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. 2022 Feb 25;11(5):630. doi: 10.3390/plants11050630

Spatial Distribution of Polyphenolic Compounds in Corn Grains (Zea mays L. var. Pioneer) Studied by Laser Confocal Microscopy and High-Resolution Mass Spectrometry

Mayya Razgonova 1,2,*, Yulia Zinchenko 2, Konstantin Pikula 3,4, Lyudmila Tekutyeva 1, Oksana Son 1, Alexander Zakharenko 5,6, Tatiana Kalenik 1, Kirill Golokhvast 3,5,7
Editors: Raymond Wightman, Bertrand Dubreucq
PMCID: PMC8912282  PMID: 35270099

Abstract

Desirable changes in the biochemical composition of food plants is a key outcome of breeding strategies. The subsequent localization of nutritional phytochemicals in plant tissues gives important information regarding the extent of their synthesis across a tissue. We performed a detailed metabolomic analysis of phytochemical substances of grains from Zea mays L. (var. Pioneer) by tandem mass spectrometry and localization by confocal microscopy. We found that anthocyanins are located mainly in the aleurone layer of the grain. High-performance liquid chromatography in combination with ion trap tandem mass spectrometry revealed the presence of 56 compounds, including 30 polyphenols. This method allows for effective and rapid analysis of anthocyanins by plotting their distribution in seeds and grains of different plants. This approach will permit a more efficient screening of phenotypic varieties during food plant breeding.

Keywords: confocal microscopy, HPLC–MS/MS, tandem mass spectrometry, polyphenolic compounds

1. Introduction

The consumption of corn for 2018–2019 reached 315 million tons in the USA, 276 million tons in China, 63 million tons in the European Union, and 66 million tons in Brazil. In maize breeding, the discovery of genes responsible for the formation of corn endosperm accelerated research on the modeling of nutritional and taste properties of the corn.

The biochemical composition of corn grains, including protein, fatty acid, saccharide, and phenolic content, significantly affect the nutritional quality and taste of corn. The content of essential amino acids, such as valine, isoleucine, leucine, lysine, methionine, threonine, tryptophan, phenylalanine, histidine, and arginine is one of the major factors that determine the nutritional value of corn [1].

Corn grains have the highest polyphenol content (6056.9 mg/kg dry weight or 15.55 μmol/g) among other grains and represent significant interest for phytochemical and metabolomic study [2,3]. Phenolic compounds can have radical scavenging, chelating and antioxidative activity. Polyphenols can prevent oxidative stress caused by metabolic imbalances between the production and scavenging of free radicals [4]. Phenolic compounds can control oxidative stress by neutralizing or reducing the formation of reactive oxygen species (ROS) or restoration of redox homeostasis by strengthening the endogenous defense system or capturing the ROS [5]. The ability of polyphenolic groups to scavenge free radicals is associated with their aromatic rings and a highly conjugated system with many hydroxyl groups. The spatial position and the number of hydroxyl groups are important reference points for the antioxidant activity of phenolic compounds [6].

Fatty acids affect the palatability and especially the odor of foods. In higher plants, the proportion of essential fatty acids in the composition of vegetable fats is very high (up to 90%). It is mainly composed of palmitic, oleic, and linoleic acids. Analysis of the fatty acid composition of corn grains showed the presence of palmitic acid, linoleic acid, vaccenic acid, oleic acid, stearic acid, and eicosanoic acid.

Monosaccharides are derivatives of polyhydric alcohols and serve as a source for the synthesis of disaccharides (sucrose, maltose, lactose), oligosaccharides, and polysaccharides (cellulose and starch). Many of them have a sweet taste, but there are gradations from tasteless to bitter substances that affect the taste qualities of grains, including corn.

Flavonoids act as exogenous antioxidants and are directly oxidized by radicals with the formation of less reactive species through the following mechanisms: inhibition of xanthine oxidase activity, modulation of channel pathways, and inhibition of nitric oxide synthase activity [7]. The antioxidant potential of flavonoids is associated with the location and the total number of OH groups, or rather, with their molecular structure [8]. The use of flavonoids in biological systems holds great promise for bone tissue engineering. Quercetin, an antioxidant flavonoid, when present in the bloodstream, improves vascular health and reduces the risk of cardiovascular disease in its conjugated form. Quercetin and its derivatives prevent blood clotting or thrombosis and prevent the likelihood of stroke [9].

