Abstract
The meat quality of ducks is closely related to the intramuscular fat (IMF) content. This study explored the candidate regulatory genes of IMF formation and lipid deposition in Chaohu ducks. The IMF of breast muscle in 100 ducks was determined and statistically analysed by normal distribution test. Duck liver samples with high IMF (CH, n = 3) and low IMF (CL, n = 3) were selected for transcriptome analysis by RNA sequencing (RNA-Seq). The IMF was in accordance with normal distribution (T = 0.001, P = 0.999). The IMF from two tails of the normal distribution was significantly different with 2.9983% ± 0.3296% in the CH group and 1.1960% ± 0.1481% in the CL group (P < 0.0001). RNA-Seq revealed 147 differentially expressed genes, including 78 up-regulated and 69 down-regulated genes in both groups. Validation by qRT-PCR was in agreement with RNA-Seq (R2 = 0.838). Gene ontology analysis revealed that organophosphate catabolism, oxidation–reduction process, cellular lipid catabolism, lipid transport, lipid localisation, lipid biosynthesis and cellular lipid catabolism were involved in lipid metabolism. Meanwhile, Kyoto Encyclopedia of Genes and Genomes pathway analysis suggested that steroid hormone biosynthesis, ovarian steroidogenesis, alpha-linolenic acid metabolism, glycosylphosphatidylinositol anchor biosynthesis and linoleic acid metabolism were involved in lipid deposition, wherein the genes COMT, NT5E, PDE4D, PLA2G4F, A-FABP, ADRA2A, HSD17B2, PPP1R3C, PPP1R3B and NR0B2 were involved in lipid deposition. This study provided insights into the molecular mechanism for regulating lipid metabolism and identified candidate genes for selecting markers to control IMF formation in Chaohu ducks.
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References
Ashburner M, Ball CA, Blake JA, Botstein D, Butler HL, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, The Gene Ontology Consortium (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29
Bader S, Kortholt A, Snippe H, Van Haastert PJM (2006) DdPDE4, a novel cAMP-specific phosphodiesterase at the surface of dictyostelium cells. J Biol Chem 281:20018–20026
Båvner A, Sanyal S, Gustafsson JÅ, Treuter E (2005) Transcriptional corepression by SHP: molecular mechanisms and physiological consequences. Trends Endocrinol Metab 16:478–488
Bonifacio MJ, Palma PN, Almeida L, Soaresdasilva P (2007) Catechol-O-methyltransferase and its inhibitors in Parkinson’s disease. CNS Drug Rev 13:352–379
Bouskila M, Hunter RW, Ibrahim AFM, Delattre L, Peggie M, van Diepen JA, Voshol PJ, Jensen J, Sakamoto K (2010) Allosteric regulation of glycogen synthase controls glycogen synthesis in muscle. Cell Metab 12:456–466
Carmean CM, Huang YH, Brady MJ (2016) Glycogen repletion in brown adipose tissue upon refeeding is primarily driven by phosphorylation-independent mechanisms. PLoS One 11:e0156148
Chabault M, Baeza E, Gigaud V, Chartrin P, Chapuis H, Boulay M, Arnould C, Abbadie FD, Berri C, Bihanduval EL (2012) Analysis of a slow-growing line reveals wide genetic variability of carcass and meat quality-related traits. BMC Genet 13:90
Chartrin P, Méteau K, Juin H, Bernadet MD, Guy G, Larzul C, Rémignon H, Mourot J, Duclos MJ, Baéza E (2006) Effects of intramuscular fat levels on sensory characteristics of duck breast meat. Poult Sci 85:914–922
Chen X, Jiang R, Geng Z (2011) Cold stress in broiler: global gene expression analyses suggest a major role of CYP genes in cold responses. Mol Biol Rep 39:425–429
Chen X, Niu J, Geng Z (2017) Gene expression and plasma lipid content in relation to intramuscular fat in Chinese indigenous Wuhua chicken. J Appl Poult Res 26:391–400
Cui H, Liu R, Zhao G, Zheng M, Chen J, Wen J (2012) Identification of differentially expressed genes and pathways for intramuscular fat deposition in pectoralis major tissues of fast-and slow-growing chickens. BMC Genom 13:213
Cui H, Zheng M, Zhao G, Liu R, Wen J (2018) Identification of differentially expressed genes and pathways for intramuscular fat metabolism between breast and thigh tissues of chickens. BMC Genom 19:55
Ding F, Li Q, Li L, Gan C, Yuan X, Gou H, He H, Han C, Wang J (2015) Isolation, culture and differentiation of duck (Anas platyrhynchos) preadipocytes. Cytotechnology 67:773–781
