Abstract
Chemosensation (smell and taste) is important to the survival and reproduction of vertebrates and is mediated by specific bindings of odorants, pheromones, and tastants by chemoreceptors that are encoded by several large gene families. This review summarizes recent comparative genomic and evolutionary studies of vertebrate chemoreceptor genes. It focuses on the remarkable diversity of chemoreceptor gene repertoires in terms of gene number and gene sequence across vertebrates and the evolutionary mechanisms that are responsible for generating this diversity. We argue that the great among-species variation of chemoreceptor gene repertoires is a result of adaptations of individual species to their environments and diets.
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS (2000) A novel family of mammalian taste receptors. Cell 100:693–702
Alioto TS, Ngai J (2005) The odorant receptor repertoire of teleost fish. BMC Genomics 6:173
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
Behrens M, Foerster S, Staehler F, Raguse JD, Meyerhof W (2007) Gustatory expression pattern of the human TAS2R bitter receptor gene family reveals a heterogenous population of bitter responsive taste receptor cells. J Neurosci 27:12630–12640
Borowsky B, Adham N, Jones KA, Raddatz R, Artymyshyn R, Ogozalek KL, Durkin MM, Lakhlani PP, Bonini JA, Pathirana S, Boyle N, Pu X, Kouranova E, Lichtblau H, Ochoa FY, Branchek TA, Gerald C (2001) Trace amines: identification of a family of mammalian G protein-coupled receptors. Proc Natl Acad Sci USA 98:8966–8971
Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611–618
Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187
Bufe B, Hofmann T, Krautwurst D, Raguse JD, Meyerhof W (2002) The human TAS2R16 receptor mediates bitter taste in response to beta-glucopyranosides. Nat Genet 32:397–401
Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, Saghatelian A, Cravatt BF, Stowers L (2007) Identification of protein pheromones that promote aggressive behaviour. Nature 450:899–902
Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ (2000) T2Rs function as bitter taste receptors. Cell 100:703–711
Conte C, Ebeling M, Marcuz A, Nef P, Andres-Barquin PJ (2002) Identification and characterization of human taste receptor genes belonging to the TAS2R family. Cytogenet Genome Res 98:45–53
Conte C, Ebeling M, Marcuz A, Nef P, Andres-Barquin PJ (2003) Evolutionary relationships of the Tas2r receptor gene families in mouse and human. Physiol Genomics 14:73–82
Dulac C (1997) Molecular biology of pheromone perception in mammals. Semin Cell Dev Biol 8:197–205
Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195–206
Dulac C, Torello AT (2003) Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 4:551–562
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
Fischer A, Gilad Y, Man O, Paabo S (2005) Evolution of bitter taste receptors in humans and apes. Mol Biol Evol 22:432–436
Gilad Y, Lancet D (2003) Population differences in the human functional olfactory repertoire. Mol Biol Evol 20:307–314
Gilad Y, Wiebe V, Przeworski M, Lancet D, Paabo S (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol 2:E5
Gilad Y, Man O, Glusman G (2005) A comparison of the human and chimpanzee olfactory receptor gene repertoires. Genome Res 15:224–230
Gilad Y, Man O, Paabo S, Lancet D (2003) Human specific loss of olfactory receptor genes. Proc Natl Acad Sci U S A 100:3324–3327
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
Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–702
Go Y (2006) Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Lineage-specific expansions and contractions of the bitter taste receptor gene repertoire in vertebrates. Mol Biol Evol 23:964–972
Go Y, Satta Y, Takenaka O, Takahata N (2005) Lineage-specific loss of function of bitter taste receptor genes in humans and nonhuman primates. Genetics 170:313–326
Grus WE, Zhang J (2004) Rapid turnover and species-specificity of vomeronasal pheromone receptor genes in mice and rats. Gene 340:303–312
Grus WE, Zhang J (2006) Origin and evolution of the vertebrate vomeronasal system viewed through system-specific genes. Bioessays 28:709–718
Grus WE, Shi P, Zhang YP, Zhang JZ (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
Grus WE, Shi P, Zhang JZ (2007) Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol Biol Evol 24:2153–2157
Hashiguchi Y, Nishida M (2005) Evolution of vomeronasal-type odorant receptor genes in the zebrafish genome. Gene 362:19–28
Hashiguchi Y, Nishida M (2006) Evolution and origin of vomeronasal-type odorant receptor gene repertoire in fishes. BMC Evol Biol 6:76
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
Hashiguchi Y, Furuta Y, Kawahara R, Nishida M (2007) Diversification and adaptive evolution of putative sweet taste receptors in threespine stickleback. Gene 396:170–179
