Next Article in Journal
Combined Effect of Cinnamon Bark Oil and Packaging Methods on Quality of Fresh Lamb Meat Patties during Storage at 4 °C
Previous Article in Journal
Reducing Antigenicity and Improving Antioxidant Capacity of β-Lactoglobulin through Covalent Interaction with Six Flavonoids
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Foods
Volume 12
Issue 15
10.3390/foods12152914
foods-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Effect of Imidacloprid on the Volatile Organic Compound Profile of Strawberries: New Insights from Flavoromics

by
Ning Yue
1,†,
Hongping Wang
1,†,
Chunmei Li
2,
Chen Zhang
1,
Simeng Li
1,
Jing Wang
1 and
Fen Jin
1,*
1
Key Laboratory of Agro-Product Quality and Safety, Institute of Quality Standards & Testing Technology for Agro-Products, Chinese Academy of Agricultural Sciences, Beijing 100081, China
2
Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Foods 2023, 12(15), 2914; https://doi.org/10.3390/foods12152914
Submission received: 27 June 2023 / Revised: 26 July 2023 / Accepted: 28 July 2023 / Published: 31 July 2023
(This article belongs to the Section Foodomics)
Browse Figures
Review Reports Versions Notes

Abstract

:
Organic agriculture is of great socioeconomic significance because it can promote the nutritional quality of horticultural crops and is environmentally friendly. However, owing to the lack of techniques for studying complex aroma-related chemical profiles, limited information is available on the influence of organic practices on the flavor quality of strawberries, one of the primary factors driving consumer preferences. Here, two-dimensional gas chromatography combined with time-of-flight mass spectrometry (GC×GC-TOF-MS) and flavoromics analysis was employed to investigate the profiles and differences in the volatile organic compounds (VOCs) of strawberries under organic (without imidacloprid) and conventional (with imidacloprid) agricultural practices. A total of 1164 VOCs, representing 23 chemical classes (e.g., aldehydes, terpenes, and furanone compounds), were detected, which is the highest number of VOCs that have ever been detected in strawberries. The sensory evaluation results indicated that there was a notable influence of imidacloprid (IMI) on the aroma of the strawberries. Principal component analysis and partial least squares discriminant analysis results suggested that the composition of volatile compounds significantly differed in the present study between the IMI-treated and non-IMI-treated groups. Furthermore, the flavor-related indicators of 25 key contributors to the differences between the two treatment groups suggested that VOC profiles can be considered an indicator for distinguishing between strawberries from different agricultural practices. Flavoromics can provide new insights into the quality of strawberries from different agricultural practices.

Graphical Abstract

1. Introduction

Strawberries (Fragaria × ananassa) are a valuable fruit, cultivated worldwide, and provide consumers with a rich sensory experience and antioxidants [1]. In 2021, the global Gross Production Value of strawberries was over US$ 22.87 billion, 7.68–37.85 times higher than that of raspberries, blueberries, and cranberries [2]. In recent years, organic farming has flourished due to prohibitions of synthetic fertilizers and pesticides, and is friendly to ecosystems, animals, and humans. Approximately 88.15% of 559 valid questionnaires agreed that organic products were better than conventional ones [3]. Akšić et al. [4] found that there was a significant difference (p < 0.05) in carbohydrate content between integrated (15.77 mg/g) and organic (10.67 mg/g) strawberries. The anthocyanin content is also significantly lower (p < 0.05) in strawberry puree from conventional cultivation systems (174.11 mg/kg) than in strawberry puree from organic cultivation systems (291.24 mg/kg) [5]. Furthermore, higher ascorbate to dehydro-ascorbate ratios, total phenolic contents, and greater antiproliferative activities were detected in organically cultivated strawberries than in conventionally grown strawberries [6]. However, there is still limited knowledge of how organic practices may affect the abundance and composition of aroma components in strawberries. Flavor is one of the primary drivers of consumer preferences for strawberries [7]. Does the organic agricultural (OA) production mode increase the flavor of strawberries in comparison with conventional agriculture (CA)? More evidence is needed to fill this knowledge gap.
The flavoromics strategy has been collectively considered, and provides new perspectives on the correlation between the aroma of foods and their chemical profiles [8], which can help us understand VOC profiles comprehensively. At the time of writing, a total of 979 VOCs have been detected in strawberries by gas chromatography-flame ionization detection (GC-FID), gas chromatography−mass spectrometry coupling (GC-MS), gas chromatography-ion mobility spectrometry (GC-IMS), and multidimensional gas chromatography (MDGC-MS) [9]. Among these techniques, MDGC-MS detected the highest amount simultaneously (567 VOCs) [10]. GC×GC-TOF-MS has been successfully used to identify aroma compounds in agro-products due to its unparalleled separation ability. Zhang et al. [11] identified 211 volatile components in green tea using GC×GC-TOF-MS, which is approximately 6.4 times more than that identified by GC-IMS. A total of 126 volatile components were detected in nuts by GC×GC-TOF-MS, approximately three times higher than that identified by GC-MS [12]. However, no information is available on the influence of pesticides on the VOC profile of strawberries. One article has reported 852 VOCs detected by GC×GC-TOF-MS in the ripe strawberry fruit under three preservative treatments, including 298 unknown compounds [13]. According to the previous study, the insecticide imidacloprid is widely used in China to protect strawberries from aphids [14], a major pest of strawberries [15]. Previous studies have reported that imidacloprid could trigger metabolic disturbances (e.g., in amino acid metabolism and saccharide catabolism) in chickpeas [16], cucumbers [17], and tomatoes [18]. However, to our knowledge, the effect of imidacloprid on the VOCs of plants has only been observed in thyme [19]. Considering the importance of VOCs to aroma and flavor perception, there is much to be further investigated regarding the VOC profiles of strawberry fruits.
Therefore, in the present study, the components and profiles of VOCs in the ripe strawberry fruit under organic (non-pesticide-treated) and conventional (pesticide-treated) cultivation practices were identified and characterized by GC×GC-TOF-MS. Furthermore, the volatile components possibly accounting for the aroma characteristics of the strawberries under different agricultural practices were explored and discussed. The results are expected to provide insights into the flavor qualities of strawberries under different agricultural practices, based on flavoromics.

2. Materials and Methods

2.1. Sample Treatment

Field experiment: Strawberry (Fragaria × ananassa Duch. cv. ‘Benihoppe’) treatments were conducted in an organic greenhouse from March 2022 to May 2022 in the Hongnile modern agricultural farm, Changping District, Beijing, China (116°09′ E, 40°13′ N). ‘Benihoppe’ is the most important strawberry cultivar grown in China. Day/night temperatures and relative humidities averaged 89.6 °F/64.4 °F (32 °C/18 °C) and 35%/80%, respectively. The organic and conventional agricultural practices in this work mainly differed with regards to pesticide control. The strawberry plants were assigned to two groups with an interval of five meters when fruit setting. The first group (control group) was sprayed with distilled water. The second group (IMI) was treated with the recommended dose (374.8 g/hm2) of imidacloprid. The two treatment groups were treated with imidacloprid and distilled water once during the growing season [20]. Both groups consisted of three replicated plots. After an exposure period of 20 days at the commercial ripening stage, six strawberry fruits were randomly selected from each plot in the two groups. These samples were rapidly frozen using liquid nitrogen, immediately transported to the laboratory, and subsequently homogenized. The homogenized fruit samples were then stored at −80 °C until they were ready for analysis.

