Interactions between CeO2 Nanoparticles and the Desert Plant

Jan 6, 2016 - University of California Center for Environmental Implications of Nanotechnology (UC CEIN), The University of Texas at El Paso,. El Paso...
0 downloads 0 Views 2MB Size
Download PDF
Research Article pubs.acs.org/journal/ascecg

Interactions between CeO2 Nanoparticles and the Desert Plant Mesquite: A Spectroscopy Approach Jose A. Hernandez-Viezcas,†,‡ Hiram Castillo-Michel,⊥ Jose R. Peralta-Videa,†,‡,§ and Jorge L. Gardea-Torresdey*,†,‡,§ †

Chemistry Department and §Environmental Science and Engineering Ph.D. Program, The University of Texas at El Paso, El Paso, Texas 79968, United States ‡ University of California Center for Environmental Implications of Nanotechnology (UC CEIN), The University of Texas at El Paso, El Paso, Texas 79968, United States ⊥ European Synchrotron Radiation Facility, B.P. 220, 38043 Grenoble, France ABSTRACT: Exploring the effects of ecosystem exposure to unusual concentrations of engineered nanoparticles (ENP) is a critical issue in current environmental research. Nanotoxicological studies on plants have focused on model and crop plants, leaving plants from desert ecosystems virtually ignored. This research was designed to explore the interactions between CeO2 ENP and the desert plant mesquite (Prosopis juliflora velutina). Mesquite plantlets were grown for 15 days in a hydroponic CeO2 ENP-nutrient suspension at concentrations ranging from 500 to 4000 mg L−1. Biochemical assays showed that ascorbateperoxidase activity in roots increased when exposed to 2000 and 4000 mg CeO2 L−1; whereas in leaves, catalase presented an increasing trend associated with the external concentration of the ENP. However, mesquite plants exhibited no visible signs of stress. At all CeO2 ENP treatments, the accumulation of Ce in root tissue was much higher (≥79%) than in the aerial part of the plant (≤21%). X-ray absorption near edge structure (XANES) and micro X-ray fluorescence (μ-XRF) showed that most of the Ce was adsorbed in the mesquite root’s epidermis and cortex suggesting passive uptake of the Ce. Lastly, it was determined that Ce in the root remained in the +4 oxidation state and it mostly remained coordinated as CeO2. KEYWORDS: Prosopis, CeO2 nanoparticles, Speciation, XANES, μ-XRF, Uptake, Desert areas

■

soil fertility, water storage, biodiversity, and food sources.8,9 Furthermore, desert plants show adaptation and survival strategies that allows them to endure harsh environments.10 For instance, it has been reported that the leguminous shrub/ tree mesquite (Prosopis spp.) can withstand 10 times greater salinity than soybean; it can also photosynthesize and fix nitrogen at leaf air temperatures of 45 °C.11,12 This desert plant creates a hospitable environment for fauna and pioneering plants by providing food and nutrients under its canopy. This unique adaptation to unforgiving environments suggests desert plants could respond differently to ENP than domesticated crops. To our knowledge only ZnO ENP have been evaluated for phytotoxicity on three desert plant species (Prosopis juliflora velutina, Salsola tragus, and Parkinsonia florida). The authors of the study reported the presence of Zn(II) as well as root size reduction in the three desert species exposed to the ZnO ENP.13,14

INTRODUCTION Advances in nanotechnology have created materials with unique physicochemical properties that have penetrated almost all industrial sectors. Thousands of tonnes of engineered nanoparticles (ENP), the building blocks of nanotechnology, are produced annually to meet the global demand.1 This evolving technology is currently on the forefront of scientific advances and its growth is forecasted to reach $3,000 billion in final goods by 2020.2 Consequently, concerns have been raised about the unknown impact nanotechnology will have on living organisms, because the release of ENP into the environment is unavoidable. Special attention has been given to the interactions between ENP and plants; owing to the association plants have with the predicted sinks of ENP such as air, soil, sediments and aquatic environments.3 Recent reviews documenting nanotoxicological studies on plants have been focused on model and crop plants.4−6 However, there are limited studies dealing with the effects of ENP on desert plants. The world arid/semiarid lands are an integral part of the environment; they comprise 1/3 of the earth surface and are inhabited by nearly 40% of the world’s population.7,8 Plants from arid/semiarid ecosystems promote © XXXX American Chemical Society

