Skip to main content
Download PDF

Identification and expression analysis of Sox family genes in echinoderms

BMC Genomics volume 25, Article number: 655 (2024) Cite this article

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.

Peer Review reports

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.

Table 1 Protein sequence features of the identified sox genes in echinoderms
Full size table

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.

Fig. 1
figure 1

Phylogenetic tree of SOX protein sequences

Full size image

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).

Fig. 2
figure 2

Motif composition and exon‒intron structures of echinoderm Sox genes

Full size image
Fig. 3
figure 3

Conserved domain structures of Sox genes

Full size image

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.

Fig. 4
figure 4

Sox gene expression patterns at different developmental stages and in different adult tissues of Strongylocentrotus purpuratus

Full size image

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.

Fig. 5
figure 5

Sox gene expression patterns at different developmental stages and in different adult tissues of Apostichopus japonicus

Full size image

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.

Fig. 6
figure 6

Sox gene expression patterns in different adult tissues of Holothuria leucospilota

Full size image

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].

References

  1. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Münsterberg A, Vivian N, Goodfellow P, Lovell-Badge R. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature. 1990;346(6281):245–250.

    Article  CAS  PubMed  Google Scholar 

  2. Cui J, Shen X, Zhao H, Nagahama Y. Genome-wide analysis of Sox genes in Medaka (Oryzias latipes) and their expression pattern in embryonic development. Cytogenet Genome Res. 2011;134(4):283–294.

  3. Abdullah M, Rehman MS-u, Rehman MSN-u, AlKahtane AA, Al-Hazani TM. Hassan F-u, Rehman Su: genome-wide identification, evolutionary and mutational analysis of the Buffalo Sox Gene Family. Animals. 2023;13(14):2246.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Schepers GE, Teasdale RD, Koopman P. Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev Cell. 2002;3(2):167–170.

    Article  CAS  PubMed  Google Scholar 

  5. Ma F, Zou Y, Ma R, Chen X, Ma L. Evolution, characterization and expression analysis of sox gene family in rainbow trout (Oncorhynchus mykiss). Czech J Anim Sci 2022, 67(4):157-166.

  6. Wei L, Yang C, Tao W, Wang D. Genome-wide identification and transcriptome-based expression profiling of the Sox Gene Family in the Nile Tilapia (Oreochromis niloticus). Int J Mol Sci. 2016;17(3):270.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Liu F, Zhou L, Zhang J, Wang Y, Wang Z, Liu X, Cai M. Genome-wide identification and transcriptome‐based expression profiling of the Sox gene family in the spinyhead croaker (Collichthys lucidus). J Fish Biol. 2022;100(1):15–24.

    Article  CAS  PubMed  Google Scholar 

  8. Hu Y, Wang B, Du H. A review on sox genes in fish. Reviews Aquaculture. 2021;13(4):1986–2003.

    Article  Google Scholar 

  9. Yu J, Zhang L, Li Y, Li R, Zhang M, Li W, Xie X, Wang S, Hu X, Bao Z. Genome-wide identification and expression profiling of the SOX gene family in a bivalve mollusc Patinopecten yessoensis. Gene. 2017;627:530–537.

  10. Crémazy F, Berta P, Girard F. Genome-wide analysis of sox genes in Drosophila melanogaster. Mech Dev. 2001;109(2):371–375.

  11. Satoh N, Rokhsar D, Nishikawa T. Chordate evolution and the three-phylum system. Proc Royal Soc B: Biol Sci. 2014;281(1794):20141729.

    Article  Google Scholar 

  12. Wang Y, Yang Y, Li Y, Chen M. Identification of sex determination locus in sea cucumber Apostichopus japonicus using genome-wide association study. BMC Genomics. 2022;23(1):1–14.

    PubMed  PubMed Central  Google Scholar 

  13. Cui Z, Zhang J, Sun Z, Liu B, Han Y, Zhao C, Chang Y. Testis-specific expression pattern of dmrt1 and its putative regulatory region in the sea urchin (Mesocentrotus Nudus). Comp Biochem Physiol B-Biochem Mol Biol. 2022;257:110668.

    Article  CAS  PubMed  Google Scholar 

  14. Slota LA, Miranda EM, McClay DR. Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus. EvoDevo. 2019;10(1):2.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Eddy SR. Profile hidden Markov models. Bioinf (Oxford England). 1998;14(9):755–763.

