Phytotoxicity of Silver Nanoparticles to Peanut (Arachis hypogaea L

Research Article pubs.acs.org/journal/ascecg

Phytotoxicity of Silver Nanoparticles to Peanut (Arachis hypogaea L.): Physiological Responses and Food Safety Mengmeng Rui,†,‡,# Chuanxin Ma,§,∥,# Xinlian Tang,‡ Jie Yang,† Fuping Jiang,† Yue Pan,† Zhiqian Xiang,† Yi Hao,† Yukui Rui,*,† Weidong Cao,⊥ and Baoshan Xing§ †

College of Resources and Environmental Sciences, China Agricultural University, 2 Yuanmingyuan West Road, 23 Haidian District, Beijing 100193, China ‡ College of Agriculture, Guangxi University, 100 East University Road, Nanning 530004, China § Stockbridge School of Agriculture, University of Massachusetts, 161 Holdsworth Way, Amherst, Massachusetts 01003, United States ∥ Department of Analytical Chemistry, Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, Connecticut 06504-1106, United States ⊥ Green Manure Group, Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture of China/Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, No. 12. South Street, Zhongguancun, 26 Haidian District, Beijing 100081, China S Supporting Information *

ABSTRACT: In the present study, we investigated the effects of silver nanoparticles (Ag NPs) on peanut (Arachis hypogaea L.) at physiological and biochemical levels as well as the impacts on peanut yield and quality. Peanuts were cultivated in sandy soil amended with different doses of Ag NPs (50, 500, and 2000 mg·kg−1) for 98 days. Physiological parameters including plant biomass, height, grain weight, and yield suggested that Ag NPs could result in severe damages in plant growth. At the biochemical level, Ag NPs did not change the predominant isozymes of each antioxidant enzyme but significantly elevated the amounts of antioxidant isozymes as compared to those of the control, and the antioxidant enzyme activities were consistent with the elevation of isozymes. Ag concentrations exhibited a dose−response fashion in peanut tissues with increasing exposure doses of Ag NPs. The evidence of Ag NPs in the edible portion of peanuts was confirmed by transmission electron microscopy (TEM) with energy-dispersive X-ray spectroscopy (EDS). Additionally, alteration of the contents of fatty acids in peanut grains upon exposure to different doses of Ag NPs indicated that metal-based NPs could impact crop yield and quality. Taken together, our results suggested that the concerns over how to efficiently and safely apply nanoparticle incorporated products in agriculture and how to control their potential impact on the food safety and food quality should draw more attention as NPs themselves could be taken up by crops and humans exposed to them through food consumption. KEYWORDS: Arachis hypogaea L., Silver nanoparticles, Phytotoxicity, Yield, Fatty acids

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INTRODUCTION

Previous studies demonstrated that the possible accumulation of ENPs in soils and sediments had exponential increases in recent years.4 In agricultural fields, NPs can be introduced into soils through NPs mixed with pesticide, fungicide, and fertilizer;8−10 sewage irrigation;11,12 and washing of nanotextiles.9 Cerium oxide (CeO2), zinc oxide (ZnO), and iron oxide (Fe3O4) NPs could enter the root cells of Zea mays, Lolium perenne L., and Cucurbita maxima through the root tips, reaching the xylem via the cortex and central cylinder.13 Medicago sativa could take up Ag NPs and translocate them via the apoplastic route.14 To date, few studies have reported the impacts of NPs on food safety from the perspectives of NPs

With fast development in nanotechnology, nanomaterial manufacturing has achieved huge success, and its production scale has been constantly expanding.1,2 The market potential of engineered nanoparticles (ENPs) has doubled every three years. For example, the global market for silver nanoparticles (Ag NPs) will increase from USD 0.79 billion in 2014 to USD 2.45 billion by 2022.3 Ag NPs have multiple applications in healthcare, textiles, and wastewater treatment. It is predicted that Ag NP concentrations in soil and sludge-treated soil will increase by 1.2 and 110 ng·kg−1 per year, respectively.4 Therefore, it is inevitable that the released NPs could pose potential risks to the environment, including soil, water bodies, and plants, which are the main sinks for environmental contaminants.5−7 © 2017 American Chemical Society

