Several Pesticides Influence the Nutritional Content of Sweet Corn

Feb 12, 2018 - Herbicides are pesticides used to eradicate unwanted plants in both crop and non-crop environments. These chemistries are toxic to weed...
1 downloads 9 Views 374KB Size
Subscriber access provided by UNIVERSITY OF THE SUNSHINE COAST

Article

Several Pesticides Influence the Nutritional Content of Sweet Corn Matthew A. Cutulle, Gregory R Armel, Dean Adam Kopsell, Henry P Wilson, James Brosnan, Jose J. Vargas, Thomas E hines, and Rebecca M Koepke-Hill J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b05885 • Publication Date (Web): 12 Feb 2018 Downloaded from http://pubs.acs.org on February 13, 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 26

1

Journal of Agricultural and Food Chemistry

Several Pesticides Influence the Nutritional Content of Sweet Corn

2 3

Matthew A. Cutulle,1,4 Gregory R. Armel,2,4 Dean A. Kopsell,3,4 Henry P. Wilson,5 James T.

4

Brosnan,4 Jose J. Vargas,4 Thomas E. Hines,5 Rebecca M. Koepke-Hill,4

5 6

1

Coastal Research and Education Center, Clemson University, Charleston, SC 29414.

7

2

Global Herbicide Development Group, BASF Corp., Research Triangle Park, NC 27709, USA.

8

3

Environmental Horticulture Department, The University of Florida, Gainesville, FL, 32611,

9

USA.

10

4

Plant Sciences Department, The University of Tennessee, Knoxville, TN 37996, USA.

11

5

Eastern Shore Agricultural Research and Extension Center, Virginia Polytechnic Institute and

12

State University, Painter VA 23420.

13 14

* To whom correspondence should be addressed. Phone: (843) 402-5399 Fax: (843) 571-4654

15

E-mail:[email protected]

16 17

One-sentence summary: Herbicides targeting the inhibition of photosynthesis, carotenoid and

18

amino acid biosynthesis were applied with or without a safener that enhances P450 metabolism,

19

and these mixtures changed levels of mineral elements, proteins, amino acids, sugars, fiber, and

20

fatty acids in sweet corn kernels.

21 22 23

1

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

24 25

Abstract: Herbicides are pesticides used to eradicate unwanted plants in both crop and non-crop

26

environments. These chemistries are toxic to weeds due to inhibition of key enzymes or

27

disruption of essential biochemical processes required for weedy plants to survive. Crops can

28

survive systemic herbicidal applications through various forms of detoxification including

29

metabolism that can be enhanced by safeners. Field studies were conducted near Louisville,

30

TN and Painter, VA to determine how the herbicides mesotrione, topramezone, nicosulfuron, and

31

atrazine applied with or without the safener isoxadifen-ethyl would impact the nutritional quality

32

of ‘Incredible’ sweet corn (Zea mays L. var. rugosa). Several herbicide treatments increased the

33

uptake of the mineral elements phosphorous, magnesium, and manganese by 8 to 75%. All

34

herbicide treatments increased protein content by 4 to 12%. Applied alone, nicosulfuron

35

produced similar levels of saturated, monounsaturated, and polyunsaturated fatty acids when

36

compared to the non-treated check, but when applied with isoxadifen-ethyl, fatty acids increased

37

28 and 44%. Nicosulfuron plus isoxadifen-ethyl or topramezone or the combination of all three

38

actives increased the concentrations of fructose and glucose (40 to 68%) whereas reducing levels

39

of maltose or sucrose when compared to the non-treated check (-15 to -21%). Disruptions in

40

biochemical pathways in plants due to the application of herbicides, safeners or other pesticides

41

has the potential to alter the nutrient quality, taste and overall plant health associated with edible

42

crops.

43 44

Keywords: amino acids, carotenoids, fatty acids, fiber, herbicide

45

2

ACS Paragon Plus Environment

Page 2 of 26

Page 3 of 26

46 47

Journal of Agricultural and Food Chemistry

1. INTRODUCTION Pesticides are substances that are used to repel, eradicate, or destroy the life cycle of

48

pests. Over 900 million metric tons of pesticides are used annually in the United States to

49

control many pests including, but not limited to insects, microbes, rodents, and weeds.1

50

Pesticides that control weeds are referred to as herbicides. There are over 300 commercially

51

available herbicides that target 27 different mechanisms within plants, including enzymes

52

involved in the biosynthesis of carotenoids, chlorophyll, amino acids, fatty acids, lipids, and

53

cellulose. The application of a pesticide concomitantly providing pest control and improved

54

nutrition in a single crop system is not intuitive, although these chemicals induce physiological

55

responses in both crops and weeds. Furthermore, collective societal attitudes towards pesticides

56

are associated with less healthy fruits and vegetables.2 However, exploitation of plant

57

biosynthetic pathways using pesticides may reveal chemical technologies that provide weed

58

control and improve the nutrition of crops.

59

The term hormesis describes how a low dose of a toxic substance, such as a pesticide, can

60

be used to increase growth or output of certain biological processes.3,4 Low use rate applications

61

of herbicides applied to specific crops can increase biomass, growth, protein content, and disease

62

resistance. In these scenarios, herbicides were usually applied at sub-lethal or less than optimal

63

rates to crops that would have been severely injured or killed had the herbicide been applied at

64

an optimal dose.4,5,6 How herbicides applied to edible crops at registered rates can impact

65

biosynthetic pathways responsible for the production or uptake of key nutrients beneficial to

66

consumers of these plants has not been demonstrated.

