Characterization of the porcine nutrient and taste receptor gene repertoire in domestic and wild populations across the globe

BMC Genomics

Eugeni Roura³  Miguel Perez-Enciso²  Antonio Reverter¹  William Burgos-Paz⁵  Nadia de Jager³  Elizabete C da Silva⁴ 

[1] Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture Flagship, Queensland Bioscience Precinct, 306 Carmody Road, St. Lucia, QLD 4067, Australia;Institut Català de Recerca i Estudis Avançats (ICREA), Carrer de Lluís Companys 23, Barcelona 08010, Spain;Centre for Nutrition and Food Sciences, The University of Queensland, St. Lucia 4067, Australia;Faculty of Agronomy and Veterinary Medicine, Darcy Ribeiro UnB, Brasília-Asa Norte, Distrito Federal 70.910-970, Brazil;Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, 08193 Bellaterra, Spain

关键词: Population genomics;    SNPs;    T2R;    T1R;    Bitter;    Taste receptor;    GPCR;    Nutrition;    Pig;   

Others  :  1089912
DOI  :  10.1186/1471-2164-15-1057

 received in 2014-08-25, accepted in 2014-11-13,  发布年份 2014

【 摘 要 】

Background

The oral GPCR nutrient/taste receptor gene repertoire consists of the Tas1r family (sweet and umami tastes), the Tas2r family (bitter taste) as well as several other potential candidate sensors of amino acids, peptones and fatty acids. Taste/nutrient receptors play a fundamental role in survival through the identification of dietary nutrients or potentially toxic compounds. In humans and rodents some variations in taste sensitivity have been related to receptor polymorphisms. Some allelic variants, in turn, have been linked to the adaptation to specific geographical locations and dietary regimes. In contrast, the porcine taste/nutrient receptor repertoire has been only partially characterized and limited information on genetic variation across breeds and geographical location exists. The present study aims at filling this void which in turn will form the bases for future improvements in pig nutrition.

Results

Our results show that the pig oral repertoire of taste/nutrient receptors consists of at least 28 receptor genes with significant transcription measured for 27. When compared to humans and rodents, the porcine gene sequences encoding sensors for carbohydrates, amino acids and fatty acids were highly conserved whilst the bitter taste gene family (known as Tas2rs) showed high divergence. We identified 15 porcine Tas2rs of which 13 are orthologous to human sequences. The single nucleotide polymorphism (SNP) sequence analysis using 79 pig genomes, representing 14 different breeds/populations, revealed that the Tas2r subset had higher variability (average π =2.8 × 10^-3) than for non-bitter taste genes (π =1.2–1.5 × 10^-3). In addition, our results show that the difference in nutrient receptor genes between Asian and European breeds accounts for only a small part of the variability, which is in contrast with previous findings involving genome wide data.

Conclusions

We have defined twenty-eight oral nutrient sensing related genes for the pig. The homology with the human repertoire is high for the porcine non-bitter taste gene repertoire and low for the porcine Tas2r repertoire. Our data suggests that bitter taste is a plastic trait, possibly associated with the ability of pigs to adapt to diverse environments and that may be subject to balancing selection.