Received: March 9, 2017 Revised: May 22, 2017 Published: June 26, 2017 6557

DOI: 10.1021/acssuschemeng.7b00736 ACS Sustainable Chem. Eng. 2017, 5, 6557−6567

Research Article

ACS Sustainable Chemistry & Engineering

thoroughly mixed with the corresponding amounts of Ag NPs (0.075, 0.75, and 3 g/pot) individually, and then each mixture was further mixed with the remaining soil to make the final concentration of Ag NPs 50, 500, and 2000 mg·kg−1. The total fertilizer (N/P2O5/K2O = 0.25:0.3:0.25 mg·kg−1 soil mixture) was applied in each treatment. A constant weight of 1.5 kg of soil mixture was used in each pot. The NP-amended soils were stabilized for 24 h prior to use. The treatment without Ag NPs additions was set as the control. Four peanut seedlings were transferred into each pot. There were 6 pots in each treatment. At 18 days from transferring, two plants with uniform size were kept for the exposure experiment and were watered with 220 mL of tap water at an interval of 48 h for 98 days. Determination of Peanut Biomass and Yield. At 10 days after the peanut gynophore entering the soil (peanut gynophore is ovary stalk of peanut flowers), the plant tissues were randomly sampled for analysis of antioxidant enzyme and their respective isoenzymes, root shape in cross section, and Ag NPs observation using TEM (EM-1230, JEOL, Japan).25 At maturity, shelled peanut fresh weight per pot was determined, and a sample of 20 fresh peanut grains per pot was randomly collected for measurements of 1000-grain weight. Root Shape in Cross Section by Optical Microscopy. At 10 days after the peanut gynophore entering the soil (peanut gynophore is ovary stalk of peanut flowers), the fully developed parts of peanut roots were fixed in Formalin−acetic acid−alcohol for 48 h, dehydrated in a series of ethanol, and embedded in paraffin wax. A serial section with 10−15 mm thickness was made using a Reichert sliding microtome. The samples were stained with safranin-fast green and then mounted in Canada balsam. The anatomical structures of peanut roots were observed under an Olympus BX51 light microscope.26 Observation of Ag NPs in the Peanut Tissues by TEM. Different peanut tissues including roots, leaves, and peanut pods were prepared for Ag NPs observation under TEM. The plant tissues were washed with 0.1 M phosphate buffer, immersed in 2.5% glutaraldehyde solution (pH 7.3), and dehydrated in a gradient ethanol series.27 The specimens were embedded in a series of mixtures of epoxy resin and then were sectioned using a microtome with a diamond knife. The ultrathin sections were placed on Cu-based grids for TEM observation (JEM-1230, JEOL, Japan).25 The selected electron-dense particles in plant cells were determined for the elemental composition by TEM combined with energy-dispersive X-ray spectroscopy (TEM-EDS) at 200 kV. Details are provided in Supporting Information section S1. Analysis of Antioxidant Enzyme Activities. A 0.2 g sample of fresh roots or pods was separately homogenized in phosphate-buffered solution (50 mM, pH 7.8) on ice. The mixtures were centrifuged at 10 000 × g for 20 min at 4 °C. The supernatant was used to analyze the activities of SOD, POD, and CAT following the protocols as described in Liu et al.28 Assay for Isozymes in Peanut Tissues. Enzyme Extraction. For SOD enzyme, fresh peanut tissues of roots and pods were homogenized in 2 mL cold potassium phosphate buffer (pH 7.8). The homogenate was then centrifuged at 12 000 × g for 20 min 4 °C. The supernatant was SOD crude extract. For POD enzyme, an equal amount of 40% sucrose solution was added into the SOD crude extract, and then the mixture was centrifuged at 12 000 × g for 20 min at 4 °C. The supernatant was POD crude extract. For CAT enzyme, the SOD crude extract was passed through a 0.45 μm ultrafiltration membrane, and then mixed with 0.5 mL of 10% sodium chloride (NaCl). The mixture was left to stand on the bench for 2−3 h and then was centrifuged at 12 000 × g for 5 min at 4 °C. Next, 150 μL of 35% formaldehyde was added into the supernatant and then centrifuged at 12 000 × g for 10 min at 4 °C. The supernatant was CAT crude extract. Details of antioxidant isozymes extraction are provided in Supporting Information section S2. Electrophoresis and Staining. The isozymes of SOD, CAT, and POD were separated on the SDS-PAGE, which was made of 12% separation gel and 5% concentration gel (Table S1). Tris-Glycine (pH 8.8) and bromophenol blue were used as electrode buffer and indicator, respectively. The protein gel was run at 80 V for 40 min, then at 120 V until the bromophenol blue reached the bottom of gel. The gels were stained by Coomassie brilliant blue for 2 h at ambient

accumulation and biotransformation. The evidence for NP accumulation in edible portions of plants was reported. For example, CeO2, ZnO, and TiO2 NPs could be taken up by roots and translocate to shoots, eventually entering the edible portions of soybean (Glycine max),15 cucumber (Cucumis sativus),16,17 and carrot (Daucus carota).18 A common finding in previous studies is that metal-based NP could induce oxidative stress in plants.19,20 The activities of superoxide dismutase (SOD) and catalase (CAT) in 2000 mg·L−1 nickel oxide NPtreated tomato (Solanum lycopersicum) plants were increased by 6.8- and 1.7-fold relative to those of the control.21 SOD, peroxidase (POD), and CAT are key antioxidant enzymes to scavenge reactive oxygen species (ROS), however, studies on the response of the isozymes of each antioxidant enzyme in terrestrial plants upon exposure to metal-based NPs are rather limited. Peanut (Arachis hypogaea L.) is one of the major oilseed crops, and its production has exceeded 14 million tons annually in China.22 Peanut seeds can produce high yield and quality oil.23,24 Peanut seeds are edible and contain various nutrients including protein, lipids, and fatty acids for human nutrition; peanut is a potential cash crop and has many value-added products that have been developed with a number of applications in bakery products, confectionery, and peanut oil products.23 In this study, we investigated the effects of Ag NPs on peanut in a pot experiment from the aspects of plant physiology and biochemistry. Peanuts were grown in different concentrations of Ag NP-amended field soil for 98 days. At harvest, physiological parameters, including biomass, shoot height, and yields, were measured in each Ag NP treatment. Ag accumulation and distribution in shoots, roots, and edible portions of Ag NPs treated peanuts were measured. Antioxidant enzyme activities and their respective isozymes were determined in Ag NP treated peanut roots and pods. The presence of Ag in edible portions as well as the evidence for alteration of the contents of fatty acids in Ag NPs treated peanut grains suggested that Ag NP exposure could pose potential and direct risks to human health. Thus, it is important to rationally and safely apply NPs in agriculture as well as to establish a comprehensive system to effectively evaluate NP impacts on crop plants.

