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  Destabilization of chromosome structure by histone H3 lysine 27 methylation

Möller, M., Schotanus, K., Soyer, J., Haueisen, J., Happ, K., Stralucke, M., et al. (2019). Destabilization of chromosome structure by histone H3 lysine 27 methylation. PLoS Genetics, 15(4): e1008093. doi:10.1371/journal.pgen.1008093.

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Item Permalink: http://hdl.handle.net/21.11116/0000-0003-710A-3 Version Permalink: http://hdl.handle.net/21.11116/0000-0003-E34D-7
Genre: Journal Article

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 Creators:
Möller, Mareike, Author
Schotanus, Klaas, Author
Soyer, Jessica, Author
Haueisen, Janine1, Author              
Happ, Kathrin1, Author              
Stralucke, Maja1, Author              
Happel, Petra, Author
Smith, Kristina M., Author
Connolly, Lanelle R., Author
Freitag, Michael, Author
Stukenbrock, Eva H.1, Author              
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1Max Planck Fellow Group Environmental Genomics, Max Planck Institute for Evolutionary Biology, Max Planck Society, ou_2068284              

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 Abstract: Chromosome and genome stability are important for normal cell function as instability often correlates with disease and dysfunction of DNA repair mechanisms. Many organisms maintain supernumerary or accessory chromosomes that deviate from standard chromosomes. The pathogenic fungus Zymoseptoria tritici has as many as eight accessory chromosomes, which are highly unstable during meiosis and mitosis, transcriptionally repressed, show enrichment of repetitive elements, and enrichment with heterochromatic histone methylation marks, e.g., trimethylation of H3 lysine 9 or lysine 27 (H3K9me3, H3K27me3). To elucidate the role of heterochromatin on genome stability in Z. tritici, we deleted the genes encoding the methyltransferases responsible for H3K9me3 and H3K27me3, kmt1 and kmt6, respectively, and generated a double mutant. We combined experimental evolution and genomic analyses to determine the impact of these deletions on chromosome and genome stability, both in vitro and in planta. We used whole genome sequencing, ChIP-seq, and RNA-seq to compare changes in genome and chromatin structure, and differences in gene expression between mutant and wildtype strains. Analyses of genome and ChIP-seq data in H3K9me3-deficient strains revealed dramatic chromatin reorganization, where H3K27me3 is mostly relocalized into regions that are enriched with H3K9me3 in wild type. Many genome rearrangements and formation of new chromosomes were found in the absence of H3K9me3, accompanied by activation of transposable elements. In stark contrast, loss of H3K27me3 actually increased the stability of accessory chromosomes under normal growth conditions in vitro, even without large scale changes in gene activity. We conclude that H3K9me3 is important for the maintenance of genome stability because it disallows H3K27me3 in regions considered constitutive heterochromatin. In this system, H3K27me3 reduces the overall stability of accessory chromosomes, generating a “metastable” state for these quasi-essential regions of the genome.

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Language(s): eng - English
 Dates: 2018-11-102019-03-152019-04-22
 Publication Status: Published online
 Pages: -
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 Rev. Method: No review
 Identifiers: DOI: 10.1371/journal.pgen.1008093
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Title: PLoS Genetics
  Other : PLoS Genet.
Source Genre: Journal
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Publ. Info: San Francisco, CA : Public Library of Science
Pages: - Volume / Issue: 15 (4) Sequence Number: e1008093 Start / End Page: - Identifier: ISSN: 1553-7390
CoNE: https://pure.mpg.de/cone/journals/resource/1000000000017180