Evidence for horizontal transmission of the P transposable element between Drosophila species.

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 other species 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 group. A wild-derived strain of D. willistoni was subsequently selected for a more comprehensive molecular examination. 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.

[1]  D. Finnegan.  Transposable elements in eukaryotes. , 1985, International review of cytology.

[2]  J. States,et al.  Isolation and fractionation of total nucleic acids from tissues and cells. , 1986, Journal of biochemical and biophysical methods.

[3]  R. Lewin.  Can genes jump between eukaryotic species? , 1982, Science.

[4]  G. Rubin,et al.  P element insertions and rearrangements at the singed locus of Drosophila melanogaster. , 1988, Genetics.

[5]  M. Uyenoyama.  Quantitative models of hybrid dysgenesis: rapid evolution under transposition, extrachromosomal inheritance, and fertility selection. , 1985, Theoretical population biology.

[6]  E. Nitasaka,et al.  Excision of one of two defective P elements as the cause of alternate mutational events (sn+ and sne) of the singed bristle allele snw in Drosophila melanogaster. , 1988, Idengaku zasshi.

[7]  G. B. Wisely,et al.  Frequent Imprecise Excision among Reversions of a P Element-Caused Lethal Mutation in Drosophila. , 1984, Genetics.

[8]  A. Greenleaf,et al.  Sites of P element insertion and structures of P element deletions in the 5' region of Drosophila melanogaster RpII215 , 1986, Molecular and cellular biology.

[9]  P. Schedl,et al.  Hybrid dysgenesis-induced revertants of insertions at the 5' end of the rudimentary gene in Drosophila melanogaster: transposon-induced control mutations. , 1986, Genetics.

[10]  T Darden,et al.  Evolution and extinction of transposable elements in Mendelian populations. , 1985, Genetics.

[11]  A. Handler,et al.  Mobility of P elements in drosophilids and nondrosophilids. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[12]  F. Ayala,et al.  GENETIC DIFFERENTIATION DURING THE SPECIATION PROCESS IN DROSOPHILA , 1974, Evolution; international journal of organic evolution.

[13]  A. Wilson,et al.  Molecular Evolution in Drosophila and the Higher Diptera II. A Time Scale for Fly Evolution , 1984 .

[14]  R. Lewin.  Fish to bacterium gene transfer. , 1985, Science.

[15]  G M Rubin,et al.  Identification and purification of a Drosophila protein that binds to the terminal 31-base-pair inverted repeats of the P transposable element. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[16]  S. Stacey,et al.  Distribution and conservation of mobile elements in the genus Drosophila. , 1986, Molecular biology and evolution.

[17]  W. Bender,et al.  Studies on the mechanism of heterochromatic position effect at the rosy locus of Drosophila melanogaster. , 1984, Genetics.

[18]  S. Daniels,et al.  Dysgenesis-induced instability of rosy locus transformation in Drosophila melanogaster: analysis of excision events and the selective recovery of control element deletions. , 1985, Genetics.

[19]  G. Rubin,et al.  Vectors for P element-mediated gene transfer in Drosophila. , 1983, Nucleic acids research.

[20]  T. Dobzhansky,et al.  GEOGRAPHY OF THE SIBLING SPECIES RELATED TO DROSOPHILA WILLISTONI, AND OF THE SEMISPECIES OF THE DROSOPHILA PAULISTORUM COMPLEX , 1971, Evolution; international journal of organic evolution.

[21]  T. Todo,et al.  Structures of defective P transposable elements prevalent in natural Q and Q-derived M strains of Drosophila melanogaster. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. G. Kidwell,et al.  Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: A Syndrome of Aberrant Traits Including Mutation, Sterility and Male Recombination. , 1977, Genetics.

[23]  T. Grigliatti,et al.  Evolution of P transposable elements: sequences of Drosophila nebulosa P elements. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[24]  M. G. Kidwell.  Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Fraser.  Symposium: Genetics in Entomology: Transposon-mediated Mutagenesis of Baculoviruses: Transposon Shuttling and Implications for Speciation , 1986 .

[26]  D. Lindsley,et al.  Genetic variations of Drosophila melanogaster , 1967 .

[27]  G. Rubin,et al.  Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome , 1983, Cell.

[28]  S. Stacey,et al.  Sequences homologous to the P mobile element of Drosophila melanogaster are widely distributed in the subgenus Sophophora , 1985, Nature.

[29]  Finnegan Dj,et al.  Transposable Elements in Eukaryotes , 1985 .

[30]  G. Rubin,et al.  Transposition of cloned P elements into Drosophila germ line chromosomes. , 1982, Science.

[31]  W. Engels.  Extrachromosomal control of mutability in Drosophila melanogaster. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. G. Kidwell.  MOLECULAR AND PHENOTYPIC ASPECTS OF THE EVOLUTION OF HYBRID DYSGENESIS SYSTEMS , 1986 .

[33]  W. Engels.  On the evolution and population genetics of hybrid-dysgenesis-causing transposable elements in Drosophila. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  G. Rubin,et al.  Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing , 1986, Cell.

[35]  R. Cortese,et al.  pEMBL: a new family of single stranded plasmids. , 1983, Nucleic acids research.

[36]  M. G. Kidwell.  Hybrid dysgenesis in Drosophila melanogaster : the relationship between the P – M and I – R interaction systems , 1979 .

[37]  P. Leder,et al.  Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[38]  D. Botstein,et al.  Advanced Bacterial Genetics: A Manual for Genetic Engineering , 1980 .

[39]  L. Ehrman,et al.  Sequences homologous to P elements occur in Drosophila paulistorum. , 1984, Proceedings of the National Academy of Sciences of the United States of America.