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

Abstract

BackgroundHelitrons 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.ResultsHere, 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13100-015-0054-4) contains supplementary material, which is available to authorized users.

DNA transposon activity is associated with increased mutation rates in genes of rice and other grasses

“…In this study, we compared the two rice species Oryza sativa and Oryza glaberrima which diverged ∼600,000 years ago 8 . These two species are closely enough related to allow reliable alignment of most of the genomes and yet distant enough to have numerous transposable element (TE) polymorphisms 9 10 .…”

Potential impact of TE-derived sRNA on gene regulation in the grassBrachypodium distachyon

“…In particular MITEs are miniaturized non autonomous TEs and hence lacking features suitable for insertion dating (SanMiguel et al 1998). Non autonomous elements are incomplete regarding their coding sequence and use the transcripts from intact elements to transpose (Roffler et al 2015). We therefore restricted our Random Forest analysis to the extensively characterized retrotransposons from Stritt et al (2019) to investigate the causative characteristics of the TEs expression upon M. oryzae infection.…”

Horizontal Gene Transfers in Plants

“…In these examples, HTTs were evidenced from homology searches using a particular TE as a query on nucleotide databases. In addition, when a TE family is widespread in taxonomic groups, the PI criteria can also be applied, as in the case of the HTT of PIF -like transposons in Triticeae [ 88 ], the Mothra helitron in angiosperms [ 89 ], or the centromeric retrotransposons in grasses [ 90 ]. With the advent of NGS-based plant genome sequencing projects over the last decade, one could tentatively search for HTTs based on whole genome similarity searches.…”