Article Cite This: J. Agric. Food Chem. 2018, 66, 3086−3092
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Several Pesticides Influence the Nutritional Content of Sweet Corn Matthew A. Cutulle,*,†,∥ Gregory R. Armel,‡,∥ Dean A. Kopsell,§,∥ Henry P. Wilson,⊥ James T. Brosnan,∥ Jose J. Vargas,∥ Thomas E. Hines,⊥ and Rebecca M. Koepke-Hill∥ †
Coastal Research and Education Center, Clemson University, Charleston, South Carolina 29414, United States Global Herbicide Development Group, BASF Corporation, Research Triangle Park, North Carolina 27709, United States § Environmental Horticulture Department, The University of Florida, Gainesville, Florida 32611, United States ∥ Plant Sciences Department, The University of Tennessee, Knoxville, Tennessee 37996, United States ⊥ Eastern Shore Agricultural Research and Extension Center, Virginia Polytechnic Institute and State University, Painter, Virginia 23420, United States ‡
ABSTRACT: Herbicides are pesticides used to eradicate unwanted plants in both crop and non-crop environments. These chemistries are toxic to weeds due to inhibition of key enzymes or disruption of essential biochemical processes required for weedy plants to survive. Crops can survive systemic herbicidal applications through various forms of detoxification, including metabolism that can be enhanced by safeners. Field studies were conducted near Louisville, Tennessee and Painter, Virginia to determine how the herbicides mesotrione, topramezone, nicosulfuron, and atrazine applied with or without the safener isoxadifen-ethyl would impact the nutritional quality of “Incredible” sweet corn (Zea mays L. var. rugosa). Several herbicide treatments increased the uptake of the mineral elements phosphorus, magnesium, and manganese by 8−75%. All herbicide treatments increased protein content by 4−12%. Applied alone, nicosulfuron produced similar levels of saturated, monounsaturated, and polyunsaturated fatty acids when compared to the nontreated check, but when applied with isoxadifen-ethyl, fatty acids increased 8 to 44% relative to the check or control. Nicosulfuron plus isoxadifen-ethyl or topramezone or the combination of all three actives increased the concentrations of fructose and glucose (40−68%), whereas reducing levels of maltose or sucrose when compared to the nontreated check (−15 to −21%). Disruptions in biochemical pathways in plants due to the application of herbicides, safeners, or other pesticides have the potential to alter the nutrient quality, taste, and overall plant health associated with edible crops. KEYWORDS: amino acids, carotenoids, fatty acids, fiber, herbicide dose.4−6 How herbicides applied to edible crops at registered rates can impact biosynthetic pathways responsible for the production or uptake of key nutrients beneficial to consumers of these plants has not been demonstrated. Mesotrione is a member of the triketone family of herbicides, which is structurally similar to leptospermone, a natural phytotoxin obtained from the Californian bottlebrush plant (Callistemon citrinus Stapf.).7 Mesotrione primarily controls broadleaf weeds from both a foliar and soil residual perspective.7 Topramezone is a member of the pyrazolone family of herbicides and typically provides better grass control and crop selectivity in corn compared to mesotrione but has limited soil residual activity.7 Both herbicides are carotenoid biosynthesis inhibitors (CBI) currently labeled for weed control in corn (Zea mays L.) production.8 These herbicides competitively inhibit the enzyme p-hydroxyphenylpyruvate dioxygenase (HPPD), an essential component for the biochemical conversion of tyrosine to plastoquinone and αtocopherol. Plastoquinone is a critical cofactor for phytoene
1. INTRODUCTION Pesticides are substances that are used to repel, eradicate, or destroy the life cycle of pests. Over 900 million metric tons of pesticides are used annually in the United States to control many pests including, but not limited to insects, microbes, rodents, and weeds.1 Pesticides that control weeds are referred to as herbicides. There are close to 300 commercially available herbicides that target 27 different mechanisms within plants, including enzymes involved in the biosynthesis of carotenoids, chlorophyll, amino acids, fatty acids, lipids, and cellulose. The application of a pesticide concomitantly providing pest control and improved nutrition in a single crop system is not intuitive, although these chemicals induce physiological responses in both crops and weeds. Furthermore, collective societal attitudes toward pesticides are associated with less healthy fruits and vegetables.2 However, exploitation of plant biosynthetic pathways using pesticides may reveal chemical technologies that provide weed control and improve the nutrition of crops. The term hormesis describes how a low dose of a toxic substance such as a pesticide can be used to increase growth or output of certain biological processes.3,4 Low use rate applications of herbicides applied to specific crops can increase biomass, growth, protein content, and disease resistance. In these scenarios, herbicides were usually applied at sublethal or less than optimal rates to crops that would have been severely injured or killed had the herbicide been applied at an optimal © 2018 American Chemical Society
