Genome-wide transcriptome and physiological analyses provide new insights into cadmium tolerance to tomato seedlings

doi:10.21203/rs.3.rs-1741029/v1

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Genome-wide transcriptome and physiological analyses provide new insights into cadmium tolerance to tomato seedlings

https://doi.org/10.21203/rs.3.rs-1741029/v1

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Background

Cadmium (Cd) pollution in agricultural soils has become one of the main environmental problems in China. This study investigated the underlying molecular mechanism controlling the effects of auxin and lignin in response to Cd stress in tomato.

Results

Cadmium treatment significantly inhibited the root growth (by 43.46%) of tomato seedlings, and induced their antioxidant enzyme activities (POD and CAT). Cadmium treatment decreased their shoot dry weight and root dry weight at day 7, 40.42% and 60.40%, respectively. The content of malondialdehyde (MDA) increased and total chlorophyll contents were reduced during the treatment. A comparative transcriptome (RNA-Seq) was de novo assembled and differentially expressed genes (DEGs) with altered expression levels were investigated among wild type cultivars A57 with or without cadmium ion treatment for 24 h. A total of 18,883 unigenes were grouped into 51 Gene Ontology (GO) categories and 89 Kyoto Encyclopedia of Genes and Genomes terms (KEGG). A number of 1,563 differentially expressed genes (DEGs) were found in Cd-exposed tomato seedlings, including 559 down-regulated genes and 1157 up-regulated genes. Go term enrichment analysis indicated that various auxin signaling pathway-related GO terms were significantly enriched in DEGs. Most genes involved in lignin biosynthesis pathway were up-regulated, for instance, COMT and CCOMT.

Conclusions

The transcriptome expression profiles of tomato seedlings under Cd stresses obtained in this study provided a resource for identifying common mechanisms in the lignification formation and the inhibition of plant growth.

Lycopersicum esculentum

cadmium

lignification

auxin transport

differentially expressed genes

transcriptome

Cadmium (Cd) is known in all organisms to generate toxicity and induce oxidative stress due to its high mobility and bioaccumulation ability, when exposure levels increase [1–3]. Oxidative stress results in a disorder of the cellular redox status caused by cadmium [4]. Constantly expanding transcriptome data sets have revealed a global picture of Cd stress response genes in certain widely studied plant species, such as Arabidopis [5], rice [6].

Cadmium is not essential for life, but is easily assimilated by plant roots and conveyed to their aerial portion. Cadmium is present in the environment which is mainly because of the implementation of cadmium-containing phosphorus fertilizers to farmland [7]. Cd gives rise to physiological interference such as water absorption, transport and indispensable elements transportation, mitochondrial phosphorylation, decreased mitochondrial respiration, photosynthesis [8, 9], stunted plant growth, chlorophyll content, chlorosis and root injury [10], changes in Mn, K, Mg and Ca uptake rates [11].

Cd stress also restrains all kinds of metabolic events leading to insufficient cellular energy supply and oxidative stress [12] and may lead to the production of reactive oxygen species (ROS) and free radicals. At the cellular level, Cd toxicity is known to cause alterations such as disruption of electron transport, membrane damage, interaction with nucleic acids and inhibition/activation of enzymes [13, 14]. The possible underlying mechanism of Cd toxicity is the binding of Cd to sulfhydryl and/or carboxyl groups or replacement of essential co-factors e.g. Zn by Cd [4, 15].

Plants have a complex mechanism of non-enzymatic and enzymatic antioxidant compounds that work together to keep ROS levels under control and to defend plant cell against oxidative injury [16]. Cd causes oxidative stress either by producing oxygen free radical or by decreasing the level of enzymatic and non-enzymatic antioxidants [17, 18]. The enhanced activities of these antioxidative enzymes seems to be the result of de novo synthesis and/or activation of the enzymes, mediated through the transcription and/or translation of specific genes [19].

Evidence indicates that high concentrations of Cd alone can influence sugar and protein metabolism and stimulate vegetative oxidative stress [20]. Cadmium had either as antagonistic or synergistic effects on cellular division rate of Chlorella sp., which was observed in mixtures of various combinations of metals [21].

