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Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach

  • Yewei Zhong , Fenglian Tong , Junlin Yan , Huiwen Tan , Adalaiti Abudurexiti , Rui Zhang , Yi Lei , Delong Li and Xiaoli Ma EMAIL logo
Published/Copyright: June 27, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

Mulberry is a common crop rich in flavonoids, and its leaves (ML), fruits (M), and branches (Ramulus Mori, RM) have medicinal value. In the present study, a total of 118 flavonoid metabolites (47 flavone, 23 flavonol, 16 flavonoid, 8 anthocyanins, 8 isoflavone, 14 flavanone, and 2 proanthocyanidins) and 12 polyphenols were identified by ultra-performance liquid chromatography–electrospray ionization-tandem mass spectrometry. The most abundant in ML were 8-C-hexosyl-hesperetin O-hexoside and astragalin, the most abundant in M were 8-C-hexosyl-hesperetin O-hexoside and naringenin, and the most abundant in RM were cyanidin 3-O-galactoside and gallocatechin–gallocatechin. The total flavonoid compositions of ML and RM were essentially the same, but the contents of flavonoid metabolite in more than half of them were higher than those in M. Compared with ML, the contents of flavone and flavonoid in RM and M were generally down-regulated. Each tissue part had a unique flavonoid, which could be used as a marker to distinguish different tissue parts. In this study, the differences between flavonoid metabolite among RM, ML, and M were studied, which provided a theoretical basis for making full use of mulberry resources.

Keywords: mulberry; flavonoid metabolites; UPLC–ESI-MS/MS

1 Introduction

Mulberry (Morus alba L.) was first recorded in the traditional Chinese Medical Book Shennong’s Herbal Classic of Materia Medica, and its leaves (ML), fruits (M), and branches Ramulus Mori (RM) can be used as medicine. Mulberry leaves are often used in the treatment of cardiovascular and cerebrovascular diseases or alopecia [1]. Mulberry is a kind of fruit in daily life. It is often used to protect the kidney and liver and reduce sugar and fat [2] and is called “Folk Holy Fruit.” Mulberry branches are often used in the treatment of arthritis and rheumatism [3]. Flavonoids constitute a major group of important secondary plant metabolites. The group includes representatives of anthocyanins, flavonoids, and chalcone. They have been reported to have a variety of biological functions in the plants themselves and have shown impressive antioxidant, anti-inflammatory, hypoglycemic, lipid-lowering, and antihypertensive effects in the human organism [4]. Flavonoids play an important role in the bioactive components of mulberry, and different parts of mulberry have different medicinal characteristics, and the differences in their flavonoid metabolites may have an important influence on this [5]. Therefore, exploring the differences of flavonoid metabolites in different parts of mulberry and revealing the possible basis of medicinal components will be an important revelation for the study of the medicinal development of mulberry.

Mulberry-specific compound 1-deoxynojirimycin has a significant hypoglycemic effect, the group’s previous study found that 1-deoxynojirimycin is the highest content in leaves, followed by the second in fruits, and the lowest in stems, which provides some reference significance for the application of mulberry research. However, there is no study on the difference in its flavonoid components, to further explore the basis of the substance active components of mulberry this study will use the metabolomics approach to fill this gap. Metabolomics of mulberry has been widely studied and reported, Jiang et al. analyzed the changes in the content of different sugar and acid components of mulberry fruits from the green stage of fruit expansion to the red and then to the ripening stage based on targeted metabolomics by LC-MS [6]. Yang et al. investigated the effect of frost on the different metabolites of two types of mulberry leaves (Morus nigra L. and Morus alba L.) [7]. In this study, metabolomics will be utilized to explore the differences in the bioactivity of flavonoids in different parts of mulberry, which will provide valuable insights into the uses of their different parts. Ultra performance liquid chromatography–electrospray ionization-tandem mass spectrometry (UPLC–ESI-MS/MS) combined with cluster analysis, principal component analysis (PCA), and orthogonal partial least squares-discrimination analysis (OPLS-DA) were used to analyze the difference of flavonoids metabolites in ML, RM, and M.

