*Institute of Medical Biology, General Genetics, University of Vienna, Austria;
Department of Botany, University of Georgia;
Institute of Cell Biology, University of Tübingen, Germany; and
§Pritzker Laboratory for Molecular Systematics and Evolution, The Field Museum, Chicago, Illinois
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Abstract |
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Introduction |
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In many instances, it is not possible to deduce the origin of satDNA families. Based on the "expansions-contractions" model outlined by Southern (1975)
, the so-called "library" hypothesis proposes that related species share a "library" of conserved satDNA sequences (Salser et al. 1976
). Even in closely related species, different library sequences may be amplified to high copy numbers, leading frequently to species specificity of major satDNAs. Recently, Mestrovic et al. (1998)
favored this hypothesis to explain satDNA evolution within the beetle genus Palorus.
Csink and Henikoff (1998)
recently proposed a general model for the function of satDNA that is based on observations that specific proteins binding at euchromatic sites during interphase bind a subset of centromeric satDNAs during metaphase. Csink and Henikoff (1998)
define centromeres basically by two functional features: (1) the late replication in S phase and (2) satDNAs making up the main component of a typical centromere to ensure the exclusion of early replication origins. Expanded satDNAs would "borrow" DNA-binding proteins for stabilization during mitosis. Accordingly, a satDNA library would consist of modules that, once amplified, ensure protein storage during mitosis and late replication in S-phase and, thereby, centromere functions. Other authors have suggested more specific functions for satDNA; for example, Bonaccorsi et al. (1990)
proposed that some Y-chromosomal satDNAs in Drosophila would ensure storage of testis-specific proteins.
However, it is not yet understood where such library modules originate. Incidentally, parts of mobile elements have been identified as the main component of specific heterochromatic satDNA families. The long direct terminal repeats of the pDv transposon (Evgen'ev et al. 1982
; Zelentsova et al. 1986
) show significant sequence similarity to the pvB370 satDNA family that is located in the centromeric heterochromatin of a number of species of the Drosophila virilis group (Heikkinen et al. 1995
). For whales and dolphins, Kapitonov, Holmquist, and Jurka (1998)
provided direct evidence that the main heterochromatic satDNA of Cetaceans is composed of long interspersed nuclear element (LINE)like repeats. The binding sites for the major centromere-binding protein (CENP-B) of mammals, the "CENP-B box," matches the terminal inverted repeats (TIRs) of pogo transposons (reviewed in Kipling and Warburton 1997
), and the protein CENP-B itself is an ancient descendant of a pogo-like DNA transposase with a conserved DNA-binding domain (Tudor et al. 1992
; Smit and Riggs 1996
). Similar observations were made for plants (Jiang et al. 1996
; Pelissier et al. 1996
).
Mobile elements are known to frequently integrate into heterochromatin where they accumulate (Felger and Sperlich 1989
; Nurminsky et al. 1994
; Carmena and Gonzalez 1995
; Pimpinelli et al. 1995
; Dimitri et al. 1997
; Dimitri and Junakovic 1999
). As was recently shown, the centromeric region of the Y chromosome of Drosophila melanogaster might have originated by insertions and amplifications of telomeric retrotransposons (Agudo et al. 1999
). Repeated arrays of mobile elements can also induce local heterochromatin formation within euchromatic regions of the chromosomes (Dorer and Henikoff 1994
; Thompson-Stewart, Karpen, and Spradling 1994
). Thus, the analysis of satDNA families may eventually reveal insights into the evolutionary dynamics of ancient mobile elements and their role as genome builders, as proposed by Jurka (1998)
.
In the present paper, we characterize a family of repetitive DNAs isolated from the genomes of the closely related Drosophila obscura group species D. subobscura, D. guanche, and D. madeirensis, which were first described as SGM sequences by Bachmann (1996)
, and we discuss their evolutionary dynamics. SGM-derived sequences are one major highly repetitive satDNA in the heterochromatin of D. guanche, and they occur in the genomes of its sibling species, D. subobscura and D. madeirensis, with a significantly lower copy number. In particular, in the latter two species, repetitive SGM elements are dispersed throughout the euchromatin and clearly show recent mobility with some functional and structural similarities to miniature inverted-repeat transposable element (MITE)like transposons. SGM sequences are homologous to some not-well-characterized insertion sequences detected earlier in other obscura group species (Marfany and Gonzàlez-Duarte 1992
; Steinemann and Steinemann 1993
; Miller et al. 1995
; Hagemann et al. 1998
; Vivas et al. 1999
). Subsections, or so-called modules, of the SGM sequence family show significant sequence similarity to short dispersed segments isolated from other species throughout the Drosophila and Sophophora radiation.
