AABArchives Animal BreedingAABArch. Anim. Breed.2363-9822Copernicus PublicationsGöttingen, Germany10.5194/aab-60-161-2017Effect of the IGF-I gene polymorphism on growth, body size, carcass and meat quality traits in Coloured Polish Merino sheepGrochowskaEwagrochowska@utp.edu.plBorysBronisławJaniszewskiPiotrKnapikJanMroczkowskiSławomirDepartment of Genetics and General Animal Breeding, UTP University of Science and Technology, Bydgoszcz, PolandNational Research Institute of Animal Production, Experimental Station, Kołuda Wielka, PolandDepartment of Meat and Fat Technology, Prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology, Warsaw, PolandNational Research Institute of Animal Production, Balice, PolandEwa Grochowska (grochowska@utp.edu.pl)14June201760216117322February201724April20175May2017This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/This article is available from https://aab.copernicus.org/articles/60/161/2017/aab-60-161-2017.htmlThe full text article is available as a PDF file from https://aab.copernicus.org/articles/60/161/2017/aab-60-161-2017.pdf
Insulin-like growth factor I, encoded by the IGF-I gene,
plays a role in cell growth and differentiation, embryogenesis, metabolism
regulation, skeletal growth, and protein synthesis. The aims of this study
were to investigate the polymorphism in the 5′ flanking region of the
IGF-I gene and evaluate associations between the single-nucleotide polymorphism (SNP) in this gene
and growth, body size, carcass and meat quality traits in Coloured Polish
Merino sheep. In total 78 live and post mortem traits were investigated.
Polymorphism in the IGF-I gene was identified with the use of
the polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP) method in 305 Coloured Polish Merino sheep. In association studies,
traits of interest were analysed with the use of the MIXED and GENMOD
procedures of the SAS statistical package. Two alleles named A and B, and two
IGF-I genotypes – AA and AB – were detected. The A allele and the
AA genotype were predominant, with the frequencies of 91.6 and 83.3 %,
respectively. The IGF-I genotype was found to have a highly
significant effect on fore shank weight (P= 0.006), kidney fat class
(P= 0.002) and EUROP fat class (P= 0.005). Furthermore, the
IGF-I genotype significantly affected external fatness of carcass
class (P= 0.038), drip loss (P= 0.049), and subjective
assessment of meat colour (P= 0.043), and it tended to be associated with
longissimus dorsi (LD) muscle width (P= 0.063) and flavour (0.067). Concluding,
the IGF-I gene could be considered as a candidate gene of selected
carcass and meat quality traits in sheep.
Introduction
Insulin-like growth factor I (IGF-I) is a polypeptide hormone that is
encoded by the IGF-I gene and is similar in molecular structure to insulin. IGF-I
participates in the somatotrophic axis together with growth-hormone-releasing hormone (GHRH), growth hormone (GH), insulin-like growth factor II (IGF-II),
and their associated binding proteins (BPs) and receptors (GHRHR, GHR,
IGF-IR and IGF-IIR). Moreover, it interacts with insulin-like growth
factor I receptors (IGF-IR) in target tissues (Jones and Clemmons, 1995) and with
proteins binding IGF in blood (IGF-BP), which can modulate action of this
hormone (e.g. Lackey et al., 1999; Schams et al., 1999). IGF-I is
also believed to mediate a wide spectrum of biological responses such as
cell growth and differentiation, embryogenesis, metabolism regulation,
skeletal growth, and protein synthesis (Baxter, 1986; Clemmons et al.,
1987; Froesch et al., 1985). For these reasons, the IGF-I gene is considered
as a
functional candidate for a number of production traits, i.e. growth, carcass
and meat quality traits in livestock.
Growth traits are important attributes in sheep breeding, as they, among
other factors, affect breeder's profit. Lamb body weight is one of the
factors that regulate incomes from meat production. Therefore, the
improvement of these traits should be one of the most important aims in
sheep production. Growth traits, like other quantitative traits, are
controlled by several genes, e.g. the IGF-I gene, and environmental
factors. However, there have been only a few association analyses of the
IGF-I gene polymorphism with growth traits in sheep. For example, Hajihosseinlo
et al. (2013), Tahmoorespur et al. (2009), Negahdary et al. (2013) and
Gholibeikifard et al. (2013) observed significant effects of the IGF-I gene
polymorphism on several growth traits in Makooei and Baluchi sheep.
Moreover, Hajihosseinlo et al. (2013) investigated the association of
nucleotide substitution in the IGF-I gene with several body size traits in sheep.
It should be pointed out that the abovementioned studies were conducted only
in Iranian sheep breeds. Therefore, there is a lack of information about
these associations in sheep breeds in other countries, especially in Europe.
To our knowledge, until now only Proskura and Szwczuk (2014) had investigated
effects of single-nucleotide polymorphism (SNP) in the third exon of the IGF-I gene on growth traits in Pomeranian
Coarsewool sheep in Poland and there was no association study involving the
IGF-I gene and body size traits in countries other than Iran, nor any subjective
assessment of body muscle and fat class in sheep. Interestingly, in cattle,
several authors have found significant associations between the IGF-I gene
polymorphism and growth traits (e.g. De la Rosa Reyna et al., 2010;
Ge et al., 2001; Li et al., 2004). Moreover, Zhang et al. (2008) reported
significant effects of nucleotide substitution in the IGF-I gene on several body
size traits in goats. Additionally, Gao et al. (2009) showed that the
IGFBP-3 gene polymorphism was associated with chosen body measurements in Chinese
beef cattle.
