The making of a genomic parasite - the Mothra family sheds light on the evolution of Helitrons in plants

Stefan Roffler, Fabrizio Menardo, Thomas Wicker

Helitrons are Class II transposons which are highly abundant in almost all eukaryotes. However, most Helitrons lack protein coding sequence. These non-autonomous elements are thought to hijack recombinase/helicase (RepHel) and possibly further enzymes from related, autonomous elements. Interestingly, many plant Helitrons contain an additional gene encoding a single-strand binding protein homologous to Replication Factor A (RPA), a highly conserved, single-copy gene found in all eukaryotes. Here, we describe the analysis of DHH_Mothra, a high-copy non-autonomous Helitron in the genome of rice (Oryza sativa). Mothra has a low GC-content and consists of two distinct blocs of tandem repeats. Based on homology between their termini, we identified a putative mother element which encodes an RPA-like protein but has no RepHel gene. Additionally, we found a putative autonomous sister-family with strong homology to the Mothra mother element in the RPA protein and terminal sequences, which we propose provides the RepHel domain for the Mothra family. Furthermore, we phylogenetically analyzed the evolutionary history of RPA-like proteins. Interestingly, plant Helitron RPAs (PHRPAs) are only found in monocotyledonous and dicotyledonous plants and they form a monophyletic group which branched off before the eukaryotic "core" RPAs. Our data show how erosion of autonomous Helitrons can lead to different "levels" of autonomy within Helitron families and can create highly successful subfamilies of non-autonomous elements. Most importantly, our phylogenetic analysis showed that the PHRPA gene was most likely acquired via horizontal gene transfer from an unknown eukaryotic donor at least 145-300 million years ago in the common ancestor of monocotyledonous and dicotyledonous plants. This might have led to the evolution of a separate branch of the Helitron superfamily in plants.