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Tc1/mariner elements are ubiquitous in eukaryotic genomes including insects. They are diverse and divided into families and sub-families. The DD34D family including mauritiana and irritans subfamilies have already been identified in two closely related species of Cecidomyiids M. destructor and M. hordei. In the current study the de novo and similarity-based methods allowed the identification for the first time of seven consensuses in M. destructor and two consensuses in M. hordei belonging to DD41D family whereas the in vitro method allowed the amplification of two and three elements in these two species respectively. Most of identified elements accumulated different mutations and long deletions spanning the N-terminal region of the transposase. Phylogenetic analyses showed that the DD41D elements were clustered in two groups belonging to rosa and Long-TIR subfamilies. The age estimation of the last transposition events of the identified Tc1/mariner elements in M. destructor showed different evolutionary histories. Indeed, irritans elements have oscillated between periods of silencing and reappearance while rosa and mauritiana elements have shown regular activity with large recent bursts. The study of insertion sites showed that they are mostly intronic and that some recently transposed elements occurred in genes linked to putative DNA-binding domains and enzymes involved in metabolic chains. Thus, this study gave evidence of the existence of DD41D family in two Mayetiola species and an insight on their evolutionary history.
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Experimental studies on DNA transposable elements (TEs) have been limited in scale, leading to a lack of understanding of the factors influencing transposition activity, evolutionary dynamics, and application potential as genome engineering tools. We predicted 130 active DNA TEs from 102 metazoan genomes and evaluated their activity in human cells. We identified 40 active (integration-competent) TEs, surpassing the cumulative number (20) of TEs found previously. With this unified comparative data, we found that the Tc1/mariner superfamily exhibits elevated activity, potentially explaining their pervasive horizontal transfers. Further functional characterization of TEs revealed additional divergence in features such as insertion bias. Remarkably, in CAR-T therapy for hematological and solid tumors, Mariner2_AG (MAG), the most active DNA TE identified, largely outperformed two widely used vectors, the lentiviral vector and the TE-based vector SB100X. Overall, this study highlights the varied transposition features and evolutionary dynamics of DNA TEs and increases the TE toolbox diversity.
Assuntos
Elementos de DNA Transponíveis , Humanos , Elementos de DNA Transponíveis/genética , Engenharia Genética/métodos , Genoma Humano , Animais , Evolução MolecularRESUMO
Callosobruchus maculatus is a major agricultural pest of legume crops worldwide and an established model system in ecology and evolution. Yet, current molecular biological resources for this species are limited. Here, we employ Hi-C sequencing to generate a greatly improved genome assembly and we annotate its repetitive elements in a dedicated in-depth effort where we manually curate and classify the most abundant unclassified repeat subfamilies. We present a scaffolded chromosome-level assembly, which is 1.01 Gb in total length with 86% being contained within the 9 autosomes and the X chromosome. Repetitive sequences accounted for 70% of the total assembly. DNA transposons covered 18% of the genome, with the most abundant superfamily being Tc1-Mariner (9.75% of the genome). This new chromosome-level genome assembly of C. maculatus will enable future genetic and evolutionary studies not only of this important species but of beetles more generally.
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Besouros , Animais , Besouros/genética , Genoma , Sequências Repetitivas de Ácido Nucleico , Cromossomo X , Elementos de DNA Transponíveis/genética , FilogeniaRESUMO
DNA transposons play a crucial role in determining the size and structure of eukaryotic genomes. In this study, a new family of IS630-Tc1-mariner (ITm) DNA transposons, named Hiker (HK), was identified. HK is characterized by a DD35E catalytic domain and is distinct from all previously known families of the ITm group. Phylogenetic analyses showed that DD35E/Hiker forms a monophyletic clade with DD34E/Gambol, indicating that they may represent a separate superfamily of ITm. A total of 178 Hiker species were identified, with 170 found mainly in Actinopterygii, one in Chondrichthyes, six in Anura and one in Mollusca. Gambol (GM), on the other hand, are found in invertebrates, with 18 in Arthropoda and one in Platyhelminthes. Hiker transposons have a total length ranging from 2.14 to 3.67 kb and contain a single open reading frame that encodes a protein of approximately 370 amino acids (range 311-413 aa). They are flanked by short terminal inverted repeats (TIRs) of 16-30 base pairs and two base pair (TA) target-site duplications. In contrast, most transposons of the Gambol family have a total length of 1.35-5.96 kb, encode a transposase protein of approximately 350 amino acids (range 306-374 aa), and are flanked by TIRs that range from 32 to 1097 bp in length. Both Hiker and Gambol transposases have several conserved motifs, including helix-turn-helix (HTH) motifs and a DDE domain. Our study observed multiple amplification waves and repeated horizontal transfer (HT) events of HK transposons in vertebrate genomes, indicating their role in diversifying and shaping the genomes of Actinopterygii, Chondrichthyes, and Anura. Conversely, GM transposons showed few Horizontal transfer events. According to cell-based transposition assays, most HK transposons are likely inactive due to the truncated DNA binding domains of their transposases. We present an updated classification of the ITm group based on these findings, which will enhance the understanding of both the evolution of ITm transposons and that of their hosts.
