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Comparative analysis of the metabolites in Pinellia ternata from two producing regions using ultra-high-performance liquid chromatography–electrospray ionization–tandem mass spectrometry

  • Shipeng Li , Ye Chen , Xianghui Liu , Congjing Zhao and Huiyuan Ya EMAIL logo
Published/Copyright: February 15, 2023
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Open Chemistry
From the journal Open Chemistry Volume 21 Issue 1

Abstract

The rhizomes of Pinellia ternata have a long history of being used as a traditional Chinese herb. To determine the chemical constituents of Pinelliae rhizome, Xi banxia and Jing banxia were collected from two different producing regions and subjected to analysis using ultra-high-performance liquid chromatography–electrospray ionization–tandem mass spectrometry. A total of 573 metabolites were identified in 12 different categories. Next, cluster analysis and principal component analysis were performed, which revealed a distinct separation between the two species. The analysis of the differential metabolites revealed that among the 155 metabolites in Xi banxia, 68 metabolites were upregulated, and 87 metabolites were downregulated. The relative concentration of flavonoids in Xi banxia was higher than that in Jing banxia, while the relative concentrations of alkaloids, phenolic acids, and terpenoids were higher in Jing banxia. These results would provide a theoretical basis for the pharmacological activity analysis and functional study of P. ternata.

Keywords: Xi banxia; Jing banxia; producing regions; primary and secondary metabolites; differential metabolites

1 Introduction

Pinellia ternata (Thunb.) Breit. is a perennial herb belonging to the Araceae family, which has great medicinal value in the form of Pinelliae rhizome (PR) [1]. P. ternata, also referred to as Banxia in China, was first documented in the “Shen Nong’s Herbal Classic” nearly 2,000 years ago. The plant matures in mid-summer and has eight species spread across the world. Several of these species are endemic to China and are distributed mainly in Sichuan, Hubei, Henan, and other provinces [2].

PR is described as pungent and bitter in taste and reportedly affects the liver, spleen, stomach, and kidney meridians. The main functions of PR include drying dampness and resolving phlegm, lowering the reversal and terminating vomiting, and dissipating swelling and stagnation [3]. In addition, PR is applied externally to reduce swelling and relieve pain [4]. Pharmacological studies have demonstrated that PR exhibits anti-fungal, anti-inflammatory, anti-oxidant, anti-coughing, sedative-hypnotic, and anti-vomiting effects. PR also inhibits the proliferation of cancer cells, exerts anti-epileptic effects, and exhibits insecticidal activity [5,6,7,8,9,10,11]. Modern pharmacological studies have revealed that PR contains a wide variety of chemical components, including alkaloids, flavonoids, organic acids, amino acids, sterols, sugars, and certain inflammatory components [12,13,14,15,16]. The study of the chemical constituents and the pharmacological functions of PR revealed that it contains 25 alkaloids, 20 organic acids, 28 amino acids, 12 flavonoids, 6 steroids and their glycosides, and 65 volatile oils [17].

Anthropological activities and environmental pollution have destroyed the habitat of wild P. ternata to a large extent, because of which the population of wild P. ternata has decreased, and its germplasm resources have been reduced [18]. Therefore, it is imperative to pay further attention to wild P. ternata and protect its existing germplasm resources. Jing banxia is an authentic medicinal PR distributed in Jingmen, Hubei Province, China. According to the “Drug Production Debate,” “the quality of PR from Jingzhou, Hubei Province, is very good” in terms of excellent processing, appearance, and medicinal value [19]. Xi banxia is produced in Xi County, Henan Province, and its earliest records are from the “Xixian Chronicle,” which was documented in the fourth year of Jiaqing in the Qing Dynasty. It is stated that just 9 g of Xi banxia could be used in place of PR15 g of PR. Xi banxia is a treasure among similar kinds of medicinal materials because of its large-sized, white and pink roots and good curative effects [20]. The quality analysis of the multi-components of P. ternata is the basis for the quality evaluation of P. ternata herbs. The existing reports have focused mainly on the analysis of certain chemical components of P. ternata, while little attention has been paid to the metabolomics of wild P. ternata from different regions.

Widely targeted metabolomics, which is also referred to as next-generation metabolomics, has been applied widely to mine novel secondary metabolites, plant metabolism and the associated effective metabolic pathways and regulatory mechanisms, gene function elucidation, medicine development, etc., and accurate qualitative and quantitative results, high throughput, high sensitivity, and wide coverage have been achieved [21,22,23,24]. Although being an authentic medicinal material from Henan, Xi banxia has not been studied so far for its chemical composition, and no database of its chemical composition is available currently.

In the present study, the metabolites of Jing banxia and Xi banxia were isolated and identified using the ultra-high-performance liquid chromatography–electrospray ionization–tandem mass spectrometry (UPLC–ESI-MS/MS) analysis. To provide theoretical and data support for the chemical composition analysis, pharmacological mechanism analysis, and further application of Xi banxia, the metabolic differences between the P. ternata plants from two different producing regions were investigated based on the involved metabolic pathways.

2 Materials and methods

2.1 Plant materials

The authentic medicinal materials, Jing banxia (Pin.t) and Xi banxia (XPin.t), used in the present study, were collected from the wild P. ternata in Jingzhou, Hubei Province and Xi County, Xinyang, Henan Province, respectively. The collected samples were identified by Professor Huiyuan Ya (the School of Food and Drug, Luoyang Normal University, Luoyang, Henan Province, China). The process of sample collection involved collecting a minimum of five only fresh samples of PR, which were then randomly sampled.

2.2 Sample extraction process

Fresh Pin.t and XPin.t samples were vacuum freeze-dried in a lyophilizer (Scientz-100F) and then ground to powder using a grinder (MM 400, Retsch) at 30 Hz for 1.5 min. Afterward, 100 mg of the sample powder was dissolved in 1.2 mL of 70% methanol extraction solution, followed by vortexing once every 30 min, each time for 30 s, and six times in total. Subsequently, the sample was placed overnight in a refrigerator at 4°C. The next day, the samples were centrifuged at 12,000 rpm for 10 min, and the resulting supernatant was collected, filtered through a microporous membrane with a pore size of 0.22 µm, and then stored in a sample vial until to be used for UPLC–MS/MS analysis. Three biological replicates were analyzed independently from each group. The samples were analyzed under the following HPLC conditions: chromatographic column, TSKgel ODS-80Ts C18 (5 µm, Tosoh Co. Ltd, Japan); solvent system, water (0.04% acetic acid):acetonitrile (0.04% acetic acid); gradient program, 100:0 V/V at 0.0 min, 5:95 V/V at 11.0 min, 5:95 V/V at 12.0 min, 95:5 V/V at 12.1 min, and 95:5 V/V at 15.0 min; flow rate, 0.8 mL/min; temperature, 40°C; sample size: 2 µL. The effluent was connected alternatively to electrospray ionization (ESI)-triple quadrupole-linear ion trap (Q-TRAP) MS.

