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Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza

  • Haihui Fu , Jun Yuan EMAIL logo , Rongpeng Liu and Xiaoyun Wang EMAIL logo
Published/Copyright: May 24, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

Cadmium (Cd) could pose threats to human health by affecting Salvia miltiorrhiza (SM) safety. Cd enrichment trait and its effects on the active ingredient synthesis in SM remain unknown. Here we investigated the Cd concentration using ICP-MS-based method, physiologies (contents of malondialdehyde and proline, and activities of superoxide dismutase, peroxidase [POD], and catalase [CAT]), and LC-MS/MS-based metabolites of SM under 25, 50, and 100 mg kg−1 Cd stress. The results revealed that Cd concentrations, as it rose in soil, increased in roots and leaves of SM with transfer factors and bioconcentration factors below 1 in Cd-treated groups; POD and CAT activities and proline content increased and then declined. Amino acids and organic acids (especially d-glutamine [d-Gln], l-aspartic acid [l-Asp], l-phenylalanine [l-Phe], l-tyrosine [l-Tyr], geranylgeranyl-PP [GGPP], and rosmarinic acid [RA]) contributed more in discriminating SM roots of different groups. GGPP was negatively related to l-Tyr and l-Phe, and RA was positively related to d-Gln and l-Asp in SM. These results revealed that SM belonged to a non-Cd-hyperaccumulator with most Cd accumulated in roots, Cd could enhance phenolic acid synthesis via regulating amino acid metabolism and might inhibit tanshinone synthesis by declining the GGPP content, and proline, POD, and CAT played vital roles in resisting Cd stress. These provided new ideas and theoretical basis for further study on medical plants’ response to heavy metals.

Graphical abstract

Keywords: S. miltiorrhiza ; Cd stress; Cd enrichment; physiological characteristics; metabolic profiles

1 Introduction

With the booming of the economy and society, serious cadmium (Cd) pollution emerged in soils, which is caused by the unreasonable production in the long-term mining and smelting, and unreasonable farming in traditional agriculture growth [1,2]. Characterized by strong bioaccumulation, high bioavailability, and strong biotoxicity, Cd migrates easily from soil to plants, which can lead to the decline of plant yield and quality [3]. Eventually, Cd enters the human body via food chains, and seriously threatens people’s health [4]. Hence, much attention has been paid to soil Cd contamination [5,6].

The plant Cd concentration would increase under Cd stress. The absorbed Cd can break the balances of production and elimination of reactive oxygen species (ROS), change the physiological state (e.g., contents of malondialdehyde [MDA], proline, and soluble protein), and affect diverse metabolism systems [7,8,9]. And plants would regulate enzyme and non-enzyme-based antioxidant system, and metabolisms of sugars, amino acids, and organic acids to ameliorate Cd stress [7,10,11]. For instance, the MDA and proline concentrations, activities of SOD, POD, and CAT, and contents of sugars, amino acids, and organic acids changed significantly in maize (Zea mays) and wheat (Triticum aestivum) with Cd treatment compared with those of the control (without Cd) [12,13,14,15].

Salvia miltiorrhiza (SM) is a perennial plant and widely distributed in north and south China [16]. The dry roots and rhizomes (called Danshen in China) of SM contain tanshinone, salvianolic acid, rosemary, and other medicinal ingredients [10]. Nowadays, SM has been widely used to treat cerebrovascular and cardiovascular diseases, hyperlipidemia, and acute ischemic stroke in China and other Asian countries [10,17,18]. With the increasing need for Danshen, the planting area of SM has expanded year by year, which increases their risk of being contaminated. SM from some production areas contained Cd concentration above the limits set by the Chinese Pharmacopoeia Commission [3]. Much attention should be paid on the research of SM response to Cd.

The previous study has found that Cd could debase the quality of SM by inhibiting the accumulation of active ingredients [19]. However, little is known as relates to Cd enrichment trait and the effect of Cd pollution on the synthesis of active ingredients in SM. In this study, SM was used as the samples and a pot-culture experiment was conducted. The queries to be addressed are as follows: (1) What is the Cd enrichment laws of SM? (2) How does Cd affect the synthesis of active ingredients in SM based on metabolisms and physiologies? The study would assist with understanding how SM responds to Cd stress physiologically and metabolically, and provide new idea for the research on mechanism of SM in response to Cd.

2 Materials and methods

2.1 Soil preparation

The soil used in the pot experiment was collected from the topsoil (0–20 cm) in Shennong Garden of the Jiangxi University of Chinese Medicine in Jiangxi, China (E 115°44′24″, N 28°41′24″). The soil was air-dried, sieved to remove gravels through a 4 mm mesh sieve, and then mixed thoroughly. The basic physicochemical properties, including total nitrogen [N], available N, total phosphorus [P], available P, total potassium [K], available K, total Cd concentration, organic matter content, and pH value, were described in previous study [20]. The total Cd concentration was 0.95 mg kg−1, which is less than the critical value (1.0 mg kg−1) of the soil to ensure normal plant growth in agriculture and forestry production [21].

The appropriate contents of cadmium chloride hemi (pentahydrate) (CdCl2·2.5H2O, Sinopharm Chemical Reagent Co., Ltd, China) were thoroughly blended with soil to obtain the final concentrations of 25, 50, and 100 mg Cd per kilogram of soil, respectively. The selected Cd concentrations were consistent with that of previous studies of Wang et al. [22] and Zhang et al. [19]. Then, the soils with and without Cd treatment were transplanted into plastic pots (16 cm in diameter × 17 cm in height) and watered every 5 days with pure water. Before use, they were equilibrated for 30 days.

