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Investigation of the Oviductal Glycoprotein 1 (OVGP1) Gene Associated with Embryo Survival and Development in the Rabbit1

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Investigation of the Oviductal Glycoprotein 1 (OVGP1) Gene Associated with Embryo Survival and Development in the Rabbit1 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 embryo survival and a similar embryonic stage of devel- rabbits between early embryo survival and development, opment at 48 h of gestation. However, at 72 h of ges- and the nonconservative SNP 12944C>G located in tation, the GG genotype showed greater early embryo exon 11 and the triallellic microsatellite [(GT)15T(G)5, survival than the CC genotype (0.56 embryos) and their (GT)14T(G)5, and (GT)11T(G)7)] located in the promot- embryos presented less embryonic development. Analy- er region of the oviductal glycoprotein 1 (OVGP1) gene. sis of the microsatellite was performed to ascertain the We analyzed an F2 cross of 2 lines of rabbits divergently presence or absence of the allele (GT)14T(G)5. At both selected for uterine capacity. A total of 172 and 159 stages of gestation, the (GT)14T(G)5/(GT)14T(G)5 gen- females were slaughtered at 48 and 72 h of gestation, otype showed greater early embryo survival (0.94 and respectively, to determine whether OVGP1 influences 1.54 embryos at 48 and 72 h of gestation, respectively) ovulation rate, fertilization rate, early embryo survival, and less embryonic development than the homozygous and embryonic stage of development. The results of the genotypes without the allele (GT)14T(G)5. SNP indicated that all genotypes showed similar early Key words: association study, embryo survival and development, oviductal glycoprotein 1 (OVGP1), rabbit ©2010 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2010. 88:1597–1602 doi:10.2527/jas.2009-2042 INTRODUCTION At present, a limited number of genes with large or moderate effects on litter size and its components Litter size is important for reducing the cost of pro- have been associated with SNP in multiparous species ducing rabbit meat, and much effort has been put into (Rothschild et al., 2007). The oviductal glycoprotein improving it by direct or indirect selection (Blasco et 1 (OVGP1) gene is a candidate gene for early prena- al., 1994). Ovulation rate (OR) and prenatal survival tal survival because OVGP1 is mainly expressed in the influence litter size in pigs, rabbits, and mice (see Blas- rabbit oviduct (Merchán et al., 2007). In other species co et al., 1993, for a review). In rabbits, early prenatal (i.e., sheep and cattle), the OVGP1 protein is also syn- survival has been shown to have an important influence thesized in the early stage of gestation (Nancarrow and on litter size; Torres et al. (1987) reported that em- Hill, 1995), and it plays an important role in fertiliza- bryo survival and development before 96 h of gestation tion and early cleavage-stage embryonic development in was responsible for the difference found in litter size several livestock species (Buhi, 2002; Killian, 2004). between 2 different rabbit lines. A divergent selection In rabbits, an SNP has been found in OVGP1, pro- experiment on uterine capacity also showed a difference ducing an AA change. Moreover, a triallelic microsatel- in early prenatal survival (Mocé et al., 2004; Peiró et lite located in the promoter region has been reported al., 2007). (Merchán et al., 2009). These mutations were associ- ated in the divergent lines selected by uterine capacity 1 This study was supported by Comisión Interministerial de Cien- cited before. The objective of this study was to ana- cia y Tecnología (CICYT) grants CICYT-AGL2001-3068-C03 and lyze the association of the SNP 12944C>G of exon 11 CICYT-AGL2005-07624-C03. 2 Corresponding author: [email protected] and the microsatellite located in the promoter region of Received April 14, 2009. OVPG1 with embryo survival and development at 48 Accepted January 18, 2010. and 72 h of gestation. 1597 Downloaded from jas.fass.org at Camino Polytechnic on April 14, 2010. 