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The chromatin basis of plant genome plasticity: Chromatin dynamics during sexual reproduction and clonal propagation

Applicant Baroux Célia
Number 130722
Funding scheme Project funding
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Embryology, Developmental Biology
Start/End 01.04.2010 - 31.12.2013
Approved amount 292'670.00
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All Disciplines (5)

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

Keywords (10)

chromatin; histone modifications; chromosome organisation; reprogramming; gamete; endosperm; sexual reproduction; clonal propagation; Arabidopsis; Rice

Lay Summary (English)

Lead
Lay summary
The plant genome harbors an extraordinary plasticity: fully differentiated plant cells can be re-programmed to produce new individuals either sexually (via the production of gametes in flower organs) or clonally (via the production of clonal sprouts from vegetative tissues). This is in stark contrast to animals that must set aside a lineage of undifferentiated cells for reproduction (germ cells) and cannot naturally regenerate from body parts. Recent studies suggest that plant ge-nome plasticity may be supported by specific chromatin organization and composition. But the precise events and control mechanisms of large-scale chromatin remodeling and chromosome organization in reprogramming processes, as described above, are barely explored. The aim of this research proposal is three-fold:(a) Sexual reproduction in plants involves double fertilization. The two female gametes are clonally derived in a multicellular structure but have distinct post-fertilization fates. We hypothesize that distinct epigenetic chromatin signatures are established early during gametogenesis to mark their cell fate. *We will seek for gametic chromatin signatures and analyze their role in gametic fate.*(b) Reproductive success relies on the endosperm, an extra-embryonic nurse tissue produced at fertilization. The dosage of paternally vs maternally-derived products is crucial for its development; alteration can result in seed abortion and hybridization failure. We discovered a specific heterochromatin fraction which responds to ploidy alterations in a parent-of-origin-dependent manner. *We will investigate the role, control, and nature of endosperm-specific heterochromatin in parental dosage regulation and the hybridization barrier.*(c) During clonal propagation, somatic cells de-differentiate under appropriate stimuli and become totipotent. Progeny is produced via somatic embryogenesis or organogenesis. We hypothesize that this genome-wide reprogramming involves specific large-scale chromatin modifica-tions. *We will describe the chromatin dynamics accompanying reprogramming in an experimental case of clonal propagation.*
Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
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
Wenjing She, Célia Baroux (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 Sciences, 28, 294-301.
Chromatin dynamics during plant sexual reproduction
Wenjing She, Celia Baroux (2014), Chromatin dynamics during plant sexual reproduction, in Frontiers in Plant Sciences, 5, 354-370.
Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants.
She Wenjing, Grimanelli Daniel, Rutowicz Kinga, Whitehead Marek W J, Puzio Marcin, Kotlinski Maciej, Jerzmanowski Andrzej, Baroux Célia (2013), Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants., in Development (Cambridge, England), 140(19), 4008-19.
Efficient and rapid isolation of early-stage embryos from Arabidopsis thaliana seeds.
Raissig Michael T, Gagliardini Valeria, Jaenisch Johan, Grossniklaus Ueli, Baroux Célia (2013), Efficient and rapid isolation of early-stage embryos from Arabidopsis thaliana seeds., in Journal of visualized experiments : JoVE, (76), x-x.
Epigenetic regulation and reprogramming during gamete formation in plants.
Baroux Célia, Raissig Michael T, Grossniklaus Ueli (2011), Epigenetic regulation and reprogramming during gamete formation in plants., in Current opinion in genetics & development, 21(2), 124-33.
An efficient method for quantitative, single-cell analysis of chromatin modification and nuclear architecture in whole-mount ovules in Arabidopsis thaliana
Wenjing She, Daniel Grimanelli, Célia Baroux, An efficient method for quantitative, single-cell analysis of chromatin modification and nuclear architecture in whole-mount ovules in Arabidopsis thaliana, in Journal of Vizualised Experiments (JoVE).

Collaboration

Group / person Country
Types of collaboration
IRD-CNRS Montpellier France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
IBP, University of Warsaw Poland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Exchange of personnel