2.3 Chromatographic mass spectrometry acquisition conditions

The construction of the metabolome database was commissioned by Wuhan Metware Biotechnology Co. Ltd. The data acquisition instrument system included the UPLC equipment (SHIMADZU Nexera X2, https://www.shimadzu.com.cn/) and the Tandem mass spectrometry (MS/MS) equipment (Applied Biosystems 4500 QTRAP, http://www.appliedbiosystems.com.cn/).

The liquid conditions mainly included the following: column: Agilent SB-C18 1.8 µm, 2.1 mm × 100 mm; mobile phase: phase A – ultrapure water (containing 0.1% formic acid) and phase B – acetonitrile (containing 0.1% formic acid); elution gradient: 0.00 min – the initial proportion of phase B – 5%, the proportion of phase B increased linearly to 95% within 9.00 min and was maintained at 95% for 1 min, 10.00–11.10 min – the proportion of phase B decreased to 5% and the proportion of phase B decreased to 5%; equilibration, 14 min; flow rate, 0.35 mL/min; column temperature, 40°C; and injection volume, 4 µL.

The mass spectrometry conditions mainly included the following: the LIT and triple quadrupole (QQQ) scans were acquired using a triple Q-TRAP mass spectrometer named the AB4500 Q TRAP UPLC–MS/MS system equipped with an ESI Turbo; the ion spray interface could be controlled using the Analyst 1.6.3 software (AB Sciex) to run the positive and negative ion modes. The ESI source operating parameters were as follows: ion source, turbo spray; source temperature, 550°C; ion spray voltage (IS), 5,500 V (positive-ion mode)/−4,500 V (negative-ion mode); ion source gas I (GSI), gas II (GSII), and curtain gas (CUR) pressures were set to 50, 60, and 25.0 psi, respectively, and the collision-induced ionization parameter was set to ‘high’. Instrument tuning and mass calibration were performed using 10 µmol/L of polypropylene glycol solution in the QQQ mode and 100 µmol/L of polypropylene glycol solution in the LIT mode, respectively. The QQQ scans were performed in the MRM mode, and the collision gas (nitrogen) level was set to ‘medium’. The DP and CE were further optimized, through which the DP and CE of the individual MRM transitions were completed. A specific set of MRM transitions in each epoch were monitored based on the metabolites eluted in each epoch.

2.4 Qualitative and semi-quantitative analysis of the metabolites

The identification and the structural analysis of the primary and secondary spectral data of the metabolites detected using mass spectrometry were based on the MWDB database (Wuhan Metware Biotechnology Co. Ltd, Wuhan, China) and certain public databases, such as MassBank (http://www.massbank.jp/), KNAPSAcK (http://kanaya.naist.jp/KNApSAcK/), HMDB (http://www.hmdb.ca/), MoToDB (http://www.ab.wur.nl/moto/), ChemBank (http://chembank.med.harvard.edu/compounds), PubChem (https://pubchemblog.ncbi.nlm.nih.gov/), NIST Chemistry Webbook (http://webbook.nist.gov/), and METLIN (http://metlin.scripps.edu/index.php). The mass spectral data were processed using the Analyst 1.6.3 software.

Metabolite quantification was performed using the MRM mode of QQQ mass spectrometry. In the MRM mode, the quadrupole filtered the precursor ions of the target substance and excluded the ions corresponding to the other molecular weights to eliminate interference. After obtaining the metabolite mass spectrometric data, the integration of the peak area was performed using MultiQuant version 3.0.2 (AB SCIEX, Concord, Ontario, Canada). Finally, the chromatographic peak area was utilized to determine the relative metabolite contents.

2.5 Statistical analysis

The present study mainly involved multivariate statistical analysis. All normalized data were subjected to the principal component analysis (PCA) and the orthogonal partial least squares discriminant analysis (orthogonal partial least squares) using the Umetrics SIMCA 14.1 software. The orthogonal partial least squares discriminant analysis (OPLS-DA) was performed using R software (www.r-project.org) for the hierarchical clustering analysis of metabolites in the samples. To identify the differentially accumulated metabolites (DAM), fold change (FC) ≥2 or FC ≤0.5, and variable importance (VIP) ≥1 in the items were used as the screening criteria. The data were log transformed (log2) and mean centered prior to OPLS-DA. The VIP values and the corresponding plots were extracted from the OPLS-DA results using the R package MetaboAnalystR (https://github.com/xia-lab/MetaboAnalystR). To prevent overfitting, a permutation test (200 permutations) was performed.

The identified metabolites were annotated using the KEGG Compound database (http://www.kegg.jp/kegg/compound/), and the annotated metabolites were then mapped to the KEGG Pathway database (http://www.kegg.jp/kegg/pathway.html). The pathways to which the significantly regulated metabolites were mapped were subjected to the metabolite sets enrichment analysis, and their significance was determined based on the p-values obtained in the hypergeometric test.

3 Results and analysis

3.1 Metabolic profiling of Pin.t and XPin.t using UPLC–MS/MS

To investigate the chemical compositions of Pin.t and XPin.t, the primary and secondary metabolites were identified through a UPLC–MS/MS analysis. The identified metabolites were then analyzed quantitatively using the software Analyst under the MRM mode (Figure 1a and b). As depicted in Figure 1c, 573 metabolites under 12 different categories were detected, including 114 flavonoids, 97 amino acids and their derivatives, 72 lipids, 63 organic acids, 51 phenolic acids, 49 kinds of alkaloids, 48 nucleotides and their derivatives, 17 lignans and coumarins, 12 terpenes, 8 tannins, 1 quinone, and 41 other metabolites. Flavonoids (19.9%), amino acids and their derivatives (16.93%), lipids (12.57%), and organic acids (10.99%) were the four main metabolites identified (Table 1 and Table S1). The flavonoids could be further categorized into eight classes, among which flavonoids (41.23%), flavonols (14.91%), flavonoid carbon glycosides (14.04%), and dihydro-flavonoids (9.65%) were the main flavonoid metabolites (Figure 1d).