Received: Revised: Accepted: Published: 3086
December 15, 2017 February 12, 2018 February 12, 2018 February 12, 2018 DOI: 10.1021/acs.jafc.7b05885 J. Agric. Food Chem. 2018, 66, 3086−3092
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Journal of Agricultural and Food Chemistry
depth of 2.5 cm in a Emory silt loam soil (Fine-silty, siliceous, active, thermic Fluventic Humic Dystrudepts) and silt loam soil (fine loamy, siliceous, thermic, Humic Hapudult) spaced at 25 cm in row and 76 cm between rows. Each plot consisted of four rows of corn, 6.1 m in length. Sweet corn was planted similarly at the VA location into a Bojac sandy loam (Typic Hapludults) with less than 1% organic matter. Preemergence (PRE) applications were made to all plots using S-metolachlor + atrazine (Biceps II Magnum: Syngenta Crop Protection, Inc.) at 2190 g of active ingredient per hectare (g ai/ha) to reduce weed pressure in the plots. The insecticide λ-cyhalothrin (Warrior: Syngenta Crop Protection, Inc.) was applied PRE to all plots at 32 g ai/ha to reduce stand loss from insects such as cutworms (Agrotis spp.). This field study included the following 7 treatments: (1) nicosulfuron 35 g ai/ha, (2) mesotrione 105 g ai/ha, (3) topramezone 18 g ai/ha, (4) nicosulfuron 35 g ai/ha + isoxadifen-ethyl 13 g ai/ha, (5) nicosulfuron 35 g ai/ha + topramezone 18 g ai/ha + isoxadifenethyl 13 g ai/ha, (6) nicosulfuron 35 g ai/ha + mesotrione 105 g ai/ha + isoxadifen-ethyl 13 g ai/ha, and (7) a treated check (atrazine at 560 g ai/ha). All treatments included atrazine at 560 g ai/ha. Atrazine, a common broadleaf herbicide used in corn production, controls weeds by inhibiting site A of the Qb binding niche of the D1 protein in photosystem II (PSII).19 Like mesotrione, rapid metabolism of atrazine affords tolerance in maize genotypes.19 Treatments contained an adjuvant of crop oil concentrate applied at 1% v/v and were applied to sweet corn plants approximately 5 to 10 cm in height. Herbicide and safener application rates were extrapolated from the product label. In Tennessee, herbicide treatments were applied using a CO2 powered backpack sprayer calibrated to deliver 215 L per hectare water carrier volume using an 8002 flat fan nozzle. In Virginia, herbicides treatments were applied with compressed air from a tractor mounted sprayer calibrated to deliver 236 L per hectare water carrier volume using an 8003 flat fan nozzle. All plots were manually hand-weeded as necessary to prevent potential variations in yield and nutrient content associated with weed competition. Visual observations of foliar injury were measured approximately seven days following herbicide treatment. Antioxidant, sugar, amino acids, protein, fatty acids, mineral elements, and fiber content in mature sweet corn kernels were measured 45 days after treatment. 2.2. Harvest and Laboratory Analysis. Eight uniform sweet corn ears were collected from the center of the treated area of each plot and stored for 48 h in a walk-in cooler (4 °C). During processing, a 5 cm section was cut from the central region of each ear of the experimental samples and saved for nutrient analyses. Five g of tissue was macerated for chemical preparation. Sugar content was assessed using a method developed by Zygmunt, fatty acids by Sukhija and Palmquist, amino acids and proteins by AOAC, fiber by Soest et al., antioxidants (carotenoids and gamma tocopherol) by Kurilich and Juvik along with Davies and Kost, and mineral content by OMOA.20−27 2.3. Data Analysis. All data were converted to percent change compared to the treated check and subjected to analysis of variance (ANOVA), and means were subsequently separated using Fisher’s protected LSD at the 95% confidence interval. Normality diagnostics were applied to data and were considered acceptable based on the Shapiro−Wilk diagnostic. All data were pooled across statistical runs considering no run-by-treatment interactions were observed.
