R-Loop Mediated trans Action of the APOLO Long Noncoding RNA

Federico Ariel; Leandro Lucero; Aurelie Christ; Maria Florencia Mammarella; Teddy Jegu; Alaguraj Veluchamy; Kiruthiga Mariappan; David Latrasse; Thomas Blein; Chang Liu; Moussa Benhamed; Martin Crespi

doi:10.1016/j.molcel.2019.12.015

R-Loop Mediated trans Action of the APOLO Long Noncoding RNA

Mol Cell. 2020 Mar 5;77(5):1055-1065.e4. doi: 10.1016/j.molcel.2019.12.015. Epub 2020 Jan 14.

Affiliations

¹ Institute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRA, Universities Paris-Sud, Evry and Paris-Diderot, Sorbonne Paris-Cite, University of Paris-Saclay, Batiment 630, 91405 Orsay, France; Instituto de Agrobiotecnología del Litoral, CONICET, FBCB, Universidad Nacional del Litoral, Colectora Ruta Nacional 168 km 0, 3000 Santa Fe, Argentina. Electronic address: fariel@santafe-conicet.gov.ar.
² Instituto de Agrobiotecnología del Litoral, CONICET, FBCB, Universidad Nacional del Litoral, Colectora Ruta Nacional 168 km 0, 3000 Santa Fe, Argentina.
³ Institute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRA, Universities Paris-Sud, Evry and Paris-Diderot, Sorbonne Paris-Cite, University of Paris-Saclay, Batiment 630, 91405 Orsay, France.
⁴ Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia.
⁵ Department of General Genetics, Center for Plant Molecular Biology (ZMBP), University of Tübingen, Auf der Morgenstelle 32, 72076 Tübingen, Germany.
⁶ Institute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRA, Universities Paris-Sud, Evry and Paris-Diderot, Sorbonne Paris-Cite, University of Paris-Saclay, Batiment 630, 91405 Orsay, France. Electronic address: martin.crespi@ips2.universite-paris-saclay.fr.

PMID: 31952990
DOI: 10.1016/j.molcel.2019.12.015

Abstract

In eukaryotes, three-dimensional genome organization is critical for transcriptional regulation of gene expression. Long noncoding RNAs (lncRNAs) can modulate chromatin conformation of spatially related genomic locations within the nucleus. Here, we show that the lncRNA APOLO (AUXIN-REGULATED PROMOTER LOOP) recognizes multiple distant independent loci in the Arabidopsis thaliana genome. We found that APOLO targets are not spatially associated in the nucleus and that APOLO recognizes its targets by short sequence complementarity and the formation of DNA-RNA duplexes (R-loops). The invasion of APOLO to the target DNA decoys the plant Polycomb Repressive Complex 1 component LHP1, modulating local chromatin 3D conformation. APOLO lncRNA coordinates the expression of distal unrelated auxin-responsive genes during lateral root development in Arabidopsis. Hence, R-loop formation and chromatin protein decoy mediate trans action of lncRNAs on distant loci. VIDEO ABSTRACT.

Keywords: DNA:RNA duplex; LHP1; R-loops; auxin; epigenetics; genome topology; lateral root; long noncoding RNAs; polycomb; trans-acting lncRNAs; transcription.

Publication types

Research Support, Non-U.S. Gov't
Video-Audio Media

MeSH terms

Arabidopsis / drug effects
Arabidopsis / genetics
Arabidopsis / metabolism*
Arabidopsis Proteins / genetics
Arabidopsis Proteins / metabolism
Chromatin / genetics
Chromatin / metabolism*
Chromatin Assembly and Disassembly* / drug effects
Gene Expression Regulation, Plant* / drug effects
Indoleacetic Acids / pharmacology
Models, Genetic
Plants, Genetically Modified / drug effects
Plants, Genetically Modified / genetics
Plants, Genetically Modified / metabolism*
R-Loop Structures
RNA Polymerase II / genetics
RNA Polymerase II / metabolism
RNA, Long Noncoding / genetics
RNA, Long Noncoding / metabolism*
RNA, Plant / genetics
RNA, Plant / metabolism*
Structure-Activity Relationship
Transcription Factors / genetics
Transcription Factors / metabolism

Substances

Arabidopsis Proteins
Chromatin
Indoleacetic Acids
LHP1 protein, Arabidopsis
RNA, Long Noncoding
RNA, Plant
Transcription Factors
RNA Polymerase II