Causes and consequences of nuclear gene positioning

Shachar, Sigal; Misteli, Tom

doi:10.1242/jcs.199786

Cited by 54 publications

(54 citation statements)

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“…In animal cells, spatial gene re-positioning upon transcriptionrelative to nuclear bodies and CTsand the clustering of gene loci into transcription factories are considered key organisational principles [21]. In plants, the situation is unclear.…”

Section: Breaking the Dogma Of A Unique Nuclear Organisation Modelspementioning

confidence: 99%

“…In plants, the situation is unclear. While gene relocation has been described for a subset of loci in Arabidopsis, there is currently no evidence that this represents a paradigm in plant cells, nor that transcription factories really occur [10,[21][22][23][24][25]. It could, however, be that the establishment of unambiguous models is hampered by the heterogeneity of nuclear organization in plant tissues (unlike animals, plants cannot be cultured in homogenous cell lineages) and their plasticity in response to environmental stimuli.…”

Section: Breaking the Dogma Of A Unique Nuclear Organisation Modelspementioning

confidence: 99%

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Probing the 3D architecture of the plant nucleus with microscopy approaches: challenges and solutions

Dumur

Duncan

Graumann

et al. 2019

Nucleus

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The eukaryotic cell nucleus is a central organelle whose architecture determines genome function at multiple levels. Deciphering nuclear organizing principles influencing cellular responses and identity is a timely challenge. Despite many similarities between plant and animal nuclei, plant nuclei present intriguing specificities. Complementary to molecular and biochemical approaches, 3D microscopy is indispensable for resolving nuclear architecture. However, novel solutions are required for capturing cell-specific, sub-nuclear and dynamic processes. We provide a pointer for utilising high-to-super-resolution microscopy and image processing to probe plant nuclear architecture in 3D at the best possible spatial and temporal resolution and at quantitative and cell-specific levels. High-end imaging and image-processing solutions allow the community now to transcend conventional practices and benefit from continuously improving approaches. These promise to deliver a comprehensive, 3D view of plant nuclear architecture and to capture spatial dynamics of the nuclear compartment in relation to cellular states and responses. Abbreviations: 3D and 4D: Three and Four dimensional; AI: Artificial Intelligence; ant: antipodal nuclei (ant); CLSM: Confocal Laser Scanning Microscopy; CTs: Chromosome Territories; DL: Deep Learning; DLIm: Dynamic Live Imaging; ecn: egg nucleus; FACS: Fluorescence-Activated Cell Sorting; FISH: Fluorescent In Situ Hybridization; FP: Fluorescent Proteins (GFP, RFP, CFP, YFP, mCherry); FRAP: Fluorescence Recovery After Photobleaching; GPU: Graphics Processing Unit; KEEs: KNOT Engaged Elements; INTACT: Isolation of Nuclei TAgged in specific Cell Types; LADs: Lamin-Associated Domains; ML: Machine Learning; NA: Numerical Aperture; NADs: Nucleolar Associated Domains; PALM: Photo-Activated Localization Microscopy; Pixel: Picture element; pn: polar nuclei; PSF: Point Spread Function; RHF: Relative Heterochromatin Fraction; SIM: Structured Illumination Microscopy; SLIm: Static Live Imaging; SMC: Spore Mother Cell; SNR: Signal to Noise Ratio; SRM: Super-Resolution Microscopy; STED: STimulated Emission Depletion; STORM: STochastic Optical Reconstruction Microscopy; syn: synergid nuclei; TADs: Topologically Associating Domains; Voxel: Volumetric pixel

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Section: Breaking the Dogma Of A Unique Nuclear Organisation Modelspementioning

confidence: 99%

Section: Breaking the Dogma Of A Unique Nuclear Organisation Modelspementioning

confidence: 99%

Probing the 3D architecture of the plant nucleus with microscopy approaches: challenges and solutions

Dumur

Duncan

Graumann

et al. 2019

Nucleus

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“…Using our high-resolution contact maps, we are also able to examine the ways in which these two mechanisms interact. It is commonly thought that compartment intervals are typically megabases in length, and are subdivided into smaller domains in a hierarchical fashion (Dixon et al, 2016; Fraser et al, 2015; Gibcus and Dekker, 2013; Gorkin et al, 2014; Nora et al, 2013; Sexton and Cavalli, 2015; Shachar and Misteli, 2017). Here, we demonstrate that compartment intervals can be as short as tens of kilobases, and can overlap loop domains in complex ways.…”