Figure 1 Qualitative and semi-quantitative analysis of the metabolites in Pin.t and XPin.t. The multi-peak mass spectral chromatogram of the metabolites acquired in the negative-ion mode (a) and positive-ion mode (b). (c) The types and proportions of the identified metabolites in Pin.t and XPin.t. (d) The types and proportions of flavonoids.
Figure 1

Qualitative and semi-quantitative analysis of the metabolites in Pin.t and XPin.t. The multi-peak mass spectral chromatogram of the metabolites acquired in the negative-ion mode (a) and positive-ion mode (b). (c) The types and proportions of the identified metabolites in Pin.t and XPin.t. (d) The types and proportions of flavonoids.

Table 1

Overview of the identified metabolites in Pinelliae rhizome

Primary classification Secondary classification Number of metabolites Type
Amino acids and derivatives Amino acids and derivatives 97 Primary metabolites
Nucleotides and derivatives Nucleotides and derivatives 48 Primary metabolites
Lipids Glycerol ester 6 Primary metabolites
Sphingolipids 1
LPC 22
LPE 18
Free fatty acids 25
Flavonoids Chalcones 8 Secondary metabolites
Dihydroflavone 11
Dihydroflavonol 5
Flavonoid 47
Flavonols 17
Flavonoid carbonoside 16
Flavanols 4
Isoflavones 6
Alkaloids Sesquiterpene alkaloids 1 Secondary metabolites
Phenolamine 11
Alkaloids 30
Plumerane 6
Steroid alkaloids 1
Phenolic acids 51 Secondary metabolites
Lignans and coumarins Lignans 15 Secondary metabolites
Coumarins 2
Others Xanthone 1 Secondary metabolites
Others 11
Saccharides and alcohols 22
Vitamin 6
Stilbene 1
Tannins Tannin 6 Secondary metabolites
Proanthocyanidins 2
Terpenoids Sesquiterpenoids 5 Secondary metabolites
Monoterpenoids 1
Triterpene 4
Triterpene saponin 1
Terpene 1
Organic acids Organic acids 63 Secondary metabolites
Quinones Quinones 1 Secondary metabolites

3.2 Multivariate statistical analysis

Multivariate statistics were used for further assessing the identified metabolites in Pin.t and XPin.t. According to the results of the hierarchical clustering analysis, the Pin.t and XPin.t samples could be distinctly categorized into two groups, with the metabolites exhibiting different accumulation patterns between these two groups (Figure 2a). To further analyze the degree of variability in the intergroup and intragroup sample data, the metabolite profiles of six samples were subjected to PCA (Figure 2b), and according to the results, the extracted two principal components PC1 and PC2 could explain 45.86% and 17.83% of the total variation, respectively. In the PCA plot, the three biological replicates of Pin.t were concentrated on the left side of the plot, while the three biological replicates of XPin.t were distributed on the right side of the plot (Figure 2b). The clustering and correlation analysis categorized the six samples into two distinct groups, with significantly and distinctly different metabolic profiles between Pin.t and XPin.t.

Figure 2 Analysis of the identified metabolites. (a) Cluster analysis of the identified metabolites in Pin.t and XPin.t. (b) PCA of Pin.t and XPin.t.
Figure 2

Analysis of the identified metabolites. (a) Cluster analysis of the identified metabolites in Pin.t and XPin.t. (b) PCA of Pin.t and XPin.t.

3.3 Differential metabolites between Pin.t and XPin.t.

The differential metabolites between Pin.t and XPin.t were screened based on a combination of FC and VIP values obtained from the OPLS-DA model. VIP ≥1.0 and FC ≥2 or ≤0.5 were used as the screening criteria. A total of 155 differential metabolites were detected between Pin.t and XPin.t, among which 68 putative metabolites were upregulated while 87 metabolites were downregulated in XPin.t compared to Pin.t (Figure 3a and b; Table S2). The differential metabolites were categorized into 11 classes, among which the main differential metabolites were categorized into three classes, namely, flavonoids (20.64%), lipids (18.06%), and alkaloids (11.61%) (Figure 3c).

Figure 3 DAM between Pin.t and XPin.t. (a) A volcano plot of the differential metabolites. Log2FC ≥1 or ≤–1 and VIP ≥1 were used as the screening criteria. (b) Heatmap of the differential metabolites. (c) The types and proportions of the differential metabolites. (d) An overview of the KEGG pathway analysis of the differential metabolites.
Figure 3

DAM between Pin.t and XPin.t. (a) A volcano plot of the differential metabolites. Log2FC ≥1 or ≤–1 and VIP ≥1 were used as the screening criteria. (b) Heatmap of the differential metabolites. (c) The types and proportions of the differential metabolites. (d) An overview of the KEGG pathway analysis of the differential metabolites.

Table 2 lists the differential primary and secondary metabolites identified between Pin.t and XPin.t. Sixty-five differential metabolites were identified as the primary metabolites, including 28 lipids, 17 amino acids and their derivatives, 12 organic acids, and 8 nucleotides along with their derivatives. In comparison to Pin.t, the differential primary metabolites that were upregulated in XPin.t included 13 lipids, 8 amino acids and their derivatives, 4 phenolic acids, and 3 nucleotides along with their derivatives. On the other hand, 90 differential metabolites were identified as secondary metabolites, including 32 flavonoids, 18 alkaloids, 17 phenolic acids, 8 lignans and coumarins, 4 tannins, 4 terpenoids, and 4 other kinds of compounds. A few secondary metabolites were upregulated in XPin.t, including 20 flavonoids, 6 alkaloids, 6 phenolic acids, 2 lignans and coumarins, 2 tannins, 1 terpenoid, and 3 other compounds.

