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Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation

  • Tingting Wang , Yuanyuan Zhao , Dexun Wang and Hongzhi Shi EMAIL logo
Published/Copyright: April 15, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

NaHCO3 accelerates the aging of tobacco leaves; however, the underlying molecular mechanisms have not been elucidated. This study aimed to explore the mechanism of NaHCO3 in the promotion of tobacco leaf maturation using transcriptome analysis. Leaves on plants or detached leaves of the tobacco variety, Honghua Dajinyuan, were sprayed with or without 1% NaHCO3. The leaf yellowing was observed, the pigment content and enzyme activities were determined and RNA sequencing (RNA-seq) was performed. Spraying NaHCO3 onto detached leaves was found to promote leaf yellowing. Pigment content, catalase activity, and superoxide dismutase activity significantly decreased, whereas peroxidase activity and malondialdehyde content significantly increased. RNA-seq demonstrated that spraying with NaHCO3 upregulated genes associated with cysteine and methionine metabolism; alpha-linolenic acid metabolism; and phenylalanine, tyrosine, and tryptophan biosynthesis and downregulated genes related to photosynthesis and carotenoid biosynthesis. Genes correlated with autophagy-other, valine, leucine, and isoleucine degradation, and the MAPK signaling pathway were upregulated while those correlated with DNA replication, phenylalanine, and tyrosine and tryptophan biosynthesis were downregulated in detached leaves sprayed with NaHCO3 compared with the plant leaves sprayed with NaHCO3. Overall, this study is the first to elucidate the molecular and metabolic mechanisms of NaHCO3 in the promotion of tobacco leaf maturation.

Keywords: tobacco; NaHCO3 ; RNA sequencing; leaf maturation

1 Introduction

Flue-cured tobacco is an important cash crop. Timely harvesting and moderate flue curing are key to ensuring the quality of this crop. Maturity is the primary quality factor for grading and a critical index for measuring the quality of tobacco leaves [1]. Insufficient maturity leads to weak hydrolytic activity of substances in the leaves, which causes difficulties during browning and flue curing. The hydrolysis of organic matter is intense in overripe leaves. As a result, the leaves turn yellow, dehydrate quickly, and are easy but not resistant to flue curing. Moderately mature tobacco leaves are easy to cure and have an ideal resistance to flue curing. In addition, the aroma content of these leaves increases with maturity, and the quality of flue-cured tobacco is good [2,3]. The upper leaves of tobacco have a high economic value; however, because the weather is not suitable for maturity later in the growing season, obtaining suitably mature and flue-cured high-quality tobacco is difficult to achieve [4]. Therefore, the degradation of substances in flue-cured tobacco must be promoted to enable rapid maturation of the leaves.

Currently, studies on the promotion of tobacco leaf ripening and yellowing have mainly focused on soil fertilizers and irrigation management [2]. Although this approach is a good strategy for accurately determining the amount of nitrogen fertilizer applied and the basic consumption of nitrogen fertilizer in the mature stage of tobacco leaves, controlling this system during the actual production process is not an easy task. Moreover, excessive nutrient consumption through delayed topping can promote the yellowing of tobacco leaves; however, delayed topping affects the quality of tobacco leaves [5]. Currently, only few reports have been published on the effects of chemical spraying on the ripening and yellowing of tobacco leaves. In nature, tobacco ripening is climacteric, characterized by high respiration and ethylene production [6]. Ethylene effectively induces leaf senescence and nicotine conversion [7]. A previous study revealed that treatment with 2-chloroethylphosphonic acid, which releases free ethylene, rapidly yields mature flue-cured tobacco leaves prior to harvest [8]. NaHCO3 affects the production of ethylene [5]. NaHCO3 stress also induces different degrees of chlorosis and yellowing [9,10] and accelerates the aging of tobacco leaves [5]. NaHCO3 is more convenient and cost-effective than ethylene. Moreover, NaHCO3 can induce nicotine demethylase activity in mature and senescent tobacco leaves after picking, promote the conversion of nicotine to nornicotine, and enable early identification of transformed strains [6]. Therefore, NaHCO3 may be a good exogenous substance to promote the maturation of tobacco leaves.

