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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.

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