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Genetic, management, and nutritional factors affecting intramuscular fat deposition in beef cattle - A review

  • Park, Seung Ju (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Beak, Seok-Hyeon (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Jung, Da Jin Sol (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Kim, Sang Yeob (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Jeong, In Hyuk (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Piao, Min Yu (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Kang, Hyeok Joong (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Fassah, Dilla Mareistia (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Na, Sang Weon (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Yoo, Seon Pil (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Baik, Myunggi (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University)
  • Received : 2018.04.19
  • Accepted : 2018.05.10
  • Published : 2018.07.01

Abstract

Intramuscular fat (IMF) content in skeletal muscle including the longissimus dorsi muscle (LM), also known as marbling fat, is one of the most important factors determining beef quality in several countries including Korea, Japan, Australia, and the United States. Genetics and breed, management, and nutrition affect IMF deposition. Japanese Black cattle breed has the highest IMF content in the world, and Korean cattle (also called Hanwoo) the second highest. Here, we review results of research on genetic factors (breed and sex differences and heritability) that affect IMF deposition. Cattle management factors are also important for IMF deposition. Castration of bulls increases IMF deposition in most cattle breeds. The effects of several management factors, including weaning age, castration, slaughter weight and age, and environmental conditions on IMF deposition are also reviewed. Nutritional factors, including fat metabolism, digestion and absorption of feed, glucose/starch availability, and vitamin A, D, and C levels are important for IMF deposition. Manipulating IMF deposition through developmental programming via metabolic imprinting is a recently proposed nutritional method to change potential IMF deposition during the fetal and neonatal periods in rodents and domestic animals. Application of fetal nutritional programming to increase IMF deposition of progeny in later life is reviewed. The coordination of several factors affects IMF deposition. Thus, a combination of several strategies may be needed to manipulate IMF deposition, depending on the consumer's beef preference. In particular, stage-specific feeding programs with concentrate-based diets developed by Japan and Korea are described in this article.

Keywords

Beef Cattle;Intramuscular Fat Deposition;Genetic Factors;Management;Nutrition

Acknowledgement

Supported by : Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET), National Research Foundation of Korea (NRF)

References

  1. Wheeler TL, Cundiff LV, Koch RM. Effect of marbling degree on beef palatability in Bos taurus and Bos indicus cattle. J Anim Sci 1994;72:3145-51. https://doi.org/10.2527/1994.72123145x
  2. Piao MY, Baik M. Seasonal variation in carcass characteristics of Korean cattle steers. Asian-Australas J Anim Sci 2015;28:442-50. https://doi.org/10.5713/ajas.14.0650
  3. Hunt MR, Garmyn AJ, O'Quinn TG, et al. Consumer assessment of beef palatability from four beef muscles from USDA Choice and Select graded carcasses. Meat Sci 2014;98:1-8. https://doi.org/10.1016/j.meatsci.2014.04.004
  4. Moody WG, Cassens RG. A quantitative and morphological study of bovine longissimus fat cells. J Food Sci 1968;33:47-52. https://doi.org/10.1111/j.1365-2621.1968.tb00882.x
  5. Smith SB, Lunt DK, Zembayashi M. Intramuscular fat deposition. The physiological process and the potential for its manipulation. In: Proceeding of the Plains Nutrition Council 2000; 2000 Apr 13-14: San Antonio, TX, USA: Texas A&M Research and Extension Center; 2000. pp. 1-12.
  6. Baik M, Vu TTT, Piao MY, Kang HJ. Association of DNA methylation levels with tissue-specific expression of adipogenic and lipogenic genes in longissimus dorsi muscle of Korean cattle. Asian-Australas J Anim Sci 2014;27:1493-8. https://doi.org/10.5713/ajas.2014.14283
  7. Baik M, Jeong JY, Vu TTT, Piao MY, Kang HJ. Effects of castration on the adiposity and expression of lipid metabolism genes in various fat depots of Korean cattle. Livest Sci 2014;168:168-76. https://doi.org/10.1016/j.livsci.2014.08.013
  8. Baik M, Nguyen TH, Jeong JY, Piao MY, Kang HJ. Effects of castration on expression of lipid metabolism genes in the liver of Korean cattle. Asian-Australas J Anim Sci 2015;28:127-34.
  9. Bong JJ, Jeong JY, Rajasekar P, et al. Differential expression of genes associated with lipid metabolism in longissimus dorsi of Korean bulls and steers. Meat Sci 2012;91:284-93. https://doi.org/10.1016/j.meatsci.2012.02.004
  10. Jeong J, Kwon EG, Im SK, Seo KS, Baik M. Expression of fat deposition and fat removal genes is associated with intramuscular fat content in longissimus dorsi muscle of Korean cattle steers. J Anim Sci 2012;90:2044-53. https://doi.org/10.2527/jas.2011-4753
  11. Jeong J, Kim JS, Nguyen TH, Lee HJ, Baik M. Wnt/beta-catenin signaling and adipogenic genes are associated with intramuscular fat content in the longissimus dorsi muscle of Korean cattle. Anim Genet 2013;44:627-35. https://doi.org/10.1111/age.12061
  12. Jeong J, Bong JJ, Kim GD, et al. Transcriptome changes favoring intramuscular fat deposition in the longissimus muscle following castration of bulls. J Anim Sci 2013;91:4692-704. https://doi.org/10.2527/jas.2012-6089
  13. Baik M, Kang HJ, Park SJ, et al. Triennial growth and development ymposium: molecular mechanisms related to bovine intramuscular fat deposition in the longissimus muscle. J Anim Sci 2017;95:2284-303.
