Indian Journal of Animal Research

  • Chief EditorK.M.L. Pathak

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Indian Journal of Animal Research, volume 56 issue 2 (february 2022) : 129-134

Effect of ESR, FSHB and PRLR Genes on Sperm Traits of Landrace and Yorkshire Boars in the Tropical Environmental Conditions of Vietnam

Do Duc Luc1,*, Ha Xuan Bo1, Nguyen Hoang Thinh1, Nguyen Chi Thanh1, Tran Xuan Manh2, Nguyen Van Hung2, Phan Thi Tuoi3, Vu Dinh Ton1, Farnir Frederic4
1Faculty of Animal Science, Vietnam National University of Agriculture, Trau Quy, Gia Lam, Hanoi 12406, Vietnam.
2Dabaco Nucleus Breeding Pig Company, Tien Du District, Bac Ninh Province 16416, Vietnam.
3Faculty of Agriculture, Forestry and Fishery, Hong Duc University, 565 Quang Trung street, Thanh Hoa city 40132, Thanh Hoa Province, Vietnam.
4Faculty of Veterinary Medicine, University of Liège, 6 Avenue de Cureghem, Liège 4000, Belgium.
Cite article:- Luc Duc Do, Bo Xuan Ha, Thinh Hoang Nguyen, Thanh Chi Nguyen, Manh Xuan Tran, Hung Van Nguyen, Tuoi Thi Phan, Ton Dinh Vu, Frederic Farnir (2022). Effect of ESR, FSHB and PRLR Genes on Sperm Traits of Landrace and Yorkshire Boars in the Tropical Environmental Conditions of Vietnam . Indian Journal of Animal Research. 56(2): 129-134. doi: 10.18805/IJAR.B-1278.
Background: Fertility traits in pigs made a restricted progress through traditional selection. Applying marker assisted selection could improve these traits. The aim of the study was to investigate the effects of candidate genes Estrogen Receptor (ESR), Follicle Stimulating Hormone Beta (FSHB) and Prolactin Receptor (PRLR) on sperm quality traits of Landrace and Yorkshire boars under tropical conditions in Northern Vietnam.

Methods: A total of 6306 ejaculates from 140 boars (92 Landrace and 48 Yorkshire) were collected to estimate sperm ejaculate volume (VOL), spermatozoon motility (MO), sperm concentration (CO) and total number of spermatozoon in ejaculate (NT). Ear tissue samples were collected for genotype identification of SNP present in ESR, FSHB and PRLR genes using PCR-RFLP technique. A mixed model was used to test the effect of different genetic and non-genetic factors on the sperm quality traits.

