Institute of Cell and Molecular Biology, University of Edinburgh, Edinburgh, Scotland
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Abstract |
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Introduction |
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Class II elements mobilize via a DNA intermediate which is excised and reintegrated elsewhere in the genome by a transposase (Plasterk 1995
). Such DNA transposons possess terminal inverted repeats (TIRs) containing transposase-binding sites. Some elements contain an open reading frame (ORF) encoding transposase (e.g., P elements in Drosophila), but copies often become nonautonomous through mutation. Other element families show characteristics of DNA-mediated mobilization but neither encode transposase nor appear to be derivatives of autonomous DNA transposons. Examples are the miniature inverted-repeat transposable elements (MITEs) found in plants (Wessler, Bureau, and White 1995
) and animals (Ünsal and Morgan 1995
; Tu 1997
) and the foldback elements distinguished by long modular TIRs containing arrays of direct subrepeats (Truett, Jones, and Potter 1981
; Liebermann et al. 1983
; Rebatchouk and Narita 1997
).
Molecular studies on ascidian development play an important role in attempts to understand the origin of vertebrates. As primitive members of the phylum Chordata, ascidians in larval stages display many vertebrate-like characteristics, such as a dorsal nerve and a tail region. We recently analyzed the genome of one ascidian, the sea squirt, Ciona intestinalis, using sequence data from short fragments and cosmid inserts of genomic DNA to estimate the number of protein-coding genes (Simmen et al. 1998
).
Apart from the partial sequencing of an LTR retrotransposon (Britten et al. 1995
), we are unaware of other work on repeats in ascidians. Here, we report the systematic search for repetitive elements in the C. intestinalis sequences. Members of several element classes are described, namely, a gypsy/Ty3-type LTR retrotransposon, non-LTR retrotransposons, a tRNA-derived SINE, a MITE, and a foldback element. A report on the methylation status of some of these elements has been presented elsewhere (Simmen et al. 1999
).
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Materials and Methods |
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Sequence Alignments and Phylogenetic Analysis
Unless stated otherwise, multiple-sequence alignments were generated using Pileup from the GCG Wisconsin Package, version 9.1 (Genetics Computer Group), using default parameters. In some cases, subsequent manual refinement was performed with an alignment editor, CINEMA (http://www.biochem.ucl.ac.uk/bsm/dbbrowser/CINEMA2.1/). Consensus sequences were derived from the multiple-sequence alignments using the GCG utility Pretty, with parameter values described in the text. Pairwise alignments were made using the GCG programs Gap and Bestfit. CLUSTAL X (Thompson et al. 1997
) was used to perform the phylogenetic analysis using the neighbor-joining approach (Saitou and Nei 1987
).
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Results and Discussion |
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Several findings indicate that Cigr-1 is a member of a recently active family. First, Southern blots with PstI-digested genomic DNA reveal multiple bands, with different individuals having distinct banding patterns, indicating that the genomic location of Cigr-1 elements differs between individuals (Simmen et al. 1999
). Second, searching the sequences from 1,486 fragments of C. intestinalis genomic DNA (see Materials and Methods) revealed four fragments with DNA similarity (BLASTN; P < 10-24) to Cigr-1. In three cases (accession numbers AJ226321, AJ227419, and AJ226522), the match was 98% or 99%, suggesting that these sequences lie in recently inserted Cigr-1type elements. Extrapolating this hit rate directly to the genome yields a Cigr-1 copy number estimate of 75. In contrast, the match with AJ226402 has only 55% nucleotide identity. It is notable, however, that the entire AJ226402 sequence is an ORF encoding 221 amino acids of the IN domain that is 50% identical to the equivalent stretch of the Cigr-1 IN. This suggests that this genome contains two families of gypsy/Ty3-type elements.
Multiple gypsy/Ty3 subfamilies within single species have been found before (e.g., Britten et al. 1995
). Further evidence of this in C. intestinalis comes from CIR2, a 176-aa fragment of the RT/RH domain of a retroelement found in C. intestinalis during a study (Britten et al. 1995
) of elements in marine species by PCR amplification using degenerate primers from Tgr1, a member of the SURL gypsy/Ty3 family, in the Hawaiian sea urchin, Tripneustes gratilla (Springer, Davidson, and Britten 1991
). CIR2 shows only a 24% match with the equivalent region of the Cigr-1 product. Also, a TBLASTN search shows that the sequences most similar to CIR2 are Tgr1 (P = 2 x 10-24) and the silkworm gypsy/Ty3 element Mag (P = 3 x 10-22), with the match to Cigr-1 being weak (P = 0.003). Thus, distinct gypsy/Ty3 families in C. intestinalis can be more similar to elements in other species than to each other.
