Genetic variation in taste receptor pseudogenes provides evidence for a dynamic role in human evolution

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Risso, Davide ^a,b   Tofanelli, Sergio ^c   Morini, Gabriella ^d   Luiselli, Donata ^b   Drayna, Dennis ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF PISA   (Italy)

^d UNIVERSITY OF GASTRONOMIC SCIENCES   (Italy)

Author keywords

Bitter taste; Evolution; Genetic polymorphisms; Pseudogenization; TAS2Rs

Indexed keywords

ALLELE; GENETIC VARIATION; HUMAN EVOLUTION; POLYMORPHISM; TASTE;

AFRICA;

G PROTEIN COUPLED RECEPTOR; TASTE RECEPTORS, TYPE 2;

AFRICA; ANIMAL; GENETIC SELECTION; GENETICS; HUMAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PRIMATE; PSEUDOGENE; SINGLE NUCLEOTIDE POLYMORPHISM; TASTE;

AFRICA; ANIMALS; BASE SEQUENCE; EVOLUTION, MOLECULAR; HUMANS; MOLECULAR SEQUENCE DATA; POLYMORPHISM, SINGLE NUCLEOTIDE; PRIMATES; PSEUDOGENES; RECEPTORS, G-PROTEIN-COUPLED; SELECTION, GENETIC; TASTE;

EID: 84908100999     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-014-0198-8     Document Type: Article

References (49)