Result: The genotype frequencies of ESR, FSHB and PRLR were in Hardy-Weinberg equilibrium for each breed. Age of boars and month of the year had significant effect on all the sperm quality traits (P<0.01) while effect of breed was found to be non-significant on all the sperm quality trait. FSHB gene significantly (P<0.05) affected VOL, MO and CO. Boars with BB genotype showed positive effect on VOL but negative effect on MO and CO in comparison with AA genotype boars. ESR gene showed only effect on VOL while PRLR affected only MO. Boars with AA and AB genotypes of ESR gene had a significantly higher VOL than those with BB genotype (P<0.05). For PRLR gen, AB genotype was associated with higher MO than AA genotype (P<0.05). These results suggest a possibility of using the existing polymorphisms in ESR, FSHB and PRLR genes to improve some sperm traits of Landrace and Yorkshire boars.
Fertility is one of the important economical traits in swine production. The reproduction efficiency of the herd depends on the fertility of sows and boars (Knox, 2014; Koketsu et al., 2017). In sows, this efficiency includes litter size, farrowing rate; while in boars, it includes fertility, sperm production and sows served per sire (Knox, 2014).
The reproductive performances made limited progress through traditional selection due to low heritability of fertility traits (Rothschild et al.,1997; Urban and Kuciel, 2001) and expressing late in life to serve as useful criteria of selection (Montaldo and Meza-Herrera, 1998) such as sperm quality traits. With a molecular genetic approaches, it is possible to improve pig fertility (Rothschild et al., 1997, Melnikova et al., 2019). Spermatogenesis is a complex process that involves stem-cell renewal, genome reorganization, genome repackaging and that culminates in the production of motile gametes (Cooke and Saunders, 2002). The process of spermatogenesis is regulated by reproductive hormones in gonadotropin axis and controlled by large number of genes. Therefore, hormone and their receptors are presumed to be good candidate genes for reproductive traits (Vincent et al., 1998).
The association between Estrogen Receptor (ESR), Follicle Stimulating Hormone Beta (FSHB) and Prolactin Receptor (PRLR) polymorphisms and reproductive traits in gilts and sows was reported in previous studies (Rothschild et al., 1996; van Rens et al., 2002; Korwin-Kossakowska et al., 2003; Kapelański et al., 2013; Hunyadi-Bagi et al., 2016; Vega et al., 2018; Melnikova et al., 2019). For ESR, the presence of allele B was significantly associated with an increased litter size (Rothschild et al., 1996; Short et al., 1997; Melnikova et al., 2019). Inversely, van Rens et al., (2002) reported that Large White × Meishan F2 crossbred gilts with AA and AB genotypes had more piglets than BB. Additionally, this polymorphism did not lead to significant differences for litter size at birth and at weaning (Hunyadi-Bagi et al., 2016, Vega et al., 2018). No significant effects of the FSHB genotype on total number born and number born alive were found (Korwin-Kossakowska et al., 2003, Hunyadi-Bagi et al., 2016). For PRLR, Terman et al., (2016) reported that AA sows produced more piglets than BB sows at the first parity. However effect of PRLR was not observed in the study of Barreras-Serrano et al., (2009).
In addition, previous researches have been conducted to investigate the effect of genotypes of the candidate genes on sperm traits in boars. The boars with genotype AA of ESR showed an improved ejaculate volume, sperm alive percentage and number of spermatozoids per ejaculation compared to the boars with AB and BB genotypes (Terman et al., 2006). Similarly, AA genotype of PRLR was associated with higher percentage of normal sperm and lower percentage of sperm with proximal plasma droplets than AB and BB genotypes in Duroc boars (Huang et al., 2006). FSHB had no significant effect on sperm quality of Piétrain and Piétrain × Hampshire boars (Lin et al., 2006).
As reported above, ESR, FSHB and PRLR could act as direct or indirect functional candidate genes for association with sperm quality traits. The objective of this study was to investigate the effects of ESR, FSHB and PRLR genes on sperm traits in Landrace and Yorkshire boars under tropical conditions in Vietnam.
The experiment was carried out on 140 breeding boars (92 Landrace and 48 Yorkshire) at Dabaco Nucleus Breeding Pig Company, Bac Ninh Province, Vietnam (40 km North from Hanoi) from May 2015 to July 2018.
A total of 6306 ejaculates (4897 from Landrace and 1409 from Yorkshire) were collected from the boars. The sperm quality traits evaluated were ejaculate volume (VOL, ml), spermatozoon motility (MO, %), sperm concentration (CO, × 103/ mm3) and total number of spermatozoon in ejaculate (NT, × 109spz). VOL was determined using a graduated cylinder after filtration of the gelatinous fraction, CO and MO were estimated using Leja counting chambers with a Computer-assisted sperm analyzers Ceros II Semen Analyzer (CASA, Hamilton Thorne CEROS Model) and NT was calculated through the products of CO and the VOL.
Genotype identification
The genomic DNA was extracted from frozen ear tissue of Landrace and Yorkshire boars using G-spin Total DNA Extraction kit (INTRON Biotechnology). The polymorphisms of ESR (T1665G), FSHB (A5894G) and PRLR (G1789A) genes were determined according to methods of Short et al., (1997), Rohrer et al., (1994) and Drogemuller et al., (2001) respectively by PCR-RFLP technique at laboratory of Department of Animal Breeding and Genetics, Vietnam National University of Agriculture and at Center for Biotechnology, Dabaco group, Bac Ninh province. The detailed information on primer sequences, restriction enzymes and allele sizes are shown in Table 1. In each PCR reaction, 1 μL (20 ng/μL) of template DNA, 0.5 μL (10 μM) of each primer and 18 μL ddH2O were added to the ready Maxime PCR Premix Kit (i-Taq DNA polymerase 2.5U, dNTPs 2.5 mM, reaction buffer 10x and gel loading buffer 1x). The thermal cycling condition of PCR reactions is presented in Table 2.

