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Article

Transcriptome Wide Identification and Expression Analysis Revealed BhTALE Gene Family Regulates Wax Gourd (Benincasa hispida) Response to Low Calcium and Magnesium Stress

by
Shahid Hussain
,
Jingjing Chang
,
Jing Li
,
Xiao Chen
,
Dasen Xie
and
Baige Zhang
*
Key Laboratory for New Technology Research of Vegetable, Vegetable Research Institute, Guangdong Academy of Agricultural Science, Guangzhou 510640, China
*
Author to whom correspondence should be addressed.
Horticulturae 2024, 10(10), 1083; https://doi.org/10.3390/horticulturae10101083
Submission received: 20 August 2024 / Revised: 3 October 2024 / Accepted: 7 October 2024 / Published: 9 October 2024
(This article belongs to the Section Genetics, Genomics, Breeding, and Biotechnology (G2B2))
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Abstract

:
The three-amino-loop-extension (TALE) family involves key transcription factors vital for maintaining different aspects of growth including leaf, flower, and fruit development and responses to stressful stimulus. Thus far, a deep understanding of the TALE gene family in wax gourd subjected to low calcium and magnesium stress has been missing. Here, we isolated 24 BhTALE genes from a wax gourd genome database. Comprehensive bioinformatic analysis, including evolutionary tree, gene structures, conserved motifs, and chemical properties, provide structural and functional insights into the BhTALE gene family. Gene ontology (GO) analysis of TALE genes unveils their involvement in growth and stress responses. Promoter analysis indicates that hormones and stresses can influence the expression of BhTALE genes. Tissue-specific expression under low calcium and magnesium stress showed that BhTALE genes were more active in the leaves and roots. Notably, BhTALE7, BhTALE10, and BhTALE14 were expressed differentially in leaves under low calcium and magnesium applications. Similarly, the induced expression pattern of BhTALE4 was recorded in the roots under low calcium and magnesium applications. Our findings underscore the pivotal role of the BhTALE gene family in dealing with low calcium and magnesium stress in the wax gourd.

