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Identification and expression analysis of Sox family genes in echinoderms
BMC Genomics volume 25, Article number: 655 (2024)
Abstract
The Sox gene family, a collection of transcription factors widely distributed throughout the animal kingdom, plays a crucial role in numerous developmental processes. Echinoderms occupy a pivotal position in many research fields, such as neuroscience, sex determination and differentiation, and embryonic development. However, to date, no comprehensive study has been conducted to characterize and analyze Sox genes in echinoderms. In the present study, the evolution and expression of Sox family genes across 11 echinoderms were analyzed using bioinformatics methods. The results revealed a total of 70 Sox genes, with counts ranging from 5 to 8 across different echinoderms. Phylogenetic analysis revealed that the identified Sox genes could be categorized into seven distinct classes: the SoxB1 class, SoxB2 class, SoxC class, SoxD class, SoxE class, SoxF class and SoxH class. Notably, the SoxB1, SoxB2, and SoxF genes were ubiquitously present in all the echinoderms studied, which suggests that these genes may be conserved in echinoderms. The spatiotemporal expression patterns observed for Sox genes in the three echinoderms indicated that various Sox members perform distinct functional roles. Notably, SoxB1 is likely involved in echinoderm ovary development, while SoxH may play a crucial role in testis development in starfish and sea cucumber. In general, the present investigation provides a molecular foundation for exploring the Sox gene in echinoderms, providing a valuable resource for future phylogenetic and genomic studies.
Introduction
Sox genes are distinguished by the presence of a high-mobility group (HMG) box, which comprises 79 amino acids. Since the initial discovery of the first Sox family gene, Sry, in 1990 [1], the Sox gene family has grown significantly, with more than 100 members identified across a diverse range of organisms, ranging from mammals and birds to reptiles, fishes, and even insects. The Sox family is divided into several distinct subfamilies [2]. The Sox family of genes plays crucial roles in various developmental processes, including sex determination/differentiation, endoderm development, angiogenesis, chondrogenesis, neurogenesis, and cardiogenesis. The breadth and depth of their influence across these diverse biological processes underscore the significance of the Sox family in the intricate machinery of life.
To obtain a thorough understanding of the evolution and function of the Sox family, it is paramount to meticulously characterize Sox genes across a diverse array of phyla. Previous studies have examined Sox family genes in mammals, teleosts, and invertebrates, revealing significant differences among these organisms. For instance, in mammals such as mice, humans, and buffalo, a total of 20 Sox genes, which can be subdivided into 8 subgroups (A, B1/B2, C, D, E, F, G, and H), have been identified [3, 4]. In contrast, teleosts exhibit a much larger Sox gene family, with 29 members reported in Oncorhynchus mykiss [5], 27 genes in Oreochromis niloticus [6], and 26 genes in Collichthys lucidus [7] and Danio rerio [8]. On the other hand, the Sox gene family appears to be more conserved in invertebrates, with 7 members in Patinopecten yessoensis [9] and 8 members in Drosophila melanogaster [10]. However, despite these advances, a critical gap remains in our knowledge of Sox genes in echinoderms. To date, no comprehensive study has been undertaken to identify and analyze Sox genes within this phylogenetically distinct group of organisms.
Echinoderms, long recognized as the invertebrate sister group nearest to vertebrates, possess a unique and distinct evolutionary classification [11]. As an ancient invertebrate group, echinoderms exhibit an exceptional array of reproductive modes [12]. Due to their rich biological characteristics, echinoderms have emerged as crucial research subjects in various fields, including embryonic development, sex determination and differentiation, and regeneration biology. Notably, recent investigations have indicated a potential link between Sox genes and certain biological processes in echinoderms [13, 14]. Despite these intriguing findings, there has been a notable absence of research focusing on a comprehensive analysis of Sox family genes in echinoderms.
The primary aim of this study was to conduct a thorough analysis of the abundance and expression patterns of Sox genes in echinoderms. Through the decoding of numerous echinoderm genomes, genome-wide identification and expression analysis of the Sox gene family were performed. The outcomes of this study have the potential to aid in elucidating the evolution and potential functions of Sox genes in echinoderms.