  14. Hood RL, Allen CE. Cellularity of bovine adipose tissue. J Lipid Res 1973;14:605-10.
  15. Owens FN, Dubeski P, Hanson CF. Factors that alter the growth and development of ruminants. J Anim Sci 1993;71:3138-50. https://doi.org/10.2527/1993.71113138x
  16. Du M, Huang Y, Das AK, et al. Meat science and muscle biology symposium: manipulating mesenchymal progenitor cell differentiation to optimize performance and carcass value of beef cattle. J Anim Sci 2013;91:1419-27. https://doi.org/10.2527/jas.2012-5670
  17. Du M, Tong J, Zhao J, et al. Fetal programming of skeletal muscle development in ruminant animals. J Anim Sci 2010;88:E51-60. https://doi.org/10.2527/jas.2009-2311
  18. Du M, Wang B, Fu X, Yang Q, Zhu MJ. Fetal praogramming in meat production. Meat Sci 2015;109:40-7. https://doi.org/10.1016/j.meatsci.2015.04.010
  19. Hausman GJ, Dodson MV, Ajuwon K, et al. Board-invited review: the biology and regulation of preadipocytes and adipocytes in meat animals. J Anim Sci 2009;87:1218-46. https://doi.org/10.2527/jas.2008-1427
  20. Bonnet M, Cassar-Malek I, Chilliard Y, Picard B. Ontogenesis of muscle and adipose tissues and their interactions in ruminants and other species. Animal 2010;4:1093-109. https://doi.org/10.1017/S1751731110000601
  21. Uezumi A, Ito T, Morikawa D, et al. Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle. J Cell Sci 2011;124:3654-64. https://doi.org/10.1242/jcs.086629
  22. Huang Y, Das AK, Yang QY, Zhu MJ, Du M. Zfp423 promotes adipogenic differentiation of bovine stromal vascular cells. PLoS One 2012;7:e47496. https://doi.org/10.1371/journal.pone.0047496
  23. Harper GS, Pethick DW. How might marbling begin? Aust J Exp Agric 2004;44:653-62. https://doi.org/10.1071/EA02114
  24. Albrecht E, Teuscher F, Ender K, Wegner J. Growth- and breedrelated changes of marbling characteristics in cattle. J Anim Sci 2006;84:1067-75. https://doi.org/10.2527/2006.8451067x
  25. Albrecht E, Gotoh T, Ebara F, et al. Cellular conditions for intramuscular fat deposition in Japanese Black and Holstein steers. Meat Sci 2011;89:13-20. https://doi.org/10.1016/j.meatsci.2011.03.012
  26. Irie M, Kouda M, Matono H. Effect of ursodeoxycholic acid supplementation on growth, carcass characteristics, and meat quality of Wagyu heifers (Japanese Black cattle). J Anim Sci 2011;89:4221-6. https://doi.org/10.2527/jas.2011-4211
  27. Cho SH, Kang GH, Seong PN, et al. Effect of slaughter age on the antioxidant enzyme activity, color, and oxidative stability of Korean Hanwoo (Bos taurus coreanae) cow beef. Meat Sci 2015;108:44-9. https://doi.org/10.1016/j.meatsci.2015.05.018
  28. Choi CB, Jung KK, Chung KY, et al. Administration of zilpaterol hydrochloride alters feedlot performance, carcass characteristics, muscle, and fat profiling in finishing Hanwoo steers. Livest Sci 2013;157:435-41. https://doi.org/10.1016/j.livsci.2013.06.035
  29. Jung S, Nam KC, Lee KH, et al. Meat quality traits of longissimus dorsi muscle from carcasses of Hanwoo steers at different yield grades. Korean J Food Sci Anim Resour 2013;33:305-16. https://doi.org/10.5851/kosfa.2013.33.3.305
  30. Greenwood PL, Siddell JP, Walmsley BJ, et al. Postweaning substitution of grazed forage with a high-energy concentrate has variable long-term effects on subcutaneous fat and marbling in Bos taurus genotypes. J Anim Sci 2015;93:4132-43. https://doi.org/10.2527/jas.2015-8962
  31. Krone KG, Ward AK, Madder KM, et al. Interaction of vitamin A supplementation level with ADH1C genotype on intramuscular fat in beef steers. Animal 2016;10:403-9. https://doi.org/10.1017/S1751731115002153
  32. Dinh TT, Blanton JR Jr, Riley DG, et al. Intramuscular fat and fatty acid composition of longissimus muscle from divergent pure breeds of cattle. J Anim Sci 2010;88:756-66. https://doi.org/10.2527/jas.2009-1951
  33. Robinson DL, Cafe LM, Greenwood PL. Developmental programming in cattle: Consequences for growth, efficiency, carcass, muscle, and beef quality characteristics. J Anim Sci 2013;91:1428-42. https://doi.org/10.2527/jas.2012-5799
  34. Lapitan RM, Del Barrio AN, Katsube O, et al. Comparison of carcass and meat characteristics of Brahman grade cattle (Bos indicus) and crossbred water buffalo (Bubalus bubalis). Anim Sci J 2007;78:596-604. https://doi.org/10.1111/j.1740-0929.2007.00480.x
  35. Lapitan RM, Del Barrio AN, Katsube O, et al. Comparison of carcass and meat characteristics of Brahman grade cattle (Bos indicus) and crossbred water buffalo (Bubalus bubalis) fed on high roughage diet. Anim Sci J 2008;79:210-7. https://doi.org/10.1111/j.1740-0929.2008.00519.x
  36. Miguel JA, Ciria J, Asenjo B, et al. Chemical composition of meat in castrated male Brahman cattle in Venezuela. J Life Sci 2011:5;562-8.
