Independent evolution of transposase and TIRs facilitated by recombination between <i>Mutator</i> transposons from divergent clades in maize.

Abstract

Nearly all eukaryotes carry DNA transposons of the Robertson's <i>Mutator</i> (<i>Mu</i>) superfamily, a widespread source of genome instability and genetic variation. Despite their pervasive impact on host genomes, much remains unknown about the evolution of these transposons. Transposase recognition of terminal inverted repeats (TIRs) is thought to drive and constrain coevolution of <i>MuDR</i> transposase genes and TIRs. To address the extent of this relationship and its impact, we compared separate phylogenies of TIRs and <i>MuDR</i> gene sequences from <i>Mu</i> elements in the maize genome. Five major clades were identified. As expected, most <i>Mu</i> elements were bound by highly similar TIRs from the same clade (homomorphic type). However, a subset of elements contained dissimilar TIRs derived from divergent clades. These "heteromorphs" typically occurred in multiple copies indicating active transposition in the genome. In addition, analysis of internal sequences showed that exchanges between elements having divergent TIRs produced new <i>mudra</i> and <i>mudrb</i> gene combinations. In several instances, TIR homomorphs had been regenerated within a heteromorph clade with retention of distinctive internal <i>MuDR</i> sequence combinations. Results reveal that recombination between divergent clades facilitates independent evolution of transposase (<i>mudra</i>), transposase-binding targets (TIRs), and capacity for insertion (<i>mudrb</i>) of active <i>Mu</i> elements. This mechanism would be enhanced by the preference of <i>Mu</i> insertions for recombination-rich regions near the 5' ends of genes. We suggest that cycles of recombination give rise to alternating homo- and heteromorph forms that enhance the diversity on which selection for <i>Mu</i> fitness can operate.