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Identification of single nucleotide polymorphisms (SNPs) of the bovine growth hormone (bGH) gene associated with growth and carcass traits in Hanwoo.

INTRODUCTION

The bovine growth hormone (bGH) gene is located in q22 of bovine chromosome 19 and includes five exons with 217 amino acids (Santome et al., 1971; Wallis, 1973; Miller et al., 1980). The gene was sequenced by Gordon et al. (1983) and Hediger et al. (1990). Its product, growth hormone, is secreted in somatotropic or acidophilic cells of the anterior pituitary gland of mammals. The hormone regulates expression of many genes including one encoding insulin-like growth factor I (IGF-I), and influences growth rate, body composition, health, and milk production (Woychik et al., 1982; Gordon et al., 1983; Sumantran et al., 1992; Ho and Hoffman, 1993; Lincoln et al., 1995; Ge et al., 2013). In general, GH binds to a GH receptor and forms a dimer. Janus kinase and mitogen-activated protein kinase are involved in GH activity (Herrington et al., 2000). Recently, studies of the bGH gene have focused on single nucleotide polymorphisms (SNPs) within the gene and how the polymorphisms influence production traits such as milk production, growth, or carcass traits in cattle.

Roth et al. (1990) found a SNP in the bGH promoter region, '253' SNP near the binding site of polyoma virus enhancer A binding protein 3 (PEA3) transcription factor. Theill and Karin (1993) identified '303' SNP in the first nucleotide of biding site of another transcription factor, thyroid hormone response element (TRE). The 303 SNP was confirmed in eight cattle breeds (Hecht and Geldermann, 1996). Ge et al. (2013) analyzed effects of the bGH SNPs on growth traits and concentrations of IGF-I in Angus, but did not find significant evidence that the SNPs were associated with the traits. However, Kim et al. (2004) reported a bGH SNP, '-120' SNP in promoter region of the gene, which was associated with 3-month weight and carcass weight in Hanwoo.

There are also many reports that bGH SNPs, especially ones in exon 5, influenced milk production in Holstein and economically important traits in beef cattle (Eppard et al., 1992; Zhang et al., 1992, 1993; Lee et al., 1993; Lucy et al., 1993; Schlee et al., 1994; Yao et al., 1996). The 2141 C > G SNP encoding the 127th amino acid of bGH involves a change from leucine (CTG) to valine (GTG) (Zhang et al., 1992, 1993; Lucy et al., 1993). For the SNP, Eppard et al. (1992) found that the GTG increased milk yields in Holstein. However, Lee et al. (1993) and Lucy et al. (1993) reported that the mutation to valine decreased milk yield in cattle. Schlee et al. (1994) demonstrated that German black and white bulls with homozygous leucine had higher plasma levels than the ones with heterozygous leucine. Yao et al. (1996) reported that the 2291 A > C bGH SNP was significantly associated with milk yield, fat, and protein content in Holstein cattle. Recently, Ardiyanti et al. (2012) reported association of bGH to fatty acid components in Japanese black cattle.

Yoon et al. (2003) found a 2258 C > T SNP of bGH in Hanwoo, causing replacement of arginine (CGG) with tryptophan (TGG). Chikuni et al. (1994) also reported a 2277 C > T SNP in bGH in Japanese cattle.

The objective of this study was to find any association of bGH SNPs with growth and carcass traits in Hanwoo.

MATERIALS AND METHODS

Animals and phenotype data

A sample of 242 Hanwoo steers from 25 sires was collected from the Korea Animal Improvement Association. All the steers were under the progeny-testing program to select Hanwoo proven sires in the National Livestock Research Institute (NLRI), Korea. The steers were raised under tightly controlled conditions of the feeding program in the Daekwanryeong and Namwon branches of NLRI. The animals were born between the spring of 1998 and the fall of 2002, castrated at 6 months of age, and raised in groups of four animals per pen (4 mx8 m). After 6 months of age, the steers were fed concentrates consisting of 15% crude protein (CP)/71% totally digestible nutrients (TDN) for a period of 60 to 90 d, 15% CP/71% TDN for a period of 180 d, and 13% CP/72% TDN for a period of 90 to 120 d. The steers had access to roughage and fresh water ad libitum throughout the entire period. All steers were slaughtered approximately at 24 months of age. Live weight of each steer was measured before slaughter using electronic scales. Following a 24-h chilling, cold carcass weight was also measured.