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MATERIALS AND METHODS

Ag NP Characterizations. Ag NPs were purchased from Shanghai Pantian Powder material Co., Ltd. Transmission electron microscopy (TEM; FEI Co., Tecnai G2 20 S-TWIN, USA) was applied to observe morphological image and to determine size distribution of Ag NPs prior to the plant exposure experiment. TEM image showed that Ag NPs was in spherical shape with an averaged diameter of 20 nm (Figure S1). Pot Experiment. Experimental Design and Plant Growth Conditions. The legume Arachis hypogaea, commonly known as peanut, which belongs to angiosperm, dicotyledon, fabales, arachis, is an oil crop grown in tropical and subtropical regions. Peanut seeds of Luhua No.11 were purchased from Beijing Hongmei plantation. Seeds were soaked in 50 °C deionized water for 4 h; then, seed germination was performed on wet filter paper in Petri dishes at 25 ± 1 °C. Experimental soil was sampled from the Shangzhuang experimental station of China Agricultural University. Sand was mixed with soil in a weight ratio of 1:5.5 (sand/sampled soil, v/v) in order to improve water drainage, increase root respiration, and prevent root rotting. Different amounts of Ag NPs powder were thoroughly blended with the soil mixture to make various exposure doses of Ag NPs, including 50, 500, and 2000 mg·kg−1. Briefly, a 0.5 kg portion of soil was 6558


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Figure 1. Physiological responses of peanuts upon exposure to different concentrations of Ag NPs. (A) and (B) represent phenotypical image of peanuts grown in Ag NPs amended soil and the individual plant at harvest, respectively. (C−G) Plant height, fresh biomass, dry biomass, 1000-grain weight, and per plant yield, respectively. Error bars represent standard error (n = 3), and different letters represent significant differences among treatments (p < 0.05). In D and E, letters in uppercase represent significant differences in root, while lowercase letters represent significant differences in shoot. All samples were centrifuged at 1000 × g for 5 min, and the supernatant was passed through a 0.2 μm membrane. The fatty acid methyl esters were analyzed by gas chromatograph (Agilent 6890) equipped with a flame ionization detector. The capillary chromatographic column specifications (60.0 m × 250 μm, ID 0.25 μm, DB-23) were used. Working conditions were as follows: injection port temperature, 260 °C; sample size, 1 μm; split ratio, 30:1; carrier gas, helium; flow rate of carrier gas, 2.0 mL·min−1; detector temperature, 270 °C; programmed temperature, 130 °C for 1 min, followed by an 6.5 °C·min−1 increase to 170 °C, then a 2.75 °C·min−1 increase up to 215 °C, and hold at 215 °C for 12 min, followed by an 4 °C·min−1 increase to 230 °C for 3 min, and end of detection.30 Chromatogram peaks of samples were compared with national standards (GB/T 22223−2008). Statistical Analysis. Statistical analyses were performed through One-Way ANOVA using the SPSS 19.0 statistical software. The mean values for each treatment were compared using the Duncan’s test at p ≤ 0.05 confidence level. All results were conducted with three replicates, and the error bars correspond to the standard error of mean.

temperature, then was washed by ultrapure water and bleached for 50 s by protein-bleaching solution. Relative intensity of Ag NPs treated isozymes was calculated using Adobe Photoshop CS version 8.0 software. Determination of Ag Concentrations. Modified procedures of sample preparation and digestion were used.29 Briefly, peanut tissues were oven-dried at 105 °C for 30 min to deactivate enzymes and then were dried at 75 °C until a constant weight was reached. The ovendried tissues were ground to a fine powder and digested by using a microwave digestion system (Milestone, Ultra WAVE, Italy). A 0.2 g sample of dry tissues was mixed with 3 mL of concentrated nitric acid and 0.5 mL of hydrogen peroxide, and the mixture was digested at 200 °C for 20 min. The digests were diluted with ultrapure water to 15 mL, and then further diluted 5 times prior to analysis using inductively coupled plasma mass spectroscopy (ICP-MS, Agilent, 7700x, USA). Determination of Fatty Acid Contents. A 0.05−0.1 g sample of dry grain was mixed with 4 mL of chloroacetic methanol, 1 mL of undecanoic acid methyl ester (internal standard), and 1 mL of nhexane. The mixture was heated at 80 °C for 2 h, then cooled down at ambient temperature prior to add 5 mL of 7% potassium carbonate. 6559


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Figure 2. Effects of Ag NPs on antioxidant enzyme activity in roots and pods of peanut plants. (A−C) SOD, POD, and CAT activities in different concentrations of Ag NPs treated roots. (D−E) Activities of SOD and POD in Ag NPs treated peanut pods. Error bars represent standard error (n = 3), and different letters represent significant differences among treatments (p < 0.05).

Figure 3. Effects of Ag NPs on antioxidant isozymes in roots and pods of peanut plants. (A) Gel image of the SOD, CAT, and POD isozymes in Ag NPs treated peanut roots. (B) POD and SOD isozyme in Ag NPs treated peanut pod.

