Abstract
Two mariner-like elements, Ramar1 and Ramar2, are described in the genome of Rhynchosciara americana, whose nucleotide consensus sequences were derived from multiple defective copies containing deletions, frame shifts and stop codons. Ramar1 contains several conserved amino acid blocks which were identified, including a specific D,D(34)D signature motif. Ramar2 is a defective mariner-like element, which contains a deletion overlapping in most of the internal region of the transposase ORF while its extremities remain intact. Predicted transposase sequences demonstrated that Ramar1 and Ramar2 phylogenetically present high identity to mariner-like elements of mauritiana subfamily. Southern blot analysis indicated that Ramar1 is widely represented in the genome of Rhynchosciara americana. In situ hybridizations showed Ramar1 localized in several chromosome regions, mainly in pericentromeric heterochromatin and their boundaries, while Ramar2 appeared as a single band in chromosome A.
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References
Augé-Gouillou C, Bigot Y, Pollet N, Hamelin MH, Meunier-Rotival M, Periquet G (1995) Human and other mammalian genomes contain transposons of the mariner family. FEBS Lett 368:541–546
Augé-Gouillou C, Bigot Y, Periquet G (1999) Mariner-like sequences are present in the genome of the fruitfly, Drosophila melanogaster. J Evol Biol 12:742–745
Augé-Gouillou C, Hamelin MH, Demattci MV, Periquet G, Bigot Y (2001) The ITR binding domain of the mariner Mos-1 transposase. Mol Genet Genomics 265:58–65
Breuer ME, Pavan C (1955) Behavior of polytene chromosomes of Rhynchosciara angelae at different stages of larval development. Chromosoma 7:371–386
Craig NL (1995) Unity in transposition reactions. Science 270:253–254
Doak TG, Doerder FP, Jahn CL, Herrick G (1994) A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common “D,35E” motif. Proc Natl Acad Sci USA 91:942–946
Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred, 2. Error probabilities. Genome Res 8:186–194
Ewing B, Hillier LD, Wendl MC, Green P (1998) Basecalling of automated sequencer traces using phred, 1. Accuracy assessment. Genome Res 8:175–185
Ficq A, Pavan C (1957) Autoradiography of polytene chromosomes of Rhynchosciara angelae at different stages of larval development. Nature 180:983–984
Finnegan DJ (1989) Eukaryotic transposable elements and genome evolution. Trends Genet 5:103–107
Gomulski LM, Torti C, Malacrida AR, Gasperi G (1997) Ccmar1, a full-length mariner element from the Mediterranean fruit fly, Ceratitis capitata. Insect Mol Biol 6:241–253
Gordon D, Abajian C, Green P (1998) Consedi a graphical tool for sequence finishing. Genome Res 8:195–202
Green CL, Frommer M (2001) The genome of the Queensland fruit fly Bactrocera tryoni contains multiple representatives of the mariner family of transposable elements. Insect Mol Biol 10:371–386
Hartl DL, Lohe AR, Lozovskaya ER (1997a) Modern thoughts on an ancient marinere: function, evolution, regulation. Ann Rev Genet 31:337–358
Hartl DL, Lohe AR, Lozovskaya ER (1997b) Regulation of the transposable element mariner. Genetica 100:177–184
Hartl DL, Lozovskaya ER, Nurminsky DI, Lohe AR (1997c) What restricts the activity of mariner like transposable element. Trends Genet 31:197–201
Jacobson JW, Medhora MM, Hartl DL (1986) Molecular structure of a somatically unstable transposase element in Drosophila. Proc Natl Acad Sci USA 83:8684–8688
Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler DA, Lewis SE, Rubin GM, Ashburner M, Celniker SE (2002) The transposable elements of Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3:84.1–84.20
Kumaresan G, Mathavan S (2004) Molecular diversity and phylogenetic analysis of mariner-like transposons in the genome of the silkworm Bombyx mori. Insect Mol Biol 13:259–271
Lampe DJ, Witherspoon DJ, Soto-Adames FN, Robertson HM (2003) Recent horizontal transfer of mellifera subfamily mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. Mol Biol Evol 20:554–562
Langin T, Capy P, Daboussi MJ (1995) The transposable element impala, a fungal member of the Tc1-mariner superfamily. Mol Gen Genet 246:19–28
Lara FJS, Tamaki H, Pavan C (1965) Laboratory culture of Rhynchosciara angelae. Am Nature 99:189–191
Leroy H, Castagnone-Sereno P, Renault S, Augé-Gouillou C, Bigot Y, Abad P (2003) Characterization of Mcmar1, a mariner-like element with large inverter terminal repeats (ITRs) from the phytoparasitic nematode Meloidogyne chitwoodi. Gene 304:35–41
