An Origanum majorana Leaf Diet Influences Myogenin Gene Expression, Performance, and Carcass Characteristics in Lambs
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Experimental Design, Diets, and Lambs Management
2.2. RNA Expression Analysis
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Flynn, J.M.; Meadows, E.; Fiorotto, M.; Klein, W.H. Myogenin Regulates Exercise Capacity and Skeletal Muscle Metabolism in the Adult Mouse. PLoS ONE 2010, 5, e13535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bordbar, F.; Mohammadabadi, M.; Jensen, J.; Xu, L.; Li, J.; Zhang, L. Identification of Candidate Genes Regulating Carcass Depth and Hind Leg Circumference in Simmental Beef Cattle Using Illumina Bovine Beadchip and Next-Generation Sequencing. Animals 2022, 12, 1103. [Google Scholar] [CrossRef] [PubMed]
- Rihan, W.; Yueying, Y.; Qinghui, F.; Xia, Q.; Xige, H.; Lu, C.; Lina, S.; Tadayuki, N.; Gerelt, B. Expression of myogenic regulatory factor genes in skeletal muscle satellite cells from Wuzhumuqin sheep in vitro. Small Rumin. Res. 2020, 193, e106251. [Google Scholar] [CrossRef]
- Mohammadabadi, M.; Bordbar, F.; Jensen, J.; Du, M.; Guo, W. Key Genes Regulating Skeletal Muscle Development and Growth in Farm Animals. Animals 2021, 11, 835. [Google Scholar] [CrossRef]
- Zhao, X.H.; Li, M.Y.; Xu, S.S.; Sun, J.Y.; Liu, G.J. Expression of Myostatin (Mstn) and Myogenin (Myog) Genes in Zi and Rhine Goose and Their Correlation with Carcass Traits. Braz. J. Poult. Sci. 2019, 21, 001–006. [Google Scholar] [CrossRef]
- Faralli, H.; Dilworth, F.J. Turning on Myogenin in Muscle: A Paradigm for Understanding Mechanisms of Tissue-Specific Gene Expression. Comp. Funct. Genom. 2012, 2012, 836374. [Google Scholar] [CrossRef] [Green Version]
- Venuti, J.M.; Morris, J.H.; Vivian, J.L.; Olson, E.N.; Klein, W.H. Myogenin is required for late but not early aspects of myogenesis during mouse development. J. Cell Biol. 1995, 128, 563–576. [Google Scholar] [CrossRef] [Green Version]
- Zhao, P.; Iezzi, S.; Carver, E. Slug is a novel downstream target of MyoD. Temporal profiling in muscle regeneration. J. Biol. Chem. 2002, 277, 30091–30101. [Google Scholar] [CrossRef] [Green Version]
- Duan, Y.; Li, F.; Liu, H.; Li, Y.; Liu, Y.; Kong, X.; Zhang, Y.; Deng, D.; Tang, Y.; Feng, Z.; et al. Nutritional and regulatory roles of leucine in muscle growth and fat reduction. Front. Biosci. 2015, 20, 796–813. [Google Scholar]
- Zhang, R.; Li, R.; Zhi, L.; Xu, Y.; Lin, Y.; Chen, L. Expression profiles and associations of muscle regulatory factor (MRF) genes with growth traits in Tibetan chickens. Br. Poult. Sci. 2018, 59, 63–67. [Google Scholar] [CrossRef]
- Fuso, A.; Ferraguti, G.; Grandoni, F. Early demethylation of non-CpG, CpC-rich, elements in the myogenin 5-flanking region: A priming effect on the spreading of active demethylation? Cell Cycle 2010, 9, 3965–3976. [Google Scholar] [CrossRef]