Owing to the major environmental challenges of soil salinity-alkalinity limiting crop productivity [11], some studies have reported global transcriptome changes following NaHCO3 treatment. For example, Ge et al. conducted transcriptional profiling of Glycine soja roots subjected to 50 mmol/L NaHCO3 treatment and found that most differentially expressed genes (DEGs) were involved in signal transduction, energy, transcription, secondary metabolism, transporters, disease, and defense responses [12]. Wang et al. found that the DEGs between Tamarix hispida roots treated and untreated with NaHCO3 were involved in signal transduction, phosphatase activity, and lipid kinase activity [13]. However, the molecular mechanism whereby NaHCO3 promotes the maturity of late-maturing tobacco leaves remains unclear.

In this study, we aimed to explore the mechanisms of NaHCO3 in the promotion of tobacco leaf maturation using transcriptome analysis. Accordingly, we treated tobacco leaves with NaHCO3 before and after picking and then conducted RNA sequencing (RNA-seq) and bioinformatics analysis.

2 Methods

2.1 Planting and sampling

The pot experiment was conducted at the Key Laboratory of Tobacco Cultivation, Physiology, and Biochemistry, Henan Agricultural University (Zhengzhou, Henan, China). The tobacco variety, Honghua Dajinyuan, was flue-cured in this study. After the tobacco seeds were disinfected, the seedlings were raised by floating. After four true leaves appeared, strong seedlings with uniform growth were selected and transplanted into pots filled with nutrient soil. The light, temperature, water, and fertilizer conditions were the same throughout the growth process of the tobacco plant. The temperature was set to 23–28°C, the light cycle was 10 h from 8:00 to 18:00 with a light intensity of 400 μmol m−2 s−1, and the humidity was 70 ± 5%. After the seedlings adapted to the pot environment, liquid fertilizer was applied to promote the growth of the tobacco plants.

At week 10, 24 pots with vigorous and consistent tobacco plant growth were selected and randomized into four treatments: the LT group was sprayed with 1% NaHCO3 solution after leaf picking (picking +1% NaHCO3); LT-CK was sprayed with the same volume of distilled water after leaf picking (picking + distilled water). The HT group was sprayed with 1% NaHCO3 solution on tobacco leaves that were not picked from tobacco plants (unpicking +1% NaHCO3); the CK group was sprayed with the same volume of distilled water, and the levels were not picked (unpicking + distilled water). Leaves from the LT and LT-CK groups were placed in a constant temperature (30°C) and humidity (80%) incubator to maintain leaf activity. Eight days after treatment, the leaves were sampled and immediately stored at −80°C for the subsequent experiments.

2.2 Physiological index detection

The chloroplast pigment content was determined using spectrophotometry. Leaf tissues were ground in liquid nitrogen. Acetone was added for pigment extraction overnight and then centrifuged at 10,000 × g for 10 min. The optical density values at 663, 646, and 470 nm were measured. The Chl a, Chl b, and carotenoid contents were determined according to a previous study [14].

Catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD) activities were determined via ultraviolet absorption spectrometry using enzyme activity kits (Suzhou Comin Biotechnology Co., Ltd., Jiangsu, China). Malondialdehyde (MDA) content was detected using the glucosinolate barbituric acid colorimetric method.

2.3 RNA extraction and library construction

Total RNA was isolated from samples using TRIzol reagent (Thermo Fisher Scientific, Waltham, MA, USA). After quality confirmation, the RNA samples were subjected to cDNA library construction. In detail, mRNA with a poly(A) tail was enriched by magnetic beads with oligo(dT), and the mRNA was interrupted using a buffer solution. Using the fragmented mRNA as a template and random oligonucleotides as primers, the first cDNA strand was synthesized using the M-MuLV reverse transcriptase system. The second cDNA strand was synthesized using a DNA polymerase I system with dNTPs as the raw material. Purified double-stranded cDNA was subjected to end repair, A-tail addition, and joint connection sequencing. A cDNA of approximately 200 bp was screened for PCR amplification using AMPure XP beads. The PCR products were purified using AMPure XP beads. The library was obtained and subjected to Illumina sequencing following the quality control procedures.

2.4 Data processing

To ensure data quality, the raw reads were subjected to quality control using fastp (version 0.19.6) [15]. Briefly, reads containing adapter were removed, reads with more than 10% N were removed, reads that were all A-base were removed, and low-quality reads (base numbers with mass value of Q ≤ 20 accounting for more than 50% of the entire read) were removed. The clean reads were subjected to reference genome alignment to Nicotiana tabacum K326 genome, published by Sierro et al. [16], using HISAT2 (version 2.2.1) [17].

