The<i>Neurospora crassa</i>White Collar-1 dependent Blue Light Response Requires Acetylation of Histone H3 Lysine 14 by NGF-1

Grimaldi, Benedetto; Coiro, Pierluca; Filetici, Patrizia; Berge, Emanuela; Dobosy, Joseph R.; Freitag, Michael; Selker, Eric U.; Ballario, Paola

doi:10.1091/mbc.e06-03-0232

Cited by 87 publications

(90 citation statements)

References 57 publications

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“…Previously, it was reported that K14 of H3 is an activation mark for light-induced gene expression in the filamentous fungus Neurospora crassa (30). Therefore, by ChIP analysis we studied this modification for the promoter of the sterigmatocystin regulatory gene aflR (Fig.…”

Section: Resultsmentioning

confidence: 99%

Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation

Nützmann

Reyes-Domínguez

Scherlach

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

312

270

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Sequence analyses of fungal genomes have revealed that the potential of fungi to produce secondary metabolites is greatly underestimated. In fact, most gene clusters coding for the biosynthesis of antibiotics, toxins, or pigments are silent under standard laboratory conditions. Hence, it is one of the major challenges in microbiology to uncover the mechanisms required for pathway activation. Recently, we discovered that intimate physical interaction of the important model fungus Aspergillus nidulans with the soil-dwelling bacterium Streptomyces rapamycinicus specifically activated silent fungal secondary metabolism genes, resulting in the production of the archetypal polyketide orsellinic acid and its derivatives. Here, we report that the streptomycete triggers modification of fungal histones. Deletion analysis of 36 of 40 acetyltransferases, including histone acetyltransferases (HATs) of A. nidulans, demonstrated that the Saga/Ada complex containing the HAT GcnE and the AdaB protein is required for induction of the orsellinic acid gene cluster by the bacterium. We also showed that Saga/Ada plays a major role for specific induction of other biosynthesis gene clusters, such as sterigmatocystin, terrequinone, and penicillin. Chromatin immunoprecipitation showed that the Saga/Ada-dependent increase of histone 3 acetylation at lysine 9 and 14 occurs during interaction of fungus and bacterium. Furthermore, the production of secondary metabolites in A. nidulans is accompanied by a global increase in H3K14 acetylation. Increased H3K9 acetylation, however, was only found within gene clusters. This report provides previously undescribed evidence of Saga/Ada dependent histone acetylation triggered by prokaryotes.

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Section: Resultsmentioning

confidence: 99%

Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation

Nützmann

Reyes-Domínguez

Scherlach

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

312

270

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“…However, in N. crassa, mutation of the GCN5 homologue ngf-1 results in loss of repression of the blue-light-responsive al-3 gene in the dark (18). An ngf-1 RIP1 mutant was found to express al-3 constitutively, suggesting that the HAT is involved not only in blue-light FIG.…”

Section: Discussionmentioning

confidence: 99%

“…Recent work in Neurospora crassa established that blue light-induced transcription of the early light-inducible genes al-3 and vvd depends on increased acetylation of histone H3 at lysine K14 (H3K14) in the promoters of these genes (18). The authors showed that acetylation and transient gene activation require the N. crassa GCN5 homologue ngf-1, and it was suggested that the specific activator, White Collar-1, is required for the recruitment of NGF-1 to al-3 and vvd promoters.…”

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confidence: 99%

Nucleosome Positioning and Histone H3 Acetylation Are Independent Processes in the Aspergillus nidulans prnD-prnB Bidirectional Promoter

