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Effects of lysine deficiency on carcass composition and activity and gene expression of lipogenic enzymes in muscles and backfat adipose tissue of fatty and lean piglets

Published online by Cambridge University Press:  07 May 2019

P. Palma-Granados ,
I. Seiquer ,
R. Benítez ,
C. Óvilo  and
R. Nieto Open the ORCID record for R. Nieto [Opens in a new window]
P. Palma-Granados
Affiliation:
Department of Physiology and Biochemistry of Animal Nutrition, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Cno.del Jueves s/n, 18100 Armilla, Granada, Spain
I. Seiquer
Affiliation:
Department of Physiology and Biochemistry of Animal Nutrition, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Cno.del Jueves s/n, 18100 Armilla, Granada, Spain
R. Benítez
Affiliation:
Department of Animal Genetics, National Institute for Agronomic Research (INIA),, Ctra. Coruña Km 7.5, 28040 Madrid, Spain
C. Óvilo
Affiliation:
Department of Animal Genetics, National Institute for Agronomic Research (INIA),, Ctra. Coruña Km 7.5, 28040 Madrid, Spain
R. Nieto*
Affiliation:
Department of Physiology and Biochemistry of Animal Nutrition, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Cno.del Jueves s/n, 18100 Armilla, Granada, Spain
*
†E-mail: rosa.nieto@eez.csic.es
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Abstract

The purpose of this study was to investigate potential mechanisms involved in fat deposition promoted by dietary lysine deficiency, particularly intramuscular fat (IMF), and differential responses between fatty and lean pigs. Carcass traits and lipogenic enzyme activities and gene expression levels in muscles and adipose tissue were investigated in Iberian (fatty) and Landrace × Large White (LDW) pigs under identical feeding level (based on body weight (BW)) and management conditions. Twenty-eight barrows of 10 kg initial BW, 14 per breed, were fed two isoproteic (200 g CP /kg DM) and isocaloric (14.7 MJ metabolizable energy/kg DM) diets with identical composition except for the lysine content (1.09% for diet adequate in lysine and 0.52% for diet deficient in lysine). At a BW of 25 kg, pigs were slaughtered. Compared with pigs fed the lysine-adequate diet, in both genotypes lysine-deficient diet led to lower carcass protein concentration, lower relative proportions of leaner components (loin, ham and shoulder; P < 0.01), and higher carcass fatty components and carcass lipid concentration (P < 0.001). Irrespective of diet, the activity and gene expression of lipogenic enzymes (fatty acid synthase (FAS), malic enzyme (ME) and glucose-6-phosphate dehydrogenase (G6PDH)) were greater in Iberian than in LDW pigs, particularly in adipose tissue where transcriptional regulators involved in the control of adipogenesis and lipogenesis were also upregulated in Iberian animals. In backfat tissue, there was a small decrease induced by or no effects of lysine-deficient diet on the activity and gene expression of lipogenic enzymes, nor in gene expression levels of upstream regulators of lipogenesis and adipogenesis. In longissimus muscle, the activity of FAS, G6PDH and ME increased with lysine deficiency in both genotypes (P < 0.01) and an upregulation of gene expression of lipogenic enzymes was specifically observed in Iberian pigs (P < 0.05 to P < 0.001). In biceps femoris muscle of lysine-deficient pigs, the activity of FAS and ME enzymes increased, ME1 gene was upregulated (added to FASN gene in the case of Iberian pigs; P < 0.01 to P < 0.001) and PPARA gene was downregulated (P < 0.05). The results show that in both fatty and lean pigs, the effect of lysine deficiency on lipid metabolism was tissue-specific, with an activation of lipogenesis in longissimus and biceps femoris muscle but no apparent stimulation in backfat adipose tissue. Suitable feeding protocols including lysine-deficient diets should be designed for each pig type in order to increase intramuscular lipids without penalizing the growth of lean carcass components.

Keywords

dietary lysinefat depotslipogenesispig genotypeRNA
Type
Research Article
Information
animal , Volume 13 , Issue 10 , October 2019 , pp. 2406 - 2418
Copyright
© The Animal Consortium 2019 

