Dynamic regulation of chromatin topology and transcription by inverted repeat-derived small RNAs in sunflower

Transposable elements (TEs) are extremely abundant in complex plant genomes. siRNAs of 24 nucleotides in length control transposon activity in a process that involves de novo methylation of targeted loci. Usually, these epigenetic modifications trigger nucleosome condensation and a permanent silencing of the affected loci. Here, we show that a TE-derived inverted repeat (IR) element, inserted near the sunflower HaWRKY6 locus, dynamically regulates the expression of the gene by altering chromatin topology. The transcripts of this IR element are processed into 24-nt siRNAs, triggering DNA methylation on its locus. These epigenetic marks stabilize the formation of tissue-specific loops in the chromatin. In leaves, an intragenic loop is formed, blocking HaWRKY6 transcription. While in cotyledons (Cots), formation of an alternative loop, encompassing the whole HaWRKY6 gene, enhances transcription of the gene. The formation of this loop changes the promoter directionality, reducing IR transcription, and ultimately releasing the loop. Our results provide evidence that TEs can act as active and dynamic regulatory elements within coding loci in a mechanism that combines RNA silencing, epigenetic modification, and chromatin remodeling machineries.