2.2 Plant material and Cd treatment

The source and treatment ways of SM seedlings were as per the study of Yuan et al. [13,20]. SM seedlings were purchased from SM planting areas (Shangdong, China). The formal identification of the samples was carried out by Assoc Prof. Xiaoyun Wang. Cultivated in Shennong garden for 30 days, the seedlings were transferred into appropriate pots containing 2.5 kg soil. Each pot contained two seedlings. A pot was taken as one replicate, and three replicates were performed for each treatment. In the experiment, seedlings without Cd treatment were used as the control group, and seedlings with 25, 50, 100 mg kg−1 Cd treatment were named TR, TS, and TT, respectively. The selected Cd concentrations were consistent with that of previous studies of Wang et al. [22] and Zhang et al. [19]. The experiment was conducted under non-greenhouse conditions. Each seedling presented uniform growth. After 15 days, plant samples were harvested for further study.

In order to perform LC-MS and physiological analyses, root samples from each pot were selected to make a composite root sample, simultaneously frozen in dry ice and stored at −80°C. Leaves and remaining roots from each pot were collected to make a composite leaf sample and root sample, respectively, to perform Cd concentration analysis. Then, both samples were dried in the oven at 60°C for 4 days. Voucher specimens (NO. DS-001) were deposited in a public herbarium in Research Center for Traditional Chinese Medicine Resources and Ethnic Minority Medicine of Jiangxi University of Chinese Medicine [20].

2.3 Determination of Cd concentration

The oven-dried samples were ground to fine powder, passed through a 2 mm sieve, and then digested with a mixture of nitric acid (HNO3) and hydrogen peroxide (H2O2) (3/1, v/v) in Teflon tanks using an electric heating board at 160℃ thoroughly. The Cd concentration was determined by inductively coupled plasma mass spectrometry (ICP-MS; Thermo Scientific, USA).

2.4 Physiological analysis

The ninhydrin colorimetry was used to determine the proline content [23,24]. A 0.05 g fresh root sample was pooled in the centrifugal tube with 5 mL of 3% sulfosalicylic acid, extracted in the boiling water bath for 10 min, and shaken frequently. The extraction was filtered into a volumetric flask. Then, the volume was constant to 25 mL with distilled water. A total of 2 mL of extraction solution mixed with 2 mL of glacial acetic acid and 2 mL of acidic ninhydrin was added in a centrifuge tube. The mixture was treated with the boiling water bath for 30 min. After cooling down to room temperature, 4 mL of toluene was added to the mixture and shaken thoroughly. When they were stratified during standing, the absorbance of the upper solution was measured at 520 nm with an ultraviolet spectrophotometer (UV-8000, Metash, China).

The content of MDA and activities of peroxidase (POD), superoxide dismutase (SOD), and catalase (CAT) were detected by assay kits (Suzhou Keming, China) [13]. A total of 0.1 g fresh samples and 1 mL solutions (1/10, v/v) were grounded in a water bath and centrifuged at 8,000 × g and 4℃ for 10 min. According to the manufacturer’s instructions, the supernatant absorbance was measured at 532 and 600 nm to assess MDA content, and at 470, 240, and 560 nm to evaluate the activities of POD, CAT, and SOD, respectively.

2.5 Metabolite analysis

The method of metabolite extraction was carried out as reported by Wang et al. [25] and Yuan et al. [13]. A total of 25 mg fresh samples was placed in a microcentrifuge tube with 500 μL of extract solution (methanol:water = 3:1 (v/v), with the isotopically labeled internal standard [IS] mixture), homogenized at 35 Hz for 4 min and sonicated for 5 min with an ice-water bath. The homogenization and sonication cycle were conducted three times. The samples were incubated for 1 h at −40℃ and centrifuged at 12,000 rpm and 4℃ for 15 min. Subsequently, the resulting supernatant was transplanted into a fresh glass vial for further analysis. Besides, the quality control (QC) sample was formed by mixing an equal aliquot of the supernatants from all samples [26].

Combining a UHPLC system (Vanquish; Thermo Fisher Scientific, USA) and Q Exactive HFX mass spectrometer (Orbitrap MS; Thermo, USA), LC-MS/MS analyses were performed to analyze sample metabolites using a Waters ACQUITY UPLC HSS T3 (2.1 mm × 100 mm, 1.8 μm; Waters, USA). Mobile phase A was water containing 5 mmol L−1 ammonium acetate and 5 mmol L−1 ammonia hydroxide, while mobile phase B was acetonitrile. The analysis was carried with elution gradient as follows: 0–0.7 min, 1.0% B; 0.7–9.5 min, 1.0–99% B; 9.5–11.8 min, 99% B; 11.8–12.0 min, 99–1% B; 12–14.8 min, 1.0% B. The column temperature was 35℃. The auto-sampler temperature was 4℃, the injection volume was 3 μL, and the flow rate was 0.5 mL min−1. The QE HFX mass spectrometer was conducted to acquire MS/MS spectra based on information-dependent acquisition mode in controlling the acquisition software (Xcalibur; Thermo, USA). In the mode, the acquisition software continuously evaluated the full scan MS spectrum. The ESI source conditions were conducted as follows: the flow rates of sheath gas and Aux gas were 30 Arb and 10 Arb, respectively, the capillary temperature was 350℃, the full MS resolution was 60,000, the MS/MS resolution was 7,500, the collision energy was 10/30/60 in NCE mod, and the spray voltage was 4.0 kV (positive) or −3.8 kV (negative).

