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PMID: 2832734 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Insertion and excision of Caenorhabditis elegans transposable element Tc1.

Molecular and cellular biology ·Vol. 8 ·No. 2 ·1988-02-00 ·Pages 737-46

Eide D, Anderson P

Abstract

The transposable element Tc1 is responsible for most spontaneous mutations that occur in Caenorhabditis elegans variety Bergerac. We investigated the genetic and molecular properties of Tc1 transposition and excision. We show that Tc1 insertion into the unc-54 myosin heavy-chain gene was strongly site specific. The DNA sequences of independent Tc1 insertion sites were similar to each other, and we present a consensus sequence for Tc1 insertion that describes these similarities. We show that Tc1 excision was usually imprecise. Tc1 excision was imprecise in both germ line and somatic cells. Imprecise excision generated novel unc-54 alleles that had amino acid substitutions, amino acid insertions, and, in certain cases, probably altered mRNA splicing. The DNA sequences remaining after Tc1 somatic excision were the same as those remaining after germ line excision, but the frequency of somatic excision was at least 1,000-fold higher than that of germ line excision. The genetic properties of Tc1 excision, combined with the DNA sequences of the resulting unc-54 alleles, demonstrated that excision was dependent on Tc1 transposition functions in both germ line and somatic cells. Somatic excision was not regulated in the same strain-specific manner as germ-line excision was. In a genetic background where Tc1 transposition and excision in the germ line was not detectable, Tc1 excision in the soma still occurred at high frequency.

