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Comprehensive transcriptome analysis of Asparagus officinalis in response to varying levels of salt stress

BMC Plant Biology volume 24, Article number: 819 (2024) Cite this article

Abstract

Background

Salt stress is a major abiotic factor that affects the distribution and growth of plants. Asparagus officinalis is primarily resistant to salt stress and is suitable for cultivation in saline-alkali soil.

Results

The study integrated the morphology, physiological indexes, and transcriptome of A. officinalis exposed to different levels of NaCl, with the aim of understanding its biological processes under salt stress. The findings indicated that exposure to salt stress led to decreases in the height and weight of A. officinalis plants. Additionally, the levels of POD and SOD, as well as the amounts of MDA, proline, and soluble sugars, showed an increase, whereas the chlorophyll content decreased. Analysis of the transcriptome revealed that 6,203 genes that showed differential expression at different salt-stress levels. Various TFs, including FAR1, MYB, NAC, and bHLH, exhibited differential expression under salt stress. KEGG analysis showed that the DEGs were primarily associated with the plant hormone signal transduction and lignin biosynthesis pathways.

Conclusion

These discoveries provide a solid foundation for an in-depth exploration of the pivotal genes, including Aux/IAA, TCH4, COMT, and POD, among others, as well as the pathways involved in asparagus’s salt stress responses. Consequently, they have significant implications for the future analysis of the molecular mechanisms underlying asparagus’s response to salt stress.

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Introduction

High levels of salt in the soil can have detrimental effects on plants, including osmotic stress, oxidative stress, ion toxicity, and nutrient deficiencies, all of which can hinder plant growth and lead to reduced crop yield and quality [1, 2]. Presently, more than 20% of irrigated land worldwide is negatively affected by salt stress [3,4,5]. Saline-alkali soil is an important cultivated land reserve, which limits the distribution of plants. Therefore, planting salt tolerant cultivated crops in salinized land can effectively alleviate the pressure on land demand [6].

A. officinalis, a perennial plant, is part of the Asparagus genus within the Asparagaceae family [7]. Asparagus has high nutritional value and medical value and is highly popular in the international market [8, 9]. Asparagus is rich in vitamins, minerals, amino acids, saponins and rutin [10, 11], and possesses effects on preventing cancer, lowering blood lipids and preventing coronary heart disease. Asparagus is believed to have strong salt tolerance, as it can grow normally in moderate saline-alkali soil below 0.3%, concerning one of the favored vegetable species for the utilization of saline-alkali land [12]. Nevertheless, the growth of asparagus seedlings is still negatively impacted by salt stress, highlighting the importance of research to enhance asparagus resistance to salt stress. However, there remains a dearth of data regarding the biological processes involved in reaction to salt stress of asparagus. Changes in protective proteins and metabolites are regulated by activating transcriptional cascades after salt stress [13]. RNA sequencing (RNA-seq) is a valuable tool for identifying potential genes and pathways involved in plant responses to salt stress [14]. Extensive research has been conducted on gene expression changes caused by salt stress [15,16,17]. Salt-tolerant genes are enriched in various pathways, including the phenylpropanoid, plant hormone signal transduction, glutathione metabolism, and MAPK signal pathways [3, 6, 18,19,20].

A. officinalis seedlings were utilized in this research and subjected to varying levels of sodium chloride (NaCl) treatment. The morphology, physiological indexes and transcriptome analysis were conducted to investigate the pivotal genes and pathways of A. officinalis under salt stress. Findings of this study will offer important information for improving the growth of crops that are more resilient to salt stress.

Results

Morphological changes of A. officinalis seedlings under salt stress

In order to investigate how A. officinalis reacts to salt stress, asparagus seedlings that were four months old were exposed to different NaCl concentrations (0 for control, 1.0% for P1 and 2.0% for P2), and the resulting morphological changes in A. officinalis were documented (Fig. 1). Following a 12-day treatment, it was observed that the growth of the A. officinalis plant was notably stunted by 1.0 and 2.0% NaCl compared to the control group (Fig. 1A). Additionally, the A. officinalis seedlings showed signs of wilting under the 2.0% NaCl condition. The plant height and fresh weight (FW) of the stem were significantly decreased by the treatments with 1.0 and 2.0% NaCl (Fig. 1B and C). Significantly, as the salt concentration increased, the growth of A. officinalis was significantly restricted.

Fig. 1
figure 1

Phenotypic characteristics changes of A. officinalis under salt stress for 12 days. (A) Phenotypes of seedlings under 0 (Control), 1.0% (P1), and 2.0% (P2) NaCl treatments. (B–C) Plant height and fresh weight (FW) of the stem. The experiment was conducted three times independently. The data showed averages and standard errors, with distinct letters indicating statistical significance (p < 0.05). Bar = 10 cm

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Physiological indexes of A. officinalis under different salt concentrations and stress duration

Physiological indexes associated with stress reactions were assessed to explore the impact of salt stress on the development of A. officinalis. The results demonstrated that salt stress had a significant impact on peroxidases (POD) and superoxide dismutases (SOD) activities, as well as malondialdehyde (MDA), proline, soluble protein, and total chlorophyll content (Fig. 2). Under varying NaCl concentrations and durations of stress, all of the above parameters, with the exception of chlorophyll content, showed varying degrees of increase compared to the control group (Fig. 2A-E). The amount of chlorophyll decreased significantly when exposed to various salt treatments, with a more pronounced reduction observed with 2.0% NaCl compared to 1.0% NaCl (Fig. 2F). These results indicate that there were differences in physiological responses of A. officinalis seedlings under different salt concentrations and stress duration, which may closely relate to the level of gene expression. Samples collected at 9 days after treatment were selected for transcriptome analysis based on the physiological indexes.

