title: Light signaling controls nuclear architecture reorganization during seedling establishment.
abstract: The spatial organization of chromatin can be subject to extensive remodeling in plant somatic cells in response to developmental and environmental signals. However, the mechanisms controlling these dynamic changes and their functional impact on nuclear activity are poorly understood. Here, we determined that light perception triggers a switch between two different nuclear architectural schemes during Arabidopsis postembryonic development. Whereas progressive nucleus expansion and heterochromatin rearrangements in cotyledon cells are achieved similarly under light and dark conditions during germination, the later steps that lead to mature nuclear phenotypes are intimately associated with the photomorphogenic transition in an organ-specific manner. The light signaling integrators DE-ETIOLATED 1 and CONSTITUTIVE PHOTOMORPHOGENIC 1 maintain heterochromatin in a decondensed state in etiolated cotyledons. In contrast, under light conditions cryptochrome-mediated photoperception releases nuclear expansion and heterochromatin compaction within conspicuous chromocenters. For all tested loci, chromatin condensation during photomorphogenesis does not detectably rely on DNA methylation-based processes. Notwithstanding, the efficiency of transcriptional gene silencing may be impacted during the transition, as based on the reactivation of transposable element-driven reporter genes. Finally, we report that global engagement of RNA polymerase II in transcription is highly increased under light conditions, suggesting that cotyledon photomorphogenesis involves a transition from globally quiescent to more active transcriptional states. Given these findings, we propose that light-triggered changes in nuclear architecture underlie interplays between heterochromatin reorganization and transcriptional reprogramming associated with the establishment of photosynthesis.
authors.affiliation: Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, 75005 Paris, France; IBENS, INSERM, U1024, 75005 Paris, France; UMR 8197, CNRS, 75005 Paris, France;
authors.forename: Clara
authors.initials: C
authors.lastname: Bourbousse
authors.affiliation: Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, 75005 Paris, France; IBENS, INSERM, U1024, 75005 Paris, France; UMR 8197, CNRS, 75005 Paris, France;
authors.forename: Imen
authors.initials: I
authors.lastname: Mestiri
authors.affiliation: Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, 75005 Paris, France; IBENS, INSERM, U1024, 75005 Paris, France; UMR 8197, CNRS, 75005 Paris, France;
authors.forename: Gerald
authors.initials: G
authors.lastname: Zabulon
authors.affiliation: Pôle de Biologie Cellulaire, Imagif, Centre de Recherche de Gif (FRC3115), CNRS, F-91198 Gif-sur-Yvette, France;
authors.forename: Mickaël
authors.initials: M
authors.lastname: Bourge
authors.affiliation: Italian Institute of Technology, CRIB-Center For Advanced Biomaterials For Health Care, 80125 Naples, Italy;
authors.forename: Fabio
authors.initials: F
authors.lastname: Formiggini
authors.affiliation: Nuclear Organization Group, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The Netherlands; and.
authors.forename: Maria A
authors.initials: MA
authors.lastname: Koini
authors.affiliation: Dynamique de la Compartimentation Cellulaire, Institut des Sciences du Végétal, CNRS UPR 2355, Saclay Plant Sciences, F-91198 Gif-sur-Yvette, France.
authors.forename: Spencer C
authors.initials: SC
authors.lastname: Brown
authors.affiliation: Nuclear Organization Group, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The Netherlands; and.
authors.forename: Paul
authors.initials: P
authors.lastname: Fransz
authors.affiliation: Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, 75005 Paris, France; IBENS, INSERM, U1024, 75005 Paris, France; UMR 8197, CNRS, 75005 Paris, France;
authors.forename: Chris
authors.initials: C
authors.lastname: Bowler
authors.affiliation: Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, 75005 Paris, France; IBENS, INSERM, U1024, 75005 Paris, France; UMR 8197, CNRS, 75005 Paris, France; barneche@ens.fr.
authors.forename: Fredy
authors.initials: F
authors.lastname: Barneche
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development* / Q000528:radiation effects*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D002467:Cell Nucleus / Q000235:genetics / Q000378:metabolism / Q000528:radiation effects; D042002:Chromatin Assembly and Disassembly / Q000235:genetics / Q000528:radiation effects; D018548:Cotyledon / Q000254:growth & development / Q000378:metabolism / Q000528:radiation effects; D019175:DNA Methylation; D020868:Gene Silencing; D017343:Genes, Plant; D006570:Heterochromatin / Q000235:genetics / Q000528:radiation effects; D047908:Intracellular Signaling Peptides and Proteins; D055537:Light Signal Transduction / Q000235:genetics; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D012319:RNA Polymerase II / Q000378:metabolism; D036226:Seedlings / Q000254:growth & development / Q000378:metabolism / Q000528:radiation effects; D044767:Ubiquitin-Protein Ligases / Q000235:genetics / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; C088435:DET1 protein, Arabidopsis; D006570:Heterochromatin; D047908:Intracellular Signaling Peptides and Proteins; D009687:Nuclear Proteins; C471983:AT2G32950 protein, Arabidopsis; D044767:Ubiquitin-Protein Ligases; D012319:RNA Polymerase II
keywords: heterochromatin; light signaling; nuclear organization; photomorphogenesis; plant development