desaturase as well as an intermediate electron carrier in the photosynthetic electron transport chain. Nicosulfuron is a sulfonylurea herbicide that kills weeds by inhibiting the enzyme acetolactate synthase (ALS). This enzyme is responsible for the biosynthesis of the branched chain amino acids valine, leucine, and isoleucine. Nicosulfuron primarily control grass weeds in a grass crop such as corn; however, nicosulfuron has limited selectivity in sweet corn (Zea mays L. var. rugosa).9,10 Using a safener, isoxadifen-ethyl, with nicosulfuron permits its use in several sweet corn varieties.11 Safeners such as isoxadifen-ethyl are a chemically diverse group of compounds that increase expression of enzymes such as glutathione S-transferases and cytochrome P450 monooxygenases.12 Activation of these enzymes results in detoxification of some herbicides. In the case of isoxadifen-ethyl, sweet corn hybrids that are heterozygous for a specific P450 (i.e., CYPcyp) can safely be treated with mixtures of certain HPPD and ALS inhibiting herbicides and isoxadifen-ethyl.11 Often ALS, HPPD inhibitors, and herbicides safeners such as isoxadifen-ethyl will be applied in mixtures to provide broad-spectrum weed control with optimal crop tolerance in several different types of corn, including sweet corn.13 Corn is the leading cereal crop in the world with greater than 1 billion metric tons produced annually and is ideally suited to conduct nutritional studies.14 Improvements in molecular and genomic technologies have allowed for improved nutrition in crops such as corn.15 In addition to nutritional benefits, sweet corn has a significant impact on the United States agricultural economy. A total of 210,972 ha of sweet corn were harvested commercially in 2014 in the United States with a total production value of $1.09 billion.16 Improving sweet corn nutrition through herbicide and safener applications could potentially be valuable by aiding in dietary changes that may decrease the incidence of diabetes, cardiovascular disease, and metabolic syndromes.15 Applications of mesotrione plus atrazine increased carotenoid (antioxidant) content in sweet corn, but nothing is known regarding what other nutrient impacts may occur from use of these mixtures.17 Additionally, there are no reports on how ALS inhibitors or safeners will impact the nutrient quality of sweet corn. Our research aims to understand how inhibitors of HPPD and ALS with and without the safener isoxadifen-ethyl can impact the uptake of mineral elements and the production of key nutrients including proteins, amino acids, fatty acids, fiber, sugars, and various antioxidants.
2. MATERIALS AND METHODS Field and laboratory studies were conducted in 2009 to evaluate postemergence (POST) applications of mesotrione, topramezone, and nicosulfuron in mixtures with atrazine applied alone or with the safener isoxadifen-ethyl. The sweet corn variety “Incredible” was chosen for these studies based on the findings of Kopsell et al. that determined it was moderately tolerant to HPPDs and able to yield increased antioxidant content via applications of mesotrione plus atrazine.17 The “Incredible” variety is a yellow kernel genotype and is a sugar enhanced variety but also maintains its sweetness longer than standard sweet corn varieties.18 2.1. Field Trials. Field trials were established at the East Tennessee Research and Education Center Blount Unit in Louisville, TN (35.84 latitude, −83.95 longitude) on June 3, 2009. “Incredible” sweet corn was seeded in a randomized complete block design with three replications. A second trial location was established at the Eastern Shore Agricultural Research and Extension Center in Painter, VA (37.58 latitude, −75.83 longitude). In TN, seeds were drill planted at a
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RESULTS AND DISCUSSION 3.1. Amino Acids. There were no significant differences in sweet corn yield among treatments, although application of mesotrione alone resulted in the greatest visual damage to corn plants (8%) (Table 1). When evaluating amino acid content, plants treated with nicosulfuron alone produced similar concentrations of amino acids when compared to the treated check except for proline, which was reduced by 7%. However, when nicosulfuron was applied with isoxadifen-ethyl, this treatment resulted in the highest kernel amino acid content,
