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Article

Effect of Growth Hormone Exon-5 Polymorphism on Growth Traits, Body Measurements, Slaughter and Carcass Characteristics, and Meat Quality in Meat-Type Lambs in Turkey

by
Vasfiye Kader Esen
1,* and
Cengiz Elmacı
2
1
Department of Breeding and Genetics, Sheep Breeding Research Institute, Balıkesir 10200, Turkey
2
Department of Animal Science, Faculty of Agriculture, Bursa Uludag University, Görükle Campus, Bursa 16059, Turkey
*
Author to whom correspondence should be addressed.
Ruminants 2022, 2(4), 420-434; https://doi.org/10.3390/ruminants2040029
Submission received: 29 September 2022 / Revised: 29 October 2022 / Accepted: 1 November 2022 / Published: 2 November 2022
(This article belongs to the Special Issue Feature Papers of Ruminants 2021-2022)
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Abstract

:
This study examined the relationship between GHE5 polymorphisms and growth and carcass characteristics of meat-type sheep breeds reared in Turkey. A total of 202 lambs were tested, consisting of five breeds. By SSCP analysis and nucleotide sequencing, 14 nucleotide changes (12 substitutions and two deletions) were identified in four variants of GHE5. In the coding region of GHE5, five substitutions occur, including c.1588C>Y(C/T) (Ala160Val), c.1603A>M(A/C), c.1604G>S(G/C) (Lys165Thr), c.1606A>W(A/T) (Gln166Leu), and c.1664C>Y(C/T). P3 female and P1 male lambs had the highest rump height at weaning, whereas P3 females and P2 males had the highest chest depth (p < 0.05). At yearling, P1 variant lambs have longer body length (BL; p < 0.05), wider leg circumferences, and thinner cannon bone perimeter (CBP) (p > 0.01), in contrast to P2 variant lambs, which have a shorter BL and thicker CBP. Furthermore, P2 had a greater percentage of neck, shoulder, and leg, P1 had a greater percentage of loin, and P3 had a greater percentage of rack, but there was no significant difference between them. A marker-assisted selection approach can be used to improve sheep carcass quality traits by taking advantage of the nucleotide substitutions found on GHE5 and the detected differences between variants.

1. Introduction

As a result of the global food shortage, researchers are striving to increase food production volumes while maintaining quality characteristics that are essential to human health. In addition to being a major source of protein, meat also contains vitamins, minerals, and fats, including fatty acids that are crucial to human nutrition [1]. It is important to develop better ways to use sheep breeds’ gene pools to increase meat and milk productivity. Animal producers can improve their economic performance by reducing feed costs per unit, monitoring genetics, controlling selection, and developing supplementary reserves. By identifying genes that underlie valuable traits, undesirable traits can be eliminated, while important traits, such as litter size, growth traits, and meat quality, can remain [2,3]. Therefore, it is essential to identify the mutations that determine animals’ valuable characteristics.
The use of DNA technology allows new methods for assessing animals to identify genes that are directly or indirectly related to commercially important qualities [4,5]. Moreover, it is possible to breed out the preferred gene variants directly on the DNA level and conduct genomic selections along with conventional selections.
Farm animal growth characteristics can be determined using the GH gene, which plays an important role in growth metabolism. GH regulates growth and metabolism in various farm animals by improving body and carcass size due to its functions, such as protein synthesis and fat separation [6]. GH genes share 97.5% homology in sheep and cattle due to a series of five exons and four introns at 1792 base pairs (bp) on the 11th chromosome [7].
A number of farm animals, including buffalo, cows, goats, and sheep, possess the GH gene, and mutations in the GH gene affect growth, carcass weight, and milk production [8]. A change in exon-5 (GHE5) or intron-3 affects milk properties, while a change in the promoter region affects carcass weight and fat content [9,10]. As well, An et al. [11] demonstrated that goats can convert glycine amino acid into serine when a C>T nucleotide change occurs in exon-3 (GHE3), and proline can be turned into histidine when a C>A nucleotide change occurs in GHE5. It is important to note, however, that these changes in nucleotides do not always result in amino acid differentiation. As an example, Bahrami et al. [12] showed that, despite the presence of polymorphism between exon-4 (GHE4) and GHE5, only one (G.1507G>C) is involved in amino acid differentiation (glycine>tyrosine), despite observing two nucleotide changes (G.1486A>G, G.1489G>C) in GHE4 and three in GHE5 (G.1503G>C, G.1507G>C, and G.1509A>G).
In Turkey, there is a widespread use of the Merino (which reproduces throughout the year and develops earlier) and indigenous Kıvırcık (high meat quality and flavor, disease resistance, thin tail structure, and marbling) breeds, as well as crossbreeds derived from these two breeds in order to meet the demand of the market [13,14]. Furthermore, lamb meat producers, particularly in the western part of Turkey, tend to keep more than one genotype in their herd, primarily because of their curiosity about their adaptability, growth rate, and rearing or fattening practices, such as Suffolk or Ramlıç (crossbreeding Rambouillet with Daglıç) [15]. The lack of molecular characterization of these meat-type breeds prevents genetic variation from being effectively utilized in animal breeding programs. Further, to the best of our knowledge, no studies have investigated the GHE5 polymorphism among these sheep breeds. Previous studies have also demonstrated that the SSCP method is an effective tool for determining the relationship between polymorphisms and yield traits in farm animals [16,17]. Therefore, the purpose of this study was to investigate the effects of the GHE5 polymorphism on lamb growth traits, body measurements, slaughter characteristics, and meat quality using the SSCP method.