Fig. 2
figure 2

Physiological indexes and enzyme activity of A. officinalis. The enzyme activities of POD (A), SOD (B) and the contents of MDA (C), proline (D), soluble protein (E) and chlorophyll (F) in A. officinalis under 0 (Control), 1.0% (P2), and 2.0% (P3) NaCl treatments (0, 3, 6, 9, and 12 days). Three replicates were performed. The data showed averages and standard errors, with distinct letters indicating statistical significance (p < 0.05)

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Transcriptome profile and correlation analysis of A. officinalis under salt stress

RNA-seq was conducted on the cladodes of seedlings to investigate the molecular mechanisms of A. officinalis in response to salt stress. Nine cDNA libraries were created, and sequencing data were collected (Additional File 1). The average number of raw reads from nine libraries was 22.79 million, while the mean number of clean reads obtained after filtering out adapters and low-quality sequences was 22.64 million. In addition, GC content ranged from 47.34 to 48.38%. All samples displayed Q20 greater than 97.21%, and Q30 values over 92.97%. Overall, the transcriptome sequencing data was excellent and is suitable for additional analysis.

The gene expression distribution of the P2 sample was generally higher than that of the control and P1 samples, as shown in the Additional File 2 A. Principal Component Analysis (PCA) indicated that control, P1 and P2 formed separate clusters, indicating high reliability among the samples (Additional File 2B). The Pearson Correlation Coefficients (PCC) for control, P1 and P2 in A. officinalis exceeded 0.86, indicating strong correlations among the three treatment groups (Additional File 2 C).

DEGs analysis of A. officinalis under salt stress

Comparisons between control and P1, control and P2, and P1 and P2 libraries were conducted for differentially expressed genes (DEGs) analysis. Gene expression profiling in all samples revealed the presence of transcripts being expressed in various treatments under salt stress conditions (Fig. 3 and Additional File 3). We created volcano plots for the three comparison groups to determine the number of DEGs that were significantly regulated (Fig. 3A-C). The quantity of DEGs peaked in the comparison between the control and P2 group, suggesting that the alterations in transcription levels in A. officinalis under 2.0% NaCl exceeded those under 1.0% NaCl. In comparison to the control group, the P1 and P2 treatment groups showed 1,570 DEGs (863 upregulated and 707 downregulated) and 4,664 DEGs (1,812 upregulated and 2,852 downregulated), respectively. Additionally, the P2 treatment group had 4,310 DEGs (1,605 upregulated and 2,705 downregulated) compared to the P1 treatment group (Fig. 3D). Venn diagram displayed the distribution of DEGs among various groups. 6,203 DEGs were enriched in all treatment groups, with a higher number of DEGs found in the comparison between the control and P2 groups compared to that between the control and P1 groups (Fig. 3E). A sequence comparative analysis was conducted to examine the TFs expressed in A. officinalis under various treatments, and 51 TF families were identified (Fig. 3F). The top eight TFs in different comparative groups included FAR1, MYB, NAC, bHLH, C2H2, B3, WRKY and HB. Biological processes related to salt stress in A. officinalis may explain the variations in TFs expression level.

Fig. 3
figure 3

DEGs of A. officinalis under salt treatments. (A-C) Analysis of DEGs using volcano plots. (D) Number of DEGs that were either upregulated or downregulated. (E) Venn diagrams of DEGs. (F) Transcription factor families

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Gene Ontology (GO) annotation analysis of DEGs among different treatments

GO annotation analysis was conducted to gain an understanding of the biological roles of DEGs under salt stress conditions (Fig. 4). The findings demonstrated that DEGs showed significant enrichment in biological processes and molecular functions. Analysis of GO revealed varying numbers of enriched terms among the three treatments as shown in Additional File 4. Comparing the control to P1, control to P2 and P1 to P2 in terms of GO categories, 2,861, 10,177, and 9,016 terms were categorized as cellular components, 1,267, 4,163, and 3,782 were categorized as molecular functions, and 2,640, 8,288, and 7,619 were categorized as biological processes (Additional File 4). As shown in Fig. 4, the primary enrichment of molecular functions was in categories related to ‘catalytic activity’, ‘binding’, and ‘transcription regulator activity’. The biological process was primarily characterized by enrichment in categories such as ‘cellular process’, ‘metabolic process’, and ‘response to stimulus’. While the primary enrichment of the cellular component was related to ‘cell’, ‘cell part’ and ‘organelle’.

Fig. 4
figure 4

Histogram of annotation analysis of Gene Ontology exposed to salt stress for different concentration in (A) Control vs. P1, (B) Control vs. P2 and (C)P1 vs. P2

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Kyoto encyclopedia of genes and genomes (KEGG) enrichment analysis of DEGs among different treatments

In order to fully grasp the biological pathways affected by various NaCl treatments, KEGG pathway enrichment analyses were conducted, revealing 20 key pathways enriched in comparisons between control and P1, control and P2, and P1 and P2, as shown in Fig. 5 and Additional File 5. DEGs in the control vs. P1 group were notably enriched in pathways such as ‘vitamin B6 metabolism’, ‘stilbenoid, diarylheptanoid and gingerol biosynthesis’, and ‘starch and sucrose metabolism’ (Fig. 5A). DEGs in the control vs. P2 group showed significant enrichment in pathways such as ‘valine, leucine and isoleucine degradation’, ‘starch and sucrose metabolism’ and ‘photosynthesis-antenna proteins’ (Fig. 5B). DEGs in the P1 vs. P2 group showed significant enrichment in pathways such as ‘zeatin biosynthesis’, ‘valine, leucine and isoleucine degradation’ and ‘starch and sucrose metabolism’ (Fig. 5C). The findings suggested that the DEGs in these pathways could have significant impacts on the reaction of A. officinalis to salt stress. However, a significant amount of DEGs were found to be enriched in phenylpropanoid biosynthesis and plant hormone signal transduction pathways under various salt treatments, suggesting that these pathways play crucial roles in stress response and warrant further investigation.

