The loss of taste genes in cetaceans

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Zhu, Kangli ^a   Zhou, Xuming ^b   Xu, Shixia ^a   Sun, Di ^a   Ren, Wenhua ^a   Zhou, Kaiya ^a   Yang, Guang ^a  

^a NANJING NORMAL UNIVERSITY   (China)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Cetacean; Molecular evolution; Pseudogenization; Taste genes

Indexed keywords

ADAPTATION; CETACEAN; GENE EXPRESSION; GENETIC ANALYSIS; MOLECULAR ANALYSIS; OSMOREGULATION; SALT; SENSORY SYSTEM; TASTE;

CETACEA; MAMMALIA;

G PROTEIN COUPLED RECEPTOR; SODIUM CHLORIDE;

ANIMAL; CETACEA; CLASSIFICATION; EVOLUTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHYSIOLOGY; TASTE BUD;

ANIMALS; BIOLOGICAL EVOLUTION; CETACEA; EVOLUTION, MOLECULAR; RECEPTORS, G-PROTEIN-COUPLED; SODIUM CHLORIDE; TASTE BUDS;

EID: 84964313013     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-014-0218-8     Document Type: Article

References (99)

1. Gatesy J, Geisler JH, Chang J, Buell C, Berta A, Meredith RW, Springer MS, McGowen MR: A phylogenetic blueprint for a modern whale. Mol Phylogenet Evol 2013, 66:479-506.
2. Zhou X, Xu S, Yang Y, Zhou K, Yang G: Phylogenomic analyses and improved resolution of Cetartiodactyla. Mol Phylogenet Evol 2011, 61:255-264.
3. Fordyce RE: Origins and evolution of Antarctic marine mammals. Geol Soc London Spec Publ 1989, 47:269-281.
4. Thewissen J, Cooper LN, George JC, Bajpai S: From land to water: the origin of whales, dolphins, and porpoises. Evo Edu Outreach 2009, 2:272-288.
5. Uhen MD: The origin (s) of whales. Annu Rev Earth Pl Sc 2010, 38:189-219.
6. Liu Y, Cotton JA, Shen B, Han X, Rossiter SJ, Zhang S: Convergent sequence evolution between echolocating bats and dolphins. Curr Biol 2010, 20:R53-R54.
7. Liu Y, Rossiter SJ, Han X, Cotton JA, Zhang S: Cetaceans on a molecular fast track to ultrasonic hearing. Curr Biol 2010, 20:1834-1839.
8. Davies K, Cotton JA, Kirwan JD, Teeling EC, Rossiter SJ: Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence. Heredity 2012, 108:480-489.
9. Kishida T, Kubota S, Shirayama Y, Fukami H: The olfactory receptor gene repertoires in secondary-adapted marine vertebrates: evidence for reduction of the functional proportions in cetaceans. Biol Lett 2007, 3:428-430.
10. McGowen MR, Clark C, Gatesy J: The vestigial olfactory receptor subgenome of odontocete whales: phylogenetic congruence between gene-tree reconciliation and supermatrix methods. Syst Biol 2008, 57:574-590.
11. Hayden S, Bekaert M, Crider TA, Mariani S, Murphy WJ, Teeling EC: Ecological adaptation determines functional mammalian olfactory subgenomes. Genome Res 2010, 20:1-9.
12. Zhou X, Sun F, Xu S, Fan G, Zhu K, Liu X, Chen Y, Shi C, Yang Y, Huang Z, Chen J, Hou H, Guo X, Chen W, Chen Y, Wang X, Lv T, Yang D, Zhou J, Huang B, Wang Z, Zhao W, Tian R, Xiong Z, Xu J, Liang X, Chen B, Liu W, Wang J, Pan S, et al: Baiji genomes reveal low genetic variability and new insights into secondary aquatic adaptations. Nat Commun 2013, 4:2708.
13. Kinnamon SC, Cummings TA: Chemosensory Transduction Mechanisms in Taste. Annu Rev Physiol 1992, 54:715-731.
14. Lindemann B: Taste reception. Physiol Rev 1996, 76:719-766.
15. Heck GL, Mierson S, DeSimone JA: Salt taste transduction occurs through an amiloride-sensitive sodium transport pathway. Science 1984, 223:403-405.
16. Hettinger TP, Frank ME: Specificity of amiloride inhibition of hamster taste responses. Brain Res 1990, 513:24-34.
17. Yoshida R, Horio N, Murata Y, Yasumatsu K, Shigemura N, Ninomiya Y: NaCl responsive taste cells in the mouse fungiform taste buds. Neuroscience 2009, 159:795-803.
18. Eylam S, Spector AC: Taste discrimination between NaCl and KCl is disrupted by amiloride in inbred mice with amiloride-insensitive chorda tympani nerves. Am J Physiol Regul Integr Comp Physiol 2005, 288:R1361-R1368.
19. Garcia J, Hankins WG: The evolution of bitter and the acquisition of toxiphobia. Olfaction Taste 1975, 5:39-45.
20. Glendinning JI: Is the bitter rejection response always adaptive? Physiol Behav 1994, 56:1217-1227.
