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The new chimeric chiron genes evolved essential roles in zebrafish embryonic development by regulating NAD+ levels

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Abstract

The origination of new genes is important for generating genetic novelties for adaptive evolution and biological diversity. However, their potential roles in embryonic development, evolutionary processes into ancient networks, and contributions to adaptive evolution remain poorly investigated. Here, we identified a novel chimeric gene family, the chiron family, and explored its genetic basis and functional evolution underlying the adaptive evolution of Danioninae fishes. The ancestral chiron gene originated through retroposition of nampt in Danioninae 48–54 million years ago (Mya) and expanded into five duplicates (chiron1–5) in zebrafish 1–4 Mya. The chiron genes (chirons) likely originated in embryonic development and gradually extended their expression in the testis. Functional experiments showed that chirons were essential for zebrafish embryo development. By integrating into the NAD+ synthesis pathway, chirons could directly catalyze the NAD+ rate-limiting reaction and probably impact two energy metabolism genes (nmnat1 and naprt) to be under positive selection in Danioninae fishes. Together, these results mainly demonstrated that the origin of new chimeric chiron genes may be involved in adaptive evolution by integrating and impacting the NAD+ biosynthetic pathway. This coevolution may contribute to the physiological adaptation of Danioninae fishes to widespread and varied biomes in Southeast Asian.

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Acknowledgements

This project is supported by the Pilot projects (XDB13020100), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31000000) and the National Natural Science Foundation of China (NSFC, 31601859). We would like to thank Prof. Manyuan Long (The University of Chicago), Prof. Wuhan Xiao (Institute of Hydrobiology, CAS), Prof. Z. Yin (Institute of Hydrobiology, CAS), Prof. Yonghua Sun (Institute of Hydrobiology, CAS), Prof. Shuhong Zhao (Huazhong Agricultural University), and Prof. Changchun Li (Huazhong Agricultural University) for providing experiment platform and technical assistance. We also thank Dr. Liandong Yang and Dr. Zaixuan Zhong (Institute of Hydrobiology, CAS) for providing the transcriptome sequencing data. We also thank Dr. Dylan Sosa and Emily Mortola (The University of Chicago) for refining the style and language.

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  1. Chengchi Fang

    Present address: Current address: Huazhong Agricultural University, Wuhan, 430070, China

Authors and Affiliations

  1. The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Chengchi Fang, Xiaoni Gan & Shunping He

  2. Kunming Institute of Botany, Chinese Academy of Science, Kunming, 650201, China

    Chengjun Zhang

  3. University of Chinese Academy of Sciences, Beijing, 100039, China

    Chengchi Fang & Shunping He

  4. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China

    Shunping He

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  1. Chengchi Fang
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  2. Xiaoni Gan
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Correspondence to Shunping He.

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Fang, C., Gan, X., Zhang, C. et al. The new chimeric chiron genes evolved essential roles in zebrafish embryonic development by regulating NAD+ levels. Sci. China Life Sci. 64, 1929–1948 (2021). https://doi.org/10.1007/s11427-020-1851-0

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  • DOI: https://doi.org/10.1007/s11427-020-1851-0

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