Non-exhaustive DNA methylation-mediated transposon silencing in the black truffle genome, a complex fungal genome with massive repeat element content
2014
Montanini, Barbara | Chen, Pao-Yang | Morselli, Marco | Jaroszewicz, Artur | Lopez, David | Martin, Francis | Ottonello, Simone | Pellegrini, Matteo | Laboratory of Functional Genomics and Protein Engineering, Biochemistry and Molecular Biology Unit, Department of Life Sciences ; Università degli studi di Parma = University of Parma (UNIPR) | Institute of Plant and Microbial Biology ; Academia Sinica | Department of Molecular, Cell, and Developmental Biology ; University of California [Los Angeles] (UCLA) ; University of California (UC)-University of California (UC) | Interactions Arbres-Microorganismes (IAM) ; Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL) | Fondazione Cariparma ; Ministry of Education, University and Research (MIUR) ; Institute for Genomics and Proteomics at UCLA
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.
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