Table 2

Statistics of the DAM between Pin.t and XPin.t

Primary classification Pin.t vs XPin.t Type
Down Up
Amino acids and derivatives 8 9 Primary metabolites
Nucleotides and derivatives 3 5 Primary metabolites
Lipids 13 15 Primary metabolites
Flavonoids 20 12 Secondary metabolites
Alkaloids 6 12 Secondary metabolites
Phenolic acids 6 11 Secondary metabolites
Lignans and coumarins 2 6 Secondary metabolites
Others 3 4 Secondary metabolites
Tannins 2 2 Secondary metabolites
Terpenoids 1 3 Secondary metabolites
Organic acids 4 8 Secondary metabolites

Furthermore, the KEGG database was employed to map the metabolites in Pin.t and XPin.t to various metabolic pathways. A total of 235 metabolites, including 52 differential metabolites, could be mapped to 44 metabolic pathways. The most enriched KEGG pathways were flavonoid biosynthesis, arginine and proline metabolism, tryptophan metabolism, pyrimidine metabolism, and cysteine and methionine metabolism (Figure 3d).

3.4 Analysis of the key differential metabolites

The dynamic distribution maps were plotted to highlight the differences in the metabolite content, and the top 10 metabolites with FC change are presented in Figure 4. Moreover, the top 10 metabolites that were significantly upregulated in XPin.t included eight flavonoids, one amino acid and its derivatives, and one other metabolite. The eight flavonoids included kaempferol-3-O-glucoside-7-O-rhamnoside, luteolin-7-O-neohesperidoside (Lonicerin), pinostrobin, alpinetin, luteolin-5,7-di-O-rutinoside, naringenin-7-O-neohesperidoside (Naringin), naringenin-7-O-rutinoside (Narirutin), and luteolin-7-O-rutinoside. The top 10 metabolites in XPin.t that were differentially downregulated were resveratrol, N-feruloylagmatine, naringenin chalcone, butin, alpha-epoxydihydroartemisinic acid, mucic acid-1,4-lactone-3,5-di-O-gallate, acetylsaikosaponin E, phloretin, phloretin-2′-O-glucoside (Phlorizin), and dihydrocharcone-4′-O-glucoside.

Figure 4 Dynamic distribution diagram of the differences in the metabolite contents.
Figure 4

Dynamic distribution diagram of the differences in the metabolite contents.

The main secondary metabolites in Pin.t and XPin.t were analyzed further, with a focus on flavonoids, phenolic acids, alkaloids, and terpenes. As visible in Figure 5 and Table 3, most of the flavonoids were present in higher concentrations in XPin.t compared to Pin.t. Conversely, most of the alkaloids, phenolic acids, and terpenoids had lower concentrations in XPin.t compared to Pin.t.

Figure 5 The heatmap depicting the main differentially accumulated secondary metabolites between Pin.t and XPin.t.
Figure 5

The heatmap depicting the main differentially accumulated secondary metabolites between Pin.t and XPin.t.

Table 3

Overview of the main differentially accumulated secondary metabolites between Pin.t and XPin.t

Primary classification Secondary classification Pin.t vs XPin.t
Down Up
Flavonoids Flavonoid 8 2
Dihydroflavone 6 2
Flavonols 4 1
Flavonoid carbonoside 1 0
Isoflavones 1 2
Dihydroflavonol 0 1
Chalcones 0 4
Phenolic acids Phenolic acids 6 11
Alkaloids Alkaloids 5 4
Phenolamine 0 6
Plumerane 0 2
Steroid alkaloids 1 0
Terpenoids Triterpene saponin 0 1
Sesquiterpenoids 1 2

4 Discussion

PR is the most widely used medicinal herb, and its tubers are used for treating a variety of diseases. As PR has extensive pharmacological activities, several studies have investigated its chemical constituents. Li et al. studied the chemical constituents of P. ternata and identified 186 compounds [17]. The report by the above authors serves as a reference for research on the chemical constituents of P. ternata. The present study also investigated the primary and secondary metabolites in Pin.t and XPin.t, and a total of 573 metabolites were identified under 12 subclasses, including flavonoids, phenolic acids, alkaloids, nucleotides, and their derivatives mainly (Table 1 and Table S1). Over 400 chemical compounds were identified in PR initially, including betaine, kaempferol, luteolin, coruscarin, kaempferol, naringin, etc. The results of the present study contributed to advancing the knowledge of the chemical constituents of PR (Table S1).

The metabolites in medicinal plants are crucial for the physiological activities of these plants and are closely associated with the defense of the plant against pests, diseases, and environmental stress. Therefore, these metabolites have important pharmacological activities [25]. Differential metabolites reflect the differences between different plant varieties, and PR from different origins differ greatly in terms of their contents of flavonoids, alkaloids, etc. [18]. Peng et al. studied 16 different wild provenances of P. ternata from Hunan Province and reported that the contents of total organic acids, alkaloids, and guanosine presented great significant differences among the different provenances and that the total organic acids and alkaloids exhibited no evident pattern of geographical and spatial variation [26]. Wang analyzed 15 samples of P. ternata from 7 different provinces and reported significant differences in organic acids, alkaloids, polysaccharides, and other metabolites in the P. ternata samples from different regions [27]. Jingzhou and Xixian are the two main production regions of PR, and the PR samples from these regions have been analyzed for the first time in the present study. The results revealed differences in flavonoids, alkaloids, phenolic acids, amino acids, and their derivatives, and organic acids between the samples from the two regions, which was consistent with the findings of previous studies (Figure 3c).

The alkaloids are among the important and effective medicinal components of P. ternata, which exhibit antitussive, anti-emetic, anti-tumor, and other effects [28]. Zeng et al. studied the relationship between the main components of P. ternata and the antitussive and expectorant effects of these components. The authors reported that the total alkaloids in P. ternata also exhibited the greatest correlation with the antitussive and expectorant effects [29]. The alkaloids in P. ternata were also observed to inhibit the spontaneous contraction of the isolated guinea pig ileum, which could then inhibit the 5-HT3 receptor and the NK1 receptor [7]. Chen et al. reported that a certain dosage of the total alkaloids in P. ternata could evidently inhibit the proliferation of human hepatoma cells in vitro [30]. In the present study, the relative expression levels of alkaloids were observed to be relatively higher in Pin.t, with 12 alkaloids exhibiting higher expression in Pin.t compared to XPin.t. Flavonoids exhibit pharmacological effects, such as anti-tumor, anti-oxidant, anti-inflammatory, and circulation improvement effects [31,32,33]. For instance, kaempferol attenuates the IL-32-induced differentiation of monocytes into macrophage-like cells. In addition, kaempferol reportedly inhibited the IL-32-induced activation of p38 and nuclear factor-kB in a dose-dependent manner in THP-1 cells [34]. Luteolin-7-O-neohesperidin (loniceratin) was reported to improve neurological function in rats [35]. Alpinin may reduce inflammation in rats with coronary heart disease via the inhibition of the MEK/ERK signal pathway, thereby improving vascular endothelial function, blood lipids, and cardiac function [36]. In the present study, 20 flavonoids exhibited higher concentrations in XPin.t compared to Pin.t. Eight among the top 10 upregulated metabolites in XPin.t compared to Pin.t were flavonoids, including kaempferol-3-O-glucoside-7-O-rhamnoside, luteolin-7-O-neohesperidoside (Lonicerin), pinostrobin, alpinetin, etc. (Figure 4). Therefore, the authors of the present study believe that these differences in the chemical composition could be due to the different pharmacological activities of Jing banxia and Xi banxia.

