Relationships between the activity of respiratory-chain complexes in pre- (biopsy) or post-slaughter muscle samples and feed efficiency in random-bred Ghezel lambs
M. J. Zamiri A D , R. Mehrabi B , G. R. Kavoosi C and H. Rajaei Sharifabadi BA Department of Animal Science, College of Agriculture, Shiraz University, Shiraz, 71441-65186, Iran.
B Former Post-Graduate Students, Department of Animal Science, College of Agriculture, Shiraz University, Shiraz, 71441-65186, Iran.
C Institute of Biotechnology, College of Agriculture, Shiraz University, 71441-65186, Iran.
D Corresponding author. Email: zamiri@shirazu.ac.ir; mjzamiri@gmail.com
Animal Production Science 57(8) 1674-1681 https://doi.org/10.1071/AN15184
Submitted: 13 April 2015 Accepted: 26 April 2016 Published: 5 July 2016
Abstract
The present study was conducted to determine the relationship between the activity of mitochondrial respiratory chain complexes in pre- and post-slaughter muscle samples and residual feed intake (RFI) in Ghezel male lambs born as a result of random mating. The study was based on the hypothesis that random-bred lambs with lower feed (or higher) RFI have lower (or higher) respiratory chain-complex activity in muscle samples. Lambs (n = 30) were fed a diet consisting of 70% concentrate and 30% alfalfa hay during a 70-day period. Individual feed intake and average daily gain were recorded to calculate the RFI, feed-conversion ratio (FCR) and adjusted FCR (aFCR). On the basis of these calculations, the lambs were classified into low and high groups for RFI, with FCR and aFCR (n = 22) being one standard deviation above or below the means; this was corroborated by Student’s t-test (P < 0.01). At the end of the experiment, a 10-g biopsy sample was taken from the posterior side of the left femoral biceps. After 24 h, the lambs were slaughtered, and a sample from the posterior side of the right femoral biceps was dissected for determination of mitochondrial protein and respiratory chain-complex activities (Complexes I–V). The RFI was not correlated with the metabolic bodyweight and average daily gain, but was positively correlated (r = 0.56) with the average daily feed intake (P < 0.01); mean daily feed intake in the low-RFI group was 200 g less than that in the high-RFI group. The FCR and aFCR were not significantly (P > 0.05) correlated with average daily feed intake (r = 0.39 and r = 0.36 respectively), but showed a negative correlation (P < 0.01) with average daily gain (r = –0.73 and r = –0.76 respectively). Although very high negative correlations were recorded between the activities of all five respiratory-chain complexes and RFI in muscle samples obtained before (–0.91 to –0.97) and after (–0.92 to –0.97) slaughter, Complexes I and V showed small negative correlations (–0.40) with FCR or aFCR (P < 0.05). Enzyme activities of the respiratory-chain Complexes I, III and V were not significantly different between the pre- and post-slaughter biopsy samples; however, the enzyme activities of respiratory-chain Complexes II and IV were slightly higher in post-slaughter samples (P < 0.01). These results suggested that it may be possible to use the enzymatic activity of respiratory-chain complexes in muscle biopsy samples for screening of lambs for RFI, providing a useful procedure for genetic selection of lambs for this component of feed efficiency. These encouraging results need to be verified in further experiments using other sheep breeds and a larger number of lambs.
Additional keywords: feed efficiency, mitochondrial enzymes, residual feed intake.
References
Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290, 457–465.| Sequence and organization of the human mitochondrial genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlt1OlsL8%3D&md5=f53ecb53ee006d1ecdc6c421d133f26bCAS | 7219534PubMed |
Arthur PF, Archer JA, Johnson DJ, Herd RM, Richardson EC, Parnell PF (2001) Genetics and phenotypic variance and covariance components for feed intake, feed efficiency and other post-weaning traits in Angus cattle. Journal of Animal Science 79, 2805–2811.
Basarab JA, Price MA, Aalhus JL, Okine EK, Snelling WM, Lyle KL (2003) Residual feed intake and body composition in young growing steers. Canadian Journal of Animal Science 83, 189–204.
| Residual feed intake and body composition in young growing steers.Crossref | GoogleScholarGoogle Scholar |
Bishop MD, Davis ME, Harvey WR, Wilson GR, Van Stavern BD (1991) Divergent selection for post weaning feed conversion in Angus beef cattle: I. Mean comparisons. Journal of Animal Science 69, 43–48.
