Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos

Abstract

Summary In animals, maternal gene products deposited into eggs regulate embryonic development before activation of the zygotic genome1. In plants, an analogous period of prolonged maternal control over embryogenesis is thought to occur based on gene-expression studies2–6. However, other gene-expression studies and genetic analyses show that some transcripts must derive from the early zygotic genome7–14, implying that the prevailing model does not fully explain the nature of zygotic genome activation in plants. To determine the maternal, paternal and zygotic contributions to the early embryonic transcriptome, we sequenced the transcripts of hybrid embryos from crosses between two polymorphic inbred lines of Arabidopsis thaliana and used single-nucleotide polymorphisms (SNPs) diagnostic of each parental line to quantify parental contributions. Although some transcripts appeared to be either inherited from primarily one parent or transcribed from imprinted loci, the vast majority of transcripts were produced in near-equal amounts from both maternal and paternal alleles, even during the initial stages of embryogenesis. Results of reporter experiments and analyses of transcripts from genes that are not expressed in sperm and egg indicate early and widespread zygotic transcription. Thus, in contrast to early animal embryogenesis, early plant embryogenesis is mostly under zygotic control.

Two Arabidopsis Loci Encode Novel Eukaryotic Initiation Factor 4E Isoforms That Are Functionally Distinct from the Conserved Plant Eukaryotic Initiation Factor 4E

“…However, RNA-Seq data can distinguish between the two genes and indicate that in flower tissue (Jiao and Meyerowitz, 2010;Niederhuth et al, 2013), shoot apical meristem (Torti et al, 2012), developing embryos (Nodine and Bartel, 2012), and the central cell of the female gamete (Schmid et al, 2012), EIF4E1B mRNA is expressed and associates with polysomes in flowers (Jiao and Meyerowitz, 2010); however, EIF4E1C mRNA was at much lower to undetectable levels in these tissues. In an analysis of 80 genomes released by the 1001 Genomes Project, EIF4E1C was predicted to be spontaneously deleted in 12 strains, suggesting that it is likely not providing any advantage to promote its retention in the genome .…”

Imprinting meets genomics: new insights and new challenges

“…In an effort to understand when the zygotic genome becomes transcriptionally active, Nodine and Bartel performed mRNA-seq on very young Arabidopsis reciprocal F 1 hybrid embryos (1-cell/2-cell, 8-cell, and ~32-cell stages) [32]. In contrast to animal models and a previous plant investigation, which described the embryo as predominantly controlled by the maternal genome [33], Nodine and Bartel found that maternally and paternally inherited genomes contribute largely equally to the early embryonic transcriptome.…”

“…Nodine and Bartel's findings [32] indicated that both genomes switch on soon after fertilization occurs [36]. Yet the plant embryo is not fully autonomous and is subject to parental conflicting control.…”

Identification of genes preferentially expressed in wheat egg cells and zygotes

“…The timing of zygotic gene 14 activation (ZGA) in plants is somewhat controversial (Baroux et al 2008;Zhao et al 2011;15 Nodine and Barte2012). Recent data, however, indicate that it follows fertilization very early 16 and the first steps of embryogenesis are mostly under zygotic control in Arabidopsis and 17 tobacco (Nodine and Bartel 2012;Zhao et al 2011). In animals, the extent of maternal 18 control and the timing of MZT vary greatly among species, and the MZT not always 19 coincides with the gradual process of ZGA (for review; Shen-Orr et al 2010).…”