Received: October 8, 2015 Revised: December 21, 2015

A

DOI: 10.1021/acssuschemeng.5b01251 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

Research Article

ACS Sustainable Chemistry & Engineering

Stem, leaf, and root tissues were taken from every replicate to determine the catalase (CAT) activity according to a modified antioxidant enzymes assay.30 Briefly, for each sample a ratio of 10% (w/v) was extracted using a glass−glass homogenizer and ice-cold phosphate buffer (25 mM KH2PO4 at pH 7.4). Extracts were centrifuged at 10000 rpm for 5 min at 4C (Eppendorf AG bench centrifuge 5417 R, Hamburg, Germany) and supernatants collected for the assay. A volume of 10 μm from the supernatant was placed in a quartz cuvette in addition to 990 μL of 10 mM H2O2 to obtain a final volume of 1 mL. Subsequently, the cuvette with the sample was mixed and the absorbance recorded during 2 min at 240 nm in a UV/vis spectrometer (PerkinElmer, Uberlinger, Germany). The ascorbate− peroxidase (APOX) enzyme activity was calculated according to Murguia et al.31 with minor modifications. Plant extract and its supernatant were obtained as described above. The supernatant was assayed after centrifugation. A volume of 100 μL of the sample, 886 μL of 0.1 M phosphate buffer (KH2PO4) at pH 7.4, 10 μL of 17 mM H2O2, and 4 μL of 25 mM ascorbate were placed in a 1 mL quartz cuvette and mixed. Absorbance was recorded at 265 nm in a UV/vis spectrometer (PerkinElmer, Uberlinger, Germany). The H2 O2 extinction coefficient was experimentally set at 36.1 mM−1 cm−1. Quantification of Ce and Nutrients in Plant Tissue. All plants were washed with 0.01 M HNO3 and MPW to remove any contaminants. Plants were then sectioned with a scalpel into root, stem, and leaf and dried at 60 °C during 4 days. The nanoceria treated samples were digested using concentrated ultratrace metal grade HNO3 and H2O2 [30% (v/v); 1:4] as described previously with slight modifications and digested using a microwave acceleration reaction system (CEMcorp).32 Samples were diluted 10-fold and analyzed using inductively coupled plasma optical emission spectrometer (ICPOES) (Optima 4300 DV, PerkinElmer). Ten blanks were analyzed to calculate Ce detection limit. Standard Reference Materials from the National institute of standards and technology 1547 and 1570a were used to validate the digestion obtaining recoveries of 95%. For quality control, spikes of Ce, micro-, and macronutrients were analyzed every 15 samples. Limits of detection and quantitation were measured at 1 and 8 μg/L, respectively. MicroXRF and XANES Studies. The distribution of Ce and other elements in the mesquite roots was performed with an incident energy of 5.8 keV during 16-bunch mode at beamline ID21 of the European Synchrotron Radiation Facility (ESRF, Grenoble France).33 The current of the storage ring ranged between 60 and 90 mA operating at 6GeV. The beam was focused with the use of K−B optics to 0.60 × 1.1 μm (V × H) The X-ray fluorescence data were processed using PyMCA software.34 For XANES data acquisition, the energy was selected using a Si(111) monochromator and scanned from 5.70 to 5.80 keV. The final Ce L(III) edge spectra were the sum of 3 individual scans. Each individual spectrum was inspected for beam induced changes, and the samples were stable in all cases. XANES data analysis was carried out using Athena software.35 Statistics. The data reported for the quantification of Ce and CAT/APOX enzyme activity are averages of three replicates ± standard errors (SE). For Ce uptake values, a one-way ANOVA test was performed followed by Tukey-HSD (honestly significant difference). For CAT/APOX enzyme activity, a one-way ANOVA test was performed. All tests were performed with the statistical package SPSS Version 12.0 (SPSS, Chicago, IL, USA). In all cases, the statistical significance was calculated on a probability of p < 0.05.

