Skip to main content
SpringerLink
Log in

The Molecular Evolution of Teleost Olfactory Receptor Gene Families

  • Chapter
  • First Online:
Chemosensory Systems in Mammals, Fishes, and Insects

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 47))

Abstract

Four olfactory receptor gene families, all of them G protein-coupled receptors, have been identified and characterized in mammals – the odorant (OR), vomeronasal (V1R and V2R) and trace amine-associated (TAARs) receptors. Much less attention has been directed towards non-mammalian members of these families. Since a hallmark of mammalian olfactory receptors is their remarkable species specificity, an evaluation of the non-mammalian olfactory receptors is instructive both for comparative purposes and in its own right. In this review I have compiled the results currently available for all four olfactory gene families and discuss their phylogenomic properties in relation to their mammalian counterparts. Representatives of all four families are found in cartilaginous fish and/or jawless fish, allowing a minimal estimate for the evolutionary origin as preceding the segregation between cartilaginous and bony fish or cartilaginous and jawless fish, respectively. Gene repertoires of teleost olfactory receptors are smaller in size (OR, ORA), comparable (olfC), or even larger (TAAR) than the corresponding mammalian gene repertoires. Despite their smaller repertoire size, the teleost OR and ORA families show much larger divergence than their mammalian counterparts. Evolutionary rates vary greatly between families, with evidence for positive selection in teleost OR genes, whereas the ora genes are subject to strong negative selection, and in fact are being conserved among all teleost species investigated. With one exception, ligands are unknown for any of the four teleost olfactory receptor gene families, and so the considerable knowledge about the odor responses of the olfactory epithelium and the olfactory bulb can only be linked indirectly to the receptor repertoires.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alioto TS, Ngai J (2005) The odorant receptor repertoire of teleost fish. BMC Genomics 6:173

    Article  PubMed  Google Scholar 

  • Alioto TS, Ngai J (2006) The repertoire of olfactory C family G protein-coupled receptors in zebrafish: candidate chemosensory receptors for amino acids. BMC Genomics 7:309

    Article  PubMed  Google Scholar 

  • Baier H, Korsching S (1994) Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals. J Neurosci 14:219–230

    PubMed  CAS  Google Scholar 

  • Barth AL, Dugas JC, Ngai J (1997) Noncoordinate expression of odorant receptor genes tightly linked in the zebrafish genome. Neuron 19:359–369

    Article  PubMed  CAS  Google Scholar 

  • Berghard A, Dryer L (1998) A novel family of ancient vertebrate odorant receptors. J Neurobiol 37:383–392

    Article  PubMed  CAS  Google Scholar 

  • Bingham J, Sudarsanam S (2000) Visualizing large hierarchical clusters in hyperbolic space. Bioinformatics 16:660–661

    Article  PubMed  CAS  Google Scholar 

  • Borowsky B, Adham N, Jones KA, Raddatz R, Artymyshyn R, Ogozalek KL, Durkin MM, Lakhlani PP, Bonini JA, Pathirana S et al. (2001) Trace amines: identification of a family of mammalian G protein-coupled receptors. Proc Natl Acad Sci USA 98:8966–8971

    Article  PubMed  CAS  Google Scholar 

  • Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611–618

    Article  PubMed  CAS  Google Scholar 

  • Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  PubMed  CAS  Google Scholar 

  • Bustamante CD, Fledel-Alon A, Williamson S, Nielsen R, Hubisz MT, Glanowski S, Tanenbaum DM, White TJ, Sninsky JJ, Hernandez RD et al. (2005) Natural selection on protein-coding genes in the human genome. Nature 437:1153–1157

    Article  PubMed  CAS  Google Scholar 

  • Coulombe-Huntington J, Majewski J (2007) Characterization of intron loss events in mammals. Genome Res 17:23–32

    Article  PubMed  CAS  Google Scholar 

  • Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195–206

    Article  PubMed  CAS  Google Scholar 

  • Elgar G (1996) Quality not quantity: the pufferfish genome. Hum Mol Genet 5:(Spec No)1437–1442

    PubMed  CAS  Google Scholar 

  • Freitag J, Beck A, Ludwig G, von Buchholtz L, Breer H (1999) On the origin of the olfactory receptor family: receptor genes of the jawless fish (Lampetra fluviatilis). Gene 226:165–174

