Alteration of Crop Yield and Quality of Wheat upon ... - ACS Publications

Subscriber access provided by UNIV OF DURHAM

Article

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

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Journal of Agricultural and Food Chemistry is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 29

Journal of Agricultural and Food Chemistry

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

1 2

nanoparticles in a life cycle study

3

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

4

Rui1,Muhammad Adeel1, Weidong Cao4, Baoshan Xing3,

5

1

6

College of Resources and Environmental Sciences, China Agricultural University,

7

Beijing, China

8

2

9

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

10

3

11

Massachusetts 01003, United States

12

4

13

of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural

14

Sciences, Beijing, China

15

Corresponding authors:

16

*

17

*

18

†

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.

19 20 21 22

1

ACS Paragon Plus Environment


23

Abstract

24

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

25

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

26

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

27

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

28

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

29

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

30

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

31

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

32

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

33

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

34

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

35

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

36

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

37

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

38

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

39

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

40

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

41

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

42

understandings on NP induced phytotoxicity.

43

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

44

phytotoxicity

45 46

2


Page 2 of 29

Page 3 of 29


47

Introduction

48

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

49

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

50

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

51

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

52

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

53

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

54

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

55

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

3

56

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

57

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

58

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

59

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

60

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

61

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

62

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

63

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

64

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

65

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

66

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

67

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

68

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

3



69

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

70

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

71

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

72

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

73

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

74

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

75

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

76

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

77

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

78

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

79

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

80

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

81

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

82

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

83

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

84

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

85

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

86

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

87

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

88

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

89

safety.

90

4


Page 4 of 29

Page 5 of 29


91

Materials and Methods

92

Preparation of Ag NPs/ Ag NPs characterization

93

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

94

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

95

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

96

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

97

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

98

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

99

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

100

size range of 3.1 ~ 8.7 nm in diameter.

101

Pot experiment and plant growth conditions

102

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

103

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

104

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

105

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

106

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

107

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

108

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

109

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

110

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

111

stabilized for 24 h prior to use.

112

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

113

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

114

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



115

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

116

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

117

85%.

118

Determination of physiological parameters

119

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

120

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

121

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

122

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

123

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

124

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

125

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

126

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

127

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

128

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

129

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

130

seeds to determine the 100-seed weight.

131

Measurements of Ag and micronutrients in wheat

132

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

133

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

134

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

135

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

136

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

6


Page 6 of 29

Page 7 of 29


137

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

138

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

139

Measurements of amino acids and total protein in wheat grains

140

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

141

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

142

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

143

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

144

concentrated using nitrogen blowing method. The concentrated samples were sealed

145

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

146

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

147

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

148

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

149

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

150

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

151

determine the protein concentration in Ag NP treated wheat grains.

152

Statistical analysis

153

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

154

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

155

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

156

differences (p ≤ 0.05) between treatments.

157 158

Results and Discussion

7



159

Effects of Ag NPs on biomass and plant height

160

Figure 2 shows physiological parameters of wheat treated with different

161

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

162

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

163

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

164

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

165

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

166

to Ag NPs.

167

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

168

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

169

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

170

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

171

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

172

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

173

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

174

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

175

73% and 60% relative to the respective control.

176

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

177

plant growth.

Seedling length was negatively correlated with exposure

178

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

179

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

180

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

8


Page 8 of 29

Page 9 of 29


181

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

182

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

183

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

184

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

185

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

186

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

187

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

188

growth.

189 190

Effects of Ag NPs on wheat grains

191

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

192

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

193

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

194

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

195

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

196

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

197

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

198

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

199

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

200

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

201

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

202

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

203

Ag NPs could lower crop yield.

9



204

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

205

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

206

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

207

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

208

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

209

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

210

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

211

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

212

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

213

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

214

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

215

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

216

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

217

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

218

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

219

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

220

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

221

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

222

investigations on simulating NPs applications with a realistic environmental

223

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

224 225

Ag contents in Ag NPs treated wheat

226

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

227

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

228

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

10


Page 10 of 29

Page 11 of 29


229

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

230

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

231

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

232

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

233

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

234

health.

235

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

236

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

237

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

238

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

239

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

240

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

241

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

242

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

243

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

244

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

245

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

246

subsequently pose the potential risks to human health.