  37. Burrow HM, Moore SS, Johnston DJ, Barendse W, Bindon BM. Quantitative and molecular genetic influences on properties of beef: a review. Aust J Exp Agric 2001;41:893-919. https://doi.org/10.1071/EA00015
  38. Marti S, Realini CE, Bach A, Pérez-Juan M, Devant M. Effect of castration and slaughter age on performance, carcass, and meat quality traits of Holstein calves fed a high-concentrate diet. J Anim Sci 2013;91:1129-40. https://doi.org/10.2527/jas.2012-5717
  39. Park GB, Moon SS, Ko YD, et al. Influence of slaughter weight and sex on yield and quality grades of Hanwoo (Korean native cattle) carcasses. J Anim Sci 2002;80:129-36. https://doi.org/10.2527/2002.801129x
  40. Seideman SC, Cross HR, Oltjen RR, Schanbacher BD. Utilization of the intact male for red meat production: a review. J Anim Sci 1982;55:826-40. https://doi.org/10.2527/jas1982.554826x
  41. Utrera RA, Van Vleck LD. Heritability estimates for carcass traits of cattle: a review. Genet Mol Res 2004;3:380-94.
  42. Yoon HB, Seo KS, Kim SD, et al. Estimation of genetic parameters for direct genetic effect for carcass traits of Hanwoo (Korean Brown cattle) steers. In: Proceedings of the 7th World Congress on Genetics Applied to Livestock Production 2002; 2002 Aug 19-23: Montpellier, France. Session 02. Breeding ruminants for meat production. Communication No. 02-89.
  43. Park B, Choi T, Kim S, Oh SH. National genetic evaluation (system) of Hanwoo (Korean naitve cattle). Asian-Australas J Anim Sci 2013;26:151-6. https://doi.org/10.5713/ajas.2012.12439
  44. Hirooka H, Groen AF, Matsumoto M. Genetic parameters for growth and carcass traits in Japanese brown cattle estimated from field records. J Anim Sci 1996;74:2112-6. https://doi.org/10.2527/1996.7492112x
  45. Nogi T, Honda T, Mukai F, Okagaki T, Oyama K. Heritabilities and genetic correlations of fatty acid compositions in longissimus muscle lipid with carcass traits in Japanese black cattle. J Anim Sci 2011;89:615-21. https://doi.org/10.2527/jas.2009-2300
  46. Oyama K. Genetic variability of Wagyu cattle estimated by statistical approaches. Anim Sci J 2011;82:367-73. https://doi.org/10.1111/j.1740-0929.2011.00895.x
  47. MacNeil MD, Nkrumah JD, Woodward BW, Northcutt SL. Genetic evaluation of Angus cattle for carcass marbling using ultrasound and genomic indicators. J Anim Sci 2010;88:517-22. https://doi.org/10.2527/jas.2009-2022
  48. Riley DG, Chase CC, Hammond AC, et al. Estimated genetic parameters for carcass traits of Brahman cattle. J Anim Sci 2002;80:955-62. https://doi.org/10.2527/2002.804955x
  49. Smith T, Domingue JD, Paschal JC, et al. Genetic parameters for growth and carcass traits of Brahman steers12. J Anim Sci 2007;85:1377-84. https://doi.org/10.2527/jas.2006-653
  50. Black DN, Neville BW, Crosswhite MR, Dahlen CR. Evaluation of implant strategies in Angus-sired steers with high or low genetic potential for marbling and gain. J Anim Sci 2015;93:5411-8. https://doi.org/10.2527/jas.2015-9296
  51. Meyer DL, Kerley MS, Walker EL, et al. Growth rate, body composition, and meat tenderness in early vs. traditionally weaned beef calves. J Anim Sci 2005;83:2752-61. https://doi.org/10.2527/2005.83122752x
  52. Wolcott ML, Graser HU, Johnston DJ. Effects of early weaning on growth, feed efficiency and carcass traits in Shorthorn cattle. Anim Prod Sci 2010;50:315-21. https://doi.org/10.1071/AN09153
  53. Wertz AE, Berger LL, Walker PM, et al. Early-weaning and postweaning nutritional management affect feedlot performance, carcass merit, and the relationship of 12th-rib fat, marbling score, and feed efficiency among Angus and Wagyu heifers. J Anim Sci 2002;80:28-37. https://doi.org/10.2527/2002.80128x
  54. Scheffler JM, McCann MA, Greiner SP, et al. Early metabolic imprinting events increase marbling scores in fed cattle. J Anim Sci 2014;92:320-4. https://doi.org/10.2527/jas.2012-6209
  55. Moisa SJ, Shike DW, Faulkner DB, et al. Central role of the PPARgamma gene network in coordinating beef cattle intramuscular adipogenesis in response to weaning age and nutrition. Gene Regul Syst Bio 2014;8:17-32.
