* Institute of Molecular Genetics RAS, Moscow, Russia; Department of Molecular Biology, Moscow State University, Russia; and
Populations, Genetique et Evolution, CNRS Gif-sur-Yvette, France
Correspondence: E-mail: gvozdev{at}img.ras.ru.
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Abstract |
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Key Words: retrotransposon Drosophila polymorphism evolution frameshifting RNAi
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Introduction |
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We present here the detailed evolutionary history of Drosophila long-terminal repeat (LTR) retrotransposon 1731 and evidences for a preferential expansion of definite structural variants of 1731 copies in the genomes of Drosophila species and cell cultures. This element has been described as a retrotransposon negatively regulated by the insect hormone ecdysone (Fourcade-Peronnet et al. 1988; Ziarczyk et al. 1989). Two classes of genomic copies of retrotransposon 1731 with different expression strategies were revealed in the D. melanogaster genome (Kalmykova, Maisonhaute, and Gvozdev 1999). The first class uses conventional translational frameshifting known to ensure the level of RT expression, depending on the efficiency of frameshifting. The bulk of genomic copies are related to the second class containing single-nucleotide deletion just downstream of the frameshifting region and providing expression of the fusion Gag-Pol polyprotein without frameshifting. We demonstrate here that evolving of 1731 retrotransposons occurred as a result of the secondary evolutionary events followed by the spread of the new variants in the genomes of D. melanogaster, D. simulans, D. mauritiana, and D. sechellia. The intraspecies and interspecies structural polymorphism of the U3 region of 1731 LTR related to the change of tissue-specific expression was revealed. Expansion of the recently evolved copies lacking frameshifting and possessing an extended profile of expression was documented in the Drosophila genomes. The loss of retrovirus-like strategy of gene expression of a retrotransposon resulted in the increased level of expression of a polyprotein, whereas a local duplication in LTR affected expression profile of this variant. This study is among the first ones to monitor a preferential spread of a definite structural variant of retrotransposon coupled with the changes of the level and profile of its expression. A possibility of a selective pressure that is responsible for the preferential expansion of a definite retrotransposon variant is discussed.
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Materials and Methods |
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D. simulans and D. sechellia stocks were collected in the Seychelles in 1985 and D. mauritiana stock was collected from Mauritius island in 1988. All stocks are from the Gif-sur-Yvette CNRS center (France) collection. The Schneider 2 (S2), Kc, and 67j25 cell cultures were used (Echalier 1997).
PCR of Genomic DNA and cDNA Libraries
Genomic DNA was prepared according to the standard method (Ashburner 1989) from the D. melanogaster adult flies. The following pairs of the oligonucleotide primers were designed to the genomic sequence of 1731 (according to GenBank sequence X07656):
Linear range of reaction for semiquantitative PCR was determined in preliminary experiments. DNA samples were amplified in the presence of dATP-P33 using Taq polymerase. PCR products were separated in 5% denaturing acrylamide gel and visualized using phosphor imager Storm-840 (Amersham) or by autoradiography.
A ZapII cDNA library (Stratagene) from ovaries of the Canton S D. melanogaster stock was kindly provided by Dr. Tulle Hazelrigg. Embryo cDNA library was in
gt11. Primers 3-4 were used to amplify phage lysate containing 106 phage particles.
Reporter Constructs Design
CaSpeR-hsp70-ß-gal vector was constructed by cloning of the hsp70 promoter into the XbaI-BamHI site of pCaSpeR-ß-gal. Frameshifting region (from 1141 to 1271 nt.) was PCR amplified both from plasmid 5c containing 1731 (Fourcade-Perronet et al. 1988) and from D. melanogaster testis cDNA (Kalmykova, Maisonhaute, and Gvozdev 1999) using primers 5'-ATGAATTCAAAATGAACTGTCGTCGCGAG-3' and 5'-ATGGATCCATGTGACTGGTAGC. The sequence designated by the bold letters contains AUG initiation codon and the sequence, which optimizes the start of translation (Cavener and Ray 1991). PCR fragments were cloned into the EcoRI-BamHI site of CaSpeR-hsp70-ß-gal. Low primer was designed to obtain fusion of ß-gal in the frame with 1731 ORF2.
