Transposon-associated epigenetic silencing duringPleurotus ostreatuslife cycle

Abstract

Transposable elements constitute an important fraction of eukaryotic genomes. Given their mutagenic potential, host-genomes have evolved epigenetic defense mechanisms to limit their expansion. In fungi, epigenetic modifications have been widely studied in ascomycetes, although we lack a global picture of the epigenetic landscape in basidiomycetes. In this study, we analysed the genome-wide epigenetic and transcriptional patterns of the white-rot basidiomycete Pleurotus ostreatus throughout its life cycle. Our results performed by using high-throughput sequencing analyses revealed that strain-specific DNA methylation profiles are primarily involved in the repression of transposon activity and suggest that 21 nt small RNAs play a key role in transposon silencing. Furthermore, we provide evidence that transposon-associated DNA methylation, but not sRNA production, is directly involved in the silencing of genes surrounded by transposons. Remarkably, we found that nucleus-specific methylation levels varied in dikaryotic strains sharing identical genetic complement but different subculture conditions. Finally, we identified key genes activated in the fruiting process through the comparative analysis of transcriptomes. This study provides an integrated picture of epigenetic defense mechanisms leading to the transcriptional silencing of transposons and surrounding genes in basidiomycetes. Moreover, our findings suggest that transcriptional but not methylation reprogramming triggers fruitbody development in P. ostreatus.

Comparative analysis of genome-wide DNA methylation in Neurospora

“…Nevertheless, a number of traits were found to be conserved among the investigated species of Neurospora, and the patterns are consistent with what is known from other fungi. For example, the overall low methylation levels in the studied Neurospora species (ranging from 2.5% in N. crassa to 1.3% in N. tetrasperma) are consistent with previous reports on N. crassa [30,31] and other fungi [3,19,46,[50][51][52]. Furthermore, in our investigated genomes, TEs were the main target of methylation, while DNA methylation elsewhere in the genome was lower; a pattern similar to that previously reported in N. crassa and other fungi [3,32].…”

“…In all Neurospora genomes in our study, we found consistently higher CHH methylation, in accordance with results from mechanistic studies in N. crassa [56]. However, the higher CHH methylation is in contrast to other fungal genomes that have orthologous DIM-2; e.g., CpG methylation is predominant in Heterobasidion parviporum and P. ostreatus, while CHG is predominantly methylated in Magnaporthe oryzae [19,46,52]. The variation in methylation context in these fungal species suggests that divergent functions of 5mCs MTases results from evolutionary differences in methylation mechanisms in association with their genome and lifestyle [57].…”

“…On occasion, the reduction of gene expression due to the methylation status of nearby TEs could prove adaptive [18]. More generally, however, spreading of epigenetic regulation of TEs is expected to lead to deleterious effects of nearby genes, typically by reducing gene expression and thereby genome function [19][20][21][22][23][24]. The trade-off in the use of methylation for epigenetic silencing of TEs may result in selection to act on the DNA methylation pattern and also influence the distribution of TEs in the genome [22][23][24].…”

“…While the importance of DNA methylation as one of the several mechanisms to control TE proliferation in fungi is widely accepted ( e.g . [ 3 , 36 ]), the deleterious effects of TE methylation on gene expression of neighbouring genes in fungal species is understudied, and is limited only to recent studies of the basidiomycete white-rot fungus Pleurotus ostreatus [ 19 , 37 ], in which the correlation between TE methylation and suppression of nearby genes was documented.…”

Molecular basis of differential parasitism between non-encapsulated and encapsulatedTrichinellarevealed by a high-quality genome assembly

“…Accordingly, we also observed a significant elevation of DNA methylation levels in the expanded gene families (Fig. 2d), as TEs are highly repressed by DNA methylation (Borgognone et al 2018). Taken together, these results might suggest that the genome and epigenome divergence between the two clades of Trichinella was mainly driven by TEs.…”