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. 2000 Dec;156(4):2007–2017. doi: 10.1093/genetics/156.4.2007

Ac insertion site affects the frequency of transposon-induced homologous recombination at the maize p1 locus.

Y L Xiao 1, X Li 1, T Peterson 1
PMCID: PMC1461373  PMID: 11102391

Abstract

The maize p1 gene regulates the production of a red pigment in the kernel pericarp, cob, and other maize floral tissues. Insertions of the transposable element Ac can induce recombination between two highly homologous 5.2-kb direct repeat sequences that flank the p1 gene-coding region. Here, we tested the effects of the Ac insertion site and orientation on the induction of recombination at the p1 locus. A collection of unique p1 gene alleles was used, which carry Ac insertions at different sites in and near the p1 locus, outside of the direct repeats, within the direct repeat sequences, and between the direct repeats, in both orientations. Recombination was scored by the numbers of colorless pericarp sectors (somatic frequency) and heritable mutations (germinal frequency). In both the somatic and germinal tests, the frequency of homologous recombination is significantly higher when Ac is inserted between the direct repeats than when Ac is inserted either within or outside the repeats. In contrast, Ac orientation had no significant effect on recombination frequency. We discuss these results in terms of the possible mechanisms of transposon-induced recombination.

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Selected References

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  1. Anderson E G, Eyster W H. Pericarp Studies in Maize. III. the Frequency of Mutation in Variegated Maize Pericarp. Genetics. 1928 Mar;13(2):111–120. doi: 10.1093/genetics/13.2.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Athma P., Grotewold E., Peterson T. Insertional mutagenesis of the maize P gene by intragenic transposition of Ac. Genetics. 1992 May;131(1):199–209. doi: 10.1093/genetics/131.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Athma P., Peterson T. Ac induces homologous recombination at the maize P locus. Genetics. 1991 May;128(1):163–173. doi: 10.1093/genetics/128.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Becker H. A., Kunze R. Binding sites for maize nuclear proteins in the subterminal regions of the transposable element Activator. Mol Gen Genet. 1996 Jun 24;251(4):428–435. doi: 10.1007/BF02172371. [DOI] [PubMed] [Google Scholar]
  5. Belmaaza A., Chartrand P. One-sided invasion events in homologous recombination at double-strand breaks. Mutat Res. 1994 May;314(3):199–208. doi: 10.1016/0921-8777(94)90065-5. [DOI] [PubMed] [Google Scholar]
  6. Biswas I., Yamamoto A., Hsieh P. Branch migration through DNA sequence heterology. J Mol Biol. 1998 Jun 19;279(4):795–806. doi: 10.1006/jmbi.1998.1769. [DOI] [PubMed] [Google Scholar]
  7. Brutnell T. P., Dellaporta S. L. Somatic inactivation and reactivation of Ac associated with changes in cytosine methylation and transposase expression. Genetics. 1994 Sep;138(1):213–225. doi: 10.1093/genetics/138.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Chiurazzi M., Ray A., Viret J. F., Perera R., Wang X. H., Lloyd A. M., Signer E. R. Enhancement of somatic intrachromosomal homologous recombination in Arabidopsis by the HO endonuclease. Plant Cell. 1996 Nov;8(11):2057–2066. doi: 10.1105/tpc.8.11.2057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chomet P. S., Wessler S., Dellaporta S. L. Inactivation of the maize transposable element Activator (Ac) is associated with its DNA modification. EMBO J. 1987 Feb;6(2):295–302. doi: 10.1002/j.1460-2075.1987.tb04753.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chopra S., Athma P., Li X. G., Peterson T. A maize Myb homolog is encoded by a multicopy gene complex. Mol Gen Genet. 1998 Nov;260(4):372–380. doi: 10.1007/s004380050906. [DOI] [PubMed] [Google Scholar]
  12. Cocciolone S. M., Cone K. C. Pl-Bh, an anthocyanin regulatory gene of maize that leads to variegated pigmentation. Genetics. 1993 Oct;135(2):575–588. doi: 10.1093/genetics/135.2.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Das O. P., Messing J. Variegated phenotype and developmental methylation changes of a maize allele originating from epimutation. Genetics. 1994 Mar;136(3):1121–1141. doi: 10.1093/genetics/136.3.1121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dooner H. K., Kermicle J. L. The Transposable Element Ds Affects the Pattern of Intragenic Recombination at the bz and R Loci in Maize. Genetics. 1986 May;113(1):135–143. doi: 10.1093/genetics/113.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Dowe M. F., Jr, Roman G. W., Klein A. S. Excision and transposition of two Ds transposons from the bronze mutable 4 derivative 6856 allele of Zea mays L. Mol Gen Genet. 1990 May;221(3):475–485. doi: 10.1007/BF00259414. [DOI] [PubMed] [Google Scholar]
