Spatiotemporal dynamics of zygotic genome activation in basal chordates revealed by interspecific hybrids

Zygotic genome activation (ZGA), a universal process in early embryogenesis that occurs during the maternal-to-zygotic transition, involves reprogramming in the zygotic nucleus that initiates global transcription. In recent decades, knowledge of this process has been acquired from research on various model organisms; however, a consensus explanation of the mechanism underlying the process, especially in relation to housekeeping gene reactivation, is lacking. Here, we used hybrids derived from two ascidian species (Ciona robusta and C. savignyi), which diverged >120 Mya with significant divergence among most orthologous genes, to symmetrically document the unique dynamics of ZGA in urochordates. We found two co-ordinated waves of ZGA, representing early developmental and housekeeping gene reactivation, during the 8-cell to 110-cell stage. Comparative analysis revealed the regulatory connection between maternal and zygotic genes as well as allelic-specific expression in a species-rather than parental-related manner, which was attributed to the divergence of cis-regulatory elements. Single-cell RNA sequencing revealed that spatial differential reactivation of paternal housekeeping genes was significantly correlated with the mechanical property of each cell type. These findings potentially provide a new system for understanding the evolution and adaptation of strategies regulating ZGA in basal chordates.