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

Nassrallah, Amr; Rougée, Martin; Bourbousse, Clara; Drevensek, Stéphanie; Fonseca, Sandra; Iniesto, Elisa; Aït-Mohamed, Ouardia; Deton-Cabanillas, Anne Flore; Zabulon, Gérald; Ahmed, Ikhlak; Stroebel, David; Masson, Vanessa; Lombard, Bérangère; Eeckhout, Dominique; Gevaert, Kris; Loew, Damarys; Genovesio, Auguste; Breyton, Cécile; Jaeger, Geert De; Bowler, Chris; Rubio, Vicente; Barneche, Frédy

doi:10.7554/elife.37892

Cited by 80 publications

(61 citation statements)

References 103 publications

(168 reference statements)

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“…While the FACT complex directly interacts with residues in H3/H4 [68–70], it interacts more strongly with H2A/H2B dimers and is considered a H2A/H2B chaperone in many organisms, including Arabidopsis [71, 72]. To test if chromatin signatures based on H2A/H2B may participate in predisposing exonic sites as TSSs in fact mutants, we analyzed wild-type ChIP-seq data for H2A, ubiquitinylation at H2A lysine 121 (H2AUb), H2B, mono-ubiquitinylation of H2B lysine 120 (H2BUb) and the H2A variant H2A.Z [73–76]. H2A.Z and H2Aub match the profiles of chromatin signatures of promoter TSSs, whereas we detect the strongest H2A signal in exons (S7D–S7F Fig).…”

Section: Resultsmentioning

confidence: 99%

Transcription-driven chromatin repression of Intragenic transcription start sites

et al. 2019

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Progression of RNA polymerase II (RNAPII) transcription relies on the appropriately positioned activities of elongation factors. The resulting profile of factors and chromatin signatures along transcription units provides a “positional information system” for transcribing RNAPII. Here, we investigate a chromatin-based mechanism that suppresses intragenic initiation of RNAPII transcription. We demonstrate that RNAPII transcription across gene promoters represses their function in plants. This repression is characterized by reduced promoter-specific molecular signatures and increased molecular signatures associated with RNAPII elongation. The conserved FACT histone chaperone complex is required for this repression mechanism. Genome-wide Transcription Start Site (TSS) mapping reveals thousands of discrete intragenic TSS positions in fact mutants, including downstream promoters that initiate alternative transcript isoforms. We find that histone H3 lysine 4 mono-methylation (H3K4me1), an Arabidopsis RNAPII elongation signature, is enriched at FACT-repressed intragenic TSSs. Our analyses suggest that FACT is required to repress intragenic TSSs at positions that are in part characterized by elevated H3K4me1 levels. In sum, conserved and plant-specific chromatin features correlate with the co-transcriptional repression of intragenic TSSs. Our insights into TSS repression by RNAPII transcription promise to inform the regulation of alternative transcript isoforms and the characterization of gene regulation through the act of pervasive transcription across eukaryotic genomes.

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Section: Resultsmentioning

confidence: 99%

Transcription-driven chromatin repression of Intragenic transcription start sites

et al. 2019

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“…That DUBm is not always associated with SAGA has been shown in different studies in yeast, Arabidopsis and humans (see a recent revision in [ 38 ]). For instance in Arabidopsis, DUBm association with SAGA is regulated by light, highlighting its dynamic nature in this organism [ 39 ]. However, the precise role of SAGA–CORE subunits in the SAGA–DUBm interaction in vivo is not fully understood.…”

Section: Discussionmentioning

confidence: 99%

SAGA–CORE subunit Spt7 is required for correct Ubp8 localization, chromatin association and deubiquitinase activity

