Abstract
The genome of all organisms is spatially organized to function efficiently. The advent of genome-wide chromatin conformation capture (Hi-C) methods has revolutionized our ability to probe the three-dimensional (3D) organization of genomes across diverse species. In this Review, we compare 3D chromatin folding from bacteria and archaea to that in mammals and plants, focusing on topology at the level of gene regulatory domains. In doing so, we consider systematic similarities and differences that hint at the origin and evolution of spatial chromatin folding and its relation to gene activity. We discuss the universality of spatial chromatin domains in all kingdoms, each encompassing one to several genes. We also highlight differences between organisms and suggest that similar features in Hi-C matrices do not necessarily reflect the same biological process or function. Furthermore, we discuss the evolution of domain boundaries and boundary-forming proteins, which indicates that structural maintenance of chromosome (SMC) proteins and the transcription machinery are the ancestral sculptors of the genome. Architectural proteins such as CTCF serve as clade-specific determinants of genome organization. Finally, studies in many non-model organisms show that, despite the ancient origin of 3D chromatin folding and its intricate link to gene activity, evolution tolerates substantial changes in genome organization.
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Acknowledgements
D.M.I. was supported by funding from the DFG SPP 22.02 ‘3D Genome Architecture in Development and Disease’ (IB139/1-1 and IB139/6-1). Research in the Ibrahim laboratory is supported by ERC starting grant 101076709 ‘SYNREG’. M.-F.S., B.M. and G.C. were supported through the Marie Skłodowska-Curie Innovative Training Network (813327 ‘ChromDesign’ and 813282 ‘PEP-NET’) under the European Union’s Horizon 2020 research and innovation program. I.J. was supported by EMBO long-term fellowship ATLF 559-2018. G.C. was additionally supported by grants from the European Research Council (Advanced Grant 3DEpi, under grant agreement number 788972), the Fondation pour la Recherche Médicale (EQU202303016280), the MSDAVENIR foundation (project EpiMuM-3D), the Centre National pour la Recherche Scientifique, the Agence Nationale de la Recherche (‘PLASMADIFF3D’ project, ANR-18-CE15-0010) and by the French National Cancer Institute (INCa PLBIO18-362).
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Szalay, MF., Majchrzycka, B., Jerković, I. et al. Evolution and function of chromatin domains across the tree of life. Nat Struct Mol Biol 31, 1824–1837 (2024). https://doi.org/10.1038/s41594-024-01427-y
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DOI: https://doi.org/10.1038/s41594-024-01427-y
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