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The Olfactory Receptor Gene Family of Marsupials

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Abstract

Olfaction in vertebrates is mediated mainly by a large family of olfactory receptors in the olfactory epithelium that belong to the superfamily of G protein-coupled receptors. Olfactory systems are well conserved among vertebrates, including marsupials, but there is a large variation in the numbers of olfactory genes in different animals. Most marsupials are nocturnal so depend on their sense of smell to locate food, avoid predators and identify potential mates in similar ways to other mammals. The olfactory bulbs are quite large in adult marsupials, suggesting that the sense of smell is very important in these animals. In addition, very undeveloped newborn marsupials have the special challenge of locating the pouch unassisted. It is likely that these newborns utilise their sense of smell for this unique pouch-finding task. The olfactory system is one of the few systems that is sufficiently developed in newborn marsupials to accomplish the task of finding the pouch. The opossum OR repertoire of one marsupial, the American opossum, is one of the largest characterised in mammals so far, containing over 1,500 genes. Interestingly comparisons of the opossum OR repertoire with the repertoire in an Australian marsupial, the tammar wallaby, suggests that a large conserved OR repertoire may be a feature of marsupials. The OR repertoires of the two marsupials show a high degree of similarity in total gene numbers and range of genes. This is unlike placental mammals, where the OR repertoires show a greater range. Results from these comparisons provide evidence for both the major forces (adaptation and genomic drift) behind the “birth-and-death” theory for the evolution of OR genes.

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References

  • Ache BW, Young JM (2005) Olfaction: diverse species, conserved principles. Neuron 48: 417–430.

    Article  PubMed  CAS  Google Scholar 

  • Aloni R, Olender T, Lancet D (2006) Ancient genomic architecture for mammalian olfactory receptor clusters. Genome Biol 7:R88.

    Article  PubMed  Google Scholar 

  • Ashwell KWS, Marotte LR, Cheng G (2008) Development of the olfactory system in a wallaby (Macropus eugenii). Brain Behav Evol 71:216–230.

    Article  PubMed  CAS  Google Scholar 

  • Ben-Arie N, Khen M, Lancet D (1993) Glutathione S-transferases in rat olfactory epithelium: purification, molecular properties and odorant biotransformation. Biochem J 292: 379–384.

    PubMed  CAS  Google Scholar 

  • Bininda-Emonds OR, Cardillo M, Jones KE, et al. (2007) The delayed rise of present-day mammals. Nature 446:507–512.

    Article  PubMed  CAS  Google Scholar 

  • Branscomb A, Seger J, White RL (2000) Evolution of odorant receptors expressed in mammalian testes. Genetics 156:785–797.

    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 

  • Cedar H, Bergman Y (2008) Choreography of Ig allelic exclusion. Curr Opin Immunol 20: 308–317.

    Article  PubMed  CAS  Google Scholar 

  • Croft DB, Eisenberg JF (2006) Behaviour. In: Armati PJ, Dickman CR, Hume ID (eds) Marsupials. Cambridge University Press, Cambridge.

    Google Scholar 

  • De la Cruz O, Blekhman R, Zhang XH, et al. (2009) A signature of evolutionary constraint on a subset of ectopically expressed olfactory receptor genes. Mol Biol Evol 26:491–494.

    Article  PubMed  Google Scholar 

  • Dreyer WJ (1998) The area code hypothesis revisited: olfactory receptors and other related transmembrane receptors may function as the last digits in a cell surface code for assembling embryos. Proc Natl Acad Sci USA 95:9072–9077.

    Article  PubMed  CAS  Google Scholar 

  • Feingold EA, Penny LA, Nienhuis AW, Forget BG (1999) An olfactory receptor gene is located in the extended human beta-globin gene cluster and is expressed in erythroid cells. Genomics 61:15–23.

    Article  PubMed  CAS  Google Scholar 

  • Feinstein P, Bozza T, Rodriguez I, Vassalli A, Mombaerts P (2004) Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117:833–846.

    Article  PubMed  CAS  Google Scholar 

  • Feldmesser E, Olender T, Khen M, et al. (2006) Widespread ectopic expression of olfactory receptor genes. BMC Genomics 7:121.

