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. 1999 Aug;152(4):1733–1740. doi: 10.1093/genetics/152.4.1733

Origination of Ds elements from Ac elements in maize: evidence for rare repair synthesis at the site of Ac excision.

X Yan 1, I M Martínez-Férez 1, S Kavchok 1, H K Dooner 1
PMCID: PMC1460708  PMID: 10430597

Abstract

Although it has been known for some time that the maize transposon Ac can mutate to Ds by undergoing internal deletions, the mechanism by which these mutations arise has remained conjectural. To gain further insight into this mechanism in maize we have studied a series of Ds elements that originated de novo from Ac elements at known locations in the genome. We present evidence that new, internally deleted Ds elements can arise at the Ac donor site when Ac transposes to another site in the genome. However, internal deletions are rare relative to Ac excision footprints, the predominant products of Ac transposition. We have characterized the deletion junctions in five new Ds elements. Short direct repeats of variable length occur adjacent to the deletion junction in three of the five Ds derivatives. In the remaining two, extra sequences or filler DNA is inserted at the junction. The filler DNAs are identical to sequences found close to the junction in the Ac DNA, where they are flanked by the same sequences that flank the filler DNA in the deletion. These findings are explained most simply by a mechanism involving error-prone DNA replication as an occasional alternative to end-joining in the repair of Ac-generated double-strand breaks.

