1 Abstract
The majority of pregnancy loss in ruminants occurs during the preimplantation stage, which is thus the most critical period determining reproductive success. While ovulation rate is the major determinant of litter size in sheep, interactions among the conceptus, corpus luteum and endometrium are essential for pregnancy success. To evaluate the role of reproductive tract function in sheep fertility, we performed a comparative transcriptome study by sequencing total RNA (mRNA and miRNA) from corpus luteum (CL) and endometrium tissues collected during the preimplantation stage of pregnancy in Finnsheep, Texel and F1 crosses. A total of 21,287 genes and 599 miRNAs were expressed in our dataset. Ten out of the top 25 most highly expressed genes were shared across tissues, indicating the complementary functions of the CL and endometrium. Moreover, highly expressed autosomal genes in the endometrium and CL were associated with biological processes such as progesterone formation (STAR and HSD3B1) in the CL and facilitation of maternal recognition of pregnancy, trophoblast elongation and implantation (LGALS15, CST3, CST6, and EEF1A1) in the endometrium. In the CL, a group of sialic acid-binding immunoglobulin (Ig)-like lectins (Siglecs), solute carriers (SLC13A5, SLC15A2, SLC44A5) and chemokines (CCL5, CXCL13, CXCL9) were upregulated in Finnsheep, while several multidrug resistance-associated proteins (MRPs) were upregulated in Texel ewes. We also identified a novel ERV gene located in a reduced FecL locus that is associated with sheep prolificacy and is upregulated in prolific Finnsheep. Moreover, we report, for the first time in any species, several genes that are active in the CL during early pregnancy (including SIGLEC13, SIGLEC14, SIGLEC6, MRP4, and CA5A). Importantly, functional analysis of differentially expressed genes suggested that Finnsheep have a better immune system than Texel and that high prolificacy in Finnsheep might be governed by immune system regulation. Taken together, the findings of this study provide new insights into the interplay between the CL and the endometrium in gene expression dynamics during early pregnancy. The data and results will serve as a basis for studying this highly critical period of pregnancy, which has wide significance in mammalian fertility and reproduction.