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Article

Genome-Wide Analysis of the Multidrug and Toxic Compound Extrusion Gene Family in the Tea Plant

by
Tao Xie
1,†,
Yumei Qian
1,†,
Deyan Wang
1,
Xiadong Yan
1,
Ying Jiang
1,
Min Li
1,
Hao Rong
1,* and
Tao Xia
2,*
1
Key Laboratory of Spin Electron and Nanomaterials of Anhui Higher Education Institutes, School of Biology and Food Engineering, Suzhou University, Suzhou 234000, China
2
State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei 230036, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(11), 2718; https://doi.org/10.3390/agronomy14112718
Submission received: 11 October 2024 / Revised: 5 November 2024 / Accepted: 15 November 2024 / Published: 18 November 2024
(This article belongs to the Section Horticultural and Floricultural Crops)
Browse Figures
Versions Notes

Abstract

:
The multidrug and toxic compound extrusion (MATE) family is the latest class of novel secondary transporters discovered in plants. However, there is currently no comprehensive analysis of the MATE gene family in the tea plant. In this study, 68 CsMATE genes were identified from the tea plant genome using bioinformatic methods. In general, we analyzed the evolutionary relationships, intron–exon structure, distribution in chromosomes, conserved domains, and gene expression patterns in different tissues and stresses of the CsMATE gene family. The 68 CsMATEs were phylogenetically divided into four major clusters (Class I to Class IV). The CsMATE genes within the same class exhibit similar structural features, while displaying certain distinctions across different classes. Evolutionary analysis indicated that the CsMATE gene family expanded mainly through gene duplication events, in addition to proximal duplication. Through the analysis of cis-acting elements, it was found that CsMATE genes may be involved in the growth, development, and stress response. Furthermore, we observed that certain CsMATE genes could be induced to exhibit expression under abiotic stress conditions such as low temperature, high salinity (NaCl), osmotic stress (PEG), and methyl jasmonate treatment (MeJA). The findings presented herein offer a crucial theoretical foundation for elucidating the biological functions of CsMATE genes, particularly in response to abiotic stress, and furnish valuable potential genetic resources for tea plant resistance breeding.

1. Introduction

The tea plant (Camellia sinensis) is a perennial economic crop that thrives in tropical, subtropical, and temperate regions and has its origins in southwest China [1]. Tea stands as the most widely consumed beverage globally and ranks among the top three non-alcoholic beverages worldwide [2]. The tea plant boasts an abundance of flavonoids, including catechins (flavanols), flavonoids, flavonols, and anthocyanidins. These compounds exhibit remarkable properties such as antioxidation, anti-inflammation, anticancer effects, cardiovascular protection, antibacterial activity, the regulation of hyperglycemia levels, as well as properties that combat obesity [3].
Flavonoids, as a crucial class of secondary metabolites in plants, are believed to exert a significant role in plant defense owing to the potent antioxidant properties [4]. Similarly to other plants, the biosynthesis of flavonoids in the tea plant involves the shikimic acid pathway, phenylpropanoid pathway, and flavonoid pathway [5,6,7]. The shikimate pathway provides the starting substrate phenylalanine for the phenylpropane pathway. Flavonoid biosynthesis occurs at different locations within plant cells’ cytoplasm and is subsequently transported to specific organelles for storage, such as vacuolar membranes for anthocyanins [8]. In contrast to the flavonoid biosynthesis pathway, there is limited knowledge about flavonoid transport [9,10]. The transportation of anthocyanins to vacuoles primarily occurs through vesicles and transporters [10,11]. Among these models, most scientists strongly support the transporter-mediated model which includes ABC transporters, the MSF superfamily, and MATE proteins [8,9,10,11,12,13].
The MATE family is the latest class of novel secondary transporters discovered. The first MATE protein was cloned from Vibrio parahemolyticus, and subsequent investigations have revealed its abundance across various species including bacteria, yeasts, animals, and plants [14,15]. Previous studies have demonstrated that MATE transporters play direct or indirect roles in numerous physiological processes within plants, encompassing aluminum stress tolerance, the detoxification of toxic complexes or heavy metals, metal ion uptake and transportation, and the transport of diverse plant hormones [16,17].
The expansion of the MATE gene family in plants leads to the differentiation of protein function. Compared with mammals and bacteria, plants exhibit a higher abundance of MATE genes. For instance, Arabidopsis, rice, tomato, alfalfa, and soybean genomes contain 56, 46, 67, 88, and 117 MATE genes, respectively, whereas bacterial and mouse genomes have less than 15 [15,18,19,20,21]. The polyploidy and tandem replication of plant genomes during evolution are the primary factors contributing to the expansion of the MATE gene family [20,22]. Among the plants studied thus far, Arabidopsis MATE proteins have been extensively researched with approximately 10 identified functions, including the regulation of plant organogenesis, ion and metabolite transportation, and conferring resistance to abiotic stress and aluminum stress [17,23,24]. The ZRZ gene in Arabidopsis belongs to the MATE gene family; the overexpression of ZRZ promotes leaf and axillary bud growth, thereby enhancing the overall growth rate [23]. Lu et al. found that the protein encoded by the cotton MATE gene Gh_D06G0281 is located on the cell membrane, and the heterologous overexpression of Gh_D06G0281 in Arabidopsis could increase the antioxidant oxidase content under different abiotic stress conditions [25]. Additionally, Arabidopsis MATE45 is involved in the regulation of anthocyanin response to abiotic stress, while also mediating abiotic stress responses through antagonizing local abscisic acid signaling [26]. In addition, the analysis conducted on rapeseed, Chinese pear, cotton, rice, flax, soybean, and populous revealed that numerous MATE genes were involved in various abiotic stress processes including salt, drought, and cold stresses [18,20,22,27,28,29,30]. In addition to investigating abiotic stress, Chen et al. also conducted a study on the transport function of MATEs in flavonoids. By performing a correlation analysis between flavonoids and the MATE genes, it was discovered that the MATE genes may play a role in the process of flavonoid accumulation [31].
The involvement of MATE proteins in numerous vital physiological processes in plants renders them potential target genes for breeding programs aimed at enhancing important traits, such as nutrient uptake, secondary metabolite content, abiotic stress tolerance, and aluminum toxicity resistance [32]. Therefore, a comprehensive analysis of the MATE gene family in the tea plant is imperative for elucidating the potential functionalities of the MATE genes. Surprisingly, despite the identification of several plant MATE transporters thus far, complete functional identification is rarely studied in the tea plant. In this study, we conducted a comprehensive study on the structure, conserved domains, chromosome localization, subcellular localization, expression patterns, and collinearity of 68 MATE genes in the tea plant. This study lays a crucial foundation for future functional investigations on CsMATEs and may offer novel insights into enhancing the stress resistance of the tea plant.

