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Evolution of Shh endoderm enhancers during morphological transition from ventral lungs to dorsal gas bladder

Author

Listed:
  • Tomoko Sagai

    (Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics)

  • Takanori Amano

    (Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics)

  • Akiteru Maeno

    (Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics)

  • Tetsuaki Kimura

    (Interuniversity Bio-Backup Project Center, National Institute for Basic Biology
    Present address: Division of Human Genetics, Department of Integrated Genetics, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan)

  • Masatoshi Nakamoto

    (Interuniversity Bio-Backup Project Center, National Institute for Basic Biology
    Present address: Department of Marine Bioscience, Faculty of Marine Science, Tokyo University of Marine Science and Technology, Minato-ku, Tokyo 108-8477, Japan)

  • Yusuke Takehana

    (Interuniversity Bio-Backup Project Center, National Institute for Basic Biology
    Laboratory of Bioresources, National Institute for Basic Biology)

  • Kiyoshi Naruse

    (Interuniversity Bio-Backup Project Center, National Institute for Basic Biology
    Laboratory of Bioresources, National Institute for Basic Biology)

  • Norihiro Okada

    (National Cheng Kung University)

  • Hiroshi Kiyonari

    (Laboratory for Animal Resources and Genetic Engineering, RIKEN Center for Developmental Biology (CDB))

  • Toshihiko Shiroishi

    (Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics)

Abstract

Shh signalling plays a crucial role for endoderm development. A Shh endoderm enhancer, MACS1, is well conserved across terrestrial animals with lungs. Here, we first show that eliminating mouse MACS1 causes severe defects in laryngeal development, indicating that MACS1-directed Shh signalling is indispensable for respiratory organogenesis. Extensive phylogenetic analyses revealed that MACS1 emerged prior to the divergence of cartilaginous and bony fishes, and even euteleost fishes have a MACS1 orthologue. Meanwhile, ray-finned fishes evolved a novel conserved non-coding sequence in the neighbouring region. Transgenic assays showed that MACS1 drives reporter expression ventrally in laryngeal epithelium. This activity has been lost in the euteleost lineage, and instead, the conserved non-coding sequence of euteleosts acquired an enhancer activity to elicit dorsal epithelial expression in the posterior pharynx and oesophagus. These results implicate that evolution of these two enhancers is relevant to the morphological transition from ventral lungs to dorsal gas bladder.

Suggested Citation

  • Tomoko Sagai & Takanori Amano & Akiteru Maeno & Tetsuaki Kimura & Masatoshi Nakamoto & Yusuke Takehana & Kiyoshi Naruse & Norihiro Okada & Hiroshi Kiyonari & Toshihiko Shiroishi, 2017. "Evolution of Shh endoderm enhancers during morphological transition from ventral lungs to dorsal gas bladder," Nature Communications, Nature, vol. 8(1), pages 1-12, April.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms14300
    DOI: 10.1038/ncomms14300
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