21. Ganchrow JR, Steiner JE, Daher M: Neonatal facial expressions in response to different qualities and intensities of gustatory stimuli. Infant Behav Dev 1983, 6:473-484.
22. Bachmanov AA, Beauchamp GK: Taste receptor genes. Annu Rev Nutr 2006, 27:389-414.
23. Bachmanov AA, Li X, Reed DR, Ohmen JD, Li S, Chen Z, Tordoff MG, de Jong PJ, Wu C, West DB: Positional cloning of the mouse saccharin preference (Sac) locus. Chem Senses 2001, 26:925-933.
24. Max M, Shanker YG, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF: Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet 2001, 28:58-63.
25. Montmayeur J, Liberles SD, Matsunami H, Buck LB: A candidate taste receptor gene near a sweet taste locus. Nat Neurosci 2001, 4:492-498.
26. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS: Mammalian sweet taste receptors. Cell 2001, 106:381-390.
27. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS: An amino-acid taste receptor. Nature 2002, 416:199-202.
28. Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS: A novel family of mammalian taste receptors. Cell 2000, 100:693-702.
29. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ: T2Rs function as bitter taste receptors. Cell 2000, 100:703-711.
30. Matsunami H, Montmayeur J, Buck LB: A family of candidate taste receptors in human and mouse. Nature 2000, 404:601-604.
31. Jiang P, Josue J, Li X, Glaser D, Li W, Brand JG, Margolskee RF, Reed DR, Beauchamp GK: Major taste loss in carnivorous mammals. Proc Natl Acad Sci USA 2012, 109:4956-4961.
32. Ugawa S, Minami Y, Guo W, Saishin Y, Takatsuji K, Yamamoto T, Tohyama M, Shimada S: Receptor that leaves a sour taste in the mouth. Nature 1998, 395:555-556.
33. Stevens DR, Seifert R, Bufe B, Müller F, Kremmer E, Gauss R, Meyerhof W, Kaupp UB, Lindemann B: Hyperpolarization-activated channels HCN1 and HCN4 mediate responses to sour stimuli. Nature 2001, 413:631-635.
34. Richter TA, Dvoryanchikov GA, Chaudhari N, Roper SD: Acid-Sensitive Two-Pore Domain Potassium (K ~ 2P) Channels in Mouse Taste Buds. J Neurophysiol 2004, 92:1928.
35. LopezJimenez ND, Cavenagh MM, Sainz E, Cruzithier MA, Battey JF, Sullivan SL: Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co-expressed in a subset of taste receptor cells. J Neurochem 2006, 98:68-77.
36. Ishimaru Y, Inada H, Kubota M, Zhuang H, Tominaga M, Matsunami H: Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci USA 2006, 103:12569-12574.
37. Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, Tränkner D, Ryba NJ, Zuker CS: The cells and logic for mammalian sour taste detection. Nature 2006, 442:934-938.
38. Horio N, Yoshida R, Yasumatsu K, Yanagawa Y, Ishimaru Y, Matsunami H, Ninomiya Y: Sour taste responses in mice lacking PKD channels. PLoS One 2011, 6:e20007.
39. Huque T, Cowart BJ, Dankulich-Nagrudny L, Pribitkin EA, Bayley DL, Spielman AI, Feldman RS, Mackler SA, Brand JG: Sour ageusia in two individuals implicates ion channels of the ASIC and PKD families in human sour taste perception at the anterior tongue. PLoS One 2009, 4:e7347.
40. Chandrashekar J, Kuhn C, Oka Y, Yarmolinsky DA, Hummler E, Ryba NJ, Zuker CS: The cells and peripheral representation of sodium taste in mice. Nature 2010, 464:297-301.
41. Hummler E, Beermann F: Scnn1 sodium channel gene family in genetically engineered mice. J Am Soc Nephrol 2000, 11(suppl 2):S129-S134.
42. Shi P, Zhang J: Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol 2006, 23:292-300.
43. Li R, Fan W, Tian G, Zhu H, He L, Cai J, Huang Q, Cai Q, Li B, Bai Y, Zhang Z, Zhang Y, Wang W, Li J, Wei F, Li H, Jian M, Li J, Zhang Z, Nielsen R, Li D, Gu W, Yang Z, Xuan Z, Ryder OA, Leung FC, Zhou Y, Cao J, Sun X, Fu Y, et al: The sequence and de novo assembly of the giant panda genome. Nature 2009, 463:311-317.
44. Zhao H, Yang J, Xu H, Zhang J: Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo. Mol Biol Evol 2010, 27:2669-2673.
45. Zhao H, Zhou Y, Pinto CM, Charles-Dominique P, Galindo-González J, Zhang S, Zhang J: Evolution of the sweet taste receptor gene Tas1r2 in bats. Mol Biol Evol 2010, 27:2642-2650.
