Alteration of Crop Yield and Quality of Wheat upon Exposure to Silver

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Alteration of crop yield and quality of wheat upon exposure to silver nanoparticles in a life cycle study Jie Yang, Fuping Jiang, Chuanxin Ma, Yu-kui Rui, Mengmeng Rui, Adeel Muhammad, Weidong Cao, and Baoshan Xing J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b04904 • Publication Date (Web): 16 Feb 2018 Downloaded from http://pubs.acs.org on February 17, 2018

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Journal of Agricultural and Food Chemistry

Alteration of crop yield and quality of wheat upon exposure to silver

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nanoparticles in a life cycle study

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Jie Yang1,†, Fuping Jiang1,†,Chuanxin Ma2, 3,†,*, Yukui Rui1,* ,Mengmeng

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Rui1,Muhammad Adeel1, Weidong Cao4, Baoshan Xing3,

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College of Resources and Environmental Sciences, China Agricultural University,

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Beijing, China

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2

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Station, New Haven, Connecticut 06504, United States

Beijing Key Laboratory of Farmland Soil Pollution Prevention and Remediation,

Department of Analytical Chemistry, The Connecticut Agricultural Experiment

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Massachusetts 01003, United States

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of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural

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Sciences, Beijing, China

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Corresponding authors:

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*

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*

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†

Stockbridge School of Agriculture, University of Massachusetts, Amherst,

Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture / Institute

Yukui Rui: [email protected]; Phone: 86-10-62733470; Chuanxin Ma: [email protected]; Phone: 1-203-974-8321. These authors contributed equally to this work.

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ACS Paragon Plus Environment


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Abstract

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Due to the rapid development of nanotechnology, metal-based nanoparticles (NPs) are

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inadvertently released into environment and may pose a potential threat to ecosystem.

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However, information for food quality and safety in NP treated crops is limited. In the

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present study, wheat (Triticum aestivum L.) was grown in different concentrations of

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Ag NP amended soil (20, 200, and 2000 mg·kg-1) for four months. At harvest,

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physiological parameters, Ag and micronutrients (Fe, Cu, and Zn) content, as well as

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amino acids and total proteins content. Results showed that with increasing the

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exposure doses, Ag NPs exhibited severe phytotoxicity, including lower biomass,

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shorter plant height and lower grain weight. Ag accumulation in roots was

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significantly higher than that in shoots and grains, respectively. Decreases in the

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contents of micronutrients (Fe, Cu, and Zn) in Ag NP treated grains suggested low

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crop quality. The results of amino acid and protein contents in Ag NPs treated wheat

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grains indicated that Ag NPs indeed altered the nutrient contents in the edible portion.

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In the amino acid profile, the presence of Ag NPs significantly decreased the contents

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of arginine and histidine by 13.0% and 11.8%, respectively. In summary, the effects

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of metal-based NPs on the edible portion of crops should be taken into account in the

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evaluation of nanotoxicity to terrestrial plants. Moreover, investigation of the

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potential impacts of NP caused nutrient alterations on human health could further our

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understandings on NP induced phytotoxicity.

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Keywords: Triticum aestivum L.; Ag NPs; amino acids; grains; micronutrients;

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phytotoxicity

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Introduction

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Silver nanoparticles (Ag NPs) is one of the most commonly used metal-based

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nanomaterials in industries and agriculture. Due to its excellent catalytic,

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superconducting properties and antibacterial activities,1 Ag NPs are widely used in a

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variety of processes such as manufacturing, biomedicine, textiles and etc.2,

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Reportedly, Ag is the most commonly used nanomaterial in consumer products,

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accounting for 435 (24%) of about 1814 NP-containing products.4 The mass

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production and application of Ag NPs have greatly increased the possibilities for

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environmental release and their potential risks to the environment and human health.

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Most studies have focused on the NPs phytotoxicity in a short term exposure and

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basic physiological response, including seed germination, root elongation and NPs

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transport/accumulation5, but lack of studies on the quality of the crops. Previous

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studies showed that Ag NPs caused physiological effects on seed germination of

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cucumber (Cucumis sativus L.), ryegrass (Lolium multifolrum L.), onion (Allium cepa

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L.), rice (Oryza sativa L.), castor (Ricinus commusnis L.).6-10 For example, A 12-day

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hydroponic experiment using rice as a model plant showed that 1000 mg·kg-1 Ag NPs

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physically destructed cell wall and damaged vacuoles in rice roots.9 Ag NPs decreased

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the number of duckweed (Lemna minor) leaves, lowered transpiration rate and

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reduced total biomass;11 Also, NPs could compromise the photosynthetic systems in

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terms of the levels of chlorophyll, soluble sugar and induce the excessive amounts of

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reactive oxygen species (ROS) in plants.12 Additionally, the presence of Ag NPs caused

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DNA damages in onion and tobacco (Nicotiana tabacum L.) roots.13 Similarly, Ag

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NPs in the root tip meristem of broad bean (Vicia faba L.) slowed down the cell cycle

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transformation rate, resulting in a decrease in mitotic index.7

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As an autotroph, plants are important components of the ecosystem. NPs can

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enter the food chain via plant. In assessing the toxicological effects of nanoparticles

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on the environment, plants should be considered as an important part of the ecosystem.