To substitute G for A (position 1214, bold letter in primer) in the fragment bearing the frameshifting region of plasmid 5c in vector pTZ19R, the primers 5'-TTGTTAAATGCGCTGGATGGTGGTG-3' (from 1196 to 1220 nt) and 5'-ACTGCATTGTTCTTGTGTCGCGCTC-3' (1171 to 1195 nt) designed as "tail-to-tail" were used. To substitute a UCC codon for an AGU codon (positions 1193 to 1195, bold letter in primer) in the construct bearing frameshifting region of plasmid 5c in vector pTZ19R, the primers 5'-TTGTTAAATGCGCTGGATAGTGGTG-3' (from 1196 to 1220 nt) and 5'-GGAGCATTGTTCTTGTGTCGCGCTC-3' (1171 to 1195 nt) were used. PCR products were ligated, sequenced, and the EcoRI-BamHI fragment that included the mutated frameshifting region was cloned into CaSpeR-hsp-ß-gal.
Cell Culture Transfection Analysis
The Schneider 2 cells were transfected according to Di Nocera and Dawid (1983). Expression of the reporter constructs under control of hsp70 promoter was induced 48 h after transfection by 20 min at 37°C. After 2 h of incubation at 25°C cells were collected. Aliquots of cells were dissolved in a sample buffer for Western analysis (0.5 M Tris-HCl pH 6.8, 10% SDS, 14 mM ß-mercaptoethanol, 14% glycerol, 0.025% bromphenolblue). For ß-galactosidase assay, the cells were lysed in Z-buffer (60 mM Na2HPO4, 40 mM NaH2PO4, 10 mM KCl, 1 mM MgSO4, 50 mM ß-mercaptoethanol, and 0.5% NP40), and expression of ß-galactosidase was assessed by ONPG (O-Nitrophenyl-ß-D-galactopyranoside; Sigma).
Western Blot Analysis
Samples of transfected cells ( 200,000 cells per sample) were separated in 8% SDS/PAGE and blotted onto Hybond-C membrane (Amersham). Blots were stained with polyclonal antiß-galactosidase IgG (ICN Pharmaceuticals Inc.) in a dilution 1:10000 or antiDrosophila
-subunit casein kinase 2 [CK2] serum, provided by C.V.C. Glover, in a dilution 1:10000. Alkaline-phosphatase-conjugated antirabbit IgG (Sigma) was used as a secondary reagent. Blots were developed using the CDP-star detection system (Tropix) according to the recommendations of the manufacturer.
RT-PCR
Total RNA was isolated from testes, ovaries, and embryos using Trizol reagent (Gibco BRL), precipitated with LiCl, and treated by DNase I (Ambion). Samples were divided for RT and RT+ reactions. First strand of cDNA was synthesized using SuperScriptII reverse transcriptase (Gibco BRL) according to the manufacturer's instructions. Control without enzyme (RT) was processed in parallel. Samples from RT+ and RT reactions were amplified in the presence of dATP-P33 using Taq polymerase. The pair of primers 7-8 was used to amplify 1731 transcripts. Primers 5'-CAGGCCCAAGATCGTGAAG-3' and 5'-TGAGAACGCAGGCGACC-3' corresponding to the constitutively expressed gene rp49 were used to prepare a probe for loading control (fragment from 384 to 817 nt according to sequence Y13939 of GenBank was amplified). Linear range of reaction was determined in preliminary experiments. Amplification of 1731 and rp49 was performed during 23 and 17 cycles, respectively, at annealing temperature 62°C. Samples of PCR reaction were separated in 5% denaturing acrylamide gel, and products were visualized using phosphor imager Storm-840 (Amersham).
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Results |
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The presence of 1731-related sequences in the genomes of melanogaster subgroup species has been earlier reported (Montchamp-Moreau et al. 1993). Using the PCR approach, we cloned and sequenced the region of a putative frameshifting encompassing nucleotide positions 1138 to 1271 of retrotransposon 1731 (fig. 1, primers 3-4) or nearly full copy of 1731 (fig. 1, primers 1-2) from the D. simulans, D. mauritiana, and D. sechellia genomes. Altogether, 25 clones from D. simulans genomic DNA, four clones from D. sechellia, and three clones from D. mauritiana were sequenced. Figure 1 presents the alignment of several sequences and demonstrates polymorphism in this region. All these clones are related to the variant without frameshifting and bear a single-nucleotide deletion just downstream of a putative frameshifting region. These copies also contain nucleotide substitutions near a frameshifting site, which were proposed to eliminate nonpreferred codons to enhance efficiency of translation in the copies with fused ORFs (Kalmykova, Maisonhaute, and Gvozdev 1999). The detection of three different positions of a single-nucleotide deletion (fig. 1: G, position 1221; T, position 1226; G, position 1227) suggests that independent events have been occurred resulting in the Gag-Pol fused ORF origination.