2. Materials and Methods

2.1. Genome-Wide Identification of CsMATE Genes in Tea Plant

The complete protein sequences and genome sequences of the tea plant were downloaded from the Tea Plant Information Archive (TPIA, http://tpia.teaplants.cn/, accessed on 1 August 2024) [33,34]. Hidden Markov Model (HMM) profiles of conserved MATE domain (MATE domain, pfam number: PF01554) acquired from InterPro (https://www.ebi.ac.uk/interpro/, accessed on 1 August 2024) were used as a query for blast to identify the CsMATEs in the tea plant [19,35]. HMMER v.2.39.0 software (https://www.ebi.ac.uk/Tools/hmmer/, accessed on 2 August 2024) was used to carry out a search of the whole genome protein sequences of the tea plant and obtained the candidate proteins of CsMATEs [36]. To improve the accuracy of subsequent analyses, we analyzed the protein length and transmembrane domain of the candidate CsMATE genes with TMHMM Server v.2.0 (https://services.healthtech.dtu.dk/services/TMHMM-2.0/, accessed on 5 August 2024) [37,38]. CsMATEs were further manually screened according to a previous study (protein length > 400 amino acid residues and 8-12 transmembrane domains) [19].

2.2. Physicochemical Parameter and Characteristic of CsMATEs

The physicochemical parameter of CsMATEs including molecular weight (MW) and theoretical isoelectric points (pI) were analyzed by the protein isoelectric point calculator v.2.0 (http://isoelectric.org/, accessed on 8 August 2024), and the subcellular localization analysis was predicted by Cell-PLoc 2.0 (http://www.csbio.sjtu.edu.cn/bioinf/Cell-PLoc-2/, accessed on 8 August 2024) [39,40]. Information about the initiation and termination sites of CsMATEs on chromosomes was extracted from GFF files from the TPIA, and location images were generated using MG2C v.2.0 (http://mg2c.iask.in/mg2c_v2.0/, accessed on 8 August 2024).

2.3. Construction of Phylogenetic Tree for CsMATE Proteins

The protein sequences of 68 CsMATEs and 56 Arabidopsis AtDTXs were, respectively, acquired from the TPIA and TAIR database (https://www.arabidopsis.org/, accessed on 9 August 2024). Multiple amino acid sequence alignments of these protein sequences were carried out by Clustal W (http://www.clustal.org/clustal2/, accessed on 12 August 2024) [41]. Phylogenetic tree was performed with neighbor-joining (NJ) method combined with 1000 bootstraps in MEGA 7.0 software [42].