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RESULTS AND DISCUSSION

exhibited severe impacts on peanut growth. Phenotypic images of peanuts and their edible portions indicated that Ag NPs notably inhibited plant growth as well as peanut pod formation (Figure 1A,B). As compared to that of the control, the plant

Effect of Ag NPs on Biomass, Plant Height, and Yield. Figure 1 shows peanut growth upon exposure to different concentrations of Ag NPs. Overall, the presence of Ag NPs 6560


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Figure 4. Ag concentrations in different exposure doses of Ag NPs treated peanuts. Ag concentrations in (A) the shoots and roots and (B) the pods, and (C) Ag distribution in different positions of the pod treated with 2000 mg·kg−1 Ag NPs. These different parts of the pod are from the same pool. Error bars represent standard error (n = 3), and different letters represent significant differences among treatments (p < 0.05). In (A), letters in uppercase represent significant differences in root and lowercase ones represent significant differences in shoot.

treatments was decreased by 86.62 and 90.63%, respectively (Figure 1B,F). The 1000-grain weight in all three Ag NPs treatments was decreased by 22.02, 59.58, and 75.55%, respectively, with increasing the concentrations of Ag NPs (Figure 1G). Thus, Ag NPs exposures severely affected the growth and yields of peanut in comparison with the Ag NPs free treatment. Our physiological results of Ag NPs treated peanuts aligned with the previous studies that metal-based NPs could physiologically cause severe damages to terrestrial plants. Le et al. reported that 50 mg·kg−1 lanthanum oxide (La2O3) NPs significantly reduced the root biomass of maize.31 Additionally, particle size can determine metal phytotoxicity as the smaller particles generally have a larger surface area to facilitate interactions with plant cells. For example, 250 mg·kg−1 Ag NPs significantly decreased the fresh biomass of Crambe abyssinica by 49 and 59% relative to those with bulk Ag and the control, respectively.32 Besides physiological effects of Ag NPs on plant biomass, the results of edible portion of Ag NPs treated peanuts also suggested that food safety should draw more attention in terms of metal accumulation, crop yield, and food quality (Figure 1). To date, some relevant work has been reported that metal-based NPs could significantly lower the crop yield. Zhao et al. reported that 800 mg·kg−1 CeO2 NPs decreased cucumber (Cucumis sativus) yield by 31.6%.17 An exposure dose of 1000 mg·L−1 Ag NPs decreased tomato (Lycopersicon esculentum) yield by 60.10%, relative to that of the control.33 Prasad et al. found that 2000 mg·L−1 ZnO NPs decreased peanut yield by 7.6%, relative to that of the control.34 In addition, the presence of NPs might alter the contents of mineral elements in mature plants and subsequently result in lower food quality and yield loss.35 Antioxidant Enzyme Activities in Peanut Roots and Pods. Antioxidant enzyme activities, SOD, POD, and CAT, in peanuts roots and pods were measured (Figure 2). A dose− response trend was found in both SOD and POD activities in different exposure doses of Ag NPs treated peanut roots (Figure 2 A,B). For instance, as compared to that of the control, SOD activities in Ag NPs treated roots were elevated by 40.31, 85.45, and 172.1% with increasing the exposure doses of Ag NPs; likewise, POD activities in Ag NPs treated roots were increased by 63.28, 132.7, and 184.9%. CAT activity was an exception as the highest activity of CAT was found in 500 mg·kg−1 NPs treated roots rather than in 2000 mg·kg−1 treatment, in which CAT activity was still 66.61% higher than

Figure 5. Observation of root cross sections among different Ag NPs treatments. (A−D) Control, 50, 500, and 2000 mg·kg−1 Ag NPs treatment, respectively.

heights in 500 and 2000 mg·kg−1 Ag NPs treatments decreased by 21.92 and 29.66%, respectively (Figure 1A,C); decreases of both fresh and dry biomass showed a dose−response manner with increasing the exposure doses of Ag NPs (Figure 1D,E). The per plant yield in 500 and 2000 mg·kg−1 Ag NPs 6561


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Figure 6. TEM images of Ag NPs in peanut tissues treated with 2000 mg·kg−1 Ag NPs. (A1−A3) TEM images of leaves, roots, and pods in the control group; (B1−B3) TEM images of leaves, roots, and pods in 2000 mg·kg−1 Ag NPs treatment; (C1) magnified image of the red circled area in the image B1. (D) EDS spectrum of the red area in B3. Labels: chloroplast (Chl), vacuole (V), plasma membrane (Pm), and starch grain (SG).

H2O2, which can be scavenged by CAT and POD, whose activities were measured in Figure 2. In agreement with our findings, 750 mg·L−1 ZnO NPs significantly increased the activities of SOD, POD, and CAT in rice (Oryza sativa L.) leaves relative to that of the control,39 and 1000 Ag NPs mg·L−1 significantly increased the activities of SOD in tomatoes, when compared with that of the control treatment.33 It was also demonstrated that the presence of Ag NPs caused increases of SOD and CAT activities and decrease of POD activity in water hyacinth (Eichhornia crassipes), suggesting that responses of antioxidant defense mechanism might vary upon NP exposure, although both CAT and POD can specifically scavenge excessive amounts of H2O2 in plants.40 The activities of SOD in CeO2 (1000 mg·L−1) and In2O3 NPs (250 and 1000 mg·L−1) treated Arabidopsis thaliana were increased by 2- to 3-fold;

