Lack of the COMPASS Component Ccl1 Reduces H3K4 Trimethylation Levels and Affects Transcription of Secondary Metabolite Genes in Two Plant–Pathogenic Fusarium Species

Studt, Lena; Janevska, Slavica; Arndt, Birgit; Boedi, Stefan; Sulyok, Michael; Humpf, Hans‐Ulrich; Tudzynski, Bettina; Strauss, Joseph

doi:10.3389/fmicb.2016.02144

Cited by 46 publications

(64 citation statements)

References 98 publications

(147 reference statements)

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“…Although disruption of cclA was found to affect growth in several filamentous fungi (Palmer et al , ; Studt et al , ), deletion of cclA as well as overexpression of kdmB did not have an impact on E. festucae development in axenic culture. No changes in morphology or growth rate were observed on PD agar, as well as under salt and pH stress conditions (Fig.…”

Section: Resultsmentioning

confidence: 99%

Regulation of subtelomeric fungal secondary metabolite genes by H3K4me3 regulators CclA and KdmB

Lukito

Chujo

Hale

et al. 2019

Molecular Microbiology

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Summary Studies on the regulation of fungal secondary metabolism highlight the importance of histone H3K4 methylation regulators Set1, CclA (Ash2) and KdmB (KDM5), but it remains unclear whether these proteins act by direct modulation of H3K4me3 at the target genes. In filamentous fungi, secondary metabolite genes are frequently located near telomeres, a site where H3K4 methylation is thought to have a repressive role. Here we analyzed the role of CclA, KdmB and H3K4me3 in regulating the subtelomeric EAS and LTM cluster genes in Epichloë festucae. Depletion of H3K4me3 correlated with transcriptional activation of these genes in ΔcclA, similarly enrichment of H3K4me3 correlated with transcriptional repression of the genes in ΔkdmB which was accompanied by significant reduction in the levels of the agriculturally undesirable lolitrems. These transcriptional changes could only be explained by the alterations in H3K4me3 and not in the subtelomerically‐important marks H3K9me3/K27me3. However, H3K4me3 changes in both mutants were not confined to these regions but occurred genome‐wide, and at other subtelomeric loci there were inconsistent correlations between H3K4me3 enrichment and gene repression. Our study suggests that CclA and KdmB are crucial regulators of secondary metabolite genes, but these proteins likely act via means independent to, or in conjunction with the H3K4me3 mark.

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Section: Resultsmentioning

confidence: 99%

Regulation of subtelomeric fungal secondary metabolite genes by H3K4me3 regulators CclA and KdmB

Lukito

Chujo

Hale

et al. 2019

Molecular Microbiology

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“…This suggests a repressive influence of H3K4me3 on the respective SM gene clusters in the WT background, because this mark was decreased in both Δ set1 and OE:: KDM5 , and accordingly increased in Δ kdm5 genome‐wide. These results are in accordance with a previous study, where we have observed an increase in BIK and FUS biosynthesis (FSR was not tested) upon deletion of CCL1 , also showing reduced levels of H3K4me3 genome‐wide (Studt et al ., ). However, in Δ ccl1 , H3K4me2/me3 levels were not affected at FUS cluster genes, and H3K4me2 was elevated at BIK cluster genes with unchanged H3K4me3 levels (Studt et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…These results are in accordance with a previous study, where we have observed an increase in BIK and FUS biosynthesis (FSR was not tested) upon deletion of CCL1 , also showing reduced levels of H3K4me3 genome‐wide (Studt et al ., ). However, in Δ ccl1 , H3K4me2/me3 levels were not affected at FUS cluster genes, and H3K4me2 was elevated at BIK cluster genes with unchanged H3K4me3 levels (Studt et al ., ). Contrary to this, the Δ set1 mutant showed a complete loss of all detectable H3K4me2 and H3K4me3.…”

Section: Discussionmentioning

confidence: 97%

“…For Δ kdm5 , GA 3 levels were reduced to about 20% in axenic culture, but elevated to about 80% during in planta growth, likely explaining the WT‐like virulence of this strain. Similar phenotypes have also been observed for Δ ccl1 (Studt et al ., ) and Δ sge1 (Michielse et al ., ) mutants before, with SGE1 encoding a global SM regulator in F. fujikuroi . This induction of GA 3 biosynthesis in planta may be mediated by a specific, possibly plant‐derived signal, thereby suggesting a more complex regulation during the infection process as opposed to axenic growth.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, we identified and functionally characterized the COMPASS component Ccl1 in F. fujikuroi and F. graminearum. In both fungi, Ccl1 is a critical factor for efficient genome-wide H3K4 trimethylation by COMPASS and has great impact on SM biosynthesis (Studt et al, 2017). However, the exact mechanism of how COMPASS affects the expression of subtelomeric SM genes in both fungi remains unclear so far.…”

