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Genome-wide identification and structural analysis of the BMP gene family in Triplophysa dalaica

BMC Genomics volume 25, Article number: 194 (2024) Cite this article

Abstract

Background

Bone morphogenetic proteins (BMPs) are part of the transforming growth factor beta (TGF-β) superfamily and play crucial roles in bone development, as well as in the formation and maintenance of various organs. Triplophysa dalaica, a small loach fish that primarily inhabits relatively high elevations and cooler water bodies, was the focus of this study. Understanding the function of BMP genes during the morphogenesis of T. dalaica helps to clarify the mechanisms of its evolution and serves as a reference for the study of BMP genes in other bony fishes. The data for the T. dalaica transcriptome and genome used in this investigation were derived from the outcomes of our laboratory sequencing.

Results

This study identified a total of 26 BMP genes, all of which, except for BMP1, possess similar TGF-β structural domains. We conducted an analysis of these 26 BMP genes, examining their physicochemical properties, subcellular localization, phylogenetic relationships, covariance within and among species, chromosomal localization, gene structure, conserved motifs, conserved structural domains, and expression patterns. Our findings indicated that three BMP genes were associated with unstable proteins, while 11 BMP genes were located within the extracellular matrix. Furthermore, some BMP genes were duplicated, with the majority being enriched in the GO:0008083 pathway, which is related to growth factor activity. It was hypothesized that genes within the BMP1/3/11/15 subgroup (Group I) play a significant role in the growth and development of T. dalaica. By analyzing the expression patterns of proteins in nine tissues (gonad, kidney, gill, spleen, brain, liver, fin, heart, and muscle), we found that BMP genes play diverse regulatory roles during different stages of growth and development and exhibit characteristics of division of labor.

Conclusions

This study contributes to a deeper understanding of BMP gene family member expression patterns in high-altitude, high-salinity environments and provides valuable insights for future research on the BMP gene family in bony fishes.

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Introduction

Bone morphogenetic proteins (BMPs) constitute a highly potent class of growth factors within the larger TGF-β superfamily. The biological actions of BMPs were initially described in the 1960s when they were found to stimulate the formation of ectopic bone [1]. Since the successful cloning and identification of the first BMP genes in the 1980s [2], more than 40 BMP genes have been identified. BMPs are crucial for osteoblast differentiation and bone formation and have been implicated in cancer development by promoting the growth and invasion of cancer cells [3, 4]. These genes also regulate various physiological systems, including the circulatory, gastrointestinal, pulmonary, urinary, reproductive, and neurological systems [5], playing critical roles in embryonic development, growth, and differentiation [6]. Based on sequence homology, BMP family genes are divided into groups according to their roles in cell differentiation and growth: BMP1/3/11/15 (Group I), BMP12/13/14 (Group II), BMP2/4/16 (Group III), BMP9/10 (Group IV), and BMP5/6/7/8 (Group V) [7, 8]. BMP1 encodes a bone morphogenetic protein, which is a metalloproteinase responsible for regulating the deposition of extracellular matrix in vertebrate fibers. It also plays a vital role in various extracellular matrix metabolism and regulatory processes, contributing to essential biological functions [9]. BMP2 and BMP4 have well-established roles in critical processes such as embryonic development and the creation and differentiation of adipose precursor cells [10]. BMP4 influences the differentiation and proliferation of lipogenic progenitor cells, with differentiated adipocytes secreting BMP4 [11]. BMP9 is involved in chronic liver disease (CLD), where its elevated expression promotes fibrosis in fibrotic livers [12]. BMP7 promotes the neuronal differentiation of bone marrow mesenchymal stem cells (BMSCs), while BMP8 plays a crucial role in preventing premature luteinization of granulosa cells for ovarian follicle development [13, 14]. BMP genes exhibit variable expression in various carp tissues, including the gills, gut, liver, spleen, skin, heart, gonads, muscle, kidneys, cephalic kidneys, brain, and blood [8].

T. dalaica is found primarily in northern China in the Yellow River tributaries and in artesian water basins such as Inner Mongolia's Dali Lake [15]. T. dalaica thrives in high-altitude environments characterized by low water temperatures, especially in high-salt alkaline waters such as still lakes and river slopes. This species exhibits remarkable adaptations to plateau conditions, including its ability to acclimate to low-oxygen aquatic habitats and endure cold temperatures [15]. This harsh environment requires specific physiological adaptations for survival and reproduction, and the BMP gene family is involved in many physiological and metabolic processes, including bone and cartilage formation. Therefore, investigating the role of BMP genes in the adaptation of this species to extreme conditions will help to unravel the underlying mechanisms of its molecular adaptation and evolution and provide some assistance for subsequent studies of the BMP gene family in scleractinian fishes.