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Detection of a translational pause is necessary for ORF frameshifting
The originally detected copy of retrotransposon 1731 contains two overlapping ORFs (Fourcade-Perronet et al. 1988). Classic ribosomal frameshifting is a ubiquitous mechanism to switch ORFs in retrotransposons. The +1 frameshifting is known to require translational pause (Farabaugh 1996). Actually, two rare ("hungry") Ser AGU codons (positions 1193 to 1195 and 1214 to 1216 [fig. 1]) are situated in the region of putative +1 frameshifting of 1731. At the same time, the bulk of 1731 copies in D. melanogaster genome contain Ser UCC or Cys UGC codons (positions 1193 to 1195 [fig.1]) and the Gly GGU codon (positions 1214 to 1216), all of them with a high value of codon usage in contrast to the rarely used Ser AGU codon in the copy with overlapping ORFs (Schields et al. 1988; Kalmykova, Maisonhaute, and Gvozdev 1999). These substitutions are tightly correlated with the presence of single-nucleotide deletions downstream of these codons. Deletion allows restoring ORF in the absence of frameshifting and provides a generation of a single fused ORF for the Gag-Pol polypeptide.
The position of a rare Ser AGU codon (1193 to 1195) has been earlier suspected as a site of frameshifting (Kalmykova, Maisonhaute, and Gvozdev 1999). At the same time, the alternate rare AGU Ser codon (positions 1214 to 1216) is situated just upstream of single-nucleotide deletions and also may be considered as a candidate to cause a pause and frameshifting. To address the role of these rare AGU codons in translational efficiency of overlapping ORFs, we used hsp70driven constructs containing translated regions of 1731 (positions 1141 to 1271) fused to lacZ ORF (fig. 2A, and see Materials and Methods). The level of ß-galactosidase protein expression and enzyme activity was evaluated using Schneider cells transfection (fig. 2B). The upper level of ß-galactosidase protein production was provided by the construct containing the region peculiar for the bulk of copies carrying single-nucleotide deletions and fused ORFs. This copy contains preferred codons UCC and GGU instead of the rare AGU codons. Activity of ß-galactosidase in the extracts of transfected cells provided by the copy with overlapping ORFs and AGU codons in the positions 1193 to 1195 and 1214 to 1216 was 10.1±3.0 times lower than that provided by the construct with preferred codons and single-nucleotide deletions (five experiments). This result corresponds well to the known 10% efficiency for translational frameshifting mechanism of the 1731 retrotransposon (Haoudi et al. 1995). Substitution of the preferred Gly GGU codon for the rare Ser AGU codon (positions 1214 to 1216) in the copy with overlapping ORFs results in a significant decrease of ß-galactosidase production (close to background level) caused by elimination of a proposed translational pause and failure of frameshifting (fig. 2B). This observation is in favor of a necessity of this rare Ser codon for efficient frameshifting and Pol translation. At the same time, substitution in a position 1193 to 1195 of UCC codon for AGU, which earlier had been suspected as a site of frameshifting, exerts no effect on the translation efficiency (not shown). Thus, the frameshifting site may be attributed to the position 1214 to 1216. Elimination of frameshifting coupled with a single-nucleotide deletion results in the elevated level of Pol ORF translation as a part of Gag-Pol polyprotein.
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To estimate the ratio of A1 and A1A2 types of 1731 in the genomes of melanogaster complex species, the pair of primers (primers 7-8 [fig. 1]) amplifying the 3' end of retrotransposon body and a part of 3' LTR was used to avoid amplification of solo LTRs. Abundant class of 1731 copies in D. melanogaster, D. simulans, and D. sechellia is represented by A1A2 variant, whereas the A1 one is predominant in D. mauritiana (fig. 4A). A noncharacterized additional band is detected in the D. simulans DNA (fig. 4A). Thus, duplication in 1731 LTR has occurred before divergence of melanogaster complex species.
