Sperm-borne mRNAs: potential roles in zygote genome activation and epigenetic inheritance

It is well accepted that sperm carry an RNA cargo with functions in early embryo development. However, most research has focused on the role of small RNAs, such as microRNAs, transfer RNAs and long non-coding RNAs, while protein-coding messenger RNAs (mRNAs) received less attention, even though they represent a substantial amount of the sperm RNA pool. Here, we curated mouse transcriptomic data from mature sperm and selected the most abundant mRNAs (above the 0.7 quantile). The obtained gene list was further filtered using two criteria: (i) mRNAs that are statistically higher in the one-cell embryo compared to the MII oocyte transcriptome, indicative of paternal mRNA contribution after fertilization; and (ii) mRNAs that are found bound to ribosomes in the one-cell embryo, indicative of positive translation in the zygote translatome. Our analysis identified 94 genes that form networks functionally involved in epigenetic chromatin organization, gene expression, RNA processing and translation during zygote genome activation. These findings underscore the significant role of sperm-borne mRNAs in early embryonic development and epigenetic inheritance, highlighting the need for further research to fully understand their functions.