An atlas of the tomato epigenome reveals that KRYPTONITE shapes TAD-like boundaries through the control of H3K9ac distribution

Author:

An Jing1ORCID,Brik Chaouche Rim1,Pereyra-Bistraín Leonardo I.12ORCID,Zalzalé Hugo12,Wang Qingyi1,Huang Ying1,He Xiaoning1ORCID,Dias Lopes Chloé1,Antunez-Sanchez Javier3ORCID,Bergounioux Catherine1,Boulogne Claire4ORCID,Dupas Cynthia4ORCID,Gillet Cynthia4,Pérez-Pérez José Manuel5ORCID,Mathieu Olivier6ORCID,Bouché Nicolas7ORCID,Fragkostefanakis Sotirios8ORCID,Zhang Yijing9,Zheng Shaojian10ORCID,Crespi Martin1ORCID,Mahfouz Magdy M.11ORCID,Ariel Federico12,Gutierrez-Marcos Jose3ORCID,Raynaud Cécile1,Latrasse David1,Benhamed Moussa1213

Affiliation:

1. Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-Saclay (IPS2), Orsay 91405, France

2. Université de Paris Cité, Institute of Plant Sciences Paris-Saclay (IPS2), Gif-sur-Yvette F-91190, France

3. School of Life Science, University of Warwick, Coventry CV4 7AL, United Kingdom

4. Imagerie-Gif, Electron Microscopy Facility, Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette 91198, France

5. Instituto de Bioingeniería, Universidad Miguel Hernández, Elche 03202, Spain

6. Institute of Genetics Reproduction and Development (iGReD), Université Clermont Auvergne, CNRS, Inserm, Clermont-Ferrand F-63000, France

7. Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, Versailles 78000, France

8. Molecular and Cell Biology of Plants, Goethe University Frankfurt, Frankfurt D-60438, Germany

9. State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Department of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai 200438, China

10. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou 310058, China

11. Laboratory for Genome Engineering and Synthetic Biology, Division of Biological Sciences, 4700 King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia

12. Instituto de Agrobiotecnología del Litoral, CONICET, Universidad Nacional del Litoral, Santa Fe 3000, Argentina

13. Institut Universitaire de France, Orsay, Gif-sur-Yvette 91190, France

Abstract

In recent years, the exploration of genome three-dimensional (3D) conformation has yielded profound insights into the regulation of gene expression and cellular functions in both animals and plants. While animals exhibit a characteristic genome topology defined by topologically associating domains (TADs), plants display similar features with a more diverse conformation across species. Employing advanced high-throughput sequencing and microscopy techniques, we investigated the landscape of 26 histone modifications and RNA polymerase II distribution in tomato ( Solanum lycopersicum ). Our study unveiled a rich and nuanced epigenetic landscape, shedding light on distinct chromatin states associated with heterochromatin formation and gene silencing. Moreover, we elucidated the intricate interplay between these chromatin states and the overall topology of the genome. Employing a genetic approach, we delved into the role of the histone modification H3K9ac in genome topology. Notably, our investigation revealed that the ectopic deposition of this chromatin mark triggered a reorganization of the 3D chromatin structure, defining different TAD-like borders. Our work emphasizes the critical role of H3K9ac in shaping the topology of the tomato genome, providing valuable insights into the epigenetic landscape of this agriculturally significant crop species.

Funder

EC | European Research Council

Agence Nationale de la Recherche

China Scholarship Council

Publisher

Proceedings of the National Academy of Sciences

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