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No study by treatment interaction occurred for any amino acid data; therefore, these data were pooled over studies. bAll treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate. a
1b 12 b 10 b 28 a 6b 6b 0b 0c 6 abc 8 ab 12 a 1 bc 4 bc 0c
leucine isoleucine
0c 6 abc 10 ab 14 a 0c 3 bc 0c a a a a a a a 0 2 8 4 8 4 0
methionine valine
0c 7 abc 9 ab 13 a −1 c 5 abc 0 bc ab ab a ab ab b b 1 4 8 1 6 0 0
alanine cysteine
0 cd 6b 3 bc 12 a −3 d 2 bcd 0 cd −4 b 4 ab 4 ab 9a 4 ab 0b 0b
significantly raising all amino acids except alanine and methionine by 9−28%. The largest increase in amino acids from the nicosulfuron plus isoxadifen-ethyl treatment was in lysine, which is beneficial from a nutrition perspective considering corn is naturally deficient in lysine.28 This deficiency of lysine in corn is most concerning in areas where corn is used as the primary source of dietary protein in both humans and domesticated animals.28 Topramezone alone and nicosulfuron plus isoxadifen-ethyl increased the amount of the branched chain amino acids leucine and isoleucine by 8−14% (Table 2). The benefits of increased branched chain amino acid consumption for humans include increased muscle tissue along with decreased muscle fatigue.29 In addition, branched chain amino acids also help regulate many mammalian biosynthetic pathways, including the regulation of blood sugar and the prevention of insulin insensitivity.30 3.2. Fatty Acids. Analysis of fatty acid content also highlighted some significant differences when comparing nicosulfuron applied alone or with isoxadifen-ethyl. The nicosulfuron plus isoxadifen-ethyl treatment was the only treatment to yield total fatty acid content significantly greater than the treated check (Table 3). This treatment significantly increased all fatty acid saturation groupings by 28 to 44%. The individual fatty acids that were increased by the nicosulfuron plus isoxadifen-ethyl treatment included arachidic acid, behenic acid, oleic, linoleic acid, α-linoleic acid, and palmitic acid. Another important trend to note is that application of nicosulfuron plus isoxadifen-ethyl increased polyunsaturated fatty acids by 44% relative to the check. Polyunsaturated fatty acids reduce bad cholesterol and the risk of heart disease in humans.31 3.3. Protein, Fiber, and Minerals. When evaluating protein, fiber, and mineral content extracted from kernels, the nicosulfuron plus isoxadifen-ethyl treatment resulted in superior nutrient content (Table 4). Protein increased by 12% relative to the treated check in kernels treated with nicosulfuron plus isoxadifen-ethyl, whereas all other treatments increased protein content between 4 and 8%. Both fiber types (acid detergent fiber and neutral detergent fiber), P, Mg, K, Mn, and Zn were increased by 14−51% with the nicosulfuron
glycine
9437 a
−7 d 9a 6 ab 10 a 3 cb 4 cb 0c
0b
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. bAll treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.
proline
3a
a
−2 c 6 ab 6 abc 10 a 2 abc 1 bc 0 bc
8418 a
2c 16 a 12 ab 12 ab 3c 7 bc 0c
8a
−4 c 7 ab 6 ab 12 a 3 abc −1 bc 0 bc
4a
−1 d 6 abc 7 ab 10 a 1 bcd 2 bcd 0 cd
a a a a a
35 105 18 35 + 13 35 + 18 + 13 35 + 105 + 13
7689 6747 7847 9002 7868
ab a ab ab ab
nicosulfuron mesotrione topramezone nicosulfuron + isoxadifen-ethyl nicosulfuron + topramezone + isoxadifen-ethyl nicosulfuron + mesotrione + isoxadifen-ethyl treated check
7 8 4 5 4
glutamic acid
a a a a a
yield (kg/ha)
threonine
5 5 5 4 5
14 DAT
aspartic acid
35 105 18 35 + 13 35 + 18 + 13 35 + 105 + 13
7 DAT
total amino acids
nicosulfuron mesotrione topramezone nicosulfuron + isoxadifen-ethyl nicosulfuron + topramezone + isoxadifen-ethyl nicosulfuron + mesotrione + isoxadifen-ethyl treated check
rate (g ai/ha)
rate (g ai/ha)
herbicide treatmentb
herbicide treatmentb
injurya (%)
amino acidsa (% increase)
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 Inhibitor Atrazine
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 Inhibitor Atrazine
lysine
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DOI: 10.1021/acs.jafc.7b05885 J. Agric. Food Chem. 2018, 66, 3086−3092
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0b 0b 0b 0b 0b 0a 0b 0a 0b 0b 0b 0b
No study by treatment interaction occurred for any fatty acid data; therefore, these data were pooled over studies. bAll treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.