2.5 Sample relationship analysis and differential expression analysis

Based on the expression levels in each sample, principal component analysis (PCA) was conducted to determine the repeatability of the samples.

Differential gene expression analysis was conducted using DESeq2 (version 2.12) [18] based on read count data. The analysis was divided into the following three parts: (1) normalization of the read count, (2) P-value calculation, and (3) multiple hypothesis test correction to obtain the false discovery rate (FDR) value. The thresholds were FDR < 0.05 and |log2FC| > log2(2). Significant DEGs are displayed on a volcano map. The DEGs were also subjected to hierarchical clustering, and the clustering results are presented using heat maps.

2.6 Function analysis

Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses were performed to determine the functions of these DEGs. GO comprises three ontologies: molecular function (MF), cellular component (CC), and biological process (BP). Pathway enrichment analysis was conducted with the KEGG pathway as the unit. A hypergeometric test was used to select significantly enriched pathways.

2.7 Gene set enrichment analysis (GSEA)

Enrichment analysis based on traditional hypergeometric tests requires a set of significant DEGs. When individual gene changes are weak, the results based on traditional enrichment analysis may be limited. GSEA (Version 4.2.0) [19] can effectively compensate for the lack of effective information mining of minor genes using traditional enrichment analysis and can more comprehensively explain the regulatory effects of certain functional units, such as pathways or GO terms. Using the expression information of all genes, the genes were ranked according to Signal2Noise. After analysis of the ranking of a specific gene set among all genes, the GO term or pathway in which the gene set resides was scored; this score is called the enrichment score (ES). Based on the gene set, the P-value was calculated using a permutation test, and the normalized ES value (NES value) was corrected using multiple tests.

3 Results

3.1 NaHCO3 induces the senescence of detached tobacco leaves

The effect of spraying NaHCO3 on live tobacco leaves was not evident (Figure 1a) whereas that of spraying on detached leaves was evident. On day 2, the leaf tips and edges began to appear green. On day 4, the leaf surfaces began to transition from a green to a yellow color. More than 95% of the leaf surface became yellow on day 8, whereas only the leaf tip and edge began to turn yellow in the CK group (Figure 1a). The pigment content decreased in a time-dependent manner in the CK and NaHCO3 spraying groups. At the same time point, the pigment content of leaves in the NaHCO3 spraying group was significantly lower than that of the CK group (P < 0.01) (Figure 1b). The activities of CAT and SOD significantly decreased (P < 0.01), whereas those of POD and MDA significantly increased after NaHCO3 treatment (P < 0.01) (Figure 1c–f).

Figure 1 Changes in the physical characteristics of leaves after spraying with NaHCO3. (a) Appearance of live leaves on day 8 and detached leaves from days 0 to 8. (b) Effect of spraying NaHCO3 on the pigment content of detached flue-cured tobacco leaves. **P < 0.01, compared with the same treatment on day 0; ## P < 0.01, compared with the CK group. (c) Effect of spraying NaHCO3 on the CAT activity of detached flue-cured tobacco leaves. **P < 0.01, compared with the CK group. (d) Effect of spraying NaHCO3 on the POD activity of detached flue-cured tobacco leaves. **P < 0.01, compared with the CK group. (e) Effect of spraying NaHCO3 on the SOD activity of detached flue-cured tobacco leaves. **P < 0.01, compared with the CK group. (f) Effect of spraying NaHCO3 on the MDA activity of detached flue-cured tobacco leaves. **P < 0.01, compared with the CK group.
Figure 1

Changes in the physical characteristics of leaves after spraying with NaHCO3. (a) Appearance of live leaves on day 8 and detached leaves from days 0 to 8. (b) Effect of spraying NaHCO3 on the pigment content of detached flue-cured tobacco leaves. **P < 0.01, compared with the same treatment on day 0; ## P < 0.01, compared with the CK group. (c) Effect of spraying NaHCO3 on the CAT activity of detached flue-cured tobacco leaves. **P < 0.01, compared with the CK group. (d) Effect of spraying NaHCO3 on the POD activity of detached flue-cured tobacco leaves. **P < 0.01, compared with the CK group. (e) Effect of spraying NaHCO3 on the SOD activity of detached flue-cured tobacco leaves. **P < 0.01, compared with the CK group. (f) Effect of spraying NaHCO3 on the MDA activity of detached flue-cured tobacco leaves. **P < 0.01, compared with the CK group.

