Olfactory Receptor Genes: Evolution

Yoshihito Niimura, The University of Tokyo, Tokyo, Japan

Published online: August 2014

DOI: 10.1002/9780470015902.a0020789.pub2

Abstract

Many mammal genomes have approximately 1000 genes encoding olfactory receptors (ORs), and OR genes constitute the largest multigene family in mammals. Comparisons among the OR gene repertoires in a broad range of species demonstrates that gene duplication and pseudogenization cause frequent gene gain and loss in this family, causing drastic evolutionary changes in the number of genes depending on species' ecological niches and other sensory modalities. For example, higher primates are equipped with a well‐developed visual system, and they have a reduced OR gene repertoires relative to mammals with lesser visual systems. Additionally, aquatic and terrestrial vertebrates retain different sets of OR genes, and these sets reflect the capacity to detect water‐soluble and airborne odorants, respectively. The origin of vertebrate OR genes can be traced back to the common ancestor of chordates, but insects and nematodes each use a distinct family of genes to encode chemoreceptors; therefore, multiple distinct chemoreceptor gene families emerged independently during animal evolution.

Key Concepts:

  • Olfactory receptor (OR) genes are the largest multigene family in mammals.

  • OR gene repertoires changed dynamically during mammalian evolution and these changes depended on each species' ecological niches and other sensory modalities.

  • Distinct chemoreceptor gene families have emerged independently multiple times during animal evolution.

  • Comparative evolutionary analysis of OR genes provides insights into the interactions between genomes and environments.

Keywords: olfactory receptor; chemoreceptor; phylogenetic analysis; multigene family; birth‐and‐death evolution; G‐protein coupled receptor; chordates; vertebrates; mammals; primates

Figure 1.

Complexity of structure–odour relationships (Rossiter, ). (a) The molecule on the left conveys a strong ambergris odour, but molecule on the right is odourless because it lacks just one of the oxygen atoms. (b) Enantiomers that have different odours. (c) Five very different molecular structures all have musky odours. (d) Four very different molecular structures all have camphoraceous odours, though there is no one functional group that is common to each of them.
Figure 2.

Number of OR genes identified from the whole genome sequences of 30 chordate species. Each number in the bar graphs indicates the number of intact genes (red), truncated genes (yellow) or pseudogenes (dark blue). For zebra finch and two turtle species, no distinction was made between truncated genes and pseudogenes. ‘P%’ indicates the fraction of pseudogenes. Data from Niimura and Nei (), Niimura (), Matsui et al. () and Wang et al. ().
Figure 3.

OR genes in the human genome. (a) Vertical bars above and below the chromosomes represent locations of intact OR genes and OR pseudogenes, respectively. The height of each bar indicates the number of OR genes existing in a nonoverlapping 1‐Mb window. (b) The OR gene cluster indicated by the red arrow in (a). The diagram (left) represents an expanded view of a 0.6‐Mb region on chromosome 3. ‘Ψ’ represents a pseudogene. All genes are encoded on the same strand. The neighbor‐joining phylogenetic tree (right) for the genes contained in this 0.6‐Mb cluster indicates that neighbouring genes within the cluster tend to be more closely related to each other than to more distantly located genes within the cluster. For example, genes 16 and 17 are more closely related to each other than they are to the other genes. HsOR11.3.2 was used as the outgroup in the phylogenetic tree. Bootstrap values greater than 80% are shown. (a) and (b) were modified from Nei et al. (). © Nature Publishing Group. (c) Schematic representation of tandem gene duplication. Unequal crossing‐over generates a new gene copy (‘B’) adjacent to the original gene. Subsequently, independent accumulation of mutations causes the sequences of the duplicates to diverge and potentially to acquire distinctive functions (‘B1’ and ‘B2’).
Figure 4.

Evolutionary dynamics of OR genes in primates (a) and in mammals (b). (a) OR gene losses during primate evolution. The common ancestor of the five primate species is estimated to have had 551 functional OR genes. The number above each branch indicates the number of the ancestral OR genes that were lost in that lineage. For example, humans have lost 212 of the 551 putative ancestral OR genes, but 57 gene duplications apparently occurred; therefore, humans currently have 396 functional OR genes. An arrowhead with red and green represents the branch at which the duplication of red/green opsin genes occurred. Colour vision system in each species is also shown (right). X‐linked red/green opsin genes and an autosomal blue opsin gene are represented schematically. Modified with permission from Matsui et al. (). © Oxford University Press. (b) Gains and losses of OR genes during mammalian evolution. The number in each box indicates the number of functional OR genes in the indicated extant species or ancestral species. The numbers with a plus or minus sign indicate estimated numbers of gene gains and losses, respectively, along each branch. Modified from Niimura and Nei (). © PLoS One.
Figure 5.

