DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis

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Abstract

DE-ETIOLATED 1 (DET1) is an evolutionarily conserved component of the ubiquitination machinery that mediates the destabilization of key regulators of cell differentiation and proliferation in multicellular organisms. In this study, we provide evidence from Arabidopsis that DET1 is essential for the regulation of histone H2B monoubiquitination (H2Bub) over most genes by controlling the stability of a deubiquitination module (DUBm). In contrast with yeast and metazoan DUB modules that are associated with the large SAGA complex, the Arabidopsis DUBm only comprises three proteins (hereafter named SGF11, ENY2 and UBP22) and appears to act independently as a major H2Bub deubiquitinase activity. Our study further unveils that DET1-DDB1-Associated-1 (DDA1) protein interacts with SGF11 in vivo, linking the DET1 complex to light-dependent ubiquitin-mediated proteolytic degradation of the DUBm. Collectively, these findings uncover a signaling path controlling DUBm availability, potentially adjusting H2Bub turnover capacity to the cell transcriptional status.

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Targeted destabilization of HY5 during light-regulated development of Arabidopsis.

M T Osterlund, C. S. Hardtke, N. Wei … (2000)

Arabidopsis seedlings display contrasting developmental patterns depending on the ambient light. Seedlings grown in the light develop photomorphogenically, characterized by short hypocotyls and expanded green cotyledons. In contrast, seedlings grown in darkness become etiolated, with elongated hypocotyls and dosed cotyledons on an apical hook. Light signals, perceived by multiple photoreceptors and transduced to downstream regulators, dictate the extent of photomorphogenic development in a quantitative manner. Two key downstream components, COP1 and HY5, act antagonistically in regulating seedling development. HY5 is a bZIP transcription factor that binds directly to the promoters of light-inducible genes, promoting their expression and photomorphogenic development. COP1 is a RING-finger protein with WD-40 repeats whose nuclear abundance is negatively regulated by light. COP1 interacts directly with HY5 in the nucleus to regulate its activity negatively. Here we show that the abundance of HY5 is directly correlated with the extent of photomorphogenic development, and that the COP1-HY5 interaction may specifically target HY5 for proteasome-mediated degradation in the nucleus.

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Photoreceptor signaling networks in plant responses to shade.

Jorge Casal (2013)

The dynamic light environment of vegetation canopies is perceived by phytochromes, cryptochromes, phototropins, and UV RESISTANCE LOCUS 8 (UVR8). These receptors control avoidance responses to preclude exposure to limiting or excessive light and acclimation responses to cope with conditions that cannot be avoided. The low red/far-red ratios of shade light reduce phytochrome B activity, which allows PHYTOCHROME INTERACTING FACTORS (PIFs) to directly activate the transcription of auxin-synthesis genes, leading to shade-avoidance responses. Direct PIF interaction with DELLA proteins links gibberellin and brassinosteroid signaling to shade avoidance. Shade avoidance also requires CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1), a target of cryptochromes, phytochromes, and UVR8. Multiple regulatory loops and the input of the circadian clock create a complex network able to respond even to subtle threats of competition with neighbors while still compensating for major environmental fluctuations such as the day-night cycles.

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FACT facilitates transcription-dependent nucleosome alteration.

Rimma Belotserkovskaya, Sangtaek Oh, Vladimir Bondarenko … (2003)

The FACT (facilitates chromatin transcription) complex is required for transcript elongation through nucleosomes by RNA polymerase II (Pol II) in vitro. Here, we show that FACT facilitates Pol II-driven transcription by destabilizing nucleosomal structure so that one histone H2A-H2B dimer is removed during enzyme passage. We also demonstrate that FACT possesses intrinsic histone chaperone activity and can deposit core histones onto DNA. Importantly, FACT activity requires both of its constituent subunits and is dependent on the highly acidic C terminus of its larger subunit, Spt16. These findings define the mechanism by which Pol II can transcribe through chromatin without disrupting its epigenetic status.

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Author and article information

Contributors

Martin Rougée

Sandra Fonseca:

ORCID: http://orcid.org/0000-0002-2021-4482

Ouardia Ait-Mohamed

Anne-Flore Deton-Cabanillas

Gerald Zabulon

David Stroebel

Vanessa Masson

Berangere Lombard

Dominique Eeckhout

Kris Gevaert

Damarys Loew

Auguste Genovesio

Geert de Jaeger

Chris Bowler:

ORCID: https://orcid.org/0000-0003-3835-6187

Vicente Rubio:

ORCID: http://orcid.org/0000-0002-8800-2400

Fredy Barneche:

