The effect of gene SKI polymorphism on carcass traits in pigs

Animal Science Papers and Reports vol. 24 (2006) no. 2, 163-168 Institute of Genetics and Animal Breeding, Jastrzębiec, Poland SHORT REPORT The effe...
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Animal Science Papers and Reports vol. 24 (2006) no. 2, 163-168 Institute of Genetics and Animal Breeding, Jastrzębiec, Poland

SHORT REPORT

The effect of gene SKI polymorphism on carcass traits in pigs Paweł Urbański1, Mariusz Pierzchała1, Agnieszka Korwin-Kossakowska1, Jolanta Kurył1, Marian Kamyczek2, Marian Różycki3 1

Polish Academy of Sciences Institute of Genetics and Animal Breeding, Jastrzębiec, 05-552 Wólka Kosowska, Poland

2

Pig Hybridization Centre, National Research Institute of Animal Production, Pawłowice, 64-122 Pawłowice, Poland

3

National Research Institute of Animal Production, 32-083 Balice/Cracow, Poland

(Received April 24, 2006, accepted June 06, 2006) Phosprotein, the product of proto-oncogene SKI, plays a role in the control of cell growth and in skeletal muscle differentiation. The aim of this study was to characterize the polymorphism of gene SKI identified with restriction endonuclease BsmAI in gilts of Polish Large White (PLW, n=117) and Polish Landrace (PL, n=51), and to analyse the relation between the SKI genotypes and carcass traits. The animals were free of RYR1T allele. In both breeds, the frequency of homozygote CC at the SKI locus occurred very low. The only significant relations between genotype and carcass traits were observed in PLW gilts for weight of loin and weight of sirloin. KEY WORDS: carcass quality / gene polymorphism /pig / SKI

Selection for increased growth rate or decreased backfat thickness was important in pig breeding during last two decades, based, among others, on OTL identification. Within this area, one of the methods used is evaluation of candidate genes polymorphism effect on phenotypic variation [Kurył 2000 – a review].

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Recently, the SKI proto-oncogene was suggested as potentially influencing carcass traits in pigs [Stratil et al. 2002]. SKI encodes a nuclear protein, binds to DNA in association with other cellular factors, and modulates transcription [Berk et al. 1997]. These proteins are involved in cell proliferation, differentiation and apoptosis. The gene SKI has also been found implicated in the control of myogenesis processes [Berk et al. 1997]. Earlier Colmenares and Stavnezer [1989] reported that the proto-oncogene SKI induces muscle cell differentiation. Transgenic pigs and mice carrying SKI sequences show marked muscle hypertrophy characterized by myofibretype specificity [Sutrave et al. 1990, Pursel et al. 1992]. The induction of MYOD1 and MYF4 expression by the SKI suggests, that this proto-oncogene acts early in the pathway, perhaps in the determination step next to MYOD1 and(or) MYF5. Thus, induction of myofibre hypertrophy suggests the SKI activity during postnatal muscle growth, perhaps in cooperation with other genes [Colmenares et al. 1991]. In order to determine a normal function of this gene in vivo, Berk et al. [1997] have disrupted the mouse SKI gene. The results confirmed its function in skeletal muscle development and showed a novel role of the factor in the morphogenesis of craniofacial structures and the central nervous system. But the exact role of the gene in development of skeletal muscle still remains unclear. In the porcine SKI mapped to pig chromosome 6, double nucleotide substitution CG→TC at positions 304-305 resulting in an amino acid substitution in the protein (Arg→Ser), was described by Stratil et al. [2002]. This polymorphism is located in exon 1, encoding functional domain responsible for transformation and muscle differentiation. The aim of this study was to evaluate the effect of the mutation described on porcine growth rate and carcass traits. A similar analysis has not been reported in literature to date. Material and methods Included were Polish Large White (PLW, n=117) and Polish Landrace (PL, n=51) gilts free of RYR1T allele. The pigs were fattened and slaughtered at the Pig Testing Station of the National Research Institute of Animal Production, Pawłowice near Leszno Wlkp, Poland. From 25 to 100 kg live body weight the commercial mixed feed was applied ad libitum. Right carcass side was dissected into lean, fat and bone according to the procedure described by Różycki [1996]. In the present study the following traits were considered: weight of right carcass side, weight of ham with shank, height of loin eye, loin eye area, loin weight, sirloin weight, meat content of valuable carcass cuts and meat content of carcass. Genomic DNA was isolated from leukocytes according to Kawasaki [1990]. The SKI genotyping was performed using PCR/RFLP technique with BsmAI (Alw26I) endonuclease, recognizing G→ C substitution, according to Stratil et al. [2002]. An amplified 350 bp fragment encompassed part of SKI exon 1. Association analyses were carried out for each of two 164

SKI gene polymorphism and carcass traits in pigs

breeds separately using the least squares method of the GLM procedure [Statistical Analysis Systems Institute Inc. 2001, according to the following model: where:

