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Conserved regulatory switches for the transition from natal down to juvenile feather in birds

Author

Listed:
  • Chih-Kuan Chen

    (University of Southern California
    Academia Sinica
    National Chung Hsing University
    National Chung Hsing University)

  • Yao-Ming Chang

    (Academia Sinica)

  • Ting-Xin Jiang

    (University of Southern California)

  • ZhiCao Yue

    (Shenzhen University Medical School
    Shenzhen University Medical School
    Shenzhen University Medical School)

  • Tzu-Yu Liu

    (University of Southern California
    National Cheng Kung University)

  • Jiayi Lu

    (University of Southern California)

  • Zhou Yu

    (University of Southern California)

  • Jinn-Jy Lin

    (National Center for High-performance Computing)

  • Trieu-Duc Vu

    (University of Michigan School of Medicine)

  • Tao-Yu Huang

    (Academia Sinica)

  • Hans I-Chen Harn

    (University of Southern California)

  • Chen Siang Ng

    (National Chung Hsing University
    National Tsing Hua University
    National Tsing Hua University
    National Tsing Hua University)

  • Ping Wu

    (University of Southern California)

  • Cheng-Ming Chuong

    (University of Southern California)

  • Wen‐Hsiung Li

    (Academia Sinica
    University of Chicago)

Abstract

The transition from natal downs for heat conservation to juvenile feathers for simple flight is a remarkable environmental adaptation process in avian evolution. However, the underlying epigenetic mechanism for this primary feather transition is mostly unknown. Here we conducted time-ordered gene co-expression network construction, epigenetic analysis, and functional perturbations in developing feather follicles to elucidate four downy-juvenile feather transition events. We report that extracellular matrix reorganization leads to peripheral pulp formation, which mediates epithelial-mesenchymal interactions for branching morphogenesis. α-SMA (ACTA2) compartmentalizes dermal papilla stem cells for feather renewal cycling. LEF1 works as a key hub of Wnt signaling to build rachis and converts radial downy to bilateral symmetry. Novel usage of scale keratins strengthens feather sheath with SOX14 as the epigenetic regulator. We show that this primary feather transition is largely conserved in chicken (precocial) and zebra finch (altricial) and discuss the possibility that this evolutionary adaptation process started in feathered dinosaurs.

Suggested Citation

  • Chih-Kuan Chen & Yao-Ming Chang & Ting-Xin Jiang & ZhiCao Yue & Tzu-Yu Liu & Jiayi Lu & Zhou Yu & Jinn-Jy Lin & Trieu-Duc Vu & Tao-Yu Huang & Hans I-Chen Harn & Chen Siang Ng & Ping Wu & Cheng-Ming Ch, 2024. "Conserved regulatory switches for the transition from natal down to juvenile feather in birds," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48303-3
    DOI: 10.1038/s41467-024-48303-3
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    References listed on IDEAS

    as
    1. Mingke Yu & Ping Wu & Randall B. Widelitz & Cheng-Ming Chuong, 2002. "The morphogenesis of feathers," Nature, Nature, vol. 420(6913), pages 308-312, November.
    2. Ang Li & Seth Figueroa & Ting-Xin Jiang & Ping Wu & Randall Widelitz & Qing Nie & Cheng-Ming Chuong, 2017. "Diverse feather shape evolution enabled by coupling anisotropic signalling modules with self-organizing branching programme," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    3. Zhicao Yue & Ting-Xin Jiang & Randall Bruce Widelitz & Cheng-Ming Chuong, 2005. "Mapping stem cell activities in the feather follicle," Nature, Nature, vol. 438(7070), pages 1026-1029, December.
    4. Xing Xu & Zhong-he Zhou & Richard O. Prum, 2001. "Branched integumental structures in Sinornithosaurus and the origin of feathers," Nature, Nature, vol. 410(6825), pages 200-204, March.
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