1. Introduction

The three-amino-loop-extension (TALE) family is found in various living organisms, including plants [1]. These myriad molecules are key regulators of delicate plant processes and pivotal to maintaining normal growth activities [2,3,4]. The TALE family involves a highly conserved sequence that was subsequently dubbed the “homeobox” because it contained altered genes that produced homologous phenotypes [5]. Knotted-like homeodomain (KNOX) and BEL1-like homeodomain (BLH/BELL) proteins are found in the TALE family gene and act as structurally and functionally similar heterodimers. The TALE family gene encodes the 63 amino acid residues of the atypical homeobox domain. The family is known as the homeobox protein superfamily because a three-amino-acid extension in the loop joins its homeodomain’s first and second helices [6,7]. The BELL and KNOX subfamilies comprise the Arabidopsis thaliana TALE transcription factors [6]. Certain relationships between these two subfamilies can control downstream genes to accomplish various biological goals. In plants, the KNOX subfamily is extensively widespread [8], comprising KNOX1, KNOX2, ELK, and Homeobox KN as its four domains [9].
The maize Knotted-1 (Kn1) gene was the first homeobox gene found in plants [10]. In Arabidopsis, a recessive mutation of the SHOOTMERISTEMLESS (STM) gene inhibited the development or upkeep of the stem apical meristem (SAM) [7]. The production of secondary cell walls involves KNAT7 [11]. GhKNL1 belongs to the TALE family, which controls the process of cotton fiber production [12]. The TALE family’s KNOX class I family genes in Arabidopsis (STM, KNAT2, BREVIPEDICELLUS (BP)/KNAT1, and KNAT6) may control xylem differentiation, floral fate, and hormonal balance [12]. Angiosperm roots’ stems, leaves, and flowers all express class II KNOX genes. The primary function of this gene group is to control how different plant organs differentiate [7,12]. Additionally, KNOX proteins play a role in controlling the anabolic metabolism of a variety of chemicals, such as lignin, cytokinin (CK), and gibberellic acid (GA) [13]. There are four domains in the BELL subfamily: SKY, BEL, Homeobox KN, and VSLTLGL (ZIBEL) [12,14]. Members of the BELL family also play important regulatory roles in flower development and transformation. Flowering is delayed when the BLH6 gene is overexpressed, whereas it happens faster when the BLH3 gene is overexpressed [15]. To create KNOX-BELL heterodimer heteromers, which can bind to particular target sequences, different KNOX and BELL combine selectively. Different combinations of two subfamilies can regulate different downstream genes in plants to fulfill their roles [16]. In the GA biochemical pathway, the dimer of BELL and KNOX StBEL5/POTH1 suppressed the production of the crucial enzyme ga20ox1 [7]. STM, a member of the KNOX family, and ATH1, PENNYWISE (PNY), a member of the BELL family, performed comparable tasks and controlled the meristem development of plants [11]. ABA-responsive gene expression is regulated by BLH1 and KNAT3 protein heterodimers in Arabidopsis, which also impact seed germination and growth [17]. KNAT1 controls the growth of pistil marginal tissue via interacting with RPL, FUL, and AP [12]. Despite their significant involvement in stress biology and plant development, a thorough investigation of the TALE gene family in wax gourd is elusive and needs attention.
The Cucurbitaceae family has many species with distinct health benefits [18,19,20,21]. Wax gourd Benincasa hispida (Thumb.) Cogn. belongs to Cucurbitaceae, also known as winter squash. Like other plants, wax gourd’s growth and development largely depends on nutrient balance. Improper nutrient availability can penalize the growth attributes of wax gourd and ultimately affect yield [22]. In wax gourd, a substantial reduction in fruit fresh yield was caused by low magnesium availability, which was directly linked to increased starch and sucrose accumulation in source leaves and decreased sucrose content in phloem exudate [22]. Physiological and biochemical investigation showed that blackheart disorder’s severity was linked to a decrease in the levels of total calcium (Ca) and calcium–pectinate [23]. In hindsight, nutrient deficiency causes an array of disorder in wax gourd plants. Nutrient deficiency affects growth by regulating various transcription factors (TFs). The identification of transcription factors governing wax gourd’s response to nutritional disorders necessitates attention. Here, we focused on the response of BhTALE genes to low magnesium and low Ca stress in the root and leaf of wax gourd.
In this work, we have conducted a detailed analysis of TALE transcription factors using numerous bioinformatic tools. An in silico study of the BhTALE genes family was performed from data retrieved on the wax gourd genome. Expression analysis of BhTALE genes was performed using Ca and Mg applications. Our study provides new insights into the role of BhTALE genes in regulating wax gourd response to low Ca and Mg.

2. Material and Methods

2.1. Identification of TALE Genes in Wax Gourd

All the sequence data were obtained from the Wax Gourd Genome Database (http://cucurbitgenomics.org/organism/22) (3 March 2024) [24]. The Arabidopsis Information Resource (TAIR; https://www.arabidopsis.org/index.jsp, 3 March 2024) database was used to retrieve Arabidopsis TALE sequences. A two-step BLAST technique was used to find the TALE genes in wax gourd. Initially, TBtools (e-value, 1 × 10−5) were utilized to seek potential wax gourd TALE genes using Arabidopsis TALEs [25]. The National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov/, 3 March 2024) BLASTP (e-value, 1 × 10−5) was then used to identify every potential wax gourd TALE further. SMART was utilized to confirm the candidate proteins (http://smart.embl.de/, 3 March 2024) [26] along with Pfam mega databases (http://pfam.xfam.org/, 3 March 2024) [26].