plus isoxadifen-ethyl treatment. No treatments increased Cu or Na in sweet corn kernels, and only the nicosulfuron plus mesotrione plus isoxadifen-ethyl treatment increased Ca levels (100%). Zn, Mg, Cu, and Fe are limiting nutrients in cereal crops, especially in areas where these crops are a primary source of nutrition for the population of that region.32 Moreover, the 67% increase of Fe from the nicosulfuron plus isoxadifen-ethyl treated plants should be further highlighted, as Fe deficiency is one of the most common nutrient deficiencies in the world. A deficiency in Fe can lead to anemia and other severe health conditions. Iron deficiency is most often observed in women and is particularly concerning during pregnancy.33 3.4. Sugar and Antioxidants. Kernals from all treatments contained the same amount of total sugars, except the nicosulfuron alone treatment, which increased total sugar content by 16% (Table 5). Fructose and glucose levels were increased by applications of topramezone, nicosulfuron plus isoxadifen-ethyl, and topramezone plus nicosulfuron plus isoxadifen-ethyl. These increases in the monosaccharides fructose and glucose tended to be offset by decreases in the disaccharides maltose or sucrose. Fructose is the sweetest of the natural sugars, and any increase should increase the perceived sweetness of the sweet corn, especially considering the offset decrease in maltose or sucrose.34 Sweetness and tenderness are the two qualities most associated with improving the eating quality of sweet corn.35 However, increases in fructose, while potentially beneficial from a sweetness perspective, may be negative from a human health perspective as fructose is not digested in the same manner as other sugars, and higher concentrations of fructose in the human diet is linked to obesity, diabetes, hypertension, and heart disease.36 There were no significant differences between any of the treatments for carotenoid content. 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 increased concentrations of nutritionally important fatty acids, protein, amino acids, fiber, sugar, and minerals in sweet corn genotypes through applications of HPPD-inhibiting and ALS-inhibiting herbicides and the safener isoxadifen-ethyl. The key question is what mechanism leads to these increases? In general, corn rapidly metabolizes herbicides such as mesotrione into non-herbicidal byproducts. Moreover, corn can rapidly outgrow sensitivity in the form of leaf tissue bleaching, which results from suppression of carotenoid biosynthesis following application of mesotrione to sensitive varieties. At the time of harvest, no mesotrione residues were found in sweet corn kernels.17 In addition, field corn hybrids rapidly metabolize nicosulfuron; however, sweet corn varieties can be much more sensitive.37 When applied with safeners such as isoxadifen-ethyl, 84% of nicosulfuron is metabolized in a few days.38 These herbicides are applied just weeks after corn emergence and are degraded in plants within days of application. That being said, how do these herbicides affect the nutrient content of sweet corn kernels harvested approximately two months after application? The most interesting and impactful treatment from these studies was nicosulfuron plus isoxadifen-ethyl. Safeners are believed to enhance enzyme activity that results in conjugating and detoxifying xenobiotics such as herbicides.12 The safener isoxadifen-ethyl has multiple impacts in the metabolism of xenobiotics in corn plants. First, isoxadifen-ethyl upregulates certain cytochrome P450 monooxygenases that appear to be