3.2 Data processing

For all samples, the raw sequencing data ranged from 40,061,984 to 48,891,692. Following removal of the low-quality data, clean data were obtained, accounting for more than 99% of all samples. After mapping to the reference genome, the total mapped genome ranged from 92.43 to 93.74%.

3.3 PCA and differential expression analysis

PCA revealed that the overall distribution characteristics of all samples in the four groups had a good separation status and less overlap with the samples in the other groups (Figure 2a). For differential expression analysis, we focused on DEGs in the LT-CK vs LT and HT vs LT groups. The former may explain the molecular mechanisms of NaHCO3 in the promotion of leaf senescence after picking, while the latter may explain the lack of significant effects of NaHCO3 on live tobacco leaves and the mechanisms of adaptation. Based on the LT-CK vs LT comparison, 1,134 DEGs (982 upregulated and 152 downregulated) were identified, while based on the HT vs LT comparison, 13,556 DEGs (5,190 upregulated and 8,366 downregulated) were identified. Volcano plots of the two groups of DEGs are shown in Figure 2b and c. Heatmaps of the DEGs are presented in Figure 2d and e.

Figure 2 PCA and differential expression analysis. (a) PCA result for samples in three groups. (b) and (c) Volcano plots of DEGs in the two comparison groups. (d) and (e) Heatmaps of DEGs in the two comparison groups.
Figure 2

PCA and differential expression analysis. (a) PCA result for samples in three groups. (b) and (c) Volcano plots of DEGs in the two comparison groups. (d) and (e) Heatmaps of DEGs in the two comparison groups.

3.4 Function analysis

DEGs in the LT-CK vs LT groups were significantly associated with metabolic processes, cellular processes, response to stimuli, and biological regulation-related BP terms. In addition, these DEGs were enriched in MFs associated with catalytic activity, transporters, and activity, and CCs related to cells, organelles, and membranes (Figure 3a). Pathway enrichment analysis revealed that some biosynthesis-, metabolism-, and signaling-related pathways were enriched, such as alpha-linolenic acid metabolism, phenylpropanoid biosynthesis, linoleic acid metabolism, photosynthesis-antenna proteins, plant hormone signal transduction, and cysteine and methionine metabolism (Figure 3b).

Figure 3 Function analysis of DEGs in LT-CK vs LT. (a) GO enrichment analysis and (b) KEGG enrichment analysis.
Figure 3

Function analysis of DEGs in LT-CK vs LT. (a) GO enrichment analysis and (b) KEGG enrichment analysis.

The DEGs between HT and LT were enriched in BPs related to metabolic processes, cellular processes, and responses to stimuli; CCs related to organelles, cells, and membranes; and MFs related to catalytic activity, binding, and transporter activity (Figure 4a). These GO terms were similar to those of the LT-CK and LT groups. These genes were involved in pathways associated with photosynthesis-antenna proteins; metabolic pathways; photosynthesis; carbon metabolism; plant hormone signal transduction; phenylalanine, tyrosine, and tryptophan biosynthesis; glycine, serine, and threonine metabolism; and biosynthesis of amino acids (Figure 4b).

Figure 4 Function analysis of DEGs in HT vs LT. (a) and (b) GO enrichment analysis and (b) KEGG enrichment analysis.
Figure 4

Function analysis of DEGs in HT vs LT. (a) and (b) GO enrichment analysis and (b) KEGG enrichment analysis.

3.4.1 GSEA

GSEA revealed that DEGs in LT-CK vs LT were positively correlated with GO terms for the negative regulation of peptidase activity, regulation of peptidase activity, defense response, incompatible interaction, and extracellular region and negatively correlated with photosystem, photosynthetic membrane, and thylakoid. The DEGs between HT and LT were negatively correlated with chloroplast organization, plastid membrane organization, photosynthesis, and pigment accumulation and positively correlated with seed maturation, dormancy, peroxisomal transport, developmental maturation, and mRNA catabolic processes. The ES GO terms with the top five highest and lowest NES are shown in Figure S1a–d.

