Horizontal Escape of the Novel Tc1-Like Lepidopteran Transposon TCp3.2 into Cydia pomonella Granulovirus

Jehle, Johannes A.; Nickel, Antje; Vlak, Just M.; Backhaus, Horst

doi:10.1007/pl00006296

Cited by 71 publications

(59 citation statements)

References 41 publications

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“…It is also not possible to distinguish whether each tetrapod species acquired SPIN independently from the same exogenous source (e.g., a common prey or parasite) or whether SPIN was acquired once by a tetrapod species from an exogenous source and then spread by HT between tetrapod species. The mechanisms underlying such recurrent HTs remain to be clarified, but we note that DNA viruses are increasingly recognized as potential intermediates for HT of mobile elements between widely divergent animals (20,(34)(35)(36). Recently Piskurek and Okada (20) reported on the transfer of a snake retroposon into the genome of taterapox virus, a poxvirus that infects West African rodents.…”

Section: Discussionmentioning

confidence: 99%

Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods

Pace

Gilbert

Clark

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

196

214

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Horizontal transfer (HT) is central to the evolution of prokaryotic species. Selfish and mobile genetic elements, such as phages, plasmids, and transposons, are the primary vehicles for HT among prokaryotes. In multicellular eukaryotes, the prevalence and evolutionary significance of HT remain unclear. Here, we identified a set of DNA transposon families dubbed SPACE INVADERS (or SPIN) whose consensus sequences are Ϸ96% identical over their entire length (2.9 kb) in the genomes of murine rodents (rat/mouse), bushbaby (prosimian primate), little brown bat (laurasiatherian), tenrec (afrotherian), opossum (marsupial), and two non-mammalian tetrapods (anole lizard and African clawed frog). In contrast, SPIN elements were undetectable in other species represented in the sequence databases, including 19 other mammals with draft whole-genome assemblies. This patchy distribution, coupled with the extreme level of SPIN identity in widely divergent tetrapods and the overall lack of selective constraint acting on these elements, is incompatible with vertical inheritance, but strongly indicative of multiple horizontal introductions. We show that these germline infiltrations likely occurred around the same evolutionary time (15-46 mya) and spawned some of the largest bursts of DNA transposon activity ever recorded in any species lineage (nearly 100,000 SPIN copies per haploid genome in tenrec). The process also led to the emergence of a new gene in the murine lineage derived from a SPIN transposase. In summary, HT of DNA transposons has contributed significantly to shaping and diversifying the genomes of multiple mammalian and tetrapod species. genome evolution ͉ lateral gene transfer ͉ transposable elements ͉ transposase L ateral or horizontal transfer (HT), the transfer of genetic material between reproductively isolated species, is a frequent occurrence in prokaryotes with selfish and mobile genetic elements such as phages, plasmids, and transposons, serving as the primary vehicles for HT of prokaryotic genes (1). In contrast, reports of HT are scarce in eukaryotes and most cases of nuclear acquisition implicate transfers from prokaryotes or endosymbionts (2-6). The best documented instances of HT between the nuclear genomes of multicellular eukaryotes involve mobile genetic elements, and in particular class 2 or DNA mediated transposons (7,8). Thus far, conspicuous cases of HT of DNA transposons have been detected among insects (8-12), fish (13) and, in one example, between plants (14). Germline invasions by retroviruses have been documented for several mammals (15-18), and there is mounting evidence supporting the horizontal introduction of a snake retroposon in ruminants (19,20). However, to our knowledge, there has been no substantiated report of HT of DNA transposons in mammals. Here, we present unequivocal evidence for the repeated HT of a DNA transposon family named SPACE INVADERS in 7 tetrapod lineages, including 5 mammalian orders. ResultsDiscovery of SPIN Transposons. While surveying DNA transposons in the draft...