2 Materials and methods

2.1 Plant materials

The three medicinal parts of mulberry were harvested from Hotan, Xinjiang, in July 2020 and identified as mulberry leaves, mulberry, and mulberry branches by Professor Haiyan Xu, College of Traditional Chinese Medicine (TCM), Xinjiang Medical University; the method of identification is based on the original identification of TCM [8]. All parts were shade-dried, air-dried, crushed through a 100-mesh sieve, and stored in the College of Pharmacy of Xinjiang Medical University (humidity at 65–70% and temperature at 4℃). Nine samples were selected in this metabolic group study and divided into three groups: stem, leaf, and fruit. Each group had three biological replicates (Table 1).

Table 1

Sample grouping

Tissue position Processing description Sample name Group
Mulberry leaves Drying and pulverizing ML1 ML
Mulberry leaves Drying and pulverizing ML2 ML
Mulberry leaves Drying and pulverizing ML3 ML
Fruit of mulberry Drying and pulverizing M1 M
Fruit of mulberry Drying and pulverizing M2 M
Fruit of mulberry Drying and pulverizing M3 M
Mulberry branch Drying and pulverizing Ramulus_Mori_1 RM
Mulberry branch Drying and pulverizing Ramulus_Mori_2 RM
Mulberry branch Drying and pulverizing Ramulus_Mori_3 RM

2.2 Standard products and reagents

The standard products used in the self-built library are as follows: Yunnan Xili Biotechnology Co., Ltd (http://www.biobiopha.com/) and Sigma Aldrich (Shanghai) Trading Co., Ltd (Sigma-Aldrich); methanol, acetonitrile, and ethanol (Merck, Germany) are chromatographic grade. The standard product was dissolved with dimethyl sulfoxide (Merck, Germany) or methanol as solvent and stored at −20℃. Before mass spectrometry, 70% methanol was diluted to different gradient concentrations.

2.3 Sample preparation and extraction

The sample was freeze-dried in a vacuum; ground (30 Hz, 1.5 min) to powder by grinding instrument (MM 400, Retsch); weighed 100 mg powder; and dissolved in 1.0 mL extraction solution (70% methanol–water solution); the dissolved samples were refrigerated overnight at 4℃, during which they were vortexed three times to improve the extraction rate; after centrifugation (rotating speed: 10,000 × g, 10 min), absorb the supernatant and use microporous filter membrane (0.22 μm) The samples were filtered and stored in the injection bottle for UPLC–MS/MS analysis.

2.4 UPLC conditions

Chromatographic column: Waters ACQUITY UPLC HSS T3 C18 (1.8 μm, 2.1 mm × 100 mm); column temperature: 40℃; mobile phase: ultra-pure water (0.04% acetic acid) as phase A and acetonitrile (0.04% acetic acid) as phase B; gradient elution procedure: 0 min, 5% B; 0–11.0 min, 5–95% B; 11.0–12.0 min, 95% B; 12.0–12.1 min, 95–5% B, 12.1–15.0 min, 5% B; flow rate 0.4 mL/min; the injection volume was 2 μl; internal standard: l-2-chlorophenylalanine (China, J&K Scientific).

2.5 Mass spectrum condition

Positive and negative ion ionization modes were used for mass spectrometry detection, and the scanning range was m/z 100–2,000. The specific parameters are shown in Table 2.

Table 2

Mass spectrometry

Mass spectrometry conditions Parameter
Mass spectrometry voltage 5,500 V
Collision-activated dissociation High
Collision energy Specific optimization
Electrospray ionization temperature 500℃
Curtain gas 25 psi
Declustering potential Specific optimization

2.6 Qualitative and quantitative analyses of metabolites

Based on the self-built database metware database (China Wuhan Jiewei Biotechnology Co., Ltd.) [9] and the public database of metabolite information, the first and second data of mass spectrometry were qualitatively analyzed. HMDB is used for structure analysis (http://www.hmdb.ca/) and METLIN (http://metlin.scripps.edu/index.php). Metabolite quantification was performed by multiple reaction monitoring (MRM) mode analysis of triple quadrupole mass spectrometry. In MRM mode, the quadrupole first selects the precursor ion (parent ion) of the target material and eliminates the corresponding ions of other molecular weight materials to preliminarily eliminate interference; the precursor ion is induced to ionize by the collision chamber and breaks to form a lot of fragment ions, and then the fragment ions are filtered by the triple quadrupole to select a required characteristic fragment ion and eliminate the interference of non-target ions, making the quantification more accurate and repeatable. After obtaining the mass spectrum analysis data of metabolites from different samples, the peak areas of all mass spectrum peaks were integrated, and the mass spectrum peaks of the same metabolite in different samples were integrated and corrected.

