Abstract
Chinese and imported pig breeds differ in fat production potential, which is associated with the polymorphisms in the 5′ proximal regulating region (5′PRR) of thyroid hormone responsive gene (THRSP). In three Chinese breeds (Dingyuan, CDY; Wannanhua, CWH; and Jixi, CJX) and one introduced breed (Yorkshire, YKS), three variant sites were located at T/C-400, A/G-376, and G/A-98 in the 5′PRR. Chinese pig breeds had higher C-400 allele frequencies than YKS. The frequencies of A-376 in CDY and G-376 in CWH were about 0.8. G-98 allele frequencies in CWH and YKS were 0.8617 and 0.8149, respectively. TGG was the dominant haplotype in YKS, CGG in CWH and CJX, and CAA in CDY. According to haplotype frequency, four breeds were clustered into three types, which was consistent with the geographical distribution of the breeds. In CDY, the average backfat thickness (BFT) was the highest with the CC-400 genotype, followed by CT-400 and TT-400 genotypes. In YKS, the pigs with CC-400 or CT-400 genotypes had higher BFT and average daily weight gain, whereas those with CC-400 or TT-400 genotypes had larger lion-eye area. No significant difference was observed in carcass traits among different genotypes at the A/G-376 and G/A-98 loci. The mRNA abundance of THRSP expression for the CCAGAG genotype was significantly higher than that for CTAGAG or TTAGAG genotype. These results indicated that the polymorphisms and genotype distribution of THRSP were closely related to the potential for fat production in pig breeds, which were the result of adaptation to artificial selection and natural selection.
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References
Armengol J, Villena JA, Hondares E, Carmona MC, Sul HS, Iglesias R, Giralt M, Villarroya F (2012) Pref-1 in brown adipose tissue: specific involvement in brown adipocyte differentiation and regulatory role of C/EBPδ. Biochem J 443:799–810. https://doi.org/10.1042/BJ20111714
Carmona MC, Iglesias R, Obregón MJ, Darlington GJ, Villarroya F, Giralt M (2002) Mitochondrial biogenesis and thyroid status maturation in brown fat require CCAAT/enhancer-binding protein alpha. J Biol Chem 277:21489–21498. https://doi.org/10.1074/jbc.M201710200
Caroli AM, Chessa S, Erhardt GJ (2009) Invited review: milk protein polymorphisms in cattle: effect on animal breeding and human nutrition. J Dairy Sci 92:5335–5352. https://doi.org/10.3168/jds.2009-2461
Chen HQ, Jiang MY (1999) Relationship between native breeding pigs trait and ecological type in Anhui Province. Chinese J Appl Ecol 10:464–466. https://doi.org/10.13287/j.1001-9332.1999.0120
Chen RS, Zhang WL, Jing RB (2007) Thirty years’ review of pork quality research. Swine Industry Science 24:90–94. https://doi.org/10.3969/j.issn.1673-5358.2007.07.026
Chen H, Chen HQ, Zhou QQ, Zhang YP, Wei HQ, Li CM, Zhang XY, Peng YL (2011) Identification of transcription regulation activity in 5′ flanking region of pig THRSP gene. Acta Veterinaria et Zootechnica Sinica 42:329–334
Chen HQ, Qin J, Zhu YJ, Pan ZT, Xie YN, Jiao MH, Chen GW, Chen H, Chu MX (2012) The polymorphisms of goat THRSP gene associated with ecological factors in Chinese indigenous goat breeds with different lipogenesis ability. Asian J Anim Vet Adv 7:802–811. https://doi.org/10.3923/ajava.2012.802.811
Cunningham BA, Moncur JT, Huntington JT, Kinlaw WB (1998) “Spot 14” protein: a metabolic integrator in normal and neoplastic cells. Thyroid 8:815–825. https://doi.org/10.1089/thy.1998.8.815