The structure of corn grain is presented in Figure 1 [10].

Figure 1.

Figure 1

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Structure of the grain of dent corn (with the symbolic designation of parts of the grain) (modified from [10]).

Previous research organized phenolic compounds according to the degree of antioxidant activity: simple phenolic acids < hydroxycinnamic acids < flavonols < flavan-3-ols < dimers of procyanidins [6]. It is known that the antioxidant activity of phenolic acids increases with an increase in the distance separating the carbonyl group and the aromatic ring, and hydroxycinnamic acid derivatives have stronger antioxidant activity than benzoic acid derivatives [11]. The 7,8-double bond of hydroxycinnamic acids also enhances their antioxidant potential, compared with hydroxybenzoic acids.

Jigh-performance liquid chromatography (HPLC) was predominantly used to identify carotenoids [12,13,14] and polyphenols [15,16] in corn grains. A review by Ranilla (2020) summarized the application of metabolomics for the characterization of metabolites in corn grains and emphasized the importance of phenotype–genotype studies aimed to explore corn genetic diversity [17]. The application of electrospray ionization mass spectrometry (ESI–MS) in combination with HPLC is a cost-effective and statistically robust method for high-throughput phenotypic characterization of corn [18]. The HPLC–ESI–MS/MS analytical configuration is widely used for the characterization of phenolic bioactive compounds in worldwide corn biodiversity. Montilla et al. (2011) characterized 10 corn landraces based on the content of phenolic fractions [19]. Das and Singh (2016) characterized four corn hybrids based on the content of phenolic acids, anthocyanins, and flavonols [20].

Another important problem is the study of spatial distribution and composition of phytochemicals in corn grains. Microscopic images are widely used as important sources of information on morphometric characteristics of cells and the architecture of plant tissue [21]. Confocal laser scanning microscopy was previously used to localize the phenolic compounds in different plants [22]. Morphological and biochemical changes in roots of corn Zea mays L. were previously studied by confocal microscopy [23,24]. To the best of the authors’ knowledge, no published studies report an application of confocal microscopy for the identification of phytochemicals in the grains of corn Zea mays L.

Considering the qualitative data of phytochemical composition obtained by HPLC–MS and literature information regarding the optical properties of identified chemicals, the combination of HPLC data with fluorescence microscopy is a good opportunity to explore the localization of phenolic compounds in plants. The combination of these methods is important for breeding since it allows us to assess whether the genes involved in the synthesis of these substances are expressed only in certain tissues (e.g., the aleurone layer, the germ layer, the vitreous endosperm) or in all grain glutes uniformly. In addition, this approach makes it possible to estimate the number and size of storing organelles (granules, chloroplasts, vesicles), since selection is important in both increasing their number and increasing their size. Thus, the combination of these methods allows us to obtain more complex information about the studied plants.

In this study, we used combined mass spectrometry and confocal laser microscopy to determine the structural properties and phytochemical composition of corn grains. In our case, the combination of HPLC–MS and fluorescence microscopy allowed us to demonstrate the localization of polyphenolic compounds in the grains of corn Zea mays L. However, the interpretation of the results of this study requires taking into account the limitations of the study design. The application of combined HPLC and fluorescent microscopy includes the possibility of spatial localization of different groups of plant chemicals in general but not the individual compounds.

2. Results

2.1. Tandem Mass Spectrometry

The extracts of corn grains were analyzed using liquid chromatography–electrospray ionization mass spectrometry (LC–ESI MS) to explore the diversity of available phytochemicals. The structural identification of each compound was carried out based on their accurate mass and MS/MS fragmentation using LC–ESI MS. In total, 56 compounds were successfully identified and characterized by comparing fragmentation patterns with those available in the literature. The results of a preliminary study showed the presence of 56 compounds corresponding to the genus Zea, some of which were identified for the first time in Zea mays L. The identified compounds, with molecular formulas m/z calculated and observed MS/MS data, and their comparative profile for corn grains are summarized in Table A1. The chromatograms of total compounds in the grain extract in positive and negative ionization modes are presented in Figure 2.