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
European Plant chromatin Workshop III Talk given at a conference CHROMATIN REPROGRAMMING ESTABLISHES COMPETENCE FOR GAMETOPHYTIC DEVELOPMENT IN ARABIDOPSIS 29.08.2013 Madrid, Spain Baroux Célia;
Invited Seminar Individual talk Chromatin Reprogramming during the somatic-to-reproductive fate transition 03.07.2013 Roscoff, France Baroux Célia;
Chromatin: from structure to epigenetics Poster Epigenetic reprogramming during plant sporogenesis and in animal primordial germ cells: how much is in commom? 26.06.2012 Strasbourg, France She Wenjing;
Invited Seminar Individual talk Chromatin Reprogramming in plant spore mother cells and animal primordial germ cells: How much is in common? 19.04.2012 University of Warsaw, Poland Baroux Célia;
Swiss Plant Science Web 2012 Talk given at a conference Epigenetic reprogramming during plant sporogenesis and in the animal primordial germ cells: how much is in common? 18.01.2012 Meiringen (CH), Switzerland Baroux Célia;
Understanding Plant Phenotypes Poster Large-scale chromatin dynamics in epigenetic reprogramming in the Megaspore Mother Cell (MMC) in Arabidopsis thaliana 04.11.2011 Zürich, Switzerland She Wenjing;
European Plant chromatin Workshop II Talk given at a conference CHROMATIN REPROGRAMMING DURING SPOROGENESIS IN ARABIDOPSIS 11.09.2011 Versailles (France), France Baroux Célia;
EMBO Conference Series: Nuclear structure and dynamics Poster Large-scale chromatin dynamics during differentiation of the Megaspore Mother Cell (MMC) in Arabidopsis thaliana 02.09.2011 Isle sur Orgues, France She Wenjing;
EMBO Conference Series: Chromatin and Epigenetics Poster Large-scale chromatin dynamics during differentiation of the Megaspore Mother Cell (MMC) in Arabidopsis thaliana 01.06.2011 Heidelberg, Germany She Wenjing;


Associated projects

Number Title Start Funding scheme
133863 Live Cell Imaging to study dynamic developmental processes and protein-protein intertactions in planta 01.12.2011 R'EQUIP
149974 Mechanisms and role of linker histones dynamics in plant reproduction 01.01.2014 Project funding
150838 Lightsheet Fluorescence Microscopy 01.12.2013 R'EQUIP

Abstract

1.Summary 1.1BackgroundThe plant genome harbors an extraordinary plasticity: fully differentiated plant cells can be re-programmed to produce new individuals either sexually (via the production of gametes in flower organs) or clonally (via the production of clonal sprouts from vegetative tissues). This is in stark contrast to animals that must set aside a lineage of undifferentiated cells for reproduction (germ cells) and cannot naturally regenerate from body parts. Recent studies suggest that plant ge-nome plasticity may be supported by specific chromatin organization and composition. But the precise events and control mechanisms of large-scale chromatin remodeling and chromosome organization in reprogramming processes, as described above, are barely explored. 1.2Hypothesis (a) Sexual reproduction in plants involves double fertilization. The two female gametes are clo-nally derived in a multicellular structure but have distinct post-fertilization fates. We hypothesize that distinct epigenetic chromatin signatures are established early during gametogenesis to mark their cell fate. (b) Reproductive success relies on the endosperm, an extra-embryonic nurse tissue produced at fertilization. The dosage of paternally vs maternally-derived products is crucial for its devel-opment; alteration can result in seed abortion and hybridization failure. We discovered a specific heterochromatin fraction which responds to ploidy alterations in a parent-of-origin-dependent manner (Baroux et al, 2007). We hypothesize that parental dosage is mediated, in part, by genes regulated in this heterochromatin fraction.(c) During clonal propagation, somatic cells de-differentiate under appropriate stimuli and become totipotent. Progeny is produced via somatic embryogenesis or organogenesis. We hypo-thesize that this genome-wide reprogramming involves specific large-scale chromatin modifications.1.3Specific AimsTo answer the above questions, we will:(a) Identify gametic chromatin signatures and analyze their role in cell fate determination.(b) Investigate the role, control, and nature of endosperm-specific heterochromatin in parental dosage regulation and the hybridization barrier.(c) Describe the chromatin dynamics accompanying reprogramming in an experimental case of clonal propagation.1.4Experimental approach(a) Chromatin organization and dynamics will be described in developing gametophytes of Ara-bidopsis using whole-mount immunolabelling, FISH, and GFP-tagged proteins. Mutant analysis will uncover the role of candidate signatures. We will investigate the conservation of the signatures in rice. (b) Quantitative and qualitative alteration of the endosperm-specific heterochromatin in hybrids and mutants will uncover its significance and molecular control, respectively. The presence of candidate genes within this fraction will be tested by FISH. For (c) a simple experimental system is chosen where somatic embryos can be induced at high efficiency from Brassica microspores.1.5SignificanceThis research will significantly contribute to elucidating the mechanistic basis of the extraordinary plasticity of plant cells and the acquisition of cell fate. Understanding parental dosage control in nonviable vs viable hybrid seeds could potentially feed applications in hybrid plant production.
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