    Article  PubMed  Google Scholar 

  • Freitag J, Krieger J, Strotmann J, Breer H (1995) Two classes of olfactory receptors in Xenopus laevis. Neuron 15:1383–1392.

    Article  PubMed  CAS  Google Scholar 

  • Freitag J, Ludwig G, Andreini I, Rossler P, Breer H (1998) Olfactory receptors in aquatic and terrestrial vertebrates. J Comp Physiol A 183:635–650.

    Article  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.

    Google Scholar 

  • Fuss SH, Omura M, Mombaerts P (2007) Local and cis effects of the H element on expression of odorant receptor genes in mouse. Cell 130:373–384.

    Article  PubMed  CAS  Google Scholar 

  • Fuss SH, Ray A (2009) Mechanisms of odorant receptor gene choice in Drosophila and vertebrates. Mol Cell Neurosci 41:101–112.

    Article  PubMed  CAS  Google Scholar 

  • Gemmell RT, Nelson J (2004) The birth and subsequent development of the common brushtail possum Trichosurus vulpecula. In: Goldingay RL, Jackson SM (eds) The Biology of Australian Possums and Gliders. Surrey Beatty & Sons, Chipping Norton.

    Google Scholar 

  • Gemmell RT, Rose RW (1989) The senses involved in movement of some newborn Macropodidae and other marsupials from cloaca to pouch. In Grigg G, Jarman P, Hume I (eds) Kangaroos, Wallabies and Rat-Kangaroos. Surrey Beatty & Sons, Chipping Norton.

    Google Scholar 

  • Glusman G, Bahar A, Sharon D, et al. (2000) The olfactory receptor gene superfamily: data mining, classification, and nomenclature. Mamm Genome 11:1016–1023.

    Article  PubMed  CAS  Google Scholar 

  • Glusman G, Clifton S, Roe B, Lancet D (1996) Sequence analysis in the olfactory receptor gene cluster on human chromosome 17: recombinatorial events affecting receptor diversity. Genomics 37:147–160.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Goldmit M, Bergman Y (2004) Monoallelic gene expression: a repertoire of recurrent themes. Immunol Rev 200:197–214.

    Article  PubMed  CAS  Google Scholar 

  • Grus WE, Shi P, Zhang J (2007) Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol Biol Evol 24:2153–2157.

    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 

  • Grus WE, Zhang J (2008) Distinct evolutionary patterns between chemoreceptors of 2 vertebrate olfactory systems and the differential tuning hypothesis. Mol Biol Evol 25:1593–1601.

    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 

  • Hasin-Brumshtein Y, Lancet D, Olender T (2009) Human olfaction: from genomic variation to phenotypic diversity. Trends Genet 25:178–184.

    Article  PubMed  CAS  Google Scholar 

  • Hughes RL, Hall LS, Tyndale-Biscoe CH, Hinds LA (1989) Evolutionary implication of macropodid organogenesis. In Grigg G, Jarman P, Hume I (eds) Kangaroos, Wallabies and Rat-Kangaroos. Surrey Beatty & Sons, Chipping Norton.

    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 328:203–204.

    Article  CAS  Google Scholar 

  • Iwema CL, Fang H, Kurtz DB, Youngentob SL, Schwob JE (2004) Odorant receptor expression patterns are restored in lesion-recovered rat olfactory epithelium. J Neurosci 24:356–369.

    Article  PubMed  CAS  Google Scholar 

  • Kambere MB, Lane RP (2007) Co-regulation of a large and rapidly evolving repertoire of odorant receptor genes. BMC Neurosci 8(Suppl 3):S2.

    Article  PubMed  Google Scholar 

  • Kambere MB, Lane RP (2009) Exceptional LINE density at V1R loci: the Lyon repeat hypothesis revisited on autosomes. J Mol Evol 68:145–159.

    Article  PubMed  CAS  Google Scholar 

  • Keller A, Vosshall LB (2008) Better smelling through genetics: mammalian odor perception. Curr Opin Neurobiol 18:364–369.

    Article  PubMed  CAS  Google Scholar 

  • Kishida T (2008) Pattern of the divergence of olfactory receptor genes during tetrapod evolution. PLoS One 3:e2385.

