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DNA and histone modifications identify a putative controlling element (CE) on the X chromosome of Sciara coprophila

ABSTRACT: In Sciara coprophila, paternally inherited X chromosomes are imprinted and selectively eliminated during early embryonic development. A controlling element (CE) located on the X chromosome is known to play a decisive role in this process, although the exact mechanism remains unknown. In this study, we test a proposed model in which the maternal cytoplasm regulates CE activity and thereby controls Xp elimination during embryogenesis. Using our de novo Sciara genome assembly, along with ChIP-Seq and MeDIP analyses, we identified a 1.2 Mb region within the CE locus that exhibits a repressive epigenetic signature on X chromosomes that are retained. These findings provide molecular support for the model. Remarkably, this signature also includes a unique enrichment of CpG methylation, suggesting a strong evolutionary conservation of imprinting mechanisms and identifying a promising candidate for the long-sought CE locus responsible for somatic Xp-chromosome elimination.

ORGANISM(S): Bradysia coprophila

PROVIDER: GSE299219 | GEO | 2025/06/11

REPOSITORIES: GEO

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Project description:In naïve human pluripotent stem cells (hPSCs) that represent the pre-implantation embryonic states, epigenetic regulators for cell identity remain poorly defined. One of the major remaining questions in naïve stem cell biology is how female cells mediate and regulate X chromosome inactivation (XCI). Recent studies incorporating single-cell RNA sequencing (scRNA-seq) have demonstrated that transcript-based technologies are insufficient to unequivocally resolve XCI regulation in a human system. Instead, 3D genomics shows immense promise for studying XCI by interrogating changes to the X chromosomes’ 3D states. Here, we sought to characterize the 3D state of the X chromosome in naïve and primed hPSCs. Using chromatin tracing, we analyzed the folding conformations of whole X chromosomes with megabase genomic resolution in multiple naïve and primed hPSC lines. Our data found that X chromosomes in female naive hPSCs exhibit a range of spatial folding conformations similar to the active X chromosome (Xa) and the inactive X chromosome (Xi) in somatic cells; these data suggest that naïve hPSCs have initiated XCI. As XCI process ultimately generates detectable differences in volume between the Xa and the Xi, we measured the radius of gyration of individual X chromosome copies across various hPSC cell lines and culture conditions. In naïve hPSCs, our results show that the X chromosomes with Xi-like conformations are not more compact than those with Xa-like conformation. This finding is directly counter to the Xi compaction typically observed in post-XCI female somatic cells. These contradictory 3D signatures of XCI suggest that female naïve hPSCs have initiated the XCI process, but are poised before XCI-driven silencing in a metastable state. As observed in H7 naïve hPSCs, this metastable state can be abolished through classically noted means, such as the loss of Xp chromatin, leading to the deleted p X chromosome (dXp). The Xp loss observed here seems to drive XIST expression and accumulation around the dXp chromosome. Overall, our findings provide insight into the previously undefined X chromosome status in naïve hPSCs in single chromosome resolution, and are critical in understanding the unique epigenetic regulation in early embryonic cells.

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DNA and histone modifications identify a putative controlling element (CE) on the X chromosome of Sciara coprophila

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