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. CAS, China) for their kind offer of DD45::GFP marker line in Col-0 and Ler background, respectively. AUTHOR CONTRIBUTIONS P.Z. and M.-x.S. designed the experiments. P.Z. and X.Z. isolated cells for RNA-seq and performed in vitro ovule microculture. K.S. and T.C. performed vector construction and plant transformation. X.Z., K.S., and Z.L. performed gene expression analyses and reporter line analysis. P.Z., D.L., Y.C., X.P, and M.-x.S. analyzed the data. P.Z. and M.-x.S. wrote the manuscript. All authors discussed the results and agreed on the manuscript before submission.