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PMID: 9343390 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Abortive gap repair: underlying mechanism for Ds element formation.

Molecular and cellular biology ·Vol. 17 ·No. 11 ·1997-11-00 ·Pages 6294-302

Rubin E, Levy AA

Abstract

The mechanism by which the maize autonomous Ac transposable element gives rise to nonautonomous Ds elements is largely unknown. Sequence analysis of native maize Ds elements indicates a complex chimeric structure formed through deletions of Ac sequences with or without insertions of Ac-unrelated sequence blocks. These blocks are often flanked by short stretches of reshuffled and duplicated Ac sequences. To better understand the mechanism leading to Ds formation, we designed an assay for detecting alterations in Ac using transgenic tobacco plants carrying a single copy of Ac. We found frequent de novo alterations in Ac which were excision rather than sequence dependent, occurring within Ac but not within an almost identical Ds element and not within a stable transposase-producing gene. The de novo DNA rearrangements consisted of internal deletions with breakpoints usually occurring at short repeats and, in some cases, of duplication of Ac sequences or insertion of Ac-unrelated fragments. The ancient maize Ds elements and the young Ds elements in transgenic tobacco showed similar rearrangements, suggesting that Ac-Ds elements evolve rapidly, more so than stable genes, through deletions, duplications, and reshuffling of their own sequences and through capturing of unrelated sequences. The data presented here suggest that abortive Ac-induced gap repair, through the synthesis-dependent strand-annealing pathway, is the underlying mechanism for Ds element formation.