that in the control (Figure 2 C). In peanut pods, SOD and POD activity in 2000 mg·kg−1 Ag NPs treatment was increased by 23.87 and 43.77% relative to that of the control, respectively (Figure 2D,E). When compared to the antioxidant activities in the roots, SOD and POD activities in 2000 mg·kg−1 treated pods were increased by 18.41 and 264.0%, respectively. Many studies have agreed that metal-based NPs induced oxidative stresses could be one of the most important explanations for phytotoxicity in terms of lipid peroxidation, DNA and cell membrane damage, and cell death.36−38 Abiotic stresses (such as heavy metals and metal-based NPs) could induce large amounts of ROS and cause oxidative damage to plants via electron transfer; induced ROS includes singlet oxygen (1O2), superoxide (O2•−), hydrogen peroxide (H2O2), and hydroxyl radical (HO•). SOD catalyzes O2•− to less toxic 6562


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ACS Sustainable Chemistry & Engineering Table 1. Relative Contents (%) of 18 Kinds of Fatty Acids in Peanut Grain Ag NPs (mg·kg−1) fatty acids decanoic acid (C10:0) lauric acid (C12:0) myristic acid (C14:0) pentadecanoic acid (C15:0) palmitic acid (C16:0) palmitoleic acid (C16:1) heptadecanoic acid (C17:0) stearic acid (C18:0) oleic acid (C18:1n9c) oinoleic acid (C18:2n6c) α-linolenic acid (C18:3n3) arachidic acid (C20:0) eicosenoic acid (C20:1) heneicosanoic acid (C21:0) eicosadienoic acid (C20:2) behenic acid (C22:0) erucic acid (C22:1n9) lignoceric acid (C24:0) total SFAa total UFAa

control 0.02 ± 0.01 ± 0.05 ± 0.011 ± 10.98 ± 0.07 ± 0.10 ± 4.63 ± 45.60 ± 32.69 ± 0.08 ± 1.55 ± 0.78 ± 0.034 ± 0.021 ± 2.17 ± 0.07 ± 1.13 ± 20.70 79.30

0.01 a 0.002 a 0.01 a 0.001 ab 0.43 a 0.02 a 0.02 a 0.45 a 0.77 a 0.21 a 0.004 b 0.04 b 0.03 b 0.002 a 0.001 a 0.15 a 0.02 a 0.07 b

50

500

0.06 ± 0.01 a 0.02 ± 0.005 a 0.04 ± 0.002 a 0.008 ± 0.001 b 11.22 ± 0.14 a 0.06 ± 0.01 a 0.07 ± 0.001 a 4.62 ± 0.27 a 43.33 ± 2.13 ab 34.78 ± 1.98 a 0.07 ± 0.01 b 1.58 ± 0.03 b 0.75 ± 0.04 b 0.036 ± 0.003 a 0.018 ± 0.002 b 2.16 ± 0.07 a 0.03 ± 0.01 b 1.16 ± 0.01 b 20.96 79.04

0.05 ± 0.01 a 0.03 ± 0.01 a 0.05 ± 0.003 a 0.013 ± 0.002 a 11.58 ± 0.38 a 0.06 ± 0.01 a 0.07 ± 0.01 a 5.06 ± 0.52 a 41.65 ± 1.24 b 33.96 ± 1.32 a 0.17 ± 0.03 a 1.87 ± 0.06 a 0.97 ± 0.07 a 0.031 ± 0.002 a 0.021 ± 0.001 a 3.00 ± 0.19 b 0.08 ± 0.03 a 1.34 ± 0.09 a 23.09 76.91

a

The SFA content is equal to the sum of C10:0, C12:0, C14:0, C 15:0, C16:0, C17:0, C18:0, C20:0, C21:0, C22:0, and C24:0; the UFA content is equal to the sum of C16:1, C18:1n9c, C20:1, and C22:1n9.

CAT activities in the 250 mg·L−1 CeO2 NPs treated were increased by 3-fold. POD activities in 1000 mg·L−1 CeO2 NPs increased by 2-fold, relative to that of the control.41 Similar results were also found in the present study that Ag NPs could trigger the elevations of SOD, POD, and CAT activities in peanuts. Zymogram Analysis of Antioxidant Isozymes in Peanut Roots and Pods. The synthesis and activity of isozymes were controlled and adjusted by their corresponding genes and their allelic form of the locus. Biotic and abiotic stressors can cause transcriptional and translational adjustments and subsequently alter the antioxidant isozymes in terms of total number of bands and mobility.42 SODs are a family of metalloenzymes and are controlled by multiple genes. SOD isozymes are stored in different cell organelles, e.g., manganese SOD (Mn-SOD) is mostly found in the mitochondrial and peroxisomes, iron SOD (Fe-SOD) localizes in the chloroplast, and copper−zinc SOD (CuZnSOD) localizes in the chloroplast and cytosol.42 As shown in Figure 3, SOD isozymes in Ag NPs treated roots and pods of peanuts were elevated in terms of bandwidth and relative intensity as compared with that of the control (Tables S2−1 and S2−4). Relevant studies regarding NPs impact on plant antioxidant isozymes are scarce; however, many similar works have been conducted in plants treated with other abiotic stressors. For example, Sekmen et al. found the significant increases of Mn-SOD, Fe-SOD, and CuZn-SOD isozymes in Gypsophila oblanceolata treated with 50 and 100 mM NaCl.43 The relative intensities of CuZn-SOD1 in 500 and 2000 mg· kg−1 Ag NPs treated root were increased by 35 and 53%, respectively; the relative intensities of CuZn-SOD2 isozyme in 50, 500, and 2000 mg·kg−1 Ag NPs treated root were increased by 42, 61, and 73%, respectively (Table S2−1). The relative intensities of CuZn-SOD isozyme in 2000 mg·kg−1 Ag NPs treated pod were increased by 12% (Table S2−4), which is consistent with a previous report that the spherical Ag NPs