Growth traits included weights of six-month (WT6), 12-month (WT12), 18-month (WT18), and 24-month (WT24) of age. Average daily gain (ADG) was also measured. Carcass quality traits included carcass weight (CWT), backfat thickness (BF), longissimus dorsi (eye) muscle area (EMA), and marbling scores (MS). According to the protocols of Korean Animal Product Grade System of Korean Institute for Animal Products Quality Evaluation, BF (mm) was measured at the 2/3 point of backfat that was located toward abdomen along the right side of the eye muscle cross-section. EMA ([cm.sup.2]) was measured in the eye muscle cross-section. MS was scored on a scale of 1 thorough 9 (1 = trace, 9 = very abundant) according to the Korean Beef Marbling Standard.

Sequence analysis of bGH gene

Genomic DNA was extracted from white blood cells of 21 unrelated Hanwoo individuals using the phenolchloroform method (Sambrook et al., 2001). We sequenced 47 bp to 2,528 bp of the bGH gene (GenBank accession number, M57764) and the flanking regions to evaluate SNP variants using the BigDye Terminator (ver. 3.1) cycle sequencing kit (Applied Biosystems, Foster City, CA) with an ABI 3730XL DNA analyzer (Applied Biosystems). Six primer sets for amplification and sequencing analysis were designed based on the GenBank sequence using Primer3 software. Primer sequences are shown in Table 1. Sequence editing was performed by visual confirmation using Sequencher 4.6 software (Gene Codes Corp., Ann Arbor, MI).

Genotyping by single-base extension (SBE)

A primer set (GH-P1-F and GH1-P1-R) was designed to generate a 639-bp product that included four SNPs in the bGH gene promoter. Another primer set (GH-E1-F and GHE1-R) was designed to generate a 328-bp product that included 679-bp SNP in the exon 1 region. A third primer set (GH-E2-F and GH-E2-R) was designed to produce a 536-bp amplicon that included 1,692-bp SNP in intron 3, while a primer set (GH-E3-F and GH-E3-R) was designed to obtain a 428-bp product that included four SNPs in exon 4 (Table 1). Primer extension was performed using a SNaPshot ddNTP Primer Extension Kit (Applied Biosystems, Foster City, CA). To purify the primer extension products, exonuclease 1 and shrimp alkaline phosphatase were added to the reaction mixtures. The samples were incubated at 37[degrees]C for 1 h and the reactions were stopped by incubating at 72[degrees]C for 15 min. The products were mixed with a Genescan 120 LIZ standard and HiDi formamide (Applied Biosystems) before being denatured at 95[degrees]C for 5 min. Electrophoresis was performed using an ABI PRISM 3130XL Genetic Analyzer and the results were analyzed using GeneMapper v.4.0 software (Applied Biosystems).

Statistical analysis

Heterozygosity, minor allele frequency (MAF), and Hardy-Weinberg equilibrium (HWE) were assessed using Haploviewer v4.2 (Barret et al., 2005). HWE was tested by comparing the expected and observed genotype frequencies using a chi-square test. Associations of growth and carcass traits for each SNP were analyzed with a mixed analysis of covariance (ANCOVA) linear model using SAS v9.1 (SAS Institute, Cary, NC). For growth traits, two fixed effect were fitted, year-season-birth place and SNP genotype. For carcass quality traits, an additional effect was included in the model, a covariate for age in days at the time of slaughter.

