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Mechanisms and role of linker histones dynamics in plant reproduction

Applicant Baroux Célia
Number 149974
Funding scheme Project funding (Div. I-III)
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Embryology, Developmental Biology
Start/End 01.01.2014 - 31.12.2017
Approved amount 430'340.00
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All Disciplines (4)

Discipline
Embryology, Developmental Biology
Molecular Biology
Genetics
Cellular Biology, Cytology

Keywords (6)

Epigenetics; Chromatin; Linker Histones; plant reproduction; Arabidopsis; developmental transitions

Lay Summary (French)

Lead
We hypothesize that H1 dynamics at the somatic-to-reproductive cell fate transition in plants underlie epigenetic reprogramming towards a ground-state epigenome, likewise in animal primordial germ cells. We aim at elucidating the mechanism and role of H1 dynamics in plant spore mother cells and the function of newly identified putative germline-specific variants
Lay summary

Les plantes possèdent une plasticité cellulaire remarquable. Tout au long de leur vie, les plantes génèrent de nouveaux types cellulaires. Cela tient en partie à l’existence de cellules souches, immortelles, au sein des méristèmes apicaux de la plante, mais aussi à des processus de trans-différentiation au sein de tissus somatiques. C’est le cas par exemple de la différentiation des cellules stomatales dans l’épiderme des feuilles, des poils absorbants dans la racine, mais aussi des cellules sporogéniques, précurseurs de la lignée germinale, dans les organes sexuels floraux.

Nous avons démontré que la transition vers un destin sporogénique est accompagnée d’une reprogrammation en profondeur de la chromatine. Ce processus pré-méiotique semble essentiel au développement post-méiotique qui aboutit à la mise en place du gamétophyte. L’éviction des histones H1 constitue l’évènement le plus précoce de cette reprogrammation chromatinienne. Les histones H1 sont des composants majeurs de la chromatine jouant un role structurel primordial dans la compaction. Cependant, au dela de cette fonction, les histones H1 contribuent également à établir l’information épigénétique, notemment  via la méthylation de l’ADN, ceci chez les plantes comme chez les animaux . L’éviction des histones H1 dans les cellules sporogéniques pose donc de nombreuses questions quand au rôle et à l’impact de cet évènement pour le développement cellulaire immédiat mais aussi pour la mémoire épigénétique dans la lignée germinale des plantes.

Au cours de ce projet SNF, nous voulons élucider le rôle structurel et fonctionnel ainsi que les mécanismes de cette dynamique des histone H1 dans les cellules sporogéniques. Nous voulons aussi élucider la fonction de gènes codant pour des formes singulières d’ histones H1 (des variants inusuels), récemment découvertes lors d'analyses génomiques et principalement exprimées dans les cellules de la lignée reproductrice – des cellules sporogéniques au jeune embryon.

