Noncoding Transcription by Alternative RNA Polymerases Dynamically Regulates an Auxin-Driven Chromatin Loop

The eukaryotic epigenome is shaped by the genome topology in three-dimensional space. Dynamic reversible variations in this epigenome structure directly influence the transcriptional responses to developmental cues. Here, we show that the Arabidopsis long intergenic noncoding RNA (lincRNA) APOLO is transcribed by RNA polymerases II and V in response to auxin, a phytohormone controlling numerous facets of plant development. This dual APOLO transcription regulates the formation of a chromatin loop encompassing the promoter of its neighboring gene PID, a key regulator of polar auxin transport. Altering APOLO expression affects chromatin loop formation, whereas RNA-dependent DNA methylation, active DNA demethylation, and Polycomb complexes control loop dynamics. This dynamic chromatin topology determines PID expression patterns. Hence, the dual transcription of a lincRNA influences local chromatin topology and directs dynamic auxin-controlled developmental outputs on neighboring genes. This mechanism likely underscores the adaptive success of plants in diverse environments and may be widespread in eukaryotes. [Display omitted] •Dual noncoding transcription shapes genome topology dynamics•Dynamic chromatin looping molds auxin-driven outputs•LincRNA-dependent oscillating chromatin conformation fine-tunes promoter activity Dynamic changes in genome topology regulate gene expression. Ariel et al. show that the dual transcription of a long intergenic noncoding RNA, APOLO, by polymerases II and V dynamically regulates chromatin conformation and the local epigenetic landscape. This mechanism directs promoter activity of PID and modulates polar auxin transport.