Birth of Three Stowaway-like MITE Families via Microhomology-Mediated Miniaturization of a Tc1/Mariner Element in the Yellow Fever Mosquito

Yang, Guojun; Fattash, Isam; Lee, Chia-Ni; Liu, Kun; Cavinder, Brad

doi:10.1093/gbe/evt146

Cited by 6 publications

(7 citation statements)

References 88 publications

(97 reference statements)

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“…While the truncated Tdr1 copies always carried sequences of various lengths between the IR/DRs (over 400 bps, Supplementary Figure S1), variants lacking the entire internal part, and basically consisting only of the IRs are detectable only in the Hsmar1 population (Supplementary Figure S2). These structures are known as m iniature i nverted repeat t ransposable e lements or MITEs, and seem to be generally associated with mariners (30,32,33). Curiously, while various Hsmar1 -derived MITE-like structures are detectable in the human genome, one particular variant, consisting from two, 37-bp IRs linked by a 6-bp intervening sequence appears to have been preferentially amplified (Figure 1E).…”

Section: Resultsmentioning

confidence: 99%

Regulated complex assembly safeguards the fidelity ofSleeping Beautytransposition

Wang

Pryputniewicz-Dobrinska

Nagy

et al. 2016

Nucleic Acids Res

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The functional relevance of the inverted repeat structure (IR/DR) in a subgroup of the Tc1/mariner superfamily of transposons has been enigmatic. In contrast to mariner transposition, where a topological filter suppresses single-ended reactions, the IR/DR orchestrates a regulatory mechanism to enforce synapsis of the transposon ends before cleavage by the transposase occurs. This ordered assembly process shepherds primary transposase binding to the inner 12DRs (where cleavage does not occur), followed by capture of the 12DR of the other transposon end. This extra layer of regulation suppresses aberrant, potentially genotoxic recombination activities, and the mobilization of internally deleted copies in the IR/DR subgroup, including Sleeping Beauty (SB). In contrast, internally deleted sequences (MITEs) are preferred substrates of mariner transposition, and this process is associated with the emergence of Hsmar1-derived miRNA genes in the human genome. Translating IR/DR regulation to in vitro evolution yielded an SB transposon version with optimized substrate recognition (pT4). The ends of SB transposons excised by a K248A excision+/integration- transposase variant are processed by hairpin resolution, representing a link between phylogenetically, and mechanistically different recombination reactions, such as V(D)J recombination and transposition. Such variants generated by random mutation might stabilize transposon-host interactions or prepare the transposon for a horizontal transfer.

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Section: Resultsmentioning

confidence: 99%

Regulated complex assembly safeguards the fidelity ofSleeping Beautytransposition

Wang

Pryputniewicz-Dobrinska

Nagy

et al. 2016

Nucleic Acids Res

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“…S3 , Supplementary Material online), which may generate small noncoding RNAs involved in gene regulation, as reported for the Nezha MITE found in cyanobacteria ( Zhou et al 2008 ). If such miniature copies are subject to subsequent amplification, this process may give rise to a homogeneous group of elements: A MITE family ( Feschotte et al 2002 ; Yang et al 2013 ). The five L. waltii miniature copies are highly conserved: They are collinear and present 93–100% nucleotide identity ( fig.…”

Section: Resultsmentioning

confidence: 99%

“…MITEs derived from hAT elements with autonomous copies in the same genome have so far been reported only in plants ( Saito et al 2005 ; Benjak et al 2009 ) and animals ( Pace et al 2008 ; Zhang et al 2013 ). Different molecular mechanisms have been proposed to explain the formation of miniature copies by internal deletions; recombination between microhomologies is often evoked ( Negoua et al 2013 ; Yang et al 2013 ). Such mechanism may also occur in yeasts, as hexameric microhomologies have been characterized in Rover1.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary Dynamics of hAT DNA Transposon Families in Saccharomycetaceae

