Sharing Marks: H3K4 Methylation and H2B Ubiquitination as Features of Meiotic Recombination and Transcription

Serrano-Quílez, Joan; Roig-Soucase, Sergi; Rodrı́guez-Navarro, Susana

doi:10.3390/ijms21124510

Cited by 13 publications

(10 citation statements)

References 165 publications

(238 reference statements)

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“…2) . H3K4me3 has been put forward as a regulator of DSB formation, promoting meiotic recombination in some eukaryotes (Tock and Henderson, 2018;Serrano-Quílez et al, 2020). In the MTS of S. pombe, the lysine-specific demethylases Lsd1/Lsd2 are recruited to the mat1 locus and involved in imprint formation (Holmes et al, 2012;Raimondi et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Euchromatin factors HULC and Set1C affect heterochromatin organization and mating-type switching in fission yeast <i>Schizosaccharomyces pombe</i>

et al. 2022

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Mating-type (P or M) of fission yeast Schizosaccharomyces pombe is determined by the transcriptionally active mat1 cassette and is switched by gene conversion using a donor, either mat2 or mat3, located in an adjacent heterochromatin region (mating-type switching; MTS). In the switching process, heterochromatic donors of genetic information are selected based on the P or M cell type and on the action of two recombination enhancers, SRE2 promoting the use of mat2-P and SRE3 promoting the use of mat3-M, leading to replacement of the content of the expressed mat1 cassette. Recently, we found that the histone H3K4 methyltransferase complex Set1C participates in donor selection, raising the question of how a complex best known for its effects in euchromatin controls recombination in heterochromatin. Here, we report that the histone H2BK119 ubiquitin ligase complex HULC functions with Set1C in MTS, as mutants in the shf1, brl1, brl2 and rad6 genes showed defects similar to Set1C mutants and belonged to the same epistasis group as set1Δ. Moreover, using H3K4R and H2BK119R histone mutants and a Set1-Y897A catalytic mutant, we found that ubiquitylation of histone H2BK119 by HULC and methylation of histone H3K4 by Set1C are functionally coupled in MTS. Cell-type biases in MTS in these mutants suggested that HULC and Set1C inhibit the use of the SRE3 recombination enhancer in M cells, thus favoring SRE2 and mat2-P. Consistent with this, imbalanced switching in the mutants was traced to compromised association of the directionality factor Swi6 with the recombination enhancers in M cells. Based on their known effects at other chromosomal locations, we speculate that HULC and Set1C control nucleosome mobility and strand invasion near the SRE elements. In addition, we uncovered distinct effects of HULC and Set1C on histone H3K9 methylation and gene silencing, consistent with additional functions in the heterochromatic domain.

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Section: Discussionmentioning

confidence: 99%

Euchromatin factors HULC and Set1C affect heterochromatin organization and mating-type switching in fission yeast <i>Schizosaccharomyces pombe</i>

et al. 2022

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“…2) (Maki et al 2018). H3K4me3 has been put forward as a regulator of DSB formation promoting meiotic recombination in some eukaryotes (Serrano-Quilez et al 2020; Tock and Henderson 2018). In the MTS of S. pombe , the lysine specific demethylases, Lsd1/Lsd2, are recruited to the mat1 locus and involved in imprint formation (Holmes et al 2012; Raimondi et al 2018).…”

Section: Discussionmentioning

confidence: 99%

Euchromatin factors HULC and Set1C affect heterochromatin organization for mating-type switching in fission yeastSchizosaccharomyces pombe

Chavez

Maki

Tsubouchi

et al. 2021

Preprint

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Mating-type switching (MTS) in fission yeast Schizosaccharomyces pombe is a highly regulated gene conversion event. In the process, heterochromatic donors of genetic information are selected based on the P or M cell type and on the use of two recombination enhancers, SRE2 promoting use of mat2-P and SRE3 promoting use of mat3-M. Recently, we found that the histone H3K4 methyltransferase complex Set1C participates in donor selection, raising the question of how a complex best known for its effects in euchromatin controls recombination in heterochromatin. Here, we report that the histone H2BK119 ubiquitin ligase complex HULC functions with Set1C in MTS, as mutants in the shf1, brl1, brl2 and rad6 genes showed defects similar to Set1C mutants and belonged to the same epistasis group as set1Δ. Moreover, using H3K4R and H2BK119R histone mutants and a Set1-Y897A catalytic mutant indicated that ubiquitylation of histone H2BK119 by HULC and methylation of histone H3K4 by Set1C are functionally coupled in MTS. Cell-type biases in mutants further showed that the regulation might be by inhibiting use of the SRE3 enhancer in M cells, in favor of SRE2. Consistently, imbalanced switching in the mutants was traced to compromised association of the directionality factor Swi6 with the recombination enhancers in M cells. Based on their known effects at other chromosomal locations, we speculate that HULC and Set1C might control nucleosome mobility and strand invasion near the SRE elements. In addition, we uncovered distinct effects of HULC and Set1C on histone H3K9 methylation and gene silencing, consistent with additional functions in the heterochromatic domain.

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“…The histone acetyltransferase (HAT) module binds histone (H) 3 lysine (K) di-and trimethylated histones and preferentially acetylates H3K9 and H3K14, which leads to gene activation [2][3][4][5]. The deubiquitinase (DUB) module removes H2BK123ub, which directly affects transcription elongation and indirectly affects other histone modifications [6,7]. The other two modules have no described enzymatic function.…”

Section: Introductionmentioning

confidence: 99%

The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters

Soffers

Alcántara

et al. 2021

Preprint

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The Spt/Ada-Gcn5 Acetyltransferase (SAGA) coactivator complex has multiple modules with different enzymatic and non-enzymatic functions. How each module contributes to gene activation in specific biological contexts is not well understood. Here we analyzed the role of the non-enzymatic core module during Drosophila oogenesis. We show that depletion of several SAGA-specific subunits belonging to the core module blocked egg chamber development during mid-oogenesis stages, resulting in stronger phenotypes than those obtained after depletion of SAGA’s histone acetyltransferase module or deubiquitination module. These results, as well as additional genetic analyses pointing to an interaction with TBP, suggested a differential role of SAGA modules at different promoter types. However, SAGA subunits co-occupied all promoter types of active genes in ChIP-seq and ChIP-nexus experiments. Thus, the SAGA complex appears to occupy promoters in its entirety, consistent with the strong biochemical integrity of the complex. The high-resolution genomic binding profiles are congruent with SAGA recruitment by activators upstream of the start site, and retention on chromatin by interactions with modified histones downstream of the start site. The stronger genetic requirement of the core module during oogenesis may therefore be explained through its interaction with TBP or its role in recruiting the enzymatic modules to the promoter. We propose the handyman principle, which posits that a distinct genetic requirement for specific components may conceal the fact that the entire complex is physically present.

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Sharing Marks: H3K4 Methylation and H2B Ubiquitination as Features of Meiotic Recombination and Transcription

Cited by 13 publications

References 165 publications

Euchromatin factors HULC and Set1C affect heterochromatin organization and mating-type switching in fission yeast <i>Schizosaccharomyces pombe</i>

Euchromatin factors HULC and Set1C affect heterochromatin organization and mating-type switching in fission yeast <i>Schizosaccharomyces pombe</i>

Euchromatin factors HULC and Set1C affect heterochromatin organization for mating-type switching in fission yeastSchizosaccharomyces pombe

The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters

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