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Materials and Methods |
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Total genomic DNA of D. subobscura, D. guanche, and D. madeirensis digested with EcoRI or MspI was ligated into the plasmid vector pUC19. White colonies were transferred to a nitrocellulose membrane and hybridized under high-stringency conditions (hybridization temperature: 68°C; washing: 0,2 x SSC, 0.1% SDS) with digoxigenin-labeled (Roche) genomic DNA of the respective species. Clones producing the strongest hybridization signals were interpreted as those containing highly repetitive DNA.
Sequencing of both strands of the obtained clones was performed according to the chain termination method (Sanger, Nicklen, and Coulson 1977
) using the Autoread sequencing kit and an A.L.F. automatic sequencer (Pharmacia).
Genomic Southern blot analyses probed with P32 random-primed SGM restriction clones were performed as described in Miller et al. (1992)
.
DNA Sequence Analysis
Nonredundant database searches were conducted using the ungapped advanced BLAST search engine of the National Center for Biotechnology Information (NCBI) on the NCBI's website (http://www.ncbi.nlm.nih.gov/BLAST), accessed in March 2000 (Altschul et al. 1997
). Multiple and pairwise alignments were performed using the program CLUSTAL W (Thompson, Higgins, and Gibson 1994
) and subsequently improved by eye (CLUSTAL W parameters used: gap opening penalty, 10.00; gap extension penalty, 0.05).
Phylogenetic Analysis
Phylogenetic analyses were performed using the PAUP*, version 4.0b4a, software package (Swofford 1998
). DNA sequence alignments were generated using the methods mentioned above. The tree topologies reported here were obtained by the neighbor-joining algorithm (Saitou and Nei 1987
) implemented in PAUP*, version 4.0b4a.
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Results and Discussion |
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In the present study, we focused our survey on tandemly arranged SGM sequences by cloning restriction satellite DNA of D. guanche. Prominent bands of 500600 bp obtained after agarose gel electrophoresis of D. guanche DNA restricted with MspI, BamHI, or PstI were subcloned and analyzed in detail (fig. 1A,
lanes 79). We did not clone the most prominent 290-bp band obtained by BamHI digestion (fig. 1A,
lane 7), since it consists of a 290-bp species-specific D. guanche satDNA described earlier (Bachmann, Raab, and Sperlich 1989
). Five of the obtained
500600-bp band restriction clones, i.e., gmsp1, gmsp2, gbam1, and gpst1 and gpst2, were picked randomly from these three independent restriction-cloning strategies and were used as probes in genomic Southern hybridizations. As shown in figure 1B,
filter-bound genomic DNAs from D. guanche, D. subobscura, and D. madeirensis digested with BamHI, MspI, and PstI were probed with the SGM restriction clone gbam1. In D. guanche, each of the three restriction digests gave rise to strong, "ladderlike" hybridization patterns with a constant monomeric length of
500600 bp (lanes 79). Such patterns are characteristic of reiterated high-copy-number DNAs with units of a specific size. The formation of multimer fragments of
1,000, 1,500 and 2,000 bp is in accordance with restriction site polymorphisms within the tandem arrays typical for heterochromatic satDNAs. Compared with D. guanche, genomic DNAs of D. madeirensis and D. subobscura yield less intense hybridization signals when hybridized with the SGM restriction clone gbam1 (lanes 16). The same patterns were obtained by reprobing the membrane with the four additional restriction clones.
