Review Article of International Journal of Animal Research
A Review on the Genetic Basis of Growth and Prolificacy Traits in Sheep
Abiye Shenkut Abebe1* and Mengistie Taye2
1Department of Animal Science, Debre Tabor University, P.O.Box 272, Ethiopia
2Department of Animal Production and Technology, Bahir Dar University, P.O.Box, 5501, Ethiopia
The performance of an animal for a particular trait is the result of its genetic merit and the effects of the environment where it exists. To set up genetic improvement in sheep, the genetic component attributed to the trait of interest need to be defined. The aim of this review was to describe major candidate genes influencing growth traits and prolificacy in sheep. Although growth and prolificacy are quantitative traits and are expected to be influenced by many genes with individual genes contributing small effects, there are major genes that have been identified with significant influence on growth and prolificacy. The CLPG, GDF8 and CAST genes are some of the major genes that have strong influence on sheep growth and carcass quality. The CLPG mutation can cause pronounced effect in the muscle found in the hindquarter and is responsible for the muscular hypertrophy phenotype in sheep. The GDF8 gene also play important role in increasing muscle depth due to mutation in the regulatory region and coding sequences. The CAST gene is an endogenous and specific inhibitor of calpain enzyme and thereby regulates the rate and extent of muscle tenderization following slaughtering. For prolificacy, BMP15, GDF9 and BMPR1B have been shown to exert significant influence on ovulation rate and litter size in various sheep breeds in the world. Both of the three genes are member of the TGF-beta family protein that encode protein product responsible for growth, differentiation and proliferation of ovarian follicles. The mechanism of action for such major genes are associated with the existence of mutation in the coding sequence resulting amino acid change as well as in the regulatory region that vary the expression level and inheritance of the genes. Up to now, better attempts have been made to describe the genetic basis of growth and prolificacy in sheep. However, more works are needed to characterize other genes influencing these traits. More importantly, making use of the identified genes in sheep breeding program through marker assisted and genomic selection should receive due attentions.
Keywords: Booroola gene, Callipyge gene, Growth trait, Myostatin gene, Sheep prolificacy
How to cite this article:
Abiye Shenkut Abebe and Mengistie Taye, A Review on the Genetic Basis of Growth and Prolificacy Traits in Sheep. International Journal of Animal Research, 2019; 4:25.
1. Falconer Douglas Scott. Introduction to quantitative genetics. Third eds. Longman Scientific and Technical, USA; 1989, P.438.
2. Souza CJ, MacDougall C, Campbell BK, McNeilly AS, Baird DT. The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1B (BMPR1B) gene. Journal Endocrinology, 2001; 169(2):1-6.
3. Freking BA, Murphy SK, Wylie AA, Rhodes SJ, Keele JW, Leymaster KA, Jirtle RL, Smith TP. Identification of the single base change causing the Callipyge muscle hypertrophy phenotype, the only known example of polar over dominance in mammals. Genome Research, 2002; 12:1496–1506.
4. Zhang L, Ma X, Xuan J, Wang H, Yuan Z, Wu M, et al. Identification of MEF2B and TRHDE Gene Polymorphisms Related to Growth Traits in a New Ujumqin Sheep Population. PLoS ONE, 2016; 11(7): doi:10.1371/journal.pone.0159504.
5. Zhi-Liang Hu, Carissa AP, James MR. Developmental progress and current status of the Animal QTLdb. Nucleic Acids Research, 2016; 44 (D1): D827-D833.
6. Zhi-Liang Hu, Carissa AP, James MR. Building a livestock genetic and genomic information knowledgebase through integrative developments of Animal QTLdb and CorrDB. Nucleic Acids Research, 2019; 47(1):701–710. doi.org/10.1093/nar/gky1084.
7. Nanekarani S, Goodarzia M. Polymorphism of Candidate Genes for Meat Production in Lori Sheep. IERI Procedia, 2014; 8:18 – 23.
8. Gholizadeh M, Rahimi-Mianji G, Nejati-Javaremi A. Genome wide association study of body weight traits in Baluchi sheep. Journal of Genetics, 2015; 94(1):143-146.
9. Abdoli R, Zamani P, Deljou A, Rezvan H. Association of BMPR-1B and GDF9 genes polymorphisms and secondary protein structure changes with reproduction traits in Mehraban ewes. Genes, 2013; 524:296-303.
10. Othman EO, Esraa AB, Eman RM. Genetic characterization of Myostatin and Callipyge genes in Egyptian small ruminant breeds. Biotechnology, 2016; 15:44-55.
11. Cockett, NE, Jackson SP, Shay TL, Nielsen D, Moore SS, Steele M R, Barendse W, Green R D, Georges M. Chromosomal location of the Callipyge gene in sheep (Ovis aries) using Bovine DNA markers. Proc. Natl. Acad. Sci. 1994; 91:3019 -3023.
