DNA methylation allows cells to switch genes in to the ‘off’ position and has been functionally linked to development, behaviour and phenotypic plasticity. It not only silences genes but also controls transposable elements (TEs) – mobile pieces of DNA, or ‘jumping genes’, that can cause mutations in the genome. Evidence suggests that it is also a dynamic process, reversible under certain enzymes, and so contributing to genomic plasticity. The amount and distribution of DNA methylation varies across species. For example, mammals typically exhibit 70-80 percent C-G nucleotide pair methylation, while Drosophila melanogaster exhibits virtually none. In fungi, there appears to be a general trend towards DNA methylation of TEs or other repetitive DNA sequences, with only a few species exhibiting gene targeting or an absence of methylation. In a recent study in Genome Biology, Matteo Pellegrini from the University of California, USA and colleagues examine the DNA methylation patterns of the fungus Tuber melanosporum – better known as the black truffle
T. melanosporum, endemic to calcareous soils of southern Europe, is one of the most highly prized and expensive edible mushrooms in the world. From a genomics point of view, it also makes for a particularly interesting subject; not only does its genome have an exceptionally high TE content (at around 58 percent), but it is also an obligate outcrossing organism. Both of these characteristics are proposed to be major driving forces for the evolution of DNA methylation of its genome.
To probe the black truffle genome Pellegrini and colleagues used whole-genome bisulfite sequencing, whereby every cytosine is converted into uracil unless that cytosine is methylated. More than 44 percent of cytosine sites in the black truffle genome were methylated, a considerably higher level than those estimated in other fungi, and setting T. melanosporum in the top rank of methylation-proficient organisms. The process was shown to be partly reversible and selective, with DNA methylation targeting TEs in a nearly exclusive manner.
However, not all TEs were targeted – approximately 300 unmethylated or poorly methylated TEs escaped modification and remained transcriptionally active, with a marked trend towards hypomethylation of TEs located within a one kilobase distance from expressed genes. This non-exhaustive TE methylation may reflect an inability to fully control such a massive amount of TEs. Alternatively, somewhat leaky TE silencing may represent an evolutionary strategy to promote genome plasticity and an ability to adapt to changes in, for example, the host-parasite relationship.
The authors provide novel insights into how a TE-rich organism exploits DNA methylation, and raises fascinating questions about its role in the preservation of genomic plasticity and adaptive evolution, which may equip this much sought after fungus with the ability to adapt and persist in the face of sudden environmental changes.