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

doi:10.1038/ncomms14229

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 IrieKoji Tamura, Guojie Zhang

Genetics, Cell Biology and Development (TMED)

Research output: Contribution to journal › Article › peer-review

42 Scopus citations

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.

Original language	English (US)
Article number	14229
Journal	Nature communications
Volume	8
DOIs	https://doi.org/10.1038/ncomms14229
State	Published - Feb 6 2017

Bibliographical note

Funding Information:
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

Publisher Copyright:
© The Author(s) 2017.

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10.1038/ncomms14229

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5473641

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Seki, R., Li, C., Fang, Q., Hayashi, S., Egawa, S., Hu, J., Xu, L., Pan, H., Kondo, M., Sato, T., Matsubara, H., Kamiyama, N., Kitajima, K., Saito, D., Liu, Y., Gilbert, M. T. P., Zhou, Q., Xu, X., Shiroishi, T., ... Zhang, G. (2017). Functional roles of Aves class-specific cis-regulatory elements on macroevolution of bird-specific features. Nature communications, 8, [14229]. https://doi.org/10.1038/ncomms14229

Seki, R, Li, C, Fang, Q, Hayashi, S, Egawa, S, Hu, J, Xu, L, Pan, H, Kondo, M, Sato, T, Matsubara, H, Kamiyama, N, Kitajima, K, Saito, D, Liu, Y, Gilbert, MTP, Zhou, Q, Xu, X, Shiroishi, T, Irie, N, Tamura, K & Zhang, G 2017, 'Functional roles of Aves class-specific cis-regulatory elements on macroevolution of bird-specific features', Nature communications, vol. 8, 14229. https://doi.org/10.1038/ncomms14229

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title = "Functional roles of Aves class-specific cis-regulatory elements on macroevolution of bird-specific features",

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.",

author = "Ryohei Seki and Cai Li and Qi Fang and Shinichi Hayashi and Shiro Egawa and Jiang Hu and Luohao Xu and Hailin Pan and Mao Kondo and Tomohiko Sato and Haruka Matsubara and Namiko Kamiyama and Keiichi Kitajima and Daisuke Saito and Yang Liu and Gilbert, {M. Thomas P} and Qi Zhou and Xing Xu and Toshihiko Shiroishi and Naoki Irie and Koji Tamura and Guojie Zhang",

note = "Funding Information: 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 Publisher Copyright: {\textcopyright} The Author(s) 2017.",

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AU - Seki, Ryohei

AU - Li, Cai

AU - Fang, Qi

AU - Hayashi, Shinichi

AU - Egawa, Shiro

AU - Hu, Jiang

AU - Xu, Luohao

AU - Pan, Hailin

AU - Kondo, Mao

AU - Sato, Tomohiko

AU - Matsubara, Haruka

AU - Kamiyama, Namiko

AU - Kitajima, Keiichi

AU - Saito, Daisuke

AU - Liu, Yang

AU - Gilbert, M. Thomas P

AU - Zhou, Qi

AU - Xu, Xing

AU - Shiroishi, Toshihiko

AU - Irie, Naoki

AU - Tamura, Koji

AU - Zhang, Guojie

N1 - Funding Information: 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 Publisher Copyright: © The Author(s) 2017.

PY - 2017/2/6

Y1 - 2017/2/6

N2 - 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.

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Functional roles of Aves class-specific cis-regulatory elements on macroevolution of bird-specific features

Abstract

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