Lignin is the primary ingredient of secondary cell walls in plant and plays a pivotal role in numerous various cell types, providing structural support for plant development, growth, and defense [22]. In Arabidopsis thaliana, p-coumarate 3-hydroxylase, cinnamate-4-hydroxylase (C4H), 4-coumarate:CoA ligase (4CL), and cinnamoyl-CoA reductase (CCR) play an essential role in adjusting the lignin content, whereas 4CL concurrently varies the component of lignin [23, 24].

RNA-seq is a highly dynamic and susceptive tool for transcriptome researches in plants, which can afford a general picture of plant biological pathways [25]. Auxin pathway-associated genes were discovered to be regulated on account of the transcriptome data, so we have concentrated on analyzing them more specifically. Our research affords essential information on the candidate genes in wild tomato cultivar in north and central China. Transcriptome and genome analyses have offered worthy information with respect to its regulation in plant species and the lignin biosynthetic pathway [26, 27].

The objective of this research is to estimate the biological effects of Cd²⁺ on metabolic pathways and the growth in tomato seedlings by means of transcriptome and physiological analysis. Histochemical stain results offered a hypothesis that cadmium stress induced the lignin formation. GO analysis exhibits a large amount of DEGs related to “catalytic” and “metabolic process” which are enriched. These messages provided novel opinions into the genetic mechanisms underlying cadmium stress-induced lignification and concurrently influenced biological procedures in tomato seedlings.

Phenotypic characterization of S. lycopersicum seedlings under cadmium stress

In all the varieties studied, the morphology and appearance of metal-treated seedlings was altered, particularly in the roots after cadmium ion treatment. We observed that root elongation was inhibited, and root and shoot in dry weight decreased (Fig.1A and B). Compared to the control, the dry weight of shoot and root of seedlings was decreased by cadmium ion stress treatment by 40.42% and 60.39% at day 7, respectively. Moreover, cadmium stress treatment restrained the root lengths of tomato seedlings, which the root length inhibition rate was in Cd²⁺-treated plants (43.42%) at day 7 compared with control (Fig.1C and D).

Total Chlorophyll content and lipid peroxidation

Malondialdehyde (MDA), as the primary lipid peroxidation by-product, was used for estimating the level of lipid peroxidation. With the prolongation of treatment time, its content also increased (Fig.2A). Its levels in controls (9.01 + 0.21 nmol/g·FW), were significantly lower than those at 10 μM Cd²⁺ (14.30 + 0.05 nmol/g·FW) at day 3. Furthermore, an evident and visible increase in lipid peroxidation was observed which occurred in roots of seedlings with 10 μM Cd²⁺at day 7.

After 7 days of exposure, the inhibitory effects of Cd on total chlorophyll in tomato leaves were shown in Fig.2B. As tomato seedlings grew, the chlorophyll content of control gradually increased. However, the chlorophyll levels of tomato seedlings treated with Cd²⁺ decreased significantly under oxidative stress. No significant differences (p＞0.05) were found between tomato seedlings treated with Cd²⁺ and control. Compared to control, the chlorophyll content in tomato seedlings treated with Cd²⁺ had more sharp decline (by 45.95%) on day 7th.

Antioxidant enzyme activities

In the present research, it was found that POD activity was altered with cadmium treatment (Fig.2C). Actually, POD activity in roots with 10 μM Cd²⁺ treatments for 3 day reached the peak value, and then declined. However, POD activity in control had peaked on the first day. As shown in Fig. 2C, POD activities were distinctly induced by cadmium ion stress at the beginning of the third day.

Likewise, CAT activity of Lycopersicum esculentum underwent a fluctuating trend following cadmium exposure (Fig.2D). When exposed to cadmium for 3 days, the CAT activity reached a maximum value of 189.74 U·g^-1 FW. After 7 days of treatment, great decrease of CAT activity occurred as presented in Fig.2D. Generally speaking, CAT activity initially went up, and then decreased. It was obvious that Cd²⁺ treatment could enhance CAT activity during the entire processing period.