2.2. Phylogenetic Tree, Conserved Motifs, Gene Structure, and Cis-Acting Elements Analysis

TALE protein sequences of 24 BhTALE (Benincasa hispida cv. B227), 19 CmTALE (Cucumis melo), 23 SlTALE (Solanum lycopersicum), and 19 AtTALE (Arabidopsis thaliana) were used for phylogenetic analysis [27]. Using MEGAX software v.10.1.8 (https://www.megasoftware.net/, 3 March 2024), the neighbor-joining (NJ) method was used to create the phylogenetic tree, and 1000 iterations of the bootstrap test were performed [28]. The results were formatted for display using Evolview V3 (https://www.evolgenius.info//evolview/#login, 3 March 2024) [29]. TBtools was used to determine the gene structure of the wax gourd BhTALE genes. To anticipate conserved motifs of the BhTALE, the online Multiple Expectation Maximization for Motif Elicitation (MEME) algorithm version 5.0.5 (http://meme-suite.org/tools/meme, 3 March 2024) was utilized. Furthermore, using the Gene Structure Display Server (GSDS) (http://gsds.cbi.pku.edu.cn, 3 March 2024), the gene sequences were compared with the predicted coding sequences to conduct the gene structure analysis, which included exon and intron [30]. Lastly, PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, 3 March 2024) was utilized to examine the cis-acting elements in 2000 bp sequences upstream of each BhTALE gene’s start codon ATG [31].

2.3. Chromosomal Localization and Protein Interaction

The physical information of BhTALE genes on the chromosomes was obtained using TBtools 1.121. The online server string (https://string-db.org) (accessed on 15 July 2023) was used to identify the interactive proteins with BhTALE proteins.

2.4. Plant Material and Nutrient Treatments

Wax gourd “Teizhu 2” variety seeds were used as research material. Wax gourd seeds were soaked in 5% NaOCl for 15 min. The soaked seeds were washed multiple times with distilled water, and then the seeds were immersed in water for three days for germination. The germinated seeds of the two-leaf stage were cultivated in Hoagland solution under controlled environmental circumstances in a lab growth chamber at the Guangdong Academy of Agricultural Science. The plants were treated with low calcium and magnesium concentrations of 0.4 mml and 0.2 mml, respectively, one week after the transfer. The low Ca concentration was based on unpublished research, whereas the low Mg concentration was derived from previous work. Throughout the experiment, the growth chamber was maintained at a 12 h light/dark photoperiod (26 ± 2 °C during the day and 18 °C at night), with a relative humidity of 70–85%. Three replicates were sampled from each treatment. Leaves from three different plants were sampled, and immediately placed in liquid nitrogen, and then kept at −80 °C for relative gene expression analysis.

2.5. Quantitative RT-PCR (qRT-PCR)

The plant total RNA purification kit (Tiangen, Beijing, China) was used according to the manufacturer’s procedure to isolate the total RNA. Total RNA (1 μg) was used for first-strand cDNA synthesis using a cDNA Kit (CWBIO, Beijing, China). The products were diluted with RNase-free water and used for the template. SYBR® Premix Ex TaqTM II (TaKaRa, Dalian China) was used in conjunction with a CFX96 Real-Time PCR Detection System (Bio-Rad, Hercules, CA, USA) to assess the expression levels of the genes. The relative expression of genes was determined using the 2−ΔΔCT method [32]. Table S1 contains a list of the primers used in the qRT-PCR test. The mRNA abundance of each sample was normalized using the internal reference gene, Actin, and three biologically separate replicates were employed for each treatment, adhering to the same protocol as our earlier investigations [33].

2.6. Statistical Analysis

The statistical software package SPSS (version 25.0, SPSS Inc., Chicago, IL, USA) was used to conduct statistical analysis (ANOVA) and determine statistical significance (p 0.05). The data were assessed and presented for all measured parameters as means with standard deviation (SD) from three biologically independent replicates. GraphPad Prism (version 7.0) (GraphPad Software, Inc., LA Jolla, CA, USA) was utilized for the graphical representation, in keeping with the procedures that were established for an earlier examination by Sharif et al. [34].

3. Results

3.1. Identification of TALE Genes in Wax Gourd Genome

We employed the BLASTP tool to extract the TALE proteins from the wax gourd genome database. The isolated proteins were subsequently examined for the Homeo-box_KNOX (HB_KN) domain. Proteins devoid of the HB_KN domain were eliminated, resulting in 24 remaining BhTALE members. Subcellular investigation revealed that all BhTALE proteins are localized in the nucleus (Table 1).