Herness MS, Gilbertson TA (1999) Cellular mechanisms of taste transduction. Annu Rev Physiol 61:873–900
Herrada G, Dulac C (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763–773
Hoon MA, Adler E, Lindemeier J, Battey JF, Ryba NJ, Zuker CS (1999) Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96:541–551
Hughes AL, Hughes MK (1993) Adaptive evolution in the rat olfactory receptor gene family. J Mol Evol 36:249–254
Keverne EB (1999) The vomeronasal organ. Science 286:716–720
Kim UK, Jorgenson E, Coon H, Leppert M, Risch N, Drayna D (2003) Positional cloning of the human quantitative trait locus underlying taste sensitivity to phenylthiocarbamide. Science 299:1221–1225
Kim UK, Wooding S, Ricci D, Jorde LB, Drayna D (2005) Worldwide haplotype diversity and coding sequence variation at human bitter taste receptor loci. Hum Mutat 26:199–204
Kim UK, Wooding S, Riaz N, Jorde LB, Drayna D (2006) Variation in the human TAS1R taste receptor genes. Chem Senses 31:599–611
Kimoto H, Haga S, Sato K, Touhara K (2005) Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898–901
Kinnamon SC, Margolskee RF (1996) Mechanisms of taste transduction. Curr Opin Neurobiol 6:506–513
Kitagawa M, Kusakabe Y, Miura H, Ninomiya Y, Hino A (2001) Molecular genetic identification of a candidate receptor gene for sweet taste. Biochem Biophys Res Commun 283:236–242
Lane RP, Young J, Newman T, Trask BJ (2004) Species specificity in rodent pheromone receptor repertoires. Genome Res 14:603–608
Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E (2002) Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 99:4692–4696
Li X, Li W, Wang H, Cao J, Maehashi K, Huang L, Bachmanov AA, Reed DR, Legrand-Defretin V, Beauchamp GK, Brand JG (2005) Pseudogenization of a sweet-receptor gene accounts for cats' indifference toward sugar. PLoS Genet 1:e3
Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645–650
Liman ER, Innan H (2003) Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci USA 100:3328–3332
Lindemann B (2001) Receptors and transduction in taste. Nature 413:219–225
Loconto J, Papes F, Chang E, Stowers L, Jones EP, Takada T, Kumanovics A, Fischer Lindahl K, Dulac C (2003) Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112:607–618
Malnic B, Godfrey PA, Buck LB (2004) The human olfactory receptor gene family. Proc Natl Acad Sci USA 101:2584–2589
Matsunami H, Buck LB (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775–784
Matsunami H, Montmayeur JP, Buck LB (2000) A family of candidate taste receptors in human and mouse. Nature 404:601–604
Max M, Shanker YG, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF (2001) Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet 28:58–63
Menashe I, Man O, Lancet D, Gilad Y (2003) Different noses for different people. Nat Genet 34:143–144
Meyerhof W (2005) Elucidation of mammalian bitter taste. Rev Physiol Biochem Pharmacol 154:37–72
Mombaerts P (1999) Molecular biology of odorant receptors in vertebrates. Annu Rev Neurosci 22:487–509
Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278
Montmayeur JP, Liberles SD, Matsunami H, Buck LB (2001) A candidate taste receptor gene near a sweet taste locus. Nat Neurosci 4:492–498
Mundy NI, Cook S (2003) Positive selection during the diversification of class I vomeronasal receptor-like (V1RL) genes, putative pheromone receptor genes, in human and primate evolution. Mol Biol Evol 20:1805–1810
Nei M (2007) The new mutation theory of phenotypic evolution. Proc Natl Acad Sci USA 104:12235–12242
Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA 94:7799–7806
Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS (2001) Mammalian sweet taste receptors. Cell 106:381–390
Niimura Y, Nei M (2003) Evolution of olfactory receptor genes in the human genome. Proc Natl Acad Sci USA 100:12235–12240
Niimura Y, Nei M (2005) Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods. Proc Natl Acad Sci USA 102:6039–6044
Niimura Y, Nei M (2006) Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates. J Hum Genet 51:505–517
Niimura Y, Nei M (2007) Extensive gains and losses of olfactory receptor genes in Mammalian evolution. PLoS ONE 2:e708
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
Parry CM, Erkner A, le Coutre J (2004) Divergence of T2R chemosensory receptor families in humans, bonobos, and chimpanzees. Proc Natl Acad Sci USA 101:14830–14834
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
Pfister P, Randall J, Montoya-Burgos JI, Rodriguez I (2007) Divergent evolution among teleost V1r receptor genes. PLoS ONE 2:e379
Prasad BC, Reed RR (1999) Chemosensation: molecular mechanisms in worms and mammals. Trends Genet 15:150–153