Assuntos
Elementos de DNA Transponíveis , Transposases , Animais , Elementos de DNA Transponíveis/genética , Filogenia , Transposases/genética , Células Eucarióticas/metabolismo , Moluscos/genéticaRESUMO
Transposable elements exert a significant effect on the size and structure of eukaryotic genomes. Tc1/mariner superfamily elements represent the widely distributed and highly variable group of DNA transposons. Tc1/mariner elements include TLE/DD34-38E, MLE/DD34D, maT/DD37D, Visitor/DD41D, Guest/DD39D, mosquito/DD37E, and L18/DD37E families, all of which are well or less scarcely studied. However, more detailed research into the patterns of prevalence and diversity of Tc1/mariner transposons enables one to better understand the coevolution of the TEs and the eukaryotic genomes. We performed a detailed analysis of the maT/DD37D family in Cnidaria. The study of 77 genomic assemblies demonstrated that maT transposons are found in a limited number of cnidarian species belonging to classes Cubozoa (1 species), Hydrozoa (3 species) и Scyphozoa (5 species) only. The identified TEs were classified into 5 clades, with the representatives from Pelagiidae (class Scyphozoa) forming a separate clade of maT transposons, which has never been described previously. The potentially functional copies of maT transposons were identified in the hydrae. The phylogenetic analysis and the studies of distribution among the taxons and the evolutionary dynamics of the elements suggest that maT transposons of the cnidarians are the descendants of several independent invasion events occurring at different periods of time. We also established that the TEs of mosquito/DD37E family are found in Hydridae (class Hydrozoa) only. A comparison of maT and mosquito prevalence in two genomic assemblies of Hydra viridissima revealed obvious differences, thus demonstrating that each individual organism might carry a unique mobilome pattern. The results of the presented research make us better understand the diversity and evolution of Tc1/mariner transposons and their effect on the eukaryotic genomes.
Assuntos
Cnidários , Culicidae , Humanos , Animais , Culicidae/genética , Cnidários/genética , Filogenia , Elementos de DNA Transponíveis , Evolução MolecularRESUMO
Diverse Tc1/mariner elements with the DD37E signature have been detected. However, their evolutionary relationship and profiles are largely unknown. Using bioinformatics methods, we defined the evolution profile of a Tc1/Mariner family, which harbors the catalytic domain with the DD37E signature, and renamed it DD37E/Mosquito (MS). MS transposons form a separate monophyletic clade in the phylogenetic tree, distinct from the other two groups of elements with the DD37E signature, DD37E/L18 and DD37E/TRT (transposon related to Tc1), and represent a very different taxonomic distribution from that of DD37E/TRT. MS is only detected in invertebrate and is mostly present in Arthropoda, as well as in Cnidaria, Ctenophora, Mollusca, Nematoda, and Platyhelminthes, with a total length of about 1.3 kb, containing an open reading frame (ORF) encoding about 340 amino acids transposases, with a conserved DD37E catalytic domain. The terminal inverted repeat (TIR) lengths range from 19 bp to 203 bp, and the target site duplication (TSD) is TA. We also identified few occurrences of MS horizontal transfers (HT) across lineages of diptera. In this paper, the distribution characteristics, structural characteristics, phylogenetic evolution, and horizontal transfer of the MS family are fully analyzed, which is conducive to supplementing and improving the Tc1/Mariner superfamily and excavating active transposons.
