Phytoprofiling of Sorbus L. Inflorescences: A Valuable and Promising Resource for Phenolics
by
,
Kristina Zymone
1,2,
Lina Raudone
2,3,*
,
Vaidotas Žvikas
2,
Valdas Jakštas
2,3 and
Valdimaras Janulis
3 1
Department of Analytical and Toxicological Chemistry, Lithuanian University of Health Sciences, Sukileliu Av. 13, LT-50162 Kaunas, Lithuania
2
Laboratory of Biopharmaceutical Research, Institute of Pharmaceutical Technologies, Lithuanian University of Health Sciences, Sukileliu Av. 13, LT-50162 Kaunas, Lithuania
3
Department of Pharmacognosy, Lithuanian University of Health Sciences, Sukileliu Av. 13, LT-50162 Kaunas, Lithuania
*
Author to whom correspondence should be addressed.
Plants 2022, 11(24), 3421; https://doi.org/10.3390/plants11243421
Submission received: 9 November 2022
/
Revised: 28 November 2022
/
Accepted: 6 December 2022
/
Published: 7 December 2022
(This article belongs to the Special Issue Plant-Based Products and Ingredients: Isolation, Characterization, Bioactivity and Applications in Several Industries)
Abstract
:The leaves and fruits of various Sorbus L. genotypes have long ethnopharmacological and food-usage histories, but inflorescences are still underutilized and neglected materials with scarce phytochemical scientific evidence. The aim of this study was to determine the phenolic profiles of inflorescence extracts of 26 Sorbus species, genotypes, and cultivars. HPLC and UPLS with MS detection were applied, and coupled data revealed unique phytochemical phenolic profiles. Neochlorogenic and chlorogenic acids were the key compounds, reaching up to 5.8 mg/g of dw. Rutin, isoquercitrin, quercetin 3-O-malonylglucoside, isorhamnetin 3-O-rutinoside, sexangularetin derivative, and kaempferol acetyl hexoside were detected in all Sorbus inflorescence samples. Overall, high quantitative heterogeneity across the various Sorbus genotypes was found by profiling. Phenolic fingerprint profiles and sexangularetin derivatives could serve as markers in authenticity studies and quality control schemes. The species S. amurensis, S. arranensis, S. commixta, and S. discolor and the cultivars ‘Chamsis Louing’, ‘Coral Beauty’, and ‘Edulis’ could be used as target genotypes for production of smart and innovative inflorescence matrix-based ingredients.
1. Introduction
Increasing consumers’ awareness about safe, health-promoting foods—and, specifically, the search for new safe and natural plant origin extracts and compounds that could be used with versatility in various industries for the production of cosmeceuticals, nutraceuticals, and pharmaceuticals—raises challenges and scientific uncertainties [1]. Furthermore, the increasing demand for innovative and functional food products with clear and clean labeling requires natural, safe, and simple ingredients that can be used conventionally [2]. Plant origin materials contain bodies of specialized metabolites that, when present in the extracts, exert health-promoting or pharmacological effects, as well as synergistic and additive effects [3]. In addition to the well-known plant materials with long ethnopharmacological histories, there are certain underutilized and neglected plants that can provide various raw materials that are extremely rich in particular groups of compounds of interest [4,5,6].
The genus Sorbus L. has a highly complicated systematics encompassing numerous subgenera and sections that determine its diversity sensu lato [7]. Furthermore, Sorbus’ extraordinary apomixis, cross-breeding, and intergeneric hybridization abilities have led to a great expansion of Sorbus genotypes, cultivars, hybrids, and varieties [8,9]. Almost all parts of the Sorbus plants have a historical record of usage in various traditional medicinal systems, as well as in food, fodder, beauty, health, and wellness-promoting products [10,11,12,13,14]. The fruits have been included in pharmacopoeias as polyvitaminic substances and in daily nutrition, but, due to their tart and specific taste, they are neglected or only used occasionally, although the ascorbic acid content exceeds the amount in oranges [4,15,16]. Nevertheless, their fruit powders could be incorporated as an ingredient in various processed foods and new products [4,17]. Extensive breeding and hybridization programs have led to several sweet-tasting rowanberries (Sorbus L. cultivars) that have potential as functional food ingredients containing amounts of carotenoids equivalent to commonly known sources, such as carrots [16,18,19,20]. Furthermore, due to their unique pattern of sugars and sugar alcohols, they could be incorporated in specialized food production [21,22]. Recent research has been devoted to elucidating the phytochemical richness and variability of phenolic profiles in the leaves of Sorbus species and varieties, as they contain more than fivefold higher amounts of phenolic compounds than commonly used fruits [23,24,25]. Although all Sorbus raw materials—namely, bark, leaves, and fruits—have been extensively investigated, the inflorescences are still one of the least studied raw materials. Sorbus plants contain decorative corymbs that cluster the dense flowers [26]. Scientific knowledge regarding the phytochemical composition of inflorescences is still limited. Olszewska et al. determined the phytochemical compositions of inflorescences of S. aucuparia, S. commixta, S. decora, S. gracilis, S. koehneana, S. torminalis, S. pohuashanensis, S. sitchensis, S. intermedia, and S. aria [23,24,25,27,28,29]. Recently, they produced a standardized inflorescence extract from S. aucuparia and determined its detailed phytochemical profile, as well as antioxidant and other biological properties [27]. However, the detailed profiling of inflorescences of other Sorbus species and cultivars has not yet been performed. Preliminary data suggest that Sorbus inflorescences contain significantly higher amounts of phenolic compounds than the fruits and even leaves [23,24,25,30]. Therefore, it is extremely important to determine their qualitative and quantitative profiles and define the analytical markers. Furthermore, the inflorescences of Sorbus contain the specific compound sexangularetin and its derivatives, which have not been detected in the fruits or leaves. These compounds could serve as authentication markers ensuring the quality of extracts [19].
Being climate- and environment-resilient, Sorbus plants are particularly attractive species for growth in standardized plantations, as they can withstand poor soils and harsh environments [31]. Sustainable and no-waste technologies could be applied for smart collection and preparation of Sorbus extracts from various raw materials rich in particular compounds [4,32].
The aim of this study was to determine the phenolic profiles of inflorescence extracts of 26 Sorbus L. species, genotypes, and cultivars. To the best of our knowledge, the profiles for the inflorescences of most species are reported for the first time. The research was focused on the phenolic profiles of the inflorescences, utilizing chemometric analysis to elucidate the chemophenetic differences and link the genotype with the pattern of phenolic acids and flavonoids. The lack of research on the phytochemical patterns of inflorescences of different Sorbus species highlights the need to elucidate the patterns and markers of the phenolic profiles. Phenolic compounds could act as chemical markers for the coupling or differentiation of species and substantiation of their parental origin. The peculiarities of the phenolic profiles could provide significant information for chemophenetic studies of this remarkably diverse genus of Sorbus.
2. Results
2.1. Quantitative Phenolic Profiling of Sorbus L. Species and Cultivars
Analysis of the qualitative and quantitative composition of the phenolic compounds in the raw plant material samples of rowan inflorescences was performed. The chromatogram of ethanol extracts from the inflorescence samples of Sorbus plants is presented in Figure S1. The results of qualitative analysis of phenolic compounds are presented in Table S1. Neochlorogenic, chlorogenic, and cryptochlorogenic acids, as well as dicaffeoylquinic acid derivative 1 and dicaffeoylquinnic acid derivative 2, were identified in all inflorescence samples tested (Table 1). Caffeoylshikimic acid was not detected only in inflorescences of S. aria and S. arranensis, and coumaroylquinic acid derivative was detected only in certain inflorescence samples. The concentrations of these caffeoylquinic acids varied significantly among the tested samples, with differences of up to twentyfold. Chlorogenic acid was the predominant component in most of the inflorescence samples from the various species and cultivars, although the predominant component in the inflorescence samples of S. arranensis and S. lancifolia was neochlorogenic acid, while quercetin 3-O-malonylglucoside was the predominant component in the inflorescences of ‘Edulis’. The greatest amount of chlorogenic acid was found in the inflorescence samples of S. commixta (31,539 ± 2503 µg/g), S. amurensis (29,733 ± 1465 µg/g), and ‘Chamsis Louing’ (25,867 ± 1557 µg/g) (Table 1). The greatest concentrations of neochlorogenic acid (18,712 ± 1740 µg/g, 17,739 ± 2442 µg/g, and 17,011 ± 441 µg/g) were found in the inflorescence samples of ‘Coral Beauty’, ‘Carpet of Gold’, and S. amurensis, respectively (Table 1).
Significant variation in the flavonol profiles depending on the Sorbus species/cultivar was determined (Table 2 and Table 3), with the amounts varying up to 33-fold. Rutin, isoquercitrin, quercetin 3-O-malonylglucoside, isorhamnetin 3-O-rutinoside, sexangularetin derivative, and kaempferol acetyl hexoside were detected in all Sorbus inflorescence samples. Isoquercitrin was the predominant component of the flavonoid complexes in the inflorescence samples of S. commixta, S. x hostii, ‘Alaja Krupnaja’, ‘Granatnaja’, ‘Koncentra’, ‘Krasnaja Nevezinskaja’, ‘Miciurinskaja Desertnaja’, ‘Nevezinskaja’, ‘Neveziskaja Zolotistaja’, ‘Nevezinskaja Zoltaja’, ‘Oranzevaja’, and ‘Titan’, while quercetin 3-O-malonylglucoside was the predominant component in the inflorescences of S. aria, S. arranensis, S. lancifolia, S. hybrida subsp. Gotlandica, S. hybrida subsp. Persecta, ‘Carpet of Gold’, ‘Chamsis Louing’, ‘Coral Beauty’, ‘Edulis’, ‘Pink Queen’, and ‘Yellow Upright’. We determined that, in the inflorescence samples of S. discolor and S. semi-incisa, the predominant flavonoid was rutin and, in the inflorescences of S. amurensis, it was hyperoside.
