Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

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. Author summary Intronic regions of eukaryotic genomes accumulate many Transposable Elements (TEs) and repeats. These intronic repeats are often targeted by epigenetic silencing mechanisms and form a repressive heterochromatin structure, even within transcriptionally active genes. However, the distribution of TEs in the intragenic regions, and their contributions to genetic diversity and evolution in plant genomes, 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 introns associated with repressive heterochromatin. Genes with heterochromatic introns implicated in various biological functions. The conserved protein OsIBM2 is required for proper transcription of a group of heterochromatin-containing genes. We also found that heterochromatic introns evolve rapidly compared to non-heterochromatic introns. Our study indicates that heterochromatin is a common feature in transcribed genes in the rice genome.