Evolutionary Relationship of Cigr-1 to Other gypsy/Ty3 Elements
To investigate Cigr-1's relationship to LTR retrotransposons in other species, a phylogenetic analysis was performed. This was based on the alignment in figure 1
of the RT domains of Cigr-1 and representative LTR retrotransposons, plus two retroviruses, using the copia element from D. melanogaster to root the tree (the complete alignment is entry ds43388 in the EMBL sequence alignment database). The neighbor-joining tree (fig. 2
) gives a phylogeny broadly similar to those found in previous studies (e.g., Malik and Eickbush 1999
). As C. intestinalis is a nonvertebrate chordate, we were interested in Cigr-1's relationship to the puffer fish element sushi (Poulter and Butler 1998
), which has been shown to be representative of most putative vertebrate gypsy/Ty3 elements found to date (Miller et al. 1999
). Miller et al. (1999)
concluded that there are at least two, and possibly four, vertebrate gypsy/Ty3 lineages (on the basis of partial RT sequences), with the non-sushi-like vertebrate elements being related to the Mag/Tgr1 group (discussed in Springer and Britten 1993
). The fact that the sushi-like elements cluster with fungal elements (e.g., MAGGY) in phylogenetic reconstructions, coupled with their apparent absence in other deuterostomes, has led to the conjecture (e.g., Poulter and Butler 1998
; Miller et al. 1999
) that they arose by horizontal transmission from either fungi or plants to an early vertebrate.
Cigr-1 affords a test of this idea, for if a horizontal transmission event occurred earlier in the primitive chordates, then the descendant lineage in C. intestinalis should form a sister group to the vertebrate sushi-like elements. The fact that Cigr-1 and sushi are not neighbors (fig. 2 ) suggests either that the putative horizontal transmission event took place after the divergence of the ascidians from the protovertebrate line or that a family of sushi-like elements exists in the Ciona genome that is yet to be discovered. Either way, the situation is complex, as the analysis also shows that nonvertebrate deuterostomes can contain gypsy/Ty3 elements bearing more similarity (in the RT domain) to the sushi-like branch than to the Mag/Tgr1 branch. Additional data and more rigorous phylogenetic analyses would clearly be useful in clarifying these issues.
In addition, a TBLASTN search revealed that in the capsid and nucleocapsid domains, Cigr-1 shows striking similarity to Tgr1 (P = 10-16) and Mag (P = 10-9), weaker similarity (P > 10-5) to Arabidopsis thaliana and HIV-1 sequences, and none to the other sequences represented in figure 2 . Lack of sequence conservation precludes a reliable phylogenetic analysis based on the CA/NC domains, but a close relationship between Cigr-1 and Tgr1 is also supported by their sharing two rare features: two CX2CX4HX4C RNA-binding motifs in the NC domain (separated in both cases by six amino acids), and only one ORF.
The differing phylogenetic signals in the CA/NC and RT/RH regions suggest that perhaps recombination events have brought together domains from previously distinct elements. We speculate that there may be a family of elements in urochordates with homology to the Mag/Tgr1 group in both the gag and the pol genes. Support for this hypothesis comes from the short CIR2 sequence which shows the strongest similarity to RT/RH of Tgr1 and Mag and little to Cigr-1. Given the evidence for recent horizontal transmission of SURL elements (a family of which Tgr1 is a member) within echinoderms (Gonzalez and Lessios 1999
), another possibility, albeit a more speculative one, is of a similar, ancient transmission to C. intestinalis.
Non-LTR Retrotransposons
Searching the genomic sequences against the protein database revealed seven fragments which had non-LTR retrotransposons as their closest matches. Three show similarity (P < 10-6) to the ORF2 products of various vertebrate L1 elements. Figure 3A
indicates the similarities with respect to a typical full-length mouse element, L1spa (EMBL accession number AF016099) (Naas et al. 1998
). In AJ226259 and AJ226190, the pattern of L1 homology is suggestive of the 5' truncated copies known to vastly outnumber full-length copies of mammalian L1's (Voliva et al. 1983
). In AJ226870, the homology is interrupted by a frameshift and three short insertions relative to L1spa. In the absence of any overlap between these sequences, there is no formal proof that they derive from insertions of a common retrotransposon. However, given their common similarity to vertebrate L1-like elements, we suggest that there is such an elementor closely related families of elementswhich we label Cili-1.
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These findings support a recent phylogenetic analysis which classified all non-LTR elements into 11 clades and suggested that each clade originated in the Precambrian era and has since evolved purely by vertical descent (Malik, Burke, and Eickbush 1999
). Under this scheme, Cili-1 would likely be in the L1 clade and Cili-2 in the LOA clade. Cili-2 therefore significantly broadens the species distribution of the LOA clade, which previously contained only arthropod elements.
