A small RNA pathway functions during the oocyte-to-embryo transition in "Caenorhabditis elegans"

A fundamental reprogramming occurs during the oocyte-to-embryo transition (OET) of an animal, from a transcriptionally silent, differentiated oocyte to a pluripotent early embryo. The two major events contributing to the cell fate change are maternal transcript degradation and embryonic genome activation (EGA). We used Caenorhabditis elegans as a model to study the mechanisms controlling EGA during this developmental window and performed a genetic screen for the unbiased identification of new involved players. We discovered several factors inhibiting a precocious onset of EGA in germ cells, among them several components of the CSR-1 endogenous-small interfering RNA (endo-siRNA) pathway. This pathway employs the Argonaute protein CSR-1 to load small RNAs and has been implicated in diverse processes in germ cells and early embryos. Here, we demonstrate a role for this pathway in the repression of embryonic genes in developing oocytes. Moreover, we found that the catalytic activity of CSR-1 to degrade RNAs is required for this function. The importance of such a post-transcriptional role is in accordance with previous findings, which described a function for the RNA-binding proteins GLD-1 and LIN-41 in germ cell fate control. Our discovery of a direct interaction of CSR-1 and LIN-41 suggests a co-regulatory role for the two proteins in EGA repression. Together, the results contribute to the understanding of the reprogramming during the C. elegans OET and highlight for the first time the importance of endo-siRNAs in this process.