induced the high yield of CuZn-SOD.44 The relative intensity of Mn-SOD isozyme in 2000 mg·kg−1 Ag NPs treated roots and pods was approximately 2- and 1.3-fold of the one in control, respectively (Tables S2−1 and S2−4). Likewise, the relative intensity of each Fe-SOD in 2000 mg·kg−1 Ag NPs treated roots and pods were also several folds higher than the control. All of these results suggested that the chloroplast and mitochondrial might be more important in scavenging O2•− under Ag NPs stress because both Fe- and Mn-SOD are mainly found in these two cell organelles. These results agreed with a previous study that the correlations between Mn-SOD/FeSOD and total SOD activity were significantly higher than the ones with other SOD isozymes in salt treated perennial ryegrass (Lolium perenne L.).42 POD and CAT are the major enzymes that scavenge H2O2, and the expression of the POD isoenzymes depends on different environmental stressors.45 Our results indicated that each POD isozyme in peanut roots exhibited a dose−response trend with increasing exposure doses of Ag NPs (Figure 3A and Table S2−2). Similarly, the intensities of POD5 isoenzymes in Cleome gynandra L. were elevated by 21.9% at day 5, and the intensities of POD1 and POD3 isoenzymes in spider flower (Cleome spinosa) were elevated by 5.4 and 11.4% at days 10 and 5, respectively, under drought stress.45 Similar to POD isozymes in the roots, 2000 mg·kg−1 Ag NPs notably induced the intensities of 7 different POD isozymes in pods (Table S2− 5). Ma et al. found 8 POD isozymes bands in black wheat, and expression in terms of bandwidth and intensity showed a dose− response increase in response to 1, 5, 10, and 15 mg·L−1 concentrations of cadmium (Cd).46 For CAT isozymes, the highest relative intensities of CAT1, CAT2, and CAT3 were all found in 500 mg·kg−1 Ag NPs treatment (Table S2−3). Shao et al. found that the expression of SOD, CAT, and POD isozymes (bandwidth and intensity) were enhanced in Andrographis paniculata with increasing NaCl concentrations.47 Our results also suggested that the changes in antioxidant isozymes were 6563


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TEM Images of Ag NP Distribution in Peanut Leaf, Root, and Pod. Figure 6 shows Ag NPs distribution in 2000 mg·kg−1 treated peanut leaf, root, and pod. In peanut leaf, majority of Ag accumulated and localized on the outer membrane of the chloroplast, while no Ag was observed in the control (Figure 6A1,B1,C1). Additionally, the presence of Ag NPs resulted in swollen and deformed chloroplasts in peanut leaves (Figure 6B1). Similarly, CeO2 NPs attached on the external membrane of chloroplasts and subsequently induced chloroplast to swell, rupture, and deform.27 Compared with those of the controls, the Ag NPs enriched regions were observed on the internal surface of the cell membrane and in vacuoles in peanut roots (Figure 6B2), and NPs agglomerates were not observed in the control (Figure 6A2). Hao et al. found that carbon nanotubes penetrated the cell wall and membrane into the root cell.54 Some Ag NPs were found in the pods of plants treated with 2000 mg·kg−1 Ag NPs (Figure 6B3), and the result was further confirmed using EDS (Figure 6D). The starch grains appeared earlier in Ag NPs treated edible portion than in the control might be a stress response in peanut upon Ag NPs exposure. These results imply the potential accumulation and NPs transfer along food chains. Qualitative and Quantitative Analysis for Fatty Acid Composition. The compositions and contents of fatty acids in peanut grains can determine the quality of peanuts and have direct impact on human health. For instance, the stability of oleic acid/linoleic acid (O/L) ratio can reflect the nutritional quality of peanut.55 Thus, investigation of the effects of Ag NPs on alteration of the compositions and contents of fatty acids in peanut grains is of great importance. As shown in Table 1, the main compositions of the fatty acids were oleic acid (C18:1n9c), linoleic acid (C18:2n6c), palmitic acid (C16:0), and stearic acid (C18:0), all of which accounted for 93.89% of the total fatty acids in peanut grains in the control (the chromatograms of gas chromatograph is provided in Figure S2). The results suggested that the contents of linoleic acid (C18:2n6c) in the 500 mg·kg−1 Ag NPs treatment was significantly increased by 5.6%, and the oleic acid (C18:1n9c) level was notably decreased by 10.0%, as compared with that of the control, which was consistent with a previous report that the oleic acid (C18:1n9c) of sunflower seeds was decreased by 2.6% and linoleic acid (C18:2n6c) was increased by 2.8% relative to that of the control, under irrigation condition.56 The stearic acid (C18:0), arachidic acid (C20:0), and behenic acid (C22:0) in the 500 mg·kg−1 Ag NPs treatment was increased by 15.5, 20.4, and 38.2%, respectively. The result was consistent with previous studies that the levels of stearic acid (C18:0), arachidic acid (C20:0), and behenic acid (C22:0) of green microalgae increased in the presence of 0.5 mg·L−1 NiCl2.57 In the 500 mg·kg−1 Ag NPs treatment, the content of saturated fatty acid (SFA) was increased by 12.0%, and the content of unsaturated fatty acid (UFA) was decreased by 3.1% relative to that of the control (Table 1). Thus, the ratio of SFA/UFA increased from 25.9 to 30.0% in the 500 mg·kg−1 Ag NPs treatments as a result of the alteration of antioxidant defense system or the activity of fatty acid desaturases.58 The O/L value in the 50 and 500 mg·kg−1 Ag NPs treatments was decreased by 10.4 and 14.8%, respectively, relative to that of the control. Previous study found that the shelf life of peanut oil became longer with increasing O/L ratio.59 The high level of UFA of peanut can help to treat and prevent cancer, strengthen immune system, and function as an anti-aging agent, while

