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Analysis of longissimus muscle quality characteristics and associations with DNA methylation status in cattle

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Abstract

Background

As cattle represent one of the most important livestock species for meat production, control of muscle development in regards to quality is an important research focus.

Objectives

In this study, the phenotypic quality traits and its associations with DNA methylation levels of the longissimus muscle in two cattle breeds were studied.

Methods

The pH value, water loss rate, fat and protein and fatty acid content were measured in three beef cattle breeds of longissimus mucle; The longissimus mucle was analyzed by MethylRAD-seq and RNA-seq. The differentially methylated and differentially expressed related genes were subjected to BSP.

Results

Methylation status of longissimus mucle was analyzed by MethylRAD-seq. Compared with Simmental, there were 39 differentially methylated and expressed genes in muscle of Yunling cattle, and 123 differentially methylated and expressed genes in Wenshan muscle. A combined analysis of MethylRAD-seq and RNA-seq results revealed differential methylation and expression level of 18 genes between Simmental and Wenshan cattle, and 14 genes between Simmental and Yunling cattle. In addition, 28 genes were differentially methylated between Wenshan and Yunling cattle. Results of promoter methylation analysis of ACAD11, FADS6 and FASN showed that the overall degree of DNA methylation of FADS6 and FASN was negatively correlated with their expression levels. Methylation level of FASN in Simmental was greater than Yunling and Wenshan. The degree of methylation at the FADS6 CpG4 site was significantly higher in Simmental than that in Yunling. The levels of methylation at the CpG7 locus of the Simmental and Yunling breeds were greater than Wenshan cattle. A negative correlation was detected between the methylation levels and the expression of FASN CpG1, CpG2, CpG3, CpG5, CpG7, and CpG10.

Conclusion

The functional and molecular regulatory mechanism of the genes related to meat quality can be revealed systematically from aspects of the genetic and epigenetic regulation. These studies will help to further explore the molecular mechanisms and phenotypic differences that regulate growth and quality of different breeds of cattle.

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References

  • Abdelrahman MM, Naguib IA, Elsayed MA, Zaazaa HA (2017) Chromatographic methods for quantitative determination of ampicillin, dicloxacillin and their impurity 6-aminopenicillanic acid. J Chromatogr Sci 56:209–215

    Article  Google Scholar 

  • Ahnstrom ML, Hunt MC, Lundstrom K (2012) Effects of pelvic suspension of beef carcasses on quality and physical traits of five muscles from four gender-age groups. Meat Sci 90:528–535

    Article  PubMed  Google Scholar 

  • Alberti P, Campo MM, Beriain MJ, Ripoll G, Sanudo C (2017) Effect of including whole linseed and vitamin E in the diet of young bulls slaughtered at two fat covers on the sensory quality of beef packaged in two different packaging systems. J Sci Food Agric 97:753–760

    Article  CAS  PubMed  Google Scholar 

  • An YC, Goettel W, Han Q, Bartels A, Liu Z, Xiao W (2017) Dynamic changes of genome-wide DNA methylation during soybean seed development. Sci Rep 7:12263

    Article  PubMed  PubMed Central  Google Scholar 

  • Arelovich HM, Lagrange S, Torre R, Martinez MF, Laborde HE (2017) Feeding value of whole raw soya beans as a protein supplement for beef cattle consuming low-quality forages. J Anim Physiol Anim Nutr 102:421–430

    Article  Google Scholar 

  • Barahona M, Olleta JL, Sanudo C, Alberti P, Panea B, Perez-Juan M, Realini CE, Campo MM (2016) Effects of whole linseed and rumen-protected conjugated linoleic acid enriched diets on beef quality. Anim Int J Anim Biosci 10:709–717

    Article  CAS  Google Scholar 

  • Baublits RT, Pohlman FW, Brown AH Jr, Yancey EJ, Johnson ZB (2006) Impact of muscle type and sodium chloride concentration on the quality, sensory, and instrumental color characteristics of solution enhanced whole-muscle beef. Meat Sci 72:704–712