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In D. guanche, SGM sequences make up approximately 10% of the whole genome. This number has been deduced from rough copy number estimates by comparative genomic dot blot analyses and is in accordance with estimates obtained from screening a complete genomic D. guanche EMBL3 library with the SGM restriction clone gbam1 under stringent hybridization conditions (data not shown). However, these estimates refer to the whole SGM family. They are not appropriate for discriminating between tandemly arranged heterochromatic and dispersed euchromatic SGM sequences.
SGM Sequences Are Composed of Sequence Modules and Are Related to Insertion Sequences
The nucleotide sequence of the D. guanche shotgun clone B49 was used as an SGM query reference for Advanced Blastn searches of the nonredundant GenBank database, accessed in March 2000, for similar sequences. B49 shows significant sequence similarity with a number of GenBank entries exclusively derived from species of the subgenera Drosophila and Sophophora (table 2
). The best matches were obtained with sequence entries from species of the obscura species group, i.e., the RNA polymerase II genes of D. subobscura and D. madeirensis, the alcohol dehydrogenase genes of D. subobscura and D. madeirensis, the Y-chromosomal insertion sequences ISY2 and ISY2/3 of D. miranda, the insertion sequence ISamb of D. ambigua, and P-"repressor-like" gene cluster units of D. guanche and D. subobscura (table 2
).
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The SGM sequences reported here share high sequence similarity with two of the modules described by Vivas et al. (1999)
, i.e., the long sequence module (LS) and the inverted repeat (IR), as shown in figure 2
. Whereas the LS module is part of all eight SGM clones analyzed here (positions 1148), the IR812 module matches only the three shotgun clones 6A-K/L, B49, and pMH712 (positions 691885). The SGM section spacing LS and IR-homologous modules shares no significant similarity with any other earlier-described GEM module. In accordance with the nomenclature of Vivas et al. (1999)
, we designated this section (positions 201690 in fig. 2
) the middle module (MM).
In all SGM sequences analyzed here and in most database entries that match the SGM query sequence B49, the MM is linked to the LS motif through a GTCT/C microsatellite of variable length (positions 149200 in fig. 1
and table 1
). The GTCT/C repeats are missing only in the intervening region of consecutive P-"repressor-like" genes of the P-element-related gene clusters of D. subobscura and D. guanche (X60436, L32023 in table 2
and fig. 4
). However, in these two cases the SGM-related section harbors the designated promoter elements CAAT-box, GC-box, octamer motif, and TATA-box (Miller et al. 1995
), which are located in the MM and IR modules. In the P-element-related gene cluster of D. subobscura and D. guanche, the SGM-related sections clearly serve a host function as de novo regulatory elements driving the expression of P-"repressor-like" proteins (Miller et al. 1995
; Miller, McDonald, and Pinsker 1997
; see below).
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SGM Sequences Are Related to Recently Active Transposons in D. subobscura and D. madeirensis
The characteristics of the SGM sequence family suggest a close relationship between SGM repeats and mobile elements. In fact, sequence alignments of the homologous RNA polymerase II genes (RpII215) of the closely related sibling species D. subobscura, D. guanche, and D. madeirensis revealed recent SGM mobility. A complete insertion sequence homologous to the SGM repeats was found to be inserted into the first large intron of the RpII215 genes of D. subobscura and D. madeirensis (table 2
) but is absent in the respective region of the D. guanche RpII215 gene (Llopart and Aguade 1999
). Taking the intronic region of the D. guanche RpII215 gene as a reference sequence (Llopart and Aguade 1999
), the exact insertion site of the SGM repeat within the homologous genes of D. subobscura and D. madeirensis could be determined. The presumptive target site is found as an unusually AT-rich 21-bp sequence which harbors palindromic features (fig. 3A
). Since the SGM-insertion sites are identical in both RpII215 homologs of the closely related species D. subobscura and D. madeirensis, it seems reasonable to assume that the insertion took place in their common ancestor 12 MYA (Gonzalez et al. 1990
; Russo, Takezaki, and Nei 1995
).
