Abstract
Intronic regions of eukaryotic genomes accumulate many Transposable Elements (TEs). Intronic TEs often trigger the formation of transcriptionally repressive heterochromatin, even within transcription-permissive chromatin environments. Although TE-bearing introns are widely observed in eukaryotic genomes, their epigenetic states, impacts on gene regulation and function, and their contributions to genetic diversity and evolution, remain poorly understood. In this study, we investigated the genome-wide distribution of intronic TEs and their epigenetic states in the Oryza sativa genome, where TEs comprise 35% of the genome. We found that over 10% of rice genes contain intronic heterochromatin, most of which are associated with TEs and repetitive sequences. These heterochromatic introns are longer and highly enriched in promoter-proximal positions. On the other hand, introns also accumulate hypomethylated short TEs. Genes with heterochromatic introns are implicated in various biological functions. Transcription of genes bearing intronic heterochromatin is regulated by an epigenetic mechanism involving the conserved factor OsIBM2, mutation of which results in severe developmental and reproductive defects. Furthermore, we found that heterochromatic introns evolve rapidly compared to non-heterochromatic introns. Our study demonstrates that heterochromatin is a common epigenetic feature associated with actively transcribed genes in the rice genome.
Highlights
Genomes of eukaryotes contain substantial numbers of transposable elements (TEs), which shape genomic structures and epigenomic landscapes [1, 2]
We investigated the genome-wide distribution of intronic TEs and their epigenetic states in the Oryza sativa genome, where TEs comprise 35% of the genome
We found that over 10% of rice genes contain introns associated with repressive heterochromatin, which are involved in various biological processes
Summary
Genomes of eukaryotes contain substantial numbers of transposable elements (TEs), which shape genomic structures and epigenomic landscapes [1, 2]. In plants with larger genomes, TEs are distributed across the gene-rich chromosome arm regions, and often affect transcription of surrounding genes [2, 5,6,7,8]. Histone modifications, including histone H3 Lys methylation (H3K9me), are tightly linked to non-CG methylation, and are associated with repressive chromatin states [16] Chromatin with these modifications results in the formation of a condensed repressive chromatin structure called heterochromatin [16,17,18], commonly associated with most TE sequences. The chromatin remodeler Decrease in DNA Methylation 1 (DDM1) is required for the maintenance of heterochromatin [19,20,21]
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