Non-coding transcription by alternative RNA polymerases regulates chromatin loop dynamics

ARIEL, FD; LATRASSE, D; ROMERO-BARRIOS, N; CHRIST, A; JEGU, T; BENHAMED, M; CRESPI, M

Santa Fe

Simposio; Long non-coding RNAs: marching towards mechanism; 2014

Keystone Symposia

The eukaryotic epigenome is shaped by the genome topology in three-dimensional space. Dynamic reversible variations in the epigenome structure direct the transcriptional responses to developmental cues. However, little is known about the control of epigenome dynamics. Here, we show that the Arabidopsis thaliana long intergenic non-coding RNA (lincRNA) APOLO is transcribed by RNA polymerase II (Pol II) and V (Pol V) complexes in response to auxin, a phytohormone controlling numerous facets of plant development. APOLO transcription facilitates the formation of an oscillating chromatin loop encompassing the promoter of its neighboring gene PID (or PINOID), a key regulator of auxin polar transport. Chromatin and RNA Immuno-precipitation (ChIP and RIP), together with Chromatin Isolation by RNA Purification (ChIRP) and Chromatin Conformation Capture (3C) served to decipher the ncRNA-mediated mechanisms controlling the chromatin loop opening and closing in response to auxin, modulating PID promoter activity. Components of the plant Polycomb Repressive Complexes as well as the transcriptional gene silencing and DNA demethylation machineries contribute to fine-tune chromatin loop dynamics. Altering APOLO expression or its 24nt siRNA-dependent DNA methylation affects loop formation and, consequently, PID expression. Hence, the active transcription of a lincRNA by alternative RNA polymerase complexes influences local chromatin topology and the expression of a neighboring locus, leading to far-reaching consequences on a variety of developmental outputs.