Profiling of carbonyl compounds in fresh cabbage with chemometric analysis for the development of freshness assessment method
-
Daimon Syukri
,
Rini
Abstract
The aim of this study was to screen the distribution of carbonyl compounds (CCs) in fresh cabbage as a sample model of multi-layered leafy vegetables for discovering the universal freshness marker of fresh produces. The distribution of CCs was observed in the three outer leaf layers of the cabbage. The profile of CCs in each leaf will guide the selection of which leaf is the appropriate part to be used to further discover a freshness marker of cabbage during storage treatment at the postharvest stage. The carbonyl compounds in each leaf were extracted using a mixture of chloroform and methanol (2:1). The extracted CCs from samples were derivatized with dansyl hydrazine. A high-performance liquid chromatography-mass spectrometer with multiplexed multiple reactions monitoring (MRM) was used for the comprehensive detection of carbonyl compounds. More than 400 peaks were observed in the MRM chromatogram from all leaves. The distribution of m/z values that represent CCs were analyzed employing the principle component analysis-discriminant analysis by relating it to the leaf position. The distribution of CC was different for each leaf where the leaves of the second and third layers were similar and significantly different from the leaves of the first layer. The accumulation of trans-2-hexenal was dominant in the first layer; therefore, the utilization of the first layer is not suitable as the part of the sample to discover the freshness marker of multi-layered leafy vegetables.
1 Introduction
Fruits and vegetables have a central role and become an important food of the human diet nowadays [1]. The consumption of fruits and vegetables in which their freshness and safety are guaranteed could increase their economic value both in domestic and overseas markets. The availability of fresh produces for the trade can be inconsistent because it has typically spent a period in retail distribution. The development of a valid freshness assessment of fresh produces must be considered by distributors and retailers instead of the consumers.
The freshness of fresh fruits and vegetable assessment generally can be exposed to a direct measurement of various conditions which offers the potential for the change in quality characteristics such as product appearances by visual inspection. During the distribution chain of fresh produces from grower–retailers–consumers, visual freshness indicators such as visible deterioration and/or de-greening are lagging indicators and ambiguous since the subjective assessment must be appropriately conveyed to the relevant personnel. Moreover, visual inspection is not visible until senescence is advanced and less suitable for freshness assessment [2]. Early detection of senescence’s symptoms can be suggested as one strong aspect of freshness assessment.
Senescence is one characteristic that indicates the deterioration of fresh produces during distribution [3]. Senescence in fresh produces is a complex and highly regulated process. According to Zhou and Gan [4], the occurrence of the senescence process in plants can be characterized by some symptoms such as chlorophyll degradation, cellular membrane and protein degradation, and moisture loss or desiccation. However, generally, senescence can often be indicated by the degradation of the cellular membrane [5] (Dornenburg and Davies, 1999). Membrane deterioration was led by a lipid degradation process that is indicated by the decrease of phospholipids [6] and unsaturated fatty acids [3], as well as the increase of peroxidized lipids [7]. A great variety of peroxidized lipids is formed during the lipid degradation of fruits and vegetables. Among them are carbonyl compounds (CCs) including carboxylic, aldehyde, and ketone compounds [8]. Therefore, the discovery of a specific accumulation of carbonyl compounds in the storage condition of fruits and vegetables could be proposed as a freshness marker.
Discoveries of universal freshness markers for all commodities would be useful as a strong indicator to indicate the freshness level of fresh produces practically. Syukri et al. [9] have reported the effort on the identification of abscisic acid as a freshness marker of soybean sprouts. However, the fresh produces are varied; therefore, the effort to screen and identify the freshness marker on other fresh produces needs to be considered. Another kind of fresh produces is a multi-layered leafy vegetable. Screening and identifying CCs in multi-layered leafy vegetables may be quite difficult because the sample material has several outer leaves that coincide. Therefore, a preliminary study to determine which leaves are appropriate to be used as sample material for CCs analysis needs to be conducted. In this study, cabbage was chosen as a representative multi-layered vegetable because of its abundant availability. Moreover, cabbage is a leafy green multi-layered leafy vegetable that is highly perishable and very susceptible to decay factors [10,11]. This study describes the identification and behavior of CCs in cabbage. Thus, it can add information on whether the pattern of formation of CCs will be the same as that of other vegetables of different types. The findings in this study will enrich the database of freshness markers candidates for universal fresh produce application.
