The sea lamprey Petromyzon marinus genome reveals the early origin of several chemosensory receptor families in the vertebrate lineage

BackgroundIn gnathostomes, chemosensory receptors (CR) expressed in olfactory epithelia are encoded by evolutionarily dynamic gene families encoding odorant receptors (OR), trace amine-associated receptors (TAAR), V1Rs and V2Rs. A limited number of OR-like sequences have been found in invertebrate chordate genomes. Whether these gene families arose in basal or advanced vertebrates has not been resolved because these families have not been examined systematically in agnathan genomes.ResultsPetromyzon is the only extant jawless vertebrate whose genome has been sequenced. Known to be exquisitely sensitive to several classes of odorants, lampreys detect fewer amino acids and steroids than teleosts. This reduced number of detectable odorants is indicative of reduced numbers of CR gene families or a reduced number of genes within CR families, or both, in the sea lamprey. In the lamprey genome we identified a repertoire of 59 intact single-exon CR genes, including 27 OR, 28 TAAR, and four V1R-like genes. These three CR families were expressed in the olfactory organ of both parasitic and adult life stages.ConclusionAn extensive search in the lamprey genome failed to identify potential orthologs or pseudogenes of the multi-exon V2R family that is greatly expanded in teleost genomes, but did find intact calcium-sensing receptors (CASR) and intact metabotropic glutamate receptors (MGR). We conclude that OR and V1R arose in chordates after the cephalochordate-urochordate split, but before the diversification of jawed and jawless vertebrates. The advent and diversification of V2R genes from glutamate receptor-family G protein-coupled receptors, most likely the CASR, occurred after the agnathan-gnathostome divergence.

[1]  Michael I. Coates,et al.  A lamprey from the Devonian period of South Africa , 2006, Nature.

[2]  D G Higgins,et al.  CLUSTAL V: multiple alignment of DNA and protein sequences. , 1994, Methods in molecular biology.

[3]  Richard Axel,et al.  Coding of olfactory information: Topography of odorant receptor expression in the catfish olfactory epithelium , 1993, Cell.

[4]  P. Bork,et al.  Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. , 2006, Developmental biology.

[5]  M. Nishida,et al.  Evolution and origin of vomeronasal-type odorant receptor gene repertoire in fishes , 2006, BMC Evolutionary Biology.

[6]  S. Karlin,et al.  Prediction of complete gene structures in human genomic DNA. , 1997, Journal of molecular biology.

[7]  A. Chess,et al.  The family of genes encoding odorant receptors in the channel catfish , 1993, Cell.

[8]  G. Satoh Characterization of novel GPCR gene coding locus in amphioxus genome: Gene structure, expression, and phylogenetic analysis with implications for its involvement in chemoreception , 2005, Genesis.

[9]  Nicholas H. Putnam,et al.  The amphioxus genome and the evolution of the chordate karyotype , 2008, Nature.

[10]  R Fredriksson,et al.  High Species Variation within the Repertoire of Trace Amine Receptors , 2005, Annals of the New York Academy of Sciences.

[11]  Jianzhi Zhang,et al.  Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. , 2007, Genome research.

[12]  M. Nei,et al.  Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates , 2006, Journal of Human Genetics.

[13]  Robert Miller,et al.  STACK: Sequence Tag Alignment and Consensus Knowledgebase , 2001, Nucleic Acids Res..

[14]  P. Sorensen,et al.  The olfactory system of migratory adult sea lamprey (Petromyzon marinus) is specifically and acutely sensitive to unique bile acids released by conspecific larvae , 1995, The Journal of general physiology.

[15]  A. Berghard,et al.  A novel family of ancient vertebrate odorant receptors. , 1998, Journal of neurobiology.

[16]  Weiming Li Potential multiple functions of a male sea lamprey pheromone. , 2005, Chemical senses.

[17]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[18]  S. Korsching,et al.  A novel olfactory receptor gene family in teleost fish. , 2007, Genome research.

[19]  N. Manoj,et al.  The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis , 2008, BMC Evolutionary Biology.

[20]  J. Ngai,et al.  The odorant receptor repertoire of teleost fish , 2005, BMC Genomics.

[21]  I. Rodriguez,et al.  Olfactory expression of a single and highly variable V1r pheromone receptor-like gene in fish species. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Martin Ebeling,et al.  Trace amine-associated receptors form structurally and functionally distinct subfamilies of novel G protein-coupled receptors. , 2005, Genomics.

[23]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[24]  J. Taylor,et al.  A genomic view of the sea urchin nervous system. , 2006, Developmental biology.

[25]  Mutsumi Nishida,et al.  Evolution of trace amine associated receptor (TAAR) gene family in vertebrates: lineage-specific expansions and degradations of a second class of vertebrate chemosensory receptors expressed in the olfactory epithelium. , 2007, Molecular biology and evolution.

[26]  John Quackenbush,et al.  TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets , 2003, Bioinform..

[27]  H. Breer,et al.  Olfactory receptors in aquatic and terrestrial vertebrates , 1998, Journal of Comparative Physiology A.

[28]  Jianzhi Zhang,et al.  Origin of the genetic components of the vomeronasal system in the common ancestor of all extant vertebrates. , 2009, Molecular biology and evolution.

[29]  R. Dubuc,et al.  Olfactory sensory neurons in the sea lamprey display polymorphisms , 2007, Neuroscience Letters.

[30]  S. Altschul A protein alignment scoring system sensitive at all evolutionary distances , 1993, Journal of Molecular Evolution.

[31]  J. Teeter Pheromone Communication in Sea Lampreys (Petromyzon marinus): Implications for Population Management , 1980 .

[32]  C. Greer,et al.  Glomerular territories in the olfactory bulb from the larval stage of the sea lamprey Petromyzon marinus , 2003, The Journal of comparative neurology.

[33]  D. T. Jones,et al.  Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. , 1989, Science.

[34]  H. Schiöth,et al.  The amphioxus (Branchiostoma floridae) genome contains a highly diversified set of G protein-coupled receptors , 2008, BMC Evolutionary Biology.

[35]  R. Axel,et al.  A novel multigene family may encode odorant receptors: A molecular basis for odor recognition , 1991, Cell.

[36]  Mee-mann Chang,et al.  A lamprey from the Cretaceous Jehol biota of China , 2006, Nature.

[37]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[38]  L. Buck,et al.  The human olfactory receptor gene family. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[39]  H. Eisthen,et al.  Evolution of Vertebrate Olfactory Systems , 1997 .

[40]  H. Breer,et al.  On the origin of the olfactory receptor family: receptor genes of the jawless fish (Lampetra fluviatilis). , 1999, Gene.

[41]  I. Rodriguez,et al.  Divergent Evolution among Teleost V1r Receptor Genes , 2007, PloS one.