Rodriguez I, Mombaerts P (2002) Novel human vomeronasal receptor-like genes reveal species—specific families. Curr Biol 12:R409–411
Rodriguez I, Del Punta K, Rothman A, Ishii T, Mombaerts P (2002) Multiple new and isolated families within the mouse superfamily of V1r vomeronasal receptors. Nat Neurosci 5:134–140
Rouquier S, Blancher A, Giorgi D (2000) The olfactory receptor gene repertoire in primates and mouse: evidence for reduction of the functional fraction in primates. Proc Natl Acad Sci USA 97:2870–2874
Ryba NJ, Tirindelli R (1997) A new multigene family of putative pheromone receptors. Neuron 19:371–379
Sainz E, Korley JN, Battey JF, Sullivan SL (2001) Identification of a novel member of the T1R family of putative taste receptors. J Neurochem 77:896–903
Saraiva LR, Korsching SI (2007) A novel olfactory receptor gene family in teleost fish. Genome Res 17:1448–1457
Shi P, Zhang J (2006) Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol 23:292–300
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
Shi P, Zhang J, Yang H, Zhang YP (2003) Adaptive diversification of bitter taste receptor genes in mammalian evolution. Mol Biol Evol 20:805–814
Shi P, Bielawski JP, Yang H, Zhang YP (2005) Adaptive diversification of vomeronasal receptor 1 genes in rodents. J Mol Evol 60:566–576
Smith CUM (2000) Biology of sensory systems. Wiley, New York
Soranzo N, Bufe B, Sabeti PC, Wilson JF, Weale ME, Marguerie R, Meyerhof W, Goldstein DB (2005) Positive selection on a high-sensitivity allele of the human bitter-taste receptor TAS2R16. Curr Biol 15:1257–1265
Tacher S, Quignon P, Rimbault M, Dreano S, Andre C, Galibert F. (2005) Olfactory receptor sequence polymorphism within and between breeds of dogs. J Hered 96: 812–816
Trask BJ, Friedman C, Martin-Gallardo A, Rowen L, Akinbami C, Blankenship J, Collins C, Giorgi D, Iadonato S, Johnson F, Kuo WL, Massa H, Morrish T, Naylor S, Nguyen OT, Rouquier S, Smith T, Wong DJ, Youngblom J, van den Engh G. (1998) Members of the olfactory receptor gene family are contained in large blocks of DNA duplicated polymorphically near the ends of human chromosomes. Hum Mol Genet 7: 13–26
Wang X, Thomas SD, Zhang J. (2004) Relaxation of selective constraint and loss of function in the evolution of human bitter taste receptor genes. Hum Mol Genet 13: 2671–2678
Wong KK, deLeeuw RJ, Dosanjh NS, Kimm LR, Cheng Z, Horsman DE, MacAulay C, Ng RT, Brown CJ, Eichler EE, Lam WL. (2007) A comprehensive analysis of common copy-number variations in the human genome. Am J Hum Genet 80: 91–104
Wooding S, Kim UK, Bamshad MJ, Larsen J, Jorde LB, Drayna D. (2004) Natural selection and molecular evolution in PTC, a bitter-taste receptor gene. Am J Hum Genet 74: 637–646
Wooding S, Bufe B, Grassi C, Howard MT, Stone AC, Vazquez M, Dunn DM, Meyerhof W, Weiss RB, Bamshad MJ. (2006) Independent evolution of bitter-taste sensitivity in humans and chimpanzees. Nature 440: 930–934
Yang H, Shi P, Zhang YP, Zhang JZ. (2005) Composition and evolution of the V2r vorneronasal receptor gene repertoire in mice and rats. Genomics 86: 306–315
Young JM, Trask BJ. (2002) The sense of smell: genomics of vertebrate odorant receptors. Human Molecular Genetics 11: 1153–1160
Young JM, Trask BJ. (2007) V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet 23: 212–215
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 Res 15: 231–240
Zhang J. (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18: 292–298
Zhang J. (2007) The drifting human genome. Proc Natl Acad Sci U S A 104: 20147–20148
Zhang J, Webb DM. (2003) Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci U S A 100: 8337–8341
Zhang X, Rodriguez I, Mombaerts P, Firestein S. (2004) Odorant and vomeronasal receptor genes in two mouse genome assemblies. Genomics 83: 802–811
Zhang X, Zhang X, Firestein S. (2007) Comparative genomics of odorant and pheromone receptor genes in rodents. Genomics 89: 441–450
Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS. (2003) The receptors for mammalian sweet and umami taste. Cell 115: 255–266
Zozulya S, Echeverri F, Nguyen T. (2001) The human olfactory receptor repertoire. Genome Biol 2: RESEARCH0018
Acknowledgement
This work was supported by a start-up fund of “Hundreds-Talent Program” from Chinese Academy of Sciences to P.S. and research grants from the National Institutes of Health to J.Z.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer-Verlag London
About this chapter
Cite this chapter
Shi, P., Zhang, J. (2009). Extraordinary Diversity of Chemosensory Receptor Gene Repertoires Among Vertebrates. 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_4
Download citation
DOI: https://doi.org/10.1007/400_2008_4
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-69918-7
Online ISBN: 978-3-540-69919-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)