- Palacios, D.; Summerbell, D.; Rigby, P.W.J.; Boyes, J. Interplay between DNA methylation and transcription factor availability: Implications for developmental activation of the mouse Myogenin gene. Mol. Cell. Biol. 2010, 30, 3805–3815. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Deaton, A.M.; Bird, A. CpG islands and the regulation of transcription. Gene Develop. 2011, 25, 1010–1022. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Masoudzadeh, S.H.; Mohammadabadi, M.R.; Khezri, A.; Kochuk-Yashchenko, O.A.; Kucher, D.M.; Babenko, O.I.; Bushtruk, M.V.; Tkachenko, S.V.; Stavetska, R.V.; Klopenko, N.I.; et al. Dlk1 Gene Expression in Different Tissues of Lamb. Iran. J. Appl. Anim. Sci. 2020, 10, 669–677. [Google Scholar]
- Shahsavari, M.; Mohammadabadi, M.; Khezri, A.; Asadi Fozi, M.; Babenko, O.; Kalashnyk, O.; Oleshko, V.; Tkachenko, S. Correlation between insulin-like growth factor 1 gene expression and fennel (Foeniculum vulgare) seed powder consumption in muscle of sheep. Anim. Biotechnol. 2021, 33, 1–11. [Google Scholar] [CrossRef]
- Bina, F.; Rahimi, R. Sweet marjoram: A review of ethnopharmacology, phytochemistry, and biological activities. J. Evid.-Based Complement. Altern. Med. 2016, 22, 175–185. [Google Scholar] [CrossRef]
- Aureli, P.; Costantini, A.; Zolea, S. Antimicrobial activity of some essential oils against Listeria monocytogenes. J. Food Prot. 1992, 55, 344–348. [Google Scholar] [CrossRef]
- Muller, R.F.; Berger, B.; Yegen, O. Chemical composition and fungi toxic properties to phytopathogenic fungi of essential oils of selected aromatic plants growing wild in Turkey. J. Agric. Food Chem. 1995, 43, 2262–2266. [Google Scholar] [CrossRef]
- Vera, R.R.; Chane-Ming, J. Chemical composition of the essential oil of marjoram (Origanum majorana L.) from Reunion Island. Food Chem. 1999, 66, 143–145. [Google Scholar] [CrossRef]
- El-Ashmawy, I.M.; Saleh, A.; Osama, M. Effects of marjoram volatile oil and grape seed extract on ethanol toxicity in male rats. Basic Clin. Pharmacol. Toxicol. 2007, 101, 320–327. [Google Scholar] [CrossRef]
- Zargary, A. Medicinal Plants, 7th ed.; Tehran University Press: Tehran, Iran, 2012; Volume 4. [Google Scholar]
- Bampidis, V.; Christodoulou, V.; Florou-Paneri, P.; Christaki, E.; Spais, A.B.; Chatzopoulou, P.S. Effect of dietary oregano leaves supplementation on performance and carcass characteristics of growing lambs. Anim. Feed Sci. Technol. 2005, 121, 285–295. [Google Scholar] [CrossRef]
- Khamisabadi, H.; Kafilzadeh, F.; Charaien, B. Effect of thyme (Thymus vulgaris) or peppermint (Mentha piperita) on performance, digestibility and blood metabolites of fattening Sanjabi lambs. Biharean Biol. 2016, 10, 118–122. [Google Scholar]
- Abdel-Moneim, M.A.; Hammady, G.A.; Hassanin, M.S.; El-Chaghaby, A. The effect of using marjoram extract as natural growth promoter on the performance and intestinal bacteria of broiler chickens. J. Anim. Poult. Prod. 2015, 6, 647–656. [Google Scholar] [CrossRef]
