Transposon-associated epigenetic silencing during Pleurotus ostreatus life cycle

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1Department of Agrarian Production, Genetics and Microbiology Research Group, Public University of Navarre, Navarre, Spain
2Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, California, USA
3UCLA-U.S Department of Energy (DOE), Institute for Genomics and Proteomics, Los Angeles, California, USA

A variable fraction of eukaryotic genomes is occupied by a group of repeated sequences known as transposable elements (TEs). These mobile elements are able to transpose throughout the host genome inducing mutations and rearrangements. Given their mutagenic potential, host-genomes have evolved specific epigenetic defense mechanisms to limit their expansion by shutting down their expression. 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 analyzed the genome-wide epigenetic (DNA methylation and small RNAs production) and transcriptional (mRNA transcription) profiles 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 ranging from 2 to 6 % are primarily involved in the repression of transposon activity, and strongly suggest that 21-22 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 and functions 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, the comparative transcriptomic analysis at different stages of P. ostreatus life cycle suggest that transcriptional but not methylation reprogramming triggers fruitbody development in P. ostreatus.