Identification of RAG-like transposons in protostomes suggests their ancient bilaterian origin.

BACKGROUND

V(D) J recombination is essential for adaptive immunity in jawed vertebrates and is initiated by the RAG1-RAG2 endonuclease. The and genes are thought to have evolved from a (RAG-like) transposon containing convergently-oriented () and genes. Elements resembling this presumptive evolutionary precursor have thus far only been detected convincingly in deuterostomes, leading to the model that the transposon first appeared in an early deuterostome.

RESULTS

We have identified numerous transposons in the genomes of protostomes, including oysters and mussels (phylum Mollusca) and a ribbon worm (phylum Nemertea), and in the genomes of several cnidarians. Phylogenetic analyses are consistent with vertical evolution of transposons within the Bilateria clade and with its presence in the bilaterian ancestor. Many of the transposons identified in protostomes are intact elements containing convergently oriented and genes flanked by terminal inverted repeats (TIRs) and target site duplications with striking similarities with the corresponding elements in deuterostomes. In addition, protostome genomes contain numerous intact adjacent gene pairs that lack detectable flanking TIRs. Domains and critical active site and structural amino acids needed for endonuclease and transposase activity are present and conserved in many of the predicted RAG1L and RAG2L proteins encoded in protostome genomes.

CONCLUSIONS

Active transposons were present in multiple protostome lineages and many were likely transmitted vertically during protostome evolution. It appears that transposons were broadly active during bilaterian evolution, undergoing multiple duplication and loss/fossilization events, with the genes that persist in present day protostomes perhaps constituting both active transposons and domesticated genes. Our findings raise the possibility that the transposon arose earlier in evolution than previously thought, either in an early bilaterian or prior to the divergence of bilaterians and non-bilaterians, and alter our understanding of the evolutionary history of this important group of transposons.