Impact of Transposable Elements on Methylation and Gene Expression across Natural Accessions of Brachypodium distachyon

Abstract

Transposable elements (TEs) constitute a large fraction of plant genomes and are mostly present in a transcriptionally silent state through repressive epigenetic modifications, such as DNA methylation. TE silencing is believed to influence the regulation of adjacent genes, possibly as DNA methylation spreads away from the TE. Whether this is a general principle or a context-dependent phenomenon is still under debate, pressing for studying the relationship between TEs, DNA methylation, and nearby gene expression in additional plant species. Here, we used the grass Brachypodium distachyon as a model and produced DNA methylation and transcriptome profiles for 11 natural accessions. In contrast to what is observed in Arabidopsis thaliana, we found that TEs have a limited impact on methylation spreading and that only few TE families are associated with a low expression of their adjacent genes. Interestingly, we found that a subset of TE insertion polymorphisms is associated with differential gene expression across accessions. Thus, although not having a global impact on gene expression, distinct TE insertions may contribute to specific gene expression patterns in B. distachyon.

Keywords: Brachypodium distachyon; DNA methylation; gene expression; transposable elements.

Fig. 1.

Genome organization and methylation distribution of Col-0 and Bd21. Circos plot displaying methylation levels as well as gene and TE density in 100-kb windows in (A) A. thaliana and (B) B. distachyon. Centromeric and pericentromeric regions are highlighted in gray. Panels (C) and (D) display CpG methylation levels (expressed as % of methylated cytosines) for the most common TE superfamilies and for genes in A. thaliana and B. distachyon, respectively.

Fig. 2.

Methylation spreading around transposable elements. Heatmaps representing methylation (CpG) spreading around TEs located in the pericentromere/centromere regions or on the arm of the chromosomes for A. thaliana (N = 18,521 classified TEs) and B. distachyon (N = 62,708 classified TEs). Scales were adapted for the six panels to account for the lower genome-wide methylation level in A. thaliana and the different methylation levels for the three contexts.

Fig. 3.

Impact of transposable elements on gene expression. (A) Average gene expression as a function of the distance to the nearest TE belonging to the four LTR retrotransposons, RLG_BdisC039, RLG_BdisC004, RLG_BdisC180, and RLC_BdisC022, in the natural accessions of B. distachyon. Each colored line represents a different accession. The dashed line represents the genome-wide level of expression. Boxplots display the expression of genes harboring a TE in their vicinity for two distance classes only, all accessions pooled together. Stars indicate Wilcoxon test levels of significance: ***<0.001. (B) Heatmap representing methylation (CpG) spreading around the ten most active LTR retrotransposon families in Bd21. Families were clustered based on the level of methylation spreading (long, intermediate, and short) around each insertion. Names on the right of the heatmap describe the TE lineage to which each family belongs. Boxplots display the age of each family estimated by Stritt et al. (2020).