A search for reverse transcriptase-coding sequences reveals new non-LTR retrotransposons in the genome of Drosophila melanogaster
© GenomeBiology.com 2000
Received: 29 August 2000
Accepted: 26 October 2000
Published: 4 December 2000
Non-long terminal repeat (non-LTR) retrotransposons are eukaryotic mobile genetic elements that transpose by reverse transcription of an RNA intermediate. We have performed a systematic search for sequences matching the characteristic reverse transcriptase domain of non-LTR retrotransposons in the sequenced regions of the Drosophila melanogaster genome.
In addition to previously characterized BS, Doc, F, G, I and Jockey elements, we have identified new non-LTR retrotransposons: Waldo, You and JuanDm. Waldo elements are related to mosquito RTI elements. You to the Drosophila I factor, and JuanDm to mosquito Juan-A and Juan-C. Interestingly, all JuanDm elements are highly homogeneous in sequence, suggesting that they are recent components of the Drosophila genome.
The genome of D. melanogaster contains at least ten families of non-site-specific non-LTR retrotransposons representing three distinct clades. Many of these families contain potentially active members. Fine evolutionary analyses must await the more accurate sequences that are expected in the next future.
Non-long terminal repeat (non-LTR) retrotransposons, also known as LINEs (long interspersed nuclear elements), make up a very large class of transposable elements that are present in most eukaryotes [1,2]. They transpose by reverse transcription of an RNA intermediate. They possess an open reading frame (ORF) with coding capacities for a protein with endonuclease, reverse transcriptase and sometimes RNase H activities. Many of them contain an additional ORF (ORF1) encoding a protein of an unknown function. Some non-LTR retrotransposons, such as R1 and R2 in arthropods, insert at specific sites in the genome [3,4], whereas the others do not show specific sites of insertion. The cleavage specificity of some elements such as R2 is the result of the activity of an endonuclease showing similarities to restriction enzymes [5,6]. The other elements, whether they are site-specific (like R1) or not (like mammalian L1 elements), have an endonuclease structurally related to apurinic/apyrimidinic (AP) endonucleases [7,8]. Non-LTR retrotransposons can be assigned to 12 clades on the basis of the sequences of their reverse transcriptase domains and appear to be as old as eukaryotes [2,9]. The chronology of the acquisition of the various enzymatic domains suggests that the first non-LTR retrotransposons contained an endonuclease related to restriction enzymes, and that the non-LTR retrotransposons that have a nuclease structurally related to AP endonucleases derived from this ancestral group. The RNase H domain would have been acquired later .
Reverse transcription of non-LTR retrotransposons is thought to occur on chromosomal DNA using the cut resulting from their endonuclease activity as a primer. This process is called target-primed reverse transcription (TPRT). The retrotransposition machinery of non-LTR retrotransposons is thought to be used for transposition of SINEs (short interspersed nuclear elements) and might also be at the origin of the formation of processed pseudogenes . The shape of eukaryotic genomes is therefore largely influenced by non-LTR retrotransposons. They are particularly abundant in mammals. Humans contain one major class of non-LTR retrotransposons, the L1 elements, which make up more than 15% of the genome . In contrast, the Drosophila melanogaster genome has more than ten non-LTR retrotransposon families, representing the Jockey, I, R1 and R2 clades [2,9], indicating that several elements have had the chance to spread in this species. Early studies of several families of non-site-specific Drosophila non-LTR retrotransposons have shown that, in many cases, they comprise recently transposed euchromatic elements dispersed on all chromosomal arms, and variously defective elements accumulated in pericentromeric heterochromatin [12,13]. Euchromatic elements can be full size or truncated at the 5' end, presumably as the result of early arrest of reverse transcription. Heterochromatic elements are retrotranspositionally inactive and represent old components of the genome.
Many non-LTR retrotransposons in D. melanogaster were discovered during analysis of spontaneous mutations, as a result of their insertion within a gene. The sequence of most of the euchromatic part of the D. melanogaster genome has recently been reported , giving an interesting opportunity for studying all the non-LTR retrotransposons present in this species.
