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. 2024 Nov 12;25:1074. doi: 10.1186/s12864-024-10998-5

Transcriptome and genome-wide analysis of the mango glycosyltransferase family involved in mangiferin biosynthesis

Yibo Bai 1,2,#, Xinran Huang 2,3,#, Rundong Yao 2,3, Muhammad Mubashar Zafar 2,✉, Waqas Shafqat Chattha 4, Fei Qiao 1,2,5,✉, Hanqing Cong 1,2,✉
PMCID: PMC11555977  PMID: 39533198

Abstract

Mangiferin, a C-glucosyl xanthone, is a biologically active glycoside naturally synthesized in mango. Glycosyltransferase can catalyze the biosynthesis of mangiferin. In this study, we identified 221 members of the UGT glycosyltransferase family in mango. The 221 MiUGT genes were grouped into 13 subfamilies through phylogenetic tree analysis with Arabidopsis, Chinese bayberry, and mango. All UGT family members in mango were unevenly distributed on 17 chromosomes and found that tandem duplication dominated the expansion of UGT family members in mango. Purification selection primarily influenced the evolution of the mango UGT family members. In addition, cis-element analysis of the mango UGT gene family revealed the presence of MYB binding sites, which are involved in flavonoid biosynthesis; which further supports the role of UGT family members in the synthesis of flavonoids. To verify these results, we analyzed the expression of UGT family members in mango leaves, stems, and different developmental stages of fruit peel. The RNA-seq and qRT-PCR results showed significant differences in the expression patterns of MiUGT genes in various tissues and developmental stages of mango. We identified MiUGT gene-specific expression at different stages of fruit development. These results lay a theoretical foundation for research on the relationship between members of the mango UGT family and the synthesis of flavonoids, mangiferin.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12864-024-10998-5.

Keywords: Flavonoids, Gene-specific expression, MiUGT, Tissues

Introduction

Flavonoids are a diverse class of secondary metabolites that play multiple functions in plants [1–3]. Currently, there are over 6000 flavonoids have been identified based on their different structures and functions [3–5]. Flavonoids in plants mainly exist in the form of glycosides and aglycones, with glycosides being the predominant form [6]. Mangiferin, a natural antioxidant C-glucoside flavonoid, was originally isolated from mango [7]. Mangiferin has various pharmacological properties, including antioxidant, anti-inflammatory, anti-diabetic, and antibacterial [8–10]. However, its practical use is limited due to low solubility in water, low efficacy, and low bioavailability [11]. Glycosylation of mangiferin through biotransformation can enhance its bioavailability [12]. As a crucial step in the biosynthesis of natural compounds, glycosylation is recognized as a key biological transformation process that regulates the levels, activities, and positions of cellular metabolites and is involved in the degradation of most biomass [13, 14].

The process of glycosylation is catalyzed by glycosyltransferases [15]. UDP-glycosyltransferases (UGTs) are a specific type of glycosyltransferase involved in the biosynthesis of various glycosides [16]. In Arabidopsis, 117 UGT genes have been identified, with five AtUGT genes confirmed to be involved in the synthesis of plant flavonoids [17]. In Panax ginseng, 253 UGT genes have been identified, highlighting the crucial role UGTs play in the biosynthesis of ginsenosides [18, 19]. The quantitative trait locus GSA1 in rice regulates metabolic flux from lignin biosynthesis to flavonoid glycoside accumulation by encoding UDP glucosyltransferase [20]. UDP-glycosyltransferase can improve mangiferin's water solubility and antioxidant properties by catalyzing the transfer of sugar moieties from donors to receptors [21]. As a member of UDP glycyltransfer, the MiCGT genes have been proven to participate in the biosynthesis of mangiferin by producing C-xyloside through UDP xylose [22].

UDP glycyltransfer was widely distributed in natural organisms, including animals, plants, yeast, and bacteria. Therefore, to distinguish UGT genes in different organisms, the UGT naming committee assigned 200 UGT subfamilies to different biological categories. Among them, UGT 71–100 belongs to the UGT subfamily of plants [23]. As a superfamily of enzymes that catalyze glucosylation, the structural characteristics of UGT family members are typical UDPGT domains, which contain binding sites for UDP glycosyl donors [24]. Glycosyltransferases are responsible for transferring the glycosyl portion from activated donor molecules to receptor molecules such as sugars, nucleic acids, and proteins, thereby forming various glycoside compounds [25].