1. The evolution of bitter and the acquisition of toxiphobia. J Garcia, WG Hankins, Olfaction and Taste 1975 5 39 45
2. T2Rs function as bitter taste receptors. J Chandrashekar, KL Mueller, MA Hoon, E Adler, L Feng, W Guo, CS Zuker, NJ Ryba, Cell 2000 100 6 703 711 10.1016/S0092-8674(00)80706-0 10761935
3. Functional diversity of bitter taste receptor TAS2R16 in primates. H Imai, N Suzuki, Y Ishimaru, T Sakurai, L Yin, W Pan, K Abe, T Misaka, H Hirai, Biol Lett 2012 8 4 652 656 10.1098/rsbl.2011.1251 22399783
4. Is the bitter rejection response always adaptive? JI Glendinning, Physiol Behav 1994 56 6 1217 1227 10.1016/0031-9384(94)90369-7 7878094
5. Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. P Shi, J Zhang, Mol Biol Evol 2006 23 2 292 300 10.1093/molbev/msj028 16207936
6. A novel family of mammalian taste receptors. E Adler, MA Hoon, KL Mueller, J Chandrashekar, NJ Ryba, CS Zuker, Cell 2000 100 6 693 702 10.1016/S0092-8674(00)80705-9 10761934
7. Lineage-specific loss of function of bitter taste receptor genes in humans and nonhuman primates. Y Go, Y Satta, O Takenaka, N Takahata, Genetics 2005 170 1 313 326 10.1534/genetics.104.037523 15744053
8. The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. B Bufe, PA Breslin, C Kuhn, DR Reed, CD Tharp, JP Slack, UK Kim, D Drayna, W Meyerhof, Curr Biol 2005 15 4 322 327 10.1016/j.cub.2005.01.047 15723792
9. Genetics and bitter taste responses to goitrin, a plant toxin found in vegetables. S Wooding, H Gunn, P Ramos, S Thalmann, C Xing, W Meyerhof, Chem Senses 2010 35 8 685 692 10.1093/chemse/bjq061 20551074
10. Genetic signature of differential sensitivity to stevioside in the Italian population. D Risso, G Morini, L Pagani, A Quagliariello, C Giuliani, S De Fanti, M Sazzini, D Luiselli, S Tofanelli, Genes Nutr 2014 9 3 401 10.1007/s12263-014-0401-y 24705770
11. Natural selection and molecular evolution in PTC, a bitter-taste receptor gene. S Wooding, UK Kim, MJ Bamshad, J Larsen, LB Jorde, D Drayna, Am J Hum Genet 2004 74 4 637 646 10.1086/383092 14997422
12. Evolution of functionally diverse alleles associated with PTC bitter taste sensitivity in Africa. MC Campbell, A Ranciaro, A Froment, J Hirbo, S Omar, JM Bodo, T Nyambo, G Lema, D Zinshteyn, D Drayna, PA Breslin, SA Tishkoff, Mol Biol Evol 2012 29 4 1141 1153 10.1093/molbev/msr293 22130969
13. Origin and differential selection of allelic variation at TAS2R16 associated with salicin bitter taste sensitivity in Africa. MC Campbell, A Ranciaro, D Zinshteyn, R Rawlings-Goss, J Hirbo, S Thompson, D Woldemeskel, A Froment, JB Rucker, SA Omar, JM Bodo, T Nyambo, G Belay, D Drayna, PA Breslin, SA Tishkoff, Mol Biol Evol 2014 31 2 288 302 10.1093/molbev/mst211 24177185
14. Pseudogenes: are they "junk" or functional DNA? ES Balakirev, FJ Ayala, Annu Rev Genet 2003 37 123 151 10.1146/annurev.genet.37.040103.103949 14616058
15. Large-scale analysis of pseudogenes in the human genome. Z Zhang, M Gerstein, Curr Opin Genet Dev 2004 14 4 328 335 10.1016/j.gde.2004.06.003 15261647
16. Death and resurrection of the human IRGM gene. C Bekpen, T Marques-Bonet, C Alkan, F Antonacci, MB Leogrande, M Ventura, JM Kidd, P Siswara, JC Howard, EE Eichler, PLoS Genet 2009 5 3 1000403 10.1371/journal.pgen.1000403 19266026
17. Not so pseudo: the evolutionary history of protein phosphatase 1 regulatory subunit 2 and related pseudogenes. L Korrodi-Gregório, J Abrantes, T Muller, J Melo-Ferreira, K Marcus, QA da Cruz e Silva, M Fardilha, PJ Esteves, BMC Evol Biol 2013 13 242 10.1186/1471-2148-13-242 24195737
18. Using pseudogene database to identify lineage-specific genes and pseudogenes in humans and chimpanzees. Q Zhang, J Hered 2014 105 3 436 443 10.1093/jhered/est097 24399747
19. When less is more: gene loss as an engine of evolutionary change. MV Olson, Am J Hum Genet 1999 64 1 18 23 10.1086/302219 9915938
20. Gene losses during human origins. X Wang, WE Grus, J Zhang, PLoS Biol 2006 4 3 52 10.1371/journal.pbio.0040052 16464126
21. Adaptive diversification of bitter taste receptor genes in Mammalian evolution. P Shi, J Zhang, H Yang, YP Zhang, Mol Biol Evol 2003 20 5 805 814 10.1093/molbev/msg083 12679530
22. Dynamic evolution of bitter taste receptor genes in vertebrates. D Dong, G Jones, S Zhang, BMC Evol Biol 2009 9 12 10.1186/1471-2148-9-12 19144204
23. Evolutionary relationships of the Tas2r receptor gene families in mouse and human. C Conte, M Ebeling, A Marcuz, P Nef, PJ Andres-Barquin, Physiol Genomics 2003 14 1 73 82 12734386