46. Zhao H, Xu D, Zhang S, Zhang J: Genomic and genetic evidence for the loss of umami taste in bats. Genome Biol Evol 2012, 4:73-79.
47. Li D, Zhang J: Diet shapes the evolution of the vertebrate bitter taste receptor gene repertoire. Mol Biol Evol 2014, 31:303-309.
48. Meyerhof W: Elucidation of mammalian bitter taste. Rev Physiol Biochem Pharmacol 2005, 154:37-72.
49. +-permeable nonselective cation channel. Proc Natl Aca Sci USA 2001, 98:1182-1187.
50. Nummela S, Hussain ST, Thewissen J: Cranial anatomy of Pakicetidae (Cetacea, Mammalia). J Vertebr Paleontol 2006, 26:746-759.
51. O'Leary MA, Uhen MD: The time of origin of whales and the role of behavioral changes in the terrestrial-aquatic transition. Paleobiology 1999, 25:534-556.
52. Miller D: Seals and Sea Lions. Stillwater: Voyageur Press; 1998.
53. Werth AJ: Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation. Anat Rec 2007, 290:546-568.
54. Yoshimura K, Shindoh J, Kobayashi K: Scanning electron microscopy study of the tongue and lingual papillae of the California sea lion (Zalophus californianus californianus). Anat Rec 2002, 267:146-153.
55. Yoshimura K, Kobayashi K: A comparative morphological study on the tongue and the lingual papillae of some marine mammals-Particularly of four species of odontoceti and zalophus. Shigaku= Odontology 1997, 85:385-407.
56. Li Y: The tongue of Baiji, Lipotes vexillifer. Acta Zool Sin 1983, 29:35-41 (In Chinese with English abstract).
57. Rozengurt E: Taste receptors in the gastrointestinal tract. I. Bitter taste receptors and α-gustducin in the mammalian gut. Am J Physiol-Gastr L 2006, 291:G171-G177.
58. Bezençon C, le Coutre J, Damak S: Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 2007, 32:41-49.
59. +-glucose cotransporter 1. Proc Natl Acad Sci USA 2007, 104:15075-15080.
60. Rozengurt E, Sternini C: Taste receptor signaling in the mammalian gut. Curr Opin Pharmacol 2007, 7:557-562.
61. Finger TE, Böttger B, Hansen A, Anderson KT, Alimohammadi H, Silver WL: Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc Natl Acad Sci USA 2003, 100:8981-8986.
62. Shah AS, Ben-Shahar Y, Moninger TO, Kline JN, Welsh MJ: Motile cilia of human airway epithelia are chemosensory. Science 2009, 325:1131-1134.
63. Deshpande DA, Wang WC, McIlmoyle EL, Robinett KS, Schillinger RM, An SS, Sham JS, Liggett SB: Bitter taste receptors on airway smooth muscle bronchodilate by localized calcium signaling and reverse obstruction. Nat Med 2010, 16:1299-1304.
64. Oya M, Suzuki H, Watanabe Y, Sato M, Tsuboi T: Amino acid taste receptor regulates insulin secretion in pancreatic β-cell line MIN6 cells. Genes Cells 2011, 16:608-616.
65. Ren X, Zhou L, Terwilliger R, Newton SS, De Araujo IE: Sweet taste signaling functions as a hypothalamic glucose sensor. Front Integr Neurosci 2009, 3:12.
66. Singh N, Vrontakis M, Parkinson F, Chelikani P: Functional bitter taste receptors are expressed in brain cells. Biochem Bioph Res Co 2011, 406:146-151.
67. Chaudhari N, Landin AM, Roper SD: A metabotropic glutamate receptor variant functions as a taste receptor. Nat Neurosci 2000, 3:113-119.
68. San Gabriel A, Uneyama H, Yoshie S, Torii K: Cloning and characterization of a novel mGluR1 variant from vallate papillae that functions as a receptor for L-glutamate stimuli. Chem Senses 2005, 30(suppl 1):i25-i26.
69. Toyono T, Seta Y, Kataoka S, Kawano S, Shigemoto R, Toyoshima K: Expression of metabotropic glutamate receptor group I in rat gustatory papillae. Cell Tissue Res 2003, 313:29-35.
70. Conigrave AD, Brown EM: Taste Receptors in the Gastrointestinal Tract II. l-Amino acid sensing by calcium-sensing receptors: implications for GI physiology. Am J Physiol-Gastr L 2006, 291:G753-G761.
71. Brand JG, Teeter JH, Silver WL: Inhibition by amiloride of chorda tympani responses evoked by monovalent salts. Brain Res 1985, 334:207-214.
72. + channel is made of three homologous subunits. Nature 1994, 367:463-467.
73. Collier DM, Snyder PM: Extracellular chloride regulates the epithelial sodium channel. J Biol Chem 2009, 284:29320-29325.