Effect of Cd on lignin content

Seven-day-old tomato seedlings were cultured in Hoagland nutrient solution with 10 μM Cd²⁺ for 7 days, and the tomato roots were cut with scissors and collected for lignin assay. Phloroglucinol staining indicating lignin deposition in the vascular tissues of tomato seedling roots was visible after Cd treatment for 7 days. As presented in Fig. 3, the visible lignin content in tomato seedling roots incubated in Cd²⁺ solutionsignificantly higher than control.

Illumina paired-end sequencing and de novo assembly

mRNA from control and cadmium-treated plants were extracted, which were used to construct cDNA libraries, separately. 20.69, 19.36, 25.24, 19.58, 23.65, and 20.49 million clean sequence reads in total were generated from the six libraries of CK1, CK2, CK3, Cd1, Cd2, and Cd3, respectively (Table 1). There were 25,852 unigenes, of the 31,214 unigenes, had been annotated. 11,124 unigenes ranged in lengths from 300-1000 bp, and 14,227 unigenes with lengths of more than 1000 bp (Table 2).

For annotation and validation of the assembled unigenes, sequence similarity searches were carried out in seven public databases, i.e., the GO, NR, NT, COG, KOG, and PFAM databases. The results manifested that, out of 56,044 unigenes, 18,883 (33.69%), 25,848 (46.12%), 25,852 (46.13%), 10,108 (18.04%), 14,553 (25.97%), 21,648 (38.63%), 20,473 (36.53%) and 25,840 (46.11%) unigenes displayed remarkable similarity to known proteins in the GO, NR, NT, COG, KOG, PFAM, SwissProt and KEGG databases, respectively (Fig.4, Table.2). Together, 31,214 (55.70%) unigenes revealed similarity to known proteins in at least one of these seven databases (Table.2).

Identification and functional enrichment analysis of the DEGs

All sequencing reads were realigned to the unigenes in order to confirm the expression levels of 56,044 de novo assembled unigenes. FPKM values for each gene between CK and Cd-treated groups were performed to obtain the DEGs in response to Cd stress. A total of 1,716 DEGs (1,157 up-regulated genes and 559 down-regulated genes) had been identified between CK and Cd-treated groups (Fig. 5).

In our study, GO and KEGG pathway were used to analyze and classify the DEGs. The numbers of DEGs in CK and Cd-treated groups were summarized in three main GO categories (Fig. 6, Table S1). Gene Ontology analyses were performed in seedlings of tomato plants in CK and Cd-treated group. In total, 18,883 genes were matched to 51 GO items, which consisted of 15 items in Cellular Component (CC), 12 items in Molecule Function (MF) and 24 items in Biological Process (BP). Given the negative logarithm of the P value, the major four biological processes identified for these genes were cellular process, metabolic process, biological regulation, and response to stimulus (Fig. 6). The largest four cellular components associated with these genes were cell, cell part, organelle, and membrane (Fig. 6). The major four molecular functions for these genes were binding, catalytic activity, transcription regulator activity, and transporter activity (Fig. 6).

For the COG analysis, 10,108 unigenes (Table 2) from all unigenes were categorized to 20 categories (Fig. 7, Table S2). The most distributed one was the cluster of general function prediction only (163), followed by secondary metabolites biosynthesis, transport and catabolism (89), transcription (78), post-translational modification, protein turnover, chaperones (71), carbohydrate transport and metabolism (61), and signal transduction mechanisms (59).

KEGG pathways were applied to analyze these DEGs. KEGG provided the integration of pathways, such as metabolic pathways, plant hormone signal transduction and plant-pathogen interaction pathways. 25,840 unigenes were mapped to 89 KEGG pathways based on KO terms for assignments (Fig. 8, Table S3). Using a probability of FDR ≤0.05, the top 20 items for KEGG pathways were presented in Figure 8. The most distributed pathways were phenylpropanoid biosynthesis (64), plant-pathogen interaction (27), glutathione metabolism (20).