2.2. Hierarchical Cluster Analysis of Phenolic Compounds in Sorbus L. Species and Cultivars
Hierarchical cluster analysis was performed for the samples of Sorbus inflorescences, using the concentrations of identified biologically active compounds as clustering variables. The investigated Sorbus inflorescence samples were grouped into seven significant clusters (Figure 1).
Inflorescence samples of the ‘Krasnaja Nevezinskaja’, ‘Neveziskaja Zolotistaja’, ‘Nevezinskaja’, ‘Koncentra’, ‘Oranzevaja’, ‘Nevezinskaja Zoltaja’, ‘Alaja Krupnaja’, ‘Granatnaja’, ‘Miciurinskaja Desertnaja’, and ‘Titan’ cultivars and S. discolor formed the first cluster. This cluster was characterized by the highest concentration of quercetin dihexoside 2 and a high concentration of isoquercitrin, while dicaffeoylquinic acid derivative 3 was not detected and low concentrations of quercetin 3-O-malonylglucoside and isorhamnetin rutinoside were detected. The second cluster grouped inflorescence samples of ‘Chamsis Louing’, ‘Pink Queen’, ‘Coral Beauty’, ‘Yellow Upright’, ‘Carpet of Gold’, S. lancifolia, S. hybrida subsp. gotlandica, S. semi-incisa, and S. hybrida subsp. persecta. The samples forming the second cluster were characterized by high concentrations of quercetin 3-O-malonylglucoside, isorhamnetin rutinoside, caffeoylshikimic acid, dicaffeoylquinic acid derivative 1, and dicaffeoylquinic acid derivative 2 and low concentrations of quercetin dihexoside 1, quercetin dihexoside 2, and isoquercitrin. The inflorescences of S. aria and S. x hostii formed the third cluster. The corresponding inflorescence samples differed from the others in their high concentrations of dicaffeoylquinic acid derivatives and low concentrations of the other identified phenolic compounds. The inflorescences of ‘Edulis’, S. arranensis, S. amurensis, and S. commixta formed the fourth, fifth, sixth, and seventh clusters, respectively. Inflorescence samples of the ‘Edulis’ cultivar differed from the others in having highest concentrations of isoquercitrin and quercetin 3-O-malonylglucoside, while inflorescence samples of S. arranensis were characterized by the highest concentrations of kaempferol coumaroyl hexoside, isorhamnetin rutinoside, kaempferol acetylhexoside, and isorhamnetin acetylhexoside and the lowest concentrations of quercetin dihexoside 1 and quercetin dihexoside 2 (Figure 1). Inflorescence samples of S. amurensis differed from the others in having the highest concentrations of quercetin dihexoside 1 and hyperoside and the lowest concentration of quercetin 3-O-malonylglucoside. Inflorescence samples of S. commixta were also found to differ from the others as they showed the highest concentrations of chlorogenic acid, cryptochlorogenic acid, and astragalin and the lowest concentrations of neochlorogenic acid and rutin
2.3. Principal Component Analysis (PCA) of Phenolic Compounds in Sorbus L. Species and Cultivars
A principal component analysis (PCA) was performed to detect similarities and differences between the analyzed samples in terms of the total concentration of caffeoylquinic acid derivatives (TCCQA), the total concentration of dicaffeoylquinic acid derivatives (TCdiCQA), the concentration of caffeoylshikimic acid (CCSA), the total concentration of quercetin monoglycosides (TCQmonoglyc), the total concentration of quercetin diglycosides (TCQdiglyc), the total concentration of kaempferol derivatives (TCK), the total concentration of isorhamnetin glycosides (TCI), and the concentration of sexangularetin derivative (CS). The PCA results based on the correlation matrix with the first principal component (PC1), the second principal component (PC2), and the third principal component (PC3) are shown in Figure 2. Three principal components explaining 76.60% of the total data variance in the datasets for the Sorbus inflorescences were used for the in-depth analysis. PC1 described 31.82% of the total variance in the data and correlated with positive loadings for the TCdiCQA (0.877), TCI (0.842), and TCK (0.602) and negative loadings for the TCQdiglyc (−0.699). PC2 accounted for 25.06% of the total variance and was characterized by positive loadings for the CCSA (0.947) and the TCCQA (0.917). PC3 described 19.72% of the total variance in the data and had strong positive correlations with TCQmonoglyc (0.837) and CS (0.786).
The inflorescences of Sorbus were clustered into four groups. Inflorescence samples of group I were closely clustered along the negative side of PC1 due to the high total concentration of quercetin diglycosides and low total concentrations of dicaffeoylquinic acids, isorhamnetin derivatives, and kaempferol derivatives. Inflorescences of group III were located on the positive side of PC1. The total concentrations of dicaffeoylquinic acids, isorhamnetin derivatives, and kaempferol derivatives that scored highly in PC1 ranged from the mean values to the highest in the corresponding samples. In contrast, the total concentration of quercetin diglycosides, which had a negative loading in PC1, was determined to be low in these inflorescence samples. Inflorescence samples of group I and group III were situated near the zero point of PC2. The concentration of caffeoylshikimic acid and total concentration of caffeoylquinic acids determined in these samples were close to the mean values. Group II was distinguished by a high concentration of caffeoylshikimic acid and a total concentration of caffeoylquinic acids that scored highly in PC2. Inflorescence samples of group IV differed from the others in their low concentration of caffeoylshikimic acid and total concentration of caffeoylquinic acids, which had positive loadings in PC2. Inflorescence samples of ‘Edulis’ were distanced from all the others and were grouped on the positive side of the PC3. This could be explained by the high concentration of sexangularetin derivative and total concentration of quercetin monoglycosides.
3. Discussion
Phenolic-rich plant materials are considered as sources for added-value ingredients that could provide positive health and nutritional effects in the frame of chronic degenerative diseases resulting from the features of modern life [33]. Plants synthesize phenolic compounds as specialized metabolites against exogenous and endogenous stress factors. Furthermore, various studies have confirmed their remarkable health effects and pharmacological activities; namely, antioxidant, anti-inflammatory, cardioprotective, neuroprotective, gut microbiota-promoting, and antidiabetic effects [24,28,33,34,35]. The latter effect is one of the main medicinal effects documented for the raw materials of Sorbus species, with the phenolic compounds being suggested as one of the bioactive fractions [19,36,37]. The majority of ethnopharmacological, phytochemical, and nutritional studies have focused on the leaves and fruits of various Sorbus species and cultivars. This study elucidated the phenolic profiles of inflorescences of Sorbus species and cultivars. High quantitative heterogeneity across various Sorbus genotypes was found in the profiling. However, the prevailing compounds that were common to all Sorbus materials tested were present in a constant manner, with the chlorogenic and neochlorogenic acids being the key components and rutin, isoquercetin, and quercetin malonyl glucoside the prevailing flavonoids. The results are consistent with our previous studies [20,38,39,40,41] and with the studies by Olszevska et al., which, to the best of our knowledge, are to date the only phytochemical studies on the inflorescences of Sorbus species [23,24,27,30]. Epidemiological and clinical studies show that hydroxycinnamic acid intake is associated with reduced risk of metabolic syndrome, diabetes, and colorectal cancer. Furthermore, chlorogenic acid can modulate colonic microbiota and, via the gut–brain axis, express health benefits [42]. Hydroxycinnamic acids have anti-inflammatory [43], neuroprotective [44], antidiabetic [45], antimicrobial [46], and ultraviolet-protective [47] effects. The amount of neochlorogenic acid we observed in the inflorescence samples was close to the amount identified by Olszewska et al. (0.19–1.98%) [24,30]. Olszewska et al. found 1.78–4.17% chlorogenic acid in their inflorescence samples, and the inflorescences of S. commixta contained significantly higher amounts of chlorogenic acid compared to the leaves (3.92% and 0.79%, respectively) [24,30]. The species and cultivars we analyzed accumulated less chlorogenic acid (0.76–2.25%).