In this study, we identified 26 BMP genes in T. dalaica based on its whole genome. We also explored the potential roles and regulatory mechanisms of these BMP genes in T. dalaica through bioinformatics analysis and comparative studies with other vertebrates. These findings lay the foundation for further exploration of BMP gene functions in T. dalaica and contribute to the understanding of its physiological characteristics at the molecular level, providing support for the protection of germplasm resources in T. dalaica.

Materials and methods

Materials

The data for the T. dalaica transcriptome (Table S1) and genome (PRJNA624716) used in this investigation were derived from the outcomes of our laboratory sequencing. The T. dalaica specimens utilized in this study were collected from Dalinuoer Lake (43°22′43″N, 116°39′24″E), Inner Mongolia [16]. For the sequencing of T. dalaica, we employed PacBio sequencing and Hi-C technology, which resulted in chromosome-level genomic and transcriptomic data [15]. The de novo assembled genome had a total size of 607.91 Mb, with a contig N50 of 9.27 Mb. The total data volume collected was 126.5 Gb and 106 Gb.

BMP gene identification and sequence analysis

The CDSs and amino acid sequences of four species, Danio rerio, Homo sapiens, Cyprinus carpio, and Xenopus laevis, were obtained from publicly available data in the Ensembl database (http://asia.ensembl.org/) and the National Center for Biotechnology Information (NCBI) website (http://www.ncbi.nlm.nih.gov/genbank/). We conducted a BLASTP alignment search against the T. dalaica genome database utilizing BMP gene protein sequences from these species as query sequences, with an e-value cutoff set at 1e-5. To confirm the accuracy of the identification of the candidate genes in T. dalaica, a reverse blast was carried out using the NCBI database. The protein sequences of T. dalaica's BMP genes were established by analyzing the intersection of the findings. We assessed the physical and chemical properties of BMP family members, including amino acid count, theoretical isoelectric point, molecular weight, and instability index, using TBtools software [17]. Subcellular localization was investigated using the WoLF PSORT website (https://www.genscript.com/wolf-psort.html), while the identification of open reading frames (ORFs) for BMP genes was executed via the utilization of ORF Finder (https://www.ncbi.nlm.nih.gov/gorf/gorf.html) [18].

Multiple sequence comparisons and phylogenetic analysis of BMP genes

The amino acid sequences of conserved domains in BMP genes belonging to the TGF superfamily were extracted using SAMRT [19]. Multiple sequence alignment was performed using BioEdit [20], aligning the protein sequences of BMP genes from D. rerio, H. sapiens, C. carpio, and X. laevis obtained from the NCBI and Ensembl databases (http://www.ebi.ac.uk/Tools/msa/clustalw2/) [21]. A phylogenetic tree was constructed in MEGA11 using the matched sequences and the neighbor-joining technique [22], with a bootstrap repeat count of 1000. The generated phylogenetic tree was further refined using the ChiPlot online tool (https://www.chiplot.online/) [23]. The BMP protein sequences of the four species D. rerio, H. sapiens, C. carpio, and X. laevis are given in Table S3.

Gene nomenclature

The BMP genes in T. dalaica were identified through a combination of multiple sequence alignment and phylogenetic analyses. BMP genes in T. dalaica were named based on BMP gene sequences from D. rerio, H. sapiens, C. carpio, and X. laevis. In instances where multiple T. dalaica genes were grouped with the other four species, a Latin numeral suffix was appended to each gene name. The final nomenclature of the BMP genes in T. dalaica, along with that of the selected species, can be found in Table 1.

Table 1 BMP gene families in the genomes of the five vertebrates
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Synteny analysis

To explore gene duplication events within T. dalaica, we conducted an intraspecific collinearity analysis. Additionally, a comparative collinearity analysis map was constructed between T. dalaica and two additional osteichthyan species, D. rerio, and C. carpio. Genomic data and annotation information for D. rerio and C. carpio were obtained from the NCBI and Ensembl databases, respectively. For both intraspecific and interspecific collinearity analyses, we used TBtools software for analysis and diagramming [17].

Chromosomal localization and gene structure analysis of the BMP genes

The chromosomal localization of T. dalaica BMP genes was ascertained by importing the complete genome annotation file of T. dalaica into TBtools software in conjunction with the BMP gene sequence data [17]. Subsequently, the physical positions of the chromosomes corresponding to the BMP genes were visualized.

