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Genome Biology and Evolution Advance Access published online on April 30, 2009
Genome Biology and Evolution, doi:10.1093/gbe/evp003
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© 2009 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

On the Origin and Evolution of Vertebrate Olfactory Receptor Genes: Comparative Genome Analysis among 23 Chordate Species

Yoshihito Niimura*

Department of Bioinformatics, Medical Research Institute, Tokyo Medical and Dental University, Tokyo, Japan

* Author for Correspondence: Yoshihito Niimura, Department of Bioinformatics, Medical Research Institute, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, JAPAN, Tel: +81-3-5803-4595, Fax: +81-3-5803-0247, E-mail: niimura{at}bioinfo.tmd.ac.jp


  Abstract

Olfaction is a primitive sense in organisms. Both vertebrates and insects have receptors for detecting odor molecules in the environment, but the evolutionary origins of these genes are different. Among studied vertebrates, mammals have ~1,000 olfactory receptor (OR) genes, while teleost fishes have much smaller (~100) numbers of OR genes. To investigate the origin and evolution of vertebrate OR genes, I attempted to determine near-complete OR gene repertories by searching whole-genome sequences of 14 non-mammalian chordates, including cephalochordates (amphioxus), urochordates (ascidian and larvacean), and vertebrates (sea lamprey, elephant shark, five teleost fishes, frog, lizard, and chicken), followed by a large-scale phylogenetic analysis in conjunction with mammalian OR genes identified from nine species. This analysis showed that the amphioxus has >30 vertebrate-type OR genes though it lacks distinctive olfactory organs, while all OR genes appear to have been lost in the urochordate lineage. Some groups of genes ({theta}, {kappa}, and {lambda}) that are phylogenetically nested within vertebrate OR genes showed few gene gains and losses, which is in sharp contrast to the evolutionary pattern of OR genes, suggesting that they are actually non-OR genes. Moreover, the analysis demonstrated a great difference in OR gene repertoires between aquatic and terrestrial vertebrates, reflecting the necessity for the detection of water-soluble and airborne odorants, respectively. However, a minor group (β) of genes that are atypically present in both aquatic and terrestrial vertebrates was also found. These findings should provide a critical foundation for further physiological, behavioral, and evolutionary studies of olfaction in various organisms.

Keywords: olfactory receptor, multigene family, molecular evolution, chordate, vertebrate, amphioxus

Received January 13, 2009; Revised March 25, 2009; Accepted March 25, 2009


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