Cerium dioxide (CeO2) ENP (nanoceria) are widely used as a catalyst for internal combustion due to its high oxygen storage capacity and as a polishing agent in chemical mechanical planarization.1,15 In addition, its UV absorbing potential makes nanoceria a prevalent ingredient in personal care products.1,16 Cerium oxide ENP can access soils through atmospheric routes. A recent review by Collin et al. estimated that nanoceria final sink will be landfills, air, soil and water in that order.17 Several studies on crop plants such as cucumber, tomato, kidney bean, rice, alfalfa, soybean, wheat, sunflower, coriander, and corn have evaluated the fate, transport, and phytotoxicity of CeO2 ENPs.18−28 Zhao et. al used micro X-ray fluorescence (μXRF) in order to evaluate the presence of CeO2 ENP in corn tissue.27 Similar synchrotron techniques in addition to X-ray absorption near edge structure (XANES) were used by Zhang and co-workers to corroborate the translocation and biotransformation of CeO2 ENP in cucumber tissue.19 Conversely, studies using CeO2 ENP foliar exposure on corn found the ENP adsorbed in the leaves but no evidence of translocation.23 The fate and effects on crop plants differ depending on the species and the CeO2 ENP concentration. Studies have reported the adverse effect CeO2 ENP have on the nutritional properties and nitrogen fixation of cilantro and soybean respectively whereas other reports show positive root grow in alfalfa, corn, and tomato.20,24−26 Therefore, it is impossible to infer the effect ENP will have on all plants species based on crop studies. Accordingly, it is necessary to understand the effect CeO2 ENP and other ENP have on desert plants. In this study, a hydroponic experiment under controlled conditions, with a high range of CeO2 ENP concentrations, was used to assess the phytotoxicity, distribution, and ENP oxidation state in the desert plant mesquite. Spectroscopic techniques were used to localize and evaluate the ENP in the plant and biochemical assays were performed to examine the stress induced by the CeO2 ENP.

■

EXPERIMENTAL SECTION

Preparation of Nanoparticle Suspension. The CeO2 ENP (ceria cubic, rods ≈8 × 67 nm, 93.8 m2 g−1, 95.14% purity) were purchased from Meliorum Technologies (Rochester, NY). Further characterization has been described elsewhere.29 Suspensions at concentrations of 0, 500, 1000, 2000, and 4000 mg CeO2 ENP/L were created in a modified Hoagland nutrient solution (mHNS). Mixtures were stirred for 5 min; afterward, direct sonication (130W, 20 kHz) was used for 30 min in an ice bath to avoid agglomeration. All suspensions were prepared the same day of the experimental setup and adjusted to pH 5.8. Mesquite Germination and Nanoparticle Exposure. Mesquite seeds from the variety Prosopis juliflora velutina were purchased from Granite seed (Lehi, UT). Seeds were immersed in a 4% NaClO solution during 30 min, then rinsed 5 times with sterilized Millipore water (MPW, 18 M·ohm). Seeds were placed in germination paper saturated with antibiotic/antimicotic solution (A5955, Sigma, St. Louis, MO). To promote germination, seeds were kept in the dark for 4 days and after plantlets emerged they were exposed to light for 1 day. Plants were transferred to jars filled with 200 mL of the ENP suspension. Each concentration had triplicate sets of 40 plants per jar. Containers were constantly aerated to provide oxygen and to maintain the ENP in suspension. The plants were suspended in the jars using plastic micropipettes and a polyurethane layer to separate the root from the aerial part of the plant; only the roots were directly exposed to the nanoparticle suspensions. Plants were grown in the ENP suspension for 15 days on a 16 h photoperiod; during this time, the solution volume was maintained with MPW. Antioxidant Enzyme Activity Quantification. After ENP exposure, the plants were washed with 0.01 M HNO3 and MPW.

■

RESULTS AND DISCUSSION Cerium and Nutrient Accumulation in Mesquite Tissues. Concentrations of Ce in mesquite tissues are shown in Table 1. As seen in this table, the uptake of Ce by roots increased as external nanoceria increased up to 1000 ppm. Plant roots exposed to 1000−4000 ppm treatments presented a statistically similar uptake of Ce, which could indicate that at this concentrations, the nanoceria is toxic for hydroponically grown mesquite plants. In spite of the high concentrations used B

DOI: 10.1021/acssuschemeng.5b01251 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