  56. Graugnard DE, Berger LL, Faulkner DB, Loor JJ. High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned Angus cattle. Br J Nutr 2010;103:953-63. https://doi.org/10.1017/S0007114509992789
  57. Smith SB, Johnson BJ. Marbling: management of cattle to maximize the deposition of intramuscular adipose tissue. Centennial, CO, USA: National Cattlemen's Beef Association; 2014.
  58. Reddy KE, Jeong J, Lee SD, et al. Effect of different early weaning regimens for calves on adipogenic gene expression in Hanwoo loin at the fattening stage. Livest Sci 2017;195:87-98. https://doi.org/10.1016/j.livsci.2016.11.014
  59. eKAPEpia. Grade evaluation of cattle [Internet]. Korea Institute for Animal Products Quality Evaluation; c2017 [cited 2017 Dec 27]. Available from: http://www.ekapepia.com/user/distribution/distDetail.do?nd1906
  60. Jones SDM, Tong AKW, Talbot S. A survey of marbling fat in Canadian beef carcasses. Can J Anim Sci 1991;71:987-91. https://doi.org/10.4141/cjas91-119
  61. Gotoh T, Joo ST. Characteristics and health benefit of highly marbled Wagyu and Hanwoo beef. Korean J Food Sci Anim Resour 2016;36:709-18. https://doi.org/10.5851/kosfa.2016.36.6.709
  62. Choi BH, Ahn BJ, Kook K, et al. Effects of feeding patterns and sexes on growth rate, carcass trait and grade in Korean native cattle. Asian-Australas J Anim Sci 2002;15:838-43. https://doi.org/10.5713/ajas.2002.838
  63. Purchas RW, Burnham DL, Morris ST. Effects of growth potential and growth path on tenderness of beef longissimus muscle from bulls and steers. J Anim Sci 2002;80:3211-21. https://doi.org/10.2527/2002.80123211x
  64. Rodriguez J, Unruh J, Villarreal M, et al. Carcass and meat quality characteristics of Brahman cross bulls and steers finished on tropical pastures in Costa Rica. Meat Sci 2014;96:1340-4. https://doi.org/10.1016/j.meatsci.2013.10.024
  65. Okumura T, Saito K, Sowa T, et al. Changes in beef sensory traits as somatic-cell-cloned Japanese black steers increased in age from 20 to 30 months. Meat Sci 2012;90:159-63. https://doi.org/10.1016/j.meatsci.2011.06.020
  66. Zembayashi M, Nishimura K, Lunt DK, Smith SB. Effect of breed type and sex on the fatty acid composition of subcutaneous and intramuscular lipids of finishing steers and heifers. J Anim Sci 1995;73:3325-32. https://doi.org/10.2527/1995.73113325x
  67. Kirkland RM, Patterson DC, Keady TW, Moss BW, Steen RW. Beef production potential of Norwegian Red and Holstein-Friesian bulls slaughtered at two ages. Animal 2007;1:1506-14.
  68. Lee S-C, Choi H-H, Shin J-S, et al. Carcass characteristics and profitability analysis based on slaughter age of Hanwoo steers. J Anim Sci Technol 2013;55:315-23. https://doi.org/10.5187/JAST.2013.55.4.315
  69. Pethick DW, Harper GS, Oddy VH. Growth, development and nutritional manipulation of marbling in cattle: a review. Aust J Exp Agric 2004;44:705-15. https://doi.org/10.1071/EA02165
  70. Agastin A, Naves M, Farant A, et al. Effects of feeding system and slaughter age on the growth and carcass characteristics of tropical-breed steers. J Anim Sci 2013;91:3997-4006. https://doi.org/10.2527/jas.2012-5999
  71. Lorenzen CL, Hale DS, Griffin DB, et al. National Beef Quality Audit: survey of producer-related defects and carcass quality and quantity attributes. J Anim Sci 1993;71:1495-502. https://doi.org/10.2527/1993.7161495x
  72. Bruns KW, Pritchard RH, Boggs DL. The relationships among body weight, body composition, and intramuscular fat content in steers. J Anim Sci 2004;82:1315-22. https://doi.org/10.2527/2004.8251315x
  73. Kern SA, Pritchard RH, Blair AD, Scramlin SM, Underwood KR. The influence of growth stage on carcass composition and factors associated with marbling development in beef cattle. J Anim Sci 2014;92:5275-84. https://doi.org/10.2527/jas.2014-7891
  74. Mader TL, Fell LR, McPhee MJ. Behavior response of non-Brahman cattle to shade in commercial feedlots. In: Proceedings of the 5th International Livestock Environment Symposium 1997; 1997: Bloomington, MN, USA. St. Joseph, MI, USA: American Society of Agriculture Biology Engineers; 1997. pp. 795-802.
