Nucleation-dependent propagation of Polycomb modifications emerges during the <i>Drosophila</i> maternal to zygotic transition

Polycomb group (PcG) histone modifications, H3K27me3 and H2Aub, emerge during early embryogenesis in Drosophila, marking the onset of zygotic genome activation. Researchers utilized ChIP-seq and live imaging of CRISPR-engineered GFP-tagged PcG components to study the spatial and temporal dynamics of these modifications. They found that PRC2-dependent H3K27me3 accumulates near a subset of E(z)-bound prospective Polycomb response elements (PREs) starting in nuclear cycle 14 (NC14), suggesting a nucleation followed by spreading pattern.

Interestingly, factors responsible for PRE binding, such as Pho, Combgap, and GAGA-factor, were absent from interphase nuclei before NC10, even though E(z) was nuclear during early interphases. Genetic experiments revealed that GAGA-factor is not essential for PcG domain establishment, while pioneer factor Zelda plays a crucial role in the deposition of H3K27me3 and H2Aub at specific Polycomb domains.

The role of Zelda at these domains is context-dependent; it aids in E(z) recruitment for some targets but licenses an E(z)-loaded PRE to deposit H3K27me3 for others. The study supports a model where the licensing of PcG domains initiates the regulatory processes governing Polycomb-regulated developmental genes.