Predictions of the secondary structure elements of BMP protein sequences, including α-helices, β-turns, extended strands, and disordered coils, were made using SOPMA (http://pbil.ibcp.fr/) [24]. Subcellular localization prediction of BMP protein sequences was performed using Cell-PLoc2.0 http://www.csbio.sjtu.edu.cn/bioinf/Cell-PLoc-2/ [25]. Information on BMP gene exons and introns was extracted from the T. dalaica whole-genome annotation file, and visualization was carried out using TBtools (http://tbtools.bioinfodata.com/) [17].

Analysis of conserved motifs and conserved structural domains of the BMP genes

MEME (http://meme-suite.org/) was used to predict protein motif patterns in the T. dalaica BMP gene family. The maximum motif value was set to 10, with a width range of 6 to 50. The results were visualized using TBtools. Conserved domain structures of BMP genes were predicted using the NCBI-Batch-CD-search tool (https://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi) and the SMART tool (http://smart.embl-heidelberg.de). TBtools and the BMP protein phylogenetic tree were used for visualization of conserved BMP protein motifs and domains [17].

GO enrichment analysis of BMP genes

GO enrichment analysis of the BMP genes was conducted using assembled transcripts obtained from whole-genome sequencing of T. dalaica. The basic unit of GO enrichment was term, and all differently expressed genes were mapped to each term in the Gene Ontology database (http://www.geneontology.org/) to obtain the number of genes in each term. Apply chi-square test or hypergeometric test to identify GO terms that are significantly enriched in differentially expressed genes compared to the entire genome background. Determine the main biological functions performed by the differentially expressed genes through significant GO functional enrichment analysis.

Expression patterns of BMP genes

The original image data derived from sequencing were converted into sequence data via base calling, yielding raw reads, which were saved in fastq file format. We used Trimmomatic software (http://www.usadellab.org/cms/index.php?page=trimmomatic) to filter the raw data, remove reads with adaptors, discard reads with more than 10% 'N' bases, and eliminate reads where more than 50% of bases had a quality score less than 20 [26]. Afterward, we applied FastQC software (http://www.bioinformatics.babraham.ac.uk/projects/fastqc) for quality control of the clean data, and ultimately, Trinity software was used for the assembly of these clean data. The transcriptome assembled by Trinity was utilized as the reference sequence (ref), onto which clean reads of each sample were mapped. We implemented the RSEM software for this process, with the Bowtie2 parameter set to a mismatch of 0 (the default Bowtie2 parameter) [27]. RSEM provided statistical analysis of the bowtie alignment results, furnishing the read count numbers for each gene in every sample [28]. These counts were subsequently subjected to TPM (transcripts per million) conversion—a normalized value indicating the quantity of transcripts for a specific gene or transcript per million total transcripts within the sample—which facilitated the analysis of gene expression levels. Ultimately, this analysis resulted in the quantified abundances of BMP gene transcripts. A heatmap of gene expression was generated using the online tool ChiPlot (https://www.chiplot.online/) [23, 29].

We also performed real-time fluorescence quantitative PCR (qRT‒PCR) analysis of selected tissues and genes to verify the accurate transcriptome abundance analysis of the gene expression trends. Three specimens of T. dalaica from the saline-alkali waters of Dali Lake (Inner Mongolia) were collected, and RNA was extracted from six tissues—brain, liver, spleen, gonad, kidney, and gill—followed by cDNA synthesis and RT‒PCR. Specific primers for certain members of the BMP gene family in T. dalaica were designed using Primer 5.0 (Table S2). The qRT‒PCR experiments were conducted using the TransStart Top Green qPCR SuperMix kit. The amplification system consisted of a 10 μL reaction mixture with 1 μL cDNA, 0.2 μL forward primer, 0.2 μL reverse primer, 5 μL TransStart Top Green qPCR SuperMix, and 3.6 μL ddH2O. The experiments were performed on a LightCycler 96 Real-Time PCR System with three biological and three technical replicates. β-actin was used as the internal control gene, and the data were processed using the 2−△△Ct method, where △△Ct = (average Ct value of the target gene in treated samples—average Ct value of the internal control gene in treated samples)—(average Ct value of the target gene in control samples—average Ct value of the internal control gene in control samples) [30]. With the kidney group set as 1 for the same gene, the relative expression levels were calculated and graphed in GraphPad Prism 9. The relative expression levels of all the genes were analyzed via one-way ANOVA followed by Duncan's multiple range test, with P < 0.05 indicating statistical significance. The final results are presented in Fig. 1.

