Startseite Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
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Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress

  • Mengyan Zhang , Lin Zhao EMAIL logo , Zhenyu Yun , Xi Wu und Qi Wu
Veröffentlicht/Copyright: 6. November 2024
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Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 19 Heft 1

Abstract

Copper (Cu) is considered one of the major heavy metal pollutants in agriculture, leading to reductions in crop yield. To reveal the molecular mechanisms of resistance to copper stress in maize (Zea mays L.) seedlings, transcriptome analysis was conducted on the hybrid variety Zhengdan 958 exposed to 0 (control), 5, and 10 mM Cu stress using RNA-seq. In total, 619, 2,685, and 1,790 differentially expressed genes (DEGs) were identified compared to 5 mM versus 0 mM Cu, 10 mM versus 0 mM Cu, and 10 mM versus 5 mM Cu, respectively. Functional categorization of DEGs according to Gene Ontology revealed that heme binding, defense response, and multiorganism processes were significantly enriched under copper stress. Additionally, Kyoto Encyclopedia of Genes and Genomes enrichment analysis suggested that the copper stress response is mediated by pathways involving phenylpropanoid biosynthesis, flavonoid biosynthesis, and glutathione metabolism, among others. The transcriptome data demonstrated that metabolite biosynthesis and glutathione metabolism play key roles in the response of maize seedlings to copper stress, and these findings provide valuable information for enhancing copper resistance in maize.

Keywords: maize; copper stress; transcriptome; differential expression analysis; functional classification; KEGG pathway

1 Introduction

Heavy metals are regarded as hazards to the environment and living organisms. Global agricultural soil pollution by heavy metals is a serious concern due to their impacts on crop yields and health risks throughout the food chain [1]. Among heavy metals, copper is an essential micronutrient for plants and participates in various morphological, physiological, and biochemical processes [2]. However, the use of Cu-containing herbicides, insecticides, and fungicides, and discharge from industrial wastewater and sewage sludge result in large amounts of copper entering the ecosystem [3]. A copper concentration in soil that exceeds a certain threshold inhibits the metabolic function, damages the cell membrane integrity, interferes with seed germination and seedling emergence, and even causes plant death [4,5,6]. Rice growth is severely inhibited by high soil Cu levels (300–500 mg/kg or above), and the roots are more sensitive than other parts of rice plants [7,8]. Excessive copper significantly reduces photosynthesis but enhances the lignification of cell walls, thus slowing the growth of wheat seedlings [9].

Maize (Zea mays L.) is an important cereal crop grown throughout the world and is also an important genetic model plant. Copper stress also affects the growth and development of maize plants through changes in plant height, germination rate, germination potential, chlorophyll content, and soluble sugar content [10]. Excess copper can also produce reactive oxygen species (ROS), inactivate enzymes, and break down protein structures, leading to phytotoxicity in maize [11,12,13]. Within the concentration range of 50–300 mg/L Cu, the maize displays a considerable tolerance of over 60% for the roots and stems. At a 400 mg/L Cu concentration, the root growth experiences a substantial 91% inhibition, while the stem growth is inhibited by 53% [14]. Cu (1 mmol/L) inhibits the activity of protective enzymes in maize seedlings and damages the structure and function of the cell membrane [15]. At the root apex of maize seedlings, Cu exposure generates oxidative damage and alters root hormonal homeostasis, leading to strong inhibition of root growth [16]. Maize seedlings are highly susceptible to stress, which directly affects agricultural production and causes considerable economic losses. In summary, the effects of Cu stress on crops are multifaceted and include physiological and biochemical reactions, changes in spectral characteristics, seed germination and defense mechanisms, growth and development, antioxidant enzyme activities, and spectral monitoring. These effects may reduce the growth rate and yield of crops; therefore, understanding these effects is highly important for both agricultural production and environmental protection.

High-throughput sequencing for transcriptome profiling is a powerful tool that has been widely used and is particularly suitable for the study of complex gene regulatory networks [17]. Transcriptomic analyses have shown that heat shock proteins, transcription factors, and secondary metabolites play important roles in the response of 21-day-old maize seedlings to heat stress [18]. Differentially expressed genes (DEGs) involved in response to cold and drought treatment during seed germination, including those in the bHLH, NAC, MYB, and WRKY families, have been identified by RNA-seq analysis, and these findings suggest that common mechanisms may participate during maize seed germination in response to different abiotic stresses [19].