S. commixta is a valuable species with an extraordinarily rich phenolic composition [29]. In our previous research [38,39,40], the fruits and leaves of this species were found to be exclusively separate from other species in the hierarchical cluster and PCA analyses, and they had the highest antioxidant activities. Furthermore, in this study, the inflorescences of S. commixta contained the greatest amounts of chlorogenic acid and, surprisingly, the lowest amounts of neochlogenic acid compared to other Sorbus species. However, the amounts of chlorogenic acid were sevenfold and twofold lower compared to the leaves and fruits, respectively [38,39]. The quantitative composition of phenolic acids in sweet rowanberries of the ‘Titan’, ‘Granatnaja’, ‘Alaja Krupnaja’ cultivars has been previously examined [16]. The greatest amounts of neochlorogenic and chlorogenic acids were in the fruits of ‘Granatnaja’, while the lowest amounts were determined in the fruits of ‘Alaja Krupnaja’. Our study determined corresponding patterns in the inflorescence samples of ‘Titan’, ‘Granatnaja’, and ‘Alaja Krupnaja’. Kylli et al. (2010) found the greatest amounts of neochlorogenic acid and chlorogenic acid in fruit samples from the cultivars ‘Titan’ and ‘Granatnaja’ [48]. We compared the amounts of hydroxycinnamic acids in leaves, fruits, and inflorescences (certain species overlapped in our previous studies), and the results demonstrated the superiority of the leaves and fruits. In contrast, Olszewska et al. (2010) determined that S. commixta inflorescences contained significantly greater amounts of total phenolics and about threefold greater amounts of chlorogenic acid compared to leaves [30]. Olszewska and Michel (2009) determined that the antioxidant activities of S. aucuparia, S. aria, and S. intermedia inflorescences were higher compared to the leaves and fruits. In fact, the phenolic content in the inflorescences and leaves of various Sorbus genotypes are comparable, and superiority strongly depends on geographic, climatic, and edaphic conditions. Further studies could target phytogeographic, phonologic, and ontogenetic profiling. The total phenolic contents in inflorescences and leaves were comparable; however, the profiles of individual flavonoids were highly variable between plant materials [24]. Flavonols are the predominant flavonoids in Sorbus materials [19]. Flavonols demonstrate cardioprotective [49], neuroprotective [50], hepatoprotective [51], anticancer [52], antimicrobial [53], anti-inflammatory [54], and anti-platelet [55] activities. On average, the total amount of identified flavonoids in the tested Sorbus inflorescences was 1.7 mg/g. The individual patterns showed high quantitative heterogeneity. Overall, the amounts of individual flavonoids in inflorescences were lower than in the leaves of the respective species (S. arranensis, S. commixta, S. discolor, S. semi-incisa) [38,40]. Olszewska determined that the total flavonoid content was superior in the inflorescences of S. aucuparia and S. intermedia compared to the leaves, and only S. aria leaves were superior to the inflorescences. In contrast, our results show that the total identified flavonoids in S. aria inflorescences were lower compared to the leaves. Hukkanen et al. (2006), for fruit samples of the ‘Titan’, ‘Granatnaja’, and ‘Alaja Krupnaja’ cultivars, determined that the greatest amount of flavonols was found in the fruits of ‘Granatnaja’, while the lowest amount was found in the fruits of ‘Alaja Krupnaja’ [16]. The pattern corresponds with the results of our present study, confirming the phytochemical impact of genotype. Quercetin derivatives have been determined to be the predominant substances in identified flavonoid complexes. The amounts of other flavonoids are significantly lower. These results are consistent with data supplied by other researchers [23]. Upon comparison of the amounts of isorhamnetin derivatives in inflorescence samples from various species and cultivars of Sorbus, we determined that the inflorescence samples of the subgenus Aria contained greater amounts of these flavonoids than the inflorescence samples of the subgenus Sorbus. The same patterns were detected by Polish scientists [23,29]. The amounts of isorhamnetin determined in the inflorescence samples of S. aria during previous research were 31–32% [56] and 44% [23] of the total flavonoid amount. Isorhamnetin could be used as an analytical marker for differentiation of raw plant materials of different subgenera. Sexangularetin is an important analytical marker of Sorbus inflorescence materials. In contrast to leaves, the inflorescences are abundant in sexangularetin derivatives; namely, methoxylated flavonoids [27]. Methoxylated flavonoids could be of particular scientific interest, as they have high metabolic stability and bioavailability [57]. The pattern for methoxylated flavonoids highlights the uniqueness of inflorescences compared to leaves and fruits. Our results showed that S. discolor had the greatest amount of sexangularetin derivatives. The genotype determined the pattern of the phenolic compounds, and the chemometric analysis distinguished two principal groups of Sorbus inflorescences; namely, the Rossica cultivar group (Table 4) and the group constituted by S. x arnoldiana cultivars and sect. Sorbus species. S. amurensis, S. aria, S. arranensis, S. commixta, and S. x hostii formed different, distinct groups or separate clusters, confirming their unique and particular phenolic profiles. The cultivars ‘Chamsis Louing’, ‘Coral Beauty’, and ‘Edulis’ and the species S. amurensis, S. arranensis, and S. commixta, remarkably, had the highest total phenolic compounds determined, ranging from 5.9 to 7.9 mg/g.
Plant inflorescences, rich in hydroxycinnamic acids and quercetin derivatives, are potent antioxidants, possess anti-inflammatory activities, and, traditionally, are used as diuretic, diaphoretic, and anti-inflammatory agents [58,59,60,61]. Furthermore, food plants provide various raw materials that contain phytochemical compounds with health benefits. The processing of the raw materials can, depending on the final concentration of compounds, create an interface between food, medicine, and cosmetics [62]. Plant material infusions targeted as daily food intake can be employed as preventive nutrition in restoring and sustaining health and wellness [60]. Sorbus inflorescences are attractive plant matrixes with notable phenolic profiles. Modulation of the stages of genotype selection, extraction, and processing can unlock their potential multi-industrial applications in future preparations.
4. Materials and Methods
4.1. Plant Material
In May 2012, inflorescence samples from Sorbus species and cultivars were collected in the southeastern region of Lithuania at the Botanical Garden of Vilnius University (54°43′48″ N 25°23′56″ E) for a phytochemical analysis. Eight rowan species (S. amurensis, S. aria, S. arranensis Hedl. (voucher specimen no. 3641), S. commixta (voucher specimen no. 3652), S. discolor Maxim. (voucher specimen no. 3653), S. lancifolia Hedl. (voucher specimen no. 3661), S. semi-incisa (Borbas) Borbas (voucher specimen no. 3663), and S. x hostii (J.Jacq.) K.Koch (voucher specimen no. 3659)), sixteen cultivars (‘Alaja Krupnaja’ (voucher specimen no. 3423), ‘Nevezinskaja’ (voucher specimen no. 3428), ‘Oranzevskaja’ (voucher specimen no. 3425), ‘Titan’ (voucher specimen no. 3424), ‘Granatnaja’ (voucher specimen no. 3433), ‘Carpet of Gold’ (voucher specimen no. 2895), ‘Chamsis Louing’ (voucher specimen no. 2887), ‘Coral Beauty’ (voucher specimen no. 2896), ‘Edulis’ (voucher specimen no. 3645), ‘Koncentra’ (voucher specimen no. 3435), ‘Krasnaja Nevezinskaja’ (voucher specimen no. 3648), ‘Miciurinskaja Desertnaja’ (voucher specimen no. 2897), ‘Nevezinskaja Zolotistaja’ (voucher specimen no. 3653), ‘Neveziskaja Zoltaja’ (voucher specimen no. 3442), ‘Pink Queen’ (voucher specimen no. 2888), ‘Yellow Upright’ (voucher specimen no. 2889)), and two S. hybrida subspecies (subsp. Gotlandica (voucher specimen no. 3656), subsp. Persecta (voucher specimen no. 3657)) were collected.
The collected raw plant material samples were dried at room temperature and stored in a dark, dry place. The research results were re-calculated for absolutely dry raw plant material.
4.2. Materials and Reagents
Analytical and chromatographic grade reagents were used for this study: gradient-grade acetonitrile, MS-grade formic acid, neochlorogenic acid, cryptochlorogenic acid, quercetin 3-O-(6″-O-malonyl)-β-D-glucoside (quercetin 3-O-malonylglucoside hereinafter), isorhamnetin 3-O-rutinoside (Sigma-Aldrich GmbH, Steinheim, Germany), HPLC-grade 99.8% trifluoracetic acid, chlorogenic acid, HPLC-grade hyperoside, HPLC-grade isoquercitrin, HPLC-grade rutin, astragalin (Carl Roth GmbH, Karlsruhe, Germany), and 96.3% ethanol (Stumbras SC, Kaunas, Lithuania). The purified deionized water (18.2 mΩ/cm) was produced using a Millipore (Burlington, MA.,USA) water purification system.
4.3. Sample Preparation
For qualitative and quantitative analysis of flavonoid glycosides and phenolic acids, the rowan inflorescence samples were crushed into particles and passed through a 355 μm sieve. The samples weighed around 0.25 g (accurate sample). The weighed raw plant material sample was then placed into a conical flask with 25 mL of 50% ethanol. The extraction was performed by submerging the materials in a BioSonic UC100 ultrasonic bath (Cuyahoga Falls, Ohio, USA) for 20 min. The obtained extract was filtered through a paper filter into a 25 mL volumetric flask and adjusted accordingly to a volume with 50% ethanol. Before high-performance liquid chromatography (HPLC) analysis, extracts were filtered through a membrane filter with a pore size of 0.22 μm (Carl Roth GmbH, Karlsruhe, Germany).
4.4. HPLC Analysis
The analysis of extracts was performed using a previously optimized and validated (Gaivelyte et al., 2014) HPLC method. Briefly, quantitative analysis was performed using a Waters 2695 Alliance system (Waters, Milford, MA, USA) with a Waters 996 photodiode array detector. Separation was performed using an ACE (ACT, Aberdeen, UK) column (C18, 150 mm × 4.6 mm, particle size: 3 μm). The mobile phase of the optimized chromatographic method consisted of eluents A (0.05% trifluoracetic acid) and B (acetonitrile). The gradient variation was as follows: 0–5 min—12% B, 5–50 min—12–30% B, 50–51 min—30–90% B, 51–56 min—90% B, 57 min—12% B. The eluent flow rate was 0.5 mL/min, and the injection volume was 10 μL. The column was temperature-controlled, and the temperature was maintained at 25 °C. Calibration curves of compounds identified in the rowan inflorescence extracts were compiled; these curves were used for quantitative assessment. Quantification of caffeoylshikimic acid and dicaffeoylquinic acid derivatives was performed using a chlorogenic acid calibration curve, quantification of quercetin diglycosides using a rutin calibration curve, quantification of kaempferol derivatives using an astragalin calibration curve, and quantification of isoramnetin and sexangularetin derivatives using an isorhamnetin 3-O-rutinoside calibration curve. Concentrations of phenolic acids were calculated at a wavelength of 325 nm, while the concentrations of flavonoids were calculated at a wavelength of 350 nm.