    CAS  Google Scholar 

  16. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–410.

    Article  CAS  PubMed  Google Scholar 

  17. Bowles J, Schepers G, Koopman P. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol. 2000;227(2):239–255.

    Article  CAS  PubMed  Google Scholar 

  18. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13(8):1194–1202.

    Article  CAS  PubMed  Google Scholar 

  19. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nguyen L-T, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–274.

    Article  CAS  PubMed  Google Scholar 

  21. Letunic I, Bork P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47(W1):W256–259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Bailey TL, Johnson J, Grant CE, Noble WS. The MEME suite. Nucleic Acids Res. 2015;43(W1):W39–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078–2079.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33(3):290–295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. R core team. R: A language and environment for statistical computing. 2013.

  27. Foster S, Oulhen N, Wessel G. A single cell RNA sequencing resource for early sea urchin development. Development 2020, 147(17):dev191528.

  28. Heenan P, Zondag L, Wilson MJ. Evolution of the Sox gene family within the chordate phylum. Gene. 2016;575(2):385–392.

    Article  CAS  PubMed  Google Scholar 

  29. Akinyemi MO, Finucan J, Grytsay A, Osaiyuwu OH, Adegbaju MS, Ogunade IM, Thomas BN, Peters SO, Morenikeji OB. Molecular evolution and inheritance pattern of sox gene family among Bovidae. Genes. 2022;13(10):1783.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Voldoire E, Brunet F, Naville M, Volff J-N, Galiana D. Expansion by whole genome duplication and evolution of the sox gene family in teleost fish. PLoS ONE. 2017;12(7):e0180936.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Wei L, Cheng D, Li D, Meng M, Peng L, Tang L, Pan M, Xiang Z, Xia Q, Lu C. Identification and characterization of Sox genes in the silkworm, Bombyx mori. Mol Biol Rep. 2011;38:3573–3584.

  32. Xu S, Zhang S, Zhang W, Liu H, Wang M, Zhong L, Bian W, Chen X. Genome-Wide Identification, Phylogeny, and Expression Profile of the Dmrt (Doublesex and Mab-3 Related Transcription Factor) Gene Family in Channel Catfish (Ictalurus punctatus). In: Front Genet vol. 13; 2022: 891204.

  33. Rizzoti K, Brunelli S, Carmignac D, Thomas PQ, Robinson IC, Lovell-Badge R. SOX3 is required during the formation of the hypothalamo-pituitary axis. Nat Genet. 2004;36(3):247–255.

    Article  CAS  PubMed  Google Scholar 

  34. Miya T, Nishida H. Expression pattern and transcriptional control of SoxB1 in embryos of the ascidian Halocynthia roretzi. Zool Sci. 2003;20(1):59–67.

    Article  CAS  Google Scholar 

  35. Angerer LM, Newman LA, Angerer RC. SoxB1 downregulation in vegetal lineages of sea urchin embryos is achieved by both transcriptional repression and selective protein turnover. 2005. 132(5): 999–1008.

  36. Lee MT, Bonneau AR, Takacs CM, Bazzini AA, DiVito KR, Fleming ES, Giraldez AJ. Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. Nature. 2013;503(7476):360–364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Yao C, Wan H, Zhang Z, Lin J, Wang Y. Genome-wide identification and expression profile of the sox gene family in different tissues and during embryogenesis in the Pacific white shrimp (Litopenaeus vannamei). Gene. 2020;763:144956.

    Article  CAS  PubMed  Google Scholar 

  38. Kamachi Y. Chap. 6 - Evolution of Sox2 and Functional Redundancy in Relation to Other SoxB1 Genes. In: Sox2 Edited by Kondoh H, Lovell-Badge R. Boston: Academic Press; 2016: 89–106.