2.2. GC×GC-TOFMS Analysis

GC conditions: carrier gas—high-purity helium (99.999%); flow—1 mL/min; split ratio—3:1; injector and transfer line temperatures—250 °C; modulation column—HV column (1.3 m × 0.25 mm I.D.×0.25 µm; Hexin Analytical Instrument Co., Ltd., Guangzhou, China); modulation period—7 s; the first-dimensional column—DB-5MS column (30 m × 0.32 mm I.D.×0.25 µm; Agilent Technologies, Santa Clara, CA, USA); temperature procedure—40 °C for 2 min, increased to 200 °C at 2 °C/min, finally ramped up to 270 °C at 6 °C/min, and held for 5 min; the second-dimensional column—DB-17 column (2 m × 0.25 mm I.D.×0.15 μm; Agilent Technologies, Santa Clara, CA, USA); oven offset temperature—+0 °C relative to the GC oven; modulator temperature offset—+30 °C relative to the secondary oven.
MS conditions: ion source temperature—250 °C; mass range—10–550 m/z; electron ionization (EI) mode—70 eV; detector voltage—−1730 V.

2.3. Qualitative Analysis and Quantitation Assurance

Calibration curves with seven calibration points were built to cover analyte amounts in the strawberry samples, with a range of 0.01–1 µg/g for 2-heptanone, benzaldehyde, 1-heptanol, 1-decene, ethyl hexanoate, DMMF, eugenol, and 1-teradecanol. The coefficients of determination (R2) were within the range of 0.9297–0.9923, illustrating the reliability of the method (Table 1 and Figure S1). Recovery experiments were carried out on strawberry samples at 0.1–0.5 µg/g with standards of 2-heptanone, benzaldehyde, 1-heptanol, 1-decene, ethyl hexanoate, DMMF, eugenol, 2-heptanone, and 1-teradecanol. Three repetitions of recovery and repeatability data were used to evaluate trueness and precision. As shown in Table 1, the recovery values for spiking the strawberry with eight external standards were 64.76–132.48%, with relative standard deviations (RSDs) of 0.48−21.17%. The limits of detection (LODs) and limits of quantification (LOQs) were calculated based on signal-to-noise (S/N) values of 3 and 10, which were in the range of 0.024–0.13 and 0.08–0.55 ng/g for the strawberry samples, respectively.

2.4. Sensory Evaluation and Statistical Analysis

Twenty-six assessors (16 females, 10 males) were assigned to sensory evaluation. The assessors were asked to evaluate the mature strawberries from two control groups and one IMI-treated group. The calyxes of fresh strawberries were removed and rinsed in water. In the sensory evaluation, the assessors rinsed their mouths with mineral water between samples, and no additional information was given to the assessors [21]. Samples were coded with three random digits. No information on sample order was provided. Based on a previously described scoring method, ‘strawberry-like aroma intensity’, ‘fresh aroma intensity’, ‘sweetness intensity’, ‘sourness intensity’, and ‘smelly intensity’ were evaluated [22].

3. Results and Discussion

3.1. GC×GC–TOFMS Topographic Plots of Strawberries under Different Treatments

The three-dimensional (3D) spectra obtained from GC×GC–TOFMS analysis are shown in Figure 1. In both treatments, most of the signals appeared in 1D-RT of 2.0–60.0 min and 2D-RT of 0.0–7.0 s. The number and relative content of volatile components in organic strawberry samples (without IMI, Figure 1A) were lower than in IMI-treated strawberry samples (Figure 1B) between 20.0 and 60.0 min of 1D-RT, and between 2.0 and 7.0 s of 2D-RT. Similar phenomena were also reported in a previous study [19], possibly due to photochemical reactions between IMI and the volatile compounds of strawberries, resulting in the release of the radical NO2 under irradiation. These results indicate that IMI treatment affected the volatile compounds of strawberries.

3.2. Identification of Volatile Components in Strawberries under Different Treatments

A total of 1164 volatile compounds (Table S2) were tentatively identified in the present study, more than have been previously detected in strawberries (979), as reviewed by Ulrich et al. [9]. The identified volatile components were classified into 23 categories in the present study (Figure 2), including esters (254), alcohols (130), ketones (101), aldehydes (77), acids (62), and others. The major compounds of esters, ketones, aldehydes, terpenes, and furanones were identified in the strawberry samples; the chromatograms and mass spectra are provided in Figure S2. The most abundant five categories were identified as the predominant flavor components of strawberries, as described in previous studies [23,24,25]. Moreover, 354 compounds were identified in strawberries for the first time compared with previous reports [9,13]. The most numerous chemical groups were the esters (61), followed by ketones (33), alkenes (33), and aldehydes (26). The results suggested that the separation ability of GC×GC-TOFMS has significant qualitative advantages.
Figure 3A shows a slightly higher total number of VOCs identified in IMI-treated strawberries (825) in comparison with the non-IMI group (779), including 440 compounds that were found in both. The number of VOCs observed in each treated group was higher (553) than in strawberries previously observed by Cannon et al. [10]. Furthermore, the combination of the most abundant five categories of aldehydes, esters, alcohols, acids, and ketones, exceeded 50% in both non-IMI and IMI-treated strawberries (Figure 3B). This result was consistent with Zhao et al. [24], where they accounted for 60% of the total. The number of aldehyde compounds under IMI treatment (68) was approximately the same as in non-IMI-treated (61) strawberries. Significantly, esters were the most numerous compounds, with higher numbers under IMI treatment (198) than in the non-IMI group (163), consistent with results reported previously in the literature [10,26]. Interestingly, IMI treatment also increased the number of alcohol and ketone compounds. This result might be due to the increased number of aldehydes, which are precursors of alcohols and ketones in strawberries, via LOX and hydroperoxide lyase (HPL) [27,28]. Similar synthetic pathways were also reported under IMI treatment in tea plants [29]. These results suggest that IMI treatment may influence the LOX-HPL pathway in strawberries. In addition, the application of IMI increased the number of acids from 37 to 51. Sharma et al. [30] and Zhou et al. [31] proposed that the accumulation of organic acids could defend against stress caused by IMI and other neonicotinoid insecticides. These results indicated that IMI triggered the stress response and interfered with the VOC composition of the strawberries.