    Article  CAS  PubMed  Google Scholar 

  • Bensink JC, Dobrenov B, Mulenga MP, Bensink ZS, McKee JJ (2002) The microbiological quality of beef tripe using different processing techniques. Meat Sci 62:85–92

    Article  PubMed  Google Scholar 

  • Chen Z, Luo J, Ma L, Wang H, Cao W, Xu H, Zhu J, Sun Y, Li J, Yao D et al (2015) MiR130b-regulation of PPARgamma coactivator-1alpha suppresses fat metabolism in goat mammary epithelial cells. PLoS One 10:e0142809

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Luo J, Sun S, Cao D, Shi H, Loor JJ (2017) miR-148a and miR-17-5p synergistically regulate milk TAG synthesis via PPARGC1A and PPARA in goat mammary epithelial cells. RNA Biol 14:326–338

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Luo J, Zhang C, Ma Y, Sun S, Zhang T, Loor JJ (2018) Mechanism of prolactin inhibition of miR-135b via methylation in goat mammary epithelial cells. J Cell Physiol 233:651–662

    Article  CAS  PubMed  Google Scholar 

  • Childs KD, Goad DW, Allan MF, Pomp D, Krehbiel C, Geisert RD, Morgan JB, Malayer JR (2002) Differential expression of NAT1 translational repressor during development of bovine intramuscular adipocytes. Physiol Genomics 10:49–56

    Article  CAS  PubMed  Google Scholar 

  • Graugnard DE, Piantoni P, Bionaz M, Berger LL, Faulkner DB, Loor JJ (2009) Adipogenic and energy metabolism gene networks in longissimus lumborum during rapid post-weaning growth in Angus and Angus × Simmental cattle fed high-starch or low-starch diets. BMC genomics 10:142

    Article  PubMed  PubMed Central  Google Scholar 

  • Hachiya T, Furukawa R, Shiwa Y, Ohmomo H, Ono K, Katsuoka F, Nagasaki M, Yasuda J, Fuse N, Kinoshita K et al (2017) Genome-wide identification of inter-individually variable DNA methylation sites improves the efficacy of epigenetic association studies. NPJ Genom Med 2:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagstrom AK, Albre J, Tooman LK, Thirmawithana AH, Corcoran J, Lofstedt C, Newcomb RD (2014) A novel fatty acyl desaturase from the pheromone glands of Ctenopseustis obliquana and C. herana with specific Z5-desaturase activity on myristic acid. J Chem Ecol 40:63–70

    Article  PubMed  PubMed Central  Google Scholar 

  • He M, Pei Z, Mohsen AW, Watkins P, Murdoch G, Van Veldhoven PP, Ensenauer R, Vockley J (2011) Identification and characterization of new long chain acyl-CoA dehydrogenases. Mol Genet Metab 102:418–429

    Article  CAS  PubMed  Google Scholar 

  • Hristov AN, Lee C, Cassidy T, Long M, Heyler K, Corl B, Forster R (2011) Effects of lauric and myristic acids on ruminal fermentation, production, and milk fatty acid composition in lactating dairy cows. J Dairy Sci 94:382–395

    Article  CAS  PubMed  Google Scholar 

  • Huang YZ, Zhang LZ, Lai XS, Li MX, Sun YJ, Li CJ, Lan XY, Lei CZ, Zhang CL, Zhao X et al (2014) Transcription factor ZBED6 mediates IGF2 gene expression by regulating promoter activity and DNA methylation in myoblasts. Sci Rep 4:4570

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang D, LaGory EL, Kenzelmann Broz D, Bieging KT, Brady CA, Link N, Abrams JM, Giaccia AJ, Attardi LD (2015) Analysis of p53 transactivation domain mutants reveals Acad11 as a metabolic target important for p53 pro-survival function. Cell Rep 10:1096–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung M, Kristiansen G, Dietrich D (2018) DNA methylation analysis of free-circulating DNA in body fluids. Methods Mol Biol 1708:621–641

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Ding X, Wang X, He T, Zhang H, Yang L, Wang T, Chen L, Gai J, Yang S (2017) Genome-wide comparative analysis of DNA methylation between soybean cytoplasmic male-sterile line NJCMS5A and its maintainer NJCMS5B. Bmc Genomics 18:596