Table 1: Primer sequences, restriction enzymes and allele sizes of 3 genes.


Table 2: Conditions of PCR reactions according to temperature (T) and time (Time).

Statistical analysis
Hardy-Weinberg equilibrium was tested using a Chi-square test or Fisher exact test (if expected count was less than 5). A mixed model was used to test several effects on the sperm quality traits. The fixed effects were ESR (AA, AB and BB), FSHB (AA, AB and BB), PRLR (AA, AB and BB) genotypes, breed (Landrace and Yorkshire), month of the year (January to December) and age of the boars (in month, used as a covariate) while boar ID number was included in the model as a random effect (repeated measurement).The data were analyzed using the mixed procedure for repeated measurements of SAS software version 9.3 (SAS 1989) to identify significant sources of variation. The least-squares means were compared using student t-tests.
Genotype frequencies
Genotypes frequencies of the tested SNP in ESR, FSHB and PRLR are shown in Table 3. For ESR gene, the frequency of AA genotype was high (0.81) in Landrace while it was very low (0.02) in Yorkshire. The BB genotype in FSHB gene was not found for Yorkshire boars. Three genotypes of PLRL were observed in both breed with AA frequencies of 0.48 and 0.25 for Landrace and Yorkshire respectively. The genotype frequencies of ESR, FSHB and PRLR were in Hardy-Weinberg equilibrium for each breed (P>0.160).

Table 3: Number of boars and ejaculates according to breeds and genotypes.

Effects of genotype on sperm traits
The effects of genotypes, breed, age and months of the years on sperm traits are shown in Table 4. VOL was significantly different between ESR (P=0.0259) and FSHB SNP genotypes (P=0.0321). An effect of FSHB and PRLR SNP on MO was found (P<0.0045). Only FSHB SNP affected CO (P=0.0318). Age of boars and month of the year significantly affected all sperm traits (P<0.0001) except CO (P=0.0661) while breed did not affect any trait (P>0.8524).

Table 4: Level of significance (p-value) of ESR, FSHB, PRLR genotypes, breed, age of boars and month of the year on sperm quality of Landrace and Yorkshire boars.

The effects of ESR genotypes on sperm traits are shown in Table 5. Boars with AA and AB genotypes had a significantly higher VOL than those with BB genotype (P=0.0259). There was no significant difference for MO, CO and NT among ESR genotypes.

Table 5: Sperm traits of Landrace and Yorkshire boars according to ESR genotype (LSM±SE).

The results in Table 6 show that FSHB genotype was significantly associated with VOL, MO and CO. Boars with BB genotype showed positive effect on VOL, in comparison with AA boars (P=0.0321). In contrast, AA genotype leaded to higher MO and CO than BB genotype (P<0.0318). Heterozygote AB leaded to intermediate results for both parameters. No significant effect of FSHB genotype on NT was observed in this study (P=0.6555).

Table 6: Sperm traits of Landrace and Yorkshire boars according to FSHB genotype (LSM±SE).

The PRLR genotype only significantly affected MO (Table 7). The boars with AB genotype showed higher MO than those with AA genotype (P=0.0044). No significant difference for PRLR genotypes was observed for VOL, CO and NT (P>0.3699).

Table 7: Sperm traits of Landrace and Yorkshire boars according to PRLR genotype (LSM±SE).

