Independent evolution of transposase and TIRs facilitated by recombination between Mutator transposons from divergent clades in maize

Authors: Hunter, Charles; MCCARTY, DONALD - University Of Florida; KOCH, KAREN - University Of Florida

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/31/2023
Publication Date: 7/25/2023
Citation: Hunter Iii, C.T., Mccarty, D.R., Koch, K.E. 2023. Independent evolution of transposase and TIRs facilitated by recombination between Mutator transposons from divergent clades in maize. Proceedings of the National Academy of Sciences (PNAS). 120 (31) e2305298120. https://doi.org/10.1073/pnas.2305298120.
DOI: https://doi.org/10.1073/pnas.2305298120

Interpretive Summary: The Mutator transposon family are mobile DNA elements that contribute genetic variation and genome instability during evolution of most eukaryotic organisms. They also serve as important tools for genetics research in maize (and other systems) by causing gene disruptions that can be extremely valuable in investigations into gene function. In collaboration with University of Florida scientists, ARS scientists at the Center for Medical, Agricultural, and Veterinary Entomology in Gainesville, FL have gained new insights into the evolution and behavior of Mu transpsons. Analysis of the maize genome revealed evolutionary dynamics whereby Mu transposons from separate lineages exchange components, including transposase-coding genes and transposase recognition sites important for function. These exchanges appear to be facilitated by the preference of Mutator transposons to transpose into recombination-rich regions associated with gene transcription, a trait not observed in most DNA transposons. Exchanges of components amongst transposon family members may help these elements escape host silencing mechanisms that suppress transposon activity. By improving our understanding of the behavior and evolution of Mutator transposons, we strengthen our ability to leverage these mobile elements in functional genetics studies and also gain a more complete picture of evolution in general. The insights gained in this work may have broad implications for other transposon families found throughout eukaryotic organisms.

Technical Abstract: Nearly all eukaryotes carry Robertson's Mutator (Mu) type DNA transposons, a widespread source of genome instability and genetic variation. Despite their pervasive impact on host genomes, much remains unknown about evolution of these transposons Adaptive change among Mu transposons is thought to be constrained by coordinate modifications of both MuDR-encoded transposases and transposase-binding sites within terminal inverted repeats (TIRs). To address the extent of this relationship and its impact, we compared separate phylogenies of TIRs and MuDR gene sequences from Mu elements in the B73 maize genome. The TIR analysis revealed five major phylogenetic groups, each composed mostly of elements with highly-similar TIRs (homo-morphic type). However, a subset of elements had paired TIRs of divergent clades. These novel “hetero-morphs” had clearly transposed in the genome, demonstrating that activity could occur with dis-similar TIRs. In addition, analysis of internal sequences showed that exchanges between elements having divergent TIRs often included new MuDRa and MuDRb combinations. Several instances also implicated regeneration of TIR homomorphs from heteromorphs but with retention of distinctive internal MuDR sequences from divergent clades. Results reveal that transposase and transposase-binding components of active Mu elements can evolve independently, and also that mechanisms for doing so are likely enhanced by preference of Mu insertions for recombination-rich regions near 5' ends of genes. We suggest that cycles of recombination give rise to alternating homo- and hetero-morph forms that may aid escape from si-RNA mediated silencing. These results highlight a previously unrecognized selective advantage of the 5'-targeting strategy used by Mu elements.