2.7 Statistical analysis

Each group had three biological replicates. Hierarchical cluster analysis, PCA, and OPLS-DA were performed by R 3.2.5 software. Adobe Photoshop CC 2019 was used for image beautification, and the Kyoto Encyclopedia of Genes and Genome (KEGG) (http://www.genome.ad.jp/kegg/) database was used for path enrichment analysis.

3 Result

3.1 Sample quality control (QC) analysis

The high stability of the instrument provides an important guarantee for the repeatability and reliability of the data. The three groups of sample extracts were mixed to prepare QC samples, and the reproducibility of samples under the same treatment method was analyzed. The reproducibility of metabolite extraction and detection can be judged by overlapping analysis of total ion current diagrams of different QC samples identified by mass spectrometry. The overlay of the total ions current (TIC) diagram is shown in Figure 1. The results showed that the total ion current curve of metabolite detection had a high degree of overlap, indicating that the signal stability of the same sample was good at different detection times.

Figure 1 The stacking diagram of TIC maps from QC samples mass spectrometry. (a) TIC of positive ion MRM. (b) TIC of negative ion MRM.
Figure 1

The stacking diagram of TIC maps from QC samples mass spectrometry. (a) TIC of positive ion MRM. (b) TIC of negative ion MRM.

3.2 Metabolic profiling

The mass spectrum data were processed by Software Analyst 1.6.3. Figure 2 shows the total ion flow diagram of the mixed sample. To compare the content difference of each metabolite in different samples, the mass spectrum analysis data of different samples were obtained by MRM, the peak area of all mass spectrum peaks was integrated, and the mass spectrum peaks of the same metabolite in different samples were integrated and corrected (Figure 3), to ensure the quality of the mixed sample. The abscissa is the retention time of metabolite detection, the ordinate is the ion current intensity of ion detection, and the peak area represents the relative content of the substance in the sample. A total of 130 flavonoid metabolites were identified and the data are shown in detail in Table S1.

Figure 2 TIC diagrams of positive ion (a) and negative ion (b) in mass spectrometry of mixed samples.
Figure 2

TIC diagrams of positive ion (a) and negative ion (b) in mass spectrometry of mixed samples.

Figure 3 Integral correction diagram for quantitative analysis of positive ion (a) and negative ion (b) of randomly selected metabolites.
Figure 3

Integral correction diagram for quantitative analysis of positive ion (a) and negative ion (b) of randomly selected metabolites.

3.3 Identification of metabolites

The flavonoid metabolites of three parts of mulberry were analyzed by UPLC–MS/MS technology and database. A total of 130 metabolites were identified, including 47 flavone, 23 flavonols, 16 flavonoids, 8 anthocyanins, 8 isoflavone, 14 flavanone, 2 proanthocyanidins, and 12 polyphenols (Table S1). The range method was used to normalize the data of metabolite content, and the R software was used to cluster the accumulation patterns of metabolites in different samples. As shown in Figure 4, we can see that there are obvious differences in the content of flavonoid metabolites among ML, M, and RM. Compared with M, the contents of most flavonoid metabolites in ML and RM were up-regulated. Compared with ML, the contents of flavone and flavonol metabolites in RM and m were down-regulated, and each tissue had a uniquely high content of flavonoid metabolites.

Figure 4 The overall cluster heat map of the sample. The metabolite content data were normalized by the extreme difference method. The transverse coordinates represented the sample name, the longitudinal coordinates represented the metabolite name, and the color represented the relative value (red for up-regulation, green for down-regulation).
Figure 4

The overall cluster heat map of the sample. The metabolite content data were normalized by the extreme difference method. The transverse coordinates represented the sample name, the longitudinal coordinates represented the metabolite name, and the color represented the relative value (red for up-regulation, green for down-regulation).

