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. 2023 Oct 12;26(11):108193.
doi: 10.1016/j.isci.2023.108193. eCollection 2023 Nov 17.

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

Robert Kucharski  1 , Nancy Ellis  2 , Tomasz P Jurkowski  3 , Paul J Hurd  2 , Ryszard Maleszka  1
Affiliations

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

Robert Kucharski et al. iScience. .

Abstract

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.

Keywords: Entomology; Evolutionary biology; Molecular biology.

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Conflict of interest statement

Authors declare that they have no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Apis mellifera DNMT3 PWWP1 and PWWP 2 domains have contrasting histone modification binding preferences Quantification of binding of GST-PWWP1 and GST-PWWP2 to MODified histone peptide arrays using anti-GST antibody. Raw spot intensities were normalized to the highest spot signal intensity (=1). For PWWP1 the highest spot intensity is H3K36me2 and for PWWP2 the highest intensity spot is H3K27me2. Bar plots represent the mean of normalized raw spot signal intensities from the left and right-side replicates of the MODified histone peptide arrays. Error bars show one standard deviation. (A) GST-PWWP1 binding specificity to histone H3 amino acids 16–35. (B) GST-PWWP2 binding specificity to histone H3 amino acids 16–35. (C) GST-PWWP1 binding specificity to histone H3 amino acids 26–45. (D) GST-PWWP2 binding specificity to histone H3 amino acids 26–45. The GST purification of the PWWP domains is shown in Figure S7.
Figure 2
Figure 2
A. mellifera DNMT3 gene structure and combinatorial generation of isoforms (A) The Sashimi plot aligned with the current A.mellifera DNMT3 gene (Linkage Group LG2; RefSeq accession: NC_037639.1). It shows quantitative comparison of exon usage across three pooled samples from the honeybee pupal brains in diploid females (queens, workers) and haploid males (drone). The black lollipops indicate the methylated CpG dinucleotides. In the latest A.mellifera genome assembly Amel_HAv3.1 this gene is located on chromosome 2 (LG2: 15,815,881-15,827,940). (B) Examples of alternatively spliced transcripts producing diverse isoforms including a combinatorial usage of the PWWP domain or missing the catalytic domain. Our full analysis of combinatorial splicing patterns is shown in Table S3.
Figure 3
Figure 3
Predicted 3D model of the honeybee PWWP domains (A) Alignment of the A. mellifera PWWP domains with the corresponding region of the human DNMT3B isoform 1 (NP_008823.1). An expanded alignment is shown in Figure S4. (B) Predicted superimposed 3D models of the PWWP1 and PWWP2 domains. The positions of cage residues occupying the turns between β1 and β2, and β3 and β4 are indicated with a dotted oval. (C) Evolutionary rate of amino acid substitutions in the PWWP, ADDz and MTase domains. Full alignments of the PWWP, ADDz and MTase domains are shows in Figures S4–S6.
Figure 4
Figure 4
Heatmap showing some interesting patterns in the PWWP domain evolution In most Hymenopterans the PWWP1 and PWWP2 domains have different branch lengths representing amino acid substitutions per site, but in one family of Chalcidoidea these lengths are similar and have large values. Also, this family shows more pronounced changes in the ADDz domain relative to the other families.
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