2.4. Conserved Motif and Intron-Exon Composition Analysis of CsMATEs

The conserved motifs in CsMATE proteins were analyzed by the Multiple Em for Motif Elicitation website (MEME, http://meme-suite.org/tools/meme, accessed 13 August 2024) using the website default parameters and setting the maximum motifs to 10. The exon–intron compositions of CsMATEs were analyzed with the tea plant GFF profile by TBtools v.2.086 [43]. The CsMATE gene structure and conserved motif pattern were visualized with the Amazing Optional Gene Viewer function in TBtools.

2.5. Identification of MATE Homologs

The gene duplication events and synteny relationships among Camellia sinensis var. sinensis, Coffea canephora, and Actinidia chinensis were performed by Multiple Collinearity Scan toolkit X version (MCScanX) software with default parameter settings [44]. The relationship of paralogous MATEs in C. sinensis and the orthologous MATEs among C. sinensis and other species were visualized by TBtools [43]. The analysis of the duplication event was applied with the MCScanX duplicat_gene_classifier program.

2.6. Cis-Acting Element Analysis of CsMATE Genes

The SAMtools v.1.19.2 software was employed to extract the 2000 bp upstream sequence of the start codon of the MATE gene family members from the tea plant GFF file. Subsequently, these obtained sequences were uploaded to the PlantCatre database (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 17 August 2024) for the prediction of cis-acting elements [45].

2.7. Tissue Expression Pattern of CsMATE Genes

The expression data of CsMATE genes in eight major tea plant developmental tissues and organs, including roots, stems, young leaves, mature leaves, old leaves, aptical buds, flowers, and fruits, were obtained from the TPIA [33,34]. The log2-transformed FPKM + 1 values were utilized to represent the expression levels of the CsMATE genes across different tissues and organs. These data were visualized using TBtools software.

2.8. Expression Patterns of CsMATE Genes Under Diverse Treatments

To investigate the response of the CsMATE genes under diverse abiotic stress treatments, the transcriptome data of tea plant genes under cold acclimation (CA1: fully acclimation at 10 °C, CA3: cold response at 4 °C), PEG, NaCl, and MeJA stress were downloaded from the TPIA [33,34]. The heat maps were constructed with TBtools by using the log2-transformed TPM ratio between the treatment group and the control group (CK). If the TPM value is lower than 1 under normal conditions and treatment conditions, the log2-transformed ratio is defined as 0, indicating that there is no difference after treatments.

3. Results

3.1. Genome-Wide Identification and Characteristics of MATE Gene Family Members in Tea Plant

To identify members of the MATE gene family in the tea plant, the MATE domain was used as a query for genome-wide analysis. A total of 98 CsMATEs were identified in the tea plant genome and named by sequence numbers from CsMATE1 to CsMATE98 according to the position on the chromosome (Tables S1 and S2). However, according to previous studies, 30 CsMATEs with a protein length < 400 amino acids or a number of transmembrane domains < 8 were excluded [27,46]. Finally, 68 CsMATE proteins were retained for further study (Table S2).
Detailed molecular characteristics of CsMATE proteins were analyzed including protein length, MW, pI, and predicted subcellular localization (Table S2). The protein length of CsMATE proteins consists of 401 (CsMATE29) to 987 (CsMATE15) amino acids. The pI of CsMATE proteins ranged from 4.73 (CsMATE17) to 9.22 (CsMATE86), and the MW ranged from 43.65 (CsMATE29) to 111.11 (CsMATE15) kDa. The results of subcellular localization prediction showed that all of the sixty-eight CsMATE proteins were cell membrane-localized, and two of them (CsMATE20 and CsMATE21) were also localized in te chloroplast, suggesting that CsMATE proteins may be involved in the membrane transport of molecular substances.

3.2. Phylogenetic Analysis of CsMATE Proteins

In order to understand the evolutionary relationship of CsMATE proteins, a neighbor-joining phylogenetic tree of MATE proteins in the tea plant and Arabidopsis was constructed. Here, 124 MATE proteins were classified into four classes named Class I to Class IV, which contain twenty-three CsMATEs and twenty-two AtDEXs, twenty CsMATEs and nineteen AtDEXs, fifteen CsMATEs and nine AtDEXs, and ten CsMATEs and six AtDEXs, respectively (Figure 1). Interestingly, parts of the MATEs of Arabidopsis or the tea plant were clustered on a single branch, such as CsMATE10, CsMATE81, CsMATE82, and CsMATE83 and AtDEX20, AtDEX21, AtDEX22, AtDEX23, AtDEX24, and AtDEX25, suggesting that both Arabidopsis and the tea plant have produced many new genes during evolution.