247

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

248

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

249

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

250

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

251

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

252

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

253

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

11


37

Plant growth


254

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

255

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

256

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

257

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

258

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

259

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

260

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

261

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

262

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

263

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

264

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

265

assuming the wheat.

266 267

The contents of micronutrients in wheat grains

268

Abiotic and biotic stressors affected nutrient uptake and mineral storage in

269

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

270

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

271

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

272

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

273

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

274

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

275

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

276

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

277

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

12


Page 12 of 29

Page 13 of 29


278

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

279

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

280

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

281

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

282

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

283

respectively.

284

Micronutrients are necessary for plant normal growth and development. Decreases

285

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

286

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

287

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

288

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

289

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

290

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

291

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

292

transcription levels of genes encoding metal ion transporters or specific enzyme

293

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

294

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

295

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

296

51

297

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

298

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

299 300

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

301

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

302

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

13



303

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

304

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

305

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

306

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

307

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

308

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

309

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

310

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

311

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

312

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

313

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

314

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

315

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

316

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

317

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

318

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

319

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

320

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

321

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

322

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

323

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

324

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

325

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

326

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

327

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


Page 14 of 29

Page 15 of 29


328

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

329

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

330

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

331

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

332

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

333

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

334

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

335

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

336

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

337

and protecting plants under metal stress.59

338

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

339

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

340

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

341

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

342

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

343

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

344

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

345

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

346

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

347

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

348

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

349

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

15



Page 16 of 29

350

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

351

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

352

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

353

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

354

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

355

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

1.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, 8451. 2.Chen, X.; Schluesener, H. J., Nanosilver: A nanoproduct in medical application. Toxicol. Lett. 2008, 176, 1. 3.Lee, H. Y.; Park, H. K.; Lee, Y. M.; Kim, K.; Park, S. B., A practical procedure for producing silver nanocoated fabric and its antibacterial evaluation for biomedical applications. Chem. Commun. 2007, 28, 2959. 4.Vance, M. E.; Kuiken, T.; Vejerano, E. P.; Mcginnis, S. P.; Jr, H. M.; Rejeski, D.; Hull, M. S., Nanotechnology in the real world: Redeveloping the nanomaterial consumer products inventory. BEILSTEIN J NANOTECH.2015, 6, 1769-80. 5.Wang, Z.; Xu, L.; Zhao, J.; Wang, X.; White, J. C.; Xing, B., CuO Nanoparticle Interaction with Arabidopsis thaliana: Toxicity, Parent-Progeny Transfer, and Gene Expression. Environ. Sci. Technol. 2016, 50, 6008. 6.El‐Temsah, Y. S.; Joner, E. J., Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environ. Toxicol. 2015, 27, 42-49. 7.Patlolla, A. K.; Berry, A.; May, L. B.; Tchounwou, P. B., Genotoxicity of Silver Nanoparticles in Vicia faba: A Pilot Study on the Environmental Monitoring of Nanoparticles. J. Env Res.Pub He. 2012, 9, 1649-1662. 8.Panda, K. K.; Achary, V. M.; Krishnaveni, R.; Padhi, B. K.; Sarangi, S. N.; Sahu, S. N.; Panda, B. B., In vitro biosynthesis and genotoxicity bioassay of silver nanoparticles using plants. Toxico. in Vitro. 2011, 25, 1097-1105. 9.Mazumdar, H., Phytotoxicity effect of Silver nanoparticles on Oryza sativa. Int. J. Chem. Res. 2011, 3, 1494-1500. 10.Yasur, J.; Rani, P. U., Environmental effects of nanosilver: impact on castor seed germination, seedling growth, and plant physiology. Environ. Sci. Pollut. Res. 2013, 20, 8636-8648. 11.Gubbins, E. J.; Batty, L. C.; Lead, J. R., Phytotoxicity of silver nanoparticles to Lemna minor L. Environ. Pollut. 2011, 159, 1551. 17



