5 Fungal Chromatin and Its Role in Regulation of Gene Expression

Freitag, Michael

doi:10.1007/978-3-642-45218-5_5

“…Luckily, technological advances, especially in high-throughput DNA sequencing, proteomics and nanoscopy, make almost any organism a facile “model”. Chromatin scaffold proteins, like core histones, are ancient and conserved in the fungi [29]. Genes for the enzymes that modify DNA or histones are also largely conserved [14, 18, 26].…”

Section: Chromatin: An Assembly Of Dna Proteins and Rnamentioning

confidence: 99%

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

Erlendson

¹

,

Friedman

²

,

Freitag

³

2017

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Chromatin and chromosomes of fungi are highly diverse and dynamic, even within species. Much of what we know about histone modification enzymes, RNA interference, DNA methylation, and cell cycle control was first addressed in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Aspergillus nidulans and Neurospora crassa. Here, we examine the three landmark regions that are required for maintenance of stable chromosomes and their faithful inheritance, namely origins of DNA replication, telomeres and centromeres. We summarize the state of recent chromatin research that explains what is required for normal function of these specialized chromosomal regions in different fungi, with an emphasis on silencing mechanism associated with subtelomeric regions, initiated by sirtuin histone deacetylases and histone H3 lysine 27 (H3K27) methyltransferases. We explore mechanisms for the appearance of “accessory” or “conditionally dispensable” chromosomes, and contrast what has been learned from studies on genome-wide chromosome conformation capture in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Neurospora crassa and Trichoderma reesei. While most of the current knowledge is based on work in a handful of genetically and biochemically tractable model organisms, we suggest where major knowledge gaps remain to be closed. Fungi will continue to serve as facile organisms to uncover the basic processes of life because they make excellent model organisms for genetics, biochemistry, cell biology and evolutionary biology.

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“…Luckily, technological advances, especially in high-throughput DNA sequencing, proteomics and nanoscopy, make almost any organism a facile "model". Chromatin scaffold proteins, like core histones, are ancient and conserved in the fungi [29]. Genes for the enzymes that modify DNA or histones are also largely conserved [14,18,26].…”

mentioning

confidence: 99%

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

Erlendson

¹

,

Friedman

²

,

Freitag

³

2017

Self Cite

View full text Add to dashboard Cite

Chromatin and chromosomes of fungi are highly diverse and dynamic, even within species. Much of what we know about histone modification enzymes, RNA interference, DNA methylation, and cell cycle control was first addressed in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Aspergillus nidulans and Neurospora crassa. Here, we examine the three landmark regions that are required for maintenance of stable chromosomes and their faithful inheritance, namely origins of DNA replication, telomeres and centromeres. We summarize the state of recent chromatin research that explains what is required for normal function of these specialized chromosomal regions in different fungi, with an emphasis on silencing mechanism associated with subtelomeric regions, initiated by sirtuin histone deacetylases and histone H3 lysine 27 (H3K27) methyltransferases. We explore mechanisms for the appearance of "accessory" or "conditionally dispensable" chromosomes, and contrast what has been learned from studies on genome-wide chromosome conformation capture in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Neurospora crassa and Trichoderma reesei. While most of the current knowledge is based on work in a handful of genetically and biochemically tractable model organisms, we suggest where major knowledge gaps remain to be closed. Fungi will continue to serve as facile organisms to uncover the basic processes of life because they make excellent model organisms for genetics, biochemistry, cell biology and evolutionary biology. CHROMATIN: AN ASSEMBLY OF DNA, PROTEINS, AND RNAChromosomes of fungi are linear segments of DNA, covered by a diverse assembly of RNA and proteins. They contain three landmarks required for function, namely origins for DNA replication, centromeric DNA as attachment points for kinetochores and telomere repeats to circumvent the end replication problem for linear DNA. Because fungi have been excellent model organisms for trail-blazing basic research since the adoption of Neurospora crassa as one of the workhorses for genetics in the 1940s [1], much of the foundation for general knowledge of eukaryotes was first uncovered with fungi, specifically the four species uniquely suited for genetics, biochemistry and genomics, Schizosaccharomyces pombe, Saccharomyces cerevisiae, Aspergillus nidulans, and N. crassa. This has certainly also been true for studies on chromatin and chromosomes.Chromatin, the building material for chromosomes, is an assembly of DNA, proteins and RNA, organized into nucleosome units, most of which contain octamers of canonical core histone proteins [2]. The three landmarks on chromosomes mentioned above, origins of replication, telomeres and centromeres, are characterized by different specialized chromatin modifications, for example DNA base modifications, like cytosine or adenine methylation, and posttranslational modifications of histones, and it is the set of gene silencing modifications at those chromosome landmarks that will be examined here in more detail. Occupancy of proteins binding spec...

