Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria

Feurtey, Alice; Lorrain, Cécile; Croll, Daniel; Eschenbrenner, Christoph; Freitag, Michael; Habig, Michael; Haueisen, Janine; Möller, Mareike; Schotanus, Klaas; Stukenbrock, Eva H.

doi:10.1186/s12864-020-06871-w

Cited by 38 publications

(49 citation statements)

References 83 publications

(140 reference statements)

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“…One SMRT cell was sequenced per genome. Genome assemblies were performed as described [71]. Genome assembly statistics are summarized in Table S7.…”

Section: Smrt Sequencing and Assembly Of Iranian Isolates Zt289 And Zmentioning

confidence: 99%

“…We annotated transposable elements with the REPET pipeline (https://urgi.versailles.inra.fr/Tools/REPET) [72] as described in [71]. Briefly, we identified repetitive element consensus sequences in each genome using TEdenovo following the developer's recommendations [72].…”

Section: Identification Of Tes and Analysis Of Te Expressionmentioning

confidence: 99%

“…All analyzed genomes and isolates used in this study are listed in Table S1 and originate from the following studies [32,33,[77][78][79][80][81][34][35][36][37]48,49,71,76]. We identified homologs of dim2 using the predicted 'deRIPed' protein sequence of Z. tritici IPO323 [25] as a template.…”

Section: Sequence Identification and Comparison Of Dna Methyltransfermentioning

confidence: 99%

“…Sequencing raw reads (FASTQ files) of all bisulfite and genomic data and the SMRT genome assemblies generated in this study are available online at Sequence Read Archive (SRA) under BioProject ID PRJNA614493. Previously published genome assemblies are available under BioProject PRJEB33986 [33], PRJNA638605, PRJNA639021 (Zpa63), PRJNA638553 (Zb87), PRJNA638515 (Zp13), PRJNA638382 (Za17), https://doi.org/10.5281/zenodo.3820378 [71], PRJNA414407 (Zt05 and Zt10) [36]. The genome sequence of the reference isolate IPO323 (Zt09) is available at: http://genome.jgi.doe.gov/Mycgr3/Mycgr3.home.html [26].…”

Section: Data Availabilitymentioning

confidence: 99%

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

Möller

Habig

Lorrain

et al. 2020

Preprint

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DNA methylation is found throughout all domains of life, yet the extent and function of DNA methylation differ between eukaryotes. Many 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 Ztdim2 DNA methyltransferase gene. 5mC is, however, present in closely related sister species. We demonstrate that inactivation of Ztdim2 occurred recently as some Z. tritici isolates carry a functional Ztdim2 gene. Moreover, we show that Ztdim2 inactivation occurred by a different path than previously hypothesized. We mapped the genome-wide distribution of 5mC in strains with and without functional Ztdim2. Presence of functional Ztdim2 correlated with high levels of 5mC in transposable elements (TEs), suggesting a role in genome defense.We identified low levels of 5mC in strains carrying inactive Ztdim2 alleles, suggesting that 5mC is maintained over time, presumably by an active Ztdnmt5 gene. Integration of a functional Ztdim2 allele in strains with mutated Ztdim2 restored normal 5mC levels, demonstrating de novo cytosine methylation activity of Ztdim2. 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 Ztdim2. We found that the presence of Ztdim2 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 dense 5mC at TEs is a polymorphic trait in Z. tritici populations that can impact genome evolution. SignificanceCytosine DNA methylation (5mC) is known to silence transposable elements in fungi and thereby appears to contribute to genome stability. The genomes of plant pathogenic fungi are highly diverse, differing substantially in transposon content and distribution. Here, we show extensive differences of 5mC levels within a single species of an important wheat pathogen that were caused by inactivation of the DNA methyltransferase ZtDim2 in the majority of studied isolates. Presence of widespread 5mC increased point mutation rates in regions with active or mutated transposable elements during mitosis. The mutation pattern is dependent on the presence of ZtDim2 and resembles a mitotic version of Repeat-Induced Point mutation (RIP). Thus, loss of 5mC may represent an evolutionary trade-off offering adaptive potential at the cost of transposon control. occurred recently as two closely related sister species of Z. tritici, Zymoseptoria ardabiliae and Zymoseptoria pseudotritici were shown to carry a single intact dim2 gene and have 5mC (25).By genome analyses of multiple Z. tritici isolates from the center of origin of the pathogen, the Middle East, we discovered several Z. tritici isolates with an intact Ztdim2 gene. This finding suggests that the loss of 5mC not only occurred very recently but is a polymorphic trait in Z.triti...

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“…One SMRT cell was sequenced per genome. Genome assemblies were performed as described [71]. Genome assembly statistics are summarized in Table S7.…”

Section: Smrt Sequencing and Assembly Of Iranian Isolates Zt289 And Zmentioning

confidence: 99%

Section: Identification Of Tes and Analysis Of Te Expressionmentioning

confidence: 99%

Section: Sequence Identification and Comparison Of Dna Methyltransfermentioning

confidence: 99%

Section: Data Availabilitymentioning

confidence: 99%

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

Möller

Habig

Lorrain

et al. 2020

Preprint

Self Cite

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“…One SMRT cell was sequenced per genome. Genome assemblies were performed as described [ 71 ]. In brief, genomes were assembled de novo using the SMRT Analysis software v.5 (Pacific Bioscience) using default and “fungal” parameters.…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2021

Self Cite

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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.

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Epigenetic Regulation of Fungal Genes Involved in Plant Colonization

Soyer

Fudal

2022

Plant Relationships

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Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria

Cited by 38 publications

References 83 publications

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

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

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

Epigenetic Regulation of Fungal Genes Involved in Plant Colonization

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