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Environmentally-controlled plant chromatin dynamics

Research staff

Fredy Barneche CNRS Research Director - Tel. : +33 (0) 144 32 35 28
Anne-Flore Deton Research assistant - Tel. : +33 (0) 144 32 35 26
Clara Bourbousse Post-Doc PSL - Tel. :+33 (0) 144 32 35 23
Laeticia Tcheng L3 ENS student
Martin Rougée Post-doc - Tel. : +33 (0) 144 32 35 23
Gianluca Teano PhD student - Tel. : +33 (0) 144 32 35 23
Ouardia Ait-Mohamed Research Ingeneer

Research aim

We are interested in determining how and why epigenetically and chromatin-based mechanisms influence plant adaptive responses to environmental cues, with a specific emphasis on light conditions.

Research activity

As multicellular organisms, plants have to regulate the expression of numerous genes in a coordinated fashion to respond to intrinsic and environmental signals. Indeed, a remarkable feature of plants is their capacity to adjust their development and physiology to external cues, a property which is presumably underlying the extraordinary fitness of these sessile organisms exposed to changing environments.

Light is such a crucial environmental factor It not only constitutes an essential energy source for photosynthesis but also provides reliable information on the environment to the plant. Light sensing by multiple photoreceptors and dowstream signaling pathways lead to multilevel cellular controls, notably determining key plant developmental transitions such as germination, flowering and photomorphogenesis (Figure 1).

Figure 1. Sensing of distinct light wavebands by the photoreceptors establish a tight control of Arabidopsis development. Phenotypic changes of a 5-day-old Arabidopsis plant subjected to a dark-to-light transition, inducing cotyledon development and the establishment of photosynthesis (greening) in response to light signaling.

A longstanding question in plant photobiology concerns how light perception can have such a strong impact on the plant developmental programs. Studies from the past 40 years have unveiled that many gene regulatory mechanisms and key transcription factors converge onto chromatin, a programmable platform that determines DNA accessibility and expression. Chromatin (histone and DNA) is known to functionally organize the genome into the nuclei of eukaryotic cells, which is key for the establishment of gene expression programs.

Hence, our research activity mainly uses photomorphogenesis, a developmental switch that plants undergo upon the first light perception event, as a paradigm to investigate the mechanisms driving nuclear and epigenome reprogramming induced by environmental signals.

We have contributed to unveil that the initial light perception event by the germinating plantlet has a rapid and spectacular influence on plant chromatin organization and composition, from single genes to higher order nuclear architecture (Figure 2). Large-scale chromatin rearrangements underlie a profound reprogramming of gene expression occurring during the ’photo’-morphogenic transition within a few hours. This short developmental window therefore offers an excellent system for dissecting the molecular mechanisms driving multilevel and coordinated chromatin changes over a large repertoire of genes, and how spatio-temporal chromatin dynamics are translated into cell specification.

Figure 2. Investigating chromatin reprogramming during photomorphogenesis.
Top panel : Dramatic reorganization of chromatin architecture in cotyledon nuclei during photomorphogenesis with the formation of 8-to-10 heavily condensed heterochromatin into so-called ’chromocenters’. Bottom panel : Heatmap representation of mRNA-seq analysis showing genome expression reprogramming in cotyledons (left panel) and massive establishment of H2Bub-marked transcriptionally permissive chromatin onto light-responsive gene (HCF107 is shown in the right panel).

Last publications

• *Nassrallah A, *Rougee M, Bourbousse C, Drevensek S, Fonseca S, Iniesto E, Ait-Mohamed O, Deton-Cabanillas AF, Zabulon G, Ahmed I, Stroebel D, Masson V, Lombard B, Eeckhout D, Gevaert K, Loew D, Genovesio A, Breyton C, de Jaeger G, Bowler C, Rubio V and F Barneche. (2018) DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis. eLife e37892.

• Bourbousse C., Benhamed M. and F. *Barneche (2018). Profiling developmentally and environmentally controlled chromatin reprogramming. (Review) Methods in Molecular Biology .

