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Retrotransposable Elements RI and R2 Interrupt the Rrna Genes of Most Insects (Transposable Elements/Sequence Specificity/Molecular Evolution) JOHN L

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Retrotransposable Elements RI and R2 Interrupt the Rrna Genes of Most Insects (Transposable Elements/Sequence Specificity/Molecular Evolution) JOHN L Proc. NatI. Acad. Sci. USA Vol. 88, pp. 3295-3299, April 1991 Evolution Retrotransposable elements RI and R2 interrupt the rRNA genes of most insects (transposable elements/sequence specificity/molecular evolution) JOHN L. JAKUBCZAK, WILLIAM D. BURKE, AND THOMAS H. EICKBUSH Department of Biology, University of Rochester, Rochester, NY 14627 Communicated by Igor B. Dawid, January 2, 1991 ABSTRACT A large number of insect species have been we have taken advantage of the remarkable insertion speci- screened for the presence of the retrotransposable elements RI ficities ofRI and R2 to determine their distribution in species and R2. These elements integrate independently at specific sites throughout the class Insecta. We present evidence that RI in the 28S rRNA genes. Genomic blots indicated that 43 of 47 and R2 are present in the rRNA genes of most insects. insect species from nine orders contained insertions, ranging in Unexpectedly, we found frequent examples of single insect frequency from a few percent to >50% of the 28S genes. species harboring multiple, highly divergent families ofRI or Sequence analysis of these insertions from 8 species revealed 22 R2 elements within their rDNA loci. elements, 21 of which corresponded to RI or R2 elements. Surprisingly, many species appeared to contain highly diver- AND gent copies of RI and R2 elements. For example, a parasitic MATERIALS METHODS wasp contained at least four families of RI elements; the Insect Species. Forficula auricularia, Libellula pulchella, Japanese beetle contained at least five families ofR2 elements. Mantis religiosa, Popillia japonica, Malacosoma america- The presence of these retrotransposable elements throughout num, Tibicen sp., Sphecius speciosus, Dissoteira Carolina, Insecta and the observation that single species can harbor Leptinotarsa decemlineata, the Xylocopinae species, and the divergent families within its rRNA-encoding DNA loci present Carabidae species were collected from the wild. Acheta interesting questions concerning the age of these elements and domestica, Blaberus craniifer, Hippodamia convergens, and the possibility of cross-species transfer. Oncopeltus fasciatus were purchased from Carolina Biolog- ical Supplies. Other species were obtained from laboratory- Transposable elements probably exist in the genome ofevery maintained stocks. Genomic Blots. For each insect, 1- to 3-.ug samples of total eukaryote (1). Among the most abundant types of these adult DNA was digested with one or more of the following elements are the retrotransposable elements that, like retro- restriction enzymes: HincII, HincII plus EcoRI, HincII plus viruses, move by means of an RNA intermediate (2). Retro- HindIII, Msp I, Hae III, Sau3A, and Taq I. Genomic blotting transposable elements can be divided into two major classes and hybridization were performed as described (12) except (3, 4). One class is similar to the retroviruses in that they that the hybridization was done at 600C without calf thymus contain long terminal repeats (LTRs) and their encoded DNA. Blots were probed with a BamHI-HindIII fragment proteins have amino acid similarity to those of the retrovi- from the 28S gene of Drosophila melanogaster, clone a56 ruses. The second class, termed Line 1-like or the non-LTR (12). This fragment contained 280 bp of 28S gene and 18 bp retrotransposable elements, lacks any type ofterminal repeat of RI sequence. The percentage of the 28S genes with and has lower levels of amino acid similarity to the retrovi- insertions in each species was calculated by laser densito- ruses. metric scanning of autoradiographs. RI and R2 (formerly called type I and type II insertions) are Cloning and DNA Sequencing. A Charon 35 library of non-LTR retrotransposable elements, each found at a precise parasitic wasp (Nasonia vitripennis) DNA (19) and an EMBL location in a fraction of the 28S rRNA genes ofBombyx mori 4 library constructed of Japanese beetle DNA were hybrid- and several dipteran species (5-12). The insertion sites for RI ized with the same probe used in the genomic blots. EcoRI- and R2 are 74 base pairs (bp) apart in a highly conserved HincII restriction fragments corresponding to variant 28S region of the 28S gene, the large subunit rRNA gene of genes were subcloned into Ml3mpl8 and M13mpl9 vectors eukaryotes (Fig. 1A). The presence of either RI or R2 within (20). To obtain the 3' junction of the elements with the 28S an rRNA-encoding DNA (rDNA) unit inactivates that unit gene, the mpl9 clones were sequenced using Sequenase (13-15). Only a few copies of RI and R2 are located outside (United States Biochemical) and the polynucleotide 5'- the rDNA units and they appear to be nonfunctional (6, 16, ACGGTCTGATCTCAGTTCGA-3' to prime synthesis at a 17). The high insertion specificity of R2 elements can