit quality. Sci. Total Environ. 2016, 563−564, 904−911. (11) Ge, Y.; Murray, P.; Hendershot, W. H. Trace metal speciation and bioavailability in urban soils. Environ. Pollut. 2000, 107 (1), 137− 144. (12) Wang, Z.; Xu, L.; Zhao, J.; Wang, X.; White, J. C.; Xing, B. CuO Nanoparticle Interaction with Arabidopsis thaliana: Toxicity, ParentProgeny Transfer, and Gene Expression. Environ. Sci. Technol. 2016, 50 (11), 6008−6016. (13) Tomasević, M.; Vukmirović, Z.; Rajsić, S.; Tasić, M.; Stevanović, B. Characterization of trace metal particles deposited on some deciduous tree leaves in an urban area. Chemosphere 2005, 61 (6), 753−760. (14) Uzu, G.; Sobanska, S.; Sarret, G.; Muñoz, M.; Dumat, C. Foliar lead uptake by lettuce exposed to atmospheric fallouts. Environ. Sci. Technol. 2010, 44 (3), 1036−1042. (15) Xiong, T. T.; Leveque, T.; Austruy, A.; Goix, S.; Schreck, E.; Dappe, V.; Sobanska, S.; Foucault, Y.; Dumat, C. Foliar uptake and metal(loid) bioaccessibility in vegetables exposed to particulate matter. Environ. Geochem. Health 2014, 36 (5), 897−909. (16) Prusty, B. A. K.; Mishra, P. C.; Azeez, P. A. Dust accumulation and leaf pigment content in vegetation near the national highway at Sambalpur, Orissa, India. Ecotoxicol. Environ. Saf. 2005, 60 (2), 228− 235. (17) Alexander, P. D.; Alloway, B. J.; Dourado, A. M. Genotypic variations in the accumulation of Cd, Cu, Pb and Zn exhibited by six commonly grown vegetables. Environ. Pollut. 2006, 144 (3), 736−745. (18) Wang, Z.; Chen, J.; Chai, L.; Yang, Z.; Huang, S.; Zheng, Y. Environmental impact and site-specific human health risks of chromium in the vicinity of a ferro-alloy manufactory, China. J. Hazard. Mater. 2011, 190 (1−3), 980−985. (19) Tschiersch, J.; Shinonaga, T.; Heuberger, H. Dry deposition of gaseous radioiodine and particulate radiocaesium onto leafy vegetables. Sci. Total Environ. 2009, 407 (21), 5685−5693. (20) Schreck, E.; Foucault, Y.; Sarret, G.; Sobanska, S.; Cécillon, L.; Castrec-Rouelle, M.; Uzu, G.; Dumat, C. Metal and metalloid foliar uptake by various plant species exposed to atmospheric industrial fallout: mechanisms involved for lead. Sci. Total Environ. 2012, 427− 428, 253−262. (21) Mombo, S.; Foucault, Y.; Deola, F.; Gaillard, I.; Goix, S.; Shahid, M.; Schreck, E.; Pierart, A.; Dumat, C. Management of human health risk in the context of kitchen gardens polluted by lead and cadmium near a lead recycling company. J. Soils Sediments 2016, 16, 1214. (22) Uzu, G.; Schreck, E.; Xiong, T.; Macouin, M.; Lévêque, T.; Fayomi, B.; Dumat, C. Urban Market Gardening in Africa: Foliar Uptake of Metal(loid)s and Their Bioaccessibility in Vegetables; Implications in Terms of Health Risks. Water, Air, Soil Pollut. 2014, 225 (11), 2185. (23) Bravin, M. N.; Michaud, A. M.; Larabi, B.; Hinsinger, P. RHIZOtest: a plant-based biotest to account for rhizosphere processes

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)



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.



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.



