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Oogenesis is a complex process regulated by precise coordination of multiple factors, including maternal genes. Zygote arrest 1 (zar1) has been identified as an ovary-specific maternal gene that is vital for oocyte-to-embryo transition and oogenesis in mouse and zebrafish. However, its function in other species remains to be elucidated. In the present study, zar1 was identified with conserved C-terminal zinc finger domains in Nile tilapia. zar1 was highly expressed in the ovary and specifically expressed in phase I and II oocytes. Disruption of zar1 led to the failed transition from oogonia to phase I oocytes, with somatic cell apoptosis. Down-regulation and failed polyadenylation of figla, gdf9, bmp15 and wee2 mRNAs were observed in the ovaries of zar1 / fish. Cpeb1, a gene essential for polyadenylation that interacts with Zar1, was down-regulated in zar1 / fish. Moreover, decreased levels of serum estrogen and increased levels of androgen were observed in zar1 / fish. Taken together, zar1 seems to be essential for tilapia oogenesis by regulating polyadenylation and estrogen synthesis. Our study shows that Zar1 has different molecular functions during gonadal development by the similar signaling pathway in different species.
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Homozygous mutation of foxh1 arrests oogenesis causing infertility in female Nile tilapia
Abstract Foxh1, a member of fox gene family, was first characterized as a transcriptional partner in the formation of the Smad protein complex. Recent studies have shown foxh1 is highly expressed in the cytoplasm of oocytes in both tilapia and mouse. However, its function in oogenesis remains unexplored. In the present study, foxh1−/− tilapia was created by CRISPR/Cas9. At 180 dah (days after hatching), the foxh1−/− XX fish showed oogenesis arrest and a significantly lower GSI. The transition of oocytes from phase II to phase III and follicle cells from one to two layers was blocked, resulting in infertility of the mutant. Transcriptomic analysis revealed that expression of genes involved in estrogen synthesis and oocyte growth were altered in the foxh1−/− ovaries. Loss of foxh1 resulted in significantly decreased Cyp19a1a and increased Cyp11b2 expression, consistent with significantly lower concentrations of serum estradiol-17β (E2) and higher concentrations of 11-Ketotestosterone (11-KT). Moreover, administration of E2 rescued the phenotypes of foxh1−/− XX fish, as indicated by the appearance of phase III and IV oocytes and absence of Cyp11b2 expression. Taken together, these results suggest that foxh1 functions in the oocytes to regulate oogenesis by promoting cyp19a1a expression, and therefore estrogen production. Disruption of foxh1 may block the estrogen synthesis and oocyte growth, leading to the arrest of oogenesis and thus infertility in tilapia.
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- Award ID(s):
- 1830753
- PAR ID:
- 10127594
- Date Published:
- Journal Name:
- Biology of Reproduction
- ISSN:
- 0006-3363
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/biolre/ioz225