12. Charlier C, Segers K, Karim L, Shay T, Gyapay G, Cockett N, Georges M. The Callipyge mutation enhances the expression of co-regulated imprinted genes in cis without affecting their imprinting status. Nature Genetics, 2001; 27(4):367-269.
13. Cockett, NE, Smit MA, Bidwell CA, Segers K, Hadfield TL, Snowder GD, Georges M, Charlier C. The Callipyge mutation and other genes that affect muscle hypertrophy in sheep. Genetic Selection Evolution, 2005; 37(1): S65-S81.
14. Cockett NE, Berghams S, Beckers MC, Shay TL, Jackson SP, Snowder GD, Georges M. The Callipyge gene of sheep. Animal Biotechnology, 1997; 8(1):23-30.
15. Jackson SP, Miller MF, Green RD. Phenotypic characterization of Rambouillet sheep expressing the Callipyge gene: III. Muscle weights and muscle weight distribution, Journal of Animal Science, 1997; 75:133–138.
16. Qanbari S, Osfoori R, Eskandarinasab MP. A preliminary study of marker data applicability in gene introgression program for Afshari sheep breed. Biotechnology, 2007; 6(4): 513-519.
17. Gabor M, Trakovicka A, Miluchova M. Analysis of polymorphis of CAST gene and CLPG gene in sheep by PCR-RFLP method. Zootehnie si Biotehnologii, 2009; 42(2):470-476.
18. Marcq, F, Elsen, JM, El Barkouki, S, et al. Investigating the role of Myostatin in the determinism of double muscling characterizing Belgian Texel sheep. Animal Genetics, 1998; 29:52.
19. Kambadur, R, Sharma, M, Smith, TP, Bass, JJ. Mutations in Myostatin (GDF8) in double muscled Belgian Blue and Piedmontese cattle. Genome Research, 1997; 7:910–916.
20. Wiener P, Smith JA, Lewis AM, Wooliams JA, Williams JL. Muscle related traits in cattle: the role of Myostatin gene in south Devon breed. Genetic Election Evolution, 2002; 24:221-32.
21. Johnson PL, McEwan JC, Dodds KG, Purchas RW, Blair HT. A directed search in the region of GDF8 for quantitative trait loci affecting carcass traits in Texel sheep. Journal of Animal Science, 2005; 83:1988–2000.
22. Hadjipavlou, G, Matika, O, Clop, A, Bishop, SC. Two single nucleotide polymorphism in the Myostatin (GDF8) gene have significant association with muscle depth of commercial Charolaise sheep. Animal Genetics, 2008; 39:346–353.
23. Hopkins DL, Taylor RG. Post-mortem Muscle Proteolysis and Meat Tenderness In: MFW Te Pas, ME Everts, and HP Haagsman (Eds.), Muscle Development of Livestock Animals: Physiology, Genetics and Meat Quality. CAB International, UK, 2004; pp. 363-381.
24. Casas E, White SN, Wheeler TL, Shackelford SD, Koohmaraie M, Riley DG, Chase Jr.CC Johnson DD, Smith TP. Effects of calpastatin and µ-calpain markers in beef cattle on tenderness traits. Journal of Animal Science, 2006; 84:520-525.
25. Azari M A, Dehnavi E, Yousefi S, Shahmohamadi L. Polymorphism of Calpastatin, Calpain and myostatin genes in native Dalagh sheep in Iran. Slovak Journal of Animal Science, 2012; 45(1): 1-6.
26. Zhou, H, Hickford, JGH, Gong, H. Polymorphism of the ovine calpastatin gene. Mol. Cell. Probes, 2007; 21:242–244.
27. Chung HY, Davis M. PCR-RFLP of the ovine calpastatin gene and its association with growth. Asian J. Anim. Vet. Adv., 2012; 7(8):641–652.
28. Mohsen Aali, Mohammad Moradi-Shahrbabak, Hosein Moradi-Shahrbabak, Mostafa Sadeghi. Detecting novel SNPs and breed-specific haplotypes at calpastatin gene in Iranian fat- and thin-tailed sheep breeds and their effects on protein structure. Gene, 2014; 537:132-139.
29. Schenkel FS, Miller SP, Jiang Z, Mandell IB, Ye X, Li H, Wilton JW. Association of a single nucleotide polymorphism in the calpastatin gene. Journal of Animal Science, 2006; 84:291-299.
30. Ciobanu DC, Bastiaansen JWM, Lonergan SM, Thomsen H, Dekkers JCM, Rothschild MF. New alleles in calpastatin gene are associated with meat quality traits in pigs. Journal of Animal Science, 2004; 82:2829-2839.
31. Byun S O, Zhou H, Forrest R H J, Frampton C M, Hickford J G. H. Association of the ovine Calpastatin gene with birth weight and growth rate to weaning. Animal Genetics, 2008; 39:572–576.