74. Kellenberger S, Schild L: Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 2002, 82:735-767.
75. Adams CM, Snyder PM, Welsh MJ: Interactions between subunits of the human epithelial sodium channel. J Biol Chem 1997, 272:27295-27300.
76. Firsov D, Robert-Nicoud M, Gruender S, Schild L, Rossier BC: Mutational analysis of cysteine-rich domains of the epithelium sodium channel (ENaC). Identification of cysteines essential for channel expression at the cell surface. J Biol Chem 1999, 274:2743-2749.
77. + channel deleted in Liddle's syndrome. EMBO J 1996, 15:2371.
78. + channel by Nedd4 in Liddle's syndrome. J Clin Invest 1999, 103:667-673.
79. Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591.
80. Weadick CJ, Chang BS: An improved likelihood ratio test for detecting site-specific functional divergence among clades of protein-coding genes. Mol Biol Evol 2012, 29:1297-1300.
81. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Pond SLK, Scheffler K: FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 2013, 30:1196-1205.
82. Woolley S, Johnson J, Smith MJ, Crandall KA, McClellan DA: TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics 2003, 19:671-672.
83. Garty H, Palmer LG: Epithelial sodium channels: function, structure, and regulation. Physiol Rev 1997, 77:359-396.
84. Hummler E, Barker P, Gatzy J, Beermann F, Verdumo C, Schmidt A, Boucher R, Rossier BC: Early death due to defective neonatal lung liquid clearance in αENaC-deficient mice. Nat Genet 1996, 12:325-328.
85. Chang SS, Grunder S, Hanukoglu A, Rösler A, Mathew PM, Hanukoglu I, Schild L, Lu Y, Shimkets RA, Nelson-Williams C: Mutations in subunits of the epithelial sodium channel cause salt wasting with hyperkalaemic acidosis, pseudohypoal-dosteronism type 1. Nat Genet 1996, 12:248-253.
86. Hansson JH, Nelson-Williams C, Suzuki H, Schild L, Shimkets R, Lu Y, Canessa C, Iwasaki T, Rossier B, Lifton RP: Hypertension caused by a truncated epithelial sodium channel γ subunit: genetic heterogeneity of Liddle syndrome. Nat Genet 1995, 11:76-82.
87. Hansson JH, Schild L, Lu Y, Wilson TA, Gautschi I, Shimkets R, Nelson-Williams C, Rossier BC, Lifton RP: A de novo missense mutation of the beta subunit of the epithelial sodium channel causes hypertension and Liddle syndrome, identifying a proline-rich segment critical for regulation of channel activity. Proc Natl Acad Sci USA 1995, 92:11495-11499.
88. Medway W, Geraci JR: Blood chemistry of the bottlenose dolphin (Tursiops truncatus). APS-Legacy Content 1965, 209:169-172.
89. Koopman HN, Westgate AJ, Read AJ, Gaskin DE: Blood chemistry of wild harbor porpoises Phocoena phocoena (L.). Mar Mammal Sci 1995, 11:123-135.
90. Ortiz RM: Osmoregulation in marine mammals. J Exp Biol 2001, 204:1831-1844.
91. Kjeld M: Salt and water balance of modern baleen whales: rate of urine production and food intake. Can J Zoo 2003, 81:606-616.
92. Birukawa N, Ando H, Goto M, Kanda N, Pastene LA, Nakatsuji H, Hata H, Urano A: Plasma and urine levels of electrolytes, urea and steroid hormones involved in osmoregulation of cetaceans. Zool Sci 2005, 22:1245-1257.
93. Hoelzel AR: Molecular Genetic Analysis of Populations: A Practical Approach. Oxford: IRL Press; 1992.
94. Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
95. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
96. Nikaido M, Rooney AP, Okada N: Phylogenetic relationships among cetartiodactyls based on insertions of short and long interspersed elements: hippopotamuses are the closest extant relatives of whales. Proc Natl Acad Sci USA 1999, 96:10261-10266.
97. Agnarsson I, May-Collado LJ: The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. Mol Phylogenet Evol 2008, 48:964-985.
98. Xiong Y, Brandley MC, Xu S, Zhou K, Yang G: Seven new dolphin mitochondrial genomes and a time-calibrated phylogeny of whales. BMC Evol Biol 2009, 9:20.
99. Zhu K-L, Zhou X-M, Xu S-X, Sun D, Zhou K-Y, Yang G: Data from The loss of taste genes in cetaceans. Dryad Digital Repos 2014, http://dx.doi.org/10.5061/dryad.7qp63.