Linker histones are fine-scale chromatin architects modulating developmental decisions in  Arabidopsis

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Abstract

Background

Chromatin provides a tunable platform for gene expression control. Besides the well-studied core nucleosome, H1 linker histones are abundant chromatin components with intrinsic potential to influence chromatin function. Well studied in animals, little is known about the evolution of H1 function in other eukaryotic lineages for instance plants. Notably, in the model plant Arabidopsis, while H1 is known to influence heterochromatin and DNA methylation, its contribution to transcription, molecular, and cytological chromatin organization remains elusive.

Results

We provide a multi-scale functional study of Arabidopsis linker histones. We show that H1-deficient plants are viable yet show phenotypes in seed dormancy, flowering time, lateral root, and stomata formation—complemented by either or both of the major variants. H1 depletion also impairs pluripotent callus formation. Fine-scale chromatin analyses combined with transcriptome and nucleosome profiling reveal distinct roles of H1 on hetero- and euchromatin: H1 is necessary to form heterochromatic domains yet dispensable for silencing of most transposable elements; H1 depletion affects nucleosome density distribution and mobility in euchromatin, spatial arrangement of nanodomains, histone acetylation, and methylation. These drastic changes affect moderately the transcription but reveal a subset of H1-sensitive genes.

Conclusions

H1 variants have a profound impact on the molecular and spatial (nuclear) chromatin organization in Arabidopsis with distinct roles in euchromatin and heterochromatin and a dual causality on gene expression. Phenotypical analyses further suggest the novel possibility that H1-mediated chromatin organization may contribute to the epigenetic control of developmental and cellular transitions.

Electronic supplementary material

The online version of this article (10.1186/s13059-019-1767-3) contains supplementary material, which is available to authorized users.

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Most cited references 86

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BigWig and BigBed: enabling browsing of large distributed datasets

W. J. Kent, A. S. Zweig, Lisa Barber … (2010)

Summary: BigWig and BigBed files are compressed binary indexed files containing data at several resolutions that allow the high-performance display of next-generation sequencing experiment results in the UCSC Genome Browser. The visualization is implemented using a multi-layered software approach that takes advantage of specific capabilities of web-based protocols and Linux and UNIX operating systems files, R trees and various indexing and compression tricks. As a result, only the data needed to support the current browser view is transmitted rather than the entire file, enabling fast remote access to large distributed data sets. Availability and implementation: Binaries for the BigWig and BigBed creation and parsing utilities may be downloaded at http://hgdownload.cse.ucsc.edu/admin/exe/linux.x86_64/. Source code for the creation and visualization software is freely available for non-commercial use at http://hgdownload.cse.ucsc.edu/admin/jksrc.zip, implemented in C and supported on Linux. The UCSC Genome Browser is available at http://genome.ucsc.edu Contact: ann@soe.ucsc.edu Supplementary information: Supplementary byte-level details of the BigWig and BigBed file formats are available at Bioinformatics online. For an in-depth description of UCSC data file formats and custom tracks, see http://genome.ucsc.edu/FAQ/FAQformat.html and http://genome.ucsc.edu/goldenPath/help/hgTracksHelp.html

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DANPOS: Dynamic analysis of nucleosome position and occupancy by sequencing

Kaifu Chen, Yuanxin Xi, Xuewen Pan … (2013)

Recent developments in next-generation sequencing have enabled whole-genome profiling of nucleosome organizations. Although several algorithms for inferring nucleosome position from a single experimental condition have been available, it remains a challenge to accurately define dynamic nucleosomes associated with environmental changes. Here, we report a comprehensive bioinformatics pipeline, DANPOS, explicitly designed for dynamic nucleosome analysis at single-nucleotide resolution. Using both simulated and real nucleosome data, we demonstrated that bias correction in preliminary data processing and optimal statistical testing significantly enhances the functional interpretation of dynamic nucleosomes. The single-nucleotide resolution analysis of DANPOS allows us to detect all three categories of nucleosome dynamics, such as position shift, fuzziness change, and occupancy change, using a uniform statistical framework. Pathway analysis indicates that each category is involved in distinct biological functions. We also analyzed the influence of sequencing depth and suggest that even 200-fold coverage is probably not enough to identify all the dynamic nucleosomes. Finally, based on nucleosome data from the human hematopoietic stem cells (HSCs) and mouse embryonic stem cells (ESCs), we demonstrated that DANPOS is also robust in defining functional dynamic nucleosomes, not only in promoters, but also in distal regulatory regions in the mammalian genome.

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Organization and cell differentiation in lateral roots of Arabidopsis thaliana.

