• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Oct 2000; 156(2): 785–797.
PMCID: PMC1461278

Evolution of odorant receptors expressed in mammalian testes.

Abstract

About 10% of mammalian odorant receptors are transcribed in testes, and odorant-receptor proteins have been detected on mature spermatozoa. Testis-expressed odorant receptors (TORs) are hypothesized to play roles in sperm chemotaxis, but they might also be ordinary nasal odorant receptors (NORs) that are expressed gratuitously in testes. Under the sperm-chemotaxis hypothesis, TORs should be subject to intense sexual selection and therefore should show higher rates of amino acid substitution than NORs, but under the gratuitous-expression hypothesis, TORs are misidentified NORs and therefore should evolve like other NORs. To test these predictions, we estimated synonymous and nonsynonymous divergences of orthologous NOR and TOR coding sequences from rat and mouse. Contrary to both hypotheses, TORs are on average more highly conserved than NORs, especially in certain domains of the OR protein. This pattern suggests that some TORs might perform internal nonolfactory functions in testes; for example, they might participate in the regulation of sperm development. However, the pattern is also consistent with a modified gratuitous-expression model in which NORs with specialized ligand specificities are both more highly conserved than typical NORs and more likely to be expressed in testes.

Full Text

The Full Text of this article is available as a PDF (272K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. [PubMed]
  • Freitag J, Ludwig G, Andreini I, Rössler P, Breer H. Olfactory receptors in aquatic and terrestrial vertebrates. J Comp Physiol A. 1998 Nov;183(5):635–650. [PubMed]
  • Holland B, Rice WR. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5083–5088. [PMC free article] [PubMed]
  • Krautwurst D, Yau KW, Reed RR. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell. 1998 Dec 23;95(7):917–926. [PubMed]
  • Levy NS, Bakalyar HA, Reed RR. Signal transduction in olfactory neurons. J Steroid Biochem Mol Biol. 1991 Oct;39(4B):633–637. [PubMed]
  • Makalowski W, Boguski MS. Evolutionary parameters of the transcribed mammalian genome: an analysis of 2,820 orthologous rodent and human sequences. Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9407–9412. [PMC free article] [PubMed]
  • Malnic B, Hirono J, Sato T, Buck LB. Combinatorial receptor codes for odors. Cell. 1999 Mar 5;96(5):713–723. [PubMed]
  • Matarazzo V, Tirard A, Renucci M, Belaïch A, Clément JL. Isolation of putative olfactory receptor sequences from pig nasal epithelium. Neurosci Lett. 1998 Jun 19;249(2-3):87–90. [PubMed]
  • McVean GT, Hurst LD. Evidence for a selectively favourable reduction in the mutation rate of the X chromosome. Nature. 1997 Mar 27;386(6623):388–392. [PubMed]
  • Metz EC, Robles-Sikisaka R, Vacquier VD. Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10676–10681. [PMC free article] [PubMed]
  • Abe K, Kusakabe Y, Tanemura K, Emori Y, Arai S. Multiple genes for G protein-coupled receptors and their expression in lingual epithelia. FEBS Lett. 1993 Feb 1;316(3):253–256. [PubMed]
  • Mombaerts P. Molecular biology of odorant receptors in vertebrates. Annu Rev Neurosci. 1999;22:487–509. [PubMed]
  • Mombaerts P. Seven-transmembrane proteins as odorant and chemosensory receptors. Science. 1999 Oct 22;286(5440):707–711. [PubMed]
  • Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. Visualizing an olfactory sensory map. Cell. 1996 Nov 15;87(4):675–686. [PubMed]
  • Asai H, Kasai H, Matsuda Y, Yamazaki N, Nagawa F, Sakano H, Tsuboi A. Genomic structure and transcription of a murine odorant receptor gene: differential initiation of transcription in the olfactory and testicular cells. Biochem Biophys Res Commun. 1996 Apr 16;221(2):240–247. [PubMed]
  • Nef P, Hermans-Borgmeyer I, Artières-Pin H, Beasley L, Dionne VE, Heinemann SF. Spatial pattern of receptor expression in the olfactory epithelium. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):8948–8952. [PMC free article] [PubMed]
  • Nikaido M, Rooney AP, Okada N. Phylogenetic relationships among cetartiodactyls based on insertions of short and long interpersed elements: hippopotamuses are the closest extant relatives of whales. Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10261–10266. [PMC free article] [PubMed]
  • Chess A, Simon I, Cedar H, Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell. 1994 Sep 9;78(5):823–834. [PubMed]