Based on GSEA-KEGG, DEGs in LT-CK vs LT were positively correlated with pathways related to alpha-linolenic acid metabolism, proteasome, various types of N-glycan biosynthesis, glutathione metabolism, phenylalanine, tyrosine, and tryptophan biosynthesis and negatively correlated with photosynthesis-antenna proteins, photosynthesis, circadian rhythm-plant, phosphonate and phosphinate metabolism, and carotenoid biosynthesis. The DEGs in HT vs LT were positively correlated with autophagy-other, valine, leucine, and isoleucine degradation, MAPK signaling pathway, and endocytosis and negatively correlated with ribosome biogenesis in eukaryotes, photosynthesis-antenna proteins, DNA replication, proteasome, phenylalanine, tyrosine, and tryptophan biosynthesis. The ES pathways with the top five highest and lowest NES are shown in Figure S2a–d.

4 Discussion

In the present study, spraying NaHCO3 on tobacco leaves after harvesting significantly promoted leaf yellowing; this finding was completely evident after 3–4 days. However, the effect of spraying NaHCO3 on tobacco leaves before harvesting was not evident.

Chloroplast pigments are one of the main components affecting the quality and availability of tobacco leaves. These pigments also determine the color of tobacco leaves after modulation. The degradation products of chloroplast pigments are closely related to the aroma of tobacco leaves [20,21]. The change in color during tobacco leaf ripening is essentially a reflection of the change in the proportion of total chlorophyll and carotenoids to total chloroplast pigments in the leaf tissue. Salt stress and saline-alkaline stress usually reduce photosynthetic efficiency and inhibit chlorophyll synthesis in plants [22,23]. Consistent with these studies, we found that the tobacco leaves turned yellow after spraying with NaHCO3. During the long-term phylogenetic evolution of plants, protective mechanisms develop against the toxicity of ROS and free radicals in cells; the active oxygen scavenging system plays a major role among these mechanisms [24]. SOD, CAT, and POD are important protective enzymes in the active oxygen removal system that can remove excess ROS in plants, prevent the rapid accumulation of high concentrations of ROS, and prevent the peroxidation of membrane lipids [25]. MDA, the final product of lipid peroxidation, is widely used as an indicator of membrane damage caused by free radicals under abiotic stresses [26]. Physiological experiments revealed that in the detached leaves, the contents of Chl a, Chl b, and carotenoids and the activities of CAT and SOD decreased significantly, while the activity of POD increased after spraying with NaHCO3. The MDA content also increased after spraying with NaHCO3. However, the effect of spraying NaHCO3 on tobacco leaves before harvesting was not evident. According to Wang et al., NaHCO3 can induce a ROS burst, which damages the growth and photosystems of tobacco [27]. In the livers of crucian carp, the SOD, POD, and CAT activities and MDA content were significantly increased by 40 and 60 mmol/L NaHCO3 [28]. We speculate that the decrease in SOD and CAT was due to the inability of detached leaves to produce SOD for ROS clearance. Our study further highlights the effects of NaHCO3 on the promotion of tobacco leaf maturation and senescence after harvesting.

We proceeded to determine the potential molecular mechanisms whereby NaHCO3 promotes the maturity of tobacco leaves using RNA-seq. Upon comparing the LT-CK and LT groups, 1,134 DEGs were identified. Pathway enrichment analysis revealed that several biosynthesis-, metabolism-, and signaling-related pathways were also enriched. For instance, alpha-linolenic acid metabolism, various types of N-glycan biosynthesis, cysteine and methionine metabolism, and phenylalanine, tyrosine, and tryptophan biosynthesis were upregulated, whereas photosynthesis and carotenoid biosynthesis were downregulated after NaHCO3 treatment. Methionine is a precursor of S-adenosyl methionine, which is a precursor of ethylene [29]. The upregulation of cysteine and metabolism of methionine may promote ethylene production and accelerate the maturity and senescence of tobacco leaves. Changes in amino acid metabolism, especially the increased synthesis of aspartic acid and asparagine, are related to maturation, senescence, ammonia accumulation, and detoxification in plants [30]. Alpha-linolenic acid metabolism produces the precursors for jasmonic acid biosynthesis [31]. Jasmonic acid promotes leaf senescence in Arabidopsis [32]. Interrupting jasmonic acid signaling or inhibiting its biosynthesis delays plant leaf senescence [33]. Altogether, NaHCO3 may promote the maturity and senescence of tobacco leaves by upregulating amino acid and alpha-linolenic acid metabolism and downregulating photosynthesis and carotenoid biosynthesis.