3.3. Profile of the Volatile Components in Strawberries under Different Treatments

Figure 4 presents the peak area profiles of the volatile compound categories for the two treatment samples. The total volatile peak area was increased 1.5-fold in the IMI-treated samples relative to the non-IMI-treated samples. The main contributions to the peak areas of the two groups were from aldehydes, esters, alcohols, acids, and ketones, and accounted for more than 90% of the areas of both treatment groups. The five types of compounds mentioned above have been reported to be critical factors contributing to the fruit aroma of the ‘Benihoppe’ strawberry [32,33]. Aldehydes were the predominant compounds in the non-IMI and IMI-treated strawberry samples, which was in keeping with the previous report [34]. Yang et al. [35] found that in postharvest strawberries in the control and 1-methylcyclopropene-treated groups, aldehydes accounted for 84.53% and 86.63%, respectively. In comparison with the non-IMI group, significantly higher (p < 0.05) peak areas for aldehydes, esters, acids, ketones, and furanone compounds were found in the IMI-treated group. It has been reported that aldehydes, esters, alcohols, and ketones are mainly metabolized by the fatty acid and amino acid pathways in berries [36]. Lipoxygenase (LOX) catalyzes the oxygenation of polyunsaturated fatty acids, and was reported to be a key enzyme in the production of VOCs in fruits. Similarly, Hamilton-Kemp et al. [30] have proved that IMI affects the transcript level of the CsLOX3 gene, which was classified as the gene encoding LOX. Therefore, IMI treatment could further affect the synthesis of aldehydes, esters, alcohols, and ketones.
Aldehydes Aldehydes are mainly associated with fresh, green notes in strawberries. Hexanal, octanal, nonanal, and (E)-2-hexenal were the primary aldehydes in non-IMI and IMI-treated strawberries, accounting for 77.51% and 68.22% of the total aldehydes, respectively (Figure 5A). Several pieces of research have confirmed that of the predominant compounds in strawberries, hexanal was responsible for the fruity notes [7,36]. A higher peak area for hexanal was found in non-IMI-treated strawberries (26.22%) than with IMI treatment (18.64%). In addition, benzaldehyde appeared only in IMI-treated strawberries (6.15%) and was identified as an off-odor aroma compound in strawberries [7]. Misran et al. [37] found that during storage, hexanal was degraded while benzaldehyde was formed, which negatively influenced the aroma of the stored strawberries.
Esters Esters represent the primary source of fruity and floral odors in strawberries. The distribution differences for specific ester compounds are clearly shown in Figure 5B. Twenty ester compounds accounted for 90% of the total esters under non-IMI treatment. Methyl hexanoate was the most predominant ester in non-IMI-treated strawberries (21.55%) with a sweet flavor, in agreement with the previous observation of pineapple [35]. This was followed by ethyl hexanoate (16.69%) and methyl butyrate (11.45%). These proportions were approximately 2–4 times higher than in the IMI-treated strawberries, which suggested that IMI treatment can influence the composition of esters. Unlike the non-IMI treatment group, the top three highest percentages of total peak areas for ester compounds in IMI-treated strawberries were for ethyl butyrate (32.31%), hexyl acetate (12.80%) and ethyl hexanoate (9.62%). Of these compounds, ethyl butyrate was detected only in the IMI-treated strawberries, and has been identified as one of the key constituents of the fresh strawberry aroma [38]. Ethyl butyrate has a natural pineapple-like aroma, and is frequently found in fruits such as mango and grape. However, several previous studies reported that the content of ethyl butyrate was reduced to below the detection limit of GC-MS and GC×GC-TOFMS in frozen (below −20 °C) strawberry samples [39,40,41]. Thus, these results indicated that IMI treatment might significantly increase the content of ethyl butyrate.
Alcohols There was little influence of IMI-treatment on the profile of alcohol compounds (Figure 5C). 2-Hexen-1-ol and 1-octanol were the most abundant alcohols in non-IMI and IMI-treated strawberries, accounting for 73.75% and 79.38%, respectively. Octacosanol, which was reported as the prominent aliphatic primary alcohol in all policosanol mixtures, was first detected in strawberries and identified only in non-IMI-treated samples (4.70%) in the present study. On the contrary, (R)-Oxiranemethanol was detected only in IMI-treated strawberries (2.66%). This compound has been recognized as a probable human carcinogen in vaping products, resulting from the thermal degradation of glycerol [41], and was included in the Harmful and Potentially Harmful Constituents List in 2019 [42]. (R)-Oxiranemethanol is primarily found in refined fats, oils, and foods containing fats and oils [43,44]. In comparison, its methyl derivative was found in green tea, and strawberries with a green odor. However, (R)-Oxiranemethanol can be rapidly hydrolyzed to glycerol, and then reacts readily with glutathione to form S-(2,3-dihydroxy propyl) glutathione. Therefore, we inferred that the appearance of (R)-Oxiranemethanol in IMI-treated strawberries was due to IMI restraining the rapid metabolic pathway of (R)-Oxiranemethanol.
Ketones Ketones are mainly associated with creamy notes in strawberries. Thirteen and eight compounds accounted for 90% of the total ketones of the IMI and non-IMI-treated groups, respectively. Consistent with previous reports, 2-heptanone appeared to be the most abundant ketone in both groups, more than 1.7-fold higher in the non-IMI-treated (54.22%) strawberries (Figure 5D), followed by acetone. 2-Heptanone was reported to be one of the major constituents giving the strawberry aroma a fruity and fresh odor [45]. Methyl isobutyl ketone was found only in the non-IMI treatment group, and accounted for 5% of the total ketone compound peak area. Previous research demonstrated that methyl isobutyl ketone significantly (VIP value > 1) correlated with the consumer liking tendency, with a fruity and ethereal odor [7]. In contrast, as shown in Figure 5D, 3-octanone (11.00%) was identified only in IMI-treated strawberries with fruity and cheesy aromas. In agreement with these results, Jelen et al. [46] have found that 3-octanone was detected only in strawberries under biotic stress. Although no further information has been reported on the mechanism of this phenomenon, we suspected that 3-octanone was involved in the biotic and abiotic stress responses of strawberries.
Others Since terpenes and furan have characteristic sensory properties, these compounds are particularly interesting in strawberries. In the current study, a total of 39 terpene compounds were detected in all of the analyzed strawberry samples (Figure 5E), which was higher than that found by the HS-SPME-GC-FID (4), HS-SPME-GC-MS (10), and HS-GC-IMS (5) methodologies [11,34,41]. In non-IMI treated strawberries, the predominant terpene, linalool, accounted for 62.67% of terpenes, followed by trans-nerolidol (25.66%), and D-limonene (8.93%). In contrast, trans-nerolidol (35.73%) ranked first in the IMI-treated group, followed by nerolidol (31.84%), and linalool (29.10%). Of these terpenes, nerolidol was found only in IMI-treated strawberries with a floral odor. Linalool was a typical aroma in those strawberries with floral and lavender flavors. IMI treatment significantly reduced the linalool content (p < 0.05), which indicated that the floral odor of strawberries might be affected by IMI. In addition, 20 furan compounds were detected in all of the analyzed strawberry samples, including eight furanone compounds (Table S1). Trans-2-(2-pentenyl) furan (49.31%) and 2-pentyl-furan (43.41%), which were first found in strawberries, were the two most predominant furan compounds and were detected only in IMI-treated samples (Figure 5F). Trans-2-(2-pentenyl) furan gives mahaleb cherries a particular aroma with a fruity flavor [47]; 2-pentyl furan was more prevalent in the soybean, roasted nuts, and dried fruits [18,33]. In soybean oil, these were made from polyunsaturated fatty acids through triplet oxygen autoxidation [48], suggesting that the production of trans-2-(2-pentenyl) furan and 2-pentyl furan might be due to lipid oxidation caused by IMI [32]. Furanone was reported as the characteristic strawberry volatile compound offering a strawberry-like odor [49]. According to Figure 5F, IMI significantly (p < 0.05) reduced the content of 4-methoxy-2,5-dimethyl-3(2H)-Furanone (DMMF), which is recognized as one of the predominant contributors to the characteristic strawberry flavor. It has been reported that D-fructose and D-fructose-1,6-bisphosphate are the predominant precursors to furanone in the glucometabolic pathway, the amount of which was significantly affected by neonicotinoid insecticides [18,32]. Therefore, the profile results of volatile constituents in the present study indicate that different agricultural practices may contribute to differences in the aroma of strawberries.

