Abstract
A novel transposon named ITmD37E was discovered in a wide range of mosquito species. Sequence analysis of multiple copies in three Aedes species showed similar terminal inverted repeats and common putative TA target site duplications. The ITmD37E transposases contain a conserved DD37E catalytic motif, which is unique among reported transposons of the IS630-Tc1-mariner superfamily. Sequence comparisons and phylogenetic analyses suggest that ITmD37E forms a novel family distinct from the widely distributed Tc1 (DD34E), mariner (DD34D), and pogo (DDxD) families in the IS630-Tc1-mariner superfamily. The inclusion in the phylogenetic analysis of recently reported transposons and transposons uncovered in our database survey provided revisions to previous classifications and identified two additional families, ITmD37D and ITmD39D, which contain DD37D and DD39D motifs, respectively. The above expansion and reorganization may open the doors to the discovery of related transposons in a broad range of organisms and help illustrate the evolution and structure-function relationships among these distinct transposases in the IS630-Tc1-mariner superfamily. The presence of intact open reading frames and highly similar copies in some of the newly characterized transposons suggests recent transposition. Studies of these novel families may add to the limited repertoire of transgenesis and mutagenesis tools for a wide range of organisms, including the medically important mosquitoes.
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- Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ashburner M., Hoy M. A., Peloquin J. J. Prospects for the genetic transformation of arthropods. Insect Mol Biol. 1998 Aug;7(3):201–213. doi: 10.1046/j.1365-2583.1998.00084.x. [DOI] [PubMed] [Google Scholar]
- Atkinson P. W., Pinkerton A. C., O'Brochta D. A. Genetic transformation systems in insects. Annu Rev Entomol. 2001;46:317–346. doi: 10.1146/annurev.ento.46.1.317. [DOI] [PubMed] [Google Scholar]
- Besansky N. J., Powell J. R. Reassociation kinetics of Anopheles gambiae (Diptera: Culicidae) DNA. J Med Entomol. 1992 Jan;29(1):125–128. doi: 10.1093/jmedent/29.1.125. [DOI] [PubMed] [Google Scholar]
- Capy P., Langin T., Higuet D., Maurer P., Bazin C. Do the integrases of LTR-retrotransposons and class II element transposases have a common ancestor? Genetica. 1997;100(1-3):63–72. [PubMed] [Google Scholar]
- Capy P., Vitalis R., Langin T., Higuet D., Bazin C. Relationships between transposable elements based upon the integrase-transposase domains: is there a common ancestor? J Mol Evol. 1996 Mar;42(3):359–368. doi: 10.1007/BF02337546. [DOI] [PubMed] [Google Scholar]
- Clark J. B., Kidwell M. G. A phylogenetic perspective on P transposable element evolution in Drosophila. Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11428–11433. doi: 10.1073/pnas.94.21.11428. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins J., Forbes E., Anderson P. The Tc3 family of transposable genetic elements in Caenorhabditis elegans. Genetics. 1989 Jan;121(1):47–55. doi: 10.1093/genetics/121.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doak T. G., Doerder F. P., Jahn C. L., Herrick G. A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common "D35E" motif. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):942–946. doi: 10.1073/pnas.91.3.942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doolittle W. F., Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature. 1980 Apr 17;284(5757):601–603. doi: 10.1038/284601a0. [DOI] [PubMed] [Google Scholar]
- Gueiros-Filho F. J., Beverley S. M. Trans-kingdom transposition of the Drosophila element mariner within the protozoan Leishmania. Science. 1997 Jun 13;276(5319):1716–1719. doi: 10.1126/science.276.5319.1716. [DOI] [PubMed] [Google Scholar]
- Henikoff S. Detection of Caenorhabditis transposon homologs in diverse organisms. New Biol. 1992 Apr;4(4):382–388. [PubMed] [Google Scholar]
- Izsvák Z., Ivics Z., Plasterk R. H. Sleeping Beauty, a wide host-range transposon vector for genetic transformation in vertebrates. J Mol Biol. 2000 Sep 8;302(1):93–102. doi: 10.1006/jmbi.2000.4047. [DOI] [PubMed] [Google Scholar]