2. Materials and Methods

2.1. Ethical Approval

The Ethical Committee at the Sheep Breeding Research Institute in Balikesir, Turkey, cleared the investigation before commencing (Approval number: 13360037), and in the same Institute’s experimental farm unit from January through June 2018, animal care and handling procedures were followed in accordance with the Declaration of Helsinki guidelines.

2.2. Animals and Feeding Regimens

In the current study, the animal background and feeding regimens were derived from the studies by Kader Esen et al. [15], Kader Esen and Elmaci [18], and Kader Esen et al. [19,20]. We studied 202 later-born lambs from five different meat-type breeds [15 Males (M) and 36 Females (F) of Kıvırcık (K), 14 M and 33 F of Karacabey Merino (KM), 14 M and 14 F of Ramlıç (R), 15 M and 34 F German Black-Head Mutton × Kıvırcık (GBK), 11 M and 16 F of Hampshire Down × Merino crossbreed (HM)] whose mean weaning age was 90.5 ± 5.7 days (mean ± SD). The lambs were housed in separate barns with their dams and suckled twice a day during the pre-weaning period. Once 15 days of age, commercial starter feed and high-quality alfalfa hay were available ad libitum. From weaning to yearling, lambs of various breeds were housed together in a single flock, and they received an average of 600 g/lamb of concentrate feed, 100 g/lamb of alfalfa hay, and 300 g/lamb of vetches–wheat mixture hay per day during the weaning period to slaughter. For the purpose of preventing unwanted matings, male and female lambs were separated after slaughter. The lambs were pastured between slaughtering and a yearling period when the weather permitted, and they received the same amount of concentrate feed, alfalfa hay, vetches–wheat mixture hay, and wheat straw ad libitum. The chemical composition of the concentrates and roughages used in this study can be seen in Table 1.

2.3. DNA Extraction, Primer Design, PCR Amplification, SSCP, and DNA Sequencing

2.3.1. DNA Extraction

Before slaughtering male lambs, blood samples were collected into sterile EDTA tubes from all lambs. Genomic DNA was amplified using a GeneAll® DNA extraction kit using the Bio-Rad T100 thermal cycler.

2.3.2. Primer Design, PCR Amplification, and SSCP Analysis

PCR primers were designed by Bahrami et al. [12] for 365 bp of GHE5. Amplification was performed with a commercial kit GeneAll® 2XAmpMaster in a 20 µL reaction containing DNA and each primer at 100 ng. After 1 min at 95 °C, 30 cycles of 30 s at 95 °C, 30 s at 60 °C, and 30 s at 72 °C followed, with a final extension of 10 min at 72 °C are used for the exon 5 region amplified. Amplification was visualized by electrophoresis 3% agarose gels, using 1× TAE Buffer.
PCR products were mixed 1:10 with loading dye containing 98% formamide and denaturated at 95 °C for 7 min. Samples were then cooled rapidly on wet ice, and acrylamide: bisacrylamide gels (29:11) were made in accordance with Green and Sambrook [21]. A vertical electrophoresis was used for 4 h at 350 V. A silver staining technique was used, according to Byun et al. [22], by modifying the formaldehyde ratio to 2% in order to make electrophoresis bands visible.