3.4. Determination of Key Volatile Compounds Accounting for the Aroma Characteristics of Strawberries in the Non-IMI Treatment and IMI Treatment Groups

In order to identify the potential volatile markers of strawberry samples from different treatments, PCA and PLS-DA were performed using the peak areas of the volatile compounds. As shown in Figure S3, strawberries with 12 replicates were collected into each treatment group, and separated in the PCA (Figure S3A) and PLS-DA plots (Figure S3B), indicating that the composition of volatile compounds varied significantly between the two treatment groups.
Table 2 lists the 47 VOCs responsible for discrimination between the two groups (VIP value > 1), including 20 esters, 8 aldehydes, 6 ketones, 4 terpenes, 4 alcohols, and 2 furanones, among others. Twenty-five of the forty-seven VOCs had relatively lower odor threshold values, except for esters. Of these VOCs, D-limonene (0.034 mg/kg), (E)-2-hexenal (0.0885 mg/kg), and 2,5-dimethyl-4-methoxy-3(2H)-furanone (DMMF, 0.00003 mg/kg), which have extremely low detection thresholds, were significantly (p < 0.05) reduced in strawberries by IMI treatment, whereas methyl salicylate (0.04 mg/kg), 2-nonanone (0.04 mg/kg), and γ-dodecalactone (0.00043 mg/kg) were significantly (p < 0.05) increased, and could be used as key biomarkers for distinguishing between the flavors of the two strawberry groups. Aroma description remains fundamental to estimating the contributions of these aroma-active volatile compounds to the overall aroma impression. All seven candidate markers were reported previously for aroma descriptions of fruits, including nona-3,5-dien-2-one (green, grassy), D-limonene (citrus, mint), (E)-2-hexenal (fruity, fresh, green), DMMF (strawberry-like, floral, fruity), methyl salicylate (holly leaf, fresh), 2-nonanone (floral, oils, and herbs), and γ-dodecalactone (peach, milk peach). Among these compounds, the relative contents of D-limonene, (E)-2-hexenal, and DMMF were detected as being higher in non-IMI-treated strawberries with leading ‘strawberry-like’ and ‘fruity’ aromas. At the same time, the other four compounds were higher in IMI-treated strawberries with central ‘green’ and ‘fresh’ aromas. The results of the sensory evaluations of strawberries from the two control groups and the one IMI-treated group are shown in Figure 6. Different tendencies were observed in the results of the control and IMI-treated groups. The ‘strawberry-like aroma’ intensity was higher for strawberries from the control group, while the ‘fresh aroma’ intensity was lower. In terms of overall preference, all 26 assessors preferred non-IMI-treated strawberries. Combining the sensory evaluation results (Figure 6) and the available flavor threshold and description results, as well as the relative contents (Table 2), it is suggested that IMI could have a negative influence on ‘strawberry-like’ aromas and a positive influence on ‘fresh’ aromas, a phenomenon which reduces the popularity of strawberries among consumers. These results could provide basic data for management regulations regarding the use of imidacloprid on strawberries in the future.

4. Conclusions

The present study investigated the distribution of, and differences in, the VOCs in strawberries from different agricultural practices, i.e., organic (without imidacloprid) and conventional (with imidacloprid). A total of 1164 VOCs, representing 23 chemical classes, were detected (354 of these for the first time) by GC×GC-TOFMS, which is the highest number of VOCs that have ever been detected in strawberries. Volatile compositions varied significantly (p < 0.05) between the two treatment groups in this study. In comparison with the non-IMI-treated group, the strawberries with the 374.8 g/hm2 IMI treatment had higher responses for five characteristic aroma compounds, including aldehydes (31.59%), acids (17.25%), esters (25.01%), ketones (5.32%), and furanones (0.11%), which have important flavor attributes for strawberries and strongly influence consumer acceptability. The results of the sensory evaluations, flavor thresholds, and odor descriptions, along with the relative content of 25 key contributors (VIP value > 1), have suggested that IMI may have a negative influence on ‘strawberry-like’ aromas and a positive influence on ‘fresh’ aromas. It is essential to point out that the vital volatile compounds evaluated in this study represent only a tiny proportion of the total key volatile compounds present in strawberry samples. The results on the volatile constituents in the present study indicated that different agricultural practices might contribute to flavor differences in strawberries. The VOC profile can be considered an indicator for distinguishing strawberries. However, the mechanisms through which pesticides (such as imidacloprid) affect the flavors of strawberries remain unclear. Thus, future work is needed to explore the mechanisms of the interactions between pesticides and strawberry aroma components using proteomic, metabolomic, and transcriptomic approaches.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/foods12152914/s1, Figure S1: The calibration curve of external standard with GC×GC-TOF-MS by headspace SPME. Figure S2: Chromatograms and mass spectra of esters (Allyl Isothiocyanate and Ethyl butyrate), ketones (3-Nonen-2-one), aldehydes (Decanal), terpenes (α-Terpineol), and furanones (DMMF). Figure S3: PCA and PLS-DA analysis in IMI treated and non-IMI treated strawberries obtained with GC×GC-TOF-MS. Table S1: The absolute recovery of external standard with GC×GC-TOFMS in the strawberry sample homogenates by headspace SPME. Table S2: The VOCs profile of the strawberries.

Author Contributions

Formal analysis, N.Y.; Funding acquisition, F.J.; Investigation, N.Y., H.W., C.Z. and S.L.; Methodology, N.Y. and F.J.; Project administration, F.J.; Software, C.Z.; Supervision, H.W., J.W., F.J. and C.L. Validation, N.Y. and S.L.; Writing, N.Y., H.W. and F.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data used to support the findings of this study can be made available by the corresponding author upon request.