Fig. 5
figure 5

Analyzation of the top 20 KEGG pathways in A. officinalis across various pairwise groups. (A) Control vs. P1. (B) Control vs. P2. (C)P1 vs. P2

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DEGs related to the pathways of plant hormone signal transduction

Plant hormones play a crucial role in controlling the growth and development of plants, as well as their response to salt stress [21]. Figure 6 and Additional File 6 display DEGs involved in the signaling transduction pathways of plant hormones. In the case of auxin signaling, 2 genes encoding auxin resistant 1 (AUX1) and auxin/indole-3-acetic acid (Aux/IAA) were upregulated, while 2 genes encoding Aux/IAA were downregulated in 1.0% NaCl treatment. In the case of 2.0% NaCl treatment, 1 gene encoding gretchen hagen 3 (GH3) was upregulated, and 15 genes encoding auxin response factor (ARF), AUX1, Aux/IAA, and small auxin-up RNA (SAUR) were downregulated. For cytokinin (CTK) signaling, 2 genes encoding histidine phosphotransfer protein (AHP) were found to be downregulated in response to 1.0% NaCl treatment, whereas 1 gene encoding AHP was upregulated and 5 genes encoding type-A response regulators (A-ARR), type-B response regulators (B-ARR), and AHP were downregulated in 2.0% NaCl treatment. During salt stress, the expression of pathogenesis-related protein 1 (PR1) and TGACG-binding factor (TGA) homologs increased in salicylic acid (SA) signaling. In the scenarios involving brassinosteroid (BR), ethylene (ETH), jasmonic acid (JA), and abscisic acid (ABA) signaling pathways, numerous DEGs were also found.

Fig. 6
figure 6

DEGs in the plant hormone signaling transduction pathways when exposed to salt stress

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DEGs involved lignin biosynthetic pathways

Analyzing the phenylpropanoid biosynthesis pathways enriched in three groups is essential for studying the important genes related to salt stress. 30 DEGs related to lignin biosynthesis were identified after screening the DEGs involved in phenylpropanoid biosynthesis (Fig. 7 and Additional File 6). Lignin, the primary constituent of plant vascular tissue, is a polymer originating from phenylpropanoids [22]. Within the pathway responsible for lignin creation, DEGs were identified including phenylalanine ammonia-lyase (PAL), caffeic acid O-methyltransferase (COMT), caffeoyl-CoA O-methyltransferase (CCoAOMT), cinnamoyl-CoA reductase (CCR), peroxidase (POD), cinnamyl alcohol dehydrogenase (CAD), and 4-coumarate–CoA ligase (4CL). In lignin biosynthesis, 5 genes encoding CCoAOMT, COMT and POD were upregulated, while 1 gene encoding POD was downregulated in 1.0% NaCl treatment. In the case of 2.0% NaCl treatment, 12 genes encoding CAD, CCoAOMT, CCR, and POD were upregulated, and 14 genes encoding 4CL, CCoAOMT, PAL, and POD were downregulated.

Fig. 7
figure 7

DEGs in the lignin biosynthetic pathways when exposed to salt stress

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Validation of the RNA-Seq data by quantitative real-time PCR (qRT-PCR)

To confirm the DEGs identified through RNA-seq analysis, qRT-PCR was conducted on a selection of 16 genes chosen from the plant hormone signaling transduction pathways (Fig. 8A) and 8 genes chosen from lignin biosynthetic pathways (Fig. 8B). The qRT-PCR findings were aligned with the transcriptome analysis, confirming the accuracy of RNA-seq data.

Fig. 8
figure 8

Validation of DEGs using qRT-PCR. Comparisons of RNA-seq data (red lines) with qRT-PCR (yellow bars) of selected genes. (A) qRT-PCR validation of the genes involved in plant hormone signaling transduction pathway. (B) qRT-PCR validation of genes involved in lignin biosynthetic pathways

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Discussion

Plants that can withstand high levels of salt are suitable for surviving in saline-alkali soil. Planting salt-tolerant plants on saline-alkali soil could alleviate farmland pressure. Transcriptome analysis is crucial for identifying the essential genes of A. officinalis in responses to salt stress [23]. In this research, morphological, physiological changes, as well as transcriptome analysis were combined to explain the response mechanisms of A. officinalis under different concentrations of NaCl.

Morphological, physiological and transcriptome analyses of A. officinalis under salt stress

Morphological changes in different treatments under salt stress can be observed (Fig. 1A). The decrease in both plant height and FW of A. officinalis was significant, particularly when exposed to 2.0% NaCl concentrations, indicating that higher levels of NaCl have a more pronounced inhibitory impact on plant development (Fig. 1B and C). The physiologic alterations may also indicate the impact of salt stress on plants (Fig. 2). Exposure to high levels of salt can trigger an overproduction of reactive oxygen species (ROS), resulting in oxidative stress and causing cell damage [24]. Yet, plants have the ability to reduce harm through their antioxidant system [25]. SOD and POD, two essential antioxidant enzymes, which are critical for maintaining ROS balance during salt stress by effectively counteracting ROS-induced damage and enhancing plant resistance to oxidative stress [26]. To mitigate the effects of salt stress on A. officinalis, the functions of SOD and POD were stimulated in this research (Fig. 2A and B). Comparable findings were also noted in various other plant species including tomato, wheat, radish and rice [27,28,29,30]. MDA, a lipid peroxidation product, can be utilized to assess the extent of cell membrane injury [25]. The study indicated that the MDA levels in A. officinalis were elevated under salt stress (Fig. 2C). Under stress conditions, the accumulation of salt resistant metabolites such as proline and soluble proteins are important in regulating cell membrane permeability [31, 32]. A. officinalis showed a significant increase in proline and soluble protein content under salt stress (Fig. 2D and E), indicating that proline and soluble protein may participate in reducing the degree of damage to plants caused by salt stress. Under salt stress, the structures of chloroplasts are disrupted leading to the decrease of chlorophyll content [33, 34]. Here, we found the chlorophyll content in A. officinalis cladodes significantly decreased in NaCl treatments (Fig. 2F). The decrease in plant growth may be caused by the decrease in chlorophyll content under salt stress conditions.