2 Materials and methods
2.1 Plant materials
This study was conducted from April 2021 to September 2022. Fresh cabbages were obtained from the local farmer for subsequent analysis in this study.
2.2 Reagents
Dansyl hydrazine (DH) and p-toluenesulfonnic acids (p-TsOH) were purchased from Sigma-Aldrich (st. Louis, MO, USA). p-Benzyloxybenzaldehyde (p-BOBA), acetonitrile, methanol, chloroform, trans-2-hexenal and formic acid were obtained from Wako Pure Chemical Industries (Osaka, Japan). Butylated hydroxy toluene (BHT) was purchased from Nacalai Tesque (Kyoto, Japan).
2.3 Sample preparation
Instantaneously after being harvested, the freshly cultivated cabbages at Gifu Perfecture, Japan (±5 kg) were taken to the lab, where they were carefully washed and dried. The cabbage was gently detached from the shattered layers. The three outer layers were separated, each measured to a maximum of 100 mg. The layers were then immediately placed into 2 mL self-standing screw cap microtubes (Watson, Kobe, Japan) with one piece of 2 mm zirconia ball, and they were submerged in liquid nitrogen for 2 min before being stored at −80°C for further analysis.
Using the Shake Master Neo (BMS, Tokyo, Japan), 20 µL of methanol containing 0.05% BHT was added to the frozen sample and crushed for 180 seconds. Then, 400 µL of chloroform and 100 µL of p-BOBA (as an internal standard) were added to the slurry. Shake Master Neo was used to homogenize the mixture for 120 seconds. The mixture was then centrifuged for 10 minutes at 12,000 rpm at 10°C. (Kubota 1720, Osaka, Japan). Finally, the organic phases were given to DH for derivatization.
2.4 DH derivatization
DH derivatization process was adapted from Tomono et al. [12] with some modifications. A portion of the organic phase (200 µL) was mixed with 400 µL acetonitrile containing 200 µg of DH and 40 µg of p-TsOH, and the resulting mixtures were mixed using a water bath shaker (personal 11, Taitec, Saitama, Japan) under 30°C, 75 rpm, and in the absence of light for 4 h. The mixtures were then evaporated to dryness in a centrifugal evaporator in a vacuum (Eyela CV-2100, Tokyo, Japan). The corresponding derivative residues were dissolved in 500 µL acetonitrile, and the solution was filtered through a 0.2 µm membrane (RC15 Minisart, Sartorius, Göttingen, Germany). About 5 µL of aliquot of this solution was analyzed using liquid chromatography electrospray ionization tandem mass spectrometric (LC/ESI-MS/MS).
2.5 LC/ESI-MS/MS analysis
Instrumentation employed for the LC/ESI-MS/MS determination of CCs consisted of a prominence HPLC 20 A series system including a high-pressure gradient pump, autosampler, and column oven (Shimadzu, Kyoto, Japan) using a Toyo Soda Kogyo gel Super-Octyl column (2.3 µm, 100 mm × 2.0 mm, TOSOH, Tokyo, Japan). The device is coupled to a triple-quadrupole mass spectrometer detector with an electrospray ionization device running in the positive ion mode (Q-TRAP 4500, AB Sciex, Framingham, MA, USA). The elution system was carried out in binary gradient mode. The mobile phases consisted of 0.1% formic acid in water as solvent A and 0.1% formic acid in acetonitrile as solvent B. The elution was performed using a linear gradient which was started at 20% solvent B and progressed to 90% solvent B over a period of 10 min. The system was then using isocratic elution at 90% of solvent B for 9 min. Further linear increase of B to 100% within 1 min was followed by a hold-time of 5 min at 100% B and 5 min column re-equilibration at 20% of solvent B. The flow rate was 0.2 mL/min. The detector conditions were as follows: ion-spray voltage +5,500 V, source temperature 300°C, curtain gas 206.8 kPa, collision gas 62.1 kPa, ion source gas 1 (sheath gas) 344.7 kPa, ion source gas 2 (drying gas) 551.6 kPa, declustering potentials at 100 V; and collision energies of 37 eV for m/z 275–374, 115 V and 39 eV for m/z 375–474, 120 V and 43 eV for m/z 475–574 and 130 V and 50 eV for m/z 575–674, respectively. Nitrogen was used as the collision gas. The derivatives of CCs with DH (CC-DHs) were detected using the multiplexing multiple reaction monitoring (MRM) of specific product ions with the an m/z value of 236.1 by CID. A total of 400 MRM transitions were monitored for each CC-DHs derivative samples, and a total of 100 channels were monitored simultaneously for each sample injection. One channel from each injection was reserved for monitoring the transition of p-BOBA-DH as internal standard (IS) at m/z 460 → 236.1. Each sample was measured in three replications with five times of injections to complete the multiplexing of the 400 MRM transitions. Analysis was done in triplicates; each replication was injected into LCMS three times.