REFERENCES

(1) Pierart, A.; Shahid, M.; Séjalon-Delmas, N.; Dumat, C. Antimony bioavailability: Knowledge and research perspectives for sustainable agricultures. J. Hazard. Mater. 2015, 289, 219−234. (2) Bonanno, G.; Cirelli, G. L.; Toscano, A.; Lo Giudice, R.; Pavone, P. Heavy metal content in ash of energy crops growing in sewagecontaminated natural wetlands: potential applications in agriculture and forestry? Sci. Total Environ. 2013, 452−453, 349−354. (3) Luo, C.; Liu, C.; Wang, Y.; Liu, X.; Li, F.; Zhang, G.; Li, X. Heavy metal contamination in soils and vegetables near an e-waste processing site, South China. J. Hazard. Mater. 2011, 186 (1), 481−490. (4) Schreck, E.; Laplanche, C.; Le Guédard, M.; Bessoule, J.-J.; Austruy, A.; Xiong, T.; Foucault, Y.; Dumat, C. Influence of fine process particles enriched with metals and metalloids on Lactuca sativa L. leaf fatty acid composition following air and/or soil-plant field exposure. Environ. Pollut. 2013, 179, 242−249. (5) Shahid, M.; Xiong, T.; Castrec-Rouelle, M.; Leveque, T.; Dumat, C. Water extraction kinetics of metals, arsenic and dissolved organic carbon from industrial contaminated poplar leaves. J. Environ. Sci. 2013, 25 (12), 2451−2459. H

DOI: 10.1021/acs.est.6b05546 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology when assessing copper bioavailability. Environ. Pollut. 2010, 158 (10), 3330−3337. (24) Goix, S.; Lévêque, T.; Xiong, T. T.; Schreck, E.; Baeza-Squiban, A.; Geret, F.; Uzu, G.; Austruy, A.; Dumat, C. Environmental and health impacts of fine and ultrafine metallic particles: Assessment of threat scores. Environ. Res. 2014, 133, 185−194. (25) Brunauer, S.; Emmett, P. H.; Teller, E. Adsorption of Gases in Multimolecular Layers. J. Am. Chem. Soc. 1938, 60 (1), 309−319. (26) Adrees, M.; Ali, S.; Rizwan, M.; Ibrahim, M.; Abbas, F.; Farid, M.; Zia-Ur-Rehman, M.; Irshad, M. K.; Bharwana, S. A. The effect of excess copper on growth and physiology of important food crops: a review. Environ. Sci. Pollut. Res. 2015, 22 (11), 8148−8162. (27) Deng, H.; Ye, Z. H.; Wong, M. H. Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metalcontaminated sites in China. Environ. Pollut. 2004, 132 (1), 29−40. (28) Hurtevent, P.; Thiry, Y.; Levchuk, S.; Yoschenko, V.; Henner, P.; Madoz-Escande, C.; Leclerc, E.; Colle, C.; Kashparov, V. Translocation of 125I, 75Se and 36Cl to wheat edible parts following wet foliar contamination under field conditions. J. Environ. Radioact. 2013, 121, 43−54. (29) Hong, J.; Peralta-Videa, J. R.; Rico, C.; Sahi, S.; Viveros, M. N.; Bartonjo, J.; Zhao, L.; Gardea-Torresdey, J. L. Evidence of translocation and physiological impacts of foliar applied CeO2 nanoparticles on cucumber (Cucumis sativus) plants. Environ. Sci. Technol. 