2.3.3. DNA Sequencing

Based on the PCR-SSCP band models, DNA sequences were obtained from each pattern using an ABI PRISM genetic analyzer (Applied Biosystem, Foster City, CA, USA). We visualized chromatograms using Bioedit Sequence Alignment Editor, discarded noisy sequences, and aligned clear sequences. The NCBI GeneBank databases were searched using nucleotide differences determined by the BLAST Algorithm between the pattern and reference sequence (Accession number: AF.002110).

2.4. Live Weight, Linear Body Measurement, and In Vivo Ultrasonographic Measurements

Lambs’ birth weights (BW) were recorded within 12 h of birth, while live weights (LW), linear body measurements, and ultrasonographic measurements were taken on the 90th, 180th, and 360th days of the study. Before morning feeding, lambs were weighed to avoid errors due to stomach fill. An experienced technician measured a lamb’s linear body measurements while standing with its head raised. A flexible calibrated tape and calipers were used to record the body lengths (BL), withers heights (WH), back heights (BH), rump heights (RH), chest depths (CD), chest widths (CW), rump widths (RW), chest circumferences (CC), leg circumferences (LC), and cannon bone perimeters (CBP) of individual lambs [23].
With a real-time ultrasound device (Mindray DP-20) and linear veterinary ultrasound transducer (Mindray 75L50EAV) operating at 7.5 MHz, the Musculus longissimus dorsi depth (MLDD), fat thickness (FT), and skin thickness (ST) of lambs between the 12th and 13th ribs were monitored after linear body measurements were recorded on each specified period [24]. Before placing the probe, the lambs were manually immobilized, their wools between the 12th and 13th ribs were parted manually, and the ultrasonic gel was used as a couplant. Measurements were taken on the left side, 4 cm away from the vertebral column. The pressure on the transducer head was kept to a minimum to prevent fat compression. The electronic calipers of the scanner were used to measure MLDD, FT, and ST after the scanned image had been captured.

2.5. Slaughter and Carcass Characteristics and Meat Quality Assessment

We randomly selected 50 male lambs from each breed in order to evaluate slaughter and carcass characteristics and meat quality. A 12-h fast and access to freshwater were provided to lambs at the Institute’s slaughterhouse before slaughter, and then they were slaughtered in accordance with commercial procedures. Slaughter weight (SW) of lambs were immediately recorded before slaughter. After skinning, we removed non-carcass components (heads, skins, feet, lungs, liver, heart, spleen, testicles, and gastrointestinal tract) and recorded hot carcass weight (HCW, including kidneys and perinephric-pelvic fat). By dividing the HCW by the SW, we calculated the hot dressing percentage (HDP). Cold carcass weight (CCW) was determined after chilled carcasses were stored at −4 °C for 24 h, and cold dressing percentage (CDP) was calculated.
We harvested the Longissimus thoracis et lumborum (LTL) muscle between the 5th and 12th thoracic vertebrae for further analysis in the laboratory after cutting each carcass into five primal parts [neck, shoulder, rack, loin, and leg] [25]. From photographs of the chilled carcass, [area (MLDA, perimeter (MLDP), depth (MLDD), width (MLDW), and fat thickness (MLDFT)] and body fatness (BF) were measured using the Fiji image measurement program (Version 1.52d) [26]. In order to measure LTL color, a white tile was calibrated with a D 65 illuminant, observed at a 10° observer angle, and observed with a colorimeter (Chroma Meter CR-410; Konica Minolta, Tokyo, Japan) [27]. Averaging three measurements after storing the samples at 4 °C for 0, 48, and 168 h determined the value of lightness (L*), redness (a*), yellowness (b*), chroma (C), and hue (h). The filter-paper method was used to determine water holding capacity (WHC) in accordance with Honikel and Hamm’s [28] description. A sample of LTL was evaluated for thawing loss (TL) and cooking loss (CL), as previously described by Choi and Kim [29] and Gonzales-Barron et al. [30]. We measured the LTL shear force (SF) on cooked samples in the Central Research Laboratory of Namık Kemal University, Tekirdağ, Turkey. Cooked LTL samples were tested using a TA.HDplus Texture Analyser and an HDP/WBV Warner Bratzler Blade from Stable Micro Systems Ltd., Surrey, UK.

2.6. Statistical Analysis

The General Linear Model procedure of Minitab [31] was used to assess the influence of GHE5 polymorphism on LW, linear body measurements, in vivo ultrasonographic measurements, slaughter and carcass characteristics, and meat quality. The repeat-measures analysis of variance was used to test whether there was a statistically significant difference between the color parameters. There have been previous adjustments made for the breed (K, KM, R, GBK, HM), gender (M, F), birth type (single, twin), dam age (2, 3, 4, 5, 6, 7+), genotype (P1, P2, P3, P4), time (90th, 180th, 360th days) the interaction between them.

