Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Identification of relevant differential genes to the divergent development of pectoral muscle in ducks by transcriptomic analysis

  • Fan Li (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Zongliang He (Nanjing Institute of Animal Husbandry and Poultry Science) ;
  • Yinglin Lu (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Jing Zhou (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Heng Cao (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Xingyu Zhang (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Hongjie Ji (Nanjing Institute of Animal Husbandry and Poultry Science) ;
  • Kunpeng Lv (Nanjing Institute of Animal Husbandry and Poultry Science) ;
  • Debing Yu (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Minli Yu (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University)
  • Received : 2023.12.01
  • Accepted : 2024.01.26
  • Published : 2024.08.01
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Abstract

Objective: The objective of this study was to identify candidate genes that play important roles in skeletal muscle development in ducks. Methods: In this study, we investigated the transcriptional sequencing of embryonic pectoral muscles from two specialized lines: Liancheng white ducks (female) and Cherry valley ducks (male) hybrid Line A (LCA) and Line C (LCC) ducks. In addition, prediction of target genes for the differentially expressed mRNAs was conducted and the enriched gene ontology (GO) terms and Kyoto encyclopedia of genes and genomes signaling pathways were further analyzed. Finally, a protein-to-protein interaction network was analyzed by using the target genes to gain insights into their potential functional association. Results: A total of 1,428 differentially expressed genes (DEGs) with 762 being up-regulated genes and 666 being down-regulated genes in pectoral muscle of LCA and LCC ducks identified by RNA-seq (p<0.05). Meanwhile, 23 GO terms in the down-regulated genes and 75 GO terms in up-regulated genes were significantly enriched (p<0.05). Furthermore, the top 5 most enriched pathways were ECM-receptor interaction, fatty acid degradation, pyruvate degradation, PPAR signaling pathway, and glycolysis/gluconeogenesis. Finally, the candidate genes including integrin b3 (Itgb3), pyruvate kinase M1/2 (Pkm), insulin-like growth factor 1 (Igf1), glucose-6-phosphate isomerase (Gpi), GABA type A receptor-associated protein-like 1 (Gabarapl1), and thyroid hormone receptor beta (Thrb) showed the most expression difference, and then were selected to verification by quantitative real-time polymerase chain reaction (qRT-PCR). The result of qRT-PCR was consistent with that of transcriptome sequencing. Conclusion: This study provided information of molecular mechanisms underlying the developmental differences in skeletal muscles between specialized duck lines.

Keywords

Acknowledgement

This work was supported by Livestock and Poultry in Jiangsu Province, the Revitalization of the Seed Industry to Unveil the Marshal Project (core seed source research project) (JBGS (2021)112) and the National Natural Science Foundation of China (32372825).