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Y chromosome is enriched by transcriptionally active 1731 copies of A1A2 type
PCR analysis revealed the excess of A1A2 copies relative to A1 copies in the DNA samples from males as compared with females in D. melanogaster stocks (fig. 5A). XO males lacking Y chromosome (fig. 5A, lane 7) are characterized by a reduced A1A2 band that is peculiar to female DNA. This observation is unexplained by random polymorphism between the stocks because the ratio of A1A2 to A1 copies in the stocks used for XO production was typical for those in other stocks. Thus, the enrichment of Y chromosome by A1A2 variant is observed. It was demonstrated that several copies of 1731 are localized within the polytenized regions of the Y chromosome that were proposed to be related to transcriptionally active chromatin of the Y chromosome (Junacovic et al. 2003). RT-PCR analysis of RNA from testes of XY and XO males revealed a decrease of the A1A2 transcript abundance in testes of XO males (fig. 5B). Thus, a fraction of testes expressed A1A2 copies is localized on the Y chromosome.
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Discussion |
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We demonstrated a high level of translational efficiency of copies lacking frameshifting using transfection of Drosophila cell culture. Frameshifting is a crucial stage in the life cycle of retroviruses and retrotransposons that is responsible for the regulation a ratio of Gag and Pol polyproteins (Farabaugh 1996). Several retrotransposons encoding fused ORF were shown to use special mechanisms such as splicing and selective protein degradation to ensure a proper ratio of Gag and Pol polyproteins (Brierley and Flavell 1990; Atwood, Lin, and Levin 1996). However, detection of abundant unprocessed 1731 Gag-Pol polyprotein in testes (Haoudi et al. 1997) indicates that processing of this polyprotein in vivo is impaired. The local change of an amino acid sequence as a result of frameshifting elimination leads probably to inactivation of the site of protease cleavage. The 1731 copies with frameshifting strategy are still present at least in the D. melanogaster genome but are related to poorly active ones according to the ESTs database and our analysis of cDNA libraries. The biological significance of this switch of expression strategy during intragenomic evolution of retrotransposon copies remains a mystery. We speculate that a selection of "single unprocessed ORF" copies in the course of Drosophila genomes evolution might be forced by the requirement of a retrotransposon fused protein for host genome. In other words, a primary infection of a genome by retrovirus might be followed by the loss of virus-like expression strategy and acquirement of a new beneficial function. We suppose that the activity of reverse transcriptase, being a part of fused 1731 polyprotein, in the germinal tissue may be recruited for the maintenance of Drosophila telomeres mainly represented by tandem arrays of HeT-A retrotransposons lacking reverse transcriptase ORF.
Natural variations of LTR sequence of 1731 in the genomes of melanogaster complex species were revealed. The predominant variant of 1731 is characterized by imperfect 28-bp duplication in LTR designated as A1A2, whereas putative ancestral variant contains only A1 sequence (fig. 3). We demonstrated that these variations of LTR sequence of 1731 exist in all the genomes of melanogaster complex species. Thus, A1A2 duplication in 1731 LTR has been rather presented in the common ancestor of these species. However, the evolutionary fate of 1731 polymorphic variants of retrotransposon is different in Drosophila species. The A1 variant is predominant in the genome of island-endemic species D. mauritiana, whereas in the genomes of the other melanogaster complex species, the A1A2 variant is more widely presented. Species specificity of distribution of polymorphic variants of copia and blood retrotransposons has been also demonstrated (Matyunina, Jordan, and McDonald 1996; Costas, Valade, and Naveira 2001), but selective advantages of observed variations remained unclear.
We demonstrated different patterns of expression of two 1731 LTR variants. The A1A2 variant is expressed in embryos, cell culture, and testes, whereas A1 is expressed only in testes of D. melanogaster. All known 1731 LTRs (from database and our data) differ by a set of nucleotide substitutions, but no correlation of a particular single-nucleotide polymorphism with A1 or A1A2 type was revealed. Thus, functional difference of LTRs of retrotransposon 1731 may be attributed to the origination of A1A2 duplication. Duplications and deletions generated during reverse transcription are common features of retrotransposons and serve as a source of polymorphism (Matyunina, Jordan, and McDonald 1996; Costas, Valade, and Naveira 2001). A1A2 duplication results in appearance of the heat-shock and hormone-response elements localized in the A2 sequence (Ziarczyk and Best-Belpomme 1991). Both repeats, as was shown by cell culture transfection experiments, play powerful but different roles in the modulating of LTR promoter activity (Ziarczyk and Best-Belpomme 1991). Local duplication could be followed by the divergence and appearance of new functions of a repeat. Binding site of Dorsal-protein, a component of chromatin-remodeling complex involved in regulation of development (Lehming et al. 1998), has been also attributed to A2 repeat (Faure, Best-Belpomme, and Champion 1996). It is not excluded that peculiarities of tissue-specific expression of 1731 may be related to the A1, A2, or A1A2 sequences.
