Skip to main content

Bitter Taste Receptors of Primates

  • Chapter
  • First Online:
  • 1337 Accesses

Part of the book series: SpringerBriefs in Biology ((BRIEFSBIOL))

Abstract

Bitter taste perception is a key detection mechanism acting to protect animals against the ingestion of bioactive molecules. Recent progress in the analysis of human bitter taste receptors, TAS2Rs, revealed the molecular basis of our bitter taste sensation. Although humans don’t depend solely on the taste to protect against harmful bioactive molecules, but also use some detoxifying tools against them, it is important to investigate bitter taste receptors of wild primates to understand the evolution and biological roles of bitter taste sensation. In this chapter, I will review the recent progress in the analysis of bitter taste receptors of primates and discuss the evolutionary aspects of these receptors. At the population level, the importance of diversity in the species is suggested by the evolutionary analysis of chimpanzee TAS2Rs. Within a species, we found that some geographical region-­specific mutation of TAS2R occurs and is maintained in Japanese macaques, as shown by genomic screening, biochemical assay, and behavioral test. Regarding the species differences, we proposed the idea that bitter taste receptors of each species show a specific pattern of sensitivities to natural ligands, suggesting the important role of amino acid changes in the course of evolution of TAS2Rs. These observations clarify some aspects of the molecular evolutionary history of TAS2Rs in wild primates.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS (2000) A novel family of mammalian taste receptors. Cell 100:693–702

    Article  PubMed  CAS  Google Scholar 

  • Behrens M, Meyerhof W (2010) Oral and extraoral bitter taste receptors. Results Probl Cell Differ 52:87–99

    Article  PubMed  CAS  Google Scholar 

  • 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 14:12630–12640

    Article  Google Scholar 

  • Behrens M, Brockhoff A, Batram C, Kuhn C, Appendino G, Meyerhof W (2009) The human bitter taste receptor hTAS2R50 is activated by the two natural bitter terpenoids andrographolide and amarogentin. J Agric Food Chem 57:9860–9866

    Article  PubMed  CAS  Google Scholar 

  • Behrens M, Meyerhof W, Hellfritsch C, Hofmann T (2011) Sweet and umami taste: natural products, their chemosensory targets, and beyond. Angew Chem Int Ed Engl 50:2220–2242

    PubMed  CAS  Google Scholar 

  • Biarnés X, Marchiori A, Giorgetti A, Lanzara C, Gasparini P, Carloni P, Born S, Brockhoff A, Behrens M, Meyerhof W (2010) Insights into the binding of phenyltiocarbamide (PTC) agonist to its target human TAS2R38 bitter receptor. PLoS One 5:e12394

    Article  PubMed  Google Scholar 

  • Brockhoff A, Behrens M, Massarotti A, Appendino G, Meyerhof W (2007) Broad tuning of the human bitter taste receptor hTAS2R46 to various sesquiterpene lactones, clerodane and labdane diterpenoids, strychnine, and denatonium. J Agric Food Chem 55:6236–6243

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bufe B, Breslin PA, Kuhn C, Reed DR, Tharp CD, Slack JP, Kim U-K (2005) The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol 15:322–327

    Article  PubMed  CAS  Google Scholar 

  • Campbell MC, Ranciaro A, Froment A, Hirbo J, Omar S, Bodo JM, Nyambo T, Lema G, Zinshteyn D, Drayna D, Breslin P, Tishkoff SA (2012) Evolution of functionally diverse alleles associated with PTC bitter taste sensitivity in Africa. Mol Biol Evol 29(4):1141–1153. doi:10.1093/molbev/msr293

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chandrashekar J, Hoon MA, Ryba NJ, Zuker CS (2006) The receptors and cells for mammalian taste. Nature 444:288–294

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Gabitto M, Peng Y, Ryba NJ, Zuker CS (2011) A gustotopic map of taste qualities in the mammalian brain. Science 333:1262–1266

    Article  PubMed  CAS  Google Scholar 

  • Chiarelli B (1963) Sensitivity to P.T.C (phenyl-thio-carbamide) in primates. Folia Primatol 1:88–94

    Article  Google Scholar 

  • Chivers DJ (1994) Diets and guts. In: Martin RD (ed) The Cambridge encyclopedia of human evolution. Cambridge University Press, New York

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Fischer A, Gilad Y, Man O, Pääbo S (2005) Evolution of bitter taste receptors in humans and apes. Mol Biol Evol 22:432–436

    Article  PubMed  CAS  Google Scholar 

  • Fisher RA, Ford EB, Huxley J (1939) Taste-testing the anthropoid apes. Nature 144:750

    Article  Google Scholar 

  • Glendinning JI (1994) Is the bitter rejection response always adaptive? Physiol Behav 56:1217–1227

    Article  PubMed  CAS  Google Scholar 

  • Go Y (2006) Lineage-specific expansions and contractions of the bitter taste receptor gene repertoire in vertebrates. Mol Biol Evol 23:964–972

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Huffman MA (1989) Observations on the illness and consumption of a possibly medicinal plant Vernonia amygdalina (DEE.), by a wild chimpanzee in the Mahale Mountains National Park, Tanzania. Primates 30:51–63

    Article  Google Scholar 

  • Huffman MA, Nakagawa N, Go Y, Imai H, Tomonaga M (2013) Monkeys, apes, and us: primatology in Japan. Springer

    Google Scholar 

  • Imai H, Suzuki N, Ishimaru Y, Sakurai T, Yin L, Pan W, Abe K, Misaka T, Hirai H (2012) Functional diversity of bitter taste receptor TAS2R16 in primates. Biol Lett 8:652–656

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kim U, 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