【 授权许可】

   
2014 da Silva et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Frantz LA, Schraiber JG, Madsen O, Megens HJ, Bosse M, Paudel Y, Semiadi G, Meijaard E, Li N, Crooijmans RP, Archibald AL, Slatkin M, Schook LB, Larson G, Groenen MA: Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus. Genome Biol 2013, 14(9):R107. BioMed Central Full Text
• [2]Groenen MA, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF, Rogel-Gaillard C, Park C, Milan D, Megens HJ, Li S, Larkin DM, Kim H, Frantz LA, Caccamo M, Ahn H, Aken BL, Anselmo A, Anthon C, Auvil L, Badaoui B, Beattie CW, Bendixen C, Berman D, Blecha F, Blomberg J, Bolund L, Bosse M, Botti S, Bujie Z, et al.: Analyses of pig genomes provide insight into porcine demography and evolution. Nature 2012, 491(7424):393-398.
• [3]Larson G, Dobney K, Albarella U, Fang M, Matisoo-Smith E, Robins J, Lowden S, Finlayson H, Brand T, Willerslev E, Rowley-Conwy P, Andersson L, Cooper A: Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 2005, 307(5715):1618-1621.
• [4]Larson G, Albarella U, Dobney K, Rowley-Conwy P, Schibler J, Tresset A, Vigne J-D, Edwards CJ, Schlumbaum A, Dinu A, Bălăçsescu A, Dolman G, Tagliacozzo A, Manaseryan N, Miracle P, Van Wijngaarden-Bakker L, Masseti M, Bradley DG, Cooper A: Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc Natl Acad Sci 2007, 104(39):15276-15281.
• [5]Jones GF: Genetic aspects of domestication, common breeds and their origin. In The Genetics of the Pig. Edited by Rothschild MFRA. Oxon, UK: Wallingford: CAB International; 1998:17-50.
• [6]Porter V: Pigs: A Handbook to the Breeds of the World. Mountfield: Helm Information Ltd; 1993.
• [7]Kosiol C, Vinar T, da Fonseca RR, Hubisz MJ, Bustamante CD, Nielsen R, Siepel A: Patterns of positive selection in six Mammalian genomes. PLoS Genet 2008, 4(8):e1000144.
• [8]Li D, Zhang J: Diet Shapes the Evolution of the Vertebrate Bitter Taste Receptor Gene Repertoire. Mol Biol Evol 2013, 31:303-309.
• [9]Bachmanov AA, Beauchamp GK: Taste receptor genes. Annu Rev Nutr 2007, 27:389-414.
• [10]Wellendorph P, Johansen LD, Bräuner-Osborne H: Chapter Five - The Emerging Role of Promiscuous 7TM Receptors as Chemosensors for Food Intake. In Vitamins & Hormones. 84th edition. Edited by Gerald L. Gerald Litwack, Jefferson Medical College, Thomas Jefferson University, Philadelphia, PA, USA: Academic; 2010:151-184.
• [11]Axelsson E, Ratnakumar A, Arendt ML, Maqbool K, Webster MT, Perloski M, Liberg O, Arnemo JM, Hedhammar A, Lindblad-Toh K: The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 2013, 495(7441):360-364.
• [12]Archibald AL, Bolund L, Churcher C, Fredholm M, Groenen MA, Harlizius B, Lee KT, Milan D, Rogers J, Rothschild MF, Uenishi H, Wang J, Schook LB: Pig genome sequence - analysis and publication strategy. BMC Genomics 2010, 11:438. BioMed Central Full Text
• [13]Roura E: Taste beyond taste. In Australian Pig Science Association Conference (APSA 2011): 2011. Adelaide, Australia: Australasian Pig Science Association; 2011:106-117.
• [14]De Jager N, Zhan M, Rzepus M, Roura E: Towards defining the taste receptor repertoire in the pig. In Australasian Pig Science Association Conference (APSA 2013). 47th edition. Edited by Pluske J. Melbourne: Australia: Australasian Pig Science Association; 2013:47.
• [15]Amaral AJ, Ferretti L, Megens HJ, Crooijmans RP, Nie H, Ramos-Onsins SE, Perez-Enciso M, Schook LB, Groenen MA: Genome-wide footprints of pig domestication and selection revealed through massive parallel sequencing of pooled DNA. PLoS One 2011, 6(4):e14782.
• [16]Lindblad-Toh K, Winchester E, Daly MJ, Wang DG, Hirschhorn JN, Laviolette JP, Ardlie K, Reich DE, Robinson E, Sklar P, Shah N, Thomas D, Fan JB, Gingeras T, Warrington J, Patil N, Hudson TJ, Lander ES: Large-scale discovery and genotyping of single-nucleotide polymorphisms in the mouse. Nat Genet 2000, 24(4):381-386.
• [17]Rosenberg MS, Subramanian S, Kumar S: Patterns of transitional mutation biases within and among mammalian genomes. Mol Biol Evol 2003, 20:988-993.
• [18]Ferretti L, Raineri E, Ramos-Onsins S: Neutrality tests for sequences with missing data. Genetics 2012, 191(4):1397-1401.
• [19]NCBI dbSNP Short Genetic Variations In [http://www.ncbi.nlm.nih.gov/SNP/ webcite]