Figure 2.

Figure 2

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The total compounds chromatogram of Zea mays L. (var. Pioneer) extract.

In the present study, 30 polyphenol compounds were identified and characterized. In addition, 26 compounds of other classes were identified, including identified for the first time in corn grains oxylipins 13-trihydroxy-octadecenoic acid and 9,12,13-Trihydroxy-trans-10-octadecenoic acid.

Figure 3 and Figure 4 show examples of the decoding spectra (collision-induced dissociation (CID) spectrum) of the ion chromatogram obtained using tandem mass spectrometry. The [M–H]− ion produced three fragment ions at m/z 171, m/z 211, and m/z 293 (Figure 3). The fragment ion at m/z 171 yields a daughter ion at m/z 153. This compound was identified in the bibliography as 13-trihydroxy-octadecenoic acid (THODE) in extracts from Bituminaria [25], Broccoli [26], Sasa veitchii [27].

Figure 3.

Figure 3

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Mass spectrum of 13-trihydroxy-octadecenoic acid (THODE) from the extract of corn grains, m/z 329.20.

Figure 4.

Figure 4

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Mass spectrum of pelargonidin-3-O-glucoside from extracts of corn grains, m/z 432.77.

The mass spectrum in the positive ion mode of pelargonidin-3-o-glucoside from extracts of corn grains is shown in Figure 4. The [M + H]+ ion produced three fragment ions at m/z 271, m/z 415, and m/z 186 (Figure 4). The fragment ion at m/z 271 yields two daughter ions at m/z 253 and m/z 121. The fragment ion at m/z 253 yields one daughter ion at m/z 235. To our knowledge, pelargonidin-3-o-glucoside was reported in Triticum aestivum L. [28,29], strawberry [30].

2.2. Confocal Microscopy

Confocal microscopy, coupled with Airyscan technology, demonstrated blue (Figure 5b, Figure 6b and Figure 7b) and red fluorescence (Figure 5c, Figure 6c and Figure 7c) in the longitudinal and transverse sections, and in the aleurone layer of the grain, respectively.

Figure 5.

Figure 5

Figure 5

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The longitudinal section of the grain (grain margin in the embryo area), 63× magnification: (a) multispectral image, excitation 405 nm with the emission in 400–470 nm (blue), excitation 488 nm with the emission in 620–700 nm (red); (b) hydroxycinnamic and ferulic acids, and lignin content in the corn grain indicated in blue spectra; (c) anthocyanin content in the grain indicated in red spectra; p, pericarp; al, aleurone.

Figure 6.

Figure 6

Figure 6

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The transverse section of the grain, a border between endosperm (left) and embryo (right), 20× magnification: (a) multispectral image, excitation 405 nm with the emission in 400–470 nm (blue), excitation 488 nm with the emission in 620–700 nm (red); (b) hydroxycinnamic and ferulic acids, and lignin content in the corn grain indicated in blue spectra; (c) anthocyanin content in the grain indicated in red spectra; p, pericarp; al, aleurone; en, endosperm; em, embryo.

Figure 7.

Figure 7

Figure 7

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The aleurone layer of the grain (upper margin of the grain, the longitudinal section), 63× magnification: (a) multispectral image, excitation 405 nm with the emission in 400–470 nm (blue), excitation 488 nm with the emission in 620–700 nm (red); (b) hydroxycinnamic and ferulic acids, and lignin content in the corn grain indicated in blue spectra; (c) anthocyanin content in the grain indicated in red spectra; p, pericarp; al, aleurone; en, endosperm.

According to the literature data, strong blue fluorescence of plant grains under UV excitation could be explained by the presence of phenolic compounds such as hydroxycinnamic [31] or ferulic acid [32], and lignin [33]. The endosperm reveals very low blue autofluorescence (Figure 6 and Figure 7) due to the very low amount of phenolic substances in the endosperm cells of seeds and grains [34]. It was reported that the pericarp of Zea mays had a total phenolic content 30–34 fold higher than endosperm [35]. Our results demonstrated that the aleurone cells (Figure 5b, Figure 6b and Figure 7b) and embryo (Figure 7b) were enriched with blue autofluorescence substances. At the same time, it is known that no lignin is present in aleurone [36], but hydroxycinnamic, ferulic, and coumaric acids were reported in aleurone cells of cereals [37,38]. Therefore, the observed blue fluorescence might be caused by hydroxycinnamic, ferulic, and coumaric acids. The main blue fluorescent compound in the pericarp is lignin, which is a heterogeneous mixture of randomly polymerized phenolic monolignols [39].