2014, 48, 4376−4385. (30) Birbaum, K.; Brogioli, R.; Schellenberg, M.; Martinoia, E.; Stark, W. J.; Günther, D.; Limbach, L. K. No evidence for cerium dioxide nanoparticle translocation in maize plants. Environ. Sci. Technol. 2010, 44 (22), 8718−8723. (31) Xiong, T. T.; Leveque, T.; Shahid, M.; Foucault, Y.; Mombo, S.; Dumat, C. Lead and cadmium phytoavailability and human bioaccessibility for vegetables exposed to soil or atmospheric pollution by process ultrafine particles. J. Environ. Qual. 2014, 43 (5), 1593− 1600. (32) Sharma, R. K.; Agrawal, M.; Marshall, F. M. Heavy metals in vegetables collected from production and market sites of a tropical urban area of India. Food Chem. Toxicol. 2009, 47 (3), 583−591. (33) U.S. Environmental Protection Agency. Integrated Risk Information System (IRIS). http://www.epa.gov/iris/. (34) Schreck, E.; Dappe, V.; Sarret, G.; Sobanska, S.; Nowak, D.; Nowak, J.; Stefaniak, E. A.; Magnin, V.; Ranieri, V.; Dumat, C. Foliar or root exposures to smelter particles: consequences for lead compartmentalization and speciation in plant leaves. Sci. Total Environ. 2014, 476−477, 667−676. (35) Xiong, T. T.; Austruy, A.; Pierart, A.; Shahid, M.; Schreck, E.; Mombo, S.; Dumat, C. Kinetic study of phytotoxicity induced by foliar lead uptake for vegetables exposed to fine particles and implications for sustainable urban agriculture. J. Environ. Sci. (Beijing, China) 2016, 46 (8), 16−27. (36) Yruela, I. Copper in plants: acquisition, transport and interactions. Funct. Plant Biol. 2009, 36 (5), 409−430. (37) Uzu, G.; Sobanska, S.; Aliouane, Y.; Pradere, P.; Dumat, C. Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation. Environ. Pollut. 2009, 157 (4), 1178−1185. (38) Ma, C.; White, J. C.; Dhankher, O. P.; Xing, B. Metal-Based Nanotoxicity and Detoxification Pathways in Higher Plants. Environ. Sci. Technol. 2015, 49 (12), 7109−7122. (39) Zuverza-Mena, N.; Martínez-Fernán dez, D.; Du, W.; Hernandez-Viezcas, J. A.; Bonilla-Bird, N.; López-Moreno, M. L.; Komárek, M.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. Exposure of engineered nanomaterials to plants: Insights into the physiological and biochemical responses-A review. Plant Physiol. Biochem. 2017, 110, 236−264. (40) Uzu, G.; Sauvain, J.-J.; Baeza-Squiban, A.; Riediker, M.; Sánchez Sandoval Hohl, M.; Val, S.; Tack, K.; Denys, S.; Pradère, P.; Dumat, C. In vitro assessment of the pulmonary toxicity and gastric availability of lead-rich particles from a lead recycling plant. Environ. Sci. Technol. 2011, 45 (18), 7888−7895.