3.3. Conserved Motif, Gene Structure, and Chromosomal Localization Analysis in CsMATEs

A total of 10 conserved motif were identified in CsMATE proteins by MEME (Figure S1). An extremely conserved motif (motif 8) existed in all CsMATE proteins, and a relatively conserved motif (motif 7) existed in all CsMATE proteins except CsMATE6, CsMATE29, CsMATE34, CsMATE81, and CsMATE82 (Figure 2B). The distribution of conserved domains in CsMATE proteins was divided into two categories: CsMATE proteins with only two conserved motifs and CsMATE proteins with at least eight conserved motifs. Among them, only ten CsMATE proteins contained two conserved motifs, and the entirety of these CsMATE proteins belonged to Class IV. The remaining 58 CsMATE proteins exhibited the presence of nearly all conserved motifs, with only 10 CsMATEs (CsMATE1, CsMATE11, CsMATE12, CsMATE13, CsMATE16, CsMATE53, CsMATE59, CsMATE82, CsMATE88 and CsMATE93) lacking a single motif and 9 CsMATEs (CsMATE6, CsMATE29, CsMATE34, CsMATE46, CsMATE47, CsMATE55, CsMATE58, CsMATE83, and CsMATE97) lacking two motifs.
The variability of exon–intron structure pattern is closely related to functional disparities and gene expression [47]. In C. sinensis, the number of introns varies significantly among members of the CsMATE gene family, ranging from 0 to 16 (Figure 2C). Among them, only seven CsMATEs did not contain introns. Furthermore, genes with closer evolutionary relationships exhibited similar exon–intron structure patterns, suggesting potential functional similarities. For instance, the 15 CsMATE members of Class III contain only 1–3 exons, while the 10 CsMATE members of Class IV contain 11–14 exons.
In order to assess the chromosomal distribution of CsMATEs, the tea plant genome annotation file was used for the characterization of CsMATEs. The results revealed that CsMATEs exhibited an uneven distribution across the fourteen chromosomes and seven scaffolds of C. sinensis (Figure 3). From the published chromosome level genomes, a total of 59 CsMATEs were mapped to the fourteen chromosomes, which were assembled relatively completely, while nine CsMATEs still remained on scaffolds. Notably, chromosome 6 harbored the highest number of CsMATEs with a count of ten, followed by chromosome 1 with a count of seven. Both chromosomes 4 and 7 contained six CsMATEs each, whereas both chromosomes 8 and 9 also possessed six CsMATEs each. Except for chromosome 13, all other chromosomes encompassed varying numbers of CsMATEs ranging from 1 to 4. Additionally, nine CsMATEs were mapped to seven scaffolds (Contig 310, Contig 341, Contig 783, Contig 1054, Contig 1197, Contig 1221, and Contig 1303), averaging one or two CsMATEs per scaffold.

3.4. CsMATEs Gene Duplication Events and Collinearity Relationships Between Four Genomes

Using MCScanX software, we identified 13346 paralogs of 8446 gene pairs (approximately 26.41%) in the C. sinensis genome. Within the CsMATE gene family, we identified 20 paralogs of 13 gene pairs, accounting for about 29.41%. Next, we analyzed the gene duplication events in the CsMATE gene family in the tea plant and showed that all CsMATEs were the result of a gene duplication event (Figure 4, Table S3). Among them, seven CsMATEs originated from proximal duplication, which are nearby but not adjacent to the chromosomal region, twenty CsMATEs originated from tandem duplication that exhibit coherent repeats, twenty CsMATEs originated from the whole-genome duplication (WGD) which are collinear genes within collinear blocks, and twenty-one CsMATEs arose from dispersed duplication belonging to other types excluding segmental, tandem, and proximal duplication. These findings indicate that gene duplication events, in addition to proximal duplication, play a pivotal role in the formation and expansion of the CsMATE gene family in C. sinensis.
To further understand the evolutionary relationships of the CsMATE genes, we conducted an analysis of the collinearity relationships between Arabidopsis, kiwifruit (A. chinensis), coffee (C. canephora), and the tea plant (Figure 5). The result revealed that a large number of orthologs exist between C. sinensis and other species. In total, forty-nine CsMATEs exhibited collinearity with MATE genes in three related species, including twenty with Arabidopsis, thirty-seven with coffee, and forty-three with kiwifruit. MATE genes in the tea plant and kiwifruit have more collinear gene pairs, indicating that they are more closely related. Interestingly, we observed that 12, 32, and 25 of the CsMATEs located in collinearity blocks between the tea plant and Arabidopsis, coffee, and kiwifruit, respectively, were single-copy genes. This result suggested that more than half of the CsMATEs in the tea plant genome had undergone loss or deletion events during evolution, a slightly higher proportion than that in the genome-wide level [33].