To initially reveal the key salt-responsive molecular mechanisms of A. officinalis seedlings, the transcriptome analysis was performed. DEGs in 2.0% NaCl treatment of 9 days were maximum compared with control and 1.0% NaCl (Fig. 3). Among these, transcription factors such as WRKY75, WRKY40, NAC79, and ABR1 displayed increased expression levels as the salt concentration increases, whereas the expression of transcription factors like ERF109, WRKY71, TCP12, and WRKY41 were suppressed in response to elevated salt concentration. These genes potentially play significant roles in salt stress responses and can be further investigated through molecular biological approaches. Analysis of KEGG enrichment revealed that the DEGs were primarily associated with the plant hormone signaling transduction and phenylpropanoid biosynthesis pathway (Fig. 5), suggesting their potential role in the mechanism of A. officinalis in combating salt stress.

Plant hormone signal transduction pathways in A. officinalis under salt stress

Plant hormones are known to have important functions in signaling transduction pathways mediated by abiotic stress [35,36,37]. Auxin is crucial for regulating plant growth and responding to stress [38]. Aux/IAA functions as a transcriptional inhibitor, controlling the activity of auxin response genes such as IAA, GH3, and SAUR through interaction with the ARF protein [39, 40]. The majority of DEGs related to auxin signaling transduction pathways were notably decreased in expression levels when exposed to elevated salt treatments, as shown in Fig. 6, which is consistent with previous studies [41]. ABA plays a crucial role in orchestrating intricate signal transduction pathways and serves as a vital plant defense hormone that enhances plant resilience in the face of abiotic stress [20, 42]. The pyrabactin resistance/pyr1-like (PYR/PYL) receptor could detect ABA and blocks the action of protein phosphatase 2 C (PP2C). This leads to the stimulation of downstream kinase SNF1-related protein kinase 2 (SnRK2), ultimately activating ABA-responsive genes [43, 44]. The salt treatment significantly regulated PYR/PYL and SnRK2 in this study (Fig. 6), suggesting the effect of salt on the ABA signaling pathway. Numerous studies have shown that CTK has both positive and negative effects on plant stress resistance [45,46,47]. Our research found that the genes AHP, B-ARR, and A-ARR showed decreased expression levels under salt stress (Fig. 6), suggesting that CTK could play a role in the reaction of A. officinalis seedlings to salt stress. An increase in ABA synthesis has been linked to a decrease in CTK levels during salt stress, serving as a strong defense mechanism for plants against salt stress [37, 48]. JA manages the main aspects of plant adaptation to environmental stress [49]. The study indicated a notable increase in the expression of jasmonate acid resistant1 (JAR1) and jasmonate ZIM domain (JAZ) genes in response to NaCl stress, as shown in Fig. 6, which is similar to previous findings [50]. Additionally, SA has the ability to control how plants react to stress [6]. The application of SA may enhance the ability of plants to withstand high salt levels [51]. The findings of this research also reveal that the TGA and PR1 genes showed a notable increase in expression levels under salt stress (Fig. 6). Additional hormones like BR may also have a significant impact on plant responses to salt stress [52]. There may be crosstalk between different plant hormones under salt stress, which requires further research.

Lignin biosynthetic pathways in A. officinalis under salt stress

The lignin biosynthesis pathways are a key element of the phenylpropanoid pathway. Lignin plays a crucial role in the structure of plant cell walls, increasing the ability of plants to withstand both biotic and abiotic stressors [53]. Lignin is produced from individual building blocks obtained from p-coumaryl alcohol, coniferyl alcohol, and sinapyl alcohol [3]. Previous studies have shown that plants could increase the degree of lignification to improve salt tolerance [54]. Some genes have been identified to be involved in the process of lignin production and storage, such as trans-cinnamate monooxygenase (CYP73A), 4CL, CCoAOMT, CAD, CCR, COMT, coniferaldehyde-5-hydroxylase (CAld5H), and hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase (HCT) [55,56,57]. Studies have indicated that salt stress can result in the accumulation of lignin, which is linked to the activity of enzymes such as CCoAOMT, C4H, CCR, POD, and C3’H [58,59,60]. Under salt stress, PheCAD2, PheCAD3, and PheCAD5 of moso bamboo (Phyllostachys pubescens) were highly upregulated, confirming their participation in salt stress responses [61]. CrCOMT was demonstrated to positively regulate stress responses in Arabidopsis under salt stress [62]. CCoAOMT was confirmed to play a role in both lignin production and response to salt stress in jute (Corchorus L.) [63]. During this research, the phenylpropanoid biosynthesis pathways showed a notable increase in activity when exposed to salt stress, leading to the identification of 30 DEGs related to lignin biosynthesis (Fig. 7). More DEGs were found in 2.0% NaCl than 1.0% NaCl, implying that the reactions of A. officinalis were more intricate under high salt concentrations. However, the transcription levels of structural genes involved in lignin biosynthesis pathways were complex under different concentrations of NaCl, which means that further investigation is required for explaining the lignin biosynthetic pathways under salt stress of A. officinalis.

When considering all the data, it appears that NaCl treatments may have an impact on the genes associated with the plant hormone signal transduction and lignin biosynthetic pathways (Fig. 9). This research has revealed that under 2.0% NaCl, the expression level of genes is more affected in A. officinalis. The existing findings may offer a theoretical foundation for comprehending the molecular processes involved in the response of A. officinalis to varying levels of salt stress. However, the specific regulatory patterns and pathways under different salt concentrations still need further exploration.