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Especially, it is of importance to investigate the effects of NPs on terrestrial plants in a

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full life cycle.14 A common finding in previous studies is that metal-based NP could

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accumulation in edible portions of plants. For instance, Zhao et al. has reported both

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Ce and Zn bioaccumulated in cucumber fruit by inductively coupled plasma-mass

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spectrometry (ICP-MS), indicates the possibility of introducing ions/ NPs into the

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food chain.15 In addition, Rui et al. found Ag NPs alteration of the contents of fatty

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acids in peanut grains which were cultivated in sandy soil. 16

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Wheat (Triticum aestivum L.) is a mono cotyledon, grass plant widely cultivated

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throughout the world. More than 40% of the protein that the human body intakes are

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supplied by wheat grain in north of China.17 In the present study, wheat was grown in

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three different concentrations (20, 200, 2000 mg·kg-1) of Ag NP amended soil for 4

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months. At harvest, we measured the physiological parameters, silver uptake, nutrient

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contents in the edible portions of wheat, as well as the analysis of amino acid profiles

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in Ag NP treated grains. The aim of the present study is to evaluate the phytotoxicity

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of Ag NP to wheat yields and food quality, providing more useful information for crop

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safety.

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Materials and Methods

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Preparation of Ag NPs/ Ag NPs characterization

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Bare Ag NPs were purchased from Shanghai Pantian Powder material Co., LTD.

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Transmission electron microscopy (TEM; JEM 200CX, Japan) was used to observe

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the particle morphology and measure particle size distribution (Figure 1). Briefly,

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NPs were dispersed in ethanol using a sonicator (KQ4200DE, China). The dispersed

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solution was air dried on a carbon coated 200-mesh copper grid and imaged under a

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TEM. The averaged particle size is 5.6 nm and the edges of NPs were neat and

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smooth. In addition, most of the nanoparticles were in ovoid shape and fell into in the

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size range of 3.1 ~ 8.7 nm in diameter.

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Pot experiment and plant growth conditions

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Experimental soil (sandy loam) was sampled from the top 15 cm by

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five-spot-sampling method at the Shangzhuang experimental station of China

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Agricultural University. The soil was air-dried for 24 h, sieved through 2 mm mesh.

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Soil was mixed with sand in a weight ratio of 3:1 (sand/sampled soil, v/v) in order to

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improve soil drainage, increase root respiration and prevent root rot. 36 plastic pots

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(18 cm diameter × 21 cm high) were filled with 3 kg of soil mixed with different

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amounts of Ag NPs powder based on the designated exposure doses, including 20,

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200, 2000 mg·kg-1. The total fertilizer (N: P2O5: K2O = 0.40: 0.47: 0.38 mg·kg-1 of

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the soil mixture) was applied in each treatment. The NP-amended soils were

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stabilized for 24 h prior to use.

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Wheat seeds (Liangxing NO.99) were purchased from Chinese Academy of

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Agricultural Sciences. The seeds were soaked in 10% sodium hypochlorite for 10

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minutes followed by repeatedly rinsing with deionized water. Nine replicates in each 5



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treatment were randomly arranged on the bench. Four seeds with uniform size were

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planted in each pot and the field capacity in each pot was maintained between 80 and

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85%.

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Determination of physiological parameters

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After three months of cultivation, the shoot height and fresh weight of wheat

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plant were measured. Briefly, three replicates were randomly selected from each

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treatment to determine the height of the aerial part, and then the upper part was

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harvested for biomass measurement. For the underground part, the pots were

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completely immersed in water and the soil attached onto the root surface was rinsed

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with tap water. All the plant samples were cleaned with tap water followed by rinsing

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three times with deionized water. Then, the fresh weight was determined in each

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treatment prior to oven-dry for element analysis. All tissues were placed at 105 °C for

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30 min and dried at 60 °C for 48 h until constant weight.

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At maturity, three replicates (pots) were randomly selected from each treatment to

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count the total number of wheat ears in each plant, and then randomly selected 100

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seeds to determine the 100-seed weight.

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Measurements of Ag and micronutrients in wheat

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The contents of Ag in wheat shoots, roots and grains and micronutrients (Fe, Zn

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and Cu) in the edible portions were measured by ICP-MS (Thermo-X7, USA). Briefly,

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the whole wheat plants were separated into roots, shoots and grains, and their dry

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biomass was recorded. The dry samples were ground to fine powders by the agate

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mortar and pestle and were digested in a mixture of plasma pure HNO3 and 30% (w/v)

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H2O2 (1:4) using a microwave accelerated reaction system (Speedwave MWS-2,

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Berghof, Germany). The digest was diluted with ultrapure water prior to analyze.

