Skip to main content
SpringerLink
Log in

Evolution of the “OR37” Subfamily of Olfactory Receptors: A Cross-Species Comparison

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Genes encoding the olfactory receptors of the “OR37” subfamily of the mouse are characterized by special features including a clustered expression pattern, assembly in two distinct gene clusters, and highly conserved putative promoter motifs. Mining the rat and dog databases revealed that these two species possess highly conserved clusters of OR37 genes at two syntenic genomic loci. In a prototherian mammal, the platypus (Ornithorhynchus anatinus), none of the characteristic OR37 genes were found. Examination of a metatherian mammal, the gray short-tailed opossum (Monodelphis domestica) revealed seven canonical OR37 genes, all phylogenetically related to cluster II genes and also organized similar to cluster II of eutherian species. In addition, their 5′ upstream regions comprised sequence motifs related to the putative regulatory sequences of cluster II genes. Typical cluster I OR37 genes were identified only in the eutherian mammals examined, including the evolutionary ancient anteater, wherein OR37 genes related to both clusters were present. Together, these results reveal novel information concerning the phylogenetic origin and important evolutionary steps of the mammalian-specific OR37 olfactory receptor family.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

References

  • Bailey JA, Yavor AM, Massa HF, Trask BJ, Eichler EE (2001) Segmental duplications: organization and impact within the current human genome project assembly. Genome Res 11:1005–1017

    Article  CAS  PubMed  Google Scholar 

  • Bailey JA, Gu Z, Clark RA, Reinert K, Samonte RV, Schwartz S, Adams MD, Myers EW, Li PW, Eichler EE (2002) Recent segmental duplications in the human genome. Science 297:1003–1007

    Article  CAS  PubMed  Google Scholar 

  • Brennan PA, Keverne EB (2004) Something in the air? New insights into mammalian pheromones. Curr Biol 14:R81–R89

    Article  CAS  PubMed  Google Scholar 

  • Buck LB (2004) Olfactory receptors and odor coding in mammals. Nutr Rev 62:S184–S188

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Dorries KM, Adkins Regan E, Halpern BP (1997) Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs. Brain Behav Evol 49:53–62

    CAS  PubMed  Google Scholar 

  • Dubchak I, Brudno M, Loots GG, Pachter L, Mayor C, Rubin EM, Frazer KA (2000) Active conservation of noncoding sequences revealed by three-way species comparisons. Genome Res 10:1304–1306

    Article  CAS  PubMed  Google Scholar 

  • Dulac C (2000) Sensory coding of pheromone signals in mammals. Curr Opin Neurobiol 10:511–518

    Article  CAS  PubMed  Google Scholar 

  • Eizirik E, Murphy WJ, O’Brien SJ (2001) Molecular dating and biogeography of the early placental mammal radiation. J Hered 92:212–219

    Article  CAS  PubMed  Google Scholar 

  • Emes RD, Beatson SA, Ponting CP, Goodstadt L (2004) Evolution and comparative genomics of odorant- and pheromone-associated genes in rodents. Genome Res 14:591–602

    CAS  PubMed  Google Scholar 

  • Fewell GD, Meredith M (2002) Experience facilitates vomeronasal and olfactory influence on Fos expression in medial preoptic area during pheromone exposure or mating in male hamsters. Brain Res 941:91–106

    Article  CAS  PubMed  Google Scholar 

  • Frazer KA, Elnitski L, Church DM, Dubchak I, Hardison RC (2003) Cross-species sequence comparisons: a review of methods and available resources. Genome Res 13:1–12

    CAS  PubMed  Google Scholar 

  • Fronicke L, Wienberg J, Stone G, Adams L, Stanyon R (2003) Towards the delineation of the ancestral eutherian genome organization: comparative genome maps of human and the African elephant (Loxodonta africana) generated by chromosome painting. Proc R Soc Lond B Biol Sci 270:1331–1340

    Google Scholar 

  • Gaillard I, Rouquier S, Chavanieu A, Mollard P, Giorgi D (2004a) Amino-acid changes acquired during evolution by olfactory receptor 912-93 modify the specificity of odorant recognition. Hum Mol Genet 13:771–780

    Article  CAS  Google Scholar 

  • Gaillard I, Rouquier S, Giorgi D (2004b) Olfactory receptors. Cell Mol Life Sci 61:456–469

