HSFA1a modulates plant heat stress responses and alters the 3D chromatin organization of enhancer-promoter interactions

Ying Huang, Jing An, Sanchari Sircar, Clara Bergis, Chloé Dias Lopes, Xiaoning He, Barbara 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 and Moussa Benhamed ()
Additional contact information
Ying Huang: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Jing An: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Sanchari Sircar: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Clara Bergis: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Chloé Dias Lopes: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Xiaoning He: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Barbara Costa: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Feng-Quan Tan: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Jeremie Bazin: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Javier Antunez-Sanchez: University of Warwick
Maria Florencia Mammarella: Universidad Nacional del Litoral
Ravi-sureshbhai Devani: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Rim Brik-Chaouche: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Abdelhafid Bendahmane: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Florian Frugier: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Chongjing Xia: Southwest University of Science and Technology
Christophe Rothan: INRA and University of Bordeaux, UMR 1332 Biologie du Fruit et Pathologie
Aline V. Probst: Université Clermont Auvergne, CNRS, INSERM, BP 38
Zouine Mohamed: Laboratoire Génomique et Biotechnologie du Fruit (GBF), UMR990, INRA/INP-ENSAT
Catherine Bergounioux: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Marianne Delarue: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Yijing Zhang: Fudan University
Shaojian Zheng: Zhejiang University
Martin Crespi: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Sotirios Fragkostefanakis: Goethe University Frankfurt am Main
Magdy M. Mahfouz: King Abdullah University of Science and Technology
Federico Ariel: Universidad Nacional del Litoral
Jose Gutierrez-Marcos: University of Warwick
Cécile Raynaud: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
David Latrasse: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)
Moussa Benhamed: Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2)

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: 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.

Date: 2023
References: View complete reference list from CitEc
Citations: View citations in EconPapers (4)

Downloads: (external link)
https://www.nature.com/articles/s41467-023-36227-3 Abstract (text/html)

Related works:
This item may be available elsewhere in EconPapers: Search for items with the same title.

Export reference: BibTeX RIS (EndNote, ProCite, RefMan) HTML/Text

Persistent link: https://EconPapers.repec.org/RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36227-3

Ordering information: This journal article can be ordered from
https://www.nature.com/ncomms/

DOI: 10.1038/s41467-023-36227-3

Access Statistics for this article

Nature Communications is currently edited by Nathalie Le Bot, Enda Bergin and Fiona Gillespie

More articles in Nature Communications from Nature
Bibliographic data for series maintained by Sonal Shukla () and Springer Nature Abstracting and Indexing ().