  • Clark AG, Begun DJ, Prout T. Female x male interactions in Drosophila sperm competition. Science. 1999 Jan 8;283(5399):217–220. [PubMed]
  • Pamilo P, Bianchi NO. Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol. 1993 Mar;10(2):271–281. [PubMed]
  • Parmentier M, Libert F, Schurmans S, Schiffmann S, Lefort A, Eggerickx D, Ledent C, Mollereau C, Gérard C, Perret J, et al. Expression of members of the putative olfactory receptor gene family in mammalian germ cells. Nature. 1992 Jan 30;355(6359):453–455. [PubMed]
  • Drutel G, Arrang JM, Diaz J, Wisnewsky C, Schwartz K, Schwartz JC. Cloning of OL1, a putative olfactory receptor and its expression in the developing rat heart. Receptors Channels. 1995;3(1):33–40. [PubMed]
  • Partridge L, Hurst LD. Sex and conflict. Science. 1998 Sep 25;281(5385):2003–2008. [PubMed]
  • Duchamp-Viret P, Chaput MA, Duchamp A. Odor response properties of rat olfactory receptor neurons. Science. 1999 Jun 25;284(5423):2171–2174. [PubMed]
  • Pilpel Y, Lancet D. The variable and conserved interfaces of modeled olfactory receptor proteins. Protein Sci. 1999 May;8(5):969–977. [PMC free article] [PubMed]
  • Potts WK, Manning CJ, Wakeland EK. The role of infectious disease, inbreeding and mating preferences in maintaining MHC genetic diversity: an experimental test. Philos Trans R Soc Lond B Biol Sci. 1994 Nov 29;346(1317):369–378. [PubMed]
  • Raming K, Konzelmann S, Breer H. Identification of a novel G-protein coupled receptor expressed in distinct brain regions and a defined olfactory zone. Receptors Channels. 1998;6(2):141–151. [PubMed]
  • Vanderhaeghen P, Schurmans S, Vassart G, Parmentier M. Olfactory receptors are displayed on dog mature sperm cells. J Cell Biol. 1993 Dec;123(6 Pt 1):1441–1452. [PMC free article] [PubMed]
  • Ressler KJ, Sullivan SL, Buck LB. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell. 1993 May 7;73(3):597–609. [PubMed]
  • Vanderhaeghen P, Schurmans S, Vassart G, Parmentier M. Specific repertoire of olfactory receptor genes in the male germ cells of several mammalian species. Genomics. 1997 Feb 1;39(3):239–246. [PubMed]
  • Ressler KJ, Sullivan SL, Buck LB. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell. 1994 Dec 30;79(7):1245–1255. [PubMed]
  • Vassar R, Ngai J, Axel R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell. 1993 Jul 30;74(2):309–318. [PubMed]
  • Walensky LD, Roskams AJ, Lefkowitz RJ, Snyder SH, Ronnett GV. Odorant receptors and desensitization proteins colocalize in mammalian sperm. Mol Med. 1995 Jan;1(2):130–141. [PMC free article] [PubMed]
  • Rice WR. Male fitness increases when females are eliminated from gene pool: implications for the Y chromosome. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6217–6221. [PMC free article] [PubMed]
  • Walensky LD, Ruat M, Bakin RE, Blackshaw S, Ronnett GV, Snyder SH. Two novel odorant receptor families expressed in spermatids undergo 5'-splicing. J Biol Chem. 1998 Apr 17;273(16):9378–9387. [PubMed]
  • Rubin BD, Katz LC. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron. 1999 Jul;23(3):499–511. [PubMed]
  • Wang F, Nemes A, Mendelsohn M, Axel R. Odorant receptors govern the formation of a precise topographic map. Cell. 1998 Apr 3;93(1):47–60. [PubMed]
  • Schmidt EE. Transcriptional promiscuity in testes. Curr Biol. 1996 Jul 1;6(7):768–769. [PubMed]
  • Wolfe KH, Sharp PM. Mammalian gene evolution: nucleotide sequence divergence between mouse and rat. J Mol Evol. 1993 Oct;37(4):441–456. [PubMed]
  • Wolfe KH, Sharp PM, Li WH. Mutation rates differ among regions of the mammalian genome. Nature. 1989 Jan 19;337(6204):283–285. [PubMed]
  • Sullivan SL, Adamson MC, Ressler KJ, Kozak CA, Buck LB. The chromosomal distribution of mouse odorant receptor genes. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):884–888. [PMC free article] [PubMed]
  • Touhara K, Sengoku S, Inaki K, Tsuboi A, Hirono J, Sato T, Sakano H, Haga T. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4040–4045. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Gene
    Gene
    Gene links
  • Gene (nucleotide)
    Gene (nucleotide)
    Records in Gene identified from shared sequence links
  • GEO Profiles
    GEO Profiles
    Related GEO records
  • HomoloGene
    HomoloGene
    HomoloGene links
  • MedGen
    MedGen
    Related information in MedGen
  • Nucleotide
    Nucleotide
    Published Nucleotide sequences
  • Protein
    Protein
    Published protein sequences
  • PubMed
    PubMed
    PubMed citations for these articles