Composite tRNA-Derived SINE
Three short novel repetitive sequences were identified via the strategy detailed in Materials and Methods. The distribution of two of thesetermed and
(approximately 170 and 100 bp long, respectively)in the cosmids revealed that they tended to colocalize, with
often being found upstream of one or more
sequences. An association between
and
was also evident from their distribution in the 1,486 random fragment sequences of genomic DNA.
Further analysis suggested that and
are the primary components of a composite tRNA-derived SINE, which we label Cics-1 (fig. 4 ). The 172-bp
consensus sequence was derived from the 23 near-full-length copies of
found in the sequences (mean similarity of the copies to the consensus 94%, SD 3%). Immediately downstream of all but one of these
copies is a short poly(A) region followed by a 12-bp motif (consensus TAATCACCCACA, termed ß) and at least a partial
sequence. (A similar pattern is seen in the data set in which only the 3' end of
is complete.)
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As indicated in figure 4, a
72-bp tRNA-derived region lies at the 5' end, containing RNA pol III promoter sites separated by 34 bp, typical of their spacing in tRNA genes and SINEs (Deininger 1989
). The similarity to individual tRNA sequences is moderate; the closest match is to a tRNA-Thr gene from D. melanogaster (X02575), with 70% identity over bases 574 of
. The relationship was also detected by the tRNAscan-SE program (Lowe and Eddy 1997
). As in most other SINEs, this segment is followed by a tRNA-unrelated sequence. BLASTN searches indicate that the closest homologs of Cics-1 in this region are AFC SINEs in African cichlids (Takahashi et al. 1998
). Bases 91112 of
perfectly match bases from almost the same location in AFCs in several cichlids (e.g., sequences AB016544 from Julidochromis transcriptus and AB009707 from Tropheus moorii; BLASTN P = 0.008). Interestingly, this tRNA-unrelated segment of AFCs has been found to be 74% identical to a 65-bp "core" sequence shared by many families of SINEs in eukaryotes (Gilbert and Labuda 1999
). Comparing the reference core sequence used in that study (human Ther-1 consensus; see fig 4
of Gilbert and Labuda 1999
) with Cics-1-
revealed 55% identity over bases 87150 of
, indicating that Cics-1 belongs to the superfamily of SINEs containing this component.
In other respects, however, Cics-1 is unusual. First, whereas many SINEs have a poly(A) tail, the data indicate that -p(A) is rarely, if ever, mobilized on its own. Rather, the almost ubiquitous presence downstream of ß and at least part of
suggests that it is the
-p(A)-ß-
fusion that is mobile. Composite SINEs have previously been found (Kaukinen and Varvio 1992
; Izsvák et al. 1996
; Serdobova and Kramerov 1998
). Second, the 3' ends of many SINEs are similar to the 3' ends of non-LTR retrotransposons and are thought to rely on the latter for mobility (Okada et al. 1997
). We therefore searched for any association between the Cili-2 3' UTR sequences and Cics-1, but none was apparent.
From sequence data alone, it is impossible to fully describe how Cics-1 arose or how it mobilizes. However, one possible scenario is that a pol III readthrough transcript of a tRNA gene or pseudogene coupled to the SINE core segment was aberrantly polyadenylated then retrotranscribed and integrated (by enzymes encoded by Cigr or Cili elements) adjacent to the ß- sequence. This event brought into proximity the pol III promoter in
and the pol III transcriptional stop signal in the
3' end (fig. 4 ). It remains unclear, though, how pol III transcripts of the element are reverse transcribed, as the copies lack flanking target site duplications and Cics-1 lacks the 3' poly(A) tail believed to help prime this step in other SINEs (Deininger 1989
). Cics-1 is not unique in this regard: composite SINEs in artiodactyls have simple repeats at the 3' end. It may be significant that several Cics-1 copies have [CATT]24 at the 3' end (e.g., in AJ226376, AJ226486, and AJ227046).
Another puzzle concerns the origin of the solitary ß- copies and
clusters, as ß-
lacks a pol III promoter. Perhaps such sequences are the result of incomplete reverse transcription of full-length transcripts (Weiner, Deininger, and Efstratiadis 1986
; Tu 1999
). The mechanism generating
clusters is unknown, although it may be relevant that a 71-bp sequence (not shown) containing a 69% match to bases 145 of
occurs in head-to-tail arrays in C. intestinalis; the cosmid cicos1, for example, contains a 29-copy array spanning bases 2650428535. Whatever the mechanisms allowing it or parts of it to mobilize, Cics-1 has been highly successful in proliferating: extrapolation from the frequency of complete or partial hits (232 in total) in the sequence sample suggests a genomic copy number of 40,000.