  75. Ames DR, Brink DR, Willms CL. Adjusting protein in feedlot diets during thermal stress. J Anim Sci 1980;50:1-6. https://doi.org/10.2527/jas1980.5011
  76. Young BA. Cold stress as it affects animal production. J Anim Sci 1981;52:154-63. https://doi.org/10.2527/jas1981.521154x
  77. Birkelo CP, Johnson DE, Phetteplace HP. Maintenance requirements of beef cattle as affected by season on different planes of nutrition. J Anim Sci 1991;69:1214-22. https://doi.org/10.2527/1991.6931214x
  78. Kang HJ, Lee IK, Piao MY, et al. Effects of ambient temperature on growth performance, blood metabolites, and immune cell populations in Korean cattle steers. Asian-Australas J Anim Sci 2016;29:436-43. https://doi.org/10.5713/ajas.15.0937
  79. Hahn GL. Environmental influences on feed intake and performance of feedlot cattle. In: Owens FN, editor. Proc. Symp. Intake by Feedlot Cattle. Stillwater OK, USA: Oklahoma State University; 1995. pp. 207-25.
  80. Yadav B, Pandey V, Yadav S, et al. Effect of misting and wallowing cooling systems on milk yield, blood and physiological variables during heat stress in lactating Murrah buffalo. J Anim Sci Technol 2016;58:2. https://doi.org/10.1186/s40781-015-0082-0
  81. Young BA. Ruminant cold stress: effect on production. Can J Anim Sci 1983;57:1601-7. https://doi.org/10.2527/jas1983.5761601x
  82. Mader TL, Davis MS. Effect of management strategies on reducing heat stress of feedlot cattle: feed and water intake. J Anim Sci 2004;82:3077-87. https://doi.org/10.2527/2004.82103077x
  83. Kang HJ, Piao MY, Lee IK, et al. Effects of ambient temperature and dietary glycerol addition on growth performance, blood parameters and immune cell populations of Korean cattle steers. Asian-Australas J Anim Sci 2017;30:505-13.
  84. Bauman DE, Davis CL. Regulation of lipid metabolism. Digestion and metabolism in the ruminant. In: Proceedings of the 4th International Symposium on Ruminant Physiology; 1975; University of New England Publishing Unit, Armidale, NSW, Australia.
  85. Hanson RW, Ballard FJ. The relative significance of acetate and glucose as precursors for lipid synthesis in liver and adipose tissue from ruminants. Biochem J 1967;105:529-36. https://doi.org/10.1042/bj1050529
  86. Nafikov RA, Beitz DC. Carbohydrate and lipid metabolism in farm animals. J Nutr 2007;137:702-5. https://doi.org/10.1093/jn/137.3.702
  87. Ballard FJ, Hanson RW, Kronfeld DS. Gluconeogenesis and lipogenesis in tissue from ruminant and nonruminant animals. Fed Proc 1969;28:218-31.
  88. Smith SB, Crouse JD. Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. J Nutr 1984;114:792-800. https://doi.org/10.1093/jn/114.4.792
  89. Smith SB, Prior RL, Koong LJ, Mersmann HJ. Nitrogen and lipid metabolism in heifers fed at increasing levels of intake. J Amin Sci 1992;70:152-60.
  90. Hocquette JF, Gondret F, Baeza E, et al. Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, and identification of putative markers. Animal 2010;4:303-19. https://doi.org/10.1017/S1751731109991091
  91. Rhoades RD, Sawyer JE, Chung KY, et al. Effect of dietary energy source on in vitro substrate utilization and insulin sensitivity of muscle and adipose tissues of Angus and Wagyu steers. J Anim Sci 2007;85:1719-26. https://doi.org/10.2527/jas.2006-498
  92. Laplaud PM, Bauchart D, Durand D, Chapman MJ. Lipoproteins and apolipoproteins in intestinal lymph of the preruminant calf, Bos spp., at peak lipid absorption. J Lipid Res 1990;31:1781-92.
  93. Pethick DW, Harper GS, Dunshea FR. Fat metabolism and turnover. In: Dijkstra J, Forbes JM, editors. Quantitative aspects of ruminant digestion and metabolism. Oxford, UK: CAB International; 1993. pp. 345-71.
  94. Andrae JG, Duckett SK, Hunt CW, Pritchard GT, Owens FN. Effects of feeding high-oil corn to beef steers on carcass characteristics and meat quality. J Anim Sci 2001;79:582-8. https://doi.org/10.2527/2001.793582x
  95. Gotoh T, Takahashi H, Nishimura T, Kuchida K, Mannen H. Meat producded by Japanese Black cattle and Wagyu. Anim Front 2014;4:46-54.
  96. Jo C, Cho SH, Chang J, Nam KC. Keys to production and processing of Hanwoo beef: A perspective of tradition and science. Anim Front 2012;2:32-8.
  97. Wan R, Du J, Ren L, Meng Q. Selective adipogenic effects of propionate on bovine intramuscular and subcutaneous preadipocytes. Meat Sci 2009;82:372-8. https://doi.org/10.1016/j.meatsci.2009.02.008
  98. Bonnet M, Faulconnier Y, Leroux C, et al. Glucose-6-phosphate dehydrogenase and leptin are related to marbling differences among Limousin and Angus or Japanese Black Angus steers. J Anim Sci 2007;85:2882-94. https://doi.org/10.2527/jas.2007-0062
  99. Abelson JL, Khan S, Liberzon I, Young EA. HPA axis activity in patients with panic disorder: review and synthesis of four studies. Depress Anxiety 2007;24:66-76. https://doi.org/10.1002/da.20220
  100. Parker KL, Rainey WE. The adrenal gland. In: Griffin JE, Ojeda SR, editors. Textbook of endocrine physiology.5th ed. New York, USA: Oxford University Press; 2004. pp. 319-48.