Fig. 9
figure 9

Proposed model for how A. officinalis seedlings reacts to salt stress. The blue arrow indicates downregulated genes, while the red arrow indicates upregulated genes

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Materials and methods

Plant materials and salt stress application

A. officinalis was grown in a greenhouse at Zhejiang Institute of Subtropical Crops in Zhejiang Province, China, with a light cycle of 16 h light and 8 h dark at a temperature of 25℃. A. officinalis was grown in containers with a blend of garden soil and peat in equal parts. Seedlings that were four months old and cultivated in a soil blend were utilized for this research.

NaCl solution was incrementally introduced to the soil until the salt level reached 0 (control), 1.0% (P1) and 2.0% (P2). After 0, 3, 6, 9, and 12 days of salt treatments, cladodes from A. officinalis seedlings were collected for measurement of physiological indexes and RNA-seq. After 12 days of treatment, the plant height and FW were both recorded. The experiments were performed with three independent biological replicates.

Detection and analysis of key physiological indexes

The height of the plant was determined by measuring from the base to the tip of the stem. The FW of A. officinalis above ground was weighed using balance. Physiological indexes including POD, SOD, MDA, proline content, soluble protein content and chlorophyll content were measured as reported [21,22,23]. The trials were conducted thrice with three sets of biological samples.

RNA extraction, transcriptome sequencing, and data processing

RNA-seq was performed using samples obtained from treatments with NaCl concentrations of 0, 1.0, and 2.0% after 9 days. The analysis was done to study the main changes of A. officinalis in response to different NaCl concentrations. Each treatment was conducted with three biological replicates.

RNA extraction from A. officinalis cladodes was performed using the RNAprep Pure Plant Kit (TIANGEN, Beijing, China) for subsequent transcriptome analysis. Genepioneer Biotechnologies Co., Ltd (Nanjing, China) performed the creation of the cDNA library and the sequencing using NovaSeq 6000 platform (150 bp paired-end reads). The sequencing data can be accessed from NCBI (BioProject ID: PRJNA1074503).

Transcriptome data and gene annotation analysis

The raw data acquired by sequencing was filtered to obtain clean reads. At the same time, calculations were performed for Q20, Q30, and GC-content. Each sample’s clean reads were individually aligned to the A. officinalis reference genome (https://www.ncbi.nlm.nih.gov/datasets/taxonomy/4686/) using the HISAT2 software [24]. The level of gene expression was calculated using fragments per kilobase of transcript per million mapped reads (FPKM) [25]. Differentially expressed genes (DEGs) were detected at three different levels of NaCl (0%, 1.0%, and 2.0%) through the utilization of DESeq2 program [26]. DEGs function annotation utilized the KEGG and GO databases. The KOBAS online analysis database(http://kobas.cbi.pku.edu.cn/home.do) was used to conduct KEGG pathway analysis, while the R package clusterProfiler was utilized for GO enrichment analysis of DEGs [27,28,29]. PlantTFDB databases (http://planttfdb.gao-lab.org/) were used to predict transcription factors (TFs) [30].

qRT-PCR

24 genes were chosen at random for qRT-PCR analysis to confirm the accuracy of the RNA-seq. The FastKing RT Kit (TaKaRa, Dalian, China) was utilized for cDNA synthesis, followed by qRT-PCR using SYBR qPCR Master Mix (Vazyme, Nanjing, China). Online software (https://sg.idtdna.com/Scitools/Applications/RealTimePCR/default.aspx) was used to design primers, and the information of primers was displayed in Additional File 7. The Light Cycler480 Real-Time System (Bio-Rad Laboratories, Hercules, CA, USA) was used for qRT-PCR analysis and the program was as reported [31]. The 2−ΔΔCt method was used for calculating the relative expression [32]. Three independent biological and technological replicates were used for each sample.

Statistical analysis

SPSS (version 23) was utilized for statistical analysis. Data mapping is displayed as average ± SD, with significance (p < 0.05) taken into account.

Conclusions

In this study, the effects of various concentrations of NaCl on four-month-old A. officinalis seedlings were researched. The changes in gene expression levels were comprehensively analyzed in the cladodes of A. officinalis seedlings. The findings suggest that A. officinalis exhibits diverse response mechanisms to varying levels of salt stress. Additional examination demonstrated that the genes related to the hormone signal transduction and lignin biosynthetic pathways in A. officinalis cladodes were be regulated when exposed to salt stress. The results offer comprehensive data that serves as a foundation for advancing our understanding of the molecular pathways activated in A. officinalis in response to salt stress, which is essential for developing salt-resistant genetic resources.

Data availability

The datasets generated and/or analyzed during the current study are available in the NCBI SRA repository, with accession number PRJNA1074503 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1074503). All data generated or analyzed during this study are included within the article and its additional files.

References

  1. Acosta-Motos JR, Álvarez S, Barba-Espín G, Hernández JA, Sánchez-Blanco MJ. Salts and nutrients present in regenerated waters induce changes in water relations, antioxidative metabolism, ion accumulation and restricted ion uptake in Myrtus communis L. plants. Plant Physiol Biochem. 2014;85:41–50.

    Article  CAS  PubMed  Google Scholar 

  2. Zamljen T, Medic A, Hudina M, Veberic R, Slatnar A. Salt stress differentially affects the primary and secondary metabolism of peppers (Capsicum annuum L.) according to the genotype, fruit part, and salinity level. Plants (Basel). 2022;11(7):853.

    CAS  PubMed  Google Scholar 

  3. Li Y, Zhang T, Kang Y, Wang P, Yu W, Wang J, Li W, Jiang X, Zhou Y. Integrated metabolome, transcriptome analysis, and multi-flux full-length sequencing offer novel insights into the function of lignin biosynthesis as a Sesuvium portulacastrum response to salt stress. Int J Biol Macromol. 2023;237:124222.

    Article  CAS  PubMed  Google Scholar 

  4. Liu Y, Wang B, Li J, Song Z, Lu B, Chi M, Yang B, Liu J, Lam Y-W, Li J, et al. Salt-response analysis in two rice cultivars at seedling stage. Acta Physiol Plant. 2017;39(10):215.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Song J, Wang B. Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot. 2015;115(3):541–53.