be site 65 bp downstream of the RI insertion site. Nucleotide explained by an encoded endonuclease activity specific to its sequences of regions within the insertion elements were 28S gene insertion site (18). Individual copies of RI and R2 obtained from the mpl8 clones using the "Universal" primer have the same 3' end but may be truncated at their 5' end, a supplied by United States Biochemical. The 3' junctions of feature common to other non-LTR retrotransposable ele- the cockroach and praying mantis elements were obtained by ments (6, 7, 11, 17). cloning 0.9- to 1.2-kilobase-pair (kb) EcoRI-HincIl frag- Although transposable elements as a group are wide- ments from a genomic digest directly into mpl9. The 3' spread, it has been difficult to study the distribution of a junction sequences of the 28S gene insertions from the particular element across broad taxonomic groups due to cicada, cicada killer, grasshopper (D. Carolina), and carpen- their dispersed genomic locations and rapid sequence diver- ter bee were amplified by the inverse polymerase chain gence that limits their detection by DNA hybridization. Here reaction (21) ofMsp I- or Mbo I-digested genomic DNA using The publication costs of this article were defrayed in part by page charge Abbreviations: rDNA, rRNA-encoding DNA; 28S gene, large sub- payment. This article must therefore be hereby marked "advertisement" unit rRNA gene of eukaryotes; LTR, long terminal repeat; ORF, in accordance with 18 U.S.C. §1734 solely to indicate this fact. open reading frame. 3295 Downloaded by guest on September 28, 2021 32% Evolution: Jakubczak et al. Proc. Nat. Acad. Sci. USA 88 (1991) the primers 5'-CCATGAGCTCGGTTTCGCTAGATAGTA- 28S genes containing insertions in the region ofthe RI and R2 GATAGGGAC-3' and 5'-CGATGAATTCCCTGTTGAGC- target sites give rise to fragments of different molecular TTGACTCTAGTCTGGC-3'. These primers (containing weights. EcoRI and Sst I tails) are complementary to conserved Examples ofgenomic blots for 10 insect species are shown regions of the 28S gene downstream of the RI site. in Fig. 1B. In each case, the DNA was digested with HincII alone or in combination with a second restriction enzyme. RESULTS HincII cleaves -60 bp 5' of the R2 site in most insects; thus Genomic Blot Assay. The presence of RI and R2 elements Table 1. Summary of insects screened for insertions near the RI in different insect species was detected using the assay and R2 sites diagramed in Fig. IA. Genomic DNA from each species was 28S digested with a series of restriction enzymes, blotted onto genes nitrocellulose paper, and probed with a 280-bp fragment of inserted, the D. melanogaster 28S gene immediately 3' of the RI and Order/species Common name % R2 insertion sites. Because the ribosomal gene sequence is highly conserved within a species, uninterrupted genes Odonata 28S L. pulchella Dragonfly 10 generate a single hybridizing restriction fragment, whereas Orthoptera A R2 RI Melanoplus femurrubrum Grasshopper s5 Snacer 18S 5.8S 28S Y D. carolina Grasshopper Ik-I---t -- A. domestica House cricket 0 M. religiosa Praying mantis 35 1 kb B. craniifer Giant cockroach 25 Locusta migratoria African migratory locust 20 HcH1| Tibicen sp. Cicada 10 / Dermaptera F. auricularia Earwig 10 280 bp probe Hemiptera 0. fasciatus Milkweed bug s5 B Rhodnius prolixus Assassin bug Homoptera -<5sS Macrosiphum euphorbiae Potato aphid 6.6 - Pseudococcus affinis Mealybqg 0 Coleoptera 4.4 - Tribolium confusum Confused flour beetle 15 H. convergens Ladybug --5 Tenebrio molitor Yellow mealworm 20 2.3 4m~~~~4 2.0 P. japonica Japanese beetle 30 e m~~~~~~~~~~~~~~~~~~~~~~~~~~~~ L. decemlineata Colorado potato beetle 40 - 1.4 Family: Carabidae Ground beetle 0 1.1 Hymenoptera 0.9 N. vitripennis Parasitic wasp 25 0.6 Nasonia giraulti Parasitic wasp 15 _ Nasonia longicornis Parasitic wasp 30 Trichomolopsis dubius Parasitic wasp 15 0.3 0 S. speciosus Cicada killer 30 Subfamily: Xylocopinae Carpenter bee 15 -<5 _ Atta cephalotes Leafcutter ant .) cn Lepidoptera I- o Q 3 E , B. E > E M 3 el!3 C.)f mori Silkmoth 10-30 O r > ~~~~~~~~n e C~ r>- : Bombyx mandarina Silkmoth 25 .2 U- It. '7 Manduca sexta Tobacco hornworm 20 Lymantria dispar Gypsy moth 30 FIG. 1. Procedure used to identify insertion elements within a M. americanum Eastern tent caterpillar 0 region of the 28S rRNA genes of insects. (A) Schematic diagram ofr Diptera a typical rDNA repeat unit in insects. The black boxes represent the Drosophila (12 species)* Fruit fly <5-65 regions that correspond to the mature 18S, 5.8S, and 28S rRNAs; the Glossina pallidipes Tsetse fly 15 line represents the transcribed and nontranscribed spacer regions. Aedes aegypti Yellow fever mosquito 10 Locations of the RI and R2 insertion sites are indicated. The HincIl Culex quinquefasciatus Southern house mosquito 10 site (HcII) 5' of the R2 insertion site is conserved among insects examined in this study. The shaded box represents the 280-bp 28S Sarcophaga bullata Flesh fly -55 gene sequence used as hybridization probe. (B) Genomic blots of The percentage of the 28S genes with insertions in each species DNA from 10 insects hybridized with the 28S gene probe.
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