Since the transcriptome response of maize seedlings to Cu stress is unclear, a bioinformatic transcriptome analysis was performed to determine the molecular response mechanism of maize seedlings in the present study. A series of genes, possibly responsible for Cu tolerance, were identified and characterized, increasing the understanding of the stress response and defense mechanisms involved. This molecular knowledge is imperative for identifying new approaches to promote tolerance to Cu stress in maize. Hence, analyzing the functional genomics underlying the mechanisms of the Cu response and identifying target genes and pathways in maize will aid in the breeding of resistant varieties.

2 Materials and methods

2.1 Culture and treatment of plant material

Seeds of the maize hybrid line “Zhengdan 958” were sterilized and imbibed in distilled water for 12 h. The imbibed seeds were germinated. The seedlings were subsequently grown in a growth cabinet under the following conditions: 25°C, 70% humidity, and a 16-h light/8/h dark cycle. Copper sulfate (CuSO4·5H2O) was used to study Cu stress. Seven-day-old seedlings were grown in Petri dishes supplemented with 0, 5, or 10 mM Cu. After 1 week, the roots of the control and Cu-treated plants were sampled for growth measurement and transcriptome sequencing, and three independent experiments were performed (CK and Cu represent the control and Cu-treated plants, respectively).

2.2 Growth measurements

Maize seedlings were washed three times in double distilled water before the measurements. The images of the seedlings were captured using a Nikon D90 unilateral camera and imported to ImageJ software (NIH, Bethesda, MD, USA) for quantitative analysis of the root length. The root weight was measured using an electronics analytical balance (Mettler Toledo, Zurich, Switzerland). About 30 individual seedlings from the control and the treatment groups were measured for the length and weight tests, and three repeated experiments were performed, respectively.

2.3 RNA isolation and library construction

Total RNA from the roots of plants treated with 0, 5, or 10 mM Cu was isolated using a TRIzol reagent kit (Invitrogen, Carlsbad, CA, USA) according to the manufacturer’s protocol. Total RNA concentration and quality were examined using a NanoDrop One spectrophotometer (NanoDrop, Wilmington, DE, USA), and the RNA was identified using RNase-free agarose gel electrophoresis. cDNA libraries were constructed and sequenced using an Illumina NovaSeq platform (Illumina, San Diego, CA, USA) by Novogene Co., Ltd. (Beijing, China).

2.4 Acquirement of mapped reads and quantification of gene abundance

After sequencing, the raw reads were filtered to obtain high-quality clean reads by removing reads containing adapters, reads containing poly-N sequences, and low-quality reads from the raw data. An index of the reference genome was built, and paired-end clean reads were aligned to the maize B73 reference genome using HISAT2 v2.0.5. The mapped reads were assembled using StringTie (v1.3.3b) [20].

2.5 Differential expression analysis

Gene expression levels were quantified using the fragments per kilobase million (FPKM) method, a standard approach for estimating the number of transcripts per gene [21]. To identify DEGs, three comparative analyses were conducted: 0 mM Cu versus 5 mM Cu, 0 mM Cu versus 10 mM Cu, and 10 mM Cu versus 5 mM Cu. Differential expression analysis was performed using the DESeq2 R package (1.20.0). DESeq2 provides statistical routines for determining differential expression in digital gene expression data using a model based on the negative binomial distribution. The resulting p values were adjusted using Benjamini and Hochberg’s approach for controlling the false discovery rate. Genes were deemed differentially expressed if they exhibited a fold change of at least 2 and an adjusted p value of 0.05 or lower, indicating a significant change in expression levels at different copper concentrations.

