Genome-wide analysis of brain and gonad transcripts reveals changes of key sex reversal-related genes expression and signaling pathways in three stages of Monopterus albus

Chi, Wei; Gao, Yu; Hu, Qing; Guo, Wei; Li, Dapeng

doi:10.1371/journal.pone.0173974

Cited by 41 publications

(29 citation statements)

References 70 publications

(63 reference statements)

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“…This was also the case in the present study, with highest levels produced by CPE treatment. Ovarian-specific expression of foxr1 has been shown in zebrafish [113], freshwater medaka (Oryzias melastigma) [114], rice field eel (Monopterus albus) [115], and European eel [73] possibly indicating an important role during early life history. The vital importance of foxr1 transcript abundance for embryonic survival around MZT was recently suggested for zebrafish [113], which is consistent with our observed high transcript levels.…”

Section: Molecular Ontogeny and Embryonic Developmentmentioning

confidence: 99%

Differential impacts of carp and salmon pituitary extracts on induced oogenesis, egg quality, molecular ontogeny and embryonic developmental competence in European eel

et al. 2020

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Low egg quality and embryonic survival are critical challenges in aquaculture, where assisted reproduction procedures and other factors may impact egg quality. This includes European eel (Anguilla anguilla), where pituitary extract from carp (CPE) or salmon (SPE) is applied to override a dopaminergic inhibition of the neuroendocrine system, preventing gonadotropin secretion and gonadal development. The present study used either CPE or SPE to induce vitellogenesis in female European eel and compared impacts on egg quality and offspring developmental competence with emphasis on the maternal-to-zygotic transition (MZT). Females treated with SPE produced significantly higher proportions of floating eggs with fewer cleavage abnormalities and higher embryonic survival. These findings related successful embryogenesis to higher abundance of mRNA transcripts of genes involved in cell adhesion, activation of MZT, and immune response (dcbld1, epcam, oct4, igm) throughout embryonic development. The abundance of mRNA transcripts of cldnd, foxr1, cea, ccna1, ccnb1, ccnb2, zar1, oct4, and npm2 was relatively stable during the first eight hours, followed by a drop during MZT and low levels thereafter, indicating transfer and subsequent clearance of maternal mRNA. mRNA abundance of zar1, epcam, and dicer1 was associated with cleavage abnormalities, while mRNA abundance of zar1, sox2, foxr1, cldnd, phb2, neurod4, and neurog1 (before MZT) was associated with subsequent embryonic survival. In a second pattern, low initial mRNA abundance with an increase during MZT and higher levels persisting thereafter indicating the activation of zygotic transcription. mRNA abundance of ccna1, npm2, oct4, neurod4, and neurog1 during later embryonic development was associated with hatch success. A deviating pattern was observed for dcbld1, which mRNA levels followed the maternal-effect gene pattern but only for embryos from SPE treated females. Together, the differences in offspring production and performance reported in this study show that PE composition impacts egg quality and embryogenesis and in particular, the transition from initial maternal transcripts to zygotic transcription.

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Section: Molecular Ontogeny and Embryonic Developmentmentioning

confidence: 99%

Differential impacts of carp and salmon pituitary extracts on induced oogenesis, egg quality, molecular ontogeny and embryonic developmental competence in European eel

et al. 2020

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“…Further, foxo3 was shown to be required for ovarian follicular development, and its knockout in mice led to sterility in female mutants due to progressive degeneration of the developing oocytes and lack of ovarian reserve of mature oocytes ( Hosaka et al, 2004 ). foxr1 was also found to have sexually dimorphic expression in eels ( Anguilla anguilla and Monopterus albus ) and marine medaka ( Oryzias melastigma ), and was predominately observed in the ovaries ( Geffroy et al, 2016 ; Chi et al, 2017 ; Lai et al, 2015 ). However, despite these observational studies, the function of foxr1 in vertebrates, especially its role in reproduction, remains unclear.…”

Section: Introductionmentioning

confidence: 96%

foxr1is a novel maternal-effect gene in fish that is required for early embryonic success