67 68

Mesotrione is a member of the triketone family of herbicides, which are structurally similar to leptospermone, a natural phytotoxin obtained from the Californian bottlebrush plant

3

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

69

(Callistemon citrinus Stapf.).7 Mesotrione primarily controls broadleaf weeds from both a foliar

70

and soil residual perspective.7 Topramezone is a member of the pyrazolone family of herbicides

71

and typically provides better grass control and crop selectivity in corn compared to mesotrione,

72

but has limited soil residual activity.7 Both herbicides are carotenoid biosynthesis inhibitors

73

(CBI) currently labeled for weed control in corn (Zea mays L.) production.8 These herbicides

74

competitively inhibit the enzyme p-hydroxyphenylpyruvate dioxygenase (HPPD), an essential

75

component for the biochemical conversion of tyrosine to plastoquinone and α-tocopherol.

76

Plastoquinone is a critical cofactor for phytoene desaturase, as well as an intermediate electron

77

carrier in the photosynthetic electron transport chain.

78

Nicosulfuron is a sulfonylurea herbicide that kills weeds by inhibiting the enzyme

79

acetolactate synthase (ALS). This enzyme is responsible for the biosynthesis of the branched

80

chain amino acids valine, leucine, and isoleucine. Nicosulfuron primarily control grass weeds in

81

a grass crop like corn; however, nicosulfuron has limited selectivity in sweet corn (Zea mays L.

82

var. rugosa).9,10 Using a safener, isoxadifen-ethyl, with nicosulfuron permits its use in several

83

sweet corn varieties.11 Safeners like isoxadifen-ethyl, are a chemically diverse group of

84

compounds that increase expression of enzymes such as glutathione S-transferases and

85

cytochrome P450 monooxygenases.12 Activation of these enzymes results in detoxification of

86

some herbicides. In the case of isoxadifen-ethyl, sweet corn hybrids that are heterozygous for a

87

specific P450 (i.e., CYPcyp) can safely be treated with mixtures of certain HPPD and ALS

88

inhibiting herbicides and isoxadifen-ethyl.11 Often ALS, HPPD inhibitors, and herbicides

89

safeners like isoxadifen-ethyl will be applied in mixtures to provide broad-spectrum weed

90

control with optimal crop tolerance in several different types of corn, including sweet corn.13

4

ACS Paragon Plus Environment

Page 4 of 26

Page 5 of 26

91

Journal of Agricultural and Food Chemistry

Corn is the leading cereal crop in the world with greater than 1 billion metric tons

92

produced annually and is ideally suited to conduct nutritional studies.14 Improvement in

93

molecular and genomic technologies have allowed for improved nutrition in crops like corn.15 In

94

addition to nutritional benefits, sweet corn has a significant impact on the U.S. agricultural

95

economy. A total of 210,972 hectares of sweet corn were harvested commercially in 2014 in the

96

U.S. with a total production value of $1.09 billion.16

97

Improving sweet corn nutrition through herbicide and safener applications could

98

potentially be valuable by aiding in dietary changes that may decrease the incidence of diabetes,

99

cardiovascular disease, and metabolic syndromes.15 Applications of mesotrione plus atrazine

100

increased carotenoid (antioxidant) content in sweet corn, but nothing is known regarding what

101

other nutrient impacts may occur from use of these mixtures.17 Additionally, there are no reports

102

on how ALS inhibitors or safeners will impact the nutrient quality of sweet corn. Our research

103

aims to understand how inhibitors of HPPD and ALS with and without the safener isoxadifen-

104

ethyl can impact the uptake of mineral elements and the production of key nutrients including

105

proteins, amino acids, fatty acids, fiber, sugars, and various antioxidants.

106 107 108

2. MATERIALS AND METHODS Field and laboratory studies were conducted in 2009 to evaluate postemergence (POST)

109

applications of mesotrione, topramezone, and nicosulfuron in mixtures with atrazine applied

110

alone or with the safener isoxadifen-ethyl. The sweet corn variety ‘Incredible’ was chosen for

111

these studies based on the findings of Kopsell et al. (2009) that determined it was moderately

112

tolerant to HPPDs, and able to yield increased antioxidant content via applications of mesotrione

5

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

113

plus atrazine.17 The ‘Incredible’ variety is a yellow kernel genotype and is a sugar enhanced

114

variety, but also maintains its sweetness longer than standard sweet corn varieties.18

115 116 117

2.1 Field Trials Field trials were established at the East Tennessee Research and Education Center

118

Blount Unit in Louisville, TN (35.84 latitude, -83.95 longitude) on June 3rd 2009. ‘Incredible’

119

sweet corn was seeded in a randomized complete block design with three replications. A second

120

trial location was established at the Eastern Shore Agricultural Research and Extension Center in

121

Painter, VA (37.58 latitude, -75.83 longitude). In TN, seeds were drill planted at a depth of 2.5

122

cm in a Emorysilt loam soil (Fine-silty, siliceous, active, thermic Fluventic Humic Dystrudepts)

123

silt loam soil (fine loamy, siliceous, thermic, Humic Hapudult) spaced at 25 cm in row and 76

124

cm between rows. Each plot consisted of four rows of corn, 6.1 m in length. Sweet corn was

125

planted similarly at the VA location into a Bojac sandy loam (Typic Hapludults) with less than

126

1% organic matter.. Preemergence (PRE) applications were made to all plots using S-metolachlor

127

+ atrazine (Biceps II Magnum: Syngenta Crop Protection, Inc.) at 2190 g of active ingredient per

128

hectare (g ai/ha) to reduce weed pressure in the plots. The insecticide lambda-cyhalothrin

129

(Warrior: Syngenta Crop Protection, Inc.) was applied preemergence (PRE) to all plots at 32 g

130

ai/ha in order to reduce stand loss from insects like cutworms (Agrotis spp.).