3.5. Cis-Acting Element Analysis in the Promoter Regions of CsMATEs

Notably, 8150 cis-acting elements were identified in the promoter region of CsMATEs (Table S4). Based on previous study, these cis-elements mainly included gene transcription, site binding, tissue expression, secondary metabolism, circadian control, cell cycle, and various responsive progresses (Figure 6). Among them, there were 6537 gene transcription elements, accounting for 80.2% of the total number identified, predominantly composed of TATA-box (3931), CAAT-box (2591), and A-box (15). The second most abundant group was light-responsive elements, which accounted for 9.95% of the overall distribution among CsMATE promoter regions. Plant hormone-responsive regulatory elements were also highly prevalent, mainly including the MeJA-response element (TGACG-motif, 72; CGTCA-motif, 72), abscisic acid-response element (ABRE, 123), salicylic acid-response element (TCA-element, 24), gibberellin-response element (GARE-motif, 21), and auxin-response element (TGA-element, 23; P-box, 33). Furthermore, the majority of CsMATEs exhibit cis-regulatory elements associated with various abiotic stresses, such as ARE elements and GC motifs associated with hypoxia stress, LTR elements associated with low temperature stress, and MBS elements associated with drought stress. The aforementioned results implied that the transcriptional level of CsMATEs may be subjected to diverse external stimuli, thereby potentially exerting significant influences on hormone signaling pathways and abiotic stress responses in the tea plant.

3.6. Expression Profile of the CsMATE Genes in Different Tissues

To investigate the potential functions of CsMATE genes, tissue expression patterns were analyzed (Figure 7). Out of the 68 CsMATE genes examined, 10 showed no expression in any tested tissue or developmental stage. However, the remaining 58 CsMATE genes were expressed in at least one tissue. The majority of CsMATE genes displayed significant variations in their expression levels among different tissues and developmental stages, and the expression of some CsMATE genes demonstrated highly tissue-specific characteristics. For instance, the expression level of CsMATE2, CsMATE5, CsMATE9, CsMATE14, CsMATE26, CsMATE29, CsMATE30, CsMATE41, CsMATE51, and CsMATE56 were higher in roots than other tissues. On the other hand, CsMATE27, CsMATE37, and CsMATE55 were highly expressed in flowers. Interestingly, the expression level of CsMATE40, CsMATE50, CsMATE92, and CsMATE97 were higher in leaves, and the expression profiles gradually changed as the leaves matured and aged. Additionally, constitutive expression was observed in 15 CsMATEs, with CsMATE10, CsMATE17, CsMATE25, CsMATE38, CsMATE61, and CsMATE85 exhibiting high expression levels across all tissues. The constitutive expression patterns of these CsMATEs suggest their potential involvement throughout the entire process of plant growth and development. Collectively, the above results indicate that different CsMATE genes may play functions in specific developmental stages and tissues of the tea plant.

3.7. Expression Profile of CsMATE Genes Under Various Treatment

As previously mentioned, the promoters of CsMATE genes were found to contain numerous cis-acting elements related to abiotic stress and hormonal responses. Therefore, the expression profile of CsMATE genes following various abiotic stresses and hormone treatments were investigated. As shown in Figure 8, the transcription of some CsMATE genes were modulated by abiotic stress treatment. For example, CsMATE5, CsMATE6, CsMATE7, CsMATE10, CsMATE11, CsMATE23, CsMATE40, CsMATE83, and CsMATE97 were significantly induced by cold acclimation (log2Foldchange > 2). Moreover, NaCl treatment resulted in the significant induction of CsMATE1, CsMATE11, CsMATE41, and CsMATE51, with CsMATE41 and CsMATE51 exhibiting an over 20-fold increase in expression levels. Under PEG stress conditions, CsMATEs were not significantly induced, except for CsMATE2, which exhibited slight induction after 48 h of PEG treatment, and CsMATE51, which showed continuous strong induction under PEG treatment. Interestingly, the expression level of CsMATE genes also underwent significant changes following MeJA treatment. Among them, six CsMATE genes (CsMATE4, CsMATE7, CsMATE41, CsMATE51, CsMATE61, and CsMATE64) were significantly up-regulated by MeJA treatment. Thereinto, it was observed that CsMATE51 was significantly induced by NaCl, PEG, and MeJA treatments, suggesting its potential involvement in different stress responses. Overall, these findings suggest that different MATE gene members in the tea plant possess diverse functions under numerous treatments.