Sarilar

Bleykasten-Grosshans

Neuvéglise

2014

Genome Biology and Evolution

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Transposable elements (TEs) are widespread in eukaryotes but uncommon in yeasts of the Saccharomycotina subphylum, in terms of both host species and genome fraction. The class II elements are especially scarce, but the hAT element Rover is a noteworthy exception that deserves further investigation.Here, we conducted a genome-wide analysis of hAT elements in 40 ascomycota. A novel family, Roamer, was found in three species, whereas Rover was detected in 15 preduplicated species from Kluyveromyces, Eremothecium, and Lachancea genera, with up to 41 copies per genome. Rover acquisition seems to have occurred by horizontal transfer in a common ancestor of these genera. The detection of remote Rover copies in Naumovozyma dairenensis and in the sole Saccharomyces cerevisiae strain AWRI1631, without synteny, suggests that two additional independent horizontal transfers took place toward these genomes. Such patchy distribution of elements prevents any anticipation of TE presence in incoming sequenced genomes, even closely related ones.The presence of both putative autonomous and defective Rover copies, as well as their diversification into five families, indicate particular dynamics of Rover elements in the Lachancea genus. Especially, we discovered the first miniature inverted-repeat transposable elements (MITEs) to be described in yeasts, together with their parental autonomous copies. Evidence of MITE insertion polymorphism among Lachancea waltii strains suggests their recent activity. Moreover, 40% of Rover copies appeared to be involved in chromosome rearrangements, showing the large structural impact of TEs on yeast genome and opening the door to further investigations to understand their functional and evolutionary consequences.

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“…According to the TEfam database (http://tefam.biochem.vt.edu/tefam/), the mosquito genome has at least 143 MITE families, with a total copy number of at least 420 000. Gnome is the youngest MITE family in the genome , with a large number (116) of identical copies. Gnome is also the youngest known animal MITE family.…”

Section: Introductionmentioning

confidence: 99%

“…Gnome is also the youngest known animal MITE family. The putative autonomous element named Ozma is the direct ancestral element for Gnome . Ozma is a novel element belonging to the recently identified ITmD37E subgroup of the Tc1 / mariner superfamily .…”

Section: Introductionmentioning

confidence: 99%

Efficient transposition of the youngest miniature inverted repeat transposable element family of yellow fever mosquito in yeast

Fattash

Lee

et al. 2015

The FEBS Journal

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Miniature inverted repeat transposable elements (MITEs) are often the most numerous DNA transposons in plant and animal genomes. The dramatic amplification of MITE families during evolution is puzzling, because the transposase sources for the vast majority of MITE families are unknown. The yellow fever mosquito genome contains > 220-Mb MITE sequences; however, transposition activity has not been demonstrated for any of the MITE families. The Gnome elements are the youngest MITE family in this genome, with at least 116 identical copies. To test whether the putative autonomous element Ozma is capable of mobilizing Gnome and its two sibling MITEs, analyses were performed in a yeast transposition assay system. Whereas the wild-type transposase resulted in very low transposition activity, mutations in the region containing a putative nuclear export signal motif resulted in a dramatic (at least 4160-fold) increase in transposition frequency. We have also demonstrated that each residue of the novel DD37E motif is required for the activity of the Ozma transposase. Footprint sequences left at the donor sites suggest that the transposase may cleave between the second and the third nucleotides from the 5' ends of the elements. The excised elements reinsert specifically at dinucleotide 'TA',~55% of them in yeast genes. The elements described in this article could potentially be useful as genetic tools for genetic manipulation of mosquitoes.

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Birth of Three Stowaway-like MITE Families via Microhomology-Mediated Miniaturization of a Tc1/Mariner Element in the Yellow Fever Mosquito

Cited by 6 publications

References 88 publications

Regulated complex assembly safeguards the fidelity ofSleeping Beautytransposition

Regulated complex assembly safeguards the fidelity ofSleeping Beautytransposition

Evolutionary Dynamics of hAT DNA Transposon Families in Saccharomycetaceae

Efficient transposition of the youngest miniature inverted repeat transposable element family of yellow fever mosquito in yeast

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