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Background  In eukaryotes, histone H3 lysine 9 (H3K9) methylation is a common mechanism involved in gene silencing and the establishment of heterochromatin. The loci of the major heterochromatic H3K9 methyltransferase Su(var)3-9 and the functionally unrelated γ subunit of the translation initiation factor eIF2 are fused in  Drosophila melanogaster . Here we examined the phylogenetic distribution of this unusual gene fusion and the molecular evolution of the H3K9 HMTase Su(var)3-9.    Results  We show that the gene fusion had taken place in the ancestral line of winged insects and silverfishs (Dicondylia) about 400 million years ago. We cloned  Su(var)3-9  genes from a collembolan and a spider where both genes ancestrally exist as independent transcription units. In contrast, we found a  Su(var)3-9 -specific exon inside the conserved intron position 81-1 of the  eIF2γ  gene structure in species of eight different insect orders. Intriguinly, in the pea aphid  Acyrthosiphon pisum , we detected only sequence remains of this  Su(var)3-9  exon in the  eIF2γ  intron, along with an  eIF2γ -independent  Su(var)3-9  gene. This reveals an evolutionary re-fission of both genes in aphids. Su(var)3-9 chromo domains are similar to HP1 chromo domains, which points to a potential binding activity to methylated K9 of histone H3. SET domain comparisons suggest a weaker methyltransferase activity of Su(var)3-9 in comparison to other H3K9 HMTases. Astonishingly, 11 of 19 previously described, deleterious amino acid substitutions found in Drosophila Su(var)3-9 are seemingly compensable through accompanying substitutions during evolution.    Conclusion  Examination of the  Su(var)3-9  evolution revealed strong evidence for the establishment of the  Su(var)3-9 / eIF2γ  gene fusion in an ancestor of dicondylic insects and a re-fission of this fusion during the evolution of aphids. Our comparison of 65 selected chromo domains and 93 selected SET domains from Su(var)3-9 and related proteins offers functional predictions concerning both domains in Su(var)3-9 proteins.

The evolution of the histone methyltransferase gene Su(var)3-9 in metazoans includes a fusion with and a re-fission from a functionally unrelated gene