3. Results

Eleven lambs were excluded from the study due to unclear genotyping (n = 4) and a small number of distributions (P4, n = 7) at the GHE5 locus.
Using the PCR-SSCP method, four different patterns were found on PCR products on polyacrylamide gels. In the NCBI GeneBank OP535358-OP535361, four unique PCR-SSCP patterns were deposited as sequences P1, P2, P3, and P4. The sequences obtained from sanger sequencing were accelerated by the Clustal W algorithm in the Bioedit program and crosschecked with the accession number AF002110.1 (Figure 1).
Two deletions (c.1563-71_c.1563-70delAA) were detected when comparing the pattern sequences and reference sequences on P1, P2, and P3 variants (Table 2). Moreover, two heterozygous substitutions [c.1563-29G>R(A/G) and c.1588C>Y(C/T)] were detected in the P2 variant. P3 variant, on the other hand, has the same deletion (c.1563-71_c.1563-70delAA) plus four substitutions [homozygous c.1563-70A>G, heterozygous c.1563-48C>S(G/C), c.1563-47C>M(A/C), and c.1664C>Y(C/T)]. There was also one deletion (c.1563-70delA) and seven substitutions [homozygous c.1563-71A>C, heterozygous c.1563-29G>R(A/G), c.1563-10C>S(G/C), C.1563-3C>Y(C/T), c.1603A>M(A/C), c.1604G>S(G/C), c.1606A>W(A/T)] were determined in P4 variant. Further, the sequenced region contains nucleotides 1561–1763 of the encoded region, with remaining nucleotides in the non-coding region.
Further analysis of the allelic variants of the GHE5 gene indicated no significant differences between male and female lambs in BW or LW recorded at different stages (p > 0.05; Figure 2). It has been observed that P3 variants in female lambs are 2.14–10.16% heavier than other variants, whereas P2 variants in male lambs are 2.86–8.33% heavier than other variants. Weight differences between male and female variants of LW180d (5.05 kg and 0.69 kg) began to widen over time, and this difference increased even more in adulthood (LW360d; and 42.46 kg 1.34 kg). In Figure 2, it is evident that this difference is not a consequence of genotype or gender but rather a result of the breed.
Figure S1 illustrates the effects of GHE5 polymorphism on body measurements at different times in meat-type lambs. Statistically significant differences were seen in RH and CD between the GHE5 variants at weaning (LW90d; p < 0.05); and BL (p < 0.05), LC, and CBP (p < 0.01) at yearling (LW360d). Nevertheless, none of the other body measurements was significantly affected at six months (LW180d; p > 0.05). P3 females and P1 male lambs had the highest RH at weaning (59.68 and 59.32 cm, respectively), whereas P3 females and P2 males had the highest CD (24.29 and 24.60 cm, respectively) (Figure S1a). However, the difference in RH and CD disappeared at six months (Figure S1b). Although BL, LC, and CBP were similar between variants in female lambs, they differed significantly in male lambs (p < 0.05 for BL and p < 0.01 for LC and CBP; Figure S1c). At yearling, P1 variant lambs have a longer BL, wider LC, and thinner CBP, in contrast to P2 variant lambs, which have a shorter BL and thicker CBP.
In real-time ultrasound measurements, none of the three parameters (MLDD, FT, and ST) differed significantly between female and male lambs on the basis of GHE5 variants (p > 0.05; Figure 3). Taking into account the number of P2 variants at the sixth month and yearling, it is obvious that the MLDD of P3 variant male lambs is higher than that of other variants.
A comparison of the carcass parameters of the GHE5 variants is provided in Figure 4. There was no significant difference in all studied parameters (p > 0.05) between variants. P1 variants recorded the highest SW (43.40 kg), HCW (20.82 kg), CCW (20.16 kg), HDP (47.94%), and CDP (46.41%), while P2 variants recorded the highest T45m (36.53 °C), T24h (7.03 °C), pH45 (6.41), and pH24h (5.56). GHE5 variants had CLs ranging from 1.30–1.53%. Similarly, none of the Musculus longissimus dorsi parameters (MLDA, MLDP, MLDD, MLDW, MLDFT) and BF were significant following image processing. P2 variants had a higher value for MLDW (6.91 cm), while P1 variants had higher values for MLDA (17.35 cm2), MLDP (17.80 cm), and MLDD (3.42 cm). In addition, the P3 variant showed a leaner profile than the other variants, with a lower MLDFT of 8.61–9.87% as well as a lower BF of 12.86–17.86%.
In Figure 5, the effects of GHE5 polymorphism on noncarcass components are presented. There was no significant difference between the non-carcass components (p > 0.05). It is noteworthy that the head (0.03–0.06 kg), feet (20–60 g), testicles (41.5–72.1 g), heart (14.4–43.3 g), liver (15.0–45.7 g), spleen (18.0–36.6 g), full stomach (0.43–0.65 kg), and empty stomach (0.07–0.18 kg) weights were higher in the P3 variant; lung (57.5–61.2 g), full intestine (0.06–0.22 kg), empty intestine (0.05–0.014 kg), omental and mesenteric fat (44.0–68.9 g), and kidney fat (5.2–11.0 g) weights were higher in the P1 variant; skin (0.19–0.21 kg), kidney (1.5–1.9 g), and other (red offals) weights (33.8–58.6 g) in the P2 variant.
The GHE5 polymorphism had no significant effect on meat-type lamb neck, shoulder, rack, loin, or leg proportions, as shown in Figure 6. There was a higher neck (0.14–0.30%), shoulder (0.18–0.74%), and leg (0.08–0.42%) percentage in the P2 variant, whereas the P3 variant had a higher rack (0.71–1.11%) percentage, and the P1 variant had a higher loin (0.46–0.70%) percentage.
A comparison of the meat quality assessment of GHE5 variants in meat-type lambs is shown in Figure 7, showing the highest SF (5.05 kg), WHC (20.15%), and TL (8.65%) observed in the P2 variant and the highest CL (28.88%) in P3 variant. Nevertheless, none of these values were statistically significant (p > 0.05).
As shown in Figure 8, no significant interactions between genotype and time were observed for all color parameters at various storage periods (p > 0.05). A clear trend can be observed in terms of L* and h values in all variants. After 48 h of storage, a decrease in a* and C was detected up to the 168th h. At the end of the storage period, the P2 variant had higher L*, b*, and h values than the other variants but had lower a* and C values.