  101. Paakkonen T, Leppaluoto J. Cold exposure and hormonal secretion: a review. Int J Circumpolar Health 2002;61:265-76. https://doi.org/10.3402/ijch.v61i3.17474
  102. Akana SF, Strack AM, Hanson ES, et al. Interactions among chronic cold, corticosterone and puberty on energy intake and deposition. Stress 1999;3:131-46. https://doi.org/10.3109/10253899909001118
  103. Kang HJ, Lee IK, Piao MY, et al. Effects of road transportation on metabolic and immunological responses in Holstein heifers. Anim Sci J 2017;88:140-8. https://doi.org/10.1111/asj.12604
  104. Mills JK, Ross DA, Van Amburgh ME. The effects of feeding medium-chain triglycerides on the growth, insulin responsiveness, and body composition of Holstein calves from birth to 85 kg of body weight. J Dairy Sci 2010;93:4262-73. https://doi.org/10.3168/jds.2010-3142
  105. Doreau M, Ferlay A. Digestion and utilization of fatty acids by ruminants. Anim Feed Sci Technol 1994;45:379-96. https://doi.org/10.1016/0377-8401(94)90039-6
  106. Zinn RA, Gulati SK, Plascencia A, Salinas J. Influence of ruminal biohydrogenation on the feeding value of fat in finishing diets for feedlot cattle. J Anim Sci 2000;78:1738-46. https://doi.org/10.2527/2000.7871738x
  107. Hess BW, Moss GE, Rule DC. A decade of developments in the area of fat supplementation research with beef cattle and sheep. J Anim Sci 2007:86:E188-204.
  108. Jeong J, Hwang JM, Seong NI, et al. Effects of supplemented $PROSOL^{(R)}$ as an emulsifier on growth performance and carcass characteristics in Hanwoo steers of final fattening period. J Anim Sci Technol 2009;51:395-406. https://doi.org/10.5187/JAST.2009.51.5.395
  109. Nelson DL, Cox MM. Lehninger principles of biochemistry. 5th ed. New Yrok, USA: W.H. Freeman; 2008.
  110. Orskov ER. Starch digestion and utilization in ruminants. J Anim Sci 1986;63:1624-33. https://doi.org/10.2527/jas1986.6351624x
  111. Harmon DL, McLeod KR. Glucose uptake and regulation by intestinal tissues: implications and whole-body energetics. J Anim Sci 2001;79:E34-49. https://doi.org/10.2527/2001.79134x
  112. Moharrery A, Larsen M, Weisbjerg MR. Starch digestion in the rumen, small intestine, and hind gut of dairy cows - a meta-analysis. Anim Feed Sci Technol 2014;192:1-14. https://doi.org/10.1016/j.anifeedsci.2014.03.001
  113. Rowe JB, Choct M, Pethick DW. Processing cereal grains for animal feeding. Aust J Agric Res 1999;50:721-36. https://doi.org/10.1071/AR98163
  114. Lozano O, Theurer CB, Alio A, et al. Net absorption and hepatic metabolism of glucose, L-lactate, and volatile fatty acids by steers fed diets containing sorghum grain processed as dry-rolled or steam-flaked at different densities. J Anim Sci 2000;78:1364-71. https://doi.org/10.2527/2000.7851364x
  115. Bindon BM. A review of genetic and non-genetic opportunities for manipulation of marbling. Aust J Exp Agric 2004;44:687-96. https://doi.org/10.1071/EA02173
  116. Wood JD, Enser M, Fisher AV, et al. Fat deposition, fatty acid composition and meat quality: a review. Meat Sci 2008;78:343-58. https://doi.org/10.1016/j.meatsci.2007.07.019
  117. Williams JE, Wagner DG, Walters LE, et al. Effect of production systems on performance, body composition and lipid and mineral profiles of soft tissue in cattle. J Anim Sci 1983;57:1020-8. https://doi.org/10.2527/jas1983.5741020x
  118. Gunter SA, Galyean ML, Malcolm-Callis KJ. Factors influencing the performance of feedlot steers limit-fed high -concentrate diets. Prof Anim Sci 1996;12:167-75.