The emission in the red spectrum mainly occurs due to the presence of various polyphenolic compounds, including anthocyanins and anthocyanidins [40].

3. Discussion

It is known that polyphenols have strong antioxidation, anticancer, anti-infection, and other valuable activities [41]. The knowledge of polyphenol distribution in plants will benefit the development of the methods of their direct extraction and further application in the food, pharmaceutical, and cosmetic industries.

Another important problem is the influence of environmental conditions on the polyphenol composition of the plants. The significant genotypic effects and interactions of the genotype with the environment suggest that breeding methodology will require careful site selection and accounting for changes in genotype rank with changes in cultivation sites.

The important characteristics such as grain color, protein, and polyphenol distribution represent significant interest for breeding. In the grain images, the fluorescence signal under UV excitation (405 nm) comes from ferulic acid [42] and lignin [33]. It should be noted that lignin is absent in aleurone, while coumaric and diferulic acids are present in the walls of aleurone cells. These acids can contribute to the autofluorescence of these cell walls [43,44].

Autofluorescence in the aleurone cell walls was not uniform, which is consistent with the studies presented below. Saadi et al. (1998) showed that autofluorescence was more intense in the anticline than in the periclinal cell walls of the corn grains [45]. Moreover, studies have shown that the content of ferulic acid in the anticlinal cell wall of the corn was twice as high as in the periclinal cell wall [46]. However, research by Phillippe et al. [34] argues that anticlinal and periclinal cell walls contain equal amounts of feruloylated arabinoxylan. Therefore, it seems that autofluorescence in the walls of anticlinal aleurone cells can additionally be caused by other substances, for example, coumaric and diferulic acids, which were found in aleurone cells [37].

Our study showed the metabolic profile of the corn Zea mays L. (var. Pioneer) represented as 56 compounds including 2 compounds identified in corn grains for the first time—namely, oxylipins 13-trihydroxy-octadecenoic acid and 9,12,13-trihydroxy-trans-10-octadecenoic acid. Laser microscopy showed the presence of polyphenolic compounds and, in particular, hydroxycinnamic and ferulic acids, and anthocyanins, in the tissues of corn grain.

The method used in this study is effective for rapid analysis of the distribution of polyphenolic compounds in seeds and grains of different plants. This approach allows the study of plant morphology and the characterization of relevant bioactive phytochemicals using an inexpensive and fast methodology. The characterization of novel corn hybrid genotypes harvested from different geographical areas is a strategic problem and addressing this problem would allow sustainable development of local agriculture.

4. Materials and Methods

4.1. Materials and Chemicals

As an object of research, we used corn grains Zea mays L., variety Pioneer P1467. The sample was harvested in 2020 in urban-type settlement Kirovsky (Primorsky Krai, Russian Far East) and obtained from a local farmer.

HPLC-grade acetonitrile was purchased from Fisher Scientific (Southborough, UK), MS-grade formic acid was from Sigma-Aldrich (Steinheim, Germany). Ultra-pure water was prepared from SIEMENS ULTRA clear (SIEMENS Water Technologies, Munich, Germany), and all other chemicals were analytical grade.

4.2. Fractional Maceration

Fractional maceration technique was applied to obtain highly concentrated extracts [47]. From 500 g of the sample, 4 g of corn seeds was randomly selected for maceration. The total amount of the extractant (ethyl alcohol of reagent grade) was divided into 3 parts, and the grains were consistently infused with the first, second, and third parts. The solid–solvent ratio was 1:20. The infusion of each part of the extractant lasted 7 days at room temperature.

