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The 5-methylcytosine DNA glycosylase ROS1 prevents paternal genome hypermethylation in Arabidopsis endosperm

ABSTRACT: DNA methylation patterning is a consequence of opposing activities of DNA methyltransferases and DNA demethylases. In many species, reproduction is a period of significant epigenome lability. In flowering plants, two distinct female gametes, the egg cell and the central cell, are fertilized, producing the embryo and the endosperm, respectively, of the seed. The endosperm is an unusual tissue, exemplified by triploidy and reduced DNA methylation. In Arabidopsis thaliana, a 5-methylcytosine DNA glycosylase, DME, demethylates regions in the central cell genome, leading to methylation differences between maternally- and paternally-inherited endosperm genomes after fertilization. Expression of DME in the central cell is required for gene imprinting, or parent-of-origin specific gene expression, in endosperm. DME is part of a four member gene family in Arabidopsis that includes ROS1, DML2 and DML3. It is unknown whether any of the other DNA glycosylases are required for endosperm methylation patterning. Using whole-genome methylation profiling, we identify ROS1 target regions in the endosperm. We show that ROS1 prevents hypermethylation of paternally-inherited alleles in the endosperm at regions that lack maternal or paternal-allele methylation in wild-type. Thus, ROS1 promotes epigenetic symmetry between parental genomes in the endosperm by preventing paternal genome hypermethylation. We propose that ROS1 and DME act in a parent-of-origin-specific manner at shared endosperm targets, and consider possible implications for the evolution of imprinting mechanisms.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE280598 | GEO | 2025/03/28

REPOSITORIES: GEO

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Project description:In plants, imprinted gene expression occurs in endosperm seed tissue and can be associated with differential DNA methylation between maternal and paternal alleles. Imprinting is theorized to have been selected for because of conflict between parental genomes in offspring, but most studies of imprinting have been conducted in Arabidopsis thaliana, an inbred primarily self-fertilizing species that should have limited parental conflict. We examined embryo and endosperm allele-specific expression and DNA methylation genome-wide in the wild outcrossing species Arabidopsis lyrata. Here we show that the majority of A. lyrata imprinted genes exhibit parentally-biased expression in A. thaliana, suggesting that there is evolutionary conservation in gene imprinting. Surprisingly, we discovered substantial interspecies differences in methylation features associated with paternally expressed imprinted genes (PEGs). Unlike A. thaliana, the maternal allele of many A. lyrata PEGs was hypermethylated in the CHG context. Increased maternal allele CHG methylation was associated with increased expression bias in favor of the paternal allele. We propose that CHG methylation maintains or reinforces repression of maternal alleles of PEGs. These data suggest that while the genes subject to imprinting are largely conserved, there is flexibility in the epigenetic mechanisms employed between closely related species to maintain monoallelic expression. This supports the idea that imprinting of specific genes is a functional phenomenon, and not simply a byproduct of seed epigenomic reprogramming. Examination of total gene expression, parent-of-origin specific allelic bias, or DNA methylation in embryo, endosperm, flower bud or seedcoat tissue from Arabidopsis lyrata accessions MN47 (MN), Karhumaki (Kar or KA), and crosses between them. High-throughput Illumina poly-A-selected mRNA-seq was used to identify imprinted genes in A. lyrata, and high-throughput Illumina whole genome bisulfite-sequencing was used to examine DNA methylation. mRNA-seq samples are designated MMxFF_T# where MM is the mother of the cross (either MN for MN47 or KA for Kar), FF is the father, T is the tissue (E for embryo, N for endosperm, S for seedcoat, b for buds), and # is the replicate numbers. Samples obtained from bisulfite sequencing follow the same naming but have suffix _BS and indicate cytosine methylation context (CpG, CHG, or CHH). For KAxMN bisulfite sequencing, additional files MMxFF_T#_BS_P_C.txt follow the same naming scheme but contain context-specific methylation data (C) from reads that mapped preferentially to one parent strain (P).

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The 5-methylcytosine DNA glycosylase ROS1 prevents paternal genome hypermethylation in Arabidopsis endosperm

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