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Selected References

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  1. Chen J., Greenblatt I. M., Dellaporta S. L. Molecular analysis of Ac transposition and DNA replication. Genetics. 1992 Mar;130(3):665–676. doi: 10.1093/genetics/130.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Dooner H. K., Belachew A. Transposition Pattern of the Maize Element Ac from the Bz-M2(ac) Allele. Genetics. 1989 Jun;122(2):447–457. doi: 10.1093/genetics/122.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dooner H. K. Genetic Fine Structure of the BRONZE Locus in Maize. Genetics. 1986 Aug;113(4):1021–1036. doi: 10.1093/genetics/113.4.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dooner H. K., Martínez-Férez I. M. Germinal excisions of the maize transposon activator do not stimulate meiotic recombination or homology-dependent repair at the bz locus. Genetics. 1997 Dec;147(4):1923–1932. doi: 10.1093/genetics/147.4.1923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dooner H., English J., Ralston E., Weck E. A single genetic unit specifies two transposition functions in the maize element activator. Science. 1986 Oct 10;234(4773):210–211. doi: 10.1126/science.234.4773.210. [DOI] [PubMed] [Google Scholar]
  6. Doseff A., Martienssen R., Sundaresan V. Somatic excision of the Mu1 transposable element of maize. Nucleic Acids Res. 1991 Feb 11;19(3):579–584. doi: 10.1093/nar/19.3.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Engels W. R., Johnson-Schlitz D. M., Eggleston W. B., Sved J. High-frequency P element loss in Drosophila is homolog dependent. Cell. 1990 Aug 10;62(3):515–525. doi: 10.1016/0092-8674(90)90016-8. [DOI] [PubMed] [Google Scholar]
  8. Fedoroff N., Wessler S., Shure M. Isolation of the transposable maize controlling elements Ac and Ds. Cell. 1983 Nov;35(1):235–242. doi: 10.1016/0092-8674(83)90226-x. [DOI] [PubMed] [Google Scholar]
  9. Gloor G. B., Nassif N. A., Johnson-Schlitz D. M., Preston C. R., Engels W. R. Targeted gene replacement in Drosophila via P element-induced gap repair. Science. 1991 Sep 6;253(5024):1110–1117. doi: 10.1126/science.1653452. [DOI] [PubMed] [Google Scholar]
  10. Greenblatt I. M. A chromosome replication pattern deduced from pericarp phenotypes resulting from movements of the transposable element, modulator, in maize. Genetics. 1984 Oct;108(2):471–485. doi: 10.1093/genetics/108.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Greenblatt I. M. Movement of modulator in maize: a test of an hypothesis. Genetics. 1974 Aug;77(4):671–678. doi: 10.1093/genetics/77.4.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Greene B., Walko R., Hake S. Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics. 1994 Dec;138(4):1275–1285. doi: 10.1093/genetics/138.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hsia A. P., Schnable P. S. 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):603–618. doi: 10.1093/genetics/142.2.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Klein A. S., Clancy M., Paje-Manalo L., Furtek D. B., Hannah L. C., Nelson O. E., Jr The mutation bronze-mutable 4 derivative 6856 in maize is caused by the insertion of a novel 6.7-kilobase pair transposon in the untranslated leader region of the bronze-1 gene. Genetics. 1988 Nov;120(3):779–790. doi: 10.1093/genetics/120.3.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kunze R., Stochaj U., Laufs J., Starlinger P. Transcription of transposable element Activator (Ac) of Zea mays L. EMBO J. 1987 Jun;6(6):1555–1563. doi: 10.1002/j.1460-2075.1987.tb02400.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lankenau D. H., Corces V. G., Engels W. R. Comparison of targeted-gene replacement frequencies in Drosophila melanogaster at the forked and white loci. Mol Cell Biol. 1996 Jul;16(7):3535–3544. doi: 10.1128/mcb.16.7.3535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lisch D., Chomet P., Freeling M. Genetic characterization of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line. Genetics. 1995 Apr;139(4):1777–1796. doi: 10.1093/genetics/139.4.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. MCCLINTOCK B. Controlling elements and the gene. Cold Spring Harb Symp Quant Biol. 1956;21:197–216. doi: 10.1101/sqb.1956.021.01.017. [DOI] [PubMed] [Google Scholar]
  19. Moreno M. A., Chen J., Greenblatt I., Dellaporta S. L. Reconstitutional mutagenesis of the maize P gene by short-range Ac transpositions. Genetics. 1992 Aug;131(4):939–956. doi: 10.1093/genetics/131.4.939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nassif N., Penney J., Pal S., Engels W. R., Gloor G. B. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol Cell Biol. 1994 Mar;14(3):1613–1625. doi: 10.1128/mcb.14.3.1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Hare K., Rubin G. M. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell. 1983 Aug;34(1):25–35. doi: 10.1016/0092-8674(83)90133-2. [DOI] [PubMed] [Google Scholar]
  22. Pohlman R. F., Fedoroff N. V., Messing J. The nucleotide sequence of the maize controlling element Activator. Cell. 1984 Jun;37(2):635–643. doi: 10.1016/0092-8674(84)90395-7. [DOI] [PubMed] [Google Scholar]
  23. Ralston E. J., English J. J., Dooner H. K. Sequence of three bronze alleles of maize and correlation with the genetic fine structure. Genetics. 1988 May;119(1):185–197. doi: 10.1093/genetics/119.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ralston E. J., English J. J., Dooner H. K. Sequence of three bronze alleles of maize and correlation with the genetic fine structure. Genetics. 1988 May;119(1):185–197. doi: 10.1093/genetics/119.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ralston E., English J., Dooner H. K. Chromosome-breaking structure in maize involving a fractured Ac element. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9451–9455. doi: 10.1073/pnas.86.23.9451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sainsard-Chanet A., Begel O. Insertion of an LrDNA gene fragment and of filler DNA at a mitochondrial exon-intron junction in Podospora. Nucleic Acids Res. 1990 Feb 25;18(4):779–783. doi: 10.1093/nar/18.4.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Scott L., LaFoe D., Weil C. F. Adjacent sequences influence DNA repair accompanying transposon excision in maize. Genetics. 1996 Jan;142(1):237–246. doi: 10.1093/genetics/142.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sugawara N., Haber J. E. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol Cell Biol. 1992 Feb;12(2):563–575. doi: 10.1128/mcb.12.2.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sutton W. D., Gerlach W. L., Peacock W. J., Schwartz D. Molecular analysis of ds controlling element mutations at the adh1 locus of maize. Science. 1984 Mar 23;223(4642):1265–1268. doi: 10.1126/science.223.4642.1265. [DOI] [PubMed] [Google Scholar]
  30. Takasu-Ishikawa E., Yoshihara M., Hotta Y. Extra sequences found at P element excision sites in Drosophila melanogaster. Mol Gen Genet. 1992 Mar;232(1):17–23. doi: 10.1007/BF00299132. [DOI] [PubMed] [Google Scholar]
  31. Van Schaik N W, Brink R A. Transpositions of Modulator, a Component of the Variegated Pericarp Allele in Maize. Genetics. 1959 Jul;44(4):725–738. doi: 10.1093/genetics/44.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Varagona M., Wessler S. R. Implications for the cis-requirements for Ds transposition based on the sequence of the wxB4 Ds element. Mol Gen Genet. 1990 Feb;220(3):414–418. doi: 10.1007/BF00391747. [DOI] [PubMed] [Google Scholar]
  33. Wessler S., Tarpley A., Purugganan M., Spell M., Okagaki R. Filler DNA is associated with spontaneous deletions in maize. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8731–8735. doi: 10.1073/pnas.87.22.8731. [DOI] [PMC free article] [PubMed] [Google Scholar]

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