- Abdel-Wahab, A. Effect of adding marjoram powder to broiler chicks diet on performance, blood and antioxidant enzyme activity. Egypt. J. Nutr. Feed. 2019, 22, 611–625. [Google Scholar] [CrossRef] [Green Version]
- Masoudzadeh, S.H.; Mohammadabadi, M.; Khezri, A.; Stavetska, R.V.; Oleshko, V.P.; Babenko, O.I.; Yemets, Z.; Kalashnik, O.M. Effects of diets with different levels of fennel (Foeniculum vulgare) seed powder on DLK1 gene expression in brain, adipose tissue, femur muscle and rumen of Kermani lambs. Small Rumin. Res. 2020, 193, e106276. [Google Scholar] [CrossRef]
- Mohammadabadi, M.; Masoudzadeh, S.H.; Khezri, A.; Kalashnyk, O.; Stavetska, R.; Klopenko, N.; Oleshko, V.; Tkachenko, S. Fennel (Foeniculum vulgare) seed powder increases Delta-Like Non-Canonical Notch Ligand 1 gene expression in testis, liver, and humeral muscle tissues of growing lambs. Heliyon 2021, 7, e08542. [Google Scholar] [CrossRef]
- Mohammadabadi, M.R.; Shaban Jorjandy, D.; Arabpoor Raghabadi, Z.; Abareghi, F.; Sasan, H.A.; Bordbar, F. The role of fennel on DLK1 gene expression in sheep heart tissue. Agric. Biotechnol. J. 2022, 14, 155–170. [Google Scholar]
- AOAC. Official Methods of Analysis, 17th ed.; Association of Official Analytical Chemists: Arlington, VA, USA, 2000. [Google Scholar]
- Van Soest, P.J.; Robertson, J.B.; Lewis, B.A. Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. J. Dairy Sci. 1991, 74, 3583–3597. [Google Scholar] [CrossRef]
- National Research Council. Nutrient Requirements of Small Ruminants: Sheep, Goats, Cervids, and New World Camelids; The National Academies Press: Washington, DC, USA, 2007. [Google Scholar] [CrossRef]
- Chay-Canul, A.J.; Espinoza-Hernández, J.C.; Ayala-Burgos, A.J.; Magaña-Monforte, J.G.; Aguilar-Perez, C.F.; Chizzotti, M.L.; Tedeschi, L.O.; Ku-Vera, J.C. Relationship of empty body weight with shrunken body weight and carcass weights in adult Pelibuey ewes at different physiological states. Small Rumin. Res. 2014, 14, 10–14. [Google Scholar] [CrossRef]
- Herbster, C.J.L.; Silva, L.P.; Marcondes, M.I.; García, I.F.F.; Oliveira, R.L.; Cabral, L.S.; Souza, J.G.; Pereira, E.S. Weight adjustment equation for hair sheep raised in warm conditions. Animal 2020, 14, 1718–1723. [Google Scholar] [CrossRef]
- Kashan, N.E.J.; Manafi Azar, G.H.; Afzalzadeh, A.; Salehi, A. Growth performance and carcass quality of fattening lambs from fat-tailed and tailed sheep breeds. Small Rumin. Res. 2005, 60, 267–271. [Google Scholar] [CrossRef]
- Pfaffl, M.W.; Horgan, G.W.; Dempfle, L. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in Real-Time PCR. Nucleic Acids Res. 2002, 30, e36. [Google Scholar] [CrossRef] [PubMed]
- SAS Institute Inc. SAS/STAT® 9.2 User’s Guide; SAS Institute Inc.: Cary, NC, USA, 2008. [Google Scholar]
- Song, J.W.; Gao, G.; Wu, W.; Mu, Y.T.; Li, Y.; Sun, Y. Study on expression of MyoG mRNA and histological characteristics of goose muscle fiber. J. Jilin Agric. Uni. 2013, 35, 89–93. [Google Scholar]