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Measurements of amino acids and total protein in wheat grains

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The contents of 16 kinds of amino acids in Ag NPs treated wheat grains were

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determined by using an automatic amino acid analyzer as described in Anjum, et al. 18.

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Briefly, the 0.1 g grounded grains was added into a test tube containing 10 mL of 6 N

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HCl and three drops of phenol. The tubes were frozen for five minutes and then

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concentrated using nitrogen blowing method. The concentrated samples were sealed

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and placed in an oven at 110 °C for 24 h. After cooling down to the ambient

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temperature, the hydrolysate was filtered and dried at 60 °C to remove HCl. The

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residue was dissolved in 2 mL water and oven dried. This procedure was repeated

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twice before dissolving in 1 mL of phosphate buffer (pH 2.2). Finally, the supernatant

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was used for determination of the contents of amino acids by automatic amino acid

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analyzer (L-8900, Japan). The protein analyzer (KDN-1000，China) was used to

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determine the protein concentration in Ag NP treated wheat grains.

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Statistical analysis

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The data are mean of three replicates ± standard error (SE). One-way ANOVA

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was used to analyze the experiment variance (SPSS 19.0 package, Chicago, IL)

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followed by Turkey’s Honestly Significant Difference test to determine statistical

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differences (p ≤ 0.05) between treatments.

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Results and Discussion

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Effects of Ag NPs on biomass and plant height

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Figure 2 shows physiological parameters of wheat treated with different

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concentrations of Ag NPs. Phenotypic images shows that Ag NPs severely inhibited

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plant growth in terms of plant size with increasing the exposure doses (Figure 2A).

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At the lowest exposure dose, the above ground part of wheat was smaller relative to

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the control, suggesting NP induced phytotoxicity. Additionally, compared with the

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control, decreases in the plant height, and fresh biomass were evident upon exposure

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to Ag NPs.

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Plant height, root length, and fresh biomass of wheat treated with different

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concentrations of Ag NPs were measured (Figure 2B and C). Compared with the

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control, the decrease in plant height was in a dose-response manner with increasing

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the exposure doses of Ag NPs (Figure 2B). The fresh biomass of shoots and roots in

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20 mg·kg-1 Ag NPs treatment slightly increased, but insignificant relative to the

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control (Figure 2C). In the 200 and 2000 mg·kg-1 treatments, the fresh biomass was

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sharply decreased. For example, at the concentration of 2000 mg·kg-1, the fresh

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biomass of shoots and roots were 0.79 and 0.44 g, respectively, which was reduced by

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73% and 60% relative to the respective control.

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Our results are in accordance with previous reports that Ag NPs impaired the 19-22

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plant growth.

Seedling length was negatively correlated with exposure

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concentrations of La2O3, Gd2O3 and Yb2O3 NPs, including radish (Raphanus

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sativus L.), tomato (Lycopersicon esculentum Mill.), lettuce (Lactuca sativa L.),

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wheat, cabbage (Brassica oleracea L.), rape (Brassica napus L.) and cucumber.19

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Exposure to 250 mg·kg-1 La2O3 NPs severely altered the root thickness, length and

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surface integrity of maize as compared to the control.20 It was reported that Ag NPs

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resulted in the inhibition of the root elongation and the reduction of the fresh biomass

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of Arabidopsis thaliana.21 Similar results were also found in Ag NPs treated wheat.22

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Although previous studies aligned with the findings that NPs could adversely impact

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on plant growth, the most studies were conducted at the seedling stage. Long-term

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studies could provide more realistic information regarding the effects of NPs on crop

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growth.

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Effects of Ag NPs on wheat grains

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At harvest, physiological parameters of mature wheat grains treated with different

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concentrations of Ag NPs were measured (Figure 3). The presence of Ag NPs

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inhibited the development of the edible portions of wheat as determined by the size of

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wheat ear (Figure 3A). Additionally, in the 200 and 2000 mg·kg-1 Ag NPs treatments,

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the wheat ear were still green as compared to the ones in control and 20 mg·kg-1 Ag

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NPs, suggesting that the presence of Ag NPs delayed the plant maturation. As shown

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in Figure 3B, the length of spike treated with 200 and 2000 mg·kg-1 Ag NPs was

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reduced by 15.4% and 27% as compared to the control, resulting in a negative linear

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curve fitting trend. Similarly, 200 and 2000 mg·kg-1 Ag NPs also decreased the

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number of seeds per pot by 15.9 and 23.7%, respectively (Figure 3C). High exposure

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dose (2000 mg·kg-1) of Ag NPs significantly reduced the 100-grain weight as

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compared to the control and other two NPs treatments (Figure 3D). Thus, exposure to

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Ag NPs could lower crop yield.