4. Discussion

A major objective of genomic selection is to select animals with the most superior performance and to transmit them to the next generation [32]. If structural and functional genomic approaches are combined, phenotypic differences between animals can be studied from a completely different perspective, which may lead to differences in final products [33]. Therefore, identifying genetic markers and candidate genes associated with economically important traits is highly valuable from both a biological and practical perspective [34].
In several studies, the GH gene, which is polymorphic in farm animals, has been shown to play a key role in growth, development, carcass quality, and milk yield [6,8,10,35]. Based on polyacrylamide gel electrophoresis bands determined by the SSCP method, our study confirms that GH levels can influence growth changes in meat-type lambs. Similar results were reported by Bastos et al. [36] in Churra de Quente sheep, where they detected two variants of GHE4 and five variants of GHE5. However, some research indicates that different exons of GH are monomorphic in different breeds [37].
In a study conducted to determine GH polymorphism in the Salsk sheep breed by using the PCR-RFLP method and endonuclease HaeIII restriction enzyme, Gorlov et al. [38] found three different genotypes (AA, AB, and BB). They also revealed that weaning weight, weight at the age of nine months, and the average daily gain of the ram lamb with the AB genotype exceeded the values of these parameters of the ram lamb with the AA genotype by 0.92 kg, 10.67 kg, and 47.3 g, respectively. The same method and enzyme were applied in another study using Boer goat bucks, and two SNPs were identified by GH gene sequencing [A781G (Ser/Gly35) and A1575G (Leu147)]. Researchers found that CC genotypes were taller than CD genotypes and that Boer bucks with AA genotypes were born with smaller CCs at birth [39]. This study, however, detected four different variants using the PCR-SSCP method, of which one (P4) was excluded from statistical analysis. In the study, we found that females carrying the P3 variant had weights of 100–440 g at birth, and males carrying the P2 variant weighed 130–360 g more than those carrying the other variants. At other periods, the P3 variant did not show increased values for females; however, after the sixth month, the P1 variant displayed higher values for males (Figure 2).
It has been shown that c.1286T>C nucleotide changes affect lamb LW, WH, BL, and CW in Tibetan and Poll Dorset sheep [40]. Similarly, five variants of GHE4 affect Makooei sheep’s LW and weight at six months and nine months [41]. The SNPs G871A, G1383A, and A1509G affected Harri sheep’s LW [42]. Awassi ewes’ GH gene variant affects lamb BW as well as the WH, RH, and CC between birth and weaning [43]. Furthermore, an SNP on the GH gene intron 2 region (C>A) significantly affects the LW of Santa Ines sheep on the 100th day [44]. GHE5 polymorphism significantly affects RH and CD at weaning (90th day) (Figure S1a). This can be attributed to c.1563-48>S(G/C), c.1563-47>M(A/C), c.1664>Y(C/T) nucleotide substitutions. Therefore, we thought that causes the higher RH and wider CD in female lambs with the P3 variant, but this effect dissipated as time progressed. During the weaning period, the highest levels of RH and CD were observed in males of P1 and P2 variants, respectively. It is possible that the c.1588>Y(C/T) mutation resulting in the change of amino acids (p.Ala160Val) may lead to a wider CD in male lambs with the P2 variant, whereas wild-type P1 males have a higher RH. Furthermore, there was no significant difference between wild-type and mutant female GHE5 variants, but wild-type male P1 variants had a higher BL and LC, and P3 variants had a thinner CBP than other male GHE5 variants at yearling (Figure S1c). This can be attributed to c.1603A>M(A/C), c.1604G>S(G/C), c.1606A>W(A/T) nucleotide substitutions, which are leading to aminoacid changes (p.Lys165Thr, p.Gln166Leu). Therefore, we thought that causes the CBP to be thicker in male lambs with the P3 variant.
Considering that 97.5% homology exists between the bovine and sheep GH genes, it may make sense to evaluate such studies together since studies on polymorphism, and meat quality in sheep are limited in the literature. Previous studies have demonstrated that GH gene variants affect the MLDA of Hereford and Limousin cattle as well as the 559G>A SNP in Hanwoo cattle [45,46]. It was found that the GHE5 polymorphism did not have a significant effect on Musculus longissimus dorsi development over time (p > 0.05) (Figure 3). Despite the fact that our results differ from Lee et al. [45] and Sedykh et al. [46], they were similar to Özay’s [47] study, which demonstrated that GHE1 polymorphism did not affect the measurement of MLD in Kıvırcık sheep.
A close relationship has been shown between GH and IGF1 since GH stimulates the liver to express IGF1, which negatively affects pituitary GH production [48,49]. Thus, it is possible to select carcass traits correlated with body growth by considering polymorphisms in GH and IGF1 in this case [49]. The carcass parameters did not differ significantly between GHE5 variants (p > 0.05). However, the SW, HCW, and CCW of P1 variants were higher than those of the other variants by 0.86–1.54 kg, by 0.83–0.91 kg, and by 0.73–0.82 kg, accordingly (Figure 4). In addition, P1 variants had higher MLDA (17.35 cm2), MLDP (17.80 cm), and MLDD (3.42 cm) values, whereas P3 variants had lower BF (7.39 mm) and MLDFT (4.76 mm).
It is rare to find studies exploring association tests with sheep GH polymorphisms. Salsk sheep were first associated with GH/HaeIII polymorphisms in a study by Gorlov et al. [38] with carcass traits such as carcass weight and yields, as well as heart and kidney weights. Meira et al. [49] then found that an SNP (rs589527314) was associated with carcass weights and yields as well as carcass finishing scores in Santa Ines sheep. In contrast to Gorlov et al. [38] and Meira et al. [49], this study did not demonstrate any effect of the GHE5 polymorphism on non-carcass components (p > 0.05; Figure 5). On the other hand, cattle GH polymorphisms have been researched more extensively. In accordance with our results, there has been no significant effect of GH polymorphism on carcass yields in Indonesian domestic cattle breeds [50] or GHE5 polymorphism in Zavot cattle [51]. Akçay et al. [51] also found that GHE5 polymorphism does not affect either LW nor CW in Zavot cattle. Furthermore, Han et al. [52] found that Hanwoo cattle with the GH1 Leu/Leu genotype have higher SW, CW, BF, MLDA, and marbling scores, but no statistical significance was found. In addition, it was found that the bGH genotype had a significant effect on yearling weight in Canchim cattle, with positive effects associated with the LV (leucine/valine) genotype [53]. As compared to homozygous Brangus bulls exhibiting the GH-MspI RFLP genotype, Hua et al. [39] indicated that heterozygous bulls with the genotype showed higher carcass ultrasound measurements and average daily gain.
There was no significant difference in SF between CC, CD, and DD genotypes of bovine GH, as found by Costello et al. [54]. Likewise, Han et al. [52] demonstrated that GH1 polymorphism did not significantly affect the meat and fat color, as defined by Korean legal grading standards where carcass and fat are scored between 1 and 7 in Hanwoo cattle. Similar to these studies [52,54], GHE5 polymorphisms did not affect meat color, a key criterion for determining meat quality.