131

This field study included the following seven treatments: (1) nicosulfuron 35 g ai/ha, (2)

132

mesotrione 105 g ai/ha, (3) topramezone 18 g ai/ha, (4) nicosulfuron 35 g ai/ha + isoxadifen-

133

ethyl 13 g ai/ha, (5) nicosulfuron 35 g ai/ha + topramezone 18 g ai/ha + isoxadifen-ethyl 13 g

134

ai/ha, (6) nicosulfuron 35 g ai/ha + mesotrione 105 g ai/ha + isoxadifen-ethyl 13 g ai/ha, and a

135

(7) treated check (atrazine at 560 g ai/ha). All treatments included atrazine at 560 g ai/ha.

6

ACS Paragon Plus Environment

Page 6 of 26

Page 7 of 26

Journal of Agricultural and Food Chemistry

136

Atrazine, a common broadleaf herbicide used in corn production and controls weeds by

137

inhibiting site A of the Qb binding niche of the D1 protein in photosystem II (PSII).19 Like

138

mesotrione, rapid metabolism of atrazine affords tolerance in maize genotypes.19 Treatments

139

contained an adjuvant of crop oil concentrate applied at 1% v/v and were applied to sweet corn

140

plants approximately 5 to 10 cm in height. Herbicide and safener application rates were

141

extrapolated from the product label. In Tennessee, herbicide treatments were applied using a CO2

142

powered backpack sprayer calibrated to deliver 215 liters per hectare water carrier volume using

143

an 8002 flat fan nozzle. In Virginia, herbicides treatments were applied with compressed air

144

from a tractor mounted sprayer calibrated to deliver 236 liters per hectare water carrier volume

145

using an 8003 flat fan nozzle. All plots were manually hand-weeded as necessary to prevent

146

potential variations in yield and nutrient content associated with weed competition.

147

Visual observations of foliar injury were measured approximately seven days following

148

herbicide treatment. Antioxidant, sugar, amino acids, protein, fatty acids, mineral elements, and

149

fiber content in mature sweet corn kernels were measured 45 days after treatment.

150 151 152

2.2 Harvest and Laboratory Analysis Eight uniform sweet corn ears were collected from the center of the treated area of each plot

153

and stored for 48 h in a walk-in cooler (4 C). During processing, a 5 cm section was cut from the

154

central region of each ear of the experimental samples and saved for nutrient analyses. Five g of

155

tissue was macerated for chemical preparation. Sugar content was assessed using a method

156

developed by Zygmunt, fatty acids by Sukhija and Palmquist, amino acids and proteins by

157

AOAC, fiber by Soest et al., antioxidants (carotenoids and gamma tocopherol) by Kurilich and

158

Juvik along with Davies and Kost, and mineral content by OMOA.20-27

7

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

159 160

2.3 Data Analysis

161

All data was converted to percent change compared to the treated check and subjected to

162

analysis of variance (ANOVA), and means were subsequently separated using Fisher’s protected

163

LSD at the 95% confidence interval. Normaility diagnostics were applied to data and were

164

considered acceptable based on the Shapiro-Wilk diagnostic. All data were pooled across

165

statistical runs considering no run-by-treatment interactions were observed.

166 167

Results and Discussion

168

3.1 Amino Acids

169

There were no significant differences in sweet corn yield among treatments although

170

application of mesotrione alone resulted in the greatest visual damage to corn plants (8%) (Table

171

1). When evaluating amino acid content, plants treated with nicosulfuron alone produced similar

172

concentrations of amino acids when compared to the treated check except for proline, which was

173

reduced by 7%. However, when nicosulfuron was applied with isoxadifen-ethyl, this treatment

174

resulted in the highest kernel amino acid content, significantly raising all amino acids except

175

alanine and methionine by 9 to 28%. The largest increase in amino acids from the nicosulfuron

176

plus isoxadifen-ethyl treatment was in lysine, which is beneficial from a nutrition perspective[e

177

considering corn is naturally deficient in lysine.28 This deficiency of lysine in corn is most

178

concerning in areas where corn is used as the primary source of dietary protein in both humans

179

and domesticated animals.28 Topramezone alone and nicosulfuron plus isoxadifen-ethyl

180

increased the amount of the branched chain amino acids leucine and isoleucine by 8 to 14%

181

(Table 2). The benefits of increased branched chain amino acid consumption for humans

8

ACS Paragon Plus Environment

Page 8 of 26

Page 9 of 26

Journal of Agricultural and Food Chemistry

182

include increased muscle tissue along with decreased muscle fatigue.29 In addition, branched

183

chain amino acids also help regulate many mammalian biosynthetic including the regulation of

184

blood sugar and the prevention of insulin insensitivity.30

185

3.2 Fatty Acids

186

Analysis of fatty acid content also highlighted some significant differences when

187

comparing nicosulfuron applied alone or with isoxadifen-ethyl. The nicosulfuron plus

188

isoxadifen-ethyl treatment was the only treatment to yield total fatty acid content significantly

189

greater than the treated check (Table 3). This treatment significantly increased all fatty acid

190

saturation groupings by 28 to 44%. The individual fatty acids that were increased by the

191

nicosulfuron plus isoxadifen-ethyl treatment included arachidic acid, behenic acid, oleic, linoleic

192

acid, alpha-linoleic acid, and palmitic acid. Another important trend to note is that application of

193

nicosulfuron plus isoxadifen-ethyl increased poly-unsaturated fatty acids by 44% relative to the

194

check. Polyunsaturated fatty acids reduce bad cholesterol and the risk of heart disease in

195

humans.31

196

3.3 Protein, Fiber, and Minerals

197

When evaluating protein, fiber, and mineral content extracted from kernels, the

198

nicosulfuron plus isoxadifen-ethyl treatment resulted in superior nutrient content (Table 4).