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Elementos de DNA Transponíveis , Animais , Elementos de DNA Transponíveis/genética , Filogenia , Artrópodes/genética , Cnidários/genética , Ctenóforos/genética , Moluscos/genética , Nematoides/genética , Platelmintos/genéticaRESUMO
Transposable elements (TEs) constitute a considerable fraction of eukaryote genomes representing a major source of genetic variability. We describe two DNA sequences isolated in the lizard Zootoca vivipara, here named Zv516 and Zv817. Both sequences are single-copy nuclear sequences, including a truncation of two transposable elements (TEs), SINE Squam1 in Zv516 and a Tc1/Mariner-like DNA transposon in Zv817. FISH analyses with Zv516 showed the occurrence of interspersed signals of the SINE Squam1 sequence on all chromosomes of Z. vivipara and quantitative dot blot indicated that this TE is present with about 4700 copies in the Z. vivipara genome. FISH and dot blot with Zv817 did not produce clear hybridization signals. Bioinformatic analysis showed the presence of active SINE Squam 1 copies in the genome of different lacertids, in different mRNAs, and intronic and coding regions of various genes. The Tc1/Mariner-like DNA transposon occurs in all reptiles, excluding Sphenodon and Archosauria. Zv817 includes a trait of 284 bp, representing an amniote ultra-conserved element (UCE). Using amniote UCE homologous sequences from available whole genome sequences of major amniote taxonomic groups, we performed a phylogenetic analysis which retrieved Prototheria as the sister group of Metatheria and Eutheria. Within diapsids, Testudines are the sister group to Aves + Crocodylia (Archosauria), and Sphenodon is the sister group to Squamata. Furthermore, large trait regions flanking the UCE are conserved at family level.
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Both ZeBrafish (ZB), a recently identified DNA transposon in the zebrafish genome, and SB, a reconstructed transposon originally discovered in several fish species, are known to exhibit high transposition activity in vertebrate cells. Although a similar structural organization was observed for ZB and SB transposons, the evolutionary profiles of their homologs in various species remain unknown. In the present study, we compared their taxonomic ranges, structural arrangements, sequence identities, evolution dynamics, and horizontal transfer occurrences in vertebrates. In total, 629 ZB and 366 SB homologs were obtained and classified into four distinct clades, named ZB, ZB-like, SB, and SB-like. They displayed narrow taxonomic distributions in eukaryotes, and were mostly found in vertebrates, Actinopterygii in particular tended to be the major reservoir hosts of these transposons. Similar structural features and high sequence identities were observed for transposons and transposase, notably homologous to the SB and ZB elements. The genomic sequences that flank the ZB and SB transposons in the genomes revealed highly conserved integration profiles with strong preferential integration into AT repeats. Both SB and ZB transposons experienced horizontal transfer (HT) events, which were most common in Actinopterygii. Our current study helps to increase our understanding of the evolutionary properties and histories of SB and ZB transposon families in animals.
Assuntos
Elementos de DNA Transponíveis , Peixe-Zebra , Animais , Peixe-Zebra/genética , Peixe-Zebra/metabolismo , Elementos de DNA Transponíveis/genética , Transposases/genéticaRESUMO
Transposable elements have a significant impact on the structure and functioning of multicellular genomes, and also serve as a source of new genes. Studying the diversity and evolution of transposable elements in different taxa is necessary for the fundamental understanding of their role in genomes. The Tc1/mariner elements are one of the most widespread and diverse groups of DNA transposons. In this work, the structure, distribution, diversity, and evolution of the L18 (DD37E) elements in the genomes of cnidarians (Cnidaria) were studied for the first time. As a result, it was found that the L18 group is an independent family (and not a subfamily of the TLE family, as previously thought) in the Tc1/mariner superfamily. Of the 51 detected elements, only four had potentially functional copies. It is assumed that the L18 transposons are of ancient origin, and, in addition, the elements found in the genomes of organisms of the Anthozoa and Hydrozoa classes do not come from a common ancestral transposon within the Cnidaria phylum. In organisms of the Hydrozoa class, L18 transposons appeared as a result of horizontal transfer at a later time period. An intraspecies comparison of the diversity of the L18 elements demonstrates high homogeneity with respect to "old" transposons, which have already lost their activity. At the same time, distant populations, as in the case of Hydra viridissima, have differences in the representation of DNA transposons and the number of copies. These data supplement the knowledge on the diversity and evolution of Tc1/mariner transposons and contribute to the study of the influence of mobile genetic elements on the evolution of multicellular organisms.
