Seed Genome Hypomethylated Regions Are Enriched In Transcription Factor Genes

Abstract

The precise mechanisms that control gene activity during seed development remain largely unknown. Previously, we showed that several genes essential for seed development, including those encoding storage proteins, fatty acid biosynthesis enzymes, and transcriptional regulators, such as ABI3 and FUS3, are located within hypomethylated regions of the soybean genome. These hypomethylated regions are similar to the DNA methylation valleys (DMVs), or canyons, found in mammalian cells. Here, we address the question of the extent to which DMVs are present within seed genomes, and what role they might play in seed development. We scanned soybean and Arabidopsis seed genomes from post-fertilization through dormancy and germination for regions that contain < 5% or < 0.4% bulk methylation in CG-, CHG-, and CHH-contexts over all developmental stages. We found that DMVs represent extensive portions of seed genomes, range in size from 5 to 76 kb, are scattered throughout all chromosomes, and are hypomethylated throughout the plant life cycle. Significantly, DMVs are enriched greatly in transcription factor genes, and other developmental genes, that play critical roles in seed formation. Many DMV genes are regulated with respect to seed stage, region, and tissue - and contain H3K4me3, H3K27me3, or bivalent marks that fluctuate during development. Our results indicate that DMVs are a unique regulatory feature of both plant and animal genomes, and that a large number of seed genes are regulated in the absence of methylation changes during development - probably by the action of specific transcription factors and epigenetic events at the chromatin level.\n\nSignificanceWe scanned soybean and Arabidopsis seed genomes for hypomethylated regions, or DNA Methylation Valleys (DMVs), present in mammalian cells. A significant fraction of seed genomes contain DMV regions that have < 5% bulk DNA methylation, or, in many cases, no detectable DNA methylation. Methylation levels of seed DMVs do not vary detectably during seed development with respect to time, region, and tissue, and are present prior to fertilization. Seed DMVs are enriched in transcription factor genes and other genes critical for seed development, and are also decorated with histone marks that fluctuate with developmental stage, resembling in significant ways their animal counterparts. We conclude that many genes playing important roles in seed formation are regulated in the absence of detectable DNA methylation events, and suggest that selective action of transcriptional activators and repressors, as well as chromatin epigenetic events play important roles in making a seed - particularly embryo formation.