Metazoan opsin evolution reveals a simple route to animal vision

被引:139
作者
Feuda, Roberto [1 ]
Hamilton, Sinead C. [1 ]
McInerney, James O. [1 ]
Pisani, Davide [1 ,2 ,3 ]
机构
[1] Natl Univ Ireland Maynooth, Dept Biol, Maynooth, Kildare, Ireland
[2] Univ Bristol, Sch Biol Sci, Bristol BS8 1UG, Avon, England
[3] Univ Bristol, Sch Earth Sci, Bristol BS8 1UG, Avon, England
基金
爱尔兰科学基金会;
关键词
ancestral character state reconstruction; Metazoa; protein evolution; GENOME; EYE; PHOTOTRANSDUCTION; DIVERSITY; FAMILIES; NEURONS; ORIGIN; LIGHT; TREE;
D O I
10.1073/pnas.1204609109
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
All known visual pigments in Neuralia (Cnidaria, Ctenophora, and Bilateria) are composed of an opsin (a seven-transmembrane G protein-coupled receptor), and a light-sensitive chromophore, generally retinal. Accordingly, opsins play a key role in vision. There is no agreement on the relationships of the neuralian opsin subfamilies, and clarifying their phylogeny is key to elucidating the origin of this protein family and of vision. We used improved methods and data to resolve the opsin phylogeny and explain the evolution of animal vision. We found that the Placozoa have opsins, and that the opsins share a common ancestor with the melatonin receptors. Further to this, we found that all known neuralian opsins can be classified into the same three subfamilies into which the bilaterian opsins are classified: the ciliary (C), rhabdomeric (R), and go-coupled plus retinochrome, retinal G protein-coupled receptor (Go/RGR) opsins. Our results entail a simple scenario of opsin evolution. The first opsin originated from the duplication of the common ancestor of the melatonin and opsin genes in a eumetazoan (Placozoa plus Neuralia) ancestor, and an inference of its amino acid sequence suggests that this protein might not have been light-sensitive. Two more gene duplications in the ancestral neuralian lineage resulted in the origin of the R, C, and Go/RGR opsins. Accordingly, the first animal with at least a C, an R, and a Go/ RGR opsin was a neuralian progenitor.
引用
收藏
页码:18868 / 18872
页数:5
相关论文
共 35 条
[1]   The dynamic genome of Hydra [J].
Chapman, Jarrod A. ;
Kirkness, Ewen F. ;
Simakov, Oleg ;
Hampson, Steven E. ;
Mitros, Therese ;
Weinmaier, Thomas ;
Rattei, Thomas ;
Balasubramanian, Prakash G. ;
Borman, Jon ;
Busam, Dana ;
Disbennett, Kathryn ;
Pfannkoch, Cynthia ;
Sumin, Nadezhda ;
Sutton, Granger G. ;
Viswanathan, Lakshmi Devi ;
Walenz, Brian ;
Goodstein, David M. ;
Hellsten, Uffe ;
Kawashima, Takeshi ;
Prochnik, Simon E. ;
Putnam, Nicholas H. ;
Shu, Shengquiang ;
Blumberg, Bruce ;
Dana, Catherine E. ;
Gee, Lydia ;
Kibler, Dennis F. ;
Law, Lee ;
Lindgens, Dirk ;
Martinez, Daniel E. ;
Peng, Jisong ;
Wigge, Philip A. ;
Bertulat, Bianca ;
Guder, Corina ;
Nakamura, Yukio ;
Ozbek, Suat ;
Watanabe, Hiroshi ;
Khalturin, Konstantin ;
Hemmrich, Georg ;
Franke, Andre ;
Augustin, Rene ;
Fraune, Sebastian ;
Hayakawa, Eisuke ;
Hayakawa, Shiho ;
Hirose, Mamiko ;
Hwang, Jung Shan ;
Ikeo, Kazuho ;
Nishimiya-Fujisawa, Chiemi ;
Ogura, Atshushi ;
Takahashi, Toshio ;
Steinmetz, Patrick R. H. .
NATURE, 2010, 464 (7288) :592-596
[2]   Gene regulatory networks and the evolution of animal body plans [J].
Davidson, EH ;
Erwin, DH .
SCIENCE, 2006, 311 (5762) :796-800
[3]   Broad phylogenomic sampling improves resolution of the animal tree of life [J].
Dunn, Casey W. ;
Hejnol, Andreas ;
Matus, David Q. ;
Pang, Kevin ;
Browne, William E. ;
Smith, Stephen A. ;
Seaver, Elaine ;
Rouse, Greg W. ;
Obst, Matthias ;
Edgecombe, Gregory D. ;
Sorensen, Martin V. ;
Haddock, Steven H. D. ;
Schmidt-Rhaesa, Andreas ;
Okusu, Akiko ;
Kristensen, Reinhardt Mobjerg ;
Wheeler, Ward C. ;
Martindale, Mark Q. ;
Giribet, Gonzalo .
NATURE, 2008, 452 (7188) :745-U5
[4]   The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals [J].
Erwin, Douglas H. ;
Laflamme, Marc ;
Tweedt, Sarah M. ;
Sperling, Erik A. ;
Pisani, Davide ;
Peterson, Kevin J. .
SCIENCE, 2011, 334 (6059) :1091-1097
[5]   Early origin of the bilaterian developmental toolkit [J].
Erwin, Douglas H. .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2009, 364 (1527) :2253-2261
[6]   Phototransduction and the Evolution of Photoreceptors [J].
Fain, Gordon L. ;
Hardie, Roger ;
Laughlin, Simon B. .
CURRENT BIOLOGY, 2010, 20 (03) :R114-R124
[7]   Modeling compositional heterogeneity [J].
Foster, PG .
SYSTEMATIC BIOLOGY, 2004, 53 (03) :485-495
[8]   The G-protein-coupled receptors in the human genome form five main families.: Phylogenetic analysis, paralogon groups, and fingerprints [J].
Fredriksson, R ;
Lagerström, MC ;
Lundin, LG ;
Schiöth, HB .
MOLECULAR PHARMACOLOGY, 2003, 63 (06) :1256-1272
[9]   Chance and Necessity in Eye Evolution [J].
Gehring, Walter J. .
GENOME BIOLOGY AND EVOLUTION, 2011, 3 :1053-1066
[10]   Deep Genomic-Scale Analyses of the Metazoa Reject Coelomata: Evidence from Single- and Multigene Families Analyzed Under a Supertree and Supermatrix Paradigm [J].
Holton, Therese A. ;
Pisani, Davide .
GENOME BIOLOGY AND EVOLUTION, 2010, 2 :310-324