Abstract
BackgroundThe Tc1/mariner superfamily might represent the most diverse and widely distributed group of DNA transposons. Several families have been identified; however, exploring the diversity of this superfamily and updating its classification is still ongoing in the life sciences.ResultsHere we identified a new family of Tc1/mariner transposons, named Incomer (IC), which is close to, but distinct from the known family DD34E/Tc1. ICs have a total length of about 1.2 kb, and harbor a single open reading frame encoding a ~ 346 amino acid transposase with a DD36E motif and flanked by short terminal inverted repeats (TIRs) (22–32 base pairs, bp). This family is absent from prokaryotes, and is mainly distributed among vertebrates (141 species of four classes), including Agnatha (one species of jawless fish), Actinopterygii (132 species of ray-finned fish), Amphibia (four species of frogs), and Mammalia (four species of bats), but have a restricted distribution in invertebrates (four species in Insecta and nine in Arachnida). All ICs in bats (Myotis lucifugus, Eptesicus fuscus, Myotis davidii, and Myotis brandtii) are present as truncated copies in these genomes, and most of them are flanked by relatively long TIRs (51–126 bp). High copy numbers of miniature inverted-repeat transposable elements (MITEs) derived from ICs were also identified in bat genomes. Phylogenetic analysis revealed that ICs are more closely related to DD34E/Tc1 than to other families of Tc1/mariner (e.g., DD34D/mariner and DD × D/pogo), and can be classified into four distinct clusters. The host and IC phylogenies and pairwise distance comparisons between RAG1 genes and all consensus sequences of ICs support the idea that multiple episodes of horizontal transfer (HT) of ICs have occurred in vertebrates. In addition, the discovery of intact transposases, perfect TIRs and target site duplications of ICs suggests that this family may still be active in Insecta, Arachnida, frogs, and fish.ConclusionsExploring the diversity of Tc1/mariner transposons and revealing their evolutionary profiles will help provide a better understanding of the evolution of DNA transposons and their impact on genomic evolution. Here, a newly discovered family (DD36E/Incomer) of Tc1/mariner transposons is described in animals. It displays a similar structural organization and close relationship with the known DD34E/Tc1 elements, but has a relatively narrow distribution, indicating that DD36E/IC might have originated from the DD34E/Tc1 family. Our data also support the hypothesis of horizontal transfer of IC in vertebrates, even invading one lineage of mammals (bats). This study expands our understanding of the diversity of Tc1/mariner transposons and updates the classification of this superfamily.
Highlights
The Tc1/mariner superfamily might represent the most diverse and widely distributed group of DNA transposons
Taxonomic distribution of ICs Using TBLASTN searching with the DD34E references (Passport, Prince, Quetzal, and Sleeping Beauty) as queries, we identified an intact Tc1/mariner-like transposon in Rhinella marina, where it harbors a newly identified transposase family with a DD36E motif, which is close to, but distinct from the previously known family of DD34E/Tc1
Phylogenetic analysis and evidence for multiple horizontal transfer (HT) events of ICs To accurately establish the evolutionary relationships of the IC elements that we identified, the conserved DDE domain of the identified IC transposases were aligned to the 28 known DNA transposases representing the eight families in the Tc1/mariner superfamily based on MAFFT v 7.310 [26]
Summary
The Tc1/mariner superfamily might represent the most diverse and widely distributed group of DNA transposons. The first transposon was discovered by Barbara McClintock in maize [1] They were subsequently detected in various organisms, such as bacteria, fungi, and insects. It is believed that TEs play important roles in genomic evolution and are regarded as important factors in determining genome expansion. They can simultaneously modify gene structures, provide sources of regulatory sequences [3, 4], and have important impacts on the structure and evolution of the genes of eukaryotes [5, 6]
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