3D genomics across the tree of life reveals condensin II as a determinant of architecture type.
Claire Hoencamp,
Olga Dudchenko,
Ahmed M O Elbatsh,
Sumitabha Brahmachari,
Jonne A Raaijmakers,
Tom van Schaik,
Ángela Sedeño Cacciatore,
Vinícius G Contessoto,
Roy G H P van Heesbeen,
Bram van den Broek,
Aditya N Mhaskar,
Hans Teunissen,
Brian Glenn St Hilaire,
David Weisz,
Arina D Omer,
Melanie Pham,
Zane Colaric,
Zhenzhen Yang,
Suhas S P Rao,
Namita Mitra,
Christopher Lui,
Weijie Yao,
Ruqayya Khan,
Leonid L Moroz,
Andrea Kohn,
Judy St Leger,
Alexandria Mena,
Karen Holcroft,
Maria Cristina Gambetta,
Fabian Lim,
Emma Farley,
Nils Stein,
Alexander Haddad,
Daniel Chauss,
Ayse Sena Mutlu,
Meng C Wang,
Neil D Young,
Evin Hildebrandt,
Hans H Cheng,
Christopher J Knight,
Theresa L U Burnham,
Kevin A Hovel,
Andrew J Beel,
Pierre-Jean Mattei,
Roger D Kornberg,
Wesley C Warren,
Gregory Cary,
José Luis Gómez-Skarmeta,
Veronica Hinman,
Kerstin Lindblad-Toh,
Federica Di Palma,
Kazuhiro Maeshima,
Asha S Multani,
Sen Pathak,
Liesl Nel-Themaat,
Richard R Behringer,
Parwinder Kaur,
René H Medema,
Bas van Steensel,
Elzo de Wit,
José N Onuchic,
Michele Di Pierro,
Erez Lieberman Aiden,
Benjamin D Rowland
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.