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Bulk RNA-sequencing of wild-type (Ler) and dme-2 calli harvested 7 days after incubation on callus-inducing medium and of de novo regenerated shoots harvested 14 days after incubation on shoot-inducing medium

ABSTRACT: Plants possess high potential for somatic cell reprogramming. Despite extensive studies on the molecular network and key genetic factors during regeneration, the underlying epigenetic landscape remains incompletely understood. Here, we explored methylome and transcriptome dynamics during two-step plant regeneration. During leaf-to-callus transition, genic CG methylation shifts, while pericentromeric regions undergo substantial CG and extensive CHH hypomethylation. Upon shoot regeneration, methylation increases across all cytosine contexts, particularly in pericentromeric regions, coinciding with RNA-directed DNA methylation (RdDM) pathway activation. However, the DEMETER (DME)-deficient dme-2 mutant exhibited significant genic CG redistribution and global non-CG hypomethylation, partly due to RdDM downregulation. The dme-2 mutant affects gene expression in pluripotency and shoot meristem development, promoting regeneration through a reprogrammed state by pericentromeric hypomethylation. Our study demonstrates the intimate linkage between DME demethylase and RdDM underlying pericentromeric non-CG methylation maintenance, providing insight into the epigenetic mechanisms balancing pluripotency states and genome stability during plant regeneration.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE269609 | GEO | 2024/10/25

REPOSITORIES: GEO

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Project description:Epigenetic reprogramming is required for proper regulation of gene expression in eukaryotic organisms. In Arabidopsis, active DNA demethylation is crucial for seed viability, pollen function, and successful reproduction. The DEMETER (DME) DNA glycosylase initiates localized DNA demethylation in vegetative and central cells, so-called companion cells that are adjacent to sperm and egg gametes, respectively. In rice, the central cell genome displays local DNA hypomethylation, suggesting that active DNA demethylation also occurs in rice, however, the enzyme responsible for this process is unknown. One candidate is the rice REPRESSOR OF SILENCING 1a (ROS1a) gene, which is related to DME and is essential for rice seed viability and pollen function. Here, we report genome-wide analyses of DNA methylation in wild-type and ros1a mutant sperm and vegetative cells. We find that the rice vegetative cell genome is locally hypomethylated compared to sperm by a process that requires ROS1a activity. We show that many ROS1a target sequences in the vegetative cell are hypomethylated in the rice central cell, suggesting that ROS1a also demethylates the central cell genome. Similar to Arabidopsis, we show that sperm non-CG methylation is indirectly promoted by DNA demethylation in the vegetative cell. These results reveal that DNA glycosylase-mediated DNA demethylation processes are conserved in Arabidopsis and rice, plant species that diverged 150 million years ago. Finally, although global non-CG methylation levels of sperm and egg differ, the maternal and paternal embryo genomes show similar non-CG methylation levels, suggesting that rice gamete genomes undergo dynamic DNA methylation reprogramming after cell fusion.

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