5 Conclusions

The UPLC–ESI-MS/MS-based metabolomics analysis was adopted to identify the chemical constituents of two authentic PRJing Banxia and Xi banxia. The results revealed a total of 573 metabolites under 12 sub-categories. Among the identified metabolites, 155 metabolites exhibited significant differences between Jing Banxia and Xi banxia. Most of the DAMs were concentrated under three categories of compounds, namely, flavonoids (20.64%), lipids (18.06%), and alkaloids (11.61%). The relative contents of 68 metabolites in Xi banxia were upregulated compared to Jing Banxia. On the other hand, the relative contents of 87 metabolites in Jing Banxia were upregulated compared to Xi banxia. Flavonoids and alkaloids were identified as the main putative bioactive components. While most of the alkaloids exhibited higher relative concentrations in Jing banxia, flavonoids had relatively higher expression levels in Xi banxia. The results of the present study improved the understanding of the chemical components and the medicinal value of Jing Banxia and Xi banxia and would serve as a theoretical reference when using PR for medicinal and other purposes.

  1. Funding information: This work was supported by Henan Provincial Science and Technology Research Project (Grant number: 212102110183).

  2. Author contributions: S.L. – formal analysis, funding acquisition, investigation, validation, writing – original draft, writing – review & editing. Y.C. – data curation, formal analysis, writing – original draft, writing – review & editing. X.L. – formal analysis, writing – original draft. C.Z. – formal analysis. H.Y. – conceptualization, investigation, project administration, resources, supervision, writing – original draft, writing – review & editing.

  3. Conflict of interest: The authors declare no competing financial interest.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: All data generated or analyzed during this study are included in this published article and its supplementary information files.

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Received: 2022-12-30
Revised: 2023-01-30
Accepted: 2023-02-01
Published Online: 2023-02-15

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/chem-2022-0287
Keywords for this article
Xi banxia; Jing banxia; producing regions; primary and secondary metabolites; differential metabolites
Creative Commons
BY 4.0