RESULTS AND DISCUSSION

The DNA segment of 2,482 bps that was located at 47 to 2,528 bp of bGH gene was sequenced, and a total of 10 SNPs were identified (Figure 1 and Table 2). Among the ten SNPs, four SNPs were located in the promoter region, i.e. 253 C > T, 303 C > T, 502 C > T, and 559 G > A. Results of association tests between the four SNPs and growth and carcass traits showed that 303 C > T and 559 G > A SNPs had significantly affected WT6 and eye muscle area (EMA), respectively at p = 0.05 level (Tables 3 and 4). The significant SNPs in the bGH gene promoter region may have limited efficiency as molecular markers, partly because the SNPs are located in the SINE/BovA2 repeat element, in which repetitive mutations occur frequently (Vaccarelli et al., 2008), suggesting that the SNPs does not strongly influence gene expression. Alternatively, the SNPs may affect growth and carcass traits due to great linkage disequilibrium with the causal variants that were closely located to the bGH SNPs (Ge et al., 2013). Kim et al. (2004) reported that a SNP at a promoter position -120 spanning a DraI restriction site was associated with 3-month weight and carcass weight in a Hanwoo population. However, our study did not confirm the SNP, partly because the SNP in Kim et al. (2004) was not detected with strong statistical evidence, i.e. comparison-wise p values were 0.025 and 0.041 for 3-month weight and carcass weight, respectively, which may be not confirmed in another random Hanwoo sample. Also, Kim et al. (2004) analyzed the association tests with estimated breeding values of the growth and carcass quality traits, while raw phenotypes were used in this study.

In this study, 679 C > T SNP was found in exon 1, 1692 T > C SNP in intron 3, and four SNPs (2141 C > G, 2258 C > T, 2277 C > T, and 2291 A > C) in exon 5 of the bGH gene. Among the SNPs in the CDS region, the 2141 C > G, the 2258 C > T, and the 2277 C > T SNPs were non-synonymous causing amino acid substitution, while the 2291 A > C SNP was a silent mutation. Among the SNPs in exon 1 and intron 3, 679 C > T and 1692 T > C did not significantly influence any growth or carcass trait (Tables 3 and 4). These results are in accordance with the report of Yao et al. (1996), in which there was no significant association of the SNPs with milk yield, fat and protein content in Holstein bulls.

The 2141 C > G SNP was non-synonymous and induced a mutation from leucine (CTG) to valine (GTG), which significantly affected ADG at p = 0.05 level (Table 3), even if HWE for the SNP was significantly deviated from expectation (Table 2). The 2258 C > T SNP was non synonymous, causing mutation of arginine to tryptophan in the process of transition from C to T. The SNP significantly affected ADG and CWT at p = 0.05 level (Tables 3 and 4). The genotype effect of the 2258 SNP on ADG was 0.74 [+ or -] 0.01 for CC and 0.71 [+ or -] 0.01 for CT, respectively (Table 3). For CWT, the estimates of CC and CT genotypes were 310.4 [+ or -] 2.4 and 298.5 [+ or -] 4.9, respectively (Table 4). For the SNP, Yoon et al. (2003) reported that MAF, Msp I (-), was low (0.00 to 0.054) in European Bos taurus species (Hereford, Angus, Charolais, Holstein, brown Swiss, Limousine, and Simmental), 0.043 to 0.229 in Asian Bos taurus breeds, except for Japanese black cattle (0.00), and 0.162 in Hanwoo. The MAF (C allele) of the 2258 SNP was 0.084 in this study (Table 4), which was lower than the frequency of the SNP in Yoon et al. (2003). This may be partly due to sampling effect, i.e. a small sample size (N = 242) in this study. For the 2258 C > T SNP, the high allele frequency of the favorable allele (C) in both European and Asian Bos taurus breeds indicate that selection for genetic improvement of ADG and CWT has been processed for the SNP or near the chromosomal region of the SNP.

