Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2018, Vol. 53, ¹ 4, p. 723-734.
(how to cite this article)

doi: 10.15389/agrobiology.2018.4.723eng

UDC 636.4:636.082:575.1

Acknowledgements:
The equipment of the Sharing Center for Farm Animal Bioresources and Bioengineering (FSC for Animal Husbandry) was used.
Supported financially by Ministry of Education and Science of the Russian Federation (the project unique identifier RFMEFI60417X0182)

 

EFFECTS OF GENOTYPES FOR IGF2, CCKAR AND MC4R
ON THE PHENOTYPIC ESTIMATIONS AND BREEDING VALUES
FOR PRODUCTIVE TRAITS IN PIGS

E.E. Melnikova1, N.V. Bardukov1, M.S. Fornara1, O.V. Kostyunina1,
A.A. Sermyagin1, A.M. Zaitsev2, N.A. Zinovieva1

1 Ernst Federal Science Center for Animal Husbandry,Federal Agency of Scientific Organizations, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail melnikovaee@vij.ru, bardukv-nikolajj@mail.ru, margaretfornara@gmail.ru, kostolan@yandex.ru, alex_sermyagin85@mail.ru, n_zinovieva@mail.ru (✉ corresponding author)
2All-Russian Research Institute for Horse Breeding, Federal Agency of Scientific Organizations, pos. Divovo, Rybnovskii Region, Ryazan Province, 391105 Russia, e-mail amzaitceff@mail.ru 

ORCID:
Melnikova E.E. orcid.org/0000-0002-7498-1871
Bardukov N.V. orcid.org/0000-0002-5497-2409
Fornara M.S. orcid.org/0000-0002-8844-177X
Kostyunina O.V. orcid.org/0000-0001-8206-3221
Sermyagin A.A. orcid.org/0000-0002-1799-6014
Zaitsev A.M. orcid.org/0000-0003-4260-602X
Zinovieva N.A. orcid.org/0000-0003-4017-6863
The authors declare no conflict of interests

Received March 21, 2018

 

Development of programs for marker-assisted selection has to be based on genetic polymorphisms, whose effect on the production traits and breeding values of animals is reliable and significant. Prospects for the use of genomic selection in pigs are associated with the development of low-density (LD) DNA arrays, which include the SNPs (single nucleotide polymorphisms) selected by the results of genome-wide association studies (GWAS) with HD-panels. Genes of insulin-like growth factor 2 (IGF2), cholecystokinin receptor A (CCKAR) and melanocortin 4 receptor (MC4R) are of interest for inclusion in LD-panels. Numerous studies have shown a significant effect of these genes on feed conversion rate, growth rate, meat content, and fat deposition. The aim of this work was to evaluate the effect of complex genotypes for IGF2, CCKAR and MC4R on growth and carcass traits of the Landrace and Large White pigs raced in Russia. In total, 1262 animals, including Large White (n = 667) and Landrace pigs (n = 595) were studied. Pig phenotypes were determined for muscle depth (MD, mm), adjusted age at 100 kg (AGE100, day) and back fat thickness (BF, back fat) at three points: BF1 (at ribs 6-7, mm), BF2 (at rib 10, mm), BF3 (at 14 rib, mm). DNA was extracted from tissue samples (ear pluck) using a DNA-Extran-2 Kit (Sintol, Russia). Polymorphism of IGF2 was determined by real-time PCR. Causative SNPs in CCKAR and MC4R genes were defined by multiplex PCR with FLASH detection. The allele frequencies of DNA-markers were pA = 27.2 % and pA = 86.3 % for IGF2, pA = 0.6 % and pA = 21.1 % for CCKAR, pA = 54.1 % and 60.0 % for MC4R in Landrace and Large White pigs, respectively. The heritability coefficients (h2) were 0.204-0.242 for BF1, BF2, and BF3, 0.309 for MD, and 0.366 for AGE100. We developed an equation model for the pig's breeding traits and found the significant effects of fixed factors in the model (breed, sex, year of birth), including specific genotypes for the analyzed genes on the phenotypic variations (for IGF2 and MC4R on BF1, BF2 and BF3, P > 0.95), and estimated breeding values (EBV) for growth and carcass traits (for each of the three markers the ratio of additive genetic variation ranged from 0.5 to 7.6 %, P > 0.95-0.999). We identified the economically desired alleles for IGF2 (allele A) and MC4R (allele A) genes. Animals which carried the homozygous genotypes for the desired alleles (AA for both of IGF2 and MC4R genes) were characterized by the significantly better scores for analyzed traits, estimated by least squares method, comparing to the individuals which were homozygous for the alternative allele G. The additive compensating effect of genotypes’ combinations for IGF2 and MC4R on the pig growth traits was established. The animals with the highest number of the A alleles for IGF2 and MC4R had preferable characteristics for the back fat thickness comparing to animals with GG genotypes (for both DNA markers). The differences between groups of animals carrying in their genotypes from four to single copy of the A alleles comparing to animals which do not have A alleles (GG genotypes for both markers) varied from 7.9 to 21.0 % for BF1, from 8.5 to 21.4 % for BF2, from 9.9 to 22.6 % for BF3, and from 2.8 to 3.2 % for MD. In this regard, the IGF2 and MC4R genotypes can be used in breeding programs of Large White and Landrace pigs raced in Russia to select the pigs with desired growth and carcass characteristics.