a
23 a 13 ab 8 ab 8 ab 14 ab 5a 7b 0a 8b 6b 10 ab 35 + 105 + 13
14 ab
13 ab 17 a 8 ab 9 ab 16 ab 12 a 9 ab 7a 9 ab 16 ab 11 ab 35 + 18 + 13
10 ab
ab ab a a 13 13 23 25 a ab ab a 17 10 10 20 10 ab 15 ab 7b 44 a 12 ab 13 ab 9 ab 44 a ab ab ab a 16 10 11 29 12 ab 9 ab 8b 33 a 15 ab 9 ab 10 ab 28 a 12 ab 7 ab 9 ab 30 a 13 ab 11 ab 9 ab 36 a 35 105 18 35 + 13
nicosulfuron mesotrione topramezone nicosulfuron + isoxadifenethyl nicosulfuron + topramezone + isoxadifen-ethyl nicosulfuron + mesotrione + isoxadifen-ethyl treated check
herbicide treatment
12 ab 12 ab 9 ab 44 a
−50 a −21 a 0a −43 a
10 a 1a 6a 11 a
behenic acid (C22:0) arachidic acid (C20:0) α-linoleic acid (C18:3) linoleic acid (C18:2) oleic acid (C18:1) stearic acid (C18:0) palmitic acid (C16:0) myristoleic acid (C14:1) total poly unsaturated fatty acids total mono unsaturated fatty acids total saturated fatty acids total fatty acids rate (g ai/ha) b
fatty acids (individual) (% increase) fatty acids (by saturation grouping) (% increase)
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 Inhibitor Atrazine
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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 % increase herbicide treatmentb nicosulfuron mesotrione topramezone nicosulfuron + isoxadifen-ethyl nicosulfuron + topramezone + isoxadifen-ethyl nicosulfuron + mesotrione + isoxadifen-ethyl treated check
rate (g ai/ha) 35 105 18 35 + 13 35 + 18 + 13 35 + 105 + 13
proteins
ADF
NDF
7 bc 6 bcd 8b 12 a 5 cd
9b 10 b 2b 30 a 8b
4c 13 b 7 bc 21 a 7 bc
0b 0b 0b 0b 0b
Ca
6 bc 12 ab 8 ab 14 a 8 ab
P
14 20 13 41 27
Mg
4d
13 b
7 bc
100 a
8 ab
0e
0b
0c
0b
0c
bc b bc a ab
K
Na a a a a a
Fe
1 bc 12 ab 6 bc 18 a 5bc
21 21 29 21 36
14 21 23 31 67
b b b ab a
20 b
3 bc
0a
26 b
0c
0c
0a
0b
Mn 33 25 38 42 75
b bc b b a
Zn
Cu
2b 16 b 4b 51 a 14 b
0 0 0 0 0
a a a a a
38 b
9b
0a
0c
0b
0a
No study by treatment interaction occurred for any protein, fiber, or mineral element data; therefore, these data were pooled over studies. All treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.
a
b
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 Inhibitor Atrazine % increase sugars herbicide treatmentb nicosulfuron mesotrione topramezone nicosulfuron + isoxadifen-ethyl nicosulfuron + topramezone + isoxadifen-ethyl nicosulfuron + mesotrione + isoxadifen-ethyl treated check
rate (g ai/ha)
total sugars
35 105 18 35 + 13 35 + 18 + 13 35 + 105 + 13
16 a −4 c 10 ab 10 ab 11 ab
48 18 63 68 63
9 ab
31 ab
0 bc
0b
fructose ab ab a a a
glucose
antioxidants sucrose
lutein
zeaxanthin
23 a 15 ab 8 bc −15 d 8 bc
−4 ab −32 c −18 bc −15 abc −21 bc
9a 17 a 0a 0a 2a
9a 1a −8 a −2 a −5 a
15 14 23 19 49
23 ab
4c
2a
7a
−1 a
21 a
0 ab
0b
0c
0a
0a
0a
0a
0 ab
ab ab a a a
antheraxanthin
γ-tocopherol
maltose
35 19 40 43 42
a a a a a
1 ab 5a 8a −3 ab −10 b
a
No study by treatment interaction occurred for any sugar or antioxidant data; therefore, these data were pooled over studies. bAll treatments (including the treated check) included atrazine at 560 g ai/ha plus an adjuvant of 1% v/v crop oil concentrate.