The mango (Mangifera indica L.) is an evergreen large tree plant in the family Rhus, genus mangifera. Due to its rich taste and potential as a traditional Chinese medicine, it has high economic cultivation value [26]. Mangiferin, a bioactive compound that is commonly found in mango leaves, stems, and rind, is renowned for its extensive pharmacological properties, which include antioxidant, anti-inflammatory, antidiabetic, and anticancer effects [27]. The health benefits of mango leaves, which are high in mangiferin, have been traditionally employed to manage diabetes and reduce inflammation, as evidenced by scientific studies [28]. Even though the stems contain reduced concentrations, they still possess valuable antioxidant and antimicrobial properties [29]. Another substantial source of mangiferin is the mango peel, which is frequently discarded. It is used in the production of dietary supplements, cosmetic products, and food preservation due to its antioxidant and antimicrobial properties [27]. With the development of science and technology, the genome of mango has been deciphered, laying the foundation for studying the biological functions of mango genes at the molecular level [30]. In previous reports, it has been demonstrated that mangiferin can be biosynthetically synthesized in mango by glycosyltransferases [22]. However, a comprehensive genome-wide analysis of the glycosyltransferase family members and their roles in mangiferin synthesis has not been conducted. Therefore, this study aims to identify the members of the glycosyltransferase family in mango, along with their evolutionary relationships and expression patterns. This will provide a theoretical foundation for further analysis of their roles in mangiferin biosynthesis.

Materials and methods

Genome-wide identification of the UGT gene family in three plant species

The protein sequences of UGT gene family members in Arabidopsis were identified from the TAIR website (https://www.arabidopsis.org), and the protein sequences of UGT gene family members in Chinese bayberry were downloaded from previous studies [31]. The whole genome sequence of mango was downloaded from the NCBI (https://www.ncbi.nlm.nih.gov) [30]. UDP-glucoronosyl and UDP-glucosyl transferase domain (PF00201) and Myb-like DNA-binding domain (PF00249) retrieve hidden Markov Model (HMM) profiles were downloaded from the Pfam website (http://pfam.xfam.org), HMMER3.0 was used for identifying members of the UGT gene family in mango. Using Pfam and SMART (http://smart.embl.de) for UGT gene validation to ensure the presence of the UDPGT domain [32].

The protein sequence of UGT gene family members of Arabidopsis, Chinese bayberry, and mango were aligned using the AGLIN function in MEGA11, the UGT phylogenetic tree was constructed by IQ-tree using the neighbor-joining (NJ) method with default parameters, and bootstrap values from 1000 replicates [33].

Physicochemical characterization of UGT family protein sequences

The isoelectric point, molecular weight, and GRAVY information of the UGT genes in mango were predicted using the ExPASY website (https://www.expasy.org) [34]. Using WoLF PSORT (https://wolfpsort.hgc.jp) website for subcellular localization prediction of UGT gene in mango [35].

Gene structure and conserved motif analysis of the UGT genes

GSDS2.0 was used for MiUGT gene structure analysis (https://gsds.gao-lab.org) [36], and the MEME website for conserved motif analysis of the MiUGT genes with default parameters (https://meme-suite.org/meme/) [37].

Chromosomal locations and Ka/Ks range of MiUGT genes

Visualize the distribution of UGT genes on chromosomes in mango by Mapchart software [38]. The duplication events were calculated by the DupGen_finder tool (https://github.com/qiao-xin/DupGen_finder) [39]. Perform collinearity analysis of mango genome and Arabidopsis genome by MCScanX. The value of Ka, Ks, and Ka/Ks ratios were calculated using MEGA X [40].

Cis-elements analysis in MiUGT genes promoter region

The 2 kb promoter sequence of the MiUGT genes was extracted by Perl and predicted the cis-elements of MiUGT genes by the PlantCARE website (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) [41].