Research Article

ACS Sustainable Chemistry & Engineering

mesquite has a higher degree of tolerance for the effect of the nanoceria than domesticated species.38 CAT/APOX Results. The APOX and CAT antioxidant activity in roots, stems, and leaves of mesquite plants exposed to nanoceria are shown in Figure 1. APOX activity in roots statistically increased at 2000 and 4000 mg L−1, suggesting an enzymatic response by the plant to increase the conversion of H2O2 into H2O. Similar results were reported in rice, APOX and dehydroascorbate reductase (an enzyme needed by APOX to reduce H2O2) were increased when exposed to 500 mg/L.23 In leaves, CAT showed an increasing trend associated with the external concentration of the ENP (Figure 1), although only at the 4000 mg/L treatment CAT activity was statistically significant. Regardless the high exposure concentration, mesquite plants showed no visible signs of stress such as necrosis, chlorosis or stunting. This is probably due to the Ce enhanced respiratory rate activities, because having 4f electron characteristics and reciprocal transformation between Ce3+ and Ce4+, it might play a role in reducing reactive oxygen species.39 Furthermore, Giraldo et al. reported the suppression of ROS inside extracted chloroplasts by nanoceria.40 Ce Localization and Speciation. Synchrotron radiation (SR) techniques such as μ-XRF and XANES have emerged as powerful tools to study the distribution and speciation of metals and metalloids. Several great reviews have focused on the use of SR techniques in plants.41−43 Figure 2a shows an optical micrograph of a cross section from mesquite root grown in mHNS−CeO2 ENP suspension. The red box in Figure 2a illustrates the area where the tricolor μ-XRF map (Figure 2b) was acquired. The obtained μ-XRF map shows high Ce adsorption in the mesquite root, corroborating the high concentrations of CE obtained in the ICP-OES analysis. Conversely, our study of ZnO ENP on mesquite showed high absorption of Zn in the plant tissue, denoting the differences in ENP solubility. The μ-XRF map (Figure 2b) does not show Ce in the root endodermis, suggesting the Ce is translocated trough the root cortex by apoplastic transport. In the apoplast, the flow is regulated by hydrostatic pressure, and the lack of membranes could facilitate Ce transport through the cortex. The Casparian strips of the endodermis create a barrier in the apoplast between the cortex and the vascular tissue. This is

Table 1. Cerium Concentrations in Root, Stem, and Leaves of Mesquite Plants Exposed Hydroponically to CeO2 ENP Suspensions (0, 500, 1000, 2000, 4000 mg Ce/L) for 15 daysa Ce dry tissue concentration (mg kg−1) treatment control 500 1000 2000 4000

root 0a 2186 2708 4504 3652

± ± ± ±

428b 532bc 520c 999bc

stem 0a 443 318 641 930

± ± ± ±

10b 51b 24bc 98c

leaves 0a 8 ± 3b 21 ± 5b 43 ± 12c 93 ± 14d

a Results are means ± SE. One way ANOVA and Tukey test were used to determine statistical significance, Means with same letter are statistically equals at p ≤ 0.05.

to explore the nanoceria−mesquite interactions, the translocation factors from root to shoots for Ce were relatively low. In plants treated with 500 mg L−1, the Ce concentration in stems was only 20% of the Ce concentration in roots, while at 4000 mg L−1 the translocation was 25%. Similar low translocation patterns have been reported in the literature, mostly due to the high stability of the CeO2 ENP.24,26−28,36 Conversely, Priester et al. reported a similar concentration of Zn in roots and stems of soybean plants exposed to 500 mg ZnO ENP kg−1.24 The CeO2 ENP did not interfere with the uptake and translocation of macronutrients (data not shown). However, some variations were observed in the uptake and translocation of microelements like Cu, Mn, and Zn. At the root level, Cu was reduced by about 30%, Mn about 40%, and Zn was increased at the 500 mg L−1 treatment, but reduced at 1000 mg L−1 and above. Changes at stem and leaf levels were less conspicuous. Liang and co-workers also documented a decrease in Mn on mugbean plants exposed to 0.63 μM Ce. As a result, the plants presented chlorosis, a visible sign of Mn deficiency.37 Similarly, reports indicate that, in hydroponically grown wheat, Ce reduced the uptake of Ca, Mg, K, Cu, and Zn.38 Hu et al. suggested that Ce could disturb the uptake of nutrients by blocking Ca ionic channels. A comparison of the reported results and results from the present study suggest that the wild

Figure 1. CAT and APOX antioxidative enzyme activity in the root, stem and leaves of mesquite plants exposed hydroponically to CeO2 ENP suspensions (0, 500, 1000, 2000, 4000 mg Ce/L) for 15 days. Asterisk above bars denotes statistical difference after one way ANOVA test at p ≤ 0.05. C