2.6 Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses

The GO enrichment analysis of DEGs was implemented using the GOseq R package, which corrected for the gene length bias, ensuring a more accurate representation of gene enrichment. GO terms with corrected p values ≤0.05 were defined as significantly enriched. The GO analysis of the DEGs revealed significant functional enrichment in three categories: molecular function (MF), biological process (BP), and cellular component (CC). Furthermore, the clusterProfiler R package was utilized to determine the statistical enrichment of DEGs in KEGG pathways.

2.7 Quantitative real-time PCR

Total RNA was reverse-transcribed into cDNA using a reverse transcription kit (TaKaRa, Tokyo, Japan). Quantitative real-time PCR was performed with SYBRPremix Ex TaqTM II (TaKaRa, Tokyo, Japan) and monitored using a Bio-Rad CFX Connect Real-time system (Bio-Rad, CA, USA). The PCR cycle was performed with a three-step method, and the relative expression was determined using the 2─∆∆CT method. GAPDH was used as the reference gene, and the details of all primers are described in Table S1. Three biological replicates were performed for each sample.

3 Results

3.1 Effects of Cu exposure on the growth and physiological properties of maize

After 7 days of copper treatment, maize seedlings growth slowed down significantly (Figure 1a). As shown in Figure 1b, the lengths of the roots of the maize plants treated with 5 and 10 mM Cu were approximately 29.16 and 57.79% shorter than those of the control plants, respectively. Additionally, as depicted in Figure 1c, the root weights of maize were significantly reduced after exposure to 5 and 10 mM Cu.

Figure 1 Effects of Cu exposure on the growth and physiological properties of maize. (a) Root growth status of maize seedlings treated with different Cu concentrations. (b) Root length under different Cu treatments. (c) Root weight under different Cu treatments.
Figure 1

Effects of Cu exposure on the growth and physiological properties of maize. (a) Root growth status of maize seedlings treated with different Cu concentrations. (b) Root length under different Cu treatments. (c) Root weight under different Cu treatments.

3.2 RNA sequencing and data quality assessment

In total, 59.6 Gb of clean reads were obtained from the transcriptomic analysis of nine samples, with the percentages of Q20 and Q30 bases exceeding 97.6 and 93.55%, respectively (Table 1). This finding indicates that the sequencing results were of high quality and appropriate for subsequent analysis. Principal component analysis (PCA) is commonly used to identify overall variance in transcriptomic data. The PCA results indicated clear differential expression among the CK, Cu5, and Cu10 groups. The first principal component accounted for 34.93% of the variance, and the second for 14.69% (Figure 2).

Table 1

Statistical analysis of RNA sequencing data from maize seedlings

Samples Clean reads Clean bases Q20 Q30
CK_1 47515052 7.13G 97.6 93.55
CK_2 46414328 6.96G 97.88 94.28
CK_3 48318746 7.25G 97.9 94.28
Cu5_1 44183970 6.63G 97.69 93.76
Cu5_2 44398012 6.66G 97.84 94.21
Cu5_3 41727134 6.26G 97.88 94.24
Cu10_1 41292278 6.19G 97.86 94.24
Cu10_2 43739870 6.56G 97.85 94.2
Cu10_3 39702768 5.96G 97.69 93.88
Figure 2 PCA plot of samples of maize seedlings grown under control and copper stress conditions. CK_1, CK_2, and CK_3 represent samples from control seedlings, whereas Cu5_1, Cu5_2, Cu5_3, Cu10_1, Cu10_2, and Cu10_3 represent the samples from seedlings exposed to copper stress.
Figure 2

PCA plot of samples of maize seedlings grown under control and copper stress conditions. CK_1, CK_2, and CK_3 represent samples from control seedlings, whereas Cu5_1, Cu5_2, Cu5_3, Cu10_1, Cu10_2, and Cu10_3 represent the samples from seedlings exposed to copper stress.