4.5. UPLC-ESI-MS Conditions
Separation of phenolic compounds was carried out with an Acquity H-class UPLC system (Waters, USA) equipped with a Waters 2998 photodiode array detector, and a triple quadrupole tandem mass spectrometer (Xevo, Waters, USA) with an electrospay ionisation source (ESI) was used to obtain MS/MS data. A YMC Triart C18 (100 × 2.0 mm 1.9 µm) column was used for analysis. The column temperature was maintained at 40 °C. Gradient elution was performed with a mobile phase consisting of 0.1% formic acid water solution (solvent A) and acetonitrile (solvent B), with the flow rate set to 0.5 mL/min. The linear gradient variation was as follows: 0–1 min—5% B, 1–5 min—5–30% B, 5–7 min—30–50% B, 7–7.5 min—50–100% B, 7.5–8 min—100%, 8–8.1 min—100–5% B, 8.1–10 min—5% B. Negative electrospray ionization was applied for analysis with the following settings: capillary voltage—2 kV, source temperature—150 °C, desolvation temperature—400 °C, desolvation gas flow—700 L/h, cone gas flow—20 L/h. Collision energy and cone voltage were optimized for each compound separately.
4.6. Statistical Analysis
Phenolic compound content was expressed as the mean ± standard deviation (SD) of three replicates. The statistical data analysis was evaluated by applying ANOVA with a Tukey HSD post hoc test. Statistically significantly different means were marked with different letters. Differences were considered statistically significant when p < 0.05. In accordance with the quantitative composition of the identified compounds, the tested samples were compared using the method of hierarchical cluster analysis with squared Euclidean distances. Principal component analysis was performed taking into account factors with eigenvalues higher than 1. The data were processed using Microsoft Office Excel 2010 (Microsoft, JAV) and SPSS 20 software.
5. Conclusions
The current study provides a comprehensive analysis of the phenolic profiles of 27 Sorbus genotypes and complements knowledge regarding the patterns of specialized metabolites in Sorbus plant materials. The findings showed that the inflorescence extracts were abundant in hydroxycinnamic acids and flavonol derivatives. The leaves and inflorescences were comparable in phenolic contents, and the significant superiority of inflorescences was not observed. Phenolic fingerprint profiles and sexangularetin derivatives could serve as markers in authenticity studies and quality control schemes. The species S. amurensis, S. arranensis, S. commixta, and S. discolor and cultivars ‘Chamsis Louing’, ‘Coral Beauty’, and ‘Edulis’ could be target genotypes for production of smart and innovative inflorescence matrix-based ingredients.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants11243421/s1, Figure S1: Sorbus L. inflorescence phytochemical profiles; Table S1: Identified phenolic compounds in Sorbus L. inflorescences.
Author Contributions
Conceptualization, V.J. (Valdimaras Janulis), K.Z. and L.R.; methodology, K.Z., V.J. (Valdas Jakštas), and V.Ž.; software, K.Z.; validation, K.Z. and V.Ž.; formal analysis, K.Z.; investigation, K.Z. and V.Ž.; resources, V.J. (Valdas Jakštas) and V.J. (Valdimaras Janulis); data curation, K.Z.; writing—original draft preparation, K.Z. and L.R.; writing—review and editing, K.Z. and L.R.; visualization, K.Z.; supervision, V.J. (Valdimaras Janulis). All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Data Availability Statement
All data generated during this study are included in this article.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Anunciato, T.P.; da Rocha Filho, P.A. Carotenoids and polyphenols in nutricosmetics, nutraceuticals, and cosmeceuticals. J. Cosmet. Dermatol. 2012, 11, 51–54. [Google Scholar] [CrossRef] [PubMed]
- Noguerol, A.T.; Pagán, M.J.; García-Segovia, P.; Varela, P. Green or clean? Perception of clean label plant-based products by omnivorous, vegan, vegetarian and flexitarian consumers. Food Res. Int. 2021, 149, 110652. [Google Scholar] [CrossRef] [PubMed]
- Wagner, H.; Ulrich-Merzenich, G. Synergy research: Approaching a new generation of phytopharmaceuticals. Phytomedicine 2009, 16, 97–110. [Google Scholar] [CrossRef] [PubMed]
- Sarv, V.; Venskutonis, P.R.; Bhat, R. The Sorbus spp.—Underutilised Plants for Foods and Nutraceuticals: Review on Polyphenolic Phytochemicals and Antioxidant Potential. Antioxidants 2020, 9, 813. [Google Scholar] [CrossRef] [PubMed]
- Šola, I.; Poljuha, D.; Mikulic-Petkovsek, M.; Davosir, D.; Pinterić, M.; Bilić, J.; Veberic, R.; Hudina, M.; Rusak, G. Biopotential of Underutilized Rosaceae Inflorescences: LC-DAD-MS Phytochemical Profiles Associated with Antioxidant, Antidiabetic, Anti-Inflammatory and Antiproliferative Activity In Vitro. Plants 2022, 11, 271. [Google Scholar] [CrossRef] [PubMed]
- Neglected and Underutilized Plant Species Strategic Action Plan of the International Plant Genetic Institute. Available online: https://www.bioversityinternational.org/fileadmin/_migrated/uploads/tx_news/Neglected_and_underutilized_plant_species_837.pdf (accessed on 19 October 2022).
- Aldasoro, J.J.; Aedo, C.; Navarro, C.; Garmendia, F.M. The Genus Sorbus (Maloideae, Rosaceae) in Europe and in North Africa: Morphological Analysis and Systematics. Syst. Bot. 1998, 23, 189–212. [Google Scholar] [CrossRef]
- Németh, C.; Papp, N.; Nosková, J.; Höhn, M. Speciation by triparental hybridization in genus Sorbus (Rosaceae). Biol. Futur. 2020, 71, 209–222. [Google Scholar] [CrossRef]
- Li, M.; Tetsuo, O.T.; Gao, Y.D.; Xu, B.; Zhu, Z.M.; Ju, W.B.; Gao, X.F. Molecular phylogenetics and historical biogeography of Sorbus sensu stricto (Rosaceae). Mol. Phylogenet. Evol. 2017, 111, 76–86. [Google Scholar] [CrossRef]
- Yu, T.; Lee, Y.J.; Jang, H.J.; Kim, A.R.; Hong, S.; Kim, T.W.; Kim, M.Y.; Lee, J.; Lee, Y.G.; Cho, J.Y. Anti-inflammatory activity of Sorbus commixta water extract and its molecular inhibitory mechanism. J. Ethnopharmacol. 2011, 134, 493–500. [Google Scholar] [CrossRef]
- Kang, D.G.; Lee, J.K.; Choi, D.H.; Sohn, E.J.; Moon, M.K.; Lee, H.S. Vascular relaxation by the methanol extract of Sorbus cortex via NO-cGMP pathway. Biol. Pharm. Bull. 2005, 28, 860–864. [Google Scholar] [CrossRef]
- McCune, L.M.; Johns, T. Antioxidant activity in medicinal plants associated with the symptoms of diabetes mellitus used by the Indigenous Peoples of the North American boreal forest. J. Ethnopharmacol. 2002, 82, 197–205. [Google Scholar] [CrossRef] [PubMed]
- Changzhi, Y.; Yonggang, Z.; Le, L.; Guojun, W.; Yingchun, L.; Tao, W.; Hui, T. Isolation of chemical compounds from Sorbus tianschanica Rupr by high-speed counter-current chromatography. J. Med. Plants Res. 2012, 6, 5142–5149. [Google Scholar] [CrossRef]
- Gil-Izquierdo, A.; Mellenthin, A. Identification and quantitation of flavonols in rowanberry (Sorbus aucuparia L.) juice. Eur. Food Res. Technol. 2001, 213, 12–17. [Google Scholar]
- Shikov, A.N.; Pozharitskaya, O.N.; Makarov, V.G.; Wagner, H.; Verpoorte, R.; Heinrich, M. Medicinal Plants of the Russian Pharmacopoeia; their history and applications. J. Ethnopharmacol. 2014, 154. [Google Scholar] [CrossRef] [Green Version]