Each family of non-LTR retrotransposons identified in this way was further analyzed at the nucleotide level: BLASTN searches were performed, both in the sequences from Release 1  and from BDGP/EDGP , to identify all members of the family in the genome, and full-size copies were identified. The BDGP/EDGP sequences appear to be a subset of Release 1 sequences. There is, however, a high error rate in the sequences of Release 1 containing repetitive DNA: comparison of a fraction of both datasets revealed 0.42% point differences in repetitive sequences compared with only 0.0046% point differences in non-repetitive sequences (see  and the Celera website ). In our analysis, we estimate that non-LTR retrotransposon sequences that could be found in both BDGP/EDGP and Release 1 datasets contain an average of one difference in every 300 base pairs (bp), that is 0.33%. About 40% of these differences are due to insertions and deletions rather than base mismatches, and they are associated with resolution of repeated residues: for example, 5 G should be 6 G, 3 T should be 2 T, 3 C should be 2 C, 8 A should be 7 A, and so on. Consequently, many full-size elements from Release 1 appear not to have coding capacities for complete ORF1 and ORF2 products because of frameshifts. We therefore chose as a representative of each new family identified a full-length element extracted from the BDGP/EDGP database.
Summary of non-LTR retrotransposon sequences found in the genome of the D. melanogaster isogenic strain y; cn bw sp
Number of elements*
85 sequences matching reverse transcriptase
18 sequences matching reverse transcriptase
9 sequences matching reverse transcriptase
11 sequences matching reverse transcriptase
Only partial elements
Only short (70-600 bp) regions with average identity of 55%
Only short (70-600 bp) regions with average identity of 60%
Elements of the Jockey clade
The Jockey clade is by far the most represented clade in D. melanogaster. It includes one site-specific element, TART, and a large variety of non-site-specific elements such as Jockey, F, Doc, BS, G and Helena, although for these last two no potentially active copy has been identified. Our analysis has revealed one additional member of the Jockey clade, the JuanDm element.
Jockey, F and Doc elements
Jockey, F and Doc are very similar in sequence and probably descend from a common ancestor [19,20]. Our analyses confirm previous studies. These families include both full-size and variously defective copies. The copy number of Jockey, F and Doc was estimated to be around 50-100 by early studies [21,22,23]. About half of these copies are located near the chromocenter. This estimate has been refined to 31.60 ± 7.51 sites on chromosomal arms for Jockey, 31.40 ± 10 for F, and 26.20 ± 4.74 for Doc . Our analyses reveal that each of these families in fact contains a very large total number of copies: at least 86 for Jockey, 94 for F and 128 for Doc. These are underestimates, as a large fraction of the heterochromatic part of the genome is not represented in the databases, and these regions are well known to contain transposable elements. We have identified seven full-size copies of Jockey, all surrounded by target site duplications (TSD) and mapping on chromosomal arms. The F and Doc families contain as many as 14 and 22 full-size copies, respectively. Surprisingly many full-size copies of F do not appear to be flanked by TSD. Large subsets of the defective copies of these families are truncated at the 5' end.
The Jockey family was reported to contain a subset of 3 kb long internally deleted elements [19,25]. Our analyses provide evidence for only two internally deleted elements of 2.6 and 2.9 kb in the genome of the y; cn bw sp strain. A subfamily of internally deleted elements might be specific for some strains, or might be confined to heterochromatic regions that are not represented in the databases.
No potentially active G element was reported by earlier studies. Only one complete G element was previously described, and it did not code for full-length ORF1 and ORF2 products . However, some characteristic domains were recognized, such as cysteine-rich motifs of ORF1 and the reverse transcriptase domain of ORF2. The chromosomal distribution of G elements appeared to be fairly stable between strains. They were found mostly in tandem arrays in the nontranscribed spacer sequence of rDNA units . Our analyses reveal 37 copies of G elements, most of which were short and variously deleted. We identified only one full-size G element surrounded by TSD, but it could not encode the complete ORF1 and ORF2 proteins. However, as this full-size element is not present in the sequences released by BDGP/EDGP, we cannot decide whether the fact that it appears to be unable to code for these products results from sequencing errors or if it is an inactive element. It is located in region 60E12-60F2 of the right arm of the second chromosome and is surrounded by other defective G elements organized in tandem repeats. In fact, the sequences of this G element and surrounding DNA are very similar to those previously described , indicating that it is the same inactive element.