Cheung¹,

Patinote²,

Guiguen³

et al. 2018

PeerJ

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The family of forkhead box (Fox) transcription factors regulates gonadogenesis and embryogenesis, but the role of foxr1 in reproduction is unknown. Evolutionary history of foxr1 in vertebrates was examined and the gene was found to exist in most vertebrates, including mammals, ray-finned fish, amphibians, and sauropsids. By quantitative PCR and RNA-seq, we found that foxr1 had an ovarian-specific expression in zebrafish, a common feature of maternal-effect genes. In addition, it was demonstrated using in situ hybridization that foxr1 was a maternally-inherited transcript that was highly expressed even in early-stage oocytes and accumulated in the developing eggs during oogenesis. We also analyzed the function of foxr1 in female reproduction using a zebrafish CRISPR/cas9 knockout model. It was observed that embryos from the foxr1-deficient females had a significantly lower survival rate whereby they either failed to undergo cell division or underwent abnormal division that culminated in growth arrest at around the mid-blastula transition and early death. These mutant-derived eggs contained dramatically increased levels of p21, a cell cycle inhibitor, and reduced rictor, a component of mTOR and regulator of cell survival, which were in line with the observed growth arrest phenotype. Our study shows for the first time that foxr1 is an essential maternal-effect gene and may be required for proper cell division and survival via the p21 and mTOR pathways. These novel findings will broaden our knowledge on the functions of specific maternal factors stored in the developing egg and the underlying mechanisms that contribute to reproductive success.

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“…The swamp eel (Monopterus albus) is rich in nutrition, has very palatable meat, and is favored by consumers. It is a major freshwater economic fish in China (Chi et al, 2017). It has the characteristic of undergoing a sex reversal: during the embryonic stage and to the first sexual maturity, it is female; it then enters an intersex state, and then some individuals develop into males (Zhao et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Analysis of the Intestinal Flora in Male Versus Female Swamp Eels (Monopterus albus)

et al. 2020

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This study aimed to analyze the intestinal flora of male versus female swamp eels, which have the unique characteristic of sex reversal. Same-aged swamp eels from the same parents, kept under the same conditions in terms of environment, diet, etc., were used as the study materials. After breeding for 1 year, 18 healthy swamp eels (nine males and nine females), weighing 39.4 ± 2.3 g, were selected. The intestinal contents of three swamp eels of the same sex were combined and labeled as follows: FM1-FM3 (n = 3) for females and MM1-MM3 (n = 3) for males. High-throughput sequencing was used to research the v3-v4 region of 16S rDNA in the intestinal flora. The results suggested significant differences in the structure, composition, and diversity of the intestinal flora of male versus female swamp eels. The relative abundances of Actinobacteria and Spirochaetes in female swamp eels were significantly higher (p < 0.05) than in male swamp eels at the phylum level. The relative abundances of Mycobacterium, Bacillus, and Vagococcus in female swamp eels were considerably higher (p < 0.05) than in male swamp eels at the genus level. The Alpha diversity of females was higher than that of males, and the Shannon index of females was also significantly higher (p < 0.05, Tukey's HSD) than that in males. Investigations of Beta diversity, including NMDS ordination, UPGMA cluster analysis, and PLS-DA analysis, showed that female and male swamp eels could be clearly distinguished based on significant differences in intestinal flora between the FM group and the MM group. LEfSe analysis showed that the dominant bacteria were Cetobacterium in male swamp eels and Clostridium_sp_ND2, Mycobacterium, Alphaproteobacteria, and Bacilli in female swamp eels. The results showed dramatic differences in the intestinal flora between the sexes, which indicates the need for a more in-depth study on sex reversal in the future.

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Genome-wide analysis of brain and gonad transcripts reveals changes of key sex reversal-related genes expression and signaling pathways in three stages of Monopterus albus

Cited by 41 publications

References 70 publications

Differential impacts of carp and salmon pituitary extracts on induced oogenesis, egg quality, molecular ontogeny and embryonic developmental competence in European eel

Differential impacts of carp and salmon pituitary extracts on induced oogenesis, egg quality, molecular ontogeny and embryonic developmental competence in European eel

foxr1is a novel maternal-effect gene in fish that is required for early embryonic success

Analysis of the Intestinal Flora in Male Versus Female Swamp Eels (Monopterus albus)

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