    Article  PubMed  Google Scholar 

  • Knapp LA, Robson J, Waterhouse JS (2006) Olfactory signals and the MHC: a review and a case study in Lemur catta. Am J Primatol 68:568–584.

    Article  PubMed  CAS  Google Scholar 

  • Krumlauf R (1992) Evolution of the vertebrate Hox homeobox genes. Bioessays 14:245–252.

    Article  PubMed  CAS  Google Scholar 

  • Lane RP, Roach JC, Lee IY, et al. (2002) Genomic analysis of the olfactory receptor region of the mouse and human T-cell receptor alpha/delta loci. Genome Res 12:81–87.

    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 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Menini A, Lagostena L, Boccaccio A (2004) Olfaction: from odorant molecules to the olfactory cortex. News Physiol Sci 19:101–104.

    PubMed  CAS  Google Scholar 

  • Miyamichi K, Serizawa S, Kimura H M, Sakano H (2005) Continuous and overlapping expression domains of odorant receptor genes in the olfactory epithelium determine the dorsal/ventral positioning of glomeruli in the olfactory bulb. J Neurosci 25:3586–3592.

    Article  PubMed  CAS  Google Scholar 

  • Mombaerts P (2004) Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol 14:31–36.

    Article  PubMed  CAS  Google Scholar 

  • Mombaerts P (2006) Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 22:713–737.

    Article  PubMed  CAS  Google Scholar 

  • Moulton DG (1974) Dynamics of cell populations in the olfactory epithelium. Ann NY Acad Sci 237:52–61.

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Niimura Y, Nozawa M (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9:951–963.

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152.

    Article  PubMed  CAS  Google Scholar 

  • Ngai J, Chess A, Dowling MM, et al. (1993) Coding of olfactory information: topography of odorant receptor expression in the catfish olfactory epithelium. Cell 72:667–680.

    Article  PubMed  CAS  Google Scholar 

  • Niimura Y (2009) On the origin and evolution of vertebrate olfactory receptor genes: comparative genome analysis among 23 chordate species. Genome Biol Evol 2009:34–44.

    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 

  • Niimura Y, Nei M (2006) Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates. J Hum Genet 51:505–517.

    Article  PubMed  CAS  Google Scholar 

  • Niimura Y, Nei M (2007) Extensive gains and losses of olfactory receptor genes in Mammalian evolution. PLoS One 2:e708.

    Article  PubMed  Google Scholar 

  • Nishizumi H, Kumasaka K, Inoue N, Nakashima A, Sakano H (2007) Deletion of the core-H region in mice abolishes the expression of three proximal odorant receptor genes in cis. Proc Natl Acad Sci USA 104:20067–20072.

    Article  PubMed  CAS  Google Scholar 

  • Nozawa M, Kawahara Y, Nei M (2007) Genomic drift and copy number variation of sensory receptor genes in humans. Proc Natl Acad Sci USA 104:20421–20426.

    Article  PubMed  CAS  Google Scholar 

  • Olender T, Lancet D, Nebert DW (2008) Update on the olfactory receptor (OR) gene superfamily. Hum Genomics 3:87–97.

    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 

  • Pilpel Y, Lancet D (1999) The variable and conserved interfaces of modeled olfactory receptor proteins. Protein Sci 8:969–977.

    Article  PubMed  CAS  Google Scholar 

  • Rawson NE, Eberwine J, Dotson R, et al. (2000) Expression of mRNAs encoding for two different olfactory receptors in a subset of olfactory receptor neurons. J Neurochem 75:185–195.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Trelles F, Tarrio R, Ayala FJ (2005) Is ectopic expression caused by deregulatory mutations or due to gene-regulation leaks with evolutionary potential? Bioessays 27:592–601.

    Article  PubMed  CAS  Google Scholar 

  • Rouquier S, Giorgi D (2007) Olfactory receptor gene repertoires in mammals. Mutat Res 616: 95–102.

    Article  PubMed  CAS  Google Scholar 

  • Rouquier S, Taviaux S, Trask BJ, et al. (1998) Distribution of olfactory receptor genes in the human genome. Nat Genet 18:243–250.