Fig. 1
figure 1

Expression of different genes in each tissue. a,b,c Three letters and the same letter indicate no significant difference, and different letters indicate significant differences

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Results

BMP gene identification and characterization

Utilizing the whole-genome data of T. dalaica, we conducted a comparison to eliminate duplicate sequences, considering other species such as D. rerio, H. sapiens, C. carpio, and X. laevis. Furthermore, by integrating information from relevant literature [31, 32], we successfully identified a total of 26 BMP gene sequences (BMP1a-BMP16) in T. dalaica, which were subsequently categorized into five groups: BMP1/3/11/15 (Group I), BMP12/13/14 (Group II), BMP2/4/16 (Group III), BMP9/10 (Group IV), and BMP5/6/7 (Group V).

These 26 genes were discovered within the T. dalaica genome and are described in Table 1. We also analyzed the physicochemical characteristics of the 26 protein sequences, which are presented in Table 2. The study revealed that the open reading frame (ORF) lengths of the 26 BMP genes varied from 738 (BMP15-1) to 3069 (BMP1b-1) base pairs (bp), with the number of exons ranging from 1 to 21. The predicted isoelectric points ranged from 4.97 to 9.94, with 11 sequences exhibiting acidity and 15 showing alkalinity. Interestingly, most BMP proteins in T. dalaica tend to precipitate under highly alkaline conditions, possibly due to the alkaline environment of the species. The predicted code sequence of the BMP gene family varies in the number of amino acids, ranging from 245 (BMP15-1) to 1022, with relative molecular masses varying from 28.07 kDa to 115.35 kDa. Notably, the average affinity coefficients for T. dalaica BMP gene family proteins were consistently negative, indicating affinities for each of these proteins. Additionally, a majority of the BMP proteins displayed a genetic instability index above 40, indicating stability, whereas those considered unstable had an index less than 30.

Table 2 Characteristics of BMP Gene Family Members in the Genome of Triplophysa dalaica
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Subcellular localization findings, as presented in Table 2, revealed that 11 BMP proteins were found in the extracellular plasma, while 9 BMP proteins were located in the plasma membrane. The remaining BMP proteins were detected in various locations, including the cell nucleus, fibromyalgia, endothelial plasma, and cellulose.

BMP Genetic System Development Analysis

To explore the evolutionary correlation of the BMP gene family in T. dalaica, we generated a comprehensive phylogenetic tree using protein sequences derived from D. rerio, H. sapiens, C. carpio, and X. laevis (Fig. 2). The phylogenetic tree analysis revealed distinct clustering of the BMP gene family in T. dalaica and other species into five groups: BMP1/3/11/15 (Group I), BMP12/13/14 (Group II), BMP2/4/16 (Group III), BMP9/10 (Group IV), and BMP5/6/7 (Group V). Notably, the BMP8a protein sequences of D. rerio, H. sapiens, C. carpio, and X. laevis formed a distinct branch. The majority of the BMP genes in T. dalaica were categorized into Group I. Phylogenetic analysis revealed a notable level of similarity between T. dalaica and two other species, D. rerio and C. carpio, both of which belong to the Cypriniformes order, in contrast to humans and the amphibian X. laevis (Fig. 2).

Fig. 2
figure 2

Phylogenetic analysis of the BMP genes of T. dalaica and selected species. The different colors on the outer ring in the figure represent the different groups, the different species are represented by different colors, and the BMP gene of T. dalaica is marked by a red star

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BMP gene collinearity analysis

We identified three occurrences of gene segment duplication in T. dalaica, all resulting from gene fragment duplications; these duplications were located on chromosomes 3 and 21, 8 and 10, and 18 and 22 (Fig. 3). BMP1a and BMP1b-2 underwent gene segment duplications and belonged to the same gene group, with their encoded proteins exhibiting activities similar to those of BMP11-1 and BMP11-2. Interestingly, segmental duplication of BMP7a occurred alongside the non-BMP gene. The BMP7 gene belongs to the TGF-β superfamily, and Fig. 4 shows that BMP7a is abundantly expressed in fins, muscles and gonads, which suggests that BMP7a may be involved in the realization of locomotor function in T. dalaica and influence sex differentiation in T. dalaica. Figure 3 shows that BMP7a is duplicated with the GDF15 gene, possibly because it belongs to the same TGF-β superfamily as the BMP7a gene is, and the GDF15 gene has an assisting role in the physiological function of BMP7a. Since T. dalaica, D. rerio, and C. carpio are all Cypriniformes, we explored interspecies collinearity among the three species and revealed a significant collinearity link. Most of the T. dalaica BMP genes exhibited collinearity with D. rerio and C. carpio genes (Fig. 5).