Sample collection and transcriptome sequencing

The plant of mango was planted in the dry and hot valley of the Youjiang River in Guangxi (Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences), select the leaves, stems, and fruits of “Hong xiangya” were about 15 days after flowering, and collect the fruit peel every week as experimental materials (Fig. S1). A total of 12 developmental stages of experimental materials were collected, with three biological replicates set for each stage. All collected samples were rapidly frozen in liquid nitrogen and stored in a -80 ℃ freezer for RNA extraction.

The RNA-prep Pure Plant Plus Kit (Polysaccharides & Polyphenolics rich) kit (Tiangen, China) was used to extract RNA from mango leaves, stems, and fruit peel. The purity and integrity of RNA were detected by spectrophotometer (NanoDrop, Thermo Scientific), agarose gel electrophoresis (1%), and Agilent 2100 bioanalyzer. At least 1 µg of RNA in each sample for transcriptome sequencing by the Illumina Novaseq 6000 platform. After quality control, clean reads were mapped onto the reference genome of Alphonso by HISAT2 (https://www.ncbi.nlm.nih.gov/sra), and gene expression levels were calculated by TPM (Transcripts Per Million) [42].

Co-expression network construction between MiUGT and MiMYB genes

The MiUGT genes with MYB binding site involvement in flavonoid biosynthetic gene regulation were screened by cis-elements analysis. The Pearson correlation coefficient between MiUGT and MiMYB genes was performed from transcriptome sequencing of samples from different tissue parts of mango by the ‘cor’ function in R. The gene pairs with correlation coefficients ≥|0.9| were considered highly correlated. The gene pairs with high correlation were visualized by Cytoscape software [43].

RNA isolation and qRT-PCR analyses

Reverse transcription of RNA from all samples into cDNA using the HiScript IV RT SuperMix for qPCR kit (Vazyme, Nanjing, China). The qRT-PCR assay was performed by ChamQ Universal SYBR qPCR Master Mix (Vazyme, Nanjing, China) on the QuantStudio 6 Flex real-time PCR system (ThermoFisher, MA, USA). All primers were listed in Table S5. The gene relative expression level was calculated using the 2−ΔΔCt method [44], with the MiTUBB gene as the reference gene in mango.

Results

Genome-wide identification and characterization of UGT genes in mango

221 UGT genes were identified in mango based on Pfam and HMMER searches. Physicochemical properties analysis showed that the range of theoretical relative molecular weight for MiUGT genes was 11.31 ~ 95.81 KDa, the range of isoelectric point was 4.67 ~ 8.94, and the range of the grand average of hydropathicity was -0.457 ~ 0.137. The prediction of subcellular localization showed that 115 MiUGT proteins were located in chloroplast, 55 MiUGT proteins were located in cytoplasm, 8 MiUGT proteins were located in endoplasmic reticulum, 10 MiUGT proteins were located in extracellular, 2 MiUGT proteins were located in mitochondrion, 20 MiUGT proteins were located in nuclear, 3 MiUGT proteins were located in peroxisomes, and 5 MiUGT proteins were located in vacuole (Table S1).

To investigate the phylogenetic relationship between UGT genes in mango and other plants. We selected the reported UGT gene family from Arabidopsis and Chinese bayberry, and the identified UGT genes in mango from this study to construct the phylogenetic tree. Based on the distance of genetic relationships, 221 UGT genes in mango were divided into 13 subfamilies, namely UGT71, UGT72, UGT91, UGT88, UGT74, UGT84, UGT80, UGT75, UGT89, UGT76, UGT85, UGT78, UGT73 (Fig. 1).

Fig. 1.

Fig. 1

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Phylogenetic tree of the UGT gene family in Arabidopsis, Chinese bayberry, and Mango. Different colored circles represent different species, and different colored lines represent different subfamilies

Gene structure and motifs analysis in the MiUGT gene family

To understand the structural diversity of UGT gene family members in mango, we analyzed the gene structures and conserved motifs of 221 MiUGT genes (Fig. 2). A total of 15 conserved motifs of the MiUGT genes, each gene contains motif 1 (UDPGT domain), and motif 15 (Glycogen Phosphorylase B) was only present in the UGT88 subfamily. In addition, the structure of the MiUGT genes was analyzed, 68 MiUGT genes (30.77%) have no introns, while 94 MiUGT genes (42.53%) contain 1–2 exons.