Auxin-mediated genes in response to Cd stress

Through the analysis of DEGs, some auxin-mediated genes in responsive to cadmium stress were discovered (Table.3). Based on the transcriptome information, 141 significant DEGs were enriched in “plant hormone signal transduction” (Ko14488), most of which were participated in JA, auxin, GA, BR, and cytokinin signaling pathways (Table S4). Compared to CK, 14 related GO terms were identified, and two pathways were significantly enriched (p < 0.05) to further explore plant hormone biosynthesis, metabolism and signal transduction in Cd-treated groups (Table S4), including “plant hormone signal transduction” (GO: 0009734), and “zeatin biosynthesis” (GO: 0009851). For the GO term “auxin-activated signaling pathway”, we analyzed the expression of 28 auxin metabolism- and signaling-related genes and found that most of the genes were up-regulated in Cd (Table S5). In “response to brassinosteroid” genes encoding gibberellin-regulated protein 1-like, AP2/ERF and B3 domain-containing transcription factor RAV1 and steroid 5-alpha-reductase DET2 (LOC101248656, LOC101259430, and LOC101255051) were significantly down-regulated in Cd-treated groups, while another gene encoding gibberellin- regulated protein 11-like (LOC101260098) were up-regulated in Cd-treated groups (Table S5). Together, these results suggest that auxin metabolism and signal transduction, as well as BR affect the elongation of root and stem in Cd-treated groups.

Expression profile of DEGs encoding enzymes involved in lignin biosynthesis

Genes involved in the lignin biosynthetic pathway have been extensively studied in model plants and some fruit species. In the present study, seventeen immensely differentially expressed genes associated with the lignin biosynthetic pathway had been identified. Compared to control, 14 DEGs were up-regulated, three DEGs were down-regulated in Cd-treated tomato, which were respectively LOC101262425, LOC101262063 and LOC101265652 (Talbe. 4). 2 DEGs (LOC101265690 and LOC101265977) encoded caffeoyl-CoA o-methyltransferase (EC:2.1.1.104). 2 DEGs (LOC101249612 and LOC101246312) encoded peroxidase (EC:1.11.1.7). 5 DEGs (LOC101253619, LOC101262977, LOC101263266, LOC101262425 and LOC101249792) encoded laccase (EC:1.10.3.2). 3 DEGs (LOC101261765, LOC101247849 and LOC101262063) encoded 5-O-(4-coumaroyl)-D-quinate 3'-monooxygenase (EC:1.14.14.96). CTOMT1 encoded caffeic acid 3-O-methyltransferase (EC:2.1.1.68). Furthermore, there were also two genes (4CL and CCR1) that were well known in the lignin synthesis pathway, but their expressions were not significant. The results suggested that cadmium ion treatment activated lignin biosynthesis process.

Photosynthetic creatures are extraordinarily susceptible to heavy metal substances. The impact of metal ions on higher plants comprises the destruction of numerous physiological functions, such as photosynthesis, mineral nutrient absorption, respiration and water absorption [28]. These detrimental effects can be minimized by improved metal isolation, tissue tolerance and antioxidant responses in the plants [29]. In the current study, we searched for various ultramicro-morphological, physiological and biochemical responses to Cd excess.

Inhibition of root growth is an obvious symptom of Cd toxicity [30]. In Arabidopsis, the effects of metals on plant aerial portions include loss of leaf area and weight as described [31]. Compared with control, growth inhibition and biomass dry weight reduction became more and more obvious with the extension of treatment time in the Cd-treated seedlings of Solanum lycopersicum (Fig. 1).

Compared with control, our research findings also revealed that lignin content was increased in roots of Cd-treated tomato seedlings (Fig. 3). Lignified roots lose their ability for nutrient absorption and subsequently the capacity for growth, which eventually led to inhibiting root of the whole plants [32]. So growth inhibition could be interpreted by the cell wall stiffening, cell division reducing and root cell death related to the intense inducement of lignification formation, peroxidase activity in cell wall, and reduction in the cell extension under heavy metal stress [33], as was found in alfalfa plants treated with Cd²⁺ [34].

In leaves of P.crispus, the increase of MDA indicated that heavy metal had given rise to oxidative harm to the plant, evidently increased lipid peroxidation and decreased chlorophyll contents [35]. In many plant species, increased MDA levels after exposure to Cd have been reported [36, 37]. Similarly, accumulation of MDA levels was also explored in the roots of L. esculentum when exposed to Cd (Fig. 2A).