Articles in the same Issue

  1. Characteristics, source, and health risk assessment of aerosol polyaromatic hydrocarbons in the rural and urban regions of western Saudi Arabia
  2. Regular Articles
  3. A network-based correlation research between element electronegativity and node importance
  4. Pomegranate attenuates kidney injury in cyclosporine-induced nephrotoxicity in rats by suppressing oxidative stress
  5. Ab initio study of fundamental properties of XInO3 (X = K, Rb, Cs) perovskites
  6. Responses of feldspathic sandstone and sand-reconstituted soil C and N to freeze–thaw cycles
  7. Robust fractional control based on high gain observers design (RNFC) for a Spirulina maxima culture interfaced with an advanced oxidation process
  8. Study on arsenic speciation and redistribution mechanism in Lonicera japonica plants via synchrotron techniques
  9. Optimization of machining Nilo 36 superalloy parameters in turning operation
  10. Vacuum impregnation pre-treatment: A novel method for incorporating mono- and divalent cations into potato strips to reduce the acrylamide formation in French fries
  11. Characterization of effective constituents in Acanthopanax senticosus fruit for blood deficiency syndrome based on the chinmedomics strategy
  12. Comparative analysis of the metabolites in Pinellia ternata from two producing regions using ultra-high-performance liquid chromatography–electrospray ionization–tandem mass spectrometry
  13. The assessment of environmental parameter along the desalination plants in the Kingdom of Saudi Arabia
  14. Effects of harpin and carbendazim on antioxidant accumulation in young jujube leaves
  15. The effects of in ovo injected with sodium borate on hatching performance and small intestine morphology in broiler chicks
  16. Optimization of cutting forces and surface roughness via ANOVA and grey relational analysis in machining of In718
  17. Essential oils of Origanum compactum Benth: Chemical characterization, in vitro, in silico, antioxidant, and antibacterial activities
  18. Translocation of tungsten(vi) oxide/gadolinium(iii) fluoride in tellurite glasses towards improvement of gamma-ray attenuation features in high-density glass shields
  19. Mechanical properties, elastic moduli, and gamma ray attenuation competencies of some TeO2–WO3–GdF3 glasses: Tailoring WO3–GdF3 substitution toward optimum behavioral state range
  20. Comparison between the CIDR or sponge with hormone injection to induce estrus synchronization for twining and sex preselection in Naimi sheep
  21. Exergetic performance analyses of three different cogeneration plants
  22. Psoralea corylifolia (babchi) seeds enhance proliferation of normal human cultured melanocytes: GC–MS profiling and biological investigation
  23. A novel electrochemical micro-titration method for quantitative evaluation of the DPPH free radical scavenging capacity of caffeic acid
  24. Comparative study between supported bimetallic catalysts for nitrate remediation in water
  25. Persicaline, an alkaloid from Salvadora persica, inhibits proliferation and induces apoptosis and cell-cycle arrest in MCF-7 cells
  26. Determination of nicotine content in locally produced smokeless tobacco (Shammah) samples from Jazan region of Saudi Arabia using a convenient HPLC-MS/MS method
  27. Changes in oxidative stress markers in pediatric burn injury over a 1-week period
  28. Integrated geophysical techniques applied for petroleum basins structural characterization in the central part of the Western Desert, Egypt
  29. The impact of chemical modifications on gamma-ray attenuation properties of some WO3-reinforced tellurite glasses
  30. Microwave and Cs+-assisted chemo selective reaction protocol for synthesizing 2-styryl quinoline biorelevant molecules
  31. Structural, physical, and radiation absorption properties of a significant nuclear power plant component: A comparison between REX-734 and 316L SS austenitic stainless steels
  32. Effect of Moringa oleifera on serum YKL-40 level: In vivo rat periodontitis model
  33. Investigating the impact of CO2 emissions on the COVID-19 pandemic by generalized linear mixed model approach with inverse Gaussian and gamma distributions
  34. Influence of WO3 content on gamma rays attenuation characteristics of phosphate glasses at low energy range
  35. Study on CO2 absorption performance of ternary DES formed based on DEA as promoting factor
  36. Performance analyses of detonation engine cogeneration cycles
  37. Sterols from Centaurea pumilio L. with cell proliferative activity: In vitro and in silico studies
  38. Untargeted metabolomics revealing changes in aroma substances in flue-cured tobacco
  39. Effect of pumpkin enriched with calcium lactate on iron status in an animal model of postmenopausal osteoporosis
  40. Energy consumption, mechanical and metallographic properties of cryogenically treated tool steels
  41. Optimization of ultra-high pressure-assisted extraction of total phenols from Eucommia ulmoides leaves by response surface methodology
  42. Harpin enhances antioxidant nutrient accumulation and decreases enzymatic browning in stored soybean sprouts
  43. Physicochemical and biological properties of carvacrol
  44. Radix puerariae in the treatment of diabetic nephropathy: A network pharmacology analysis and experimental validation
  45. Anti-Alzheimer, antioxidants, glucose-6-phosphate dehydrogenase effects of Taverniera glabra mediated ZnO and Fe2O3 nanoparticles in alloxan-induced diabetic rats
  46. Experimental study on photocatalytic CO2 reduction performance of ZnS/CdS-TiO2 nanotube array thin films
  47. Epoxy-reinforced heavy metal oxides for gamma ray shielding purposes
  48. Black mulberry (Morus nigra L.) fruits: As a medicinal plant rich in human health-promoting compounds
  49. Promising antioxidant and antimicrobial effects of essential oils extracted from fruits of Juniperus thurifera: In vitro and in silico investigations
  50. Chloramine-T-induced oxidation of Rizatriptan Benzoate: An integral chemical and spectroscopic study of products, mechanisms and kinetics
  51. Study on antioxidant and antimicrobial potential of chemically profiled essential oils extracted from Juniperus phoenicea (L.) by use of in vitro and in silico approaches
  52. Screening and characterization of fungal taxol-producing endophytic fungi for evaluation of antimicrobial and anticancer activities
  53. Mineral composition, principal polyphenolic components, and evaluation of the anti-inflammatory, analgesic, and antioxidant properties of Cytisus villosus Pourr leaf extracts
  54. In vitro antiproliferative efficacy of Annona muricata seed and fruit extracts on several cancer cell lines
  55. An experimental study for chemical characterization of artificial anterior cruciate ligament with coated chitosan as biomaterial
  56. Prevalence of residual risks of the transfusion-transmitted infections in Riyadh hospitals: A two-year retrospective study
  57. Computational and experimental investigation of antibacterial and antifungal properties of Nicotiana tabacum extracts
  58. Reinforcement of cementitious mortars with hemp fibers and shives
  59. X-ray shielding properties of bismuth-borate glass doped with rare earth ions
  60. Green supported silver nanoparticles over modified reduced graphene oxide: Investigation of its antioxidant and anti-ovarian cancer effects
  61. Orthogonal synthesis of a versatile building block for dual functionalization of targeting vectors
  62. Thymbra spicata leaf extract driven biogenic synthesis of Au/Fe3O4 nanocomposite and its bio-application in the treatment of different types of leukemia
  63. The role of Ag2O incorporation in nuclear radiation shielding behaviors of the Li2O–Pb3O4–SiO2 glass system: A multi-step characterization study
