The EFR-XI-k duet: Dynamic adaptation of plants to pathogen attack through transposable element-induced chromatin topology changes

MENCIA, REGINA

Congreso; The EFR-XI-k duet: Dynamic adaptation of plants to pathogen attack through transposable element-induced chromatin topology changes; 2023

Plant genomes contain a high proportion of transposable elements (TEs), reaching up to 90% in some species of grasses. The model plant Arabidopsis thaliana has 20% of its genome composed of TEs and other repetitive elements. To control TE movement, plants use the RNA-dependent DNA methylation (RdDM) pathway to transcriptionally silence them. As a side effect, TE silencing can also impact the transcription of neighboring genes. Recently, we discover that the proximity of transposable element-derived inverted repeats (IRs) to coding genes significantly impacts both gene expression and chromatin topology. Several IRs in the Arabidopsis genome were identified to potentially carry regulatory functions based on their position and ability to produce 24nt small RNAs in a PolII-dependent manner, which can induce DNA methylation. Notably, one IR located between the EFR and XI-k genes, occupying almost the entire intergenic region drew our attention due to its unique position separating two pathogen response-related genes. When transcribing the XI-k gene, RNA Polymerase II (PolII) continues generating a long transcript that includes the IR, which can be processed by the small RNA synthesis machinery, resulting in 21-24 nucleotide siRNAs that activate DNA methylation at their loci. This DNA methylation induces a conformational change in the chromatin, creating a short-range DNA loop containing the coding region of EFR. EFR is a pattern recognition receptor associated with pathogens (PAMPs) that can activate pathogen-triggered immunity (PTI) responses, thus acting in the first line of immune responses. We found that the identified IR can dynamically affect EFR expression; furthermore, this element is not conserved in different natural varieties of Arabidopsis. This variation in the presence of the IR correlates with differences in genome topology, EFR expression, and plant response to the Pseudomonas syringae pathogen attack. Our results represent a unique case of potential adaptive evolution to pathogens caused by TE movement and the consequent alteration of the three-dimensional organization of chromatin in a dynamic process involving two adjacent genes in the genome.