There are some limitations in this association study. First of all, the sample size was small (N = 242), such that some significant SNPs for growth and carcass quality traits may not have been detected. Second, there may have been a chance of a false positive SNP, i.e. spurious SNPs with significant evidence that have no true effects on the tested traits. Some significant SNPs, e.g. the 303 C > T SNP for WT6 or the 2258 C > T SNP for CWT (Tables 3 and 4), had MAF less than 0.05, for which efficiency of marker-assisted selection would not be high.

Our results indicate that four SNPs in the bGH gene were associated with growth and carcass quality traits in Hanwoo (Tables 3 and 4). However, further study is needed to validate effects of the significant SNPs, before considering implementation of marker-assisted selection in Hanwoo commercial populations.

http://dx.doi.org/ 10.5713/ajas.2013.13248

ACKNOWLEDGEMENTS

This research was supported by a grant titled as "Development of production technologies for high quality & nutrional values of beef in Hanwoo from the Technology Development Program for Agriculture and Forestry (Project No. 311016-3), Ministry of Agriculture, Forestry, and Fisheries, Republic of Korea. Jong-Joo Kim's work was also supported by the Yeungnam University Research Grant 2012.

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Ji-Hong Leea, Yun-Mi Lee (1,a), Jea-Young Lee (2), Dong-Yep Oh (3), Dae-Jin Jeong (3), and Jong-Joo Kim (1), *

Gyeongbuk Provincial College, Yecheon, Gyeongbuk, Korea

* Corresponding Author: Jong-Joo Kim. Tel: +82-53-810-3027, Fax: +82-53-801-3027, E-mail: kimjj@ynu.ac.kr

(1) School of Biotechnology, Yeungnam University, Gyeongsan, Gyeongbuk, Korea.

(2) Department of Statistics, Yeungnam University, Gyeongsan, Gyeongbuk, Korea.

(3) Gyeongbuk Livestock Research institution, Yeongju, Gyeongbuk, Korea.

(a) The two authors contributed equally.

Submitted May 7, 2013; Accepted Jun. 15, 2013; Revised Jul. 1, 2013

Table 1. Sequences of primers for sequencing the bovine growth
hormone (bGH) gene in Hanwoo

                           Primer
             Primer name  size (bp)   Primer sequence

Sequencing   GH1-N1   F      20       CCAGGGATTGAACCTGAGTC
                      R      21       CCATTAGCACAGGCTGCCAGT
             GH1-N2   F      20       AGTGGAGACGGGATGATGAC
                      R      21       CCTCCTGGTCTCTCCCTAGGC
             GH1-N3   F      21       CATTTGGCCAAGTTTGAAATG
                      R      20       CATCCAGAACACCCAGGTTG
             GH1-N4   F      18       AACCGCGCACCAGCTTAG
                      R      20       GAGAAGCTGAAGGACCTGGA
             GH1-N5   F      20       TCTCACTGCTCCTCATCCAG
                      R      20       GCAGATCCTCAAGCAGACCT
             GH1-N6   F      20       CTTCGGCCTCTCTGTCTCTC
                      R      21       GAAGACAATAGCAGGCATGCT
Genotyping   GH1-P1   F      20       CCAGGGATTGAACCTGAGTC
                      R      20       TGAGTCGTCTGGTGAACTGG
             GH1-E1   F      20       ACGGGAACAGGATGAGTGAG
                      R      20       CACATTCGGAAGCCCTAAAG
             GH1-E2   F      20       CAGGTTGCCTTCTGCTTCTC
                      R      20       CGTGCATTCTCCTGGCTAAG
             GH1-E3   F      20       TTTTCCCCTTTTGAAACCTC
                      R      20       CGATGCAATTTCCTCATTTT

                                          Fragment    Annealing temp
             Primer name     Location     size (bp)    ([degrees]C)

