Crosstalk between sex-related genes and apoptosis signaling reveals molecular insights into sex change in a protogynous hermaphroditic teleost fish, ricefield eel Monopterus albus

Abstract

The ricefield eel Monopterus albus is a protogynous hermaphroditic synbranchiform species that undergoes sequential sex change from female to male, offering an interesting model for study in the mechanisms of sequential hermaphroditism in vertebrates. To explore the expression patterns and molecular mechanisms of key genes underlying sex change in the ricefield eel M. albus, a comprehensive study of the transcriptomes of gonads at five sexual stages (ovary, early intersexual stage gonad, middle intersexual stage gonad, late intersexual stage gonad, and testis) was performed. In total, 107,260,808 raw reads and 101,886,556 clean reads were obtained, and 41,216 genes were detected in the gonad tissues. The expression levels of 21 differentially expressed genes were verified by quantitative real-time PCR (qRT-PCR) and found to be in accordance with the RNA-seq data, suggesting that the RNA-seq data were reliable. Furthermore, the expression of female-related genes decreased as sex change progressed, whereas male-related genes exhibited the opposite expression patterns. Notably, apoptosis-related genes had close relationships with sex change, including genes associated with endocytosis, calcium signaling pathways, and 7 other pathways. In particular, apoptosis signaling was delivered to the p53 network, which may be associated with sex change. Importantly, tgfb3, fshr, camk4 and calmodulin may be the key genes, which helps balance germ cell apoptosis and proliferation during sex change. These results reveal specific molecular signatures in the gonad that are related to sex change and apoptosis signaling, which will be useful for enhancing our understanding of sequential hermaphroditism and sex change in the ricefield eel M. albus and other teleost.