J. E. MALAMY, P Benfey (1997)

Lateral root formation in plants involves the stimulation of mature pericycle cells to proliferate and redifferentiate to create a new organ. The simple organization of the root of Arabidopsis thaliana allows the development of lateral root primordia to be characterized histologically. We have divided the process of lateral root development into 8 stages defined by specific anatomical characteristics and cell divisions. To identify the cell types in the developing primordium we have generated a collection of marker lines that express beta-glucuronidase in a tissue- or cell type-specific manner in the root. Using these tools we have constructed a model describing the lineage of each cell type in the lateral root. These studies show that organization and cell differentiation in the lateral root primordia precede the appearance of a lateral root meristem, with differential gene expression apparent after the first set of divisions of the pericycle.

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Author and article information

Contributors

Andrzej Jerzmanowski: andyj@ibb.waw.pl

Célia Baroux:

ORCID: http://orcid.org/0000-0001-6307-2229

cbaroux@botinst.uzh.ch

Journal

Journal ID (nlm-ta): Genome Biol

Journal ID (iso-abbrev): Genome Biol

Title: Genome Biology

Publisher: BioMed Central (London )

ISSN (Print): 1474-7596

ISSN (Electronic): 1474-760X

Publication date (Electronic): 7 August 2019

Publication date PMC-release: 7 August 2019

Publication date Collection: 2019

Volume: 20

Electronic Location Identifier: 157

Affiliations

[1 ]ISNI 0000 0004 1937 0650, GRID grid.7400.3, Institute of Plant and Microbial Biology, , Zürich-Basel Plant Science Center, University of Zürich, ; Zürich, Switzerland

[2 ]ISNI 0000 0001 1958 0162, GRID grid.413454.3, Institute of Biochemistry and Biophysics, , Polish Academy of Sciences, ; Pawinskiego 5a, 02-106 Warsaw, Poland

[3 ]ISNI 0000000419368710, GRID grid.47100.32, Department of Molecular, Cellular & Developmental Biology, , Yale University, ; 352a Osborn memorial laboratories, New Haven, CT, 06511 USA

[4 ]Département de Biologie, IBENS, Ecole Normale Supérieure, CNRS, INSERM, PSL Research University, 46 rue d’Ulm, F-75005 Paris, France

[5 ]ISNI 0000 0004 1937 1290, GRID grid.12847.38, College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, , University of Warsaw, ; 02-089 Warsaw, Poland

[6 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Department of Biomedical Engineering, , Northwestern University, ; Evanston, IL 60208 USA

[7 ]ISNI 0000 0004 1937 1290, GRID grid.12847.38, Faculty of Biology, , University of Warsaw, ; Pawinskiego 5a, 02-106 Warsaw, Poland

Author information

Célia Baroux http://orcid.org/0000-0001-6307-2229

Article

Publisher ID: 1767

DOI: 10.1186/s13059-019-1767-3

PMC ID: 6685187

PubMed ID: 31391082

SO-VID: a6366066-e8a2-4d2e-9d0a-7dc0ab396e09

License:

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 10 January 2019

Date accepted : 21 July 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;

Award ID: 310013A_149974

Award Recipient : Célia Baroux

Funded by: systemsX.ch Initiative

Award ID: 2014/235

Award ID: MecanX

Award Recipient : Christoph Ringli Célia Baroux

Funded by: Forschungskredit, University of Zürich

Funded by: Marie Curie EU COFUND programme

Award ID: PLANTFELLOWS 2010-267243

Award Recipient : Kinga Rutowicz

Funded by: Polish National Science Center

Award ID: 2011/01/N/NZ2/04849

Award Recipient : Maciej Lirski

Funded by: Polish Ministry of Science and Higher Education

Award ID: MNiSW/PO4A/03928

Award Recipient : Andrzej Jerzmanowski

Funded by: Agence National de la Recherche

Award ID: ANR-10-LABX-54 MEMOLIFE

Award Recipient : Fredy Barneche

Funded by: Agence Nationale de la Recherche

Award ID: ANR-10-IDEX-0001-02 PSL

Award Recipient : Fredy Barneche

Funded by: Université Paris-Sud

Award ID: Doctoral Fellowship

Award Recipient : Gianluca Teano

Funded by: European COST action

Award ID: CA 16212 "INDEPTH"

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: ANR-18-CE13-0004-01 Chromalight

Award Recipient : Fredy Barneche

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: linker histones,h1,chromatin,heterochromatin,histone methylation,developmental transitions,nucleosome occupancy

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ScienceOpen disciplines: Genetics

Keywords: linker histones, h1, chromatin, heterochromatin, histone methylation, developmental transitions, nucleosome occupancy

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Linker histones are fine-scale chromatin architects modulating developmental decisions in Arabidopsis

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Abstract

Background

Results

Conclusions

Electronic supplementary material

Related collections

Arabidopsis genomics

Most cited references 86

BigWig and BigBed: enabling browsing of large distributed datasets

DANPOS: Dynamic analysis of nucleosome position and occupancy by sequencing

Organization and cell differentiation in lateral roots of Arabidopsis thaliana.

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Cited by 41

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