409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452

12.Ma, C.; White, J. C.; Dhankher, O. P.; Xing, B., Metal-Based Nanotoxicity and Detoxification Pathways in Higher Plants. Environ. Sci. Technol. 2015, 49, 7109. 13.Ghosh, M.; Manivannan, J.; Sinha, S.; Chakraborty, A.; Mallick, S. K.; Bandyopadhyay, M.; Mukherjee, A., In vitro and in vivo genotoxicity of silver nanoparticles. Mutat. Res.Genet. Toxicol. Environ. Mutag. 2012, 749, 60-69. 14.Yang, J.; Cao, W.; Rui, Y., Interactions between nanoparticles and plants: phytotoxicity and defense mechanisms. Plant Interact. 2017, 12, 158-169. 15.Zhao, L.; Sun, Y.; Hernandezviezcas, J. A.; Servin, A. D.; Hong, J.; Niu, G.; Peraltavidea, J. R.; Duartegardea, M.; Gardeatorresdey, 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, 11945. 16.Rui, M.; Ma, C.; Tang, X.; Yang, J.; Jiang, F.; Pan, Y.; Xiang, Z.; Hao, Y.; Rui, Y. K.; Cao, W., Phytotoxicity of silver nanoparticles to peanut ( Arachis hypogaea L.): physiological responses and food safety. ACS Sustain.Chem. 2017. 17.Jiang, X.; Tian, J.; Zhi, H.; Zhang, W., Protein content and amino acid composition in grains of wheat-related species. Agric Sci China. 2008, 7, 272-279. 18.Anjum, F. M.; Ahmad, I.; Butt, M. S.; Sheikh, M. A.; Pasha, I., Amino acid composition of spring wheats and losses of lysine during chapati baking. J. Food Compos.Anal. 2005, 18, 523-532. 19.Ma, Y.; Kuang, L.; He, X.; Bai, W.; Ding, Y.; Zhang, Z.; Zhao, Y.; Chai, Z., Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere. 2010, 78, 273-279. 20.Yue, L.; Ma, C.; Zhan, X.; White, J. C.; Xing, B., Molecular mechanisms of maize seedling response to La2O3 NP exposure: water uptake, aquaporin gene expression and signal transduction. Environ. Sci. Nano.2017, 4. 21.Qian, H.; Peng, X.; Han, X.; Ren, J.; Sun, L.; Fu, Z., Comparison of the toxicity of silver nanoparticles and silver ions on the growth of terrestrial plant model Arabidopsis thaliana. J. Environ. Sci. 2013, 25, 1947-1956. 22.Dimkpa, C. O.; Mclean, J. E.; Martineau, N.; Britt, D. W.; Haverkamp, R.; Anderson, A. J., Silver nanoparticles disrupt wheat (Triticum aestivum L.) growth in a sand matrix. Environ. Sci. Technol. 2013, 47, 1082-1090. 23.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, 11945-11951. 24.Song, U.; Jun, H.; Waldman, B.; Roh, J.; Kim, Y.; Yi, J.; Lee, E. J., Functional analyses of nanoparticle toxicity: a comparative study of the effects of TiO 2 and Ag on tomatoes (Lycopersicon esculentum). Ecotoxicol. Environ. Saf.2013, 93, 60-67. 25.Jie, H.; Wang, L.; Sun, Y.; Zhao, L.; Niu, G.; Tan, W.; Rico, C. M.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L., Foliar applied nanoscale and microscale CeO 2 and CuO alter cucumber ( Cucumis sativus ) fruit quality. Sci. Total Environ. 2016, s 563–564, 904-911. 26.Castiglione, M. R.; Giorgetti, L.; Geri, C.; Cremonini, R., The effects of nano-TiO 2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis L. and Zea mays L. J. Nanopart. Res. 2011, 13, 2443-2449. 27.Nair, P. M. G.; Chung, I. M., Changes in the Growth, Redox Status and Expression of Oxidative Stress Related Genes in Chickpea ( Cicer arietinum L.) in Response to Copper Oxide Nanoparticle