    Article  PubMed  CAS  Google Scholar 

  • Fried HU, Fuss SH, Korsching SI (2002) Selective imaging of presynaptic activity in the mouse olfactory bulb shows concentration and structure dependence of odor responses in identified glomeruli. Proc Natl Acad Sci USA 99:3222–3227

    Article  PubMed  CAS  Google Scholar 

  • Friedrich RW, Korsching SI (1997) Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18:737–752

    Article  PubMed  CAS  Google Scholar 

  • Friedrich RW, Korsching SI (1998) Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. J Neurosci 18:9977–9988

    PubMed  CAS  Google Scholar 

  • Fukuda N, Yomogida K, Okabe M, Touhara K (2004) Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility. J Cell Sci 117:5835–5845

    Article  PubMed  CAS  Google Scholar 

  • Fuss SH, Korsching SI (2001) Odorant feature detection: activity mapping of structure response relationships in the zebrafish olfactory bulb. J Neurosci 21:8396–8407

    PubMed  CAS  Google Scholar 

  • Gloriam DE, Bjarnadottir TK, Yan YL, Postlethwait JH, Schioth HB, Fredriksson R (2005) The repertoire of trace amine G-protein-coupled receptors: large expansion in zebrafish. Mol Phylogenet Evol 35:470–482

    Article  PubMed  CAS  Google Scholar 

  • Grus WE, Shi P, Zhang YP, Zhang J (2005) Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. Proc Natl Acad Sci USA 102:5767–5772

    Article  PubMed  CAS  Google Scholar 

  • Hamdani El H, Doving KB (2002) The alarm reaction in crucian carp is mediated by olfactory neurons with long dendrites. Chem Senses 27:395–398

    Article  PubMed  Google Scholar 

  • Hamdani El H, Doving KB (2006) Specific projection of the sensory crypt cells in the olfactory system in crucian carp, Carassius carassius. Chem Senses 31:63–67

    Article  PubMed  Google Scholar 

  • Hamdani El H, Doving KB (2007) The functional organization of the fish olfactory system. Prog Neurobiol 82:80–86

    Article  PubMed  Google Scholar 

  • Hansen A, Zielinski BS (2005) Diversity in the olfactory epithelium of bony fishes: development, lamellar arrangement, sensory neuron cell types and transduction components. J Neurocytol 34:183–208

    Article  PubMed  CAS  Google Scholar 

  • Hansen A, Rolen SH, Anderson K, Morita Y, Caprio J, Finger TE (2003) Correlation between olfactory receptor cell type and function in the channel catfish. J Neurosci 23:9328–9339

    PubMed  CAS  Google Scholar 

  • Hansen A, Anderson KT, Finger TE (2004) Differential distribution of olfactory receptor neurons in goldfish: structural and molecular correlates. J Comp Neurol 477:347–359

    Article  PubMed  CAS  Google Scholar 

  • Hashiguchi Y, Nishida M (2006) Evolution and origin of vomeronasal-type odorant receptor gene repertoire in fishes. BMC Evol Biol 6:76

    Article  PubMed  Google Scholar 

  • Hashiguchi Y, Nishida M (2007) 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. Mol Biol Evol 24:2099–2107

    Article  PubMed  CAS  Google Scholar 

  • Hoppe R, Lambert TD, Samollow PB, Breer H, Strotmann J (2006) Evolution of the “OR37” subfamily of olfactory receptors: a cross-species comparison. J Mol Evol 62:460–472

    Article  PubMed  CAS  Google Scholar 

  • Hu J, Zhong C, Ding C, Chi Q, Walz A, Mombaerts P, Matsunami H, Luo M (2007) Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 317:953–957

    Article  PubMed  CAS  Google Scholar 

  • Irie-Kushiyama S, Asano-Miyoshi M, Suda T, Abe K, Emori Y (2004) Identification of 24 genes and two pseudogenes coding for olfactory receptors in Japanese loach, classified into four subfamilies: a putative evolutionary process for fish olfactory receptor genes by comprehensive phylogenetic analysis. Gene 325:123–135

    Article  PubMed  CAS  Google Scholar 

  • Kajiya K, Inaki K, Tanaka M, Haga T, Kataoka H, Touhara K (2001) Molecular bases of odor discrimination: Reconstitution of olfactory receptors that recognize overlapping sets of odorants. J Neurosci 21:6018–6025

