Physiological Chemistry I, Biocenter, University of Würzburg, Würzburg, Germany
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Abstract |
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Introduction |
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To our knowledge, only one complete Ty3/Gypsy-like retrotransposon has been isolated to date from vertebrates: the Sushi retrotransposon from the Japanese pufferfish Fugu rubripes (Poulter and Butler 1998
). Sushi belongs to the Ty3 family and is related to Maggy from the rice blast fungus Magaporthe grisea (Farman et al. 1996
; Poulter and Butler 1998
; Malik and Eickbush 1999
). Other partial elements (mostly partial pol sequences) have been identified in lampreys, fishes, amphibians, and reptiles (Britten et al. 1995
; Tristem et al. 1995
; Marracci et al. 1996
; Miller et al. 1999
). While Hsr1 from the terrestrial salamander Hydromantes displays a higher degree of similarity to the pufferfish Sushi element (Marracci et al. 1996
; Poulter and Butler 1998
; data not shown), the other vertebrate partial pol sequences are difficult to assign to a particular Ty3/Gypsy family because of their shortness and the lack of resolution afforded by the analyses of individual enzymatic domains (Malik and Eickbush 1999
and references therein).
The fish genus Xiphophorus (Teleostei: Poeciliidae) is an established model for cancer research and for the analysis of sex determination and many questions of evolutionary biology (Kallman 1984
; Ryan and Wagner 1987
; Meyer and Lydeard 1993
; Schartl 1995
). Overexpression of the receptor tyrosine kinase oncogene Xmrk is responsible for the formation of hereditary melanoma in Xiphophorus (for review, see Schartl 1995
). The Xmrk oncogene has been formed by gene duplication of the preexisting Xmrk proto-oncogene. Both the Xmrk proto-oncogene and the oncogene are located in the subtelomeric region of the X and Y sex chromosomes in the platyfish Xiphophorus maculatus (strain Rio Jamapa), where they are closely linked to the sex determination locus (Gutbrod and Schartl 1999
; Nanda et al. 2000
; unpublished results). Several repetitive DNA elements, including a Y chromosomespecific large cluster of LTR-like sequences, the non-LTR retrotransposons Rex1 and Rex3, and the nonautonomous LTR element TX-1, have already been identified in this region (Schartl et al. 1999
; Volff et al. 1999
; Nanda et al. 2000
; Volff, Körting, and Schartl 2000
). We report here the discovery of Jule, a novel vertebrate LTR retrotransposon from the Ty3/Gypsy superfamily belonging to the Mag family. Although there are only three to four copies of Jule per haploid genome in X. maculatus, two of them are associated with the Xmrk genes on the sex chromosomes of the platyfish.
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Materials and Methods |
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DNA Manipulations
Genomic DNA was isolated as described (Schartl et al. 1996
). The genomic library of X. maculatus consists of 3545-kb inserts cloned into cosmid Lawrist7 (Burgtorf et al. 1998
). Cosmid sequencing was performed by transposon mutagenesis (Fischer et al. 1996
). Sequencing reactions were performed using the ThermoSequenase fluorescent labeled primer cycle sequencing kit with 7-deaza-dGTP (Amersham Pharmacia Biotech) and run on an ALFexpress automated laser fluorescent sequencer (Amersham Pharmacia Biotech). The DNA probe used in Southern blot hybridization experiments was a 1.8-kb fragment from the pol gene of Jule (fig. 1
) cloned into plasmid pJOE2114 (Fischer et al. 1996
), resulting in plasmid pROST56-214. This fragment was obtained by transposon mutagenesis of an original Jule 7.3-kb EcoRI fragment cloned into pJOE2114 (plasmid pROST56). The 3' end of the 1.8-kb fragment corresponded to the unique internal EcoRI restriction site in Jule located at approximately the C-terminal domain of the integrase (fig. 1
). Because there is no other EcoRI site in Jule, this probe is likely to reveal different copies of Jule after cutting genomic DNA with EcoRI. For Southern blot analysis, genomic DNA was blotted after restriction enzyme digestion onto positively charged nylon membranes and hybridized with the insert of pROST56-214 at 42°C in 35% formamide, 0.1% Na-pyrophosphate, 50 mM Tris-Cl (pH 7.5), 5 x SSC, 1% sodium dodecyl sulfate (SDS), 5 x Denhardt's solution, and 100 µg/ml calf thymus DNA. Filters were washed with 2 x SSC1% SDS at 50°C (low stringency).
