Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles

Abstract

Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species with active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation.

Author Summary

Transposable elements (TEs) are enigmatic genetic units that have played important roles in the evolution of eukaryotic genomes. Since their discovery in the 1950s, they have gained increasing attention and are known today as active genome modelers in multiple species. Although these elements have been widely studied in plants, much less is known about their occurrence and impact on the fungal kingdom. Using a diverse set of basidiomycete and ascomycete fungi, we quantified and characterized a huge diversity of DNA and RNA transposable elements, and we identified species that had 0.02 to 29.8% of their genomes occupied by transposable elements. In addition, using our basidiomycete model Pleurotus ostreatus, we demonstrated how TE insertions produced detrimental effects on the expression of upstream and downstream genes, which were downregulated compared with the control groups. This silencing mechanism was present in the basidiomycetes tested but exhibited a patchy distribution in ascomycetes, and might be related to specific genome defense mechanisms that control transposon proliferation. This finding reveals the broader impact of transposable elements in fungi. In addition to their importance as long-term evolutionary forces, they play major roles in the more dynamic transcriptome regulation of certain species.