Fornes O, Castro-Mondragon JA, Khan A, van der Lee R, Zhang X, Richmond PA, Modi BP, Correard S, Gheorghe M, Baranašić D, Santana-Garcia W, Tan G, Chèneby J, Ballester B, Parcy F, Sandelin A, Lenhard B, Wasserman WW, Mathelier A (2020) JASPAR 2020: update of the open-access database of transcription factor binding profiles. Nucleic Acids Res 48(D1):D87–D92. https://doi.org/10.1093/nar/gkz1001
Giordano A, Smorlesi A, Frontini A, Barbatelli G, Cinti S (2014) White, brown and pink adipocytes: the extraordinary plasticity of the adipose organ. Eur J Endocrinol 170:R159–R171. https://doi.org/10.1530/EJE-13-0945
Goszczynski DE, Mazzucco JP, Ripoli MV, Villarreal EL, Rogberg-Muñoz A, Mezzadra CA, Melucci LM, Giovambattista G (2016) Genetic characterisation of PPARG, CEBPA and RXRA, and their influence on meat quality traits in cattle. J Anim Sci Technol 58:14. https://doi.org/10.1186/s40781-016-0095-3
Hurley WL (2019) Review: mammary gland development in swine: embryo to early lactation. Animal 13(S1):s11–s19. https://doi.org/10.1017/S1751731119000521
Johansson EM, Kannius-Janson M, Bjursell G, Nilsson J (2003) The p53 tumor suppressor gene is regulated in vivo by nuclear factor 1-C2 in the mouse mammary gland during pregnancy. Oncogene 22:6061–6070. https://doi.org/10.1038/sj.onc.1206884
Johansson EM, Kannius-Janson M, Gritli-Linde A, Bjursell G, Nilsson J (2005) Nuclear factor 1-C2 is regulated by prolactin and shows a distinct expression pattern in the mouse mammary epithelial cells during development. Mol Endocrinol 19:992–1003. https://doi.org/10.1210/me.2004-0359
Khristi V, Chakravarthi VP, Singh P, Ghosh S, Pramanik A, Ratri A, Borosha S, Roby KF, Wolfe MW, Rumi MAK (2018) ESR2 regulates granulosa cell genes essential for follicle maturation and ovulation. Mol Cell Endocrinol 474:214–226. https://doi.org/10.1016/j.mce.2018.03.012
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Kirschner LS, Mariash CN (1999) Adipose S14 mRNA is abnormally regulated in obese subjects. Thyroid 9:143–148. https://doi.org/10.1089/thy.1999.9.143
Kistler WS, Baas D, Lemeille S, Paschaki M, Seguin-Estevez Q, Barras E, Ma W, Duteyrat JL, Morlé L, Durand B, Reith W (2015) RFX2 is a major transcriptional regulator of spermiogenesis. PLoS Genet 11:e1005368. https://doi.org/10.1371/journal.pgen.1005368
Kuemmerle NB, Kinlaw WB (2011) THRSP (thyroid hormone responsive). Atlas Genet Cytogenet Oncol Haematol 15:480–482
Li QG, Wang CL, Xu JY (2015) Slaughter determination and meat quality analysis between the native breed of Weizhu and introduced breed Large white pig. Swine Production 1:57–58. https://doi.org/10.13257/j.cnki.21-1104/s.2015.01.023
Ma Y, Zhang S, Zhang K, Fang C, Xie S, Du X, Li X, Ni D, Zhao S (2018) Genomic analysis to identify signatures of artificial selection and loci associated with important economic traits in Duroc pigs. G3 (Bethesda) 8:3617–3625. https://doi.org/10.1534/g3.118.200665
Ma L, Sonstegard TS, Cole JB, VanTassell CP, Wiggans GR, Crooker BA, Tan C, Prakapenka D, Liu GE, Da Y (2019) Genome changes due to artificial selection in U.S. Holstein cattle. BMC Genomics 20:128. https://doi.org/10.1186/s12864-019-5459-x
Ramayo-Caldas Y, Fortes MR, Hudson NJ, Porto-Neto LR, Bolormaa S, Barendse W, Kelly M, Moore SS, Goddard ME, Lehnert SA, Reverter A (2014) A marker-derived gene network reveals the regulatory role of PPARGC1A, HNF4G, and FOXP3 in intramuscular fat deposition of beef cattle. J Anim Sci 92:2832–2845. https://doi.org/10.2527/jas.2013-7484