Genotype frequencies
From literature review, the used ESR, FSHB and PRLR SNP were shown to have three genotypes (AA, AB and BB) with varying frequencies in different swine populations. Most of the previous studies reported the predominance AA genotype for ESRS NP, in comparison with AB and BB genotypes (Terman and Kumalska 2012, Vega et al., 2018). For FSHB SNP, the predominant genotype seemed to be BB in Large White and Landrace pigs. For the PRLR gene SNP, AA genotype showed higher frequency than the others in several reports (Huang et al., 2006, Barreras-Serrano et al., 2009).
For ESR, BB genotype in Yorkshire (0.52) was higher than in Landrace (0.03) boars. In contrast, a very low frequency of AA genotype was observed in Yorkshire while it was very high in Landrace in current study. Terman et al., (2006) found a high frequency (0.83) of allele A in boar of seven different breeds. While boar with BB genotype was not observed in Piétrain and Hampshire × Piétrain. Zinnatova et al., (2014) found only heterozygote AB in the Landrace and Large White boars.
The AA genotype of the FSHB gene was more frequent than BB genotype in both breeds. In particularly, there was not any Yorkshire boars with BB genotype observed in the present study. A research by Lin et al., (2006) revealed that allele A showed a high frequency in Piétrain (0.83) and the Piétrain × Hampshire (0.82) boars. Similarly, Korwin-Kossakowska et al., (2003) reported allele A frequencies of more than 0.90 in a synthetic pig line, which was selected for reproductive traits. In contrast, studies of Kapelański et al., (2013) and Polasik et al., (2016) showed that BB genotype in Landrace gilts was predominant. In the last two study, the frequency of BB was more than 0.82.
In our study, the allele A of the PRLR SNP was more frequent than allele B in both breeds. This result is in agreement with findings in the Duroc and Landrace boars (Huang et al., 2006). The effect of selection, different allelic frequencies in the founder animals and random genetic drift could have caused allele frequencies to differ among lines (Linville et al., 2001).
Effects of genotype on sperm traits
In the present study, the ESR gene SNP was proven to significantly (P<0.05) affect only ejaculate volume in boars. VOL of the boars carrying allele A was higher than those carrying allele B. This finding is not in agreement with the report of Terman et al., (2006) where VOL was not significantly different between boars carrying alleles A and B. Additionally, the authors also found the effect of ESR genotypes on CO, sperm alive percentage and number of alive sperm. The total number spermatozoa were significantly higher in BB boars compared to AA and AB genotypes in Danube white pigs (Stoyanova et al., 2010) and in Large White pigs (Kostenko and Sydorenko, 2011).
The polymorphism of the FSHB locus was significantly associated with VOL, MO and CO of the boars. Boars with BB genotype showed the highest ejaculate VOL and the lowest CO and MO values. In contrast, AA genotype was associated with the lowest ejaculate VOL but with the highest CO and MO. Inversely, Lin et al., (2006) did not find any association between FSHB and sperm traits in Piétrain and Piétrain × Hampshire boars. Ford et al., (1997) reported a negative relationship in mature Meishan boars between FSH secretion and testicular size accompanied with decreased total daily sperm production; FSH affected spermatogenesis (Zanella et al., 1999). The functional association evidence of the FSHB gene arises from knockout experiments showing that deficiency at the FSHB gene leads to decrease sperm concentration to 75% in mice (Layman, 2000).
In current study, PRLR gene significantly affected sperm motility of the Landrace and Yorkshire boars. MO of boars with AA genotype was lower than those with AB. This result was not consistent with report of Huang et al., (2006) that Duroc boars with the AA genotype had significantly better semen quality, which higher VOL (P<0.05) and MO tended to be higher than those with the AB genotype (P<0.1). In contrast, no significant effect of the PRLR locus was observed on any semen trait of the Piétrain and the Piétrain × Hampshire crossbred population (Lin et al., 2006). These results indicate that effect of PRLR depends on the different breeds.
The boars with AA, AB (ESR) and BB (FSHB) genotypes produced ejaculates of larger volume than the other genotypes. The AA (FSHB) and AB (PRLR) genotype were significantly associated with higher percentage of MO than the others. Only AA genotype of FSHB showed high CO compared to BB genotype. Genotypes did not affect VAC and NT of sperm. These results suggest a possibility of using the existing polymorphisms in ESRFSHB and PRLR gene to improve some sperm traits of boars.
The authors thank the directorate of Dabaco nucleus breeding pigs company, Bac Ninh Province, Vietnam for the contribution.
This study was funded by Ministry of Agriculture and Rural Development, Vietnam.
Ethical approval
Not applicable for this type of study in Vietnam.
Informed consent
This data are published with consent of Dabaco nucleus breeding pigs company, Bac Ninh Province, Vietnam.
Conflict of interest
The authors declare that they have no conflict of interest.

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