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Amniotes co-opt intrinsic genetic instability to protect germ-line genome integrity

Author

Listed:
  • Yu H. Sun

    (University of Rochester Medical Center)

  • Hongxiao Cui

    (Northwest A&F University)

  • Chi Song

    (The Ohio State University)

  • Jiafei Teng Shen

    (Zhejiang University School of Medicine)

  • Xiaoyu Zhuo

    (Washington University School of Medicine)

  • Ruoqiao Huiyi Wang

    (University of Rochester Medical Center
    Northwest A&F University)

  • Xiaohui Yu

    (Northwest A&F University)

  • Rudo Ndamba

    (University of Rochester Medical Center)

  • Qian Mu

    (University of Rochester Medical Center)

  • Hanwen Gu

    (University of Rochester Medical Center)

  • Duolin Wang

    (University of Rochester Medical Center)

  • Gayathri Guru Murthy

    (University of Rochester Medical Center)

  • Pidong Li

    (Grandomics Biosciences Co., Ltd)

  • Fan Liang

    (Grandomics Biosciences Co., Ltd)

  • Lei Liu

    (Grandomics Biosciences Co., Ltd)

  • Qing Tao

    (Grandomics Biosciences Co., Ltd)

  • Ying Wang

    (University of California)

  • Sara Orlowski

    (University of Arkansas)

  • Qi Xu

    (McGill University)

  • Huaijun Zhou

    (University of California)

  • Jarra Jagne

    (Cornell University College of Veterinary Medicine)

  • Omer Gokcumen

    (University at Buffalo, State University of New York)

  • Nick Anthony

    (University of Arkansas)

  • Xin Zhao

    (McGill University)

  • Xin Zhiguo Li

    (University of Rochester Medical Center)

Abstract

Unlike PIWI-interacting RNA (piRNA) in other species that mostly target transposable elements (TEs), >80% of piRNAs in adult mammalian testes lack obvious targets. However, mammalian piRNA sequences and piRNA-producing loci evolve more rapidly than the rest of the genome for unknown reasons. Here, through comparative studies of chickens, ducks, mice, and humans, as well as long-read nanopore sequencing on diverse chicken breeds, we find that piRNA loci across amniotes experience: (1) a high local mutation rate of structural variations (SVs, mutations ≥ 50 bp in size); (2) positive selection to suppress young and actively mobilizing TEs commencing at the pachytene stage of meiosis during germ cell development; and (3) negative selection to purge deleterious SV hotspots. Our results indicate that genetic instability at pachytene piRNA loci, while producing certain pathogenic SVs, also protects genome integrity against TE mobilization by driving the formation of rapid-evolving piRNA sequences.

Suggested Citation

  • Yu H. Sun & Hongxiao Cui & Chi Song & Jiafei Teng Shen & Xiaoyu Zhuo & Ruoqiao Huiyi Wang & Xiaohui Yu & Rudo Ndamba & Qian Mu & Hanwen Gu & Duolin Wang & Gayathri Guru Murthy & Pidong Li & Fan Liang , 2023. "Amniotes co-opt intrinsic genetic instability to protect germ-line genome integrity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36354-x
    DOI: 10.1038/s41467-023-36354-x
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