Partitioning of Transposon-Rich Maternal DNA is a Prerequisite for Embryonic Gene Activation

The maternal-to-zygotic transition (MZT) marks a fundamental shift in embryonic control from maternally supplied factors to zygotic gene activation, a process critical for vertebrate development. Contrary to the long-standing view that gene promoters are the earliest transcriptional targets, we demonstrate that maternally inherited transposon-rich repetitive DNA regions in zebrafish embryos are initially transcriptionally active and bound by RNA Polymerase II (Pol II). Following fertilization, these repetitive regions undergo progressive chromatin compaction, directed by the histone methyltransferase G9a, which releases Pol II to relocate from intergenic loci to gene promoters, enabling robust activation of developmental genes. Loss of G9a disrupts this process, causing persistent Pol II binding at repetitive elements and delaying activation of embryonic genes. Our findings redefine vast genomic repetitive DNA regions as a collective regulatory sponge that is essential for timely gene activation and reveal a novel mechanism by which maternal chromatin partitioning governs embryonic developmental progression.