MeSH Terms
Animals Base Sequence Caenorhabditis/genetics DNA Transposable Elements Genotype Molecular Sequence Data Mutation RNA Splicing RNA, Messenger/genetics
Chemicals
DNA Transposable Elements RNA, Messenger
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Eide D
Department of Genetics, University of Wisconsin, Madison 53706.
Anderson P
References (64)
64 references, click to expand
  1. Insertion of DNA activates the cryptic bgl operon in E. coli K12.
    Nature. 1981 Oct 22;293(5834):625-9 PMID: 6270569
  2. Lambda replacement vectors carrying polylinker sequences.
    J Mol Biol. 1983 Nov 15;170(4):827-42 PMID: 6315951
  3. The gene structures of spontaneous mutations affecting a Caenorhabditis elegans myosin heavy chain gene.
    Genetics. 1985 Jan;109(1):67-79 PMID: 2981757
  4. Sequence-specific insertion of the Drosophila transposable genetic element 17.6.
    Nature. 1984 Jul 26-Aug 1;310(5975):332-3 PMID: 6087153
  5. RNA splice site selection: evidence for a 5' leads to 3' scanning model.
    Science. 1983 Jun 24;220(4604):1351-5 PMID: 6304877
  6. Splicing of messenger RNA precursors.
    Annu Rev Biochem. 1986;55:1119-50 PMID: 2943217
  7. DNA sequence at the integration sites of the insertion element IS1.
    Cell. 1978 Mar;13(3):411-8 PMID: 350411
  8. A symmetrical six-base-pair target site sequence determines Tn10 insertion specificity.
    Cell. 1982 Jan;28(1):155-63 PMID: 6279310
  9. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing.
    Cell. 1986 Jan 17;44(1):7-19 PMID: 3000622
  10. Evidence in a nematode for regulation of transposon excision by tissue-specific factors.
    Mol Gen Genet. 1986 Mar;202(3):410-5 PMID: 3012268
  11. The evolutionary implications of mobile genetic elements.
    Annu Rev Genet. 1984;18:271-93 PMID: 6099089
  12. The genetics of Caenorhabditis elegans.
    Genetics. 1974 May;77(1):71-94 PMID: 4366476
  13. A simple method to recover intact high molecular weight RNA and DNA after electrophoretic separation in low gelling temperature agarose gels.
    Anal Biochem. 1979 Oct 1;98(2):305-9 PMID: 386835
  14. The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family.
    Cell. 1982 Jul;29(3):995-1004 PMID: 6295641
  15. DNA rearrangements associated with a transposable element in yeast.
    Cell. 1980 Aug;21(1):239-49 PMID: 6250713
  16. Molecular Genetics of the Bithorax Complex in Drosophila melanogaster.
    Science. 1983 Jul 1;221(4605):23-9 PMID: 17737996
  17. High-frequency excision of transposable element Tc 1 in the nematode Caenorhabditis elegans is limited to somatic cells.
    Cell. 1984 Mar;36(3):599-605 PMID: 6321037
  18. IS1 insertion generates duplication of a nine base pair sequence at its target site.
    Cell. 1978 Mar;13(3):419-26 PMID: 350412
  19. Unique insertion site of Tn7 in the E. coli chromosome.
    Nature. 1982 Jun 17;297(5867):601-3 PMID: 6283361
  20. Target sequences for the C. elegans transposable element Tc1.
    Nucleic Acids Res. 1983 Oct 25;11(20):7137-40 PMID: 6314277
  21. Activation of a transposable element in the germ line but not the soma of Caenorhabditis elegans.
    Nature. 1987 Aug 20-26;328(6132):726-8 PMID: 3039378
  22. Transposase promotes double strand breaks and single strand joints at Tn10 termini in vivo.
    Cell. 1984 Nov;39(1):181-90 PMID: 6091910
  23. New M13 vectors for cloning.
    Methods Enzymol. 1983;101:20-78 PMID: 6310323
  24. Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus.
    Cell. 1986 Oct 24;47(2):285-96 PMID: 3021338
  25. A trans-acting product needed for P factor transposition in Drosophila.
    Science. 1984 Dec 7;226(4679):1194-6 PMID: 6095450
  26. Integration site preferences of the Alu family and similar repetitive DNA sequences.
    Nucleic Acids Res. 1985 Dec 20;13(24):8939-54 PMID: 3001654
  27. Mutations in the unc-54 myosin heavy chain gene of Caenorhabditis elegans that alter contractility but not muscle structure.
    Cell. 1982 Jul;29(3):773-81 PMID: 7151169
  28. Sequence of the C. elegans transposable element Tc1.
    Nucleic Acids Res. 1983 Jun 25;11(12):4201-9 PMID: 6306578
  29. C. elegans unc-105 mutations affect muscle and are suppressed by other mutations that affect muscle.
    Genetics. 1986 Aug;113(4):853-67 PMID: 3744029
  30. Excision of the DBA ecotropic provirus in dilute coat-color revertants of mice occurs by homologous recombination involving the viral LTRs.
    Cell. 1983 Jun;33(2):379-87 PMID: 6305507
  31. The P family of transposable elements in Drosophila.
    Annu Rev Genet. 1983;17:315-44 PMID: 6320712
  32. Evidence for a transposon in Caenorhabditis elegans.
    Cell. 1983 Jan;32(1):55-65 PMID: 6297788
  33. Long terminal repeat nucleotide sequence and specific insertion of the gypsy transposon.
    Proc Natl Acad Sci U S A. 1984 Jul;81(14):4462-4 PMID: 6087324
  34. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans.