- Hukkanen, A.T.; Pölönen, S.S.; Kärenlampi, S.O.; Kokko, H.I. Antioxidant capacity and phenolic content of sweet rowanberries. J. Agric. Food Chem. 2006, 54, 112–119. [Google Scholar] [CrossRef]
- Berna, E.; Kampuse, S.; Dukalska, L.; Murniece, I. The chemical and physical properties of sweet rowanberries in powder sugar. In Proceedings of the 6th Baltic Conference on Food Science and Technology “Innovations for Food Science and Production”, Jelgava, Latvia, 5–6 May 2011; pp. 163–168. [Google Scholar]
- Jurikova, T.; Sochor, J.; Mlcek, J.; Balla, S.; Klejdus, B.; Baron, M.; Ercisli, S.; Ozturk Yilmaz, S. Polyphenolic profile of interspecific crosses of rowan (Sorbus aucuparia L.). Ital. J. Food Sci. 2014, 26, 317–324. [Google Scholar]
- Sołtys, A.; Galanty, A.; Podolak, I. Ethnopharmacologically important but underestimated genus Sorbus: A comprehensive review. Phytochem. Rev. 2020, 19, 491–526. [Google Scholar] [CrossRef]
- Zymone, K.; Raudone, L.; Raudonis, R.; Marksa, M.; Ivanauskas, L.; Janulis, V. Phytochemical Profiling of Fruit Powders of Twenty Sorbus L. Cultivars. Molecules 2018, 23, 2593. [Google Scholar] [CrossRef] [Green Version]
- Grussu, D.; Stewart, D.; McDougall, G.J. Berry polyphenols inhibit α-amylase in vitro: Identifying active components in rowanberry and raspberry. J. Agric. Food Chem. 2011, 59, 2324–2331. [Google Scholar] [CrossRef]
- Chukwuma, C.I.; Islam, S. Sorbitol increases muscle glucose uptake ex vivo and inhibits intestinal glucose absorption ex vivo and in normal and type 2 diabetic rats. Appl. Physiol. Nutr. Metab. 2017, 42, 377–383. [Google Scholar] [CrossRef] [Green Version]
- Olszewska, M. Separation of quercetin, sexangularetin, kaempferol and isorhamnetin for simultaneous HPLC determination of flavonoid aglycones in inflorescences, leaves and fruits of three Sorbus species. J. Pharm. Biomed. Anal. 2008, 48, 629–635. [Google Scholar] [CrossRef] [PubMed]
- Olszewska, M.A.; Michel, P. Antioxidant activity of inflorescences, leaves and fruits of three sorbus species in relation to their polyphenolic composition. Nat. Prod. Res. 2009, 23, 1507–1521. [Google Scholar] [CrossRef] [PubMed]
- Olszewska, M.A. Flavonoid profile of Sorbus intermedia. Chem. Nat. Compd. 2009, 45, 722–724. [Google Scholar] [CrossRef]
- Battey, N.H. February—Constructing a corymb. J. Exp. Bot. 2003, 54, 605–608. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olszewska, M.A.; Kolodziejczyk-Czepas, J.; Rutkowska, M.; Magiera, A.; Michel, P.; Rejman, M.W.; Nowak, P.; Owczarek, A. The Effect of Standardised Flower Extracts of Sorbus aucuparia L. on Proinflammatory Enzymes, Multiple Oxidants, and Oxidative/Nitrative Damage of Human Plasma Components In Vitro. Oxid. Med. Cell Longev. 2019, 2019, 9746358. [Google Scholar] [CrossRef] [Green Version]
- Olszewska, M.A. New validated high-performance liquid chromatographic method for simultaneous analysis of ten flavonoid aglycones in plant extracts using a C18 fused-core column and acetonitrile-tetrahydrofuran gradient. J. Sep. Sci. 2012, 35, 2174–2183. [Google Scholar] [CrossRef]
- Olszewska, M.A.; Presler, A.; Michel, P. Profiling of phenolic compounds and antioxidant activity of dry extracts from the selected Sorbus species. Molecules 2012, 17, 3093–3113. [Google Scholar] [CrossRef]
- Olszewska, M.A.; Nowak, S.; Michel, P.; Banaszczak, P.; Kicel, A. Assessment of the content of phenolics and antioxidant action of inflorescences and leaves of selected species from the genus sorbus sensu stricto. Molecules 2010, 15, 8769–8783. [Google Scholar] [CrossRef] [Green Version]
- Mikulic-Petkovsek, M.; Krska, B.; Kiprovski, B.; Veberic, R. Bioactive Components and Antioxidant Capacity of Fruits from Nine Sorbus Genotypes. J. Food Sci. 2017, 82, 647–658. [Google Scholar] [CrossRef]
- Sarv, V.; Venskutonis, P.R.; Rätsep, R.; Aluvee, A.; Kazernavičiūtė, R.; Bhat, R. Antioxidants Characterization of the Fruit, Juice, and Pomace of Sweet Rowanberry (Sorbus aucuparia L.) Cultivated in Estonia. Antioxidants 2021, 10, 1779. [Google Scholar] [CrossRef]
- Rana, A.; Samtiya, M.; Dhewa, T.; Mishra, V.; Aluko, R.E. Health benefits of polyphenols: A concise review. J. Food Biochem. 2022, 46, e14264. [Google Scholar] [CrossRef] [PubMed]
- Olszewska, M.A.; Gędas, A.; Simões, M. Antimicrobial polyphenol-rich extracts: Applications and limitations in the food industry. Food Res. Int. 2020, 134, 109214. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.A.; Keogh, J.B.; Clifton, P.M. Polyphenols and Glycemic Control. Nutr. 2016, 8, 17. [Google Scholar] [CrossRef] [PubMed]
- Bailie, A.; Renaut, S.; Ubalijoro, E.; Guerrero-Analco, J.A.; Saleem, A.; Haddad, P.; Arnason, J.T.; Johns, T.; Cuerrier, A. Phytogeographic and genetic variation in Sorbus, a traditional antidiabetic medicine-adaptation in action in both a plant and a discipline. Peer J. 2016, 4, e2645. [Google Scholar] [CrossRef] [Green Version]
- Termentzi, A.; Alexiou, P.; Demopoulos, V.; Kokkalou, E. The aldose reductase inhibitory capacity of Sorbus domestica fruit extracts depends on their phenolic content and may be useful for the control of diabetic complications. Pharmazie 2008, 63, 693–696. [Google Scholar]
- Gaivelyte, K.; Jakstas, V.; Razukas, A.; Janulis, V. Variation in the Contents of Neochlorogenic Acid, Chlorogenic Acid and Three Quercetin Glycosides in Leaves and Fruits of Rowan (Sorbus) Species and Varieties from Collections in Lithuania. Nat. Pro. Commun. 2013, 8, 1105–1110. [Google Scholar] [CrossRef] [Green Version]
- Raudonis, R.; Raudone, L.; Gaivelyte, K.; Viškelis, P.; Janulis, V. Phenolic and antioxidant profiles of rowan (Sorbus L.) fruits. Nat. Prod. Res. 2014, 28, 1231–1240. [Google Scholar] [CrossRef]
- Raudone, L.; Raudonis, R.; Gaivelyte, K.; Pukalskas, A.; Viškelis, P.; Venskutonis, P.R.; Janulis, V. Phytochemical and antioxidant profiles of leaves from different Sorbus L. species. Nat. Prod. Res. 2015, 29, 281–285. [Google Scholar] [CrossRef]
- Gaivelyte, K.; Jakstas, V.; Razukas, A.; Janulis, V. Variation of quantitative composition of phenolic compounds in rowan (Sorbus aucuparia L.) leaves during the growth season. Nat. Prod. Res. 2014, 28, 1018–1020. [Google Scholar] [CrossRef]
- Coman, V.; Vodnar, D.C. Hydroxycinnamic acids and human health: Recent advances. J. Sci. Food Agric. 2020, 100, 483–499. [Google Scholar] [CrossRef]
- Hussein, R.M.; Sawy, D.M.; Kandeil, M.A.; Farghaly, H.S. Chlorogenic acid, quercetin, coenzyme Q10 and si-lymarin modulate Keap1-Nrf2/heme oxygenase-1 signaling in thioacetamide-induced acute liver toxicity. Life Sci. 2021, 277, 119460. [Google Scholar] [CrossRef] [PubMed]
- Gray, N.E.; Alcazar Magana, A.; Lak, P.; Wright, K.M.; Quinn, J.; Stevens, J.F.; Maier, C.S.; Soumayanath, A. Centella asiatica: Phytochemistry and mechanisms of neuroprotection and cognitive enhancement. Phytochem. Rev. 2018, 7, 161–194. [Google Scholar] [CrossRef] [PubMed]
