The Zygotic Transition Is Initiated in Unicellular Plant Zygotes with Asymmetric Activation of Parental Genomes

Abstract

The zygotic transition, from a fertilized egg to an embryo, is central to animal and plant reproduction. Animal embryos depend upon maternally provided factors until zygotic genome activation (ZGA). In plants, the timing and parental genome contributions to ZGA are unresolved. Here, we use the flowering plant Oryza sativa (rice) to characterize transcriptomes of time-staged isogenic and hybrid zygotes following fertilization. Large-scale transcriptomic changes were observed in unicellular zygotes, including upregulation of S-phase genes, a characteristic of ZGA. The parental contributions to ZGA were highly asymmetric. Zygotic transcription was primarily from the maternal genome and included genes for basic cellular processes. Transcription of the paternal genome was highly restricted but unexpectedly included genes encoding putative pluripotency factors expressed at the onset of ZGA. Thus, distinct transcriptional activities are exhibited by the parental genomes during the initiation of embryogenesis, which presumptively derive from divergent pre-zygotic transcriptional states established in the gametes.

Reprogramming of 24nt siRNAs in rice gametes

“…Three lines of evidence indicated RNA contamination from ovary in egg cells was minimal. First, our egg or zygote isolation method has previously been shown to have little mRNA contamination from maternal tissue (Anderson et al 2017;Li et al 2019). Second, we performed differential expression analysis of the miRNAs, and found that eight miRNAs had high levels in all three replicates of ovary but were nearly undetectable in all six replicates of egg cells (Fig.…”

“…Analysis of published gamete transcriptomes did not reveal any obvious explanation for egg or sperm siRNA patterns, though they did show dramatic differences in mRNA levels for some RdDM factors such as RDR2 (Anderson et al 2013;Anderson et al 2017) (Supplemental Fig. 7).…”

“…We first looked at microRNA (miRNA) expression across different sample types and produced a complete list of miRNA abundances (Supplemental Dataset 1). miRNAs are predicted to be more cell-autonomous than siRNAs (Grant-Downton et al 2013), and since mRNA expression is globally different between egg, sperm, and seedling (Russell et al 2012;Anderson et al 2013;Anderson et al 2017), we also expected regulators of gene expression, such as miRNAs, to be differentially expressed across sample types. We first performed principal component analysis (PCA, Fig .…”

“…There are currently no available small RNA transcriptomes from sperm cells other than Arabidopsis, and none from egg cells for any plant. Due to the small size of the sperm cell relative to the egg cell (~1/1000 the volume), the transcriptome of the fertilized egg is primarily determined by the egg cell (Autran et al 2011;Del Toro-De León et al 2014;Anderson et al 2017;Zhao et al 2019).…”

Epigenetic responses to abiotic stresses during reproductive development in cereals

“…It was further suggested that this is epigenetically regulated (e.g., Baroux and Grossniklaus 2015; Grimanelli et al 2005; Nodine and Bartel 2012; Zhao et al 2017; Zhao and Sun 2015). However, recent evidence using genome-wide transcriptional analysis in maize and rice revealed that zygotic genome activation occurs soon after fertilization, exhibiting a highly dynamic and partially transient pattern of gene expression (Chen et al 2017; Anderson et al 2017). These include genes involved in hormone biosynthesis and responses, RdDM, and other pathways associated with massive chromatin changes after fertilization.…”