2.6 Data processing
Data processing of each peak of CC derivatives including the multivariate statistical analyses was conducted in Marker View™ software 1.2.1. (AB-Sciex, Framingham, MA, USA). CC peaks were extracted using Gaussian smoothing of 1.5 points, noise percentage of 50%, baseline sub. window of 8.0 min, peak splitting factor of 4 points, retention time tolerance of 1 min, minimum intensity of 1,500 cps, minimum peak with of 2 points, and minimal signal/noise of 20. All mass spectra were identified, quantified, and normalized with an internal standard and sample weight. The multivariate statistical analyses including principal component analysis with discriminant analysis (PCA-DA) were conducted to find any differential features between each of the sample groups. The suspicious candidates were identified using Lipidmaps (www.lipidmaps.org), human metabolome databases (www.hmdb.ca), the METLIN database (metlin.scripps.edu), and chemicalbook (www.chemicalbook.com).
3 Results and discussion
The occurrence of CCs of cabbage according to leaves position was investigated by using metabolomics approach. CCs, as a product of lipid peroxidation, are related to the environmental stress on fresh produces and might accumulate in a trace level. The utilization of mass spectrometric analysis is a powerful tool to identify the occurrence of trace metabolites in biological samples [12,13]. Although the used sample was fresh material, there were more than 400 peaks detected in all leaves of cabbage. Figure 1 indicates the corresponding CC maps, where all of the CC-DHs detected in the extraction sample were plotted as circles as a function of their retention times (horizontal axis) and m/z values (vertical axis). The area of the circles represents the intensities of peaks for the detected CCs relatives to that of IS and its corresponding sample weight. Figure 1 shows the comparison of the m/z values of CC-DHs in the range of 275–650 that were contained in all leaves of fresh cabbage. The large varieties of chemical compounds containing carbonyl groups in plants generate many CC-DHs compounds that were detected in samples. However, the CC-DHs profile of each leaf was quite different. It indicates that there has been a chemical change of CCs presented in each leaf. Although the occurrence of CC-DHs seemed predominant in layer 1, however, due to the large number of observed CC-DHs, the characterization of the CCs as the product of lipid peroxidation cannot be observed objectively. Therefore, the results were analyzed statistically by PCA-DA.
The CC distribution in cabbage leaves.
PCA is a statistical technique that eliminates variables from the collected data’s dimensions (principal components). Based on their spatial proximity, this research uncovers the links and similarities among group samples. PCA-DA enables the grouping of samples into recognized groups when employed as a supervised approach. This method of classifying samples produces the most significant separation between known classes of samples and makes them easier to differentiate from one another. As a result, Figure 2 shows the score plots for the profile of CC-DHs in each examined cabbage leaf. The distribution of CC-DHs in layers 2 and 3 was comparable to yet distinct from that in layer 1. Layer 1 produced greater reactions to environmental stress than either layer 2 or layer 3.
PCA scores plots of CC-DHs in three outer leaves of fresh cabbage.
