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Open Access Research

Non-exhaustive DNA methylation-mediated transposon silencing in the black truffle genome, a complex fungal genome with massive repeat element content

Barbara Montanini1, Pao-Yang Chen23, Marco Morselli15, Artur Jaroszewicz3, David Lopez3, Francis Martin4, Simone Ottonello1* and Matteo Pellegrini3*

Author Affiliations

1 Laboratory of Functional Genomics and Protein Engineering, Biochemistry and Molecular Biology Unit, Department of Life Sciences, University of Parma, Parma 43124, Italy

2 Institute of Plant and Microbial Biology, Academia Sinica, Taipei 11529, Taiwan

3 Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles 90095, CA, USA

4 Ecogenomics of Interactions’ Lab, UMR “Tree-Microbe Interactions” INRA-Nancy, Champenoux 54180, France

5 Present address: Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles 90095, CA, USA

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Genome Biology 2014, 15:411  doi:10.1186/s13059-014-0411-5

Published: 31 July 2014

Abstract

Background

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.

Results

Whole-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.

Conclusions

Evidence 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.