Investigation of the oviductal glycoprotein 1 (OVGP1) gene associated
with embryo survival and development in the rabbit1
M. L. García,*2 R. Peiró,† M. J. Argente,* M. Merchán,‡ J. M. Folch,‡ A. Blasco,†
and M. A. Santacreu†
*Departamento de Tecnología Agroalimentaria, Universidad Miguel Hernández de Elche, 03312, Orihuela,
Spain; †Instituto de Ciencia y Tecnología Animal, Universidad Politécnica de Valencia, PO Box 22012, 46071,
Valencia, Spain; and ‡Departament de Ciència Animal i dels Aliments,
Universitat Autònoma de Barcelona, 08193, Bellaterra, Spain
ABSTRACT: An association study was performed in
rabbits between early embryo survival and development,
and the nonconservative SNP 12944C>G located in
exon 11 and the triallellic microsatellite [(GT)15T(G)5,
(GT)14T(G)5, and (GT)11T(G)7)] located in the promoter region of the oviductal glycoprotein 1 (OVGP1) gene.
We analyzed an F2 cross of 2 lines of rabbits divergently
selected for uterine capacity. A total of 172 and 159
females were slaughtered at 48 and 72 h of gestation,
respectively, to determine whether OVGP1 influences
ovulation rate, fertilization rate, early embryo survival,
and embryonic stage of development. The results of the
SNP indicated that all genotypes showed similar early
embryo survival and a similar embryonic stage of development at 48 h of gestation. However, at 72 h of gestation, the GG genotype showed greater early embryo
survival than the CC genotype (0.56 embryos) and their
embryos presented less embryonic development. Analysis of the microsatellite was performed to ascertain the
presence or absence of the allele (GT)14T(G)5. At both
stages of gestation, the (GT)14T(G)5/(GT)14T(G)5 genotype showed greater early embryo survival (0.94 and
1.54 embryos at 48 and 72 h of gestation, respectively)
and less embryonic development than the homozygous
genotypes without the allele (GT)14T(G)5.
Key words: association study, embryo survival and development, oviductal glycoprotein 1 (OVGP1), rabbit
©2010 American Society of Animal Science. All rights reserved.
INTRODUCTION
Litter size is important for reducing the cost of producing rabbit meat, and much effort has been put into
improving it by direct or indirect selection (Blasco et
al., 1994). Ovulation rate (OR) and prenatal survival
influence litter size in pigs, rabbits, and mice (see Blasco et al., 1993, for a review). In rabbits, early prenatal
survival has been shown to have an important influence
on litter size; Torres et al. (1987) reported that embryo survival and development before 96 h of gestation
was responsible for the difference found in litter size
between 2 different rabbit lines. A divergent selection
experiment on uterine capacity also showed a difference
in early prenatal survival (Mocé et al., 2004; Peiró et
al., 2007).
1
This study was supported by Comisión Interministerial de Ciencia y Tecnología (CICYT) grants CICYT-AGL2001-3068-C03 and
CICYT-AGL2005-07624-C03.
2
Corresponding author: [email protected]
Received April 14, 2009.
Accepted January 18, 2010.
J. Anim. Sci. 2010. 88:1597–1602
doi:10.2527/jas.2009-2042
At present, a limited number of genes with large
or moderate effects on litter size and its components
have been associated with SNP in multiparous species
(Rothschild et al., 2007). The oviductal glycoprotein
1 (OVGP1) gene is a candidate gene for early prenatal survival because OVGP1 is mainly expressed in the
rabbit oviduct (Merchán et al., 2007). In other species
(i.e., sheep and cattle), the OVGP1 protein is also synthesized in the early stage of gestation (Nancarrow and
Hill, 1995), and it plays an important role in fertilization and early cleavage-stage embryonic development in
several livestock species (Buhi, 2002; Killian, 2004).
In rabbits, an SNP has been found in OVGP1, producing an AA change. Moreover, a triallelic microsatellite located in the promoter region has been reported
(Merchán et al., 2009). These mutations were associated in the divergent lines selected by uterine capacity
cited before. The objective of this study was to analyze the association of the SNP 12944C>G of exon 11
and the microsatellite located in the promoter region of
OVPG1 with embryo survival and development at 48
and 72 h of gestation.
