Genética da macroevolução das aves

quarta-feira, fevereiro 08, 2017

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.