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Gracia A, Vieira FG, Rozas J (2009) Molecular evolution of the major chemosensory gene families in insects. Heredity 103:208–216.

    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 (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 

  • Schneider N, Fletcher T, Shaw G, Renfree MB (2009) The olfactory system of the tammar wallaby is developed at birth and directs the neonate to its mother’s pouch odours. Reproduction 138:849–857.

    Article  PubMed  CAS  Google Scholar 

  • Serizawa S, Miyamichi K, Nakatani H, et al. (2003) Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302:2088–2094.

    Article  PubMed  CAS  Google Scholar 

  • Shykind BM, Rohani SC, O’Donnell S, et al. (2004) Gene switching and the stability of odorant receptor gene choice. Cell 117:801–815.

    Article  PubMed  CAS  Google Scholar 

  • Singh N, Ebrahimi FA, Gimelbrant AA, et al. (2003) Coordination of the random asynchronous replication of autosomal loci. Nat Genet 33:339–341.

    Article  PubMed  CAS  Google Scholar 

  • Stephen DL (2009) Trace amine-associated receptors are olfactory receptors in vertebrates. Ann NY Acad Sci 1170:168–172.

    Article  Google Scholar 

  • Stoddart DM (1980) The Ecology of Vertebrate Olfaction. Chapman and Hall, London and New York.

    Book  Google Scholar 

  • Sullivan SL, Adamson MC, Ressler KJ, Kozak CA Buck LB (1996) The chromosomal distribution of mouse odorant receptor genes. Proc Natl Acad Sci USA 93:884–888.

    Article  PubMed  CAS  Google Scholar 

  • Tacher S, Quignon P, Rimbault M, et al. (2005) Olfactory receptor sequence polymorphism within and between breeds of dogs. J Hered 96:812–816.

    Article  PubMed  CAS  Google Scholar 

  • Tian H, Ma M (2008) Activity plays a role in eliminating olfactory sensory neurons expressing multiple odorant receptors in the mouse septal organ. Mol Cell Neurosci 38:484–488.

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Young JM, Endicott RM, Parghi SS, et al. (2008) Extensive copy-number variation of the human olfactory receptor gene family. Am J Hum Genet 83:228–242.

    Article  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, De la Cruz O, Pinto JM, et al. (2007) Characterizing the expression of the human olfactory receptor gene family using a novel DNA microarray. Genome Biol 8:R86.

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ziegler A, Dohr G, Uchanska-Ziegler B (2002) Possible roles for products of polymorphic MHC and linked olfactory receptor genes during selection processes in reproduction. Am J Reprod Immunol 48:34–42.

    Article  PubMed  Google Scholar 

  • Zuri I, Su W, Halpern M (2003) Conspecific odor investigation by gray short-tailed opossums (Monodelphis domestica). Physiol Behav 80:225–232.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. ARC Centre of Excellence for Kangaroo Genomics, Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, ACT, 0200, Australia

    Margaret L. Delbridge, Amir Mohammadi & Jennifer A. Marshall Graves

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  1. Margaret L. Delbridge
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  2. Amir Mohammadi
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  3. Jennifer A. Marshall Graves
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Correspondence to Margaret L. Delbridge .

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Editors and Affiliations

  1. , Ecology, Evolution&Genetics, The Austral, ARC Centre for Excellence for Kangaroo G, Research School of Biology, building 46, Canberra ACT, 0200, Australia

    Janine E. Deakin

  2. , Ecology, Evolution&Genetics, The Austral, ARC Centre for Excellence for Kangaroo G, Research School of Biology, building 46, Canberra ACT, 0200, Australia

    Paul D. Waters

  3. , Ecology, Evolution and Genetics, ARC Centre of Excellence for Kangaroo Ge, Buidling 46, Canberra ACT, 0200, Australia

    Jennifer A. Marshall Graves

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Delbridge, M.L., Mohammadi, A., Graves, J.A.M. (2010). The Olfactory Receptor Gene Family of Marsupials. In: Deakin, J., Waters, P., Marshall Graves, J. (eds) Marsupial Genetics and Genomics. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9023-2_21

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