Fig. 2.

Fig. 2

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The motif and structural analysis of the UGT genes in mango

Genome distribution and the expansion of MiUGTs

As shown in Fig. 3, MiUGT genes were unevenly distributed on 20 chromosomes, with a higher number of 45 MiUGT genes on Chr 15. There were a small number of MiUGT genes on Chr 6, Chr 13, and Chr 17, which were one respectively. Gene duplication events play a crucial role in the evolution and expansion of gene families. The collinearity analysis showed that there are 43 UGT homologous gene pairs between Arabidopsis and mango (Fig. 4 and Table S4). In this study, we analyzed the duplication events of the MiUGT genes and found that only tandem duplication events occurred in the MiUGT gene family. This result indicated that tandem duplication was important in MiUGT gene expansion. To understand the evolution of UGT genes in mango, we calculated the Ka/Ks ratio of duplication events. The results showed that the ratio of Ka/Ks was mainly concentrated between 0–1, indicating that the MiUGT genes were mainly affected by purification selection during evolution (Fig. 5).

Fig. 3.

Fig. 3

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Chromosome distribution map of MiUGT gene family

Fig. 4.

Fig. 4

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Collinearity relationships of UGTs among A. thaliana and M. indica

Fig. 5.

Fig. 5

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The Ka/Ks ratio of duplication events in MiUGT genes

Analysis of cis-elements in the promoter regions of MiUGT genes

We selected the promoter region of the MiUGT genes (2000 bp upstream of the DNA sequence translation start site) for cis-element analysis. 1226 cis-acting elements have been identified and 14 cis-elements were found in the promoter region of the MiUGT genes. As expected, the ABRE motifs involved in abscisic acid response and the TGACG motifs involved in MeJA response were enriched in all MiUGT genes. The cis-element (MBSI) of the MYB binding site involved in flavonoid biosynthetic gene regulation, the cis-element (MBS) of the MYB binding site involved in drought-inducibility, and the cis-element (MRE) of the MYB binding site involved in light responsiveness were found in the MiUGT promoter region. This result suggested that the MYB genes may bind to the UGT genes and participate in the growth and development of mango (Fig. 6).

Fig. 6.

Fig. 6

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2000-bp promoter sequence analysis in members of the MiUGT gene family. Different colors represent different cis-elements

The interaction relationship between MiUGT genes and MiMYB genes

To identify the interaction between the MiUGT and MiMYB genes, we selected the MiMYB genes and MiUGT genes with MYB binding site involvement in flavonoid biosynthetic gene regulation in the promoter region for correlation analysis. We selected 20 MiUGT genes with MYB binding sites to calculate the Pearson correlation coefficient between candidate MiUGT genes and MiMYB by the expression level in different tissues of mango. Through screening, it was found that there was a high correlation (P ≥ 0.9) between 60 MiMYB genes and 13 MiUGT genes. There was a high negative correlation between the MiMYB genes (Mi08G0079000, Mi04G0090900, Mi03G0073600) and the MiUGT genes (Mi04G0197100, Mi15G0019600, Mi04G0197100). There was a high positive correlation between other gene pairs (Fig. 7).

Fig. 7.

Fig. 7

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Co-expression analysis of MiUGT genes with MiMYB genes. The black line represents a positive correlation between genes, while the red line represents a negative correlation between genes

Expression patterns and co-expression networks of MiUGT in different organs

To further determine the expression patterns of the MiUGT genes in different tissues of mango, we performed transcriptome sequencing on the stems, leaves, and fruit peels at different developmental stages of the fruit. The heatmap results have shown that there were similar expression patterns of MiUGT genes in stems and leaves, at least half of the MiUGT genes were highly expressed in leaves and stems (Fig. 8). There were significant differences in the expression of MiUGT genes in different stages of fruit peel development. 40 MiUGT genes were mainly expressed in the early stage of mango fruit development, while 50 MiUGT genes were highly expressed in the middle stage. Interestingly, 12 MiUGT genes were specifically highly expressed in the post-ripening stage of mango. These results indicated that the MiUGT genes played a key role in the mango's different tissues and developmental stages.

Fig. 8.