Fig. 3
figure 3

Analysis of BMP gene covariance in T. dalaica. The gray line indicates the genome covariance of T. dalaica, and the colored line connecting the BMP genes indicates the duplication of BMP genes in T. dalaica. The position of the BMP genes on the chromosomes is indicated by the short black line, and the density of the genes on each chromosome is shown at the same time

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Fig. 4
figure 4

Analysis of the BMP gene expression pattern in T. dalaica. The square color scale of the heatmap indicates the TPM values after row normalization; the specific values are marked in the color block, and the maximum value is indicated in red

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Fig. 5
figure 5

Interspecies covariance analysis of T. dalaica with D. rerio and C. carpio. a represents the covariance results of T. dalaica with D. rerio, b represents the covariance results of T. dalaica with C. carpio, gray lines represent the covariance blocks of T. dalaica with D. rerio and C. carpio, and red lines represent the highlighted BMP gene blocks. The abbreviations "Td", "Dr" and "Cc" denote T. dalaica, D. rerio and C. carpio, respectively

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Chromosomal localization and gene structure analysis of the BMP genes

We determined the chromosomal location of the BMP gene family in T. dalaica using TBtools software [17], and the results are presented in Fig. 6. This investigation revealed that the 26 BMP genes in T. dalaica were dispersed among 19 chromosomes (1, 2, 4, 6, 8, 10, 11, 12, 13, 14, 15, 16, 17, 18, 20, 21, 22, 23, 25). Intriguingly, an overrepresentation of BMP genes was observed on chromosomes 4, 11, and 15, suggesting a non-uniform and stochastic distribution pattern within the species. Additionally, we observed close proximity of BMP9 and BMP3b-2 on chromosome 17, suggesting the potential formation of a gene cluster resulting from early gene duplication events (Fig. 6) [33, 34].

Fig. 6
figure 6

Chromosomal locations of BMP genes in the T. dalaica genome

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To investigate the structural variation of the BMP gene family, we used TBtools to visualize the exon‒intron architectures of the 26 BMP genes (Fig. 7) [17]. The results showed that BMP1b-1 had the highest number of exons (21), while the number of other exons ranged from 2 to 21. We also generated an NJ phylogenetic tree to examine T. dalaica BMP gene protein sequences and assess gene arrangement. BMP genes with similar structural properties were grouped in the evolutionary tree. These findings shed light on the diversity and evolution of the BMP gene family. Furthermore, the secondary structure prediction indicated that T. dalaica BMP gene proteins contain α-helices, β-turns, extended strands, and irregular coils (Table 3). The percentage of α-helices ranged from 11.17% (BMP1a) to 32.41% (BMP9), β-turns from 1.23% (BMP13a) to 5.84% (BMP1a), extended strands from 13.05% (BMP12) to 27.77% (BMP1a), and irregular coils from 46.73% (BMP9) to 62.45% (BMP15–1). The secondary structure prediction suggested that irregular coils are the predominant structural component of T. dalaica BMP genes.

Fig. 7
figure 7

Gene structure of the BMP gene of T. dalaica. The phylogenetic tree on the left was constructed in MEGA11 based on the neighbor‒joining method, with a bootstrap value of 1000, and different colors represent different groups

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Table 3 Secondary structure of the BMP gene protein from Triplophysa dalaica
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Analysis of conserved motifs and structural domains of the BMP genes

We utilized the MEME online program to investigate the conserved protein motifs of the BMP gene family in T. dalaica, resulting in the identification of ten conserved protein motifs (Fig. 8(b)). Notably, motif 1 featured a conserved sequence of LYVDFKDJGWDDWIIAPEGYEAYYCEGEC, motif 2 was characterized by a conserved sequence of CCVPTKLSPISVLYLDDSENVVLKKY, and motif 4 exhibited a conserved sequence of EBMVVESCGCR, all with a length of 11 amino acids. The analysis revealed that genes with closer evolutionary relationships displayed more similar motif architectures. While motif 9 was found to be exclusively conserved in BMP1a, BMP1b-1, and BMP1b-2, motifs 1, 2, and 4 were detected in all the other family members, underscoring their notable conservation within the core functional domains of the BMP genes (Fig. 8). The distribution of motifs aligns with the phylogenetic tree, demonstrating that genes within the same subgroup exhibited similar motif patterns (Fig. 8(a)).

Fig. 8
figure 8

Conserved motifs of the BMP gene of T. dalaica. a The phylogenetic tree on the left was constructed in MEGA11 based on the neighbor‒joining method, with a bootstrap value of 1000, and different colors represent different groups. b All motifs were identified by the MEME database, and different colored blocks represent different motifs

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Moreover, as depicted in Fig. 9, the BMP gene family members in T. dalaica that clustered together under the same branch exhibited notable similarities in terms of conserved protein domains. These observations are consistent with the observed distribution patterns and the results of the phylogenetic tree analysis. Notably, the BMP1a, BMP1b-1, and BMP1b-2 genes produced proteins with distinct conserved domains ("ZnMc," "CUB," "Fxa"), arising from their unique gene structures. BMP1, classified as a zinc-dependent metalloproteinase, does not belong to the TGF-β superfamily [35, 36].