3.3 Identification and comparison of stress-specific DEGs

Based on the screening criteria (fold-change ≥2 and adjusted p value ≤0.05), 619 DEGs (362 upregulated and 257 downregulated DEGs) were identified in the roots of maize plants treated with 5 mM Cu compared to those in the CK group. Similarly, 2,685 DEGs (1,875 upregulated and 810 downregulated) were identified in the roots of maize plants treated with 10 mM Cu compared to those in the CK group, whereas a total of 1,790 DEGs (1,210 upregulated and 580 downregulated) were found in the roots of maize plants treated with 10 mM Cu compared to those in the 5 mM Cu group (Figure 3a). According to the three abovementioned comparisons, the total number of upregulated genes was greater than that of downregulated genes. Additionally, most DEGs were identified from the Cu10 vs CK comparison. A Venn diagram of the DEGs revealed that 135 DEGs were identified from all three comparisons (Figure 3b). A heatmap of the hierarchical clustering analysis revealed that the DEGs in the 10 mM Cu-treated group were effectively distinguished from those in the 5 mM Cu-treated and CK groups (Figure 3c).

Figure 3 Bar chart (a), Venn diagram (b), and heatmap (c) of DEGs in maize seedlings under copper stress compared to the control seedlings. Genes that met the following criteria were considered differentially expressed: DESeq2 padj ≤ 0.05 and |log2FoldChange| ≥ 1.0. (a) The x-axis indicates Cu5 vs CK, Cu10 vs CK, and Cu10 vs Cu5. The y-axis indicates the number of genes. The blue and yellow colors represent upregulated and downregulated genes, respectively. (b) Cu5 vs CK, Cu10 vs CK, and Cu10 vs Cu5 comparisons. In (c), the red and green colors represent upregulated and downregulated genes, respectively.
Figure 3

Bar chart (a), Venn diagram (b), and heatmap (c) of DEGs in maize seedlings under copper stress compared to the control seedlings. Genes that met the following criteria were considered differentially expressed: DESeq2 padj ≤ 0.05 and |log2FoldChange| ≥ 1.0. (a) The x-axis indicates Cu5 vs CK, Cu10 vs CK, and Cu10 vs Cu5. The y-axis indicates the number of genes. The blue and yellow colors represent upregulated and downregulated genes, respectively. (b) Cu5 vs CK, Cu10 vs CK, and Cu10 vs Cu5 comparisons. In (c), the red and green colors represent upregulated and downregulated genes, respectively.

3.4 Functional classification of DEGs

GO enrichment analysis results revealed the top 30 significantly enriched (padj ≤ 0.05) functional terms (Figure 4). Similar terms were significantly enriched in the DEGs identified from the Cu5 vs CK and Cu10 vs CK comparisons. Heme binding was the most highly enriched term in the MF category. Symplast, cell junction, and plasmodesma were the most highly enriched terms in the CC category. Defense response and multiorganism process were the most highly enriched terms in the BP category. In the Cu10 vs Cu5 comparison, heme binding remained the most highly enriched term in the MF category, and plasma membrane part and cell wall organization or biogenesis were the most highly enriched terms in the CC and BP categories, respectively.

Figure 4 GO terms significantly enriched in DEGs. (a) Cu5 vs CK comparison, (b) Cu10 vs CK comparison, and (c) Cu10 vs Cu5 comparison. The GO terms associated with MFs, CCs, and BPs are shown.
Figure 4

GO terms significantly enriched in DEGs. (a) Cu5 vs CK comparison, (b) Cu10 vs CK comparison, and (c) Cu10 vs Cu5 comparison. The GO terms associated with MFs, CCs, and BPs are shown.

3.5 KEGG pathway enrichment analysis of DEGs

The results from the KEGG pathway enrichment analysis revealed the most highly enriched pathways (Figure 5). Phenylpropanoid biosynthesis was the most dominant pathway in the Cu5 vs CK comparison, followed by glutathione metabolism; cutin, suberin, and wax biosynthesis; monoterpenoid biosynthesis; and sesquiterpenoid and triterpenoid biosynthesis. In the Cu10 vs CK comparison, five pathways, namely, phenylpropanoid biosynthesis, flavonoid biosynthesis, stilbenoid, diarylheptanoid and gingerol biosynthesis, glutathione metabolism, and biosynthesis of various plant secondary metabolite pathways, were significantly enriched. In addition, the flavonoid biosynthesis and phenylpropanoid biosynthesis pathways were significantly enriched in the Cu10 vs Cu5 comparison.