    Article  PubMed  CAS  Google Scholar 

  • Koshimizu K, Ohigashi H, Huffman MA (1994) Use of Vernonia amygdalina by wild chimpanzee: possible roles of its bitter and related constituents. Physiol Behav 56:1209–1216

    Article  PubMed  CAS  Google Scholar 

  • Kuhn C, Bufe B, Batram C, Meyerhof W (2010) Oligomerization of TAS2R bitter taste receptors. Chem Senses 35:395–406

    Article  PubMed  CAS  Google Scholar 

  • Lalueza-Fox C, Gigli E, de la Rasilla M, Fortea J, Rosas A (2009) Bitter taste perception in Neanderthals through the analysis of the TAS2R38 gene. Biol Lett 5:809–811

    Article  PubMed  Google Scholar 

  • Margolskee RF (2002) Molecular mechanisms of bitter and sweet taste transduction. J Biol Chem 277:1–4

    Article  PubMed  CAS  Google Scholar 

  • Matsunami H, Montmayeur JP, Buck LB (2000) A family of candidate taste receptors in human and mouse. Nature 404:601–604

    Article  PubMed  CAS  Google Scholar 

  • Meyerhof W (2005) Elucidation of mammalian bitter taste. Rev Physiol Biochem Pharmacol 154:37–72

    Article  PubMed  CAS  Google Scholar 

  • Meyerhof W, Batram C, Kuhn C, Brockhoff A, Chudoba E, Bufe B, Appendino G, Behrens M (2010) The molecular receptive ranges of human TAS2R bitter taste receptors. Chem Senses 35:157–170

    Article  PubMed  CAS  Google Scholar 

  • Mueller KL, Hoon MA, Erlenbach I, Chandrashekar J, Zuker CS, Ryba NJ (2005) The receptors and coding logic for bitter taste. Nature 434:225–229

    Article  PubMed  CAS  Google Scholar 

  • Nishida T, Uehara S (1983) Natural diet of chimpanzees (Pan troglodytes schweinfurthii): long-­term record from the Mahale Mountains, Tanzania. Afr Study Monogr 3:109–130

    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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pronin AN, Xu H, Tang H, Zhang L, Li Q, Li X (2007) Specific alleles of bitter receptor genes influence human sensitivity to the bitterness of aloin and saccharin. Curr Biol 17:1403–1408

    Article  PubMed  CAS  Google Scholar 

  • Sakurai T, Misaka T, Ishiguro M, Masuda K, Sugawara T, Ito K, Kobayashi T, Matsuo S, Ishimaru Y, Asakura T, Abe K (2010) Characterization of the beta-d-glucopyranoside binding site of the human bitter taste receptor hTAS2R16. J Biol Chem 285:28373–28378

    Article  PubMed  CAS  Google Scholar 

  • Sandell MA, Breslin PA (2006) Variability in a taste-receptor gene determines whether we taste toxin in food. Curr Biol 16:792–794

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stanford CB (1998) Chimpanzee and red colobus: the ecology of predator and prey. Harvard University Press, Cambridge

    Google Scholar 

  • Sugawara T, Go Y, Udono T, Morimura N, Tomonaga M, Hirai H, Imai H (2011) Diversification of bitter taste receptor gene family in western chimpanzees. Mol Biol Evol 28:921–931

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama Y, Koman J (1992) The flora of Bossou: its utilization by chimpanzees and humans. Afr Study Monogr 13:127–169

    Google Scholar 

  • Suzuki A (1965) An ecological study of wild Japanese monkeys in snowy areas. Primates 6:31–72

    Article  Google Scholar 

  • Suzuki N, Sugawara T, Matsui A, Go Y, Hirai H, Imai H (2010) Identification of non-taster Japanese macaques for a specific bitter taste. Primates 51:285–289

    Article  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Ueda T, Ugawa S, Yamamura H, Imaizumi Y, Shimada S (2003) Functional interaction between T2R taste receptors and G-protein alpha subunits expressed in taste receptor cells. J Neurosci 23:7376–7380

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wooding S (2006) Phenylthiocarbamide: a 75-year adventure in genetics and natural selection. Genetics 172:2015–2023

    PubMed  CAS  Google Scholar 

  • Wooding S (2011) Signatures of natural selection in a primate bitter taste receptor. J Mol Evol 73:257–265

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yarmolinsky DA, Zuker CS, Ryba NJ (2009) Common sense about taste: from mammals to insects. Cell 139:234–244

    Article  PubMed  CAS  Google Scholar 

  • Yin L, Liu W, Zhao Q, Qin D, Li X, Wang D, Jin T, Chen M, Pan W (2011) A video-aided study of the diet of wild white-headed Langurs (Trachypithecus leucocephalus). Folia Primatol 82:33–44

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

I thank Ms. N. Suzuki, Mr. T. Hayakawa, Drs. T. Sugawara, Y. Go, A. Matsui, and H. Hirai, in the Molecular Biology Section, the Kyoto University Primate Research Institute, for valuable discussions and Drs. Y. Ishimaru, T. Misaka, and K. Abe of the University of Tokyo for cooperation in functional analysis of TAS2Rs. I also thank Dr. E. Nakajima for English correction. Our work was financially supported by Global COE program A06 and by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (2137009, 22247036, 22650053), and from the Ministry of the Environment (D-1007) and grants from the Takeda Foundation for Science and the Suzuken Memorial Foundation to H.I.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2013 The Author(s)

About this chapter

Cite this chapter

Shichida, Y., Yamashita, T., Imai, H., Kishida, T. (2013). Bitter Taste Receptors of Primates. In: Evolution and Senses. SpringerBriefs in Biology. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54222-3_2

Download citation

Publish with us

Policies and ethics