TART elements insert preferentially at the tips of the chromosomes with HeT-A elements and constitute the telomeres of the Drosophila chromosomes [27,28]. As the telomeric regions are not represented in the released sequences we did not expect to pull out TART or HeT-A elements. Not surprisingly, we have identified only 11 sequences matching TART reverse transcriptase, and none of them encodes a large protein. We found only some short regions with less than 60% identity to HeT-A. This emphasizes the idea that TART and HeT-A elements have a strong preference for telomeric regions.
The number of copies of BS elements was estimated to be around five to ten [25,29]. Although the first two copies were identified as recent insertions within a gypsy element, they seem to transpose very infrequently because their distribution pattern is highly conserved between strains as judged by Southern blot analyses . Our analyses reveal 19 copies of BS in the genome, only two of which are full size and surrounded by TSD.
Helena elements are non-LTR retrotransposons related to BS elements. They exist in various Drosophila species [30,31,32]. Hybridization studies have revealed sequences homologous to the D. virilis Helena element close to the chromocenter of D. melanogaster, and one copy was partly sequenced (GenBank accession code AF012030). We have found nine sequences matching Helena reverse transcriptase. No full-size copy is recognizable. They are unable to encode a large protein and the mean genetic distance between the different copies is very high. Presumably, these are the remnants of very ancient elements related to Helena, present in D. melanogaster or an ancestor species, and now extinct in D. melanogaster.
Some of the sequences found in our HMM search are equally distant from Helena and BS (52% identity). They possibly represent a new family, denoted Helena/BS in Figure 1. We noticed after this work was completed that a new non-LTR retrotransposon has recently been identified. The X element (GenBank accession code AF237761) belongs to the Helena/BS family.
Elements of the I clade
Until now the I element was the only member of the I clade to have been identified in D. melanogaster. This element has been extensively studied because it is responsible for the IR system of hybrid dysgenesis . We have identified You, a new element of the I clade.
Studies of the I element family have been recently reviewed [37,38]. It is known that active I elements, also called I factors, are present only in some strains that are called inducer strains. Inducer strains are expected to contain five to ten full-size I elements in euchromatic regions, and about 30 defective elements mostly localized within pericentromeric heterochromatin [24,36,39,40]. The isogenic y; cn bw sp strain is inducer. Six full-size I elements can be identified in the sequences of Release 1. There is probably a seventh one for which sequences are available for both the 5' and 3' ends but not the middle. None of these elements has the coding capacities of an active I factor [41,42]. We assume that this is due to sequencing errors. All these copies are surrounded by TSD. They map on euchromatic sites. We have also identified six 5' truncated elements that are surrounded by TSD, and eight that are not. In addition, about 30 elements more divergent from active I elements are found. None of those is full size. Some are 5' truncated, some 3' truncated, some are truncated at both ends, and many have internal deletions. They are usually within unallocated scaffolds, strongly suggesting that they are in heterochromatic regions. Those that possess the 3' end of I terminate with a sequence related to TAA (TAAA)n instead of the regular TAA repeats of the active I elements. This termination was shown to be characteristic of I elements localized in pericentromeric heterochromatin .
Strikingly, we have noticed that the six You elements that could be localized, map in distal or proximal regions of chromosomal arms: 1F and 19E-F on chromosome X, 39E and 40A on chromosome II, and 60F and 79E-F on chromosome III. This is a very unusual distribution, and it would be interesting to determine whether You elements are also localized similarly in other D. melanogaster strains. Examining the sequences surrounding You elements did not reveal an obvious bias for insertion sites. Their unusual distribution is therefore unlikely to be the result of sequence preference for insertion. Alternatively, euchromatic copies of You could be the few survivors of a former broader You family that is in the process of being eliminated from the genome by stochastic loss, as in the case of Drosophila mariner elements . Their confinement near the frontiers between euchromatin and heterochromatin could reflect a lower rate of loss of sequences in these regions.
The You family is also present in other species of the D. melanogaster subgroup : Figure 5b shows the result of hybridization of a You-specific DNA probe (Figure 6) to a Southern blot of genomic DNA digested with SmaI and SacI. The probe reveals an internal SmaI-SacI fragment of 4.9 kb. A 4.9 kb band hybridizing strongly to the probe is observed in D. melanogaster and in sibling species D. simulans and D. mauritiana, indicating that these species contain several copies of potentially full-size You elements. The more distant species D. teissieri and D. yakuba show much weaker signals, and the presence of the 4.9 kb fragment is not certain. These species contain sequences related to You, but these sequences are divergent from those of the D. melanogaster You elements. Finally, no hybridization signal is detected in D. virilis, which is outside the D. melanogaster subgroup , even with longer exposures.