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Table 1. Data for the genotypes and traits analyzed
Item
Genotype
SNP12944C>G
CC
CG
GG
Total
(GT)14T(G)5/(GT)14T(G)5
(GT)14T(G)5/−
−/−
Total
Microsatellite
MATERIALS AND METHODS
All experimental procedures involving animals were
approved by the Universidad Politécnica de Valencia
Research Ethics Committee.
Animals
A total of 331 animals (Table 1) from an F2 population were generated from a reciprocal cross of High and
Low lines of a divergent selection experiment on uterine capacity described by Argente et al. (1997). Details
on the lines, breeding schemes, and crossbreeding are
given by Peiró et al. (2008).
Animals were housed in individual metal cages at the
experimental farm of Universidad Miguel Hernández de
Elche. They were kept under a controlled photoperiod
(16 h light:8 h dark) and fed a pelleted commercial
diet.
Embryo Recovery
All data were gathered in the same gestation. A total
of 172 and 159 nonlactating females were slaughtered
48 or 72 h postcoitum, respectively, by intravenous injection of sodium thiopental in a dose of 50 mg/kg of
BW (thiobarbital, B. Braun Medical S.A., Barcelona,
Spain).
The entire reproductive tract was removed. Ovulation rate was estimated as the number of corpora hemorrhagica after slaughtering. Oviducts and uteri were
separated and flushed once with 5 and 10 mL of 150
mM ammonium bicarbonate solution at room temperature. Embryo recovery and classification were carried
out by 3 operators. The total numbers of embryos (TE)
and oocytes (OO) were recovered and counted. Embryos were classified as normal (NorE) or abnormal
(AE) according to the method of Hafez (2000). At 48
h of gestation, all embryos were recovered from the oviducts and NorE were classified as early morulae (EM)
or compacted morulae (CM). At 72 h of gestation, embryos were recovered from oviducts and uterine horns
and were classified as EM, CM, or blastocysts (BL).
Ovulation rate
48 h of gestation
72 h of gestation
121
163
47
331
21
135
174
330
40
58
21
119
10
48
62
120
50
52
10
112
7
46
60
113
Traits
The following traits were calculated: OR, fertilization
rate [FR; FR = (TE/TE + OO) × 100], NorE, percentage of NorE [%NorE; %NorE = (NorE/NorE +
AE) × 100], percentage of EM [%EM; %EM = (EM/
NorE) × 100], percentage of CM [%CM; %CM = CM/
NorE × 100], and percentage of BL [%BL; %BL =
(BL/NorE) × 100]. Early embryo survival (EES) was
analyzed as NorE recovered, fitting OR as a covariate.
Genotyping of the Rabbit OVGP1
in the F2 Population
At least 3 mL of venous blood from the marginal
ear vein was collected in K3EDTA plastic tubes with a
concentration of 1.8 mg of EDTA per 1 mL of blood.
The samples were stored frozen (−20°C) until assayed.
Genomic DNA was extracted from blood samples following the ABI Prism 6100 Nucleic Acid PrepStation
protocol (Applied Biosystems, Foster City, CA). Genotyping of the nonsilent 12944C>G SNP and the triallelic microsatellite [(GT)15T(G)5, (GT)14T(G)5, and
(GT)11T(G)7)] was performed following the protocol
described by Merchán et al. (2009). The genotypes for
the SNP were designed as CC, CG, and GG. For the
association study of the microsatellite, the genotypes
were grouped based on the allele (GT)14T(G)5 because
previous analyses indicated that this allele had a positive effect on reproductive traits (Merchán et al., 2009).
According to the presence or absence of this allele,
the studied genotypes were grouped as (GT)14T(G)5/
(GT)14T(G)5, (GT)14T(G)5/−, or −/− .