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The SGM-homologous RpII215 insertion sequences of D. subobscura and D. madeirensis were 741 and 784 bp long, and no open reading frames (ORFs) coding for any known proteins were found by using the blastx program in an advanced BLAST search (http://www.ncbi.nlm.nih.gov/BLAST/). Furthermore, both RpII215 insertion sequences were translated in all six potential reading frames, and their hypothetical products were scanned for homology to reverse transcriptase or integrase motifs known to be characteristic for RNA or DNA transposons. No such motifs were detected. Thus, the structural features of these recently inserted SGM insertion sequences of D. subobscura and D. madeirensis more closely resemble short interspersed nucleotide elements or MITEs described earlier for other organisms (Bureau and Wessler 1994
; Song et al. 1998
; Izsvak et al. 1999
; Zhang, Arbuckle, and Wessler 2000
). This idea is supported by secondary-structure predictions deduced by the MFOLD prediction program (http://bioweb.pasteur.fr/seqanal/interfaces/mfold-simple.html) which indicate that SGM sequences can form energetically stable hairpin structures (data not shown). Although these predictions have to be confirmed by experimental data, these stable structures show some similarities to the deduced structures of MITEs (Izsvák et al. 1999
). In contrast to the tandemly arranged SGM sequences that are a major satDNA in D. guanche, we designate these mobile dispersed, euchromatic elements as SGM insertion sequences (SGM-IS). A second case for recent SGM mobility in the same species cluster was detected in the upstream regulatory section of the Adh genes of D. subobscura and D. madeirensis. Based on genomic sequence data obtained from the respective Adh loci of D. subobscura, D. madeirensis, and D. guanche (Marfany and Gonzàlez-Duarte 1993
), SGM-IS elements were only detected in the first two species and were absent in D. guanche at homologous positions (fig. 3B
). The accessible Adh sequences of D. madeirensis and D. subobscura (X60112 and M55545 in Marfany and Gonzàlez-Duarte 1993
) start with a 194-bp section and a 196-bp section homologous to the 3' region of the SGM-IS element described above, both harboring the characteristic 3' subterminal 14-bp IR and the 44-bp termini (fig. 3B
). Since more upstream sequence data are available from the homologous Adh region of D. guanche (X60113), the exact insertion site could be determined. Similar to the deduced SGM insertion site in the RpII215 genes of D. madeirensis and D. subobscura, the IS-Adh target site is highly AT-rich, but no clear palindromic motifs are present (fig. 3B
).
Insertion sequences which are related to the SGM-IS elements reported here have previously been described in other obscura group species, i.e., the insertion sequence ISY2/3 in the neo-Y-chromosomal LCP genes in D. miranda (Steinemann and Steinemann 1993
), the retrosequence 812 in the Adh pseudogene of D. subobscura (Marfany and Gonzàlez-Duarte 1992
), SGM-like insertion sequences in the domesticated P-element "repressor-like" A-cluster units of D. guanche and related sequences (Miller et al. 1995
; Paricio et al. 1996
), the ISamb element inserted into exon 3 of a P-element derivative in D. ambigua (Hagemann et al. 1998
), and the diverse so-called GEM repeat family found in various obscura group species (Vivas et al. 1999
).
The phylogenetic relationships of the SGM elements reported here are shown in figure 4
. Genetic distances were calculated for all pairwise comparisons of the 15 SGM-related sequences and used to construct a neighbor-joining dendrogram. As deduced from the dendrogram, the SGM-sat DNAs gmsp1, gmsp2, gbam1, and gpst1 and gpst2 form a clade, indicating that the tandemly repeated SGM sequences of heterochromatic origin have evolved according to the concept of concerted evolution (Dover and Tautz 1986
). However, within the clade of SGM-sat DNAs, two subfamilies of SGM restriction satellite sequences can be clearly identified, i.e., the msp type and the bam/pst type. The high bootstrap values support our SGM classification proposed here with regard to (1) the dispersed SGM-IS elements and their euchromatic derivatives, (2) the D. guanchespecific heterochromatic SGM-sat DNAs, and (3) SGM-like IS elements from other obscura group species.