Acknowledgments

The authors gratefully acknowledge the Agricultural Science and Technology Innovation Program, and the Young Talents Program of the Chinese Academy of Agricultural Sciences.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Giampieri, F.; Tulipani, S.; Alvarez-Suarez, J.; Quiles, J.; Mezzetti, B.; Battino, M. The strawberry: Composition, nutritional quality, and impact on human health. Nutrition 2012, 28, 9–19. [Google Scholar] [CrossRef]
  2. FAO. Gross Production Value (Current Thousand US$)—Strawberries (1961–2020); Food and Agriculture Organization of the United Nations: Rome, Italy, 2012. Available online: https://www.fao.org/faostat/en/#data/QV/visualize (accessed on 20 July 2023).
  3. Melovic, B.; Ćirović, D.; Backović, T.; Dudic, B.a.Z.; Gubiniova, K. Attracting Green Consumers as a Basis for Creating Sustainable Marketing Strategy on the Organic Market—Relevance for Sustainable Agriculture Business Development. Foods 2020, 9, 1552. [Google Scholar] [CrossRef]
  4. Fotiric Aksic, M.; Tosti, T.; Sredojević, M.; Milivojević, J.; Meland, M.; Natić, M. Comparison of Sugar Profile between Leaves and Fruits of Blueberry and Strawberry Cultivars Grown in Organic and Integrated Production System. Plants 2019, 4, 205. [Google Scholar] [CrossRef] [Green Version]
  5. Bursać Kovačević, D.; Putnik, P.; Dragović-Uzelac, V.; Vahčić, N.; Babojelić, M.S.; Levaj, B. Influences of organically and conventionally grown strawberry cultivars on anthocyanins content and color in purees and low-sugar jams. Food Chem. 2015, 181, 94–100. [Google Scholar] [CrossRef]
  6. Olsson, M.E.; Andersson, C.S.; Oredsson, S.; Berglund, R.H.; Gustavsson, K.-E. Antioxidant Levels and Inhibition of Cancer Cell Proliferation in Vitro by Extracts from Organically and Conventionally Cultivated Strawberries. J. Agric. Food Chem. 2006, 54, 1248–1255. [Google Scholar] [CrossRef]
  7. Fan, Z.; Hasing, T.; Johnson, T.S.; Garner, D.M.; Schwieterman, M.L.; Barbey, C.R.; Colquhoun, T.A.; Sims, C.A.; Resende, M.F.R.; Whitaker, V.M. Strawberry sweetness and consumer preference are enhanced by specific volatile compounds. Hortic. Res. 2021, 8, 66. [Google Scholar] [CrossRef]
  8. Ronningen, I.; Miller, M.; Xia, Y.; Peterson, D.G. Identification and Validation of Sensory-Active Compounds from Data-Driven Research: A Flavoromics Approach. J. Agric. Food Chem. 2018, 66, 2473–2479. [Google Scholar] [CrossRef]
  9. Ulrich, D.; Kecke, S.; Olbricht, K. What Do We Know about the Chemistry of Strawberry Aroma? J. Agric. Food Chem. 2018, 66, 3291–3301. [Google Scholar] [CrossRef]
  10. Cannon, R.; Agyemang, D.; Curto, N.; Yusuf, A.; Chen, M.; Janczuk, A. In-depth analysis of Ciflorette strawberries (Fragaria × ananassa ‘Ciflorette’) by multidimensional gas chromatography and gas chromatography-olfactometry: In-depth analysis of Ciflorette strawberries. Flavour Fragr. J. 2015, 30, 302–319. [Google Scholar] [CrossRef]
  11. Zhang, L.; Zeng, Z.; Zhao, C.; Kong, H.; Lu, X.; Xu, G. A comparative study of volatile components in green, oolong and black teas by using comprehensive two-dimensional gas chromatography–time-of-flight mass spectrometry and multivariate data analysis. J. Chromatogr. A 2013, 1313, 245–252. [Google Scholar] [CrossRef]
  12. Ao, X.; Mu, Y.; Li, L.; Liu, D.; Lv, Z. Roasting intervention for the volatile composition of three varieties of nuts originating from Torreya yunnanensis. J. Food Biochem. 2022, 46, e14044. [Google Scholar] [CrossRef]
  13. Reis, L.; Forney, C.; Jordan, M.; Pennell, K.; Fillmore, S.A.E.; Orane Schemberger, M.; Ayub, R. Metabolic Profile of Strawberry Fruit Ripened on the Plant Following Treatment With an Ethylene Elicitor or Inhibitor. Front. Plant Sci. 2020, 11, 995. [Google Scholar] [CrossRef]
  14. Yue, N. Residue of Imidacloprid in Strawberries and its Effect on Quality. Master’s Thesis, Chinese Academy of Agricultural Sciences, Beijing, China, 2021. [Google Scholar] [CrossRef]
  15. JMPR. Pesticide Residues in Food 2008 (Evaluations—PART 1). 2009. Available online: https://www.fao.org/fileadmin/templates/agphome/documents/Pests_Pesticides/JMPR/Evaluation08/Imidacloprid.pdf (accessed on 20 July 2023).
  16. Shahid, M.; Khan, M.S.; Ahmed, B.; Syed, A.; Bahkali, A.H. Physiological disruption, structural deformation and low grain yield induced by neonicotinoid insecticides in chickpea: A long term phytotoxicity investigation. Chemosphere 2021, 262, 128388. [Google Scholar] [CrossRef]
  17. Liu, N.; Li, J.; Lv, J.; Yu, J.; Xie, J.; Wu, Y.; Tang, Z. Melatonin alleviates imidacloprid phytotoxicity to cucumber (Cucumis sativus L.) through modulating redox homeostasis in plants and promoting its metabolism by enhancing glutathione dependent detoxification. Ecotoxicol. Environ. Saf. 2021, 217, 112248. [Google Scholar] [CrossRef]
  18. Touzout, N.; Mehallah, H.; Moralent, R.; Moulay, M.; Nemmiche, S. Phytotoxic evaluation of neonicotinoid imidacloprid and cadmium alone and in combination on tomato (Solanum lycopersicum L.). Ecotoxicology 2021, 30, 1126–1137. [Google Scholar] [CrossRef]
  19. Arbid, Y.; Sleiman, M.; Richard, C. Photochemical interactions between pesticides and plant volatiles. Sci. Total Environ. 2022, 807, 150716. [Google Scholar] [CrossRef] [PubMed]