• [20]Esteve-Codina A, Paudel Y, Ferretti L, Raineri E, Megens HJ, Silio L, Rodriguez MC, Groenen MA, Ramos-Onsins SE, Perez-Enciso M: Dissecting structural and nucleotide genome-wide variation in inbred Iberian pigs. BMC Genomics 2013, 14:148. BioMed Central Full Text
• [21]Toro MA, Rodrigañez J, Silio L, Rodriguez C: Genealogical analysis of a closed herd of Black Hairless Iberian pigs. Conserv Biol 2000, 14(6):1843-1851.
• [22]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
• [23]Yu G, Xiang H, Wang J, Zhao X: The phylogenetic status of typical Chinese native pigs: analyzed by Asian and European pig mitochondrial genome sequences. J Anim Sci Biotechnol 2013, 4(1):9. BioMed Central Full Text
• [24]Yang S, Zhang H, Mao H, Yan D, Lu S, Lian L, Zhao G, Yan Y, Deng W, Shi X, Han S, Li S, Wang X, Gou X: The Local Origin of the Tibetan Pig and Additional Insights into the Origin of Asian Pigs. PLoS One 2011, 6(12):e28215.
• [25]Burgos-Paz W, Souza CA, Megens HJ, Ramayo-Caldas Y, Melo M, Lemus-Flores C, Caal E, Soto HW, Martinez R, Alvarez LA, Aguirre L, Iniguez V, Revidatti MA, Martinez-Lopez OR, Llambi S, Esteve-Codina A, Rodriguez MC, Crooijmans RP, Paiva SR, Schook LB, Groenen MA, Perez-Enciso M: Porcine colonization of the Americas: a 60 k SNP story. Heredity 2013, 110(4):321-330.
• [26]Goedbloed DJ, Megens HJ, Van Hooft P, Herrero-Medrano JM, Lutz W, Alexandri P, Crooijmans RPMA, Groenen M, Van Wieren SE, Ydenberg RC, Prins HHT: Genome-wide single nucleotide polymorphism analysis reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations. Mol Ecol 2013, 22(3):856-866.
• [27]Ramírez O, Burgos-Paz W, Casas E, Ballester M, Bianco E, Olalde I, Novella V, Gut M, Lalueza-Fox C, Saña M, Pérez-Enciso M: Genome data from a 16th century pig illuminate modern breed relationships. Heredity 2014. in press
• [28]Xu H, Staszewski L, Tang H, Adler E, Zoller M, Li X: Different functional roles of T1R subunits in the heteromeric taste receptors. Proc Natl Acad Sci U S A 2004, 101(39):14258-14263.
• [29]Humphrey B, Tedó G, Klasing KC, Roura E: Characterization of porcine umami taste receptors (pT1r1 and pT1r3). 41èmes Journées de la Recherche Porcine: 2009; Paris, France 2009, 165-166.
• [30]Roura E, Humphrey B, Klasing K, Swart M: Is the pig a good umami sensing model for humans? A comparative taste receptor study. Flavour and Fragrance Journal 2011, 26(4):282-285.
• [31]Kiuchi S, Yamada T, Kiyokawa N, Saito T, Fujimoto J, Yasue H: Genomic structure of swine taste receptor family 1 member 3, TAS1R3, and its expression in tissues. Cytogenet Genome Res 2006, 115(1):51-61.
• [32]Roura E, Humphrey B, Tedo G, Ipharraguerre IR: Unfolding the codes of short-term feed appetence in farm and companion animals: a comparative oronasal nutrient sensing biology review. Can J Anim Sci 2008, 88(4):535-558.
• [33]Shi P, Zhang J, Yang H, Zhang YP: Adaptive diversification of bitter taste receptor genes in Mammalian evolution. Mol Biol Evol 2003, 20(5):805-814.
• [34]Moran AW, Al-Rammahi MA, Arora DK, Batchelor DJ, Coulter EA, Daly K, Ionescu C, Bravo D, Shirazi-Beechey SP: Expression of Na+/glucose co-transporter 1 (SGLT1) is enhanced by supplementation of the diet of weaning piglets with artificial sweeteners. Br J Nutr 2010, 104(5):637-646.
• [35]Haid DC, Jordan-Biegger C, Widmayer P, Breer H: Receptors responsive to protein breakdown products in g-cells and d-cells of mouse, swine and human. Front Physiol 2012, 3:65.
• [36]Colombo M, Trevisi P, Gandolfi G, Bosi P: Assessment of the presence of chemosensing receptors based on bitter and fat taste in the gastrointestinal tract of young pig. J Anim Sci 2012, 90(Suppl 4):128-130.
• [37]Hayakawa T, Suzuki-Hashido N, Matsui A, Go Y: Frequent Expansions of the Bitter Taste Receptor Gene Repertoire during Evolution of Mammals in the Euarchontoglires Clade. Mol Biol Evol 2014, 31(8):2018-2031.
• [38]Ballari SA, Barrios-García MN: A review of wild boar Sus scrofa diet and factors affecting food selection in native and introduced ranges. Mamm Rev 2014, 44(2):124-134.
• [39]Brown AG, Basell LS, Robinson S, Burdge GC: Site Distribution at the Edge of the Palaeolithic World: A Nutritional Niche Approach. PLoS One 2013, 8(12):e81476.
