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, the Eukaryotic Rolling-circle Transposable Elements

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  • Authors: Jainy Thomas1, Ellen J. Pritham2
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    Affiliations: 1: Department of Human Genetics, University of Utah, Salt Lake City, UT 84112; 2: Department of Human Genetics, University of Utah, Salt Lake City, UT 84112; 3: Université Paul Sabatier, Toulouse, France, MD; 4: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
  • Received 08 August 2014 Accepted 22 December 2014 Published 02 July 2015
  • Ellen Pritham, pritham@genetics.utah.edu
image of <span class="jp-italic">Helitrons</span>, the Eukaryotic Rolling-circle Transposable Elements
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  • Abstract:

    , the eukaryotic rolling-circle transposable elements, are widespread but most prevalent among plant and animal genomes. Recent studies have identified three additional coding and structural variants of called , , and . and make up a substantial fraction of many genomes where nonautonomous elements frequently outnumber the putative autonomous partner. This includes the previously ambiguously classified DINE-1-like repeats, which are highly abundant in and many other animal genomes. The purpose of this review is to summarize what we have learned about in the decade since their discovery. First, we describe the history of autonomous , and their variants. Second, we explain the common coding features and difference in structure of canonical versus the endonuclease-encoding . Third, we review how and are classified and discuss why the system used for other transposable element families is not applicable. We also touch upon how genome-wide identification of candidate is carried out and how to validate candidate . We then shift our focus to a model of transposition and the report of an excision event. We discuss the different proposed models for the mechanism of gene capture. Finally, we will talk about where are found, including discussions of vertical versus horizontal transfer, the propensity of and to capture and shuffle genes and how they impact the genome. We will end the review with a summary of open questions concerning the biology of this intriguing group of transposable elements.

  • Citation: Thomas J, Pritham E. 2015. , the Eukaryotic Rolling-circle Transposable Elements. Microbiol Spectrum 3(4):MDNA3-0049-2014. doi:10.1128/microbiolspec.MDNA3-0049-2014.

Key Concept Ranking

Protein Phosphatase 1
0.4511114
DNA Transposons
0.42165303
0.4511114

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/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0049-2014
2015-07-02
2017-07-26

Abstract:

, the eukaryotic rolling-circle transposable elements, are widespread but most prevalent among plant and animal genomes. Recent studies have identified three additional coding and structural variants of called , , and . and make up a substantial fraction of many genomes where nonautonomous elements frequently outnumber the putative autonomous partner. This includes the previously ambiguously classified DINE-1-like repeats, which are highly abundant in and many other animal genomes. The purpose of this review is to summarize what we have learned about in the decade since their discovery. First, we describe the history of autonomous , and their variants. Second, we explain the common coding features and difference in structure of canonical versus the endonuclease-encoding . Third, we review how and are classified and discuss why the system used for other transposable element families is not applicable. We also touch upon how genome-wide identification of candidate is carried out and how to validate candidate . We then shift our focus to a model of transposition and the report of an excision event. We discuss the different proposed models for the mechanism of gene capture. Finally, we will talk about where are found, including discussions of vertical versus horizontal transfer, the propensity of and to capture and shuffle genes and how they impact the genome. We will end the review with a summary of open questions concerning the biology of this intriguing group of transposable elements.

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FIGURE 1

Structure and coding capacity of canonical animal and plant , , , and IS. (A) Structure of a typical animal . (B) A typical plant encoding Rep/Helicase and RPA proteins; one to three RPA genes can be found on either side of the Rep/Helicase gene. (C) Structure of a typical nonautonomous plant or animal ; they do not encode the Rep/Helicase gene but share the common structural features. (D) Structure and coding capacity of a ; have sub terminal inverted repeats (subTIRs) (red), and a short palindrome at the 3′ end (stem loop). The subTIRs can either be palindromic or form a palindrome with the short inverted repeats (sideways triangle), near the subTIR, if present. (E) Structure of a -associated INterspersed Element (); s are nonautonomous but have the same structural features as that of the autonomous partner. (F) Structure and coding capacity of (G) Structure and coding capacity of (redrawn from reference 12 ). (H) Structure of a bacterial IS element that is proposed to transpose by rolling-circle mechanism (redrawn from references 9 , 46 ). The genes that are occasionally carried by are indicated with a black asterisk (*) and are included only if they were found in multiple families or across species. Sequences flanking the elements are shown in red. doi:10.1128/microbiolspec.MDNA3-0049-2014.f1

