Functional roles of Aves class-specific cis-regulatory elements on macroevolution of bird-specific features
Ryohei Seki, Cai Li, Qi Fang, Shinichi Hayashi, Shiro Egawa, Jiang Hu, Luohao Xu, Hailin Pan, Mao Kondo, Tomohiko Sato, Haruka Matsubara, Namiko Kamiyama, Keiichi Kitajima, Daisuke Saito, Yang Liu, M. Thomas P. Gilbert, Qi Zhou, Xing Xu, Toshihiko Shiroishi, Naoki Irie, Koji Tamura & Guojie Zhang
Nature Communications 8, Article number: 14229 (2017)
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Evolutionary developmental biology Gene regulation Genomics
Received: 25 April 2016 Accepted: 12 December 2016 Published online: 06 February 2017
Figure 6: Sim1 and flight feather evolution.
Abstract
Unlike microevolutionary processes, little is known about the genetic basis of macroevolutionary processes. One of these magnificent examples is the transition from non-avian dinosaurs to birds that has created numerous evolutionary innovations such as self-powered flight and its associated wings with flight feathers. By analysing 48 bird genomes, we identified millions of avian-specific highly conserved elements (ASHCEs) that predominantly (>99%) reside in non-coding regions. Many ASHCEs show differential histone modifications that may participate in regulation of limb development. Comparative embryonic gene expression analyses across tetrapod species suggest ASHCE-associated genes have unique roles in developing avian limbs. In particular, we demonstrate how the ASHCE driven avian-specific expression of gene Sim1 driven by ASHCE may be associated with the evolution and development of flight feathers. Together, these findings demonstrate regulatory roles of ASHCEs in the creation of avian-specific traits, and further highlight the importance of cis-regulatory rewiring during macroevolutionary changes.
Acknowledgements
We thank Professor Jon Fjeldså of the University of Copenhagen for valuable comments. This project was supported by Strategic Priority Research Program of the Chinese Academy of Sciences (XDB13000000) and Lundbeckfonden grant R190-2014-2827. K.T. was supported by JSPS KAKENHI Grant (JP15H04374), grant from The Naito Foundation, and Next Generation World-Leading Researchers from the Cabinet Office, Government of Japan (LS007). R.S., S.E. and H.M. are JSPS Research Fellows (JSPS KAKENHI Grant Numbers JP14J07050 (R.S.), JP15J06859 (S.E.), JP15J06385 (H.M.)). C.L. was partially supported by Lundbeckfonden grant R52-5062 to M.T.P.G.). N.I. was partially supported by Platform Project for Supporting in Drug Discovery and Life Science Research Platform for Dynamic Approaches to Living System from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) and Japan Agency for Medical Research and Development (AMED). Photographs of the adult Cochin bantam and Brahmas bantam and their fertilized eggs were provided by the National BioResource Project (NBRP) Chicken/Quail of the MEXT, Japan.
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Author notes
Ryohei Seki & Cai Li
These authors contributed equally to this work
Affiliations
Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan
Ryohei Seki & Toshihiko Shiroishi
Department of Developmental Biology and Neurosciences, Graduate School of Life Sciences, Tohoku University, Aobayama 6-3, Aoba-ku, Sendai 980-8578, Japan
Ryohei Seki, Shinichi Hayashi, Shiro Egawa, Mao Kondo, Tomohiko Sato, Haruka Matsubara, Namiko Kamiyama, Keiichi Kitajima, Daisuke Saito & Koji Tamura
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China
Cai Li, Qi Fang, Jiang Hu, Luohao Xu, Hailin Pan, Yang Liu & Guojie Zhang
China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China
Cai Li, Qi Fang, Hailin Pan & Guojie Zhang
Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen 1350, Denmark
Cai Li & M. Thomas P. Gilbert
Department of Genetics, Cell Biology and Development, University of Minnesota, 321 Church Street SE, Minneapolis, Minnesota 55455, USA
Shinichi Hayashi
Frontier Research Institute for Interdisciplinary Sciences (FRIS), Tohoku University, Aobayama 6-3, Aoba-ku, Sendai 980-8578, Japan
Daisuke Saito
Norwegian University of Science and Technology, University Museum, N-7491 Trondheim, Norway
M. Thomas P. Gilbert
Department of Integrative Biology University of California, Berkeley, California 94720, USA
Qi Zhou
Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China
Xing Xu
Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
Naoki Irie
Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, Copenhagen 2100, Denmark
Guojie Zhang
Contributions
G.Z., K.T. and N.I. designed the study. C.L., Q.F., J.H., L.X., H.P. and Y.L. conducted the computational analyses. R.S., S.H., S.E., M.K., T.S., H.M., N.K., K.K. and D.S. conducted the wet-lab experiments and analysed the data. G.Z., K.T., N.I., X.X., R.S. and C.L. wrote the manuscript. M.T.P.G., Q.Z. and T.S provided critical comments for improving the manuscript.
Competing interests
The authors declare no competing financial interests.
Corresponding authors
Correspondence to Naoki Irie or Koji Tamura or Guojie Zhang.
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