24. Proceedings of the SMBE Tri-National Young Investigators' Workshop. Lineage-specific expansions and contractions of the bitter taste receptor gene repertoire in vertebrates. Y Go, Mol Biol Evol 2005 23 5 964 972 10.1093/molbev/msj106
25. Relaxation of selective constraint and loss of function in the evolution of human bitter taste receptor genes. X Wang, SD Thomas, J Zhang, Hum Mol Genet 2004 13 21 2671 2678 10.1093/hmg/ddh289 15367488
26. Evolution of bitter taste receptors in humans and apes. A Fischer, Y Gilad, O Man, S Pääbo, Mol Biol Evol 2005 22 3 432 436 10.1093/molbev/msi027 15496549
27. An integrated map of genetic variation from 1,092 human genomes. GR Abecasis, A Auton, LD Brooks, MA DePristo, RM Durbin, RE Handsaker, HM Kang, GT Marth, GA McVean, Nature 2012 491 7422 56 65 10.1038/nature11632 23128226
28. http://browser.1000genomes.org/index.html 1000 Genomes Browser. []
29. The UCSC Table Browser data retrieval tool. D Karolchik, AS Hinrichs, TS Furey, KM Roskin, CW Sugnet, D Haussler, WJ Kent, Nucleic Acids Res 2004 32 493 D496 10.1093/nar/gkh103 14681465
30. http://genome.ucsc.edu/cgi-bin/hgTables UCSC Table Browser. []
31. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, García-Girón C, Gordon L, Hourlier T, Hunt S, Juettemann T, Kähäri AK, Keenan S, Komorowska M, Kulesha E, Longden I, Maurel T, McLaren WM, Muffato M, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, et al. Ensembl 2013. Nucleic Acids Res 41 (D1):D48-D55.
32. http://www.ensembl.org/index.html Ensembl Genome Browser. []
33. Haploview: analysis and visualization of LD and haplotype maps. JC Barrett, B Fry, J Maller, MJ Daly, Bioinformatics 2005 21 2 263 265 10.1093/bioinformatics/bth457 15297300
34. Median-joining networks for inferring intraspecific phylogenies. HJ Bandelt, P Forster, A Röhl, Mol Biol Evol 1999 16 1 37 48 10.1093/oxfordjournals.molbev.a026036 10331250
35. PLINK: a tool set for whole-genome association and population-based linkage analyses. S Purcell, B Neale, K Todd-Brown, L Thomas, MA Ferreira, D Bender, J Maller, P Sklar, PI de Bakker, MJ Daly, PC Sham, Am J Hum Genet 2007 81 3 559 575 10.1086/519795 17701901
36. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. L Excoffier, HE Lischer, Mol Ecol Resour 2010 10 3 564 567 10.1111/j.1755-0998.2010.02847.x 21565059
37. MUSCLE: multiple sequence alignment with high accuracy and high throughput. RC Edgar, Nucleic Acids Res 2004 32 5 1792 1797 10.1093/nar/gkh340 15034147
38. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. K Tamura, G Stecher, D Peterson, A Filipski, S Kumar, Mol Biol Evol 2013 30 12 2725 2729 10.1093/molbev/mst197 24132122
39. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. P Librado, J Rozas, Bioinformatics 2009 25 11 1451 1452 10.1093/bioinformatics/btp187 19346325
40. A new test for detecting recent positive selection that is free from the confounding impacts of demography. H Li, Mol Biol Evol 2011 28 1 365 375 10.1093/molbev/msq211 20709734
41. Inference from gene trees in a subdivided population. M Bahlo, RC Griffiths, Theor Popul Biol 2000 57 2 79 95 10.1006/tpbi.1999.1447 10792974
42. http://www.stats.ox.ac.uk/griff/software.html GENETREE software. []
43. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. F Tajima, Genetics 1989 123 3 585 595 2513255
44. Statistical tests of neutrality of mutations. YX Fu, WH Li, Genetics 1993 133 3 693 709 8454210
45. The effect of hitch-hiking on genes linked to a balanced polymorphism in a subdivided population. MH Schierup, D Charlesworth, X Vekemans, Genet Res 2000 76 1 63 73 10.1017/S0016672300004547 11006635
46. The effects of multilocus balancing selection on neutral variability. A Navarro, NH Barton, Genetics 2002 161 2 849 863 12072479
47. Measures of human population structure show heterogeneity among genomic regions. BS Weir, LR Cardon, AD Anderson, DM Nielsen, WG Hill, Genome Res 2005 15 11 1468 1476 10.1101/gr.4398405 16251456
48. SNP@Evolution: a hierarchical database of positive selection on the human genome. F Cheng, W Chen, E Richards, L Deng, C Zeng, BMC Evol Biol 2009 9 221 10.1186/1471-2148-9-221 19732458
49. Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. KE Langergraber, K Prüfer, C Rowney, C Boesch, C Crockford, K Fawcett, E Inoue, M Inoue-Muruyama, JC Mitani, MN Muller, MM Robbins, G Schubert, TS Stoinski, B Viola, D Watts, RM Wittig, RW Wrangham, K Zuberbühler, S Pääbo, L Vigilant, Proc Natl Acad Sci U S A 2012 109 39 15716 15721 10.1073/pnas.1211740109 22891323