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Co-option of a non-retroviral endogenous viral element in planthoppers

Author

Listed:
  • Hai-Jian Huang

    (Ningbo University
    Ningbo University)

  • Yi-Yuan Li

    (Ningbo University
    Ningbo University)

  • Zhuang-Xin Ye

    (Ningbo University
    Ningbo University
    Nanjing Forestry University)

  • Li-Li Li

    (Ningbo University
    Ningbo University)

  • Qing-Ling Hu

    (Ningbo University
    Ningbo University)

  • Yu-Juan He

    (Ningbo University
    Ningbo University)

  • Yu-Hua Qi

    (Ningbo University
    Ningbo University)

  • Yan Zhang

    (Ningbo University
    Ningbo University)

  • Ting Li

    (Ningbo University
    Ningbo University)

  • Gang Lu

    (Ningbo University
    Ningbo University)

  • Qian-Zhuo Mao

    (Ningbo University
    Ningbo University)

  • Ji-Chong Zhuo

    (Ningbo University
    Ningbo University)

  • Jia-Bao Lu

    (Ningbo University
    Ningbo University)

  • Zhong-Tian Xu

    (Ningbo University
    Ningbo University)

  • Zong-Tao Sun

    (Ningbo University
    Ningbo University)

  • Fei Yan

    (Ningbo University
    Ningbo University)

  • Jian-Ping Chen

    (Ningbo University
    Ningbo University
    Nanjing Forestry University)

  • Chuan-Xi Zhang

    (Ningbo University
    Ningbo University)

  • Jun-Min Li

    (Ningbo University
    Ningbo University)

Abstract

Non-retroviral endogenous viral elements (nrEVEs) are widely dispersed throughout the genomes of eukaryotes. Although nrEVEs are known to be involved in host antiviral immunity, it remains an open question whether they can be domesticated as functional proteins to serve cellular innovations in arthropods. In this study, we found that endogenous toti-like viral elements (ToEVEs) are ubiquitously integrated into the genomes of three planthopper species, with highly variable distributions and polymorphism levels in planthopper populations. Three ToEVEs display exon‒intron structures and active transcription, suggesting that they might have been domesticated by planthoppers. CRISPR/Cas9 experiments revealed that one ToEVE in Nilaparvata lugens, NlToEVE14, has been co-opted by its host and plays essential roles in planthopper development and fecundity. Large-scale analysis of ToEVEs in arthropod genomes indicated that the number of arthropod nrEVEs is currently underestimated and that they may contribute to the functional diversity of arthropod genes.

Suggested Citation

  • Hai-Jian Huang & Yi-Yuan Li & Zhuang-Xin Ye & Li-Li Li & Qing-Ling Hu & Yu-Juan He & Yu-Hua Qi & Yan Zhang & Ting Li & Gang Lu & Qian-Zhuo Mao & Ji-Chong Zhuo & Jia-Bao Lu & Zhong-Tian Xu & Zong-Tao S, 2023. "Co-option of a non-retroviral endogenous viral element in planthoppers," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43186-2
    DOI: 10.1038/s41467-023-43186-2
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    1. Yusuke Inoue & Tomonori Saga & Takumi Aikawa & Masahiko Kumagai & Atsuko Shimada & Yasushi Kawaguchi & Kiyoshi Naruse & Shinichi Morishita & Akihiko Koga & Hiroyuki Takeda, 2017. "Complete fusion of a transposon and herpesvirus created the Teratorn mobile element in medaka fish," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    2. Masayuki Horie & Tomoyuki Honda & Yoshiyuki Suzuki & Yuki Kobayashi & Takuji Daito & Tatsuo Oshida & Kazuyoshi Ikuta & Patric Jern & Takashi Gojobori & John M. Coffin & Keizo Tomonaga, 2010. "Endogenous non-retroviral RNA virus elements in mammalian genomes," Nature, Nature, vol. 463(7277), pages 84-87, January.
    3. Hai-Jun Xu & Jian Xue & Bo Lu & Xue-Chao Zhang & Ji-Chong Zhuo & Shu-Fang He & Xiao-Fang Ma & Ya-Qin Jiang & Hai-Wei Fan & Ji-Yu Xu & Yu-Xuan Ye & Peng-Lu Pan & Qiao Li & Yan-Yuan Bao & H. Frederik Ni, 2015. "Two insulin receptors determine alternative wing morphs in planthoppers," Nature, Nature, vol. 519(7544), pages 464-467, March.
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