3.2. Evolutionary Analysis of BhTALE Genes

Phylogenetic analysis is generally performed to understand the evolution of a particular gene or gene family. A phylogenetic study was performed to investigate the evolutionary traits of BhTALE genes in relation to other species, including Arabidopsis, Cucumis melo, Citrullus lanatus, and Solanum lycopersicum. The highest proportion of TALE genes was ascribed to KNOX-1, followed by KNOX-II (Figure 1). The BELL group comprises five further subfamilies, designated BELL-I through BELL-V. The BELL-I and BELL-V possess the greatest quantity of TALE genes, whereas the BELL-II, BELL-III, and BELL-IV display a moderate number of TALE genes.

3.3. Chromosomal Localization of BhTALE Genes

Chromosomal localization was conducted to elucidate the physical positioning of BhTALE genes. The genome of the wax gourd has 12 chromosomes, with the BhTALE gene spread randomly across them (Figure 2). Chromosome seven contains the highest number of genes, totaling six, followed by chromosomes four, five, and six, each with three genes. Chromosomes 1, 3, and 7 each contained only 2 BhTALE genes.

3.4. Gene Structure and Motif Analysis

Analyzing gene structure is essential for comprehending the evolutionary composition of a certain gene or gene family. The genomic and CDS sequences delineated the structure of the BhTALE gene. The exons (CDS) and introns were randomly dispersed, as revealed by structural analysis (Figure 3). Most BhTALE genes contain 4 to 5 exons in their structure. Conversely, 2–3 introns were observed in the majority of the BhTALE genes.
The MEME web service identified four motifs in the protein sequence of BhTALE (Figure 3). The highly conserved motif 1 (Homeobox) was identified in all BhTALEs. Conversely, motif 2 (POX) was absent in numerous instances. Motif 3 (KNOX II) was documented in significant quantities, but motif 4 (KNOX I) was lacking in several BhTALEs.

3.5. Gene Ontology Analysis of BhTALE Genes

The gene ontology (GO) analysis included three categories: biological functions (BFs), molecular functions (MFs), and cellular components (CCs). The BFs indicated that BhTALE genes play a role in flowering, hormone regulation, organ development, and stress response (Figure 4). The BhTALE genes demonstrated DNA binding capability as indicated by their molecular function. CCs indicated that all BhTALE genes are located in the nucleus.

3.6. Promoter Analysis of BhTALE Genes

The 1.5 kb promoter region upstream of BhTALE genes was obtained from the wax gourd genome database, and the anticipated cis elements were identified using the PlantCARE database. The projected cis-acting elements were categorized into three separate groups: hormone, stress, and growth. The hormonal components include cis elements for almost all major hormones, such as GA, SA, ABA, MeJA, auxin, and ERE (ethylene-responsive elements). The BhTALE genes may respond to many environmental stressors—for instance, situations such as anoxia, low temperature, thirst, and hypoxia. The drought-responsive element MBS is located in the upstream region of the BhTALE gene (Figure 5). The BhTALE genes modulate essential growth processes, including the cell cycle, metabolic activity, blooming, circadian rhythm, and leaf development.

3.7. Interactive Protein Analysis

The STRING online database facilitates interactive protein analysis, serving as a crucial instrument for finding functional partners. In this study, we selected two BhTALE proteins (BhTALE15 and BhTALE17) as references to identify their functional predictions (Figure 6). For BhTALE, an array of key proteins was found in interactions. The majority of the interacting proteins belong to the ovate transcription factor family.

3.8. Expression of BhTALE Genes in Response to Low Calcium and Magnesium

Transcriptomic analysis was performed of wax gourd roots subjected to low calcium stress. We analyzed the expression of BhTALE genes from the transcriptomic data to understand their role in regulating wax gourd responses to low calcium stress. The data revealed that only BhTALE21 showed induced expression 1 and 5 d after treatment with low calcium stress. Apart from that, BhTALE2, BhTALE16, and BhTALE18 were sharply induced in CK-5d (control treatment for 5 days) but not in other samples (Figure 7). The majority of BhTALE genes displayed reduced expression in all the samples (control and low calcium).
To further understand the role of BhTALE genes in response to calcium and magnesium, we performed qRT-PCR analysis. The expression analysis of eight BhTALE genes was performed in roots and shoots exposed to calcium and magnesium (Figure 8). Varied expression patterns were observed amongst the BhTALE genes. For instance, the BhTALE1 induced sharply in response to low Ca-leaf (low calcium treatment to leaf) and Ca-root (calcium treatment to roots). Similarly, BhTALE3 and BhTALE18 also increased significantly in low Ca-leaf (8 and 40 folds, respectively) compared to others. BhTALE10 and BhTALE14 showed a high expression trend under low Ca-leaf and Mg-leaf only. BhTALE22 was triggered in response to Ca-root but had moderate expression under all other treatments.

