DNA methyltransferases contribute to the fungal development, stress tolerance and virulence of the entomopathogenic fungus Metarhizium robertsii

Wang, Yulong; Wang, Tiantian; Qiao, Lintao; Zhu, Jianyu; Fan, Jian‐Gao; Zhang, Tingting; Wang, Zhang-Xun; Li, Wanzhen; Chen, Anhui; Huang, Bo

doi:10.1007/s00253-017-8197-5

Cited by 40 publications

(37 citation statements)

References 43 publications

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“…However, no sequence preference is observed for MoRID-dependent cytosine methylation in M. oryzae, which is different from that in N. crassa [44]. DNA methylation levels were 71%, 10%, and 8% that of WT in ∆MrRID, ∆MrDIM-2, and ∆MrRID/DIM-2, respectively, showing that deletion of both MrRID and MrDIM-2 exerts an additive effect on DNA methylation in Metarhizium robertsii [67]. Although all members of the DNMT1 family have been found in fungi, no homologs of DNMT3 have been identified in any fungal species to date ( Figure 1) [44,58].…”

Section: Dna Methyltransferases In Fungal Plant Pathogensmentioning

confidence: 69%

“…Although numerous fungi have no or low DNA methylation, the roles of DNA methylation in controlling the pathogenicity of pathogenic fungi has been demonstrated. The spore median lethal times (LT50s) for the ∆MrDIM-2 and ∆MrRID/∆DIM-2 strains in Galleria mellonella were respectively decreased by 47.7% and 65.9%, proving that MrDIM-2 is crucial for the pathogenicity of M. robertsii [67]. DMT1, which is a DNA MTase ortholog of Dim-2, contributes to the changes of MAGGY methylation status between M. oryzae isolates, Br48, and GFSI1-7-2 [63].…”

Section: Effect Of Dna Methylation On Fungal Pathogenicitymentioning

confidence: 99%

“…Mutation of CpBck1 in C. parasitica leads to the significant changes of the DNA methylation proportion and a sporadic occurrence of sectors [75]. DNA methylation impacts fungal development by regulating the transcription of genes related to metabolic activities and energetic metabolism in the M. robertsii [67]. On the contrary, DNA methylation is not directly associated with gene expression involved in sexual development in C. militaris [74].…”

Section: Impact Of Dna Methylation On the Development Of Fungal Plantmentioning

confidence: 99%

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The Pattern and Function of DNA Methylation in Fungal Plant Pathogens

Zhang

et al. 2020

Microorganisms

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To successfully infect plants and trigger disease, fungal plant pathogens use various strategies that are dependent on characteristics of their biology and genomes. Although pathogenic fungi are different from animals and plants in the genomic heritability, sequence feature, and epigenetic modification, an increasing number of phytopathogenic fungi have been demonstrated to share DNA methyltransferases (MTases) responsible for DNA methylation with animals and plants. Fungal plant pathogens predominantly possess four types of DNA MTase homologs, including DIM-2, DNMT1, DNMT5, and RID. Numerous studies have indicated that DNA methylation in phytopathogenic fungi mainly distributes in transposable elements (TEs), gene promoter regions, and the repetitive DNA sequences. As an important and heritable epigenetic modification, DNA methylation is associated with silencing of gene expression and transposon, and it is responsible for a wide range of biological phenomena in fungi. This review highlights the relevant reports and insights into the important roles of DNA methylation in the modulation of development, pathogenicity, and secondary metabolism of fungal plant pathogens. Recent evidences prove that there are massive links between DNA and histone methylation in fungi, and they commonly regulate fungal development and mycotoxin biosynthesis.

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Section: Dna Methyltransferases In Fungal Plant Pathogensmentioning

confidence: 69%

Section: Effect Of Dna Methylation On Fungal Pathogenicitymentioning

confidence: 99%

Section: Impact Of Dna Methylation On the Development Of Fungal Plantmentioning

confidence: 99%

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The Pattern and Function of DNA Methylation in Fungal Plant Pathogens

Zhang

et al. 2020

Microorganisms

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“…On the contrary, neither barren perithecia nor fertility defect are observed in N. crassa crosses homozygous for the rid null allele [12], although this fungus shows heavy DNA methylation of repeats subjected to RIP. The function of rid orthologs has also been addressed in fungal species that reproduce asexually ( Aspergillus flavus [87], Cryphonectria parasitica [88], Metarhizium robertsii [89]). Interestingly, in these species, in addition to a decrease of DNA methylation contents, the absence of DMT-like fungal specific Masc1/RID proteins results in a large palette of phenotypes including reduction of clonal dispersion (conidiation and sclerotial production), defects of mycelium morphology, decrease in secondary metabolite production and/or virulence toward plant hosts.…”

Section: Discussionmentioning

confidence: 99%

A RID-like cytosine methyltransferase homologue controls sexual development in the fungusPodospora anserina