5. Conclusions

In the current study, we investigated the association between GHE5 polymorphisms and meat quality characteristics in meat-type sheep breeds reared in Turkey using PCR-SSCP. The relation between GHE5 variants and several growth and carcass traits, including body measurements, MLD development, weights, carcass, and noncarcass components, retail carcass percentage, meat quality, and color change during storage, was established. In conclusion, through the use of nucleotide substitutions on GHE5 and detected differences between variants, a marker-assisted selection approach can improve sheep carcass quality traits. It is also recommended that the results obtained be confirmed with studies conducted on a larger population.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ruminants2040029/s1. Figure S1: Effect of GHE5 polymorphism on body measurements at different periods in meat-type lambs.

Author Contributions

Conceptualization, V.K.E. and C.E.; methodology, V.K.E.; software, V.K.E.; validation, V.K.E.; formal analysis, V.K.E.; investigation, V.K.E.; resources, V.K.E.; data curation, V.K.E.; writing—original draft preparation, V.K.E.; writing—review and editing, V.K.E.; visualization, V.K.E.; supervision, C.E.; project administration, V.K.E.; funding acquisition, V.K.E. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Ministry of Agriculture and Forestry, General Directorate of Agricultural Research of the Republic of Turkey, grant number TAGEM/HAYSUD/B/18/A4/P2/308.

Institutional Review Board Statement

The animal study protocol was approved by the Ethics Committee of Sheep Breeding Research Institute, Balıkesir, Turkey (protocol code 13360037 and date of approval 11 April 2018).