DOI: 10.1021/acssuschemeng.5b01251 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

Research Article

ACS Sustainable Chemistry & Engineering

Figure 2. Images of the transversal section (30 μm) of a mesquite root hydroponically exposed to 500 mg/L of CeO2/L. (A) Video microscope image of the root section. (B) Tricolor μ-XRF map (red = Ce, Green = Ca, and blue = K). (C) Averaged Ce L(III) XANES from the three white marks in B, named Ce XANES 2 (solid black color), and the spectra from the LCF (dotted red color).

consistent with the μ-XRF results that show Ce in the cortex but not in the xylem and phloem. Similarly, Zhao and coworkers suggested apoplastic transport of Ce in corn exposed to CeO2 ENP.27 Figure 2c displays the averaged spectra from the marks on Figure 2b (the sample is the average of 3 spectra) and the linear combination fitting (LCF). The double white line at 5729 and 5737 eV suggests an environment where Ce is present mostly as Ce(IV) and the high 5729/5737 ratio proposes that most of the Ce in the analyzed spectra is coordinated as the CeO2 ENP. To corroborate the previous assumptions LCF was performed using the following as model compounds: CeO2 ENP, Ce hydroxide, Ce sulfate, and Ce(III) acetate. It was estimated from the LCF that 81% of the Ce in the analyzed spots maintained the original CeO2 coordination. Similar results were found in crops such as bean, soybean and corn.21,27,44 Zhang et al. reported CeO2 and CePO4 as the Ce species found in cucumber roots treated with CeO2 ENP, the authors suggest a partial reduction to Ce3+ in the CeO2 adsorbed in the root followed by a precipitation as CePO4.45

chlorosis, necrosis, wilting or stunting. This suggests that mesquite has a higher degree of tolerance for the effect of the nanoceria than domesticated crop species. SR techniques showed that most of the Ce present in the mesquite roots was adsorbed to root epidermis and cortex. Thus, it is suggested that CeO2 ENP follow apoplastic movement in the mesquite root. Plants can change the speciation of metals and undergo toxic effects due to its accumulation; nevertheless XANES analysis showed that in mesquite CeO2 was the main chemical specie of Ce. To our knowledge, this is the first report on the effect of CeO2 ENP on desert plants, and further studies are needed to evaluate the interactions between ENP and desert plant species.

CONCLUSION There is serious concern regarding the potential ENP impacts to the ecosystem. Previous studies have investigated ENP− crops interactions, but few have dealt with desert plant species. Here, mesquite plants grown in hydroponic conditions were exposed to high concentrations of nanoceria to evaluate its transport, fate and potential toxicity. The concentration of Ce in mesquite tissue showed a high concentration of Ce in the roots and a low translocation to the aerial part of the plant. In addition, the nanoceria treatment caused a reduction in micronutrients that was consistent with previous crop studies. Biochemical assays documented that while antioxidant enzyme activity was incremented at high CeO2 ENP treatments in root and leaves, mesquite plants showed no visible signs of stress like

ACKNOWLEDGMENTS This material is based upon work supported by the National Science Foundation and the Environmental Protection Agency under Cooperative Agreement Number DBI-0830117. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation or the Environmental Protection Agency. This work has not been subjected to EPA review and no official endorsement should be inferred. This work was also supported by Grant 2G12MD007592 from the National Institutes on Minority Health and Health Disparities (NIMHD), a component of the National Institutes of Health (NIH). Authors also acknowledge the USDA grant 2011-38422-

■

AUTHOR INFORMATION

Corresponding Author

*J. L. Gardea-Torresdey. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

■

■

D

DOI: 10.1021/acssuschemeng.5b01251 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

