Genome-wide identification, evolution of histone lysine demethylases (KDM) genes and their expression during gonadal development in Nile tilapia

Histone lysine demethylases (KDM) are responsible for histone demethylation and are involved in gene expression regulation. Previous studies have shown that histone lysine demethylation plays an important role in gonadal development of vertebrates. The KDM family consists of eight subfamilies, i.e., kdm1, kdm2, kdm3, kdm4, kdm5, kdm6, kdm7 and JmjC-only subfamily. In this study, 13 to 63 KDM genes in 23 representative species were identified based on the available version of genome assembly. Phylogenetic relationships, domain architecture, and synteny of these genes were comprehensively analyzed and the results suggested KDM genes probably originated from the early diverging metazoan and significantly expanded in vertebrates with multiple whole genome duplication, especially in the third-round whole genome duplication (3R-WGD) and polyploidization of teleosts. The subfamilies of kdm2, kdm3, kdm4, kdm5, kdm6 and kdm7 were duplicated with 1R-2R events, and duplicates of kdm2a, kdm4a, kdm5b and kdm6b were resulted from 3R-WGD. Based on transcriptome data, the KDM genes were found to be dominantly expressed in the ovary and testis. More than 80% of KDM genes displayed sexual dimorphic expression, with 15 genes dominantly expressed in ovaries, and 12 genes dominantly expressed in testes. Importantly, from transcriptome data, qRT-PCR and fluorescence in situ hybridization during sex reversal, genes with higher expression in ovary than testis, such as kdm1b and two JmjC-only subfamily members hspbap1 and riox1, were downregulated, while other genes, such as kdm3c, kdm5bb, kdm6ba, kdm6bb and kdm7b, with higher expression in testis than ovary, were upregulated in ovotestis, indicating these genes play critical roles in the gonadal development and sex reversal. This study provided new insights into the evolution of the KDM genes and a fundamental clue for understanding their important roles in sex differentiation and gonadal development in teleosts.