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The Ph.D. thesis of Vasfiye Kader Esen, on which this paper is based, inspired the development of this paper. The authors would like to thank Selim Esen and Orhan Karadağ for their assistance in collecting data, laboratory analysis, and valuable contributions to this study.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Figure 1. ClustalW algorithm-based alignment of the GHE5 variants’ sequences with the NCBI reference sequence AF002110.1.
Figure 1. ClustalW algorithm-based alignment of the GHE5 variants’ sequences with the NCBI reference sequence AF002110.1.
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Figure 2. Effects of GHE5 polymorphism on live weight at different periods. BW: Birth weight, LW: Live weight.
Figure 2. Effects of GHE5 polymorphism on live weight at different periods. BW: Birth weight, LW: Live weight.
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Figure 3. Effect of GHE5 polymorphism on Musculus longissimus dorsi development at different periods in meat-type lambs. MLDD: Musculus longissimus dorsi depth; FT: Fat thickness; ST: Skin thickness.
Figure 3. Effect of GHE5 polymorphism on Musculus longissimus dorsi development at different periods in meat-type lambs. MLDD: Musculus longissimus dorsi depth; FT: Fat thickness; ST: Skin thickness.
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Figure 4. Effect of GHE5 polymorphism on carcass parameters in meat-type lambs. SW: Slaughter weight; HCW: Hot carcass weight; HDP: Hot dressing percentage; CCW: Cold carcass weight; CDP: Cold dressing percentage; ChL: Chilling loss; T45m: Carcass temperature after 45 min, T24h: Carcass temperature after 24 h, MLDA: Musculus longissimus dorsi area, MLDP: Musculus longissimus dorsi perimeter, MLDD: Musculus longissimus dorsi depth, MLDW: Musculus longissimus dorsi width, MLDFT: Fat thickness of Musculus longissimus dorsi, BF: Body fatness.
Figure 4. Effect of GHE5 polymorphism on carcass parameters in meat-type lambs. SW: Slaughter weight; HCW: Hot carcass weight; HDP: Hot dressing percentage; CCW: Cold carcass weight; CDP: Cold dressing percentage; ChL: Chilling loss; T45m: Carcass temperature after 45 min, T24h: Carcass temperature after 24 h, MLDA: Musculus longissimus dorsi area, MLDP: Musculus longissimus dorsi perimeter, MLDD: Musculus longissimus dorsi depth, MLDW: Musculus longissimus dorsi width, MLDFT: Fat thickness of Musculus longissimus dorsi, BF: Body fatness.
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Figure 5. Effect of GHE5 polymorphism on non-carcass components in meat-type lambs. O and M fat: Omental and mesenteric fat. 1 weight after chilling at 4 °C for 24 h.
Figure 5. Effect of GHE5 polymorphism on non-carcass components in meat-type lambs. O and M fat: Omental and mesenteric fat. 1 weight after chilling at 4 °C for 24 h.
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Figure 6. Effect of GHE5 polymorphism on retail carcass percentage of meat-type lambs.
Figure 6. Effect of GHE5 polymorphism on retail carcass percentage of meat-type lambs.
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Figure 7. Effect of GHE5 polymorphism on meat quality assessment SF: Shear force; WHC: Water holding capacity; TL: Thawing loss; CL: Cooking loss.
