Physical clustering of <i>FLC</i> alleles during Polycomb-mediated epigenetic silencing in vernalization

Rosa, Stefanie; Lucia, Filomena De; Mylne, Joshua S.; Zhu, Danling; Ohmido, Nobuko; Pendle, Ali; Kato, Naohiro; Shaw, Peter; Dean, Caroline

doi:10.1101/gad.221713.113

Cited by 79 publications

(85 citation statements)

References 36 publications

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“…The observations that both heterochromatin domains (present study) and individual euchromatin loci, such as light-responsive genes (64), are subject to spatial rearrangements during photomorphogenesis indicate that genome topology is significantly modified during this transition. These findings add to the recent report that spatial clustering of FLC alleles contribute to their epigenetic repression during vernalization, a process that relies on Polycomb-based chromatin modifications (66).…”

Section: Discussion Nuclear Rearrangements and Increased Transcriptiosupporting

confidence: 54%

“…Although we cannot exclude that expression of the LTR AtGP1 transgene could also be controlled by trans-acting factors superimposing RdDM-based repression, two-layered silencing has nonetheless been identified using mutant plants for the Morpheus' molecule1 (MOM1) putative helicase (70,71) and for the MORC ATPase (72), which are both believed to be involved in DNA or chromosomal remodeling processes. Based on these findings, it is possible that some heterochromatin loci might be sensitive to a position-dependent or condensation-dependent regulatory control during cotyledon development, a process that may relate to the observed relationship between chromatin-based repression and subnuclear positioning of multicopy transgenes (73) and of the FLC gene (66,74). Future studies aimed at dissecting nuclear architectural changes during photomorphogenesis should allow an assessment of the functional impact of heterochromatin organization and genome topology structuration on the reprogramming of gene expression.…”

Section: Discussion Nuclear Rearrangements and Increased Transcriptiomentioning

confidence: 99%

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Light signaling controls nuclear architecture reorganization during seedling establishment

Bourbousse

Mestiri

Zabulon

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

108

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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,

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Section: Discussion Nuclear Rearrangements and Increased Transcriptiosupporting

confidence: 54%

Section: Discussion Nuclear Rearrangements and Increased Transcriptiomentioning

confidence: 99%

Light signaling controls nuclear architecture reorganization during seedling establishment

Bourbousse

Mestiri

Zabulon

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

108

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“…Conformational changes of higher order chromatin structure are also reported for Polycomb-mediated silenced loci in Drosophila and mammals, known as polycomb bodies within nucleus (Lanzuolo et al, 2007;Bantignies and Cavalli, 2011;Nora et al, 2012). Similarly in plants, it has been observed that FLC chromatin is repositioned in nucleus by vernalization (Rosa et al, 2013). Therefore, Polycomb-mediated silencing of FLC by vernalization may also involve physical repositioning of chromatin.…”

Section: Polycomb-mediated Flc Repression By Vernalizationmentioning

confidence: 89%

Genetic and Epigenetic Mechanisms Underlying Vernalization

Kim

Sung

2014

The Arabidopsis Book

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Plants have evolved a number of monitoring systems to sense their surroundings and to coordinate their growth and development accordingly. Vernalization is one example, in which flowering is promoted after plants have been exposed to a long-term cold temperature (i.e. winter). Vernalization results in the repression of floral repressor genes that inhibit the floral transition in many plant species. Here, we describe recent advances in our understanding of the vernalization-mediated promotion of flowering in Arabidopsis and other flowering plants. In Arabidopsis, the vernalization response includes the recruitment of chromatin-modifying complexes to floral repressors and thus results in the enrichment of repressive histone marks that ensure the stable repression of floral repressor genes. Changes in histone modifications at floral repressor loci are stably maintained after cold exposure, establishing the competence to flower the following spring. We also discuss similarities and differences in regulatory circuits in vernalization responses among Arabidopsis and other plants.

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“…For example, the chromatin dynamics in plants in response to environmental stresses or stimuli has been revealed by the chromatin tagging system (Matsunaga et al 2013). In the flowering of A. thaliana, the system revealed that the FLC gene loci were clustered during vernalization (Rosa et al 2013, Zhu et al 2015. In response to genotoxic stresses in the nuclei of A. thaliana, the arrangement of homologous loci could be detected by the chromatin tagging system (Hirakawa et al 2015).…”

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confidence: 99%

Chromatin Tagging Systems Contribute to Live Imaging Analyses for Chromatin Dynamics

Hirakawa

Matsunaga

2016

CYTOLOGIA

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Summary Chromatin tagging systems are based on bacterial operator/repressor systems combined with fluorescence proteins. They can visualize spatiotemporally the specific loci where the tandem array of an operator sequence is inserted and three-dimensionally analyze chromatin dynamics in a nucleus of living cells. This method in combination with RNA imaging or an induction system of DNA breaks make it possible to analyze chromatin dynamics at RNA transcription and DNA repair. Chromatin tagging systems are also applied to dynamic analyses of organelle genomes. In this review, we introduce their fundamental principles and recent applications.

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Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization

Cited by 79 publications

References 36 publications

Light signaling controls nuclear architecture reorganization during seedling establishment

Light signaling controls nuclear architecture reorganization during seedling establishment

Genetic and Epigenetic Mechanisms Underlying Vernalization

Chromatin Tagging Systems Contribute to Live Imaging Analyses for Chromatin Dynamics

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