Figure 5 KEGG pathways significantly enriched in DEGs. (a) Cu5 vs CK comparison, (b) Cu10 vs CK comparison, and (c) Cu10 vs Cu5 comparison.
Figure 5

KEGG pathways significantly enriched in DEGs. (a) Cu5 vs CK comparison, (b) Cu10 vs CK comparison, and (c) Cu10 vs Cu5 comparison.

3.6 DEGs related to phenylpropanoid and flavonoid biosyntheses

Regarding phenylpropanoid biosynthesis, we identified 24 downregulated and 5 upregulated DEGs in the Cu10 vs Cu5 comparison, 4 upregulated and 9 downregulated DEGs in the Cu5 vs CK comparison, and 24 downregulated and 19 upregulated DEGs in the Cu10 vs CK comparison (Table 2). Most DEGs controlling phenylpropanoid biosynthesis that were identified from the Cu10 vs CK and Cu10 vs Cu5 comparisons, including genes involved in peroxidase syntheses, such as prx39, IDP7923, and pox2, were downregulated. The Cu10 vs Cu5 and Cu10 vs CK comparisons identified 15 upregulated DEGs and 11 upregulated and 3 downregulated DEGs related to flavonoid biosynthesis, respectively (Table 2).

Table 2

KEGG pathway enrichment analysis of DEGs

Pathway ID Pathway padj Count Up Down
Cu5 vs CK
zma00940 Phenylpropanoid biosynthesis 0.001 13 4 9
zma00480 Glutathione metabolism 0.001 10 4 6
zma00073 Cutin, suberin, and wax biosynthesis 0.002 5 0 5
zma00902 Monoterpenoid biosynthesis 0.012 3 0 3
zma00909 Sesquiterpenoid and triterpenoid biosynthesis 0.014 3 3 0
zma02010 ABC transporters 0.039 5 2 3
zma00591 Linoleic acid metabolism 0.039 3 2 1
zma00561 Glycerolipid metabolism 0.051 6 2 4
Cu10 vs CK
zma00940 Phenylpropanoid biosynthesis 0.000 43 19 24
zma00941 Flavonoid biosynthesis 0.000 14 11 3
zma00945 Stilbenoid, diarylheptanoid and gingerol biosynthesis 0.001 10 9 1
zma00480 Glutathione metabolism 0.001 22 15 7
zma00999 Biosynthesis of various plant secondary metabolites 0.004 14 8 6
zma00910 Nitrogen metabolism 0.037 9 2 7
zma04016 MAPK signaling pathway – plant 0.037 24 19 5
zma03030 DNA replication 0.042 11 0 11
zma00460 Cyanoamino acid metabolism 0.043 9 5 4
zma00950 Isoquinoline alkaloid biosynthesis 0.068 5 5 0
zma00360 Phenylalanine metabolism 0.068 7 7 0
zma04075 Plant hormone signal transduction 0.070 34 26 8
zma00906 Carotenoid biosynthesis 0.079 8 2 6
zma00904 Diterpenoid biosynthesis 0.080 6 5 1
zma00350 Tyrosine metabolism 0.086 7 7 0
zma00591 Linoleic acid metabolism 0.086 5 3 2
Cu10 vs Cu5
zma00941 Flavonoid biosynthesis 0.000 15 15 0
zma00940 Phenylpropanoid biosynthesis 0.000 29 5 24
zma00910 Nitrogen metabolism 0.005 8 1 7
zma00902 Monoterpenoid biosynthesis 0.009 4 4 0
zma00480 Glutathione metabolism 0.039 13 10 3
zma00904 Diterpenoid biosynthesis 0.070 5 5 0

3.7 DEGs related to glutathione metabolism

In the present study, we identified 3 downregulated and 10 upregulated DEGs related to glutathione metabolism in the Cu10 vs Cu5 comparison, 6 downregulated and 4 upregulated DEGs related to glutathione metabolism in the Cu5 vs CK comparison, and 7 downregulated and 15 upregulated DEGs related to glutathione metabolism in the Cu10 vs CK comparison. Most of these genes were upregulated in the Cu10 vs CK and Cu10 vs Cu5 comparisons but downregulated in the Cu5 vs CK comparison, suggesting that maize seedlings suffered more oxidative stress during exposure to high Cu concentrations (Table 2).

