Dataset Information

Robust gdf9 and bmp15 expression in the oocytes of ovotestes through the Figla-independent pathway in the hermaphroditic black porgy, Acanthopagrus schlegelii.

ABSTRACT: More than 1,500 fish species are hermaphroditic, but no hermaphroditic lineage appears to be evolutionarily ancient in fishes. Thus, whether more than one sex at a time was present during the evolutionary shift from gonochorism to hermaphroditism in fishes is an intriguing question. Ectopic oocytes were created in the ovotestes of protandrous black porgy via the withdrawal of estradiol (E2) administration. These ectopic oocytes reprogrammed the surrounding cells, which changed from Sertoli cells to follicle-like cells. We observed that gdf9 and bmp15 expression was localized in the primary oocytes and gradually decreased after oocytes entered a secondary oocyte stage. Robust expression of gdf9 and bmp15 in ectopic oocytes was associated with the surrounding Sertoli cells. However, blocking Cyp19a1a activity and increasing androgen levels did not stimulate the expression of gdf9 and bmp15. Thus, the robust gdf9 and bmp15 expression was not related to the inappropriate male microenvironment. Furthermore, in vitro data demonstrated that gdf9 and bmp15 were not downstream genes of Figla signaling. Therefore, our results suggest that there are two independent mechanisms, a Figla-dependent pathway and a Figla-independent pathway, by which oocyte-surrounding cells are altered from a male somatic fate to a female somatic fate. This functional switch might clarify how oocytes created an appropriate microenvironment during the transition from the ancient gonochorism to the present hermaphroditism.

SUBMITTER: Wu GC

PROVIDER: S-EPMC5658113 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Robust gdf9 and bmp15 expression in the oocytes of ovotestes through the Figla-independent pathway in the hermaphroditic black porgy, Acanthopagrus schlegelii.

Wu Guan-Chung GC Luo Jia-Wun JW Li Hau-Wen HW Huang Chen-Hsiu CH Chang Ching-Fong CF

PloS one 20171026 10

More than 1,500 fish species are hermaphroditic, but no hermaphroditic lineage appears to be evolutionarily ancient in fishes. Thus, whether more than one sex at a time was present during the evolutionary shift from gonochorism to hermaphroditism in fishes is an intriguing question. Ectopic oocytes were created in the ovotestes of protandrous black porgy via the withdrawal of estradiol (E2) administration. These ectopic oocytes reprogrammed the surrounding cells, which changed from Sertoli cells ...[more]

PMID: 29073214

Similar Datasets

Project description:High nutritional value and the development of efficient biotechnological methods of controlled production have made black porgy (Acanthopagrus schlegelii) an economically important fish in Chinese aquaculture in recent years. However, aquaculture production of the species faces multiple issues associated with reduced growth rate, low reproduction ability, and high mortality during production, which are associated with the species' limited tolerance to low temperatures. To date, comprehensive information on the genetic-based mechanisms of cold tolerance and adaptation to low temperature in the species are still unavailable. In this study, the HiSeq™2500 (Illumina) sequencing platform was used to analyze the transcriptomic profile of the liver tissue in the black porgy subjected to different extents of cold shock, including a control temperature group (AS, T = 15 °C), an intermediate temperature group (AL1, T = 10 °C), and an acute low-temperature stress group (AL2, T = 5 °C). For this purpose, three standardized cDNA libraries of AS, AL1, and AL2 were established. We obtained 43,258,908, 48,239,072, and 38,983,833 clean reads from the AS group, AL1 group, and AL2 group, respectively. After pairwise comparison, 70 differentially expressed genes (DEGs) were identified in the examined fish groups. Among them, 60 genes were found to be significantly differentially expressed after trend analysis. GO annotation and enrichment results showed that they were mainly enriched into three categories: biological processes (12 subcategories), molecular functions (7 subcategories), and cellular components (7 subcategories). KEGG analysis results indicated that all significantly differentially expressed genes were annotated to 102 signaling pathways, including biological rhythm, cholesterol metabolism, glycerolipid metabolism, animal autophagy, FoxO signaling pathway, steroid biosynthesis, and regulation of adipocyte lipolysis and apoptosis. Four of them, namely: G6PC, GPX1, GCK, and HSPE1 were randomly selected for further qRT-PCR verification of data reliability obtained by RNA-Seq technology. In this study, we found that environmental acute cold stress mainly affected the black porgy's biological processes related to metabolism, apoptosis, and signal transduction. The data that we have reported provides baseline information for further studies concerning the genetic responses of the black porgy under cold stress conditions, the improvement of its aquaculture production, and other economically important matters regarding their limited tolerance to cold shock.

Project description:Unlike gonochoristic fishes, sex is fixed after gonadal differentiation (primary sex determination), and sex can be altered in adults (secondary sex determination) of hermaphroditic fish species. The secondary sex determination of hermaphroditic fish has focused on the differences between testicular tissue and ovarian tissue during the sex change process. However, comprehensive studies analyzing ovarian tissue or testicular tissue independently have not been performed. Hermaphroditic black porgy shows a digonic gonad (ovarian tissue with testicular tissue separated by connective tissue). Protandrous black porgy has stable maleness during the first two reproductive cycles (<2 years old), and approximately 50% enter femaleness (natural sex change) during the third reproductive cycle. Precocious femaleness is rarely observed in the estradiol-17β (E2)-induced female phase (oocytes maintained at the primary oocyte stage), and a reversible female-to-male sex change is found after E2 is withdrawn in <2-year-old fish. However, precocious femaleness (oocytes entering the vitellogenic oocyte stage) is observed in testis-removed fish in <2-year-old fish. We used this characteristic to study secondary sex determination (femaleness) in ovarian tissue via transcriptomic analysis. Cell proliferation analysis showed that BrdU (5-bromo-2'-deoxyuridine)-incorporated germline cells were significantly increased in the testis-removed fish (female) compared to the control (sham) fish (male) during the nonspawning season (2 months after surgery). qPCR analysis showed that there were no differences in pituitary-releasing hormones (lhb and gtha) in pituitary and ovarian steroidogenesis-related factors (star, cyp11a1, hsd3b1, and cyp19a1a) or female-related genes (wnt4a, bmp15, gdf9, figla, and foxl2) in ovarian tissues between intact and testis-removed fish (2 months after surgery). Low expression of pituitary fshb and ovarian cyp17a1 was found after 2 months of surgery. However, we did find small numbers of genes (289 genes) showing sexual fate dimorphic expression in both groups by transcriptomic analysis (1 month after surgery). The expression profiles of these differentially expressed genes were further examined by qPCR. Our present work identified several candidate genes in ovarian tissue that may be involved in the early period of secondary sex determination (femaleness) in black porgy. The data confirmed our previous suggestion that testicular tissue plays an important role in secondary sex determination in protandrous black porgy.

Dataset Information

Robust gdf9 and bmp15 expression in the oocytes of ovotestes through the Figla-independent pathway in the hermaphroditic black porgy, Acanthopagrus schlegelii.

Publications

Robust gdf9 and bmp15 expression in the oocytes of ovotestes through the Figla-independent pathway in the hermaphroditic black porgy, Acanthopagrus schlegelii.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets