Sex and fetal genome influence gene expression in pig endometrium at the end of gestation

Abstract

Abstract Background A fine balance of feto-maternal resource allocation is required to support pregnancy, which depends on interactions between maternal and fetal genetic potential, maternal nutrition and environment, endometrial and placental functions. In particular, some imprinted genes have a role in regulating the exchange of nutrients between the mother and the fetus. Results In this study, we investigated the influence of the fetal genome and sex on the expression of 42 genes, including imprinted genes, at the maternal interface (endometrium) during late gestation. Pure and reciprocal crossed fetuses were produced using two extreme breeds for fetal maturity and piglet survival: Large White (LW) and Meishan (MS). Hence, in the same uterus, endometrial samples were associated with its purebred or crossbred fetuses. We first described a change in gene expression in the endometrium during late gestation (14 differentially expressed genes (DEGs)) and between the two extreme breeds (9 DEGs). The change in expression of 11 genes in LW during late gestation compared to two genes in MS suggests a delay in endometrial processes in LW. The analyses highlighted breed differences in the regulation of endometrial angiogenesis, in nutrient transport and energy metabolism. Correlation networks linked endometrial gene expression with fetal biometrics at D90 and placental measures at D110. We pointed out for the first time the impact of fetal sex and genome on endometrial expression at 90 days of gestation, emphasing AMPD3, CITED1 and H19 genes. We have demonstrated that fetal sex affects the expression of five imprinted genes in LW endometrium. Fetal genome influenced the expression of four genes in LW endometrium but not in MS endometrium. Intriguingly, both fetal sex and fetal genome interact to influence endometrial gene expression. Conclusions These data give new evidence for sexual dimorphism in the pregnant endometrium and provide evidence for the contribution of the fetal genome to feto-maternal interactions at the end of gestation. They suggest that the paternal genome may contribute significantly to piglet survival, especially in crossbreeding production systems. They once again demonstrated the plasticity of the endometrium and the importance of deciphering the dialogue between the placenta and the endometrium.