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Between Drosophila Species Copyright 0 1990 by the Genetics Society of America Evidence for Horizontal Transmission of theP Transposable Element Between Drosophila Species Stephen B. Daniels,* Kenneth R. Peterson: Linda D. Strausbaugh,* Margaret G. Kidwell+ and Arthur Chovnick*' *Department of Molecular and Cell Biology, University of Connecticut, Stows, Connecticut 06268, and ?Departmentof Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721 Manuscript received September 2 1, 1989 Accepted for publication November 2, 1989 ABSTRACT Several studies have suggested that P elements have rapidly spread through natural populations of Drosophila melanogaster within the last four decades. This observation, together with the observation that P elements are absent in the otherspecies of the melanogaster subgroup, has lead to the suggestion that P elements may have entered the D. melanogaster genome by horizontal transmission from some more distantly related species. In an effort to identify the potential donor in the horizontal transfer event, we have undertaken an extensive survey of the genus Drosophila using Southern blot analysis. The results showed that P-homologous sequences are essentially confined to the subgenus Sophophora. The strongest P hybridization occurs in species from the closely related willistoni and saltans groups. The D. melanogaster P element is most similar to the elements from the willistoni group. A wild- derived strain of D. willistoni was subsequently selected for a more comprehensive molecular exami- nation. As part of the analysis, a complete P element was cloned and sequenced from this line. Its nucleotide sequence was found to be identical to the D. melanogaster canonical P, with the exception of a single base substitution at position 32. When the cloned element was injected into D. melanogaster embryos, it was able to both promote transposition of a coinjected marked transposon and induce singed-weak mutability, thus demonstrating its ability to function as an autonomous element. The results of' this study suggest that D. willistoni may have served as the donor species in the horizontal transfer of P elements to D.melanogaster. ERY little is known about the origin and evolu- have been shown to be the causative agents of one of V tionaryhistory of mobile element systems.A the two well-documentedsystems of hybrid dysgenesis mobile element family might originate in a species de in D. melanogaster. Hybrid dysgenesis is a syndrome novo by mutational or recombination events that alter of correlated genetic abnormalities thatis induced in or reorder sequences already present within the ge- thegermline of progeny from certain intraspecific nome (e.g., FINNEGAN1985). Alternatively, mobile crosses(KIDWELL, KIDWELL and SVED1977). [For elements might be acquiredby horizontal transmission comprehensive reviews of P elements andP-M hybrid from some other species. Such transfer events could dysgenesis, see ENGELS (1 983, 1989).] be mediated by one or moreof a number of different P elements in D. melanogaster exhibitalmost no vectors (e.g., viruses). At present, information on the sequence polymorphism but are heterogeneous with mechanismsand relative frequencies of these two respect to size (O'HARE andRUBIN 1983). They can modes of origin is completely lacking. If horizontal bedivided into two types, complete (autonomous) transmission should proveto be other thana relatively elements and defective (nonautonomous) ones. Com- isolated, rare event, then the implications could have pleteelements are 2.9 kb in lengthand encode a a dramatic impact on many aspects of evolutionary transposaseenzyme (RIo, LASKI and RUBIN 1986). theory. Defective elements are deletion-derivatives that are The well-characterized P transposable element fam- smaller and variable in size. The deletion of internal ily represents an ideal system in which to examine a P element sequences occurs at a high frequency under variety of evolutionary issues. P elements were first conditions of activetransposition (VOELKERet al. detected in Drosophilamelanogaster andhave been 1984; DANIELSet al. 1985; SEARLESet al. 1986; Tsu- extensively studied at both the genetic and molecular BOTA and SCHEDL1986). Both types of elements have levels. They are particularly interesting because they 31-bp inverted terminal repeats and create an 8-bp target site duplication upon insertion. Defective ele- ' To whom reprint requests 5hould be addressed. ments can undergo transposition onlyin the presence The public;ktion costs of this article were partly defrayed by the payme~~t of active autonomous elements. of page charges. This articlen~ust therefore be hereby marked "advertisement" in accord;~ncewith 18 U.S.C. $1754 solrly to indicate this fact. One way tostudy