• [40]Meyerhof W, Batram C, Kuhn C, Brockhoff A, Chudoba E, Bufe B, Appendino G, Behrens M: The molecular receptive ranges of human TAS2R bitter taste receptors. Chem Senses 2010, 35(2):157-170.
• [41]Herrero-Medrano JM, Megens HJ, Groenen MA, Bosse M, Perez-Enciso M, Crooijmans RP: Whole-genome sequence analysis reveals differences in population management and selection of European low-input pig breeds. BMC Genomics 2014, 15(1):601. BioMed Central Full Text
• [42]Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJP: T2Rs Function as Bitter Taste Receptors. Cell 2000, 100(6):703-711.
• [43]Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E: Human receptors for sweet and umami taste. Proc Natl Acad Sci U S A 2002, 99(7):4692-4696.
• [44]Bosse M, Megens HJ, Frantz LA, Madsen O, Larson G, Paudel Y, Duijvesteijn N, Harlizius B, Hagemeijer Y, Crooijmans RP, Groenen MA: Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression. Nat Commun 2014, 5:4392.
• [45]Ramayo-Caldas Y, Castello A, Pena RN, Alves E, Mercade A, Souza CA, Fernandez AI, Perez-Enciso M, Folch JM: Copy number variation in the porcine genome inferred from a 60 k SNP BeadChip. BMC Genomics 2010, 11:593. BioMed Central Full Text
• [46]Paudel Y, Madsen O, Megens HJ, Frantz LA, Bosse M, Bastiaansen JW, Crooijmans RP, Groenen MA: Evolutionary dynamics of copy number variation in pig genomes in the context of adaptation and domestication. BMC Genomics 2013, 14:449. BioMed Central Full Text
• [47]Hudson RR, Kreitman M, Aguade M: A test of neutral molecular evolution based on nucleotide data. Genetics 1987, 116(1):153-159.
• [48]McDonald J, Kreitman M: Adaptive protein evolution at the Adh locus in Drosophila. Nature 1991, 351:652-654.
• [49]Bosse M, Megens HJ, Madsen O, Paudel Y, Frantz LA, Schook LB, Crooijmans RP, Groenen MA: Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genet 2012, 8(11):e1003100.
• [50]ExPASy [http://www.expasy.org/ webcite]
• [51]Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT: The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009, 55(4):611-622.
• [52]Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45.
• [53]Rubin CJ, Megens HJ, Martinez Barrio A, Maqbool K, Sayyab S, Schwochow D, Wang C, Carlborg O, Jern P, Jorgensen CB, Archibald AL, Fredholm M, Groenen MA, Andersson L: Strong signatures of selection in the domestic pig genome. Proc Natl Acad Sci U S A 2012, 109(48):19529-19536.
• [54]Fang X, Mou Y, Huang Z, Li Y, Han L, Zhang Y, Feng Y, Chen Y, Jiang X, Zhao W, Sun X, Xiong Z, Yang L, Liu H, Fan D, Mao L, Ren L, Liu C, Wang J, Li K, Wang G, Yang S, Lai L, Zhang G, Li Y, Wang J, Bolund L, Yang H, Wang J, Feng S, et al.: The sequence and analysis of a Chinese pig genome. GigaScience 2012, 1(1):16. BioMed Central Full Text
• [55]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25(16):2078-2079.
• [56]Flicek PAM, Barrell D, Beal K, Brent S, CarvalhoSilva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, Gordon L, Hendrix M, Hourlier T, Johnson N, Kähäri AK, Keefe D, Keenan S, Kinsella R, Komorowska M, Koscielny G, Kulesha E, Larsson P, Longden I, McLaren W, Muffato M, Overduin B, Pignatelli M, Pritchard B, Riat HS, Ritchie GR, et al.: Ensembl 2012. Nucleic Acids Res 2012, 40(Database issue):D84-D90.
• [57]Ng PC, Henikoff S: SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 2003, 31(13):3812-3814.
• [58]Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, Genomes Project Analysis G: The variant call format and VCFtools. Bioinformatics 2011, 27(15):2156-2158.
• [59]Zhang Z, Li J, Yu J: Computing Ka and Ks with a consideration of unequal transitional substitutions. BMC Evol Biol 2006, 6:44. BioMed Central Full Text
• [60]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25(11):1451-1452.
• [61]R Development Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3900051070, URL. 2008. http://www.Rproject.org webcite
• [62]Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC: PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007, 81(3):559-575.
• [63]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 2005, 14(8):2611-2620.
• [64]Earl DA, von Holdt BM: STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 2011. 101007/s12686-011-9548-7
• [65]Australian Animal Welfare Standards and Guidelines [http://www.daff.gov.au/animal-plant-health/welfare/standards-guidelines webcite]