Duchez A, Boudreau LH, Naika GS, Bollinger JG, Belleannee C, Cloutier N, Laffont B, Mendozavillarroel RE, Levesque T, Rolletlabelle E (2015) Platelet microparticles are internalized in neutrophils via the concerted activity of 12-lipoxygenase and secreted phospholipase A2-IIA. Proc Natl Acad Sci USA 27:E3564–E3573
Garg A, Sankella S, Xing C, Agarwal AK (2016) Whole-exome sequencing identifies ADRA2A mutation in atypical familial partial lipodystrophy. JCI Insight 1:e86870
Hocquette J, Gondret F, Baeza E, Medale F, Jurie C, Pethick DW (2010) Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, and identification of putative markers. Animal 4:303–319
Horton JD, Goldstein JL, Brown MS (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Investig 109:1125–1131
Huang YN, Wang J, Chen BJ, Jiang QY, Guo YF, Lan GQ, Jiang HS (2016) Gene expression and enzyme activity of lipoprotein lipase correlate with intramuscular fat content in Guangxi san-huang and Arbor Acres chickens. Genet Mol Res 2:1–13
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T (2007) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484
Kim D, Salzberg SL (2011) TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol 12:1–15
Leveille GA, Ohea EK, Chakrabarty K (1968) In vivo lipogenesis in the domestic chicken. Exp Biol Med 128:398–401
Li DL, Chen J, Wen J, Zhao G, Zheng M, Liu C (2013) Growth, carcase and meat traits and gene expression in chickens divergently selected for intramuscular fat content. Br Poult Sci 54:183–189
Li B, Weng Q, Dong C, Zhang Z, Li R, Liu J, Jiang A, Li Q, Jia C, Wu W (2018) A key gene, PLIN1, can affect porcine intramuscular fat content based on transcriptome analysis. Genes 9:194
Link R, Daunt D, Barsh G, Chruscinski A, Kobilka B (1992) Cloning of two mouse genes encoding alpha 2-adrenergic receptor subtypes and identification of a single amino acid in the mouse alpha 2-C10 homolog responsible for an interspecies variation in antagonist binding. Mol Pharmacol 42:16–27
Ma J, Chai J, Shang Y, Li Y, Chen R, Jia J, Jiang S, Peng J (2015) Swine PPAR-γ2 expression upregulated in skeletal muscle of transgenic mice via the swine Myozenin-1 gene promoter. Transgenic Res 24:409–420
Martínez-Álvaro M, Paucar Y, Satué K, Blasco A, Hernández P (2017) Liver metabolism traits in two rabbit lines divergently selected for intramuscular fat. Animal 12:1217–1223
Matitaputty PR, Wijaya CH, Bansi H, Laudadio V, Tufarelli V (2015) Influence of duck species and cross-breeding on sensory and quality characteristics of Alabio and Cihateup duck meat. CyTA J Food 4:522–526
Mortimer SI, Der Werf JHJV, Jacob RH, Hopkins DL, Pannier L, Pearce KL, Gardner GE, Warner RD, Geesink GH, Edwards JEH (2014) Genetic parameters for meat quality traits of Australian lamb meat. Meat Sci 96:1016–1024
Munro S, Ceulemans H, Bollen M, Diplexcito J, Cohen PTW (2005) A novel glycogen-targeting subunit of protein phosphatase 1 that is regulated by insulin and shows differential tissue distribution in humans and rodents. FEBS J 272:1478–1489
Murakami M, Taketomi Y, Miki Y, Sato H, Yamamoto K, Lambeau G (2014) Emerging roles of secreted phospholipase A2 enzymes: the 3rd edition. Biochimie 107:105–113
Ockner RK, Manning JA, Poppenhausen RB, Ho WKL (1972) A binding protein for fatty acids in cytosol of intestinal mucosa, liver, myocardium, and other tissues. Science 177:56–58
Otto TC, Lane MD (2008) Adipose development: from stem cell to adipocyte. Crit Rev Biochem Mol Biol 40:229–242
Plante J, Simard M, Rantakari P, Cote M, Provost PR, Poutanen M, Tremblay Y (2009) Epithelial cells are the major site of hydroxysteroid (17β) dehydrogenase 2 and androgen receptor expression in fetal mouse lungs during the period overlapping the surge of surfactant. J Steroid Biochem Mol Biol 117:139–145
Resnyk CW, Carré W, Wang X, Porter TE, Simon J, Le Bihan-Duval E, Duclos MJ, Aggrey SE, Cogburn LA (2017) Transcriptional analysis of abdominal fat in chickens divergently selected on bodyweight at two ages reveals novel mechanisms controlling adiposity: validating visceral adipose tissue as a dynamic endocrine and metabolic organ. BMC Genom 18:626
Resta R, Yamashita Y, Thompson LF (1998) Ecto-enzyme and signaling functions of lymphocyte CD73. Immunol Rev 161:95–109
Royan M, Navidshad B (2016) Peroxisome proliferator-activated receptor gamma (PPARγ), a key regulatory gene of lipid metabolism in chicken. Worlds Poult Sci J 72:773–784