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Relevant studies regarding metal-based NP impacts on edible portion of crops

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have been reported.23, 24 Jie et al. reported that NPs altered the contents of mineral

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elements in mature cucumber, consequently decreasing food quality and crop yield.25

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The presence of TiO2 NPs (0.2, 1.0, 2.0, and 4.0%) delayed the seed germination of

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maize and resulted in the reduction of mitotic index and the increase of chromosomal

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aberrations in the first 24 h exposure.26 CuO NPs decreased the shoot and root growth

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of chickpea (Cicer arietinum L.) and greatly induced the levels of ROS, which could

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be one of the most important reasons that caused the cytotoxicity in root cells.27 Wang

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et al. reported that CeO2 NPs increased the fruit biomass of tomato by extending the

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growth cycle.28 However, exposure to 500 mg·kg-1 CeO2 NPs significantly increased

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the wheat grain yield as compared to the control.29 Rui et al. noted per plant yield of

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peanuts showed a negative dose-response manner with increasing the exposure doses

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of Ag NPs, similar to our findings, high exposure dose of Ag NPs dramatically

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reduced the 1000-grain weight of peanuts.16 The decreases in the total numbers of

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corn (Zea mays L.) cobs were evident upon exposure to 400 and 800 mg·kg-1 CeO2

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and ZnO NPs. Additionally, NP ZnO caused inhibition of flower fertilization or

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pollination in corn, suggesting greater phytotoxicity than that induced by NP CeO2.30

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Given the evidence that NPs resulted in the reduction of crop yields, the further

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investigations on simulating NPs applications with a realistic environmental

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concentration in agricultural fields should be conducted among different crop species.

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Ag contents in Ag NPs treated wheat

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The Ag contents in shoots, roots and grains treated with different concentrations

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of Ag NPs were determined (Figure 4). The Ag contents in different concentrations

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of Ag NPs treated roots were approximately 3.33, 10.8, 15.2-fold of the control with

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increasing the exposure doses of Ag NPs. However, there was no difference among

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all the three Ag NPs treatments. A dose-response fashion of Ag accumulation in

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wheat shoots and grains was evident. The Ag contents in the Ag NPs treated roots

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were significantly higher than that in the shoots and grains. Evidence for the Ag

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accumulation in wheat grains implied the potential risk to food chains and human

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health.

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Previous studies have demonstrated that metal-based NPs could accumulate in

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the roots and translocate to the aboveground part. Ma et al. also reported that Ag NPs

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accumulated in Crambe abyssinica roots and translocated to shoots.31 Ag accumulated

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in Potamogeton crispus L. increased in a dose-dependent manner and caused the

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considerable physiological, biochemical and ultrastructural alterations 32. Using X-ray

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fluorescence (XRF), Stegemeier et al. found that Ag NPs accumulated in the root

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apoplast of alfalfa (Medicago sativa), and mainly accumulated in the border cells and

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elongation zone. 1 Recent studies showed that Si NPs and CeO2 NPs were transported

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from roots to shoots via xylem sap in cotton (Gossypium spp) .33, 34 Ag NPs might also

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be transported via xylem route to the edible portion of peanuts.16 NPs could

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accumulate in plants, which provides the basis for our research on food safety and

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subsequently pose the potential risks to human health.

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Other factors (solubility, plant species, culture medium and etc.) could also

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determine the NP accumulation in plants. Metal accumulation in plants is mostly

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dependent on metal speciation. For example, the contents of Ag in AgNO3 and Ag

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NPs treated barley (Hordeum vulgare L.) leaves were 18.16 and 4.75 mg·kg-1,

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respectively.35 Upon 500 mg·kg-1 CeO2 NPs exposure, the Ce contents in rice grains

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were approximately 14.4-fold as compared with soybean pod.36,

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substrates is another factor that can determine metal/NP accumulation in plants.

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Plant growth


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Previous studies demonstrated that the Ce accumulation in lettuce seedlings grown in

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agar, potting mix and sand, was notably different.38-40 Metal-based NPs could enter

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the plant cells via physical damage, endocytosis, water or ionic channels, complexion

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with carrier proteins or root exudates and so forth.41-43

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According with the National Food Hygiene Standard of China (NFHSC), the

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acceptable daily intake of Ag in food is 35.4μg. We should pay attention to the

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rational use of Ag NPs products and its disadvantages as Judy et al. has confirmed

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NPs can transfer through food chain and biomagnification in ecosystem.44 There are

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trophic transfer and biomagnification of TiO2 NPs from daphnia to zebrafish as Zhu et

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al. had described.45 These studies are enough to draw our attention to the safety of the

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use of Ag NPs since Ag might be accumulated in human being via food chain by

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assuming the wheat.