1598 García et al. Table 1. Data for the genotypes and traits analyzed Item Genotype Ovulation rate 48 h of gestation 72 h of gestation SNP12944C>G CC 121 40 50 CG 163 58 52 GG 47 21 10 Total 331 119 112 Microsatellite (GT)14T(G)5/(GT)14T(G)5 21 10 7 (GT)14T(G)5/− 135 48 46 −/− 174 62 60 Total 330 120 113 MATERIALS AND METHODS Traits All experimental procedures involving animals were The following traits were calculated: OR, fertilization approved by the Universidad Politécnica de Valencia rate [FR; FR = (TE/TE + OO) × 100], NorE, per- Research Ethics Committee. centage of NorE [%NorE; %NorE = (NorE/NorE + AE) × 100], percentage of EM [%EM; %EM = (EM/ NorE) × 100], percentage of CM [%CM; %CM = CM/ Animals NorE × 100], and percentage of BL [%BL; %BL = (BL/NorE) × 100]. Early embryo survival (EES) was A total of 331 animals (Table 1) from an F2 popula- analyzed as NorE recovered, fitting OR as a covariate. tion were generated from a reciprocal cross of High and Low lines of a divergent selection experiment on uter- ine capacity described by Argente et al. (1997). Details Genotyping of the Rabbit OVGP1 on the lines, breeding schemes, and crossbreeding are in the F2 Population given by Peiró et al. (2008). Animals were housed in individual metal cages at the At least 3 mL of venous blood from the marginal experimental farm of Universidad Miguel Hernández de ear vein was collected in K3EDTA plastic tubes with a Elche. They were kept under a controlled photoperiod concentration of 1.8 mg of EDTA per 1 mL of blood. (16 h light:8 h dark) and fed a pelleted commercial The samples were stored frozen (−20°C) until assayed. diet. Genomic DNA was extracted from blood samples fol- lowing the ABI Prism 6100 Nucleic Acid PrepStation protocol (Applied Biosystems, Foster City, CA). Geno- Embryo Recovery typing of the nonsilent 12944C>G SNP and the tri- allelic microsatellite [(GT)15T(G)5, (GT)14T(G)5, and All data were gathered in the same gestation. A total (GT)11T(G)7)] was performed following the protocol of 172 and 159 nonlactating females were slaughtered described by Merchán et al. (2009). The genotypes for 48 or 72 h postcoitum, respectively, by intravenous in- the SNP were designed as CC, CG, and GG. For the jection of sodium thiopental in a dose of 50 mg/kg of association study of the microsatellite, the genotypes BW (thiobarbital, B. Braun Medical S.A., Barcelona, were grouped based on the allele (GT)14T(G)5 because Spain). previous analyses indicated that this allele had a posi- The entire reproductive tract was removed. Ovula- tive effect on reproductive traits (Merchán et al., 2009). tion rate was estimated as the number of corpora hem- According to the presence or absence of this allele, orrhagica after slaughtering. Oviducts and uteri were the studied genotypes were grouped as (GT)14T(G)5/ separated and flushed once with 5 and 10 mL of 150 (GT)14T(G)5, (GT)14T(G)5/−, or −/− . mM ammonium bicarbonate solution at room tempera- ture. Embryo recovery and classification were carried Statistical Analysis out by 3 operators. The total numbers of embryos (TE) and oocytes (OO) were recovered and counted. Em- Table 1 shows the number of females per genotype bryos were classified as normal (NorE) or abnormal and trait used in this experiment. Ovulation rate at 48 (AE) according to the method of Hafez (2000). At 48 and 72 h of gestation was analyzed with the following h of gestation, all embryos were recovered from the ovi- model: ducts and NorE were classified as early morulae (EM) or compacted morulae (CM). At 72 h of gestation, em- y = μ + YS + FH + I + O bryos were recovered from oviducts and uterine horns ijklmno i j k l and were classified as EM, CM, or blastocysts (BL). + Gm + Sn + eijklmno, Downloaded from jas.fass.org at Camino Polytechnic on April 14, 2010. Oviductal glycoprotein 1 and embryo survival 1599 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 NorE FR %NorE %EM %CM %BL Mean 12.9 11.9 98.1 99.3 13.3 86.7 11.8 97.6 99.1 12.2 72.9 14.9 SD 2.5 2.3 4.9 3.7 25.7 25.7 2.7 6.3 2.9 25.8 24.3 24.7 where YSi is the effect of year-season (with 3 levels), Rv for all the embryonic stages of development was FHj is the effect of hemorrhagic follicles (with 3 levels: established as one-third of the phenotypic SD of the 0, between 1 and 5, and 6 or more follicles), Ik is the trait, or 8%. effect of the interval between weaning and mating for In Bayesian statistics, we do not work with signifi- slaughtering (with 2 levels: until 1 mo or more than cances, but with actual probabilities (see Blasco, 2001, 1 mo), Ol is the effect of operator (with 3 levels), Gm for a comparison between classical and Bayesian meth- is the effect of OVPG1 genotype [with 3 levels: CC, ods in animal genetics) so that we can estimate, on CG, and GG for the SNP 12944C>G, or (GT)14T(G)5/ one side, the probability of a difference being greater (GT)14T(G)5, (GT)14T(G)5/−, and −/− for the micro- than an Rv, which we call the probability of relevance, satellite], Sn is the effect of the time of gestation (with Pr, or, on the other side, the probability of a differ- 2 levels: 48 and 72 h after mating), and eijklmno is the ence being, in absolute value, less than an Rv (i.e., the error.
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