Antagonist <i>Xist</i> and <i>Tsix</i> co-transcription during mouse oogenesis and maternal <i>Xist</i> expression during pre-implantation development calls into question the nature of the maternal imprint on the X chromosome

During the first divisions of the female mouse embryo, the paternal X-chromosome is coated by <i>Xist</i> non-coding RNA and gradually silenced. This imprinted X-inactivation principally results from the apposition, during oocyte growth, of an imprint on the X-inactivation master control region: the X-inactivation center (<i>Xic</i>). This maternal imprint of yet unknown nature is thought to prevent <i>Xist</i> upregulation from the maternal X (X^M) during early female development. In order to provide further insight into the X^M imprinting mechanism, we applied single-cell approaches to oocytes and pre-implantation embryos at different stages of development to analyze the expression of candidate genes within the <i>Xic</i>. We show that, unlike the situation pertaining in most other cellular contexts, in early-growing oocytes, <i>Xist</i> and <i>Tsix</i> sense and antisense transcription occur simultaneously from the same chromosome. Additionally, during early development, <i>Xist</i> appears to be transiently transcribed from the X^M in some blastomeres of late 2-cell embryos concomitant with the general activation of the genome indicating that X^M imprinting does not completely suppress maternal <i>Xist</i> transcription during embryo cleavage stages. These unexpected transcriptional regulations of the <i>Xist</i> locus call for a re-evaluation of the early functioning of the maternal imprint on the X-chromosome and suggest that <i>Xist</i>/<i>Tsix</i> antagonist transcriptional activities may participate in imprinting the maternal locus as described at other loci subject to parental imprinting.