Lohe AR, Moriyame EN, Lidholm DA, Hartl DL (1995) Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Mol Biol Evol 12:62–72
Mandrioli M (2003) Identification and chromosomal localization of mariner-like elements in the cabbage moth Mamestra brassicae (Lepidoptera). Chromosome Res 11:319–322
Nonato E, Pavan C (1951) A new species of Rhynchosciara Rubsaamen, 1894 (Diptera, Mycetophilidae). Rev Brasil Biol 11:435–437
Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Pietrokovski S, Henikoff S (1997) A helix-turn-helix DNA-binding motif predicted for transposases of DNA transposons. Mol Gen Genet 254:689–695
Prasad MD, Nagaraju J (2003) A comparative phylogenetic analysis of full-length mariner elements isolated from Indian tasar silkmoth, Antheraea mylitta (Lepidoptera: saturniidae). J Biosci 28:443–453
Ren X, Park Y, Miller TA (2006) Intact mariner-like element in tobacco budworm, Heliothis virescens (Lepidoptera: Noctuidae). Insect Mol Biol 15:743–748
Robertson HM (1993) The mariner transposable element is widespread in insects. Nature 362:241–245
Robertson HM, MacLeod EG (1993) Five major subfamilies of mariner transposable elements in insects, including the Mediterranean fruit fly, and related arthropods. Insect Mol Biol 2:125–139
Robertson HM, Lampe DJ (1995) Distribution of transposable elements in arthropods. Annu Rev Entomol 40:333–357
Robertson HM, Asplund ML (1996) Bmmar1: a basal lineage of the mariner family of transposable elements in the silkworm moth, Bombyx mori. Insect Biochem Mol Biol 26:945–954
Robertson HM, Walden KKO (2003) Bmmar6, a second mori subfamily mariner transposon from the silkworm moth Bombyx mori. Insect Mol Biol 12:167–171
Rudkin GT, Corlette SL (1957) Disproportionate synthesis of DNA in polytene chromosome region. Proc Natl Acad Sci 43:964–968
Russell VW, Shukle RH (1997) Molecular and cytological analysis of a mariner transposon from Hessian fly. J Hered 88:72–76
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Evol Biol 4(4):406–425
Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Santelli RV, Siviero F, Machado-Santelli GM, Lara FJS, Stocker AJ (2004) Molecular characterization of the B-2 DNA puff gene of Rhynchosciara americana. Chromosoma 113:167–176
Shao H, Tu Z (2001) Expanding the diversity of the IS630-Tc1-mariner superfamily: discovery of a unique DD37E tranposon and reclassification of the DD37D and DD39D transposons. Genetics 159:1103–1115
Siviero F, Rezende-Teixeira P, Andrade A, Machado-Santelli GM, Santelli RV (2006) Analysis of expressed sequence tags from Rhynchosciara americana salivary glands. Insect Mol Biol 15:109–118
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Torti C, Gomulski LM, Malacrida AR, Capy P, Gasperi G (1998) Characterization and evolution of mariner elements from closely related species of fruit flies (Diptera: Tephritidae). J Mol Evol 46:288–298
van Luenen HG, Colloms SD, Plasterk RH (1994) The mechanism of transposition of Tc3 in C. elegans. Cell 79:293–301
Zakharkin SO, Willis RL, Litvinova OV, Jinwal UK, Headley VV, Benes H (2004) Identification of two mariner-like elements in the genome of the mosquito Ochlerotatus atropalpus. Insect Biochem Mol Biol 34:377–386
Wang J, Staten RT, Miller A, Park Y (2005) Inactivated mariner-like elements (MLE) in pink bollworm, Pectinophora gossypiella. Insect Mol Biol 14:547–553
Wheeler DL, Chappey C, Lash AE, Leipe DD, Madden TL, Schuler GD, Tatusova TA, Rapp BA (2000) Database resources of the National Center for Biotechnology Information. Nucl Acids Res 28(1):10–14
Yoshiyama M, Honda H, Shono T, Kimura K (2000) Survey of mariner-like elements in the housefly, Musca domestica. Genetica 108:81–86
Acknowledgments
We thank the Dr. Paolo M.A. Zanotto and Juliana Velasco for the sequencing support and Roberto Cabado for preparing confocal images. We thank the FAPESP and CNPq by financial support and fellowship.
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Rezende-Teixeira, P., Siviero, F., Andrade, A. et al. Mariner-like elements in Rhynchosciara americana (Sciaridae) genome: molecular and cytological aspects. Genetica 133, 137–145 (2008). https://doi.org/10.1007/s10709-007-9193-y
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DOI: https://doi.org/10.1007/s10709-007-9193-y