Materials and methods
Sequence identification
The Sox genes in 11 echinoderms, including Anneissia japonica, Acanthaster planc, Apostichopus japonicus, Asterias rubens, Heliocidaris erythrogramma, Heliocidaris tuberculate, Holothuria leucospilota, Lytechinus variegatus, Patiria miniate, Plazaster borealis, and Strongylocentrotus purpuratus, were identified through a combination of HMM and BLAST search methods. Initially, the relevant files for the echinoderms were downloaded from their respective databases, and the HMG domain query (accession: PF00505) was collected from the InterPro database (https://www.ebi.ac.uk/interpro/). Subsequently, a concurrent search for SOX proteins within all the genomes was conducted using both HMMER V3.4 [15] and BLAST V2.12.0 [16] through the HMG domain. The initial E values were set at 1.0 for the HMM searches and 1 × 10− 5 for BLAST. Next, the candidate genes identified by both methods were merged, and any duplicate genes were eliminated. If several transcripts were annotated for a specific gene, the transcript exhibiting the longest length was chosen for further analysis. Additionally, potential SOX orthologs were screened for the conserved motif RPMNAFMVW [17]. Finally, the protein properties of the identified Sox genes were calculated using TBtools v2.096 [18].
Phylogenetic analysis
Diverse sets of Sox protein sequences from various species, including humans, mice, zebrafish, tilapia, and fruit fly, were downloaded from the NCBI (Supplementary Table S1). The amino acid sequence of the HMG box of these Sox proteins, along with those identified from 11 echinoderms, were extracted utilizing the Batch SMART plug-in within TBtools v2.096 [18]. These sequences were subsequently subjected to phylogenetic analysis. MAFFT v7.525 [19] was used to generate multiple sequence alignments. Subsequently, IQTREE v2.3.1 [20] was employed to construct phylogenetic trees utilizing the specific settings of --bnni, -m MFP, -B 4000, and -T AUTO. The phylogenetic tree was then visualized through the use of an online tool (iTOL) [21].
Conserved domain, gene structure and motif
To clarify the Sox gene structure and exon details, a general feature format file (GFF) was utilized. Prediction of the conserved motifs within the Sox genes was achieved through the application of MEME [22], with the following parameters: a ceiling of 20 motifs, a minimum motif length of 6, a maximum motif length of 50, and default settings for all remaining parameters. Both the conserved motifs and the gene structure were graphically represented using TBtools v2.096 [18]. Furthermore, the conserved domains of Sox genes were identified utilizing the Batch SMART plug-in within TBtools v2.096 [18], and the results were visualized through the iTOL online tool [21].
Expression profiling of Sox genes in different echinoderms
To investigate the spatiotemporal expression patterns of Sox genes in echinoderms, publicly accessible RNA-seq data for S. purpuratus, A. japonicus, and H. leucospilota were retrieved from the NCBI SRA database (refer to Data availability). Subsequently, Fastp software [20], with default parameters, was used to filter the raw RNA sequencing reads. Next, the genome was indexed, and the filtered reads were aligned utilizing HISAT2 [23]. After converting the resulting Sam files to Bam files and sorting them with SAMtools [24], the TPM value for each gene was calculated by StringTie v2.2.0 [25] according to the gff file. The TPM values were categorized as follows: <2, no expression; <20, very low expression; <100, low expression; <500, moderate expression; <2500, high expression; and < 12,500, very high expression. Finally, heatmaps depicting the gene expression levels were created using the R package ggplot2 [26]. Additionally, the available single-cell sequencing data from S. purpuratus [27] were downloaded (GEO: GSE149221) and analyzed to better elucidate the expression pattern of the Sox genes during early development.