Yijkl = µ + Gi + Oj + β(xij - x) + eij yij – trait measured on ij-th animal; µ – overall mean; Gi – effect of SKI genotype; Oj – sire effect;

β(xij - x) – linear regression for weight of right carcass side (for carcass traits) and age at slaughter (for growth rate traits); eij – random error. Results and discussion The frequency of genotypes and alleles at the SKI locus is shown in Table 1. The G305C polymorphism present in exon 1 was identified with enzyme BsmAI. Three SKI /G305C genotypes were observed in breeds tested, but the frequency of genotype CC was low in both (11.1% in PLW and 1.96% in PL). In PLW the frequency of homozygotes GG was similar to that of heterozygotes whereas in PL the most frequent was GG genotype. Stratil et al. [2002] reported the highest frequency of SKI C allele in Pietrain pigs, whereas Meishan pigs appeared to be monomorphic for the allele G. However, one should mention that in a cited study by Stratil et al. [2002] number of animals of individual breeds was very low (6 and 12, respectively). Table 1. Frequency of genotypes and alleles at locus SKI in Polish Large White (PLW) and Polish Landrace (PL) gilts Breed

Number of animals

Number and frequency genotypes

alleles

GG

GC

CC

G

C

PLW

117

50 (42.7%)

54 (46.1%)

13 (11.11%)

0.66

0.34

PL

51

37 (72.5%)

13 (25.4%)

1 (1.96%)

0.85

0.15

A significant relationship between production traits and the genotype at the SKI locus was observed for two traits and in PLW gilts only (Tab. 2). The tested transversion – G305C – was found significant for weight of loin and weight of sirloin. 165

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Table 2. Least squares means (LSM) and their standard errors (SE) for two carcass traits as affected significantly by genotype at the SKI locus in Polish Large White pigs SKI genotype at nucleotide G305C Carcass trait

Weight of sirloin (kg) Weight of loin (kg)

GG

GC

CC

LSM

SE

LSM

SE

LSM

SE

0.359Aa 6.769a

0.006 0.089

0.340B 6.556b

0.005 0.084

0.339b 6.749

0.009 0.138

aA...

Within rows means bearing different superscripts differ significantly at: small letters − P≤0.05; capital − P≤0.01.

The homozygotes of the G allele showed the highest value of these traits, compared to heterozygotes and homozygotes of allele C. Heterozygotes showed the lowest weight of loin compared to both homozygotes. Such phenomenon observed earlier for certain human genes was named a negative (or positive) heterosis – Comings and MacMurray [2000] – who suggested that if the regulation of the gene is dose-dependent, the presence of a regulatory sequence in a heterozygous state could modify the gene function. Similar associations were also observed in our earlier studies regarding MyoD genes family [Cieślak et al. 2002, Urbański et al. 2005, 2006, WyszyńskaKoko et al. 2006]. We did not observe any significant relation between SKI genotypes and carcass traits in PL pigs tested in this study. A low number of animals (51 only) may be the reason for insignificance of associations studied (Tab. 1). The SKI proto-oncogene has been mapped to chromosome 6 by Stratil et al. [2002], where two other genes – RYR1 [Fujii et al. 1991] and H-FABP [Gerbens et al. 1997] – as well as QTLs important for growth rate and carcass traits [Paszek et al. 1999 and Geldermann et al. 2003] have been localized. The RYR1 genotype is known to affect carcass quality. In the present study, however, this was excluded as the gilts analysed were free of RYR1T allele. Thus, the observed effect of SKI genotype on carcass traits has not been modified by RYR1 gene linked to SKI locus. REFERENCES 1. BERK M., DESAI S.Y., HEYMAN CH.H., COLMENARES C., 1997 – Mice lacking the ski protooncogene have defects in neurulation, craniofacial patterning, and skeletal muscle development. Genes & Development 11, 2029-2039. 2. CIEŚLAK D., KURYŁ J., KAPELAŃSKI W., PIERZCHAŁA M., GRAJEWSKA S., BOCIAN M., 2002 – A relationship between genotypes at MYOG, MYF3 and MYF5 loci and carcass meat and fat deposition traits in pigs. Animal Science Papers and Reports 20, 77-92. 3. COLMENARES C., STAVNEZER E., 1989 – The ski oncogene induces muscle differentiation in quail embryo cells. Cell 59, 293-303.