After the original data were converted into mzXML format using the software ProteoWizard (https://proteowizard.sourceforge.io/), the R package XCMS (version 3.2) was used for the peak recognition, extraction, alignment, and integration. The preprocesses of the original data included the following: (1) Data filtering: The filtering standard was to remove the data with no definite substance name or no spectrum comparison similarity. (2) Missing values processing: Substances of more than 50% missing in comparisons were filtered directly, and substances of less than 50% missing were performed the imputation of missing values using the k-nearest neighbor algorithm. (3) Normalization: The IS or total ion current of each sample was used for the normalization. A total of 1,111 and 305 peaks of the original data were retained for positive and negative ion modes, respectively. The excel sheets, including the name of peak and sample, and the standard data of normalized peak area were obtained for further data analysis.

2.6 Statistical analysis

The changes in the Cd enrichment, and physiological and metabolic traits were presented in the study coupled with the results of the previous study [13,20]. First, the transfer factor (TF) and bioconcentration factor (BCF) of Cd were calculated as follows [27,28,29]:

TF = Cd concentration of aboveground parts (mg kg−1)/Cd concentration of roots (mg kg−1),

BCF = Cd concentration in the tissues/Cd concentration in soils.

Second, the multivariate ordination principal component analysis (PCA) was conducted to reveal the overall distribution of the samples. The supervised partial least squares discrimination analysis (PLS-DA) was utilized to assess the differences in roots between the control and Cd treatment groups. The PLS-DA model was validated by permutation tests (200) or ANOVA of the cross-validated residuals (CV-ANOVA). A Q2 value of above 0.5 and an R2 value of above 0.7 for the permutation test or p value of below 0.05 for the CV-ANOVA denoted the highly significant model [30]. The variable importance in projection (VIP) was crucial for explaining the data of the PLS-DA model. Metabolites with a p value of below 0.05 and a VIP of above 1.0 were filtered out as differential metabolites, playing larger roles in distinguishing roots between the control and Cd addition groups [20].

Third, the pathway analysis of all the metabolites was conducted by the software MetaboAnalyst 4.0 (http://www. metaboanalyst.ca/faces/ModuleView.xhtml). Based on the pathway impact value of above 0.1, the potential metabolic target pathways were obtained [20,31]. The Venn diagram was obtained using the software Venny 2.1 (http://bioinfogp.cnb.csic.es/tools/venny/) to present the overlap of all the named metabolites in the control and Cd treatment groups. Subsequently, t-test and correlation analyses were conducted to evaluate the variability of identical metabolites in samples, and relationships between Cd concentration in tissues (leaves and roots) and Cd concentration in soils and relationships among Cd concentration, contents of Pro and MDA, activities of SOD, CAT, and POD, and relative contents of d-glutamine (d-Gln), l-aspartic acid (l-Asp), l-tyrosine (l-Tyr), l-phenylalanine (l-Phe), geranylgeranyl-PP (GGPP), and rosmarinic acid (RA) in roots with SPSS 18.0 (SPSS Inc., USA), respectively. The PCA and PLS-DA models were performed by SIMCA-P version 14.1 (Umetrics, Sweden). All data were log10-transformed before analysis.

3 Results

3.1 Cd concentration in leaves and roots

With the increase in soil Cd concentration, Cd concentrations in leaves and roots increased significantly (p < 0.05) (Figure 1a–c). Under 100 mg kg−1 Cd stress, Cd concentrations both in leaves and roots reached the maximum (15.53 mg kg−1 for leaves and 16.66 mg kg−1 for roots), which were 99.68 and 99.70% higher than that in the control group, respectively (Figure 1a and b).

Figure 1 Enrichment characteristics of Cd in leaves and roots of S. miltiorrhiza with different levels of soil Cd stress. (a) and (b) Cd concentration in SM leaves and roots with different levels of soil Cd stress, respectively, and the data are presented as the mean value ± SE (n = 3); (c) relationships of Cd concentration in leaves and roots and soil Cd concentration, respectively; different letters indicate significant differences among different treatments.
Figure 1

Enrichment characteristics of Cd in leaves and roots of S. miltiorrhiza with different levels of soil Cd stress. (a) and (b) Cd concentration in SM leaves and roots with different levels of soil Cd stress, respectively, and the data are presented as the mean value ± SE (n = 3); (c) relationships of Cd concentration in leaves and roots and soil Cd concentration, respectively; different letters indicate significant differences among different treatments.

Besides, with the increase in soil Cd concentration, the TF and BCF of SM changed significantly (p < 0.05). The max-TF was presented in roots of the control group (Table 1). As soil Cd concentration rose, the seedling BCF value decreased first, then increased, and finally declined significantly (p < 0.05), while the max-BCF value was also in the control group (Table 1). With the increase in soil Cd concentration, the BCFs in roots increased. The BCFs of tissue samples with 100 mg kg−1 Cd treatment were higher than those in other groups (p < 0.05) (Table 1). All TFs and BCFs were below 1 except the TF value in roots of the control group (Table 1).