Sequencing   GH1-N1   F       47-558         512            56
                      R                                     56
             GH1-N2   F       451-972        522            56
                      R                                     56
             GH1-N3   F      852-1,413       562            56
                      R                                     56
             GH1-N4   F     1,314-1,839      526            56
                      R                                     56
             GH1-N5   F     1,722-2,186      465            56
                      R                                     56
             GH1-N6   F     2,105-2,528      424            56
                      R                                     56
Genotyping   GH1-P1   F                      639            62
                      R                                     62
             GH1-E1   F                      328            58
                      R                                     58
             GH1-E2   F                      536            58
                      R                                     58
             GH1-E3   F                      428            54
                      R                                     54

Table 2. Genotype and allele frequencies of SNPs within the bGH
gene of Hanwoo

                          Genotype allele frequency
SNP          Position        (No. of individuals)

253 C > T    Promoter   CC(131)   CT(82)   TT(22)
                        0.557     0.349    0.094
303 C > T    Promoter   CC(202)   CT(28)   TT(5)
                        0.860     0.119    0.021
502 C > T    Promoter   CC(152)   CT(74)   TT(9)
                        0.647     0.315    0.038
559 G > A    Promoter   GG(231)   GA(4)    AA(0)
                        0.983     0.017    0.000
679 C > T    Exon1      CC(225)   CT(5)    TT(0)
                        0.978     0.022    0.000
1692 T > C   Intron3    CC(5)     CT(56)   TT(147)
                        0.024     0.269    0.707
2141 C > G   Exon5      CC(196)   CG(27)   GG(8)
                        0.848     0.117    0.035
2258 C > T   Exon5      CC(192)   CT(39)   TT(0)
                        0.831     0.169    0.000
2277 C > T   Exon5      CC(222)   CT(9)    TT(0)
                        0.961     0.039    0.000
2291 A > C   Exon5      CC(10)    CA(67)   AA(154)
                        0.043     0.290    0.667

             No. of
SNP          individuals   MAF (1)   H (2)   HWE (3)

253 C > T        235        0.268    0.392    0.089

303 C > T        235        0.081    0.149    0.002

502 C > T        235        0.196    0.315    0.999

559 G > A        235        0.009    0.017    0.895

679 C > T        230        0.011    0.022    0.868

1692 T > C       208        0.159    0.267    0.903

2141 C > G       231        0.093    0.169    0.000

2258 C > T       231        0.084    0.155    0.161

2277 C > T       231        0.019    0.038    0.763

2291 A > C       231        0.188    0.306    0.436

(1) Heterozygosity. (2) Minor allele frequency. (3) p value indicates
degree of deviation of genotype distribution from Hardy-Weinberg
equilibrium.

Table 3. Least square mean and standard error of genotype effects of
bGH gene for growth traits in Hanwoo

                Traits
                 (kg)

SNP 303 C > T                    CC(202)
                WT6      168.51 [+ or -] 1.77 (b)
                WT12     277.35 [+ or -] 2.27
                WT18     411.72 [+ or -] 2.98
                WT24     564.35 [+ or -] 4.03
                ADG        0.73 [+ or -] 0.01
2141 C > G                       CC(196)
                WT6      168.02 [+ or -] 1.78
                WT12     276.60 [+ or -] 2.34
                WT18     410.86 [+ or -] 3.09
                WT24     562.55 [+ or -] 4.13
                ADG        0.73 [+ or -] 0.01 (a)
2258 C > T                       CC(192)
                WT6      167.25 [+ or -] 1.89
                WT12     278.02 [+ or -] 2.46
                WT18     414.89 [+ or -] 3.23
                WT24     567.62 [+ or -] 4.33
                ADG        0.74 [+ or -] 0.01 (b)

                         Genotype means [+ or -]
                Traits    standard errors (No.
                 (kg)        of individuals)