Statistical Analysis
Table 1 shows the number of females per genotype
and trait used in this experiment. Ovulation rate at 48
and 72 h of gestation was analyzed with the following
model:
yijklmno = μ + YSi + FHj + Ik + Ol
+ Gm + Sn + eijklmno,
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Oviductal glycoprotein 1 and embryo survival
Table 2. Mean and SD for ovulation rate (OR); normal embryos (NorE); fertilization rate (FR); percentage of
NorE (%NorE); and percentages of early morulae (%EM), compacted morulae (%CM), and blastocysts (%BL)
48 h of gestation
72 h of gestation
Item
OR
NorE
FR
%NorE
%EM
%CM
Mean
SD
12.9
2.5
11.9
2.3
98.1
4.9
99.3
3.7
13.3
25.7
86.7
25.7
where YSi is the effect of year-season (with 3 levels),
FHj is the effect of hemorrhagic follicles (with 3 levels:
0, between 1 and 5, and 6 or more follicles), Ik is the
effect of the interval between weaning and mating for
slaughtering (with 2 levels: until 1 mo or more than
1 mo), Ol is the effect of operator (with 3 levels), Gm
is the effect of OVPG1 genotype [with 3 levels: CC,
CG, and GG for the SNP 12944C>G, or (GT)14T(G)5/
(GT)14T(G)5, (GT)14T(G)5/−, and −/− for the microsatellite], Sn is the effect of the time of gestation (with
2 levels: 48 and 72 h after mating), and eijklmno is the
error.
Fertilization rate, EES, and embryonic stage of development at 48 h of gestation were analyzed using the
former model without the effect of time of gestation.
Fertilization rate, EES, and embryonic stage of development at 72 h of gestation were analyzed using the
same model as before, including the effect of the presence or absence of embryos in the uterus. Early embryo
survival at 48 and 72 h was analyzed as NorE, with OR
included as a covariate.
Traits were analyzed using a Bayesian approach.
Data were conditionally distributed as
(
)
y b , σ2e  N Xb, Iσ2e , where b contains the effects to be estimated. The
known incidence matrix is X, and I is the identity matrix. Bounded uniform priors were used for all unknown
parameters. Marginal posterior distributions of all unknowns were estimated using Gibbs sampling. A chain
of 120,000 samples was used, with a burn-in period of
20,000. Convergence was tested using the Z-criterion of
Geweke, and Monte Carlo sampling errors were computed using the time-series procedures described by
Geyer (1992).
Inferences were made from the estimated marginal
posterior distributions of the differences (D) between
genotypes as in the study by Peiró et al. (2008). We
proposed what we consider to be relevant values, Rv,
for these differences. We consider Rv = 0.5 kits and Rv
= 3.5% to be relevant differences for OR and FR, as
discussed by Peiró et al. (2008), and Rv = 0.25 embryos
to be a relevant difference for EES because Mocé et al.
(2004) found that one-half the difference in the number
of implanted embryos in the lines that originated from
our population occurred before 72 h of gestation. The
NorE
FR
%NorE
%EM
%CM
%BL
11.8
2.7
97.6
6.3
99.1
2.9
12.2
25.8
72.9
24.3
14.9
24.7
Rv for all the embryonic stages of development was
established as one-third of the phenotypic SD of the
trait, or 8%.
In Bayesian statistics, we do not work with significances, but with actual probabilities (see Blasco, 2001,
for a comparison between classical and Bayesian methods in animal genetics) so that we can estimate, on
one side, the probability of a difference being greater
than an Rv, which we call the probability of relevance,
Pr, or, on the other side, the probability of a difference being, in absolute value, less than an Rv (i.e., the
probability of both treatments being similar in biological or economic terms), which we call the probability
of similarity, Ps. The latter probability allowed us to
distinguish a case in which both treatments had equal
effects (increased Ps) from a case in which we did not
find differences between treatments because of poor
precision. In the latter case, both Ps and Pr would be
decreased.
RESULTS
Table 2 shows means and SD for the traits measured.
Fertilization rate was high (approximately 98%) at 48
and 72 h of gestation. The %NorE was large, and most
embryos were also classified as CM in both stages of
gestation.
Features of D between the CC and GG genotypes are
presented in Table 3. All Monte Carlo SE were small
and the Geweke Z-test did not detect a lack of convergence in any case. Marginal posterior distributions were
approximately normal.
