Evolution of Shh endoderm enhancers during morphological transition from ventral lungs to dorsal gas bladder.
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.
Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Tomoko
T
Sagai
Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Takanori
T
Amano
Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Akiteru
A
Maeno
Interuniversity Bio-Backup Project Center, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan.
Tetsuaki
T
Kimura
Interuniversity Bio-Backup Project Center, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan.
Masatoshi
M
Nakamoto
Interuniversity Bio-Backup Project Center, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan.|Laboratory of Bioresources, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan.
Yusuke
Y
Takehana
Interuniversity Bio-Backup Project Center, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan.|Laboratory of Bioresources, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan.
Kiyoshi
0000-0001-9185-3495
K
Naruse
Department of Life Sciences, National Cheng Kung University, Tainan 701, Taiwan.
Norihiro
N
Okada
Laboratory for Animal Resources and Genetic Engineering, RIKEN Center for Developmental Biology (CDB), Kobe, Hyogo 650-0047, Japan.
Hiroshi
H
Kiyonari
Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Toshihiko
T
Shiroishi
D000400:Air Sacs / Q000196:embryology*; D000818:Animals; D030801:Animals, Genetically Modified; D001665:Binding Sites; D003066:Coenzyme A Ligases / Q000235:genetics; D004742:Enhancer Elements, Genetic; D019143:Evolution, Molecular; D005399:Fishes / Q000196:embryology / Q000235:genetics; D051858:Forkhead Transcription Factors / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental; D017930:Genes, Reporter; D053823:Hedgehog Proteins / Q000235:genetics*; D007438:Introns; D007830:Larynx / Q000196:embryology / Q000378:metabolism; D008168:Lung / Q000196:embryology*; D051379:Mice; D018345:Mice, Knockout; D024101:Mitochondrial Proteins / Q000235:genetics; D009990:Oryzias; D010802:Phylogeny; D012045:Regulatory Sequences, Nucleic Acid; D015398:Signal Transduction
D051858:Forkhead Transcription Factors; D053823:Hedgehog Proteins; D024101:Mitochondrial Proteins; C499057:Acsm1 protein, mouse; D003066:Coenzyme A Ligases