3.4 Differential flavonoid metabolite analysis based on PCA

PCA uses several main components to reveal the internal structure between multiple variables. In this study, two main components, PC1 and PC2, were extracted and were 48.99% and 41.82%, respectively, and the cumulative contribution rate was 90.81%. In the PCA score diagram (Figure 5), M, RM, and ML were separated clearly, and the repeated samples were allocated closely together, which indicated that the experiment was repeatable and reliable. The obvious separation of M, mix (mixed QC group), ML, and RM showed that there was a great difference among the four groups.

Figure 5 Differential flavonoid metabolite analysis on the basis of (a) principal component (PCA) and (b) PCA loadings.
Figure 5

Differential flavonoid metabolite analysis on the basis of (a) principal component (PCA) and (b) PCA loadings.

3.5 Differential flavonoid metabolite analysis based on OPLS-DA

OPLS-DA, combined with orthogonal signal correction and PLS-DA, can decompose X matrix information into two kinds of information related to Y and unrelated. By removing unrelated differences, the different variables can be screened, which can maximize the difference between groups and is beneficial to the search for differential metabolites. The prediction parameters to evaluate the model were R 2 X, R 2 Y, and Q 2. Among them, R 2 X and R 2 Y represent the interpretation rate of the model to the X and Y matrices, respectively, and Q 2 represents the prediction ability of the model. The closer these three indexes are to 1, the more stable and reliable the model is. When Q 2 > 0.5, it can be considered an effective model, and Q 2 > 0.9 is an excellent model. In this study (Figure 6), the contents of flavonoid metabolites in the two groups were compared by the OPLS-DA model to evaluate M and RM (R 2 X = 0.973, R 2 Y = 1, Q 2 = 1), ML and M (R 2 X = 0.975, R 2 Y = 1, Q 2 = 1), and ML and RM (R 2 X = 0.984, R 2 Y = 1, Q 2 = 1). The Q 2 values of the three comparison groups were more than 0.9, which indicated that the model was stable and reliable and could be used to further screen different flavonoid metabolites.

Figure 6 Identification analysis of flavonoid metabolites based on OPLS-DA. (a–c) OPLS-DA model plots for the comparison group M vs RM, ML vs M, and ML vs RM, respectively. (d–f) OPLS-DA loading plots for the comparison group M vs RM, ML vs M, and ML vs RM, respectively.
Figure 6

Identification analysis of flavonoid metabolites based on OPLS-DA. (a–c) OPLS-DA model plots for the comparison group M vs RM, ML vs M, and ML vs RM, respectively. (d–f) OPLS-DA loading plots for the comparison group M vs RM, ML vs M, and ML vs RM, respectively.

3.6 Differential flavonoid metabolite screening, functional annotation, and enrichment analysis

Differential flavonoid metabolites were screened for each comparison group by combining the fold change and variable importance in project (VIP) values of the OPLS-DA model. The screening criteria were as follows: fold change ≥2 and fold change ≤0.5 and VIP ≥ 1. The screening results are shown in Table 3 and Table S2. From the screening results, we knew that there were 44 different metabolites of flavonoids between M and RM (29 up-regulated and 15 down-regulated). There were 38 between ML and M (9 up-regulated and 29 down-regulated) and 39 between ML and RM (18 up-regulated and 21 down-regulated). Most of the flavonoid metabolites were down-regulated in M and RM compared to ML, and most were also down-regulated in M compared to RM.

Table 3

The number of differential metabolites among groups

Group name Total number of differences Down-regulated Up-regulated
M_vs_RM 44 15 29
ML_vs_M 38 29 9
ML_vs_RM 39 21 18

After cross-comparison of differential metabolites in three comparison groups in the Venn diagram, two common differential metabolites, sissotrin and eriodictyol O-malonylhexoside, were observed (Figure 7a), and 18 common differential metabolites were observed among comparison groups M vs RM and ML vs M. Twenty-two common differential metabolites were observed among comparison groups M vs RM and ML vs RM, in the comparison group, ML vs M and ML vs RM had 10 common metabolites. The results showed that the flavonoid metabolites causing differences in M, RM, and ML were different. Through the comparative analysis of metabolites among the three tissue parts in the Venn diagram (Figure 7b), it was found that there were unique metabolites among each tissue site, which was consistent with the results of the previous clustering heat map.