Research Article

ACS Sustainable Chemistry & Engineering

(16) Yabe, S.; Sato, T. Cerium oxide for sunscreen cosmetics. J. Solid State Chem. 2003, 171 (1), 7−11. (17) Collin, B.; Auffan, M.; Johnson, A. C.; Kaur, I.; Keller, A. A.; Lazareva, A.; Lead, J. R.; Ma, X.; Merrifield, R. C.; Svendsen, C.; White, J. C.; Unrine, J. M. Environmental release, fate and ecotoxicological effects of manufactured ceria nanomaterials. Environ. Sci.: Nano 2014, 1 (6), 533−548. (18) Zhao, L.; Sun, Y.; Hernandez-Viezcas, J. A.; Servin, A. D.; Hong, J.; Niu, G.; Peralta-Videa, J. R.; Duarte-Gardea, M.; Gardea-Torresdey, J. L. Influence of CeO2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: A life cycle study. J. Agric. Food Chem. 2013, 61 (49), 11945−11951. (19) Zhang, P.; Ma, Y.; Zhang, Z.; He, X.; Zhang, J.; Guo, Z.; Tai, R.; Zhao, J.; Chai, Z. Biotransformation of ceria nanoparticles in cucumber plants. ACS Nano 2012, 6 (11), 9943−9950. (20) Wang, Q.; Ebbs, S. D.; Chen, Y.; Ma, X. Trans-generational impact of cerium oxide nanoparticles on tomato plants. Metallomics 2013, 5 (6), 753−759. (21) Majumdar, S.; Peralta-Videa, J. R.; Bandyopadhyay, S.; CastilloMichel, H.; Hernandez-Viezcas, J. A.; Sahi, S.; Gardea-Torresdey, J. L. Exposure of cerium oxide nanoparticles to kidney bean shows disturbance in the plant defense mechanisms. J. Hazard. Mater. 2014, 278, 279−287. (22) Rico, C. M.; Hong, J.; Morales, M. I.; Zhao, L.; Barrios, A. C.; Zhang, J.-Y.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. Effect of cerium oxide nanoparticles on rice: a study involving the antioxidant defense system and in vivo fluorescence imaging. Environ. Sci. Technol. 2013, 47 (11), 5635−5642. (23) 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. (24) Priester, J. H.; Ge, Y.; Mielke, R. E.; Horst, A. M.; Moritz, S. C.; Espinosa, K.; Gelb, J.; Walker, S. L.; Nisbet, R. M.; An, Y.-J.; Schimel, J. P.; Palmer, R. G.; Hernandez-Viezcas, J. A.; Zhao, L.; GardeaTorresdey, J. L.; Holden, P. A. Soybean susceptibility to manufactured nanomaterials with evidence for food quality and soil fertility interruption. Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (37), E2451− E2456. (25) López-Moreno, M. L.; de la Rosa, G.; Hernández-Viezcas, J. A.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. X-ray absorption spectroscopy (XAS) corroboration of the uptake and storage of CeO2 nanoparticles and assessment of their differential toxicity in four edible plant species. J. Agric. Food Chem. 2010, 58 (6), 3689−3693. (26) Morales, M. I.; Rico, C. M.; Hernandez-Viezcas, J. A.; Nunez, J. E.; Barrios, A. C.; Tafoya, A.; Flores-Marges, J. P.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. Toxicity assessment of cerium oxide nanoparticles in cilantro (Coriandrum sativum L.) plants grown in organic soil. J. Agric. Food Chem. 2013, 61 (26), 6224−6230. (27) Zhao, L.; Peralta-Videa, J. R.; Varela-Ramirez, A.; CastilloMichel, H.; Li, C.; Zhang, J.; Aguilera, R. J.; Keller, A. A.; GardeaTorresdey, J. L. Effect of surface coating and organic matter on the uptake of CeO 2 NPs by corn plants grown in soil: insight into the uptake mechanism. J. Hazard. Mater. 2012, 225, 131−138. (28) Schwabe, F.; Tanner, S.; Schulin, R.; Rotzetter, A.; Stark, W.; von Quadt, A.; Nowack, B. Dissolved cerium contributes to uptake of Ce in the presence of differently sized CeO 2-nanoparticles by three crop plants. Metallomics 2015, 7 (3), 466−477. (29) Keller, A. A.; Wang, H.; Zhou, D.; Lenihan, H. S.; Cherr, G.; Cardinale, B. J.; Ji, Z. Stability and aggregation of metal oxide nanoparticles in natural aqueous matrices. Environ. Sci. Technol. 2010, 44 (6), 1962−1967. (30) Gallego, S. M.; Benavides, M. P.; Tomaro, M. L. Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci. 1996, 121 (2), 151−159. (31) Murgia, I.; Tarantino, D.; Vannini, C.; Bracale, M.; Carravieri, S.; Soave, C. Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced

30835 and the NSF Grants EEC-1449500, CHE-0840525, and DBI-1429708. J. L. Gardea-Torresdey acknowledges the Dudley family for the Endowed Research Professorship, the Academy of Applied Science/US Army Research Office, Research and Engineering Apprenticeship program (REAP) at UTEP, grant # W11NF-10-2-0076, subgrant 13-7, and STARs programs of the University of Texas System. Ce X-ray spectromicroscopy experiments were performed on the ID21 beamline at the European Synchrotron Radiation Facility (ESRF), Grenoble, France.

