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

Abstract

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.

Long non-coding RNAs in plants: emerging modulators of gene activity in development and stress responses

“…DNA methylation changes chromatin structure of the HaWRKY6 locus and promotes the formation of a loop encompassing the whole locus to enhance transcription of HaWRKY6 . The level of DNA methylation, and consequently, the formation of the loop and the expression level of HaWRKY6 are regulated in a tissue-specific manner (Gagliardi et al 2019 ) . Another lncRNA, PMS1T , identified by map-based cloning in rice, contributes to photoperiod-sensitive male sterility by producing phase-siRNAs in a miR2118-dependent manner (Fan et al 2016 ) (Fig.…”

RdDM pathway is required forTobamovirus-induced symptomatology production

“…They evidenced a non-canonical mechanism of regulation in which the enrichment of DNA methylation in flanking regions of WRKY6 is associated with the formation of chromatin loops that ends up altering transcription rates. Although a reduction of methylation in these regions together with stable methylation in one intron correlates with the formation of an intragenic loop that inhibites the transcription of the gene (Gagliardi et al, 2019).…”

Short‐range regulatory chromatin loops in plants

“…1a). Recently, we have identified a case of gene looping in the sunflower HaWRKY6 locus that regulates tissue‐specifically the expression of the gene (Gagliardi et al , 2019). In cotyledons, a chromatin loop comprising the entire locus, from promoter to TTS, allows efficient recycling of RNAPII, increasing HaWRKY6 levels (Gagliardi et al , 2019).…”

“…Recently, we have identified a case of gene looping in the sunflower HaWRKY6 locus that regulates tissue‐specifically the expression of the gene (Gagliardi et al , 2019). In cotyledons, a chromatin loop comprising the entire locus, from promoter to TTS, allows efficient recycling of RNAPII, increasing HaWRKY6 levels (Gagliardi et al , 2019). In Flowering Locus C ( FLC ), a loop between the gene promoter and TTS is disrupted after 2 wk of cold incubation, leading to a drop in FLC expression and flowering transition (Crevillen et al , 2013).…”