- Zhang, G.X.; Tang, Y.; Zhang, T.; Wang, J.Y.; Wang, Y.J. Expression profiles and association analysis with growth traits of the MyoG and Myf5 genes in the Jinghai yellow chicken. Mol. Biol. Rep. 2014, 41, 7331–7338. [Google Scholar]
- Lv, X.Y.; Sun, W.; Su, R.; Li, D.; Wang, Q.Z.; Musa, H.H.; Chen, L.; Zhang, Y.F.; Wu, W.Z. Correlation between sheep YAP1 temporal and spatial expression trends and MSTN and MyoG gene expression. Genet. Mol. Res. 2015, 14, e4381. [Google Scholar] [CrossRef] [PubMed]
- Forutan, K.; AminAfshar, M.; Zargari, K.; Chamaniand, M.; Emam Jome Kashan, N. The Expression of Myogenin and Myostatin Genes in Baluchi Sheep. Iran. J. Appl. Anim. Sci. 2016, 6, 873–878. [Google Scholar]
- Kuang, L.; Xie, X.; Zhang, X.Y.; Zheng, Y.C. Expression profiles of myostatin, myogenin, and Myosin heavy chain in skeletal muscles of two rabbit breeds different in growth rate. Anim. Biotechnol. 2014, 25, 223–233. [Google Scholar] [CrossRef]
- Cornelison, D.D.W.; Wold, B.J. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 1997, 191, 270–283. [Google Scholar] [CrossRef] [Green Version]
- Akizawa, Y.; Kanno, H.; Kawamichi, Y.; Matsuda, Y.; Ohta, H.; Fujii, H. Enhanced expression of myogenic differentiation factors and skeletal muscle proteins in human amnion-derived cells via the forced expression of myod1. Brain Dev. 2013, 35, 349–355. [Google Scholar] [CrossRef]
- Lee, E.J.; Malik, A.; Pokharel, S.; Ahmad, S.; Mir, B.A.; Cho, K.H.; Kim, J.; Kong, J.C.; Lee, D.M.; Chung, K.Y.; et al. Identification of genes differentially expressed in myogenin knock-down bovine muscle satellite cells during differentiation through RNA sequencing analysis. PLoS ONE 2014, 9, e922447. [Google Scholar] [CrossRef]
- Lahr, D.A.; Otterby, D.E.; Johnson, D.G.; Linn, J.G.; Lundquist, R.G. Effects of moisture content of complete diets on feed intake and milk production by cows. J. Dairy Sci. 1983, 66, 1891–1900. [Google Scholar] [CrossRef] [PubMed]
- Mertens, D.R. Impact of NDF content and digestibility on dairy cow performance. WCDS Adv. Dairy Technol. 2009, 21, 191–201. [Google Scholar]
- Kolling, G.J.; Panazzolo, D.M.; Gabbi, A.M.; Stumpf, M.T.; Passos, M.B.D.; Cruz, E.A.D.; Fischer, V. Oregano extract added into the diet of dairy heifers changes feeding behavior and concentrate intake. Sci. World J. 2016, 2016, 8917817. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaves, A.V.; Stanford, K.; Gibson, L.L.; McAllister, T.A.; Benchaar, C. Effects of carvacrol and cinnamaldehyde on intake, rumen fermentation, growth performance, and carcass characteristics of growing lambs. Anim. Feed Sci. Technol. 2008, 145, 396–408. [Google Scholar] [CrossRef]
- Hajalizadeh, Z.; Dayani, O.; Khezri, A.; Tahmasbi, R.; Mohammadabadi, M.R. The effect of adding fennel (Foeniculum vulgare) seed powder to the diet of fattening lambs on performance, carcass characteristics and liver enzymes. Small Rumin. Res. 2019, 175, 72–77. [Google Scholar] [CrossRef]
