Local Rather than Global H3K27me3 Dynamics Are Associated with Differential Gene Expression in Verticillium dahliae

Kramer, Holger; Seidl, Michael; Thomma, Bart P.H.J.; Cook, David E.

doi:10.1128/mbio.03566-21

Cited by 17 publications

(40 citation statements)

References 66 publications

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“…Whenever environmental or internal cues are required, additional factors are expected to be necessary to complete this feedback to establish and maintain H3K27me3 occupancy. For example, those genes encoding secondary metabolites and effectors from pathogenic fungi are usually associated with H3K27me3 occupancy (Zhang et al ., 2021; Kramer et al ., 2022; Moser Tralamazza et al ., 2022). They are transcriptionally silenced in the ex planta growth stage and are highly expressed during in planta growth stage, whereas altered transcription is tightly associated with dynamics of histone modification (Zhang et al ., 2021).…”

Section: Discussionmentioning

confidence: 99%

The additional PRC2 subunit and Sin3 histone deacetylase complex are required for the normal distribution of H3K27me3 occupancy and transcriptional silencing in Magnaporthe oryzae

Lin

Shi

et al. 2022

New Phytologist

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Development in higher organisms requires proper gene silencing, partially achieved through trimethylation of lysine 27 on histone H3 (H3K27me3). However, how the normal distribution of this modification is established and maintained and how it affects gene expression remains unclear, especially in fungi. Polycomb repressive complex 2 (PRC2) catalyses H3K27me3 to assemble transcriptionally repressed facultative heterochromatin and is crucial in animals, plants, and fungi.Here, we report on the critical role of an additional PRC2 subunit in the normal distribution of H3K27me3 occupancy and the stable maintenance of gene repression in the rice fungal pathogen Magnaporthe oryzae. P55, identified as an additional PRC2 subunit, is physically associated with core subunits of PRC2 and is required for a complete level of H3K27me3 modification.Loss of P55 caused severe global defects in the normal distribution of H3K27me3 and transcriptional reprogramming on the H3K27me3-occupied genes. Furthermore, we found that the Sin3 histone deacetylase complex was required to sustain H3K27me3 occupancy and stably maintain gene repression by directly interacting with P55.Our results revealed a novel mechanism by which P55 and Sin3 participate in the normal distribution of facultative heterochromatic modifications and the stable maintenance of gene repression in eukaryotes.

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Section: Discussionmentioning

confidence: 99%

The additional PRC2 subunit and Sin3 histone deacetylase complex are required for the normal distribution of H3K27me3 occupancy and transcriptional silencing in Magnaporthe oryzae

Lin

Shi

et al. 2022

New Phytologist

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“…The copyright holder for this preprint this version posted December 3, 2022. ; https://doi.org/10.1101/2022.12.01.518749 doi: bioRxiv preprint (23,43). Interestingly, S. pombe lost both Polycomb silencing and 5mC but still develops epimutations based on H3K9me heterochromatin -triggered by sRNAs-to acquire drug resistance (44).…”

Section: Discussionmentioning

confidence: 99%

“…This is not the only relevant transcription-repressive modification lost in these fungi, because the majority of Mucorales also lack DNA 5mC methyltransferases. These mechanisms have been reported as essential for epimutations governing effector expression during host colonization in several plant pathogens (23, 43). Interestingly, S. pombe lost both Polycomb silencing and 5mC but still develops epimutations based on H3K9me heterochromatin –triggered by sRNAs– to acquire drug resistance (44).…”

Section: Discussionmentioning

confidence: 99%

“…During host infection, epimutations persist and are induced in specific organs, suggesting a role in pathogenesis (42). Epimutations that promote drug resistance and host colonization pose a concern both for public health and agriculture (24,37,(43)(44)(45), as they could elude detection due to their transient, unstable nature. Therefore, it is critical to elucidate the repertoire of epigenetic modifications these pathogens deploy, and how these pathways operate and interact to modify gene expression in response to environmental cues.…”

Section: Introductionmentioning

confidence: 99%

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Heterochromatin and RNAi act independently to ensure genome stability in Mucorales human fungal pathogens

