Two-Step Maternal-to-Zygotic Transition with Two-Phase Parental Genome Contributions

The maternal-to-zygotic transition (MZT) is an essential developmental turning point in both plants and animals. In plants, the timing of MZT and parental contributions to the zygotic transcriptome remain unclear. Here, by overcoming technical limitations, we characterize the Arabidopsis egg cell, zygote, and embryo transcriptomes across multiple stages. Using these datasets, we demonstrate that MZT occurs during zygote development and is a two-step interrelated process of rapid maternal transcript degradation followed by large-scale de novo transcription. Parental contributions to the zygotic transcriptome are stage-dependent: the spherical zygote is characterized by a maternally dominated transcriptome, whereas the elongated zygote transcriptome shows equal parental contributions. Our results show that plant MZT is similar to that in animals, showing a typical two-step process, and that zygotic genome activation is required for zygote elongation and division, indicating that de novo transcripts are essential for the establishment of zygote polarity and embryogenesis promotion. [Display omitted] •Plant maternal-to-zygotic transition (MZT) occurs during zygote development•Zygotic genome activation (ZGA) is required for zygote elongation and division•Plant MZT starts with rapid maternal transcript clearance that is followed by ZGA•Maternal and paternal genomes contribute equally to the de novo transcripts in zygote Maternal-to-zygotic transition (MZT) is an essential developmental turning point in both plants and animals. Zhao et al. characterize Arabidopsis egg cell, zygote, and embryo transcriptomes and demonstrate that a two-step MZT process occurs during zygote development. Relative parental contributions from maternal and paternal genomes to the zygotic transcriptome are stage dependent.