Figure 7 Venn diagram of differences in metabolites between groups (a) and among different medicinal parts (b).
Figure 7

Venn diagram of differences in metabolites between groups (a) and among different medicinal parts (b).

Different metabolites interact with each other to form different pathways. The KEGG database was used to annotate and display the different metabolites, as shown in Figure 8. KEGG classification results showed that the different metabolites were mainly involved in the biosynthesis of flavonoids and flavonol, isoflavone biosynthesis, flavonoid biosynthesis, and so on. Differential metabolites of M vs RM are mainly annotated and enriched in the biosynthesis of secondary metabolites, flavonoid biosynthesis, isoflavonoid biosynthesis, and flavone and flavonol biosynthesis. Differential metabolites of ML vs M are mainly annotated and enriched in flavone and flavonol biosynthesis and isoflavonoid biosynthesis. Differential metabolites of ML vs RM are mainly annotated and enriched in the biosynthesis of secondary metabolites, isoflavonoid biosynthesis, and flavonoid biosynthesis.

Figure 8 Comparison group M vs RM (a), ML vs M (b), and ML vs RM (c) differential metabolites KEGG classification.
Figure 8

Comparison group M vs RM (a), ML vs M (b), and ML vs RM (c) differential metabolites KEGG classification.

4 Discussion

Mulberry is a kind of common plant with medicinal and food value. Its leaves, branches, and fruits all have a hypoglycemic effect, but its clinical application is different, which may be caused by the difference in the content of some metabolites. In this study, the contents of flavonoid metabolites in three parts of mulberry were analyzed and compared. The results showed that there were significant differences in the content of flavonoid metabolites in the three parts. Compared with ML, most of the flavonoid metabolites of M and RM were down-regulated, and compared with RM, most of the flavonoid metabolites of m were down-regulated. The content of flavone in M was similar to that of the flavonol. According to the content of flavonoid, the medicinal value of ML and RM may be better than that of M. According to the enrichment results of KEGG, it is speculated that the functional differences may be caused by the content differences of flavone, flavonol, anthocyanins, and isoflavones.

4.1 Differential metabolites associated with flavonoids and flavonols

Compared with ML, the contents of flavone and flavonol in M and RM were lower. Rutin, a flavone, was identified in all samples, and there was no significant difference in content. Rutin can reduce cholesterol levels and reduce insulin resistance in diabetic mice through antioxidant stress and inflammatory reaction [10]. Luteolin was only identified in M and ML, and the content of M was higher than that of ML, but the content of its glycoside derivatives was generally lower than that of ML. Luteolin has good anti-inflammatory, antioxidant, and antidiabetic properties [11]. We found that 3′-oxymethyl myricetin was only identified in M. Myricetin and its glycoside derivatives had antioxidant, anti-inflammatory, and anti-diabetes activities, and it showed stronger antioxidant and anti-diabetes activities than other flavonoids [12]. There was no significant difference between the three parts. Astragaloside can regulate blood glucose and improve the antioxidant capacity of the body [13,14]. Quercetin has no significant difference in all three tissue parts, but its glycoside derivatives have differences. Quercetin and its derivatives have a variety of biological activities such as anti-cancer, hypoglycemic, anti-inflammatory, antioxidant, and so on [15].

4.2 Differential metabolites associated with anthocyanins

Anthocyanin is a kind of plant pigment, with a strong antioxidant function, which can eliminate free radicals and improve glucose and lipid metabolism, anti-inflammatory, and other effects [16]. Hu et al. study found that anthocyanins can ameliorate oxidative stress in the body and increase testosterone levels by inhibiting the production of reactive oxygen species to mitigate potential damage to mitochondrial membranes [17]. In Chen et al. study, anthocyanins reduced H2O2-induced oxidative stress in the retinal pigment epithelium by decreasing the level of oxidative products and increasing antioxidant enzyme activities, which could have a beneficial effect on age-related macular degeneration [18]. Similarly, anthocyanins can potentially benefit their associated diseases such as diabetes, obesity, inflammation, and cancer by ameliorating oxidative stress [19]. In this study, only geranium-3-O-glucoside and malvin were identified in RM. The contents of cyanidin galactoside and cyanidin-3-O-glucoside in RM were higher.

