Noncoding transcription by alternative rna polymerases dynamically regulates an auxin-driven chromatin loop

Federico D. Ariel; Teddy Jégu; David Latrasse; Natali Romero-Barrios; Aurélie Christ; Moussa Benhamed; Martín D. Crespi

doi:10.1016/j.molcel.2014.06.011

Noncoding transcription by alternative rna polymerases dynamically regulates an auxin-driven chromatin loop

Federico D. Ariel, Teddy Jégu, David Latrasse, Natali Romero-Barrios, Aurélie Christ, Moussa Benhamed, Martín D. Crespi

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

311 Scopus citations

Abstract

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. © 2014 Elsevier Inc.

Original language	English (US)
Pages (from-to)	383-396
Number of pages	14
Journal	Molecular Cell
Volume	55
Issue number	3
DOIs	https://doi.org/10.1016/j.molcel.2014.06.011
State	Published - Aug 2014

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank Herve Vaucheret for rdd seeds, Francois Roudier for clf and swn seeds, and both of them for constructive discussions, as well as Allison Mallory for careful reading of the manuscript. We also thank Craig Pikaard for NRPE1-FLAG-transformed seeds and Koji Goto for LHP1-GFP-transformed seeds. F.A. is an EMBO postdoc fellow; N.R.-B. and T.J. are Paris-Sud University PhD fellows. This work was funded by LABEX Saclay Plant Sciences and the France-Brazilian COFECUB Exchange program.

ASJC Scopus subject areas

Cell Biology
Molecular Biology

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10.1016/j.molcel.2014.06.011

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title = "Noncoding transcription by alternative rna polymerases dynamically regulates an auxin-driven chromatin loop",

abstract = "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. {\textcopyright} 2014 Elsevier Inc.",

author = "Ariel, {Federico D.} and Teddy J{\'e}gu and David Latrasse and Natali Romero-Barrios and Aur{\'e}lie Christ and Moussa Benhamed and Crespi, {Mart{\'i}n D.}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Herve Vaucheret for rdd seeds, Francois Roudier for clf and swn seeds, and both of them for constructive discussions, as well as Allison Mallory for careful reading of the manuscript. We also thank Craig Pikaard for NRPE1-FLAG-transformed seeds and Koji Goto for LHP1-GFP-transformed seeds. F.A. is an EMBO postdoc fellow; N.R.-B. and T.J. are Paris-Sud University PhD fellows. This work was funded by LABEX Saclay Plant Sciences and the France-Brazilian COFECUB Exchange program.",

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AU - Benhamed, Moussa

AU - Crespi, Martín D.

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Herve Vaucheret for rdd seeds, Francois Roudier for clf and swn seeds, and both of them for constructive discussions, as well as Allison Mallory for careful reading of the manuscript. We also thank Craig Pikaard for NRPE1-FLAG-transformed seeds and Koji Goto for LHP1-GFP-transformed seeds. F.A. is an EMBO postdoc fellow; N.R.-B. and T.J. are Paris-Sud University PhD fellows. This work was funded by LABEX Saclay Plant Sciences and the France-Brazilian COFECUB Exchange program.

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N2 - 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. © 2014 Elsevier Inc.

AB - 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. © 2014 Elsevier Inc.

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Noncoding transcription by alternative rna polymerases dynamically regulates an auxin-driven chromatin loop

Abstract

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