    Dev Biol. 1977 Mar;56(1):110-56 PMID: 838129
  35. Tc1(Hin): a form of the transposable element Tc1 in Caenorhabditis elegans.
    Can J Biochem Cell Biol. 1985 Jul;63(7):752-6 PMID: 2994862
  36. The 17-kb Tam1 element of Antirrhinum majus induces a 3-bp duplication upon integration into the chalcone synthase gene.
    EMBO J. 1984 May;3(5):1015-9 PMID: 16453519
  37. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  38. Specificity of insertion of IS1.
    J Mol Biol. 1985 Oct 5;185(3):517-24 PMID: 2997452
  39. Spontaneous unstable unc-22 IV mutations in C. elegans var. Bergerac.
    Genetics. 1984 Dec;108(4):859-77 PMID: 6096205
  40. The DNA of Caenorhabditis elegans.
    Genetics. 1974 May;77(1):95-104 PMID: 4858229
  41. Isolation of the closed circular form of the transposable element Tc1 in Caenorhabditis elegans.
    Nature. 1984 Oct 4-10;311(5985):485-6 PMID: 6090946
  42. Controlling element-induced alterations in UDPglucose:flavonoid glucosyltransferase, the enzyme specified by the bronze locus in maize.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5623-7 PMID: 16592474
  43. Protein structural domains in the Caenorhabditis elegans unc-54 myosin heavy chain gene are not separated by introns.
    Proc Natl Acad Sci U S A. 1983 Jul;80(14):4253-7 PMID: 6576334
  44. A mutant affecting the heavy chain of myosin in Caenorhabditis elegans.
    J Mol Biol. 1974 Dec 5;90(2):291-300 PMID: 4453018
  45. Molecular cloning of the muscle gene unc-22 in Caenorhabditis elegans by Tc1 transposon tagging.
    Proc Natl Acad Sci U S A. 1986 Apr;83(8):2579-83 PMID: 3010313
  46. Genetic evidence that Tn10 transposes by a nonreplicative mechanism.
    Cell. 1986 Jun 20;45(6):801-15 PMID: 3011280
  47. Extrachromosomal copies of transposon Tc1 in the nematode Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 1984 Jul;81(13):4018-22 PMID: 6330730
  48. Nearly precise excision: a new type of DNA alteration associated with the translocatable element Tn10.
    Cell. 1979 Apr;16(4):733-8 PMID: 455447
  49. Transposition of Tc1 in the nematode Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 1985 Mar;82(6):1756-60 PMID: 2984668
  50. Immunocytochemical localization of two myosins within the same muslce cells in Caenorhabditis elegans.
    Cell. 1978 Oct;15(2):413-9 PMID: 363276
  51. A transposable element inserted just 5' to a Drosophila glue protein gene alters gene expression and chromatin structure.
    Cell. 1983 Aug;34(1):75-84 PMID: 6309414
  52. Analysis of a transposable element in Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 1983 Jun;80(12):3585-9 PMID: 6304721
  53. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome.
    Cell. 1983 Aug;34(1):25-35 PMID: 6309410
  54. Specificity of transposon Tn5 insertion.
    Genetics. 1983 Dec;105(4):813-28 PMID: 6315531
  55. Sites of P element insertion and structures of P element deletions in the 5' region of Drosophila melanogaster RpII215.
    Mol Cell Biol. 1986 Oct;6(10):3312-9 PMID: 3025586
  56. Hybrid dysgenesis-induced revertants of insertions at the 5' end of the rudimentary gene in Drosophila melanogaster: transposon-induced control mutations.
    Genetics. 1986 Sep;114(1):165-82 PMID: 3021567
  57. Molecular identification and isolation of the Waxy locus in maize.
    Cell. 1983 Nov;35(1):225-33 PMID: 6313224
  58. Circles with two tandem LTRs are precursors to integrated retrovirus DNA.
    Cell. 1984 Mar;36(3):673-9 PMID: 6697392
  59. Excision of copia element in a revertant of the white-apricot mutation of Drosophila melanogaster leaves behind one long-terminal repeat.
    Mol Gen Genet. 1985;199(1):1-6 PMID: 2987642
  60. New bacteriophage lambda vectors with positive selection for cloned inserts.
    Methods Enzymol. 1983;101:3-19 PMID: 6310332
  61. Insertion of a movable genetic element, 297, into the T-A-T-A box for the H3 histone gene in Drosophila melanogaster.
    Proc Natl Acad Sci U S A. 1982 Jul;79(13):4143-7 PMID: 6287469
  62. Mating signals control expression of mutations resulting from insertion of a transposable repetitive element adjacent to diverse yeast genes.
    Cell. 1980 Nov;22(2 Pt 2):427-36 PMID: 6256080
  63. A role for exon sequences and splice-site proximity in splice-site selection.
    Cell. 1986 Aug 29;46(5):681-90 PMID: 2427200
  64. Molecular analysis of ds controlling element mutations at the adh1 locus of maize.
    Science. 1984 Mar 23;223(4642):1265-8 PMID: 17759347
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/mcb.8.2.737-746.1988
Published
1988-02-00
Pages
737-46
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC363199
Subset
IM
Grants
NIGMS NIH HHS · GM30132 · United States
External Links
PubMed source DOI: 10.1128/mcb.8.2.737-746.1988 PMC Full Text View journal details
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