Abstract
BackgroundWe investigated how an extremely transposon element (TE)-rich organism such as the plant-symbiotic ascomycete truffle Tuber melanosporum exploits DNA methylation to cope with the more than 45,000 repeated elements that populate its genome.ResultsWhole-genome bisulfite sequencing performed on different developmental stages reveals a high fraction of methylated cytosines with a strong preference for CpG sites. The methylation pattern is highly similar among samples and selectively targets TEs rather than genes. A marked trend toward hypomethylation is observed for TEs located within a 1 kb distance from expressed genes, rather than segregated in TE-rich regions of the genome. Approximately 300 hypomethylated or unmethylated TEs are transcriptionally active, with higher expression levels in free-living mycelium compared to fruitbody. Indeed, multiple TE-enriched, copy number variant regions bearing a significant fraction of hypomethylated and expressed TEs are found almost exclusively in free-living mycelium. A reduction of DNA methylation, restricted to non-CpG sites and accompanied by an increase in TE expression, is observed upon treatment of free-living mycelia with 5-azacytidine.ConclusionsEvidence derived from analysis of the T. melanosporum methylome indicates that a non-exhaustive, partly reversible, methylation process operates in truffles. This allows for the existence of hypomethylated, transcriptionally active TEs that are associated with copy number variant regions of the genome. Non-exhaustive TE methylation may reflect a role of active TEs in promoting genome plasticity and the ability to adapt to sudden environmental changes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-014-0411-5) contains supplementary material, which is available to authorized users.
Highlights
We investigated how an extremely transposon element (TE)-rich organism such as the plant-symbiotic ascomycete truffle Tuber melanosporum exploits DNA methylation to cope with the more than 45,000 repeated elements that populate its genome
long terminal repeat (LTR) transposons Non-LTR transposons DNA transposons with previous reports indicating that methylation acts as a TE silencing mechanism [29,30], these results suggest that TE methylation levels in Tuber are associated with transcriptional repression of TEs
This work describes the selective methylation and associated transcriptional silencing of transposons in a complex fungal genome with massive repeat element content
Summary
We investigated how an extremely transposon element (TE)-rich organism such as the plant-symbiotic ascomycete truffle Tuber melanosporum exploits DNA methylation to cope with the more than 45,000 repeated elements that populate its genome. DNA methylation is a heritable epigenetic modification involved in the regulation of a variety of processes ranging from development to genomic imprinting, gene regulation and transposon silencing [1] It is found in animals, plants, and some fungi, but has been lost in various invertebrate lineages [2]. A genome-wide picture of DNA methylation has emerged recently from methylome studies carried out on more than 20 eukaryotic organisms belonging to four different lineages [3,4,5,6,7] As revealed by these studies, DNA cytosine methylation occurs either within symmetric CG/CHG, or asymmetric CHH sequence contexts (where H stands for A, C, or T). DNA methylation is an essential process in both plants and animals; its disruption leads to a variety of abnormal phenotypes, including altered development and cancer, but it appears to be dispensable in the model filamentous fungus Neurospora crassa and in various invertebrates [2,9,10]
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