References

  1. Picard B, Berri C, Lefaucheur L, Molette C, Sayd T, Terlouw C. Skeletal muscle proteomics in livestock production. Brief Funct Genomics 2010;9:259-78. https://doi.org/10.1093/bfgp/elq005
  2. Joo ST, Kim GD, Hwang YH, Ryu YC. Control of fresh meat quality through manipulation of muscle fiber characteristics. Meat Sci 2013;95:828-36. https://doi.org/10.1016/j.meatsci.2013.04.044
  3. Li C, Xiong T, Zhou MF, et al. Characterization of microRNAs during embryonic skeletal muscle development in the Shan Ma duck. Animals (Basel) 2020;10:1417. https://doi.org/10.3390/ani10081417
  4. Ren LT, Liu AF, Wang QG, Wang HG, Dong DQ, Liu LB. Transcriptome analysis of embryonic muscle development in Chengkou mountain chicken. BMC Genomics 2021;22:431. https://doi.org/10.1186/s12864-021-07740-w
  5. Bismuth K, Relaix F. Genetic regulation of skeletal muscle development. Exp Cell Res 2010;316:3081-6. https://doi.org/10.1016/j.yexcr.2010.08.018
  6. Lin RY, Li JQ, Yang Y, et al. Genome-wide population structure analysis and genetic diversity detection of four Chinese indigenous duck breeds from Fujian Province. Animals (Basel) 2022;12:2302. https://doi.org/10.3390/ani12172302
  7. Huo WR, Weng KQ, Gu TT, et al. Effect of muscle fiber characteristics on meat quality in fast- and slow-growing ducks. Poult Sci 2021;100:101264. https://doi.org/10.1016/j.psj.2021.101264
  8. Tang H, Gong YZ, Wu CX, Jiang J, Wang Y, Li K. Variation of meat quality traits among five genotypes of chicken. Poult Sci 2009;88:2212-8. https://doi.org/10.3382/ps.2008-00036
  9. Werner C, Janisch S, Kuembet U, Wicke M. Comparative study of the quality of broiler and turkey meat. Br Poult Sci 2009;50:318-24. https://doi.org/10.1080/00071660902806939
  10. Kokoszynski D, Piwczynski D, Arpasova H, Hrncar C, Saleh M, Wasilewski R. A comparative study of carcass characteristics and meat quality in genetic resources Pekin ducks and commercial crossbreds. Asian-Australas J Anim Sci 2019;32:1753-62. https://doi.org/10.5713/ajas.18.0790
  11. Costa V, Angelini C, De Feis I, Ciccodicola A. Uncovering the complexity of transcriptomes with RNA-Seq. J Biomed Biotechnol 2010;2010:853916. https://doi.org/10.1155/2010/853916
  12. Jiang Z, Zhou X, Li R, et al. Whole transcriptome analysis with sequencing: methods, challenges and potential solutions. Cell Mol Life Sci 2015;72:3425-39. https://doi.org/10.1007/s00018-015-1934-y
  13. Zhang ZR, Du HR, Yang CW, et al. Comparative transcriptome analysis reveals regulators mediating breast muscle growth and development in three chicken breeds. Anim Biotechnol 2019;30:233-41. https://doi.org/10.1080/10495398.2018.1476377
  14. Cui H, Zheng M, Zhao G, Liu R, Wen J. Identification of differentially expressed genes and pathways for intramuscular fat metabolism between breast and thigh tissues of chickens. BMC Genomics 2018;19:55. https://doi.org/10.1186/s12864-017-4292-3
  15. Hu ZG, Gao JT, Ge LY, Zhang JQ, Zhang HL, Liu XL. Characterization and comparative transcriptomic analysis of skeletal muscle in Pekin duck at different growth stages using RNA-Seq. Animals (Basel) 2021;11:834. https://doi.org/10.3390/ani11030834
  16. Gill N, Dhillon B. RNA-seq data analysis for differential expression. Methods Mol Biol 2022;2391:45-54. https://doi.org/10.1007/978-1-0716-1795-3_4
  17. Huo WR, Weng KQ, Li Y, et al. Comparison of muscle fiber characteristics and glycolytic potential between slow and fast growing broilers. Poult Sci 2022;101:101649. https://doi.org/10.1016/j.psj.2021.101649
  18. Ismail I, Joo ST. Poultry meat quality in relation to muscle growth and muscle fiber characteristics. Korean J Food Sci Anim Resour 2017;37:873-83.
  19. Rehfeldt C, Kuhn G. Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci 2006;84(Suppl 13):E113-23. https://doi.org/10.2527/2006.8413_supple113x
  20. Ryu YC, Kim BC. The relationship between muscle fiber characteristics, postmortem metabolic rate, and meat quality of pig longissimus dorsi muscle. Meat Sci 2005;71:351-7. https://doi.org/10.1016/j.meatsci.2005.04.015