Despite the fact that the IGF-I gene plays a role in the growth of an organism, it
could also be directly or indirectly associated with other traits,
i.e. carcass and meat quality traits, as SNPs in this gene could be markers in
linkage with causative mutations in other genes. For example, Behzadi et al. (2015)
investigated effects of the IGF-I gene polymorphism on carcass traits in
sheep. Moreover, Sun et al. (2014) studied correlations between the IGF-I gene
expression and carcass and net meat weight in Hu sheep. Siadkowska et al. (2006)
and Curi et al. (2005) observed associations between the IGF-I gene
polymorphism and several carcass traits in cattle. In the case of meat
quality traits, there have only been a few association analyses in sheep.
Behzadi et al. (2015) investigated effects of the IGF-I gene on the level of
triglycerides and cholesterol in blood. Su et al. (2014) analysed
relationships between the IGF-I gene expression and diameter and density of
muscle fibre as well as muscle tenderness in Hu sheep. In pigs, Wang et al. (2009,
2010) observed effects of the IGFBP-3 and IGFBP-5 gene
polymorphisms on meat colour and pH of various meat cuts, respectively.
Among many factors affecting growth, body size, carcass and meat quality
traits, effects of many candidate genes still need to be investigated,
especially in sheep. Identification of associations between candidate gene
polymorphisms and the abovementioned attributes can provide useful markers
for selection of economically favourable traits. However, little is known
about the effect of the IGF-I gene polymorphism on growth, body size, carcass and
meat quality traits in sheep, especially in European breeds. Moreover, to
our knowledge no previous association studies between IGF-I genotypes and many
important carcass and meat quality traits in sheep have been conducted.
Therefore, the aims of the present study were to investigate the polymorphism
in the 5′ flanking region of the IGF-I gene and to evaluate the associations between
SNP in this gene and a wide spectrum of growth, body size, carcass and meat
quality traits in Coloured Polish Merino sheep.
Materials and methods
In total, 305 purebred Coloured Polish Merino lambs of both sexes were
investigated. The Coloured Polish Merino is a sheep breed used for its wool
and meat. It is included in the Programme of Farm Animal Genetic Resources
Conservation supervised by the National Research Institute of Animal
Production (NRIAP) in Poland. Sheep were kept indoors, but they also grazed
on a pasture six times a week at the NRIAP Experimental Station Kołuda
Wielka. Lambs were sired by nine different rams and were produced during a
period of 3 years – from 2011 to 2013. Suckling lambs were fed dry
granulated mash and meadow hay ad libitum. Procedures involving animals were approved
by the local animal research ethics committee and the local veterinary service.
Growth data (body weight on the second, 30th, 56th and 78th days
of life) were collected for 277 male and female lambs. Moreover, the average
daily gains between the second and 30th, 30th and 56th, and
56th and 78th days were calculated.
In total, 305 male and female lambs were ultrasonically (USG) scanned
according to the procedure described by Krupiński et al. (2009) using an
Aloka SSD-900 device with a UST-5818-5 transducer (B-5MHz). In brief, USG
examination of a cross section of the longissimus dorsi (LD) muscle was performed on the right body
side perpendicularly to the spine axis behind the last thoracic vertebrae.
Measurements of width, depth and area of the LD muscle and fat depth over LD
muscle were performed on USG images with the use of MultiScan ver. 18.03 software.
In total, 106 ram lambs were chosen for slaughter during the 3
experimental years. Before slaughter, the following body measurements were
carried out on lambs: withers height, chest depth, body length, shoulder
width, hip width and leg depth. The measurements were taken while the lambs
were in a standing position, according to the methodology of Kawęcka (2013).
Subjective evaluations of muscling as well as fatness with the use
of a five-point system (ranges from one to five with a 0.5 precision, with a
value of five being the meatiest or fattiest class) were undertaken in the
lumbar part of the spine behind the last rib near the kidney according to the
methodology of Jarrige (1988). Slaughters, carcass cutting and leg
dissection took place three or four times a year from March to April
according to the methodology of Nawara et al. (1963) and Krupiński et
al. (2009) in the abattoir of the NRIAP Experimental Station Kołuda
Wielka. Mean age at slaughter was 105 days (SD 4.2, range 92–119 days). In
brief, lambs were weighed twice: 1 day before slaughter (final weight)
and on the day of slaughter (pre-slaughter weight). Then animals were
electrically stunned, exsanguinated and skinned. Subsequently, carcasses
were weighed (hot carcass weight) and maintained in a chilling room, where
the temperature was held at approximately 4 ∘C for 18 h.
After chilling carcasses were weighed again (cold carcass weight) and the
cold carcass dressing out was calculated by dividing the cold carcass weight
by the pre-slaughter weight and multiplying by 100. In the next step,
carcasses were visually graded for muscle and fat class on a nine-point
scale (with the value of nine being the meatiest or fattiest class) according to the methodology implemented at ram evaluation
stations in Germany as described by Krupiński et al. (2009).
Conformation and muscling were assessed on each of the three parts of
carcass separately: on the fore part of the carcass consisting of middle
neck and shoulder, on the full loin part including rib and loin, and on the
leg part. The evaluation of fatness involved two traits: kidney fat class
and external fatness of carcass class. Carcasses were also categorised in
terms of muscle and fat class according to the EUROP grading system as
described by Krupiński et al. (2009). Subsequently, the following
dimensions of carcasses were measured according to the methodology of Nawara
et al. (1963): carcass length, breast depth, breast width, rump width, rump
girth, leg depth, leg length index and loin width. Then carcasses were halved,
and the right carcass side was weighed and taken for further examination.