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Data Deposition
The nucleotide sequences reported in this paper have been deposited in the GenBank database under accession numbers AF278691 and AF278692. The sequence alignment used to generate the Ty3/Gypsy retrotransposon phylogeny has been deposited in the EMBL Nucleotide Sequence Database under accession number DS43387.
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Results |
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A 4.8-kb sequence delimited by two 202-nt LTRs and overlapping two 6.5- and 7.5-kb genomic EcoRI fragments was detected in cosmid G17 069 (accession number AF278691). The conceptual translation product of this sequence shows a significant degree of similarity to several LTR retrotransposonencoded proteins (see below). Hence, this 4.8-kb sequence probably corresponds to a new fish LTR retrotransposon, which we called Jule-1 (for Jumping long element; fig. 1 ). A second, longer Jule element (9.2 kb, accession number AF278691) was detected in cosmid GO8 133 (Jule-2; fig. 1 ). The 9.2-kb sequence includes a 7.3-kb EcoRI fragment and ends in two 2.0- and 6.3-kb genomic EcoRI fragments.
Structural Analysis of Jule Elements
Jule encodes a putative translation product with the traditional LTR retrotransposon domains Gag (structural core protein) and Pol (protease, reverse transcriptase, RNase H, and integrase, in that order) (figs. 1 and 2
). No Env (envelope) domain or gene was detected. Jule Gag protein contains two putative CCHC nucleic acidbinding sites: a canonical CX2CX4HX4C zinc finger, already described in retroviruses and several other retrotransposons, preceded by a slightly different CX2CX3HX4C motif, which has been found in some other retrotransposons (Springer, Davidson, and Britten 1991
; Pardue et al. 1996
). As observed for other integrases, Jule integrase contains an HH-CC zinc fingerlike domain in its N-terminal domain, along with the classical DD35E motif (fig. 2
). Neither the conserved GPY/F domain nor the putative chromodomain (Malik and Eickbush 1999
) could be detected in the integrase of Jule. The reverse trancriptase of Jule contains all classical conserved domains according to Xiong and Eickbush (1990)
(not shown).
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Jule is delimited by two 3-nt inverted repeats (TGT and ACA) corresponding to the extremities of the LTRs (fig. 1
). A promoter was predicted between positions 131 and 181 of the LTRs, with a transcriptional starting site at position 174 (NNPP/eukaryotic promoter prediction, BCM Search Launcher; Smith et al. 1996
). A potential polyadenylation signal ATTAAA was detected at position 140. The ATTAAA sequence displays an activity comparable to that of the canonical polyadenylation sequence AATAAA (Zhao, Hyman, and Moore 1999
). Several LTR retrotransposons use cellular tRNAs as primers for reverse transcription (Mak and Kleiman 1997
). No tRNA candidate could be unambiguously identified in the case of Jule. As observed for numerous other retrotransposons (Boeke and Chapman 1991
), a polypurine tract (AAAAGGGGAGGAA) is adjacent to the 3' LTR. Jule elements are flanked by 5-nt direct repeats which probably correspond to the duplication of the target sequence generated during integration of the retrotransposon. The two Jule elements sequenced show different target duplication sequences: CTCTA for Jule-1, and GTCTT for Jule-2.
Association Between Jule Retrotransposons and Xmrk Genes
Jule-1 was identified in cosmid G17 069, which contains the 5' part of the X allele of the Xmrk proto-oncogene. Further sequencing showed that Jule-1 is in fact integrated in the first intron of this gene, 802 nt downstream from the first exon, in an opposite orientation to Xmrk. No Jule element was found at the same position in the Y allele of the Xmrk proto-oncogene or in both alleles of the Xmrk oncogene (not shown). Jule-2 was identified in cosmid GO8 133, which includes a large part of the 3' portion of the Y allele of the Xmrk oncogene and approximately 20 kb of 3' genomic flanking sequence. Jule-2 is integrated in the same orientation as Xmrk only 56 nt downstream of the polyadenylation signal of this gene. Using the insert of plasmid pROST56-214 (Jule-specific; see Materials and Methods) and a Rex5-specific probe in Southern blot hybridization experiments, Jule and Rex5 were both detected 3' of the X allele of the Xmrk oncogene as well (not shown). Nevertheless, the sizes and numbers of EcoRI fragments detected were different: the Jule and Rex5 probes hybridized with the same 7.3-kb fragment on the Y chromosome but with two different fragments on the X chromosome (4.8 and 6.1 kb, respectively). This suggests either the presence of X and/or Y chromosome-specific mutations after integration of both retrotransposons, or, alternatively, that they are not integrated exactly at the same position.
