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Proc Natl Acad Sci U S A. 2015 May 26;112(21):E2836-44. doi: 10.1073/pnas.1503512112. Epub 2015 May 11.

Light signaling controls nuclear architecture reorganization during seedling establishment.

Author information

1
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;
2
Pôle de Biologie Cellulaire, Imagif, Centre de Recherche de Gif (FRC3115), CNRS, F-91198 Gif-sur-Yvette, France;
3
Italian Institute of Technology, CRIB-Center For Advanced Biomaterials For Health Care, 80125 Naples, Italy;
4
Nuclear Organization Group, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The Netherlands; and.
5
Dynamique de la Compartimentation Cellulaire, Institut des Sciences du Végétal, CNRS UPR 2355, Saclay Plant Sciences, F-91198 Gif-sur-Yvette, France.
6
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.

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.

KEYWORDS:

heterochromatin; light signaling; nuclear organization; photomorphogenesis; plant development

PMID:
25964332
PMCID:
PMC4450433
DOI:
10.1073/pnas.1503512112
[Indexed for MEDLINE]
Free PMC Article

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