Chromatin landscape at cis-regulatory elements orchestrates cell fate decisions in early embryogenesis

Francesco Cardamone, Annamaria Piva, Eva Löser, Bastian Eichenberger, Mari Carmen Romero-Mulero, Fides Zenk, Emily J. Shields, Nina Cabezas-Wallscheid, Roberto Bonasio, Guido Tiana, Yinxiu Zhan () and Nicola Iovino ()
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Francesco Cardamone: Max Planck Institute of Immunobiology and Epigenetics
Annamaria Piva: IRCCS
Eva Löser: Max Planck Institute of Immunobiology and Epigenetics
Bastian Eichenberger: IRCCS
Mari Carmen Romero-Mulero: Max Planck Institute of Immunobiology and Epigenetics
Fides Zenk: EPFL – Ecole Polytechnique Federal Lusanne
Emily J. Shields: University of Pennsylvania Perelman School of Medicine
Nina Cabezas-Wallscheid: Max Planck Institute of Immunobiology and Epigenetics
Roberto Bonasio: University of Pennsylvania Perelman School of Medicine
Guido Tiana: Università degli Studi di Milano and INFN
Yinxiu Zhan: IRCCS
Nicola Iovino: Max Planck Institute of Immunobiology and Epigenetics

Nature Communications, 2025, vol. 16, issue 1, 1-22

Abstract: Abstract The establishment of germ layers during early development is crucial for body formation. The Drosophila zygote serves as a model for investigating these transitions in relation to the chromatin landscape. However, the cellular heterogeneity of the blastoderm embryo poses a challenge for gaining mechanistic insights. Using 10× Multiome, we simultaneously analyzed the in vivo epigenomic and transcriptomic states of wild-type, E(z)-, and CBP-depleted embryos during zygotic genome activation at single-cell resolution. We found that pre-zygotic H3K27me3 safeguards tissue-specific gene expression by modulating cis-regulatory elements. Furthermore, we demonstrate that CBP is essential for cell fate specification functioning as a transcriptional activator by stabilizing transcriptional factors binding at key developmental genes. Surprisingly, while CBP depletion leads to transcriptional arrest, chromatin accessibility continues to progress independently through the retention of stalled RNA Polymerase II. Our study reveals fundamental principles of chromatin-mediated gene regulation essential for establishing and maintaining cellular identities during early embryogenesis.

Date: 2025
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DOI: 10.1038/s41467-025-57719-4

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