Jule Belongs to the Mag Family of Ty3/Gypsy Retrotransposons
Among sequences present in protein databases, the Gag-Pol polyprotein of Jule shows the highest similarity to proteins encoded by the retrotransposon Mag from the silkworm Bombyx mori (Michaille et al. 1990
; Garel, Nony, and Prudhomme 1994
; fig. 2
). In particular, the Jule polyprotein displays 40% amino acid identity (425 of 1,054 residues) and 57% amino acid similarity (612 of 1,054 residues) to the Pol polyprotein of Mag (expected value E = 0.0). The Mag family of Ty3-Gypsy retrotransposons also includes the echinoid retrotransposon SURL from Tripneustes gratilla (sea urchin retroviral-like retrotransposon; Springer, Davidson, and Britten 1991
) and several sequences from the nematode Caenorhabditis elegans (Malik and Eickbush 1999
) (fig. 1 ). Phylogenetic analysis of the Pol protein of Mag-related C. elegans retrotransposons revealed the presence of different subgroups in the genome of this nematode. Nevertheless, all of these subgroups were included in a single C. elegansspecific group in a global phylogenetic tree of Mag-related retrotransposons (data not shown). Hence, only one subgroup, represented by an element located on C. elegans chromosome III, was used for further analysis (accession number Z38112; three mismatches were introduced to regenerate the amino acid sequence; figs. 1 and 3
). Another copy of this element is also present on chromosome V (accession number ZZ99711), and solo LTR sequences were found on chromosomes II (AL110494), III (ALZ99293), IV (AL132862), and V (Z81489). This element is 5.1 kb in length, is delimited by two 218-nt LTRs, and is flanked by 5-nt target site duplications (CTAAA). Only one CX2CX4HX4C zinc finger was detected in the Gag protein of this C. elegans element.
We identified a corrupted Mag/Jule-related element, detected in a database genomic sequence from the nematode Ascaris lumbricoides (accession number L22247; fig. 3
) and identified as containing the small nuclear RNA U2-1 gene and the U2-2 pseudogene (Shambaugh, Hannon, and Nilsen 1994
). This element is truncated at its 3' end (the integrase-encoding region is absent; fig. 3
) and corrupted by several frameshifts. The truncated element is flanked by two perfect 2.2-kb inverted repeats, each containing the U2-1 and U2-2 (pseudo)genes (not shown). Protease, reverse transcriptase, and RnaseH domains could be identified in the partial Pol sequence (fig. 3
and data not shown). The Gag sequence contains a CX2CX3PX4C-X6-CX2CX4HX4C motif reminiscent of the CX2CX3HX4C-X6-CX2CX4HX4C double zinc finger domain present in Jule. Searching public databases for other sequences similar to Mag and Jule led to the identification and partial reconstruction of two different retrotransposons from the African malaria mosquito Anopheles gambiae. These sequences were generated by the Genoscope sequencing center (www.genoscope.cns.fr). Partial reconstruction of reverse transcriptase/RNase H domains of A. gambiae retrotransposon 1 was done using sequences including AL152894, AL155210, and AL141680 (fig. 3
). The Pol region from reverse transcriptase to integrase of A. gambiae retrotransposon 2 was obtained using sequences including AL139931, AL147383, and AL14105 (fig. 3
). Because of the lack of sequences available, reconstruction could not be further extended to determine the complete structure of these elements.
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Jule, Mag, SURL, and the A. gambiae, A. lumbricoides, and C. elegans elements were found to belong to the so-called Mag family of retrotransposons (fig. 4
). To our knowledge, Jule is the first retrotransposon from the Mag family that has been identified to date in vertebrates. Jule is clearly more related to elements from the Mag family than to the other complete vertebrate Ty3/Gypsy retrotransposon Sushi from the pufferfish F. rubripes (Poulter and Butler 1998
), which clearly belongs to the Ty3 family (fig. 4 ). Furthermore, we found no evidence for a closer relationship between Jule and the different partial Ty3/Gypsy sequences already isolated from vertebrates (see Introduction), which were too short to be included in the phylogenetic analysis.