Keywords: pigs, Large White breed, Landrace, IGF2, CCKAR, MC4R genes, polymorphisms, estimated breeding value (EBV), growth and carcass traits.

 

Full article (Rus)

Full article (Eng)

 

REFERENCES

  1. Sermyagin A.A., Naryshkina E.N., Karpushkina T.V., Strekozov N.I., Zinov'eva N.A. Molochnoe i myasnoe skotovodstvo, 2015, 7: 2-5 (in Russ.). 
  2. Sermyagin A.A., Gladyr' E.A., Kharitonov S.N., Ermilov A.N., Strekozov N.I., Brem G., Zinov'eva N.A. Genome-wide association study for milk production and reproduction traits in Russian Holstein cattle population. Agricultural Biology [Sel’skokhozyaistvennaya Biologiya], 2016, 51(2): 182-193 CrossRef
  3. Zinov'eva N.A., Sermyagin A.A., Kostyunina O.V. Zhivotnovodstvo Rossii, 2018, 7: 53-55 (in Russ.). 
  4. Ramos A.M., Crooijmas R.P., Affara N.A., Amaral A.J., Archibald A.L., Beever J.E., Benedixen C., Churcher C., Clark R., Dehais P., Hansen M. S., Hedegaard J., Hu Z.L., Kerstens H.H., Law A.S., Megens H.-J., Milan D., Nonneman D.J., Rohrer G.A., Rothschild M.F., Smith T.P.L., Schnabel R.D., Van Tassell C.P., Taylor J.F., Wiedmann R.T., Schook L.B., Groenen M.A.M. Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PLoS ONE, 2009, 4(8): 6524 CrossRef
  5. Meuwissen T.H.E., Hayes B.J., Goddard M.E. Prediction of total genetic value using genome-wide dense marker maps. Genetics, 2001, 157(4): 1819-1829.
  6. VanRaden P.M., Null D.J., Sargolzaei M., Wiggans G.R., Tooker M.E., Cole J.B., Sonstegard T.S., Faust M.A., Doak G.A. Genomic imputation and evaluation using high-density Holstein genotypes. J. Dairy Sci., 2013, 96(1): 668-678 CrossRef
  7. Habier D., Fernando R.L., Dekkers JCM. Genomic selection using low-density marker panels. Genetics, 2009, 182(1): 343-353 CrossRef
  8. Huang Y., Hickey J.M., Cleveland M.A., Maltecca C. Assessment of alternative genotyping strategies to maximize imputation accuracy at minimal cost. Genet. Sel. Evol., 2012, 44(1): 25 CrossRef
  9. Cleveland M.A., Hickey J.M. Practical implementation of cost-effective genomic selection in commercial pig breeding using imputation. J. Anim. Sci., 2013, 91(8): 3583-3592 CrossRef
  10. Abell C.E., Dekkers J.C.M., Rothschild M.F., Mabry J.W., Stalder K.J. Total cost estimation for implementing genome-enabled selection in a multi-level swine production system. Genet. Sel. Evol., 2014, 46(1): 32 CrossRef
  11. Pig QTLdb. Available https://www.animalgenome.org/cgi-bin/QTLdb/SS/index. Accessed May 10, 2018.
  12. Van Laere A.-S. From QTL to QTN. Identification of a quantitative trait nucleotide influencing muscle development and fat deposition in pig. Doctoral thesis. Swedish University of Agricultural Sciences, Uppsala, 2005.
  13. Van Laere A.S., Nguyen M., Braunschweig M., Nezer C., Collette C., Moreau L., Archibald A.L., Haley C.S., Buys N., Tally M., Andersson G., Georges M., Andersson L. A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature, 2003, 425 (6960): 832-836 CrossRef
