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.
authors.affiliation: CNRS, Institut des Sciences du Végétal, Saclay Plant Sciences, 91198 Gif-sur-Yvette and Université Paris Diderot-Paris 7, 75013 Paris, France.
authors.forename: Federico
authors.initials: F
authors.lastname: Ariel
authors.affiliation: Institut de Biologie des Plantes, UMR8618 Université Paris-Sud XI, SPS Saclay Plant Sciences, 91405 Orsay, France.
authors.forename: Teddy
authors.initials: T
authors.lastname: Jegu
authors.affiliation: Institut de Biologie des Plantes, UMR8618 Université Paris-Sud XI, SPS Saclay Plant Sciences, 91405 Orsay, France.
authors.forename: David
authors.initials: D
authors.lastname: Latrasse
authors.affiliation: CNRS, Institut des Sciences du Végétal, Saclay Plant Sciences, 91198 Gif-sur-Yvette and Université Paris Diderot-Paris 7, 75013 Paris, France.
authors.forename: Natali
authors.initials: N
authors.lastname: Romero-Barrios
authors.affiliation: CNRS, Institut des Sciences du Végétal, Saclay Plant Sciences, 91198 Gif-sur-Yvette and Université Paris Diderot-Paris 7, 75013 Paris, France.
authors.forename: Aurélie
authors.initials: A
authors.lastname: Christ
authors.affiliation: Institut de Biologie des Plantes, UMR8618 Université Paris-Sud XI, SPS Saclay Plant Sciences, 91405 Orsay, France; Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia. Electronic address: moussa.benhamed@u-psud.fr.
authors.forename: Moussa
authors.initials: M
authors.lastname: Benhamed
authors.affiliation: CNRS, Institut des Sciences du Végétal, Saclay Plant Sciences, 91198 Gif-sur-Yvette and Université Paris Diderot-Paris 7, 75013 Paris, France. Electronic address: crespi@isv.cnrs-gif.fr.
authors.forename: Martin
authors.initials: M
authors.lastname: Crespi
mesh_terms: D017360:Arabidopsis / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D042002:Chromatin Assembly and Disassembly; D019175:DNA Methylation; D012321:DNA-Directed RNA Polymerases / Q000378:metabolism*; D044127:Epigenesis, Genetic; D018506:Gene Expression Regulation, Plant; D018745:Genome, Plant; D007210:Indoleacetic Acids / Q000494:pharmacology*; D009154:Mutation; D010937:Plant Growth Regulators / Q000494:pharmacology*; D063146:Polycomb-Group Proteins / Q000378:metabolism; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism; D012319:RNA Polymerase II / Q000378:metabolism*; D062085:RNA, Long Noncoding / Q000235:genetics*; D018749:RNA, Plant / Q000235:genetics*
chemical_list: D029681:Arabidopsis Proteins; D007210:Indoleacetic Acids; D010937:Plant Growth Regulators; D063146:Polycomb-Group Proteins; D062085:RNA, Long Noncoding; D018749:RNA, Plant; C405165:PINOID protein, Arabidopsis; D017346:Protein Serine-Threonine Kinases; D012319:RNA Polymerase II; C538841:RNA polymerase V, Arabidopsis; D012321:DNA-Directed RNA Polymerases