- Smeti, S.; Hajji, H.; Mekki, I.; Mahouachi, M.; Atti, N. Effects of dose and administration form of rosemary essential oils on meat quality and fatty acid profile of lamb. Small Rumin. Res. 2018, 158, 62–68. [Google Scholar] [CrossRef]
- Tekippe, J.A.; Hristov, A.N.; Heyler, K.S.; Cassidy, T.W.; Zheljazkov, V.D.; Ferreira, J.F.; Karnati, K.; Varga, G.A. Rumen fermentation and production effects of Origanum vulgare L. in lactating dairy cows. J. Dairy Sci. 2011, 94, 5065–5079. [Google Scholar] [CrossRef]
- Mohiti-Asli, M.; Hosseini, S.A.; Meymandipur, A.; Mahdavi, A. Phytogenics in Animal Nutrition; Animal Sciences Research Institute Press: Karaj, Iran, 2011; pp. 20–40. [Google Scholar]
- Safari, H.; Mohiti Asli, M.; Mohammadpour, F. Effect of purslane powder on performance, quality and oxidative stability of meat and some blood metabolites in fattening lambs. Anim. Prod. Res. 2016, 5, 15–26. [Google Scholar]
- Cherif, M.; Salem, H.; Abidi, S. Effect of the addition of Nigella sativa seeds to low or high concentrate diets on intake, digestion, blood metabolites, growth and carcass traits of Barbarine lamb. Small Rumin. Res. 2017, 158, 1–8. [Google Scholar] [CrossRef]
- Somasiri, S.C.; Kenyon, P.R.; Kemp, P.D.; Morel, P.C.H.; Morris, S.T. Growth performance and carcass characteristics of lambs grazing forage mixes inclusive of plantain (Plantago lanceolata L.) and chicory (Cichorium intybus L.). Small Rumin. Res. 2015, 127, 20–27. [Google Scholar] [CrossRef]
- Fazaeli, H.; Shafeyee-Varzaneh, H.; Kalvandi, R.; Solgi, M.; Farahpour, A.; Bashiri-Safa, J. Effect of powder and root extracted of Foeniculum vulgare on the performance of fattening Mehraban lambs. J. Rum. Res. 2018, 6, 69–84. [Google Scholar]
- Yagoubi, Y.; Hajji, H.; Smeti, S.; Mahouachi, M.; Kamoun, M.; Atti, N. Growth performance, carcass and non-carcass traits and meat quality of Barbarine lambs fed rosemary distillation residues. Animals 2018, 12, 2407–2414. [Google Scholar]
- Karami, M.; Alimon, A.R.; Yong, M.G.; Awis, Q.S.; Ivan, M. Effects of dietary herbal antioxidants supplemented on feedlot growth performance and carcass composition of male goats. Am. J. Anim. Vet. Sci. 2010, 5, 33–39. [Google Scholar] [CrossRef] [Green Version]
- Dudko, P.; Junkuszew, A.; Bojar, W.; Milerski, M.; Szczepaniak, K.; Le Scouarnec, J.; Schmidová, J.; Tomczuk, K.; Grzybek, M. Effect of dietary supplementation with preparation comprising the blend of essential oil from Origanum vulgare (lamiaceae) and Citrus spp. (citraceae) on coccidia invasion and lamb growth. Ital. J. Anim. Sci. 2018, 17, 57–65. [Google Scholar] [CrossRef]
- Wang, H.X.; Schreurs, N.M.; Corner-Thomas, R.A.; Ekanayake, W.; Cranston, L.M.; Morris, S.T.; Kenyon, P.R. Effects of early weaning onto herb-clover mixes on lamb carcass characteristics. N. Z. J. Anim. Sci. Prod. 2018, 78, 189–193. [Google Scholar]
Ingredients | Diets * | |