  119. Costa ASH, Costa P, Bessa RJB, et al. Carcass fat partitioning and meat quality of Alentejana and Barrosã young bulls fed high or low maize silage diets. Meat Sci 2013;93:405-12. https://doi.org/10.1016/j.meatsci.2012.10.010
  120. Chung KY, Lunt DK, Kawachi H, Yano H, Smith SB. Lipogenesis and stearoyl-CoA desaturase gene expression and enzyme activity in adipose tissue of short- and long-fed Angus and Wagyu steers fed corn- or hay-based diets. J Anim Sci 2007;85:380-7. https://doi.org/10.2527/jas.2006-087
  121. Arnett EJ, Fluharty FL, Loerch SC, et al. Effects of forage level in feedlot finishing diets on carcass characteristics and palatability of Jersey beef. J Anim Sci 2012;90:960-72. https://doi.org/10.2527/jas.2011-4027
  122. Yamada T, Nakanishi N. Effects of the roughage/concentrate ratio on the expression of angiogenic growth factors in adipose tissue of fattening Wagyu steers. Meat Sci 2012;90:807-13. https://doi.org/10.1016/j.meatsci.2011.11.019
  123. Essen-Gustavsson B, Karlsson A, Lundstrom K, Enfalt AC. Intramuscular fat and muscle fibre contents in halothane gene free pigs fed high or low protein diets and its relation to meat quality. Meat Sci 1994;38:269-77. https://doi.org/10.1016/0309-1740(94)90116-3
  124. D'Sousa DND, Pethick DW, Dunshea FR, Pluske JP, Mullan BP. Nutritional manipulation increases intramuscular fat levels in the Longissimus muscle of female finisher pigs. Aust J Agric Res 2003;54:745-9. https://doi.org/10.1071/AR03009
  125. Li L, Zhu Y, Wang X, He Y, Cao B. Effects of different dietary energy and protein levels and sex on growth performance, carcass characteristics and meat quality of F1 Angus ${\times}$ Chinese Xiangxi yellow cattle. J Anim Sci Biotechnol 2014;5:21-32. https://doi.org/10.1186/2049-1891-5-21
  126. Marino R, Braghieri A, Albenzio M, et al. Effect of rearing system and of dietary protein level on leptin, growth, and carcass composition in young Podolian bulls. J Anim Sci 2009;87:3097-104. https://doi.org/10.2527/jas.2009-1862
  127. Kawakita Y, Abe H, Hodate K, et al. The relation between plasma leptin concentrations and carcass lipid contents in Japanese Black steers. Livest Prod Sci 2001;73:25-34. https://doi.org/10.1016/S0301-6226(01)00231-7
  128. Sato M, Hiragun A, Mitsui H. Preadipocytes possess cellular retinoid binding proteins and their differentiation is inhibited by retinoids. Biochem Biophys Res Commun 1980;95:1839-45. https://doi.org/10.1016/S0006-291X(80)80113-6
  129. Ohyama M, Matsuda K, Torii S, et al. The interaction between vitamin A and Thiazolidinedione on bovine adipocyte differentiation in primary culture. J Anim Sci 1998;76:61-5. https://doi.org/10.2527/1998.76161x
  130. Oka A, Maruo Y, Miki T, Yamasaki T, Saito T. Influence of vitamin A on the quality of beef from the Tajima strain of Japanese Black cattle. Meat Sci 1998;48:159-67. https://doi.org/10.1016/S0309-1740(97)00086-7
  131. Adachi K, Kawano H, Tsuno K, et al. Relationship between serum biochemical values and marbling scores in Japanese Black steers. J Vet Med Sci 1999;61:961-4. https://doi.org/10.1292/jvms.61.961
  132. Gorocica-Buenfil MA, Fluharty FL, Bohn T, Schwartz SJ, Loerch SC. Effect of low vitamin A diets with high-moisture or dry corn on marbling and adipose tissue fatty acid composition of beef steers. J Anim Sci 2007;85:3355-66. https://doi.org/10.2527/jas.2007-0172
  133. Pickworth CL, Loerch SC, Fluharty FL. Restriction of vitamin A and D in beef cattle finishing diets on feedlot performance and adipose accretion. J Anim Sci 2012;90:1866-78. https://doi.org/10.2527/jas.2010-3590
  134. Oka A. Vitamin A in feeding of beef cattle. Proc Jpn Soc Anim Nutr Metab 1999;43:137-44.
  135. Bedo G, Santisteban P, Aranada A. Retinoic acid regulates growth hormone gene expression. Nature 1989;339:231-4. https://doi.org/10.1038/339231a0
  136. Dalke BS, Roeder RA, Kasser TR, et al. Dose-response effects of recombinant bovine somatotropin implants on feedlot performance in steers. J Anim Sci 1992;70:2130-7. https://doi.org/10.2527/1992.7072130x
  137. Kawachi H. Micronutrients affecting adipogenesis in beef cattle. Anim Sci J 2006;77:463-71. https://doi.org/10.1111/j.1740-0929.2006.00373.x
  138. Molotkov A, Fan X, Duester G. Excessive vitamin A toxicity in mice genetically deficient in either alcohol dehydrogenase Adh1 or Adh3. Eur J Biochem 2002;269:2607-12. https://doi.org/10.1046/j.1432-1033.2002.02935.x
  139. Ziouzenkova O, Orasaun G, Sharlach M, et al. Retinaldehyde represses adipogenesis and diet-induced obesity. Nat Med 2007;13:695-702. https://doi.org/10.1038/nm1587
  140. Ward AK, McKinnon JJ, Hendrick S, Buchanan FC. The impact of vitamin A restriction and ADH1C genotype on marbling in feedlot steers. J Anim Sci 2012;90:2476-83. https://doi.org/10.2527/jas.2011-4404
  141. Ishida Y, Taniguchi H, Baba S. Possible involvement of 1 alpha,25-dihydroxyvitamin D3 in proliferation and differentiation of 3T3-L1 cells. Biochem Biophys Res Commun 1988;151:1122-7. https://doi.org/10.1016/S0006-291X(88)80482-0
  142. Hida Y, Kawada T, Kayahashi S, Ishihara T, Fushiki T. Counteraction of retimoic acid and 1,25-dihydroxyvitamin D3 on up-regulation of adipocyte differentiation with $PPAR{\gamma}$ ligand, an antidiabetic thiazolidinedione, in 3T3-Ll cells. Life Sci 1998;62:PL205-11.