4.3. Liquid Chromatography

HPLC was performed using Shimadzu LC-20 Prominence HPLC (Shimadzu, Kyoto, Japan) equipped with a UV sensor and C18 silica reverse phase column (4.6 × 150 mm, particle size: 2.7 µm) to perform the separation of multicomponent mixtures. The gradient elution program with two mobile phases (A, deionized water; B, acetonitrile with formic acid 0.1% v/v) was as follows: 0–2 min, 0% B; 2–50 min, 0–100% B; control washing 50–60 min 100% B. The entire HPLC analysis was performed with a UV–vis detector SPD-20A (Shimadzu, Kyoto, Japan) at a wavelength of 230 nm for identification of catechin, epicatechin, quercetin, and other compounds [48]; the temperature was 50 °C, and the total flow rate 0.25 mL min−1. The injection volume was 10 µL. Additionally, liquid chromatography was combined with a mass spectrometric ion trap to identify compounds.

4.4. Mass Spectrometry

MS analysis was performed on an ion trap amaZon SL (Bruker Daltoniks, Bremen, Germany) equipped with an ESI source in negative ion mode. The optimized parameters were obtained as follows: ionization source temperature: 70 °C, gas flow: 9 L/min, nebulizer gas (atomizer): 7.3 psi, capillary voltage: 4500 V, endplate bend voltage: 1500 V, fragmentary: 280 V, collision energy: 60 eV. An ion trap was used in the scan range m/z 100–1.700 for MS and MS/MS. All experiments were repeated three times. A four-stage ion separation mode (MS/MS mode) was implemented.

4.5. Optical Microscopy

Before the microscopic examination, a longitudinal and transverse dissection of corn grains was performed with MS-2 sled microtome (Tochmedpribor, Ukraine). The obtained sliced corn grains were placed on microscopic cover glass through immersion oil to reduce light refraction by air gaps.

The autofluorescence parameters of a slice of corn grain were determined using an inverted confocal microscope (confocal laser scanning microscopy—CLSM, LSM 800, Carl Zeiss Microscopy GmbH, Berlin, Germany). The autofluorescence spectrum was chosen using lambda scan mode of the confocal microscope, which allows to determine the emission maximum in a specific sample and obtain spectral acquisition. The specimen was excited by each laser separately and two main peaks of autofluorescence were revealed: excitation by a UV laser, 405 nm (solid state, diode, 5mW) with the emission maxima in the ranges 400–470 nm (blue); excitation by a blue laser, 488 nm (solid state, diode, 10 mW) with the emission maximum in 620–700 nm (red). The used power and detector gain for blue and red channels were 5% and 750 V, and 7% and 850 V, respectively.

The images were obtained using objectives Plan-Apochromat 20×/0.8 M27 and Plan-Apochromat 63×/1.40 Oil DIC M27 with 20× and 63× magnification, correspondingly. The zoom factor was 0.5. Airyscan at the SR mode was used to increase resolution. The software ZEN 2.1 (Carl Zeiss Microscopy GmbH, Berlin, Germany) was used for image acquisition.

5. Conclusions

We determined the qualitative characteristics of secondary metabolites in the tissues of corn Zea mays L. (var. Pioneer). In total, 56 compounds were identified, including 2 compounds identified in corn grains for the first time—namely, oxylipins 13-trihydroxy-octadecenoic acid and 9,12,13-trihydroxy-trans-10-octadecenoic acid.

The combination of these data with fluorescence microscopy data revealed the most probable localization of phenolic and polyphenolic compounds. In addition, confocal microscopy allowed us to assess the localization of hydroxycinnamic and ferulic acids in aleurone cells and embryos and anthocyanin content in pericarp and aleurone cells. The combination of these methods is important for breeding since it allows us to assess whether the genes involved in the synthesis of these substances are expressed only in certain tissues (the aleurone layer, the germ layer, the vitreous endosperm) or in all grain glutes uniformly. In addition, this approach makes it possible to estimate the number and size of storing organelles (granules, chloroplasts, vesicles), since selection is important both in the area of increasing their number and increasing their size. Thus, the combination of these methods allows us to obtain more complete information about the variables under study. In addition, it shows that confocal microscopy can be used to obtain preliminary information during volumetric screenings of varietal samples, which will allow selecting target groups for more detailed analysis much faster and without the use of expensive reagents.

Appendix A

Table A1.

The list of compounds identified in ethanolic extracts of Zea mays L. (var. Pioneer) grains.