Assuntos
Cnidários , Elementos de DNA Transponíveis , Animais , Cnidários/genética , Elementos de DNA Transponíveis/genética , PrevalênciaRESUMO
Here, a new superfamily of IS630-Tc1-mariner (ITm) DNA transposons, termed Sailor, is identified, that is characterized by a DD82E catalytic domain and is distinct from all previously known superfamilies of the ITm group. Phylogenetic analyses revealed that Sailor forms a monophyletic clade with a more intimate link to the clades of Tc1/mariner and DD34E/Gambol. Sailor was detected in both prokaryotes and eukaryotes and invaded a total of 256 species across six kingdoms. Sailor is present in nine species of bacteria, two species of plantae, four species of protozoa, 23 species of Chromista, 12 species of Fungi and 206 species of animals. Moreover, Sailor is extensively distributed in invertebrates (a total of 206 species from six phyla) but is absent in vertebrates. Sailor transposons are 1.38-6.98 kb in total length and encoded transposases of ~676 aa flanked by TIRs with lengths between 18, 1362 and 4 bp (TATA) target-site duplications. Furthermore, our analysis provided strong evidence of Sailor transmissions from prokaryotes to eukaryotes and internal transmissions in both. These data update the classification of the ITm group and will contribute to the understanding of the evolution of ITm transposons and that of their hosts.
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Bees (Apoidea), the largest and most crucial radiation of pollinators, play a vital role in the ecosystem balance. Transposons are widely distributed in nature and are important drivers of species diversity. However, transposons are rarely reported in important pollinators such as bees. Here, we surveyed 37 bee genomesin Apoidea, annotated the pogo and Tc1/mariner transposons in the genome of each species, and performed a phylogenetic analysis and determined their overall distribution. The pogo and Tc1/mariner families showed high diversity and low abundance in the 37 species, and their proportion was significantly higher in solitary bees than in social bees. DD34D/mariner was found to be distributed in almost all species and was found in Apis mellifera, Apis mellifera carnica, Apis mellifera caucasia, and Apis mellifera mellifera, and Euglossa dilemma may still be active. Using horizontal transfer analysis, we found that DD29-30D/Tigger may have experienced horizontal transfer (HT) events. The current study displayed the evolution profiles (including diversity, activity, and abundance) of the pogo and Tc1/mariner transposons across 37 species of Apoidea. Our data revealed their contributions to the genomic variations across these species and facilitated in understanding of the genome evolution of this lineage.
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Transposable elements (TEs) exert a significant effect on the structure and functioning of the genomes and also serve as a source of the new genes. The study of the TE diversity and evolution in different taxa is indispensable for the fundamental understanding of their roles in the genomes. IS630/Tc1/mariner (ITm) transposable elements represent the most prevalent and diverse group of DNA transposons. In this work, we studied the diversity, evolutionary dynamics and the phylogenetic relationships of the ITm transposons found in three ctenophore species: Mnemiopsis leidyi, Pleurobrachia bachei, Beroe ovata. We identified 29 ITm transposons, seven of which possess the terminal inverted repeats (TIRs) and an intact transposase, and, thus, are, presumably, active. Four other ITm transposons have the features of domesticated TEs. According to the results of the phylogenetic analysis, the ITm transposons of the ctenophores represent five groups - MLE/DD34D, TLE/DD34-38E, mosquito/DD37E, Visiror/DD41D and pogo/DDxD. Pogo/DDxD superfamily turnes out to be the most diverse and prevalent, since it accounts for more than 40% of the TEs identified. The data obtained in this research will fill the gap of knowledge of the diversity and evolution of the ITm transposons in the multicellular genomes and will lay the ground for the study of the TE effects on the evolution of the ctenophores.
