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

doi:10.1126/science.abe2218

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 MitraChristopher 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

Genetics

Research output: Contribution to journal › Article › peer-review

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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.

Original language	English (US)
Article number	abe2218
Journal	Science
Volume	372
Issue number	6545
DOIs	https://doi.org/10.1126/science.abe2218
State	Published - May 28 2021

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Hoencamp, C., Dudchenko, O., Elbatsh, A. M. O., Brahmachari, S., Raaijmakers, J. A., van Schaik, T., Cacciatore, Á. S., Contessoto, V. G., van Heesbeen, R. G. H. P., van den Broek, B., Mhaskar, A. N., Teunissen, H., St Hilaire, B. G., Weisz, D., Omer, A. D., Pham, M., Colaric, Z., Yang, Z., Rao, S. S. P., ... Rowland, B. D. (2021). 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science, 372(6545), Article abe2218. https://doi.org/10.1126/science.abe2218

Hoencamp, C, Dudchenko, O, Elbatsh, AMO, Brahmachari, S, Raaijmakers, JA, van Schaik, T, Cacciatore, ÁS, Contessoto, VG, van Heesbeen, RGHP, van den Broek, B, Mhaskar, AN, Teunissen, H, St Hilaire, BG, Weisz, D, Omer, AD, Pham, M, Colaric, Z, Yang, Z, Rao, SSP, Mitra, N, Lui, C, Yao, W, Khan, R, Moroz, LL, Kohn, A, St. Leger, J, Mena, A, Holcroft, K, Gambetta, MC, Lim, F, Farley, E, Stein, N, Haddad, A, Chauss, D, Mutlu, AS, Wang, MC, Young, ND, Hildebrandt, E, Cheng, HH, Knight, CJ, Burnham, TLU, Hovel, KA, Beel, AJ, Mattei, PJ, Kornberg, RD, Warren, WC, Cary, G, Gómez-Skarmeta, JL, Hinman, V, Lindblad-Toh, K, Palma, FD, Maeshima, K, Multani, AS, Pathak, S, Nel-Themaat, L, Behringer, RR, Kaur, P, Medema, RH, van Steensel, B, de Wit, E, Onuchic, JN, Di Pierro, M, Aiden, EL & Rowland, BD 2021, '3D genomics across the tree of life reveals condensin II as a determinant of architecture type', Science, vol. 372, no. 6545, abe2218. https://doi.org/10.1126/science.abe2218

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

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.",

author = "Claire Hoencamp and Olga Dudchenko and Elbatsh, {Ahmed M.O.} and Sumitabha Brahmachari and Raaijmakers, {Jonne A.} and {van Schaik}, Tom and Cacciatore, {{\'A}ngela Sede{\~n}o} and Contessoto, {Vin{\'i}cius G.} and {van Heesbeen}, {Roy G.H.P.} and {van den Broek}, Bram and Mhaskar, {Aditya N.} and Hans Teunissen and {St Hilaire}, {Brian Glenn} and David Weisz and Omer, {Arina D.} and Melanie Pham and Zane Colaric and Zhenzhen Yang and Rao, {Suhas S.P.} and Namita Mitra and Christopher Lui and Weijie Yao and Ruqayya Khan and Moroz, {Leonid L.} and Andrea Kohn and {St. Leger}, Judy and Alexandria Mena and Karen Holcroft and Gambetta, {Maria Cristina} and Fabian Lim and Emma Farley and Nils Stein and Alexander Haddad and Daniel Chauss and Mutlu, {Ayse Sena} and Wang, {Meng C.} and Young, {Neil D.} and Evin Hildebrandt and Cheng, {Hans H.} and Knight, {Christopher J.} and Burnham, {Theresa L.U.} and Hovel, {Kevin A.} and Beel, {Andrew J.} and Mattei, {Pierre Jean} and Kornberg, {Roger D.} and Warren, {Wesley C.} and Gregory Cary and G{\'o}mez-Skarmeta, {Jos{\'e} Luis} and Veronica Hinman and Kerstin Lindblad-Toh and Palma, {Federica Di} and Kazuhiro Maeshima and Multani, {Asha S.} and Sen Pathak and Liesl Nel-Themaat and Behringer, {Richard R.} and Parwinder Kaur and Medema, {Ren{\'e} H.} and {van Steensel}, Bas and {de Wit}, Elzo and Onuchic, {Jos{\'e} N.} and {Di Pierro}, Michele and Aiden, {Erez Lieberman} and Rowland, {Benjamin D.}",

year = "2021",

month = may,

day = "28",

doi = "10.1126/science.abe2218",

language = "English (US)",

volume = "372",

journal = "Science",

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T1 - 3D genomics across the tree of life reveals condensin II as a determinant of architecture type

AU - Hoencamp, Claire

AU - Dudchenko, Olga

AU - Elbatsh, Ahmed M.O.

AU - Brahmachari, Sumitabha

AU - Raaijmakers, Jonne A.

AU - van Schaik, Tom

AU - Cacciatore, Ángela Sedeño

AU - Contessoto, Vinícius G.

AU - van Heesbeen, Roy G.H.P.

AU - van den Broek, Bram

AU - Mhaskar, Aditya N.

AU - Teunissen, Hans

AU - St Hilaire, Brian Glenn

AU - Weisz, David

AU - Omer, Arina D.

AU - Pham, Melanie

AU - Colaric, Zane

AU - Yang, Zhenzhen

AU - Rao, Suhas S.P.

AU - Mitra, Namita

AU - Lui, Christopher

AU - Yao, Weijie

AU - Khan, Ruqayya

AU - Moroz, Leonid L.

AU - Kohn, Andrea

AU - St. Leger, Judy

AU - Mena, Alexandria

AU - Holcroft, Karen

AU - Gambetta, Maria Cristina

AU - Lim, Fabian

AU - Farley, Emma

AU - Stein, Nils

AU - Haddad, Alexander

AU - Chauss, Daniel

AU - Mutlu, Ayse Sena

AU - Wang, Meng C.

AU - Young, Neil D.

AU - Hildebrandt, Evin

AU - Cheng, Hans H.

AU - Knight, Christopher J.

AU - Burnham, Theresa L.U.

AU - Hovel, Kevin A.

AU - Beel, Andrew J.

AU - Mattei, Pierre Jean

AU - Kornberg, Roger D.

AU - Warren, Wesley C.

AU - Cary, Gregory

AU - Gómez-Skarmeta, José Luis

AU - Hinman, Veronica

AU - Lindblad-Toh, Kerstin

AU - Palma, Federica Di

AU - Maeshima, Kazuhiro

AU - Multani, Asha S.

AU - Pathak, Sen

AU - Nel-Themaat, Liesl

AU - Behringer, Richard R.

AU - Kaur, Parwinder

AU - Medema, René H.

AU - van Steensel, Bas

AU - de Wit, Elzo

AU - Onuchic, José N.

AU - Di Pierro, Michele

AU - Aiden, Erez Lieberman

AU - Rowland, Benjamin D.

PY - 2021/5/28

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JO - Science

JF - Science

IS - 6545

M1 - abe2218

ER -

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

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