The PWWP domain and the evolution of unique DNA methylation toolkits in Hymenoptera

DNMT3 in Hymenoptera has a unique duplication of the essential PWWP domain. Using GST-tagged PWWP fusion proteins and histone arrays we show that these domains have gained new properties and represent the first case of PWWP domains binding to H3K27 chromatin modifications, including H3K27me3, a key modification that is important during development. Phylogenetic analyses of 107 genomes indicate that the duplicated PWWP domains separated into two sister clades, and their distinct binding capacities are supported by 3D modeling. Other features of this unique DNA methylation system include variable copies, losses, and duplications of DNMT1 and DNMT3, and combinatorial generations of DNMT3 isoforms including variants missing the catalytic domain. Some of these losses and duplications of are found only in parasitic wasps. We discuss our findings in the context of the crosstalk between DNA methylation and histone methylation, and the expanded potential of epigenomic modifications in Hymenoptera to drive evolutionary novelties. [Display omitted] •Insect DNA methylation remains largely unexplored•The PWWP domain duplication is a unique feature of DNMT3s in Hymenoptera•This study shows the first case of PWWP domains binding to H3K27 chromatin modification•DNA methylation system is highly diverse in Hymenoptera with variable copies of DNMTs Entomology; Molecular biology; Evolutionary biology