199

Protein increased by 12% relative to the treated check in kernels treated with nicosulfuron plus

200

isoxadifen-ethyl, whereas all other treatments increased protein content between 4 to 8% Both

201

fiber types (acid detergent fiber, neutral detergent fiber), P, Mg, K, Mn, and Zn were increased

202

by 14 to 51% with the nicosulfuron plus isoxadifen-ethyl treatment. No treatments increased

203

copper or sodium in sweet corn kernels, and only the nicosulfuron plus mesotrione plus

204

isoxadifen-ethyl treatment increased calcium levels (100%). Zn, Mg, Cu, and Fe are limiting

9

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

205

nutrients in cereal crops, especially in areas where these crops are a primary source of nutrition

206

for the population of that region.32 Moreover, the 67% increase of Fe from the nicosulfuron plus

207

isoxadifen-ethyl treated plants should be further highlighted, as Fe deficiency is one of the most

208

common nutrient deficiencies in the world. A deficiency in Fe can lead to anemia and other

209

severe health conditions. Iron deficiency is most often observed in women and is particularly

210

concerning during pregnancy.33

211 212 213

3.4 Sugar and Antioxidants Kernals from all treatments contained the same amount of total sugars, except the

214

nicosulfuron alone treatment, which increased total sugar content by 16% (Table 5). Fructose

215

and glucose levels were increased by applications of topramezone, nicosulfuron plus isoxadifen-

216

ethyl, and topramezone plus nicosulfuron plus isoxadifen-ethyl. These increases in the

217

monosaccharides fructose and glucose tended to be offset by decreases in the disaccharides

218

maltose or sucrose. Fructose is the sweetest of the natural sugars and any increase should

219

increase the perceived sweetness of the sweet corn, especially considering the offset decrease in

220

maltose or sucrose.34 Sweetness and tenderness are the two qualities most associated with

221

improving the eating quality of sweet corn.35 However, increases in fructose, while potentially

222

beneficial from a sweetness perspective, may be negative from a human health perspective as

223

fructose is not digested in the same manner as other sugars and higher concentrations of fructose

224

in the human diet is linked to obesity, diabetes, hypertension, and heart disease.36 There were no

225

significant differences between any of the treatments for carotenoid content.

226 227

Mesotrione, topramezone, nicosulfuron and isoxadifen-ethyl are all currently registered for pre- or postemergence applications to various types of corn. Data from our studies demonstrated

10

ACS Paragon Plus Environment

Page 10 of 26

Page 11 of 26

Journal of Agricultural and Food Chemistry

228

increased concentrations of nutritionally important fatty acids, protein, amino acids, fiber, sugar

229

and minerals in sweet corn genotypes through applications of HPPD-inhibiting and ALS-

230

inhibiting herbicides and the safener isoxadifen-ethyl. The key question is: what mechanism

231

leads to these increases? In general, corn rapidly metabolizes herbicides like mesotrione into

232

non-herbicidal byproducts. Moreover, corn can rapidly outgrow sensitivity in the form of leaf

233

tissue bleaching, which results from suppression of carotenoid biosynthesis following application

234

of mesotrione to sensitive varieties.At the time of harvest, no mesotrione residues were found in

235

sweet corn kernels.17 In addition, field corn hybrids rapidly metabolize nicosulfuron; however,

236

sweet corn varieties can be much more sensitive.37 When applied with safeners, like isoxadifen-

237

ethyl, 84% of nicosulfuron is metabolized in a few of days.38 These herbicides are applied just

238

weeks after corn emergence and are degraded in plants within days of application. That being

239

said, how do these herbicides affect the nutrient content of sweet corn kernels harvested

240

approximately 2 months after application?

241

The most interesting and impactful treatment from these studies was nicosulfuron plus

242

isoxadifen-ethyl. Safeners are believed to enhance enzyme activity that results in conjugating

243

and detoxifying xenobiotics such as herbicides.12 The safener isoxadifen-ethyl has multiple

244

impacts in the metabolism of xenobiotics in corn plants. First, isoxadifen-ethyl upregulates

245

certain cytochrome P450 monooxygenases that appear to be the primary mechanism by which it

246

detoxifies herbicides like nicosulfuron.39 Second, it can upregulate glutathione S-transferases.40

247

Overexpression of glutathione S-transferases improves stress tolerance in plants.41 If we assume

248

plant growth requires upregulation of key plant processes, then this may help explain some of the

249

responses noted with the mixture of nicosulfuron plus isoxadifen-ethyl. However, if this is the

250

case, then why do the three-way mixtures of HPPD plus nicosulfuron plus isoxadifen-ethyl

11

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

251

provide less pronounced improvements in sweet corn kernel nutrient content? Also, if the

252

safener is so critical in helping with these nutrient increases, then why do we observe increases

253

in total sugars, some mineral elements, neutral detergent fiber, key amino acids, and behenic acid

254

with applications of nicosulfuron, mesotrione, or topramezone applied without isoxadifen-ethyl

255

(Tables 3,4, and 5) These dramatic increases that result from various applications of specific

256

herbicides with or without isoxadifen, highlight the complexity of the pathways and mechanisms

257

involved in these nutritional changes.