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 2

Amino acid alignment of the Rep motifs of select and An alignment of the Rep motif of from 12 species and from seven species (redrawn from reference 11 ). Identical residues are shaded in black and conservative changes are shaded in gray. Amino acids that distinguish from are boxed in red. The black triangles and stars above the alignment denote the two histidine residues and the two tyrosines respectively, which are known to be critical for catalytic activity of the rolling-circle elements. Sequences representing have “Hele” and have “Helit” as suffix to the name of the organism. The accessions and coordinates of the sequences used in this alignment are available in reference 11 . doi:10.1128/microbiolspec.MDNA3-0049-2014.f2

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 3

Criteria for classifying and . (A) Classification criteria for ; colors of the 5′ and 3′ ends denote common ancestry. belong to the same family (Family A) when they share > 80% identity over the last 30 bp (denoted by an orange 3′ end). Subfamilies share 80% sequence identity in the 3′ end but have different 5′ ends (Family A, subfamily B). belonging to family C have a different 3′ end. Exemplars have internal sequences that are > 20% diverged compared with any other exemplar. (B) Classification criteria for belonging to the same family share 100% sequence identity across the 11-bp subterminal inverted repeats (subTIRs) (Family A). A subfamily has at least 80% identity over last 60 bp at the 3′ end (excluding variable Ts) (Family A, subfamily B). belonging to Family C have a different subTIR. Exemplars have internal sequences that are > 20% diverged. doi:10.1128/microbiolspec.MDNA3-0049-2014.f3

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 4

Genome-wide identification of (A) A pipeline for genome-wide identification of candidate and their verification. Examples of structure and repeat-based tools that could be used for annotating candidate are listed on the respective side. The black star denotes that they are pipelines that use a set of tools. (B) Alignment of two copies inserted at different locations to identify the boundary of the element. Homology drops at the boundary of the element and the sequences at the boundary have canonical features. (C) Empty site verification for a . The first line is host sequence with a insertion and the second line is the paralogous site without the insertion. (D) Alignment of two -associated INterspersed Element () copies at different locations to identify the boundary of the element. Homology drops at the boundary of the element. Since the insertion is in T-rich sequence, the precise boundary of the element can be unambiguously identified only through the identification of an empty site (E). Empty site verification of a copy. The first line is the host sequence containing insertion and second line is the paralogous site without insertion. The accession numbers and coordinates are given in black. doi:10.1128/microbiolspec.MDNA3-0049-2014.f4

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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Proposed model for the transposition of The blue line indicates the , the small triangle indicates the 5′ end of the and the star indicates the 3′ end of the . (A) The first tyrosine (Y1) residue of the Rep protein (shown as black oval) cleaves at the 5′ end of the in the donor strand (shown as green lines) and the second tyrosine (Y2) residue cleaves the target DNA (shown as black lines). The tyrosine residues covalently join to the 5′ end of the respective strands. (B) The free 3′ hydroxyl in the target DNA attacks the DNA–Y1 bond and forms a covalent bond with the donor strand resulting in strand transfer. The free 3′ hydroxyl in the donor strand serves as a primer for DNA synthesis by host DNA polymerase. The strand is displaced by 5′ to 3′ activity of the Helicase protein and remains single-stranded (ss) with the help of ssDNA-binding protein. (C) At the termination site, the free Y1 residue cleave the 3′ end and becomes covalently linked to the 5′ end of the nicked strand and initiates the strand transfer when the 3′ hydroxyl of the cleaved attacks the Y2 at the 5′ end of the target DNA and forms a covalent bond. (D) The heteroduplex is passively resolved by DNA replication (redrawn from references 2 , 46 ). doi:10.1128/microbiolspec.MDNA3-0049-2014.f5