Bottje WG, Carstens GE (2009) Association of mitochondrial function and feed efficiency in poultry and livestock species. Journal of Animal Science 87, E48–E63.
| Association of mitochondrial function and feed efficiency in poultry and livestock species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3mtVWksQ%3D%3D&md5=5cdb3893e783c67652c042898e740474CAS | 19028862PubMed |
Bottje WG, Carstens GE (2012) Variation in metabolism: biological efficiency of energy production and utilization that affects feed efficiency. In ‘Feed efficiency in the beef industry’. (Ed. RA Hill) pp. 250–273. (Wiley-Blackwell: Oxford, UK)
Bottje WG, Kong BW (2013) Feed efficiency: mitochondrial function to global gene expression. Journal of Animal Science 91, 1582–1593.
| Feed efficiency: mitochondrial function to global gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntFWrtLg%3D&md5=03b52fa0f7a57e22f47ce03283268559CAS |
Bottje WG, Tang Z, Iqbal M, Cawthon D, Okimoto R, Wing T, Cooper M (2002) Association of mitochondrial function with feed efficiency within a single genetic line of male broilers. Poultry Science 81, 546–555.
| Association of mitochondrial function with feed efficiency within a single genetic line of male broilers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383ltVyqsw%3D%3D&md5=65ca2f2a162285201723d07866bc5e31CAS |
Bottje WB, Pumford NR, Ojano-Dirain C, Iqbal M, Lassiter K (2006) Feed efficiency and mitochondrial function. Poultry Science 85, 8–14.
| Feed efficiency and mitochondrial function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVKktg%3D%3D&md5=e133ec900effd30d32980cd1d91e6d56CAS |
Bouhours-Nouet N, May-Panloup P, Coutant R, de Casson FB, Descamps Ph, Douay O, Reynier P, Ritz P, Malthiery Y, Simard G (2005) Maternal smoking is associated with mitochondrial DNA depletion and respiratory chain complex III deficiency in placenta. American Journal of Physiology. Endocrinology and Metabolism 288, E171–E177.
| Maternal smoking is associated with mitochondrial DNA depletion and respiratory chain complex III deficiency in placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGju74%3D&md5=3e9a7b166462a3031afb437234859299CAS | 15585597PubMed |
Castro JA, Picornell A, Ramon M (1998) Mitochondrial DNA: a tool for population genetic studies. International Microbiology 1, 327–332.
Davis ME, Wick MP, Maquivar MG (2012) Hormonal regulation of feed efficiency. In ‘Feed efficiency in the beef industry’. (Ed. RA Hill) pp. 225–250. (Wiley-Blackwell: Oxford, UK)
Herd RM, Arthur PF (2009) Physiological basis for residual feed intake. Journal of Animal Science 87, E64–E71.
| Physiological basis for residual feed intake.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3mtVWksA%3D%3D&md5=dbc3e7f231e26b74ef480ad84dbebce5CAS | 19028857PubMed |
Herd RM, Bishop SC (2000) Genetic variation in residual feed intake and its association with other production traits in British Hereford cattle. Livestock Production Science 63, 111–119.
| Genetic variation in residual feed intake and its association with other production traits in British Hereford cattle.Crossref | GoogleScholarGoogle Scholar |
Iqbal M, Pumford NR, Tang ZX, Lassiter K, Wing T, Cooper M, Bottje WG (2004) Low feed efficient broilers within a single genetic line exhibit greater oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity. Poultry Science 83, 474–484.
| Low feed efficient broilers within a single genetic line exhibit greater oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c7ls1agtw%3D%3D&md5=9863062b513f605da3b338ded67d9fd5CAS | 15049502PubMed |
Knott SA, Cummins LJ, Dunshea FR, Leury BJ (2008) The use of different models for the estimation of residual feed intake (RFI) as a measure of feed efficiency in meat sheep. Animal Feed Science and Technology 143, 242–255.
| The use of different models for the estimation of residual feed intake (RFI) as a measure of feed efficiency in meat sheep.Crossref | GoogleScholarGoogle Scholar |
Koch RM, Swiger LA, Chambers D, Gregory KE (1963) Efficiency of feed use in beef cattle. Journal of Animal Science 22, 486–494.
Kolath WH (2006) The relationship between mitochondria and residual feed intake in feedlot cattle. PhD Thesis, University of Missouri-Columbia, Columbia, MO.
Kolath WH, Kerley MS, Golden JW, Keister DH (2006) The relationship between mitochondrial function and residual feed intake in steers. Journal of Animal Science 84, 861–865.
