Epigenetic regulation of nuclear processes in fungal plant pathogens

Kramer, Holger; Cook, David E.; Seidl, Michael; Thomma, Bart P.H.J.

doi:10.1371/journal.ppat.1011525

Cited by 7 publications

References 163 publications

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Enhanced oxidative stress resistance in Ustilago maydis and its implications on the virulence

Cuamatzi-Flores,

Colón-González,

Requena-Romo

et al. 2024

Int Microbiol

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The phytopathogenic fungus Ustilago maydis causes corn smut by suppressing host plant defenses, including the oxidative burst response. While many studies have investigated how U. maydis responds to oxidative stress during infection, the consequences of heightened resistance to oxidative stress on virulence remain understudied. This study aimed to identify the effects on virulence in U. maydis strains exhibiting enhanced resistance to hydrogen peroxide (H2O2).To achieve this, we exposed U. maydis SG200 to 20 escalating H2O2 shocks, resulting in an adapted strain resistant to concentrations as high as 60 mM of H2O2, a lethal dose for the initial strain. Genetic analysis of the adapted strain revealed five nucleotide substitutions, two minor copy number variants, and a large amplification event on chromosome nine (1–149 kb) encompassing the sole catalase gene. Overexpressing catalase increased resistance to H2O2; however, this resistance was lower than that observed in the adapted strain. Additionally, virulence was reduced in both strains with enhanced H2O2 resistance.In summary, enhanced H2O2 resistance, achieved through either continuous exposure to the oxidative agent or through catalase overexpression, decreased virulence. This suggests that the response to the oxidative stress burst in U. maydis is optimal and that increasing the resistance to H2O2 does not translate into increased virulence. These findings illuminate the intricate relationship between oxidative stress resistance and virulence in U. maydis, offering insights into its infection mechanisms.

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Enhanced oxidative stress resistance in Ustilago maydis and its implications on the virulence

Cuamatzi-Flores,

Colón-González,

Requena-Romo

et al. 2024

Int Microbiol

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Natural genomic variation in rice blast genomes is associated with specific heterochromatin modifications

Rowe,

Huang,

Zhang

et al. 2023

Preprint

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Genome organization in eukaryotes exhibits non-random patterns tied to transcription, replication, and chromatin. However, the driving forces across these processes, and their impacts on genome evolution remain unclear. To address this, we analyzed sequence data from 86 Magnaporthe oryzae isolates, a globally important plant pathogenic fungus, alongside new reference genomes, to investigate DNA sequence variation and the epigenome. Histone modification profiles were obtained through genome-wide chromatin immunoprecipitation-sequencing of the four new reference strains, which revealed that repressive histone marks (H3K27me3, H3K9me3) were associated with SNP and INDEL frequency. Densely grouped SNPs were found to reside in heterochromatin, often outside transposable elements, highlighting the link between heterochromatin and DNA variation. Even when controlling for selection, silent SNP frequency/kb was higher in H3K27me3-associated genes. Effector genes, key to pathogenicity, also displayed this trend. Comparing the reference strains, euchromatic regions were often syntenic, while heterochromatic regions trended towards non-syntenic. Heterochromatin emerged as a major factor associated with diverse DNA variations in M. oryzae populations, even when accounting for selective pressure. This underscores heterochromatin's pivotal role in shaping genetic diversity in these mainly asexually reproducing fungi.

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RNAi epimutations conferring antifungal drug resistance are inheritable

Pérez-Arques,

Navarro-Mendoza,

et al. 2024

Preprint

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Epimutations modify gene expression and lead to phenotypic variation, although the encoding DNA sequence remains unchanged. Epimutations mediated by RNA interference (RNAi) and/or chromatin modifications can confer antifungal drug resistance and may impact virulence traits in fungi. However, whether these epigenetic modifications can be transmitted across generations following sexual reproduction was unclear. This study demonstrates that RNAi epimutations conferring antifungal drug resistance are transgenerationally inherited in the human fungal pathogen Mucor circinelloides. Our research reveals that RNAi-based antifungal resistance follows a DNA sequence-independent, non-Mendelian inheritance pattern. Small RNAs (sRNAs) are the exclusive determinants of inheritance, transmitting drug resistance independently of other known repressive epigenetic modifications. Unique sRNA signature patterns can be traced through inheritance from parent to progeny, further supporting RNA as an alternative molecule for transmitting information across generations. This study marks a significant advance in understanding epigenetic inheritance, highlighting RNAi-exclusive epimutations as a widespread phenomenon in the pathogenic M. circinelloides species complex. Understanding how epimutations occur, propagate, and confer resistance may enable their detection in other eukaryotic pathogens, provide solutions for challenges posed by rising antimicrobial drug resistance (AMR), and also advance research on phenotypic adaptability and its evolutionary implications.

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Epigenetic regulation of nuclear processes in fungal plant pathogens

Cited by 7 publications

References 163 publications

Enhanced oxidative stress resistance in Ustilago maydis and its implications on the virulence

Enhanced oxidative stress resistance in Ustilago maydis and its implications on the virulence

Natural genomic variation in rice blast genomes is associated with specific heterochromatin modifications

RNAi epimutations conferring antifungal drug resistance are inheritable

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