  17. Eichenbaum Z., Livneh Z. Intermolecular transposition of IS10 causes coupled homologous recombination at the transposition site. Genetics. 1995 Jul;140(3):861–874. doi: 10.1093/genetics/140.3.861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Eisses J. F., Lafoe D., Scott L. A., Weil C. F. Novel, developmentally specific control of Ds transposition in maize. Mol Gen Genet. 1997 Sep;256(2):158–168. doi: 10.1007/s004380050557. [DOI] [PubMed] [Google Scholar]
  19. Emerson R A. Genetical Studies of Variegated Pericarp in Maize. Genetics. 1917 Jan;2(1):1–35. doi: 10.1093/genetics/2.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Greenblatt I M, Brink R A. Twin Mutations in Medium Variegated Pericarp Maize. Genetics. 1962 Apr;47(4):489–501. doi: 10.1093/genetics/47.4.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Grotewold E., Athma P., Peterson T. A possible hot spot for Ac insertion in the maize P gene. Mol Gen Genet. 1991 Nov;230(1-2):329–331. doi: 10.1007/BF00290684. [DOI] [PubMed] [Google Scholar]
  24. Grotewold E., Drummond B. J., Bowen B., Peterson T. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell. 1994 Feb 11;76(3):543–553. doi: 10.1016/0092-8674(94)90117-1. [DOI] [PubMed] [Google Scholar]
  25. Hagemann A. T., Craig N. L. Tn7 transposition creates a hotspot for homologous recombination at the transposon donor site. Genetics. 1993 Jan;133(1):9–16. doi: 10.1093/genetics/133.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hiraizumi Y. Spontaneous recombination in Drosophila melanogaster males. Proc Natl Acad Sci U S A. 1971 Feb;68(2):268–270. doi: 10.1073/pnas.68.2.268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jarvis P., Belzile F., Page T., Dean C. Increased Ac excision (iae): Arabidopsis thaliana mutations affecting Ac transposition. Plant J. 1997 May;11(5):907–919. [PubMed] [Google Scholar]
  28. Kermicle J. L. Probing the component structure of a maize gene with transposable elements. Science. 1980 Jun 27;208(4451):1457–1459. doi: 10.1126/science.208.4451.1457. [DOI] [PubMed] [Google Scholar]
  29. Kidwell M. G., Kidwell J. F. Selection for male recombination in Drosophila melanogaster. Genetics. 1976 Oct;84(2):333–351. doi: 10.1093/genetics/84.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kondo K., Inokuchi H., Ozeki H. The transposable element Tn3 promotes general recombination at the neighboring regions. Jpn J Genet. 1989 Dec;64(6):417–434. doi: 10.1266/jjg.64.417. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Lebel E. G., Masson J., Bogucki A., Paszkowski J. Stress-induced intrachromosomal recombination in plant somatic cells. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):422–426. doi: 10.1073/pnas.90.2.422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lechelt C., Peterson T., Laird A., Chen J., Dellaporta S. L., Dennis E., Peacock W. J., Starlinger P. Isolation and molecular analysis of the maize P locus. Mol Gen Genet. 1989 Oct;219(1-2):225–234. doi: 10.1007/BF00261181. [DOI] [PubMed] [Google Scholar]
  34. Levy A. A., Fridlender M., Rubin U. H., Sitrit Y. Binding of Nicotiana nuclear proteins to the subterminal regions of the Ac transposable element. Mol Gen Genet. 1996 Jun 24;251(4):436–441. doi: 10.1007/BF02172372. [DOI] [PubMed] [Google Scholar]
  35. Lowe B., Mathern J., Hake S. Active Mutator elements suppress the knotted phenotype and increase recombination at the Kn1-O tandem duplication. Genetics. 1992 Nov;132(3):813–822. doi: 10.1093/genetics/132.3.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mathern J., Hake S. Mu element-generated gene conversions in maize attenuate the dominant knotted phenotype. Genetics. 1997 Sep;147(1):305–314. doi: 10.1093/genetics/147.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Orr-Weaver T. L., Szostak J. W., Rothstein R. J. Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354–6358. doi: 10.1073/pnas.78.10.6354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Osman F., Fortunato E. A., Subramani S. Double-strand break-induced mitotic intrachromosomal recombination in the fission yeast Schizosaccharomyces pombe. Genetics. 