4. Discussion

The tea plant (Camellia sinensis), the origin of the second most widely consumed beverage globally after water, is highly esteemed by consumers for its distinctive bioactivity and health benefits [48]. The secondary metabolites, particularly polyphenols, are pivotal in determining both the flavor and health-promoting properties of tea [49]. Among these compounds, the MATE gene family is prevalent across various plant species and plays a critical role in transporting diverse secondary metabolites, as well as enhancing plant resistance to stressors [17,29,50,51,52]. Consequently, conducting a comprehensive whole-genome identification and expression analysis of the tea MATE gene family holds significant scientific importance and practical implications.
While there have been some reports of MATE gene family studies across different plant taxa, a thorough investigation specifically focusing on tea plant MATE genes remains rarely reported [18,53]. In the current study, 68 CsMATE genes were identified by an exhaustive analysis of the tea plant genome. These genes exhibit uneven distribution throughout the genome across various chromosomes. For instance, there are ten CsMATE genes located on chromosome 6, while only one CsMATE gene resides on chromosomes 11 and 12—mirroring patterns observed in other plant species [54,55]. Phylogenetic analyses indicate that members of the CsMATE gene family likely originated from a common ancestral gene followed by lineage-specific divergence during evolutionary processes. The identified CsMATE gene members can be categorized into four distinct subgroups, consistent with findings reported for MATE genes in other organisms, such as Arabidopsis and apple [46]. Moreover, a gene structure analysis reveals the variability among these CsMATE genes concerning the intron number and positioning—ranging from 0 to 16—which may correlate with the functional diversity and regulatory mechanisms governing their expression. By examining conserved motifs within CsMATE gene members, we discovered that those within identical subgroups typically share similar motif compositions; notably, Class IV members predominantly contain motifs 7 and 8, which could account for the functional diversification among CsMATE gene members.
The tea plant is believed to have evolved from its ancestor, Ericales, through a whole-genome triplication (WGT) and WGD event, which may have resulted in an increased frequency of genomic rearrangements [56]. In comparison to the number of CsMATE gene families in the tea plant, potato, rice, mung bean, and Daucus carota exhibit 48, 46, 48, and 45 MATE gene family members, respectively [18,53,57,58]. This suggests that genome duplication during the evolution of the tea plant has significantly contributed to the diversity observed within the CsMATE gene family. Gene duplication primarily occurs through various mechanisms including WGD/segmental duplications, tandem duplications, proximal duplications, and dispersed duplications [59]. Among these mechanisms, WGD/segmental duplications (29.4%), tandem duplications (29.4%), and dispersed duplications (30.9%) are identified as the principal contributors to the formation and expansion of the CsMATE gene family; this aligns with previous research findings. Only about 10% of CsMATE genes arise from proximal duplication events. However, due to the limited studies on proximal duplication in plants thus far, its underlying causes remain unclear. Further evolutionary relationship analyses reveal that MATE gene family members from the tea plant share certain collinearity relationships with those from C. sinensis, coffee, and A. chinensis—wherein A. chinensis exhibits the highest degree at 63.2%, indicating a closer evolutionary relationship between the tea plant and A. chinensis.
The analysis of expression patterns has revealed the tissue-specificity of the CsMATE gene members in the tea plant. Studies have demonstrated that most CsMATE genes are expressed in various tissues, including the root, stem, and leaf, albeit at different levels. For example, CsMATE10/26/31/32 exhibit high expression in the root, suggesting their potential involvement in substance absorption or expulsion processes. Research has shown that AtDTX18, the homologous gene of CsMATE26, exhibits increased expression in roots and is capable of coumaroylagmatine transport and extracellular accumulation [24]. Conversely, CsMATE85/38/33 show higher expression levels in the stem, indicating their possible role in transporting substances from underground to aboveground parts. The differential expression of these CsMATE gene members may be associated with distinct requirements for secondary metabolite synthesis and transport among different tissues. Furthermore, under stress conditions, such as cold temperatures, droughts, or high salt environments, significant changes are observed in CsMATE genes expression levels, which suggests an important role for the response to abiotic stress. For instance, AtDTX50, a homologous gene of CsMATE2, acts as an ABA effector transporter. dtx50 mutants exhibit enhanced drought tolerance compared to wild-type plants [60]. Similarly, cotton GhDTX27 and CsMATE17 are homologous genes, and the heterologous overexpression of GhDTX27 enhances plant resistance against droughts, salt, and cold stresses in Arabidopsis [25]. This observation aligns with the analysis results on cis-elements present within CsMATE genes. Many members of the CsMATE gene family contain stress-related cis-acting elements which further supports their crucial role.
Additionally, we have observed that CsMATE51 exhibits responsiveness to various abiotic stresses, including NaCl, PEG, and MeJA. This phenomenon may be attributed to the presence of specific cis-acting elements within its structure. The identification of the ABA response element in the promoter region of CsMATE51 implies potential regulation by genes involved in the ABA signaling pathway, consequently influencing tea plant’s resistance to abiotic stresses such as drought stress. A previous study showed that the stresses can be alleviated by the application of MeJA, which is a hormone involved in plant signaling. MeJA can induce the synthesis of defensive compounds and initiate the expression of related genes, which can be used to combat the toxicity of salt stress, drought stress, low temperature stress, heavy metal stress, and other elements. Therefore, we speculated that CsMATE51 may also participate in abiotic stress regulation in this way. The genomic annotation of the tea plant has revealed that CsMATE51 encodes the Transparent testa 12 (TT12) protein. However, there is a lack of research on the involvement of TT12 in plant abiotic stress, which primarily pertains to anthocyanin-related processes. Based on this, we are more interested in the subsequent study on whether CsMATE51 participates in abiotic stress.
In addition to the relationship between abiotic stress and the MATE gene family, many studies have also studied the accumulation and transport of flavonoids by the MATE gene family. The analysis of the MATE gene family in upland cotton revealed that GhMATE12, GhMATE16, and GhMATE38 potentially participate in proanthocyanidins transport [35]. The investigation on Daucus carota demonstrated that DcMATE21 may be involved in the process of anthocyanin accumulation [57]. Chen et al. only identified 41 members of the MATE gene family from the tea plant, which could be attributed to an incomplete genome assembly and varying screening standards [31]. They discovered that TEA006173 plays a crucial role in flavonoid accumulation. Based on the aforementioned studies, it is speculated that the MATE gene family not only participates in the abiotic stress response, but also contributes to flavonoid transport and accumulation processes, thereby further elucidating the functional diversity of the MATE gene family.
In this study, certain advancements have been achieved in the whole-genome identification and expression analysis of the CsMATE gene family in the tea plant, but numerous issues require further exploration. Firstly, it is necessary to clarify the regulatory mechanism of CsMATE gene expressions in different tissues and development stages of the tea plant. Secondly, it is necessary to further explore the specific functions of CsMATE genes, especially the mechanism in plant stress resistance. Finally, through technological approaches such as gene editing, the expression levels of CsMATE genes can be modified to improve the stress tolerance of the tea plant.