18


Page 18 of 29

Page 19 of 29


453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496

Exposure. J. Plant Growth Regul. 2015, 34, 350-361. 28.Wang, Q.; Ma, X.; Zhang, W.; Pei, H.; Chen, Y., The impact of cerium oxide nanoparticles on tomato (Solanum lycopersicum L.) and its implications for food safety. Metallomics. 2012, 4, 1105. 29.Rico, C. M.; Morales, M. I.; Mccreary, R.; Castillo-Michel, H.; Barrios, A. C.; Hong, J.; Tafoya, A.; Lee, W. Y.; Varela-Ramirez, A.; Peralta-Videa, J. R., Cerium oxide nanoparticles modify the antioxidative stress enzyme activities and macromolecule composition in rice seedlings. Environ. Sci. Technol. 2013, 47, 14110. 30.Zhao, L.; Sun, Y.; Hernandez-Viezcas, J. A.; Hong, J.; Majumdar, S.; Niu, G.; Duarte-Gardea, M.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L., Monitoring the environmental effects of CeO2 and ZnO nanoparticles through the life cycle of corn (Zea mays) plants and in situ μ-XRF mapping of nutrients in kernels. Environ. Sci. Technol. 2015, 49, 2921. 31.Ma, C.; Chhikara, S.; Minocha, R.; Long, S.; Musante, C.; White, J. C.; Xing, B.; Dhankher, O. P., Reduced Silver Nanoparticle Phytotoxicity in Crambe abyssinica with Enhanced Glutathione Production by Overexpressing Bacterial γ-Glutamylcysteine Synthase. Environ. Sci. Technol. 2015, 49, 10117. 32.Xu, Q. S.; Hu, J. Z.; Xie, K. B.; Yang, H. Y.; Du, K. H.; Shi, G. X., Accumulation and acute toxicity of silver in Potamogeton crispus L. J. Hazard. Mater. 2010, 173, 186. 33.Le, V. N.; Ma, C.; Rui, Y.; Liu, S.; Li, X.; Xing, B.; Liu, L., Phytotoxic Mechanism of Nanoparticles: Destruction of Chloroplasts and Vascular Bundles and Alteration of Nutrient Absorption. Sci. Rep. 2015, 5, 11618. 34.Le, V. N.; Rui, Y.; Xin, G.; Li, X.; Liu, S.; Han, Y., Uptake, transport, distribution and Bio-effects of SiO 2 nanoparticles in Bt-transgenic cotton. J. Nanobiotecg.2014, 12, 50. 35.Fayez, K.; El-Deeb, B.; Mostafa, N., Toxicity of biosynthetic silver nanoparticles on the growth, cell ultrastructure and physiological activities of barley plant. Acta Physiol.Plant. 2017, 39, 155. 36.Priester, J. H.; Ge, Y.; Mielke, R. E.; Horst, A. M.; Moritz, S. C.; Espinosa, K.; Gelb, J.; Walker, S. L.; Nisbet, R. M.; An, Y. J., Soybean susceptibility to manufactured nanomaterials with evidence for food quality and soil fertility interruption. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 14734-14735. 37.Rico, C. M.; Morales, M. I.; Barrios, A. C.; McCreary, R.; Hong, J.; Lee, W.-Y.; Nunez, J.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L., Effect of cerium oxide nanoparticles on the quality of rice (Oryza sativa L.) grains. J. Agric. Food. Chem. 2013, 61, 11278-11285. 38.Cui, D.; Zhang, P.; Ma, Y.; He, X.; Li, Y.; Zhang, J.; Zhao, Y.; Zhang, Z., Effect of cerium oxide nanoparticles on asparagus lettuce cultured in an agar medium. Environ. Sci. Nano. 2014, 1, 459-465. 39.Gui, X.; Zhang, Z.; Liu, S.; Ma, Y.; Zhang, P.; He, X.; Li, Y.; Zhang, J.; Li, H.; Rui, Y., Fate and phytotoxicity of CeO2 nanoparticles on lettuce cultured in the potting soil environment. PLoS One. 2015, 10, e0134261. 40.Zhang, P.; Ma, Y.; Liu, S.; Wang, G.; Zhang, J.; He, X.; Zhang, J.; Rui, Y.; Zhang, Z., Phytotoxicity, uptake and transformation of nano-CeO 2 in sand cultured romaine lettuce. Environ. Pollut. 2017, 220, 1400-1408. 41.Rico, C. M.; Majumdar, S.; Duarte-Gardea, M.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L., Interaction of nanoparticles with edible plants and their possible implications in the food chain. J. Agric. Food. Chem. 2011, 59, 3485-3498. 42.Hall, J.; Williams, L. E., Transition metal transporters in plants. J. Exp. Bot. 2003, 54, 2601-2613.

19



497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540

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:

20


Page 20 of 29

Page 21 of 29


541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571

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

24


Page 24 of 29

Page 25 of 29


Figure 2

25



Figure 3

26


Page 26 of 29

Page 27 of 29


Figure 4

27



Figure 5

28


Page 28 of 29

Page 29 of 29


603 604

TOC Graphic

29


Alteration of Crop Yield and Quality of Wheat upon ... - ACS Publications

Recommend Documents