Science.: co-auth.: M.C. Gambetta

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Science. 2021 May 28;372(6545):984-989. doi: 10.1126/science.abe2218.

3D genomics across the tree of life reveals condensin II as a determinant of architecture type

Claire Hoencamp # 1, Olga Dudchenko # 2 3 4, Ahmed M O Elbatsh # 1, Sumitabha Brahmachari # 4, Jonne A Raaijmakers # 5, Tom van Schaik # 6, Ángela Sedeño Cacciatore # 1, Vinícius G Contessoto # 4 7, Roy G H P van Heesbeen # 5, Bram van den Broek 8, Aditya N Mhaskar 1, Hans Teunissen 6, Brian Glenn St Hilaire 2 3, David Weisz 2 3, Arina D Omer 2, Melanie Pham 2, Zane Colaric 2, Zhenzhen Yang 9, Suhas S P Rao 2 3 10, Namita Mitra 2 3, Christopher Lui 2, Weijie Yao 2, Ruqayya Khan 2 3, Leonid L Moroz 11, Andrea Kohn 11, Judy St Leger 12, Alexandria Mena 13, Karen Holcroft 14, Maria Cristina Gambetta 15, Fabian Lim 16, Emma Farley 16, Nils Stein 17 18 19, Alexander Haddad 2, Daniel Chauss 20, Ayse Sena Mutlu 3, Meng C Wang 3 21 22, Neil D Young 23, Evin Hildebrandt 24, Hans H Cheng 24, Christopher J Knight 25, Theresa L U Burnham 26 27, Kevin A Hovel 27, Andrew J Beel 10, Pierre-Jean Mattei 10, Roger D Kornberg 10, Wesley C Warren 28, Gregory Cary 29, José Luis Gómez-Skarmeta 30, Veronica Hinman 31, Kerstin Lindblad-Toh 32 33, Federica Di Palma 34, Kazuhiro Maeshima 35 36, Asha S Multani 37, Sen Pathak 37, Liesl Nel-Themaat 37, Richard R Behringer 37, Parwinder Kaur 19, René H Medema 5, Bas van Steensel 6, Elzo de Wit 6, José N Onuchic 4 38, Michele Di Pierro 4 39, Erez Lieberman Aiden 40 3 4 9 19 32, Benjamin D Rowland 41Affiliations expand

Abstract

We investigated genome folding across the eukaryotic tree of life. We find two types of three-dimensional (3D) genome architectures at the chromosome scale. Each type appears and disappears repeatedly during eukaryotic evolution. The type of genome architecture that an organism exhibits correlates with the absence of condensin II subunits. Moreover, condensin II depletion converts the architecture of the human genome to a state resembling that seen in organisms such as fungi or mosquitoes. In this state, centromeres cluster together at nucleoli, and heterochromatin domains merge. We propose a physical model in which lengthwise compaction of chromosomes by condensin II during mitosis determines chromosome-scale genome architecture, with effects that are retained during the subsequent interphase. This mechanism likely has been conserved since the last common ancestor of all eukaryotes.