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Complete Depletion of Primordial Germ Cells Results in Masculinization of Monopterus albus, a Protogynous Hermaphroditic Fish

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Abstract

Primordial germ cells (PGCs) play an important role in sexual fate determination and gonadal development in gonochoristic fish, such as zebrafish and medaka. However, little is known about the function of PGCs in hermaphroditic fish. Rice field eel (Monopterus albus), a protogynous hermaphroditic fish, is an economically valuable aquaculture species. We eliminated PGCs in rice field eels during embryogenesis via morpholino-mediated knockdown dead end (dnd). The PGCs-depleted gonads developed into testis-like structures with Sertoli cells and Leydig cells. The gene expression pattern of 15-month-old PGCs-depleted gonads showed that male-biased genes, dmrt1, sox9a, gsdf, and amh, were significantly higher than that of the WT, whereas female-biased genes, foxl2 and cyp19a1a, were significantly decreased. These results indicate that PGCs are essential for ovarian differentiation in rice field eel, and PGCs-depleted gonads develop into sterile males without undergoing the female and intersex stages. Our study is the first to identify the role of PGCs in sex differentiation in rice field eel, a protogynous hermaphrodite teleost. And it is of great significance in rice field eel for discovering the underlying mechanism of sex differentiation and establishing sex control technology.

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Acknowledgements

We are grateful to Ms. Fang Zhou (Analytical & Testing Center, IHB, CAS) for providing microscope services and Ms. Ming Li for her help in fry culture and microinjection.

Funding

This study was supported by the National Key R&D Program of China (2018YFD0901200, 2018YFD0900203), National Natural Science Foundation of China (31772833, 32072961, 32102790), China Agriculture Research System of MOF and MARA (CARS-46) and China Postdoctoral Science Foundation (2021M693345).

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Authors and Affiliations

  1. State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Innovation Academy of Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, 430072, China

    Mingxi Hou, Ke Feng, Hongrui Luo, Yinjun Jiang, Wen Xu, Yongming Li, Yanlong Song, Ji Chen, Binbin Tao, Zuoyan Zhu & Wei Hu

  2. Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    Wei Hu

  3. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China

    Mingxi Hou, Yinjun Jiang, Wen Xu & Wei Hu

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  1. Mingxi Hou
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  2. Ke Feng
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  3. Hongrui Luo
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  4. Yinjun Jiang
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  5. Wen Xu
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  7. Yanlong Song
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  8. Ji Chen
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  9. Binbin Tao
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  10. Zuoyan Zhu
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  11. Wei Hu
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Contributions

Wei Hu and Mingxi Hou conceived and designed research; Mingxi Hou, Hongrui Luo, and Yinjun Jiang performed the experiments; Ke Feng, Wen Xu, Binbin Tao and Yongming Li contributed to sample collection; Ji Chen and Yanlong Song contributed new reagents/analytic tools; Wei Hu, Zuoyan Zhu, Mingxi Hou and Binbin Tao analyzed data and wrote the manuscript.

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Correspondence to Binbin Tao or Wei Hu.

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Hou, M., Feng, K., Luo, H. et al. Complete Depletion of Primordial Germ Cells Results in Masculinization of Monopterus albus, a Protogynous Hermaphroditic Fish. Mar Biotechnol 24, 320–334 (2022). https://doi.org/10.1007/s10126-022-10106-2

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