Results
Identification of Sox genes in echinoderms
A comprehensive analysis of 11 representative echinoderms yielded the discovery of a set of 70 Sox genes. For reference purposes, the complete amino acid sequences of these Sox genes are listed in Supplementary Table S2. Across the various species examined, the number of Sox genes observed varied from 5 to 8. Moreover, the characteristics of all the identified Sox proteins are comprehensively outlined in Table 1. The findings revealed significant differences in the biophysical properties of these Sox proteins. Specifically, the amino acid (AA) length of these proteins varies widely, ranging from 114 to 1367 residues. Similarly, the molecular weight (MW) also exhibited a broad spectrum, falling within the range of 13329.97 to 149705.86 Da. Additionally, the protein instability index (PI) values varied significantly, ranging from 5.20 to 10.70. Notably, the majority of the Sox proteins analyzed demonstrated instability indices exceeding 40, indicating their inherent instability.
Phylogenetic tree of the Sox proteins from echinoderms and other animals
A phylogenetic tree including Sox protein sequences obtained from both vertebrates and invertebrates was constructed to investigate the evolutionary relationships among Sox genes in echinoderms. As shown in Fig. 1, the 70 Sox genes from echinoderms were divided into 7 classes: the SoxB1 class, SoxB2 class, SoxC class, SoxD class, SoxE class, SoxF class and SoxH class. Within the SoxB1, SoxB2, and SoxF classes, 11 genes were identified from 11 echinoderms. The SoxC class comprises 9 Sox genes derived from 9 echinoderms, excluding A. japonica and P. borealis. Similarly, a SoxD class was formed by 9 Sox genes from 9 echinoderms. Additionally, the SoxE class included 11 Sox genes isolated from 10 echinoderms. Notably, Sox genes belonging to the SoxH class were specifically identified in sea cucumbers and starfish.
Gene structures and conserved motifs of Sox genes
The exon‒intron variation among the Sox genes of echinoderms is distinctly portrayed in Fig. 2. The exon counts of the Sox genes, which varied from 1 to 8 within the same class of 11 echinoderms, displayed a significant degree of similarity in their exon‒intron configurations. This observation suggested the existence of conserved patterns among distinct subsets of the Sox family. Furthermore, all the predicted Sox proteins contained motif 1, which suggests that this motif is a common functional element shared by members of this gene family. Proteins within the same class also display greater similarity in their motif structural features, further highlighting the conservation of specific characteristics among related Sox proteins. Additionally, some Sox genes were found to contain coiled-coil regions, low-complexity regions, and internal repeats (Fig. 3).
Spatiotemporal expression of sox genes in three echinoderms
RNA-seq datasets from different developmental stages and adult tissues of S. purpuratus were analyzed to investigate the expression patterns of different Sox genes. As illustrated in Fig. 4, the expression level of SoxB1 was particularly prominent during the early development stage, after which it gradually decreased from the initial stage of unfertilized eggs. SoxB2 exhibited a similar expression pattern to SoxB1, albeit with a reduced expression level at the corresponding developmental stage. The expression of SoxC initially increased, followed by a subsequent decrease, beginning at the unfertilized egg stage. Conversely, SoxD and SoxE maintained low expression levels during the early developmental stages. Notably, the primary expression phase of SoxF occurred between late gastrula and the pluteus. These results were verified at the single-cell level (Figure S1). For example, the expression of SoxB1 was prominent across specific clusters (7–10) from early time points, including the 8-cell stage to the early blastula stage (Figure S2), which is very similar to that previously reported for SoxB2 [28]. In addition, SoxC was rarely expressed during the 8-cell stage and 64-cell stage but later exhibited expanded expression across different clusters from the morula stage (Figure S3). Furthermore, at the adult stage, SoxB1 and SoxB2 exhibited the highest expression levels in the ovary, whereas SoxF demonstrated peak expression in the testis. Additionally, SoxC, SoxD, and SoxE exhibited consistently low expression across all tissues examined.