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 6

-containing gene fragment captured at the DNA level and RNA level. (A) The structure of () exemplar that has captured the promoter, 5′ untranslated region (UTR), Exon1, and Intron1 of the (protein inhibitor of activated signal transducer and activator of transcription 1 [STAT-1]) gene, which inhibits STAT1-mediated gene activation and the DNA-binding activity. (B) Structure of the containing the cDNA of protein phosphatase 1, regulatory (inhibitor) subunit 12C () gene; contains seven exons (blue box), 3′ UTR (pink box), polyAs (yellowish green box) and 11-bp target site duplication (TSD) (purple arrows). (C) Empty site for the retroposed mRNA; first line is the containing the cDNA and second line is a paralogous site within another but without the retrogene. The black bold letters shows the TSD. The accession and coordinates of the are given. The flanking AT dinucleotide of the insertion is shown in red. doi:10.1128/microbiolspec.MDNA3-0049-2014.f6

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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Active transposition-based models for gene capture. (A) End bypass model ( 2 ). (a) The Rep/Helicase protein cleaves the 5′ end of the (red line) and invades the target site (blue line) (shown in c) (see transposition model, Figure 5 for details). (b and c) Capture of flanking sequence (black line) occurs when the protein fails to recognize the termination signal (black star). Later the transposition is terminated by a cryptic random termination signal (four star) and the donor strand is cleaved and transferred to the target site (redrawn from reference 2 ). (B) Modified end bypass/chimeric transposition model ( 69 ). (a) The Rep/Helicase protein cleaves the 5′ end of the (red line) and invades the target site (blue line). (b and c) Capture of the flanking sequence occurs when the protein fails to recognize the termination signal or the 3′ end is truncated. The 3′ end of another (green line) in the proper orientation is recognized and is used a new 3′ end, thus creating a novel composite element. The protein cleaves the donor strand at the new termination signal and the donor strand is transferred to the target site. doi:10.1128/microbiolspec.MDNA3-0049-2014.f7

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 8

Filler DNA model and site-specific recombination model of gene captures. (A) Filler DNA model (for review see reference 56 ). When a double-strand break occurs in the acceptor DNA () (red line), the host exonuclease creates 3′ single-stranded (ss) overhangs. The free 3′ ssDNA anneals to the donor DNA based on microhomology triggering the synthesis of new DNA, which then anneals back to the acceptor DNA. The new DNA acquired from the donor acts as the template for the other strand. Hence, the now contains host sequences from a random location, which could be of genic or nongenic origin depending on which region of the host was used for repair. (B) Site-specific recombination model ( 107 ). The sites of recombination are marked by crosses. The capture of the host sequence by the would require three recombinational events, one within and two flanking the host sequence. As do not encode integrase a host integrase is used for the capture. doi:10.1128/microbiolspec.MDNA3-0049-2014.f8

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 9

Distribution of across the eukaryotic tree of life. The four-pointed star shows the presence of , the five-pointed star represents the presence of , and the rectangular bars represent the presence of the Rep protein. The tree of life was redrawn from reference 192 . The numbers within parentheses represent the numbers of whole genome sequences available at the NCBI whole genome shotgun (wgs) database as per 18 June 2014 http://www.ncbi.nlm.nih.gov/. The plus sign within parentheses indicates that the respective element was identified from the transcriptome assembly deposited at the wgs database. The dot within parentheses indicates that were identified from the Mucorales group of fungi traditionally classified as a Zygomycete but are not deposited as Zygomycetes at NCBI. TBLASTN searches ( 193 ) were employed against the wgs database to identify sequences homologous to the Rep protein query and the signature amino acids (see Figure 2 ) were used to differentiate from proteins (we do not know how this correlates with structure outside of animals and plants). Hits with very low copy number and of short contigs were not reported because of the possibility of contamination. doi:10.1128/microbiolspec.MDNA3-0049-2014.f9