  14. Chang K.C. Key signalling factors and pathways in the molecular determination of skeletal muscle phenotype. Animal, 2007, 1(5): 681-698 CrossRef
  15. Estelle? J., Mercade? A., Noguera J.L., Pérez-Enciso M., O?vilo C., Sánchez A., Folch J.M. Effect of the porcine IGF2-intron3-G3072A substitution in an outbred Large White population and in an Iberian×Landrace cross. J. Anim. Sci., 2005, 83(12): 2723-2728. CrossRef
  16. Heuven H.C.M., Bovenhuis H., Janss L.L.G., Van Arendonk J.A.M. Efficiency of population structures for mapping of Mendelian and imprinted quantitative trait loci (QTL) in outbred pigs using variance component methods. Genet. Sel. Evol.,2005, 37: 35-655 CrossRef
  17. Oczkowicz M., Tyra M., Walinowicz K., Rózycki M., Rejduch B. Known mutation (A3072G) in intron3 of the IGF2 gene is associated with growth and carcass composition in Polish pig breeds. J. Appl. Genet., 2009, 50(3): 257-259 CrossRef
  18. Kostyunina O.V., Svezhentseva N.A., Zinov'eva N.A., Dotsev A.V., Shakhina A.V., Sizareva E.I., Gladyr' E.A. Effect of ESR and IGF2 marker genotypes on the breeding values of the large white boars. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2011, 6: 54-59.
  19. Kostyunina O.V., Kramarenko S.S., Svezhentseva N.A., Sizareva E.I., Zinov'eva N.A. The association of IGF2 with productive traits of pigs of large white breed in the aspect of sexual differentiation. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2015, 50(6): 736-745 CrossRef
  20. Crawley J.N., Fiske S.M., Durieux C., Derrien M., Roques B.P. Centrally administered cholecystokinin suppresses feeding through a peripheral-type receptor mechanism. J. Pharmacol. Exp. Ther., 1991, 257: 1076-1080.
  21. Asin K.E., Bednarz L. Differential effects of CCK-JMV-180 on food intake in rats and mice. Pharmacol. Biochem. Be., 1992, 42(2): 291-295.
  22. Clutter A.C., Sasaki S., Pomp D. Rapid communication: the cholecystokinin type-A receptor (CCKAR) gene maps to porcine chromosome 8. J. Anim. Sci., 1998, 76(7): 1983-1984.
  23. Houston R.D., Haley C.S., Archibald A.L., Cameron N.D., Plastow G.S., Rance K.A. A polymorphism in the 5’ untranslated region of the porcine Cholecystokinin Type-A Receptor (CCKAR) gene affects feed intake and growth. Genetics, 2006, 174(3): 1555-1563 CrossRef
  24. Johnson R. Effect of DNA markers in Nebraska selection lines. Nebraska Swine Reports, 2010: 44-50. Available https://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1260&con-text=coopext_swine. Accessed May 10, 2018.
  25. Mountjoy K.G., Mortrud M.T., Low M.J., Simerly R.B., Cone R.D. Localization of the melanocortin-4 receptor (MC4-R) in neuroendocrine and autonomic control circuits in the brain. Mol. Endocrinol., 1994, 8(10): 1298-1308.
  26. Kim K.S., Larsen N.J., Rothschild M.F. Rapid communication: linkage and physical mapping of the porcine melanocortin-4 receptor (MC4R) gene. J. Anim. Sci., 2000, 78(3): 791-792.
  27. Kim K.S., Larsen N., Short T., Plastow G., Rothschild M.F. A missense variant of the melanocortin 4 receptor (MC4R) gene is associated with fatness, growth and feed intake traits. Mamm. Genome, 2000, 11(2): 131-135.