Table 1

TF and BCF of SM under different levels of Cd stress

Cd treatment TF BCF of roots BCF of leaves BCF of the seedlings
CK 1.00 ± 0.02a 0.05 ± 0.00a 0.05 ± 0.00a 0.95 ± 0.00a
TR 0.21 ± 0.01b 0.13 ± 0.00b 0.03 ± 0.00b 0.43 ± 0.01b
TS 0.23 ± 0.00b 0.12 ± 0.00b 0.03 ± 0.00b 0.65 ± 0.01c
TT 0.93 ± 0.04a 0.17 ± 0.00c 0.16 ± 0.00c 0.52 ± 0.01d

CK, TR, TS, and TT stand for roots in the control, 25 mg kg−1 Cd, 50 mg kg−1 Cd, and 100 mg kg−1 Cd group, respectively (the same below). The data were presented as the mean value ± SE (n = 3). The data with different little letters in same column show significant difference (p < 0.05).

3.2 Physiological characteristics in roots

The proline content in roots went up significantly at first and then went down significantly with an increase in soil Cd concentration (p < 0.05). The proline content in 50 mg kg−1 Cd added group was higher than other groups (p < 0.05) (Figure 2a). But as soil Cd concentration increased, the MDA content declined (Figure 2b). The activities of POD and CAT in roots increased and then decreased significantly with the increase in soil Cd concentration (p < 0.05) (Figure 2c and d). The maximal activities of POD and CAT both appeared in roots of 50 mg kg−1 Cd added group (Figure 2c and d). However, the SOD activity of roots revealed no significant differences in different levels of Cd-contaminated groups (Figure 2e).

Figure 2 Physiological characteristics of SM roots with different levels of soil Cd stress. (a) and (b) Effect of Cd on the content of proline (a) and MDA (b) in SM roots, respectively. (c)–(e) Effect of Cd on the activities of POD, CAT, and SOD in SM roots, respectively. The data were presented as the mean value ± SE (n = 3); different letters indicate significant differences among different treatments.
Figure 2

Physiological characteristics of SM roots with different levels of soil Cd stress. (a) and (b) Effect of Cd on the content of proline (a) and MDA (b) in SM roots, respectively. (c)–(e) Effect of Cd on the activities of POD, CAT, and SOD in SM roots, respectively. The data were presented as the mean value ± SE (n = 3); different letters indicate significant differences among different treatments.

3.3 Metabolomic changes in roots

A total of 305 metabolites were identified, as shown in the previous study (Table S1). Most of them were C-containing and N-containing metabolites (e.g., amino acids, organic acids, fatty acids, etc.). The relative contents of these metabolites of the control group differed from those in Cd-treated groups (Figures 4 and 5; Figure A1; Table S1). Besides, a metabolic map was obtained according to pathway analysis results, involving all the identified metabolites (Figure 5). The target pathways (with the PI value of above 0.1) are presented in Table S3, coupled with amino acid metabolism and some secondary metabolism as the central metabolic pathways (Table S2). Some of them were involved in the synthesis of active ingredients (Figure 5).

Figure 3 Changes in metabolites in SM roots under different levels of Cd stress. (a) The score plots of PCA for metabolomic data from SM roots under different levels of Cd stress PC1, the first principal component; PC2, the second principal component. The ellipse indicates the Hotelling’s T2 (95%); (b–d) score plots of PLS-DA for metabolomic data from SM roots of the control and the 25 mg kg−1 (b), 50 mg kg−1 (c), and 100 mg kg−1 (d) Cd group, respectively.
Figure 3

Changes in metabolites in SM roots under different levels of Cd stress. (a) The score plots of PCA for metabolomic data from SM roots under different levels of Cd stress PC1, the first principal component; PC2, the second principal component. The ellipse indicates the Hotelling’s T2 (95%); (b–d) score plots of PLS-DA for metabolomic data from SM roots of the control and the 25 mg kg−1 (b), 50 mg kg−1 (c), and 100 mg kg−1 (d) Cd group, respectively.

Figure 4 Variation in the differential metabolites in SM roots under different levels of Cd stress. (a–c) Overlap of the up-differential metabolites, down-differential metabolites, and all the differential metabolites of SM roots in response to different Cd stress, respectively. (d) Heatmap analysis of the same differential metabolites in SM roots in response to different Cd stress.
Figure 4

Variation in the differential metabolites in SM roots under different levels of Cd stress. (a–c) Overlap of the up-differential metabolites, down-differential metabolites, and all the differential metabolites of SM roots in response to different Cd stress, respectively. (d) Heatmap analysis of the same differential metabolites in SM roots in response to different Cd stress.

Figure 5 Relative contents of l-Phe (a), l-Tyr (b), d-Gln (c), l-Asp (d), GGPP (e), and RA (f) of SM roots under different levels of Cd stress. The data are presented as the mean value ± SE (n = 3); different letters indicate significant differences among different treatments.
Figure 5

Relative contents of l-Phe (a), l-Tyr (b), d-Gln (c), l-Asp (d), GGPP (e), and RA (f) of SM roots under different levels of Cd stress. The data are presented as the mean value ± SE (n = 3); different letters indicate significant differences among different treatments.

3.4 Differential metabolites in roots

According to the result of PCA analysis and PLS-DA models, root samples in the control and Cd treatment groups were clearly distinguished in the pot experiment (Figure 3). The results of the significant PLS-DA model (with VIP of above 1) and the t-test (with a p value below 0.05) (Figure 3b–d and Figure A2) facilitated the identification of differential metabolites, with 175 differential metabolites for the discrimination of the control group and 25 mg kg−1 Cd-added group, 161 for the discrimination of the control group and 50 mg kg−1 Cd-added group, and 192 for the discrimination of the control group and 100 mg kg−1 Cd-added group (Figure 4; Tables S1 and S2).