Reyes-Domínguez

Narendja²,

Berger³

et al. 2008

Eukaryot Cell

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In Aspergillus nidulans, proline can be used as a carbon and nitrogen source, and its metabolism requires the integration of three signals, including proline induction and nitrogen and carbon metabolite derepression. We have previously shown that the bidirectional promoter in the prnD-prnB intergenic region undergoes drastic chromatin rearrangements such that proline induction leads to the loss of positioned nucleosomes, whereas simultaneous carbon and nitrogen metabolite repression results in the partial repositioning of these nucleosomes. In the proline cluster, the inhibition of deacetylases by trichostatin A leads to partial derepression and is associated with a lack of nucleosome positioning. Here, we investigate the effect of histone acetylation in the proline cluster using strains deleted of essential components of putative A. nidulans histone acetyltransferase complexes, namely, gcnE and adaB, the orthologues of the Saccharomyces cerevisiae GCN5 and ADA2 genes, respectively. Surprisingly, GcnE and AdaB are not required for transcriptional activation and chromatin remodeling but are required for the repression of prnB and prnD and for the repositioning of nucleosomes in the divergent promoter region. Chromatin immunoprecipitation directed against histone H3 lysines K9 and K14 revealed that GcnE and AdaB participate in increasing the acetylation level of at least one nucleosome in the prnD-prnB intergenic region during activation, but these activities do not determine nucleosome positioning. Our results are consistent with a function of GcnE and AdaB in gene repression of the proline cluster, probably an indirect effect related to the function of CreA, the DNA-binding protein mediating carbon catabolite repression in A. nidulans.In eukaryotic cells, the acetylation of histones is correlated with both transcriptional activation and the chromatin rearrangements usually associated with it. A turning point in our understanding of the mechanism of histone acetylation was the demonstration of the intrinsic acetylase activity of the Tetrahymena pyriformis p55 protein (7), the homologue of the Saccharomyces cerevisiae Gcn5p protein, which was already known to be involved in the transcriptional activation of a number of genes in this organism (reviewed in reference 33). Homologues, possibly orthologues, of Gcn5p, are universally present in eukaryotes. Gcn5p and its homologues interact with chromatin in large multiprotein complexes, such as ADA and SAGA (17). SAGA is a multiprotein complex whose Gcn5p subunit possesses histone acetyltransferase (HAT) activity. Gcn5p acetylates several lysine residues on the N termini of histones, including K9 and K14 on histone H3 and K8 and K16 on histone H4 (21). The Gcn5-containing complexes share several subunits, such as Ada2p, Ada3p, Spt3p, and Tra1p (24), and it has been estimated that the yeast SAGA complex regulates the expression of ϳ10% of S. cerevisiae genes, with approximately one-third of them being negatively regulated (23). Gcn5p forms a ternary complex with Ada2p an...

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“…Changes in chromatin structure may lead to short-or long-term alterations of the transcriptional activities of genes, and thus they are crucial for cell differentiation, metabolite production (126), and environmental adaptation (127). Epigenetic and chromatin rearrangement data obtained for higher eukaryotes or microorganisms such as yeast are often not applicable to filamentous fungi.…”

Section: Chromatin Structure Rearrangement and Histone Modificationmentioning

confidence: 99%

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

Schmoll

Dattenböck

Carreras-Villaseñor

et al. 2016

Microbiol Mol Biol Rev

163

195

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SUMMARYThe genusTrichodermacontains fungi with high relevance for humans, with applications in enzyme production for plant cell wall degradation and use in biocontrol. Here, we provide a broad, comprehensive overview of the genomic content of these species for “hot topic” research aspects, including CAZymes, transport, transcription factors, and development, along with a detailed analysis and annotation of less-studied topics, such as signal transduction, genome integrity, chromatin, photobiology, or lipid, sulfur, and nitrogen metabolism inT. reesei,T. atroviride, andT. virens, and we open up new perspectives to those topics discussed previously. In total, we covered more than 2,000 of the predicted 9,000 to 11,000 genes of eachTrichodermaspecies discussed, which is >20% of the respective gene content. Additionally, we considered available transcriptome data for the annotated genes. Highlights of our analyses include overall carbohydrate cleavage preferences due to the different genomic contents and regulation of the respective genes. We found light regulation of many sulfur metabolic genes. Additionally, a new Golgi 1,2-mannosidase likely involved inN-linked glycosylation was detected, as were indications for the ability ofTrichodermaspp. to generate hybrid galactose-containingN-linked glycans. The genomic inventory of effector proteins revealed numerous compounds unique toTrichoderma, and these warrant further investigation. We found interesting expansions in theTrichodermagenus in several signaling pathways, such as G-protein-coupled receptors, RAS GTPases, and casein kinases. A particularly interesting feature absolutely unique toT. atrovirideis the duplication of the alternative sulfur amino acid synthesis pathway.

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TheNeurospora crassaWhite Collar-1 dependent Blue Light Response Requires Acetylation of Histone H3 Lysine 14 by NGF-1

Cited by 87 publications

References 57 publications

Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation

Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation

Nucleosome Positioning and Histone H3 Acetylation Are Independent Processes in the Aspergillus nidulans prnD-prnB Bidirectional Promoter

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

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