SNP 303 C > T                    CT(28)
                WT6      170.53 [+ or -] 4.68 (b)
                WT12     284.18 [+ or -] 5.985
                WT18     428.40 [+ or -] 7.855
                WT24     577.10 [+ or -] 10.64
                ADG        0.75 [+ or -] 0.02
2141 C > G                       CG(27)
                WT6      167.95 [+ or -] 4.73
                WT12     281.04 [+ or -] 6.20
                WT18     420.74 [+ or -] 8.19
                WT24     566.09 [+ or -] 10.95
                ADG        0.74 [+ or -] 0.02 (a)
2258 C > T                       CT(39)
                WT6      168.46 [+ or -] 3.84
                WT12     273.14 [+ or -] 4.99
                WT18     400.85 [+ or -] 6.56
                WT24     548.59 [+ or -] 8.79
                ADG        0.71 [+ or -] 0.01 (a)

                Traits
                 (kg)                                p-value

SNP 303 C > T                     TT(5)
                WT6      137.81 [+ or -] 11.01 (a)   0.019
                WT12     261.69 [+ or -] 14.07       0.275
                WT18     404.56 [+ or -] 18.46       0.114
                WT24     594.13 [+ or -] 25.00       0.284
                ADG        0.81 [+ or -] 0.04        0.062
2141 C > G                        GG(8)
                WT6      149.54 [+ or -] 8.55        0.103
                WT12     276.18 [+ or -] 11.21       0.788
                WT18     418.93 [+ or -] 14.80       0.470
                WT24     596.31 [+ or -] 19.79       0.241
                ADG        0.81 [+ or -] 0.03 (b)    0.038
2258 C > T                        TT(0)
                WT6                                  0.779
                WT12                                 0.381
                WT18                                 0.057
                WT24                                 0.054
                ADG                                  0.015

(a,b) Mean values with different superscript letters within the same
row are significantly different (p < 0.05).

Table 4. Least square mean and standard error of genotype effects of
bGH gene for carcass quality traits in Hanwoo

SNP               Traits

559 G > A                               GG(231)
             CWT (kg)            309.62 [+ or -] 2.18
             LMA ([cm.sup.2])     76.17 [+ or -] 0.55 (b)
             BF (mm)               7.10 [+ or -] 0.19
             MS                    5.82 [+ or -] 0.23
2258 C > T                              CC(192)
             CWT (kg)            310.41 [+ or -] 2.41 (b)
             LMA ([cm.sup.2])     76.11 [+ or -] 0.61
             BF (mm)               6.97 [+ or -] 0.21
             MS                    5.79 [+ or -] 0.27

                                Genotype means [+ or -]
                                    standard errors
SNP               Traits          (No. of individuals)

559 G > A                                GA(4)             AA(0)
             CWT (kg)            296.37 [+ or -] 15.44
             LMA ([cm.sup.2])     67.89 [+ or -] 3.89 (a)
             BF (mm)               7.80 [+ or -] 1.36
             MS                    3.89 [+ or -] 1.65
2258 C > T                               CT(39)            TT(0)
             CWT (kg)            298.50 [+ or -] 4.93 (a)
             LMA ([cm.sup.2])     74.93 [+ or -] 1.24
             BF (mm)               7.40 [+ or -] 0.44
             MS                    5.48 [+ or -] 0.54

SNP               Traits        p-value

559 G > A
             CWT (kg)           0.397
             LMA ([cm.sup.2])   0.037
             BF (mm)            0.614
             MS                 0.249
2258 C > T
             CWT (kg)           0.031
             LMA ([cm.sup.2])   0.392
             BF (mm)            0.375
             MS                 0.615

(a,b) Mean values with different superscript letters within the same
row are significantly different (p < 0.05).
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Author:Leea, Ji-Hong; Lee, Yun-Mi; Lee, Jea-Young; Oh, Dong-Yep; Jeong, Dae-Jin; Kim, Jong-Joo
Publication:Asian - Australasian Journal of Animal Sciences
Article Type:Report
Geographic Code:9SOUT
Date:Oct 1, 2013
Words:4406
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