    PubMed  CAS  Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298

    Article  PubMed  CAS  Google Scholar 

  • Lane RP, Young J, Newman T, Trask BJ (2004) Species specificity in rodent pheromone receptor repertoires. Genome Res 14:603–608

    Article  PubMed  CAS  Google Scholar 

  • Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714

    Article  PubMed  CAS  Google Scholar 

  • Lastein S, Hamdani El H, Doving KB (2006) Gender distinction in neural discrimination of sex pheromones in the olfactory bulb of crucian carp, Carassius carassius. Chem Senses 31:69–77

    Article  PubMed  CAS  Google Scholar 

  • Leinders-Zufall T, Cockerham RE, Michalakis S, Biel M, Garbers DL, Reed RR, Zufall F, Munger SD (2007) Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc Natl Acad Sci USA 104:14507–14512

    Article  PubMed  CAS  Google Scholar 

  • Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645–650

    Article  PubMed  CAS  Google Scholar 

  • Loh YH, Brenner S, Venkatesh B (2008) Investigation of loss and gain of introns in the compact genomes of pufferfishes (Fugu and Tetraodon). Mol Biol Evol 25:526–535

    Article  PubMed  CAS  Google Scholar 

  • Luu P, Acher F, Bertrand HO, Fan J, Ngai J (2004) Molecular determinants of ligand selectivity in a vertebrate odorant receptor. J Neurosci 24:10128–10137

    Article  PubMed  CAS  Google Scholar 

  • Ma M (2007) Encoding olfactory signals via multiple chemosensory systems. Crit Rev Biochem Mol Biol 42:463–480

    Article  PubMed  CAS  Google Scholar 

  • Matsunami H, Buck LB (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775–784

    Article  PubMed  CAS  Google Scholar 

  • Michel WC, Sanderson MJ, Olson JK, Lipschitz DL (2003) Evidence of a novel transduction pathway mediating detection of polyamines by the zebrafish olfactory system. J Exp Biol 206:1697–1706

    Article  PubMed  CAS  Google Scholar 

  • Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278

    Article  PubMed  CAS  Google Scholar 

  • Morita Y, Finger TE (1998) Differential projections of ciliated and microvillous olfactory receptor cells in the catfish, Ictalurus punctatus. J Comp Neurol 398:539–550

    Article  PubMed  CAS  Google Scholar 

  • Nakatani Y, Takeda H, Kohara Y, Morishita S (2007) Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 17:1254–1265

    Article  PubMed  CAS  Google Scholar 

  • Ngai J, Dowling MM, Buck L, Axel R, Chess A (1993) The family of genes encoding odorant receptors in the channel catfish. Cell 72:657–666

    Article  PubMed  CAS  Google Scholar 

  • Niimura Y, Nei M (2005) Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods. Proc Natl Acad Sci USA 102:6039–6044

    Article  PubMed  CAS  Google Scholar 

  • Nikonov AA, Caprio J (2007) Highly specific olfactory receptor neurons for types of amino acids in the channel catfish. J Neurophysiol 98:1909–1918

    Article  PubMed  CAS  Google Scholar 

  • Pfister P, Rodriguez I (2005) Olfactory expression of a single and highly variable V1r pheromone receptor-like gene in fish species. Proc Natl Acad Sci USA 102:5489–5494

    Article  PubMed  CAS  Google Scholar 

  • Pfister P, Randall J, Montoya-Burgos JI, Rodriguez I (2007) Divergent evolution among teleost V1r receptor genes. PLoS ONE 2:e379

    Article  PubMed  Google Scholar 

  • Restrepo D, Miyamoto T, Bryant BP, Teeter JH (1990) Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science 249:1166–1168

    Article  PubMed  CAS  Google Scholar 

  • Rolen SH, Sorensen PW, Mattson D, Caprio J (2003) Polyamines as olfactory stimuli in the goldfish Carassius auratus. J Exp Biol 206:1683–1696

    Article  PubMed  CAS  Google Scholar 

  • Ryba NJ, Tirindelli R (1997) A new multigene family of putative pheromone receptors. Neuron 19:371–379

    Article  PubMed  CAS  Google Scholar 

  • Saraiva LR, Korsching SI (2007) A novel olfactory receptor gene family in teleost fish. Genome Res 17:1448–1457

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Miyasaka N, Yoshihara Y (2005) Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish. J Neurosci 25:4889–4897

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Miyasaka N, Yoshihara Y (2007) Hierarchical regulation of odorant receptor gene choice and subsequent axonal projection of olfactory sensory neurons in zebrafish. J Neurosci 27:1606–1615