A total of 13,556 DEGs were identified in the HT vs LT groups. These DEGs were positively correlated with autophagy-other, valine, leucine, and isoleucine degradation, ether lipid metabolism, and MAPK signaling pathways and negatively correlated with photosynthesis-antenna proteins, DNA replication, proteasomes, phenylalanine, tyrosine, and tryptophan biosynthesis. During leaf senescence, autophagic activity increases to remove damaged organelles, oxidized proteins, and other toxic compounds from cells [27]. The upregulation of the autophagy pathway may explain the inability to identify the effect of NaHCO3 on live tobacco leaves. Interestingly, among these pathways, phenylalanine, tyrosine, and tryptophan biosynthesis had opposite effects in the two comparison groups. Phenylalanine, tyrosine, and tryptophan are aromatic amino acids [34]. A previous study revealed that aromatic amino acids accumulate during leaf senescence [35]. Mou et al. [36] also suggested that amino acids and derivatives, such as tryptophan, proline, tyrosine, and phenylalanine, accumulate significantly during leaf senescence. The accumulation of these amino acids is a strategy for maintaining osmotic balance during leaf senescence. In addition to aromatic amino acids, the contents of valine, leucine, and isoleucine significantly increase during late senescence [37]. Therefore, upregulation of the valine, leucine, and isoleucine degradation pathways may also be one of the adaptive mechanisms of live tobacco leaves after treatment with NaHCO3. The MAPK signaling pathway is an important signal transduction pathway in plants and has been suggested to be associated with Arabidopsis leaf senescence [38]. Overall, we speculate that live tobacco leaves may adapt to NaHCO3 stress via amino acid degradation, increasing autophagic activity and regulating some signaling pathways.

In the production process, tobacco plants might mature late due to abnormal climate or improper fertilizer operation. Spraying NaHCO3 on the leaves after harvesting can induce the aging and yellow effect of detached leaves of flue-cured tobacco. The main reason is that exogenous NaHCO3 promotes the metabolism of macromolecular substances in flue-cured tobacco and increases the coordination of substances contained in tobacco leaves. The curing properties of refractory yellow tobacco were improved, and the chemical composition and aroma quality of the cured tobacco were positively affected. Exogenous NaHCO3-induced leaf aging greatly reduced the influence of climate on flue-cured tobacco quality. The effect of exogenous NaHCO3 on the maturation and senescence of field flue-cured tobacco, the application of detached leaf senescence technology in field production, and the effect of spraying NaHCO3 on the quality of cured tobacco leaves still need further research.

5 Conclusion

To our knowledge, this is the first study to elucidate the molecular and metabolic mechanisms by which NaHCO3 promotes the maturation of tobacco leaves. NaHCO3 may enhance amino acid and alpha-linolenic acid metabolism and weaken photosynthesis to promote the maturity and senescence of tobacco leaves after harvesting. Therefore, NaHCO3 might be a good exogenous substance that promotes the maturation of tobacco leaves and the conversion of nicotine to nornicotine after harvesting. Live tobacco leaves may adapt to NaHCO3 stress through amino acid degradation, increasing autophagic activity and regulating some signaling pathways. However, further experiments are required to confirm our results.

# Co-first authors.

  1. Funding information: This study was supported by the Science and Technology Project of China National Tobacco Corporation (No. 110202103016) and Science and Technology Project of China National Tobacco Corporation Yunnan Province (No. 2022530000241015). There are no conflicts of interest of the authors with the funding company.

  2. Author contributions: T.T.W. and H.Z.S. concepted and designed the research; T.T.W. and Y.Y.Z. acquired data; T.T.W., H.Z.S., and D.X.W. analyzed and interpretated data; T.T.W. and Y.Y.Z. drafted the manuscript; H.Z.S. revised the manuscript for important intellectual content. All authors read and approved the final 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. The data generated in this study were deposited in the NCBI with the accession number of PRJNA1035810 via http://www.ncbi.nlm.nih.gov/bioproject/1035810.

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Received: 2023-12-07
Revised: 2024-02-22
Accepted: 2024-03-08
Published Online: 2024-04-15

© 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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https://doi.org/10.1515/biol-2022-0849
Keywords for this article
tobacco; NaHCO3; RNA sequencing; leaf maturation
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
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  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
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  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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