Rempel LA, Nonneman DJ, Rohrer GA (2012) Polymorphism within thyroid hormone responsive (THRSP) associated with weaning-to-oestrus interval in swine. Anim Genet 43:364–365. https://doi.org/10.1111/j.1365-2052.2011.02303.x
Shimada M, Mochizuki K, Goda T (2011) Feeding rats dietary resistant starch reduces both the binding of ChREBP and the acetylation of histones on the Thrsp gene in the jejunum. J Agric Food Chem 59:1464–1469. https://doi.org/10.1021/jf103111u
Verardo LL, Silva FF, Lopes MS, Madsen O, Bastiaansen JW, Knol EF, Kelly M, Varona L, Lopes PS, Guimarães SE (2016) Revealing new candidate genes for reproductive traits in pigs: combining Bayesian GWAS and functional pathways. Genet Sel Evol 48:9. https://doi.org/10.1186/s12711-016-0189-x
Wang X, Carre W, Zhou H, Lamont SJ, Cogburn LA (2004) Duplicated Spot 14 genes in the chicken: characterization and identification of polymorphisms associated with abdominal fat traits. Gene 332:79–88. https://doi.org/10.1016/j.gene.2004.02.021
Wang C, Wang H, Zhang Y, Tang Z, Li K, Liu B (2015) Genome-wide analysis reveals artificial selection on coat colour and reproductive traits in Chinese domestic pigs. Mol Ecol Resour 15:414–424. https://doi.org/10.1111/1755-0998.12311
Wu YJ, Zhang P, Fu YR, Su SG, Tian GY, Zhang H, Li QG (2019) Measurement of carcass qulity traits in Dingyuan black pig. Swine Prod 5:78–80. https://doi.org/10.13257/j.cnki.21-1104/s.2019.05.027
Yuan Q (2010) Investigation and evaluation of cultivated land quality grade in China (Anhui). China Land Press, Beijing
Zhang W, Peng W, Zhao M, Lin D, Zeng Z, Zhou W, Bartlam M (2011) Expression, purification and preliminary crystallographic analysis of human thyroid hormone responsive protein. Acta Crystallogr, Sect F: Struct Biol Cryst Commun 67(Pt 8):941–946. https://doi.org/10.1107/S1744309111021099
Zhao SG (2003) China’s pig industry. China Agriculture Press, Beijing
Zhou QQ, Chen HQ, Wei HQ, Qin J, Chen H, Zhang YP (2011) Association of polymorphism in the coding region of THRSP gene with lipogenesis capability in pigs. Prog Biochem Biophys 38:84–90. https://doi.org/10.3724/SP.J.1206.2010.00419
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The work was supported by the National Natural Science Foundation of China (NSFC) [Grant No. 31172180] and Project of Anhui Province Scientific Technology Plan (No. 17030701007).
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HC: conceptualization, funding acquisition, methodology, project administration, supervision, writing—review & editing. XW: investigation, methodology, project administration, roles/writing—original draft, writing—review & editing. JC, WQ: formal analysis, investigation, writing—review & editing. GC, HC: formal analysis, writing—review & editing. XS, MZ, and NB: formal analysis.
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All procedures that involved animals were approved by the animal care and use committee at the institution in which the experiment was conducted. All procedures that involved animals were also approved and authorized by the Chinese Ministry of Agriculture.
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Xiaohong Wang and Jin Cheng contributed equally to this work.
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Wang, X., Cheng, J., Qin, W. et al. Polymorphisms in 5′ proximal regulating region of THRSP gene are associated with fat production in pigs. 3 Biotech 10, 267 (2020). https://doi.org/10.1007/s13205-020-02266-6
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DOI: https://doi.org/10.1007/s13205-020-02266-6