The testes-specific expressed putative ancestor A1 variant has been replaced in most of the melanogaster complex species by the A1A2 variant with extended profile of expression. Selective amplification of A1A2 type of 1731 in the D. melanogaster cell cultures of embryonic origin as compared with the A1 variant might be explained by the silencing of the A1 copies expression in embryos of D. melanogaster. This observation corroborates the earlier detected relationship between the transposition rate and the level of retrotransposon transcription (Boeke et al. 1985; Pasyukova et al. 1997).
We demonstrated that the bulk of genomic copies are represented by the newly arisen variant lacking frameshifting. Predominance of A1A2 variant in the D. melanogaster genome allows us to deduce that variant lacking frameshifting is related to A1A2 type. The 1731 retrotransposon family is attributed to ancient ones and characterized by the presence of a numerous defective heterochromatic copies (Alonso-Gonzalez, Dominguez, and Albornoz 2003). The database of Drosophila heterochromatic sequences is limited, impeding the monitoring of the details of evolutionary pathway of 1731 copies. The potentially active fraction of these elements related to A1A2 type lacking frameshifting is represented at least by euchromatic copy (AE003680), the testes transcribed copy containing intact ORF (Kalmykova, Maisonhaute, and Gvozdev 1999), and 1731 variant preferentially amplified in S2 cell culture (ESTs database). Fragments of 1731 copies containing single A1 repeat and fused ORF are presented in nonannotated database of heterochromatic scaffold of D. melanogaster (AABU01002750; AABU01002695). On the other hand, the A1A2 copies with overlapping ORFs (Fourcade-Peronnet et al. 1988) and fused ORF (Kalmykova, Maisonhaute, and Gvozdev 1999 [GenBank sequence AE003680]) are known. Probably, generation of fused ORF followed by loss of frameshifting and duplication in LTR has occurred independently, but successive recombination might spawn a variant containing both these traits. This variant has been spread and survives in the Drosophila genome.
Several 1731 copies with remarkable conservation between D. melanogaster stocks were shown to be located within polytenized regions of the Y chromosome, whereas none of the 16 other families of transposable elements exhibits this peculiarity (Junacovic et al. 2003). It has been proposed that conservation of 1731 copies positions may indicate acquisition of a new function (Alonso-Gonzalez, Dominguez, and Albornoz 2003; Junacovic et al. 2003). We attributed the bulk of Y-specific 1731 copies to A1A2 type and demonstrated their transcriptional activity in testes.
The copy number and transcription activity of retrotransposons are supposed to be under strong control of the genome defense system. RNAi is now considered as a mechanism of silencing of retrotransposons, thus controlling their expression and transposition (Wu-Scharf et al. 2000; Aravin et al. 2001; Kogan et al. 2003; Shi et al. 2004). Expression of 1731 was shown to be up-regulated in ovaries of flies bearing mutation in the RNAi spn-E gene encoding putative RNA helicase (Aravin et al. 2001). We demonstrated that only A1A2 structural variant is up-regulated in spn-E ovaries, and the A1 testes-specific variant remains silent. Thus, the host defense RNAi system prevents the expansion of actively transcribed A1A2 variant of 1731 in the female germline. Present results clearly indicate that the genomic expansion of active variants of retrotransposons is under host-genome control. Despite the functioning of retrotransposon silencing system, expansion of definite variants of retroelements lacking retrovirus-like expression strategy has been occurred in the course of genome evolution. We propose that invasion of host genome by retrovirus with a peculiar expression strategy may be followed by recurrent events of alteration of this type of expression and multiplication of newly evolved copies. These changes ensure an increased level and extended profile of the retrotransposon fused polyprotein expression, which might be beneficial for the organism.
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Acknowledgements |
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Footnotes |
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References |
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