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 10

The abundance of -generated DNA in different organisms. The different organisms include (1.6%; 1.9/120 Mb), (1.2%; 5/419 Mb), spp. (4%; 15/374 Mb), (1%; 7.4/734 Mb), (6.6%; 136.4/2066 Mb) ( 83 ), (2.3%; 2.3/100 Mb) ( 81 ), (3%; 8.9/297 Mb) ( 133 ), (4.2%; 19.7/465.7 Mb) ( 84 ), (6.62%; 17.1/260 Mb) ( 84 ), (5%; 9.5/189 Mb) ( 56 ), and (5.8%; 109.5/1887 Mb) ( 51 ). doi:10.1128/microbiolspec.MDNA3-0049-2014.f10

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 11

Distribution of horizontally transferred and their phylogenetic relationship. (A) A venn diagram showing the distribution of different horizontally transferred families—, and ( 70 ), Lep1 ( 115 )—and nonautonomous -associated INterspersed Elements () ( 11 , 33 ). (B) Phylogenetic relationship between different organisms that carry horizontally transferred . The exact divergence of Microsporidia from other groups is not known. The phylogenetic tree is redrawn from reference ( 70 ). The distribution of a family (black) is shown as organisms within the black ellipse. The colors of letters for each organism are related to the group in the phylogeny. The red rectangle shows the distribution of and red letters represent the family. doi:10.1128/microbiolspec.MDNA3-0049-2014.f11

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 12

Tandem copies of and -associated INterspersed Elements (). (A) Tandem copies of four having 5′ TC and 3′ CTAG are counted as indicated by the horizontal black line underneath the box. Boxes with the same color indicate that they have > 85% sequence identity. Sequences homologous to multiple ends can be identified within a single . The sequences that are homologous to 5′ ends are shown before the dots and sequences that are homologous to 3′ ends are shown after the dots within the box. (B) Empty site of the tandem described above. The first line is host sequences with the insertion and second line is an orthologous site in another bat . (C) Three tandem copies of a insertion in the genome. One copy is truncated because it is at the end of the contig. The copies are 99% identical to each other. doi:10.1128/microbiolspec.MDNA3-0049-2014.f12

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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FIGURE 13

Examples of the impact of on gene structure and expression. (A) Insertion of a in the promoter (Yellow box with letter P) disrupts the transcription of the gene ( 102 , 169 ). (B) A insertion upstream of the promoter can increase the expression of the gene ( 170 ). (C) A -associated INterspersed Element () insertion in the promoter region of P element disrupts the promoter but provides a promoter ( 172 , 173 ). (D) Chimeric transcript generated from a containing multiple gene fragments (maroon, light orange and light pink boxes) (e.g., 82 , 98 , 101 ). (E) insertions in the 5′ UTR contributes to transcript diversity ( 51 , 84 ). (F) Insertion in the 3′ UTR can disrupt the polyadenylation of the transcripts causing loss of function ( 174 ). (G) insertion provides novel alternative polyadenylation sites ( 51 ). (H) insertions in the 3′ UTR provides putative microRNA binding sites ( 51 ). (I) Insertion of a in an intron can disrupt or alter splicing increasing transcript diversity ( 51 , 82 ) often causing loss of function ( 99 , 177 ). (J) provide cryptic splice sites and create novel fusion transcripts ( 51 , 82 ). (K) Two different waves of amplification provided binding sites for the protein involved in dosage compensation (shown in orange and red bars) on the X chromosomes that were generated ∼ 15 and ∼1 million years ago ( 127 ). (L) insertions contribute to long noncoding RNAs ( 51 ). doi:10.1128/microbiolspec.MDNA3-0049-2014.f13

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014
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TABLE 1

The classification of nonautonomous families as or

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0049-2014

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