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.

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

Biological, Environmental Sciences and Engineering

Research output: Contribution to journal › Article › peer-review

173 Scopus citations

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.

Original language	English (US)
Pages (from-to)	1055-1065.e4
Number of pages	10648946
Journal	Molecular cell
Volume	77
Issue number	5
DOIs	https://doi.org/10.1016/j.molcel.2019.12.015
State	Published - Jan 14 2020

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We want to thank Dr. Tom Beeckman for the seeds of ProARF7:ARF7-GR transformed plants. This work was supported by grants from ANPCyT (PICT 2016-0289 and 2016-0007, Agencia Nacional de Promocio´ n Cientı´fica y Tecnolo´ gica, Argentina); CNRS (Laboratoire International Associe´ NOCOSYM); the Laboratoire d’Excellence (LABEX) Saclay Plant Sciences (SPS; ANR-10-LABX-40); and ANR grants (ANR 15-CE20-0002-01 and ANR 16-CE20-0003-04 SPLISIL), as well as the EPIMMUNITY International project between IPS2, France, and KAUST University, Saudi Arabia.

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10.1016/j.molcel.2019.12.015

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@article{11f2e0c240254a30b92370fd30901ae5,

title = "R-Loop Mediated trans Action of the APOLO Long Noncoding RNA.",

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.",

author = "Federico Ariel and Leandro Lucero and Aurelie Christ and Mammarella, {Maria Florencia} and Teddy Jegu and Alaguraj Veluchamy and Kiruthiga Mariappan and David Latrasse and Thomas Blein and Chang Liu and Moussa Benhamed and Martin Crespi",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We want to thank Dr. Tom Beeckman for the seeds of ProARF7:ARF7-GR transformed plants. This work was supported by grants from ANPCyT (PICT 2016-0289 and 2016-0007, Agencia Nacional de Promocio´ n Cientı´fica y Tecnolo´ gica, Argentina); CNRS (Laboratoire International Associe´ NOCOSYM); the Laboratoire d{\textquoteright}Excellence (LABEX) Saclay Plant Sciences (SPS; ANR-10-LABX-40); and ANR grants (ANR 15-CE20-0002-01 and ANR 16-CE20-0003-04 SPLISIL), as well as the EPIMMUNITY International project between IPS2, France, and KAUST University, Saudi Arabia.",

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doi = "10.1016/j.molcel.2019.12.015",

language = "English (US)",

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T1 - R-Loop Mediated trans Action of the APOLO Long Noncoding RNA.

AU - Ariel, Federico

AU - Lucero, Leandro

AU - Christ, Aurelie

AU - Mammarella, Maria Florencia

AU - Jegu, Teddy

AU - Veluchamy, Alaguraj

AU - Mariappan, Kiruthiga

AU - Latrasse, David

AU - Blein, Thomas

AU - Liu, Chang

AU - Benhamed, Moussa

AU - Crespi, Martin

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We want to thank Dr. Tom Beeckman for the seeds of ProARF7:ARF7-GR transformed plants. This work was supported by grants from ANPCyT (PICT 2016-0289 and 2016-0007, Agencia Nacional de Promocio´ n Cientı´fica y Tecnolo´ gica, Argentina); CNRS (Laboratoire International Associe´ NOCOSYM); the Laboratoire d’Excellence (LABEX) Saclay Plant Sciences (SPS; ANR-10-LABX-40); and ANR grants (ANR 15-CE20-0002-01 and ANR 16-CE20-0003-04 SPLISIL), as well as the EPIMMUNITY International project between IPS2, France, and KAUST University, Saudi Arabia.

PY - 2020/1/14

Y1 - 2020/1/14

N2 - 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.

AB - 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.

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UR - https://linkinghub.elsevier.com/retrieve/pii/S1097276519309281

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U2 - 10.1016/j.molcel.2019.12.015

DO - 10.1016/j.molcel.2019.12.015

M3 - Article

C2 - 31952990

SN - 1097-2765

VL - 77

SP - 1055-1065.e4

JO - Molecular cell

JF - Molecular cell

IS - 5

ER -

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

Abstract

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