(41) Eichert, T.; Kurtz, A.; Steiner, U.; Goldbach, H. E. Size exclusion limits and lateral heterogeneity of the stomatal foliar uptake pathway for aqueous solutes and water-suspended nanoparticles. Physiol. Plant. 2008, 134 (1), 151−160. (42) Larue, C.; Castillo-Michel, H.; Sobanska, S.; Cécillon, L.; Bureau, S.; Barthès, V.; Ouerdane, L.; Carrière, M.; Sarret, G. Foliar exposure of the crop Lactuca sativa to silver nanoparticles: evidence for internalization and changes in Ag speciation. J. Hazard. Mater. 2014, 264, 98−106. (43) Corredor, E.; Testillano, P. S.; Coronado, M.-J.; GonzálezMelendi, P.; Fernández-Pacheco, R.; Marquina, C.; Ibarra, M. R.; de la Fuente, J. M.; Rubiales, D.; Pérez-de-Luque, A.; et al. Nanoparticle penetration and transport in living pumpkin plants: in situ subcellular identification. BMC Plant Biol. 2009, 9 (1), 45. (44) Salim, R.; Al-Subu, M. M.; Atallah, A. Effects of root and foliar treatments with lead, cadmium, and copper on the uptake distribution and growth of radish plants. Environ. Int. 1993, 19 (4), 393−404. (45) Rico, C. M.; Majumdar, S.; Duarte-Gardea, M.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. Interaction of nanoparticles with edible plants and their possible implications in the food chain. J. Agric. Food Chem. 2011, 59 (8), 3485−3498. (46) Capelo, A.; Santos, C.; Loureiro, S.; Pedrosa, M. A. Phytotoxicity of lead on Lactuca sativa: Effects on growth, mineral nutrition, photosynthetic activity and oxidant. Fresenius Environ. Bull. 2012, 21 (2), 450−459. (47) Monteiro, M. S.; Santos, C.; Soares, A. M. V. M; Mann, R. M. Assessment of biomarkers of cadmium stress in lettuce. Ecotoxicol. Environ. Saf. 2009, 72 (3), 811−818. (48) An, Y.-J. Assessment of comparative toxicities of lead and copper using plant assay. Chemosphere 2006, 62 (8), 1359−1365. (49) Losak, T.; Hlusek, J.; Martinec, J.; Jandak, J.; Szostkova, M.; Filipcik, R.; Manasek, J.; Prokes, K.; Peterka, J.; Varga, L.; et al. Nitrogen fertilization does not affect micronutrient uptake in grain maize (Zea mays L.). Acta Agric. Scand., Sect. B 2011, 61 (6), 543−550. (50) An, Y.-J.; Kim, Y.-M.; Kwon, T.-I.; Jeong, S.-W. Combined effect of copper, cadmium, and lead upon Cucumis sativus growth and bioaccumulation. Sci. Total Environ. 2004, 326 (1−3), 85−93. (51) Poschenrieder, C.; Cabot, C.; Martos, S.; Gallego, B.; Barceló, J. Do toxic ions induce hormesis in plants? Plant Sci. 2013, 212, 15−25. (52) Kuzminov, F. I.; Brown, C. M.; Fadeev, V. V.; Gorbunov, M. Y. Effects of metal toxicity on photosynthetic processes in coral symbionts, Symbiodinium spp. J. Exp. Mar. Biol. Ecol. 2013, 446, 216−227. (53) Cambrollé, J.; Mateos-Naranjo, E.; Redondo-Gómez, S.; Luque, T.; Figueroa, M. E. Growth, reproductive and photosynthetic responses to copper in the yellow-horned poppy, Glaucium flavum Crantz. Environ. Exp. Bot. 2011, 71 (1), 57−64. (54) Kupper, H.; Kroneck, P. Heavy metal uptake by plants and cyanobacteria. Met. Ions Biol. Syst. 2005, 44, 97−142. (55) Barceló, J.; Poschenrieder, C. Plant water relations as affected by heavy metal stress: A review. J. Plant Nutr. 1990, 13 (1), 1−37. (56) Xiong, Z.; Wang, H. Copper toxicity and bioaccumulation in Chinese cabbage (Brassica pekinensis Rupr.). Environ. Toxicol. 2005, 20, 188−194. (57) De Carvalho, R. P.; Guedes, K. J.; Pinheiro, M. V. B.; Krambrock, K. Biosorption of copper by dried plant leaves studied by electron paramagnetic resonance and infrared spectroscopy. Hydrometallurgy 2001, 59 (2−3), 407−412. (58) De Carvalho, R. P.; Freitas, J. R.; de Sousa, A.-M. G.; Moreira, R. L.; Pinheiro, M. V. B.; Krambrock, K. Biosorption of copper ions by dried leaves: chemical bonds and site symmetry. Hydrometallurgy 2003, 71 (1−2), 277−283. (59) Labanowska, M.; Filek, M.; Kurdziel, M.; Bidzińska, E.; Miszalski, Z.; Hartikainen, H. EPR spectroscopy as a tool for investigation of differences in radical status in wheat plants of various tolerances to osmotic stress induced by NaCl and PEG-treatment. J. Plant Physiol. 2013, 170 (2), 136−145. I