  21. Gentry JG, McGlone JJ, Blanton JR, Miller MF. Impact of spontaneous exercise on performance, meat quality, and muscle fiber characteristics of growing/finishing pigs. J Anim Sci 2002;80:2833-9. https://doi.org/10.2527/2002.80112833x
  22. Alsoufi MA, Liu Y, Cao CW, et al. Integrated transcriptomics profiling in chahua and digao chickens' breast for assessment molecular mechanism of meat quality traits. Genes (Basel) 2022;14:95. https://doi.org/10.3390/genes14010095
  23. San JS, Du YT, Wu GF, Xu RF, Yang JC, Hu JM. Transcriptome analysis identifies signaling pathways related to meat quality in broiler chickens - the extracellular matrix (ECM) receptor interaction signaling pathway. Poult Sci 2021;100:101135. https://doi.org/10.1016/j.psj.2021.101135
  24. Chrominski K, Tkacz M. Comparison of high-level microarray analysis methods in the context of result consistency. PLoS One 2015;10:e0128845. https://doi.org/10.1371/journal.pone.0128845
  25. Shi JP, Wang XY, Song YL, Liu T, Cheng SR, Zhang QW. Excavation of genes related to the mining of growth, development, and meat quality of two crossbred sheep populations based on comparative transcriptomes. Animals (Basel) 2021;11:1492. https://doi.org/10.3390/ani11061492
  26. Tomczak KK, Marinescu VD, Ramoni MF, et al. Expression profiling and identification of novel genes involved in myogenic differentiation. FASEB J 2004;18:403-5. https://doi.org/10.1096/fj.03-0568fje
  27. Wu JJ, Rong S, Zhou J, Yuan WJ. The role and mechanism of PKM2 in the development of LPS-induced acute kidney injury. Histol Histopathol 2021;36:845-52. https://doi.org/10.14670/hh-18-343
  28. Chhipa AS, Patel S. Targeting pyruvate kinase muscle isoform 2 (PKM2) in cancer: What do we know so far? Life Sci 2021;280:119694. https://doi.org/10.1016/j.lfs.2021.119694
  29. Dayton TL, Jacks T, Vander Heiden MG. PKM2, cancer metabolism, and the road ahead. EMBO Rep 2016;17:1721-30. https://doi.org/10.15252/embr.201643300
  30. Gao F, Zhang XJ, Wang SY, et al. TSP50 promotes the Warburg effect and hepatocyte proliferation via regulating PKM2 acetylation. Cell Death Dis 2021;12:517. https://doi.org/10.1038/s41419-021-03782-w
  31. Zhang T, Lu HZ, Wang L, Yin MC, Yang LK. Specific expression pattern of IMP metabolism related-genes in chicken muscle between cage and free range conditions. PLoS One 2018;13:e0201736. https://doi.org/10.1371/journal.pone.0201736
  32. Jaensch N, Correa, Jr. IR, Watanabe R. Stable cell surface expression of GPI-anchored proteins, but not intracellular transport, depends on their fatty acid structure. Traffic 2014;15:1305-29. https://doi.org/10.1111/tra.12224
  33. Kinoshita T. Biosynthesis and biology of mammalian GPI-anchored proteins. Open Biol 2020;10:190290. https://doi.org/10.1098/rsob.190290
  34. Jianmin Z, Jingting S, Yanju S, Yan H, Chi S, Wenqi Z. Expression of insulin-like growth factor system genes in liver tissue during embryonic and early post-hatch development in duck (Anas platyrhynchos Domestica). Anim Biotechnol 2014;25:73-84. https://doi.org/10.1080/10495398.2013.812560
  35. Li Y, Xu ZY, Li HY, Xiong YZ, Zuo B. Differential transcriptional analysis between red and white skeletal muscle of Chinese Meishan pigs. Int J Biol Sci 2010;6:350-60. https://doi.org/10.7150/ijbs.6.350
  36. Liu YL, Guo W, Pu ZY, et al. Developmental changes of insulin-like growth factors in the liver and muscle of chick embryos. Poult Sci 2016;95:1396-402. https://doi.org/10.3382/ps/pew043
  37. Sun W, Ge Y, Cui JP, Yu YF, Liu BL. Scutellarin resensitizes oxaliplatin-resistant colorectal cancer cells to oxaliplatin treatment through inhibition of PKM2. Mol Ther Oncolytics 2021;21:87-97. https://doi.org/10.1016/j.omto.2021.03.010
  38. Liu HY, Han JM, Cao SY, et al. Hepatic autophagy is suppressed in the presence of insulin resistance and hyperinsulinemia: inhibition of FoxO1-dependent expression of key autophagy genes by insulin. J Biol Chem 2009;284:31484-92. https://doi.org/10.1074/jbc.m109.033936