Maternal genome dominance in early plant embryogenesis

Abstract

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.

Developmental and genomic architecture of plant embryogenesis: from model plant to crops

“…In maize hybrids, maternal and paternal contributions play an essential role in heterosis and kernel development ( Meyer et al., 2007 ). In Arabidopsis , the effects of hybridization of different ecotypes have been proposed to at least partly explain the differences seen in parent-of-origin gene expression between different hybrid combinations ( Autran et al., 2011 ; Nodine and Bartel, 2012 ; Del Toro-De León et al., 2014 ; Del Toro-De León et al., 2016 ; Zhao et al., 2019 ; Alaniz-Fabián et al., 2020 ). The effect of maternal and paternal gene contributions at early stages of embryo development on hybrid vigor has not been critically evaluated and might be of great importance for seed yield.…”