A D53 repression motif induces oligomerization of TOPLESS corepressors and promotes assembly of a corepressor-nucleosome complex

Ma, Honglei; Duan, Jingbo; Ke, Jiyuan; He, Yuanzheng; Gu, Xin; Xu, Ting-Hai; Yu, Hong; Wang, Yonghong; Brunzelle, Joseph S.; Jiang, Yi; Rothbart, Scott B.; Xu, H. Eric; Li, Jiayang; Melcher, Karsten

doi:10.1126/sciadv.1601217

Title: A D53 repression motif induces oligomerization of TOPLESS corepressors and promotes assembly of a corepressor-nucleosome complex

Journal Article · Fri Jun 02 00:00:00 EDT 2017 · Science Advances

DOI:https://doi.org/10.1126/sciadv.1601217· OSTI ID:1438874

Ma, Honglei ^[1]; Duan, Jingbo ^[2];

^[3]; He, Yuanzheng ^[3]; Gu, Xin ^[3];

^[1];

^[2]; Wang, Yonghong ^[2]; Brunzelle, Joseph S. ^[4]; Jiang, Yi ^[5]; Rothbart, Scott B. ^[3]; Xu, H. Eric ^[1];

^[2];

^[3]

Chinese Academy of Sciences (CAS), Shanghai (China); Van Andel Research Inst., Grand Rapids, MI (United States)
Chinese Academy of Sciences, Beijing (People’s Republic of China)
Van Andel Research Inst., Grand Rapids, MI (United States)
Northwestern Univ., Argonne, IL (United States). Synchrotron Research Center
Chinese Academy of Sciences (CAS), Shanghai (China)

TOPLESS are tetrameric plant corepressors of the conserved Tup1/Groucho/TLE (transducin-like enhancer of split) family. Herein, we show that they interact through their TOPLESS domains (TPDs) with two functionally important ethylene response factor–associated amphiphilic repression (EAR) motifs of the rice strigolactone signaling repressor D53: the universally conserved EAR-3 and the monocot-specific EAR-2. We present the crystal structure of the monocot-specific EAR-2 peptide in complex with the TOPLESS-related protein 2 (TPR2) TPD, in which the EAR-2 motif binds the same TPD groove as jasmonate and auxin signaling repressors but makes additional contacts with a second TPD site to mediate TPD tetramer-tetramer interaction. We validated the functional relevance of the two TPD binding sites in reporter gene assays and in transgenic rice and demonstrate that EAR-2 binding induces TPD oligomerization. Moreover, we demonstrate that the TPD directly binds nucleosomes and the tails of histones H3 and H4. Higher-order assembly of TPD complexes induced by EAR-2 binding markedly stabilizes the nucleosome-TPD interaction. These results establish a new TPD-repressor binding mode that promotes TPD oligomerization and TPD-nucleosome interaction, thus illustrating the initial assembly of a repressor-corepressor-nucleosome complex.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Outstanding Young Scientist Foundation of Chinese Academy of Sciences (CAS); Youth Innovation Promotion Association of Chinese Academy of Sciences (CAS); Van Andel Research Institute; Ministry of Science and Technology (China); National Science Foundation (NSF); National Institutes of Health (NIH); Michigan Economic Development Corporation; Michigan Technology Tri-Corridor; USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357; 2012ZX09301001, 2012CB910403; 2013CB910600; XDB08020303; 2013ZX09507001; 91217311; DK071662; GM102545; GM104212; CA181343; 085P1000817

OSTI ID:: 1438874

Journal Information:: Science Advances, Vol. 3, Issue 6; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 51 works

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Drought Response in Wheat: Key Genes and Regulatory Mechanisms Controlling Root System Architecture and Transpiration Efficiency Kulkarni, Manoj; Soolanayakanahally, Raju; Ogawa, Satoshi Frontiers in Chemistry, Vol. 5 https://doi.org/10.3389/fchem.2017.00106	journal	December 2017
Molecular evolution and diversification of the SMXL gene family Moturu, Taraka Ramji; Thula, Sravankumar; Singh, Ravi Kumar Journal of Experimental Botany, Vol. 69, Issue 9 https://doi.org/10.1093/jxb/ery097	journal	March 2018
Strigolactone promotes cytokinin degradation through transcriptional activation of CYTOKININ OXIDASE/DEHYDROGENASE 9 in rice Duan, Jingbo; Yu, Hong; Yuan, Kun Proceedings of the National Academy of Sciences, Vol. 116, Issue 28 https://doi.org/10.1073/pnas.1810980116	journal	June 2019
Structural plasticity of D3-D14 ubiquitin ligase in strigolactone signalling. Shabek, Nitzan; Ticchiarelli, Fabrizio; Mao, Haibin Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.34020	text	January 2018
Triazole ureas covalently bind to strigolactone receptors and regulate signaling Nakamura, Hidemitsu; Hirabayashi, Kei; Miyakawa, Takuya https://doi.org/10.1101/362830	posted_content	July 2018
Molecular basis of strigolactone perception in root-parasitic plants: aiming to control its germination with strigolactone agonists/antagonists Miyakawa, Takuya; Xu, Yuqun; Tanokura, Masaru Cellular and Molecular Life Sciences, Vol. 77, Issue 6 https://doi.org/10.1007/s00018-019-03318-8	journal	October 2019
Fellowship of the rings: a saga of strigolactones and other small signals Machin, Darren C.; Hamon‐Josse, Maxime; Bennett, Tom New Phytologist, Vol. 225, Issue 2 https://doi.org/10.1111/nph.16135	journal	September 2019
Structural plasticity of D3–D14 ubiquitin ligase in strigolactone signalling Shabek, Nitzan; Ticchiarelli, Fabrizio; Mao, Haibin Nature, Vol. 563, Issue 7733 https://doi.org/10.1038/s41586-018-0743-5	journal	November 2018

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