No. Class Compound Molecular Formula Calculated Mass Molecular Ion [M−H]− Molecular Ion [M+H]+ Fragmenation Ion MS2 Fragmentation Ion MS3 Fragmentation Ion MS4 References
POLYPHENOLS
1 Phenolic acid Caffeic acid [(2E)-3-(3,4-Dihydroxyphenyl)acrylic acid] C9H8O4 180.1574 181 135 119 Dracocephalum palmatum [49]; Eucalyptus [50]; Triticum [51]; Salvia miltiorrhiza [52]
2 Phenolic acid Hydroxy methoxy dimethylbenzoic acid C10H12O4 196.1999 197 177; 153 125 F. herrerae; F. glaucescens [53]
3 Phenolic acid Hydroxyferulic acid C10H10O5 210.1834 211 193; 125 Andean blueberry [54];
4 Stilbene Resveratrol [trans-Resveratrol; 3,4′,5-Trihydroxystilbene; Stilbentriol] C14H12O3 228.2433 229 209 163 146 A. cordifolia; F. glaucescens; F. herrerae [53]; Radix polygoni multiflori [55]
5 Dihydroxybenzoic acid 3,4-Diacetoxybenzoic acid C10H11O6 238.1935 237 119 Potato leaves [56];
Triticum aestivum L. [57];
6 Flavan-3-ol Epiafzelechin [(epi)Afzelechin] C15H14O5 274.2687 275 245; 176 175 Cassia granidis [58];
Cassia abbreviata [59,60];
A. cordifolia; F. glaucescens; F. herrerae [53]
7 Flavonol Kaempferol [3,5,7-Trihydroxy-2-(4-hydro-xyphenyl)-4H-chromen-4-one] C15H10O6 286.2363 285 185; 117; 257 117 Rhus coriaria (Sumac) [61];
Lonicera japonicum [62]; Andean blueberry [54]; Potato [63];
Potato leaves [56];
8 Flavan-3-ol Catechin [D-Catechol] C15H14O6 290.2681 291 261; 189 173; 242 191; 143 Potato [64]; Triticum [51]; millet grains [65];
Solanaceae [66]; Beer [67]; V. edulis [53]; Vigna inguiculata [68];
Radix polygoni multiflori [55]; Senna singueana [69]; Camellia kucha [70];
9 Flavan-3-ol (epi)catechin C15H14O6 290.2681 291 261; 173 243; 173 C. edulis [53]; Radix polygoni multiflori [55]; Camellia kucha [70];
10 Hydroxycinnamic acid Caffeoylmalic acid C13H12O8 296.2296 295 277; 171 233; 113 Potato leaves [56];
Strawberry [71]
11 Flavonol Quercetin C15H10O7 302.2357 303 275; 245; 203; 175 175 Rhus coriaria [61];
Potato leaves [56];
Vigna sinensis [72];
Impatiens glandulifera Royle [73];
Eucalyptus [50]; Triticum [51]; millet grains [65];
Tomato [74];
Bougainvillea [75]
12 Flavan-3-ol Gallocatechin [+(−) Gallocatechin] C15H14O7 306.2675 307 277; 207 207; 159 millet grains [65];
Solanaceae [66];
Licania ridigna [76];
G. linguiforme [53];
Senna singueana [69];
Vaccinium myrtillus [77]
13 Flavonol Myricetin C15H10O8 318.2351 319 291; 219; 174 259; 191 243; 161 Dracocephalum palmatum [49];
Potato [63,64];
Perilla frutescens [78];
Tomato [74];
Mentha [79];
Salvia miltiorrhiza [52];
Rubus occidentalis [80];
Sanguisorba officinalis [81];
Radix polygoni multiflori [55]
14 Flavone Cirsiliol C17H14O7 330.2889 329 229; 171; 293 211; 155 183 Ocimum [82]
15 Flavone 5,7-Dimetoxy-3,3′,4′-trihydroxyflavone C17H14O7 330.2889 331 315; 270 313 285; 257 Oxalis corniculata [83]
16 Flavone Luteolin 7,3′-disulphate C15H10O12S2 446.3627 447 287 152 Zostera marina [84]
17 Flavone Apigenin 7-sulfate C15H10O8S 350.3001 351 337; 308 308; 291 G. linguiforme [53];
sulphates [85]
18 Lignan Matairesinol [(−)-Matairesinol; Artigenin Congener] C20H22O6 358.3851 359 324; 289; 127 144 127 Punica granatum [86];
Wheat [87];
Lignans [88]
