Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

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.

Hypermethylation of Auxin-Responsive Motifs in the Promoters of the Transcription Factor Genes Accompanies the Somatic Embryogenesis Induction in Arabidopsis

“…The question of the functionality of intron methylation in LEC1 remains open. The methylation of introns is primarily postulated as controlling gene expression by maintaining the heterochromatin marks within the gene in order to silence the transposons [ 116 , 138 , 139 ] or as affecting the gene splicing [ 132 , 140 , 141 ]. However, the LEC1 gene is built of only one intron, which lacks transposon elements.…”

Epigenetics: a catalyst of plant immunity against pathogens

“…However, stress-induced epigenetic change can act as a catalyst to Darwinian evolution of the plant immune system (Figure 3). Apart from mediating TIR, which can offer relatively short-term benefits to progeny in parent-matched environments (Lopez et al, 2021), stress-induced epigenetic change can accelerate genetic change in immune-regulatory genes through mobilome-induced structural variants and 5-mC-induced point mutations, which are selected for by Darwinian evolution (Kawakatsu et al, 2016;Wilkinson et al, 2019, Ossowski et al, 2010Espinas et al, 2020).…”

The Role of DNA Methylation in Genome Defense in Cnidaria and Other Invertebrates

“…Methylation of transposons in invertebrates presumably leads to formation of localized heterochromatin-like structures in a manner analogous to those formed after CHG methylation of transposons in plants. The presence of heterochromatic regions within highly active genes may appear paradoxical, but has clear precedents in plants (see, for example, Espinas et al [2020] ) and is likely to apply more generally given the extensive methylation of transposons typical of vertebrate genomes. A role of this kind provides a simple rationalization for the high level of conservation of the CpG methylation apparatus (MBDs, SRA proteins, histone deacetylases, heterochromatin proteins, etc.)…”