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The contents of micronutrients in wheat grains

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Abiotic and biotic stressors affected nutrient uptake and mineral storage in

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plants .46 Hence, it is necessary to investigate the changes of micronutrient contents in

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Ag NP treated crops. Figure 5 shows the contents of micronutrients, Fe, Cu，Zn, in

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different Ag NPs treated wheat. A common trend among all the three elements was

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that exposure to higher concentrations of Ag NPs significantly lowered the nutrient

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contents in wheat grains. Fe plays an important role in chlorophyll synthesis and

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directly involves in plant photosynthesis. When exposed to 2000 mg·kg-1 Ag NPs, the

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Fe content was only 0.5-fold of the control. Other Ag NP treatments also caused

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decreases in the Fe contents, but insignificant. Zn is an important component in auxin

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synthesis and in the enzymes of the metal activators. The Zn content was significantly

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decreased by 32.7% and 60% NPs in 200 and 2000 mg·kg-1 Ag NP treated grains,

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respectively. As a structural element of some metal proteins, Cu can participate in the

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electron transfer in the chloroplasts and mitochondria, as well as the oxidative stress

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of plants.47 Similar to the contents of Fe and Zn, the Cu contents markedly were

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reduced by 15.85% and 48.58% in 200 and 2000 mg·kg-1 Ag NPs treated grains,

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respectively.

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Micronutrients are necessary for plant normal growth and development. Decreases

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in the levels of micronutrients can result in the reduction of crop quality and yield. Ag

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NPs (5 ~ 12 nm) caused a significant decrease in the levels of Fe and Zn in

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Arabidopsis leaves.21 32% and 40% decreases in Cu contents were found in bean

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shoot grown in 250 and 500 mg·kg-1 ZnO NP amended soil.48 It was reported that Zn

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and Cu share the same transporter, and high levels of Zn could reduce the Cu uptake

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due to antagonistic effects.1, 49 Dimkpa et al. reported that ZnO NPs altered the uptake

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of Fe and Mn in beans due to the increased bioavailability of Zn; additionally, the

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transcription levels of genes encoding metal ion transporters or specific enzyme

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activities were altered upon ZnO NP exposures.50 Rico et al. found that the contents of

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Fe and S in CeO2 NPs treated rice were lower than the control.37 Similarly, Ag and

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CeO2 NPs also caused nutrient displacement in tomato fruit and cotton, respectively.33,

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51

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plant roots, and directly or indirectly block the passages of aquaporin proteins and

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metal transports, both of which determine the levels of mineral nutrients in plants.20

Previous studies also demonstrated that NPs could accumulate on the surface of

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Analysis of amino acids and protein in Ag NPs treated wheat grains

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The contents of amino acid in different concentrations of Ag NPs treated wheat

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grain are shown in Table 1. Increased levels of Zn and other metals could notably

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enhance histidine production in plants.52 Exposure to 20 and 200 mg·kg−1 Ag NPs

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decreased the histidine content by 5.9 and 2.9%, respectively, relative to the control.

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Decreases in the histidine contents upon exposure to Ag NPs suggested that the

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bioavailability of Zn or other nutrient elements were lowered, which was consistent

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with the results of nutrient displacement in Figure 5. Aspartic acid and glutamic acid

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play an important role in nitrogen transport and storage.53 The content of aspartic acid

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was only decreased by 2.8% in the 200 mg·kg−1 Ag NP treatment. However, exposure

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to 2000 mg·kg−1 Ag NPs resulted in 8.3% and 7.9% in the contents of aspartic and

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glutamic acid, respectively. Leucine and glutamic acid were predominant in wheat

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grains, both accounting for 46% of the total amino acids in the control and the ratio

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had no change in Ag NPs treatments. Both leucine and isoleucune belong to the

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branched chain amino acids (BCAAs) and can provide an alternative source of

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energy.54 In the 2000 mg·kg−1 Ag NPs treatment, the content of leucine and

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isoleucune was decreased by 8.8% and 11.1%, respectively. Additionally, across the

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treatments with 20 and 200 mg·kg−1 Ag NPs, most of the amino acid contents were

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not significantly changed. However, as the exposure dose of Ag NPs increased to

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2000 mg·kg−1, the levels of most of the amino acids were significantly decreased,

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while there were some exceptions, including serine, glycine, cysteine, valine, and etc.,

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all of whose contents were not changed as compared to their respective control. The

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total protein content in 200 and 2000 mg·kg−1 Ag NPs treatments was decreased by

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2.8% and 12.1%, respectively, relative to the control.

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Wheat nutrient quality is mainly determined by the balance of amino acid content

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and protein content of wheat grain, and its level is directly related to the degree of

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human nutrition utilization.18 Therefore, it is important to study the effects of Ag NPs

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on amino acid compositions and protein content in wheat grains. Rico et al. reported 14


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that cerium oxide (CeO2) NPs had no impact on alanine, cysteine, leucine, methionine,

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proline and glutamic acid content, but exposure to 62.5 mg·kg-1 CeO2 increased the

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levels of aspartic acid, glycine, lysine, histidine and arginine.55 In CeO2 and TiO2 NP

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treated barely kernels (Hordeum vulgare L.), the contents of cysteine, glutamic acid,

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lysine and proline were increased by 17.4~62.9 % relative to the control.56 Olkhovych

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et al. suggested that the increases in amino acids were to maintain homeostasis in

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plants.57 The contents of proline in Spirodela polyrhiza was increased significantly by

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AgNO3 and Ag NPs exposure 58, which probably attributed to that proline can play a

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role in chelating heavy metals, scavenging free radicals, maintaining water balance

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and protecting plants under metal stress.59

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The presence of Ag NPs altered the protein contents at the plant seedling stage

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has been reported.60 Exposure to 200 mg·kg−1 TiO2 NPs resulted in a more than 20%

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reduction of the protein content in A. thaliana shoots,61 aligning with our findings.