The homozygote genotypes had similar OR and FR
at 48 and 72 h of gestation because the difference between homozygote genotypes was small (Table 3). At
48 h of gestation, both homozygote genotypes had similar EES, but they seemed to have a smaller %EM (D =
−6.16%). At 72 h of gestation, the CC genotype showed
less EES than the GG genotype (D = −0.56 embryos;
P = 86%). Indeed, the probability of the GG genotype
having at least 0.5 embryos more than the CC genotype
was Pr = 73%. Furthermore, their embryos presented
a greater embryonic stage of development because the
CC genotype showed a smaller %EM and a greater
%BL than the GG genotype.
Table 3 also shows results for the CC and CG genotypes. Both genotypes had similar OR (Ps = 90%), FR
(Ps = 100%), and embryo survival and development at
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García et al.
Table 3. Features of the estimated marginal posterior distributions of the differences
(D) between different genotypes of the 12944C>G SNP of oviductal glycoprotein 1
(OVGP1) for ovulation rate (OR); fertilization rate (FR); early embryo survival (EES);
and percentages of early morulae (%EM), compacted morulae (%CM), and blastocysts
(%BL) at 48 and 72 h of gestation1
CC-GG
Item
OR
48 h
FR
EES
%EM
72 h
FR
EES
%EM
%CM
%BL
1
CC-CG
D
SD
P, %
0.39
−1.77
0.03
−6.16
−3.02
−0.56
−10.32
2.48
7.60
0.42
1.28
0.34
7.28
2.20
0.51
8.92
10.85
7.25
83
91
54
79
91
86
86
58
83
D
SD
P, %
0.01
−0.42
0.17
5.88
−3.19
−0.80
1.14
−6.22
5.40
0.28
1.01
0.26
5.58
1.19
0.30
5.07
6.01
4.12
52
67
73
85
99
100
59
85
90
P, % = P(D >0) when D >0 and P(D <0) when D <0.
48 h of gestation. Nevertheless, when the traits were
analyzed at 72 h of gestation, we observed that the CC
genotype had less EES (D = −0.80 embryos) than the
CG genotype. Moreover, the probability that the CG
genotype had at least 0.5 embryos more than the CC
genotype was Pr = 96%. However, similar embryonic
stages of development were observed.
Table 4 shows the results of the estimated D between
the (GT)14T(G)5/(GT)14T(G)5 and −/− genotypes.
The (GT)14T(G)5/(GT)14T(G)5 genotype had a greater
OR than the −/− genotype. At 48 h of gestation, the
(GT)14T(G)5/(GT)14T(G)5 genotype had greater EES
(D = 0.94 embryos) than the −/− genotype. Furthermore, the (GT)14T(G)5/(GT)14T(G)5 genotype showed
less embryonic development than the −/− genotype
because the %EM was greater (D = 27.52%). At 72 h
of gestation, the (GT)14T(G)5/(GT)14T(G)5 genotype
had a greater FR (D = 7.24%) and EES (D = 1.54 embryos) than the −/− genotype. Indeed, the probability
of the (GT)14T(G)5/(GT)14T(G)5 genotype having at
least 0.5 embryos more than the −/− genotype was
Pr = 90%. Regarding the embryonic stage of development, the (GT)14T(G)5/(GT)14T(G)5 genotype showed
a greater %EM (D = 9.13%) and a smaller %BL (D =
−20.53%).
The (GT)14T(G)5/(GT)14T(G)5 genotype had an OR
similar to the heterozygote genotype (Table 4). The
(GT)14T(G)5/(GT)14T(G)5 genotype showed a decreased FR, although the difference was relatively small.
Although the (GT)14T(G)5/(GT)14T(G)5 genotype had
less EES at 48 h of gestation than the heterozygote
genotype, the homozygote genotype showed greater
EES at 72 h of gestation (0.89 embryos). Moreover, the
probability of the homozygote genotype having at least
Table 4. Features of the estimated marginal posterior distributions of the differences (D) between different genotypes of the microsatellite of oviductal glycoprotein 1 (OVGP1) for ovulation rate (OR); fertilization rate (FR);
early embryo survival (EES); and percentages of early morulae (%EM), compacted morulae (%CM), and blastocysts (%BL) at 48 and 72 h of gestation1
[(GT)14T(G)5/(GT)14T(G)5] − (−/−)
Item
OR
48 h
FR
EES
%EM
72 h
FR
EES
%EM
%CM
%BL
1
[(GT)14T(G)5/(GT)14T(G)5] − [(GT)14T(G)5/−]
D
SD
P, %
1.47
2.17
0.94
27.52
7.24
1.54
9.13
11.89
−20.53
0.84
2.84
0.73
26.06
3.91
0.97
16.85
19.50
13.67
96
78
90
85
96
94
71
73
93
D
SD
P, %
0.10
−3.16
−0.34
−12.86
3.10
0.89
−5.30
2.72
2.63
0.53
1.63
0.41
15.94
3.38
0.65
11.62
14.03
9.48
58
97
76
79
55
90
66
58
60
P, % = P(D >0) when D >0 and P(D <0) when D <0.