    Article  CAS  PubMed  Google Scholar 

  6. Zhu W, Cao H, Wang Q, Niu Y, Sadeghnezhad E, Han S, Liu M, Wang L, Liu Z. Transcriptome analysis revealed MAPK and hormone pathway involving in exogenous melatonin-regulated salt tolerance in sour jujube. Fruit Res. 2023; 3(1).

  7. Abdelrahman M, Nakabayashi R, Mori T, Ikeuchi T, Mori M, Murakami K, Ozaki Y, Matsumoto M, Uragami A, Tsujimoto H, et al. Comparative metabolome and transcriptome analyses of susceptible Asparagus officinalis and resistant wild A. kiusianus reveal insights into stem blight disease resistance. Plant Cell Physiol. 2020;61(8):1464–76.

    Article  CAS  PubMed  Google Scholar 

  8. Takahashi H, Yoshida C, Takeda T. Sugar composition in Asparagus spears and its relationship to soil chemical properties. J Appl Glyosci. 2019;66(1):47–50.

    Article  CAS  Google Scholar 

  9. Yang Y-Q, Sun Q, Li C-M, Chen H-F, Zhao F, Huang J-H, Zhou J-S, Li X, Lan B. Biological characteristics and genetic diversity of Phomopsis asparagi, causal agent of asparagus stem blight. Plant Dis. 2020; 104.

  10. Negi JS, Singh P, Joshi GP, Rawat MS, Bisht VK. Chemical constituents of Asparagus. Pharmacogn Rev. 2010;4(8):215–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Shirasawa K, Ueta S, Murakami K, Abdelrahman M, Kanno A, Isobe S. Chromosome-scale haplotype-phased genome assemblies of the male and female lines of wild asparagus (Asparagus kiusianus), a dioecious plant species. Dna Res. 2022;29(1):dsac002.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Gao H, Zhang X, Liang Y, Dong L, Han C, Cao Y. Comprehensive evaluation of salt tolerance in asparagus germplasm accessions (Asparagus officinalis L.) at different growth dtages. J Food Qual. 2021.

  13. Liu Z, Hua Y, Wang S, Liu X, Zou L, Chen C, Zhao H, Yan Y. Analysis of the Prunellae Spica transcriptome under salt stress. Plant Physiol Biochem. 2020;156:314–22.

    Article  CAS  PubMed  Google Scholar 

  14. Elnaggar A, Mosa KA, Ramamoorthy K, El-Keblawy A, Navarro T, Soliman SSM. De novo transcriptome sequencing, assembly, and gene expression profiling of a salt-stressed halophyte (Salsola Drummondii) from a saline habitat. Physiol Plant. 2021;173(4):1695–714.

    Article  CAS  PubMed  Google Scholar 

  15. Hu J, Zhuang Y, Li X, Li X, Sun C, Ding Z, Xu R, Zhang D. Time-series transcriptome comparison reveals the gene regulation network under salt stress in soybean (Glycine max) roots. BMC Plant Biol. 2022;22(1):157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lu X, Ma L, Zhang C, Yan H, Bao J, Gong M, Wang W, Li S, Ma S, Chen B. Grapevine (Viti Comprehensive evaluation s vinifera) responses to salt stress and alkali stress: transcriptional and metabolic profiling. BMC Plant Biol. 2022;22(1):528.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Singh A, Roychoudhury A. Gene regulation at transcriptional and post-transcriptional levels to combat salt stress in plants. Physiol Plant. 2021;173(4):1556–72.

    Article  CAS  PubMed  Google Scholar 

  18. Amirbakhtiar N, Ismaili A, Ghaffari MR, Nazarian Firouzabadi F, Shobbar Z-S. Transcriptome response of roots to salt stress in a salinity-tolerant bread wheat cultivar. PLoS ONE. 2019;14(3):e0213305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lei P, Liu Z, Hu Y, Kim H, Liu S, Liu J, Xu L, Li J, Zhao Y, Yu Z, et al. Transcriptome analysis of salt stress responsiveness in the seedlings of wild and cultivated Ricinus communis L. J Biotechnol. 2021;327:106–16.

    Article  CAS  PubMed  Google Scholar 

  20. Song Q, Joshi M, Joshi V. Transcriptomic analysis of short-term salt stress response in watermelon seedlings. Int J Mol Sci. 2020;21(17):6036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ribeiro PR, Willems LAJ, Silva AT, Fernandez LG, de Castro RD, Bucher J, Snoek BL, Hilhorst HWM, Ligterink W. Transcriptome profiling of Ricinus communis L. provides new insights underlying the mechanisms towards thermotolerance during seed imbibition and germination. Ind Crop Prod. 2018;126:380–93.

    Article  CAS  Google Scholar 

  22. Lam PY, Wang L, Lui ACW, Liu H, Takeda-Kimura Y, Chen M-X, Zhu F-Y, Zhang J, Umezawa T, Tobimatsu Y, et al. Deficiency in flavonoid biosynthesis genes CHS, CHI, and CHIL alters rice flavonoid and lignin profiles. Plant Physiol. 2022;188(4):1993–2011.

    Article  CAS  PubMed  Google Scholar 

  23. Yang T, Tian M, Gao T, Wang C, Wang X, Chen C, Yang W. Genome-wide transcriptomic analysis identifies candidate genes involved in jasmonic acid-mediated salt tolerance of alfalfa. PeerJ. 2023;11:e15324.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Choudhury S, Panda P, Sahoo L, Panda SK. Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav. 2013;8(4):e23681.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Guo X, Ahmad N, Zhao S, Zhao C, Zhong W, Wang X, Li G. Effect of salt stress on growth and physiological properties of asparagus seedlings. Plants (Basel). 2022;11(21):2836.