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Evidence for the elevations of the protein contents could be ascribed to abiotic

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stresses induced plant defense mechanisms. For examples, the content glutelin were

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reduced in rice grain in the 125 mg·kg−1 CeO2 NP treatment.37 Upon exposure to 400

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mg·kg−1 CeO2 NPs, the glutelin content in cucumber fruit was notably decreased by

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65%, whereas 25% increases were evident at 800 mg·kg−1 CeO2 NPs.62

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There are many studies on the bioavailability of Ag NPs and Ag+, which suggest

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that the toxic effects of Ag NPs may be caused by Ag+.63 However, up to now, it is

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still debatable whether the toxicity of Ag NPs is caused by Ag+ released or itself.

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Both Ag NPs and ions treatment heighten the oxidized glutathione (GSSG) in wheat

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cultivate 14 days in a sand matrix.22 Jiang et al. found that 0.5 mg·L-1 Ag NPs caused

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root exfoliation, but higher concentrations of AgNO3 (5, 10 mg·L-1) did not cause

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same effect, and the study found the conversion of Ag NPs to Ag+ is less than 3%,

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indicating that Ag+ is not a major factor contributing to the toxicity of Ag NPs.58 In

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addition, when Ag NPs were applied to mung bean( Vigna radiate L) and

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sorghum(Sorghum bicolor L), it was found that Ag+ played a major role in agarose,

356

whereas Ag NPs toxicity was mainly induced by the particle properties in soil.

357

On one hand, it may be related to the presence of a large number of binding ligands

358

(such as thiols, sulfides, chlorides, phosphates, etc.) in the soil, thus reducing the

359

bioavailability of Ag+

360

followed by chemical or photochemical reduction to Ag NPs.68

66, 67

64, 65

+

; On the other hand, Ag NPs being converted to Ag ,

361

In conclusions, the impacts of NPs on the nutrient composition of crops have not

362

yet been fully studied. Many studies have shown that Ag NPs modulated fatty acid in

363

peanus,16 Au NPs altered the oil content of Brassica juncea leaves

364

affected the sugars, lignin contents in rice

365

lettuce.40 In the present study, wheat was grown in Ag NPs-amended agricultural soils

366

until maturity. Our results suggested that Ag NPs significantly inhibited plant growth

367

and delayed the wheat ripening. Besides the significant reduction of crop yield, the

368

results of the contents of micronutrients, amino acids and protein in Ag NPs treated

369

wheat grains suggested that the presence of Ag NPs could significantly alter the crop

370

quality. Our findings could provide important and useful information for evaluation

371

on the safety of metal-based NP application in agriculture and human health.

29, 37

69

and CeO2 NPs

and nitrate and starch levels in

16


Page 17 of 29


372

373

Acknowledgement

374

The project was supported by National Key R ＆ D Program of China

375

(2017YFD0801300), National Natural Science Foundation of China (No. 41371471

376

and No. 41130526), NSFC-Guangdong Joint Fund (U1401234) and BARD

377

（IS-4964-16R）.