Most of the same differential metabolites identified in all the groups were amino acids and organic acids (Figure 4d). This differed from the previous studies, which adopted different data processing methods [12,19]. The major contributors from these metabolites could take part in the synthesis of salvianolic acids and tanshinones (Figures 4 and 6; Table S3). With the increase in the soil Cd concentration, the relative contents of l-Phe and l-Tyr increased and then decreased significantly (p < 0.05) (Figure 5a and b), but relative contents of d-Gln and l-Asp declined and then increased significantly (p < 0.05) (Figure 5c and d). The maximum relative contents of l-Phe and l-Tyr are both shown in roots with the treatment of 100 mg kg−1 Cd (Figure 5a and b). Besides, with the increase in the soil Cd concentration, the relative content of GGPP decreased and then increased significantly (p < 0.05) (Figure 5e), and the relative content of RA increased significantly (p < 0.05) (Figure 5f). Besides, GGPP was negatively correlated with l-Tyr and l-Phe, respectively (p < 0.05); RA was positively correlated with d-Gln and l-Asp, respectively (p < 0.05); l-Asp was positively correlated with d-Gln (p < 0.05) (Table 2).

Figure 6 Schematic diagram of the metabolic pathways under different levels of Cd stress. l-Tyr, l-Phe, GGPP, and GAs stand for l-Tyrosine, l-Phenylalanine, GGPP, and gibberellins, respectively. Metabolisms in orange, blue, and red backgrounds were amino acid metabolism, synthesis of tanshinones, and synthesis of salvianolic acids, respectively. log2(FC) stands for an estimate of the log2-transformed ratio of the relative content of metabolites in roots of the Cd stress group to that of the control group; R, S, and T stand for an estimate of the log2-transformed ratio of the relative content of metabolites in roots of the 25, 50, and 100 mg kg−1 Cd stress group to that of the control group, respectively.
Figure 6

Schematic diagram of the metabolic pathways under different levels of Cd stress. l-Tyr, l-Phe, GGPP, and GAs stand for l-Tyrosine, l-Phenylalanine, GGPP, and gibberellins, respectively. Metabolisms in orange, blue, and red backgrounds were amino acid metabolism, synthesis of tanshinones, and synthesis of salvianolic acids, respectively. log2(FC) stands for an estimate of the log2-transformed ratio of the relative content of metabolites in roots of the Cd stress group to that of the control group; R, S, and T stand for an estimate of the log2-transformed ratio of the relative content of metabolites in roots of the 25, 50, and 100 mg kg−1 Cd stress group to that of the control group, respectively.

Table 2

Correlations (r, Pearson’s correlation coefficient) among SOD, CAT, POD, d-Gln, l-Asp, l-Tyr, l-Phe, GGPP, and RA in SM roots

R SOD CAT POD d-Gln l-Asp l-Tyr l-Phe GGPP RA
SOD 1
CAT −0.03 1
POD −0.24 0.26 1
d-Gln −0.41 −0.23 −0.32 1
l-Asp −0.28 0.34 −0.19 0.79** 1
l-Tyr 0.01 0.77** 0.66* −0.58 −0.18 1
l-Phe 0.26 0.92** 0.14 −0.42 0.21 0.74** 1
GGPP −0.38 −0.59 −0.34 0.88** 0.42 −0.76 ** −0.77 ** 1
RA −0.10 0.54 −0.26 0.61 * 0.95 ** 0.03 0.46 0.20 1

l-Asp, l-Tyr, l-Phe, GGPP, and RA stand for proline, d-glutamine, l-aspartic acid, l-tyrosine, l-phenylalanine, geranylgeranyl-PP, and rosmarinic acid, respectively; significance, p value < 0.05: * , p < 0.05; ** , p < 0.01.

4 Discussion

4.1 Accumulation characteristics of Cd in SM

The study revealed that SM was a non-Cd-hyperaccumulator with a substantial part of Cd enriched in roots. Although in the pot experiment, Cd concentration in leaves was lower than that in roots under each level of soil Cd treatment, the Cd concentration in the two tissues was much smaller than 100 mg kg−1 (the threshold value for the Cd-hyperaccumulator in soils is 100 mg kg−1 Cd) (Figure 1). TF could reveal the ability to enrich and transport heavy metals from roots to aboveground parts in plants [28]. BCF could reflect the enrichment ability of plants [29]. All the TFs and BCFs in Cd addition groups were below 1 (Table 1). The enrichment characteristics of Cd in SM differed from the Cd-hyperaccumulators, which could enrich at least 100 mg kg−1 Cd in soils of 100 mg kg−1 Cd or more, with the TF and the seedling BCF of above 1 under different levels of Cd stress [5,32].

Simultaneously, in the study, with the increase in the Cd concentration, change trend of POD and CAT activities, and the proline content in SM were different from those in hyperaccumulator Phytolacca americana (Figure 2) [33]. As soil Cd concentration rose, SM absorbed much Cd in roots, part of which was transferred to leaves, resulting in the increase in the leaf Cd concentration (Figure 1a). As soil-added Cd levels increased, the dilution of root Cd was enhanced along with the remarkable increase in TF and BCFs (Table 1; Figure 1) [34]. Similarly, with the increasing concentration of added Cd, Cd concentration in roots and leaves of Murraya paniculata, Catharanthus roseus, and Loropetalum chinense increased, and the roots of all these plants could accumulate more Cd than the leaves [35].

