The African coelacanth genome provides insights into tetrapod evolution.

Animals; Animals, Genetically Modified; Biological Evolution; Chick Embryo; Conserved Sequence/genetics; Enhancer Elements, Genetic/genetics; Evolution, Molecular; Extremities/anatomy & histology/growth & development; Fishes/anatomy & histology/classification/genetics/physiology; Genes, Homeobox/genetics; Genome/genetics; Genomics; Immunoglobulin M/genetics; Mice; Molecular Sequence Annotation; Molecular Sequence Data; Phylogeny; Sequence Alignment; Sequence Analysis, DNA; Vertebrates/anatomy & histology/genetics/physiology

Abstract :

[en] The discovery of a living coelacanth specimen in 1938 was remarkable, as this lineage of lobe-finned fish was thought to have become extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features. Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues show the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.

Disciplines :

Genetics & genetic processes
Biochemistry, biophysics & molecular biology
Zoology

Author, co-author :

Amemiya, Chris T.

Alfoldi, Jessica

Lee, Alison P.

Fan, Shaohua

Philippe, Herve

Maccallum, Iain

Braasch, Ingo

Manousaki, Tereza

Schneider, Igor

Rohner, Nicolas

More authors (81 more)

Language :

English

Title :

The African coelacanth genome provides insights into tetrapod evolution.

Publication date :

2013

Journal title :

Nature

ISSN :

0028-0836

eISSN :

1476-4687

Publisher :

Nature Publishing Group, London, United Kingdom

Volume :

496

Issue :

7445

Pages :

311-6

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www.nature.com/nature/journal/v496/n7445/full/nature12027.html

Available on ORBi :