  64. A stimuli-responsive in situ spray hydrogel co-loaded with naringenin and gentamicin for chronic wounds
  65. Assessment of the impact of γ-irradiation on the piperine content and microbial quality of black pepper
  66. Antioxidant, sensory, and functional properties of low-alcoholic IPA beer with Pinus sylvestris L. shoots addition fermented using unconventional yeast
  67. Screening and optimization of extracellular pectinase produced by Bacillus thuringiensis SH7
  68. Determination of polyphenols in Chinese jujube using ultra-performance liquid chromatography–mass spectrometry
  69. Synergistic effects of harpin and NaCl in determining soybean sprout quality under non-sterile conditions
  70. Field evaluation of different eco-friendly alternative control methods against Panonychus citri [Acari: Tetranychidae] spider mite and its predators in citrus orchards
  71. Exploring the antimicrobial potential of biologically synthesized zero valent iron nanoparticles
  72. NaCl regulates goldfish growth and survival at three food supply levels under hypoxia
  73. An exploration of the physical, optical, mechanical, and radiation shielding properties of PbO–MgO–ZnO–B2O3 glasses
  74. A novel statistical modeling of air pollution and the COVID-19 pandemic mortality data by Poisson, geometric, and negative binomial regression models with fixed and random effects
  75. Treatment activity of the injectable hydrogels loaded with dexamethasone In(iii) complex on glioma by inhibiting the VEGF signaling pathway
  76. An alternative approach for the excess lifetime cancer risk and prediction of radiological parameters
  77. Panax ginseng leaf aqueous extract mediated green synthesis of AgNPs under ultrasound condition and investigation of its anti-lung adenocarcinoma effects
  78. Study of hydrolysis and production of instant ginger (Zingiber officinale) tea
  79. Novel green synthesis of zinc oxide nanoparticles using Salvia rosmarinus extract for treatment of human lung cancer
  80. Evaluation of second trimester plasma lipoxin A4, VEGFR-1, IL-6, and TNF-α levels in pregnant women with gestational diabetes mellitus
  81. Antidiabetic, antioxidant and cytotoxicity activities of ortho- and para-substituted Schiff bases derived from metformin hydrochloride: Validation by molecular docking and in silico ADME studies
  82. Antioxidant, antidiabetic, antiglaucoma, and anticholinergic effects of Tayfi grape (Vitis vinifera): A phytochemical screening by LC-MS/MS analysis
  83. Identification of genetic polymorphisms in the stearoyl CoA desaturase gene and its association with milk quality traits in Najdi sheep
  84. Cold-acclimation effect on cadmium absorption and biosynthesis of polyphenolics, and free proline and photosynthetic pigments in Spirogyra aequinoctialis
  85. Analysis of secondary metabolites in Xinjiang Morus nigra leaves using different extraction methods with UPLC-Q/TOF-MS/MS technology
  86. Nanoarchitectonics and performance evaluation of a Fe3O4-stabilized Pickering emulsion-type differential pressure plugging agent
  87. Investigating pyrolysis characteristics of Shengdong coal through Py-GC/MS
  88. Extraction, phytochemical characterization, and antifungal activity of Salvia rosmarinus extract
  89. Introducing a novel and natural antibiotic for the treatment of oral pathogens: Abelmoschus esculentus green-formulated silver nanoparticles
  90. Optimization of gallic acid-enriched ultrasonic-assisted extraction from mango peels
  91. Effect of gamma rays irradiation in the structure, optical, and electrical properties of samarium doped bismuth titanate ceramics
  92. Combinatory in silico investigation for potential inhibitors from Curcuma sahuynhensis Škorničk. & N.S. Lý volatile phytoconstituents against influenza A hemagglutinin, SARS-CoV-2 main protease, and Omicron-variant spike protein
  93. Physical, mechanical, and gamma ray shielding properties of the Bi2O3–BaO–B2O3–ZnO–As2O3–MgO–Na2O glass system
  94. Twofold interpenetrated 3D Cd(ii) complex: Crystal structure and luminescent property
  95. Study on the microstructure and soil quality variation of composite soil with soft rock and sand
  96. Ancient spring waters still emerging and accessible in the Roman Forum area: Chemical–physical and microbiological characterization
  97. Extraction and characterization of type I collagen from scales of Mexican Biajaiba fish
  98. Finding small molecular compounds to decrease trimethylamine oxide levels in atherosclerosis by virtual screening
  99. Prefatory in silico studies and in vitro insecticidal effect of Nigella sativa (L.) essential oil and its active compound (carvacrol) against the Callosobruchus maculatus adults (Fab), a major pest of chickpea
  100. Polymerized methyl imidazole silver bromide (CH3C6H5AgBr)6: Synthesis, crystal structures, and catalytic activity
  101. Using calcined waste fish bones as a green solid catalyst for biodiesel production from date seed oil
  102. Influence of the addition of WO3 on TeO2–Na2O glass systems in view of the feature of mechanical, optical, and photon attenuation
  103. Naringin ameliorates 5-fluorouracil elicited neurotoxicity by curtailing oxidative stress and iNOS/NF-ĸB/caspase-3 pathway
  104. GC-MS profile of extracts of an endophytic fungus Alternaria and evaluation of its anticancer and antibacterial potentialities
  105. Green synthesis, chemical characterization, and antioxidant and anti-colorectal cancer effects of vanadium nanoparticles
  106. Determination of caffeine content in coffee drinks prepared in some coffee shops in the local market in Jeddah City, Saudi Arabia
  107. A new 3D supramolecular Cu(ii) framework: Crystal structure and photocatalytic characteristics
  108. Bordeaux mixture accelerates ripening, delays senescence, and promotes metabolite accumulation in jujube fruit
  109. Important application value of injectable hydrogels loaded with omeprazole Schiff base complex in the treatment of pancreatitis
  110. Color tunable benzothiadiazole-based small molecules for lightening applications
  111. Investigation of structural, dielectric, impedance, and mechanical properties of hydroxyapatite-modified barium titanate composites for biomedical applications
  112. Metal gel particles loaded with epidermal cell growth factor promote skin wound repair mechanism by regulating miRNA
  113. In vitro exploration of Hypsizygus ulmarius (Bull.) mushroom fruiting bodies: Potential antidiabetic and anti-inflammatory agent
  114. Alteration in the molecular structure of the adenine base exposed to gamma irradiation: An ESR study
  115. Comprehensive study of optical, thermal, and gamma-ray shielding properties of Bi2O3–ZnO–PbO–B2O3 glasses
  116. Lewis acids as co-catalysts in Pd-based catalyzed systems of the octene-1 hydroethoxycarbonylation reaction
  117. Synthesis, Hirshfeld surface analysis, thermal, and selective α-glucosidase inhibitory studies of Schiff base transition metal complexes
  118. Protective properties of AgNPs green-synthesized by Abelmoschus esculentus on retinal damage on the virtue of its anti-inflammatory and antioxidant effects in diabetic rat
  119. Effects of green decorated AgNPs on lignin-modified magnetic nanoparticles mediated by Cydonia on cecal ligation and puncture-induced sepsis
  120. Treatment of gastric cancer by green mediated silver nanoparticles using Pistacia atlantica bark aqueous extract
  121. Preparation of newly developed porcelain ceramics containing WO3 nanoparticles for radiation shielding applications
  122. Utilization of computational methods for the identification of new natural inhibitors of human neutrophil elastase in inflammation therapy
  123. Some anticancer agents as effective glutathione S-transferase (GST) inhibitors