Navarro-Mendoza

Pérez-Arques

Heitman

2022

Preprint

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Chromatin modifications play a fundamental role in controlling transcription and genome stability and yet despite their importance, are poorly understood in early-diverging fungi. We present the first comprehensive study of histone-lysine and DNA methyltransferases across the Mucoromycota, uncovering H3K9-methylated heterochromatin as the major chromatin modification repressing transcription in these fungi, which lack both Polycomb silencing and cytosine methylation. Although RNA interference (RNAi) facilitates the formation of heterochromatin in many eukaryotic organisms, we show that RNAi is not required to maintain either genomic or centromeric heterochromatin in Mucor. H3K9-methylation and RNAi act independently to control centromeric regions, suggesting a functional sub-specialization. Whereas the H3K9 methyltransferase Clr4 and heterochromatin formation are essential for cell viability, RNAi is dispensable for viability yet acts as the main epigenetic, regulatory force repressing transposition of GremLINE1 elements. Mutations inactivating canonical RNAi lead to rampant transposition and insertional inactivation of targets resulting in antimicrobial drug resistance. This fine-tuned, Rdrp2-dependent RNAi activity is critical for genome stability, restricting GremLINE1 transposable elements to the centromeres where they occupy long heterochromatic islands. Taken together, our results suggest that RNAi and heterochromatin formation are independent genome defense and regulatory mechanisms in the Mucorales, contributing to a paradigm shift from the co-transcriptional gene silencing observed in fission yeasts to models in which heterochromatin and RNAi operate independently in early-diverging basal fungi.

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“…Histone methylation is an important epigenetic modification that can regulate gene expression and mainly occurs at the lysine residues of histones [ 15 , 16 ]. The trimethylation of histone H3 lysine 27 (H3K27me3) modification is mainly regulated dynamically by intracellular lysine methyltransferases and demethylases [ 17 , 18 ].…”

Section: Introductionmentioning

confidence: 99%

Hypoxic condition induced H3K27me3 modification of the LncRNA Tmem235 promoter thus supporting apoptosis of BMSCs

et al. 2022

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Bone marrow mesenchymal stem cells (BMSCs) have strong regenerative potential and show good application prospects for treating clinical diseases. However, in the process of BMSC transplantation for treating ischemic and hypoxic diseases, BMSCs have high rates of apoptosis in the hypoxic microenvironment of transplantation, which significantly affects the transplantation efficacy. Our previous studies have confirmed the key role of long non-coding RNA Tmem235 (LncRNA Tmem235) in the process of hypoxia-induced BMSC apoptosis and its downstream regulatory mechanism, but the upstream mechanism by which hypoxia regulates LncRNA Tmem235 expression to induce BMSC apoptosis is still unclear. Under hypoxic conditions, we found that the level of LncRNA Tmem235 promoter histone H3 lysine 27 trimethylation modification (H3K27me3) was significantly increased by CHIP-qPCR. Moreover, H3K27me3 cooperated with LncRNA Tmem235 promoter DNA methylation to inhibit the expression of LncRNA Tmem235 and promote apoptosis of BMSCs. To study the mechanism of hypoxia-induced modification of LncRNA Tmem235 promoter H3K27me3 in the hypoxia model of BMSCs, we detected the expression of H3K27 methylase and histone demethylase and found that only histone methylase enhancer of zeste homolog 2 (EZH2) expression was significantly upregulated. Knockdown of EZH2 significantly decreased the level of H3K27me3 modification in the LncRNA Tmem235 promoter. The EZH2 promoter region contains a hypoxia-responsive element (HRE) that interacts with hypoxia-inducible factor-1alpha (HIF-1α), which is overexpressed under hypoxic conditions, thereby promoting its overexpression. In summary, hypoxia promotes the modification of the LncRNA Tmem235 promoter H3K27me3 through the HIF-1α/EZH2 signaling axis, inhibits the expression of LncRNA Tmem235, and leads to hypoxic apoptosis of BMSCs. Our findings improve the regulatory mechanism of LncRNA Tmem235 during hypoxic apoptosis of BMSCs and provide a more complete theoretical pathway for targeting LncRNA to inhibit hypoxic apoptosis of BMSCs.

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Local Rather than Global H3K27me3 Dynamics Are Associated with Differential Gene Expression in Verticillium dahliae

Cited by 17 publications

References 66 publications

The additional PRC2 subunit and Sin3 histone deacetylase complex are required for the normal distribution of H3K27me3 occupancy and transcriptional silencing in Magnaporthe oryzae

The additional PRC2 subunit and Sin3 histone deacetylase complex are required for the normal distribution of H3K27me3 occupancy and transcriptional silencing in Magnaporthe oryzae

Heterochromatin and RNAi act independently to ensure genome stability in Mucorales human fungal pathogens

Hypoxic condition induced H3K27me3 modification of the LncRNA Tmem235 promoter thus supporting apoptosis of BMSCs

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