MeSH Terms
DNA Repair/genetics DNA Transposable Elements/genetics Models, Genetic Plants, Genetically Modified Plants, Toxic Polymerase Chain Reaction Recombination, Genetic Sequence Analysis, DNA Sequence Deletion Tobacco/genetics Zea mays/genetics
Chemicals
DNA Transposable Elements
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Rubin E
Department of Plant Genetics, The Weizmann Institute of Science, Rehovot, Israel.
Levy A A
References (51)
51 references, click to expand
  1. Molecular analysis of the Ubiquitous (Uq) transposable element system of Zea mays.
    Mol Gen Genet. 1991 Nov;230(1-2):201-8 PMID: 1660565
  2. DNA sequence of the maize transposable element Dissociation.
    Nature. 1984 Jan 12-18;307(5947):127-30 PMID: 6318121
  3. DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins.
    Cell. 1986 Dec 5;47(5):793-806 PMID: 3022939
  4. S elements: a family of Tc1-like transposons in the genome of Drosophila melanogaster.
    Genetics. 1995 Dec;141(4):1425-38 PMID: 8601484
  5. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process.
    Mol Cell Biol. 1984 Jun;4(6):1020-34 PMID: 6330525
  6. Transcription of transposable element Activator (Ac) of Zea mays L.
    EMBO J. 1987 Jun;6(6):1555-63 PMID: 16453772
  7. Isolation of the transposable maize controlling elements Ac and Ds.
    Cell. 1983 Nov;35(1):235-42 PMID: 6313225
  8. Somatic excision of the Mu1 transposable element of maize.
    Nucleic Acids Res. 1991 Feb 11;19(3):579-84 PMID: 1849263
  9. Adjacent sequences influence DNA repair accompanying transposon excision in maize.
    Genetics. 1996 Jan;142(1):237-46 PMID: 8770601
  10. Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses.
    Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1411-5 PMID: 8108422
  11. One-sided invasion events in homologous recombination at double-strand breaks.
    Mutat Res. 1994 May;314(3):199-208 PMID: 7513053
  12. Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis.
    Science. 1991 Sep 6;253(5024):1125-8 PMID: 1653453
  13. Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bs1 retroelement of maize.
    Plant Cell. 1994 Aug;6(8):1177-86 PMID: 7919987
  14. Transposon-mediated chromosomal rearrangements and gene duplications in the formation of the maize R-r complex.
    EMBO J. 1995 May 15;14(10):2350-63 PMID: 7774593
  15. Molecular evolution of the Ac/Ds transposable-element family in pearl millet and other grasses.
    Genetics. 1995 Mar;139(3):1411-9 PMID: 7768448
  16. Mechanisms of nonhomologous recombination in mammalian cells.
    Mol Cell Biol. 1985 Oct;5(10):2599-607 PMID: 3016509
  17. Implications for the cis-requirements for Ds transposition based on the sequence of the wxB4 Ds element.
    Mol Gen Genet. 1990 Feb;220(3):414-8 PMID: 2160051
  18. Transposition in plants: a molecular model.
    EMBO J. 1985 Mar;4(3):585-90 PMID: 15926218
  19. A versatile system for detecting transposition in Arabidopsis.
    Plant J. 1993 Feb;3(2):273-89 PMID: 8220445
  20. Chromosome organization and genic expression.
    Cold Spring Harb Symp Quant Biol. 1951;16:13-47 PMID: 14942727
  21. Germinal and somatic activity of the maize element Activator (Ac) in Arabidopsis.
    Genetics. 1992 Jun;131(2):449-59 PMID: 1322854
  22. Preferential transposition of the maize element Activator to linked chromosomal locations in tobacco.
    Plant Cell. 1990 Aug;2(8):701-7 PMID: 1967054
  23. Sequences near the termini are required for transposition of the maize transposon Ac in transgenic tobacco plants.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9385-8 PMID: 2556710
  24. Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations.
    Plant Cell. 1992 Mar;4(3):333-47 PMID: 1354004
  25. DNA sequence analyses support the role of interrupted gap repair in the origin of internal deletions of the maize transposon, MuDR.
    Genetics. 1996 Feb;142(2):603-18 PMID: 8852857
  26. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair.
    Mol Cell Biol. 1994 Mar;14(3):1613-25 PMID: 8114699
  27. Molecular analysis of the loss of somatic instability in the bz2::mu1 allele of maize.
    Mol Gen Genet. 1991 Sep;229(1):147-51 PMID: 1654506
  28. Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):5055-60 PMID: 8643528
  29. High-frequency P element loss in Drosophila is homolog dependent.
    Cell. 1990 Aug 10;62(3):515-25 PMID: 2165865
  30. High-frequency illegitimate integration of transfected DNA at preintegrated target sites in a mammalian genome.
    Mol Cell Biol. 1996 Jan;16(1):10-8 PMID: 8524285
  31. The nucleotide sequence of the maize controlling element Activator.
    Cell. 1984 Jun;37(2):635-43 PMID: 6327080
  32. The double-strand-break repair model for recombination.
    Cell. 1983 May;33(1):25-35 PMID: 6380756
  33. Capture of flanking DNA by a P element in Drosophila melanogaster: creation of a transposable element.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):693-7 PMID: 1846960
  34. Illegitimate recombination in plants: a model for T-DNA integration.
    Genes Dev. 1991 Feb;5(2):287-97 PMID: 1995418
  35. Nested retrotransposons in the intergenic regions of the maize genome.
    Science. 1996 Nov 1;274(5288):765-8 PMID: 8864112
  36. On the formation of spontaneous deletions: the importance of short sequence homologies in the generation of large deletions.
    Cell. 1982 Jun;29(2):319-28 PMID: 6288254
  37. Structural analysis of Tc1 elements in Caenorhabditis elegans var. Bristol (strain N2).
    Plasmid. 1989 Jul;22(1):10-21 PMID: 2550981
  38. The Ds1 controlling element family in maize and Tripsacum.
    J Mol Evol. 1987;26(4):329-34 PMID: 2836599
  39. A P element chimera containing captured genomic sequences was recovered at the vestigial locus in Drosophila following targeted transposition.
    Genetics. 1992 Aug;131(4):917-27 PMID: 1325388
  40. Filler DNA is associated with spontaneous deletions in maize.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8731-5 PMID: 2247441
  41. Genetic characterization of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line.
    Genetics. 1995 Apr;139(4):1777-96 PMID: 7789777
  42. Nuclear dna amounts in angiosperms.
    Philos Trans R Soc Lond B Biol Sci. 1976 May 27;274(933):227-74 PMID: 6977
  43. Targeted alterations of the Caenorhabditis elegans genome by transgene instructed DNA double strand break repair following Tc1 excision.
    EMBO J. 1992 Jan;11(1):287-90 PMID: 1740110
  44. P element insertions and rearrangements at the singed locus of Drosophila melanogaster.
    Genetics. 1988 May;119(1):75-83 PMID: 2840331
  45. Molecular analysis of Ac transposition and DNA replication.
    Genetics. 1992 Mar;130(3):665-76 PMID: 1312981
  46. Visual detection of transposition of the maize element activator (ac) in tobacco seedlings.
    Science. 1989 Apr 14;244(4901):204-7 PMID: 17835353
  47. A mathematical model and a computerized simulation of PCR using complex templates.
    Nucleic Acids Res. 1996 Sep 15;24(18):3538-45 PMID: 8836180
  48. A single genetic unit specifies two transposition functions in the maize element activator.
    Science. 1986 Oct 10;234(4773):210-1 PMID: 17746481
  49. The putative transposase of transposable element Ac from Zea mays L. interacts with subterminal sequences of Ac.
    EMBO J. 1989 Nov;8(11):3177-85 PMID: 2555157
  50. Molecular analysis of ds controlling element mutations at the adh1 locus of maize.
    Science. 1984 Mar 23;223(4642):1265-8 PMID: 17759347
  51. P element-mediated in vivo deletion analysis of white-apricot: deletions between direct repeats are strongly favored.
    Genetics. 1994 Mar;136(3):1001-11 PMID: 8005410
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1997-11-00
Pages
6294-302
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC232480
Subset
IM
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