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4. COLMENARES C., TEUMER J.K., STAVNEZER E., 1991 – Transformation-defective v-ski induces MyoD and myogenin expression but not myotube formation. Molecular and Cellular Biology 11, 1167-1170. 5. COMINGS D.E., MACMURRAY J.P., 2000 – Molecular heterosis: a review. Molecular Genetics and Metabolism 71, 19-31. 6. FUJII J., OTSU K., ZORZATO F., DE LEON S., KHANNA V.K., WEILER J.E., O’BRIEN P.J., MACLENNAN D.H., 1991 – Identification of a mutation in porcine ryanodine receptor associated with malignant hyperthermia. Science 253, 448-451. 7. GELDERMANN H., MULLER E., MOSER G., REINER G., BARTENSCHLAGER H., CEPICA S., STRATIL A., KURYŁ J., MORAN C., DAVOLI R., BRUNSCH C., 2003 – Genome-wide linkage and QTL mapping in porcine F2 families generated from Pietrain, Meishan and Wild Boar crosses. Journal of Animal Breeding and Genetics 120, 363-393. 8. GERBENS F., RETTENBERGER G., LENSTRA J.A., VEERKAMP J.H., TE PAS M.F.W., 1997 – Characterization, chromosomal localization and genetic variation of the porcine heart fatty acid binding protein gene. Mammalian Genome 8, 328-322. 9. KAWASAKI E.S., 1990 – Sample preparation from blood, cells and other fluids. In: PCR Protocols. A guide to Methods and Applications (M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J., White, Eds.). Academic Press, New York, pp. 3-12. 10. KURYŁ J., 2000 – Geny cech ilościowych zwierząt gospodarskich – aktualny stan badań (The current state of research in the quantitative traits loci in farm animals – a review). In Polish, summary in English. Prace i Materiały Zootechniczne 56, 7-50. 11. PASZEK A.A., WILKIE P.J., FLICKINGER G.H., ROHRER G.A., ALEXANDER J.L., BEATTIE C.W., SCHOOK B.L., 1999 – Interval mapping of growth in divergent swine cross. Mammalian Genome 10, 117-122. 12. PURSEL V.G., SUTRAVE P., WALL R.J., KELLY A.M., HUGHES S.H., 1992 – Transfer of c-ski gene into swine to enhance muscle development. Theriogenology 37, 278. 13. RÓŻYCKI M., 1996 – Zasady postępowania przy ocenie świń w Stacjach Kontroli Użytkowości Rzeźnej Trzody Chlewnej. Stan hodowli i wyniki oceny świń. (Procedures applied by Pig Slaughter Performance Testing Stations. Current situation in breeding and results of pig evaluation). In Polish. National Institute of Animal Production, Cracow. 14. Statistical Analysis Systems Institute, 2001 – SAS/STAT user’s guide, version 8.2, SAS Institute Inc. Cary, NC, USA. 15. STRATIL A., REINER G., PEELMAN L.J., DAVOLI R., VAN POUCKE M., ZAMBONELLI P., GELDERMANN H., 2002 – An Alw26I PCR-RFLP in exon 1 of the porcine SKI oncogene and mapping the gene to the RYR1 (CRC) linkage group on chromosome 6. Animal Genetics 33(5), 377-379. 16. SUTRAVE P., KELLY A.M., HUGHES S.H., 1990 – Ski can cause selective growth of skeletal muscle transgenic mice. Genes & Development 4, 1462-1472. 17. URBAŃSKI P., PIERZCHAŁA M., KAMYCZEK M., RÓŻYCKI M., KURYŁ J., 2005 – Relations between the polymorphisms in the coding and 5’- flanking regions of the porcine MYOD1 and MYF5 genes and selected productive traits in Line 990 gilts. Animal Science Papers and Reports 23(4), 249-258. 18. URBAŃSKI P., PIERZCHAŁA M., KAMYCZEK M., RÓŻYCKI M., KURYŁ J., 2006 – Relations between the polymorphism in the coding and 5’-flanking regions of the porcine MYOD1 and MYF5 genes and productive traits in pigs. Journal of Animal and Feed Sciences 15, 225-235.

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Paweł Urbański, Mariusz Pierzchała, Agnieszka Korwin-Kossakowska, Jolanta Kurył, Marian Kamyczek, Marian Różycki

Analiza wpływu polimorfizmu genu SKI na cechy tuszy świń Streszczenie Protoonkogen SKI pełni ważną rolę w procesie wzrostu i rozwoju organizmu oraz jest zaangażowany w proces rozwoju mięśni szkieletowych. Produktami tego genu są białka jądrowe, uczestniczące, między innymi, w indukcji procesów miogenezy. Celem badań była charakterystyka polimorfizmu genu SKI świń dwóch ras hodowanych w Polsce – wielkiej białej polskiej (PLW) i polskiej białej zwisłouchej (PL) – i ocena wpływu tego polimorfizmu na cechy tuszy. Badaniami objęto zwierzęta wolne od genu RYR1T, aby wykluczyć wpływ genotypu RYR1 na cechy tuszy. W obu rasach zaobserwowano bardzo niską frekwencję osobników homozygotycznych CC. Istotne zależności między genotypem a badanymi cechami stwierdzono tylko w rasie wbp (PLW) i to wyłącznie w odniesieniu do masy polędwicy i masy polędwiczki. Autorzy wnioskują, że znajomość genotypu SKI może być przydatna w selekcji ukierunkowanej na poprawę wymienionych cech tuszy, jednak badania te powinny być kontynuowane na materiale obejmującym inne rasy i linie, aby stwierdzić, czy zaobserwowane zależności mają charakter uniwersalny.

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