Decreased chlorophyll content in leaves had been demonstrated that Cd²⁺ restrained enzymes associated with carotenoid and chlorophyll biosynthesis, generated peroxidation of chloroplast membranes, and retarded the mergence of these pigments into photosystem complexes [38, 39]. Cadmium has been reported to alter many physiological processes, especially chlorophyll degradation [40]. Cd also impaired photosynthesis by inducing nutritional disorders [41]. With respect to tomato seedlings exposed to Cd²⁺, the loss in chlorophyll content was presented in Fig. 3B, which could be due to peroxidation of chloroplast membranes mediated by Cd²⁺. The above results were in agreement with their findings as described by Maksymiec et al. [42] and Piotrowska et al. [37]. Cadmium inhibits photosynthesis which brings about the reduction of biomass growth and the prevention of chlorophyll to incorporate into photosynthetic membranes of chloroplast [43].

Plants can respond to oxidative pressure by promoting enzymatic antioxidant systems. John et al. [44] had confirmed a gently increase in the antioxidant activities when Cd concentration rose in mustard. Compared with control, the POD activities were significantly higher in roots of cotton at all Cd levels [45]. Similarly, Hashem et al. [46] also evidenced that CAT and POD were enhanced in Cd-stressed tomato seedlings. In the present study, it was observed that POD activity was up-regulated under Cd stress (Fig. 2C).

CAT activity was enhanced in tobacco plants under toxicity of heavy metal cadmium [47]. Excess Cd induced enhancement of CAT and SOD antioxidant enzymes which play important role in alleviating Cd toxicity [48]. According to these opinions of the authors, Cd tolerance could be associated with the enhancement of CAT activity. In the present study, CAT activity was significantly higher in the roots of tomato seedlings grown under Cd stress conditions (Figure.2D). However, scavenging enzyme activity of reactive oxygen species was unaffected or depressed in rice leaves by excessive Cd [49]. The difference suggested that the impact of Cd stress on the antioxidant enzymes was very intricate and associated with plant tissues, treatment time, genotypes and plant species.

Bochicchio et al. [50] demonstrated the ‘stress-induced morphogenic response’ (SIMR) as a decrease in principal root (PR) length and an increase in the number of lateral roots (LRs). In Arabidopsis, the remodeling of the root architecture also incorporates the increase in root diameter either as an extension of cortical parenchyma layers and as a consequence of metal-induced xylogenesis in response to Cd and Cu [50, 51].

Metallothioneins (MT) were a kind of heavy metal-binding proteins rich in cysteine, which can protect against oxidative stress and cadmium toxicity [52]. Haberkorn et al. [53] evidenced that cadmium and zinc induced MT genes transcription is triggered through the activation of MREs-bonded metal transcription factor-1 (MTF-1). In higher plants, these sites of photosynthetic reaction may be the primary target of prevention in response to Cd stress [54].

More and more studies have shown that the responses to Cd stress are involved in a variety of plant phytohormones [55]. Cd-induced slight oxidative stress in barley leads to the inhibition of root growth through adjusting IAA signaling pathway in root tip [56]. In rice, auxin signal modification plays a major role in the expression of cell-cycle genes under Cd stress [57]. Cd stress inhibits the contents of free IAA in maize roots, manifesting there is an interaction between GH3-mediated auxin levels and Cd [58]. Previous research has shown that auxin and its transport are involved in plant responses to abiotic stress [59]. In our study, the different expression patterns of auxin-related genes, including auxin transport, auxin synthesis, and downstream auxin response genes, under Cd treatment in tomato have been investigated. The expressions of most auxin-related were up-regulated by Cd treatment (Table S4). However, RNA-Seq data also showed that genes related to response to brassinosteroid were obviously reduced by Cd treatment in tomato seedlings (Table S4).