Nuño-Cabanes

García-Molinero

Martín-Expósito

et al. 2020

Epigenetics & Chromatin

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Background Histone H2B deubiquitination is performed by numerous deubiquitinases in eukaryotic cells including Ubp8, the catalytic subunit of the tetrameric deubiquitination module (DUBm: Ubp8; Sus1; Sgf11; Sgf73) of the Spt-Ada-Gcn5 acetyltransferase (SAGA). Ubp8 is linked to the rest of SAGA through Sgf73 and is activated by the adaptors Sus1 and Sgf11. It is unknown if DUBm/Ubp8 might also work in a SAGA-independent manner. Results Here we report that a tetrameric DUBm is assembled independently of the SAGA–CORE components SPT7, ADA1 and SPT20. In the absence of SPT7, i.e., independent of the SAGA complex, Ubp8 and Sus1 are poorly recruited to SAGA-dependent genes and to chromatin. Notably, cells lacking Spt7 or Ada1, but not Spt20, show lower levels of nuclear Ubp8 than wild-type cells, suggesting a possible role for SAGA–CORE subunits in Ubp8 localization. Last, deletion of SPT7 leads to defects in Ubp8 deubiquitinase activity in in vivo and in vitro assays. Conclusions Collectively, our studies show that the DUBm tetrameric structure can form without a complete intact SAGA–CORE complex and that it includes full-length Sgf73. However, subunits of this SAGA–CORE influence DUBm association with chromatin, its localization and its activity.

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“…Monoubiquitination of histone H2B is dynamically regulated and can also be reversed by histone deubiquitinases (Huang and Cochran, 2013). Among the 50 deubiquitination enzymes in Arabidopsis, ubiquitin-specific protease 26 (UBP26), UBP22, and OTLD1 (a putative histone deubiquitinase) are known to target histones H2B (Komander et al, 2009;Isono and Nagel, 2014;Nassrallah et al, 2018). UBP26 acts as a transcriptional repressor involved in seed development, and also acts as a transcriptional activator in flowering by activating FLOWERING LOCUS C (FLC) (Luo et al, 2008;Schmitz et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

“…UBP26 acts as a transcriptional repressor involved in seed development, and also acts as a transcriptional activator in flowering by activating FLOWERING LOCUS C (FLC) (Luo et al, 2008;Schmitz et al, 2009). UBP22, regulated by a light-signaling factor DE-ETIOLATED1, may contribute to the light-dependent control on H2Bub homeostasis and photomorphogenesis (Nassrallah et al, 2018). OTLD1 has been reported to be involved in plant organ growth and development by repressing the expression of GA20OX, WUS, OSR2, ARL, and ABI5, and may associate directly and function together with the KDM1-type lysine demethylases to regulate gene expression (Krichevsky et al, 2011;Keren and Citovsky, 2016).…”

Section: Introductionmentioning

confidence: 99%

Reversible Histone H2B Monoubiquitination Fine-Tunes Abscisic Acid Signaling and Drought Response in Rice

Tang

et al. 2019

Molecular Plant

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Histone H2B monoubiquitination (H2Bub1) plays important roles in several physiological and developmental processes, but its roles in the regulation of plant stress responses remain elusive. Here, we report that H2Bub1 is crucially involved in abscisic acid (ABA) signaling and drought response in rice. We found that rice HISTONE MONOUBIQUITINATION2 (OsHUB2), an E3 ligase for H2Bub1, interacted with OsbZIP46, a key transcription factor regulating ABA signaling and drought response in rice. Genetic analyses suggest that OsHUB2, upregulated by drought and ABA, positively modulates ABA sensitivity and drought resistance. The H2Bub1 levels were increased in the target genes of OsbZIP46 under the drought stress and ABA treatments, which were positively correlated with their increased expression levels. Interestingly, MODD, a reported suppressor of ABA signaling and drought resistance by mediating OsbZIP46 deactivation and degradation, could reduce the H2Bub1 levels in the target genes of OsbZIP46 by recruiting a putative deubiquitinase OsOTLD1. Suppression of OsOTLD1 in vivo resulted in increased H2Bub1 levels and expression of OsbZIP46 target genes. Collectively, these findings established an elaborate mechanism of histone monoubiquitination in the fine-turning of ABA signaling and drought response by balancing H2Bub1 deposition and removal.

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

Cited by 80 publications

References 103 publications

Transcription-driven chromatin repression of Intragenic transcription start sites

Transcription-driven chromatin repression of Intragenic transcription start sites

SAGA–CORE subunit Spt7 is required for correct Ubp8 localization, chromatin association and deubiquitinase activity

Reversible Histone H2B Monoubiquitination Fine-Tunes Abscisic Acid Signaling and Drought Response in Rice

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