378 379

Reference

380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408

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43.Kurepa, J.; Paunesku, T.; Vogt, S.; Arora, H.; Rabatic, B. M.; Lu, J.; Wanzer, M. B.; Woloschak, G. E.; Smalle, J. A., Uptake and distribution of ultrasmall anatase TiO2 Alizarin red S nanoconjugates in Arabidopsis thaliana. Nano Lett. 2010, 10, 2296-2302. 44.Judy, J. D.; Unrine, J. M.; Bertsch, P. M., Evidence for biomagnification of gold nanoparticles within a terrestrial food chain. Environ. Sci. Technol. 2011, 45, 776-81. 45.Zhu, X.; Wang, J.; Zhang, X.; Chang, Y.; Chen, Y., Trophic transfer of TiO2 nanoparticles from daphnia to zebrafish in a simplified freshwater food chain. Chemosphere. 2010, 79, 928. 46.Marschner, H.; Rimmington, G., Mineral nutrition of higher plants. Plant Cell Environ. 1988, 11, 147-148. 47.Inmaculada, Y., Copper in plants: acquisition, transport and interactions. Funct. Plant Biol. 2009, 36, 409-430. 48.Medina-Velo, I. A.; Barrios, A. C.; Zuverza-Mena, N.; Hernandez-Viezcas, J. A.; Chang, C. H.; Ji, Z.; Zink, J. I.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L., Comparison of the effects of commercial coated and uncoated ZnO nanomaterials and Zn compounds in kidney bean (Phaseolus vulgaris) plants. J. Hazard. Mater. 2017, 332, 214-222. 49.Bañuelos, G. S.; Ajwa, H. A., Trace Elements in Soils and Plants. J Environ.Sci.Heal A. 1999, 34, 951-974. 50.Dimkpa, C. O.; Hansen, T.; Stewart, J.; Mclean, J. E.; Britt, D. W.; Anderson, A. J., ZnO nanoparticles and root colonization by a beneficial pseudomonad influence essential metal responses in bean (Phaseolus vulgaris). Nanotoxicology. 2015, 9, 271. 51.Vittori, A. L.; Carbone, S.; Gatti, A.; Vianello, G.; Nannipieri, P., Uptake and translocation of metals and nutrients in tomato grown in soil polluted with metal oxide (CeO₂, Fe₃O₄, SnO₂, TiO₂) or metallic (Ag, Co, Ni) engineered nanoparticles. Environ. Sci. Pollut. Res. Int. 2015, 22, 1841. 52.Salt, D. E.; Prince, R. C.; Baker, A. J.; Raskin, I.; Pickering, I. J., Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ. Sci. Technol. 1999, 33, 713-717. 53.Gaufichon, L.; Reisdorf-Cren, M.; Rothstein, S. J.; Chardon, F.; Suzuki, A., Biological functions of asparagine synthetase in plants. Plant Sci. 2010, 179, 141-153. 54.Heazlewood, J. L.; Day, D. A.; Millar, A. H., Lipoic Acid-Dependent Oxidative Catabolism of α-Keto Acids in Mitochondria Provides Evidence for Branched-Chain Amino Acid Catabolism in Arabidopsis. Plant Physiol. 2004, 134, 838. 55.Rico, C. M.; Lee, S. C.; Rubenecia, R.; Mukherjee, A.; Hong, J.; Peraltavidea, J. R.; Gardeatorresdey, J. L., Cerium oxide nanoparticles impact yield and modify nutritional parameters in wheat (Triticum aestivum L.). J. Agric. Food Chem. 2014, 62, 9669. 56.Pošćić, F.; Mattiello, A.; Fellet, G.; Miceli, F.; Marchiol, L., Effects of Cerium and Titanium Oxide Nanoparticles in Soil on the Nutrient Composition of Barley (Hordeum vulgare L.) Kernels. Inter. J. Env Res.Pub He. 2016, 13, 577. 57.Olkhovych, O.; Volkogon, M.; Taran, N.; Batsmanova, L.; Kravchenko, I., The effect of copper and zinc nanoparticles on the growth parameters, contents of ascorbic acid, and qualitative composition of amino acids and acylcarnitines in Pistia stratiotes L.(Araceae). Nanoscale Res.Lett. 2016, 11, 218. 58.Jiang, H. S.; Li, M.; Chang, F. Y.; Li, W.; Yin, L. Y., Physiological analysis of silver nanoparticles and AgNO3 toxicity to Spirodela polyrhiza. Environ. Toxicol. Chem. 2012, 31, 1880. 59.Mallick, N., Copper-induced oxidative stress in the chlorophycean microalga Chlorella vulgaris:

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response of the antioxidant system. J. Plant Physiol. 2004, 161, 591. 60.Krishnaraj, C.; Jagan, E.; Ramachandran, R.; Abirami, S.; Mohan, N.; Kalaichelvan, P., Effect of biologically synthesized silver nanoparticles on Bacopa monnieri (Linn.) Wettst. plant growth metabolism. Process Biochem. 2012, 47, 651-658. 61.Liu, H.; Ma, C.; Chen, G.; White, J. C.; Wang, Z.; Xing, B.; Dhankher, O. P., Titanium Dioxide Nanoparticles

Alleviate

Tetracycline

Toxicity

to

Arabidopsis

thaliana

(L.).

ACS

Sustain.Chem.Eng. 2017, 5, 3204-3213. 62.Zhao, L.; Peralta-Videa, J. R.; Rico, C. M.; Hernandez-Viezcas, J. A.; Sun, Y.; Niu, G.; Servin, A.; Nunez, J. E.; Duarte-Gardea, M.; Gardea-Torresdey, J. L., CeO₂ and ZnO nanoparticles change the nutritional qualities of cucumber (Cucumis sativus). J. Agric. Food Chem. 2014, 62, 2752. 63.Navarro, E.; Piccapietra, F.; Wagner, B.; Marconi, F.; Kaegi, R.; Odzak, N.; Sigg, L.; Behra, R., Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ. Sci. Technol. 2008, 42, 8959-64. 64.Yin, L.; Colman, B. P.; Mcgill, B. M.; Wright, J. P.; Bernhardt, E. S., Effects of Silver Nanoparticle Exposure on Germination and Early Growth of Eleven Wetland Plants. PLoS One. 2012, 7, e47674. 65.Lee, W. M.; Jin, I. K.; An, Y. J., Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor : Media effect on phytotoxicity. Chemosphere. 2012, 86, 491-9. 66.Xiu, Z. M.; Ma, J.; Alvarez, P. J., Differential effect of common ligands and molecular oxygen on antimicrobial activity of silver nanoparticles versus silver ions. Environ. Sci. Technol. 2011, 45, 9003. 67.Reinsch, B. C.; Levard, C.; Li, Z.; Ma, R.; Wise, A.; Gregory, K. B.; Jr, B. G.; Lowry, G. V., Sulfidation of silver nanoparticles decreases Escherichia coli growth inhibition. Environ. Sci. Technol. 2012, 46, 6992-7000. 68.Glover, R. D.; Miller, J. M.; Hutchison, J. E., Generation of Metal Nanoparticles from Silver and Copper Objects: Nanoparticle Dynamics on Surfaces and Potential Sources of Nanoparticles in the Environment. Acs Nano. 2011, 5, 8950. 69.Arora, S.; Kumar, S.; Nayan, R.; Khanna, P. K.; Zaidi, M. G. H., Gold-nanoparticle induced enhancement in growth and seed yield of Brassica juncea. Plant Growth.Regul. 2012, 66, 303-310.