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References

AOAC. 2000. Official Methods of Analysis. 17th Edition, The Association of Official Analytical Chemists, Gaithersburg, MD, USA.Google Scholar
Barea, R, Isabel, B, Nieto, R, López-Bote, C and Aguilera, JF 2013. Evolution of the fatty acid profile of subcutaneous back-fat adipose tissue in growing Iberian and Landrace × Large White pigs. Animal 7, 688–698.CrossRefGoogle ScholarPubMed
Bazin, R and Ferre, P 2001. Assays of lipogenic enzymes. Adipose tissue protocols. In Methods in Molecular Biology (ed. Ailhaud, G), vol. 155, pp. 121–127. Springer, Totowa, NJ, USA.Google Scholar
Benítez, R, Fernández, A, Isabel, B, Núñez, Y, De Mercado, E, Gómez Izquierdo, E, García-Casco, J, López-Bote, C and Óvilo, C 2018. Modulatory effects of breed, feeding status and diet on adipogenic, lipogenic and lipolytic gene expression in growing Iberian and Duroc pigs. International Journal of Molecular Sciences 19, 22; doi: 10.3390/ijms19010022.CrossRefGoogle Scholar
Castellano, R, Perruchot, MH, Conde-Aguilera, JA, van Milgen, J, Collin, A, Tesseraud, S, Mercier, Y and Gondret, F 2015. A methionine deficient diet enhances adipose tissue lipid metabolism and alters anti-oxidant pathways in young growing pigs. PloS One, 10, e0130514.CrossRefGoogle ScholarPubMed
Conde-Aguilera, JA, Barea, R, Le Floc’h, N, Lefaucheur, L and van Milgen, J 2010. A sulfur amino acid deficiency changes the amino acid composition of body protein in piglets. Animal 4, 1349–1358.CrossRefGoogle ScholarPubMed
Conde-Aguilera, JA, Aguinaga, MA, Aguilera, JF and Nieto, R 2011. Nutrient and energy retention in weaned Iberian piglets fed diets with different protein concentrations. Journal of Animal Science 89, 754–763.CrossRefGoogle ScholarPubMed
Conde-Aguilera, JA, Cobo-Ortega, C, Mercier, Y, Tesseraud, S and van Milgen, J 2014. The amino acid composition of tissue protein is affected by the total sulfur amino acid supply in growing pigs. Animal 8, 401–409.CrossRefGoogle ScholarPubMed
Doran, O, Moule, SK, Teye, GA, Whittington, FM, Hallett, KG and Wood, JD 2006. A reduced protein diet induces stearoyl-CoA desaturase protein expression in pig muscle but not in subcutaneous adipose tissue: relationship with intramuscular lipid formation. British Journal of Nutrition 95, 609–617.CrossRefGoogle Scholar
Folch, J, Lees, M and Sloane Stanley, GH 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497–509.Google ScholarPubMed
Font-i-Furnols, M, Tous, N, Esteve-Garcia, E and Gispert, M 2012. Do all the consumers accept marbling in the same way? The relationship between eating and visual acceptability of pork with different intramuscular fat content. Meat Science 91, 448–453.CrossRefGoogle ScholarPubMed
Freire, JPB, Mourot, J, Cunha, LF, Almeida, JAA and Aumaitre, A 1998. Effect of the source of dietary fat on postweaning lipogenesis in lean and fat pigs. Annals of Nutrition and Metabolism 42, 90–95.CrossRefGoogle ScholarPubMed
Gondret, F and Lebret, B 2002. Feeding intensity and dietary protein level affect adipocyte cellularity and lipogenic capacity of muscle homogenates in growing pigs, without modification of the expression of sterol regulatory element binding protein. Journal of Animal Science 80, 3184–3193.CrossRefGoogle ScholarPubMed
Katsumata, M 2011. Promotion of intramuscular fat accumulation in porcine muscle by nutritional regulation. Animal Science Journal 82, 17–25CrossRefGoogle ScholarPubMed
Katsumata, M, Kobayashi, SI, Matsumoto, M, Tsuneishi, E and Kaji, Y 2005. Reduced intake of dietary lysine promotes accumulation of intramuscular fat in the longissimus dorsi muscles of finishing gilts. Animal Science Journal 76, 237–244.CrossRefGoogle Scholar
Kloareg, M,Noblet, J and van Milgen, J 2007. Deposition of dietary fatty acids, de novo synthesis and anatomical partitioning of fatty acids in finishing pigs. British Journal of Nutrition 97, 35–44.CrossRefGoogle ScholarPubMed
Kramer, JKG and Zhou, J 2001. Conjugated linoleic acid and octadecenoic acids: Extraction and isolation of lipids. European Journal of Lipid Science and Technologgy, 103, 594–600.3.0.CO;2-R>CrossRefGoogle Scholar
Madeira, MS, Pires, VM, Alfaia, CM, Costa, AS, Luxton, R, Doran, O, Bessa, RJB and Prates, JA 2013. Differential effects of reduced protein diets on fatty acid composition and gene expression in muscle and subcutaneous adipose tissue of Alentejana purebred and Large White× Landrace× Pietrain crossbred pigs. The British Journal of Nutrition 110, 216–229.CrossRefGoogle Scholar
Ministerio de Agricultura, Alimentación y Medio Ambiente (MAGRAMA) 2018. Producción y mercados ganaderos. Porcino. Retrieved on 15 January 2018 from http://www.mapama.gob.es/es/ganaderia/temas/produccion-y-mercados-ganaderos/sectores-ganaderos/porcino/default.aspx (in Spanish).Google Scholar