- Santana-Gálvez, J.; Cisneros-Zevallos, L.; Jacobo-Velázquez, D.A. Chorogenic acid: Recent advances on its dual role as a food additive and a nutraceutical against metabolic syndrome. Molecules 2017, 22, 358. [Google Scholar] [CrossRef] [PubMed]
- Khan, F.; Bamunuarachchi, N.I.; Tabassum, N.; Kim, Y.M. Caffeic Acid and Its Derivatives: Antimicrobial Drugs toward Micro-bial Pathogens. J. Agric. Food Chem. 2021, 69, 2979–3004. [Google Scholar] [CrossRef]
- Stevanato, R.; Bertelle, M.; Fabris, S. Photoprotective characteristics of natural antioxidant polyphenols. Regul. Toxicol. Phar-macol. 2014, 69, 71–77. [Google Scholar] [CrossRef]
- Kylli, P.; Nohynek, L.; Puupponen-Pimiä, R.; Westerlund-Wikström, B.; McDougall, G.; Stewart, D.; Heinonen, M. Rowanberry phenolics: Compositional analysis and bioactivities. J. Agric. Food Chem. 2010, 58, 11985–11992. [Google Scholar] [CrossRef]
- Ferenczyova, K.; Kalocayova, B.; Bartekova, M. Potential implications of quercetin and its derivatives in cardioprotection. Int. J. Mol. Sci. 2020, 21, 1585. [Google Scholar] [CrossRef] [Green Version]
- Tahir, M.S.; Almezgagi, M.; Zhang, Y.; Bashir, A.; Abdullah, H.M.; Gamah, M.; Wang, V.; Zhu, Q.; Shen, X.; Ma, Q.; et al. Mechanistic new insights of flavonols on neurodegenerative diseases. Biomed. Pharmacother 2021, 137, 111253. [Google Scholar] [CrossRef]
- Wang, H.; Chen, L.; Zhang, X.; Xu, L.; Xie, B.; Shi, H.; Duan, Z.; Zhang, H.; Ren, F. Kaempferol protects mice from d-GalN/LPS-induced acute liver failure by regulating the ER stress-Grp78-CHOP signaling pathway. Biomed. Pharm. 2019, 111, 468–475. [Google Scholar] [CrossRef]
- Kubina, R.; Iriti, M.; Kabała-Dzik, A. Anticancer potential of selected flavonols: Fisetin, kaempferol, and quercetin on head and neck cancers. Nutrients 2021, 13, 845. [Google Scholar] [CrossRef]
- Chandra, H.; Bishnoi, P.; Yadav, A.; Patni, B.; Mishra, A.P.; Nautiyal, A.R. Antimicrobial resistance and the alternative resources with special emphasis on plant-based antimicrobials—A review. Plants 2017, 6, 16. [Google Scholar] [CrossRef]
- Lesjak, M.; Beara, I.; Simin, N.; Pintać, D.; Majkić, T.; Bekvalac, K.; Orcic, D.; Mimica-Dukić, N. Antioxidant and anti-inflammatory activities of quercetin and its derivatives. JFF 2018, 40, 68–75. [Google Scholar] [CrossRef]
- Stochmal, A.; Rolnik, A.; Skalski, B.; Zuchowski, J.; Olas, B. Antiplatelet and Anticoagulant Activity of Isorhamnetin and Its Derivatives Isolated from Sea Buckthorn Berries, Measured in Whole Blood. Molecules 2022, 27, 4429. [Google Scholar] [CrossRef] [PubMed]
- Olszewska, M.A.; Michel, P. Activity-guided isolation and identification of free radical-scavenging components from various leaf extracts of Sorbus aria (L.) Crantz. Nat. Prod. Res. 2012, 26, 243–254. [Google Scholar] [CrossRef] [PubMed]
- Walle, T. Methoxylated flavones, a superior cancer chemopreventive flavonoid subclass? Semin. Cancer Biol. 2007, 17, 354–362. [Google Scholar] [CrossRef] [Green Version]
- Marțiș, G.S.; Mureșan, V.; Marc, R.M.; Mureșan, C.C.; Pop, C.R.; Buzgău, G.; Mureșan, A.E.; Ungur, R.A.; Muste, S. The Physicochemical and Antioxidant Properties of Sambucus nigra L. and Sambucus nigra Haschberg during Growth Phases: From Buds to Ripening. Antioxidants 2021, 10, 1093. [Google Scholar] [CrossRef]
- Marksa, M.; Zymone, K.; Ivanauskas, L.; Radušienė, J.; Pukalskas, A.; Raudone, L. Antioxidant profiles of leaves and inflorescences of native, invasive and hybrid Solidago species. Ind. Crop. Prod. 2020, 145, 112123. [Google Scholar] [CrossRef]
- Shikov, A.N.; Tsitsilin, A.N.; Pozharitskaya, O.N.; Makarov, V.G.; Heinrich, M. Traditional and Current Food Use of Wild Plants Listed in the Russian Pharmacopoeia. Front. Pharmacol. 2017, 8, 841. [Google Scholar] [CrossRef]
- Tsioutsiou, E.E.; Giordani, P.; Hanlidou, E.; Biagi, M.; De Feo, V.; Cornara, L. Ethnobotanical Study of Medicinal Plants Used in Central Macedonia, Greece. Evid. Based. Complement. Alternat. Med. 2019, 2019, 22. [Google Scholar] [CrossRef]
- Jennings, H.M.; Merrell, J.; Thompson, J.L.; Heinrich, M. Food or medicine? The food–medicine interface in households in Sylhet. J. Ethnopharmacol. 2015, 167, 97–104. [Google Scholar] [CrossRef] [PubMed]
Figure 1.
Dendrogram of hierarchical cluster analysis of Sorbus inflorescence samples according to the phytochemical composition and heatmap of the percentage compositions of identified phenolic compounds: 1—neochlorogenic acid; 2—chlorogenic acid; 3—cryptochlorogenic acid; 4—caffeoylshikimic acid; 5—quercetin dihexoside 1; 6—quercetin dihexoside 2; 7—quercetin pentose hexoside; 8—quercetin dihexoside 3; 9—rutin; 10—hyperoside; 11—isoquercitrin; 12—kaempferol coumaroyl glucoside; 13—quercetin 3-O-malonylglucoside; 14—isorhamnetin rutinoside; 15—astragalin; 16—dicaffeoylquinic acid derivative 1; 17—sexangularetin derivative; 18—dicaffeoylquinic acid derivative 2; 19—kaempferol acetyl hexoside; 20—dicaffeoylquinic acid derivative 3; 21—isorhamnetin acetyl hexoside.
Figure 1.
Dendrogram of hierarchical cluster analysis of Sorbus inflorescence samples according to the phytochemical composition and heatmap of the percentage compositions of identified phenolic compounds: 1—neochlorogenic acid; 2—chlorogenic acid; 3—cryptochlorogenic acid; 4—caffeoylshikimic acid; 5—quercetin dihexoside 1; 6—quercetin dihexoside 2; 7—quercetin pentose hexoside; 8—quercetin dihexoside 3; 9—rutin; 10—hyperoside; 11—isoquercitrin; 12—kaempferol coumaroyl glucoside; 13—quercetin 3-O-malonylglucoside; 14—isorhamnetin rutinoside; 15—astragalin; 16—dicaffeoylquinic acid derivative 1; 17—sexangularetin derivative; 18—dicaffeoylquinic acid derivative 2; 19—kaempferol acetyl hexoside; 20—dicaffeoylquinic acid derivative 3; 21—isorhamnetin acetyl hexoside.
Figure 2.
PCA loading plots (A,B) and score plots (C,D) for different Sorbus inflorescence samples. 1—S. amurensis; 2—S. aria; 3—S. arranensis; 4—S. commixta; 5—S. discolor; 6—S. x hostii; 7—S. hybrida subsp. Gotlandica; 8—S. hybrida subsp. Persecta; 9—S. lancifolia; 10—S. semi-incisa; 11—‘Alaja Krupnaja’; 12—‘Carpet of Gold’; 13—‘Chamsis Louing’; 14—‘Coral Beauty’; 15 –’Edulis’; 16—‘Granatnaja’; 17—‘Koncentra’; 18—‘Krasnaja Nevezisnskaja’; 19—‘Miciurinskaja Desertnaja’; 20—‘Nevezinskaja’; 21—‘Nevezinskaja Zolotistaja’; 22—‘Nevezinskaja Zoltaja’; 23—‘Oranzevaja’; 24—‘Pink Queen’; 25—‘Titan’; 26—‘Yellow Upright’.
Figure 2.
PCA loading plots (A,B) and score plots (C,D) for different Sorbus inflorescence samples. 1—S. amurensis; 2—S. aria; 3—S. arranensis; 4—S. commixta; 5—S. discolor; 6—S. x hostii; 7—S. hybrida subsp. Gotlandica; 8—S. hybrida subsp. Persecta; 9—S. lancifolia; 10—S. semi-incisa; 11—‘Alaja Krupnaja’; 12—‘Carpet of Gold’; 13—‘Chamsis Louing’; 14—‘Coral Beauty’; 15 –’Edulis’; 16—‘Granatnaja’; 17—‘Koncentra’; 18—‘Krasnaja Nevezisnskaja’; 19—‘Miciurinskaja Desertnaja’; 20—‘Nevezinskaja’; 21—‘Nevezinskaja Zolotistaja’; 22—‘Nevezinskaja Zoltaja’; 23—‘Oranzevaja’; 24—‘Pink Queen’; 25—‘Titan’; 26—‘Yellow Upright’.
Table 1.
Concentrations of phenolic acids (µg/g DW) in Sorbus inflorescences.