To classify the CC-DHs that are present in layer 1 and responsible for lipid peroxidation due to the environmental stress of cabbage, the loading plot of CC-DHs is displayed. Figure 3 indicates that the loading plots can describe the CC-DHs behavior and difference among layers. Based on the information on the PCA score plot of layer 1, a highly potential marker ion of carbonyl compound derivatives (m/z, retention time pairs) was pointed. The CC-DH was the compound with m/z 346 with a retention time of 10.3 min.
Loading plots of CC-DHs in three outer leaves of fresh cabbage.
To identify the marker ion with m/z 346 at 10.3 min, the fragment elucidation was further conducted since the detected marker ion is a protonated molecule that consists of CC and DH compounds. Furthermore, to obtain intact molecular weight (MW) of potential CC that reacted with DH from the suspected marker ion, the detected m/z was subtracted by the m/z value of 1 and 263 from H+ adduct ion and DH moiety, respectively. The resulting value was subsequently added by 16, which corresponds to the MW of oxygen presented in the carbonyl skeleton, as described in Figure 4. It was found that 98 was MW for the potential marker ion corresponding to the stress condition of layer 1 of fresh cabbage. This value was subsequently searched against online databases to find possible structures where trans-2-hexenal was thought as the name of the marker ion. The mass fragmentation of detected metabolite was compared to the mass fragmentation of the reference standard of trans-2-hexenal which indicated a similar pattern of fragmentations.
The fragment elucidation of marker ion for obtaining the molecular weight of predominant CC in the first layer of fresh cabbage.
Trans-2-hexenal is a volatile compound classified as CC and is commonly emitted by wounded or stressed plants [14]. The occurrence of trans-2-hexenal has been hypothesized as a product of membrane lipid degradation. The accumulation of trans-2-hexenal in layer 1 of fresh cabbage indicates that, although the produces are considered fresh, lipid degradation occurs. In the determination of freshness marker of fresh produces, ideally, the markers are not present in the fresh state and accumulated during senescence. Therefore, this study has provided strong evidence that in multi-layered leafy vegetables, the utilization of the first layer is not appropriate to be utilized as sample material to screen and identify a potential freshness marker.
4 Conclusion
Determining the sample position for the identification of freshness markers of multi-layered leafy vegetables in metabolomics experiments is important. A freshness marker should not be present in the fresh state of fresh produces and accumulated rapidly or gradually during senescence in the postharvest stages. In cabbage, the utilization of the second or third layer is suggested as the appropriate part to be selected as the representative sampling position for the determination of a potential universal freshness marker of fresh produces.
Acknowledgments
The authors are grateful to the Faculty of Agricultural Technology, Andalas University, Indonesia, and UGSAS-Gifu University for the support for this study. The authors are also grateful to the students for preparing the sample used in this work.
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Funding information: This publication was financed by a grant from the The Research and Community Service Institute of Andalas University with No. T/UN.16.17/PT.01.03/Pangan-RPT/2023.
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Author contributions: D.S.: Wrote the manuscript and Conceptualization; R.: grammar check; A.B.J.: Statistical check; K.N.: Conceptualization.
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Conflict of interest: The authors state no conflict of interest.
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Data availability statement: All data generated or analyzed during this study are included in this published article.