  20. Institute for the Control of Agrochemicals, Ministry of Agriculture and Rural Affairs. Registered Data-Imidacloprid 10% China Pesticide Information Network. 2023. Available online: http://www.chinapesticide.org.cn/zgnyxxw/eng/dataCenter?hash=reg-info (accessed on 20 July 2023).
  21. Drake, M.A. Sensory Evaluation. In Encyclopedia of Dairy Sciences, 3rd ed.; McSweeney, P.L.H., McNamara, J.P., Eds.; Academic Press: Oxford, UK, 2022; pp. 572–576. [Google Scholar]
  22. Ikegaya, A.; Ohba, S.; Toyoizumi, T.; Arai, E. Quality Evaluation of Strawberries Grown in Various Regions by Singaporeans and Japanese. Int. J. Fruit Sci. 2021, 21, 883–895. [Google Scholar] [CrossRef]
  23. Yan, J.-w.; Ban, Z.-j.; Lu, H.-y.; Li, D.; Poverenov, E.; Luo, Z.-s.; Li, L. The aroma volatile repertoire in strawberry fruit: A review. J. Sci. Food Agric. 2018, 98, 4395–4402. [Google Scholar] [CrossRef] [PubMed]
  24. Zhao, J.; Liu, J.; Wang, F.; Wang, S.; Feng, H.; Xie, X.; Hao, F.; Zhang, L.; Fang, C. Volatile constituents and ellagic acid formation in strawberry fruits of selected cultivars. Food Res. Int. 2020, 138, 109767. [Google Scholar] [CrossRef]
  25. Parra-Palma, C.; Úbeda, C.; Gil, M.; Ramos, P.; Castro, R.I.; Morales-Quintana, L. Comparative study of the volatile organic compounds of four strawberry cultivars and it relation to alcohol acyltransferase enzymatic activity. Sci. Hortic. 2019, 251, 65–72. [Google Scholar] [CrossRef]
  26. Liu, L.; Xiao, W.; Ji, M.-l.; Yang, C.; Li, L.; Gao, D.-s.; Fu, X.-l. Effects of molybdenum on nutrition, quality, and flavour compounds of strawberry (Fragaria × ananassa Duch. cv. Akihime) fruit. J. Integr. Agric. 2017, 16, 1502–1512. [Google Scholar] [CrossRef]
  27. Scott, G.; Williams, C.; Wallace, R.W.; Du, X. Exploring Plant Performance, Fruit Physicochemical Characteristics, Volatile Profiles, and Sensory Properties of Day-Neutral and Short-Day Strawberry Cultivars Grown in Texas. J. Agric. Food Chem. 2021, 69, 13299–13314. [Google Scholar] [CrossRef] [PubMed]
  28. Myung, K.; Hamilton-Kemp, T.R.; Archbold, D.D. Biosynthesis of trans-2-Hexenal in Response to Wounding in Strawberry Fruit. J. Agric. Food Chem. 2006, 54, 1442–1448. [Google Scholar] [CrossRef]
  29. Hamilton-Kemp, T.R.; Archbold, D.D.; Collins, R.W.; Yu, K. Emission patterns of wound volatile compounds following injury of ripe strawberry fruit. J. Sci. Food Agric. 2003, 83, 283–288. [Google Scholar] [CrossRef]
  30. Sharma, A.; Yuan, H.; Kumar, V.; Ramakrishnan, M.; Kohli, S.K.; Kaur, R.; Thukral, A.K.; Bhardwaj, R.; Zheng, B. Castasterone attenuates insecticide induced phytotoxicity in mustard. Ecotoxicol. Environ. Saf. 2019, 179, 50–61. [Google Scholar] [CrossRef]
  31. Zhou, Q.; Cheng, X.; Wang, S.; Liu, S.; Chaoling, W. Effects of Chemical Insecticide Imidacloprid on the Release of C6 Green Leaf Volatiles in Tea Plants (Camellia sinensis). Sci. Rep. 2019, 9, 625. [Google Scholar] [CrossRef] [Green Version]
  32. Jan, S.; Singh, B.; Bhardwaj, R.; Kapoor, D.; Kour, J.; Singh, R.; Alam, P.; Noureldeen, A.; Darwish, H. Application of melatonin and PGPR alleviates thiamethoxam induced toxicity by regulating the TCA cycle in Brassica juncea L. Saudi J. Biol. Sci. 2022, 29, 1348–1354. [Google Scholar] [CrossRef] [PubMed]
  33. Forney, C.; Kalt, W.; Jordan, M. The Composition of Strawberry Aroma Is Influenced by Cultivar, Maturity, and Storage. HortScience 2000, 35, 1022–1025. [Google Scholar] [CrossRef] [Green Version]
  34. Liu, L.; Ji, M.-L.; Chen, M.; Sun, M.-y.; Fu, X.-l.; Li, L.; Gao, D.-S.; Zhu, C.-Y. The flavor and nutritional characteristic of four strawberry varieties cultured in soilless system. Food Sci. Nutr. 2016, 4, 858–868. [Google Scholar] [CrossRef] [Green Version]
  35. Yang, X.; Yan, R.; Chen, Q.; Fu, M. Analysis of flavor and taste attributes differences treated by chemical preservatives: A case study in strawberry fruits treated by 1-methylcyclopropene and chlorine dioxide. J. Food Sci. Technol 2020, 57, 4371–4382. [Google Scholar] [CrossRef]
  36. Maoz, I.; Rikanati, R.D.; Schlesinger, D.; Bar, E.; Gonda, I.; Levin, E.; Kaplunov, T.; Sela, N.; Lichter, A.; Lewinsohn, E. Concealed ester formation and amino acid metabolism to volatile compounds in table grape (Vitis vinifera L.) berries. Plant Science 2018, 274, 223–230. [Google Scholar] [CrossRef]
  37. Misran, A.; Padmanabhan, P.; Sullivan, J.; Khanizadeh, S.; Gopinadhan, G. Composition of phenolics and volatiles in strawberry cultivars and influence of preharvest hexanal treatment on their profiles. Can. J. Plant Sci. 2014, 95, 115–126. [Google Scholar] [CrossRef] [Green Version]
  38. Sokołowska, B.; Połaska, M.; Dekowska, A.; Woźniak, Ł.; Roszko, M. Degradation of Preservatives with the Formation of Off-Odor Volatile Compounds—The Case of Strawberry-Flavored Bottled Water. Beverages 2020, 6, 67. [Google Scholar] [CrossRef]
  39. Peinado, I.; Rosa, E.; Heredia, A.; Escriche, I.; Andrés, A. Influence of processing on the volatile profile of strawberry spreads made with isomaltulose. Food Chem. 2013, 138, 621–629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Kim, Y.-H.; Kim, K.-H.; Szulejko, J.; Parker, D. Quantitative Analysis of Fragrance and Odorants Released from Fresh and Decaying Strawberries. Sensors 2013, 13, 7939–7978. [Google Scholar] [CrossRef] [Green Version]