5. Conclusions

In summary, 68 putative CsMATEs were identified from the tea plant genome. Subsequently, detailed descriptions of CsMATEs regarding fundamental characteristics, phylogenetic analysis, and expression profiles specific to different tissues and developmental stages were provided. Furthermore, we conducted an analysis on the expression patterns of CsMATE genes under various abiotic stress conditions and hormone treatments, leading us to identify several potential key genes involved in responses to different stress conditions. The results of this study lay an important theoretical basis for clarifying the biological functions of CsMATEs, especially in abiotic stress-related functions in the tea plant.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/agronomy14112718/s1, Figure S1: Amino acid sequence logos of conserved domains in CsMATEs. The bit score exhibits the information content for each position in the sequence; Table S1: Manual filtering of 98 putative CsMATE proteins in tea plant; Table S2: Details of the 68 CsMATE genes in tea plant; Table S3: Duplication event of the 68 CsMATEs; Table S4: Cis-acting regulatory elements identified in the promoter regions of CsMATE genes; Table S5: The RNA-seq data (FPKM) of CsMATEs in different tissues and developmental stages; Table S6: The RNA-seq data (FPKM) of CsMATEs in different abiotic and hormone treatments.

Author Contributions

Conceptualization, T.X. (Tao Xia) and H.R.; methodology, T.X. (Tao Xie), Y.Q., Y.J. and H.R.; software, T.X. (Tao Xie) and Y.Q.; validation, M.L., D.W., and X.Y.; formal analysis, T.X. (Tao Xie) and H.R.; investigation, M.L.; resources, Y.J.; data curation, T.X. (Tao Xie) and Y.Q.; writing—original draft preparation, T.X. (Tao Xie) and Y.Q.; writing—review and editing, T.X. (Tao Xia) and H.R.; visualization, Y.Q.; project administration, H.R.; funding acquisition, T.X. (Tao Xia), Y.Q., H.R., T.X. (Tao Xie), Y.J., and M.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Provincial Natural Science Foundation of Anhui (grant No. 1908085MC100), the Open Fund of State Key Laboratory of Tea Plant Biology and Utilization (grant No. SKLTOF20220107), the Doctoral (Post) Research Initiation Fund Project of Suzhou University (grant Nos. 2021BSK022, 2021BSK048, 2022BSK036, 2023BSK019), the National Natural Science Foundation of China (grant No. U21A20232), the Key Scientific Research Project of Suzhou University (grant No. 2024yzd02), the Anhui Province Higher Education Science Research Project (grant No. 2024AH051823), the Suzhou Science and Technology Plan Project (grant No. SZKJXM202208), and the Anhui Provincial Key Laboratory Open Fund Funded Project (grant No. FECPP202201).