| Species/Cultivars | Compound | ||||||
|---|---|---|---|---|---|---|---|
| Neochlorogenic Acid | Chlorogenic Acid | Cryptochlorogenic Acid | Caffeoylshikimic Acid | Dicaffeoylquinic Acid Derivative 1 | Dicaffeoylquinic Acid Derivative 2 | Dicaffeoylquinic Acid Derivative 3 | |
| S. amurensis | 1701 ± 44 ab 1 | 2973 ± 147 ab | 463 ± 17 b | 131 ± 2 b | 721 ± 42 a | 72 ± 1 a | nd 2 |
| S. aria | 432 ± 96 ijk | 691 ± 126 kl | 81 ± 10 cd | nd | 285 ± 39 jkl | 58 ± 0 g | 113 ± 16 a |
| S. arranensis | 1397 ± 28 bc | 1161 ± 22 ijkl | 120 ± 2 c | nd | 606 ± 0 abcd | 73 ± 1 a | 120 ± 4 a |
| S. commixta | 95 ± 12 k | 3154 ± 250 a | 721 ± 86 a | 126 ± 7 bc | 401 ± 40 fghijk | 67 ± 2 abcdef | nd |
| S. discolor | 1118 ± 15 cde | 1167 ± 60 ijkl | 55 ± 0 cd | 74 ± 1 fg | 312 ± 1 ijkl | 67 ± 0 abcdef | nd |
| S. x hostii | 307 ± 1 jk | 632 ± 32l | 47 ± 1 d | 57 ± 0 gh | 298 ± 18 ijkl | 60 ± 1 fg | 65 ± 1 c |
| S. hybrida subsp. Gotlandica | 661 ± 43 ghij | 1060 ± 70 jkl | 37 ± 1 d | 65 ± 2 fgh | 612 ± 65 abc | 69 ± 3 abcd | nd |
| S. hybrida subsp. Persecta | 1040 ± 4 cdef | 1305 ± 42 ghijkl | 63 ± 3 cd | 76 ± 1 f | 598 ± 12 abcde | 69 ± 1 abcde | 73 ± 3 c |
| S. lancifolia | 1313 ± 41 cd | 1260 ± 143 hijkl | 59 ± 1 cd | 68 ± 2 fgh | 679 ± 95 a | 69 ± 2 abc | nd |
| S. semi-incisa | 464 ± 12 hij | 1068 ± 41 jkl | 66 ± 5 cd | 56 ± 0 h | 487 ± 9 bcdefgh | 73 ± 0 a | 69 ± 0c |
| ‘Alaja Krupnaja’ | 819 ± 6 efgh | 1340 ± 68 ghijkl | 45 ± 4 d | 77 ± 1 f | 187 ± 15 l | 60 ± 1 fg | nd |
| ‘Carpet of Gold’ | 1774 ± 244 a | 1793 ± 293 defghij | 96 ± 15 | 127 ± 9 bc | 467 ± 48 cdefghi | 70 ± 1 abc | nd |
| ‘Chamsis Louing’ | 1042 ± 67 cedf | 2587 ± 156 abc | 59 ± 0 cd | 111 ± 5 cd | 590 ± 42 abcde | 71 ± 2 ab | nd |
| ‘Coral Beauty’ | 1871 ± 174 a | 2406 ± 144 cd | 95 ± 0 cd | 157 ± 6 a | 567 ± 49 abcdef | 71 ± 2 ab | 72 ± 1 |
| ‘Edulis’ | 979 ± 139 defg | 1407 ± 207 fghijk | 56 ± 8 cd | 66 ± 4 fgh | 651 ± 88 ab | 65 ± 7 abcdefg | 96 ± 4b |
| ‘Granatnaja’ | 1134 ± 30 cde | 1959 ± 34 cdefgh | 59 ± 0 cd | 78 ± 0 f | 212 ± 2 l | 61 ± 0 fg | nd |
| ‘Koncentra’ | 688 ± 23 fghi | 1663 ± 41 efghij | 42 ± 0 d | 71 ± 1 fgh | 247 ± 3 kl | 61 ± 1 defg | nd |
| ‘Krasnaja Nevezisnskaja’ | 808 ± 104 efgh | 1838 ± 266 defhgi | 46 ± 4 d | 74 ± 4 fg | 264 ± 42 jkl | 63 ± 1 cdefg | nd |
| ‘Miciurinskaja Desertnaja’ | 1094 ± 8 cde | 2038 ± 103 cdefg | 52 ± 1 cd | 82 ± 0 ef | 192 ± 8 l | 60 ± 1 fg | nd |
| ‘Nevezinskaja’ | 921 ± 63 efg | 1994 ± 169 cdefgh | 56 ± 4 cd | 82 ± 2 ef | 331 ± 34 ghijkl | 66 ± 2 abcdef | nd |
| ‘Nevezinskaja Zolotistaja’ | 899 ± 132 efg | 1973 ± 218 cdefgh | 51 ± 2 cd | 76 ± 4 f | 296 ± 24 ijkl | 64 ± 0 bcdefg | nd |
| ‘Nevezinskaja Zoltaja’ | 955 ± 25 efg | 2195 ± 50 cde | 49 ± 1 cd | 77 ± 0 f | 317 ± 3 hijkl | 66 ± 1 abcdef | nd |
| ‘Oranzevaja’ | 661 ± 44 ghij | 1496 ± 147 efghij | 42 ± 3 d | 70 ± 2 fgh | 226 ± 7 l | 62 ± 1 defg | nd |
| ‘Pink Queen’ | 1040 ± 44 cdef | 1896 ± 212 cdefghi | 50 ± 4 cd | 104 ± 1 d | 498 ± 36 bcdefg | 70 ± 2 abc | nd |
| ‘Titan’ | 950 ± 112 efg | 1957 ± 232 cdefgh | 61 ± 10 cd | 82 ± 3 ef | 222 ± 12l | 61 ± 0 efg | nd |
| ‘Yellow Upright’ | 889 ± 99 efg | 2094 ± 358 cdef | 43 ± 4 d | 112 ± 11 cd | 433 ± 65 defghij | 62 ± 1 defg | nd |
1 Averages marked in different letters in the columns show statistically significant difference (at p < 0.05); 2 nd—not detected.
Table 2.
Concentrations of quercetin derivatives (µg/g DW) in Sorbus inflorescences.
| Species/Cultivars | Compounds | |||||||
|---|---|---|---|---|---|---|---|---|
| Quercetin Dihexoside 1 | Quercetin Dihexoside 2 | Quercetin Pentose Hexoside | Quercetin Dihexoside 3 | Rutin | Hyperoside | Isoquercitrin | Quercetin 3-O-Malonylglucoside | |
| S. amurensis | 437 ± 12 a 1 | 112 ± 6 fg | nd | nd | 54 ± 2 p | 567 ± 11 a | 399 ± 15 fg | 50 ± 8 i |
| S. aria | nd2 | nd | nd | 6 ± 0 j | 105 ± 7 no | nd | 88 ± 6 l | 223 ± 18 fg |
| S. arranensis | 23 ± 1 kl | 11 ± 0 pr | nd | 75 ± 1 de | 242 ± 2 gh | 64 ± 1 lmn | 25 ndhi | 994 ± 5 b |
| S. commixta | nd | nd | nd | 46 ± 1 fgh | 44 ± 1 p | 336 ± 21 b | 389 ± 23 g | 65 ± 1 hi |
| S. discolor | 261 ± 8 b | 124 ± 5 ef | nd | 154 ± 8 a | 439 ± 19 a | 261 ± 5 c | 356 ± 2 g | 108 ± 1 fghi |
| S. x hostii | 25 ± 1 kl | 24 ± 0 op | 20 ± 1c | 23 ± 0 i | 94 ± 3 op | 63 ± 1 lmn | 256 ± 6 hi | 210 ± 3 fgh |
| Subsp. Gotlandica | 23 ± 1 kl | 63 ± 2 k | nd | 23 ± 0 i | 204 ± 2 hij | 24 ± 0 no | 205 ± 1 ijk | 442 ± 3 d |
| Subsp. Persecta | 25 ± 1 kl | 65 ± 1 jk | nd | 39 ± 2 h | 379 ± 8 b | 33 ± 1 mno | 349 ± 3 g | 970 ± 12 b |
| S. lancifolia | 59 ± 3 j | 29 ± 2 no | nd | 62 ± 4 ef | 126 ± 12 mno | 125 ± 9 ghij | 199 ± 21 ijk | 604 ± 70 c |
| S. semi-incisa | nd | nd | nd | 50 ± 1 fgh | 290 ± 10 | 66 ± 3 lm | 122 ± 3 kl | 262 ± 17 ef |
| ‘Alaja Krupnaja’ | 47± 2 jk | 101 ± 1 gh | nd | 78 ± 1 d | 465 ± 2 a | 97 ± 2 ijkl | 713 ± 12 b | 133 ± 0 fghi |
| ‘Carpet of Gold’ | 113 ± 10 g | 82 ± 4 ij | nd | 42 ± 1 gh | 292 ± 16 def | 72 ± 5 klm | 173 ± 10 ijkl | 385 ± 14 de |
| ‘Chamsis Louing’ | 111 ± 3 gh | 30 ± 1 no | nd | 88 ± 0 cd | 213 ± 1 hij | 151 ± 0 efg | 179 ± 4 ijkl | 851 ± 35 b |
| ‘Coral Beauty’ | 124 ± 1 fg | 42 ± 1 lmn | nd | 49 ± 1 fgh | 176 ± 0 ijkl | 124 ± 1 ghij | 159 ± 0 jkl | 400 ± 1 de |
| ‘Edulis’ | 61 ± 4 j | 49 ± 2 klm | nd | 22 ± 0 i | 164 ± 11 jklm | 257 ± 21 c | 874 ± 48 a | 1670 ± 115 a |
| ‘Granatnaja’ | 118 ± 1 g | 126 ± 3 ef | 90 ± 3 a | 153 ± 5 a | 357 ± 9 b | 182 ± 8 def | 526 ± 15 de | 94 ± 8 ghi |
| ‘Koncentra’ | 166 ± 5 de | 160 ± 4 bc | nd | 58 ± 1 fg | 185 ± 6 ijkl | 172 ± 2 def | 512 ± 2 de | 97 ± 0 ghi |
| ‘Krasnaja Nevezisnskaja’ | 181 ± 17 d | 170 ± 15 b | nd | 50 ± 7 fgh | 152 ± 15 klmn | 207 ± 17 d | 593 ± 60 cd | 113 ± 8 fghi |
| ‘Miciurinskaja Desertnaja’ | 123 ± 1 fg | 120 ± 1 ef | 90 ± 1 a | 141 ± 3 a | 306 ± 5 cde | 182 ± 6 de | 480 ± 9 ef | 85 ± 3 ghi |
| ‘Nevezinskaja’ | 131 ± 3 fg | 138 ± 2 de | nd | 51 ± 0 fgh | 192 ± 10 ijk | 129 ± 2 ghi | 494 ± 11 e | 96 ± 7 ghi |
| ‘Nevezinskaja Zolotistaja’ | 168 ± 11 de | 152 ± 12 bcd | nd | 60 ± 7 ef | 173 ± 18 ijklm | 200 ± 19 d | 559 ± 51 de | 94 ± 11 ghi |
| ‘Nevezinskaja Zoltaja’ | 216 ± 2 c | 202 ± 3 a | nd | 75 ± 5 de | 222 ± 17 hi | 254 ± 12 c | 654 ± 33 bc | 130 ± 1 fghi |
| ‘Oranzevaja’ | 144 ± 5 ef | 150 ± 1 cd | nd | 59 ± 2 f | 206 ± 12 hij | 141 ± 7 fgh | 520 ± 21 de | 82 ± 0 ghi |
| ‘Pink Queen’ | 120 ± 7 fg | 38 ± 1 lmno | nd | 113 ± 10 b | 341 ± 27 bcd | 206 ± 19 d | 204 ± 17 ijk | 531 ± 66 cd |
| ‘Titan’ | 87 ± 6 hi | 89 ± 5 hi | 51 ± 2 b | 96 ± 7 c | 249 ± 19 fgh | 109 ± 10 hijk | 328 ± 23 gh | 85 ± 8 ghi |
| ‘Yellow Upright’ | 70 ± 11 ij | 31 ± 4 mno | nd | nd | 139 ± 15 lmno | 88 ± 10 jkl | 151 ± 16 jkl | 866 ± 111 b |
1 Averages marked in different letters in the columns show statistically significant difference (at p < 0.05); 2 nd—not detected.