■

REFERENCES

(1) Piccinno, F.; Gottschalk, F.; Seeger, S.; Nowack, B. Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J. Nanopart. Res. 2012, 14 (9), 1−11. (2) Roco, M. C. The long view of nanotechnology development: the National Nanotechnology Initiative at 10 years. In Nanotechnology Research Directions for Societal Needs in 2020; Springer: Amsterdam, The Netherlands, 2011; pp 1−28. (3) Keller, A. A.; Vosti, W.; Wang, H.; Lazareva, A. Release of engineered nanomaterials from personal care products throughout their life cycle. J. Nanopart. Res. 2014, 16 (7), 1−10. (4) Deng, Y. Q.; White, J. C.; Xing, B. S. Interactions between engineered nanomaterials and agricultural crops: implications for food safety. J. Zhejiang Univ., Sci., A 2014, 15 (8), 552−572. (5) Arruda, S. C. C.; Silva, A. L. D.; Galazzi, R. M.; Azevedo, R. A.; Arruda, M. A. Z. Nanoparticles applied to plant science: A review. Talanta 2015, 131, 693−705. (6) 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. (7) Bidak, L. M.; Kamal, S. A.; Halmy, M. W. A.; Heneidy, S. Z. Goods and services provided by native plants in desert ecosystems: Examples from the northwestern coastal desert of Egypt. Glob. Ecol. Cons. 2015, 3, 433−447. (8) White, R. P.; Nackoney, J. Drylands, People, and Ecosystem Goods and Services: A Web-Based Geospatial Analysis (PDF Version); World Resources Institute: Washington, DC, 2003. (9) UEMG. Global drylands: a UN system-wide response; United Nations Environment Management Group: Geneva, 2011. (10) Smith, S. D.; Monson, R. K.; Anderson, J. E. Physiological ecology of North American desert plants. 2012, Springer Science & Business Media. (11) Luna-Suárez, S.; Luna-Guido, M. L.; Frias-Hernández, J. T.; Olalde-Portugal, V.; Dendooven, L. Soil processes as affected by replacement of natural mesquite ecosystem with maize crop. Biol. Fertil. Soils 1998, 27 (3), 274−278. (12) Felker, P.; Takeoka, G.; Dao, L. Pod mesocarp flour of North and South American species of leguminous tree Prosopis (mesquite): Composition and food applications. Food Rev. Int. 2013, 29 (1), 49− 66. (13) De La Rosa, G.; López-Moreno, M. L.; Hernandez-Viezcas, J. A.; Montes, M. O.; Peralta-Videa, J.; Gardea-Torresdey, J. Toxicity and biotransformation of ZnO nanoparticles in the desert plants Prosopis julif lora-velutina, Salsola tragus and Parkinsonia f lorida. Int. J. Nanotechnol. 2011, 8 (6−7), 492−506. (14) Hernandez-Viezcas, J. A.; Castillo-Michel, H.; Servin, A. D.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. Spectroscopic verification of zinc absorption and distribution in the desert plant Prosopis juliflora-velutina (velvet mesquite) treated with ZnO nanoparticles. Chem. Eng. J. 2011, 170 (2), 346−352. (15) Bozek, F.; Mares, J. A. R. O. M. I. R.; Bozek, M. I. L. O. S; Huzlik, J. I. R. I. Emission of Particulate Matter While Applying the Envirox TM Additive. In Proceedings of the 5th WSEAS International Conference on Waste Management, Water Pollution, Air Pollution, Indoor Climate, Iasi, Romania, July 1−3, 2011; pp 170−175. E

DOI: 10.1021/acssuschemeng.5b01251 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