  41. Li, X.-X.; Fukuhara, K.; Hayata, Y. Concentrations of Character Impact Odorants in ‘Toyonoka’ Strawberries Quantified by Standard Addition Method and PQ Column Extraction with GC-MS Analysis. J. Jpn. Soc. Hortic. Sci. 2009, 78, 200–205. [Google Scholar] [CrossRef] [Green Version]
  42. USDA. Harmful and Potentially Harmful Constituents in Tobacco Products and Tobacco Smoke: Established List. U.S. Food and Drug Administration. 2019. Available online: https://www.fda.gov/tobacco-products/rules-regulations-and-guidance/harmful-and-potentially-harmful-constituents-tobacco-products-and-tobacco-smoke-established-list (accessed on 20 July 2023).
  43. Sleiman, M.; Logue, J.M.; Montesinos, V.N.; Russell, M.L.; Litter, M.I.; Gundel, L.A.; Destaillats, H. Emissions from Electronic Cigarettes: Key Parameters Affecting the Release of Harmful Chemicals. Environ. Sci. Technol. 2016, 50, 9644–9651. [Google Scholar] [CrossRef] [Green Version]
  44. Rietjens, I.M.C.M.; Michael, A.; Bolt, H.M.; Siméon, B.; Andrea, H.; Nils, H.; Christine, K.; Angela, M.; Gloria, P.; Daniel, R.; et al. The role of endogenous versus exogenous sources in the exposome of putative genotoxins and consequences for risk assessment. Arch. Toxicol. 2022, 96, 1297–1352. [Google Scholar] [CrossRef]
  45. Negri, A.; Allegra, D.; Simoni, L.; Rusconi, F.; Tonelli, C.; Espen, L.; Galbiati, M. Comparative analysis of fruit aroma patterns in the domesticated wild strawberries “Profumata di Tortona” (F. moschata) and “Regina delle Valli” (F. vesca). Front. Plant Sci. 2015, 6, 56. [Google Scholar] [CrossRef] [Green Version]
  46. Jelen, H.; Krawczyk, J.; Larsen, T.O.; Jarosz, A.; Gołebniak, B. Main compounds responsible for off-odour of strawberries infected by Phytophthora cactorum. Lett. Appl. Microbiol. 2005, 40, 255–259. [Google Scholar] [CrossRef]
  47. Pérez, A.G.; Olías, R.; Sanz, C.; Olías, J.M. Furanones in Strawberries:  Evolution during Ripening and Postharvest Shelf Life. J. Agric. Food Chem. 1996, 44, 3620–3624. [Google Scholar] [CrossRef]
  48. Smouse, T.H.; Chang, S.S. A systematic characterization of the reversion flavor of soybean oil. J. Am. Oil Chem. Soc. 1967, 44, 509–514. [Google Scholar] [CrossRef] [PubMed]
  49. Lu, H.; Ban, Z.; Wang, K.; Li, D.; Li, D.; Poverenov, E.; Li, L.; Luo, Z. Aroma volatiles, sensory and chemical attributes of strawberry (Fragaria × ananassa Duch.) achenes and receptacle. Int. J. Food Sci. Technol. 2017, 52, 2614–2622. [Google Scholar] [CrossRef]
Foods 12 02914 g001 550
Figure 1. Fingerprints of volatile compounds in non-IMI-treated and IMI-treated strawberries obtained with GC×GC-TOF-MS. (A) non-IMI-treated; (B) IMI-treated.
Figure 1. Fingerprints of volatile compounds in non-IMI-treated and IMI-treated strawberries obtained with GC×GC-TOF-MS. (A) non-IMI-treated; (B) IMI-treated.
Foods 12 02914 g001
Foods 12 02914 g002 550
Figure 2. The numbers of compounds in IMI-treated and non-IMI-treated strawberries, obtained by GC×GC-TOFMS.
Figure 2. The numbers of compounds in IMI-treated and non-IMI-treated strawberries, obtained by GC×GC-TOFMS.
Foods 12 02914 g002
Foods 12 02914 g003 550
Figure 3. Comparison of the composition of compounds in 23 catalogs with those in IMI-treated and non-IMI-treated strawberries, obtained by GC×GC-TOF-MS. (A) Compounds in different treatments; (B) compounds in 23 catalogs.
Figure 3. Comparison of the composition of compounds in 23 catalogs with those in IMI-treated and non-IMI-treated strawberries, obtained by GC×GC-TOF-MS. (A) Compounds in different treatments; (B) compounds in 23 catalogs.
Foods 12 02914 g003
Foods 12 02914 g004 550
Figure 4. Comparison of the peak areas of compounds in 23 catalogs, for IMI-treated and non-IMI-treated strawberries, obtained by GC×GC-TOFMS. (A) peak areas > 0.5 × 105; (B) peak areas < 0.5 × 105. * represents a significant difference.
Figure 4. Comparison of the peak areas of compounds in 23 catalogs, for IMI-treated and non-IMI-treated strawberries, obtained by GC×GC-TOFMS. (A) peak areas > 0.5 × 105; (B) peak areas < 0.5 × 105. * represents a significant difference.
Foods 12 02914 g004
Foods 12 02914 g005 550
Figure 5. Relative contents of the volatile organic compounds in strawberries from non-IMI treatment and IMI treatment groups. (A) Aldehydes; (B) esters; (C) alcohols; (D) ketones; (E) terpenes; (F) furans.
Figure 5. Relative contents of the volatile organic compounds in strawberries from non-IMI treatment and IMI treatment groups. (A) Aldehydes; (B) esters; (C) alcohols; (D) ketones; (E) terpenes; (F) furans.
Foods 12 02914 g005
Foods 12 02914 g006 550
Figure 6. Results of the sensory evaluations of mature strawberries.
Figure 6. Results of the sensory evaluations of mature strawberries.
Foods 12 02914 g006
Table
Table 1. The calibration curve and method sensitivity of external standard with GC×GC-TOFMS by headspace SPME.
Table 1. The calibration curve and method sensitivity of external standard with GC×GC-TOFMS by headspace SPME.
CompoundsStandard CurveCorrelation Coefficient (R2)LOD
(ng/g)		LOQ
(ng/g)		Average Absolute Recovery (%)
0.5 (µg/g)0.2 (µg/g)0.1 (µg/g)RSD (%)
2-Heptanoney = 261.48x + 19,9660.97410.0240.0891.8997.12132.484.43–9.09
Benzaldehydey = 492.68x + 35,8380.97770.0430.1464.7684.08101.734.74–16.87
1-Heptanoly = 325.99x + 125.20.99160.160.5570.5485.03103.454.97–8.99
1-Deceney = 469.76x + 56,5240.97720.0440.1572.71108.57130.475.00–14.38