    Article  PubMed  PubMed Central  Google Scholar 

  • Li M, Lu X, Xia H, Zhang C, Wang X, Chen Z, Zhang H, Qu K, Huang B, Moore S et al (2019) In-depth characterization of the pituitary transcriptome in Simmental and Chinese native cattle. Domest Anim Endocrinol 66:35–42

    Article  CAS  PubMed  Google Scholar 

  • Meeusen JW, Donato LJ, Jaffe AS (2016) Should apolipoprotein B replace LDL cholesterol as therapeutic targets are lowered? Curr Opin Lipidol 27:359–366

    Article  CAS  PubMed  Google Scholar 

  • Moisa SJ, Shike DW, Faulkner DB, Meteer WT, Keisler D, Loor JJ (2014) Central role of the PPARgamma gene network in coordinating beef cattle intramuscular adipogenesis in response to weaning age and nutrition. Gene Regul Syst Biol 8:17–32

    Google Scholar 

  • Oh D, Lee Y, La B, Yeo J, Chung E, Kim Y, Lee C (2012) Fatty acid composition of beef is associated with exonic nucleotide variants of the gene encoding FASN. Mol Biol Rep 39:4083–4090

    Article  CAS  PubMed  Google Scholar 

  • Pyles LA, Lilly CL, Mullett CJ, Polak ES, Elliott EM, Neal WA (2017) LDL cholesterol level in fifth-grade schoolchildren associates with stature. J Lipid Res 58:2197–2201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reith C, Staplin N, Herrington WG, Stevens W, Emberson J, Haynes R, Mafham M, Armitage J, Cass A, Craig JC et al (2017) Effect on non-vascular outcomes of lowering LDL cholesterol in patients with chronic kidney disease: results from the Study of Heart and Renal Protection. BMC Nephrol 18:147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy R, Gautier M, Hayes H, Laurent P, Osta R, Zaragoza P, Eggen A, Rodellar C (2001) Assignment of the fatty acid synthase (FASN) gene to bovine chromosome 19 (19q22) by in situ hybridization and confirmation by somatic cell hybrid mapping. Cytogenet Cell Genet 93:141–142

    Article  CAS  PubMed  Google Scholar 

  • Roy R, Taourit S, Zaragoza P, Eggen A, Rodellar C (2005) Genomic structure and alternative transcript of bovine fatty acid synthase gene (FASN): comparative analysis of the FASN gene between monogastric and ruminant species. Cytogenet Genome Res 111:65–73

    Article  CAS  PubMed  Google Scholar 

  • Savadkoohi S, Hoogenkamp H, Shamsi K, Farahnaky A (2014) Color, sensory and textural attributes of beef frankfurter, beef ham and meat-free sausage containing tomato pomace. Meat Sci 97:410–418

    Article  PubMed  Google Scholar 

  • Schmidt JW, Bosilevac JM, Kalchayanand N, Wang R, Wheeler TL, Koohmaraie M (2014) Immersion in antimicrobial solutions reduces Salmonella enterica and Shiga toxin-producing Escherichia coli on beef cheek meat. J Food Prot 77:538–548

    Article  CAS  PubMed  Google Scholar 

  • Scollan N, Hocquette JF, Nuernberg K, Dannenberger D, Richardson I, Moloney A (2006) Innovations in beef production systems that enhance the nutritional and health value of beef lipids and their relationship with meat quality. Meat Sci 74:17–33

    Article  CAS  PubMed  Google Scholar 

  • Spanier AM, Flores M, Toldra F, Aristoy MC, Bett KL, Bystricky P, Bland JM (2004) Meat flavor: contribution of proteins and peptides to the flavor of beef. Adv Exp Med Biol 542:33–49

    Article  CAS  PubMed  Google Scholar 

  • Stern JL, Paucek RD, Huang FW, Ghandi M, Nwumeh R, Costello JC, Cech TR (2017) Allele-specific DNA methylation and its interplay with repressive histone marks at promoter-mutant TERT genes. Cell Rep 21:3700–3707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stirzaker C, Song JZ, Davidson B, Clark SJ (2004) Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Can Res 64:3871–3877