In A. japonicus (as depicted in Fig. 5), SoxB1, SoxB2, and SoxD exhibited similar expression trends. However, notably, the expression levels of SoxB2 and SoxD were significantly lower than those of SoxB1. Additionally, the expression of SoxC was particularly pronounced during the gastrula and doliolaria stages, surpassing its expression in other developmental stages. On the other hand, SoxF demonstrated a greater expression level specifically in the pentactula stage than in the other developmental stages. It was also observed that the expression of Sox genes decreased gradually from the initial stage in unfertilized eggs. At the adult stage, SoxB1 presented the highest expression in the ovary and spine, but SoxB2 and SoxF exhibited the highest expression levels in the back epidermis and nerve ring, respectively. Intriguingly, SoxH displayed high expression specifically in the testis, with no detectable expression in other tissues. Furthermore, SoxC, SoxD, and SoxE maintained consistently low expression levels across all tissues examined.
The analysis of Sox gene expression across various tissues of H. leucospilota revealed distinct patterns (Fig. 6). Specifically, SoxB1, SoxB2, SoxC and SoxE exhibited low or even no expression across all tissues examined. Conversely, SoxF exhibited a widespread moderate expression pattern and was prominently expressed in multiple tissues, such as coelomocytes, vessels, respiratory trees, rete mirabile, polian vesicles, muscle, body walls, and ovaries. Additionally, SoxH was significantly expressed specifically in the testis.
Discussion
Comprehensive identification of Sox family genes has been conducted across diverse animal groups [29,30,31]. However, the understanding of Sox genes in aquatic invertebrates remains limited. Despite the availability of echinoderm genome sequences for several years, a thorough investigation of Sox genes in these organisms has yet to be undertaken. In the present study, a comprehensive analysis of Sox genes was carried out across different echinoderms. This investigation revealed the presence of five to seven Sox genes across different echinoderms. Based on previous research, the variation observed in the number of Sox family genes can be ascribed to disparities in genome size and the occurrence rate of genomic duplication events [32]. Despite their ubiquitous presence across the animal kingdom, Sox genes exhibit unique species-specific traits. For example, SoxA and SoxG are exclusively found in mammals. This pattern was confirmed in this study. No SoxA or SoxG genes were detected in echinoderms, while the SoxB, SoxC, SoxD, SoxE, SoxF and SoxH genes were detected in this study. Similar results were reported in a previous study in which a single C, D, E, F and H and two SoxB proteins were identified in Ciona [28]. In addition, the SoxB1, SoxB2 and SoxF genes were found in all the studied echinoderms, which suggested that these genes may be conserved in echinoderms.
Unlike certain fish species that possess four SoxB1 paralogs (Sox1a, Sox1b, Sox2, and Sox3), all echinoderms investigated in this study exhibited a single SoxB1 gene, suggesting that the SoxB1 gene is conserved within the echinoderm lineage. Previous research has demonstrated that the SoxB1 gene plays a pivotal role in the initial stages of embryonic development [33,34,35]. In particular, SoxB1 has been proven to be a crucial factor in the initiation of the zygotic developmental program [36]. In this study, the ApjSoxB1 gene was highly expressed in the zygote stage of sea cucumbers. These results indicated that SoxB1 may perform similar functions in echinoderms. Notably, the expression level of SoxB1 in the ovaries of the three echinoderms was significantly greater than that in the testis. Similar results have been reported for L. vannamei [37]. Thus, it would be intriguing to explore whether SoxB1 plays important roles in the oogenesis of echinoderms.
It is believed that the SoxB1 and SoxB2 genes emerged through the tandem duplication of a genomic segment harboring the putative ancestral SoxB gene [38]. SoxB2 has been extensively studied in invertebrates. For instance, the SoxB2 gene plays a crucial role in the maturation of the sperm nucleus in Eriocheir sinensis [39]. A similar function can also be found in scallops [40]. In contrast, the present investigation revealed that SoxB2 gene expression was absent or present at minimal levels in the testes of the three echinoderms examined. In addition, previous studies showed that SoxB2 can function in neurogenesis, ciliogenesis and skeletal patterning in sea urchins [41]. These results suggested that SoxB2 may have different functions in echinoderms. Furthermore, in this study, the spatial and temporal expression patterns of SoxB2 in sea cucumbers were very similar to those in sea urchins. Therefore, SoxB2 may have a conserved function in echinoderms.