Ethyl Hexanoatey = 906.61x + 111,2170.92970.0690.2379.49126.9885.040.48–2.88
DMMFy = 521.59x + 4945.20.99230.0360.1382.73110.2789.823.52–12.25
Eugenoly = 610.89x − 6562.20.98870.130.4269.0974.1783.7511.57–21.17
1-Teradecanoly = 340.58x − 11,4550.96850.0530.1869.6479.3696.035.83–10.49
Table
Table 2. GC×GC-TOFMS peak areas (% on the total area) of difference contributors (VIP value > 1) in non-IMI and IMI treated strawberry samples.
Table 2. GC×GC-TOFMS peak areas (% on the total area) of difference contributors (VIP value > 1) in non-IMI and IMI treated strawberry samples.
CategoryCompoundsCAS NumberVIP ValueRelative ContentAroma DescriptionOdor Threshold
(mg/kg)		Medium
Non-IMIIMI
EstersPropanoic acid, 2-methyl-, 3-hydroxy-2,2,4-trimethylpentyl ester77-68-91.080.015 ± 0.0010.016 ± 0.001 0.58 dair
Methyl 3-hydroxyoctanoate7367-87-51.150.011 ± 0.0030.055 ± 0.006
3-Methylheptyl acetate72218-58-72.020.011 ± 0.0020.012 ± 0.006
Methyl 3-hydroxytetradecanoate55682-83-21.000.011 ± 0.0020.030 ± 0.007
Pentyl hexanoate540-07-82.160.009 ± 0.0010.039 ± 0.004floral, fresh, rose
Octyl 2-methylbutyrate29811-50-51.000.017 ± 0.0030.011 ± 0.002
Butanoic acid, hexyl ester2639-63-61.580.547 ± 0.0460.615 ± 0.022pineapple0.203 dwater
S-Methyl 3-methylbutanethioate23747-45-71.020.053 ± 0.0060.037 ± 0.011
Methyl 3-hydroxyhexanoate21188-58-91.020.029 ± 0.0040.067 ± 0.006 0.05oil
4-Octenoic acid, methyl ester1732-00-91.280.053 ± 0.014/
Acetic acid, phenylmethyl ester140-11-42.150.140 ± 0.0140.442 ± 0.046floral
Methyl salicylate119-36-82.240.087 ± 0.0170.388 ± 0.026holly leaf, fresh0.04water
2-Buten-1-ol, 3-methyl-, acetate1191-16-81.410.013 ± 0.0040.032 ± 0.015
Acetic acid, octyl ester112-14-11.430.124 ± 0.0380.224 ± 0.047 0.047 dwater
Acetic acid, heptyl ester112-06-11.470.017 ± 0.0040.050 ± 0.007 0.42 dwater
Methyl hexanoate106-70-70.884.694 ± 1.9342.389 ± 0.492fruity, pineapple0.07water
Hexanoic acid, 2-methylpropyl ester105-79-31.070.008 ± 0.0020.002 ± 0.001
Ethylene glycol di-n-butyrate105-72-61.110.062 ± 0.0210.030 ± 0.005
Acetic acid, 2-phenylethyl ester103-45-71.410.013 ± 0.0020.034 ± 0.004 0.24959 dwater
Butanoic acid, decyl ester12983171.060.002 ± 0.0010.042 ± 0.004
KetonesMethyl nicotinate93-60-72.050.122 ± 0.0230.331 ± 0.100
2-Nonanone821-55-61.270.078 ± 0.0160.231 ± 0.017floral, oils and herbs0.04 dwater
Nona-3,5-dien-2-one80387-31-11.360.070 ± 0.0150.225 ± 0.058green grassy
1-Octen-3-one4312-99-61.200.027 ± 0.0040.073 ± 0.010soap, gasoline0.000003 dwater
2-Undecanone112-12-91.300.005 ± 0.0020.030 ± 0.002green, citrus, fresh0.0055 dwater
γ-Dodecalactone2305-05-71.200.024 ± 0.0050.310 ± 0.043peach, milk peach0.00043 dwater
TerpenesD-Limonene5989-27-52.510.399 ± 0.169/citrus, mint0.034 dwater
β-Cyclocitral432-25-71.170.049 ± 0.0110.065 ± 0.004tobacco, floral0.003water
β-Myrcene123-35-32.530.005 ± 0.0020.017 ± 0.006sweet orange, balsam0.0012 dwater
nerol106-25-21.220.007 ± 0.0010.012 ± 0.001lemon0.68 dwater
AcidsAcetohydroxamic acid546-88-31.290.015 ± 0.007/
Aldehydes(Z)-4-Heptenal6728-31-01.050.004 ± 0.0010.003 ± 0.002
(E)-2-Hexenal6728-26-31.082.963 ± 2.6871.732 ± 1.576fruity, fresh, green0.0885 dwater
(E,Z)-2,6-Nonadienal557-48-21.110.471 ± 0.0990.389 ± 0.026cucumber0.0008 dwater
Benzaldehyde, 4-ethyl-4748-78-11.000.006 ± 0.0030.007 ± 0.004bitter almond0.013 dair
(Z)-2-Decenal2497-25-81.350.081 ± 0.0070.102 ± 0.023tallow, waxy, fatty
Benzeneacetaldehyde122-78-11.080.122 ± 0.0200.183 ± 0.022hyacinth, almond and cherry0.004 dwater
Decanal112-31-21.380.530 ± 0.1130.481 ± 0.044thrill0.003water
4-Oxononanal74327-29-01.220.006 ± 0.001/
Cycloalkanes1,7-Dimethyl-4-(1-methylethyl)cyclodecane645-10-31.980.009 ± 0.004/
Furanone5-(acetyloxy)dihydro-5-methyl-2(3H)-furanone57681-51-31.050.002 ± 0.001/
2,5-Dimethyl-4-methoxy-3(2H)-furanone (DMMF)4077-47-81.512.157 ± 0.2910.022 ± 0.007strawberry-like,
floral, fruity,		0.00003 dwater
Alcohols2-Hexen-1-ol56922-75-91.042.468 ± 0.7204.343 ± 1.994
1-Nonanol143-08-81.460.344 ± 0.0710.365 ± 0.019sweet orange, sweet and green rose0.001
1-Decanol112-30-11.540.009 ± 0.0010.082 ± 0.005fatty0.0066 dwater
1-Heptanol111-70-61.020.040 ± 0.0070.077 ± 0.007fat, pungent, citrus0.0054 dwater
3-Nonen-1-ol, (Z)-10340-23-51.630.007 ± 0.0010.012 ± 0.003
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Yue, N.; Wang, H.; Li, C.; Zhang, C.; Li, S.; Wang, J.; Jin, F. The Effect of Imidacloprid on the Volatile Organic Compound Profile of Strawberries: New Insights from Flavoromics. Foods 2023, 12, 2914. https://doi.org/10.3390/foods12152914

AMA Style

Yue N, Wang H, Li C, Zhang C, Li S, Wang J, Jin F. The Effect of Imidacloprid on the Volatile Organic Compound Profile of Strawberries: New Insights from Flavoromics. Foods. 2023; 12(15):2914. https://doi.org/10.3390/foods12152914

Chicago/Turabian Style

Yue, Ning, Hongping Wang, Chunmei Li, Chen Zhang, Simeng Li, Jing Wang, and Fen Jin. 2023. "The Effect of Imidacloprid on the Volatile Organic Compound Profile of Strawberries: New Insights from Flavoromics" Foods 12, no. 15: 2914. https://doi.org/10.3390/foods12152914

APA Style

Yue, N., Wang, H., Li, C., Zhang, C., Li, S., Wang, J., & Jin, F. (2023). The Effect of Imidacloprid on the Volatile Organic Compound Profile of Strawberries: New Insights from Flavoromics. Foods, 12(15), 2914. https://doi.org/10.3390/foods12152914

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop