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Chromatin Dynamics and Development

Published on 12 November 2018



We study the molecular mechanisms by which chromatin factors activate gene transcription in plants, following very precise spatio-temporal patterns. In particular, we would like to understand how, at corresponding loci, chromatin is brought from a repressed to an active state and is maintained and propagated through time and cell division in specific cell types. To this end, we use Arabidopsis as model organism and employ an integrated experimental approach that combines genetics, biochemistry and next generation sequencing analyses.


Project leader

Cristel Carles
Assistant Professor, Chair UGA/CNRS
Laboratoire de Physiologie Cellulaire & Végétale
CEA-Grenoble
17 avenue des Martyrs
38 054 Grenoble cedex 09
France
Phone: 33 (0)4 38 78 41 95
Fax: 33 (0)4 38 78 50 91

Research project

We employ various molecular biology strategies to study
(i) the dynamics of chromatin landscapes,
(ii) the dynamics of activator binding activities (chromatin activators and transcription factors), and to
(iii) characterise novel chromatin activators.

Our strategy should allow understand the crosstalk between chromatin structure and transcription factor binding, two phenomenons often studied independently even though they are closely linked.

Dynamics of chromatin activation: temporal and spatial resolution at the developing flower
Plant ontogeny is associated with highly flexible cell fates that allow organogenetic programs to take place throughout the plant lifespan. During organogenesis, small clusters of stem cells acquire new fates before differentiating into specific cell types. Such events are initiated by the activation of developmental genes specific to clusters of cells that will give rise to specific organ primordia. We aim at deciphering the molecular events that take place at the level of the chromatin and underlie this transition. To this end, we develop and exploit new methodologies enabling a genome-wide analysis of chromatin activation dynamics. Our model of study is the Arabidopsis floral meristem for which genetic tools enable the isolation of synchronized tissues and/or specific tissue types, in large amounts. This permits to follow, in vivo, the transcriptional status of floral developmental genes at different stages of flower development.

Characterization of novel transcriptional and chromatin activators
We previously showed that ULTRAPETALA1 (ULT1), a plant-specific chromatin activator, induces gene expression through the removal of chromatin repressive marks. Taking ULT1 as an anchor, our goal is to identify novel transcriptional activators and characterize their molecular assembly during flower development in Arabidopsis. To that aim, we use (1) yeast-two-hybrid screen (2) Bimolecular Fluorescent Complementation and (3) in planta immuno-precipitation approaches.
Meta-analysis of binding maps for ULT1 and ULT1 partners, together with chromatin features will allow temporal resolution of their assembly and function during gene activation events.


Keywords

Chromatin, transcriptional activation, plant development, stem cells, differentiation, flower morphogenesis, Arabidopsis thaliana

About members

Cristel Carles, PhD: Associate Professor, UJF/CNRS Chair
email, 33 (0)4 38 78 41 95
Cristel did her PhD at the Laboratory of Plant Genome and Development, University of Perpignan in the team of Michel Delseny, where she studied transcriptional regulation of seed development and maturation. Next, she moved to the lab of Jennifer Fletcher, at the Plant Gene Expression Center, UC Berkeley (USA), where she worked as a Post-doctoral Researcher and then as a Research Associate. There, she studied molecular regulation of stem cell fate in Arabidopsis and characterized transcriptional activators that regulate shoot apex activities, such as flowering time and flower development, via interactions with chromatin complexes. This is how she came to get fascinated by epigenetics and chromatin dynamics, for which plant provide great models of study, thanks to their flexible developmental processes. Back to France, Cristel joined the team of Christophe Brugidou for one year, to characterize the silencing supressor of the Rice Yellow Mottle Virus at the Research and Development Institute in Montpellier. She then moved to the University of Grenoble-Alpes on an Associate Professor CNRS Chair for the Biology Department. Hosted by the Institute of Life Sciences Research and Technologies she leads the Chromatin Dynamics and Development group since october 2010, in the Plant and Cell Physiology Laboratory, Floral Regulator team.