In mammals, SoxC genes participate in neural and mesenchymal progenitor cell survival, in part by activating this transcriptional intermediary of the Hippo signaling pathway [42]. Although SoxC has been identified in some aquatic invertebrates, little research has investigated its function. A previous study showed that SoxB2 and SoxC orthologs play a consistent role in the early neural specification of sea urchins [43]. In this study, the expression of SoxC genes in different echinoderms was similar in early development, and the expression level was the highest in the nerve tissue of sea cucumber and sea urchin at the adult stage. Therefore, SoxC genes may play a conserved neurogenic role in echinoderms. Similarly, SoxD and SoxE have been shown to be involved in neurodevelopmental processes [44,45,46,47]. However, in the present study, the expression patterns of SoxD and SoxE were different from that of SoxC. Therefore, the functions of SoxD and SoxE in echinoderms need further study.
SoxH genes, which were previously thought to be mammalian specific, have been identified in several invertebrates, including ascidians [28], oysters [48], clams [49], scallops [9], and abalone [50]. SoxH usually has male-biased expression in these mollusks. The current study revealed comparable expression patterns in both H. leucospilota and A. japonicus, indicating that SoxH may play a role in determining or facilitating male sexual development in starfish and sea cucumber. Furthermore, these observations suggest that the function of SoxH may be conserved across invertebrates and vertebrates. In vertebrates, SoxF has been found to be associated with vascular development [51, 52]. In addition, SoxF is part of a negative feedback loop in the wingless pathway that controls proliferation in Drosophila wing discs [53]. However, to date, the function of the SoxF gene in aquatic invertebrates remains unclear. In the present study, SoxF was ubiquitously expressed in early developmental stage and adult tissues. A similar result was found in the Pacific abalone Haliotis discus hannai [50]. These results suggest that the SoxF gene has diverse functions in aquatic invertebrates. In general, the present investigation provides a molecular foundation for exploring the Sox gene in echinoderms, providing a valuable resource for future phylogenetic and genomic studies.
Conclusion
In this study, a systematic analysis of Sox family genes in 11 echinoderms was performed. A total of 70 Sox genes were found, and the number of Sox genes in different echinoderms ranged from 5 to 8. All Sox genes from echinoderms were classified into 7 classes: the SoxB1 class, SoxB2 class, SoxC class, SoxD class, SoxE class, SoxF class and SoxH class. Furthermore, the spatiotemporal expression of Sox genes from three echinoderms suggested that different Sox family members have different functions. Notably, SoxH may play a crucial role in the testis development of starfish and sea cucumber, while SoxB1 is likely involved in echinoderm ovary development. In general, the present investigation provides a molecular foundation for exploring the Sox gene in echinoderms, providing a valuable resource for future phylogenetic and genomic studies.
Data availability
The datasets generated and/or analyzed during the current study are available in the NCBI [GCA_001949145.1, GCA_011630105.1, GCA_002754855.1, GCA_902459465.3, GCA_025617745.1, GCA_025618425.1, GCA_029531755.1, GCA_018143015.1, GCA_015706575.1, GCA_021014325.1, GCA_000002235.4, PRJNA81157, PRJNA413998, PRJNA646282, and PRJNA747844].
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Acknowledgements
This work was supported by the High-Performance Computing Platform of Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences.
Funding
This work was supported by the Natural Science Foundation of Shandong Province [ZR2021QD158, ZR2021MC151], the Open Project Program of Key Laboratory of Ecological Warning, Protection & Restoration for Bohai Sea, Ministry of Natural Resources [2022204], and the Scientific Research Project of Yantai Vocational College [2023XBZD003].
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Q.C.W. and T.G.C. conducted the experiments and data processing. Q.C.W. and X.J.L. conceived and supervised the project. X.J.L., H.L. and L.H.F. contributed to the data collection. All authors reviewed the manuscript.
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Li, X., Cao, T., Liu, H. et al. Identification and expression analysis of Sox family genes in echinoderms. BMC Genomics 25, 655 (2024). https://doi.org/10.1186/s12864-024-10547-0
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DOI: https://doi.org/10.1186/s12864-024-10547-0