19 Hydroxycinnamic acid derivative Caffeic acid derivative C16H18O9Na 377.2985 377 341; 215 179; 113 Bougainvillea [75]
20 Gallate ester, derivative of epiafzelechin Epiafzelechin 3-O-gallate C22H18O9 426.3729 427 301; 171; 382 171 Camellia kucha [70];
21 Flavone Apigenin-C-hexoside C21H20O10 432.3775 433 418; 314; 265; 219; 155 257; 169 Triticum durum [89];
Beer [67]
22 Anthocyanidin Pelargonidin-3-O-glucoside (callistephin) C21H21O10 433.3854 433 271; 185 253; 121 235 Triticum aestivum L. [28,29]; strawberry [30]
23 Anthocyanidin Cyanidin-3-O-glucoside [Cyanidin 3-O-beta-D-Glucoside; Kuromarin] C21H21O11+ 449.3848 447 285 199 Triticum [29,51];
acerola [90]; rice [91]; Vigna sinensis [72]; Rapeseed petals [92]
24 Flavone Luteolin-7-O-beta-glucuronide C21H18O12 462.3604 463 447; 395; 359; 285; 199; 149 287; 199 Mentha [93,94];
rat plasma [95];
Newbouldia laevis [60]
25 Flavonol Kaempferol-3-O-glucuronide C21H18O12 462.3604 463 287; 198 269; 198 Strawberry [71];
A.cordifolia; G. linguiforme [53];
Rhus coriaria [61]
26 Anthocyanidin Delphinidin malonyl hexoside C24H23O15 551.4304 551 465; 287; 185 287; 115 F. glaucescens [53]
27 Flavone Chrysoeriol C-hexoside-C-pentoside C27H30O15 594.5181 595 578; 536; 509; 425 294 Triticum aestivum L. [57,96];
T. durum [89]
28 Flavonol Quercetin 3,4′-di-O-beta-glucopyranoside [Quercetin diglucoside] C27H30O17 626.5169 627 465 447; 405; 303 Potato leaves [56];
Potato [63]; Rapeseed petals [92];
29 Flavone Tricin trimethyl ether 7-O-hexosyl-hexoside C30H36O17 668.5966 669 345; 387; 283 Triticum aestivum L. [97]
30 Flavan-3-ol (Epi)fisetinidol-(epi)catechin-A-(epi)fisetinidol C45H36O16 832.7577 831 721; 693; 609; 575; 537; 506 Chamaecrista nictitans [98]
OTHER COMPOUNDS
31 Amino acid L-Lysine C6H14N2O2 146.1876 147 119 Lonicera japonica [62];
32 Amino acid L-threanine C7H14N2O3 174.1977 175 159 Camellia kucha [70]
33 Amino acid L-Tryptophan [Tryptophan; (S)-Tryptophan] C11H12N2O2 204.2252 205 161; 159 143 Passiflora incarnata [99];
Vigna unguiculata [100];
Camellia kucha [70];
34 Omega-5 fatty acid Myristoleic acid [Cis-9-Tetradecanoic acid] C14H26O2 226.3550 227 209; 168 127 F. glaucescens [53]
35 Monobasic saturated carboxylic acid Myristic acid [Tetradecanoic acid; N-Tetradecanoic acid] C14H28O2 228.3709 229 142; 205 114 Rhododendron adamsii [101]
36 Medium-chain fatty acid Hydroxy dodecanoic acid C12H22O5 246.3001 247 238 203 174 F. glaucescens [53]
37 Ribonucleoside composite of adenine (purine) Adenosine C10H13N5O4 267.2413 268 136 Lonicera japonica [62]
38 Omega-3 fatty acid; octadecatetraenoic acid Stearidonic acid [6,9,12,15-Octadecatetraenoic acid; Moroctic acid] C18H28O2 276.4137 277 259; 177 177 Salviae Miltiorrhizae [102];
G. linguiforme [53];
Rhus coriaria [61]
39 Omega-3 fatty acid Linolenic acid (Alpha-Linolenic acid; Linolenate) C18H30O2 278.4296 279 243; 173 173 131 Salviae [102];
rice [91];
Pinus silvestris [103]
40 Diterpenoid Isocryptotanshinone II C19H20O3 296.3603 297 279; 197 173 Salviae Miltiorrhizae [102]
41 Alpha-omega dicarboxylic acid Octadecanedioic acid [1,16-Hexadecanedicarboxylic acid] C18H34O4 314.4602 313 295; 183 293; 179 275; 177 F. glaucescens [53]