572 573 574 575 576 577 578 21



579

Figure captions

580

Fig. 1. TEM images of Ag NPs used in this experiment. (A) is observed at a scale of

581

200 nm；(B) is a local enlarged drawing of (A), which scale is 50nm.

582

Fig 2. Physiological responses of wheat upon exposure to different concentrations of

583

Ag NPs. Fig. A represents phenotypical image of wheat grown in Ag NPs amended

584

soil; Fig. B and C represent plant height and fresh biomass, respectively. Error bars

585

represent standard error (n=3), and same letters mean no statistical difference between

586

treatments at Turkey’s test (p ≤ 0.05).

587

Fig 3. Physiological responses of wheatear and wheat grains upon exposure to

588

different concentrations of Ag NPs. Fig. A represents phenotypical image of wheatear

589

treated with different concentrations of Ag NPs. Fig. B-D show the results of spike

590

length, number of grains per pot, and 100-grain weight, respectively. Error bars

591

represent standard error (n=3), and same letters mean no statistical difference between

592

treatments at Turkey’s test (p ≤ 0.05).

593

Fig 4. Ag contents in different exposure doses of Ag NP treated wheat. Insert shows

594

the Ag content in grains. Error bars represent standard error (n=3), and the same

595

letters mean no statistical difference between treatments at Turkey’s test (p ≤ 0.05).

596

Fig 5. Micronutrient contents in different exposure doses of Ag NP treated wheat

597

grains. Error bars represent standard error (n=3), and the same letters mean no

598

statistical difference between treatments at Turkey’s test (p ≤ 0.05).

599 600 601

22


Page 22 of 29

Page 23 of 29


602

Table 1. The contents of amino acids in wheat grains grown in Ag NPs-amended Soil (g/100g grains) Ag NPs (mg·kg−1 soil) Control alanine arginine aspartic acid cysteine glycine glutamic acid histidine isoleucine leucine lysine methionine phenylalanine serine threonine tyrosine valine protein

0.52±0.01 a 0.69±0.03 a 0.72±0.05 a 0.34±0.02 a 0.58±0.02 a 5.07±0.10 a 0.34±0.01 a 0.54±0.03 a 1.14±0.05 a 0.37±0.02 a 0.22±0.02 a 0.78±0.04 a 0.73±0.03 a 0.39±0.02 a 0.45±0.02 a 0.69±0.03 a 1.81±0.10 a

20

200

0.48±0.02 ab 0.67±0.02 a 0.68±0.02 ab 0.35±0.01 a 0.53±0.04 a 5.07±0.10 a 0.32±0.01 b 0.57±0.02 a 1.10±0.03 ab 0.38±0.01 a 0.21±0.01 a 0.76±0.02 a 0.70±0.02 a 0.38±0.01 ab 0.47±0.04 a 0.65±0.00 a 1.65±0.05 ab

0.70±0.03 b 0.37±0.01 ab 0.72±0.02 a 0.58±0.03 a 0.51±0.03 ab 0.35±0.03 a 0.66±0.04 a 0.22±0.00 a 0.56±0.03 a 1.13±0.03 a 0.45±0.03 a 0.79±0.02 a 0.38±0.01 a 0.33±0.00 ab 0.67±0.02 a 5.29±0.21 a 1.76±0.05 bc

2000 0.66±0.02 b 0.36±0.00 b 0.70±0.03 a 0.56±0.02 a 0.47±0.00 b 0.33±0.01 a 0.65±0.01 a 0.21±0.01 a 0.48±0.00 b 1.04±0.03 b 0.49±0.02 a 0.69±0.03 b 0.34±0.01 b 0.30±0.01 c 0.60±0.01 b 4.67±0.22 b 1.59±0.11 c

Note: Error bars represent standard error (n=3), and the same letters mean no statistical difference between treatments at Turkey’s test (p ≤ 0.05).

23



Figure 1

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Figure 2

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Figure 3

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Figure 4

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Figure 5

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603 604

TOC Graphic

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Alteration of Crop Yield and Quality of Wheat upon Exposure to Silver

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