Horizontal Transposon Transfer in Eukarya: Detection, Bias, and Perspectives

Wallau, Gabriel Luz; Ortiz, Mauro Freitas; Loreto, Élgion Lúcio Silva

doi:10.1093/gbe/evs055

Cited by 113 publications

(124 citation statements)

References 80 publications

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“…However, these distributions are not known, and consequently, the sympatric relationships between the species that belong to the 13,551 monocots and dicots genera cannot be established. Nevertheless, our estimation exceeds by several orders of magnitude the number of HTTs documented until now in both plants and animals (Wallau et al 2012). The last 20 yr of genomic studies in plants have demonstrated the impact of TEs on the structure, evolution, and function of eukaryotic genomes (Feschotte 2008;Rebollo et al 2012).…”

Section: Discussioncontrasting

confidence: 54%

“…However, although horizontal gene transfers are very common in Bacteria (Rocha 2013), evidence of HTTs in eukaryotes remains scarce, although recent reports suggest their potential impact in genome evolution . Three criteria have been defined for the detection of HTTs: patchy distributions of TEs in phylogenies; identification of TEs exhibiting high sequence similarity between distantly related taxa; and phylogenetic incongruence between the host and TEs Kuraku et al 2012;Wallau et al 2012;Walsh et al 2013). An exhaustive search for HTTs that meet these three criteria in a wide taxonomic range thus requires a comprehensive set of genomic resources.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

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Widespread and frequent horizontal transfers of transposable elements in plants

et al. 2014

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Vertical, transgenerational transmission of genetic material occurs through reproduction of living organisms. In addition to vertical inheritance, horizontal gene transfer between reproductively isolated species has recently been shown to be an important, if not dominant, mechanism in the evolution of prokaryotic genomes. In contrast, only a few horizontal transfer (HT) events have been characterized so far in eukaryotes and mainly concern transposable elements (TEs). Whether these are frequent and have a significant impact on genome evolution remains largely unknown. We performed a computational search for highly conserved LTR retrotransposons among 40 sequenced eukaryotic genomes representing the major plant families. We found that 26 genomes (65%) harbor at least one case of horizontal TE transfer (HTT). These transfers concern species as distantly related as palm and grapevine, tomato and bean, or poplar and peach. In total, we identified 32 cases of HTTs, which could translate into more than 2 million among the 13,551 monocot and dicot genera. Moreover, we show that these TEs have remained functional after their transfer, occasionally causing a transpositional burst. This suggests that plants can frequently exchange genetic material through horizontal transfers and that this mechanism may be important in TE-driven genome evolution.

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Section: Discussioncontrasting

confidence: 54%

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Widespread and frequent horizontal transfers of transposable elements in plants

et al. 2014

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“…S2). Third, we conservatively collapsed many species into lineages within which HTT events have been characterized in previous studies (9). Fourth, the available insect genome sequences represent a very small fraction of the known diversity of insects.…”

Section: Significancementioning

confidence: 99%

“…In fact, most of the genetic material that is horizontally transferred in animals and plants consists of transposable elements (TEs) (9)(10)(11), which are pieces of DNA able to move from a chromosomal locus to another (12). The greater ability of TEs to move between organisms certainly relates to their intrinsic ability to transpose within genomes, which genes cannot do.…”

