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Traveler, a New DD35E Family of Tc1/Mariner Transposons, Invaded Vertebrates Very Recently.

ABSTRACT: The discovery of new members of the Tc1/mariner superfamily of transposons is expected based on the increasing availability of genome sequencing data. Here, we identified a new DD35E family termed Traveler (TR). Phylogenetic analyses of its DDE domain and full-length transposase showed that, although TR formed a monophyletic clade, it exhibited the highest sequence identity and closest phylogenetic relationship with DD34E/Tc1. This family displayed a very restricted taxonomic distribution in the animal kingdom and was only detected in ray-finned fish, anura, and squamata, including 91 vertebrate species. The structural organization of TRs was highly conserved across different classes of animals. Most intact TR transposons had a length of ∼1.5 kb (range 1,072-2,191 bp) and harbored a single open reading frame encoding a transposase of ∼340 aa (range 304-350 aa) flanked by two short-terminal inverted repeats (13-68 bp). Several conserved motifs, including two helix-turn-helix motifs, a GRPR motif, a nuclear localization sequence, and a DDE domain, were also identified in TR transposases. This study also demonstrated the presence of horizontal transfer events of TRs in vertebrates, whereas the average sequence identities and the evolutionary dynamics of TR elements across species and clusters strongly indicated that the TR family invaded the vertebrate lineage very recently and that some of these elements may be currently active, combining the intact TR copies in multiple lineages of vertebrates. These data will contribute to the understanding of the evolutionary history of Tc1/mariner transposons and that of their hosts.

SUBMITTER: Zong W

PROVIDER: S-EPMC7093834 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundA family of Tc1/mariner transposons with a characteristic DD38E triad of catalytic amino acid residues, named Intruder (IT), was previously discovered in sturgeon genomes, but their evolutionary landscapes remain largely unknown.ResultsHere, we comprehensively investigated the evolutionary profiles of ITs, and evaluated their cut-and-paste activities in cells. ITs exhibited a narrow taxonomic distribution pattern in the animal kingdom, with invasions into two invertebrate phyla (Arthropoda and Cnidaria) and three vertebrate lineages (Actinopterygii, Agnatha, and Anura): very similar to that of the DD36E/IC family. Some animal orders and species seem to be more hospitable to Tc1/mariner transposons, one order of Amphibia and seven Actinopterygian orders are the most common orders with horizontal transfer events and have been invaded by all four families (DD38E/IT, DD35E/TR, DD36E/IC and DD37E/TRT) of Tc1/mariner transposons, and eight Actinopterygii species were identified as the major hosts of these families. Intact ITs have a total length of 1.5-1.7 kb containing a transposase gene flanked by terminal inverted repeats (TIRs). The phylogenetic tree and sequence identity showed that IT transposases were most closely related to DD34E/Tc1. ITs have been involved in multiple events of horizontal transfer in vertebrates and have invaded most lineages recently (< 5 million years ago) based on insertion age analysis. Accordingly, ITs presented high average sequence identity (86-95%) across most vertebrate species, suggesting that some are putatively active. ITs can transpose in human HeLa cells, and the transposition efficiency of consensus TIRs was higher than that of the TIRs of natural isolates.ConclusionsWe conclude that DD38E/IT originated from DD34E/Tc1 and can be detected in two invertebrate phyla (Arthropoda and Cnidaria), and in three vertebrate lineages (Actinopterygii, Agnatha and Anura). IT has experienced multiple HT events in animals, dominated by recent amplifications in most species and has high identity among vertebrate taxa. Our reconstructed IT transposon vector designed according to the sequence from the "cat" genome showed high cut-and-paste activity. The data suggest that IT has been acquired recently and is active in many species. This study is meaningful for understanding the evolution of the Tc1/mariner superfamily members and their hosts.

Project description: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.

Project description:BackgroundTc1/mariner and Zator, as two superfamilies of IS630-Tc1-mariner (ITm) group, have been well-defined. However, the molecular evolution and domestication of pogo transposons, once designated as an important family of the Tc1/mariner superfamily, are still poorly understood.ResultsHere, phylogenetic analysis show that pogo transposases, together with Tc1/mariner, DD34E/Gambol, and Zator transposases form four distinct monophyletic clades with high bootstrap supports (> = 74%), suggesting that they are separate superfamilies of ITm group. The pogo superfamily represents high diversity with six distinct families (Passer, Tigger, pogoR, Lemi, Mover, and Fot/Fot-like) and wide distribution with an expansion spanning across all the kingdoms of eukaryotes. It shows widespread occurrences in animals and fungi, but restricted taxonomic distribution in land plants. It has invaded almost all lineages of animals-even mammals-and has been domesticated repeatedly in vertebrates, with 12 genes, including centromere-associated protein B (CENPB), CENPB DNA-binding domain containing 1 (CENPBD1), Jrk helix-turn-helix protein (JRK), JRK like (JRKL), pogo transposable element derived with KRAB domain (POGK), and with ZNF domain (POGZ), and Tigger transposable element-derived 2 to 7 (TIGD2-7), deduced as originating from this superfamily. Two of them (JRKL and TIGD2) seem to have been co-domesticated, and the others represent independent domestication events. Four genes (TIGD3, TIGD4, TIGD5, and POGZ) tend to represent ancient domestications in vertebrates, while the others only emerge in mammals and seem to be domesticated recently. Significant structural variations including target site duplication (TSD) types and the DDE triad signatures (DD29-56D) were observed for pogo transposons. Most domesticated genes are derived from the complete transposase genes; but CENPB, POGK, and POGZ are chimeric genes fused with additional functional domains.ConclusionsThis is the first report to systematically reveal the evolutionary profiles of the pogo transposons, suggesting that pogo and Tc1/Mariner are two separate superfamilies of ITm group, and demonstrating the repeated domestications of pogo in vertebrates. These data indicate that pogo transposons have played important roles in shaping the genome and gene evolution of fungi and animals. This study expands our understanding of the diversity of pogo transposons and updates the classification of ITm group.

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Traveler, a New DD35E Family of Tc1/Mariner Transposons, Invaded Vertebrates Very Recently.

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