Abstract
Pre-implantation development is a dynamic, complex and precisely regulated process that is critical for mammalian development. There is currently no description of the role of the long noncoding RNAs (lncRNAs) during the pre-implantation stages in the goat. The in vivo transcriptomes of oocytes (n = 3) and pre-implantation stages (n=19) at seven developmental stages in the goat were analyzed by RNA sequencing (RNA-Seq). The major zygotic gene activation (ZGA) event was found to occur between the 8- and 16-cell stages in the pre-implantation stages. We identified 5,160 differentially expressed lncRNAs (DELs) in developmental stage comparisons and functional analyses of the major and minor ZGAs. Fourteen lncRNA modules were found corresponding to specific pre-implantation developmental stages by weighted gene co-expression network analysis (WGCNA). A comprehensive analysis of the lncRNAs at each developmental transition of high correlation modules was done. We also identified lncRNA-mRNA networks and hub-lncRNAs for the high correlation modules at each stage. The extensive association of lncRNA target genes with other embryonic genes suggests an important regulatory role for lncRNAs in embryonic development. These data will facilitate further exploration of the role of lncRNAs in the developmental transformation in the pre-implantation stage.
Highlights
Pre-implantation development comprises complex and dynamic regulatory processes involving specific and stable gene expression patterns that maintain the viability of the embryo
10,197 differentially expressed mRNAs were identified, and the largest change was observed between 8-cell and 16-cell in two consecutive comparison groups (Figure 2C). Functional analysis of these differentially expressed mRNAs was enriched in 110 Gene Ontology (GO) terms, including “metabolic,” “binding,” and “biosynthetic processes,” as well as “enzymatic activity,” such as “cell part,” “cellular macromolecule metabolic process,” “cellular biosynthetic process,” “ribonucleotide binding,” “phosphoprotein phosphatase activity” and other terms. This stratification indicated that goat zygotic gene activation (ZGA) occurs between the 8- and 16-cell stages (Figure 2D)
The top 5 hub-long noncoding RNAs (lncRNAs) in the 6-cell stage goat all target activating transcription factor 1(ATF1), which has proved to be one of the key regulators of the ZGA (Table S11). These results indicate that the hublncRNAs we identified in our current weighted gene co-expression network analysis (WGCNA) may have a critical regulatory role in the pre-implantation developmental stage of the goat
Summary
Pre-implantation development comprises complex and dynamic regulatory processes involving specific and stable gene expression patterns that maintain the viability of the embryo. Highly complex tissues are composed of different cell types that are formed by cell fate and cell differentiation (Lokken and Ralston, 2016; Bissiere et al, 2018). Analysis of the spatiotemporal patterns of gene expression in goat pre-implantation stages is essential for clarifying early developmental processes in this species. The key stage in the transition from germ cells to embryonic development is zygotic gene activation (ZGA), which induces developmental blocks of embryonic development (Lee et al, 2014). The timing of mammalian ZGA process is species-specific; it occurs from the point of oocyte maturation until mRNA transcriptional activity in the embryo. The initiation of major ZGA events have been reported to be the 2-cell stage in mouse (Xue et al, 2013), 4-cell stage in pig (Cao et al, 2014), and LncRNA During in Vivo Pre-Implantation
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