Fig. 8

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Heatmap of MiUGT genes expression in mango peel, stem, and leaf

QRT-PCR analysis of MiUGT genes under different organs in mango

To validate the expression of the MiUGT genes in various tissue parts of mango, we selected different subfamily genes for qRT-PCR validation. To verify the expression and potential function of the MiUGT genes in different tissues of mango, the MiUGT genes that can bind to the MiMYB genes were selected for qRT-PCR verification. The results showed that the genes Mi02G0155500, MiUn0001G0005900, and Mi14G0155300 were mainly highly expressed in leaves and stems, the gene of Mi15G0020000 was mainly highly expressed in stems, and the genes of Mi15G0112400 and Mi04G0197100 were mainly highly expressed in the peel at the early stage of fruit development. The genes of Mi02G142500, Mi15G0019600, Mi01G0200100, Mi02G0122200, Mi09G0013400, Mi01G0085700, and Mi05G0071100 were mainly highly expressed in the peel at the middle stage of fruit ripening (Fig. 9).

Fig. 9.

Fig. 9

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QRT-PCR analysis of the expression of MiUGT genes in stems, leaves, and fruit peels

Discussion

Mango leaves and bark contain various naturally bioactive glycosides [26]. Mangiferin is a glycoside flavonoid compound with medicinal activity, mainly enriched in mango leaves, stems, and peels, commonly used for the defense and treatment of human diseases [8, 45, 46]. Previous studies have shown that using enzymatic glycosylation of mangiferin to produce more soluble mangiferin can solve the problem of poor solubility and low bioavailability of mango [22]. UGT, as a UDP glycyltransferase, catalyzed the glycosylation of glycoside substances [47]. It has been reported in multiple species such as G. biloba [48], tobacco [49], Arabidopsis [50], rice [51], cabbage [52], and sweet orange [50]. In G. biloba, UGT716A1 has been identified as a multi-substrate UFGT with a broad in vitro flavonoid substrate spectrum [48]. In our study, we identified 221 UGT family members in mango and analyzed the physicochemical properties based on the gene structures. The relative molecular weight of the MiUGT protein ranges from 11.31 KDa (Mi09G0013700) to 95.81 KDa (Mi08G0030900), and the pI range of the MiUGT protein ranges from 4.67 (Mi02G015500) to 8.94 (Mi04G0074600). The majority of the MiUGT protein’s pI was less than 7. These results indicated that similar to most studies on dicotyledonous plants [53], the MiUGT gene family tends to favor acidic amino acids, and over time, the differentiation of MiUGT gene family members is inconsistent, leading to structural differences [54]. Subcellular localization prediction of 221 MiUGT genes revealed that half of the MiUGT genes were located on chloroplast. Previous studies have shown that light affects the transcription of chloroplast localization genes and regulates the related functions of photosynthesis [55]. These results indicated that the MiUGT genes play a crucial role in plant growth, development, and adaptation to environmental changes. Based on phylogenetic tree analysis of UGT genes in Arabidopsis, Chinese bayberry, and mango, 221 MiUGT genes were divided into 13 subfamilies. The genes in all 13 subfamilies have conserved UDP-glucosyl transferase domains. The conserved motifs among the same subfamily are relatively similar, for instance, motif 15 (Glycogen Phosphorylase B) mainly exists in the UGT88 subfamily. As a key enzyme in the first step of glycogen reaction, glycogen phosphatase can provide sufficient energy for the glycogen metabolism process [56], this may enable members of the MiUGT88 subfamily to play a unique role in plant development.

During the evolutionary process, plants undergo various gene duplication events, which result in the differentiation of different family members [57]. The chromosome mapping results showed that 221 members of the MiUGT gene family were unevenly distributed on 20 chromosomes of mango, with the most MiUGT genes distributed on Chr 15. Tandem duplication usually leads to the development of gene clusters [58]. We observed that the MiUGT genes only contain tandem duplication events, involving 72 pairs of genes distributed on 16 chromosomes, indicating that tandem duplication is the main cause of the expansion of the mango UGT gene family (Table S2). This result was similar to previous research, the BpUGT genes were involved in segment duplication and tandem duplication events in B. papyrifera. Tandem duplication has been proven to be the main driving force for the expansion of the BpUGT family [59]. The Ka/Ks ratio indicates the selection pressure during plant evolution [25]. The Ka/Ks > 1 of duplicated genes indicated the necessity of the UGT genes in E. pubescens survival. In this study, the Ka/Ks results indicated that the evolution of MiUGT genes is mainly influenced by purification selection.