  39. Liu ZQ, Jiang XH, Qi HY, Xiong LW, Qiu GF. A novel SoxB2 gene is required for maturation of sperm nucleus during spermiogenesis in the Chinese mitten crab, Eriocheir sinensis. Sci Rep. 2016;6(1):32139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Liang S, Liu D, Li X, Wei M, Yu X, Li Q, Ma H, Zhang Z, Qin Z. SOX2 participates in spermatogenesis of Zhikong scallop Chlamys farreri. Sci Rep. 2019;9(1):76.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Anishchenko E, Arnone MI, D’Aniello S. SoxB2 in sea urchin development: implications in neurogenesis, ciliogenesis and skeletal patterning. EvoDevo. 2018;9(1):5.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Bhattaram P, Penzo-Méndez A, Sock E, Colmenares C, Kaneko KJ, Vassilev A, DePamphilis ML, Wegner M, Lefebvre V. Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat Commun. 2010;1(1):9.

    Article  PubMed  Google Scholar 

  43. Burke RD, Moller DJ, Krupke OA, Taylor VJ. Sea urchin neural development and the metazoan paradigm of neurogenesis. Genesis. 2014;52(3):208–221.

    Article  PubMed  Google Scholar 

  44. Li L, Medina-Menéndez C, García-Corzo L, Córdoba-Beldad CM, Quiroga AC, Barca EC, Zinchuk V, Muñoz-López S, Rodríguez-Martín P, Ciorraga M. SoxD genes are required for adult neural stem cell activation. Cell Rep 2022, 38(5):110313.

  45. Mizuseki K, Kishi M, Shiota K, Nakanishi S, Sasai Y. SoxD: an essential mediator of induction of anterior neural tissues in Xenopus embryos. Neuron. 1998;21(1):77–85.

    Article  CAS  PubMed  Google Scholar 

  46. Stolt CC, Wegner M. SoxE function in vertebrate nervous system development. Int J Biochem Cell Biol. 2010;42(3):437–440.

    Article  CAS  PubMed  Google Scholar 

  47. McCauley DW, Bronner-Fraser M. Importance of SoxE in neural crest development and the evolution of the pharynx. Nature. 2006;441(7094):750–752.

    Article  CAS  PubMed  Google Scholar 

  48. Zhang N, Xu F, Guo X. Genomic analysis of the Pacific oyster (Crassostrea gigas) reveals possible conservation of vertebrate sex determination in a mollusc. G3: Genes Genomes Genet. 2014;4(11):2207–2217.

  49. Ghiselli F, Milani L, Chang PL, Hedgecock D, Davis JP, Nuzhdin SV, Passamonti M. De novo assembly of the Manila clam ruditapes philippinarum transcriptome provides new insights into expression bias, mitochondrial doubly uniparental inheritance and sex determination. Mol Biol Evol. 2012;29(2):771–786.

    Article  CAS  PubMed  Google Scholar 

  50. Zhang Q, Huang J, Fu Y, Chen J, Wang W. Genome-wide identification and expression profiles of sex-related gene families in the Pacific abalone Haliotis discus hannai. Comp Biochem Physiol D-Genomics Proteom. 2024;50:101205.

    Article  CAS  Google Scholar 

  51. Zhou Y, Williams J, Smallwood PM, Nathans J. Sox7, Sox17, and Sox18 cooperatively regulate Vascular Development in the Mouse Retina. PLoS ONE. 2015;10(12):e0143650.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Francois M, Koopman P, Beltrame M. SoxF genes: key players in the development of the cardio-vascular system. Int J Biochem Cell Biol. 2010;42(3):445–448.

    Article  CAS  PubMed  Google Scholar 

  53. Dichtel-Danjoy M-L, Caldeira J, Casares F. SoxF is part of a novel negative-feedback loop in the wingless pathway that controls proliferation in the Drosophila wing disc. 2009;136 (5):761–769.

Download references

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].

Author information

Authors and Affiliations

  1. Yantai Vocational College, Yantai, 264003, China

    Xiaojing Li & Longhai Fu

  2. Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, 264003, China

    Tiangui Cao, Hui Liu & Quanchao Wang

  3. Key Laboratory of Ecological Warning, Protection & Restoration for Bohai Sea, Ministry of Natural Resources, Qingdao, 266061, China

    Quanchao Wang

Authors
  1. Xiaojing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tiangui Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Longhai Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Quanchao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to Quanchao Wang.

Ethics declarations

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Ethical guidelines

Not applicable.

Ethical approval and consent to participate

Not applicable.

Additional information

Publisher’s Note

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

Electronic supplementary material

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12864-024-10547-0

Keywords

BMC Genomics

ISSN: 1471-2164

Contact us