Building the genome architecture during the maternal to zygotic transition

Proper higher-order chromatin folding can profoundly impact gene expression. In early animal development, chromatin undergoes dramatic reorganization to convert terminally differentiated gametes to early embryos. The recent rapid development of ultra-sensitive chromatin analysis technologies has revealed a drastic reconstruction of chromatin architecture, which includes a surprising relaxation followed by de novo and slow establishment of 3D genome organization in early embryos. Such progress adds another fascinating dimension to epigenetic reprogramming in early development that also features degradation of maternal RNA and activation of the zygotic genome during the maternal to zygotic transition (MZT). Nevertheless, the role of higher-order chromatin architecture in this critical developmental time window is yet to be understood. In this article, we review the latest findings from a variety of species (with a primary focus on mammals) on the establishment of 3D chromatin structure in gametogenesis and early development. These data shed light on how chromatin organization is regulated, and how it coordinates with MZT and other crucial events in early development. Finally, we discuss the crucial questions that remain to be answered in the future.