Grognet

Timpano

Carlier

et al. 2019

Preprint

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21DNA methyltransferases are ubiquitous enzymes conserved in bacteria, plants and 22 opisthokonta. These enzymes, which methylate cytosines, are involved in numerous 23 biological processes, notably development. In mammals and higher plants, methylation 24 patterns established and maintained by the cytosine DNA methyltransferases (DMTs) are 25 essential to zygotic development. In fungi, some members of an extensively conserved 26 fungal-specific DNA methyltransferase class are both mediators of the Repeat Induced Point 27 mutation (RIP) genome defense system and key players of sexual reproduction. Yet, no DNA 28 methyltransferase activity of these purified RID (RIP deficient) proteins could be detected in 29 vitro. These observations led us to explore how RID-like DNA methyltransferase encoding 30 genes would play a role during sexual development of fungi showing very little genomic DNA 31 methylation, if any. 32To do so, we used the model ascomycete fungus P. anserina. We identified the 33 PaRid gene, encoding a RID-like DNA methyltransferase and constructed knocked-out 34ΔPaRid defective mutants. Crosses involving P. anserina ΔPaRid mutants are sterile. Our 35 results show that, although gametes are readily formed and fertilization occurs in a ΔPaRid 36 background, sexual development is blocked just before the individualization of the dikaryotic 37 cells leading to meiocytes. Complementation of ΔPaRid mutants with ectopic alleles of 38 PaRid, including 39 demonstrated that the catalytic motif of the putative PaRid methyltransferase is essential to 40 ensure proper sexual development and that the expression of PaRid is spatially and 41 temporally restricted. A transcriptomic analysis performed on mutant crosses revealed an 42 overlap of the PaRid-controlled genetic network with the well-known mating-types gene 43 developmental pathway common to an important group of fungi, the Pezizomycotina. 44 45 46 3 Author Summary 47Sexual reproduction is considered to be essential for long-term persistence of 48 eukaryotic species. Sexual reproduction is controlled by strict mechanisms governing which 49 haploids can fuse (mating) and which developmental paths the resulting zygote will follow. In 50 mammals, differential genomic DNA methylation patterns of parental gametes, known as 51 'DNA methylation imprints' are essential to zygotic development, while in plants, global 52 genomic demethylation often results in female-sterility. Although animal and fungi are 53 evolutionary related, little is known about epigenetic regulation of gene expression and 54 development in multicellular fungi. Here, we report on a gene of the model fungus Podospora 55 anserina, encoding a protein called PaRid that looks like a DNA methyltrasferase. We 56 showed that expression of the catalytically functional version of the PaRid protein is required 57 in the maternal parental strain to form zygotes. By establishing the transcriptional profile of 58PaRid mutant strain, we identified a set of PaRid direct and/or indirect target genes. Half o...

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“…Generation of gene deletion and complementation mutant. Target genes were deleted as described previously (29). In brief, the 5= and 3= flanking regions of the MrSDN gene were amplified and inserted into the binary vector pDHt-SK-bar.…”

Section: Methodsmentioning

confidence: 99%

Degradation of Fungal MicroRNAs Triggered by Short Tandem Target Mimics Is via the Small-RNA-Degrading Nuclease

Wang

Yang

et al. 2019

Appl Environ Microbiol

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MicroRNAs (miRNAs) have been recognized as sequence-specific regulators of the genome, transcriptome, and proteome in eukaryotes. However, the functions and working mechanisms of hundreds of fungal miRNA-like (miR-like) RNAs are obscure. Here, we report that a short tandem target mimic (STTM) triggered the degradation of several fungal miR-like RNAs in two different fungal species, Metarhizium robertsii and Aspergillus flavus, and that small-RNA-degrading nucleases (SDNs) were indispensable for such degradation. STTMs were most effective when the fungal polymerase II (Pol II) promoter was used for their expression, while the Pol III promoter was less effective. The length of the STTM spacer, approximately 48 to 96 nucleotides, and the number of miR-like RNA binding sites, from 2 to 4 copies, showed no significant difference in the degradation of miR-like RNAs. STTMs modulated the miR-like RNA expression levels in at least two different fungal species, which further impacted fungal asexual growth and sporulation. Further analysis showed that the degraded miR-like RNAs in STTM mutants led to the upregulation of potential target genes involved in fungal development and conidial production, which result in different phenotypes in these mutants. The STTM technology developed in this study is an effective and powerful tool for the functional dissection of fungal miR-like RNAs. IMPORTANCE The development and application of STTM technology to block miR-like RNAs in M. robertsii and A. flavus may allow for efficient generation of miR-like RNA mutants in various fungi, providing a powerful tool for functional genomics of small RNA molecules in fungi.

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DNA methyltransferases contribute to the fungal development, stress tolerance and virulence of the entomopathogenic fungus Metarhizium robertsii

Cited by 40 publications

References 43 publications

The Pattern and Function of DNA Methylation in Fungal Plant Pathogens

The Pattern and Function of DNA Methylation in Fungal Plant Pathogens

A RID-like cytosine methyltransferase homologue controls sexual development in the fungusPodospora anserina

Degradation of Fungal MicroRNAs Triggered by Short Tandem Target Mimics Is via the Small-RNA-Degrading Nuclease

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