258

Another partial explanation for the increases nutrient content may be related to the increases

259

in mineral elements concentrations observed in this study. Several of the herbicide treatments in

260

our studies stimulated uptake of mineral elements from soil (Table 4). The uptake of certain

261

mineral elements may be increased in corn under stress. The stress in our studies most likely

262

was induced in reaction to the herbicide treatments. Although the degree of corn injury

263

following herbicide treatment was modest in these studies, this stress was only measured visually

264

at a fixed point in time, and the total stress from these herbicides may not have been captured

265

thoroughly via a subjective rating. Corn placed under stress can increase uptake of Fe, Mg, Mn,

266

Cu, and N from the soil.42 In addition, increases in mineral element concentrations have the

267

potential to enhance biochemical processes that impact the synthesis of many nutrients. For

268

example, increases in Fe content in pea (Pisum sativum L.) seedlings causedto have more

269

unsaturated fatty acids.43 The nicosulfuron plus isoxadifen-ethyl treatment in our studies

270

displayed the highest levels of iron content and similarly altered the ratios of fatty acids in the

271

corn kernels leading to increases in unsaturated fatty acids (Table 3 and 4). Also, deficiencies in

272

Mg, Mn, and Fe in alfalfa (Medicage sativa L.) have led to decreases in the production of key

273

amino acids.44 The aforementioned mineral elements were increased by the nicosulfuron plus

12

ACS Paragon Plus Environment

Page 12 of 26

Page 13 of 26

Journal of Agricultural and Food Chemistry

274

isoxadifen-ethyl treatment in our studies, and most amino acids evaluated were also increased by

275

this treatment.

276

The concept of herbicides increasing certain nutrients (e.g., carotenoid, antioxidants) was

277

documented previously at the University of Tennessee.17 Our studies concluded that many

278

different, seemingly unconnected, plant processes can be changed in the presence of herbicides

279

and isoxadifen-ethyl. These results again highlight the complex biochemical and physiological

280

mechanisms activated when multiple herbicides or herbicides plus safeners such as isoxadifen-

281

ethyl are applied to crops like sweet corn. These interactions could be further elucidated through

282

transcriptome and metabolomics studies to uncover the exact sequence of activities that occur

283

following application until harvest. More comprehensive experiments should focus on multiple

284

variety trials and include additional corn herbicide safeners, such as cyprosulfamide across

285

multiple additional states with different soil types and climatic conditions. Additionally, taste

286

panel tests should be developed for assessing the impact of safener plus herbicide treatments on

287

the taste of sweet corn. Calcium and sugar content can both impact flavor; thus, coupling specific

288

plant genetics with key herbicides and safeners may improve or modify not only the nutritional

289

content but also the taste of sweet corn or other fruits, vegetables, and grains.35,45,46 These results

290

may help create a novel subfield in agriculture where pesticide application strategies are not only

291

evaluated for their ability to control pests, but for their potential to enhance crop nutrition and

292

taste.

293

13

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

294 295 296 297 298 299 300 301 302 303 304 305

REFERENCES 1. Anonymous. The EPA and Food Security. http://www.epa.gov/pesticides/factsheets/securty.htm 2. Saba, A.; Messina, F. Attitudes towards organic foods and risk/benefit perception associated with pesticides. Food Qual. and Prefer. 2003, 14, 637-635. 3. Southam, C.M.; Erlich, J. Effects of extracts on western red-cedar heartwood on certain wooddecaying fungi in culture. Phytopath. 1943, 33, 517-24. 4. Duke, S.O.; Cedergreen, N.; Velini, E.D.; Belz, R.G. Hormesis: Is it an important factor in herbicide use and allelopathy. Out. on Pest Manag. 2006, 17, 29-33. 5. Ries, S.K.; Chmiel, H.; Dilley, D.R.; Filner, P. Increase in nitrate reductase activity and

306

protein content of plants treated with simazine. Proc. Nat. Acad. Sci. USA. 1967, 58, 526-

307

532.

308 309 310

6. Wiedman, S.J.; Appleby, A.P. Plant growth stimulation by sublethal concentrations of herbicides. Weed Res. 1972, 12, 65-74. 7. Grossman, K.; Ehrhardt, T. On the mechanism of action and selectivity of the corn herbicide

311

topramezone: a new inhibitor of 4-hydroxyphenylpyruvate dioxygenase. Pest. Manag.

312

Sci. 2007, 63, 429-439

313

8. Mitchell, G.; Bartlett, D.W.; Fraser, T.E.M.; Hawkes, T.R.; Holt, D.C.; Townson, J.K.;

314

Wichert, R.A. Mesotrione: a new selective herbicide for use in maize. Pest Management

315

Sci. 2001, 57, 120-128.

316 317

9. O’Sullivan, J.; Sikkema, P.H.; Thomas, R.J. Sweet corn (Zea mays) cultivar tolerance to nicosulfuron, Can. J. Plant Sci. 2000, 80, 419-423.

14

ACS Paragon Plus Environment

Page 14 of 26

Page 15 of 26

318 319 320 321 322 323 324

Journal of Agricultural and Food Chemistry

10. Dobbels, A.F.; Kapusta, G. Postemergence weed control in corn (Zea mays) with nicosulfuron combinations Weed Technol. 1993, 7, 844-850. 11. Williams II, M.W.; J.K. Pataky. Factors affecting differential sensitivity of sweet corn to HPPD-inhibiting herbicides. Weed Sci. 2010, 58, 289-294. 12. Reichers, D.E.; Kreuz, K.; Zhang, Q. Detoxification without intoxication: herbicide safeners activate plant defense gene expression. Plant Physiol. 2010, 153, 3-13. 13. Currie, R.; Geier, P. "Weed Control with Accent, Callisto, Isoxadifen, Impact, Cinch,

325

Dicamba, and Atrazine in Irrigated Corn," Kansas Agricultural Experiment Station

326

Research Reports: 2016, Vol. 2: Iss. 7. https://doi.org/10.4148/2378-5977.1267.

327

14. Ai, Y.; Jane, Jay-Lin. Macronutrients in corn and human nutrition. Comp. Rev. In Food Sci.

328 329 330 331 332 333

and Food Safety. 2016, 15, 581-598. 15. Newell-McGloughlin, M. Nutritionally Improved Agricultural Crops. Plant Physiol. 2008, 147, 939-953. 16. U.S. Department of Agriculture, Nat. Agric. Stat. Service – Agricultural Statistics (2017, www.nass.usda.gov/Publications/Ag_Statistics). 17. Kopsell, D.A.; Armel, G.R.; Mueller, T.C.; Sams, C.E.; Deyton, D.E.; McElroy, J.S.;

334

Kopsell, D.E. Increase in nutritionally important sweet corn kernel carotenoids following

335

mesotrione and atrazine applications. J. Agric. Food. Chem. 2009, 57, 6362-6368.

