New Insights Into the Role of Follicle-Stimulating Hormone in Sex Differentiation of the Protogynous Orange-Spotted Grouper, Epinephelus coioides

Abstract

Follicle-stimulating hormone (FSH) signaling is considered to be essential for early gametogenesis in teleosts, but its functional roles during sex differentiation are largely unknown. In this study, we investigated the effects of long-term and short-term FSH injection on sex differentiation in the protogynous orange-spotted grouper ( Epinephelus coioides ). Long-term FSH treatment initially promoted the formation of ovaries but subsequently induced a male fate. The expression of female pathway genes was initially increased but then decreased, whereas the expression of male pathway genes was up-regulated only during long-term FSH treatment. The genes related to the synthesis of sex steroid hormones, as well as serum 11-ketotestosterone and estradiol, were also up-regulated during long-term FSH treatment. Short-term FSH treatment activated genes in the female pathway (especially cyp19a1a ) at low doses but caused inhibition at high doses. Genes in the male pathway were up-regulated by high concentrations of FSH over the short term. Finally, we found that low, but not high, concentrations of FSH treatment activated cyp19a1a promoter activities in human embryonic kidney (HEK) 293 cells. Overall, our data suggested that FSH may induce ovarian differentiation or a change to a male sex fate in the protogynous orange-spotted grouper, and that these processes occurred in an FSH concentration-dependent manner.

In vivoeffect of recombinant FSH and LH administered to meagre (Argyrosomus regius) at the initial stages of sex differentiation

“…These previous studies would indicate that the hormone and doses used were effective, although all these studies worked with fish at a more advanced stage of gametogenesis. Treatments with porcine FSH to orange-spotted grouper induced and accelerated sexual differentiation (Huang et al, 2019). A dose of 100 IU of porcine FSH accelerated differentiation into an ovary and then induced a sex change to testes.…”

“…Additionally, immunoreactivity against FSHb and LHb (beta protein of the gonadotropins) was not detected in the pituitary of the Malabar grouper, ( Epinephelus malabaricus ) during sexual differentiation suggesting that pituitary gonadotropins do not play a major role in sex differentiation (Murata et al, 2012). Consequentially, the role of FSH in sexual differentiation remains unclear (Huang et al, 2019) or is different in different fish species (Murozumi et al, 2014).…”

The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus

“…Hypothalamic and pituitary hormonal signals were also implicated in the regulation of gonadal sex change in hermaphrodite teleosts, including bluehead wrasse [ 61 , 62 ], honeycomb grouper [ 63 ], and the orange-spotted grouper [ 64 ]. In ricefield eels, the precocious sexual change could be induced by the administration of gonadotropin-releasing hormone analogue (sGnRH-A) [ 10 , 65 ] and ovine-luteinizing hormone (oLH) [ 66 ].…”

Single-cell RNA sequencing reveals gonadal dynamic changes during sex differentiation in hermaphroditic protogynous orange-spotted grouper (<i>Epinephelus coioides</i>)

“…The origin of germ cells and the reasons for this preference toward female-first maturation remain unknown and have long been of interest to scientists. Many genes are involved in sex differentiation ( Han et al, 2019 ; Huang et al, 2019 ; Sun et al, 2017 ), but the mechanism underlying sex differentiation in groupers remains unclear. Therefore, to better understand how sex differentiation is regulated at the cellular level, we performed scRNA-seq and revealed gene expression patterns in sex differentiation.…”