Elements of the R1 clade
Most non-LTR retrotransposons of the R1 clade are site-specific: R1Dm inserts preferentially at one site into the rDNA units. Recently, we have described two new subfamilies of elements - Waldo-A and Waldo-B - that belong to the R1 clade and do not seem to have strong insertion site preference.
Waldo-A and Waldo-B elements
The Waldo-A and Waldo-B families were first identified by analyzing the sequences released by BDGP/EDGP and are described elsewhere . Members of both subfamilies are found in the present study. There are two full-size Waldo-A and five full-size Waldo-B elements. Most of them are surrounded by TSD. All 5'-truncated Waldo-A elements are surrounded by TSD and are very similar to complete Waldo-A elements (>98% identity at the DNA level). Only a minority of Waldo-B 5'-truncated elements is surrounded by TSD. In addition variously defective elements with less than 98% identity to Waldo-A or Waldo-B elements have been found.
Only fragments of elements with similarity to R1Dm have been found in our search, presumably because R1Dm inserts preferentially within rDNA repeats, which are not represented in the databases.
Elements of other clades
Partial R2Dm elements were identified in the BDGP/EDGP sequences but not in Release 1, presumably for the same reasons as for R1Dm.
We have found sequences that match the reverse transcriptase of the non-LTR retrotransposons Q in Anopheles gambiae  and LOA in D. silvestris . These non-LTR retrotransposons belong to the LOA and the CR1 clades, respectively, which were supposed to have no representatives in D. melanogaster. We have also found some short sequences showing weak similarities to the element Bilbo in D. subobscura , which also belongs to the LOA clade. As in the case of Helena, these sequences are presumably remnants of very ancient elements from the LOA and CR1 clades, once present in D. melanogaster or an ancestor and now extinct.
Put together, the sequences of BS, Doc, F, G, I, Jockey, JuanDm, Waldo-A, Waldo-B and You elements presented in this work make 1134 kb, which is almost 1% of the 120 Mb of Release 1 . This percentage would certainly increase if our analysis could be extended to all heterochromatic portions of the genome. In particular pericentromeric heterochromatin regions are known to be enriched in defective transposable elements that are thought to be old components of the genome [12,13]. Only a small subset of the sequences in Release 1 (3.8 Mb) presumably originate from these regions because they could not be localized on chromosomal arms . Many of the defective copies of non-LTR retrotransposons were found in these unlocalized sequences.
The mean genetic distance between members of a given family reflects their degree of heterogeneity. Assuming that non-LTR retrotransposons of different families accumulate mutations at the same rate, elements belonging to old families are expected to be more heterogeneous than elements of recent families. This reasoning does not take into account, however, possible bursts of invasion of a genome by a particular element or subset of elements of one family. This situation is well documented in the case of the I element family . Indeed, active I elements that are now present in D. melanogaster have invaded the species very recently, during the 20th century. However, all D. melanogaster strains contain defective heterochromatic I elements that display an average of 94% sequence identity with each other and with the I factor . These are very old remnants of former active I elements that were present in the common ancestor of all species from the D. melanogaster subgroup and were lost in the ancestor of the D. melanogaster species lineage. It is therefore not inconceivable that this kind of event may also have occurred in the case of other non-LTR retrotransposon families. When possible, we have estimated the genetic distance between only the subset of longest available elements within a family. This was done for the Doc, F, G, I, Jockey, JuanDm, Waldo-A, Waldo-B and You families (data not shown). Not surprisingly, the subset of longest elements is constantly more homogeneous than the whole family, indicating that the longest elements are probably still active or result from recent inactivation. One should keep in mind, however, that the error rate in the repeated sequences in Release 1 is not negligible and therefore the degree of heterogeneity observed in a small number of copies is probably overestimated.
The high rate of errors in repetitive sequences of Release 1 renders thorough analysis of transposable element families uncertain. For example, on the basis of the recognition of reverse transcriptase coding capacities, You elements were not recognized in the sequences of Release 1 (Figure 1a) but were identified in the BDGP/EDGP sequences (Figure 1b). It is possible that some non-LTR retrotransposon families have been missed by our study. More accurate sequences of repetitive DNA regions are expected in the near future . They will provide invaluable material for the thorough phylogenetic analyses of families of transposable elements. In particular, analysis of the sequences and organization of the different copies of a given family will provide information useful in understanding the processes by which these elements evolve in the genome.