  28. Hernández-Sánchez J., Visscher P., Plastow G., Haley C. Candidate gene analysis for quantitative traits using the transmission disequilibrium test: the example of the melanocortin 4-receptor in pigs. Genetics, 2003, 164(2): 637-644.
  29. Stachowiak M., Szydlowski M., Obarzanek-Fojt M., Switonski M. An effect of a missense mutation in the porcine melanocortin-4 receptor (MC4R) gene on production traits in Polish pig breeds is doubtful. Anim. Genet., 2005, 37(1): 55-57 CrossRef
  30. Houston R.D., Cameron N.D., Rance K.A. A melanocortin-4 receptor (MC4R) polymorphism is associated with performance traits in divergently selected large white pig populations. Anim. Genet., 2004, 35(5): 386-390 CrossRef
  31. Chen J.F., Xiong Y.Z., Zuo B., Zheng R., Li F.E., Lei M.G., Li J.L., Deng C.Y., Jiang S.W. New evidences of effect of melanocortin-4 receptor and insulin-like growth factor 2 genes on fat deposition and carcass traits in different pig populations. Asian-Australian Journal of Animal Science, 2005, 18(11): 1542-1547 CrossRef
  32. Óvilo C., Fernández A., Rodríguez M.C., Nieto M, Silióa L. Association of MC4R gene variants with growth, fatness, carcass composition and meat and fat quality traits in heavy pigs. Meat Science, 2006, 73(1): 42-47 CrossRef
  33. Van den Maagdenberg K., Stinckens A., Claeys E., Seynaeve M., Clinquart A., Georges M., Buys N., De Smet S. The Asp298Asn missense mutation in the porcine melanocortin-4 receptor (MC4R) gene can be used to affect growth and carcass traits without an effect on meat quality. Animal, 2007, 1(8): 1089-1098 CrossRef
  34. Park H.B., Carlborg O., Marklund L., Andersson L. Melanocortin-4 receptor (MC4R) genotypes have no major effect on fatness in a Large White × Wild Boar intercross. Anim. Genet., 2002, 33(2): 155-157 CrossRef
  35. Bruun C.S., Jorgensen C.B., Nielsen V.H., Andersson L, Fredholm M. Evaluation of the porcine melanocortin 4 receptor (MC4R) gene as a positional candidate for a fatness QTL in a cross between Landrace and Hampshire. Anim. Genet., 2006, 37(4): 359-362 CrossRef
  36. Jokubka R., Maak S., Kerziene S., Swalve H.H. Association of a melanocortin 4 receptor (MC4R) polymorphism with performance traits in Lithuanian White pigs. J. Anim. Breed. Genet., 2006, 123(1): 12-22 CrossRef
  37. Salajpal K., Ðiki? M., Karolyi D., Šurina J., Matkovic M., Liker B. Effect of MC4R polymorphism on physiological stress response in pigs. Poljoprivreda, 2007, 13(1): 46-50. Available https://hrcak.srce.hr/16049. Accessed May 10, 2018.
  38. Misztal I., Tsuruta S., Strabel T., Auvray B., Druet T., Lee D.H. BLUPF90 and related programs (BGF90). Proc. 7th World Congress on genetics applied to livestock production. Montpellier, France, 2002, 28(28-07): 21-22.
  39. Dube B., Mulugeta S.D., Dzama K. Genetic relationship between growth and carcass traits in Large White pigs. S. Afr. J. Anim. Sci., 2013, 43(4): 482-492.

 

back