Figure 7. Effect of GHE5 polymorphism on meat quality assessment SF: Shear force; WHC: Water holding capacity; TL: Thawing loss; CL: Cooking loss.
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Figure 8. Genotype × time interaction on color parameters of Longissimus thoracis et lumborum muscle during the storage period. L*: lightness, a*: redness, b*: yellowness, C: chroma, h: hue.
Figure 8. Genotype × time interaction on color parameters of Longissimus thoracis et lumborum muscle during the storage period. L*: lightness, a*: redness, b*: yellowness, C: chroma, h: hue.
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Table
Table 1. Chemical composition of concentrate and roughages 1.
Table 1. Chemical composition of concentrate and roughages 1.
ItemDMCP CAEECFNDFADF
Concentrate feed89.4412.659.433.229.6639.9012.95
Alfalfa hay87.4923.2014.512.0720.3835.4323.00
Vetch–wheat mixture hay89.498.715.661.2641.8663.5946.68
DM: Dry matter (g/kg fed basis); CP: Crude protein (g/kg DM); CA: Crude Ash (g/kg DM); EE: Ether extract (g/kg DM); CF: Crude fiber (g/kg DM); NDF: Neutral detergent fiber (g/kg DM); ADF: Acid detergent fiber (g/kg DM). 1 Data in the table is extracted from Kader Esen et al. [15].
Table
Table 2. Sequence variation in GHE5.
Table 2. Sequence variation in GHE5.
NoPosition 1Nucleotide Sequences Chromosome Location 2SNP rs IDAmino Acid Changing
P1P2P3P4
1c.1563-71---C11:14,855,698--
2c.1563-70----11:14,855,699--
3c.1563-69AAGA11:14,855,701--
4c.1563-48CCS(G/C)C11:14,855,722--
5c.1563-47CCM(A/C)C11:14,855,723--
6c.1563-29GR(A/G)GR(A/G)11:14,855,741--
7c.1563-10CCCS(G/C)11:14,855,760--
8c.1563-3CCCY(C/T)11:14,855,767--
9c.1588CY(C/T)CC11:14,855,795-p.Ala160Val
10c.1603AAAM(A/C)11:14,855,809-p.Lys165Thr
11c.1604GGGS(G/C)11:14,855,810-p.Lys165Thr
12c.1606AAAW(A/T)11:14,855,812-p.Gln166Leu
13c.1664CCY(C/T)C11:14,855,871rs.596456087-
1 Positions are numbered according to the guidelines presented on AF002110.1. 2 Chromosome locations are given according to the guidelines presented on ENSOARG00020016511.
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Esen, V.K.; Elmacı, C. Effect of Growth Hormone Exon-5 Polymorphism on Growth Traits, Body Measurements, Slaughter and Carcass Characteristics, and Meat Quality in Meat-Type Lambs in Turkey. Ruminants 2022, 2, 420-434. https://doi.org/10.3390/ruminants2040029

AMA Style

Esen VK, Elmacı C. Effect of Growth Hormone Exon-5 Polymorphism on Growth Traits, Body Measurements, Slaughter and Carcass Characteristics, and Meat Quality in Meat-Type Lambs in Turkey. Ruminants. 2022; 2(4):420-434. https://doi.org/10.3390/ruminants2040029

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Esen, Vasfiye Kader, and Cengiz Elmacı. 2022. "Effect of Growth Hormone Exon-5 Polymorphism on Growth Traits, Body Measurements, Slaughter and Carcass Characteristics, and Meat Quality in Meat-Type Lambs in Turkey" Ruminants 2, no. 4: 420-434. https://doi.org/10.3390/ruminants2040029

APA Style

Esen, V. K., & Elmacı, C. (2022). Effect of Growth Hormone Exon-5 Polymorphism on Growth Traits, Body Measurements, Slaughter and Carcass Characteristics, and Meat Quality in Meat-Type Lambs in Turkey. Ruminants, 2(4), 420-434. https://doi.org/10.3390/ruminants2040029

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