• *Barneche F, Baroux C. (2017) Unreeling the chromatin thread : a genomic perspective on organization around the periphery of the Arabidopsis nucleus. Genome Biol . 18(1):97 doi : 10.1186/s13059-017-1239-6.

• Jégu T, Veluchamy A, Ramirez-Prado JS, Rizzi-Paillet C, Perez M, Lhomme A, Latrasse D, Coleno E, Vicaire S, Legras S, Jost B, Rougée M, Barneche F, Bergounioux C, Crespi M, Mahfouz M, Hirt H, Raynaud C and Benhamed M. (2017) The Arabidopsis SWI/SNF protein BAF60 mediates seedling growth control by modulating DNA accessibility. Genome Biology 18(1):114. doi : 10.1186/s13059-017-1246-7.

• Snoek BL, Pavlova P, Tessadori F, Peeters AJM, Bourbousse C, Barneche F, de Jong JH, Fransz PF, van Zanten M. (2017) Genetic Dissection of Morphometric Traits Reveals that Phytochrome B Affects Nucleus Size and Heterochromatin Organization in Arabidopsis thaliana. G3 . doi : 10.1534/g3.117.043539.

• Schalk C, Drevensek S, Kramdi A, Kassam M, Ahmed I, Cognat V, Graindorge S, Bergdoll M, Baumberger N, Heintz D, Bowler C, Genschik P, Barneche F, Colot V, Molinier J. (2016) DNA DAMAGE BINDING PROTEIN 2 (DDB2) Shapes the DNA Methylation Landscape. The Plant Cell . pii : tpc.00474.2016.

• Venturelli S, Belz RG, Kämper A, Berger A, von Horn K, Wegner A, Böcker A, Zabulon G, Langenecker T, Kohlbacher O, Barneche F, Weigel D, Lauer UM, Bitzer M, Becker C. (2015) Plants Release Precursors of Histone Deacetylase Inhibitors to Suppress Growth of Competitors. The Plant Cell . 27(11):3175-89. doi : 10.1105/tpc.15.00585

• Bourbousse C, Mestiri I, Zabulon G, Bourge M, Formiggini F, Koini MA, Brown SC, Fransz P, Bowler C, Barneche F. (2015) Light signaling controls nuclear architecture reorganization during seedling establishment. Proc Natl Acad Sci U S A.

• *Barneche F., Malapeira J. and P. Mas (2014) The impact of chromatin dynamics on plant light responses and circadian clock function. J. Exp. Bot.. (Review).

• Bourbousse C., Ahmed I., Roudier F., Zabulon G., Blondet E., Balzergue S., Colot V., Bowler C., Barneche F. (2012) Histone H2B Monoubiquitination Facilitates the Rapid Modulation of Gene Expression during Arabidopsis Photomorphogenesis. PLoS Genet..

Former lab members

- Gérald Zabulon. After a long and fruitful carrier at the ENS, Gerald can now enjoy a well-deserved retirement.
- Anne-Sophie Fiorucci PhD student, now joined the laboratory of Prof. Christian Fankhauser at the CIG (Lausanne, Switzerland) as a post-doc.
- Clara Bourbousse PhD student and now Post-Doc. After a first post-doc in the laboratory of Julie Law at the Salk Institute (San Diego, USA) she recently came back for a 2nd post-doc experience.
- Stéphanie Drevensek Post-doc, now joined the Institute of Plant Sciences-Paris Saclay (IPS2) (France) as a Research Associate.
- Ikhlak Ahmed PhD student co-supervised by Chris Bowler and Vincent Colot at the IBENS, now joined the Weill Cornell Medical College (Qatar) as a Research Associate.
- Massimo Rainieri, Post-doc, is now teaching Biology in a public high-school.
- Enric Castells, Post-doc, now joined the Biokit biotech company (Barcelona, Spain) as a Research Scientist.