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

Jing An, Rim Brik Chaouche, Leonardo I Pereyra-Bistraín, Hugo Zalzalé, Qingyi Wang, Ying Huang, Xiaoning He, Chloé Dias Lopes, Javier Antunez-Sanchez, Catherine Bergounioux, Claire Boulogne, Cynthia Dupas, Cynthia Gillet, José Manuel Pérez-Pérez, Olivier Mathieu, Nicolas Bouché, Sotirios Fragkostefanakis, Yijing Zhang, Shaojian Zheng, Martin Crespi, Magdy M Mahfouz, Federico Ariel, Jose Gutierrez-Marcos, Cécile Raynaud, David Latrasse, Moussa Benhamed

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. 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.

PNAS. July 2024