    Article  CAS  Google Scholar 

  • Turner SP, Navajas EA, Hyslop JJ, Ross DW, Richardson RI, Prieto N, Bell M, Jack MC, Roehe R (2011) Associations between response to handling and growth and meat quality in frequently handled Bos taurus beef cattle. J Anim Sci 89:4239–4248

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Lv J, Zhang L, Dou J, Sun Y, Li X, Fu X, Dou H, Mao J, Hu X et al (2015) MethylRAD: a simple and scalable method for genome-wide DNA methylation profiling using methylation-dependent restriction enzymes. Open Biol 5:150130

    Article  PubMed  PubMed Central  Google Scholar 

  • Wen S, Zhou G, Song S, Xu X, Voglmeir J, Liu L, Zhao F, Li M, Li L, Yu X et al (2015) Discrimination of in vitro and in vivo digestion products of meat proteins from pork, beef, chicken, and fish. Proteomics 15:3688–3698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whayne TF (2017) Low-density lipoprotein cholesterol (LDL-C): how Low? Curr Vasc Pharmacol 15:374–379

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Zhang Y, Liu W, Lu X, Li C (2017) Genome-wide analysis of DNA methylation in five tissues of sika deer (Cervus nippon). Gene 645:48–54

    Article  PubMed  Google Scholar 

  • Yao Z, Liu X, Shim JM, Lee KW, Kim HJ, Kim JH (2016) Properties of a fibrinolytic enzyme secreted by Bacillus amyloliquefaciens RSB34, isolated from Doenjang. J Microbiol Biotechnol 27:9–18

    Article  Google Scholar 

  • Yi L, Gao F, Siqin B, Zhou Y, Li Q, Zhao X, Jia X, Zhang H (2017) Construction of an SNP-based high-density linkage map for flax (Linum usitatissimum L.) using specific length amplified fragment sequencing (SLAF-seq) technology. Plos One 12:e0189785

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhai D, Li S, Dong G, Zhou D, Yang Y, Wang X, Zhao Y, Yang Y, Lin Z (2018) The correlation between DNA methylation and transcriptional expression of human dopamine transporter in cell lines. Neurosci Lett 662:91–97

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Xie WJ, Liu S, Meng L, Gu C, Gao YQ (2017) DNA methylation landscape reflects the spatial organization of chromatin in different cells. Biophys J 113:1395–1404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang HM, Xia HL, Jiang HR, Mao YJ, Qu KX, Huang BZ, Gong YC, Yang ZP (2018) Longissimus dorsi muscle transcriptomic analysis of Yunling and Chinese simmental cattle differing in intramuscular fat content and fatty acid composition. Genome 61:549–558

    Article  CAS  PubMed  Google Scholar 

  • Zheng H, Gao L, Feng Y, Yuan L, Zhao H, Cornelius LA (2009) Down-regulation of Rap1GAP via promoter hypermethylation promotes melanoma cell proliferation, survival, and migration. Can Res 69:449–457

    Article  CAS  Google Scholar 

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Funding

National Natural Science Foundation of China (31872324,31472067, 31802035), This study was funded by the National High Technology Research and Development Program of China (2013AA102505–5), China Postdoctoral Science Foundation (2017M621841).

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Authors

Contributions

Zhangping Yang conceived and designed the experiments. Zhi Chen, Xin Xu, Wenqiang Wang and Hongliang Shen performed the experiments. Zhi Chen, Mingxun Li, Huimin Zhang and Yongjiang Mao analyzed the data. Zhi Chen wrote the paper.

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Correspondence to Zhangping Yang.

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Chen, Z., Chu, S., Xu, X. et al. Analysis of longissimus muscle quality characteristics and associations with DNA methylation status in cattle. Genes Genom 41, 1147–1163 (2019). https://doi.org/10.1007/s13258-019-00844-4

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  • DOI: https://doi.org/10.1007/s13258-019-00844-4

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