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Phylogenetic relationships of MATE proteins of Arabidopsis and the tea plant. Blue dots represent MATE proteins from the tea plant and red dots represent MATE proteins from Arabidopsis. Branch colors represent different classes. The numbers assigned to branches indicate the reliability.
Figure 1. Phylogenetic relationships of MATE proteins of Arabidopsis and the tea plant. Blue dots represent MATE proteins from the tea plant and red dots represent MATE proteins from Arabidopsis. Branch colors represent different classes. The numbers assigned to branches indicate the reliability.
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Figure 2. Intron–exon and motif composition of CsMATEs. (A) Phylogenetic tree of CsMATEs. (B) 10 conserved motifs in CsMATE proteins. (C) Intron–exon composition of CsMATEs.
Figure 2. Intron–exon and motif composition of CsMATEs. (A) Phylogenetic tree of CsMATEs. (B) 10 conserved motifs in CsMATE proteins. (C) Intron–exon composition of CsMATEs.
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Figure 3. The distribution of CsMATEs on tea plant chromosomes. Font colors represent different classes. MB, megabase.
Figure 3. The distribution of CsMATEs on tea plant chromosomes. Font colors represent different classes. MB, megabase.
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Figure 4. Synteny of CsMATEs in C. sinensis. Grey and red lines represent synteny blocks and CsMATE gene pairs, respectively.
Figure 4. Synteny of CsMATEs in C. sinensis. Grey and red lines represent synteny blocks and CsMATE gene pairs, respectively.
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Figure 5. The collinearity of MATE genes in C. sinensis and three other species. (A) C. sinensis and A. thaliana; (B) C. sinensis and C. canephora; (C) C. sinensis and A. chinensis. Grey lines represent collinear blocks among C. sinensis, A. thaliana, C. canephora, and A. chinensis; red lines represent the syntenic MATE gene pairs.
Figure 5. The collinearity of MATE genes in C. sinensis and three other species. (A) C. sinensis and A. thaliana; (B) C. sinensis and C. canephora; (C) C. sinensis and A. chinensis. Grey lines represent collinear blocks among C. sinensis, A. thaliana, C. canephora, and A. chinensis; red lines represent the syntenic MATE gene pairs.
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Figure 6. Cis-acting elements in CsMATE promoters.
Figure 6. Cis-acting elements in CsMATE promoters.
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Figure 7. Spatiotemporal expression pattern of CsMATE genes. The heatmap of CsMATEs expression with log2 (FPKM + 1).
Figure 7. Spatiotemporal expression pattern of CsMATE genes. The heatmap of CsMATEs expression with log2 (FPKM + 1).
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Figure 8. Expression analysis of CsMATE genes under diverse abiotic stress and hormone treatment (A–D).
Figure 8. Expression analysis of CsMATE genes under diverse abiotic stress and hormone treatment (A–D).
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Xie, T.; Qian, Y.; Wang, D.; Yan, X.; Jiang, Y.; Li, M.; Rong, H.; Xia, T. Genome-Wide Analysis of the Multidrug and Toxic Compound Extrusion Gene Family in the Tea Plant. Agronomy 2024, 14, 2718. https://doi.org/10.3390/agronomy14112718

AMA Style

Xie T, Qian Y, Wang D, Yan X, Jiang Y, Li M, Rong H, Xia T. Genome-Wide Analysis of the Multidrug and Toxic Compound Extrusion Gene Family in the Tea Plant. Agronomy. 2024; 14(11):2718. https://doi.org/10.3390/agronomy14112718

Chicago/Turabian Style

Xie, Tao, Yumei Qian, Deyan Wang, Xiadong Yan, Ying Jiang, Min Li, Hao Rong, and Tao Xia. 2024. "Genome-Wide Analysis of the Multidrug and Toxic Compound Extrusion Gene Family in the Tea Plant" Agronomy 14, no. 11: 2718. https://doi.org/10.3390/agronomy14112718

APA Style

Xie, T., Qian, Y., Wang, D., Yan, X., Jiang, Y., Li, M., Rong, H., & Xia, T. (2024). Genome-Wide Analysis of the Multidrug and Toxic Compound Extrusion Gene Family in the Tea Plant. Agronomy, 14(11), 2718. https://doi.org/10.3390/agronomy14112718

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