The kidney, kidney fat and the rest of the diaphragm were removed. At first,
the right carcass side was divided into three parts: the fore part of the
carcass, the full loin part, and the leg part, and each part was weighed.
Subsequently, these three parts were divided into the following cuts: scrag,
middle neck, shoulder, breast and flank, rib, loin, tenderloin, leg, fore
shank, and hind shank, according to the methodology of Nawara et al. (1963).
All cuts were weighed. On the surface, where a rib was cut from a loin,
width, depth and the area of the eye of loin and fat depth over the eye of
loin were measured. Moreover, fat depth over the ribs in the thickest point
of this layer was recorded. The leg was dissected for three tissues:
muscles, bones and fat, which were weighed separately and a yield of each
tissue in the leg was calculated.
Furthermore, loin muscles from the right carcass side were vacuum-packed and
transported to the Institute of Agricultural and Food Biotechnology
(Poland), where meat quality analyses were undertaken. The pH measurements
were performed on samples of longissimus lumborum (LL) muscle
24 h postmortem (pH24h) using a German Mettler Toledo 1140 pH meter with an integrated Mettler Toledo
electrode (ISO 2917, 2001). Results were averaged from the three
measurements per one sample. For an instrumental evaluation of meat colour,
steaks (thickness approximately 10 mm each) were cut crosswise in the
direction of the LL muscle fibres and exposed to daylight or electric light
for 15 min. The values of reflectance coordinates – L* (lightness),
a* (redness) and b* (yellowness) – were gathered using a
Konica Minolta chronometer CR-400. Drip loss value was measured on the LL muscle. Before, the test samples
were weighed, individually packed in plastic bags, held at
4 ∘C for 48 h and weighed again. The value of drip loss was
defined as a percentage weight loss calculated from the difference between
initial and final weight of the sample. Water, intramuscular fat and total
protein content percentages were determined on minced samples of the LL muscles
according to the methods described in ISO 1442 (2000), 1444 (2000) and
PN-75/A-04018 (2000), respectively, using a Kjeltec system 1002 distilling unit
and a Soxtherm device manufactured by Gerhardt Analytical Systems. Water
holding capacity was investigated in minced LL muscle samples according to the
method devised by Grau and Hamm (1952) with later modifications made by
Pohja and Ninivaara (1957). Cooking loss was analysed on samples of the
longissimus dorsi (LD) muscle. First of all, the samples were weighed, then packed in plastic
bags, heated in water until they reached 75 ∘C in the centre
of the sample and were weighed again at the end of the analysis. The value
of cooking loss was calculated from a difference in sample weights recorded
before and after the process of heating and was expressed as a percentage.
Furthermore, shear force was determined in cooked and cooled-down samples of
lamb loin. For this purpose cylinder-shaped samples (2.5 cm diameter) of the
LD muscle were extracted parallel to the direction of muscle fibres and were
subjected to shear force (N cm-2) measurement with the use of a Zwick Roell
ZO with a 0.5 kN head and Warner Bratzler device with a blade speed of
100 mm min-1. Moreover, subjective visual evaluations of meat colour and marbling
were performed on the LL muscle by a team of five people using an eight-point
scale for colour, where one is related to the lightest and eight is related to the
darkest colour, and a four-point scale for marbling, with a score of one
relating to minor marbling and four relating to the greatest marbling. Subjective
sensory evaluation of aroma, succulence, tenderness and flavour were
performed on boiled LD muscle using a five-point scale for each trait
according to the methodology of Baryłko-Pikielna (1975), where one was related
to bad levels and five was related to very good levels of the trait.
Total genomic DNA was purified from the blood using a
MasterPureTM DNA Purification Kit for Blood Version II
(Epicentre, USA). Polymorphism in the 5′ flanking region of the ovine IGF-I gene was
detected with the use of the polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP) method. A fragment of the ovine IGF-I gene was
amplified using primers reported by Ge et al. (1997). DNA amplifications
were performed in a Mastercycler Pro (Eppendorf AG, Germany) in 20 µL
reaction volume containing 50 ng of genomic DNA, 5 pmol of each primer
(forward and reverse), 200 µM of each dNTP and 1 U DreamTaq DNA
polymerase (Thermo Scientific, USA) in a one-fold DreamTaq reaction buffer.
The temperature profile of the reaction consisted of denaturation at
94 ∘C for 2 min, followed by 30 amplification cycles, including
denaturation at 94 ∘C for 30 s, annealing at 66 ∘C for
30 s and extension at 72 ∘C for 30 s, with a final 5 min extension
step at 72 ∘C. The PCR reaction products were digested with 4 U of
HaeII (NEB, UK) restriction enzyme (Yilmaz et al., 2005) for 2 h at
37 ∘C. Digested PCR products were separated on 2 % agarose gels
in 1 × TBE (Tris-borate-EDTA) buffer for 90 min at 120 V and visualised by Midori Green (Nippon Genetics,
Germany) staining. PCR products representing the AA and AB genotypes were
cleaned up with the use of an ExoSAP-IT® Affymetrix (USA) and
sequenced in both directions in Genomed, Poland. Allele and genotype
frequencies in the IGF-I locus were calculated. Furthermore, observed and expected
heterozygosity as well as the Hardy–Weinberg equilibrium test calculations
were made in the Arlequin 3.5.1.2 (Excoffier and Lischer, 2010).