References
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- Design and fabrication of a fish feed mixing cum pelleting machine for small-medium scale aquaculture industry
- Indicators of swamp buffalo business sustainability using partial least squares structural equation modelling
- Effect of arbuscular mycorrhizal fungi on early growth, root colonization, and chlorophyll content of North Maluku nutmeg cultivars
- How intergenerational farmers negotiate their identity in the era of Agriculture 4.0: A multiple-case study in Indonesia
- Responses of broiler chickens to incremental levels of water deprivation: Growth performance, carcass characteristics, and relative organ weights
- The improvement of horticultural villages sustainability in Central Java Province, Indonesia
- Effect of short-term grazing exclusion on herbage species composition, dry matter productivity, and chemical composition of subtropical grasslands
- Analysis of beef market integration between consumer and producer regions in Indonesia
- Analysing the sustainability of swamp buffalo (Bubalus bubalis carabauesis) farming as a protein source and germplasm
- Toxicity of Calophyllum soulattri, Piper aduncum, Sesamum indicum and their potential mixture for control Spodoptera frugiperda
- Consumption profile of organic fruits and vegetables by a Portuguese consumer’s sample
- Phenotypic characterisation of indigenous chicken in the central zone of Tanzania
- Diversity and structure of bacterial communities in saline and non-saline rice fields in Cilacap Regency, Indonesia
- Isolation and screening of lactic acid bacteria producing anti-Edwardsiella from the gastrointestinal tract of wild catfish (Clarias gariepinus) for probiotic candidates
- Effects of land use and slope position on selected soil physicochemical properties in Tekorsh Sub-Watershed, East Gojjam Zone, Ethiopia
- Design of smart farming communication and web interface using MQTT and Node.js
- Assessment of bread wheat (Triticum aestivum L.) seed quality accessed through different seed sources in northwest Ethiopia
- Estimation of water consumption and productivity for wheat using remote sensing and SEBAL model: A case study from central clay plain Ecosystem in Sudan
- Agronomic performance, seed chemical composition, and bioactive components of selected Indonesian soybean genotypes (Glycine max [L.] Merr.)
- The role of halal requirements, health-environmental factors, and domestic interest in food miles of apple fruit
- Subsidized fertilizer management in the rice production centers of South Sulawesi, Indonesia: Bridging the gap between policy and practice
- Factors affecting consumers’ loyalty and purchase decisions on honey products: An emerging market perspective
- Inclusive rice seed business: Performance and sustainability
- Design guidelines for sustainable utilization of agricultural appropriate technology: Enhancing human factors and user experience
- Effect of integrate water shortage and soil conditioners on water productivity, growth, and yield of Red Globe grapevines grown in sandy soil
- Synergic effect of Arbuscular mycorrhizal fungi and potassium fertilizer improves biomass-related characteristics of cocoa seedlings to enhance their drought resilience and field survival
- Control measure of sweet potato weevil (Cylas formicarius Fab.) (Coleoptera: Curculionidae) in endemic land of entisol type using mulch and entomopathogenic fungus Beauveria bassiana
- In vitro and in silico study for plant growth promotion potential of indigenous Ochrobactrum ciceri and Bacillus australimaris
- Effects of repeated replanting on yield, dry matter, starch, and protein content in different potato (Solanum tuberosum L.) genotypes
- Review Articles
- Nutritional and chemical composition of black velvet tamarind (Dialium guineense Willd) and its influence on animal production: A review
- Black pepper (Piper nigrum Lam) as a natural feed additive and source of beneficial nutrients and phytochemicals in chicken nutrition
- The long-crowing chickens in Indonesia: A review
- A transformative poultry feed system: The impact of insects as an alternative and transformative poultry-based diet in sub-Saharan Africa
- Short Communication
- Profiling of carbonyl compounds in fresh cabbage with chemometric analysis for the development of freshness assessment method
- Special Issue of The 4th International Conference on Food Science and Engineering (ICFSE) 2022 - Part I
- Non-destructive evaluation of soluble solid content in fruits with various skin thicknesses using visible–shortwave near-infrared spectroscopy
- Special Issue on FCEM - International Web Conference on Food Choice & Eating Motivation - Part I
- Traditional agri-food products and sustainability – A fruitful relationship for the development of rural areas in Portugal
- Consumers’ attitudes toward refrigerated ready-to-eat meat and dairy foods
- Breakfast habits and knowledge: Study involving participants from Brazil and Portugal
- Food determinants and motivation factors impact on consumer behavior in Lebanon
- Comparison of three wine routes’ realities in Central Portugal
- Special Issue on Agriculture, Climate Change, Information Technology, Food and Animal (ACIFAS 2020)
- Environmentally friendly bioameliorant to increase soil fertility and rice (Oryza sativa) production
- Enhancing the ability of rice to adapt and grow under saline stress using selected halotolerant rhizobacterial nitrogen fixer