Direct link to Lay Summary Last update: 08.01.2014

Responsible applicant and co-applicants

Employees

Publications

Publication
Linker histones are fine-scale chromatin architects modulating developmental decisions in Arabidopsis
Rutowicz Kinga, Lirski Maciej, Mermaz Benoît, Teano Gianluca, Schubert Jasmin, Mestiri Imen, Kroteń Magdalena A., Fabrice Tohnyui Ndinyanka, Fritz Simon, Grob Stefan, Ringli Christoph, Cherkezyan Lusik, Barneche Fredy, Jerzmanowski Andrzej, Baroux Célia (2019), Linker histones are fine-scale chromatin architects modulating developmental decisions in Arabidopsis, in Genome Biology, 20(1), 157-157.
Cell-Type Specific Chromatin Analysis in Whole-Mount Plant Tissues by Immunostaining.
She Wenjing, Baroux Célia, Grossniklaus Ueli (2018), Cell-Type Specific Chromatin Analysis in Whole-Mount Plant Tissues by Immunostaining., in Baroux Célia, Bemer Marian (ed.), Springer, NY, 1675, 443-454.
Technical Review: Microscopy and Image Processing Tools to Analyze Plant Chromatin: Practical Considerations.
Baroux Célia, Schubert Veit (2018), Technical Review: Microscopy and Image Processing Tools to Analyze Plant Chromatin: Practical Considerations., in Bemer Marian, Baroux Célia (ed.), Springer, NY, 1675, 537-589.
Automated 3D Gene Position Analysis Using a Customized Imaris Plugin: XTFISHInsideNucleus
Ashenafi Mariam, Baroux Célia (2018), Automated 3D Gene Position Analysis Using a Customized Imaris Plugin: XTFISHInsideNucleus, in Bemer Marian, Baroux Célia (ed.), Springer, New York, 1.
Transmission Electron Microscopy Imaging to analyse chromatin density distribution at the nanoscale level
Fabrice T.N, Cherkezeyan L., Ringli C., Baroux C. (2018), Transmission Electron Microscopy Imaging to analyse chromatin density distribution at the nanoscale level, in Bemer Marian, Baroux Célia (ed.), Springer, New York, 1.
PHO1 Exports Phosphate from the Chalazal Seed Coat to the Embryo in Developing Arabidopsis Seeds.
Vogiatzaki Evangelia, Baroux Célia, Jung Ji-Yul, Poirier Yves (2017), PHO1 Exports Phosphate from the Chalazal Seed Coat to the Embryo in Developing Arabidopsis Seeds., in Current biology : CB, 27(19), 2893.
Phylogeny-based systematization of arabidopsis proteins with histone H1 globular domain
Kotlinski M., Knizewski L., Muszewska A., Rutowicz K., Lirski M., Schmidt A., Baroux C., Ginalski K., Jerzmanowski A. (2017), Phylogeny-based systematization of arabidopsis proteins with histone H1 globular domain, in Plant Physiology, 174(1), 27-34.
Unreeling the chromatin thread: A genomic perspective on organization around the periphery of the Arabidopsis nucleus
Barneche F., Baroux C. (2017), Unreeling the chromatin thread: A genomic perspective on organization around the periphery of the Arabidopsis nucleus, in Genome Biology, 18(1), 1-3.
Non-random chromosome arrangement in triploid endosperm nuclei.
Baroux Célia, Pecinka Ales, Fuchs Jörg, Kreth Gregor, Schubert Ingo, Grossniklaus Ueli (2016), Non-random chromosome arrangement in triploid endosperm nuclei., in Chromosoma, 1-10.
Quantitative Genetics Identifies Cryptic Genetic Variation Involved in the Paternal Regulation of Seed Development.
Pires Nuno D, Bemer Marian, Müller Lena M, Baroux Célia, Spillane Charles, Grossniklaus Ueli (2016), Quantitative Genetics Identifies Cryptic Genetic Variation Involved in the Paternal Regulation of Seed Development., in PLoS genetics, 12(1), 1005806-1005806.
Chromatin dynamics during cellular differentiation in the female reproductive lineage of flowering plants
Baroux Celia, Autran Daphne (2015), Chromatin dynamics during cellular differentiation in the female reproductive lineage of flowering plants, in Plant Journal, 83(1), 160-176.
Chromatin dynamics in Pollen Mother Cells underpin a common scenario at the somatic-to-reproductive fate transition of both the male and female lineages in Arabidopsis
She Wenjing, Baroux Celia (2015), Chromatin dynamics in Pollen Mother Cells underpin a common scenario at the somatic-to-reproductive fate transition of both the male and female lineages in Arabidopsis, in Frontiers in Plant Science, 6, 1/294-7.
The Maternal-to-Zygotic Transition in Flowering Plants: Evidence, Mechanisms, and Plasticity.
Baroux Celia, Grossniklaus Ueli (2015), The Maternal-to-Zygotic Transition in Flowering Plants: Evidence, Mechanisms, and Plasticity., in Current topics in developmental biology, 113, 351-71.
An Efficient Method for Quantitative, Single-cell Analysis of Chromatin Modification and Nuclear Architecture in Whole-mount Ovules in Arabidopsis
She Wenjing, Grimanelli Daniel, Baroux Celia (2014), An Efficient Method for Quantitative, Single-cell Analysis of Chromatin Modification and Nuclear Architecture in Whole-mount Ovules in Arabidopsis, in Jove-Journal of Visualized Experiments, (88), 51530.
Chromatin dynamics during plant sexual reproduction
She Wenjing, Baroux Celia (2014), Chromatin dynamics during plant sexual reproduction, in Frontiers in Plant Science, 5, 1/534.
Meiotic chromosome movements in plants, a puppet show?
Varas Javier, Baroux Celia (2014), Meiotic chromosome movements in plants, a puppet show?, in Frontiers in Plant Science, 5, 1/502.