An association analysis was performed between IGF-I genotypes and growth traits
using the MIXED procedure of the SAS software package (SAS,
2008). The following mixed effect model I was applied:
Yijklm=μ+ai+bj+ck+dl+fm+eijklm,
where Yijklm is the performance of the nth individual lamb for each
trait of interest, μ is the general mean for each trait of interest,
ai is the fixed effect of the ith IGF-I genotype (i= AA, AB),
bj is the fixed effect of the jth sex (j= male, female),
ck is the fixed effect of the kth litter size (k= 1, single;
2, twin and only one lamb born with triplet litter size was also included),
dl is the fixed effect of the lth year of observation (l= 2011,
2012, 2013), fm is the random effect of the mth sire (m= sire
1, 2, … 9) and eijklm is the random error. For all variables
two-way interactions between fixed effects were tested in the model;
however, they did not have a significant effect on investigated traits and
were therefore excluded from the final model.
An association analysis between IGF-I genotypes and body size traits as well as
IGF-I genotypes and slaughter traits was undertaken with the use of the model I
described above without the effect of the sex because only male lambs were
investigated. Moreover, final weight and cold carcass weight were found to
be significant and were included in the final models as a covariate for live
and post mortem attributes, respectively. Weight was not included as the covariate in
the model where the Y variable was the final weight, pre-slaughter weight, a tissue
proportion or dressing out. In the case of final and pre-slaughter weight,
slaughter age was found to be significant and was included as the covariate
in the model. Furthermore, final weight was fitted in the model as the
covariate for hot and cold carcass weight. For all variables, two-way
interactions between fixed effects were tested in the model but were not
significant for almost all of the traits, with the exception of withers
height, chest depth, leg depth (body measurement), scrag weight, and hot and
cold carcass weight; therefore, they were included in the models only for
the abovementioned traits, but not for all other characteristics.
Moreover, an association of IGF-I genotypes with USG measurements of the LD muscle was
also estimated with the use of the model I described above; however,
slaughter age was included as the covariate. For all variables, two-way
interactions between fixed effects were tested in the model but did not
have a significant effect on investigated traits, with the exception of fat
depth over the LD muscle; therefore, it was fitted in the model only for this
trait. An association analysis between IGF-I genotypes
and meat quality traits was performed with the use of the model I described
above without the effect of sex and litter size. For all variables, two-way
interactions between fixed effects were tested in the model but did not
show any significant effect on investigated traits; therefore, they were not
included in the final model. In the case of each model, when a genotype was
shown to be statistically significant, the significance of deviations was
verified with the Tukey–Kramer test.
Associations of IGF-I genotypes with subjective assessment of live animal and
carcass traits were analysed with the use of the GENMOD procedure of the SAS
software package (SAS, 2008). The generalised linear model
included the fixed effects of IGF-I genotype, litter size, year of observation
and sire. Moreover, final weight and cold carcass weight were found to be
significant and were fitted in the model as the covariates for live and post mortem
attributes, respectively.
ResultsIdentification of alleles
PCR-RFLP analysis of polymorphism in the 5′ flanking region of the IGF-I gene in
Coloured Polish Merino sheep revealed two alleles, named A and B, and only
two genotypes: AA and AB. The HaeII digested allele A amplicon, while allele B
remained undigested. Sequence analysis showed that two SNPs differed allele
A from allele B. The first polymorphism covered G/C transversion, while the
second covered G/A transition, at positions 85 and 87, respectively (nucleotide
positions are relative to the first nucleotide in the sequence; GenBank no. LC151296.1).
IGF-I allele and genotype frequencies (%) in Coloured Polish Merino
sheep.
Results of association analysis between IGF-I genotypes and growth
traits – LSM ± SE (standard error) – in Coloured Polish Merino sheep.
TraitUnitLSM*± SE P valueAAABN22750Body weight on second day of lifekg5.11 ± 0.105.08 ± 0.130.783Body weight on 30th day of lifekg12.80 ± 0.1812.61 ± 0.280.527Body weight on 56th day of lifekg19.30 ± 0.3219.04 ± 0.450.545Body weight on 78th day of lifekg26.56 ± 0.4626.21 ± 0.600.511Average daily gain between second and 30th days of lifeg255.36 ± 3.95250.10 ± 7.220.505Average daily gain between 30th and 56th days of lifeg249.69 ± 6.75247.59 ± 8.890.789Average daily gain between 56th and 78th days of lifeg328.00 ± 8.13324.75 ± 12.440.796N9016Final weightkg34.64 ± 0.5433.77 ± 1.160.487Pre-slaughter weightkg32.40 ± 0.5131.80 ± 1.070.601
* LSM is least squares mean.
Results of association analysis between IGF-I genotypes and body size
traits (LSM ± SE) in Coloured Polish Merino sheep.
* LSM is least squares mean. Values with different superscripts a,b within a
row are significantly different (P< 0.05). Values in bold were applied to
highlight highly significant effect of the IGF-I gene on carcass traits.
Results of association analysis between IGF-I genotypes and meat quality
traits (LSM ± SE) in Coloured Polish Merino sheep.
* LSM is least squares mean. Values with different superscripts a,b within a
row are significantly different (P< 0.05). Values in bold were applied to highlight
significant effects of the IGF-I gene on meat quality traits.
Results of association analysis between IGF-I genotypes and subjective
assessment of live animal and carcass traits in Coloured Polish Merino sheep
(n= 106).