3.9. Expression Analysis under Low Mg Stress

Mg is a subtle element for plant growth and development. We determined the expression of BhTALE genes under low Mg stress. For instance, the expression of BhTALE1 was sharply induced under low Mg compared to CK (Figure 9). Similarly, the expression of BhTALE3 increased in response to low Mg and reached a maximum of 2.2 folds. The BhTALE4 and BhTALE10 genes displayed reduced expression patterns under low Mg stress. The expression of BhTALE7, 14, and 18 was also triggered by low Mg compared to that of CK. BhTALE22 showed no significant difference in CK and low Mg.

4. Discussion

4.1. Ca and Mg Nutrients

Magnesium, despite being found in plant tissues in very low amounts, is an essential macronutrient. It performs numerous crucial functions in plant physiology, growth, development, production, and ability to withstand adverse conditions [35]. For instance, its many functions in photosynthesis can be greatly influenced by its presence, which directly affects plant productivity [36]. In addition, Mg2+ is essential for preserving the structural integrity of cell membranes and halting the breakdown of lipid bilayers in a variety of environmental settings [37]. The development of pollen is negatively impacted by an inadequate supply of Mg2+, which in turn reduces the overall fertility of the plant [38]. As a result, there is poor fruit set, which lowers the quantity of fruits produced and so directly impacts agricultural productivity [22]. Ca is a crucial mineral component that has a significant impact on fruit quality. Its formation of insoluble Ca-pectate with soluble pectin is one of its vital roles in maintaining the integrity of fruit cells and intercellular cohesiveness [39]. Thus, insufficient calcium content may cause membrane deterioration and/or cell wall disintegration. The disruption of the cell membrane leads to the oxidation of phenolic compounds, which is catalyzed by peroxidase (POD) and polyphenol oxidase (PPO), resulting in the occurrence of browning [40]. Protein kinases activate when sensors detect high calcium levels. Activated kinases control several genes that result in stress tolerance phenotypes [41]. Mg2+ and Ca tango is crucial for nutritional homeostasis that further fine-tunes plant growth [42]. An array of transcriptional activities could be initiated following Mg and Ca crosstalk during various developmental stages of a plant. Multiple families of ion channels and transporters have been discovered that play a role in the transportation of Ca and Mg2+ across the plasma membrane and intracellular membranes [43]. The role of the BhTALE gene family in regulating the response of wax gourd to low Ca and Mg2+ remains obscure. Here, we systemically characterized the BhTALE genes from wax gourd genome database and performed expression analysis under low and Ca and Mg2+ stress.

4.2. TALE Genes Are Widely Distributed across the Genome

The TALE gene family is extensively distributed in eukaryotes and controls growth and development. Previous research on plants concentrated on several species’ entire homeobox gene sets [44]. This work examined 21 BhTALE gene family members from the wax gourd genome database [45]. As anticipated, they were all randomly distributed over seven chromosomes and found in the nucleus (Table 1) (Figure 2).
We built an unrooted phylogenetic tree based on the amino acid sequences of the 21 genes to investigate the evolutionary relationships and classification of the proteins they express. Unlike earlier research, we categorized these proteins into seven classes [46,47]. While BELL genes are separated into five classes, KNOX genes are arranged in two classes (Figure 1). Our classification results are further supported by the ML-phylogenetic tree built with the best model and the annotations of the SMART database [31,48]. Certain domains or combinations of domains represent each class.
According to the gene structure study findings, introns are present in every TALE gene. Gene structures among members of the same class are similar. Additionally, the phylogenetic tree’s adjacent members share comparable exon lengths (Figure 3). According to the analysis and annotation of protein motifs, individuals belonging to the same class have comparable protein motifs, which is in line with other research on the poplar TALE family [49].

