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Single-cell three dimensional genome structures of rice egg, sperm, and unicellular zygote

ABSTRACT: Chromatin conformation capture assays, such as 3C and Hi-C, allow for studies of three-dimensional (3D) genome structures in bulk samples through proximity ligation of DNA. However, the difference between cells can only be observed by single-cell measurements that avoid ensemble averaging3, 4,5. To study 3D chromatin organization and dynamics before and after fertilization in flowering plants, we analyzed the 3D genomes of rice egg, sperm, and unicellular zygote as well as shoot cells. We show that chromatin architectures of rice egg and sperm are comparable to that of somatic cells and are reorganized after fertilization in unicellular zygote. The rice single cell 3D genomes display specific features of chromosome compartments and configuration of telomeres/centromeres compared to those shown in mammalian single cells. Active and silent chromatin domains gather to form multiple foci in the nuclear space. Notably, the 3D genomes of egg, unicellular zygote, and shoot cells contain a compact silent center (CSC), which is absent in sperm. CSC is dynamically reorganized after fertilization and is likely to be involved in gene regulation related to zygotic genome activation (ZGA). Our results reveal specific 3D genome features of plant gametes and unicellular zygote and provide a spatial chromatin basis for ZGA and gene expression in plant.

ORGANISM(S): Oryza sativa Japonica Group

PROVIDER: GSE123109 | GEO | 2019/05/26

REPOSITORIES: GEO

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Project description:The formation of a zygote by the fusion of egg and sperm involves the two gametic transcriptomes. In flowering plants, the embryo sac embedded within the ovule contains the egg cell, while the pollen grain contains two sperm cells inside a supporting vegetative cell. The difficulties of collecting isolated gametes and consequent low recovery of RNA have restricted in-depth analysis of gametic transcriptomes in flowering plants. We isolated living egg cells, sperm cells, and pollen vegetative cells from rice, and identified transcripts for ~36,000 genes by deep sequencing. The three transcriptomes are highly divergent, with about three quarters of those genes differentially expressed in the different cell types. Distinctive expression profiles were observed for genes involved in chromatin conformation, including an unexpected expression in the sperm cell of genes associated with active chromatin. Furthermore, both the sperm cell and the pollen vegetative cell were deficient in expression of key RNAi components. Differences in gene expression were also observed for genes for hormonal signaling and cell cycle regulation. The egg cell and sperm cell transcriptomes reveal major differences in gene expression to be resolved in the zygote, including pathways affecting chromatin configuration, hormones and cell cycle. The sex-specific differences in expression of RNAi components suggest that epigenetic silencing in the zygote might act predominantly through female-dependent pathways. More generally, this study provides a detailed gene expression landscape for flowering plant gametes, enabling the identification of specific gametic functions and their contributions to zygote and seed development. The gene expression profiles of the three gametic cells, egg cell (EC), sperm cell (Sp) and vegetative cell (Ve) were compared via RNA-seq using three biological replicates for each. Differential expression (DE) analysis was performed using edgeR and the resulting DE genes were assessed for Gene Ontology term enrichment.

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Single-cell three dimensional genome structures of rice egg, sperm, and unicellular zygote

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