336

18.Purdue Extension available from:

337

https://www.hort.purdue.edu/rhodcv/hort410/ID562003/Sweet_Corn.pdf

338

Accessed (October 2017).

339 340

19. Abendroth, J.A.; Martin, A.R.; Roeth, F.W. Plant response to combinations of mesotrione and photosystem II inhibitors. Weed Technol. 2006, 20, 267-274.

15

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

341

20. Zygmunt, L.C. High pressure liquid chromatographic determination of mono and

342

disaccharides in presweetened cereals: collaborative study. JAOAC Int. 1982, 65, 256-

343

264.

344

21. Sukhija, P.S.; Palmquist, D.L. Rapid method for determination of total fatty acid content and

345

composition of feedstuffs and feces. J. Agric. Food Chem. 1988, 36, 1202-1206.

346

22. Van Soest, P.J.; Robertson, J.B.; Lewis, B.A. Methods for dietary fiber, neutral detergent

347

fiber, and nonstarch polysaccharides in relation to animal nutrition. J. of Dairy Sci. 1991,

348

74, 3583-3597.

349

23. AOAC Official Method 994.12 JAOAC 70:171-174, 1987.

350

24. Combustion Analysis (LECO) AOAC Official Method 990.03, 2006.

351

25. Official Methods of Analysis, 17th edition. 2000. Association of Official Analytical

352

Chemists. Perkin Elmer 5300 DV ICP. Perkin Elmer, 710 Bridgeport Avenue, Shelton,

353

CT 0648425.

354 355 356

26. Kurilich, A.C.;Juvik, J.A. Quantification of carotenoid and tocopherol antioxidants in Zea mays. J. Agric. Food Chem. 1999, 47, 1948–1955. 27. Davies, B. H.; Kost, H. P. Chromatographic methods for the separation of carotenoids. In

357

CRC Handbook of Chromatography, Plant Pigments: Fat Soluble Pigments; Kost ,

358

H.P., Zweig, G., Sherma, J., Eds.; CRC Press: Boca Raton, FL, 1998; Vol. 1, pp 1-185.

359 360 361

28. Young V.R.; Pellett PL. Plant proteins in relation to human protein and amino acid nutrition. Am. J. Clin. Nutr. 1994, 59(5), 1203S-12S. 29. Jackman, S.R.; Witard, O.C.; Jeukendrup, A.E.; Tipton, K.D. Branched-chain amino acid

362

ingestion can ameliorate soreness from eccentric exercise. Med. Sci. Sports Exerc. 2010,

363

42, 962-970.

16

ACS Paragon Plus Environment

Page 16 of 26

Page 17 of 26

364 365 366

Journal of Agricultural and Food Chemistry

30. Xiaoping, C.; Yang, W. Branched-chain amino acids and the association with type 2 diabetes. J. Diabetes Investig. 2015, 6, 369-370. 31. Ruxton, C.H.S.; Reed, S.C.; Simpson, M.J.A.; Millington, K.J. The health benefits of omega-

367

3 polyunsaturated fatty acids: a review of the evidence. J. Hum. Nutr. Dietet.

368

2004, 17, 449-459.

369 370 371 372 373

32. White, P.J.; M.R. Broadley. Biofortifying crops with essential mineral elements. Trends In Plant Sci. 2005, 10, 586-593. 33.American Society of Hematology available from: http://www.hematology.org/Patients/Anemia/Pregnancy.aspx (Accessed October 2017). 34. Joesten, Melvin D; Hogg, John L; Castellion, Mary E (2007). "Sweetness Relative to

374

Sucrose (table)". The World of Chemistry: Essentials (4th ed.). Belmont, California:

375

Thomson Brooks/Cole. p. 359. ISBN 0-495-01213-0. Retrieved 14 September 2010.

376

35. Azanza, F.; Juvik, J.A.; Klein, B.P. Relationships between sensory quality attributes and

377

kernel chemical composition of fresh-frozen sweet corn. J. of Food Qual. 1994,

378

17, 159-172.

379

36. Johnson, R.J.; Segal, M.S.; Sautin, Y.; Nakagawa, T.; Feig, D.I.; Kang, D.H.; Gersch, M.S.;

380

Benner, S.; Sanchez-Lozada, L.G. Potential role of sugar (fructose) in the epidemic

381

of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and

382

cardiovascular disease. Am. J. Clin. Nutr. 2007, 86(4), 899-906.

383

37. Gallaher, K., T.C. Mueller, R.M. Hayes, O. Schwartz; M. Barrett. Absorption,

384

translocation, and metabolism of primisulfuron and nicosulfuron in broadleaf signalgrass

385

(Brachiaria platyphylla) and corn. Weed Sci. 1999, 47, 8-12.

17

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

386

38. Burton, J.B.; Maness, E.P.; Monks, D.W.; Robinson, D.K. Sulfonylurea selectivity and

387

safener activity in ‘Landmark’ and ‘Merit’ sweet corn. Pestic. Biochem. Physiol. 1993,

388

48, 163-172.

389

39. Paporisch, A.; Rubin, B. Isoxadifen safening mechanism in sweet corn genotypes

390

with differential response to P450-metabolized herbicides. Pest. Biochem. and Phy. 2017,

391

138, 22-28.

392

40. Sun, L.; Wu, R.; Su, W.; Gao, Z.; Lu, C. Physiological basis for isoxadifen-ethyl

393

induction of nicosulfuron detoxification in maize hybrids. Plos One. 2017,

394

DOI:10.1371/journal.pone.0173502.