ORCID: http://orcid.org/0000-0002-7014-7097

Christian S Hardtke: Role: Senior Editor

Richard Amasino: Role: Reviewing Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 07 September 2018

Publication date Collection: 2018

Volume: 7

Electronic Location Identifier: e37892

Affiliations

[1 ]Centro Nacional de Biotecnología Darwin MadridSpain

[2 ]deptInstitut de biologie de l’Ecole normale supérieure (IBENS) Ecole normale supérieure, CNRS, INSERM, Université PSL ParisFrance

[3 ]Université Paris-Sud OrsayFrance

[4 ]deptCentre de Recherche, Laboratoire de Spectrométrie de Masse Protéomique Institut Curie PSL Research University 75005 ParisFrance

[5 ]deptDepartment of Plant Systems Biology VIB-Ghent University Technologiepark GhentBelgium

[6 ]VIB Center for Plant Systems Biology GhentBelgium

[7 ]deptDepartment of Biochemistry Ghent University GhentBelgium

[8 ]VIB Center for Medical Biotechnology GhentBelgium

[9 ]Université Grenoble Alpes, Institut de Biologie Structurale GrenobleFrance

University of Lausanne Switzerland

University of Wisconsin United States

United Kingdom

University of Regensburg Germany

Author notes

[‡]

Biochemistry Department, Faculty of Agriculture, Cairo University, Giza, Egypt.

[§]

Institut of Plant Sciences Paris-Saclay (IPS2), UMR 9213/UMR1403, CNRS, INRA, Université Paris-Sud, Université d’Evry, Université Paris-Diderot, Paris, France.

[#]

Salk Institute for Biological Studies, La Jolla, United States.

[¶]

Weill Cornell Medicine - Qatar (WCM-Q) Education City, Doha, Qatar.

[†]

These authors contributed equally to this work.

Author information

Amr Nassrallah https://orcid.org/0000-0002-2229-2855

Sandra Fonseca http://orcid.org/0000-0002-2021-4482

Elisa Iniesto http://orcid.org/0000-0003-1662-7361

Chris Bowler https://orcid.org/0000-0003-3835-6187

Vicente Rubio http://orcid.org/0000-0002-8800-2400

Fredy Barneche http://orcid.org/0000-0002-7014-7097

Article

Publisher ID: 37892

DOI: 10.7554/eLife.37892

PMC ID: 6128693

PubMed ID: 30192741

SO-VID: 94347f87-eaad-46fc-9d28-2ede7fd2c6c9

License:

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 26 April 2018

Date accepted : 22 August 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: ANR-11-JSV2-003-01

Award Recipient : Fredy Barneche

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: ANR-10-LABX-54

Award Recipient : Chris Bowler

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: ANR-10-IDEX-0001-02

Award Recipient : Chris Bowler

Funded by: Université Paris-Sud;

Award ID: PhD Fellowship

Award Recipient : Martin Rougée

Funded by: Université Paris-Sud;

Award ID: PhD Fellowship

Award Recipient : Clara Bourbousse

Funded by: FundRef http://dx.doi.org/10.13039/501100003329, Ministerio de Economía y Competitividad;

Award ID: Grant BIO2013-46539-R

Award Recipient : Vicente Rubio

Funded by: Agencia Estatal de Investigacíon/Fondo Europeo de Desarollo regional/European Union;

Award ID: Grant BIO2016-80551-R

Award Recipient : Vicente Rubio

Funded by: Fundación Bancaria Caixa d'Estalvis i Pensions de Barcelona;

Award ID: PhD Fellowship

Award Recipient : Amr Nassrallah

Funded by: FundRef http://dx.doi.org/10.13039/501100003329, Ministerio de Economía y Competitividad;

Award ID: PhD Fellowship

Award Recipient : Elisa Iniesto

Funded by: FundRef http://dx.doi.org/10.13039/501100003329, Ministerio de Economía y Competitividad;

Award ID: Ramón y Cajal grant RYC-2014-16308

Award Recipient : Sandra Fonseca

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Custom metadata

Author impact statement Light signaling components interact with a histone H2B deubiquitination module, adjusting chromatin states at global level during Arabidopsis seedling development.

ScienceOpen disciplines: Life sciences

Keywords: epigenome,histone h2b deubiquitination,light signaling,det1,saga complex,photomorphogenesis,a. thaliana

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: epigenome, histone h2b deubiquitination, light signaling, det1, saga complex, photomorphogenesis, a. thaliana

DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis

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Abstract

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Arabidopsis genomics

Most cited references 75

Targeted destabilization of HY5 during light-regulated development of Arabidopsis.

Photoreceptor signaling networks in plant responses to shade.

FACT facilitates transcription-dependent nucleosome alteration.

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