  124. Clay-based bricks’ rich illite mineral for gamma-ray shielding applications: An experimental evaluation of the effect of pressure rates on gamma-ray attenuation parameters
  125. Stability kinetics of orevactaene pigments produced by Epicoccum nigrum in solid-state fermentation
  126. Treatment of denture stomatitis using iron nanoparticles green-synthesized by Silybum marianum extract
  127. Characterization and antioxidant potential of white mustard (Brassica hirta) leaf extract and stabilization of sunflower oil
  128. Characteristics of Langmuir monomolecular monolayers formed by the novel oil blends
  129. Strategies for optimizing the single GdSrFeO4 phase synthesis
  130. Oleic acid and linoleic acid nanosomes boost immunity and provoke cell death via the upregulation of beta-defensin-4 at genetic and epigenetic levels
  131. Unraveling the therapeutic potential of Bombax ceiba roots: A comprehensive study of chemical composition, heavy metal content, antibacterial activity, and in silico analysis
  132. Green synthesis of AgNPs using plant extract and investigation of its anti-human colorectal cancer application
  133. The adsorption of naproxen on adsorbents obtained from pepper stalk extract by green synthesis
  134. Treatment of gastric cancer by silver nanoparticles encapsulated by chitosan polymers mediated by Pistacia atlantica extract under ultrasound condition
  135. In vitro protective and anti-inflammatory effects of Capparis spinosa and its flavonoids profile
  136. Wear and corrosion behavior of TiC and WC coatings deposited on high-speed steels by electro-spark deposition
  137. Therapeutic effects of green-formulated gold nanoparticles by Origanum majorana on spinal cord injury in rats
  138. Melanin antibacterial activity of two new strains, SN1 and SN2, of Exophiala phaeomuriformis against five human pathogens
  139. Evaluation of the analgesic and anesthetic properties of silver nanoparticles supported over biodegradable acacia gum-modified magnetic nanoparticles
  140. Review Articles
  141. Role and mechanism of fruit waste polyphenols in diabetes management
  142. A comprehensive review of non-alkaloidal metabolites from the subfamily Amaryllidoideae (Amaryllidaceae)
  143. Discovery of the chemical constituents, structural characteristics, and pharmacological functions of Chinese caterpillar fungus
  144. Eco-friendly green approach of nickel oxide nanoparticles for biomedical applications
  145. Advances in the pharmaceutical research of curcumin for oral administration
  146. Rapid Communication
  147. Determination of the contents of bioactive compounds in St. John’s wort (Hypericum perforatum): Comparison of commercial and wild samples
  148. Retraction
  149. Retraction of “Two mixed-ligand coordination polymers based on 2,5-thiophenedicarboxylic acid and flexible N-donor ligands: The protective effect on periodontitis via reducing the release of IL-1β and TNF-α”
  150. Topical Issue on Phytochemicals, biological and toxicological analysis of aromatic medicinal plants
  151. Anti-plasmodial potential of selected medicinal plants and a compound Atropine isolated from Eucalyptus obliqua
  152. Anthocyanin extract from black rice attenuates chronic inflammation in DSS-induced colitis mouse model by modulating the gut microbiota
  153. Evaluation of antibiofilm and cytotoxicity effect of Rumex vesicarius methanol extract
  154. Chemical compositions of Litsea umbellata and inhibition activities
  155. Green synthesis, characterization of silver nanoparticles using Rhynchosia capitata leaf extract and their biological activities
  156. GC-MS analysis and antibacterial activities of some plants belonging to the genus Euphorbia on selected bacterial isolates
  157. The abrogative effect of propolis on acrylamide-induced toxicity in male albino rats: Histological study
  158. A phytoconstituent 6-aminoflavone ameliorates lipopolysaccharide-induced oxidative stress mediated synapse and memory dysfunction via p-Akt/NF-kB pathway in albino mice
  159. Anti-diabetic potentials of Sorbaria tomentosa Lindl. Rehder: Phytochemistry (GC-MS analysis), α-amylase, α-glucosidase inhibitory, in vivo hypoglycemic, and biochemical analysis
  160. Assessment of cytotoxic and apoptotic activities of the Cassia angustifolia aqueous extract against SW480 colon cancer
  161. Biochemical analysis, antioxidant, and antibacterial efficacy of the bee propolis extract (Hymenoptera: Apis mellifera) against Staphylococcus aureus-induced infection in BALB/c mice: In vitro and in vivo study
  162. Assessment of essential elements and heavy metals in Saudi Arabian rice samples underwent various processing methods
  163. Two new compounds from leaves of Capparis dongvanensis (Sy, B. H. Quang & D. V. Hai) and inhibition activities
  164. Hydroxyquinoline sulfanilamide ameliorates STZ-induced hyperglycemia-mediated amyleoid beta burden and memory impairment in adult mice
  165. An automated reading of semi-quantitative hemagglutination results in microplates: Micro-assay for plant lectins
  166. Inductively coupled plasma mass spectrometry assessment of essential and toxic trace elements in traditional spices consumed by the population of the Middle Eastern region in their recipes
  167. Phytochemical analysis and anticancer activity of the Pithecellobium dulce seed extract in colorectal cancer cells
  168. Impact of climatic disturbances on the chemical compositions and metabolites of Salvia officinalis
  169. Physicochemical characterization, antioxidant and antifungal activities of essential oils of Urginea maritima and Allium sativum
  170. Phytochemical analysis and antifungal efficiency of Origanum majorana extracts against some phytopathogenic fungi causing tomato damping-off diseases
  171. Special Issue on 4th IC3PE
  172. Graphene quantum dots: A comprehensive overview
  173. Studies on the intercalation of calcium–aluminium layered double hydroxide-MCPA and its controlled release mechanism as a potential green herbicide
  174. Synergetic effect of adsorption and photocatalysis by zinc ferrite-anchored graphitic carbon nitride nanosheet for the removal of ciprofloxacin under visible light irradiation
  175. Exploring anticancer activity of the Indonesian guava leaf (Psidium guajava L.) fraction on various human cancer cell lines in an in vitro cell-based approach
  176. The comparison of gold extraction methods from the rock using thiourea and thiosulfate
  177. Special Issue on Marine environmental sciences and significance of the multidisciplinary approaches
  178. Sorption of alkylphenols and estrogens on microplastics in marine conditions
  179. Cytotoxic ketosteroids from the Red Sea soft coral Dendronephthya sp.
  180. Antibacterial and biofilm prevention metabolites from Acanthophora spicifera
  181. Characteristics, source, and health risk assessment of aerosol polyaromatic hydrocarbons in the rural and urban regions of western Saudi Arabia
  182. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part II
  183. Green synthesis, characterization, and evaluation of antibacterial activities of cobalt nanoparticles produced by marine fungal species Periconia prolifica
  184. Combustion-mediated sol–gel preparation of cobalt-doped ZnO nanohybrids for the degradation of acid red and antibacterial performance
  185. Perinatal supplementation with selenium nanoparticles modified with ascorbic acid improves hepatotoxicity in rat gestational diabetes
  186. Evaluation and chemical characterization of bioactive secondary metabolites from endophytic fungi associated with the ethnomedicinal plant Bergenia ciliata
  187. Enhancing photovoltaic efficiency with SQI-Br and SQI-I sensitizers: A comparative analysis
  188. Nanostructured p-PbS/p-CuO sulfide/oxide bilayer heterojunction as a promising photoelectrode for hydrogen gas generation
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