the primary mechanism by which it detoxifies herbicides such as nicosulfuron.39 Second, it can upregulate glutathione Stransferases.40 Overexpression of glutathione S-transferases improves stress tolerance in plants.41 If we assume plant growth requires upregulation of key plant processes, then this may help explain some of the responses noted with the mixture of nicosulfuron plus isoxadifen-ethyl. However, if this is the case, then why do the three-way mixtures of HPPD plus nicosulfuron plus isoxadifen-ethyl provide less pronounced improvements in sweet corn kernel nutrient content? Also, if the safener is so critical in helping with these nutrient increases, then why do we observe increases in total sugars, some mineral elements, neutral detergent fiber, key amino acids, and behenic acid with applications of nicosulfuron, mesotrione, or topramezone applied without isoxadifen-ethyl (Tables 3−5)? These dramatic increases that result from various applications of specific herbicides with or without isoxadifen highlight the complexity of the pathways and mechanisms involved in these nutritional changes. Another partial explanation for the increases in nutrient content may be related to the increases in mineral elements concentrations observed in this study. Several of the herbicide treatments in our studies stimulated uptake of mineral elements from soil (Table 4). The uptake of certain mineral elements may be increased in corn under stress. The stress in our studies
most likely was induced in reaction to the herbicide treatments. Although the degree of corn injury following herbicide treatment was modest in these studies, this stress was only measured visually at a fixed point in time, and the total stress from these herbicides may not have been captured thoroughly via a subjective rating. Corn placed under stress can increase uptake of Fe, Mg, Mn, Cu, and N from the soil.42 In addition, increases in mineral element concentrations have the potential to enhance biochemical processes that impact the synthesis of many nutrients. For example, increases in Fe content in pea (Pisum sativum L.) seedlings caused them to have more unsaturated fatty acids.43 The nicosulfuron plus isoxadifen-ethyl treatment in our studies displayed the highest levels of Fe content and similarly altered the ratios of fatty acids in the corn kernels, leading to increases in unsaturated fatty acids (Tables 3 and 4). Also, deficiencies in Mg, Mn, and Fe in alfalfa (Medicage sativa L.) have led to decreases in the production of key amino acids.44 The aforementioned mineral elements were increased by the nicosulfuron plus isoxadifen-ethyl treatment in our studies, and most amino acids evaluated were also increased by this treatment. The concept of herbicides increasing certain nutrients (e.g., carotenoids, antioxidants) was documented previously at the University of Tennessee.17 Our studies concluded that many different, seemingly unconnected, plant processes can be 3090
DOI: 10.1021/acs.jafc.7b05885 J. Agric. Food Chem. 2018, 66, 3086−3092
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Journal of Agricultural and Food Chemistry
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changed in the presence of herbicides and isoxadifen-ethyl. These results again highlight the complex biochemical and physiological mechanisms activated when multiple herbicides or herbicides plus safeners such as isoxadifen-ethyl are applied to crops such as sweet corn. These interactions could be further elucidated through transcriptome and metabolomics studies to uncover the exact sequence of activities that occur following application until harvest. More comprehensive experiments should focus on multiple variety trials and include additional corn herbicide safeners, such as cyprosulfamide across multiple additional states with different soil types and climatic conditions. Additionally, taste panel tests should be developed for assessing the impact of safener plus herbicide treatments on the taste of sweet corn. Calcium and sugar content can both impact flavor; thus, coupling specific plant genetics with key herbicides and safeners may improve or modify not only the nutritional content but also the taste of sweet corn or other fruits, vegetables, and grains.35,45,46 These results may help create a novel subfield in agriculture where pesticide application strategies are not only evaluated for their ability to control pests but for their potential to enhance crop nutrition and taste.
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AUTHOR INFORMATION
Corresponding Author
*Phone: (843) 402-5399; Fax: (843) 571-4654; E-mail:
[email protected]. ORCID
Matthew A. Cutulle: 0000-0002-3572-2498 Notes
The authors declare no competing financial interest.
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DOI: 10.1021/acs.jafc.7b05885 J. Agric. Food Chem. 2018, 66, 3086−3092