consistent with the activities of antioxidant enzymes in Ag NPs treated peanuts, suggesting that the increase in antioxidant activity was a result of the elevated isoenzyme expression under the abiotic stress conditions. The root proteomic study showed that the presence of Ag NPs mainly altered the oxidative stress related proteins, including SOD and POD in rice, garden rocket (Eruca sativa Mill), and other higher plants. 48 Thus, investigation of the patterns of antioxidant isozymes is helpful to understand the defense mechanisms of terrestrial plants in responses to metal-based NP exposure. Ag Concentrations in Ag NPs Treated Peanut Tissues. Ag concentrations in different exposure doses of Ag NPs treated peanut tissues were determined. A dose−response trend was found in Ag accumulation in peanut shoots and roots (Figure 4A). For example, with increasing exposure doses of Ag NPs, Ag concentration in 500 mg·kg−1 Ag NPs treated roots was approximately 6-fold of the one in 50 mg·kg−1 Ag NPs treated roots. When increasing Ag NPs concentration to 2000 mg·kg−1, Ag concentration in the roots was about 90 mg·kg−1, which was almost 90- and 15-fold of that in 50 and 500 mg·kg−1 Ag NPs treatments, respectively. A similar trend was also evident in peanut pods (Figure 4B). Significant high levels of Ag were found in 2000 mg·kg−1 Ag NPs treated pods. We further analyzed the Ag concentration in each position of pod treated with 2000 mg·kg−1 Ag NPs (Figure 4C). The Ag concentration in peanut grains was as high as 20.35 mg·kg−1, which was 5.3- and 3.1-folds higher than that in husk and pod, respectively. Previous studies have demonstrated that metal-based NPs could accumulate in the roots and translocate to the aboveground part.18,49 For example, Si NPs and CeO2 NPs were transported from roots to shoots via xylem sap in cotton.27,50 Ag NPs accumulated in Crambe abyssinica roots and translocate to shoots.32 C60 presented in soil at 2500 mg·kg−1 was taken up by and accumulated in different positions of radish (Raphanus sativus L.).51 By using synchrotron radiation X-ray spectroscopy, Hernandez-Viezcas et al. found that CeO2 and ZnO NPs could enter the edible portion of soybean,15 and CeO2 and TiO2 NPs could transfer into cucumber and enter the food chain.16,17 In the present study, Ag NPs might be transported into the peanut edible portion via the xylem route and direct contact, thereby posing the potential risks to human health. Observation of Root Cross Section by Optical Microscopy. Images of transverse paraffin sections of peanut root treated with different concentrations of Ag NPs are shown in Figure 5. The results indicated that Ag NPs had an impact on morphology of peanut root. The root diameter was decreased in the 2000 mg·kg−1 Ag NPs treatment, and root epidermal cell size decreased in different Ag NPs treatments (Figure 5A1,B1,C1,D1), as compared with that of the control. Previous studies suggested that metal-based NPs could be accumulated and transported in plants by penetrating the root epithelia and reaching the cortex, xylem, and phloem through symplastic or apoplastic systems.5,52 Significant difference of xylem vessel was observed in the dissection structures of peanut roots treated with 50 and 500 mg·kg−1 Ag NPs treatments (Figure 5B,C) and multiple cavities appeared in the xylem, whose structures were severely altered in the presence of 2000 mg·kg−1 Ag NPs (Figure 5D). In comparison with other abiotic stress, water stress could also reduce the number of secondary root cortical cells, and result in decreases of diameter of the secondary xylem vessels of Z. mays roots.53 6564