Evolution of OR genes in vertebrates. (a) Neighbour‐joining phylogenetic tree constructed by using all intact OR genes identified from amphioxus, lamprey, zebrafish, and human. Several non‐OR GPCR genes were used as the outgroup. Bootstrap values are shown for major clades. Modified from Niimura (). © Oxford University Press. (b) Number of intact OR genes in each gene group for each species. The volume of a sphere is proportional to the number of genes in the group. Terrestrial‐type and aquatic‐type OR genes are represented by red and blue, respectively. Data from Niimura () and Wang et al. ().
close

References

Barton RA (2006) Olfactory evolution and behavioral ecology in primates. American Journal of Primatology 68: 545–558.

Baydar A, Petrzilka M and Schott M (1993) Olfactory thresholds for androstenone and Galaxolide: sensitivity, insensitivity and specific anosmia. Chemical Senses 18: 661–668.

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

Bushdid C, Magnasco MO, Vosshall LB and Keller A (2014) Humans can discriminate more than 1 trillion olfactory stimuli. Science 343: 1370–1372.

Cummins SF, Erpenbeck D, Zou Z et al. (2009) Candidate chemoreceptor subfamilies differentially expressed in the chemosensory organs of the mollusc Aplysia. BMC Biology 7: 28.

Flegel C, Manteniotis S, Osthold S, Hatt H and Gisselmann G (2013) Expression profile of ectopic olfactory receptors determined by deep sequencing. PLoS One 8: e55368.

Fredriksson R, Lagerström MC, Lundin LG and Schiöth HB (2003) The G‐protein‐coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Molecular Pharmacology 63: 1256–1272.

Gilad Y, Przeworski M and Lancet D (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biology 2: E5.

Go Y and Niimura Y (2008) Similar numbers but different repertoires of olfactory receptor genes in humans and chimpanzees. Molecular Biology and Evolution 25: 1897–1907.

Hayden S, Bekaert M, Crider TA et al. (2010) Ecological adaptation determines functional mammalian olfactory subgenomes. Genome Research 20: 1–9.

Herz R (2007) The Scent of Desire: Discovering Our Enigmatic Sense of Smell. New York, NY: HarperCollins Publishers.

Jaeger SR, McRae JF, Bava CM et al. (2013) A mendelian trait for olfactory sensitivity affects odor experience and food selection. Current Biology 23: 1601–1605.

Keller A, Zhuang H, Chi Q, Vosshall LB and Matsunami H (2007) Genetic variation in a human odorant receptor alters odour perception. Nature 449: 468–472.

Kirkness EF, Haas BJ, Sun W et al. (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proceedings of the National Academy of Sciences of the USA 107:12168–12173.

Mainland JD, Keller A, Li YR et al. (2014) The missense of smell: functional variability in the human odorant receptor repertoire. Nature Neuroscience 17: 114–120.

Matsui A, Go Y and Niimura Y (2010) Degeneration of olfactory receptor gene repertories in primates: no direct link to full trichromatic vision. Molecular Biology and Evolution 27: 1192–1200.

McRae JF, Mainland JD, Jaeger SR et al. (2012) Genetic variation in the odorant receptor OR2J3 is associated with the ability to detect the “grassy” smelling odor, cis‐3‐hexen‐1‐ol. Chemical Senses 37: 585–593.

Menashe I, Abaffy T, Hasin Y et al. (2007) Genetic elucidation of human hyperosmia to isovaleric acid. PLoS Biology 5: e284.

Mori K and Sakano H (2011) How is the olfactory map formed and interpreted in the mammalian brain? Annual Review of Neuroscience 34: 467–499.

Nei M and Rooney AP (2005) Concerted and birth‐and‐death evolution of multigene families. Annual Review of Genetics 39:121–152.