3.8 qRT–PCR verification

Seven DEGs involved in phenylpropanoid biosynthesis, flavonoid biosynthesis, and glutathione metabolism were randomly selected for qRT‒PCR analysis to verify the reproducibility of the gene expression data obtained by RNA-seq analysis. As shown in Figure 6, the expression patterns of these DEGs (px5, umc2381, gst15, rboh4, GRMZM2G122787, a1, and glu4) were consistent with the FPKM values obtained from RNA-seq, which confirms the effectiveness of DEGs in this study.

Figure 6 Validation of the expression of genes in maize seedlings using qRT‒PCR. The error bars represent the standard deviations of three independent biological replicates. A value of p < 0.05 indicates a statistically significant difference.
Figure 6

Validation of the expression of genes in maize seedlings using qRT‒PCR. The error bars represent the standard deviations of three independent biological replicates. A value of p < 0.05 indicates a statistically significant difference.

4 Discussion

Copper pollution has attracted extensive attention. Crops suffering from copper stress show toxic symptoms, which subsequently result in poor seed germination, stunted growth, and decreased yield [22]. Maize seedlings are unable to tolerate 1 mM Cu, and this concentration inhibits the root growth and activities of protective enzymes in maize seedlings [15]. At the concentrations tested in this study, toxic effects were detected in the roots of the maize seedlings (Figure 1). The abovementioned toxicity symptoms can lead to reduced agricultural productivity, which has economic and food security implications.

With the development of high-throughput sequencing technology, RNA-seq technology has been successfully applied to transcriptome analysis of rice [23], wheat [24], maize [25], and other crops [26]. Specifically, this study enhances our comprehension of the molecular mechanisms underlying maize’s reaction to copper stress. A total of 23,413 genes were identified by transcriptome analysis in maize seedlings under different conditions. Further, the identification of DEGs (619, 2,685, and 1,790) in different copper concentration comparisons (Cu5 vs CK, Cu10 vs CK, and Cu10 vs Cu5) suggested that maize seedlings exhibit a range of responses to varying levels of copper stress (Figure 3a). We found that the DEGs in the 10 mM Cu-treated group were effectively distinguished from those in the 5 mM Cu-treated and CK groups (Figure 3c), suggesting that the effect of high Cu concentration on gene expression patterns was more obvious. The GO enrichment analysis of the DEGs reveals a consistent enrichment pattern in Cu5 vs CK and Cu10 vs CK comparisons, including heme binding, cell–cell junction, and defense response, which contrast with the Cu10 vs Cu5 comparison (Figure 4). These results indicate that the physiological and molecular responses exhibit significant variation as the concentration of Cu increases.

Glutathione is a low molecular weight tripeptide compound that contains a sulfhydryl group and is an important metal chelator and antioxidant [27], which protects cells, retains enzyme activity and protein function, and prevents damage to the cytoplasm and outer membrane [28,29]. Glutathione is also an important cofactor for glutathione glycol peroxidase, glyceraldehyde 3-phosphate dehydrogenase, glyoxalase, and triose dehydrogenase [30]. In addition, glutathione is involved in the formation of disulfide bonds in proteins and the maintenance of the transport of amyloid across cell membranes [31,32]. In the present study, we isolated 28 genes involved in glutathione metabolism from the Cu5 vs CK, Cu10 vs CK, and Cu10 vs Cu5 comparisons. Most of the upregulated genes, such as gst5, gst12, gst15, gst23, gst31, and gst35, were related to the synthesis of glutathione S-transferase (GST). Due to the high affinity of GST to the sulfhydryl group, it shows strong detoxification ability. GST is also a key enzyme in glutathione metabolism, catalyzing the initial steps of this pathway. High levels of copper stress increase the expression levels of GST-related genes in maize, and the GST activity in maize may increase during exposure to copper stress. Modulation of glutathione metabolism in response to copper stress suggests that these genes and their associated metabolic pathways may be targets for genetic improvement to enhance copper tolerance in maize. Collectively, these findings elucidate the complex interplay between glutathione metabolism and plant resistance to environmental stress, providing valuable insights for future research aimed at improving crop resistance to heavy metal toxicity.