Fig. 9
figure 9

Structural domains of the BMP gene of T. dalaica. The phylogenetic tree on the left was constructed in MEGA11 based on the neighbor‒joining method, with a bootstrap value of 1000, and different colors represent different groups

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GO enrichment analysis of the BMP genes

We conducted a GO enrichment analysis, and the results presented in Table 4 revealed the involvement of the BMP gene family in T. dalaica in a total of 15 distinct GO pathways. Among these pathways, eight were associated with molecular functions (F), six were related to biological processes (P), and one was linked to cellular components (C). Notably, the GO pathways related to molecular functions were primarily associated with growth and development processes, including activities such as metallopeptidase activity, calcium ion binding, metalloendopeptidase activity, zinc ion binding, growth factor activity, receptor binding activity, and protein domain-specific binding. The GO pathways linked to biological processes predominantly included protein hydrolysis, cellular cytoskeleton organization, cell migration, and cell adhesion. The examination of the T. dalaica BMP gene phylogenetic tree (Fig. 7) suggested that the BMP1/3/11/15 (Group I) subfamily is involved primarily in these biological processes. Most BMP genes were enriched in the GO:0008083 pathway, associated with growth factor activity, aligning with the characteristic function of the BMP gene family, suggesting that the BMP1/3/11/15 (Group I) subfamily predominantly plays a role in T. dalaica's growth and development processes.

Table 4 GO enrichment analysis of the BMP gene family
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Expression analysis

Comprehending gene expression patterns plays a vital role in revealing gene functionality. In our study, we conducted an analysis of BMP gene expression data from various tissues of T. dalaica, thus shedding light on the expression patterns of members of the BMP gene family. The expression of several BMP genes in six tissues, T. dalaica, brain, liver, spleen, gonad, kidney and gill, was analyzed via real-time fluorescence quantitative PCR to verify the trend in the abundance of the BMP gene transcriptome. As shown in Fig. 1, the expression of BMP1a was greater in the liver than in the other tissues. BMP2a had the highest expression in the gill, BMP3b-2 had a much greater expression in the brain than in the other tissues, and BMP7b-1 had the highest expression in the gonad and the second highest expression in the brain. Similarly, the expression of BMP13b was greater in the gonad and spleen than in the other tissues. Figure 1 shows that the change in expression of the BMP gene in different tissues was the same as the change in expression in terms of transcriptome abundance (Fig. 4), which also indicated that the change in gene expression in the transcriptome abundance analysis in this study was correct. The heatmap revealed that the majority of the BMP genes in T. dalaica were expressed in the brain, gonads, gills, muscles, and fins, while exhibiting comparatively lower expression levels in the kidney, liver, spleen, and heart tissues. In particular, the brain presented noteworthy expression levels of BMP11-2, BMP3b-1, BMP3b-2, BMP11-1, and BMP9, with BMP3b-2 demonstrating the highest expression. This discovery indicates that BMP11s are likely secreted by neurons, suggesting their preference for expression in the brain [33]. In muscle tissues, BMP genes are universally expressed, with BMP12 and BMP1b-2 exhibiting the highest expression levels. In the gills, BMP2a, BMP3a, BMP2b, BMP10a, and BMP10b exhibited increased expression levels (Fig. 4). BMP1a is highly expressed in the gonads, liver, and heart; BMP1b-1, in muscles and gonads; and BMP1b-2, in muscles and gonads, suggesting that BMP1 is broadly involved in the development of gonads and metabolism in T. dalaica (Fig. 4). BMP3a, BMP3b-1, and BMP3b-2 are highly expressed in the brain, fins, gills, and muscles, suggesting the potential impact of BMP3 on skeletal plasticity. BMP11 is highly expressed in the brain, fins, and muscles, suggesting its potential role in the development, differentiation, and tissue formation of the nervous system in T. dalaica. BMP15-1 and BMP15-2 are highly expressed in muscles and gonads, suggesting that they play a role in reproductive system development. GO enrichment analysis revealed that the BMP1/3/11/15 (Group I) genes primarily contributed to the growth and development of T. dalaica.