In most of the cases, SGM-IS and SGM-like insertions were detected in nonfunctional, rapidly degenerating genomic sections, e.g., eroding pseudogenes (ISAdh 812), inactive DNA transposons (ISamb), and a translocated gene cluster that is in the process of degeneration due to its proximity to constitutive heterochromatin (ISY2/3). In the case of the neo-promoter elements detected in the domesticated P-neogene cluster of D. guanche, D. subobscura, and D. madeirensis, such an SGM-related insertion sequence was integrated into the fourth exon of an eroding P element in their common ancestor more than 4 MYA (Miller, McDonald, and Pinsker 1997
). In contrast to the insertions mentioned above, the SGM-IS elements IS-RpII215 (fig. 3A
) and IS-Adh (fig. 3B
) of the common ancestor of D. subobscura and D. madeirensis are very recent ones integrated into less rapidly degenerating host gene regions.
Evolutionary Dynamics of SGM Elements in obscura Group Species
SGM elements are a family of repetitive DNAs found in the obscura group species D. subobscura, D. guanche, and D. madeirensis. Based on the molecular analysis of at least two independent cases of recent SGM mobility, i.e., by inserting into euchromatic host gene loci of D. subobscura and D. madeirensis, the exact molecular structure and function of this IS element family could be deduced. Derivatives of once-active SGM-like insertion sequences were detected in other obscura group species, suggesting earlier bursts of activity. SGM-IS elements share the following characteristic features: (1) short lengths, ranging from 600 to 1,200 bp; (2) 14-bp IRs, one at the 5'-terminal and the other at the 3'-subterminal position upstream of a characteristic 44-bp terminal section; and (3) a well-conserved central region without coding function, composed of modules named LS, GTCT/C-microsatellite, MM, and the IR812 section (fig. 5A
).
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According to the model recently proposed by Csink and Henikoff (1998)
, centromeres are basically defined by two main functional features, i.e., their late replication in S phase and their storage function of specific DNA-binding proteins during mitosis. During interphase, these proteins are bound at euchromatic sites and used for regulation of gene expression. Following this model, it seems plausible to assume that the TE-derived SGM-sat DNA cluster of D. guanche would consist of a collection of modules appropriate to ensure protein storage during mitosis and late replication during S phase, and hence centromere function. As shown by Dorer and Henikoff (1994)
, tandem copies of P-element transgenes located in the euchromatin become silenced by a homology-dependent, epigenetic mechanism that is similar to position effect variegation (Dorer and Henikoff 1994, 1997
). Repeat-induced silencing effects have previously been reported in plants and fungi (Matzke and Matzke 1995
; Selker 1997
). In Drosophila, cases for cosuppression acting at the transcriptional and posttranscriptional levels have recently been reported (Pal-Bhadra, Bhadra, and Birchler 1997, 1999
; Jensen, Gassama, and Heidmann 1999
). Epigenetic silencing mechanisms were found throughout all living kingdoms and are now considered an ancient evolutionary defense mechanism against invading genomic parasites (Bingham 1997
; Yoder, Walsh, and Bestor 1997
; McDonald 1998
; Wolffe and Matzke 1999).
Based on the data of this survey and others found in the literature, we propose the following evolutionary scenario: SGM-like insertion sequences have been active in different lineages of obscura group species, causing insertions in the genomes of D. miranda, D. ambigua, and D. subobscura, D. guanche, and D. madeirensis. In the common ancestor of the latter species triad, an SGM-insertion into a degenerating P transposon gave rise to de novo promoter elements driving the expression of the downstream-located P-"repressor-like" protein in the domesticated P-element gene cluster (Miller et al. 1995, 1999
; Miller, McDonald, and Pinsker 1997
; fig. 5C
). This stochastic insertional event might have provided a starting point for the functional "resurrection" of the P-derived coding section in the common ancestor at least 4 MYA by reactivating the expression of P-"repressor-like" proteins. Molecular domestication of such P-"repressor-like" proteincoding genes has arisen independently at least twice in the course of Drosophila evolution (Nouaud and Anxolabéhère 1997
; Nouaud et al. 1999
; Miller et al. 1999
). Recent examples of molecular domestication of TE-derived coding sections now serving essential host genome functions have recently been described in mammals (Best et al. 1996
; Agrawal, Eastman, and Schatz 1998
; Hiom, Melek, and Gellert 1998
).