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“…In yeast, it was shown that Asf1 promotes histone H3 acetylation at lysine 56 by the histone acetyltransferase Rtt109 [ 57 , 86 , 87 ]. However, while a number of proteins involved in histone modifications have been studied in filamentous fungi [ 29 , 88 ], it is not yet known if ASF1 is required for their function.…”

Section: Discussionmentioning

confidence: 99%

“…In general, chromatin modifiers can mediate changes of the DNA itself, e.g. through methylation, changes in nucleosome positioning, incorporation of histone variants, or numerous histone modifications [ 29 – 32 ]. In recent years, several genes with potential functions in chromatin modification were found to be involved in fruiting body morphogenesis, pointing to an important role for regulatory events at chromatin level in this process [ 33 – 36 ].…”

Section: Introductionmentioning

confidence: 99%

The transcription factor PRO44 and the histone chaperone ASF1 regulate distinct aspects of multicellular development in the filamentous fungus Sordaria macrospora

Schumacher

¹

,

Lütkenhaus

²

,

Altegoer

³

et al. 2018

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BackgroundFungal fruiting bodies are complex three-dimensional structures that are formed to protect and disperse the sexual spores. Their morphogenesis requires the concerted action of numerous genes; however, at the molecular level, the spatio-temporal sequence of events leading to the mature fruiting body is largely unknown. In previous studies, the transcription factor gene pro44 and the histone chaperone gene asf1 were shown to be essential for fruiting body formation in the ascomycete Sordaria macrospora. Both PRO44 and ASF1 are predicted to act on the regulation of gene expression in the nucleus, and mutants in both genes are blocked at the same stage of development. Thus, we hypothesized that PRO44 and ASF1 might be involved in similar aspects of transcriptional regulation. In this study, we characterized their roles in fruiting body development in more detail.ResultsThe PRO44 protein forms homodimers, localizes to the nucleus, and is strongly expressed in the outer layers of the developing young fruiting body. Analysis of single and double mutants of asf1 and three other chromatin modifier genes, cac2, crc1, and rtt106, showed that only asf1 is essential for fruiting body formation whereas cac2 and rtt106 might have redundant functions in this process. RNA-seq analysis revealed distinct roles for asf1 and pro44 in sexual development, with asf1 acting as a suppressor of weakly expressed genes during morphogenesis. This is most likely not due to global mislocalization of nucleosomes as micrococcal nuclease-sequencing did not reveal differences in nucleosome spacing and positioning around transcriptional start sites between Δasf1 and the wild type. However, bisulfite sequencing revealed a decrease in DNA methylation in Δasf1, which might be a reason for the observed changes in gene expression. Transcriptome analysis of gene expression in young fruiting bodies showed that pro44 is required for correct expression of genes involved in extracellular metabolism. Deletion of the putative transcription factor gene asm2, which is downregulated in young fruiting bodies of Δpro44, results in defects during ascospore maturation.ConclusionsIn summary, the results indicate distinct roles for the transcription factor PRO44 and the histone chaperone ASF1 in the regulation of sexual development in fungi.Electronic supplementary materialThe online version of this article (10.1186/s12863-018-0702-z) contains supplementary material, which is available to authorized users.

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5 Fungal Chromatin and Its Role in Regulation of Gene Expression

Cited by 6 publications

References 221 publications

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

The transcription factor PRO44 and the histone chaperone ASF1 regulate distinct aspects of multicellular development in the filamentous fungus Sordaria macrospora

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