BMP7a, BMP7b-1, and BMP7b-2 are expressed primarily in the fins, muscles, and gonads. BMP7a is almost not expressed in the spleen, and the expression of BMP7b-1 and BMP7b-2 in the spleen and liver of T. dalaica is also negligible. BMP12 expression is almost nonexistent in the spleen and heart, suggesting that it plays a minor role in the physiological processes of the spleen and heart in T. dalaica. Similarly, BMP13b is hardly expressed in the liver, fins, or heart. BMP14 was also almost not expressed in the spleen or heart. It is hypothesized that these genes do not participate in the physiological functions of the corresponding tissues in T. dalaica under normal physiological conditions. However, further research may be needed to determine the specific roles of these genes.

Discussion

The primary functions of BMP genes include the control of osteoblast and chondrocyte development and differentiation and the promotion of bone healing, all of which are crucial for bone production [32, 37, 38]. The BMP gene family comprises essential signaling molecules involved in regulating cell division, proliferation, function, and tissue morphogenesis [39]. Furthermore, due to their significance as growth factors, they have a wide range of potential applications in various industries, including skeletal disease therapy and regenerative medicine [40, 41].

Leveraging whole-genome sequencing data collected by our research team, we successfully identified a comprehensive set of 26 BMP gene family members in the T. dalaica genome. Within this study, we conducted an in-depth analysis encompassing the physicochemical characteristics, subcellular localization, phylogenetic associations, intraspecies and interspecies collinearity, chromosomal mapping, and gene structure of these 26 BMP gene family members in T. dalaica, as well as the identification of conserved motifs and domains. The classification of these BMP genes within the T. dalaica genome was determined through the evaluation of sequence homology and evolutionary relationships. We identified five different subgroups, namely, the BMP 1/3/11/15 (Group I), BMP 12/13/14 (Group II), BMP 2/4/16 (Group III), BM 9/10 (Group IV), and BMP 5/6/7/8 (Group V) subgroups, which differed from the findings of previous studies of cobia [32]. These findings align with the research outcomes documented in previous studies on carp [33]. Compared to the other species studied (D. rerio and X. laevis), T. dalaica has a relatively complete BMP gene family, which includes three BMP1 genes, three BMP3 genes, three BMP7 genes, two BMP11 genes, and two BMP15 genes. This difference may be the result of the scleractinian WGD event [34]. This gene duplication results in new copies of genes with the potential for differentiated functions or new functions adapted to new environments, likely due to the specific survival environment of the T. dalaica species, which allows these genes to be expressed in large numbers [42, 43]. This phenomenon aligns with the ecological adaptations of scleractinian fishes [44, 45]. Notably, T. Dalaica may have undergone a gene deletion event during evolution, as the BMP8 gene is missing in T. dalaica compared to other scleractinian fishes (e.g., zebrafish, carp, etc.) and vertebrates [45].

In T. dalaica, the BMP15 gene is highly expressed in muscles and gonads and plays a significant role in the development of the reproductive system [46, 47]. The BMP11 gene is produced by neurons and is significantly expressed in the brain (Fig. 4) [33]. Most of the BMP genes belong to BMP1/3/11/15 (Group I) and are likely influenced by the specific environmental conditions in which T. dalaica thrives [48]. The results of our phylogenetic analysis revealed that T. dalaica, D. rerio, and C. carpio, all of which belong to the Cypriniformes order, share a close evolutionary relationship and form a distinct cluster. This separation distinguishes them from amphibians, such as X. laevis, and mammals, such as H. sapiens. These findings align with the taxonomic criteria for species classification, indicating that BMP genes in T. dalaica have maintained a high degree of conservation throughout their evolutionary history. The conserved base sequence, analysis of structurally conserved domains, and evolutionary relationships among T. dalaica BMP genes further suggest that BMP genes within the same subgroup share comparable base sequences, types of structural domains, and distribution patterns [49, 50]. This observation aligns with the common amino acid sequences shared among members of the TGF-β superfamily. Notably, there was repetition and fragmentation of the genes BMP1a and BMP1b-2 and of BMP11-1 and BMP-11–2, which belong to the same gene group. Notably, this phenomenon was also observed for genes outside the BMP group, including BMP7a. Furthermore, a Gene Ontology (GO) enrichment analysis of the BMP genes revealed that, except for BMP1a, BMP1b-1, and BMP1b-2, the remaining BMP genes were associated with the GO pathway related to growth factor activity. By analyzing the expression patterns of BMP genes, we observed that genes within the BMP1/3/11/15 subgroup (Group I) exhibited relatively high expression levels in most tissues. This finding suggested the significant role of these genes in the growth and development of T. dalaica. These findings are consistent with prior studies, such as those conducted in cobia and carp, where BMP15 exhibited high expression across multiple tissues and is generally regarded as crucial for female fertility [32]. T. dalaica lives in high-altitude and saline-alkaline environments, leading to the development of unique morphological and physiological characteristics adapted to extreme conditions. The genes BMP1, BMP13, BMP15, and BMP16 are highly expressed in the gonads and likely play key roles in reproductive development and regulating sex ratios to adapt to harsh environments. BMP2, BMP3, BMP4, BMP6, BMP10, and BMP16 are highly expressed in the gills, which is speculated to be a result of the environmental adaptation of T. dalaica, which involves the evolution of more efficient gills to obtain more oxygen.