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No signal was detected in more divergent fishes, including O. mykiss (rainbow trout), E. lucius (pike), D. rerio (zebrafish), C. carpio (carp), A. anguilla (European eel), and A. sturio (sturgeon) (fig. 5 ). This indicates either that Jule is not present in theses fishes or that the level of sequence similarity is too low to be detected by Southern blot hybridization.
Using Jule amino acid sequence as a query, database searches identified related elements in the genomes of other teleost fishes, including the zebrafish D. rerio (fig. 6A ) and the two genome project pufferfishes, F. rubripes (Japanese pufferfish; fig. 6B ) and T. nigroviridis (freshwater pufferfish; fig. 6C-1 and C-2 ). The sequence from D. rerio is the conceptual translation product of an embryo-expressed sequence tag (accession number AA495349) showing 56% amino acid identity and 71% amino acid similarity to a part of Jule reverse transcriptase (fig. 6A ). The relatively low level of nucleotide identity with Jule (58%) explains why the D. rerio element was not detected by Southern blot hybridization.
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Discussion |
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In addition to known members of the Mag family, including Mag from the silkworm B. mori (Michaille et al. 1990
; Garel, Nony, and Prudhomme 1994
) and SURL from the sea urchin T. gratilla (Springer, Davidson, and Britten 1991
), we identified additional elements in the nematodes C. elegans (this observation has been already made by others, e.g., Malik and Eickbush [1999
]) and A. lumbricoides and in the malaria vector, the African mosquito A. gambiae.
In classical phylogenies, the sea urchin T. gratilla is more related to the fish Xiphophorus (both are deuterostomes) than to nematodes and insects, A. gambiae is more related to B. mori (both insects) than to Xiphophorus, and C. elegans is more related to A. lumbricoides (both nematodes) than to A. gambiae (http://www.ncbi.nlm.nih.gov/Taxonomy). Hence, there are some discrepancies between the phylogeny of retrotransposons of the Mag family (fig. 4
) and the phylogeny of their host genomes. This phenomenon, which has been already observed for some other transposons (Capy, Anxolabéhère, and Langin 1994
; Cummings 1994
), might result from differences in evolutionary rates. Sequences with a higher rate of evolution can typically be "pulled down" to the root in a tree and will give the impression that they diverged earlier from a lineage than they evolutionarily did. Nevertheless, comparison of protein distances between Mag-related retrotransposons and other elements revealed that the members of the Mag family included in this study have evolved roughly at the same rate (not shown). More likely, discrepancies between Mag-related retrotransposon and host phylogenies might be explained by the presence of ancient retrotransposon lineages, which diverged before their host genomes did (Capy, Anxolabéhère, and Langin 1994
; Cummings 1994
). Some members of these lineages might have been lost or not detected. This hypothesis is consistent with the presence of two phylogenetically distinct A. gambiae elements, each of them more related to elements from other organisms than to the other A. gambiae sequence (fig. 4
). This strongly suggests that the Mag family of Ty3/Gypsy retrotransposons is polyphyletic. Finally, horizontal interspecific gene transfer of Mag-related retrotransposons could potentially have influenced the topology of the phylogeny of the Mag family. SURL elements can be transmitted horizontally (Gonzalez and Lessios 1999
).
As reported for Mag and SURL elements, no envelope gene or domain could be detected in the other Mag-related elements identified in this work, and neither GPY/F motif nor chromodomain (Malik and Eickbush 1999
) could be found in their integrase domain. The sizes of the LTRs in the Mag family vary between 77 nt for Mag (Michaille et al. 1990
; Garel, Nony, and Prudhomme 1994
) and 254 nt for SURL (Springer, Davidson, and Britten 1991
). The size of the intervening region between both LTRs is relatively constant (between 4,340 nt for Jule and 4,750 nt for SURL). In the majority of Mag-related retrotransposons, including Jule and the related element from T. nigroviridis, the A. lumbricoides element, Mag, and SURL, the Gag protein contains two successive zinc fingerlike motifs. One exception is the C. elegans element, in which only one zinc finger was detected. This was not a specificity of the copy chosen for analysis, because related elements from C. elegans showed only one motif as well. According to the phylogeny of Mag-related elements (fig. 4
), the most simple explanation is that the last ancestor of the Mag family had two zinc fingerlike motifs and that one of them has been lost in C. elegans. As observed for Mag (Garel, Nony, and Prudhomme 1994
) and for other retrotransposons, integration of Jule generates a 5-nt duplication of the target sequence. The low similarity between the target sequences of both Jule elements (CTCTA and GTCTT) suggests low or no sequence specificity, as reported for Mag (Garel, Nony, and Prudhomme 1994
).