Section: Discussionmentioning

confidence: 99%

Cohesin loss eliminates all loop domains, leading to links among superenhancers and downregulation of nearby genes

Rao

Huang

Hilaire

et al. 2017

Preprint

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SUMMARY:The human genome folds to create thousands of intervals, called "contact domains," that exhibit enhanced contact frequency within themselves. "Loop domains" form because of tethering between two loci -almost always bound by CTCF and cohesin -lying on the same chromosome. "Compartment domains" form when genomic intervals with similar histone marks co-segregate. Here, we explore the effects of degrading cohesin. All loop domains are eliminated, but neither compartment domains nor histone marks are affected. Loci in different compartments that had been in the same loop domain become more segregated. Loss of loop domains does not lead to widespread ectopic gene activation, but does affect a significant minority of active genes. In particular, cohesin loss causes superenhancers to co-localize, forming hundreds of links within and across chromosomes, and affecting the regulation of nearby genes. Cohesin restoration quickly reverses these effects, consistent with a model where loop extrusion is rapid. INTRODUCTION:Many studies have shown that the insulator protein CTCF and the ring-shaped cohesin complex colocalize on chromatin (Parelho et al., 2008; Rubio et al., 2008; Wendt et al., 2008) and lie at the anchors of loops (Heidari et al., 2014; Rao et al., 2014; Splinter et al., 2006; Tang et al., 2015) and the boundaries of contact domains (sometimes called "topologically constrained domains", "topologically . CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/139782 doi: bioRxiv preprint first posted online May. 18, 2017; 2 associated domains", or "physical domains") (Dixon et al., 2012; Lieberman-Aiden et al., 2009; Nora et al., 2012; Phillips-Cremins et al., 2013; Rao et al., 2014; Sexton et al., 2012). These findings suggest that these proteins play a role in regulating genome folding (Benabdallah and Bickmore, 2015; Dekker and Misteli, 2015; Lupiáñez et al., 2016; Merkenschlager and Nora, 2016; Phillips-Cremins and Corces, 2013; Uhlmann, 2016). Similarly, deletion of individual CTCF sites can interfere with loop and contact domain formation (Guo et al., 2015; Narendra et al., 2015;Sanborn et al., 2015; de Wit et al., 2015). However, low-resolution experiments examining genome-wide depletion of CTCF and cohesin have thus far observed only limited effects on chromosome architecture, reporting that compartments and contact domains still appear to be present (Seitan et al., 2013; Sofueva et al., 2013; Zuin et al., 2014). These results have made it difficult to ascertain the role of CTCF and cohesin in the regulation of genome topology at the chromosome scale.Here, we examine the effects of cohesin loss on nuclear architecture, epigenetic state, and transcription. By generating maps of DNA-DNA contacts of much higher resolution, we are able to characterize the effects of global cohesin loss on nuclear architecture more clearly than in earlier studies. We demonstrate that ...

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“…The CAB gene cluster rapidly moved from the nuclear interior region to the nuclear peripheral region in response to light (Feng et al 2014). This repositioning event in the nucleus occurred before the activation of transcription, suggesting that nuclear position of genes is closely related with gene activity (Shachar and Misteli 2017).…”

mentioning

confidence: 96%

FISH with Padlock Probes Can Efficiently Reveal the Genomic Position of Low or Single-Copy DNA Sequences

Matsunaga

2017

CYTOLOGIA

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A padlock probe is a circularized oligonucleotide containing complementary sequences of target regions. Padlock probes combined with rolling-circle amplification enable fluorescence in situ hybridization (FISH) to reproducibly detect the genomic position of low or single-copy DNA sequences. The FISH with padlock probes revealed that a plant gene cluster of tandemly arrayed three paralogues responsible for photosynthesis rapidly moved from the interior subnuclear region to the peripheral subnuclear region in response to light. Using a pair of peptide nucleic acids as a double-strand opener for the target region, the efficiency of FISH with padlock probes at the detection of a single-copy genomic region was much improved. FISH with padlock probes will give us reliable data of dynamics, arrangement and position of a specific single locus in both the nucleus and the condensed chromosomes.

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Causes and consequences of nuclear gene positioning

Cited by 54 publications

References 71 publications

Probing the 3D architecture of the plant nucleus with microscopy approaches: challenges and solutions

Probing the 3D architecture of the plant nucleus with microscopy approaches: challenges and solutions

Cohesin loss eliminates all loop domains, leading to links among superenhancers and downregulation of nearby genes

FISH with Padlock Probes Can Efficiently Reveal the Genomic Position of Low or Single-Copy DNA Sequences

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