Nei M, Niimura Y and Nozawa M (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nature Reviews Genetics 9: 951–963.

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

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

Niimura Y and Nei M (2003) Evolution of olfactory receptor genes in the human genome. Proceedings of the National Academy of Sciences of the USA 100: 12235–12240.

Niimura Y and Nei M (2005a) Comparative evolutionary analysis of olfactory receptor gene clusters between humans and mice. Gene 346: 13–21.

Niimura Y and Nei M (2005b) Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods. Proceedings of the National Academy of Sciences of the USA 102: 6039–6044.

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

Niimura Y (2009) On the origin and evolution of vertebrate olfactory receptor genes: comparative genome analysis among 23 chordate species. Genome Biology and Evolution 1: 34–44.

Niimura Y (2012a) Evolution of chemosensory receptor genes in primates and other mammals. In: Hirai H, Imai G, Go Y (eds) Post‐Genome Biology of Primates, pp. 43–62. Tokyo: Springer.

Niimura Y (2012b) Olfactory receptor multigene family in vertebrates: from the viewpoint of evolutionary genomics. Current Genomics 13: 103–114.

Olender T, Waszak SM, Viavant M et al. (2012) Personal receptor repertoires: olfaction as a model. BMC Genomics 13: 414.

Parmentier M, Libert F, Schurmans S et al. (1992) Expression of members of the putative olfactory receptor gene family in mammalian germ cells. Nature 355: 453–455.

Peñalva‐Arana DC, Lynch M and Robertson HM (2009) The chemoreceptor genes of the waterflea Daphnia pulex: many Grs but no Ors. BMC Evolutionary Biology 9: 79.

Raible F, Tessmar‐Raible K, Arboleda E et al. (2006) Opsins and clusters of sensory G‐protein‐coupled receptors in the sea urchin genome. Developmental Biology 300: 461–475.

Rossiter KJ (1996) Structure‐odor relationships. Chemical Reviews 96: 3201–3240.

Saito H, Chi Q, Zhuang H, Matsunami H and Mainland JD (2009) Odor coding by a mammalian receptor repertoire. Science Signaling 2: ra9.

Sato K, Pellegrino M, Nakagawa T et al. (2008) Insect olfactory receptors are heteromeric ligand‐gated ion channels. Nature 452: 1002–1006.

Shirasu M, Yoshikawa K, Takai Y et al. (2014) Olfactory receptor and neural pathway responsible for highly selective sensing of musk odors. Neuron 81: 165–178.

Spehr M, Gisselmann G, Poplawski A et al. (2003) Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299: 2054–2058.

Thomas JH and Robertson HM (2008) The Caenorhabditis chemoreceptor gene families. BMC Biology 6: 42.

Tribolium Genome Sequencing Consortium (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452: 949–955.

Wang Z, Pascual‐Anaya J, Zadissa A et al. (2013) The draft genomes of soft‐shell turtle and green sea turtle yield insights into the development and evolution of the turtle‐specific body plan. Nature Genetics 45: 701–706.

Wicher D, Schäfer R, Bauernfeind R et al. (2008) Drosophila odorant receptors are both ligand‐gated and cyclic‐nucleotide‐activated cation channels. Nature 452: 1007–1111.

Whissell‐Buechy D and Amoore JE (1973) Odour‐blindness to musk: simple recessive inheritance. Nature 242: 271–273.

Young JM, Shykind BM, Lane RP et al. (2003) Odorant receptor expressed sequence tags demonstrate olfactory expression of over 400 genes, extensive alternate splicing and unequal expression levels. Genome Biology 4: R71.

Further Reading

Bargmann CI (2006) Comparative chemosensation from receptors to ecology. Nature 444: 295–301.

Crasto CJ (ed.) (2013) Olfactory Receptors. New York, NY: Humana Press.

Wyatt TD (2003) Pheromones and Animal Behavior: Chemical Signals and Signatures. Cambridge: Cambridge University Press.

Related Sub-Topics:

Reconstruction of Phylogeny | Evolution of Coding and Functional Modules | Adaptive Evolution | Human Evolution | Molecular Evolution | Sensory Systems | Protein Evolution
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Olfactory Receptor Genes: Evolution
 
How to Cite close
Niimura, Yoshihito(Aug 2014) Olfactory Receptor Genes: Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020789.pub2]