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Conclusions |
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TEs harbor an attractive repertoire of functional abilities for a host cell. Cis-regulatory sections within the elements orchestrate tempo and mode of TE expression, thus representing mobile enhancers. Proteins encoded by TEs mainly direct their propagation within the genome by recruitment of host-encoded factors. They mediate excision, replication, and integration of defined DNA fragments, and some of these proteins are able to manipulate important host factors by altering their original function. Furthermore, TEs are common targets for host-mediated silencing mechanisms by modification of TE chromatin structure. Thus, to co-opt such TE structures and functions by taming their "anarchistic behavior" can be an important evolutionary innovation for the benefit of a host genome.
Indeed, cases are accumulating in the recent literature indicating that derivatives of once-active TEs are co-opted by the host genome by means of (1) adaptation to de novo regulatory units derived from TE cis-regulatory units driving the expression of adjacent host-encoded genes (for review, see McDonald et al. 1997
; Wessler 1998
); (2) molecular domestication, i.e., the molecular transition into a new host-encoded function (Miller et al. 1992, 1999
; Miller, McDonald, and Pinsker 1997
); and (3) conversion into a functional chromosomal structure, i.e., the telomere (Pardue and DeBaryshe 1999
) or the centromere (Kipling and Warburton 1997
; Kapitonov, Holmquist, and Jurka 1998
; Agudo et al. 1999
; this study).
The SGM sequence family provides an excellent model system with which to study the evolutionary dynamics of mobile elements co-opted by a host genome. The widespread distribution in the species of the D. obscura group indicates that SGM elements were already present in the common ancestor of the group 2025 MYA (Russo, Takezaki, and Nei 1995
). For example, they have played an important role in the heterochromatization of the translocated neo-Y-chromosomal LCP gene cluster of D. miranda (Steinemann and Steinemann 1993
) and in the erosion of autosomal P transposons in D. ambigua (Hagemann et al. 1998
). Evidence for their more recent transpositional activity comes from an insertion into the progenitor of the P-neogene cluster in the common ancestor of D. subobscura, D. guanche, and D. madeirensis (>4 MYA), giving rise to the de novo A-type promoter driving the expression of domesticated P-element "repressor-like" coding genes (Miller et al. 1995
; Miller, McDonald, and Pinsker 1997
). SGM elements retained their activity in the common ancestor of the closely related species D. subobscura and D. madeirensis (12 MYA), as indicated by their presence in the RpII215 and Adh genes, respectively (this study), and their absence in RpII215 of D. guanche. In this endemic species, SGM sequence derivatives account for up to 10% of the genome and are tandemly organized in a heterochromatic, species-specifically amplified satDNA.
As proposed by Csink and Henikoff (1998)
, centromeres are basically defined by their late replication in S phase and their storage function of specific DNA-binding proteins during cell division. Accordingly, the main function of the SGM-satDNA sequences of D. guanche would be provided by suitable sequence modules to ensure protein storage during mitosis. The species-specific amplification of TE-derived modules toward a major SGM-sat DNA in D. guanche strongly supports the library hypothesis outlined by Salser et al. (1976)
stating that each species has a specific collection of sequences with the potential for gaining centromere function once they are tandemly amplified to high copy numbers.
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Supplementary Material |
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Acknowledgements |
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Footnotes |
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1 Abbreviations: IR, inverted repeat; LS, long sequence; MITE, miniature interspersed transposable element; MM, middle module; MYA, million years ago; satDNA, satellite DNA; SGM sequences, Drosophila subobscura, Drosophila guanche, and Drosophila madeirensis; SGM-sat DNA, SGM-related satellite DNAs of D. guanche; SGM-IS elements, insertion sequences of D. subobscura, D. guanche, and D. madeirensis; SINE, short interspersed repeat sequence; TIR, terminal inverted repeat.
2 Keywords: Drosophila genomics
genome evolution
interspersed repeats
mobile elements
repetitive DNA
satellite DNA
transposons
3 Address for correspondence and reprints: Wolfgang J. Miller, Institut für Medizinische Biologie, AG Allgemeine Genetik, Universität Wien, Währingerstrasse 10, A-1090 Vienna, Austria. E-mail: wolfgang.miller{at}univie.ac.at
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