Lawrence CB, Davies NT (1986) A novel, simple and rapid method for the isolation of mitochondria which exhibit respiratory control from rat small intestinal mucosa. Biochimica et Biophysica Acta (BBA). Bioenergetics 848, 35–40.
| A novel, simple and rapid method for the isolation of mitochondria which exhibit respiratory control from rat small intestinal mucosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XosVymuw%3D%3D&md5=a30ea38ab43aa7336a86e5f4f6ba129bCAS |
Litten JC, Corson AM, Hall AD, Clarke L (2004) The relationship between growth performance, feed intake, endocrine profile and carcass quality of different maternal and paternal lines of pigs. Livestock Production Science 89, 33–39.
| The relationship between growth performance, feed intake, endocrine profile and carcass quality of different maternal and paternal lines of pigs.Crossref | GoogleScholarGoogle Scholar |
Ojano-Dirain C, Iqbal M, Cawthon D, Swonger S, Wing T, Cooper M, Bottje WG (2004) Determination of mitochondrial function and site-specific defects in electron transport in duodenal mitochondria in broilers with low and high feed efficiency. Poultry Science 83, 1394–1403.
| Determination of mitochondrial function and site-specific defects in electron transport in duodenal mitochondria in broilers with low and high feed efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFGlsrc%3D&md5=93228ef6849d15ce8ee61cb26a6d12deCAS | 15339016PubMed |
Ojano-Dirain C, Iqbal M, Wing T, Cooper M, Bottje WG (2005) Glutathione and respiratory chain complex activity in duodenal mitochondria of broilers with low and high feed efficiency. Poultry Science 84, 782–788.
| Glutathione and respiratory chain complex activity in duodenal mitochondria of broilers with low and high feed efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktF2iuro%3D&md5=758f45d05dbd8b2e8da46617483d03eaCAS | 15913191PubMed |
Rajaei Sharifabadi H, Zamiri MJ, Rowghani E, Bottje WG (2012) Relationship between the activity of mitochondrial respiratory chain complexes and feed efficiency in fat-tailed Ghezel lambs. Journal of Animal Science 90, 1807–1815.
| Relationship between the activity of mitochondrial respiratory chain complexes and feed efficiency in fat-tailed Ghezel lambs.Crossref | GoogleScholarGoogle Scholar |
Redden RR, Surber LMM, Roeder BL, Nichols BM, Paterson JA, Kott RW (2011) Residual feed efficiency established in a post-weaning growth test may not result in more efficient ewes on the range. Small Ruminant Research 96, 155–159.
| Residual feed efficiency established in a post-weaning growth test may not result in more efficient ewes on the range.Crossref | GoogleScholarGoogle Scholar |
Richardson EC, Herd RM, Arthur PF, Wright J, Xu G, Dibley K, Oddy VH (1996) Possible physiological indicators for net feed conversion efficiency in beef cattle. Proceedings of the Australian Society of Animal Production 21, 103–106.
Robinson DL, Oddy VH (2004) Genetic parameters for feed efficiency, fatness, muscle area and feeding behaviour of feedlot finished beef cattle. Livestock Production Science 90, 255–270.
| Genetic parameters for feed efficiency, fatness, muscle area and feeding behaviour of feedlot finished beef cattle.Crossref | GoogleScholarGoogle Scholar |
Sandelin B (2005) Association of mitochondrial biochemistry and electron transport chain protein expression with feed efficiency in Angus cattle. PhD Thesis, University of Arkansas, Fayetteville, AR.
Smith SN (2009) Residual feed intake of Angus cattle divergently selected for feed conversion ratio. MSc Thesis, Ohio State University, Columbus, OH.
Smith SN, Davis ME, Loerch SC (2010) Residual feed intake of Angus beef cattle divergently selected for feed conversion ratio. Livestock Science 132, 41–47.
| Residual feed intake of Angus beef cattle divergently selected for feed conversion ratio.Crossref | GoogleScholarGoogle Scholar |
Zhao X, Li N, Guo W, Hu X, Liu Z, Gong G, Wang A, Feng J, Wu C (2004) Further evidence for paternal inheritance of mitochondrial DNA in the sheep (Ovis aries). Heredity 93, 399–403.
| Further evidence for paternal inheritance of mitochondrial DNA in the sheep (Ovis aries).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVKms7w%3D&md5=703e21651cf464993b904b158c12f778CAS | 15266295PubMed |