TraitUnitP valueLive animal traits Muscle class1–50.107Fat class1–50.383Carcass traits Conformation and muscle class of the fore part of carcass1–90.373Conformation and muscle class of the full loin part of carcass1–90.115Conformation and muscle class of the leg part of carcass1–90.190Kidney fat class1–90.002External fatness of carcass class1–90.038EUROP conformation classEUROP0.916EUROP fat class1, 2, 3L, 3H, 4L, 4H, 50.005
Values in bold are significant or highly significant.
Allele and genotype frequencies
IGF-I allele and genotype frequencies in the investigated breed are shown in
Table 1. The A allele was predominant (91.6 %), while the B allele
occurred with the frequency of 8.4 %. The most frequent group was AA
homozygotes (83.3 %), while 16.7 % of lambs carried the AB genotype. The
value of observed heterozygosity (Ho) was equal to 0.167, and was higher
than the value of expected heterozygosity (He), which amounted to 0.153.
The population was in the Hardy–Weinberg equilibrium (P= 0.247).
Effect of the IGF-I gene polymorphism on traits measured in live animals
Mixed-model association analyses of the IGF-I genotypes were performed for body
weights, average daily gains, body measurements and ultrasound LD muscle
measurements. Effects of the IGF-I gene polymorphism on these traits in Coloured
Polish Merino sheep are presented in Tables 2–4. None of
the analyses showed any significant effect of the IGF-I genotype on
the abovementioned characteristics; however, the IGF-I gene polymorphism tended to
be associated with LD muscle width (P= 0.063). AB heterozygous lambs had wider
LD muscle (0.14 cm) than in AA homozygotes (Table 4). Results of the
generalised linear model analyses of the IGF-I genotype effect on body muscle and
fat class are presented in Table 7. No associations between the IGF-I gene
polymorphism and these traits were found.
Effect of the IGF-I gene polymorphism on carcass traits
Tables 5 and 7 show the results of association analyses between the
IGF-I gene polymorphism and carcass traits in Coloured Polish Merino sheep.
IGF-I genotype was associated with fore shank weight (P= 0.006). Heterozygous
lambs had heavier fore shank (4.3 %) than AA homozygous animals.
Furthermore, the IGF-I genotype was found to have highly significant effects on
kidney fat class (P= 0.002) and EUROP fat class (P= 0.005) and a significant
effect on external fatness of carcass class (P= 0.038). No significant
associations between IGF-I genotype and other investigated carcass traits were detected.
Effect of the IGF-I gene polymorphism on meat quality traits
Results of association analyses of the IGF-I gene polymorphism with meat quality
traits in Coloured Polish Merino sheep are presented in Table 6. The IGF-I gene
polymorphism was significantly associated with drip loss (P= 0.049). Meat
from AA homozygous lambs was characterised by lower average drip loss
(-0.86 %) than meat from heterozygotes AB. Moreover, the IGF-I gene
polymorphism had a significant effect on the subjective assessment of meat colour
(P= 0.043). AA homozygous ram lambs had meat characterised by the higher
average value of this trait (0.34 point) when compared to meat form
heterozygotes AB. Furthermore, the IGF-I genotype tended to be associated with the
flavour (P= 0.067).
Discussion
In the present study, polymorphism in the 5′ flanking region of the IGF-I gene
and its association with growth, body size, carcass and meat quality traits
in Coloured Polish Merino sheep were analysed. Two alleles, named A and B,
and only two genotypes, AA and AB, were detected. The A allele was
predominant (91.6 %), which consequently resulted in the higher frequency
of the AA homozygotes (83.3 %) than the AB heterozygotes. These results
are consistent with the study of Yilmaz et al. (2005), who also reported a
high frequency of the A allele and the AA genotype (89 and 77 %,
respectively) in Polypay sheep. Conversely, Tahmoorespur et al. (2009)
and Nazari et al. (2016) detected lower frequencies of the AA
genotype (45 and 28 %) and identified the BB homozygotes (9 and
34 %) in Baluchi and Zandi sheep, respectively. Furthermore, Hajihosseinlo
et al. (2013) and Kazemi et al. (2011) identified three genotypes in this
locus in Makooei (AA – 52 %, AG – 42 % and GG – 6 %) and Zel (AA – 47 %,
AB – 47 % and BB – 6 %) sheep, respectively. He et al. (2012)
found two SNPs in the 5′ regulatory region of the IGF-I gene in four sheep breeds
in China. Dorset and Texel sheep were characterised by very high AA genotype
frequencies (100 and 93.8 %, respectively) and a lack of the BB homozygotes.
Conversely, percentage frequency of the AA genotype in Hu sheep was low
(37.9 %) and moderate in Small-Tailed Han sheep (64.6 %) when compared to
Dorset and Texel sheep in the study of He et al. (2012). Moreover, Scatà
et al. (2010) identified two SNPs (g.855G > C and
g.857G > A) in the 5′ UTR of the IGF-I gene in Gentile di Puglia,
Altamurana and Sarda sheep breeds. Proskura and Szewczuk (2014) analysed the
g.271C > T in the third exon of the IGF-I gene and they found that the T allele
was predominant in Pomeranian Coarsewool sheep (79.5 %). Similarly,
Scatà et al. (2010) also observed high frequencies of the T allele in Gentile
di Puglia (61.3 %) and Sarda (54.5 %), but slightly lower in Altamurana
sheep (43.1 %). Conversely, Gholibeikifard et al. (2013) reported a
very low frequency of the T allele (5 %) in Baluchi sheep and they did not
find TT homozygotes. Niżnikowski et al. (2015) investigated
polymorphism in the third exon of the IGF-I gene in different sheep breeds in
Poland and they detected the T allele only in Charollais ewes. To summarise,
allele and genotype frequencies in the IGF-I locus vary between different sheep
breeds; therefore, studies covering other sheep breeds should be continued.