Conclusion

In this research, we identified a total of 26 bone morphogenetic protein (BMP) genes within the genome of T. dalaica. Our phylogenetic and covariance analyses revealed that T. dalaica exhibited the closest genetic relationship to D. rerio and C. carpio, revealing strong covariance. We further examined the BMP genes in T. dalaica and identified instances of gene duplication, which can likely be attributed to whole-genome duplication (WGD) events. Upon scrutinizing the gene expression patterns, we noticed that the duplicated BMP genes in T. dalaica exhibited elevated expression levels. Furthermore, through extensive Gene Ontology (GO) enrichment analysis, it became evident that the BMP1/3/11/15 genes (Group I) played a primary role in the growth and development of T. dalaica. This study contributes to a deeper understanding of BMP gene family member expression patterns in high-altitude, high-salinity environments and provides valuable insights for future research on the BMP gene family in bony fishes.

Availability of data and materials

The datasets supporting the results of this article are included within manuscript and available on request (Dr. Chuanjiang Zhou). The Triplophysa dalaica genome DNA sequencing data have been deposited into the NCBI Sequence Read Archive under BioProject: PRJNA624716 (https://academic. oup.com/gbe/article/13/8/evab153/6311268). The datasets generated and analysed during the current study are available in the NCBI GenBank: OR733217-OR733242 (Data will be released when the manuscript published).

Abbreviations

GO:

Gene Ontology

CDS:

Coding sequence

F:

Molecular Functions

P:

Biological Processes

C:

Cellular Components

WGD:

Whole Genome Duplication

TPM:

Transcripts Per Kilobase of exon model per Million mapped reads

NJ:

Neighbor-Joining Algorithm

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Acknowledgements

This study was supported by the High-Performance Computing Center of Henan Normal University.

Funding

This work was supported by the following funding bodies: the National Natural Science Foundation of China (U2004146, 31872199), the Henan Province Department of Science and Technology (182102110046, 222102110294), and the Training Plan of Young Excellent Teachers in Colleges and Universities of Henan Province (2019GGJS063).

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  1. College of Fisheries, Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Henan Normal University, Xinxiang, 453007, People’s Republic of China

    Yizheng Zhang, Rui Han, Zhigang Ma, Yongtao Tang & Guoxing Nie

  2. College of Life Sciences, Henan Normal University, Xinxiang, 453007, People’s Republic of China

    Jinhui Yu, Meng Zhang, Yikai Li & Chuanjiang Zhou

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Contributions

Yizheng Zhang: Methodology, Formal analysis, Visualization, Writing original draft. Jinhui Yu: Methodology, Formal analysis, Visualization. Rui Han, Meng Zhang and Yikai Li: Investigation, Methodology, Formal analysis, Visualization. Zhigang Ma: Methodology, Formal analysis, Visualization. Yongtao Tang: Methodology, Formal analysis, Visualization. Guoxing Nie: Investigation, Conceptualization, Project administration, Supervision. Chuanjiang Zhou: Investigation, Methodology, Writing original draft, Conceptualization,Project administration, Funding acquisition, Supervision, Writing—review & editing.

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Correspondence to Guoxing Nie or Chuanjiang Zhou.

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The authors declare that all methods were carried out in accordance with relevant guidelines and regulations. All experiments involving animals and all experimental protocols were approved by the Animal Research and Ethics Committee of Henan Normal University and the Laboratory Animal Guidelines for the Ethical Review of Animal welfare (GB/T 35892–2018) and were conducted in accordance with the research standards, all methods were carried out in accordance with relevant guidelines and regulations, all methods are reported in accordance with ARRIVE guidelines for the reporting of animal experiments.

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Supplementary Information

Additional file 1: Table S1

. Triplophysa dalaica transcriptome data used in this study.

Additional file 2: Table S2

. Primers used for qRT‒PCR of the BMP gene family.

Additional file 3: Table S3. NCBI accession numbers for the BMP protein sequences of the four species.

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Zhang, Y., Yu, J., Han, R. et al. Genome-wide identification and structural analysis of the BMP gene family in Triplophysa dalaica. BMC Genomics 25, 194 (2024). https://doi.org/10.1186/s12864-024-10049-z

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