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006

    Article  PubMed  CAS  Google Scholar 

  • Schmachtenberg O (2006) Histological and electrophysiological properties of crypt cells from the olfactory epithelium of the marine teleost Trachurus symmetricus. J Comp Neurol 495:113–121

    Article  PubMed  Google Scholar 

  • Shi P, Zhang J (2007) Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Res 17:166–174

    Article  PubMed  CAS  Google Scholar 

  • Silvotti L, Giannini G, Tirindelli R (2005) The vomeronasal receptor V2R2 does not require escort molecules for expression in heterologous systems. Chem Senses 30:1–8

    Article  PubMed  CAS  Google Scholar 

  • Speca DJ, Lin DM, Sorensen PW, Isacoff EY, Ngai J, Dittman AH (1999) Functional identification of a goldfish odorant receptor. Neuron 23:487–498

    Article  PubMed  CAS  Google Scholar 

  • Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, Zimmer RK, Hatt H (2003) Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299:2054–2058

    Article  PubMed  CAS  Google Scholar 

  • Sprague J, Bayraktaroglu L, Bradford Y, Conlin T, Dunn N, Fashena D, Frazer K, Haendel M, Howe DG, Knight J et al. (2008) The zebrafish information network: the zebrafish model organism database provides expanded support for genotypes and phenotypes. Nucleic Acids Res 36:D768–D772

    Article  PubMed  CAS  Google Scholar 

  • Studer RA, Penel S, Duret L, Robinson-Rechavi M (2008) Pervasive positive selection on duplicated and nonduplicated vertebrate protein coding genes. Genome Res 11:11

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Valentincic T, Kralj J, Stenovec M, Koce A, Caprio J (2000) The behavioral detection of binary mixtures of amino acids and their individual components by catfish. J Exp Biol 203:3307–3317

    PubMed  CAS  Google Scholar 

  • Valentincic T, Miklavc P, Dolenek J, Pliberek K (2005) Correlations between olfactory discrimination, olfactory receptor neuron responses and chemotopy of amino acids in fishes. Chem Senses 30(Suppl 1):i312–i314

    Article  PubMed  CAS  Google Scholar 

  • Vielma A, Ardiles A, Delgado L, Schmachtenberg O (2008) The elusive crypt olfactory receptor neuron: evidence for its stimulation by amino acids and cAMP pathway agonists. J Exp Biol 211:2417–2422

    Article  PubMed  CAS  Google Scholar 

  • Weth F, Nadler W, Korsching S (1996) Nested expression domains for odorant receptors in zebrafish olfactory epithelium. Proc Natl Acad Sci USA 93:13321–13326

    Article  PubMed  CAS  Google Scholar 

  • Yamagami S, Suzuki N (2005) Diverse forms of guanylyl cyclases in medaka fish – their genomic structure and phylogenetic relationships to those in vertebrates and invertebrates. Zoolog Sci 22:819–835

    Article  PubMed  CAS  Google Scholar 

  • Yasuoka A, Endo K, Asano-Miyoshi M, Abe K, Emori Y (1999) Two subfamilies of olfactory receptor genes in medaka fish, Oryzias latipes. : genomic organization and differential expression in olfactory epithelium. J Biochem 126:866–873

    PubMed  CAS  Google Scholar 

  • Young JM, Trask BJ (2007) V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet 23:212–215

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Rodriguez I, Mombaerts P, Firestein S (2004) Odorant and vomeronasal receptor genes in two mouse genome assemblies. Genomics 83:802–811

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

I would like to thank Kim Robin Korsching for helping with the figures.

Author information

Authors and Affiliations

  1. Institut für Genetik, Universität zu Köln, Germany

    Sigrun Korsching

Authors
  1. Sigrun Korsching
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sigrun Korsching .

Editor information

Editors and Affiliations

    Rights and permissions

    Reprints and permissions

    Copyright information

    © 2008 Springer-Verlag London

    About this chapter

    Cite this chapter

    Korsching, S. (2008). The Molecular Evolution of Teleost Olfactory Receptor Gene Families. In: Korsching, S., Meyerhof, W. (eds) Chemosensory Systems in Mammals, Fishes, and Insects. Results and Problems in Cell Differentiation, vol 47. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_2008_11

    Download citation

    Publish with us

    Policies and ethics

    Search

    Navigation