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Egg envelopes (chorions) in medaka,  Oryzias latipes , are composed of three major glycoproteins: ZI-1, − 2, and − 3. These gene-encoded chorion glycoproteins are expressed in the liver and/or ovarian oocytes of sexually mature female fish. In medaka, the glycoproteins produced in the female liver are induced by estrogen as Choriogenin (Chg.) H and Chg. H minor (m), which correspond to the zona pellucida (ZP) B (ZPB) protein in mammals, and Chg. L, which corresponds to ZPC in mammals. Chg. H, Chg. Hm, and Chg. L, are then converted to ZI-1, − 2, and − 3, respectively, during oogenesis in medaka ovaries.  In the present study, we established a medaka line in which the  chg.l  gene was inactivated using the transcription activator-like effector nuclease (TALEN) technique. Neither intact  chg.l  transcripts nor Chg. L proteins were detected in livers of sexually mature female homozygotes for the mutation (homozygous  chg.l  knockout:  chg.l−/− ). The  chg.l−/−  females spawned string-like materials containing “smashed eggs.” Closer examination revealed the oocytes in the ovaries of  chg.l−/−  females had thin chorions, particularly at the inner layer, despite a normal growth rate. In comparing chorions from normal ( chg.l +/+) and  chg.l−/−  oocytes, the latter exhibited abnormal architecture in the chorion pore canals through which the oocyte microvilli pass. These microvilli mediate the nutritional exchange between the oocyte and surrounding spaces and promote sperm-egg interactions during fertilization. Thus, following in vitro fertilization, no embryos developed in the artificially inseminated oocytes isolated from  chg.l−/−  ovaries. These results demonstrated that medaka ZI-3 (Chg.L) is the major component of the inner layer of the chorion, as it supports and maintains the oocyte’s structural shape, enabling it to withstand the pressures exerted against the chorion during spawning, and is essential for successful fertilization. Therefore, gene products of oocyte-specific ZP genes that may be expressed in medaka oocytes cannot compensate for the loss Chg. L function to produce offspring for this species.

Targeted deletion of liver-expressed Choriogenin L results in the production of soft eggs and infertility in medaka, Oryzias latipes