4.3 Differential metabolites associated with isoflavones

Isoflavone is ubiquitous in soybean. Fourteen isoflavones were detected in this study. It was worth noting that sissotrin was the only identified differential isoflavone metabolite among the three comparison groups. Sissotrin is only detected in ML and RM, but not in M. The content of RM is higher than that of ML, which has an antioxidant effect, but it has a weakening effect on glucose tolerance [20,21]. In this study, genistein was only identified in ML, which can inhibit angiogenesis and antioxidation and improve palmitic acid-induced insulin resistance in HepG2 cells [22].

The most abundant in M were 8-C-hexosyl-hesperetin O-hexoside and naringenin; the most abundant in ML were 8-C-hexosyl-hesperetin O-hexoside and astragalin; and the most abundant in RM were cyanidin 3-O-galactoside and gallocatechin–gallocatechin. Among the different sites, 8-C-hexosyl-hesperetin O-hexoside was the highest in ML, the next highest in M, and the lowest in RM; naringenin was the highest in M, the next highest in RM, and the lowest in ML; astragalin was the highest in ML, second in RM, and the lowest in M; cyanidin 3-O-galactoside and gallocatechin–gallocatechin were the highest in RM, second in ML, and the lowest in M. Lee et al. investigated the leaf and fruit contents of Korean mulberry variety Baekokwang flavonoid content, and in agreement with this study, the content was higher in ML than in M [23]. The reason for the differences in flavonoid content in different parts of the plant may be the differences in the expression of flavonoid-related genes [24]. Xu et al. studied the flavonoid biosynthesis genes in mulberry leaves at different harvest times and found that low temperatures may lead to an increase in flavonoid content by increasing the expression of flavonoid biosynthesis-related genes [25]. Similarly, the flavonoid content varied even in the same parts of the same species of mulberry in some findings [26], which may also be due to the harvest time and environment of mulberry, among others, influencing the expression of flavonoid-related genes. Although these factors may affect the content of flavonoid components to a certain extent by influencing gene expression, different parts of mulberry do have different medicinal properties, and the present study to explore the differences in flavonoid components of different parts of mulberry is an important revelation for a deeper understanding and guidance of mulberry application.

Some studies have shown that diabetes is associated with antioxidant activity, inflammation, as well as glycolipid metabolism, and the content differences of flavonoid metabolites in each site mainly involve flavone, flavonol, anthocyanins, isoflavone metabolic pathways, and the metabolites with differences in each pathway also show different degrees of antidiabetic activity, and the content of flavonoid metabolites in each site ML is comparable to that in RM and generally higher than that in M. Therefore, it was inferred from this plant metabolome that mulberry leaves and mulberry branches may be superior to mulberry fruits in their antidiabetic activities, and the reason for the difference in activities may result from the difference in flavone, flavonol, anthocyanins, and isoflavone contents. Subsequent studies can extract the effective sites at each site separately for experimental comparison and further verify this inference.

# Yewei Zhong and Fenglian Tong contributed equally to this work.

  1. Funding information: Financial support of this work was from the Xinjiang Uygur Autonomous Region of the major science and technology projects in China (Grant Numbers 2022A03019-3) and the Xinjiang Uygur Autonomous Region of the Tianshan Talent Program in China (Grant Numbers 2022TSYCCX0104).

  2. Author contributions: Y.Z. and F.T.: conceptualization, methodology, data analysis, manuscript writing. J.Y. and H.T.: conceptualization, data analysis. A.A. and R.Z.: sample collection, processing. Y.L. and D.L.: data collation and graphing. X.M.: funding acquisition, conceptualization, supervision, manuscript review and revising.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2023-11-01
Revised: 2024-05-04
Accepted: 2024-05-14
Published Online: 2024-06-27

© 2024 the author(s), published by De Gruyter

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

Articles in the same Issue

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  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
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https://doi.org/10.1515/biol-2022-0886
Keywords for this article
mulberry; flavonoid metabolites; UPLC–ESI-MS/MS
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
  8. Detection of serum interleukin-18 level and neutrophil/lymphocyte ratio in patients with antineutrophil cytoplasmic antibody-associated vasculitis and its clinical significance
  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
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  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
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  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
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  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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