395

41. Roxas, V.P.; Smith Jr, R.K.; Allen, E.R.; Allen, R.D. Overexpression of glutathione S-

396

transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings

397

during stress. Nat. Biotech. 1997, DOI:10.1038/nbt1097-988.

398

42. Gunes, A.; Inal, A.; Alpaslan, M.; Eraslan, F.; Bagci, E.G.; Cicek, N. Salicylic acid

399

induced changes on some physiological parameters symptomatic for oxidative stress and

400

mineral nutrition in maize (Zea mays L.) grown under salinity. J. Plant Phy. 2007,

401

164, 728-736.

402

43. Shijian, X.; Lin, D.; Sun, H.; Yang, X.; Zhang, X. Excess iron alters the fatty acid

403

composition of chloroplast membrane and decreases the photosynthesis rate: a study in

404

hydroponic pea seedlings. Act. Phy. Plant. 2015, 37, 212.

405 406 407 408

44. Sheldon, V.L.;. Blue, W.M.G.; Albrecht, W.M.A. Biosynthesis of amino acids according to soil fertility. Plant and Soil. 1951, 3, 33-40. 45. Tordoff, M.G.; Sandell, M.A. Vegetable bitterness is related to calcium content. Appetite. 2009, 52, 498-504.

18

ACS Paragon Plus Environment

Page 18 of 26

Page 19 of 26

409 410

Journal of Agricultural and Food Chemistry

46. Lertrat, K.; Pulam, T. Breeding for increased sweetness in sweet corn. Int. J. of Plant Breed. 2007, 1, 27-30.

19

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

Page 20 of 26

Table 1. Percent Injury and yield for ‘Incredible’ sweet corn (Zea mays L. var rugosa) following applications of carotenoid and amino acid biosynthesis inhibitors applied alone and in mixtures with the Photosystem II inhibitors atrazine. Injurya Herbicide treatmentb

Rate g ai/ha

7 DAT

Yield 14 DAT

————— % —————

———————kg/ha———————

Nicosulfuron

35

5a

7 ab

7689 a

Mesotrione

105

5a

8a

6747 a

Topramezone

18

5a

4 ab

7847 a

35 + 13

4a

5 ab

9002 a

35 +

5a

4 ab

7868 a

4a

8a

8418 a

3a

0b

9437 a

Nicosulfuron + Isoxadifen-ethyl Nicosulfuron + Topramezone + Isoxadifen-ethyl Nicosulfuron+ Mesotrione+

18 + 13 35 + 105 + 13

Isoxadifen-ethyl Treated checkc

---

a

No study by treatment interaction occurred for percent visual injury ratings of sweet corn or for sweet corn yield, therefore these data were pooled over studies.

b

All treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.

c

Treated check was not included in the statistical analysis.

20

ACS Paragon Plus Environment

Page 21 of 26

Journal of Agricultural and Food Chemistry

Table 2. Percent increase in concentrations of key amino acids for ‘Incredible’ sweet corn (Zea mays L. var. rugose) following applications of carotenoid and amino acid biosynthesis inhibitors applied alone and in mixtures with the Photosystem II inhibitors atrazine. Amino Acidsa Total Aspartic Herbicide treatmentb

Rate

Amino

Glutamic Threonine

Acid

Proline

Glycine

Cysteine

Alanine

Valine

Methionine

Isoleucine

Leucine

Lysine

Acid

Acids ———————————————— % increase ———————————————

g ai/ha Nicosulfuron

35

-1 d

-4 c

2c

-2 c

-7 d

-4 b

0 cd

1 ab

0c

0a

0c

0c

1b

Mesotrione

105

6 abc

7 ab

16 a

6 ab

9a

4 ab

6b

4 ab

7 abc

2a

6 abc

6 abc

12 b

Topramezone

18

7 ab

6 ab

12 ab

6 abc

6 ab

4 ab

3 bc

8a

9 ab

8a

10 ab

8 ab

10 b

35 + 13

10 a

12 a

12 ab

10 a

10 a

9a

12 a

1 ab

13 a

4a

14 a

12 a

28 a

Nicosulfuron +

35 +

1 bcd

3 abc

3c

2 abc

3 cb

4 ab

-3 d

6 ab

-1 c

8a

0c

1 bc

6b

Topramezone +

18 +

Isoxadifen-ethyl

13 2 bcd

-1 bc

7 bc

1 bc

4 cb

0b

2 bcd

0b

5 abc

4a

3 bc

4 bc

6b

0 cd

0 bc

0c

0 bc

0c

0b

0 cd

0b

0 bc

0a

0c

0c

0b

Nicosulfuron + Isoxadifen-ethyl

Nicosulfuron+

35 +

Mesotrione+

105 +

Isoxadifen-ethyl c

Treated check

13 ---

a

No study by treatment interaction occurred for any amino acid data, therefore these data were pooled over studies.

b

All treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.

c

Treated check was not included in the statistical analysis.