Phenylpropanoids are specialized metabolites derived from phenylalanine. In plants, phenylpropanoid biosynthesis produces a variety of aromatic metabolites with important biological functions [33]. Peroxidase catalyzes redox reactions to produce ROS during phenylpropanoid biosynthesis. ROS are important signaling molecules during normal plant growth and development of plants. ROS-related redox signals play a crucial role in plant growth and development as well as adaptation to the environment, controlling almost all physiological processes of cells, such as gene expression and translation, metabolism, and death due to aging [34]. The KEGG pathway enrichment analysis revealed that phenylpropanoid biosynthesis was the most significant enrichment pathway among the DEGs identified from the Cu5 vs CK, Cu10 vs CK, and Cu10 vs Cu5 comparisons (Figure 5). Downregulation of peroxidase genes, including pox2, px17, px24, prx39, and prx69, may have a significant impact on phenylpropanoid biosynthesis and maize root growth, which provides valuable insights into potential targets for genetic modification to enhance stress tolerance and increase seed germination rate.

Flavonoids are important secondary metabolites formed in the long-term ecological adaptation process of plants, which are used to resist invasion of harsh ecological conditions, animals, and microorganisms [35,36,37]. These basic carbon skeleton compounds are widely distributed in plants. Flavonoids exhibit tissue, developmental, and environmental factor specificity in plant metabolism, participate in plant ecological defense, serve as messengers in reproductive processes, and play an important role in plant growth and stress responses [38]. Previous studies have shown that flavonoids have multiple functions; for example, flavonoids accumulate and have antioxidant abilities, thereby improving maize plant adaptability to abiotic stress [39]. In this study, the expression of several key genes (a1, chi6, hct9, fomt4, fht1, and umc2381) involved in flavonoid biosynthesis showed significant differences in maize seedlings before and after Cu stress, suggesting that flavonoids may be related to Cu stress. Transcriptome analysis was used to annotate upregulated genes related to flavonoid biosynthesis, including chalcone-flavanone isomerase family protein, flavonoid 3′-monooxygenase, anthranilate N-benzoyltransferase protein, cytochrome P45, spermidine hydroxycinnamoyl transferase, and hydroxycinnamoyltransferase. This upregulation suggests that plants synergistically increase their flavonoid production under copper stress, which may help mitigate oxidative damage and protect plants from the toxic effects of copper. In summary, this study provides evidence that flavonoids are dynamically regulated in maize responses to copper stress, highlighting their critical role in plant detoxification and defense against heavy metal poisoning.

5 Conclusion

In conclusion, transcriptome studies of maize seedling roots provide data on their tolerance mechanisms to copper stress. Through RNA-seq data analysis, we identified 619, 2,685, and 1,790 DEGs in the Cu5 vs CK, Cu10 vs CK and Cu10 vs Cu5 comparisons, respectively. By integrating the current findings and existing data, copper stress was shown to affect the metabolism and biosynthesis of various plant compounds. Although the exact roles of the candidate genes involved in these pathways remain to be elucidated, the results of this study provide valuable information for further analysis of the response mechanism to copper stress.

  1. Funding information: This work was supported by the National Key R&D Program of China (2019YFA0906200).

  2. Author contributions: M.Z. and L.Z. designed the study, performed the experiments, and analyzed the data. L.Z. and Z.Y. wrote and revised the manuscript. X.W. and Q.W. helped in conducting the experiment. All authors read and approved the final 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.

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Received: 2024-04-17
Revised: 2024-06-06
Accepted: 2024-08-08
Published Online: 2024-11-06

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

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

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  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
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https://doi.org/10.1515/biol-2022-0953
Schlagwörter für diesen Artikel
maize; copper stress; transcriptome; differential expression analysis; functional classification; KEGG pathway
Creative Commons
BY 4.0

Artikel in diesem Heft

  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
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  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
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  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
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  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
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  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
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  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
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  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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Heruntergeladen am 22.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2022-0953/html
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