Noncoding transcription shapes genome topology

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

Paris

Conferencia; Post-transcriptional Gene Regulation in Plants; 2015

PGRP Organizing Committee

Noncoding RNAs have emerged as major components of the eukaryotic transcriptome. Genome-wide analyses revealed the existence of thousands of long noncoding RNAs (lncRNAs) in several plant species. Plant lncRNAs are transcribed by the plant-specific RNA polymerases Pol IV and Pol V, leading to transcriptional gene silencing, as well as by Pol II. They are involved in a wide range of regulatory mechanisms impacting on gene expression, including chromatin remodeling, modulation of alternative splicing, fine-tuning of miRNA activity, and the control of mRNA translation or accumulation. Recently, dual noncoding transcription by alternative RNA polymerases was implicated in epigenetic and chromatin conformation dynamics. Reversible variations in the epigenome shape the genome topology in three-dimensional space structure, directly influencing the transcriptional responses to developmental cues. We have shown 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. Genome-wide identification of APOLO?interacting loci may reveal an intricate mechanism shaping genome topology driven by noncoding transcription, thus allowing the coordination of gene expression.