Section: Introductionmentioning

confidence: 99%

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Set1 and Kdm5 are antagonists for H3K4 methylation and regulators of the major conidiation‐specific transcription factor gene ABA1 in Fusarium fujikuroi

Janevska

Güldener

Sulyok

et al. 2018

Environmental Microbiology

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SummaryHere we present the identification and characterization of the H3K4‐specific histone methyltransferase Set1 and its counterpart, the Jumonji C demethylase Kdm5, in the rice pathogen Fusarium fujikuroi. While Set1 is responsible for all detectable H3K4me2/me3 in this fungus, Kdm5 antagonizes the H3K4me3 mark. Notably, deletion of both SET1 and KDM5 mainly resulted in the upregulation of genome‐wide transcription, also affecting a large set of secondary metabolite (SM) key genes. Although H3K4 methylation is a hallmark of actively transcribed euchromatin, several SM gene clusters located in subtelomeric regions were affected by Set1 and Kdm5. While the regulation of many of them is likely indirect, H3K4me2 levels at gibberellic acid (GA) genes correlated with GA biosynthesis in the wild type, Δkdm5 and OE::KDM5 under inducing conditions. Whereas Δset1 showed an abolished GA3 production in axenic culture, phytohormone biosynthesis was induced in planta, so that residual amounts of GA3 were detected during rice infection. Accordingly, Δset1 exhibited a strongly attenuated, though not abolished, virulence on rice. Apart from regulating secondary metabolism, Set1 and Kdm5 function as activator and repressor of conidiation respectively. They antagonistically regulate H3K4me3 levels and expression of the major conidiation‐specific transcription factor gene ABA1 in F. fujikuroi.

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COMPASS core subunits MpSet1 and MpSwd3 regulate Monascus pigments synthesis in Monascus purpureus

Wu,

Gao,

Liu

2024

J Basic Microbiol

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In eukaryotes, methylation of histone H3 at lysine 4 (H3K4me) catalyzed by the complex of proteins associated with Set1 (COMPASS) is crucial for the transcriptional regulation of genes and the development of organisms. In Monascus, the functions of COMPASS in establishing H3K4me remain unclear. This study first identified the conserved COMPASS core subunits MpSet1 and MpSwd3 in Monascus purpureus and confirmed their roles in establishing H3K4me2/3. Loss of MpSet1 and MpSwd3 resulted in slower growth and development and inhibited the formation of cleistothecia, ascospores, and conidia. The loss of these core subunits also decreased the production of extracellular and intracellular Monascus pigments (MPs) by 94.2%, 93.5%, 82.7%, and 82.5%, respectively. In addition, RNA high‐throughput sequencing and quantitative real‐time polymerase chain reaction (qRT‐PCR) showed that the loss of MpSet1 and MpSwd3 altered the expression of 2646 and 2659 genes, respectively, and repressed the transcription of MPs synthesis‐related genes. In addition, the ΔMpset1 and ΔMpswd3 strains demonstrated increased sensitivity to cell wall stress with the downregulation of chitin synthase‐coding genes. These results indicated that the COMPASS core subunits MpSet1 and MpSwd3 help establish H3K4me2/3 for growth and development, spore formation, and pigment synthesis in Monascus. These core subunits also assist in maintaining cell wall integrity.

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Lack of the COMPASS Component Ccl1 Reduces H3K4 Trimethylation Levels and Affects Transcription of Secondary Metabolite Genes in Two Plant–Pathogenic Fusarium Species

Cited by 46 publications

References 98 publications

Regulation of subtelomeric fungal secondary metabolite genes by H3K4me3 regulators CclA and KdmB

Regulation of subtelomeric fungal secondary metabolite genes by H3K4me3 regulators CclA and KdmB

Set1 and Kdm5 are antagonists for H3K4 methylation and regulators of the major conidiation‐specific transcription factor gene ABA1 in Fusarium fujikuroi

COMPASS core subunits MpSet1 and MpSwd3 regulate Monascus pigments synthesis in Monascus purpureus

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