Other Cd was accumulated in roots and root Cd concentration increased. The abiotic stress could cause metabolic disorders which affected cell mass, lipid content, and/or morphological structures [15]. The enhanced Cd would lead to the accumulation of ROS and the peroxidation of membrane lipid in Cd non-hyperaccumulating plants [36,37]. The synergism of antioxidant enzymes (e.g., POD, CAT, and SOD) in plants could eliminate oxygen free radical and alleviate Cd toxicity with the antioxidant enzymes activities significantly increasing under low Cd stress (Figure 2). In many non-Cd-hyperaccumulators, due to low Cd tolerance, the activities of antioxidant enzymes would present a declining trend with the increase in the Cd level [7,12]. However, they might still remarkably clean the active oxygen free radical and lower the lipid peroxidation of plants, resulting in the lower MDA content of plants under Cd stress than that in other Cd-contaminated plants (Figure 2) [7]. The change trends of the antioxidant enzyme activities differed from those of P. americana, but showed the same change as Daucus carota, under Cd stress conditions [38,39].

4.2 Effect of Cd on the synthesis of phenolic acids in SM

Cd stress enhanced the synthesis of phenolic acids (especially RA) in SM roots, which was the precursor of other salvianolic acids with complex structure, theoretically, and boosted with soil Cd increasing (Figure 5) [8,40]. In the study, the major contributors in distinguishing the samples in different levels of Cd stress groups included d-Gln, l-Phe, l-Tyr, and RA (Figure 4; Table S2). First, SM roots could enhance the synthesis of RA indirectly by regulating the metabolism of d-Gln and l-Asp (Figure 6). Amino acids (e.g., Gln, Asp, and Tyr) could participate in the detoxification of plants, such as nitrogen metabolism and secondary metabolism [41,42,43], and bind with the heavy metal ions to reduce their toxicity [14]. Among them, Gln was the first type of organic N compounds converted from N absorbed by plants from soils and participated in various life activities (e.g., amino acid metabolism) [11], and Asp was a free amino acid, and acted as the amino donor of amino acid metabolism, nucleotide metabolism, and TCA cycle [44]. In the current study, l-Asp was positively correlated with d-Gln, and both d-Gln and l-Asp were positively correlated with RA (p < 0.05) and, as soil-added Cd concentration increased from 25 to 100 mg kg−1, the relative contents of d-Gln and l-Asp increased (Figure 5; Table 2). This might be because as soil Cd concentration increased, the increased d-Gln formed into glutamate, which was a free amino acid, as l-Asp was, and could bind Cd and alleviate toxic effects of Cd on roots (Figure 6) [45]. This might retain the concentration of free Cd in roots to the level to enhance some metabolisms (e.g., RA synthesis) (Figure 6) [6]. By the way, this also suggested that amino group was the main site of Cd binding in SM.

Second, SM roots could enhance the synthesis of RA indirectly by regulating the metabolism of l-Phe and l-Tyr (Figure 6). l-Phe and l-Tyr were the precursors of phenylpropanoid pathway and the tyrosine-derived pathway, respectively, and both the pathways were involved in the biosynthesis of RA [8]. In the study, as soil-added Cd concentration changed from 0 to 50 mg kg−1, relative contents of RA, l-Phe, and l-Tyr increased significantly (p < 0.05) (Figure 5). However, with soil-added Cd concentration increasing from 50 to 100 mg kg−1, the relative content of RA increased significantly and relative contents of l-Phe and l-Tyr declined significantly (p < 0.05), with the relative contents of both the amino acids in roots of 100 mg kg−1 Cd-added group becoming twice more than that of the control group, respectively (Figure 5). Both POD and CAT showed positive correlations with l-Tyr, and CAT was positively correlated with l-Phe (Table 2). This might be caused by that, although both the relative contents of l-Phe and l-Tyr declined as soil Cd concentration ranged from 50 to 100 mg kg−1, the accumulated l-Phe and l-Tyr, coupled with the enhancement of POD and CAT activities, could also promote the synthesis of RA in SM roots (Table 2), which in turn could alleviate Cd toxicity [14]. Conversely, Strejckova et al. [46] and Zhang et al. [19] proved that Cd stress restrained the synthesis of RA in Scenedesmus quadricauda and SM, respectively. The differences might be resulted from that the tolerance and response to Cd varied greatly among plants of different species, varieties, or populations [47].

4.3 Effect of Cd on the synthesis of tanshinones in SM

As reported above, GGPP was one of the major contributors mainly in distinguishing samples of the control and Cd-added groups (Table S2). GGPP was the critical precursor of synthesizing tanshinones, parts of the main active ingredients of SM roots [8]. In the present study, with increasing soil Cd concentration, the relative content of GGPP significantly decreased and then increased (p < 0.05), with the relative content of GGPP in the control group higher than those in the Cd-added groups (Figure 5e). This illustrated that Cd stress could suppress the synthesis of tanshinones. Consistent with the result of the study, Zhang et al. [19] revealed that the accumulation of tanshinones was higher in the control group than that of the Cd-treated group. This might be caused by the comprehensive regulation of metabolites and genes.