DOI: 10.1021/acs.est.6b05546 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology (60) Merdy, P.; Guillon, E.; Aplincourt, M.; Dumonceau, J.; Vezin, H. Copper sorption on a straw lignin: experiments and EPR characterization. J. Colloid Interface Sci. 2002, 245 (1), 24−31. (61) Hoffmann, S. K.; Goslar, J.; Ratajczak, I.; Mazela, B. Fixation of copper-protein formulation in wood: Part 2. Molecular mechanism of fixation of copper(II) in cellulose, lignin and wood studied by EPR. Holzforschung 2008, 62 (3), 300−308. (62) Davies, G.; Fataftah, A.; Cherkasskiy, A.; Ghabbour, E. A.; Radwan, A.; Jansen, S. A.; Kolla, S.; Paciolla, M. D.; Sein, L. T., Jr.; Buermann, W.; et al. Tight metal binding by humic acids and its role in biomineralization. J. Chem. Soc., Dalton Trans. 1997, No. 21, 4047− 4060. (63) Guimarães, E.; Mangrich, A. S.; Machado, V. G.; Traghetta, D. G.; Lobo, M. A. Criterious Preparation and Characterization of Earthworm-composts in View of Animal Waste Recycling: Part II. A Synergistic Utilization of EPR and 1H NMR Spectroscopies on the Characterization of Humic Acids from Vermicomposts. J. Braz. Chem. Soc. 2001, 12 (6), 734−741. (64) Flogeac, K.; Guillon, E.; Aplincourt, M. Surface Complexation of Copper(II) on Soil Particles: EPR and XAFS Studies. Environ. Sci. Technol. 2004, 38 (11), 3098−3103. (65) Lamour, E.; Routier, S.; Bernier, J.-L.; Catteau, J.-P.; Bailly, C.; Vezin, H. Oxidation of Cu II to Cu III, Free Radical Production, and DNA Cleavage by Hydroxy-salen−Copper Complexes. Isomeric Effects Studied by ESR and Electrochemistry. J. Am. Chem. Soc. 1999, 121 (9), 1862−1869. (66) Peisach, J.; Blumberg, W. E. Structural implications derived from the analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins. Arch. Biochem. Biophys. 1974, 165 (2), 691− 708. (67) Kent, R. D.; Vikesland, P. J. Dissolution and Persistence of Copper-Based Nanomaterials in Undersaturated Solutions with Respect to Cupric Solid Phases. Environ. Sci. Technol. 2016, 50 (13), 6772−6781. (68) Maksymiec, W. Effect of copper on cellular processes in higher plants. Photosynthetica 1998, 34 (3), 321−342. (69) Rizwan, M.; Ali, S.; Qayyum, M. F.; Ok, Y. S.; Adrees, M.; Ibrahim, M.; Zia-ur-Rehman, M.; Farid, M.; Abbas, F. Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review. J. Hazard. Mater. 2017, 322, 2− 16. (70) Hong, J.; Rico, C. M.; Zhao, L.; Adeleye, A. S.; Keller, A. A.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. Toxic effects of copperbased nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa). Environ. Sci. Process. Impacts 2015, 17 (1), 177−185. (71) Dietz, K. J.; Herth, S. Plant nanotoxicology. Trends Plant Sci. 2011, 16 (11), 582−589. (72) Halliwell, B. Reactive oxygen species in living systems: Source, biochemistry, and role in human disease. Am. J. Med. 1991, 91 (3), S14−S22. (73) Faisal, M.; Saquib, Q.; Alatar, A. A.; Al-Khedhairy, A. A.; Hegazy, A. K.; Musarrat, J. Phytotoxic hazards of NiO-nanoparticles in tomato: a study on mechanism of cell death. J. Hazard. Mater. 2013, 250−251, 318−332. (74) Kozlov, M. V.; Haukioja, E.; Bakhtiarov, a V; Stroganov, D. N.; Zimina, S. N. Root versus canopy uptake of heavy metals by birch in an industrially polluted area: contrasting behaviour of nickel and copper. Environ. Pollut. 2000, 107 (3), 413−420. (75) Cherfi, A.; Abdoun, S.; Gaci, O. Food survey: levels and potential health risks of chromium, lead, zinc and copper content in fruits and vegetables consumed in Algeria. Food Chem. Toxicol. 2014, 70, 48−53. (76) Arnal, N.; de Alaniz, M. J. T.; Marra, C. A. Cytotoxic effects of copper overload on human-derived lung and liver cells in culture. Biochim. Biophys. Acta, Gen. Subj. 2012, 1820 (7), 931−939. (77) Fahmy, B.; Cormier, S. A. Copper oxide nanoparticles induce oxidative stress and cytotoxicity in airway epithelial cells. Toxicol. In Vitro 2009, 23 (7), 1365−1371.

(78) Sharma, R. K.; Agrawal, M.; Marshall, F. M. Heavy metal (Cu, Zn, Cd and Pb) contamination of vegetables in urban India: a case study in Varanasi. Environ. Pollut. 2008, 154 (2), 254−263. (79) Liu, H.; Probst, A.; Liao, B. Metal contamination of soils and crops affected by the Chenzhou lead/zinc mine spill (Hunan, China). Sci. Total Environ. 2005, 339 (1−3), 153−166. (80) Cao, H.; Chen, J.; Zhang, J.; Zhang, H.; Qiao, L.; Men, Y. Heavy metals in rice and garden vegetables and their potential health risks to inhabitants in the vicinity of an industrial zone in Jiangsu, China. J. Environ. Sci. 2010, 22 (11), 1792−1799.

J

DOI: 10.1021/acs.est.6b05546 Environ. Sci. Technol. XXXX, XXX, XXX−XXX