21

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

Page 22 of 26

Table 3. Percent increase in concentrations of key fatty acids for ‘Incredible’ sweet corn (Zea mays L. var. rugosa) following applications of carotenoid and amino acid biosynthesis inhibitors applied alone and in mixtures with the Photosystem II inhibitors atrazine. Fatty Acids (by saturation grouping)

Fatty Acids (individual) Alpha-

Total Total

Total Mono-

Total Poly-

Myristoleic

Palmitic

Stearic

Oleic

Linoleic

Herbicide treatmentb

Rate

Fatty

Unsaturated

Unsaturated

Acid

Acid

Acid

Acid

Acid

Behenic

Acid

acid

(C20:0)

(C22:0)

Acid

Fatty Acids

Arachidic Linoleic

Saturated

Fatty Acids

Fatty Acids

(C14:1)

(C16:0)

(C18:0)

(C18:1)

(C18:2) (C18:3)

Acids

—————————————— % increase ———————————-

g ai/ha Nicosulfuron

35

13 ab

12 ab

15 ab

12 ab

-50 a

12 ab

10 a

16 ab

12 ab

10 ab

17 a

13 ab

Mesotrione

105

11 ab

7 ab

9 ab

12 ab

-21 a

9 ab

1a

10 ab

13 ab

15 ab

10 ab

13 ab

Topramezone

18

9 ab

9 ab

10 ab

9 ab

0a

8b

6a

11 ab

9 ab

7b

10 ab

23 a

35 + 13

36 a

30 a

28 a

44 a

-43 a

33 a

11 a

29 a

44 a

44 a

20 a

25 a

Nicosulfuron +

35 +

11 ab

10 ab

16 ab

9 ab

7a

9 ab

12 a

16 ab

9 ab

8 ab

17 a

13 ab

Topramezone +

18 +

Isoxadifen-ethyl

13 10 ab

6b

14 ab

8b

0a

7b

5a

14 ab

8 ab

8 ab

13 ab

23 a

0b

0b

0b

0b

0a

0b

0a

0b

0b

0b

0b

0b

Nicosulfuron + Isoxadifen-ethyl

Nicosulfuron+

35 +

Mesotrione+

105 +

Isoxadifen-ethyl c

Treated check

13 ---

22

ACS Paragon Plus Environment

Page 23 of 26

Journal of Agricultural and Food Chemistry

a

No study by treatment interaction occurred for any fatty acid data, therefore these data were pooled over studies.

b

All treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.

c

Treated check was not included in the statistical analysis.

23

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

Page 24 of 26

Table 4. Percent increase in concentrations of proteins, acid detergent fiber (ADF), neutral detergent fiber (NDF), and key minerals for Incredible’ sweet corn (Zea mays L. var. rugose) following applications of carotenoid and amino acid biosynthesis inhibitors applied alone and in mixtures with the Photosystem II inhibitors atrazine. Proteins, Acid Detergent Fiber, Neutral Detergent Fiber, and Mineralsa Herbicide treatmentb

Rate

Proteins

ADF

NDF

Ca

P

Mg

K

Na

Fe

Mn

Zn

Cu

———————————————— % increase ———————————————

g ai/ha Nicosulfuron

35

7 bc

9b

4c

0b

6 bc

14 bc

1 bc

21 a

14 b

33 b

2b

0a

Mesotrione

105

6 bcd

10 b

13 b

0b

12 ab

20 b

12 ab

21 a

21 b

25 bc

16 b

0a

Topramezone

18

8b

2b

7 bc

0b

8 ab

13 bc

6 bc

29 a

23 b

38 b

4b

0a

35 + 13

12 a

30 a

21 a

0b

14 a

41 a

18 a

21 a

31 ab

42 b

51 a

0a

Nicosulfuron +

35 +

5 cd

8b

7 bc

0b

8 ab

27 ab

5bc

36 a

67 a

75 a

14 b

0a

Topramezone +

18 +

Isoxadifen-ethyl

13 4d

13 b

7 bc

100 a

8 ab

20 b

3 bc

0a

26 b

38 b

9b

0a

0e

0b

0c

0b

0c

0c

0c

0a

0b

0c

0b

0a

Nicosulfuron + Isoxadifen-ethyl

Nicosulfuron+

35 +

Mesotrione+

105 +

Isoxadifen-ethyl c

Treated check

13 ---

a

No study by treatment interaction occurred for any protein, fiber, or mineral element data, therefore these data were pooled over studies.

b

All treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.

c

Treated check was not included in the statistical analysis.

24

ACS Paragon Plus Environment

Page 25 of 26

Journal of Agricultural and Food Chemistry

Table 5. Percent increase in concentrations of key sugars and antioxidants for Incredible’ sweet corn (Zea mays L. var. rugose) following applications of carotenoid and amino acid biosynthesis inhibitors applied alone and in mixtures with the Photosystem II inhibitors atrazine. Sugars

Antioxidants Gamma-

Herbicide treatmentb

Rate

Total Sugars

Fructose

Glucose

Maltose

Sucrose

Lutein

Zeaxanthin

antheraxanthin tocopherol

———————————————— % ———————————————

g ai/ha Nicosulfuron

35

16 a

48 ab

35 ab

23 a

-4 ab

9a

9a

15 a

1 ab

Mesotrione

105

-4 c

18 ab

19 ab

15 ab

-32 c

17 a

1a

14 a

5a

Topramezone

18

10 ab

63 a

40 a

8 bc

-18 bc

0a

-8 a

23 a

8a

35 + 13

10 ab

68 a

43 a

-15 d

-15 abc

0a

-2 a

19 a

-3 ab

Nicosulfuron +

35 +

11 ab

63 a

42 a

8 bc

-21 bc

2a

-5 a

49 a

-10 b

Topramezone +

18 +

Isoxadifen-ethyl

13 9 ab

31 ab

23 ab

4c

2a

7a

-1 a

21 a

0 ab

0 bc

0b

0b

0c

0a

0a

0a

0a

0 ab

Nicosulfuron + Isoxadifen-ethyl

Nicosulfuron+

35 +

Mesotrione+

105 +

Isoxadifen-ethyl c

Treated check

13 ---

a

No study by treatment interaction occurred for any sugar or antioxidant data, therefore these data were pooled over studies.

b

All treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.

c

Treated check was not included in the statistical analysis.

25

ACS Paragon Plus Environment

Journal of Agricultural and Food Chemistry

338x190mm (96 x 96 DPI)

ACS Paragon Plus Environment

Page 26 of 26