    CAS  PubMed  Google Scholar 

  26. Kaya C, Higgs D, Ashraf M, Alyemeni MN, Ahmad P. Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiol Plant. 2020;168(2):256–77.

    Article  CAS  PubMed  Google Scholar 

  27. Biczak R, Telesiński A, Pawłowska B. Oxidative stress in spring barley and common radish exposed to quaternary ammonium salts with hexafluorophosphate anion. Plant Physiol Biochem. 2016;107:248–56.

    Article  CAS  PubMed  Google Scholar 

  28. Dugasa MT, Cao F, Ibrahim W, Wu F. Differences in physiological and biochemical characteristics in response to single and combined drought and salinity stresses between wheat genotypes differing in salt tolerance. Physiol Plant. 2019;165(2):134–43.

    Article  CAS  PubMed  Google Scholar 

  29. Rahman A, Hossain MS, Mahmud J-A, Nahar K, Hasanuzzaman M, Fujita M. Manganese-induced salt stress tolerance in rice seedlings: regulation of ion homeostasis, antioxidant defense and glyoxalase systems. Physiol Mol Biol Pla. 2016;22(3):291–306.

    Article  CAS  Google Scholar 

  30. Yang Y, Yao Y, Li J, Zhang J, Zhang X, Hu L, Ding D, Bakpa EP, Xie J. Trehalose alleviated salt stress in tomato by regulating ROS metabolism, photosynthesis, osmolyte synthesis, and trehalose metabolic pathways. Front Plant Sci. 2022;13:772948.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Athar H-u-R, Zulfiqar F, Moosa A, Ashraf M, Zafar ZU, Zhang L, Ahmed N, Kalaji HM, Nafees M, Hossain MA, et al. Salt stress proteins in plants: an overview. Front Plant Sci. 2022;13:999058.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Li W, Meng R, Liu Y, Chen S, Jiang J, Wang L, Zhao S, Wang Z, Fang W, Chen F, et al. Heterografted chrysanthemums enhance salt stress tolerance by integrating reactive oxygen species, soluble sugar, and proline. Hortic Res. 2022;9:uhac073.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhang Z, Mao C, Shi Z, Kou X. The amino acid metabolic and carbohydrate metabolic pathway play important roles during salt-stress response in tomato. Front Plant Sci. 2017;8:1231.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Zhang X, Han C, Liang Y, Yang Y, Liu Y, Cao Y. Combined full-length transcriptomic and metabolomic analysis reveals the regulatory mechanisms of adaptation to salt stress in asparagus. Front Plant Sci. 2022;13:1050840.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Ku Y-S, Sintaha M, Cheung M-Y, Lam H-M. Plant hormone signaling crosstalks between biotic and abiotic stress responses. Int J Mol Sci. 2018;19(10):3206.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ribba T, Garrido-Vargas F, O’Brien JA. Auxin-mediated responses under salt stress: from developmental regulation to biotechnological applications. J Exp Bot. 2020;71(13):3843–53.

    Article  CAS  PubMed  Google Scholar 

  37. Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G. How plant hormones mediate salt stress responses. Trends Plant Sci. 2020;25(11):1117–30.

    Article  CAS  PubMed  Google Scholar 

  38. Pavlović I, Pěnčík A, Novák O, Vujčić V, Radić Brkanac S, Lepeduš H, Strnad M, Salopek-Sondi B. Short-term salt stress in Brassica rapa seedlings causes alterations in auxin metabolism. Plant Physiol Biochem. 2018;125:74–84.

    Article  PubMed  Google Scholar 

  39. Luo J, Zhou J-J, Zhang J-Z. Aux/IAA gene family in plants: molecular structure, regulation, and function. Int J Mol Sci. 2018;19(1):259.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Szemenyei H, Hannon M, Long JA. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science. 2008;319(5868):1384–6.

    Article  CAS  PubMed  Google Scholar 

  41. Korver RA, Koevoets IT, Testerink C. Out of shape during stress: a key role for auxin. Trends Plant Sci. 2018;23(9):783–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Li Y, Zhou J, Li Z, Qiao J, Quan R, Wang J, Huang R, Qin H. Salt and ABA response ERF1 improves seed germination and salt tolerance by repressing ABA signaling in rice. Plant Physiol. 2022;189(2):1110–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Huang K-C, Lin W-C, Cheng W-H. Salt hypersensitive mutant 9, a nucleolar APUM23 protein, is essential for salt sensitivity in association with the ABA signaling pathway in Arabidopsis. BMC Plant Biol. 2018;18(1):40.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Huang S, Ma Z, Hu L, Huang K, Zhang M, Zhang S, Jiang W, Wu T, Du X. Involvement of rice transcription factor OsERF19 in response to ABA and salt stress responses. Plant Physiol Biochem. 2021;167:22–30.

    Article  CAS  PubMed  Google Scholar 

  45. Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, et al. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell. 2011;23(6):2169–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Prerostova S, Dobrev PI, Gaudinova A, Hosek P, Soudek P, Knirsch V, Vankova R. Hormonal dynamics during salt stress responses of salt-sensitive Arabidopsis thaliana and salt-tolerant Thellungiella salsuginea. Plant Sci. 2017;264:188–98.

    Article  CAS  PubMed  Google Scholar 

  47. Žižková E, Dobrev PI, Muhovski Y, Hošek P, Hoyerová K, Haisel D, Procházková D, Lutts S, Motyka V, Hichri I. Tomato (Solanum lycopersicum L.) SlIPT3 and SlIPT4 isopentenyltransferases mediate salt stress response in tomato. BMC Plant Biol. 2015;15(1):85.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Ghanem ME, Albacete A, Martínez-Andújar C, Acosta M, Romero-Aranda R, Dodd IC, Lutts S, Pérez-Alfocea F. Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L). J Exp Bot. 2008;59(11):3039–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Du M, Zhao J, Tzeng DTW, Liu Y, Deng L, Yang T, Zhai Q, Wu F, Huang Z, Zhou M, et al. MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate-mediated plant immunity in tomato. Plant Cell. 2017;29(8):1883–906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhang W, Liu S, Li C, Zhang P, Zhang P. Transcriptome sequencing of Antarctic Moss under salt stress emphasizes the important roles of the ROS-scavenging system. Gene. 2019;696:122–34.