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confidence: 99%

Massive horizontal transfer of transposable elements in insects

Peccoud

Loiseau

Cordaux

et al. 2017

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

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Horizontal transfer (HT) of genetic material is central to the architecture and evolution of prokaryote genomes. Within eukaryotes, the majority of HTs reported so far are transfers of transposable elements (TEs). These reports essentially come from studies focusing on specific lineages or types of TEs. Because of the lack of large-scale survey, the amount and impact of HT of TEs (HTT) in eukaryote evolution, as well as the trends and factors shaping these transfers, are poorly known. Here, we report a comprehensive analysis of HTT in 195 insect genomes, representing 123 genera and 13 of the 28 insect orders. We found that these insects were involved in at least 2,248 HTT events that essentially occurred during the last 10 My. We show that DNA transposons transfer horizontally more often than retrotransposons, and unveil phylogenetic relatedness and geographical proximity as major factors facilitating HTT in insects. Even though our study is restricted to a small fraction of insect biodiversity and to a recent evolutionary timeframe, the TEs we found to be horizontally transferred generated up to 24% (2.08% on average) of all nucleotides of insect genomes. Together, our results establish HTT as a major force shaping insect genome evolution.horizontal transfer | transposable elements | insects | genome evolution | biogeography H orizontal transfer (HT) is the transmission of genetic material between organisms through a mechanism other than reproduction. In prokaryotes, HT is pervasive, its mechanisms are well understood, and it is now viewed as one of the main forces shaping genome architecture and evolution (1, 2). In contrast, the study of HT in eukaryotes is less documented, but has been increasingly investigated. The majority of genes horizontally acquired by eukaryotes come from bacteria, but the extent to which these transfers have contributed to eukaryote evolution is still unclear (3, 4). Gene transfers from eukaryote to eukaryote appear to be largely limited to filamentous organisms, such as oomycetes and fungi (5, 6).In animals and plants, very few cases of such horizontal gene transfers (HGTs) have been reported so far (7,8). In fact, most of the genetic material that is horizontally transferred in animals and plants consists of transposable elements (TEs) (9-11), which are pieces of DNA able to move from a chromosomal locus to another (12). The greater ability of TEs to move between organisms certainly relates to their intrinsic ability to transpose within genomes, which genes cannot do. HT of TEs (HTT) may allow these elements to enter naive genomes, which they invade by making copies of themselves, and then escape before they become fully silenced by anti-TE defenses (13). A growing number of studies have identified such HTT (11,[14][15][16]. However, a common drawback of these studies has been the inclusion of a limited set of TEs (11) or organisms (16), which hampers our understanding of the breadth of HTT, its contribution to genome evolution, and of the factors and barriers shaping these transfe...

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“…However, compelling evidence in a wide variety of taxa has increasingly revealed that Horizontal Transfer (HT), the exchange of genetic material between isolated sexual species, is an effective way in which TEs invade new genomes and colonize other species [11,12]. Currently, around 2853 Horizontal Transposon Transfer (HTT) events have been reported [13].…”

Section: Introductionmentioning

confidence: 99%

Evolutionary history of the mariner element galluhop in avian genomes

et al. 2017

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Background: Transposable elements (TEs) are highly abundant genomic parasites in eukaryote genomes. Although several genomes have been screened for TEs, so far very limited information is available regarding avian TEs and their evolutionary histories. Taking advantage of the rich genomic data available for birds, we characterized the evolutionary history of the galluhop element, originally described in Gallus gallus, through the use of several bioinformatic analyses. Results: galluhop homologous sequences were found in 6 of 72 genomes analyzed: 5 species of Galliformes (Gallus gallus, Meleagris gallopavo, Coturnix japonica, Colinus virginianus, Lyrurus tetrix) and one Buceritiformes (Buceros rhinoceros). The copy number ranged from 5 to 10,158, in the genomes of C. japonica and G. gallus respectively. All 6 species possessed short elements, suggesting the presence of Miniature Inverted repeats Transposable Elements (MITEs), which underwent an ancient massive amplification in the G. gallus and M. gallopavo genomes. Only 4 species showed potential MITE full-length partners, although no potential coding copies were detected. Phylogenetic analysis of reconstructed coding sequences showed that galluhop homolog sequences form a new mariner subfamily, which we termed Gallus. Inter-species and intragenomic galluhop distance analyses indicated a high identity between the consensus of B. rhinoceros and the other 5 related species, and different emergence ages of the element between the Galliformes species and B. rhinocerus, suggesting that horizontal transfer took place from Galliformes to a Buceritiformes ancestor, probably through an intermediate species.Conclusions: Overall, our results showed that mariner elements have amplified to high copy numbers in some avian species, and that this transposition burst probably occurred in the common ancestor of G. gallus and M. gallopavo. In addition, although no coding sequences could be found currently, they probably existed, allowing an ancient massive MITE amplification in these 2 species. The other 4 species also have MITEs, suggesting that this new mariner family is prone to give rise to such non-autonomous derivatives. Last, our results suggest that a horizontal transfer event of a galluhop element occurred between Galliformes and Buceritiformes.

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Horizontal Transposon Transfer in Eukarya: Detection, Bias, and Perspectives

Cited by 113 publications

References 80 publications

Widespread and frequent horizontal transfers of transposable elements in plants

Widespread and frequent horizontal transfers of transposable elements in plants

Massive horizontal transfer of transposable elements in insects

Evolutionary history of the mariner element galluhop in avian genomes

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