Minnich, A, Tian, N, Byan, L, and Bilder, G 2001. A potent PPARα agonist stimulates mitochondrial fatty acid β-oxidation in liver and skeletal muscle. American Journal of Physiology-Endocrinology and Metabolism 280, E270–E279.CrossRefGoogle ScholarPubMed
Morales, J, Pérez, JF, Baucells, MD, Mourot, J and Gasa, J 2002. Comparative digestibility and lipogenic activity in Landrace and Iberian finishing pigs fed ad libitum corn and corn-sorghum-acorn based diets. Livestock Production Science 77, 195–205.CrossRefGoogle Scholar
Mourot, J and Kouba, M 1999. Development of intra-and intermuscular adipose tissue in growing large white and Meishan pigs. Reproduction Nutrition Development 39, 125–132.CrossRefGoogle ScholarPubMed
Nieto, R, Lara, L, Barea, R, García-Valverde, R, Conde-Aguilera, JA and Aguilera, JF 2013. Growth of body components and carcass composition of Iberian pigs of 10 to 150 kg body weight as affected by the level of feeding and dietary protein concentration. Journal of Animal Science 91, 4197–4207.CrossRefGoogle ScholarPubMed
Nieto, R, Barea, R, Lara, L, Palma-Granados, P and Aguilera, JF 2015. Lysine requirement relative to total dietary protein for optimum performance and carcass protein deposition of Iberian piglets. Animal Feed Science and Technology 206, 48–56.CrossRefGoogle Scholar
Óvilo, C, Benítez, R, Fernández, A, Núñez, Y, Fernández, AI, Rodríguez, C, Isabel, B, Rey, AI, López-Bote, C and Silió, L 2014. Longissimus dorsi transcriptome analysis of purebred and crossbred Iberian pigs differing in muscle characteristics. BMC Genomics 15, 413; doi: 10.1186/1471-2164-15-413CrossRefGoogle ScholarPubMed
Palma-Granados, P, Haro, A, Seiquer, I, Lara, L, Aguilera, JF and Nieto, R 2017a. Similar effects of lysine deficiency in muscle biochemical characteristics of obese and lean piglets. Journal of Animal Science 95, 3025–3036.Google Scholar
Palma-Granados, P, Haro, A, Lara, L, Aguilera, JF, Nieto, R and Seiquer, I 2017b. Differences on meat colour and composition between “Landrace × Large White” and “Iberian” pigs under identical nutritional and management conditions. Animal Production Science. https://doi.org/10.1071/AN16375, Published online by CSIRO Publishing 19 July 2017.Google Scholar
Palma-Granados, P, Seiquer, I and Nieto, R 2017c. Actividad de enzimas lipogénicas en grasa dorsal y longissimus dorsi de lechones ibéricos y Landrace x Large White. (Lipogenic enzyme activity in backfat adipose tissue and longissiumus dorsi muscle of Iberian and Landrace × Large-White piglets). In XVII Jornadas sobre Producción Animal, AIDA, 30-31 May 2017, Zaragoza, Spain, pp. 249–251.Google Scholar
Pugliese, C and Sirtori, F 2012. Quality of meat and meat products produced from southern European pig breeds. Meat Science 90, 511–518.CrossRefGoogle Scholar
Rivera-Ferre, MG, Aguilera, JF and Nieto, R 2005. Muscle fractional protein synthesis is higher in Iberian than in Landrace growing pigs fed adequate or lysine-deficient diets. Journal of Nutrition 135, 469–478.CrossRefGoogle ScholarPubMed
Rivera-Ferre, MG, Aguilera, JF and Nieto, R 2006. Differences in whole-body protein turnover between Iberian and Landrace pigs fed adequate or lysine-deficient diets. Journal of Animal Science 84, 3346–3355.CrossRefGoogle ScholarPubMed
Roy, N, Lapierre, H and Bernier, JF 2000. Whole-body protein metabolism and plasma profiles of amino acids and hormones in growing barrows fed diets adequate or deficient in lysine. Canadian Journal of Animal Science 80, 585–595.CrossRefGoogle Scholar
Steibel, JP, Poletto, R, Coussens, PM and Rosa, GJM 2009. A powerful and flexible linear mixed model framework for the analysis of relative quantification RT-PCR data. Genomics 94, 146–152.CrossRefGoogle ScholarPubMed
Tous, N, Lizardo, R, Vila, B, Gispert, M, Font-i-Furnols, M and Esteve-Garcia, E. 2014. Effect of reducing dietary protein and lysine on growth performance, carcass characteristics, intramuscular fat, and fatty acid profile of finishing barrows. Journal of Animal Science 92, 129–140CrossRefGoogle Scholar
van Lunen, TA and Cole, DJA 1996. Energy-amino acid interactions in modern pig genotypes. In: Garnsworthy, PC, Wiseman, J and Haresign, W, editors. Recent Advances in Animal Nutrition. UK: Nottinghan University Press. p. 233–261.Google Scholar
Vandesompele, J, De Preter, K, Pattyn, F, Poppe, B, Van Roy, N, De Paepe, A and Speleman, F 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research0034.1–0034.12CrossRefGoogle Scholar
Wood, JD, Enser, M, Fisher, AV, Nute, GR, Sheard, PR, Richardson, RI, Hughes, SI and Whittington, FM 2008. Fat deposition, fatty acid composition and meat quality: A review. Meat Science 78, 343–358.CrossRefGoogle ScholarPubMed