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Oviductal glycoprotein 1 and embryo survival
0.5 embryos more than the heterozygote genotype was
Pr = 82%. At both stages of gestation, both genotypes
had similar embryonic stages of development.
DISCUSSION
We propose the OVPG1 as a candidate gene to explain part of the variability in EES in the rabbit. Until
72 h of gestation, the embryos are still in the oviduct,
where the OVPG1 is mainly expressed (Merchán et al.,
2007).
The full sequence and structure of the rabbit OVPG1
was reported by Merchán et al. (2007). A SNP 12944C>G
associated with the lines divergently selected by uterine
capacity was found in exon 11, determining the AA
change Arg468Gly. Moreover, a triallelic microsatellite
located in the promoter region was reported (Merchán
et al., 2009).
In this paper, we study the association of this gene
with the EES and early embryo development at 48 and
72 h of gestation. The GG genotype had greater EES
(0.56 embryos) and less development at 72 h of gestation than the CC genotype. The difference found between homozygote genotypes for the SNP at 72 h of
gestation is relevant, representing 21 and 40% of the
phenotypic SD of EES and %EM, respectively. Merchán et al. (2009) found that the GG genotype had 0.83
more implanted embryos and 0.58 more kits born alive
than the CC genotype in the same population. A large
part of the difference at implantation was then found at
72 h of gestation. Similar results were found when the
microsatellite was analyzed, representing 57 and 83% of
the phenotypic SD of EES and %BL, respectively. At
this stage of gestation, it seems that the heterozygote
genotype had EES similar to the GG genotype and that
their embryos showed less embryonic development. No
clear pattern of results was observed when the microsatellite was analyzed.
These polymorphisms were found in a divergent selection experiment on uterine capacity in the rabbit,
as described by Merchán et al. (2009). However, the
line selected to decrease uterine capacity was associated
with the polymorphisms with greater EES.
Little information is available on the effect of OVGP1
on EES and early embryo development. Yong et al.
(2002) suggested that early embryo development is inhibited when the C-terminal region of the oviductin
protein is blocked. Because the SNP 12944C>G was
located in exon 11 and it produces an AA change that
is located in the C-terminal region of the protein, this
SNP could modify embryo survival and development.
On the other hand, the microsatellite was located in
the promoter region, and it could change OVGP1 and
protein expression. Results from an in vitro experiment
with sheep showed an improvement in embryo survival
when the concentration of oviductin was augmented
(Hill et al., 1996a). Contradictory results were obtained
when oviductin concentration was related to the embry-
1601
onic stage of development (Hill et al., 1996a,b; Kouba
et al., 2000, in pigs).
The analyzed polymorphisms, located in the promoter region of OVPG1 in rabbits, revealed a conservative
region homologous to that in humans. These polymorphisms are known to be close to ERE gene transactivation, the TATA-box region, and also the transcriptional
region (Merchán et al., 2009). In humans, several studies have indicated that the presence of polymorphisms
in the promoter region can modify gene expression because these polymorphisms can alter the transcription
factors, the chromatin structure, or the DNA conformation (Kashi et al., 1997; Iglesias et al., 2004; Szalai et
al., 2005; Buckland, 2006).
In conclusion, the GG genotype of the SNP of exon
11 and the (GT)14T(G)5/(GT)14T(G)5 genotype of the
microsatellite located in the promoter region of OVPG1
showed a favorable association with EES and less embryo development in the first stages of gestation. More
research is needed to confirm the association of these
polymorphisms in commercial lines.
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