Miniature Inverted-Repeat Transposable Element
A third short novel repeat was identified via the strategy detailed in Materials and Methods. Fifteen near-full-length copies were found, and a 193-bp consensus sequence was derived (fig. 5
). Many incomplete copies, either truncated or containing internal deletions, were also found; the copy number was estimated to be 17,000. The element's features are characteristic of MITEs found in plants and insects (Wessler, Bureau, and White 1995
; Tu 1997
), so we label it Cimi-1. First, Cimi-1 has perfectly matching 30-bp TIRs. Second, the sequence is A+T-rich (60%). Third, the elements are usually flanked by 24-bp A+T-rich direct repeats, consistent with the bias to A+T-rich insertion target sites found for other MITEs (Tu 1997
). Thirteen out of 15 copies are immediately flanked by TA on both sides; the two copies that do not are also those with the least similarity to the consensus (fig. 5
), consistent with the possibility that the putative original TA repeats have been altered by mutation. Furthermore, in 6 out of these 13 cases, the direct repeat is TATA. This is a far higher frequency than expected by chance. In the flanking sequences shown in figure 5
, 27% of the dinucleotides are TA, so the proportion of copies in which the TA direct repeats are also embedded purely by chance within TATA repeats on both sides can be estimated as 0.272 = 0.07, sixfold less than the observed proportion (6/13). As TA and TATA are palindromic, this analysis cannot establish whether these repeats are target site duplications or part of Cimi-1's TIRs. In principle, this can be resolved by examining cases in which Cimi-1 inserts into a known sequence, but unfortunately no such cases were found.
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Foldback Element
A scan of the four C. intestinalis cosmid sequences for inverted repeats found one prominent pair in Cicos41. Subsequent analysis revealed a 2,444-bp element (fig. 6
) spanning bases 1832720770, in which each inverted repeat arm has a modular architecture, including a tandem array of subrepeats. These features are shared by foldback transposable elements in various eukaryotes, e.g., in Drosophila (Potter 1982
), the sea urchin (Hoffman-Liebermann et al. 1985
), and plants (Rebatchouk and Narita 1997
).
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How foldback elements mobilize is unknown, although their structural similarities to class II elements suggest transposition mediated by a transposase. By analogy with DNA transposons, the transposase would be expected to be encoded in the non-repetitive middle domain (M). However, most foldbacks show no evidence of M encoding proteins and the size and sequence of M can vary among members of a family (Hoffman-Liebermann et al. 1985
), suggesting that most copies are nonautonomous. The Ciona M domain is only 969 bp and shows no sign of encoding a transposase: the longest ORF encodes a 99-aa product with no similarity to any known protein. The foldback in cosmid Cicos41 was the only example found, so proof that it belongs to a family of dispersed repeats will require further work. If this was found to be true, it would imply that the Ciona genome also contains an as yet unidentified DNA transposon encoding a transposase capable of also mobilizing the foldback element.
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Conclusions |
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The discovery of these elements should aid efforts to unravel the evolutionary history and significance of various classes of eukaryotic mobile elements. Analysis of the Cigr-1 LTR retrotransposon indicates that its history may have involved domain-swapping, as the RT/RH domains are similar to those in vertebrate sushi-like elements, whereas the CA/NC domains bear close similarity to those in echinoderm SURL elements. The non-LTR elements support a recent phylogeny (Malik, Burke, and Eickbush 1999
) which classed all non-LTR elements into 11 clades; the two Ciona elements fall into separate clades and significantly broaden the species distribution in the LOA clade. The two most abundant elements are a MITE and a modular tRNA-derived SINE with several unusual features: no flanking repeats, an internal poly(A) region, and a downstream segment that is also found independently in the genome. Finally, the foldback element is, to our knowledge, the first example of this class in a chordate. We also speculate that the genome may harbor additional families of elements, specifically, another branch of gypsy/Ty3 LTR retrotransposons and an autonomous DNA transposon.
Further study of these repeats should be particularly useful in tracing the origins of vertebrate elements. We have already shown that the Ciona host genome is unlikely to suppress element mobility via the mechanism often suggested as serving this function in mammalian genomes, i.e., cytosine methylation (Simmen et al. 1999
). Finally, we also believe that the current study validates the strategy of systematically searching genomic sequences for repetitive elements, rather than just detecting elements from well-known families.
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Acknowledgements |
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Footnotes |
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1 Abbreviations: RT, reverse transcriptase; TIR, terminal inverted repeat.
2 Keywords: retrotransposon
SINEs
LINEs
foldback element
inverted repeat
Ciona intestinalis.
3 Address for correspondence and reprints: Martin W. Simmen, Institute of Cell and Molecular Biology, University of Edinburgh, Mayfield Road, King's Buildings, Edinburgh EH9 3JR, United Kingdom. E-mail: m.simmen{at}ed.ac.uk
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