- Jarvik T., Lark K. G. Characterization of Soymar1, a mariner element in soybean. Genetics. 1998 Jul;149(3):1569–1574. doi: 10.1093/genetics/149.3.1569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kidwell MG, Lisch DR. Transposable elements and host genome evolution. Trends Ecol Evol. 2000 Mar;15(3):95–99. doi: 10.1016/s0169-5347(99)01817-0. [DOI] [PubMed] [Google Scholar]
- Lampe D. J., Akerley B. J., Rubin E. J., Mekalanos J. J., Robertson H. M. Hyperactive transposase mutants of the Himar1 mariner transposon. Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11428–11433. doi: 10.1073/pnas.96.20.11428. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lampe D. J., Walden K. K., Robertson H. M. Loss of transposase-DNA interaction may underlie the divergence of mariner family transposable elements and the ability of more than one mariner to occupy the same genome. Mol Biol Evol. 2001 Jun;18(6):954–961. doi: 10.1093/oxfordjournals.molbev.a003896. [DOI] [PubMed] [Google Scholar]
- Lohe A. R., De Aguiar D., Hartl D. L. Mutations in the mariner transposase: the D,D(35)E consensus sequence is nonfunctional. Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1293–1297. doi: 10.1073/pnas.94.4.1293. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maurer P., Réjasse A., Capy P., Langin T., Riba G. Isolation of the transposable element hupfer from the entomopathogenic fungus Beauveria bassiana by insertion mutagenesis of the nitrate reductase structural gene. Mol Gen Genet. 1997 Sep;256(2):195–202. doi: 10.1007/s004380050561. [DOI] [PubMed] [Google Scholar]
- Moore S. P., Powers M., Garfinkel D. J. Substrate specificity of Ty1 integrase. J Virol. 1995 Aug;69(8):4683–4692. doi: 10.1128/jvi.69.8.4683-4692.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Myers E. W., Sutton G. G., Delcher A. L., Dew I. M., Fasulo D. P., Flanigan M. J., Kravitz S. A., Mobarry C. M., Reinert K. H., Remington K. A. A whole-genome assembly of Drosophila. Science. 2000 Mar 24;287(5461):2196–2204. doi: 10.1126/science.287.5461.2196. [DOI] [PubMed] [Google Scholar]
- Plasterk R. H., Izsvák Z., Ivics Z. Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet. 1999 Aug;15(8):326–332. doi: 10.1016/s0168-9525(99)01777-1. [DOI] [PubMed] [Google Scholar]
- Rai K. S., Black W. C., 4th Mosquito genomes: structure, organization, and evolution. Adv Genet. 1999;41:1–33. doi: 10.1016/s0065-2660(08)60149-2. [DOI] [PubMed] [Google Scholar]
- Raz E., van Luenen H. G., Schaerringer B., Plasterk R. H., Driever W. Transposition of the nematode Caenorhabditis elegans Tc3 element in the zebrafish Danio rerio. Curr Biol. 1998 Jan 15;8(2):82–88. doi: 10.1016/s0960-9822(98)70038-7. [DOI] [PubMed] [Google Scholar]
- Robertson H. M., Asplund M. L. Bmmar1: a basal lineage of the mariner family of transposable elements in the silkworm moth, Bombyx mori. Insect Biochem Mol Biol. 1996 Sep-Oct;26(8-9):945–954. doi: 10.1016/s0965-1748(96)00061-6. [DOI] [PubMed] [Google Scholar]
- Robertson H. M., MacLeod E. G. Five major subfamilies of mariner transposable elements in insects, including the Mediterranean fruit fly, and related arthropods. Insect Mol Biol. 1993;2(3):125–139. doi: 10.1111/j.1365-2583.1993.tb00132.x. [DOI] [PubMed] [Google Scholar]
- Smit A. F., Riggs A. D. Tiggers and DNA transposon fossils in the human genome. Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1443–1448. doi: 10.1073/pnas.93.4.1443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tarchini R., Biddle P., Wineland R., Tingey S., Rafalski A. The complete sequence of 340 kb of DNA around the rice Adh1-adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell. 2000 Mar;12(3):381–391. doi: 10.1105/tpc.12.3.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tu Z., Hagedorn H. H. Biochemical, molecular, and phylogenetic analysis of pyruvate carboxylase in the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol. 1997 Feb;27(2):133–147. doi: 10.1016/s0965-1748(96)00078-1. [DOI] [PubMed] [Google Scholar]