Heterogeneous Lineages of DNA Transposons Encode a TET/JBP Dioxygenase in Fungi

Epigenetic DNA modification is a key component of the defense system against invading nucleic acids such as transposons. TET/JBP dioxygenases oxidize 5-methylcytosine and lead to its replacement by cytosine in mammals. Expansion of TET/JBP genes and their association with DNA transposons were previously reported in Basidiomycota fungi. In this study, a thorough bioinformatics investigation of TET/JBP genes revealed that diverse groups of DNA transposons have captured a TET/JBP dioxygenase in three lineages of fungi: Pucciniomycetes (rusts) and Agaricomycetes (mushrooms) in Basidiomycota, and Pezizomycetes (morels and truffles) in Ascomycota. TET/JBP genes encoded by DNA transposons can be classified into three types, designated as PU, AG, and PE here. The PU type is distributed in Pucciniomycetes and encoded by seven different lineages of DNA transposons (Dileera, hAT, Harbinger, IS3EU, EnSpm, ESTA, and Helitron). The AG type is distributed in Agaricomycetes, and encoded by two lineages of DNA transposons (Kyakuja and Zisupton). The PE type is distributed in Pezizomycetes and Agaricomycetes, and encoded by five lineages of DNA transposons (Zisupton, IS3EU, EnSpm, Plavaka, and Helitron). Phylogenetic analysis indicated several transmission events from certain DNA transposon lineage to another. These transposon-encoded TET/JBP dioxygenases likely contribute to the escape of transposons from the methylation-based silencing system in fungi.