The DNA sequence upstream of the gene coding region is the gene promoter, which contains multiple cis-acting elements [60]. We identified 10 types of homeostatic elements in the MiUGT genes. Interestingly, the presence of MBSI elements was found in 20 MiUGT genes. In previous studies, the MYB genes are involved in synthesizing flavonoids [61]. For example, in gerbera, overexpression of GhMYB1a can promote the accumulation of anthocyanins [62]. The FhMYB21L2 gene activates the FhFLS2 gene to promote the accumulation of flavonols in flowers in Freesia hybrida [63]. To further verify the relationship between MiUGT genes and MiMYB genes, we constructed a co-expression network of candidate MiUGT genes and MiMYB genes, with 74 positive and 3 negative correlations. The transcription factors of MYB have been reported to regulate the biosynthesis and accumulation of anthocyanins in chrysanthemum [64] and celery [65]. Combined with previous research results, MiMYB genes may be involved in the synthesis of flavonoids in mango by regulating MiUGT genes.

The UGT genes have been proven to be involved in plant growth, development, and stress resistance [21]. We performed transcriptome sequencing on the stems, leaves, and peel of mango at different stages of development to elucidate the expression of the MiUGT genes in different tissues and developmental stages. In this study, the MiUGT genes were highly expressed specifically in stems, leaves, and fruit peels at different developmental stages, indicating its involvement in the growth and development of mangoes. In addition, we conducted qRT-PCR analysis on MiUGT genes that may be regulated by MiMYB genes. We found that the MiUGT genes that can bind to MiMYB genes are highly expressed in leaves, stems, and various epidermal development stages. This result indicated that different MiMYB-MiUGT pathways were involved in the biosynthesis of mangiferin in other tissues.

Conclusions

Mangiferin has many pharmacological properties such as anti-inflammatory, antipyretic and analgesic, and antibacterial. In actual production, due to the poor solubility of mangiferin, the low bioavailability limits the clinical application of mangiferin. Therefore, the identification of mangiferin biosynthesis and glycosylation genes is beneficial to improve the utilization of mangiferin. In this study, mango was used as the experimental material to identify the UGT gene family and evolution process of mangiferin synthesis, and the MiUGT genes that interact with the MiMYB genes were excavated by cis-element analysis. Combined with transcriptome and qRT-PCR, the expression of candidate the MiUGT genes in different tissues and peels of mango at different developmental stages of fruit was revealed. It laid a solid theoretical foundation for further revealing the biosynthetic pathway of mangiferin.

Supplementary Information

Supplementary Material 1. (5.1MB, pdf)
Supplementary Material 2. (28.4KB, xlsx)

Acknowledgements

Not applicable.

Authors’ contributions

FQ, HC, and YB designed the experiments. YB and XH performed the experiments. YB, XH, RY and MMZ analyzed the data. YB and WSC wrote the paper. All authors read and approved the final manuscript.

Funding

The research was supported by the Major Science and Technology plan of Hainan Province (ZDKJ2021012), the Hainan Provincial Natural Science Foundation of China (322MS133), the Open Project of Guangxi Key Laboratory of Biology for Mango (GKLBM02205), and Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No.1630032024023).

Data availability

The RNA-seq data were deposited to the Sequence Read Archive (SRA) at NCBI under the accession number PRJNA1120973 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1120973).

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Yibo Bai and Xinran Huang contributed equally to this work.

Contributor Information

Muhammad Mubashar Zafar, Email: m.mubasharzafar@gmail.com.

Fei Qiao, Email: fei.qiao@catas.cn.

Hanqing Cong, Email: hanqing.cong@catas.cn.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Material 1. (5.1MB, pdf)
Supplementary Material 2. (28.4KB, xlsx)

Data Availability Statement

The RNA-seq data were deposited to the Sequence Read Archive (SRA) at NCBI under the accession number PRJNA1120973 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1120973).

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