Lignification is part of the normal differentiation program and functioning of specific cell types, but can also be triggered in response to various biotic and abiotic stresses [60]. A role of laccase during the initial stages of lignification may serve to limit cellular damage by H₂O₂ before polysaccharide deposition in the cell wall is completed [61]. The release of apoplastic H₂O₂ and cell wall lignification led to growth inhibition [62, 63]. Most DEGs (CTOMT1, LOC101249612, LOC101265690, LOC101247849,and LOC101261765) involved in lignin biosynthesis in the COMT and C3’H pathway were up-regulated which were the key genes to trigger lignification, except for LOC101262063 (Table. 4). PAL is involved in the conversion of L-phenylalanine to trans-cinnamic acid, a key intermediate in the pathway of phenolics and lignin [64]. Therefore, in this study, enhance activity of PAL (LOC101246969) is responsible to the increase of phenol and lignin concentration (Table. 4).

Previous studies mostly have focused on the effects of physiological indicators or comparing these morphological changes. Few studies had explained these mechanism of action at the molecular level. The results of our study suggested that lignin contents were increased, dry weight biomass were reduced and principal roots were inhibited under Cd stress. However, our RNA-Seq data explained these phenomena at gene expression levels.

Plant material and growing conditions

Wild type seeds of Lycopersicum esculentum A57 which were purchased from Huazhong Agricultural University were applied in this experiment. It was disinfected with 10% NaClO for 20 min, followed by washing twice with sterilize-distilled water. Sterile seeds were planted on 1/2 MS medium, vernalizated for 3 days at 4℃, and germinated in a greenhouse under light conditions (25 + 2℃, 16 h light/8 h darkness). On day 7 of growth, seedlings with uniform size were chosen and transferred into plate holes with half strength of Hoagland nutrient solution [65] on plastic pots (one plant per pot) including 10 μM Cd²⁺. Nutrient solution was replaced after every four days. Seedlings were grown in a controlled growth cabinet at constant light intensity (250-350 μmol m^-2s^-1), and a relative humidity of 55-60%, light/dark regime of 16 h/8 h at 25 + 2 ℃. All the morphological parameters were determined after from 1 to 7 days of treatment.

Phenotypic parameters and Histochemical staining

After cadmium ion treatment, plants were reaped and separated into stem, leaf and root, respectively. Six plants were randomly selected from each treatment and their biomass, taproot and lateral root length were determined. Chlorophyll content was measured on the basis of the method of Pei et al. [66].

For lignin staining, the samples were rinsed several times with distilled water and then incubated for 5 min in phloroglucinol-HCl solution (1% [w/v] phloroglucinol in 6 N HCl) [67]. After dying, phloroglucinol-HCl was replaced by distilled water and the samples were placed on glass slides.

Biochemical Analysis

Fresh samples (0.2g) were ground to homogenate in 0.6% 2-thiobarbituric acid (TBA) (10 ml) in 10% trichloroacetic acid (TCA) with a pestle and mortar. Malondialdehyde (MDA) content was determined to represent the degree of lipid peroxidation as reported by Daud et al. [45]. The MDA content was represented as nmol g^-1 fresh weight.

Guaiacol was used as the substrate to determine peroxidase (POD) activity by Morales et al. [68] with some modifications. H₂O₂was served as the substrate to measure catalase (CAT) activity according to Luna [69].

Transcriptomic analysis

After harvest, tomato seedlings from both control and Cd treatment were frozen in liquid nitrogen with three independent biological replicates. Total RNA was extracted and purified with Trizol reagent (Invitrogen, CA, USA) through lysis buffer on the grounds of the manufacturer’s instructions [70]. Total RNA quality was assayed with RNA 6000 Nano LabChip Kit by Agilent 2100 Bioanalyzer (Agilent Technologies, USA) with a RNA Integrity (RIN) score >7.0. Total RNA (about 10 μg) was subjected with oligo (dT) attached magnetic beads (Invitrogen) to isolate (poly A) mRNA. Following purification, mRNAs were broken down small fragments with divalent cations at a gradual increase in temperature. First and second-strand cDNA was synthesized by means of the broken mRNA fragments as template. Then, the cDNA fragments were screened and enriched through PCR amplication to create the ultimate optimized library on the grounds of the instruction for mRNASeq sample preparation kit (Illumina, San Diego, USA). Paired-end sequencing with average insertion size of 300 bp (+50 bp) was accomplished on an IlluminaHiseq2000 (Illumina Inc., San Diego, CA, USA) in Genepioneer Biotechnology Company (Nanjing, China).

