Recent loss of the Dim2 DNA methyltransferase decreases mutation rate in repeats and changes evolutionary trajectory in a fungal pathogen

DNA methylation is found throughout all domains of life, yet the extent and function of DNA methylation differ among eukaryotes. Strains of the plant pathogenic fungus Zymoseptoria tritici appeared to lack cytosine DNA methylation (5mC) because gene amplification followed by Repeat-Induced Point mut...

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Published in:	PLoS genetics Vol. 17; no. 3; p. e1009448
Main Authors:	Möller, Mareike, Habig, Michael, Lorrain, Cécile, Feurtey, Alice, Haueisen, Janine, Fagundes, Wagner C, Alizadeh, Alireza, Freitag, Michael, Stukenbrock, Eva H
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 22-03-2021 Public Library of Science (PLoS)
Subjects:	5-Methylcytosine - metabolism Aegilops Alleles Analysis Ascomycota - classification Ascomycota - enzymology Ascomycota - genetics Ascomycota - isolation & purification Biology and life sciences Chromosomes Control Deoxyribonucleic acid DNA DNA (Cytosine-5-)-Methyltransferase 1 - deficiency DNA (Cytosine-5-)-Methyltransferase 1 - metabolism DNA methylation DNA methyltransferase Enzymes Epigenetics Evolution Evolution, Molecular Fungi Gene amplification Gene expression Gene mutations Gene silencing Genomes Geography Goat grass Mass spectroscopy Methyltransferases Mitosis Mutation Mutation Rate Mutation rates Pathogens Phylogeography Physical Sciences Physiological aspects Quantitative Trait Loci Sibling species Structure Triticum aestivum Germany Iran
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Summary:	DNA methylation is found throughout all domains of life, yet the extent and function of DNA methylation differ among eukaryotes. Strains of the plant pathogenic fungus Zymoseptoria tritici appeared to lack cytosine DNA methylation (5mC) because gene amplification followed by Repeat-Induced Point mutation (RIP) resulted in the inactivation of the dim2 DNA methyltransferase gene. 5mC is, however, present in closely related sister species. We demonstrate that inactivation of dim2 occurred recently as some Z. tritici isolates carry a functional dim2 gene. Moreover, we show that dim2 inactivation occurred by a different path than previously hypothesized. We mapped the genome-wide distribution of 5mC in strains with or without functional dim2 alleles. Presence of functional dim2 correlates with high levels of 5mC in transposable elements (TEs), suggesting a role in genome defense. We identified low levels of 5mC in strains carrying non-functional dim2 alleles, suggesting that 5mC is maintained over time, presumably by an active Dnmt5 DNA methyltransferase. Integration of a functional dim2 allele in strains with mutated dim2 restored normal 5mC levels, demonstrating de novo cytosine methylation activity of Dim2. To assess the importance of 5mC for genome evolution, we performed an evolution experiment, comparing genomes of strains with high levels of 5mC to genomes of strains lacking functional dim2. We found that presence of a functional dim2 allele alters nucleotide composition by promoting C to T transitions (C→T) specifically at CpA (CA) sites during mitosis, likely contributing to TE inactivation. Our results show that 5mC density at TEs is a polymorphic trait in Z. tritici populations that can impact genome evolution.
Bibliography:	new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Department of Biochemistry and Biophysics, Oregon State University, Corvallis, Oregon, United States of America The authors have declared that no competing interests exist.
ISSN:	1553-7404 1553-7390 1553-7404
DOI:	10.1371/journal.pgen.1009448