The IGF-I locus was characterised by a low genetic diversity in the investigated
Coloured Polish Merino sheep population. The value of observed
heterozygosity (0.167) was slightly higher than the value of expected
heterozygosity (0.153). Moradian et al. (2013) also observed two alleles in
the IGF-I locus in Makooei sheep; nevertheless, values of Ho and He were
higher: 0.42 and 0.40, respectively. The Coloured Polish Merino sheep population
was in the Hardy–Weinberg equilibrium (P= 0.247), indicating no selection
for investigated IGF-I locus. Similarly, Negahdary et al. (2013), who
investigated polymorphism of the 5′ flanking region of the IGF-I gene, reported
that the population of Makooei sheep was in the Hardy–Weinberg equilibrium
(P> 0.05). Conversely, Nazari et al. (2016), who studied the
IGF-I locus in Zandi sheep, showed that this population was not in the
Hardy–Weinberg equilibrium (P< 0.01).
The IGF-I gene affects many important processes in an organism, growth
being among them (Akers, 2006; Burgos and Cant, 2010). Circulating IGF-I concentration has an
impact on fetal and neonatal size and postnatal growth in several species
(Baker et al., 1993; Breier et al., 1988; Duclos et al., 1999; Yakar et al.,
2002; Zapf and Froesch, 1999). However, association analysis did not show
significant effects of the IGF-I gene polymorphism on growth traits in Coloured
Polish Merino sheep. Similarly, Nazari et al. (2016) did not find
significant associations between SNP in the 5′ flanking region of the
IGF-I gene and growth traits in Zandi sheep. Also, Proskura and Szewczuk (2014)
did not show any relationships between the C/T substitution
(g.271C > T) in the IGF-I gene and growth traits in Pomeranian
Coarsewool sheep in Poland. Moreover, Gholibeikifard et al. (2013) did not observe
the effects of SNP, located in the third exon of the IGF-I gene, on growth traits
in Baluchi sheep. Conversely, Tahmoorespur et al. (2009) showed significant
associations of the IGF-I gene polymorphism in the 5′ flanking region with average
daily gain (ADG) from birth to weaning in Baluchi sheep. Heterozygous lambs
had higher ADG from birth to weaning than homozygotes AA and BB.
Furthermore, Hajihosseinlo et al. (2013) observed significant effects of
nucleotide variation in the 5′ flanking region of the IGF-I gene with several
growth traits in Makooei sheep: birth weight (BW), weaning weight (WW), 6-month
weight (SW)
and average daily gains from birth to weaning (GBW). Additionally, a significant
association of polymorphism in the 5′ flanking region of the IGF-I gene with
BW, WW, SW, breeding value estimated for body weight in the sixth month of
life (EBV 6MW), GBW and average daily gains from the sixth month to the ninth month of
life (GSN) were found in Makooei sheep (Negahdary et al., 2013). AG heterozygous Makooei
sheep had higher values of the traits EBV 6MW, 6MW and WW than homozygotes.
Conversely, AA homozygous sheep had higher BW and GBW (Negahdary et
al., 2013). Furthermore, Sun et al. (2014), who investigated the effects of
different factors on the level of the IGF-I gene expression and its associations
with growth traits, observed a positive correlation of this gene's
expression with body weight in Hu sheep. Other authors analysed the effects
of the IGF-I gene polymorphisms with growth traits in other livestock species.
For example, Ge et al. (2001) showed associations between variation in the
IGF-I gene and growth traits in Angus cattle and suggested that this polymorphism
could have an impact on gene transcription and consequently on animal
phenotype. Szewczuk et al. (2013) reported effects of two SNPs in the
IGF-I gene on body weight in the second month of life in calves and average daily
gains in the periods from the first to the second months and from the second
to the third months of life and for the whole rearing period. Zhang et al.
(2008) investigated polymorphism of the IGF-I gene and its association with
growth and body size traits in Nanjiang Huang goats. They found a significant
effect of G/C substitution on birth weight, body weight at 6 months, body
weight at 12 months, heart girth at 2 months, body length at 6 months,
wither height at 6 months, wither height at 12 months and heart girth at
12 months in the goats. Concluding, there are analyses that confirm associations
of the IGF-I gene polymorphisms with growth traits in sheep and other livestock
species; however, there are other reports that are opposite to these
findings. The growth of animals is a complex process that is under the
control of several genes and environmental factors. Moreover, the effects of the
IGF-I gene polymorphism on growth traits seem to depend on sheep breed.
Therefore, before introducing DNA tests in sheep breeding, additional
analyses of this gene's polymorphism and its association with growth traits
in different sheep breeds should be undertaken.