  143. Ji S, Doumit ME, Hill RA. Regulation of adipogenesis and key adipogenic gene expression by 1, 25-dihydroxyvitamin D in 3T3-L1 cells. PLoS One 2015;10:e0126142. https://doi.org/10.1371/journal.pone.0126142
  144. Wang B, Yang Q, Harris CL, et al. Nutrigenomic regulation of adipose tissue development-role of retinoic acid: a review. Meat Sci 2016;120:100-6. https://doi.org/10.1016/j.meatsci.2016.04.003
  145. Smith SB, Kawachi H, Choi CB, et al. Cellular regulation of bovine intramuscular adipose tissue development and composition. J Anim Sci 2009;87:E72-82. https://doi.org/10.2527/jas.2008-1340
  146. Committee on Animal Nutrition, National Research Council. Nutrient requirements of beef cattle. 8th ed. Washington, DC, USA: The National Academies Press; 2016.
  147. Rebouche CJ. Ascorbic acid and carnitine biosynthesis. Am J Clin Nutr 1991;54:1147-52. https://doi.org/10.1093/ajcn/54.6.1147s
  148. Kawada T, Aoki N, Kamei Y, et al. Comparative investigation of vitamins and their analogues on terminal differentiation, from preadipocytes to adipocytes, of 3T3-L1 cells. Comp Biochem Physiol 1990;96:323-6. https://doi.org/10.1016/0300-9629(90)90699-S
  149. Torii S, Matsumoto K, Matsui T, Yano H. Effect of Vitamin A, C and D on glycerol-3-phosphate dehydrogenase activity of sheep preadipocytes in primary culture. Anim Sci Technol (Jpn.) 1995;66:1039-42.
  150. Ohashi H, Takizawa H, Matsui M. Effect of vitamin C on the quality of Wagyu beef. Res Bull Aichi Agric Res Center 2000;32:207-14.
  151. Pogge DJ, Hansen SL. Supplemental vitamin C improves marbling in feedlot cattle consuming high sulfur diets. J Anim Sci 2013;91:4303-14. https://doi.org/10.2527/jas.2012-5638
  152. Nathanielsz PW, Poston L, Taylor PD. In utero exposure to maternal obesity and diabetes: animal models that identify and characterize implications for future health. Obstet Gynecol Clin North Am 2007;34:201-12. https://doi.org/10.1016/j.ogc.2007.03.006
  153. Long NM, Tousley CB, Underwood KR, et al. Effects of earlyto mid-gestational undernutrition with or without protein supplementation on offspring growth, carcass characteristics, and adipocyte size in beef cattle. J Anim Sci 2012;90:197-206.
  154. Mohrhauser DA, Taylor AR, Underwood KR, et al. The influence of maternal energy status during midgestation on beef offspring carcass characteristics and meat quality. J Anim Sci 2015;95:786-93.
  155. Underwood KR, Tong JF, Price PL, et al. Nutrition during mid to late gestation affects growth, adipose tissue deposition, and tenderness in cross-bred beef steers. Meat Sci 2010;86:588-93. https://doi.org/10.1016/j.meatsci.2010.04.008
  156. Radunz AE, Fluharty FL, Relling AE, et al. Prepartum dietary energy source fed to beef cows: II. Effects on progeny postnatal growth, glucose tolerance, and carcass composition. J Anim Sci 2012;90:4962-74. https://doi.org/10.2527/jas.2012-5098
  157. Moisa SJ, Shike DW, Faulkner DB, et al. Central role of the $PPAR{\gamma}$ gene network in coordinating beef cattle intramuscular adipogenesis in response to weaning age and nutrition. Gene Regul Syst Bio 2014;8:17-32.
  158. Bell AW, Greenwood PL. Prenatal origins of postnatal variation in growth, development and productivity of ruminants. Anim Prod Sci 2016;56:1217-32. https://doi.org/10.1071/AN15408
  159. Greenwood P, Edward C, Bell A. Developmental programming and beef production. Anim Front 2017;7:38-47.
  160. National Institute of Animal Science, Rural Development Administration. Korean feeding standard for Hanwoo. Sejong, Korea: Ministry of Agriculture, Food and Rural Affairs; 2007.
  161. Esteve Rafols M. Adipose tissue: cell heterogeneity and functional diversity. Endocrinol Nutr 2014;61:100-12. https://doi.org/10.1016/j.endonu.2013.03.011
  162. Bauman DE, Mellenberger RW, Derrig RG. Fatty acid synthesis in sheep mammary tissue. J Dairy Sci 1973;56:1312-8. https://doi.org/10.3168/jds.S0022-0302(73)85352-4
  163. Pyatt NA, Berger LL. Review: Potential effects of vitamins A and D on marbling deposition in beef cattle. Prof Anim Sci 2005;21:174-81.

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