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(3) Silver Nanoparticles Market by Application (Electronics & Electrical, Healthcare, Food & Beverages, Textiles) and Segment Forecasts to 2022; Report ID 978-1-68038-413-0; Grand View Research: San Francisco, CA, 2015. (4) Sun, T. Y.; Conroy, G.; Donner, E.; Hungerbühler, K.; Lombi, E.; Nowack, B. Probabilistic modelling of engineered nanomaterial emissions to the environment: a spatio-temporal approach. Environ. Sci.: Nano 2015, 2 (4), 340−351. (5) 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. (6) Oberdö rster, G.; Oberdö rster, E.; Oberdö rster, J. Nanotoxicology: An Emerging Discipline Evolving from Studies of Ultrafine Particles. Environ. Health Perspect. 2005, 113, 823. Supplemental Web Sections. (7) Wang, S.; Kurepa, J.; Smalle, J. A. Ultra-small TiO2 nanoparticles disrupt microtubular networks in Arabidopsis thaliana. Plant, Cell Environ. 2011, 34 (5), 811−820. (8) Ghormade, V.; Deshpande, M. V.; Paknikar, K. M. Perspectives for nano-biotechnology enabled protection and nutrition of plants. Biotechnol. Adv. 2011, 29 (6), 792−803. (9) Nowack, B.; Ranville, J. F.; Diamond, S.; Gallego-Urrea, J. A.; Metcalfe, C.; Rose, J.; Horne, N.; Koelmans, A. A.; Klaine, S. J. Potential scenarios for nanomaterial release and subsequent alteration in the environment. Environ. Toxicol. Chem. 2012, 31 (1), 50−59. (10) Weir, A.; Westerhoff, P.; Fabricius, L.; Hristovski, K.; Von Goetz, N. Titanium dioxide nanoparticles in food and personal care products. Environ. Sci. Technol. 2012, 46 (4), 2242−2250. (11) Brar, S. K.; Verma, M.; Tyagi, R.; Surampalli, R. Engineered nanoparticles in wastewater and wastewater sludge−Evidence and impacts. Waste Manage. 2010, 30 (3), 504−520. (12) Kiser, M. A.; Ryu, H.; Jang, H.; Hristovski, K.; Westerhoff, P. Biosorption of nanoparticles to heterotrophic wastewater biomass. Water Res. 2010, 44 (14), 4105−4114. (13) Dietz, K.-J.; Herth, S. Plant nanotoxicology. Trends Plant Sci. 2011, 16 (11), 582−589. (14) Stegemeier, J. P.; Schwab, F.; Colman, B. P.; Webb, S. M.; Newville, M.; Lanzirotti, A.; Winkler, C.; Wiesner, M. R.; Lowry, G. V. Speciation matters: Bioavailability of silver and silver sulfide nanoparticles to alfalfa (Medicago sativa). Environ. Sci. Technol. 2015, 49 (14), 8451−8460. (15) Hernandez-Viezcas, J. A.; Castillo-Michel, H.; Andrews, J. C.; Cotte, M.; Rico, C.; 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. (16) Servin, A. D.; Morales, M. I.; Castillo-Michel, H.; HernandezViezcas, J. A.; Munoz, B.; Zhao, L.; Nunez, J. E.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. Synchrotron Verification of TiO2 Accumulation in Cucumber Fruit: A Possible Pathway of TiO2 Nanoparticle Transfer from Soil into the Food Chain. Environ. Sci. Technol. 2013, 47 (20), 11592−11598. (17) 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. (18) Ebbs, S. D.; Bradfield, S. J.; Kumar, P.; White, J. C.; Musante, C.; Ma, X. Accumulation of zinc, copper, or cerium in carrot (Daucus carota) exposed to metal oxide nanoparticles and metal ions. Environ. Sci.: Nano 2016, 3 (1), 114−126. (19) Atha, D. H.; Wang, H.; Petersen, E. J.; Cleveland, D.; Holbrook, R. D.; Jaruga, P.; Dizdaroglu, M.; Xing, B.; Nelson, B. C. Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environ. Sci. Technol. 2012, 46 (3), 1819−1827. (20) Mukherjee, A.; Peralta-Videa, J. R.; Bandyopadhyay, S.; Rico, C. M.; Zhao, L.; Gardea-Torresdey, J. L. Physiological effects of

decreasing the level of SFA can reduce low-density lipoprotein cholesterol levels and lower the risk of cardiovascular diseases.60,61 Taken together, the results of the contents of fatty acids upon exposure to 50 and 500 mg·kg−1 Ag NPs suggested that the presence of Ag NPs indeed reduce the quality of peanut grains and might even cause potential impacts on human health.

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CONCLUSIONS In the present study, peanuts as a target plant were grown in Ag NPs-contaminated agricultural soils until maturity. Our results suggested that Ag NPs significantly inhibited plant growth and reduced crop yield. At the biochemical level, the responses of antioxidant isozymes were analyzed in order to reveal the roles of each antioxidant contributes in scavenging ROS and defending NP-induced oxidative stress in the terrestrial plants. Besides the significant reduction of crop yield, the fatty acids in Ag NPs treated peanut grains also indicated that the presence of Ag NPs could significantly alter the crop quality. The evidence of Ag NPs in peanut grains indicated that NPs transfer should draw much attention from the perspectives of food safety and human health as the edible portion of the peanuts has been widely used in food or been directly consumed.

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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/acssuschemeng.7b00736. Additional information including sample preparation for TEM image, assays for antioxidant isozymes, results of the relative intensity of each isozymes, TEM image of Ag NPs, and gas chromatogram of fatty acid in peanut grain (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: 8610-62733470. ORCID

Yukui Rui: 0000-0003-2256-8804 Baoshan Xing: 0000-0003-2028-1295 Present Address

C.M.: 123 Huntington Street, New Haven, Connecticut 06504, United States. Author Contributions #

M.R. and C.M. contributed equally to this work.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The project was supported by National Natural Science Foundation of China (Nos. 41371471, 41130526, and U1401234).

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REFERENCES

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Phytotoxicity of Silver Nanoparticles to Peanut (Arachis hypogaea L

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