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Ctenóforos , Culicidae , Animais , Ctenóforos/genética , Elementos de DNA Transponíveis/genética , Filogenia , Transposases/genéticaRESUMO
DNA transposons play a significant role in shaping the size and structure of eukaryotic genomes. The Tc1/mariner transposons are the most diverse and widely distributed superfamily of DNA transposons and the structure and distribution of several Tc1/mariner families, such as DD35E/TR, DD36E/IC, DD37E/TRT, and DD41D/VS, have been well studied. Nonetheless, a greater understanding of the structure and diversity of Tc1/mariner transposons will provide insight into the evolutionary history of eukaryotic genomes. Here, we conducted further analysis of DD37D/maT and DD39D (named Guest, GT), which were identified by the specific catalytic domains DD37D and DD39D. Most transposons of the maT family have a total length of approximately 1.3 kb and harbor a single open reading frame encoding a ~ 346 amino acid (range 302-398 aa) transposase protein, flanked by short terminal inverted repeats (TIRs) (13-48 base pairs, bp). In contrast, GTs transposons were longer (2.0-5.8 kb), encoded a transposase protein of ~400 aa (range 140-592 aa), and were flanked by short TIRs (19-41 bp). Several conserved motifs, including two helix-turn-helix (HTH) motifs, a GRPR (GRKR) motif, a nuclear localization sequence, and a DDD domain, were also identified in maT and GT transposases. Phylogenetic analyses of the DDD domain showed that the maT and GT families each belong to a monophyletic clade and appear to be closely related to DD41D/VS and DD34D/mariner. In addition, maTs are mainly distributed in invertebrates (144 species), whereas GTs are mainly distributed in land plants through a small number of GTs are present in Chromista and animals. Sequence identity and phylogenetic analysis revealed that horizontal transfer (HT) events of maT and GT might occur between kingdoms and phyla of eukaryotes; however, pairwise distance comparisons between host genes and transposons indicated that HT events involving maTs might be less frequent between invertebrate species and HT events involving GTs may be less frequent between land plant species. Overall, the DD37D/maT and DD39D/GT families display significantly different distribution and tend to be identified in more ancient evolutionary families. The discovery of intact transposases, perfect TIRs, and target site duplications (TSD) of maTs and GTs illustrates that the DD37D/maT and DD39D/GT families may be active. Together, these findings improve our understanding of the diversity of Tc1/mariner transposons and their impact on eukaryotic genome evolution.
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Elementos de DNA Transponíveis/genética , Eucariotos/genética , Evolução Molecular , Transposases/genética , Animais , Invertebrados/genética , FilogeniaRESUMO
The number of reports concerning horizontal transposon transfers (HTT) in metazoan species is considerably increased, alongside with the exponential growth of genomic sequence data However, our understanding of the mechanisms of such phenomenon is still at an early stage. Nematodes constitute an animal phylum successfully adapted to almost every ecosystem and for this reason could potentially contribute to spreading the genetic information through horizontal transfer. To date, few studies describe HTT of nematode retrotransposons. This is due to the lack of annotation of transposable elements in the sequenced nematode genomes, especially DNA transposons, which are acknowledged as the best horizontal travelers among mobile sequences. We have therefore started a survey of DNA transposons and their possible involvement in HTT in sequenced nematode genomes. Here, we describe 83 new Tc1/mariner elements distributed in 17 nematode species. Among them, nine families were possibly horizontally transferred between nematodes and the most diverse animal species, including ants as preferred partner of HTT. The results obtained suggest that HTT events involving nematodes Tc1/mariner elements are not uncommon, and that nematodes could have a possible role as transposon reservoir that, in turn, can be redistributed among animal genomes. Overall, this could be relevant to understand how the inter-species genetic flows shape the landscape of genetic variation of organisms inhabiting specific environmental communities.