Collaboration

Group / person Country
Types of collaboration
Prof Lukas Pelkmans, Institute of Molecular Life Science, University of Zürich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Dr Fredy Barneche, IBENS Paris France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr Zuzanna Kaczmarka, EMBL Grenoble France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Prof Andrzej Jerzmanowski, University of Warsaw Poland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Dr Daniel Grimanelli, IRD France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr Lusik Cherkezeyan, Backman's Biophotonics Laboratory at Northwestern University United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
European Plant Chromatin Workshop Talk given at a conference The role of linker histone proteins in plant cell reprogramming. 01.06.2017 Vienna, Austria Schubert Jasmin; Rutowicz Kinga; Baroux Célia;
PSC - Plant Science Center Symposium 2015 Poster Mechanisms and Role of H1 linker histones in plant reproduction 03.12.2016 Zürich, Switzerland Schubert Jasmin;
PhD School , Plant Development Talk given at a conference 3D organization of the plant chromatin shifting the paradigm from a static to a dynamic viewpoint 05.10.2016 Retzbach, Germany Baroux Célia;
Trinational Arabidopsis Meeting Talk given at a conference Role and mechanisms of H1 linker histone dynamics in plant cell fate Transitions 14.09.2016 Vienna, Austria Baroux Célia;
Trinational Arabidopsis Meeting Poster The rearrangement of linker histone proteins in cell reprogramming. 14.09.2016 Vienna, Austria Rutowicz Kinga;
Conference on Chromatin and Transcription Poster Establishing a high-content microscopy screening approach for identifying chromatin modifiers underlying plant cell transdifferentiation 27.08.2016 Heidelberg, Germany Rutowicz Kinga;
Plant Fellow Annual Symposium Talk given at a conference Is the rearrangements of linker histones required for cell plasticity in plants? 23.06.2016 Zürich, Switzerland Rutowicz Kinga;
conference EpiGene Swiss kick-off meeting Talk given at a conference H1 linker histones in plant cell fate transitions 06.06.2016 Weggis, Switzerland Baroux Célia;
conference EpiGene Swiss kick-off meeting Poster Mechanism and Role of linker histone development in Plant reproduction 06.06.2016 Weggis, Switzerland Schubert Jasmin;
Sexual Plant Reproduction International Congress Talk given at a conference Chromatin Dynamics During Sporogenesis 18.03.2016 Tucson, Arizon (USA), Switzerland Baroux Célia;
Conference on Plant Epigenetics "Epitraits" Poster Impact of H1 depletion on plant chromatin architecture 14.01.2016 IGBMC, Strasbourg, France Baroux Célia;
Conference - EMBO - Nuclear structure and dynamics Poster Mechanism and Role of linker histone development in Plant reproduction 07.10.2014 Isle sur Sorgues, France Schubert Jasmin;
7th PhD School Plant Development Poster Mechanism and Role of linker histone development in Plant reproduction 12.09.2014 Retzbach, Germany Schubert Jasmin;


Knowledge transfer events

Active participation

Title Type of contribution Date Place Persons involved
«3D Mikroskopie» Workshop 09.12.2015 Department of Plant and Microbial Biology, Switzerland Baroux Célia; Schubert Jasmin;
PSC Youth Discovery Workshop (AGORA Program) Performances, exhibitions (e.g. for education institutions) 01.12.2015 IPMB, University of Zürich, Switzerland Baroux Célia; Schubert Jasmin;


Self-organised

Title Date Place
PhD Course (PSC Graduate School): Advanced Microscopy Imaging of Plant Tissues and Image Processing 07.12.2016 Institute of Plant and Microbial Biology, University of Zürich, Switzerland

Communication with the public

Communication Title Media Place Year
Talks/events/exhibitions Scientifica German-speaking Switzerland 2015

Awards

Title Year
Forschungskredit, University of Zürich, PostDoc fellowship, salary only 2016
Marie Curie Fellowship , co-funding type, "Plant Fellows" 40% salary only 2015

Associated projects

Number Title Start Funding scheme
164086 Imaging of Deep-Lying Tissues with Enhanced Resolution and Sensitivity to Study Plant Development 01.12.2015 R'EQUIP
170167 IMAGO : Imaging and Modeling Growth and plasticity in plant Ovules 01.11.2016 Project funding (Div. I-III)
130722 The chromatin basis of plant genome plasticity: Chromatin dynamics during sexual reproduction and clonal propagation 01.04.2010 Project funding (Div. I-III)

Abstract

Unlike most animals, plants retain a remarkable cellular plasticity post-embryogenesis. Throughout their life cycle, plants undergo several developmental phase transitions producing new physiological states (e.g. dormancy), organs (e.g. flowers) or specialized cells (e.g. gametes) that were not established at embryogenesis. Critically, these transitions are associated with large-scale and dynamic event of chromatin reorganization. Current efforts are aiming at establishing the causal link between these events and cell fate acquisition. During our former SNF-funded project, we have shown that the somatic-to-reproductive fate transition in Arabidopsis is associated with chromatin reprogramming which partly establishes the post-meiotic, gametophytic fate. H1 depletion from the chromatin of spore mother cells is the earliest event of chromatin reprogramming. No canonical H1 variants is detectable throughout the female gametophyte and embryogenesis, raising the question of the function of this particular chromatin state, particularly with regard to epigenetic reprogramming. We now aim at elucidating (i) the mechanisms and role of H1 dynamics in plant reproduction and (ii) the role of putative germline specific H1-related variants. We will use molecular genetics approaches, notably to misregulate H1 variants in a conditional and cell-specific manner, together with standard techniques in developmental biology to analyse subtle developmental and cell fate alterations in the mutants, but also high-resolution imaging of fluorescent reporters and chromatin markers, as well as transcriptome studies and FRAP analyses of the H1 variants to assess their chromatin binding properties. Collectively, this project will provide the first insight on the developmental role of H1 dynamics during cellular reprogramming in plants.
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