Schaloske RH, Dennis EA (2006) The phospholipase A2 superfamily and its group numbering system. BBA Mol Cell Biol Lipids 1761:1246–1259
Shokryzadan P, Rajion MA, Meng GY, Boo LJ, Ebrahimi M, Royan M, Sahebi M, Azizi P, Abiri R, Jahromi MF (2017) Conjugated linoleic acid: a potent fatty acid linked to animal and human health. Crit Rev Food Sci Nutr 57:2737–2748
Steibel JP, Poletto R, Coussens PM, Rosa GJM (2009) A powerful and flexible linear mixed model framework for the analysis of relative quantification RT-PCR data. Genomics 94:146–152
Suzuki K, Irie M, Kadowaki H, Shibata T, Kumagai M, Nishida A (2005) Genetic parameter estimates of meat quality traits in Duroc pigs selected for average daily gain, longissimus muscle area, back fat thickness, and intramuscular fat content. J Anim Sci 83:2058–2065
Uemoto Y, Ohtake T, Sasago N, Takeda M, Abe T, Sakuma H, Kojima T, Sasaki S (2017) Effect of two non-synonymous ecto-5′-nucleotidase variants on the genetic architecture of inosine 5′-monophosphate (IMP) and its degradation products in Japanese Black beef. BMC Genom 18:874
Van Laack RLJM, Stevens SG, Stalder KJ (2001) The influence of ultimate pH and intramuscular fat content on pork tenderness and tenderization. J Anim Sci 79:392–397
Wang Y, Chen H, Han D, Chen Y, Muhatai G, Kurban T, Xing J, He J (2017) Correlation of the A-FABP gene polymorphism and mRNA expression with intramuscular fat content in three-yellow chicken and Hetian-Black chicken. Anim Biotechnol 28:37–43
Warner RD, Greenwood PL, Pethick DW, Ferguson DM (2010) Genetic and environmental effects on meat quality. Meat Sci 86:171–183
Xu T, Gu L, Schachtschneider KM, Liu X, Huang W, Xie M, Hou S (2014) Identification of differentially expressed genes in breast muscle and skin fat of postnatal Pekin duck. PLoS One 9:e107574
Yan Q, Jichao H, Yulian C, Haochun C, Liang Z, Ming H, Guanghong Z (2017) Meat quality, fatty acid composition and sensory evaluation of Cherry Valley, spent layer and crossbred ducks. Anim Sci J 88:156–165
Zhang R, Lin Y, Zhi L, Liao H, Zuo L, Li Z, Xu Y (2017) Expression profiles and associations of adiponectin and adiponectin receptors with intramuscular fat in Tibetan chicken. Br Poult Sci 58:151–157
Zhao X, Ren W, Siegel PB, Li J, Wang Y, Yin H, Zhang Y, Lai S, Shu G, Zhu Q (2017) Meat quality characteristics of chickens as influenced by housing system, sex, and genetic line interactions. Ital J Anim Sci 17:462–468
Zhao C, Yao X, Chen X, Wu W, Xi F, Yang G, Yu T (2018) Knockdown of ubiquitin D inhibits adipogenesis during the differentiation of porcine intramuscular and subcutaneous preadipocytes. Cell Prolif 51:e12401
Zois CE, Harris AL (2016) Glycogen metabolism has a key role in the cancer microenvironment and provides new targets for cancer therapy. J Mol Med 94:137–154
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Financial support for this research was granted by the National Science and Technology Support Plan Program of China (2015BAD03B06).
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KG drafted the manuscript and prepared the figures and tables; ZG, XC and KG conceived and designed the experiments and revised them critically for important content; KG, JK and LY performed the experiments; KG and XC analysed the data; JK and LY contributed reagents and materials. All authors approved the final draft of the manuscript submitted for review and publication.
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All experimental procedures and sample collection were performed according to the Regulations for the Administration of Affairs Concerning Experimental Animals (Ministry of Science and Technology, China; revised in June 2004) and approved by the Institutional Animal Care and Use Committee of Anhui Agricultural University, Hefei, China, under permit no. ZXD-P20140809. This experiment was performed in accordance with approved relevant guidelines and regulations.
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Ge, K., Chen, X., Kuang, J. et al. Comparison of liver transcriptome from high- and low-intramuscular fat Chaohu ducks provided additional candidate genes for lipid selection. 3 Biotech 9, 251 (2019). https://doi.org/10.1007/s13205-019-1780-y
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DOI: https://doi.org/10.1007/s13205-019-1780-y