    CAS  Google Scholar 

  • Glusman G, Bahar A, Sharon D, Pilpel Y, White J, Lancet D (2000a) The olfactory receptor gene superfamily: data mining, classification, and nomenclature. Mammal Genome 11:1016–1023

    CAS  Google Scholar 

  • Glusman G, Sosinsky A, Ben Asher E, Avidan N, Sonkin D, Bahar A, Rosenthal A, CliftonS, Roe B, Ferraz C, Demaille J, Lancet D (2000b) Sequence, structure, and evolution of a complete human olfactory receptor gene cluster. Genomics 63:227–245

    Article  CAS  Google Scholar 

  • Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–702

    Article  CAS  PubMed  Google Scholar 

  • Godfrey PA, Malnic B, Buck LB (2004) The mouse olfactory receptor gene family. Proc Natl Acad Sci USA 101:2156–2161

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Ho PJ, Thein SL (2000) Gene regulation and deregulation: a beta globin perspective. Blood Rev 14:78–93

    Article  CAS  PubMed  Google Scholar 

  • Hoppe R, Weimer M, Beck A, Breer H, Strotmann J (2000) Sequence analyses of the olfactory receptor gene cluster mOR37 on mouse chromosome 4. Genomics 66:284–295

    Article  CAS  PubMed  Google Scholar 

  • Hoppe R, Breer H, Strotmann J (2003a) Organization and evolutionary relatedness of OR37 olfactory receptor genes in mouse and human. Genomics 82:355–364

    Article  CAS  Google Scholar 

  • Hoppe R, Frank H, Breer H, Strotmann J (2003b) The clustered olfactory receptor gene family 262: genomic organization, promoter elements, and interacting transcription factors. Genome Res 13:2674–2685

    Article  CAS  Google Scholar 

  • Hudson R, Distel H (1986) Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol Behav 37:123–128

    Article  CAS  PubMed  Google Scholar 

  • Hughes MK, Hughes AL (1993) Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. Mol Biol Evol 10:1360–1369

    CAS  PubMed  Google Scholar 

  • Huson DH (1998) SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73

    Article  CAS  PubMed  Google Scholar 

  • Keverne EB (1999) The vomeronasal organ. Science 286:716–720

    Article  CAS  PubMed  Google Scholar 

  • Kubick S, Strotmann J, Andreini I, Breer H (1997) Subfamily of olfactory receptors characterized by unique structural features and expression patterns. J Neurochem 69:465–475

    CAS  PubMed  Google Scholar 

  • Madsen O, Scally M, Douady CJ, Kao DJ, DeBry RW, Adkins R, Amrine HM, Stanhope MJ, de Jong WW, Springer MS (2001) Parallel adaptive radiations in two major clades of placental mammals. Nature 409:610–614

    Article  CAS  PubMed  Google Scholar 

  • Malnic B, Godfrey PA, Buck LB (2004) The human olfactory receptor gene family. Proc Natl Acad Sci USA 101:2584–2589

    Article  CAS  PubMed  Google Scholar 

  • Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723

    Article  CAS  PubMed  Google Scholar 

  • Margulies EH, Maduro VV, Thomas PJ, Tomkins JP, Amemiya CT, Luo M, Green ED (2005) Comparative sequencing provides insights about the structure and conservation of marsupial and monotreme genomes. Proc Natl Acad Sci USA 102:3354–3359

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ (2001a) Molecular phylogenetics and the origins of placental mammals. Nature 409:614–618

    Article  CAS  Google Scholar 

  • Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001b) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351

    Article  CAS  Google Scholar 

  • Newman T, Trask BJ (2003) Complex evolution of 7E olfactory receptor genes in segmental duplications. Genome Res 13:781–793

    Article  CAS  PubMed  Google Scholar 

  • Niimura Y, Nei M (2003) Evolution of olfactory receptor genes in the human genome. Proc Natl Acad Sci USA 100:12235–12240

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1973) Ancient linkage groups and frozen accidents. Nature 244:259–262

    Article  Google Scholar 

  • Olender T, Feldmesser E, Atarot T, Eisenstein M, Lancet D (2004a) The olfactory receptor universefrom whole genome analysis to structure and evolution. Genet Mol Res 3:545–553