4.3. In Silico Analysis Shows the Stress-Responsive Nature of BhTALE Genes

Responsive elements located upstream of the gene promoter site selectively bind transcription factors to control gene transcription. In line with previous research, this study discovered that the BhTALE promoter sequence includes several cis elements linked to abiotic stress and hormonal response, including the methyl jasmonate response element, abscisic acid response element, and gibberellin response element (Figure 5) [7,50]. It is suggested that there is considerable conservatism in the BhTALE gene promoter. According to earlier research, ABRE has been linked to severe salt stress in plants, ABA induction, and plant dryness [51,52,53]. Furthermore, many components are associated with stress, including ARE, MBS, and LTR. The findings suggest a role for BhTALE in abiotic stress in wax gourds. Additionally, protein–protein network analysis and gene function prediction demonstrate that the BhTALE family is crucial in controlling ovule and inflorescence development. Consistent with the previous study’s findings, gene functional prediction and protein-protein network analysis also revealed interactions between BhTALE15 and BhTALE17 and various other proteins involved in floral organs [7].

4.4. BhTALE Genes Regulate Wax Gourd Response to Low Calcium and Magnesium

Low calcium is a type of nutrient stress that causes many deficiency symptoms. For instance, low calcium stress can restrict root growth, resulting in poor plant vigor and smaller leaves. Leaves smaller than normal size mean lower photosynthetic capacity and overall stunted plant growth [54,55,56]. Magnesium, on the other hand, is equally important to plants for maintaining their growth activities. Magnesium is at the front and center of chlorophyll and is indispensable for properly functioning photosynthetic machinery [28]. In our study, the wax gourd plants were treated with low calcium stress and magnesium to investigate the role of the BhTALE gene family. In particular, under low calcium, calcium, and magnesium applications, BhTALE7, BhTALE10, and BhTALE14 were expressed differentially in leaves. Analogously, the induced expression pattern of BhTALE4 was recorded in the roots under low calcium and magnesium applications. The sole high expression of BhTALE18 under low calcium was also recorded (Figure 8). From the obtained data, it can be assumed that these genes could be vital in regulating the response of wax gourd to low calcium and magnesium. The expression of BhTALE10, BhTALE14, and BhTALE18 was induced through distinct treatments significantly and separately. These genes could be considered for functional studies to characterize their role under low calcium stress.

5. Conclusions

Bioinformatics and expression analysis of the BhTALE gene family under calcium and magnesium treatment in wax gourd was performed in this study. Our in silico analysis revealed the potential biological and molecular functions of BhTALE genes in wax gourd developmental and stress biology. The expression analysis of BhTALE genes yielded valuable insights regarding their hypothesized function in modulating the growth of wax gourd plants in response to low calcium and magnesium stress. The BhTALE genes displayed responsiveness to nutrient stress, underscoring their critical role in growth regulation and stress responses. Compared to the delicate cultivar, Teizhu 2 exhibited a markedly diminishing performance under low calcium and magnesium environments. The results above highlight the possible significance of BhTALE transporters in endowing wax gourd with calcium and magnesium stresses.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae10101083/s1, Primer sequences are available in Table S1.

Author Contributions

S.H.: writing—original draft, data analysis, and formal analysis. S.H., X.C. and J.C.: data analysis, investigation. S.H., D.X. and J.L.: writing—review and editing. B.Z. and S.H.: conceived and designed the experiment. B.Z. secured the funding and contributed to review editing. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Guangdong Basic and Applied Basic Research Foundation (2023A1515030283); Special fund for scientific innovation strategy-construction of high leveled Academy of Agricultural Sciences (R2023PY-JG006); Agricultural Competitive Industry Discipline Team Building Project of Guangdong Academy of Agricultural Sciences (202303TD).

Institutional Review Board Statement

All scientific ethics were considered before submission. The Guangdong Academy of Agriculture Science provided the seeds and plant materials.

Data Availability Statement

Data is contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare that they have no known competing financial interests. We have no non-financial conflicts of interest that could affect the production of this manuscript.