Table 3.
Concentrations of derivatives of the other flavonoids (µg/g DW) in Sorbus inflorescences.
| Species/Cultivars | Compounds | |||||
|---|---|---|---|---|---|---|
| Kaempferol Coumaroyl Glucoside | Isorhamnetin Rutinoside | Astragalin | Sexangularetin Derivative | Kaempferol Acetyl Hexoside | Isorhamnetin Acetyl Hexoside | |
| S. amurensis | 40 ± 9 fghi 1 | 23 ± 6 gh | 44 ± 3 de | 148 ± 20 bc | 14 ± 1 i | nd 2 |
| S. aria | 14 ± 1 jk | 48 ± 7 defg | 13 ± 1 j | 19 ± 2 k | 28 ± 0 hi | 74 ± 6 e |
| S. arranensis | 141 ± 0 a | 186 ± 3 a | 15 ± 0 hij | 135 ± 7 bcd | 238 ± 7 a | 421 ± 1 a |
| S. commixta | 19 ± 0 jk | 25 ± 1 gh | 185 ± 1 a | 123 ± 10 cde | 159 ± 19 bc | nd |
| S. discolor | 107 ± 0 c | 41 ± 7 efgh | 73 ± 2 c | 199 ± 11 a | 45 ± 2 gh | nd |
| S. x hostii | 48 ± 2 efgh | 59 ± 1 cdef | 25 ± 2 g | 44 ± 6 hijk | 67 ± 5 fg | 83 ± 1 |
| Subsp. Gotlandica | 75 ± 1 d | 112 ± 1 b | 35 ± 3 f | 32 ± 2 ijk | 133 ± 4 cd | 183 ± 1 c |
| Subsp. Persecta | 51 ± 5 efg | 66 ± 3 cde | 24 ± 3 gh | 24 ± 1 jk | 90 ± 7 ef | 139 ± 1 d |
| S. lancifolia | 117 ± 22 c | 111 ± 19 b | nd | 54 ± 13 ghi | 125 ± 19 d | 262 ± 24 b |
| S. semi-incisa | 120 ± 4 bc | 198 ± 3 a | 14 ± 1 ij | 32 ± 1 ijk | 133 ± 1 cd | 123 ± 0 d |
| ‘Alaja Krupnaja’ | 76 ± 1 d | 76 ± 3 cd | 53 ± 0 d | 76 ± 4 fg | 17 ± 1 i | 22 ± 1 f |
| ‘Carpet of Gold’ | 101 ± 3 c | 74 ± 13 cd | 77 ± 4 bc | 32 ± 0 ijk | 111 ± 1 de | nd |
| ‘Chamsis Louing’ | nd | 207 ± 19 a | nd | 10 ndef | 19 ± 0 hi | nd |
| ‘Coral Beauty’ | 29 ± 2 hij | 81 ± 4 bc | 19 ± 0 ghij | 41 ± 2 hijk | 78 ± 1 f | nd |
| ‘Edulis’ | nd | 109 ± 16 b | 46 ± 5 de | 147 ± 4 bc | 79 ± 2 f | 254 ± 23 b |
| ‘Granatnaja’ | 63 ± 1 de | 38 ± 1 efgh | 23 ± 2 ghi | 76 ± 3 fg | 17 ± 2 i | nd |
| ‘Koncentra’ | 31 ± 2 ghij | 17 ± 4 gh | 51 ± 1 de | 69 ± 2 gh | 18 ± 1 i | nd |
| ‘Krasnaja Nevezisnskaja’ | 27 ± 2 hij | 22 ± 1 gh | 51 ± 2 de | 111 ± 8 de | 21 ± 1 hi | nd |
| ‘Miciurinskaja Desertnaja’ | 54 ± 0 ef | 35 ± 3 efgh | 21 ± 1 ghij | 61 ± 1 ghi | 13 ± 2 i | nd |
| ‘Nevezinskaja’ | 26 ± 0 ij | 2 ndgh | 43 ± 3 ef | 125 ± 12 cde | 17 ± 0 i | nd |
| ‘Nevezinskaja Zolotistaja’ | 23 ± 4 ij | 22 ± 1 gh | 45 ± 3 de | 118 ± 5 cde | 19 ± 1 hi | nd |
| ‘Nevezinskaja Zoltaja’ | 30 ± 1 hij | 35 ± 5 efgh | 48 ± 1 de | 165 ± 5 a | 21 ± 1 hi | nd |
| ‘Oranzevaja’ | 32 ± 1 ghij | 13 ± 1 h | 53 ± 0 d | 100 ± 5 ef | 19 ± 1 hi | nd |
| ‘Pink Queen’ | nd | 190 ± 14 a | nd | 74 ± 9 fg | 17 ± 1 i | nd |
| ‘Titan’ | 47 ± 4 efgh | 28 ± 3 fgh | 23 ± 2 ghi | 77 ± 2 fg | 28 ± 2 hi | nd |
| ‘Yellow Upright’ | 19 ± 1 ijk | 113 ± 6 b | 24 ± 3 gh | 69 ± 9 gh | 136 ± 16 cd | nd |
1 Averages marked in different letters in the columns show statistically significant difference (at p < 0.05); 2 nd—not detected.
Table 4.
Sorbus L. species and cultivars.
| Species and Cultivars | ||
|---|---|---|
| 1 | S. amurensis | Sorbus aucuparia subsp. pohuashanensis |
| 2 | S. aria | sect. Aria Pers. |
| 3 | S. arranensis | sect. Sorbus/sect. Aria. |
| 4 | S. commixta | sect. Sorbus |
| 5 | S. discolor | Sorbus subg. Albocarmesinae |
| 6 | S. x hostii | S. chamaemespilus (L.Crantz. × S. mougeotii Soy.—Willem ex Godr.) |
| 7 | S. hybrida subsp. gotlandica | sect. Sorbus/sect. Aria. (S. aucuparia × S. rupicola) |
| 8 | S. hybrida subsp. persecta | sect. Sorbus/sect. Aria. (S. aucuparia × S. rupicola) |
| 9 | S. lancifolia | sect. Sorbus |
| 10 | S. semi-incisa | sect. Sorbus |
| 11 | ‘Alaja Krupnaja’ | Cultivar of the group Rossica Major. S. aucuparia × Pyrus sp. × S. aucuparia var. moravica |
| 12 | ‘Carpet of Gold’ | Sorbus × arnoldiana [Sorbus aucuparia × Sorbus discolor] |
| 13 | ‘Chamsis Louing’ | Sorbus × arnoldiana [Sorbus aucuparia × Sorbus discolor] |
| 14 | ‘Coral Beauty’ | Sorbus × arnoldiana [Sorbus aucuparia × Sorbus discolor] |
| 15 | ‘Edulis’ | Cultivar of the group Edulis S. aucuparia var. dulcis, S. aucuparia var. edulis |
| 16 | ‘Granatnaja’ | Cultivar of the group Rossica Major (S. aucuparia × Crataegus sanguinea Pall.) |
| 17 | ‘Koncentra’ | Cultivar of the group Edulis |
| 18 | ‘Krasnaja Nevezinskaja’ | Cultivar of the group Rossica |
| 19 | ‘Miciurinskaja Desertnaja’ | Cultivar of the group Rossica Major ([S. aucuparia × Aronia melanocarpa (Michx.) Elliott.] × Mespilus germanica L.) |
| 20 | ‘Nevezinskaja’ | Cultivar of the group Rossica |
| 21 | ‘Nevezinskaja Zolotistaja’ | Cultivar of the group Rossica |
| 22 | ‘Nevezinskaja Zoltaja’ | Cultivar of the group Rossica |
| 23 | ‘Oranzevaja’ | Cultivar of the group Rossica |
| 24 | ‘Pink Queen’ | Sorbus × arnoldiana [Sorbus aucuparia × Sorbus discolor] |
| 25 | ‘Titan’ | Cultivar of the group Rossica Major (S. aucuparia × Sorbaronia alpina (S. aria × Aronia arbutifolia) × mixture of pollen from Malus sp. and Pyrus sp. |
| 26 | ‘Yellow Upright’ | Sorbus × arnoldiana [Sorbus aucuparia × Sorbus discolor] |
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Zymone, K.; Raudone, L.; Žvikas, V.; Jakštas, V.; Janulis, V. Phytoprofiling of Sorbus L. Inflorescences: A Valuable and Promising Resource for Phenolics. Plants 2022, 11, 3421. https://doi.org/10.3390/plants11243421
AMA Style
Zymone K, Raudone L, Žvikas V, Jakštas V, Janulis V. Phytoprofiling of Sorbus L. Inflorescences: A Valuable and Promising Resource for Phenolics. Plants. 2022; 11(24):3421. https://doi.org/10.3390/plants11243421
Chicago/Turabian StyleZymone, Kristina, Lina Raudone, Vaidotas Žvikas, Valdas Jakštas, and Valdimaras Janulis. 2022. "Phytoprofiling of Sorbus L. Inflorescences: A Valuable and Promising Resource for Phenolics" Plants 11, no. 24: 3421. https://doi.org/10.3390/plants11243421
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