Muriel Kabus, L3 Erasmus student
Emmanuel Thévenon, CNRS technician, email, 04 38 78 35 14
Caroline Thouly, PhD student, ENS fellowship, email
Gilles Vachon, CNRS researcher, email, 04 38 78 41 95

Former members

Ali Awada, M2 UGA-Univ Nabathieh (March-July 2017)
Elda Bauda
, L2 UGA (June 2017)
Béatrice Berthet
, Master student
Robert Blanvillain
, joined the Expression of the plastid genome team of our laboratory
Pauline Brun, L3 UGA (Jan 2017)
Evelina Damyanova, Master student, Sofia University, Bulgaria (Nov 2013–April 2014)
Armelle Dongois, M1 UBP Clermont (May–Aug 2014)
Julia Engelhorn
, former Post-doctoral Fellow on a Marie-Curie Intra-European Fellowship, now member of the "Epigenetic control of plant development" group (dir. Jose Gutierrez-Marcos)
Kateryna Fal, visiting PhD student, Basel University, Switzerland (May 2013, Jan 2014)
Enora Frémy, M1 student (March-May 2016)
Huan He, former master student, now PhD student at UGA (Mohamed-Ali HAKIMI team at the Institut Albert Bonniot of Grenoble)
Pauline Hérisson-Garin, L3 UGA (Jan 2018)
Claire Jourdain, M1 UPS Toulouse (March-June 2017)
Morgane Lapeyre, L3 Pro student (March-July 2016)
Fanny Moreau, former PhD Student on a Rhône-Alpes Region Fellowship
Emeline Pano, UC Fresno, USA (May– July 2017)
Marie Pireyre, former master student, now PhD student at the DynaMo Center, University of Copenhagen
Emmanuel Tergemina, former master student, now PhD student in Franziska Turck lab, Max Planck Institute, Cologne.


We welcome enquiries from highly-motivated postdocs, graduate and master students wanting to contribute to the research topics developed in our team.

Publications

Papers relevant to the Chromatin Dynamics and Development topic
Yan W, Chen D, Smaczniak C, Engelhorn J, Liu H, Yang W, Graf A, Carles CC, Zhou DX, Kaufmann K
Dynamic and spatial restriction of Polycomb activity by plant histone demethylases.
Nature Plants, 2018, 4(9): 681-689

Hugouvieux V, Silva CS, Jourdain A, Stigliani A, Charras Q, Conn V, Conn SJ, Carles CC, Parcy F and Zubieta C
Tetramerization of MADS family transcription factors SEPALLATA3 and AGAMOUS is required for floral meristem determinacy in Arabidopsis.
Nucleic Acids Research, 2018, 46(10): 4966-4977

Vachon G, Engelhorn J and Carles CC
Interactions between transcription factors and chromatin regulators in the control of flower development.
Journal of Experimental Botany, 2018, 69(10): 2461-2471

Engelhorn J, Wellmer F and Carles CC
Profiling histone modifications in synchronized floral tissues for quantitative resolution of chromatin and transcriptome dynamics.
Methods in Molecular Biology, 2018, 1675: 271-296

Engelhorn J, Blanvillain R, Kröner C, Parrinello H, Rohmer M, Posé D, Ott F, Schmid M and Carles CC
Dynamics of H3K4me3 chromatin marks prevails over H3K27me3 for gene regulation during flower morphogenesis in Arabidopsis thaliana.
Epigenomes, 2017, 1(2): 8
Institute and at CEA highlights

Moreau F, Thevenon E, Blanvillain R, Lopez-Vidriero I, Franco-Zorrilla JM, Dumas R, Parcy F, Morel P, Trehin C and Carles CC
The Myb-domain protein ULTRAPETALA1 INTERACTING FACTOR 1 controls floral meristem activities in Arabidopsis.
Development, 2016, 143(7): 1108-1119
Institute highlight

Engelhorn J, Blanvillain R and Carles CC
Gene activation and cell fate control in plants: A chromatin perspective.
Cellular and Molecular Life Sciences, 2014, 71(16): 3119-3137

