Epigenome in Early Mammalian Development: Inheritance, Reprogramming and Establishment

Drastic epigenetic reprogramming takes place during preimplantation development, leading to the conversion of terminally differentiated gametes to a totipotent embryo. Deficiencies in remodeling of the epigenomes can cause severe developmental defects, including embryonic lethality. However, how chromatin modifications and chromatin organization are reprogrammed upon fertilization in mammals has long remained elusive. Here, we review recent progress in understanding how the epigenome is dynamically regulated during early mammalian development. The latest studies, including many from genome-wide perspectives, have revealed unusual principles of reprogramming for histone modifications, chromatin accessibility, and 3D chromatin architecture. These advances have shed light on the regulatory network controlling the earliest development and maternal-zygotic transition. Fertilization triggers drastic epigenomic reprogramming that converts fully differentiated gametes to totipotent embryos. Early embryos show noncanonical epigenomes compared with somatic cells and embryonic stem cells. Allele- and locus-specific inheritance and erasure of parental epigenetic information ensure a successful transition from the parents to the early embryos. Subsequent establishment of proper zygotic epigenome is essential for embryogenesis. Chromatin reprogramming during early development includes multilevel reorganization of chromatin accessibility, chromatin modifications, and higher-order chromatin architecture.