After fertilization, zygotic genome activation (ZGA) results in a transcriptionally competent embryo. Hybrid transcriptome experiments in Arabidopsis have concluded that the maternal and paternal genomes make equal contributions to zygotes and embryos, yet embryo defective (emb) mutants in the Columbia (Col) ecotype display early maternal effects. Here we show that hybridization of Col with Landsberg erecta (Ler) or Cape Verde Islands (Cvi) ecotypes decreases maternal effects of emb mutants. Reanalysis of Col/Ler and Col/Cvi transcriptomes confirmed equal parental contributions in Col/Cvi early embryos. By contrast, thousands of genes in Col/Ler zygotes and 1-cell embryos were biallelic in one cross and monoallelic in the reciprocal cross, with analysis of intron reads pointing to active transcription as responsible for this parent-of-origin bias. Our analysis shows that, contrary to previous conclusions, the maternal and paternal genomes in Col/Ler zygotes are activated in an asymmetric manner. The decrease in maternal effects in hybrid embryos compared to isogenic Col plus differences in genome activation between Col/Cvi and Col/Ler suggest that neither of these hybrids accurately reflects general trends of parent-of-origin regulation in Arabidopsis embryogenesis.

Previous studies have alternately supported and discounted the hypothesis that the maternal genome plays a predominant role in early embryogenesis in plants. We used 24 embryo defective (emb) mutants of Arabidopsis thaliana to test for maternal and paternal effects in early embryogenesis. 5 emb mutants had equal maternal and paternal effects, 5 showed maternal effects and weak paternal effects, and the remaining 14 emb mutants conditioned only maternal effects, demonstrating a more important role for the maternal allele for most of these EMB genes. To assess genome-wide maternal and paternal contributions to early embryos, we produced allele-specific transcriptomes from zygote to mature stage embryos derived from reciprocal crosses of Columbia-0 and Tsu-1, a hybrid combination we show to be a faithful proxy for isogenic Columbia-0. Parent-of-origin analysis of these transcriptomes revealed a reciprocal maternal bias in thousands of genes from the zygote to octant stage. This bias greatly diminished by the globular stage, and was absent at later stages. Comparison with egg cell transcriptomes revealed no correlation between transcript levels in the egg and maternal bias in pre-globular embryos, suggesting that the maternal bias observed in early embryos is due to preferential zygotic transcription of maternal alleles. Taken together, the functional and transcriptome data presented here support a predominant role for the maternal genome in early Arabidopsis embryogenesis. SignificanceIn both animals and plants, the zygote is produced by the union of the egg and sperm cells. In animals, it is well accepted that mRNAs and proteins from the egg direct the first steps of embryogenesis. Here we present genetic and genomic experiments that support a predominant role for the maternal genome in early embryogenesis of plants, as well. In contrast to animals, our data suggest that this maternal influence is primarily derived not from inheritance of egg transcripts, but from preferential transcription of maternal alleles in the zygote and early embryo. This transient maternal zygotic bias may reflect an ancestral condition to diminish paternal influence on early embryogenesis in outcrossing plants.