Jule-like sequences were detected in all members of the family Poeciliidae tested so far and in other Cyprinodontiformes (Fundulus sp. and O. latipes). Related elements were also found in less related fishes, including O. niloticus, the two pufferfishes F. rubripes and T. nigroviridis, and the zebrafish D. rerio. Hence, Jule-related sequences are present in teleost species that diverged about 100 MYA (Benton 1990
). No related sequences could be identified by database searching in other vertebrate lineages. Considering the large amount of sequences available, particularly for Homo sapiens (more than 80% estimated coverage of the human genome with working draft sequences at the time of analysis), this suggests that the different retrotransposon lineages constituting the Mag family are absent or present at very low copy numbers in certain vertebrate lineages. Alternatively, they might be present in special genomic niches that have been only poorly sequenced to date because of their high content of repetitive DNA. Although there is no evidence for such a phenomenon, Jule-related retrotransposons might also have been reintroduced through horizontal transfer from a nonvertebrate species into the teleost lineages at least 100 MYA.
While Jule-2 is more corrupted, the low level of corruption of Jule-1 suggests that Jule-1 is the result of a recent retrotransposition event. Although Jule-1 and Jule-2 are both associated with a version of the Xmrk gene, their different locations (in intron 1 of the Xmrk proto-oncogene and 3' of the Xmrk oncogene, respectively) and their different target site duplication sequences indicate that they are the result of two different retrotransposition events. The high degree of nucleotide identity between Jule-1 and Jule-2 suggests again recent activity of a Jule element. Generally, the only selective pressure conserving retrotransposon enzymatic functions during evolution is their own ability to transpose. The low copy number of Jule retrotransposons detected by Southern blot hybridization in Poeciliidae and some other teleost species suggests that this retrotransposon did not maintain its functionality through frequent retrotransposition in its host genomes. If Jule did it, there is a counterbalancing mechanism of elimination maintaining a low copy number of the retrotransposon. An alternative hypothesis is the horizontal transfer of Jule between fishes. The SURL elements, which, like Jule, belong to the Mag family of retrotransposons, can be transmitted horizontally between echinoid species (Gonzalez and Lessios 1999
).
There are only three to four copies of Jule per haploid genome in X. maculatus (depending on whether the haploid genome considered contains the Y or the X sex chromosome). Curiously, two of these copies, which resulted from two different retrotransposition events, are physically associated with the Xmrk genes: one copy is associated with the Xmrk oncogene, and a second one is associated with one allele of the Xmrk proto-oncogene. Both are in the same subtelomeric region of the sex chromosomes of the platyfish. Both Jule-1 (X-specific) and Jule-2 (presenting sex-specific differences according to Southern blot analysis) insertions are closely linked to the sex determination locus: analysis of about 200 individuals of one strain of X. maculatus showed absence of recombination between both Jule insertions and the sex determination locus (unpublished data). We have strong evidence of the accumulation of other repetitive elements in this region (Volff et al. 1999
; Volff, Körting, and Schartl 2000
; unpublished data). This region is also prone to other DNA rearrangements, including deletions, insertions, and DNA amplification, with some of them being specific for either the X or the Y sex chromosome (Schartl et al. 1999
; Nanda et al. 2000
; unpublished data). Such sex-linked rearrangements might contribute to the initiation of divergence between the primitive sex chromosomes of X. maculatus and to recombinational isolation of the sex-determining locus. Such a phenomenon is reminiscent of the accumulation of certain retrotransposons on the Y chromosome of some Drosophila species (Steinemann and Steinemann 1997
; Chalvet et al. 1998
).
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Acknowledgements |
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Footnotes |
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1 Abbreviations: aa, amino acids; LTR, long terminal repeat; nt, nucleotides.
2 Keywords: SURL
Gag
Pol
Xmrk
sex chromosomes
3 Address for correspondence and reprints: Jean-Nicolas Volff, Physiological Chemistry I, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany. E-mail: volff{at}biozentrum.uni-wuerzburg.de
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