42 Unsaturated essential fatty acid Oxo-eicosatetraenoic acid C20H30O3 318.4504 319 301 186 F. potsii [53]
43 Oxylipin 13- Trihydroxy-Octadecenoic acid [THODE] C18H34O5 330.4596 329 171; 211; 293 153 Bituminaria [25];
Broccoli [26]; Sasa veitchii [27]
44 Oxylipin 9,12,13- Trihydroxy-trans-10-octadecenoic acid C18H34O5 330.4596 329 171; 229 127 Potato leaves [56]
45 Unsaturated essential fatty acid Eicosatetraenedioic acid C20H30O4 334.4498 335 321; 124 291 G. linguiforme [53]
46 Isoquinoline alkaloid Berberine [Berberin; Umbelletine; Berbericine] C20H18NO4 336.3612 337 321; 225 291 291 Tinospora cordifolia [104,105]
47 Pentacyclic diterpenoid Gibberellic acid C19H22O6 346.3744 347 345; 259 329; 173 289 Triticum aestivum [106]
48 Berberine alkaloid Palmatine [Berbericinine; Burasaine] C21H22NO4 352.4037 353 337; 163 308 293 Ocotea [107,108]
49 Androgen; anabolic steroid Vebonol C30H44O3 452.6686 453 435; 336; 209 336; 226 209 Rhus coriaria [61];
Hylosereus polyrhizus [109]
50 Triterpenoid Oleanoic acid C30H48O3 456.7003 457 411; 249; 183 227; 169 Pear [110]; Ocimum [82]
51 Triterpenoid Maslinic acid C30H48O4 472.6997 473 425; 319; 201 291 Pear [110]; Folium Eriobotryae [111];
Malus domestica [112]
52 Thromboxane receptor antagonist Vapiprost C30H39NO4 477.6350 478 460; 337; 263; 155 263; 155 245; 189; 111 Rhus coriaria [61];
Hylosereus polyrhizus [109]
53 Indole sesquiterpene alkaloid Sespendole C33H45NO4 519.7147 520 184 184; 125 Rhus coriaria [61]; Hylosereus polyrhizus [109]
54 2-arylbenzofuran flavonoid Lithospermic acid A C27H22O12 538.4564 539 521; 409; 340; 241 395; 252; 167 Mentha [79,93,94]; Salvia multiorrizae [52]
55 Carotenoid (all-E)-lutein 3′-O-myristate C40H54O 550.8562 551 533; 505; 469;429; 373; 345 453; 410 Carotenoids [113]
56 Triterpenoid 3-O-glucuronide-29-hydroxyoleanolic acid C35H52O11 648.7808 649 473; 367; 291; 229 456; 385; 269 408; 305; 262; 187 Bougainvillea [75]
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Author Contributions

Conceptualization, M.R.; methodology, M.R. and A.Z.; investigation, M.R., Y.Z. and K.P.; resources, L.T., O.S. and T.K.; writing—original draft preparation, M.R.; supervision, K.G.; project administration, L.T. and T.K.; funding acquisition, L.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research was carried out with financial support of the Ministry of Education and Science of the Russian Federation within the framework of the implementation of a complex project for the creation of high-tech production provided by the Decree of the Russian Federation Government dated 9 April 2010 № 218. The project is entitled “Development of industrial technology and organization in the Far Eastern Federal District of the high-tech production of feed Vitamin A of increased stability and bioavailability”, agreement № 075-11-2021-065, 25 June 2021.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in the current study are available in the article.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Data Availability Statement

The data presented in the current study are available in the article.

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