The annotations of the sequences of Release 1 are in progress. Most copies of non-LTR retrotransposons that we have found in the present study are not annotated yet. The coordinates of all sequences identified in our studies are available as an additional data file with the online version of this paper.
Materials and methods
Identification of reverse transcriptase sequences
Drosophila melanogaster sequences produced by Celera  and the BDGP/EDGP  were used in the analysis. A six-frame translation of all the sequences was produced. To reduce the size of the data set to be analyzed by time-consuming HMM software, only amino-acid sequences containing a motif [FY]XDD, which is conserved among reverse transcriptases , were extracted for the analysis. The HMMER 2.1.1 software  was used to identify all sequences in this subset matching the full-length model of reverse transcriptase, which was built using a seed alignment of reverse transcriptase sequences (accession number PF00078) obtained from the Pfam database . Only matches with scores above zero were considered in the analysis.
Handling of sequences was facilitated by scripts from the SEALS package . The results of HMMER searches were analyzed using scripts that we designed specially, grouped into families and classified on the basis of their similarities to known retrotransposons. The relationships between the families of non-LTR retrotransposons were determined by making neighbor-joining trees using the CLUSTAL W software .
Analysis of non-LTR retrotransposon families
BLASTN searches were performed in sequences of Release 1 and of BDGP/EDGP using WU-BLAST 2.0 package  and full-length elements from different families as queries. The results were analyzed using scripts that were especially written and based on the BioPerl package . All high-scoring pairs (HSPs) with percentage identities greater than 70% and lengths greater than 200 nucleotides were used to define distinct copies in the same family. These limiting values were arbitrarily chosen to take into account all diverged and truncated copies in a family while filtering out doubtful hits. HSPs in the same hit were checked manually for overlaps or internal deletions relative to a full-length element and joined together when necessary. Genomic coordinates for all copies were determined in this way and element sequences with flanking regions were extracted for further analysis. Target site duplications were searched in a semi-manual manner with the aid of bl2seq program from the NCBI BLAST package . Divergence of elements within a family was determined in the following manner: the longest element sequence in a family was used in BLAST searches against all other sequences in the family and resulting BLAST output was converted into multiple alignment with the MView program . The alignment obtained was used to calculate genetic distances between copies in a family by CLUSTAL W software. Divergence of a family was determined as a mean genetic distance between the longest element and all the other elements in a family. The error rate was estimated by comparing sequences of full-length Jockey and JuanDm elements which have the same flanking sequences (100-200 bp flanks were used) in both Release 1 and BDGP/EDGP databases.
Digestion of genomic DNA, gel electrophoresis, transfer on NytranN nylon membranes (Schleicher and Schuell) and hybridization with 32P-labeled DNA probes were performed following standard procedures  and suppliers' specifications. Hybridizations were carried out overnight at 42°C in 50% formamide. Washes were in 2x standard sodium sulfate (SSC), 0.1% sodium dodecyl sulfate (SDS) followed by 0.1 × SSC, then 0.1% SDS at 42°C. The DNA fragments used as probes were obtained by PCR amplifications from the isogenic y; cn bw sp strain genomic DNA using standard conditions with Taq DNA polymerase (Promega). For the JuanDm probe oligonucleotides 5'-AAGGAATAAACCACTAGTGGAGCGCC-3' and 5'-CAGGGAGTGTAAGCTTGGAGTGATG-3' were used as primers. For the You probe oligonucleotides 5'-GATCTTCTTATCAACGCGTACGTGC-3' and 5'-CCCAGGAGTATTGTGGATCCGTTAAG-3' were used as primers.
The following additional data are included with the online version of this paper: the coordinates of all sequences identified in this study.
We thank all who contributed open-source software used in this project (BioPerl, HMMER, SEALS, Clustal W and MView), Alexander Blinov for providing resources and support in the computer research, Ael Laglaine for help in the study of You elements, Christophe Terzian for helpful advice and Stephen Wicks for assistance with manuscript preparation. This work was supported by grants from the Russian Foundation for Basic Research (RFBR), from the Centre National de la Recherche Scientifique (CNRS) and from the Association pour la Recherche sur le Cancer (ARC).
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