title: Tetrapod V1R-like ora genes in an early-diverging ray-finned fish species: the canonical six ora gene repertoire of teleost fish resulted from gene loss in a larger ancestral repertoire.
abstract: BACKGROUND
  Chemical senses serve a multitude of essential functions across the animal kingdom. Vertebrates employ four GPCR families to detect odors, among them the v1r/ora gene family. The V1R family is known to evolve rapidly in the lobe-finned lineage giving rise to tetrapods, but the homologous ORA family consists of just six highly conserved genes in teleost fish, with direct orthologs in the lobe-finned fish coelacanth. Thus, the teleost repertoire of six canonical ora genes was assumed to be the ancestral feature before the divergence of ray-finned and lobe-finned fish. So far, this hypothesis has not been tested with earlier diverging ray-finned fish.
  
  
  RESULTS
  We have newly identified the complete ora gene repertoires of five teleost species, and of spotted gar, a basal ray-finned fish, using thorough data mining and extensive phylogenetic analysis. The genomes of eight further teleost species were re-analyzed for their ORA repertoires. We report that direct orthologs of the six canonical ora genes (ora1-6) were present in all newly analyzed species, with faithfully preserved exon/intron structure and mostly preserved genomic arrangement in symmetric pairs for ora1-4. In four teleost species including medaka and cave fish we observe species-specific gene duplication events. Thus, the ora gene repertoire in teleost fish is not quite as strictly conserved as previously assumed. In fact, the examination of non-synonymous vs. synonymous substitution rates (dN/dS) shows pronounced negative selection in five of the six ora genes, but also rare occurrence of positive selection in ora3 and ora6. Surprisingly, spotted gar possesses beyond the six canonical genes three additional genes, ora7-8b, orthologous to coelacanth genes v1r07-10. No orthologs for these genes were found in teleosts and cartilaginous fish.
  
  
  CONCLUSIONS
  Early diverging ray-finned fish such as the spotted gar possess several v1r-like genes previously assumed to be restricted to the lobe-finned lineage, but now found to be already present in the most recent common ancestor of lobe- and ray-finned fish. Thus, the presence of just six canonical ora genes in many teleost species is not the ancestral feature of the ray-finned lineage, but caused by loss of two ancestral genes in teleosts.
authors.affiliation: Institute of Genetics, University of Cologne, 50674, Cologne, Germany.
authors.forename: Veronika
authors.initials: V
authors.lastname: Zapilko
authors.affiliation: Institute of Genetics, University of Cologne, 50674, Cologne, Germany. sigrun.korsching@uni-koeln.de.
authors.forename: Sigrun I
authors.initials: SI
authors.lastname: Korsching
mesh_terms: D000818:Animals; D019143:Evolution, Molecular; D005399:Fishes / Q000235:genetics*; D020440:Gene Duplication / Q000235:genetics; D014714:Vertebrates / Q000235:genetics*
references.citation: Mol Biol Evol. 2009 Feb;26(2):407-19
references.pmid: 19008528
references.citation: Bioinformatics. 2009 May 1;25(9):1189-91
references.pmid: 19151095
references.citation: Genome Res. 2010 Jan;20(1):10-8
references.pmid: 19952141
references.citation: Mar Genomics. 2008 Mar;1(1):23-31
references.pmid: 21798150
references.citation: Genome Res. 2007 Feb;17(2):166-74
references.pmid: 17210926
references.citation: Bioinformatics. 2008 Feb 15;24(4):492-7
references.pmid: 18174178
references.citation: Mol Biol Evol. 2013 Apr;30(4):772-80
references.pmid: 23329690
references.citation: Nature. 2011 Oct 13;478(7368):241-5
references.pmid: 21937988
references.citation: Genome Res. 2005 Feb;15(2):231-40
references.pmid: 15653832
references.citation: Bioinformatics. 2005 May 15;21(10):2531-3
references.pmid: 15713735
references.citation: J Biol Chem. 2014 Jul 11;289(28):19778-88
references.pmid: 24831010
references.citation: Mol Biol Evol. 1999 Oct;16(10):1315-28
references.pmid: 10563013
references.citation: Comp Biochem Physiol C Toxicol Pharmacol. 2014 Jun;163:24-36
references.pmid: 24486528
references.citation: Genome Res. 2013 Oct;23(10):1740-8
references.pmid: 23878157
references.citation: J Fish Biol. 2012 Jul;81(2):559-75
references.pmid: 22803724
references.citation: PLoS One. 2007;2(8):e708
references.pmid: 17684554
references.citation: BMC Genomics. 2014;15:650
references.pmid: 25091523
references.citation: Methods Mol Biol. 2009;537:163-83
references.pmid: 19378144
references.citation: Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W465-9
references.pmid: 18424797
references.citation: Gene. 2012 May 15;499(2):273-9
references.pmid: 22450365
references.citation: Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
references.pmid: 12136088
references.citation: BMC Evol Biol. 2010;10:8
references.pmid: 20067610
references.citation: Genome Res. 2004 May;14(5):988-95
references.pmid: 15123596
references.citation: BMC Genomics. 2014;15:586
references.pmid: 25015101
references.citation: Mol Biol Evol. 2007 Oct;24(10):2153-7
references.pmid: 17666439
references.citation: BMC Evol Biol. 2009;9:194
references.pmid: 19664233
references.citation: Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4313-8
references.pmid: 19237578
references.citation: J Hered. 2011 Jan-Feb;102(1):113-7
references.pmid: 20881030
references.citation: Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W609-12
references.pmid: 16845082
references.citation: BMC Bioinformatics. 2006;7:439
references.pmid: 17032440
references.citation: Genome Res. 2003 Apr;13(4):533-43
references.pmid: 12670995
references.citation: Nat Rev Genet. 2008 Dec;9(12):951-63
references.pmid: 19002141
references.citation: Can J Physiol Pharmacol. 2003 Apr;81(4):329-41
references.pmid: 12769225
references.citation: Genome Biol Evol. 2014 May;6(5):1135-44
references.pmid: 24803573
references.citation: PLoS One. 2007;2(4):e379
references.pmid: 17440615
references.citation: Gene. 2011 Oct 1;485(1):16-21
references.pmid: 21712081
references.citation: BMC Evol Biol. 2007 Oct 12;7:192
references.pmid: 17935625
references.citation: Syst Biol. 2010 May;59(3):307-21
references.pmid: 20525638
references.citation: Proc Natl Acad Sci U S A. 2005 Apr 12;102(15):5489-94
references.pmid: 15809442
references.citation: Nature. 2014 Jan 9;505(7482):174-9
references.pmid: 24402279
references.citation: Genome Res. 2007 Oct;17(10):1448-57
references.pmid: 17717047