1. HSFA1a modulates plant heat stress responses and alters the 3D chromatin organization of enhancer-promoter interactions
- Author
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Ying Huang, Jing An, Sanchari Sircar, Clara Bergis, Chloé Dias Lopes, Xiaoning He, Barbara Da Costa, Feng-Quan Tan, Jeremie Bazin, Javier Antunez-Sanchez, Maria Florencia Mammarella, Ravi-sureshbhai Devani, Rim Brik-Chaouche, Abdelhafid Bendahmane, Florian Frugier, Chongjing Xia, Christophe Rothan, Aline V. Probst, Zouine Mohamed, Catherine Bergounioux, Marianne Delarue, Yijing Zhang, Shaojian Zheng, Martin Crespi, Sotirios Fragkostefanakis, Magdy M. Mahfouz, Federico Ariel, Jose Gutierrez-Marcos, Cécile Raynaud, David Latrasse, Moussa Benhamed, Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Université d'Évry-Val-d'Essonne (UEVE)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), University of Warwick [Coventry], Instituto de Agrobiotecnología del Litoral [Santa Fe] (IAL), Consejo Nacional de Investigaciones Científicas y Técnicas [Buenos Aires] (CONICET)-Universidad Nacional del Litoral [Santa Fe] (UNL), Southwest University of Science and Technology [Mianyang] (SWUST), Biologie du fruit et pathologie (BFP), Université de Bordeaux (UB)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Génétique, Reproduction et Développement (GReD), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Clermont Auvergne (UCA), UMR 990, Université d'Auvergne - Clermont-Ferrand I (UdA)-Institut National de la Santé et de la Recherche Médicale (INSERM), King Abdullah University of Science and Technology (KAUST), Fudan University [Shanghai], Zhejiang University, Goethe-University Frankfurt am Main, Institut Universitaire de France (IUF), Ministère de l'Education nationale, de l’Enseignement supérieur et de la Recherche (M.E.N.E.S.R.), This work was supported by the European Research Council ERC (Project 101044399-3Dwheat), Agence National de la Recherche ANR (ANR-21-CE20-0036-4D Heat Tomato) and by the Institut Universitaire de France (IUF) to M.B. Moreover, this work was supported by China Scholar Council fellowships (201806690005) to Y.H. Figure 6 was created using BioRender (www.biorender.com) with publication permissions., ANR-21-CE20-0036,4D-Heat,Une approche 4D nucleome pour identifier les activateurs contrôlant la réponse au stress thermique de la tomat(2021), and European Project: 101044399,3Dwheat
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stress thermique ,Multidisciplinary ,[SDV]Life Sciences [q-bio] ,General Physics and Astronomy ,General Chemistry ,Expression des genes ,General Biochemistry, Genetics and Molecular Biology ,Facteur de transcription ,tomate ,chaleur ,Fruit ,[SDV.BV]Life Sciences [q-bio]/Vegetal Biology ,Plante ,chromatine - Abstract
The complex and dynamic three-dimensional organization of chromatin within the nucleus makes understanding the control of gene expression challenging, but also opens up possible ways to epigenetically modulate gene expression. Because plants are sessile, they evolved sophisticated ways to rapidly modulate gene expression in response to environmental stress, that are thought to be coordinated by changes in chromatin conformation to mediate specific cellular and physiological responses. However, to what extent and how stress induces dynamic changes in chromatin reorganization remains poorly understood. Here, we comprehensively investigated genome-wide chromatin changes associated with transcriptional reprogramming response to heat stress in tomato. Our data show that heat stress induces rapid changes in chromatin architecture, leading to the transient formation of promoter-enhancer contacts, likely driving the expression of heat-stress responsive genes. Furthermore, we demonstrate that chromatin spatial reorganization requires HSFA1a, a transcription factor (TF) essential for heat stress tolerance in tomato. In light of our findings, we propose that TFs play a key role in controlling dynamic transcriptional responses through 3D reconfiguration of promoter-enhancer contacts.
- Published
- 2023
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