Differentially expressed genes analysis

The raw reads produced by Hiseq2000 were filtrated to remove low-quality reads to obtain clean reads. Clean reads were aligned to the reference genome of Solanum lycopersicum with the HISAT program [71]. Subsequently, The fragments per kilobase of transcript per million mapped reads (FPKM) were applied to describe as the expression levels of unigene by means of the computation of StringTie software package [72]. Gene function was annotated in view of the following databases: Eukaryotic ortholog Groups (KOG/COG) (v0.2.28), Nr (NCBI non-redundant protein sequences) (v0.2.28) [73], Swiss-Prot protein database (v0.2.28), Protein family (PFAM) (HMMER 3) [74], and Gene Ontology (GO) [75]. The DEGs were further carried out and calculated through the DEGseq R package (1.12.0) [76]. FDRs≤0.05 (False Discovery Rates), Log₂ |fold-change| >1 and statistical significance (p value <0.05) were set as threshold for the DEGs between CK and Cd treatment. The DEGs were also carried out to KEGG pathway enrichment analysis by KOBAS (2.0.12) [77] and Gene Ontology (GO) enrichment analysis through GOseq software (1.10.0) [78].

Acknowledgments

We thank Tao-Tao Wang at Huazhong Agricultural University, Wuhan, China, for supplying Lycopersicum esculentum A57 seeds.

Author contributions

GS and YQL conducted experiments. QWL analyzed data. HHW and MLY contributed to the paper writing and review. JHZ designed the experiments, and drafted the manuscript. All authors read and approved the manuscript.

Funding

This research was supported by Natural Science Foundation of Hunan Province (No.2019JJ40282), General project of Education Department of Hunan Province (19C0757), Graduate Scientific Research Innovation Project of Hunan Province (CX20211006), and Talent Acquisition Fund of Hunan University of Science and Technology (E52062). The authors thank these organizations for financial support.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request. The datasets supporting the conclusions of this article are included within the article and its additional files, The raw Illumina sequence reads have been deposited into the National Genomics Data Center (https://bigd.big.ac.cn/) under accession number CRA005680.

Ethics approval and consent to participate

This article does not involve any human or animal testing performed by any of the authors.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Table 1 Summary of transcriptome sequencing data in untreated and Cd-treated seedlings of tomato.

#Sample	Read Sum	Base Sum	GC (%)	N (%)	Q20 (%)	Q30 (%)
CK1	20693643	6208092900	43.2	0	97.22	92.48
CK2	19356764	5807029200	43.13	0	97.42	92.92
CK3	25244621	7573386300	43.11	0	97.49	93.05
Cd1	19577707	5873312100	43.07	0	97.41	92.9
Cd2	23653409	7096022700	43.07	0	97.44	92.97
Cd3	20494798	6148439400	43.07	0	97.35	92.79

Table 2 Summary statistics of the number of unigenes mapping all annotated databases in untreated and Cd-treated seedlings of tomato transcriptomes.

#Anno_Database	Annotated_Number	300<=length<1000	length>=1000
COG_Annotation	10108	3395	6638
GO_Annotation	18883	7242	11341
KEGG_Annotation	25840	11120	14219
KOG_Annotation	14553	5443	8938
Pfam_Annotation	21648	8407	12934
Swissprot_Annotation	20473	7875	12271
nr_Annotation	25848	11122	14225
All_Annotated	25852	11124	14227
All	31214
Up-regulated genes (DEGs)	1157
Down-regulated genes (DEGs)	559

Table 3 Detailed annotations of DEGs associated with auxin signaling and transduction.