On the one hand, the synthesis of tanshinones was inhibited due to the competitive consumption of phosphoenol pyruvate (PEP) in the process of phenolic acid accumulation in SM roots under Cd stress. PEP is an important metabolite connecting glycolysis, tanshinone synthesis, and phenolic acid synthesis (Figure 6) [48]. In the study, GGPP was negatively correlated with both l-Tyr and l-Phe (p < 0.05), both of which were closely related to RA synthesis (Figure 6; Table 2) [8]. With high concentration of Cd stress, RA was enriched in SM roots (Figure 5). This would consume a certain amount of PEP, which might lead to the content of PEP being lower than the detectable level and the decrease in GGPP in the study (Table S1). On the other hand, Cd stress suppressed the synthesis of tanshinones via downregulating the expression of GGPPS genes. In the present study, the relative content of GGPP in the control group was higher than those of all the Cd-added groups in SM roots (Figure 5e). The expression of genes in SM roots could be affected by Cd stress [49]. Ali et al. [50] discovered that Cd could downregulate the expression of GGPPS genes, exhibiting a wide range of responses to abiotic stresses, and suppressed the activities of GGPP synthases in SM roots.

5 Conclusion

Cd is one of the major heavy metal pollutants in the environment threatening human health by affecting medicinal plant quality. Our study characterized the associated roles of physiological and metabolic regulation in the synthesis of active ingredients in SM with different levels of Cd treatment. First, in all groups, the Cd concentration in leaves was lower than that in roots, and all the TF and BCFs in Cd-treated groups were below 1. Besides, with the increase in the soil Cd concentration, the proline content increased and then declined significantly with the decrease in MDA content; activities of POD and CAT rose and then declined significantly with SOD activity showing no significant differences. This verified that SM was a non-Cd-hyperaccumulator and primarily enriched Cd in roots, with proline, POD, and CAT playing vital roles in resisting Cd stress.

Second, amino acids (especially d-Gln, l-Tyr, l-Asp, and l-Phe) and organic acids (especially GGPP and RA) were major contributors in significantly distinguishing samples with different levels of Cd. As soil Cd concentration increased, the relative content of RA increased significantly, GGPP decreased and then increased significantly with GGPP relative content in control group higher than those in Cd-treated groups, d-Gln and l-Asp declined and then increased, and l-Phe and l-Tyr first increased and then decreased. Besides, RA was positively related to both d-Gln and l-Asp, and GGPP was negatively related to both l-Tyr and l-Phe. This illustrated that Cd treatment enhanced the synthesis of RA by regulating the metabolism of amino acids (especially d-Gln, l-Tyr, l-Asp, and l-Phe) but might suppress the synthesis of tanshinones by decreasing the content of GGPP. The findings revealed Cd enrichment laws of SM and its active ingredient synthesis response to Cd by regulating metabolism and physiology. This provides theoretical basis for the further study on molecular mechanisms of SM response to Cd.

# Haihui Fu and Jun Yuan contributed equally to this work.

Acknowledgements

We are grateful for the support by Nanjing Genepioneer Biotechnologies Co. Ltd, during metabolomics analysis, and the help of Assoc. Prof. Yuye Zhu (School of Pharmacy of Jiangxi University of traditional Chinese Medicine) during seedling cultivation.

  1. Funding information: This work was funded by the Jiangxi Education Department S&T Program [GJJ2200978], Jiangxi Provincial Health Commission S&T Plan [SKJP220227132], Jiangxi Provincial Administration of Traditional Chinese Medicine S&T Program [2022A392], Scientific Research Foundation for Doctor of the Jiangxi University of Chinese Medicine [2020BSZR011], and Joint Project with the Government of Zhangshu City, Jiangxi Province [20220346].

  2. Author contributions: All authors contributed to the study conception and design material preparation. Data collection and analysis were performed by Jun Yuan, and Haihui Fu. The first draft of the manuscript was written by Jun Yuan, Haihui Fu, and Xiaoyun Wang, and all authors commented on previous versions of the manuscript. All authors have read and agreed to the present version of the manuscript.

  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.

Appendix

Figure A1 Classification characteristics of metabolites in SM roots with different levels of soil Cd stress. (a–d) Classification characteristics of metabolites in SM roots of the control, 25, 50, and 100 mg kg−1 Cd group, respectively.
Figure A1

Classification characteristics of metabolites in SM roots with different levels of soil Cd stress. (a–d) Classification characteristics of metabolites in SM roots of the control, 25, 50, and 100 mg kg−1 Cd group, respectively.

Figure A2 Permutation test results of PLS-DA models for metabolomic data from SM roots. (a–c) The permutation test results of PLS-DA models for roots of the control and 25 mg kg−1 Cd group (R2Y[1] = 0.99, Q2[1] = 0.58, CV-ANOVA p = 0.03), of the control and 50 mg kg−1 Cd group (R2Y[1] = 0.97, Q2[1] = 0.54, CV-ANOVA p = 0.03) and of the control and 100 mg kg−1 Cd group (R2Y[1] = 0.93, Q2[1] = 0.47, CV-ANOVA p = 0.01), respectively.
Figure A2

Permutation test results of PLS-DA models for metabolomic data from SM roots. (a–c) The permutation test results of PLS-DA models for roots of the control and 25 mg kg−1 Cd group (R2Y[1] = 0.99, Q2[1] = 0.58, CV-ANOVA p = 0.03), of the control and 50 mg kg−1 Cd group (R2Y[1] = 0.97, Q2[1] = 0.54, CV-ANOVA p = 0.03) and of the control and 100 mg kg−1 Cd group (R2Y[1] = 0.93, Q2[1] = 0.47, CV-ANOVA p = 0.01), respectively.