the evolutionary origins and Genettcc 124: :4:39-:4.5.5 (b'rb~n~a~.y,1990) 340 S. B. Daniels et al. histories of mobile element families is to undertake analysis, we isolated, cloned and sequenced an intact, surveys of their phylogenetic distributions.At present, functional D. willistoni P element. Our results support it is known that P-homologous sequences are distrib- the hypothesis that P elements have been transferred uted throughout thespecies groups that comprise the horizontally between Drosophila species. subgenus Sophophora (ANXOLAB~HERE, NOUAUDand P~RIQUET1985; LANSMANet al. 1985; DANIELSand MATERIALS AND METHODS STRAUSBAUGH1986), although they are absent from Fly stocks: All of the species used in this study are listed the species most closely related toD. melanogaster, i,e., in Table 1 or in the legend to Figure 3; each listing includes the species of the melanogaster subgroup (BROOKFIELD, one of the following designations to denote the laboratory MONTGOMERYand LANGLEY1984). This observation, from which the stock was obtained: BG, National Drosophila Species Resource Center, Bowling Green State University; together with theobservation that P elements are WH, W. HEED,University of Arizona; JC, J. COYNE,Uni- completelylacking in old laboratory strains of D. versity of Chicago, FA, F. AYALA,University of California melanogaster (BINGHAM,KIDWELL and RUBIN 1982; at Davis; LE, L. EHRMAN,State University of New York at ANXOLAB~H~RE,KIDWELL and P~RIQUET1988), sug- Purchase; MS, M. SEIGER,Wright State University. The D. willistoni P element was cloned from a line estab- gests that the transposon may entered the P have D. lished from a single female caught in Florida in 1983 by M. melanogaster genome by horizontal transmission, per- SEIGER.This isofemale line has been designated "willi #7." hapsas the result of some infectious process (e.g., Strains of D. melanogaster that wereemployed in this BINGHAM,KIDWELL, and RUBIN1982). Moreover, it study are as follows: Harwich and r2are strong P strains has been proposed that a distantly related memberof that contain many P element copies. Canton S is an M strain devoid of P elements (i.e., it is a true M strain). rySU6is a true the genusmay have served as the donorspecies (DAN- M strain with a small deletion in the coding region of the IELS et al. 1984; DANIELSand STRAUSBAUCH1986). rosy gene. C(I)DX,yf;ry5"6 is a compound-X, true M strain Whether P elements are of recent origin in D. mela- bearing the ry5"' allele. y sn"; ry50his an M strain containing nogaster or whether their introduction occurred at the hypermutable singed-weak allele (ENGELS1979, 1989) some more distant point in time has been the subject and a rosy eye color marker. ry5u6P[ry+ A2-3](99B), abbre- viated A2-3(99B), is a rySfJhline transformed with the engi- of some debate (e.g., ENGELS1986). neered P element, P[ry+A2-31, which contains a copy of a If the introduction weresufficiently recent to essen- wild type rosy gene inserted into afunctional P element with tially preclude any appreciable base sequence diver- a deleted third intron [for further details, see LASKI,RIO gence,then: (1) there must be at least one species and RUBIN(1 986) and ROBERTSONet al. (1988)]; A2-3(99B) otherthan D.melanogaster thatcontains an intact, contains two elements in reverse tandem at cytological functional P element, and (2) the elements (or atleast position 99B(H. ROBERTSON,personal communication). A2- 3(99B)/ryjOS individuals were obtained from the F, progeny a subset of them) within this species must have se- of a cross between homozygous A2-3(99B) and ry506 lines. quences that are virtually identical to those of the D. See LINDSLEYand GRELL(1 968) for a description of genetic melanogaster canonical P (O'HAREand RUBIN1983). symbols not described. The results of previous studies would suggest that the Plasmids: pr25.1 contains a genomic fragment from the D. melanogaster P strain, 82 (SPRADLING andRUBIN 1982). mostreasonable place to start a search for such a The cloned DNA consists of a complete P element flanked potential donor species is within the genus itself. Al- by genomic sequences from cytologicalregion 17C; the though there have beena number of studies that have nucleotide sequence of this P element has been determined examined the phylogenetic distributions of P-homol- (O'HAREand RUBIN1983). The 1.7-kb XhoIISalI fragment ogoussequences within Drosophila (BROOKFIELD, from the center of the P element was used as probe in some of our experiments. MONTGOMERY and LANGLEY1984; DANIELSet al. pr25.7BWC ("both wings clipped"), constructed by K. 1984; ANXOLAB~H~RE,NOUAUD and P~RIQUET1985; O'HARE,contains a P element that is lacking 39 bp from its LANSMANet al. 1985; DANIELSand STRAUSBAUCH 5' and 23bp from its3' end.
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