Term	DEGs Significant	GO ID	p value
auxin-activated signaling pathway	28	GO:0009734	-1.256331771
auxin biosynthetic process	5	GO:0009851	1.083509662
auxin transmembrane transporter activity	4	GO:0080161	1.400836057
basipetal auxin transport	7	GO:0010540	2.764018475
response to jasmonic acid	14	GO:0009753	1.440580428
brassinosteroid biosynthetic process	2	GO:0016132	2.382323196
regulation of auxin polar transport	1	GO:2000012	-1.027095463
auxin transport	13	GO:0060918	3.399362574
regulation of auxin mediated signaling p...	1	GO:0010928	1.042422854
response to auxin	34	GO:0009733	-1.354626393
response to cytokinin	8	GO:0009735	-1.350790477
cellular response to gibberellin stimulu...	6	GO:0071370	1.280062768
response to gibberellin	12	GO:0009739	-4.473627363
response to brassinosteroid	6	GO:0009741	-1.023033803

Table 4 Detailed annotations of DEGs associated with lignin biosynthetic pathway.

#id	CK-FPKM	Cd-FPKM	log2FoldChange	qvalue	significant	GO ID	KEGG_annotation
4CL	28.98715	34.55645	0.236926309	2.86E-07	not	GO:0016207	4-coumarate--CoA ligase [EC:6.2.1.12]
CCR1	29.860155	44.214443	0.497520387	1.04E-16	not	GO:0016621	cinnamoyl-CoA reductase [EC:1.2.1.44]
CTOMT1	29.626913	66.121094	1.101397554	5.70E-164	up	GO:0047763	caffeic acid 3-O-methyltransferase [EC:2.1.1.68]
LOC101249612	0.461796	1.68591	1.542133784	6.97E-06	up	GO:0009809	caffeic acid 3-O-methyltransferase [EC:2.1.1.68]
LOC101265690	2.672695	6.658911	1.314368494	8.97E-12	up	GO:0042409	caffeoyl-CoA O-methyltransferase [EC:2.1.1.104]
LOC101253619	1.170203	3.438956	1.487695192	1.66E-09	up	GO:0046274	laccase [EC:1.10.3.2]
LOC101247849	0.361496	2.348821	2.264957896	5.93E-13	up	GO:0009809	5-O-(4-coumaroyl)-D-quinate 3'-monooxygenase [EC:1.14.14.96]
LOC101262977	1.176061	2.37976	1.036114636	6.63E-07	up	GO:0046274	laccase [EC:1.10.3.2]
LOC101265977	3.606585	7.44251	1.172200124	5.31E-14	up	GO:0042409	caffeoyl-CoA O-methyltransferase [EC:2.1.1.104]
LOC101261765	0.125054	0.399141	1.631670688	0.0028687	up	GO:0046409	5-O-(4-coumaroyl)-D-quinate 3'-monooxygenase [EC:1.14.14.96]
LOC101265652	13.670917	4.568423	-1.613453213	1.05E-39	down	GO:0009809	cinnamoyl-CoA reductase-like SNL6
LOC101262063	0.400778	0.118556	-1.141969154	0.04969517	down	GO:0009809	5-O-(4-coumaroyl)-D-quinate 3'-monooxygenase [EC:1.14.14.96]
LOC101246312	1.27602	4.342206	1.616526025	7.83E-14	up	GO:0009809	peroxidase [EC:1.11.1.7]
LOC101263266	1.241215	2.483099	1.026043362	1.06E-06	up	GO:0046274	laccase [EC:1.10.3.2]
LOC101249792	1.05105	2.468036	1.042706113	1.31E-07	up	GO:0046274	laccase [EC:1.10.3.2]
LOC112940917	0.016894	0.063731	2.811961749	0.018955	up	GO:0005777	4-coumarate--CoA ligase-like 1
LOC101250429	1.589057	3.431661	1.136230979	2.51E-12	up	GO:0050412	Cinnamate beta-D-glucosyltransferase
LOC101246969	0.4204	0.572002	2.05759594	0.000443	up	GO:0009800	phenylalanine ammonia-lyase [EC:4.3.1.24]
LOC101262425	1.59433	0.568402	-1.46331875	3.49E-07	down	GO:0046274	laccase [EC:1.10.3.2]

No competing interests reported.

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Genome-wide transcriptome and physiological analyses provide new insights into cadmium tolerance to tomato seedlings

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