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Received: 2023-01-03
Revised: 2023-03-21
Accepted: 2023-03-25
Published Online: 2023-05-24

© 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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  77. Screening of the best time window for MSC transplantation to treat acute myocardial infarction with SDF-1α antibody-loaded targeted ultrasonic microbubbles: An in vivo study in miniswine
  78. Inhibition of TAZ impairs the migration ability of melanoma cells
  79. Molecular complexity analysis of the diagnosis of Gitelman syndrome in China
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  81. Identification of winter wheat pests and diseases based on improved convolutional neural network
  82. Ultra-multiplex PCR technique to guide treatment of Aspergillus-infected aortic valve prostheses
  83. Virtual high-throughput screening: Potential inhibitors targeting aminopeptidase N (CD13) and PIKfyve for SARS-CoV-2
  84. Immune checkpoint inhibitors in cancer patients with COVID-19
  85. Utility of methylene blue mixed with autologous blood in preoperative localization of pulmonary nodules and masses
  86. Integrated analysis of the microbiome and transcriptome in stomach adenocarcinoma
  87. Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy
  88. DUSP2 inhibits the progression of lupus nephritis in mice by regulating the STAT3 pathway
  89. Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series
  90. Genetic alterations of KRAS and TP53 in intrahepatic cholangiocarcinoma associated with poor prognosis
  91. Granulomatous polyangiitis involving the fourth ventricle: Report of a rare case and a literature review
  92. Studying infant mortality: A demographic analysis based on data mining models
  93. Metaplastic breast carcinoma with osseous differentiation: A report of a rare case and literature review
  94. Protein Z modulates the metastasis of lung adenocarcinoma cells
  95. Inhibition of pyroptosis and apoptosis by capsaicin protects against LPS-induced acute kidney injury through TRPV1/UCP2 axis in vitro
  96. TAK-242, a toll-like receptor 4 antagonist, against brain injury by alleviates autophagy and inflammation in rats
  97. Primary mediastinum Ewing’s sarcoma with pleural effusion: A case report and literature review
  98. Association of ADRB2 gene polymorphisms and intestinal microbiota in Chinese Han adolescents
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  100. Study on the cytokines related to SARS-Cov-2 in testicular cells and the interaction network between cells based on scRNA-seq data
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  102. HP1 induces ferroptosis of renal tubular epithelial cells through NRF2 pathway in diabetic nephropathy
  103. Intravaginal estrogen management in postmenopausal patients with vaginal squamous intraepithelial lesions along with CO2 laser ablation: A retrospective study
  104. Hepatocellular carcinoma cell differentiation trajectory predicts immunotherapy, potential therapeutic drugs, and prognosis of patients
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  106. Identification of lysosome-related genes in connection with prognosis and immune cell infiltration for drug candidates in head and neck cancer
  107. Development of an instrument-free and low-cost ELISA dot-blot test to detect antibodies against SARS-CoV-2
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  110. The G protein-coupled receptor-related gene signatures for predicting prognosis and immunotherapy response in bladder urothelial carcinoma
  111. α-Fetoprotein contributes to the malignant biological properties of AFP-producing gastric cancer
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  114. Significance of sTREM-1 and sST2 combined diagnosis for sepsis detection and prognosis prediction
  115. Diagnostic value of serum neuroactive substances in the acute exacerbation of chronic obstructive pulmonary disease complicated with depression
  116. Research progress of AMP-activated protein kinase and cardiac aging
  117. TRIM29 knockdown prevented the colon cancer progression through decreasing the ubiquitination levels of KRT5
  118. Cross-talk between gut microbiota and liver steatosis: Complications and therapeutic target
  119. Metastasis from small cell lung cancer to ovary: A case report
  120. The early diagnosis and pathogenic mechanisms of sepsis-related acute kidney injury
  121. The effect of NK cell therapy on sepsis secondary to lung cancer: A case report
  122. Erianin alleviates collagen-induced arthritis in mice by inhibiting Th17 cell differentiation
  123. Loss of ACOX1 in clear cell renal cell carcinoma and its correlation with clinical features
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  125. Crosstalk between lactic acid and immune regulation and its value in the diagnosis and treatment of liver failure
  126. Clinicopathological features and differential diagnosis of gastric pleomorphic giant cell carcinoma
  127. Traumatic brain injury and rTMS-ERPs: Case report and literature review
  128. Extracellular fibrin promotes non-small cell lung cancer progression through integrin β1/PTEN/AKT signaling
  129. Knockdown of DLK4 inhibits non-small cell lung cancer tumor growth by downregulating CKS2
  130. The co-expression pattern of VEGFR-2 with indicators related to proliferation, apoptosis, and differentiation of anagen hair follicles
  131. Inflammation-related signaling pathways in tendinopathy
  132. CD4+ T cell count in HIV/TB co-infection and co-occurrence with HL: Case report and literature review
  133. Clinical analysis of severe Chlamydia psittaci pneumonia: Case series study
  134. Bioinformatics analysis to identify potential biomarkers for the pulmonary artery hypertension associated with the basement membrane
  135. Influence of MTHFR polymorphism, alone or in combination with smoking and alcohol consumption, on cancer susceptibility
  136. Catharanthus roseus (L.) G. Don counteracts the ampicillin resistance in multiple antibiotic-resistant Staphylococcus aureus by downregulation of PBP2a synthesis
  137. Combination of a bronchogenic cyst in the thoracic spinal canal with chronic myelocytic leukemia
  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
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  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
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  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
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  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
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  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0603
Keywords for this article
S. miltiorrhiza; Cd stress; Cd enrichment; physiological characteristics; metabolic profiles
Creative Commons
BY 4.0

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  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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