Research Article

ACS Sustainable Chemistry & Engineering photooxidative stress and to nitric oxide-induced cell death. Plant J. 2004, 38 (6), 940−953. (32) Packer, A. P.; Larivière, D.; Li, C.; Chen, M.; Fawcett, A.; Nielsen, K.; Mattson, K.; Chatt, A.; Scriver, C.; Erhardt, L. S. Validation of an inductively coupled plasma mass spectrometry (ICPMS) method for the determination of cerium, strontium, and titanium in ceramic materials used in radiological dispersal devices (RDDs). Anal. Chim. Acta 2007, 588, 166−172. (33) Susini, J.; Salomé, M.; Neuhaeusler, O.; Dhez, O.; Eichert, D.; Fayard, B.; Somogyi, A.; Bohic, S.; Bleuet, P.; Martinez-Criado, G.; et al. The X-ray microscopy and micro-spectroscopy facility at the ESRF. Synchrotron Radiat. News 2003, 16, 35−43. (34) Solé, V. A.; Papillon, E.; Cotte, M.; Walter, P.; Susini, J. A Multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochim. Acta, Part B 2007, 62, 63−68. (35) Ravel, B.; Newville, M. Athena, Artemis, Hephaestus: Data Analysis for X-ray Absorption Spectroscopy Using IFEFFIT. J. Synchrotron Radiat. 2005, 12, 537−541. (36) Cornelis, G.; Ryan, B.; McLaughlin, M. J.; Kirby, J. K.; Beak, D.; Chittleborough, D. Solubility and batch retention of CeO2 nanoparticles in soils. Environ. Sci. Technol. 2011, 45 (7), 2777−2782. (37) Liang, C.; Huang, X.; Tao, W.; Zhou, Q. Effect of rare earths on plants under supplementary ultraviolet-B radiation: II. Effect of cerium on antioxidant defense system in rape seedlings under supplementary ultraviolet-B radiation. J. Rare Earths 2006, 24 (3), 364−368. (38) Hu, X.; Ding, Z.; Chen, Y.; Wang, X.; Dai, L. Bioaccumulation of lanthanum and cerium and their effects on the growth of wheat (Triticum aestivum L.) seedlings. Chemosphere 2002, 48 (6), 621−629. (39) Hong, F.; Wang, X.; Liu, C.; Su, G.; Song, W.; Wu, K.; Tao, Y.; Zhao, G. Effect of Ce3+ on spectral characteristic of D1/D2/Cytb559 complex from spinach. Sci. China Series B: Chem. 2003, 46 (1), 42−50. (40) Giraldo, J. P.; Landry, M. P.; Faltermeier, S. M.; McNicholas, T. P.; Iverson, N. M.; Boghossian, A. A.; Reuel, N. F.; Hilmer, A. J.; Sen, F.; Brew, J. A.; Strano, M. S. Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat. Mater. 2014, 13 (4), 400−408. (41) Lombi, E.; Scheckel, K. G.; Kempson, I. M. In situ analysis of metal (loid) s in plants: state of the art and artefacts. Environ. Exp. Bot. 2011, 72 (1), 3−17. (42) Lombi, E.; Susini, J. Synchrotron-based techniques for plant and soil science: opportunities, challenges and future perspectives. Plant Soil 2009, 320 (1−2), 1−35. (43) Sarret, G.; Pilon-Smits, E. A. H.; Castillo Michel, H.; Isaure, M. P.; Zhao, F. J.; Tappero, R. Use of synchrotron-based techniques to elucidate metal uptake and metabolism in plants. Adv. Agron. 2013, 119, 1−82. (44) Hernandez-Viezcas, J. A.; Castillo-Michel, H.; Andrews, J. C.; Cotte, M.; Rico, C. M.; Peralta-Videa, J. R.; Ge, Y.; Priester, J. H.; Holden, P. A.; Gardea-Torresdey, J. L. In situ synchrotron X-ray fluorescence mapping and speciation of CeO2 and ZnO nanoparticles in soil cultivated soybean (Glycine max). ACS Nano 2013, 7 (2), 1415−1423. (45) Zhang, P.; Ma, Y.; Zhang, Z.; He, X.; Zhang, J.; Guo, Z.; Tai, R.; Zhao, J.; Chai, Z. Biotransformation of ceria nanoparticles in cucumber plants. ACS Nano 2012, 6 (11), 9943−9950.

■

NOTE ADDED AFTER ASAP PUBLICATION There was an error in the second author affiliation in the version published ASAP on January 13, 2016. The corrected version was published on January 15, 2016.

F

DOI: 10.1021/acssuschemeng.5b01251 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX