EFFECT OF G.13700A>G AND G.25783C>T IN PIT-1 GENE ON GROWTH TRAITS OF DUROC, LANDRACE, YORKSHIRE PIG
X. Dong1, Z. Liu1, X. Wang1, Q. Chen1, G. Bai2, G. Lan1, Q. Wang1, M. Li1, D. Yan1, and S. Lu1*
1 Faculty of Animal Science and Technology, Yunnan Agricultural University, Fengyuan Road 452, Panlong, Kunming 650201, Yunnan, China
2Dehong Animal Husbandry Station, Dehong 679399, Yunnan, China
[1]* Corresponding author’s email: 86127447@qq.com
ABSTRACT
Pituitary specific transcription factor-1 (Pit-1) gene is responsible for pituitary development and growth hormone expression, which is considered a pivotal candidate gene for growth in pig. This study aims to detect novel single nucleotide polymorphisms (SNPs) in porcine Pit-1 gene, investigate its effect on growth traits in the Duroc, Landrace and Yorkshire pigs. Two novel polymorphisms were detected, one located in the intron 2 (g. 13700 A>G) and another located in exon 4 (g.25783 C>T) which caused an amino acid change from threonine to methionine (Thr36Met). At g.13700 A>G site, the frequency of A allele was higher than G allele in Duroc, Landrace and Yorkshire. At the g.25783 C>T site, it was remarkable differences in allelic frequencies and genotypic frequencies among the three pig breeds. This study demonstrated the significant genotype effect of Pit-1 on body weights at 70 d, age when reached 30kg, 50kg, 100kg and average daily gain from 30kg to 100kg. According to our results, the novel Pit-1 polymorphisms may be useful in pig selection as molecular markers and required in future studies.
Keywords, Pit-1, pig , growth traits, polymorphisms.
INTRODUCTION
In domestic animals, there are many promising candidate genes for growth distributed in growth hormone (GH) axis. Pit-1 belongs to POU domain protein family,it is an interdependent gene of GH gene pathway (Cogan et al. 1998; Negahdary et al. 2013). Pit-1 controls the development of anterior pituitary and plays regulatory role in gene transcription of pituitary hormone secreting cells, inducing the differentiation of hepatic progenitor cells and delaying human’s adrenarche (Lee et al. 2005; Taha et al. 2005; Tordjman et al, 2019).
Pit-1 is a specifically expressed transcription factor, which involves in activating the expression of GH, prolactin (PRL) and thyroid stimulation hormone-β subunit (TSH-β) genes (Sudeep et al,2016; Tordjman et al,2019). It regulates the transcription and expression of these genes and involves in cell differentiation and proliferation (Roche et al, 2012), thus plays direct or indirect effects to the growth traits and fatty deposits properties of animals ( Forand et al, 2016). Li et al (1990) reported mutation of Pit-1 gene will hinder the secrete of GH, PRL and TSH-β hormones, which causes animal dwarfism. In human and mice, the absence of Pit-1 activity results in the lack of multiple pituitary hormones, which leads to dwarfism (Aarskog et al.1997; Cohen et al. 1999).
Pig’s Pit-1 gene was located on chromosome 13. It was the significant associations between polymorphisms and growth traits of pigs that indicates Pit-1 may be a potential candidate gene for growth (Zhao et al,2004; Jin et al,2018). A polymorphic locus of BamHI was found in Pit-1 gene in Meishan pigs (Tuggle et al.1993) and the polymorphism of MspI was found (Yu et al.1993). The growth rate and amounts of fat were related to the expression of Pit-1 in pigs (Andersson et al. 1994). In Poland pigs, it was reported that mutations within the Pit-1 gene associated with fattening performance (Piórkowska et al. 2013). Yu et al (1995) found the MspI site of Pit-1 was related to birth weight and backfat thickness. Yang et al (2006) found polymorphism in intron 5 was related significantly to growth traits. Zhang et al (2017) reported that the polymorphisms of RsaI site of Pit-1 gene at exon 5 to intron 5 have a certain effect on pig’s growth traits. Moreover, Pit-1 polymorphisms within intron 4 to the 3’ untranslated region were associated with expected progeny difference (EPD)for production performance in Landrace (Franco et al. 2005).
This study detects SNPs of pig’s Pit-1 gene by PCR-SSCP and DNA sequencing, further investigates the relationship between SNPs and growth performance in three pig breeds. We detected two novel polymorphisms and analyzed with growth traits, which could be useful to pig breeding.
MATERIALS AND METHODS
Animals and Trait Measurements: We used 391 pigs, including 59 Duroc (40 boar and 19 sows), 72 Landrace (46 boar and 26 sows) and 260 Yorkshire (165 boar and 95 sows) pigs, only noninbred individuals for at least 3 generations were included. In 2020, all the pigs were raised in Fuyuefa Livestock and Poultry Breeding limited liability company, Yunnan province, China. Every individual was fed with at least 1.5 square meters in semi-open barn and raised separately by sex. The feeding program includes two feeds: one for growers (weighing from 30 to 70 kg), the energy for growers was at least 13.5 MJ/Kg, the crude protein for growers was between 17%-19%, and the digestible protein for growers was at least 14.0 respectively. Another for finishers (from 70 to 100 kg), energy of feeds for finishers was at least 13.0 MJ/Kg, the crude protein for finishers was between 16%-18%, and the digestible protein for finishers was at least 12.8 respectively. Body weights at born (BW0), body weights at 21d (BW21), body weights at 70 d (BW70) were measured. The age when they reached 30kg (D30), 50kg (D50), 100kg (D100) were recorded by Feed Intake Recording Equipment (Osborne Industries, US). We also measured the ADG from 30kg to 100kg (ADG of 30-100 kg) and the backfat thickness (measure the thickness of Dorsal fat layer by B-mode ultrasound diagnosis instrument, the site was located between the reciprocal third and fourth ribs, 5 cm from dorsal midline) when the body weight reached to 100kg (BFT).
DNA extraction and genotyping: Genomic DNA was extracted from the ear tissues using a standard phenol-chloroform method then quantified using a NanoDrop spectrophotometer (GE Healthcare Life Sciences, Uppsala, Sweden). Genotyping was performed on genomic DNA using PCR-SSCP assays, which was described as follows: 5 μL aliquot of each amplicon was diluted in denaturing solution (98% formamide, 10 mM EDTA, 0.025% bromophenol blue, 0.025% xylene-cyanol) denatured at 95 °C for 5 min, rapidly cooled on ice and resolved in acrylamide:bisacrylamide (29:1) gels at 400 V for 4 h at 4 °C, in 1 × TBE buffer (89 mM Tris base, 89 mM boric acid, 2 mM EDTA, pH 8.0). Then, the gels were silver-stained according to the method of Bassam et al (1991). SNPs of the pig Pit-1 gene (GenBank, accession number NM_214379) were screened from the coding region and partial intron region. The primers used for SNP screening are shown in Table 1. PCR amplifications were carried out in 25 μL reaction volumes containing at the following final concentrations: 50 ng of template DNA, 400 μM of dNTPs (Sangon, China), 0.25 μM of each primer and 1 unit (U) of Taq polymerase (TaKaRa, Japan). The PCR protocol consisted of an initial denaturation at 94 °C for 5 min, followed by 36 cycles of denaturation at 94 °C for 30 s, annealing at 60°C for 30 s, and extension at 72 °C for 30 s, with a final extension at 72 °C for 10 min.
Statistical analysis: Gene frequencies were determined by direct counting. Gene heterozygosity (H) and polymorphism information content (PIC) were calculated according to Nei’s and Botstein’s methods (Nei and Roychoudhury, 1974; Botstein et al., 1980), respectively. The genotype and allele frequencies were tested for Hardy-Weinberg equilibrium using the χ2 test. The associations analyses were tested with a statistical model using the MIXED model procedures (SAS10; SAS Institute, Inc.). The following model was used:
yijk= μ + Gi + Sj + eijk.
Where yijk is observation of traits; μ is population mean; Giis fixed effect of genotypes; Sj is fixed effect of sex; eijk is random residual error. Least square means and respective standard errors for genotypes were estimated based on the statistical model and significant levels were set at P < 0.05 and P < 0.01, respectively.
RESULTS
Detection of single nucleotide polymorphisms: This work amplified nine fragments from genomic DNA by PCR. The PCR products were assayed by the SSCP technique and detect any single base substitution by sequencing the products with unique patterns. Two novel SNPs were identified. One polymorphism was in the intron 2 (g. 13700 A>G). Another one was located in exon 4 (g.25783 C>T) which caused missense mutation, a threonine was changed to methionine (Thr36Met). The g.13700 A>G was one polymorphism in the intron 2 and g.25783 C>T was one substitution located in exon 4. The g.13700 A>G polymorphism showed similar in different breeds, the frequency of A allele was higher than G allele.
Genotype frequencies: In Table 2, it shows the different breeds’ allele frequencies and genotype of Pit-1 gene SNPs. The polymorphism information content of g.13700 A>G was similar in the experimental individuals and different breeds; it has higher frequency of A allele than G allele. With respect to this marker, theses three breeds were not at Hardy-Weinberg equilibrium (P<0.01). In Duroc, Landrace and Yorkshire breed, H of the mutant loci was 0.4585, 0.4614 and 0.4617, which represented the genetic diversity was relatively abundant. At g.25783 C>T site, frequency of C allele in Duroc, Landrace and Yorkshire was 0.7373, 0.4653 and 0.6654. In Duroc, frequency of the CC genotype was higher than other two genotypes, while the Landrace and Yorkshire breeds were primarily CT genotype.
Relationship between Pit-1 gene genotypes and growth traits: By association analysis of the growth performance and genotypes in these three breeds, the results are shown in the Table 3. At g.13700 A>G site, in Duroc, individuals with AA genotype had higher D100 than GG genotype (P < 0.05); individuals with AG genotype had greater BW70 than AA genotype, whereas which had lower D30 (P < 0.01) in Landrace. The GG genotype had greater ADG of 30-100 kg than other two genotypes (P < 0.05); individuals with AA genotype had higher D50 but lower ADG of 30-100 kg than GG genotype in Yorkshire (P < 0.01). At g.25783 C>T site, individuals with TT genotype had lower backfat thickness of 100kg body weight in Duroc (P < 0.05); individuals with CC genotype had significantly higher D100 but lower ADG of 30-100 kg than genotype TT in Landrace (P < 0.01). In Yorkshire, genotype TT showed greater in ADG of 30-100 kg compared to genotype CC (P < 0.05).
Table 1 Segmental amplification primers of Pit-1 gene.
sequence of primers (5’→3’) |
location |
size of products |
Forward primer: GTCGCATAAATACCAGCAC |
exon 1
12048-12412 bp |
365 |
Reverse primer: ATTCAAAGCGTCCATCCT |
Forward primer: GTGGATGGATTTGGTC |
intron1
13587-13780 bp |
194 |
Reverse primer: TTTACTTCCGAGGTTTA |
Forward primer: CCAACCTCCTCAATGTCTGTGC |
exon2
15698-15868 bp |
173 |
Reverse primer: GGTGTCCCAAAACTCAATCTCA |
Forward primer: CAGATAGAAATGGGGGATAA |
exon3
23488-23838 bp |
351 |
Reverse primer: GGGATTGAACAGTAACAGAGTA |
Forward primer: TTTCACAGGATACACCCAA |
exon4
25742-25907 bp |
166 |
Reverse primer: GCTTCCTCCAGCCATT |
Forward primer: GACTATTTGCCGATTTGA |
intron4
25888-26134 bp |
247 |
Reverse primer: ACTTGCCTTGCTATGTGA |
Forward primer: GCAAAAACAACTGAAAAATGTATGG |
exon5
26482-26800 bp |
319 |
Reverse primer: AGGCTGTGGTGTAGGCTGGT |
Forward primer: AACGAACAACAATCAGG |
intron5
27269-27486 |
218 |
Reverse primer: TTGCTCAGTGGGTTAAGGGT |
Forward primer: CCATCTCACACCTCCCAGTA |
exon6
27452-27605 |
154 |
Reverse primer: CTCTGCCTTCGGTTGC |
Table 2 The genotypic and allelic frequencies of Pit-1 gene SNPs in different pig breeds.
SNP site |
breed |
genotype |
genotypic frequency |
allele |
allelic frequency |
χ2 |
H |
PIC |
A13700G |
D |
AA |
0.542(32) |
A |
0.644 |
18.3** |
0.459 |
0.353 |
AG |
0.203(12) |
|
|
GG |
0.254(15) |
G |
0.356 |
L |
AA |
0.514(37) |
A |
0.639 |
15.1** |
0.461 |
0.355 |
AG |
0.250(18) |
|
|
GG |
0.236(17) |
G |
0.361 |
Y |
AA |
0.523(136) |
A |
0.639 |
65.0** |
0.462 |
0.355 |
AG |
0.231(60) |
|
|
GG |
0.246(64) |
G |
0.362 |
C25783T |
D |
CC |
0.525(31) |
C |
0.737 |
0.519 |
0.387 |
0.312 |
CT |
0.424(25) |
|
|
TT |
0.0508(3) |
T |
0.263 |
L |
CC |
0.278(20) |
C |
0.465 |
4.37* |
0.498 |
0.374 |
CT |
0.375(27) |
|
|
TT |
0.347(25) |
T |
0.535 |
Y |
CC |
0.404(105) |
C |
0.665 |
7.93** |
0.445 |
0.346 |
CT |
0.523(136) |
|
|
TT |
0.0731(19) |
T |
0.335 |
Note:D: Duroc , L: Landrace, Y: Yorkshire; *: P<0.05,**: P<0.01. 3.84<χ2<6.63 represents P<0.05, χ2>6.63:P<0.01.
Table 3 Least squares means ± SE for growth traits among genotypes of 2 SNPs in Pit-1 gene.
Site |
breed |
genotype |
n |
BW0 |
BW21 |
BW70 |
D30 |
D50 |
D100 |
ADG of 30-100 kg |
BFT |
A13700G |
D |
AA |
32 |
1.84±0.06 |
7.59±0.11 |
28.15±0.40 |
72.74±0.67 |
101.47±0.68 |
169.11±0.89a |
730±8 |
9.38±0.19 |
AG |
12 |
1.82±0.09 |
7.52±0.17 |
27.38±0.62 |
73.94±1.04 |
101.87±1.05 |
168.02±1.38ab |
748±12 |
9.53±0.30 |
GG |
15 |
1.88±0.09 |
7.36±0.17 |
27.83±0.55 |
73.00±0.93 |
101.59±0.94 |
165.69±1.23b |
757±11 |
9.20±0.27 |
L |
AA |
37 |
1.73±0.03 |
7.20±0.15 |
26.62±0.42bB |
74.94±0.70aA |
103.28±0.72 |
168.71±0.82 |
715±12b |
9.36±0.18 |
AG |
18 |
1.69±0.05 |
7.11±0.23 |
28.67±0.57aA |
71.35±0.96bB |
102.22±0.99 |
168.80±1.12 |
730±10ab |
9.19±0.25 |
GG |
17 |
1.77±0.05 |
7.09±0.24 |
28.47±0.67aAB |
71.88±1.13bAB |
102.58±1.17 |
169.85±1.31 |
759±8a |
9.51±0.29 |
Y |
AA |
136 |
1.72±0.02 |
7.31±0.09 |
26.77±0.22 |
74.12±0.40 |
103.32±0.41A |
169.42±0.45 |
720±6bB |
9.43±0.09 |
AG |
60 |
1.74±0.03 |
7.10±0.11 |
27.44±0.33 |
73.22±0.62 |
100.76±0.62B |
170.70±0.68 |
723±7bAB |
9.66±0.14 |
GG |
64 |
1.72±0.05 |
7.44±0.20 |
27.13±0.32 |
73.22±0.60 |
100.70±0.60B |
170.96±0.66 |
741±4aA |
9.67±0.13 |
C25783T |
D |
CC |
31 |
1.77±0.08 |
7.60±0.16 |
27.83±0.41 |
72.97±0.69 |
101.71±0.70 |
169.02±0.93 |
733±8 |
9.69±0.19a |
CT |
25 |
1.89±0.06 |
7.60±0.11 |
27.81±0.43 |
73.39±0.73 |
101.44±0.74 |
166.96±0.98 |
749±9 |
9.15±0.20a |
TT |
3 |
1.83±0.14 |
7.18±0.28 |
28.92±1.27 |
71.74±2.15 |
101.63±2.16 |
168.97±2.88 |
721±25 |
8.45±0.59b |
L |
CC |
20 |
1.73±0.07 |
7.14±0.31 |
28.49±0.57 |
71.65±0.97 |
100.85±0.90 |
170.68±1.04aA |
709±10B |
9.45±0.24 |
CT |
27 |
1.64±0.06 |
7.23±0.28 |
26.88±0.47 |
73.82±0.81 |
102.62±0.75 |
167.90±0.87bAB |
756±9A |
9.36±0.20 |
TT |
25 |
1.77±0.04 |
7.14±0.17 |
28.16±0.57 |
72.98±0.98 |
100.94±0.90 |
166.62±1.05bB |
749±10A |
9.18±0.24 |
Y |
CC |
105 |
1.75±0.03 |
7.30±0.13 |
27.20±0.25 |
73.33±0.46 |
102.93±0.48 |
170.80±0.50 |
729±5b |
9.50±0.10 |
CT |
136 |
1.74±0.02 |
7.23±0.09 |
26.84±0.22 |
73.89±0.41 |
102.09±0.43 |
169.19±0.46 |
741±4a |
9.58±0.09 |
TT |
19 |
1.68±0.03 |
7.28±0.14 |
27.02±0.59 |
72.60±1.09 |
102.52±1.13 |
168.92±1.20 |
742±12a |
9.50±0.25 |
Note: Among genotypes within each SNP for each trait, A,B means without a common superscript differ (P < 0.01).a–b means without a common superscript differ (P < 0.05). n indicates the number of individuals. BW21, BW70 represents body weight at 49 and 70 days. D30, D50, D100 represents days to 30 ,50, 100 kg body weight, BFT represents the backfat thickness of 100kg body weight.
DISCUSSION
In animal production, the underlying genetic nature of traits with economic interest is complex and manifests as continuous variation. Growth traits are influenced by both genetic factors and environment. Due to the current availability of neutral polymorphisms, identifying the chromosome regions which effect growth performance could be achieved (Molaee et al. 2009; Negahdary et al. 2013). For Pit-1 gene polymorphisms, several studies have been done (Xu et al,2015; Jin et al,2018; Zhang et al,2020; Sakar,2022). It was supposed by SSCP analysis of genes that those genes could have associations with growth traits, which helps establish the allelic variants as markers to aid in selection.
This study showed Pit-1’s significant genotype effect on growth performance of pigs. However, the same genotype in different pig breed which was associated with different phenotype. Thus, the associations identified in this report may be caused by linkage disequilibrium (LD) to a linked QTL instead of related to function of Pit-1 gene. In this connection, Yu et al. used haplotype analysis to show that LD is significant in the region surrounding Pit-1 for backfat in Meishan × commercial crosses (Yu et al. 1995; Yu et al. 1999). This implied that the linkage disequilibrium of Pit-1 with another locus may explain the pronounced discrepancies about its possible genotype effects among labs. The region near Pit-1 on pig chromosome 13 was associated with backfat thickness (Bidanel et al. 2001) according to QTL mapping research. Franco confirmed that Pit-1 polymorphisms were associated with fat thickness and average daily gain (Franco, et al. 2005). Stančeková et al reported that DD genotype of MspI site in Pit-1 gene was associated with significantly better backfat thickness in European Large White pigs and a crossbred population of Large White × Landrace. In Landrace breed, it was found that CC genotype significantly reduced backfat thickness and increased Lean meat percentage, eye muscle area and hind legs proportion (Liu et al. 2009). In this study, we did not detect Pit-1 MspI in the three populations. But, at the g.25783 C>T site, in Duroc breed, individuals with TT genotype had lower BFT (P < 0.05).
Overall, in this study, two novel SNPs of Pit-1 gene were identified. Genotypic and allelic frequencies of g.13700 A>G and g.25783 C>T significantly differed among the three pig breeds. This study indicates that polymorphism may be contributed to variation in traits analyzing, and enable these polymorphisms to contribute to breeding programs and molecular marker-assisted selection.
Acknowledgements: This work was supported by Leading Talents of Industrial Technology of Yunnan Province (YNWR-CYJS-2018-056), Yunnan University Science and technology innovation team.
REFERENCES
- Aarskog, D.., H. G. Eiken, R. Bjerknes and Myking (1997). Pituitary dwarfism in the R271W Pit-1 gene mutation. Eur J Pediatr,156(11):829-34. doi: 10.1007/s004310050722.
- Andersson L., C. S. Haley, H. Ellegren, S. A. Knott., M. Johansson, K. Andersson, L. Andersson-Eklund, I. Edfors-Lilja, M. Fredholm and I. Hansson (1994). Genetic mapping of quantitative trait loci for growth and fatness in pigs. Science, 263(5154):1771-1774. doi: 10.1126/science.8134840.
- Bidanel, P., D. Milan, N. Iannuccelli, Y. Amigues, M. Y. Boscher F. Bourgeois, J. C. Caritez, J. Gruand, P. Le Roy, H. Lagant, R. Quintanilla, C. Renard, J. Gellin,. L. Ollivier and C. Chevalet (2001). Detection of quantitative trait loci for growth and fatness in pigs. Genet Sel Evol,33(3):289-309. doi: 10.1186/1297-9686-33-3-289.
- Bose, S., S. Ganguly, S. Kumar, and F. R. Boockfor (2016). A Pit-1 Binding Site Adjacent to E-box133 in the Rat PRL Promoter is Necessary for Pulsatile Gene Expression Activity. Neurochem Res,41(6):1390-1400. doi: 10.1007/s11064-016-1843-y.
- Bassam, B. J., G. Caetano-Anollés and P. M. Gresshoff (1991). Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem,196(1):80-3. doi: 10.1016/0003-2697(91)90120-i.
- Cogan, J. D. and J. A. Phillips 3rd. (1998). Growth disorders caused by genetic defects in the growth hormone pathway. Adv Pediatr, 45:337-361.
- Cohen, L. E., K. Zanger, T. Brue, F. E. Wondisford, and S. Radovick (1999). Defective retinoic acid regulation of the Pit-1 gene enhancer: a novel mechanism of combined pituitary hormone deficiency. Mol Endocrinol,13(3):476-484. doi: 10.1210/mend.13.3.0251.
- Forand, A., E. Koumakis, A. Rousseau, Y. Sassier, C. Journe, J. F. Merlin, C. Leroy, V. Boitez, P. Codogno, G. Friedlander and I. Cohen. (2016). Disruption of the Phosphate Transporter Pit1 in Hepatocytes Improves Glucose Metabolism and Insulin Signaling by Modulating the USP7/IRS1 Interaction. Cell Rep,16(10):2736-2748. doi: 10.1016/j.celrep.2016.08.012.
- Franco, M. M., R. C. Antunes, H. D. Silva and L. R. Goulart (2005). Association of PIT1, GH and GHRH polymorphisms with performance and carcass traits in Landrace pigs. J Appl Genet,46(2):195-200.
- Jin S., T. He, L. Yang, Y. Tong, X. Chen and Z. Geng (2018). Association of polymorphisms in Pit-1 gene with growth and feed efficiency in meat-type chickens. Asian-Australas J Anim Sci,31(11):1685-1690. doi: 10.5713/ajas.18.0173.
- Lee, E. J., T. Russell, L. Hurley and J. L. Jameson (2005). Pituitary transcription factor-1 induces transient differentiation of adult hepatic stem cells into prolactin-producing cells in vivo. Mol Endocrinol,19(4):964-971. doi: 10.1210/me.2004-0034.
- Li, S., E. B. Crenshaw 3rd, E. J. Rawson, D. M. Simmons, L. W. Swanson and M. G. Rosenfeld (1990). Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene pit-1. Nature,347(6293):528-533. doi: 10.1038/347528a0.
- Liu, , T. Xiao, W. He, H. Ma, X. Liu, F. Liu and J. He (2009). Genetic Effect of three Loci related with Growth and Carcass Traits in Swine. Scientia Agricultura Sinica,42(2):742-747.doi: 10.3864/j.issn.0578-1752.2009.02.046.
- Molaee, V., R. Osfoori, M. P. E. Nasab and S. Qanbari (2009). Genetic relationships among six Iranian indigenous sheep populations based on microsatellite analysis. Small Rum. Res. 84(1):121–124. doi:10.1016/j.smallrumres.2009.05.004.
- Negahdary, , A. Hajihosseinlo and M. Ajdary (2013). PCR-SSCP variation of IGF1 and PIT1 Genes and their Association with Estimated Breeding Values of Growth Traits in Makooei Sheep. Genet Res Int,(7):1-6. doi: 10.1155/2013/272346.
- Nei, M., and A. K Roychoudhury (1974).Sampling variances of heterozygosity and genetic distance. Genetics,76(2):379-390. doi: 10.1093/genetics/76.2.379.
- Piórkowska, K., K. Ropkamolik and M. Oczkowicz (2013). Association study of Pit-1 and GHRH SNPs with economically important traits in pigs of three breeds reared in Poland. Animal Science Papers & Reports, 31(4):303-314.
- Roche, C., R. Rasolonjanahary, S. Thirion, I. Goddard, A. Fusco, D. Figarella-Branger, H. Dufour, T. Brue, J. L. Franc, A. Enjalbert and Barlier (2012). Inactivation of transcription factor pit-1 to target tumoral somatolactotroph cells. Hum Gene Ther,23(1):104-114. doi: 10.1089/hum.2011.105
- Sakar, Ç.M., and U. Zülkadir (2022). Determination of the relationship between Anatolian black cattle growth properties and myostatin, GHR and Pit-1 gene. Anim Biotechnol,33(3):536-545. doi: 10.1080/10495398.2021.1884566.
- Song, C., B. Gao, Y. Teng, X. Wang, Z. Wang, Q. Li, H. Mi, R. Jing and J. Mao (2005).MspI polymorphisms in the 3rd intron of the swine POU1F1 gene and their associations with growth performance. J Appl Genet,46(3):285-289.
- Stanceková, K., D. Vasícek, D. Peskovicová, J. Bulla and A. Kúbek (1999). Effect of genetic variability of the porcine pituitary-specific transcription factor (PIT-1) on carcas traits in pigs. Anim Genet,30(4):313-315. doi: 10.1046/j.1365-2052.1999.00484.x.
- Taha, D., P. E. Mullis, L. Ibáñez and F. Zegher de. (2005).Absent or delayed adrenarche in Pit-1/POU1F1 deficiency. Horm Res, 64(4):175-9. doi: 10.1159/000088793.
- Tordjman, K. M., Y. Greenman, Z. Ram, D. Hershkovitz, O. Aizenstein, O. Ariel and S. L. Asa (2019). Plurihormonal Pituitary Tumor of Pit-1 and SF-1 Lineages, with Synchronous Collision Corticotroph Tumor: a Possible Stem Cell Phenomenon. Endocr Pathol,30(1):74-80. doi: 10.1007/s12022-018-9562-3.
- Tuggle, C. K., T. P. Yu, J. Helm and M. F. Rothschild (1993). Cloning and restriction fragment length polymorphism analysis of a cDNA for swine PIT-1, a gene controlling growth hormone expression. Anim Genet,24(1):17-21. doi: 10.1111/j.1365-2052.1993.tb00913.x.
- Xu, Z. Q., J. He, C. L. Ji, Y. Zhang, Q. H. Nie, D. X. Zhang, X. Q. Zhang (2015). Polymorphisms in the 5'-flanking regions of the GH, PRL, and Pit-1 genes with Muscovy duck egg production. J Anim Sci, 93(1):28-34. doi: 10.2527/jas.2014-8071.
- Yang, D., H. Chen, X. Lan, Z. Zhang, L. Tang, L. Zhang, X. Wang, Y. Wang and H. Niu (2006). Association of polymorphisms in the Pit-1 intron 5 with body measurements in Chinese Cattle. Animal Biotechnology Bulletin,10(1),356-359.
- Yu, T. P., M. F. Rothschild and C. K. Tuggle (1993). Rapid communication: a MspI restriction fragment length polymorphism at the swine PIT-1 locus. J Anim Sci,71(8):2275. doi: 10.2527/1993.7182275x.
- Yu, T. P., C. K. Tuggle, C. B. Schmitz and M. F. Rothschild (1995). Association of PIT1 polymorphisms with growth and carcass traits in pigs. J Anim Sci, 73(5):1282-8. doi: 10.2527/1995.7351282x.
- Yu, T. P., L. Wang, C. K. Tuggle and M. F. Rothschild (1999). Mapping genes for fatness and growth on pig chromosome 13: a search in the region close to the pig PIT1 gene. J. Anim. Breed. Gene. 116(4): 269–280. doi:10.1046/j.1439-0388.1999.00198.x.
- Zhao, Q., M. E. Davis and H. C. Hines (2004). Associations of polymorphisms in the Pit-1 gene with growth and carcass traits in Angus beef cattle. J Anim Sci, 82(8):2229-2233. doi: 10.2527/2004.8282229x.
- Zhang, C., B. Du, C. Wu and S. Zhang (2017). Analysis of the Association Between Polymorphism of Pit-1 Gene and Growth Traits in Pig. Genomics and Applied Biology, 36(2):564-569. doi: 13417/j.gab.036.000564.
- Zhang, S., Y. Cui, X. Ma, J. Yong, L. Yan, M. Yang, J. Ren, F. Tang, L. Wen and J. Qiao (2020).Single-cell transcriptomics identifies divergent developmental lineage trajectories during human pituitary development. Nat Commun,11(1):5275. doi: 10.1038/s41467-020-19012-4.
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