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Elementos de DNA Transponíveis/genética , Genoma , Nematoides/genética , Animais , Evolução Biológica , Bases de Dados Genéticas , Transferência Genética Horizontal , Nematoides/classificação , Filogenia , RNA Ribossômico 18S/classificação , RNA Ribossômico 18S/genéticaRESUMO
BACKGROUND: A 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. RESULTS: Here, 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. CONCLUSIONS: We 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.
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BACKGROUND: Tc1/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. RESULTS: Here, 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. CONCLUSIONS: This 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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Although the DD41D (named as Visitor, VS) family of Tc1/mariner transposons was discovered in Arthropods and Mollusca, the evolution profile of this family is still largely unknown. We found that VS is widespread in the animal kingdom, including 140 species of 18 orders in invertebrates and 30 species of 12 orders in vertebrates, and one land plant species. Our data revealed multiple horizontal transfer events in both invertebrates and vertebrates and invasion into multiple lineages of mammals, including Chiroptera (seven species), Dasyuromorphia/Marsupialia (one species), Didelphimorphia/Marsupialia (one species), Diprotodontia/Marsupialia (two species), and Primates (one species). Phylogenetic analysis revealed a close relationship of VSs to DD37D/maT and DD34D/mariner and confirmed that VSs with the DD40D signature identified previously are not a distinct family but originated from DD41D/VS. Age analysis revealed that the most recent invasion of VSs was found in ray-finned fishes and a toad, followed by relatively young invasions in bats and marsupials, whereas VSs in mammals, jawless fishes, and lizards were mainly represented by ancient copies, suggesting old age. Phylogenetic analyses and comparison of pairwise distances between VSs and recombination-activating gene 1 (RAG1) support horizontal transfer events of VSs in vertebrates. The intact VSs from bats were nonfunctional as determined by the transposition activity assay. Some vertebrate lineages and species were identified as the hot hosts of Tc1/mariner transposons. Overall, our study presents the evolution profile of VSs and suggests that VSs play roles in diversifying and shaping the genomes of diverse animal lineages.
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Evolução Biológica , Elementos de DNA Transponíveis , Invertebrados/genética , Vertebrados/genética , Animais , Proteínas de Ligação a DNA , Transferência Genética Horizontal , TransposasesRESUMO
Here, we comprehensively analysed the abundance, diversity, and activity of Tc1/mariner transposons in African coelacanth (Latimeria chalumnae). Fifteen Tc1/mariner autonomous transposons were identified and grouped into six clades: DD34E/Tc1, DD34D/mariner, DD35D/Fot, DD31D/pogo, DD30-31D/pogo-like, and DD32-36D/Tigger, belonging to three known families: DD34E/Tc1, DD34D/mariner, and DD×D/pogo (DD35D/Fot, DD31D/pogo, DD30-31D/pogo-like, and DD32-36D/Tigger). Thirty-one miniature inverted-repeat transposable element (MITE) transposons of Tc1/mariner were also identified, and 20 of them display similarity to the identified autonomous transposons. The structural organization of these full Tc1/mariner elements includes a transposase gene flanked by terminal inverted repeats (TIRs) with TA dinucleotides. The transposases contain N-terminal DNA binding domain and a C-terminal catalytic domain characterized by the presence of a conservative D(Asp)DE(Glu)/D triad that is essential for transposase activity. The Tc1/mariner superfamily in coelacanth exhibited very low genome coverage (0.3%), but it experienced an extraordinary difference of proliferation dynamics among the six clades identified; moreover, most of them exhibited a very recent and current proliferation, suggesting that some copies of these transposons are putatively active. Additionally, at least four functional genes derived from Tc1/mariner transposons were found. We provide an up-to-date overview of Tc1/mariner in coelacanth, which may be helpful in determining genome and gene evolution in this living fossil.
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Elementos de DNA Transponíveis , Peixes/genética , Animais , Evolução Molecular , Filogenia , Transposases/genéticaRESUMO
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 â¼1.5 kb (range 1,072-2,191 bp) and harbored a single open reading frame encoding a transposase of â¼340 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.
Assuntos
Elementos de DNA Transponíveis , Evolução Molecular , Animais , Sequência de Bases , Sequência Conservada , Filogenia , Vertebrados/genéticaRESUMO
BACKGROUND: The 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. RESULTS: Here 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. CONCLUSIONS: Exploring 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.