Abstract
Doublesex and mab-3-related transcription factor (dmrt) genes are widely distributed across various biological groups and play critical roles in sex determination and neural development. Here, we applied bioinformatics methods to exam cross-species changes in the dmrt family members and evolutionary relationships of the dmrt genes based on genomes of 17 fish species. All the examined fish species have dmrt1–5 while only five species contained dmrt6. Most fish harbored two dmrt2 paralogs (dmrt2a and dmrt2b), with dmrt2b being unique to fish. In the phylogenetic tree, 147 DMRT are categorized into eight groups (DMRT1–DMRT8) and then clustered in three main groups. Selective evolutionary pressure analysis indicated purifying selections on dmrt1–3 genes and the dmrt1–3–2(2a) gene cluster. Similar genomic conservation patterns of the dmrt1–dmrt3–dmrt2(2a) gene cluster with 20-kb upstream/downstream regions in fish with various sex-determination systems were observed except for three regions with remarkable diversity. Synteny analysis revealed that dmrt1, dmrt2a, dmrt2b, and dmrt3–5 were relatively conserved in fish during the evolutionary process. While dmrt6 was lost in most species during evolution. The high conservation of the dmrt1–dmrt3–dmrt2(2a) gene cluster in various fish genomes suggests their crucial biological functions while various dmrt family members and sequences across fish species suggest different biological roles during evolution. This study provides a molecular basis for fish dmrt functional analysis and may serve as a reference for in-depth phylogenomics.
Highlights
Doublesex and Mab-3-related transcription factor genes are originally homologous to Doublesex (Dsx) in Drosophila melanogaster and Male abnormal 3 (Mab-3) in Caenorhabditis elegans, both of which play important roles in sex determination (Burtis and Baker, 1989; Zhu et al, 2000; Zarkower, 2001)
Seven dmrt genes have been identified in fish to date, including dmrt1–6 and dmrt2b. dmrt genes have been reported in more than 30 fish species and a number of functional studies have been performed to reveal that regardless of the sex determination mechanism, the majority of fish dmrt genes (Table 3) are related to sexual development (Li et al, 2008, 2018; Liu et al, 2009; Herpin and Schartl, 2011; Yoshizawa et al, 2011; Xu et al, 2013)
Based on the cross-species comparisons of dmrt family genes and copy numbers, we found that some of the dmrt genes were duplicated in S. salar and A. japonica (S. salar: dmrt2, 3, 5; A. japonica: dmrt1–3; see Table 1)
Summary
Doublesex and Mab-3-related transcription factor (dmrt) genes are originally homologous to Doublesex (Dsx) in Drosophila melanogaster and Male abnormal 3 (Mab-3) in Caenorhabditis elegans, both of which play important roles in sex determination (Burtis and Baker, 1989; Zhu et al, 2000; Zarkower, 2001). The mouse dmrt gene is expressed in the testis and ovary, in addition to other various tissues (Kim et al, 2003) It can regulate the formation and development of ovarian follicles (Balciuniene et al, 2006). We employed the fine genomic map of largemouth bass recently obtained using third-generation sequencing by our team and collected the dmrt sequences of 16 fish species with different taxonomic positions from published whole-genome sequences, in order to analyze the sequence structure, phylogenetic relationship, sequence conservation, and synteny of members of the fish dmrt family These findings will lay a solid foundation for a more systematic understanding of the structural characteristics of these members in fish dmrt family, and for further investigations into the different functions of fish dmrt family members in sex determination or differentiation along with their underlying mechanisms
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