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Section: Discussionmentioning

confidence: 99%

Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods

Pace

Gilbert

Clark

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

196

214

View full text Add to dashboard Cite

show abstract

“…Like viruses, DNA transposons are examples of genomic parasites, and the ability of bats to safely harbor large loads of a variety of viruses may suggest similar genetic tolerance with regard to DNA transposons. On the other hand, viruses remain the best candidates as potential vectors for the horizontal introduction of DNA transposons and other TEs (Miller and Miller 1982;Fraser et al 1983;Jehle et al 1998;Piskurek and Okada 2007). Thus, the propensity of bats to tolerate massive and diverse viral infections may have facilitated the recurrent horizontal introduction of DNA transposons and/ or their evolutionary persistence in vespertilionid bats.…”

Section: Discussionmentioning

confidence: 99%

Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus

Ray¹,

Feschotte²,

Pagán³

et al. 2008

Genome Res.

150

163

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DNA transposons, or class 2 transposable elements, have successfully propagated in a wide variety of genomes. However, it is widely believed that DNA transposon activity has ceased in mammalian genomes for at least the last 40 million years. We recently reported evidence for the relatively recent activity of hAT and Helitron elements, two distinct groups of DNA transposons, in the lineage of the vespertilionid bat Myotis lucifugus. Here, we describe seven additional families that have also been recently active in the bat lineage. Early vespertilionid genome evolution was dominated by the activity of Helitrons, mariner-like and Tc2-like elements. This was followed by the colonization of Tc1-like elements, and by a more recent explosion of hAT-like elements. Finally, and most recently, piggyBac-like elements have amplified within the Myotis genome and our results indicate that one of these families is probably still expanding in natural populations. Together, these data suggest that there has been tremendous recent activity of various DNA transposons in the bat lineage that far exceeds those previously reported for any mammalian lineage. The diverse and recent populations of DNA transposons in genus Myotis will provide an unprecedented opportunity to study the impact of this class of elements on mammalian genome evolution and to better understand what makes some species more susceptible to invasion by genomic parasites than others.

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“…Repeated horizontal input of these elements, perhaps from some closely associated source, such as a parasite or a symbiont, is a definite possibility, and this scenario is commonly invoked for evolution of mariner͞Tc transposons (12,14,50). Indeed, horizontal escape of a Tc-like transposon has been reported from a lepidopteran genome into a closely associated granulovirus (51), and a Tc-like transposon has been detected in the genome of the prokaryotic Wolbachia endosymbiont of Drosophila ananassae (gi accession no. 58698412) and in the assembled genomic contigs of its host (http:͞͞genome.ucsc.edu͞cgi-bin͞hgBlat?dbϭdroAna1).…”

Section: Discussionmentioning

confidence: 99%

Diverse DNA transposons in rotifers of the class Bdelloidea

Arkhipova

Meselson

2005

Proc. Natl. Acad. Sci. U.S.A.

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We surveyed the diversity, structural organization, and patterns of evolution of DNA transposons in rotifers of the class Bdelloidea, a group of basal triploblast animals that appears to have evolved for millions of years without sexual reproduction. Representatives of five superfamilies were identified: ITm (IS630͞Tc͞mariner), hAT, piggyBac, helitron, and foldback. Except for mariners, no fully intact copies were found. Mariners, both intact and decayed, are present in high copy number, and those described here may be grouped in several closely related lineages. Comparisons across lineages show strong evidence of purifying selection, whereas there is little or no evidence of such selection within lineages. This pattern could have resulted from repeated horizontal transfers from an exogenous source, followed by limited intragenomic proliferation, or, less plausibly, from within-host formation of new lineages under host-or element-based selection for function, in either case followed by eventual inactivation and decay. Unexpectedly, the flanking sequences surrounding the majority of mariners are very similar, indicating either insertion specificity or proliferation as part of larger DNA segments. Members of all superfamilies are present near chromosome ends, associated with the apparently domesticated retroelement Athena, in large clusters composed of diverse DNA transposons, often inserted into each other, whereas the examined gene-rich regions are nearly transposon-free.foldback ͉ hAT ͉ helitron ͉ mariner ͉ piggyBac

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Horizontal Escape of the Novel Tc1-Like Lepidopteran Transposon TCp3.2 into Cydia pomonella Granulovirus

Cited by 71 publications

References 41 publications

Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods

Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods

Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus

Diverse DNA transposons in rotifers of the class Bdelloidea

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