since 16 May 2013

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Scopus citations^®

546

Scopus citations^®
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437

OpenCitations

542

Bibliography

Smith, J. L. B. A living fish of mesozoic type. Nature 143, 455-456 (1939).
Nulens, R., Scott, L.&Herbin, M. AnUpdated Inventory of All Known Specimens of the Coelacanth, Latimeria Spp. Smithiana Vol. 3 (South African Institute for Aquatic Biodiversity, 2010).
Erdmann, M. V., Caldwell, R. L. & Kasim Moosa, M. Indonesian 'king of the sea' discovered. Nature 395, 335 (1998).
Smith, J. L. B. Old Fourlegs: the Story of the Coelacanth (Longmans, Green, 1956).
Zhu, M. et al. Earliest known coelacanth skull extends the range of anatomically modern coelacanths to the Early Devonian. Nature Commun. 3, 772 (2012).
Zimmer, C. At the Water's Edge: Fish with Fingers, Whales with Legs, and How Life Came Ashore but then Went Back to Sea (Free Press, 1999).
Zardoya, R.&Meyer, A. The completeDNAsequence of the mitochondrial genome of a "living fossil," the coelacanth (Latimeria chalumnae). Genetics 146, 995-1010 (1997).
Amemiya, C. T. et al. Complete HOX cluster characterization of the coelacanth provides further evidence for slowevolution of its genome. Proc.Natl Acad. Sci.USA 107, 3622-3627.
Larsson, T. A., Larson, E. T. & Larhammar, D. Cloning and sequence analysis of the neuropeptide Y receptors Y5 and Y6 in the coelacanth Latimeria chalumnae. Gen. Comp. Endocrinol. 150, 337-342 (2007).
Noonan, J. P. et al. Coelacanth genome sequence reveals the evolutionary history of vertebrate genes. Genome Res. 14, 2397-2405 (2004).
Gnerre, S. et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl Acad. Sci. USA 108, 1513-1518 (2011).
Bogart, J. P., Balon, E. K.& Bruton, M. N. The chromosomes of the living coelacanth and their remarkable similarity to those of one of the most ancient frogs. J. Hered. 85, 322-325 (1994).
Cantarel, B. L. et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 18, 188-196 (2008).
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotech. 29, 644-652 (2011).
Pallavicini, A. et al. Analysis of the transcriptome of the Indonesian coelacanth Latimeria menadoensis. BMC Genomics (in the press).
Schultze, H. P.&Trueb, L. Origins of the Higher Groups of Tetrapods: Controversy and Consensus. (Comstock Publishing Associates, 1991).
Meyer, A. & Dolven, S. I. Molecules, fossils, and the origin of tetrapods. J. Mol. Evol. 35, 102-113 (1992).
Brinkmann, H., Venkatesh, B., Brenner, S. & Meyer, A. Nuclear protein-coding genessupport lungfish andnot the coelacanth as the closest living relatives of land vertebrates. Proc. Natl Acad. Sci. USA 101, 4900-4905 (2004).
Lartillot, N.&Philippe, H.A Bayesian mixturemodel for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 21, 1095-1109 (2004).
Takezaki, N., Rzhetsky, A. & Nei, M. Phylogenetic test of the molecular clock and linearized trees. Mol. Biol. Evol. 12, 823-833 (1995).
Tajima, F. Simplemethods for testing themolecular evolutionary clock hypothesis. Genetics 135, 599-607 (1993).
Bejerano, G. et al. A distal enhancer and an ultraconserved exon are derived froma novel retroposon. Nature 441, 87-90 (2006).
Voss, S. R. et al. Origin ofamphibian and avian chromosomes by fission, fusion, and retention of ancestral chromosomes. Genome Res. 21, 1306-1312 (2011).
Smith, J. J. & Voss, S. R. Gene order data from a model amphibian (Ambystoma): newperspectives on vertebrate genomestructure andevolution. BMCGenomics 7, 219 (2006).
Inoue, J. G., Miya, M., Venkatesh, B. & Nishida, M. The mitochondrial genome of Indonesian coelacanth Latimeria menadoensis (Sarcopterygii: Coelacanthiformes) and divergence time estimation between the two coelacanths. Gene 349, 227-235 (2005).
Holder, M. T., Erdmann, M. V., Wilcox, T. P., Caldwell, R. L. & Hillis, D. M. Two living species of coelacanths? Proc. Natl Acad. Sci. USA 96, 12616-12620 (1999).
Canapa, A. et al. Composition and phylogenetic analysis of vitellogenin coding sequences in the Indonesian coelacanth Latimeriamenadoensis. J. Exp. Zool..B 318, 404-416 (2012).
The Chimpanzee Sequencing and Analysis Consortium. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437, 69-87 (2005).
Zhang, J. et al. Loss of fish actinotrichia proteins and the fin-to-limb transition. Nature 466, 234-237 (2010).
Jovelin, R. et al. Evolution of developmental regulation in the vertebrate FgfD subfamily. J. Exp. Zool.B 314, 33-56 (2010).
Braasch, I. & Postlethwait, J. H. The teleost agouti-related protein 2 gene is an ohnolog gone missing from the tetrapod genome. Proc. Natl Acad. Sci. USA 108, E47-E48 (2011).
Navratilova, P. et al. Systematic human/zebrafish comparative identification of cisregulatory activity around vertebrate developmental transcription factor genes. Dev. Biol 327, 526-540 (2009).
Xie, X. et al. Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites. Proc. Natl Acad. Sci. USA 104, 7145-7150 (2007).
Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55-61 (2012).
Shubin, N., Tabin, C. & Carroll, S. Deep homology and the origins of evolutionary novelty. Nature 457, 818-823 (2009).
Montavon, T. et al. A regulatory archipelago controls Hox genes transcription in digits. Cell 147, 1132-1145 (2011).
Wright, P. A. Nitrogen excretion: three end products, many physiological roles. J. Exp. Biol. 198, 273-281 (1995).
Kosakovsky Pond, S. L. et al. A random effects branch-site model for detecting episodic diversifying selection. Mol. Biol. Evol. 28, 3033-3043 (2011).
Häberle, J. et al. Molecular defects in human carbamoy phosphate synthetase I: mutational spectrum, diagnostic and protein structure considerations. Hum. Mutat. 32, 579-589 (2011).
Carroll, R. L. Vertebrate Paleontology and Evolution (W.H. Freeman and Company, 1988).
Gekas, C. et al. Hematopoietic stem cell development in the placenta. Int. J. Dev. Biol. 54, 1089-1098 (2010).
Bejerano, G. et al. Ultraconserved elements in the human genome. Science 304, 1321-3125 (2004).
Wellik, D. M. Hox patterning of the vertebrate axial skeleton. Dev. Dyn. 236, 2454-2463 (2007).
Scotti, M. & Kmita, M. Recruitment of 59 Hoxa genes in the allantois is essential for proper extra-embryonic function in placental mammals. Development 139, 731-730 (2012).
Bengtén, E. et al. Immunoglobulin isotypes: structure, function, and genetics. Curr. Top. Microbiol. Immunol. 248, 189-219 (2000).
Ota, T., Rast, J. P., Litman, G. W. & Amemiya, C. T. Lineage-restricted retention of a primitive immunoglobulin heavy chain isotype within the Dipnoi reveals an evolutionary paradox. Proc. Natl Acad. Sci. USA 100, 2501-2506 (2003).
Gregory, T. R. The Evolution of the Genome 1-71 (Elsevier Academic, 2004).
Stamatakis, A., Ludwig, T. & Meier, H. RAxML-III: a fast program for maximum likelihood-basedinference of large phylogenetic trees. Bioinformatics21, 456-463 (2005).
Smith, J. J., Sumiyama, K. & Amemiya, C. T. A living fossil in the genome of a living fossil: Harbinger transposons in the coelacanth genome.Mol. Biol. Evol. 29, 985-993 (2012).