    CAS  Google Scholar 

  • Olender T, Fuchs T, Linhart C, Shamir R, Adams M, Kalush F, Khen M, Lancet D (2004b) The canine olfactory subgenome. Genomics 83:361–372

    Article  CAS  Google Scholar 

  • Raming K, Krieger J, Strotmann J, Boekhoff I, Kubick S, Baumstark C, Breer H (1993) Cloning and expression of odorant receptors. Nature 361:353–356

    Article  CAS  PubMed  Google Scholar 

  • Ressler KJ, Sullivan SL, Buck LB (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597–609

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez I (2004) Pheromone receptors in mammals. Horm Behav 46:219–230

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Frisch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Shepherd GM (1994) Discrimination of molecular signals by the olfactory receptor neuron. Neuron 13:771–790

    Article  CAS  PubMed  Google Scholar 

  • Strotmann J, Wanner I, Krieger J, Raming K, Breer H (1992) Expression of odorant receptors in spatially restricted subsets of chemosensory neurones. NeuroReport 3:1053–1056

    CAS  PubMed  Google Scholar 

  • Strotmann J, Wanner I, Helfrich T, Beck A, Breer H (1994a) Rostro-caudal patterning of receptor–expressing olfactory neurones in the rat nasal cavity. Cell Tissue Res 278:11–20

    CAS  Google Scholar 

  • Strotmann J, Wanner I, Helfrich T, Beck A, Meinken C, Kubick S, Breer H (1994b) Olfactory neurones expressing distinct odorant receptor subtypes are spatially segregated in the nasal neuroepithelium. Cell Tissue Res 276:429–438

    CAS  Google Scholar 

  • Strotmann J, Conzelmann S, Beck A, Feinstein P, Breer H, Mombaerts P (2000) Local permutations in the glomerular array of the mouse olfactory bulb. J Neurosci 20:6927–6938

    CAS  PubMed  Google Scholar 

  • Vassar R, Ngai J, Axel R (1993) Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309–318

    Article  CAS  PubMed  Google Scholar 

  • Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28:360–385

    CAS  PubMed  Google Scholar 

  • Young JM, Trask BJ (2002) The sense of smell: genomics of vertebrate odorant receptors. Hum Mol Genet 11:1153–1160

    CAS  PubMed  Google Scholar 

  • Young JM, Kambere M, Trask BJ, Lane RP (2005) Divergent V1R repertoires in five species: Amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs. Genome Res15:231–240

    Google Scholar 

  • Zhang X, Firestein S (2002) The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5:124–133

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Stefan Kubick and Isabella Andreini for their initial contribution to this study. We thank Michael Klaiber for his help with sequence analyses. We are grateful to Nelli Dick and Susan Mahaney for excellent technical assistance. Opossums were kindly provided by Prof. Ulrich Zeller, Humboldt-University, Berlin. Hair follociles from a great anteater were kindly provided by Prof. Henning Wiesner from the Hellabrunn Zoo, Munich. Platypus genomic DNA was kindly provided by Denis O’Meally from the Evolutionary Biology Unit of The Australian Museum, Sydney. We would like to thank Dr. Andreas Schlüter from the Staatliches Museum für Naturkunde in Stuttgart for his assistance importing the sample to Germany. This work was supported by the Deutsche Forschungsgemeinschaft, SFB 495. Support for P.B.S. was provided in part by NIH Grant RR014214.

Author information

Authors and Affiliations

  1. Institute of Physiology, University of Hohenheim, Garbenstrasse 30, 70593, Stuttgart, Germany

    Reiner Hoppe, Thomas D. Lambert, Heinz Breer & Joerg Strotmann

  2. Department of Veterinary Integrative Biosciences, Texas A&M University, 4458 TAMU, College Station, TX, 77843-4458, USA

    Paul B. Samollow

Authors
  1. Reiner Hoppe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas D. Lambert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul B. Samollow
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Heinz Breer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joerg Strotmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joerg Strotmann.

Additional information

[Reviewing Editor: Dr. Lauren Ancel Meyers]

Reiner Hoppe and Thomas D. Lambert are contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoppe, R., Lambert, T.D., Samollow, P.B. et al. Evolution of the “OR37” Subfamily of Olfactory Receptors: A Cross-Species Comparison. J Mol Evol 62, 460–472 (2006). https://doi.org/10.1007/s00239-005-0093-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-005-0093-4

Keywords

Search

Navigation