Running title: Somatic cell transcriptional support to the oocyte Summary Sentence: Oocytes rely on the surrounding cumulus cells to complete their RNA reserves required for their maturation through transzonal projections; a synapse-like system.

Even after several decades of quiescent storage in the ovary, the female germ cell is capable of reinitiating transcription to build its reserves that are essential to support early embryonic development. In the current model of mammalian oogenesis, there exists bilateral communication between the gamete and the surrounding cells that is limited to paracrine signaling and direct transfer of small molecules via gap junctions existing at the end of the somatic cells’ projections that are in contact with the oolema. The purpose of this work was to explore the role of cumulus cell projections as a means of conductance of large molecules including RNA to the mammalian oocyte. By studying nascent RNA with confocal and transmission electron microscopy in combination with transcript detection , we show that the somatic cells surrounding the fully grown bovine oocyte contribute to the maternal reserves by actively transferring large cargo, including mRNA and long non-coding RNA. This occurrence was further demonstrated by the re-construction of cumulus oocyte complexes with transfected cumulus cells transferring a synthetic transcript. We propose selective transfer of transcripts occurs which delivery is supported by a remarkable synapse-like vesicular trafficking connection between the cumulus cells and the gamete. This unexpected exogenous contribution to the maternal stores offers a new perspective to the determinants of female fertility.