The IGF-I hormone plays a crucial role in the postnatal linear growth of animals
(e.g. Yakar et al., 2002; Zapf and Froesch, 1999). In this study an
association of the IGF-I gene polymorphism with body size traits and subjective
assessment of body muscle and fat class in Coloured Polish Merino sheep was
investigated; however, the effects of IGF-I genotypes on these traits were not
significant. Conversely, Hajihosseinlo et al. (2013), who investigated
associations of the IGF-I gene polymorphism in the 5′ flanking region with such
body size traits as height and length of body, wither height, chest width
and
rump length in Makooei sheep, found a significant effect of this gene's
genotypes on sheep body length. Moreover, Chelongar et al. (2014) observed a
significant effect of SNP in the first exon of the IGF-I gene on fat-tail fat
thickness (the thick rump). AA homozygotes were superior in terms of this
trait, whereas GG male lambs had the lowest fat thickness. The
associations of nucleotide variation in the first exon of the IGF-I gene with
tail length and width (rump length and width) in Makooei sheep was not
significant (Chelongar et al., 2014). Associations between the IGF-I gene
polymorphism and body size traits were also investigated in other livestock
species. For example, Zhang et al. (2008) found the significant effects of
G/C substitution in the fourth intron of the IGF-I gene on heart girth at
2 months, body length at 6 months, wither height at 6 months, wither height at
12 months and heart girth at 12 months in Nanjiang Huang goats. Gao et al. (2009)
showed that the polymorphism in the IGFBP-3 locus was associated with rump
width and heart girth at 24 and 36 months in Chinese beef cattle.
Furthermore, Mullen et al. (2011) reported that SNP in the IGF-I gene (IGF1i6; G
allele) was positively associated (P< 0.05) with body condition
score in Holstein-Friesian dairy cattle, while Lynch et al. (2010) showed a
relationship between IGF1i2 and body condition score at calving in a cohort of 241
dairy cows. IGF-I protein affects longitudinal bone growth by promoting osteoblast
division and proliferation. Furthermore, it regulates muscle growth by
enhancing myocyte differentiation and multiplication and has an impact on
cartilage growth by increasing chondrocyte colony formation (Duclos et al.,
1999; Yakar et al., 2002; Zapf and Froesch, 1999). It should be pointed out
that there is limited information about effects of the IGF-I gene polymorphism on
body size traits, especially in sheep. Moreover, to our knowledge it was the
first association analysis of IGF-I genotypes and subjective assessment of body
muscle and fat class in sheep. Therefore, similar association analyses
should be undertaken in other sheep breeds.
IGFs, their receptors and BPs play a crucial role in
muscle growth and differentiation (Oksbjerg et al., 2004). In this study
effects of the IGF-I gene polymorphism with ultrasound measurements of LD muscle in
Coloured Polish Merino sheep was not significant; however, it tended to
be associated with the width of this muscle. Additionally, LD muscle dimensions
were also measured post mortem, but no significant associations between the IGF-I gene
polymorphism and these traits were showed. No other paper was found in the
literature concerning association between IGF-I genotypes and ultrasound LD muscle
measurements in sheep. Interestingly, in cattle the SNP in the IGF-I gene tended
to be associated with the ultrasound LD area (P= 0.06) (Curi et al., 2005). As
the current study was the first association analysis of IGF-I genotypes with
ultrasound LD muscle measurements in sheep, similar analysis in other sheep
breeds should be undertaken in order to investigate possible breed effects on these traits.
In this study effects of IGF-I genotypes on carcass traits in Coloured Polish
Merino sheep were investigated. Among 40 traits, significant associations
between IGF-I genotypes and fore shank weight, EUROP fat class, kidney fat class
and external fatness of carcass class in Coloured Polish Merino ram lambs
were found. Similarly, Behzadi et al. (2015) investigated effects of the
IGF-I gene polymorphism on fat-related traits in Mehraban sheep. They observed a
tendency for an association between SNP in this gene and dorsal fat
thickness (P= 0.07); however, effects of this nucleotide variation in
abdominal fat and fat-tail weight were not significant. Furthermore,
Siadkowska et al. (2006) reported correlations between polymorphism in the
5′ non-coding region of the IGF-I gene and lean and fat weight of valuable cuts
and a percentage of fat of valuable cuts in Polish Holstein-Friesian cattle.
Moreover, concerning the IGF2 gene polymorphism, CT heterozygous Polish
Holstein-Friesian bulls had more fat in valuable cuts in the 15th month
of life (Zwierzchowski et al., 2010). Also in cattle, Curi et al. (2005)
observed a significant association of IGF-I/SnaBI polymorphism in the regulatory
region of the IGF-I gene with subcutaneous back fat assessed by ultrasonography.
In pigs, Wang et al. (2006) investigated effects of polymorphism of the
IGF-I receptor gene (IGF-IR) on back-fat thickness and lean percentage estimated by
ultrasonography, and they found less back-fat thickness (P< 0.05) and
a greater lean percentage (P< 0.01) in AA homozygous Yorkshire pigs
than BB individuals. To summarise, the results of the abovementioned
research showed that polymorphisms in the IGF-I gene, as well as IGF2 and IGF-IR, were
associated with several fat traits of sheep, cattle and pig carcasses.
Indeed, the IGF-I gene was shown to be involved in fat cell development in
transgenic mice (Rajkumar et al., 1999). Rajkumar et al. (1999) observed
enhanced expression of this gene during differentiation of precursor cells
into mature fat cells. Furthermore, Anderson et al. (1988) found that
circulating IGF-I protein was negatively correlated with carcass fat percentage, fat
accretion rate and fat thickness in Simmental crossbred bulls. Additionally,
Davis and Simmen (1997) found associations between lower plasma
IGF-I protein
concentrations and higher marbling scores as well as dorsal fat thickness in
Angus bulls. Concluding, the IGF-I gene should be considered as a potential
candidate gene of fat-related carcass traits in sheep.