    Article  CAS  PubMed  Google Scholar 

  51. Ahanger MA, Aziz U, Alsahli AA, Alyemeni MN, Ahmad P. Influence of exogenous salicylic acid and nitric oxide on growth, photosynthesis, and ascorbate-glutathione cycle in salt stressed Vigna angularis. Biomolecules. 2020;10(1):42.

    Article  CAS  Google Scholar 

  52. Tian P, Liu J, Mou C, Shi C, Zhang H, Zhao Z, Lin Q, Wang J, Wang J, Zhang X et al. GW5-Like, a homolog of GW5, negatively regulates grain width, weight and salt resistance in rice. Journal of Integrative Plant Biology. 2019; 61(11):1171–1185.

  53. Shafi A, Chauhan R, Gill T, Swarnkar MK, Sreenivasulu Y, Kumar S, Kumar N, Shankar R, Ahuja PS, Singh AK. Expression of SOD and APX genes positively regulates secondary cell wall biosynthesis and promotes plant growth and yield in Arabidopsis under salt stress. Plant Mol Biol. 2015;87(6):615–31.

    Article  CAS  PubMed  Google Scholar 

  54. Kim HJ, Triplett B. Involvement of extracellular Cu/Zn superoxide dismutase in cotton fiber primary and secondary cell wall biosynthesis. Plant Signal Behav. 2008;3(12):1119–21.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Ni Z, Han X, Yang Z, Xu M, Feng Y, Chen Y, Xu L-a. Integrative analysis of wood biomass and developing xylem transcriptome provide insights into mechanisms of lignin biosynthesis in wood formation of Pinus massoniana. Int J Biol Macromol. 2020;163:1926–37.

    Article  CAS  PubMed  Google Scholar 

  56. Quiroga Mn, Guerrero C, Botella MA, Barceló A, Amaya I, Medina MI, Alonso FJ, de Forchetti SM, Tigier H, Valpuesta V. A tomato peroxidase involved in the synthesis of lignin and suberin1. Plant Physiol. 2000;122(4):1119–28.

    Article  Google Scholar 

  57. Wang G-L, Huang Y, Zhang X-Y, Xu Z-S, Wang F, Xiong A-S. Transcriptome-based identification of genes revealed differential expression profiles and lignin accumulation during root development in cultivated and wild carrots. Plant Cell Rep. 2016;35(8):1743–55.

    Article  CAS  PubMed  Google Scholar 

  58. Li C, Qi Y, Zhao C, Wang X, Zhang Q. Transcriptome profiling of the salt stress response in the leaves and roots of halophytic Eutrema salsugineum. Front Genet. 2021;12:770742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Srivastava S, Vishwakarma RK, Arafat YA, Gupta SK, Khan BM. Abiotic stress induces change in Cinnamoyl CoA reductase (CCR) protein abundance and lignin deposition in developing seedlings of Leucaena leucocephala. Physiol Mol Biol Pla. 2015;21(2):197–205.

    Article  CAS  Google Scholar 

  60. Tang Y, Liu F, Xing H, Mao K, Chen G, Guo Q, Chen J. Correlation analysis of lignin accumulation and expression of key genes involved in lignin biosynthesis of ramie (Boehmeria nivea). Genes (Basel). 2019;10(5):389.

    Article  CAS  PubMed  Google Scholar 

  61. Vasupalli N, Hou D, Singh RM, Wei H, Zou L-H, Yrjälä K, Wu A, Lin X. Homo- and Hetero-dimers of CAD enzymes regulate lignification and abiotic stress response in moso bamboo. Int J Mol Sci. 2021;22(23):12917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Zhang K, Cui H, Cao S, Yan L, Li M, Sun Y. Overexpression of CrCOMT from Carex rigescens increases salt stress and modulates melatonin synthesis in Arabidopsis thaliana. Plant Cell Rep. 2019;38(12):1501–14.

    Article  CAS  PubMed  Google Scholar 

  63. Kahie MA, Wang Y, Fang P, Qi J, Lei R, Xu J, Lin L, Zhang L, Zhang J, Tao A. Evolution and expression analysis of the caffeoyl-CoA 3-O-methyltransferase (CCoAOMT) gene family in jute (Corchorus L). BMC Genomics. 2023;24(1):204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by Special funding project of Zhejiang Academy of Agricultural Sciences (2024XJXK03) , Technology Service Team Project of Ouhai science and technology innovation center of Zhejiang Academy of Agricultural Sciences, and Ouhai Science Innovation Center Program of Zhejiang Academy of Agricultural Sciences (20220HKC0005).

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  1. Zhejiang Institute of Subtropical Crops, Zhejiang Academy of Agricultural Sciences, 334 Xueshan Road, Wenzhou, Zhejiang, 325005, China

    Shuangshuang Wen, Jiali Ying, Youju Ye, Yunfei Cai & Renjuan Qian

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S.W: Design experiments, Investigation, Analyze the data, Write manuscripts. J.Y: Investigation, Analyze the data. Y.Y: Provide ideas, Investigation. Y.C: Investigation. R.Q: Provide ideas, Design experiments, Writing-review & editing. All authors reviewed the manuscript.

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Wen, S., Ying, J., Ye, Y. et al. Comprehensive transcriptome analysis of Asparagus officinalis in response to varying levels of salt stress. BMC Plant Biol 24, 819 (2024). https://doi.org/10.1186/s12870-024-05540-4

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BMC Plant Biology

ISSN: 1471-2229

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