---|---|---|
MOL0 | MOL4 | |
Origanum majorana leaf | 0 | 4 |
Chopped alfalfa hay | 30 | 30 |
Ground barley grain | 28 | 28 |
Chopped wheat straw | 10 | 10 |
Wheat bran | 13 | 13 |
Ground corn grain | 9 | 5 |
Soybean meal | 8 | 8 |
Vitamins (A, D and E) ** | 0.6 | 0.6 |
Limestone | 0.3 | 0.3 |
Sodium bicarbonate | 0.5 | 0.5 |
Trace-mineralized salt *** | 0.6 | 0.6 |
Chemical composition | ||
Organic matter (g/kg DM) | 926.1 | 922.5 |
Dry matter (g/kg) | 899.6 | 900.6 |
Crude protein (g/kg DM) | 139.8 | 140 |
Metabolizable energy (Mcal/Kg DM) | 2.52 | 2.52 |
NDFom (g/kg DM) | 393.3 | 413.3 |
ADFom (g/kg DM) | 240.2 | 240.2 |
Ether extract (g/kg DM) | 22.5 | 24.3 |
Parameters | MOL0 | MOL4 | SEM | p Value |
---|---|---|---|---|
Initial weight (kg) | 26.02 | 26.00 | 0.33 | 0.98 |
Final weight (kg) | 42.55 | 46.05 | 0.74 | 0.003 |
Average daily gain (g) | 210 | 270 | 10.96 | 0.007 |
Dry matter intake (kg/day) | 1.45 | 1.42 | 0.02 | 0.23 |
Hot carcass weight (kg) | 20.38 | 22.70 | 0.38 | 0.02 |
Cold carcass weight (kg) | 19.65 | 22.29 | 0.67 | 0.02 |
Feed conversion ratio * (g body weight gain/kg dry matter intake) | 145 | 190 | 0.26 | 0.001 |
Empty body weight (kg) | 39.10 | 42.77 | 0.64 | 0.004 |
Hot dressing percentage | 47.89 | 49.29 | 0.63 | 0.24 |
Cold dressing percentage | 46.65 | 48.40 | 0.56 | 0.15 |
Shoulder (kg)—percentage of right half carcass | 0.97 | 1.52 | 0.12 | 0.02 |
Loin (kg)—percentage of right half carcass | 1.78 | 1.94 | 0.05 | 0.02 |
Leg (kg)—percentage of right half carcass | 2.66 | 2.95 | 0.07 | 0.004 |
Lean meat (kg) | 13.74 | 15.75 | 0.51 | 0.01 |
Lean/bone ratio | 4.20 | 4.32 | 0.30 | 0.001 |
Tissue | Relative Expression of Myogenin | SEM | p Value | |
---|---|---|---|---|
MOL0 | MOL4 | |||
Loin | 1 | 3.5 * | 0.13 | 0.03 |
Leg | 1 | 3.9 * | 0.14 | 0.01 |
Shoulder | 1 | 3.6 * | 0.12 | 0.02 |
Source of Variation | df | Mean Square |
---|---|---|
Tissue | 2 | 0.065 ** |
MOL | 1 | 32.000 ** |
Tissue × MOL | 2 | 0.065 ** |
Coeff Var | 3.03 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Safaei, S.M.H.; Dadpasand, M.; Mohammadabadi, M.; Atashi, H.; Stavetska, R.; Klopenko, N.; Kalashnyk, O. An Origanum majorana Leaf Diet Influences Myogenin Gene Expression, Performance, and Carcass Characteristics in Lambs. Animals 2023, 13, 14. https://doi.org/10.3390/ani13010014
Safaei SMH, Dadpasand M, Mohammadabadi M, Atashi H, Stavetska R, Klopenko N, Kalashnyk O. An Origanum majorana Leaf Diet Influences Myogenin Gene Expression, Performance, and Carcass Characteristics in Lambs. Animals. 2023; 13(1):14. https://doi.org/10.3390/ani13010014
Chicago/Turabian StyleSafaei, Seyed Mohammad Hadi, Mohammad Dadpasand, Mohammadreza Mohammadabadi, Hadi Atashi, Ruslana Stavetska, Nataliia Klopenko, and Oleksandr Kalashnyk. 2023. "An Origanum majorana Leaf Diet Influences Myogenin Gene Expression, Performance, and Carcass Characteristics in Lambs" Animals 13, no. 1: 14. https://doi.org/10.3390/ani13010014