As mentioned before, among several carcass and carcass cut weights, IGF-I
genotype was only associated with fore shank weight in Coloured Polish
Merino lambs. Contrary to our results, other authors showed an effect of
this gene's polymorphism on carcass weights. For example, Behzadi et al. (2015)
reported a tendency of the IGF-I gene polymorphism to be associated with
carcass weight (P= 0.07). Moreover, Sun et al. (2014) found that an
expression of the IGF-I gene was positively correlated with carcass weight in Hu
sheep. Siadkowska et al. (2006) observed a correlation between polymorphism
in the 5′ non-coding region of the IGF-I gene and cold carcass weight in Polish
Holstein-Friesian cattle. Curi et al. (2005) found significant association of
IGF-I/SnaBI polymorphism in the regulatory region of the IGF-I gene with hot carcass
weight, but the effect of this SNP on carcass yield was insignificant in
beef cattle. Zwierzchowski et al. (2010) reported effects of the IGF2 gene
polymorphism on cold carcass weight and percentage meat content in valuable
cuts at the age of 11 months in Polish Holstein-Friesian cattle. It should
be pointed out that there is a dearth of information about the association of
the IGF-I gene polymorphism with carcass traits in sheep. To our knowledge, until
now only Behzadi et al. (2015) had investigated effects of SNP in this gene on
carcass traits in Iranian sheep. In the current study we reported results of
association analyses in Polish sheep breeds involving new carcass traits,
which have not been investigated before. These results suggest that the
IGF-I gene should be considered as a potential candidate gene of carcass traits
in sheep, and similar studies involving other sheep breeds in different
countries should be continued.
In this study, association analysis between the IGF-I gene polymorphism and meat
quality traits was undertaken. A significant effect of IGF-I SNP on natural drip
loss in Coloured Polish Merino sheep was found. Meat from AA male lambs had
lower natural drip loss than meat from heterozygous individuals. Moreover,
an association of this nucleotide variation in the IGF-I gene with subjective
meat colour was observed. In this case, meat from AA homozygous ram lambs
was slightly darker than meat from heterozygotes. Little is known about
associations of the IGF-I gene polymorphism with meat quality traits in sheep. To
our knowledge, this study is the first that presents the effect of IGF-I genotypes
on several new meat quality traits in sheep. Other authors have shown
association analyses of the IGF-I gene polymorphism with various meat quality
traits in sheep, but with different traits than investigated in this study. For example,
Behzadi et al. (2015) found significant effects of nucleotide variation in
the first exon of the IGF-I gene with the level of triglycerides and cholesterol
in blood. Su et al. (2014) analysed relationships of the IGF-I gene expression in
LD muscle with meat quality traits in Hu sheep. They observed that the
expression of this gene was positively and significantly (P<0.01)
correlated with muscle fibre diameter and muscle fibre shear stress, and
negatively and significantly (P< 0.01) correlated with muscle fibre
density. Furthermore, Davis and Simmen (1997) showed that lower plasma
IGF-I protein concentrations were associated with higher marbling scores in Angus cattle.
Wang et al. (2009) observed an effect of the IGFBP-3 gene polymorphism on meat
colour in pigs. Moreover, Wang et al. (2010) found an association between
the IGFBP-5 gene and pH of various meat cuts in pigs. SNPs in the IGF-I gene may have a
direct or indirect effect on meat quality traits in sheep, cattle and pigs.
There is also a possibility that SNPs detected in the IGF-I gene are not causative
mutations for the investigated effects on meat quality traits, but are
markers in linkage with the causative mutations in the other genes. As the
results of this study constitute the first information gathered on the IGF-I gene
polymorphism association with several meat quality parameters in sheep,
further investigation should be carried out to evaluate potential
breed-specific effects of SNPs in this gene on lamb quality.
Conclusion
In the present study, information about the IGF-I gene polymorphism and its effect
on a wide range of growth, body size, carcass and meat quality traits in
Coloured Polish Merino sheep were reported. Associations between IGF-I genotype
and fore shank weight (P= 0.006), kidney fat class (P= 0.002), EUROP fat
class (P= 0.005), external fatness of carcass class (P= 0.038), natural
drip loss (P= 0.049) and subjective assessment of meat colour (P= 0.043)
were found. Therefore, the IGF-I gene polymorphism could be used as a marker for an
improvement of these traits in Coloured Polish Merino sheep. Moreover, in
the case of several investigated traits, the present study provided the first
information about the effect of this marker in sheep. Concluding, the
results suggest that the IGF-I gene could be considered as a candidate gene of
certain carcass and meat quality traits in sheep; however, further
investigations are recommended in other sheep breeds in the world in order
to evaluate potential breed- and/or flock-specific effects of this gene's
polymorphism on sheep production traits. Furthermore, the IGF-I gene is well
known for its role in many processes in an organism, which is a result of its
pleiotropic function; therefore, before using IGF-I polymorphism in a production
system, association analyses regarding other traits, which were not
investigated in this study, i.e. reproductive and milk production
attributes, should be carried out to confirm that selection will not have
negative consequences for the breed.
The original data of the paper will be available upon request to the
corresponding author.
The authors declare that they have no conflict of interest.
Acknowledgements
This project was founded by National Science Centre, Poland, project no. NN311521440.
Part of this work was supported by the project “Realization of
the second stage of the Regional Innovation Centre”, which was co-financed
by the European Regional Development Fund under the Regional Operational
Programme for Kujawsko-Pomorskie Voivodeship for the years 2007–2013.
Edited by: Steffen Maak
Reviewed by: Roman Niżnikowski and two anonymous referees
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