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Epigenome adaptations to light

Research staff

Fredy Barneche CNRS Research Director - Tel. : +33 (0) 144 32 35 28
Clara Bourbousse CNRS Research Scientist - Tel. : +33 (0) 144 32 35 28
Geoffrey Schivre (PhD student)
Elodie Armanet (PhD student)
Ivona Biocanin (PhD student)
Clarisse Zigue (PhD student, upcoming arrival)
Mhairi Davidson (Post-doc)
Lorenzo Concia (Post-Doc)
Adrien Vidal (Bioinformatician)

Research aim

Fredy and Clara lead a research axis aimed at determining how and why epigenetically and chromatin-based mechanisms influence plant adaptive responses to environmental cues, with a specific emphasis on light conditions.

 See also the ChromaLight web page

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 that presumably underlies the extraordinary fitness of these sessile organisms exposed to changing environments. Light is such a crucial environmental factor.

Light 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). This short developmental window 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 1. Sensing of distinct light wavebands by the photoreceptors establish a tight control of Arabidopsis development.

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. 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.

Figure 2. Investigating chromatin reprogramming during photomorphogenesis.

Recently, in a collaborative work with the Rubio team, we have identified a functional role for the long-known association of the DET1 light signaling component on chromatin. This study unveiled a mechanism that controls the abundance of specific epigenetic marks during Arabidopsis photomorphogenesis. The factors involved are conserved in other eukaryotic organisms, including mammals, in which they influence cell proliferation and differentiation.

Figure 3. Proposed model depicting the DET1 complex activity in regulating histone H2Bub homeostasis through ubiquitin-mediated control of the DUBm stability (Nassrallah et al, 2018). The UBP22 de-ubiquitination module (DUBm) controls histone H2Bub deubiquitination over most genes, possibly promoting their transcription under optimal growth conditions. The DET1 complex favor degradation of the DUBm via its DDA1 subunit. DET1 affinity for non-acetylated histone H2B (Benvenuto et al, 2002) may favor this degradation process nearby H2Bub-rich regions.

In brief, 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.

Selected publications

• Teano G., Concia L., Carron L., Wolff L., Adamusova K., Fojtova M., Bourge M., Kramdi A., Colot V., Grossniklaus U., Bowler C, Baroux C., Carbonne A., Probst A.V., Prochazkova Schrumpfova P., Fajkus J., Amiard S., Grob S., *Bourbousse C., *Barneche F. (2020) Histone H1 protects telomeric repeats from H3K27me3 invasion in Arabidopsis. BioRXiv

• *Cañibano, E., *Bourbousse, C., Garcia-Leon, M., Wolff, L., Garcia-Baudino, C., Barneche, F., Rubio, V., and Fonseca, S. (2021). DET1-mediated COP1 regulation avoids HY5 activity over second-site targets to tune plant photomorphogenesis. Mol. Plant

• Bourbousse C., Barneche F., and Laloi C. (2020). Plant chromatin catches the sun. Front. Plant Sci..

• Arabidopsis S2Lb links AtCOMPASS-like and SDG2 activity in H3K4me3 independently from histone H2B monoubiquitination. (2019) *Fiorucci AS, *Bourbousse C, Concia L, Rougée M, Deton-Cabanillas AF, Zabulon G, Layat E, Latrasse D, Kim SK, Chaumont N, Lombard B, Stroebel D, Lemoine S, Mohammad A, Blugeon C, Loew D, Bailly C, Bowler C, Benhamed M, Barneche F. Genome Biology

• DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis. (2018) *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. eLife

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

• Unreeling the chromatin thread : a genomic perspective on organization around the periphery of the Arabidopsis nucleus. (2017) *Barneche F, Baroux C. Genome Biology .

• The Arabidopsis SWI/SNF protein BAF60 mediates seedling growth control by modulating DNA accessibility. (2017) 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.  Genome Biology

• 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

• DNA DAMAGE BINDING PROTEIN 2 (DDB2) Shapes the DNA Methylation Landscape. 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) The Plant Cell .

• Plants Release Precursors of Histone Deacetylase Inhibitors to Suppress Growth of Competitors. (2015) 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. The Plant Cell

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

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

Former lab members

 Léa Wolff. Research engineer, now traveling around the world
 Gianluca Teano. PhD student, now psot-doc at IPS2-Paris Saclay University (France)
 Ouardia Ait-Mohamed. Bioinformatics engineer, now working at the Curie Institute (France)
 Anne-Flore Deton. Research assistant, now working at CEA-Grenoble University
 Martin Rougée PhD student, now project manager (DNA Script company, Paris, France)
 Gérald Zabulon (Research assistant). After a long and fruitful carrier at the ENS, Gerald can now enjoy a well-deserved retirement.
 Anne-Sophie Fiorucci. PhD student, now Assistant Professor at Paris Saclay University
 Stéphanie Drevensek. Post-doc, now Research scientist at Polytechnique.
 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 Head Of Project Management at Uriach (Barcelona, Spain)