Engelhorn J, Moreau F, Fletcher JC and Carles CC
ULTRAPETALA1 and LEAFY pathways function independently in specifying identity and determinacy at the Arabidopsis floral meristem.
Annals of Botany, 2014, 114(7): 1497-1505
Mandel T, Moreau F, Kutsher Y, Fletcher JC, Carles CC and Williams LE
The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity.
Development, 2014, 141(4): 830-841
Monfared MM, Carles CC, Rossignol P, Pires HR and Fletcher JC
The ULT1 and ULT2 trxG genes play overlapping roles in Arabidopsis development and gene regulation.
Molecular Plant, 2013, 6(5): 1564-1579
Smaczniak C, Immink RG, Muiño JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S, Parcy F, Xu L, Carles CC, Angenent GC and Kaufmann K
Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development.
Proceedings of the National Academy of Sciences, 2012, 109(5): 1560-1565
Carles CC and Fletcher JC
Missing links between histones and RNA Pol II arising from SAND?
Epigenetics, 2010, 5(5): 381-385
Carles CC and Fletcher JC
The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants.
Genes & Development, 2009, 23: 2723-2728
Carles CC, Choffnes-Inada D, Reville K, Lertpiriyapong K and Fletcher JC
ULTRAPETALA1 encodes a SAND domain putative transcriptional regulator that controls shoot and floral meristem activity in Arabidopsis.
Development, 2005, 132(5): 897-911
Carles CC, Lertpiriyapong K, Reville K and Fletcher JC
The ULTRAPETALA1 gene functions early in Arabidopsis development to restrict shoot apical meristem activity, and acts through WUSCHEL to regulate floral meristem determinacy.
Genetics, 2004, 167(4): 1893-903
Reviews and Book Chapters

Chahtane H, Denay G, Engelhorn J, Monniaux M, Moyroud E, Moreau F, Carles C, Tichtincky G, Zubieta C and Parcy F
Floral development: An integrated view. In From Molecules to Living Organisms: An Interplay Between Biology and Physics: Lecture Notes of the Les Houches School of Physics: Volume 102, July 2014 (Lecture Notes of the Les Houches Summer School), Session CII, (E. Pebay-Peyroula, H. Nury, F. Parcy, R.W.H. Ruigrok, C. Ziegler and L.F. Cugliandolo, Eds) Oxford University Press, 2016, pp 464


 
Carles CC, Ha CM, Jun JH, Fiume E and Fletcher JC
Analyzing shoot apical meristem development.
Methods in Molecular Biology, 2010, 655: 105-129

Carles CC and Fletcher JC
Shoot apical meristem maintenance: The art of a dynamic balance.
Trends in Plant Science, 2003, 8(8): 394-401

Sharma VK, Carles C and Fletcher JC
Maintenance of stem cell populations in plants.
Proceedings of the National Academy of Sciences USA, 2003, 100(Suppl 1): 11823-11829
Other topics

Mandel T, Candela H, Landau U, Asis L, Zelinger E, Carles CC and Williams LE

Differential regulation of meristem size, morphology and organization by the ERECTA, CLAVATA and class III HD-ZIP pathways.
Development, 2016, 143(9): 1612-1622

Ó'Maoiléidigh DS, Thomson B, Raganelli A, Wuest SE, Ryan PT, Kwa?niewska K, Carles CC, Graciet E and Wellmer F
Gene network analysis of Arabidopsis thaliana flower development through dynamic gene perturbations.
Plant Journal, 2015, 83(2): 344-358

Rodor J, Jobet E, Bizarro J, Vignols F, Carles C, Suzuki T, Nakamura K and Echeverria M
AtNUFIP, an essential protein for plant development, reveals the impact of snoRNA gene organisation on the assembly of snoRNPs and rRNA methylation in Arabidopsis thaliana.
Plant Journal, 2011, 65(5): 807-819
Williams L*, Carles CC*, Osmont KS* and Fletcher JC
A database analysis method identifies an endogenous trans -acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes.
Proceedings of the National Academy of Sciences USA, 2005, 102(27): 9703-9708
*LW, CCC, and KSO contributed equally to this work.

Contracts and grants

CNRS Excellence Chair, University of Grenoble-Alpes (2009-2014)
ANR JCJC (2011-2014)
ADR (2011-2014), Rhône-Alpes region
French Ambassy Stipend to Julia Engelhorn


Collaborators

Kerstin Kaufmann, Laboratory of Molecular Biology, Wageningen University, The Netherlands
Markus Schmid, Molecular Biology of Plants & Animals, Max Planck Institute for Developmental Biology, Tübingen, Germany
Frank Wellmer, Smurfit Institute of Genetics, Trinity College Dublin, Ireland
Leor Eshed Williams, The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Israël