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Horticulturae 10 01083 g001
Figure 1. A phylogenetic study of the BhTALE gene family. The amino acid sequences were used to create the phylogenetic tree using machine learning techniques. Seven groups were created from the BhTALE genes, and ITOL was used to display the final tree.
Figure 1. A phylogenetic study of the BhTALE gene family. The amino acid sequences were used to create the phylogenetic tree using machine learning techniques. Seven groups were created from the BhTALE genes, and ITOL was used to display the final tree.
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Figure 2. BhTALE gene location on chromosomes. The wax gourd has 12 chromosomes, with the number of chromosomes located at each chromosome. The relative locations of the BhTALE genes are indicated on the chromosomes. The program used to create the schematic depiction was TBtools (Version 1.098765).
Figure 2. BhTALE gene location on chromosomes. The wax gourd has 12 chromosomes, with the number of chromosomes located at each chromosome. The relative locations of the BhTALE genes are indicated on the chromosomes. The program used to create the schematic depiction was TBtools (Version 1.098765).
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Figure 3. Conserved motifs and gene structure analysis of BhTALE gene family. Diagram showing the conserved motif in (A) and the gene structure in (B). Gene display structure and the MEME web server provided the gene structure analysis and motif distribution, respectively.
Figure 3. Conserved motifs and gene structure analysis of BhTALE gene family. Diagram showing the conserved motif in (A) and the gene structure in (B). Gene display structure and the MEME web server provided the gene structure analysis and motif distribution, respectively.
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Figure 4. Gene ontology analysis of BhTALE genes in wax gourd. The analysis revealed different GO enrichment terms associated with BhTALE genes.
Figure 4. Gene ontology analysis of BhTALE genes in wax gourd. The analysis revealed different GO enrichment terms associated with BhTALE genes.
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Figure 5. The pie chart representing the percentage of different cis elements in the promoter region of BhTALE genes. The wax gourd BhTALE genes’ cis-acting elements. Growth-related, stress-responsive, and hormonal regulatory components were reflected in the data.
Figure 5. The pie chart representing the percentage of different cis elements in the promoter region of BhTALE genes. The wax gourd BhTALE genes’ cis-acting elements. Growth-related, stress-responsive, and hormonal regulatory components were reflected in the data.
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Figure 6. The predictive functional partners of BhTALE proteins. BhTALE5 and BhTALE7 was used as a reference in the String online tool for functional predictor analysis.The green color boxes represents homodimeric while the orange boxes represents heterodimeric interactions.
Figure 6. The predictive functional partners of BhTALE proteins. BhTALE5 and BhTALE7 was used as a reference in the String online tool for functional predictor analysis.The green color boxes represents homodimeric while the orange boxes represents heterodimeric interactions.
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Figure 7. BhTALE gene expression in response to low and high calcium treatments. The RPKM values were converted and normalized using the log2 transformation method before being shown on the color scale bar.
Figure 7. BhTALE gene expression in response to low and high calcium treatments. The RPKM values were converted and normalized using the log2 transformation method before being shown on the color scale bar.
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Figure 8. The expression of BhTALE genes was investigated in wax gourd roots and leaves that had been treated with calcium and magnesium. The mean values ± standard deviation (SD) of the three replicates is depicted by bars. Distinct lowercase letters denote substantial differences at p < 0.05. nd represents non-detected expression.
