DNA methylation modification is associated with gonadal differentiation in Monopterus albus

Abstract

Background Both testis and ovary can be produced sequentially in an individual with the same genome when sex reversal occurs in the teleost Monopterus albus, and epigenetic modification is supposed to be involved in gonadal differentiation. However, DNA methylation regulation mechanism underlying the gonadal differentiation remains unclear. Results Here, we used liquid chromatography-electrospray ionization tandem mass spectrometry (LC–ESI–MS/MS) to simultaneously determine endogenous levels of both 5-methyl-2′-deoxycytidine (m5dC) and 5-hydroxymethyl-2′-deoxycytidine (hm5dC) during gonadal differentiation. Overall DNA methylation level was upregulated from ovary to testis via ovotestis. As a de novo methylase, dnmt3aa expression was also upregulated in the process. Notably, we determined transcription factor Foxa1 for dnmt3aa gene expression. Site-specific mutations and chromatin immunoprecipitation showed that Foxa1 can bind to and activate the dnmt3aa promoter. Furthermore, DNA methylation levels of key genes foxl2 (forkhead box L2) and cyp19a1a (cytochrome P450, family 19, subfamily A, polypeptide 1a) in regulation of female hormone synthesis were consistently upregulated during gonadal differentiation. Conclusions These data suggested that dynamic change of DNA methylation modification is associated with gonadal differentiation.

Comprehensive analysis of genome‐wide DNA methylation and transcriptomics between ovary and testis in Monopterus albus

“…Overall, the methylation level of the gonads of ricefield eel is lower than in the two fish. Moreover, our analyses revealed that the C methylation level in the genome level increases during sex reversal from female to male in ricefield eel, which is consistent with liquid chromatography‐electrospray ionization tandem mass spectrometry results (Wang et al, 2020). Specifically, the CG methylation level within 3000 bp upstream of the start codon is higher in the testis (49.51%) than in the ovary (47.89%).…”

Integrated chromatin accessibility and DNA methylation analysis to reveal the critical epigenetic modification and regulatory mechanism in gonadal differentiation of the sequentially hermaphroditic fish, Monopterus albus

“…M. albus is a hermaphroditic fish whose sex changes from female through intersex to male during its life cycle [5]. Recently, many studies from various perspectives were conducted to analyse the mechanism of sex reversal and abundant data were generated that support their insight [6][7][8][9]. However, the underlying mechanism of sex reversal remains unclear.…”

Dnmt3aa but Not Dnmt3ab Is Required for Maintenance of Gametogenesis in Nile Tilapia (Oreochromis niloticus)

“…In Nile tilapia and bluehead wrasse ( Thalassoma bifasciatum ), the expressions of dnmt3aa and dnmt3ab are significantly higher in the testes than in the ovaries, and significantly increased during the sex reversal from female to male induced by Fadrozole [ 26 ] or social cues [ 27 , 28 ]. In ricefield eel, dnmt3aa and dnmt3ab are highly expressed in spermatocytes of testes, with the expression of dnmt3aa significantly increased during the female to male sex reversal [ 25 , 29 ]. These studies suggest that dnmt3aa and dnmt3ab may play important roles in the gonadal development of fish; however, their detailed expression profiles during the sex determination and differentiation and gonadal development of teleosts are unclear.…”