1996 Feb;142(2):341–357. doi: 10.1093/genetics/142.2.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Peterson T. Intragenic transposition of Ac generates a new allele of the maize P gene. Genetics. 1990 Oct;126(2):469–476. doi: 10.1093/genetics/126.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Plasterk R. H. The origin of footprints of the Tc1 transposon of Caenorhabditis elegans. EMBO J. 1991 Jul;10(7):1919–1925. doi: 10.1002/j.1460-2075.1991.tb07718.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Prado F., Aguilera A. Role of reciprocal exchange, one-ended invasion crossover and single-strand annealing on inverted and direct repeat recombination in yeast: different requirements for the RAD1, RAD10, and RAD52 genes. Genetics. 1995 Jan;139(1):109–123. doi: 10.1093/genetics/139.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Preston C. R., Engels W. R. P-element-induced male recombination and gene conversion in Drosophila. Genetics. 1996 Dec;144(4):1611–1622. doi: 10.1093/genetics/144.4.1611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Puchta H., Dujon B., Hohn B. Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site-specific endonuclease. Nucleic Acids Res. 1993 Nov 11;21(22):5034–5040. doi: 10.1093/nar/21.22.5034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Puchta H., Dujon B., Hohn B. 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):5055–5060. doi: 10.1073/pnas.93.10.5055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Puchta H., Swoboda P., Gal S., Blot M., Hohn B. Somatic intrachromosomal homologous recombination events in populations of plant siblings. Plant Mol Biol. 1995 May;28(2):281–292. doi: 10.1007/BF00020247. [DOI] [PubMed] [Google Scholar]
  46. Rinehart T. A., Dean C., Weil C. F. Comparative analysis of non-random DNA repair following Ac transposon excision in maize and Arabidopsis. Plant J. 1997 Dec;12(6):1419–1427. doi: 10.1046/j.1365-313x.1997.12061419.x. [DOI] [PubMed] [Google Scholar]
  47. Rubin E., Levy A. A. Abortive gap repair: underlying mechanism for Ds element formation. Mol Cell Biol. 1997 Nov;17(11):6294–6302. doi: 10.1128/mcb.17.11.6294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Ruggiero-Lopez D., Biol M. C., Louisot P., Martin A. Participation of an endogenous inhibitor of fucosyltransferase activities in the developmental regulation of intestinal fucosylation processes. Biochem J. 1991 Nov 1;279(Pt 3):801–806. doi: 10.1042/bj2790801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Shalev G., Levy A. A. The maize transposable element Ac induces recombination between the donor site and an homologous ectopic sequence. Genetics. 1997 Jul;146(3):1143–1151. doi: 10.1093/genetics/146.3.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Sved J. A., Eggleston W. B., Engels W. R. Germ-line and somatic recombination induced by in vitro modified P elements in Drosophila melanogaster. Genetics. 1990 Feb;124(2):331–337. doi: 10.1093/genetics/124.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Svoboda Y. H., Robson M. K., Sved J. A. P-element-induced male recombination can be produced in Drosophila melanogaster by combining end-deficient elements in trans. Genetics. 1995 Apr;139(4):1601–1610. doi: 10.1093/genetics/139.4.1601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wessler S. R., Baran G., Varagona M. The maize transposable element Ds is spliced from RNA. Science. 1987 Aug 21;237(4817):916–918. doi: 10.1126/science.3039661. [DOI] [PubMed] [Google Scholar]
  53. Xiao Y. L., Peterson T. Intrachromosomal homologous recombination in Arabidopsis induced by a maize transposon. Mol Gen Genet. 2000 Feb;263(1):22–29. doi: 10.1007/pl00008672. [DOI] [PubMed] [Google Scholar]
  54. Xu X., Hsia A. P., Zhang L., Nikolau B. J., Schnable P. S. Meiotic recombination break points resolve at high rates at the 5' end of a maize coding sequence. Plant Cell. 1995 Dec;7(12):2151–2161. doi: 10.1105/tpc.7.12.2151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Yan X., Martínez-Férez I. M., Kavchok S., Dooner H. K. Origination of Ds elements from Ac elements in maize: evidence for rare repair synthesis at the site of Ac excision. Genetics. 1999 Aug;152(4):1733–1740. doi: 10.1093/genetics/152.4.1733. [DOI] [PMC free article] [PubMed] [Google Scholar]

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