Figure 8. The expression of BhTALE genes was investigated in wax gourd roots and leaves that had been treated with calcium and magnesium. The mean values ± standard deviation (SD) of the three replicates is depicted by bars. Distinct lowercase letters denote substantial differences at p < 0.05. nd represents non-detected expression.
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Figure 9. Expression study of BhTALE genes in wax gourd leaves treated with low Mg. The mean values ± standard deviation (SD) of the three replicates is depicted by bars. Distinct lowercase letters denote substantial differences at p < 0.05.
Figure 9. Expression study of BhTALE genes in wax gourd leaves treated with low Mg. The mean values ± standard deviation (SD) of the three replicates is depicted by bars. Distinct lowercase letters denote substantial differences at p < 0.05.
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Table 1. The genome information of the BhTALE gene family.
Table 1. The genome information of the BhTALE gene family.
NameGene IDChromosomal LocationSubcellular
BhTALE1Bhi02G000349Chr2: 8718933 … 8740554 (−)Nucleus
BhTALE2Bhi03G001512Chr 3: 41081772 … 41087777 (−)Nucleus
BhTALE3Bhi03G001611Chr 3: 44246973 … 44252304 (−)Nucleus
BhTALE4Bhi03G000473Chr 3: 11851118 … 11855225 (−)Nucleus
BhTALE5Bhi04G000450Chr 4: 12570212 … 12575367 (−)Nucleus
BhTALE6Bhi04G000431Chr 4: 12094162 … 12100830 (−)Nucleus
BhTALE7Bhi04G000020Chr 4: 649004 … 654299 (−)Nucleus
BhTALE8Bhi04G000553Chr 4: 15727426 … 15742670 (+)Nucleus
BhTALE9Bhi04G000431Chr 4: 12094162 … 12100830 (−)Nucleus
BhTALE10Bhi05G001210Chr 5: 47747978 … 47752706 (−)Nucleus
BhTALE11Bhi06G001339Chr 5: 47747978 … 47752706 (−)Nucleus
BhTALE12Bhi07G001403Chr 7: 48154292 … 48163762 (+)Nucleus
BhTALE13Bhi08G000192Chr 8: 7980115 … 7986683 (−)Nucleus
BhTALE14Bhi09G002444Chr 9: 77103490 … 77108059 (−)Nucleus
BhTALE15Bhi09G002609Chr 9: 81520308 … 81524945 (+)Nucleus
BhTALE16Bhi09G002444Chr 9: 77103490 … 77108059 (−)Nucleus
BhTALE17Bhi09G000031Chr 9: 606684 … 610404 (−)Nucleus
BhTALE18Bhi10G001574Chr 10: 48974608 … 48979463 (+)Nucleus
BhTALE19Bhi10G000146Chr 10: 4078350 … 4083322 (+)Nucleus
BhTALE20Bhi10G001790Chr 10: 56344392 … 56350654 (−)Nucleus
BhTALE21Bhi11G001983Chr 11: 64704085 … 64708775 (−)Nucleus
BhTALE22Bhi11G001620Chr 11: 54758024 … 54762277 (+)Nucleus
BhTALE23Bhi12G000276Chr 12: 8560884 … 8566030 (+)Nucleus
BhTALE24Bhi12G000297Chr 12: 9196808 … 9201184 (−)Nucleus
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Hussain, S.; Chang, J.; Li, J.; Chen, X.; Xie, D.; Zhang, B. Transcriptome Wide Identification and Expression Analysis Revealed BhTALE Gene Family Regulates Wax Gourd (Benincasa hispida) Response to Low Calcium and Magnesium Stress. Horticulturae 2024, 10, 1083. https://doi.org/10.3390/horticulturae10101083

AMA Style

Hussain S, Chang J, Li J, Chen X, Xie D, Zhang B. Transcriptome Wide Identification and Expression Analysis Revealed BhTALE Gene Family Regulates Wax Gourd (Benincasa hispida) Response to Low Calcium and Magnesium Stress. Horticulturae. 2024; 10(10):1083. https://doi.org/10.3390/horticulturae10101083

Chicago/Turabian Style

Hussain, Shahid, Jingjing Chang, Jing Li, Xiao Chen, Dasen Xie, and Baige Zhang. 2024. "Transcriptome Wide Identification and Expression Analysis Revealed BhTALE Gene Family Regulates Wax Gourd (Benincasa hispida) Response to Low Calcium and Magnesium Stress" Horticulturae 10, no. 10: 1083. https://doi.org/10.3390/horticulturae10101083

APA Style

Hussain, S., Chang, J., Li, J., Chen, X., Xie, D., & Zhang, B. (2024). Transcriptome Wide Identification and Expression Analysis Revealed BhTALE Gene Family Regulates Wax Gourd (Benincasa hispida) Response to Low Calcium and Magnesium Stress. Horticulturae, 10(10), 1083. https://doi.org/10.3390/horticulturae10101083

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