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

• Main Authors: Patties Ina, Fiebig Petra, Fassl Anne, Krauss Veiko, Sass Heinz
• Format: Article
• Language: English
• Published: BMC 2006-03-01
• Series: BMC Evolutionary Biology
• Online Access: http://www.biomedcentral.com/1471-2148/6/18

<p>Abstract</p> <p>Background</p> <p>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 <it>Drosophila melanogaster</it>. Here we examined the phylogenetic distribution of this unusual gene fusion and the molecular evolution of the H3K9 HMTase Su(var)3-9.</p> <p>Results</p> <p>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 <it>Su(var)3-9 </it>genes from a collembolan and a spider where both genes ancestrally exist as independent transcription units. In contrast, we found a <it>Su(var)3-9</it>-specific exon inside the conserved intron position 81-1 of the <it>eIF2γ </it>gene structure in species of eight different insect orders. Intriguinly, in the pea aphid <it>Acyrthosiphon pisum</it>, we detected only sequence remains of this <it>Su(var)3-9 </it>exon in the <it>eIF2γ </it>intron, along with an <it>eIF2γ</it>-independent <it>Su(var)3-9 </it>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.</p> <p>Conclusion</p> <p>Examination of the <it>Su(var)3-9 </it>evolution revealed strong evidence for the establishment of the <it>Su(var)3-9</it>/<it>eIF2γ </it>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.</p>