32. Yilmaz O, Sezenler T, Ata N, Yaman Y, Cemal I, Karaca O. Polymorphism of the ovine Calpastatin gene in some Turkish sheep breeds. Turkish Journal of Veterinary and Animal Sciences, 2014; 38: 354-357.
33. Nikmarda M, Molaeea V, Eskandarinasaba MP, Djadida ND, Vajhib AR. Calpastatin polymorphism in Afshari sheep and its possible correlation with growth and carcass traits. Journal of Applied Animal Research, 2012; 40(4):346-350.
34. Mohammadi M, Beigi Nasiri MT, Alami-Saeid KH, Fayazi J, Mamoee Mand, Sadr AS. Polymorphism of Calpastatin gene in Arabic sheep using PCR- RFLP. African Journal of Biotechnology, 2008; 7(15):2682-2684.
35. Walling G.A, Wilson AD, McTeir BL, Visscher PM, Simm G, Bishop SC. A candidate region approach allows efficient QTL detection in UK Suffolk and Texel populations, in: Proc. 7th World Cong. Genet. Appl. Livest. Prod., Montpellier, 19–23 August 2002.
36. Forutan K, Afshar AM, Zargari K, Chamani M, Kashan N The expression of Myogenic and Myostatin genes in Baluchi sheep. Iranian Journal of Applied Animal Science, 2016; 6(4): 873-878.
37. Pasandideh M, Rahimi-Mianji G, Gholizadeh M. A genome scan for quantitative trait loci affecting average daily gain and Kleiber ratio in Baluchi Sheep. Journal of Genetics, 2014; 97(2): 493-503
38. McEwan JC, Gerard EM, Jopson NB, Nicoll GB, Greer GJ, Dodds KG, Bain WE, Burkin HR, Lord EA, Broad TE. Localization of a QTL for rib-eye muscling on OAR18, Animal Genetics, 1998; 29(1): 66.
39. Abdoli R, Zamani P, Mirhoseini SZ, Ghavi Hossein-Zadeh N, Nadri S. A review on prolificacy genes in sheep. Reproduction in Domestic Animals, 2016; 1-7. doi: 10.1111/rda.12733.
40. Abdoli R, Mirhoseini SZ, Ghavi Hossein-Zadeh N, Zamani P. Screening for causative mutations of major prolificacy genes in Iranian fat-tailed sheep. International Journal of Fertility and Sterility, 2018; 12(1): 51-55.
41. Talebi R, Ahmadi A, Afraz F, Sarry J, Woloszyn F, Fabre S. Detection of single nucleotide polymorphisms at prolificacy major genes in the Mehraban sheep and association with litter size. Annals of Animal Science, 2018; doi:10.2478/aoas-2018-0014.
42. Demars J, Fabre S, Sarry J, Rossetti R, Gilbert H, Persani L, et al. Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyper prolificacy phenotype in sheep. PLoS Genetics, 2013; 9(4): doi:10.1371/journal.pgen.1003482.
43. Bodin L, Di Pasquale E, Fabre S, Bontoux M, Monget P, Persani L, Mulsant P. A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. Endocrinology, 2017; 148: 393-400.
44. Amini1 H, Ajaki A, Farahi M, Heidari M, Pirali A, Forouzanfar M, Eghbalsaied S. The novel T755C mutation in BMP15 is associated with the litter size of Iranian Afshari, Ghezel, and Shal breeds. Archive Animal Breeding, 2018; 61:153–160.
45. Davis GH, Balakmrishnan L, Ross IK, Wilson T, Galloway SM, Lumsden BM, et al. Investigation of the Booroola (FecB) and Inverdale (FecXI) mutations in 21 prolific breeds and strains of sheep sampled in 13 countries. Journal of Animal Reproduction Science, 2006; 92:87-96.
46. Nanekarani S, Goodarzi M, Khederzadeh S, Torabi S, Landy N. Detection of polymorphism in booroola gene and growth differentiation factor 9 in Lori sheep breed. Tropical Journal of Pharmaceutical Research, 2016; 15(8): 1605-1611.
47. Våge AI, Husdal M, Kent MP, Klemetsdal G, Boman IA. A missense mutation in growth differentiation factor 9 (GDF9) is strongly associated with litter size in sheep. BMC Genetics, 2013; 14:1-8.
48. Hanrahan, JP, Gregan, SM, Mulsant, P, Mullen, M, Davis, GH, Powell, R, Galloway, SM. Mutations in the genes for oocyte derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biology of Reproduction, 2004; 70:900–909.
49. Montgomery GW, Galloway SM, Davis GH, MacNatty KP. Genes controlling ovulation in sheep. Journal of Reproduction and Fertility, 2001; 121:843-852.
50. Dinçel D, Ardiçli S Soyudal, B, Mehlika ER, Alpay F, Şamli H, Balci F. Analysis of FecB, BMP15 and CAST Gene Mutations in Sakiz Sheep. Kafkas Univ Vet Fak Derg, 2015; 21(4): 483-488.
This work and its PDF file(s) are licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.