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. plant development | photomorphogenesis | light signaling | nuclear organization | heterochromatin C hromatin allows dense packaging of chromosomal DNA into a small and constrained nuclear space. It also serves as a structural framework for regulatory processes that control the functional status of genome domains with variable sizes, notably by dynamically influencing the subnuclear partitioning of generich and repeat-rich domains within euchromatic and heterochromatic regions, respectively (reviewed in refs. 1-3). These chromatin-based processes impact plasticity in the regulation of nuclear programs during both vegetative and reproductive phases of the plant life cycle (recently reviewed in refs. 4-8). In many cases, such events combine local chromatin variations with prominent changes in nuclear architecture and higher-order chromatin organization.Spatial chromatin organization is well exemplified by the extreme cases of transcriptionally silent chromocenters that contain the majority of ribosomal DNA repeats, such as the (peri)centromeric domains of mice and several plant species that include transposable elements (TE) and non-TE repeated sequences (9,

The LINC complex contributes to heterochromatin organisation and transcriptional gene silencing in plants

“…Previous studies have highlighted that chromatin organisation is different in distinct genetic backgrounds (Tessadori et al, 2009) and cellular contexts (Tessadori et al, 2007a), and that it depends on environmental conditions such as light (Bourbousse et al, 2015;Tessadori et al, 2007b) or growth medium (Vaillant et al, 2008). For these reasons, standardised experimental procedures were applied to reduce phenotypic variability within and across repetitions of a given genotype, and mutant datasets were normalised with WT plants grown within the same experiments (see Materials and Methods).…”

Dynamic Changes in Plant Nuclear Organization in Response to Environmental and Developmental Signals

“…Recently, Bourbousse et al (2015) investigated the relationship between developmental stages and light responsiveness. During germination, nuclear size and chromatin organization are independent of light conditions.…”

SHORT HYPOCOTYL 1 Encodes a SMARCA3-like Chromatin Remodeling Factor Regulating Elongation

“…In plants, accumulating evidence suggests that lightmediated gene expression and responses also require chromatin reorganization Bertrand et al, 2005;Benhamed et al, 2006;Fisher and Franklin, 2011;Han et al, 2015;Bourbousse et al, 2015). For example, in Arabidopsis, the transcription factor PICKLE encodes an ATP-dependent Chromodomain Helicase-DNA Binding3 (CHD3)-type chromatin remodeling factor of the SWI/SNF family (Ogas et al, 1999;Kwon and Wagner, 2007).…”

“…Chromatin remodelers have been shown to play important roles in plant light signaling (reviewed Barneche et al, 2014;Han et al, 2015;Bourbousse et al, 2015). For example, the CHD3 subfamily chromatin remodeling factor PICKLE represses photomorphogenesis (Jing et al, 2013).…”