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. 2001 Apr;157(4):1723–1733. doi: 10.1093/genetics/157.4.1723

Regulation of activator/dissociation transposition by replication and DNA methylation.

F Ros 1, R Kunze 1
PMCID: PMC1461610  PMID: 11290726

Abstract

In maize the transposable elements Activator/Dissociation (Ac/Ds) transpose shortly after replication from one of the two resulting chromatids ("chromatid selectivity"). A model has been suggested that explains this phenomenon as a consequence of different affinity for Ac transposase binding to holo-, hemi-, and unmethylated transposon ends. Here we demonstrate that in petunia cells a holomethylated Ds is unable to excise from a nonreplicating vector and that replication restores excision. A Ds element hemi-methylated on one DNA strand transposes in the absence of replication, whereas hemi-methylation of the complementary strand causes a >6.3-fold inhibition of Ds excision. Consistently in the active hemi-methylated state, the Ds ends have a high binding affinity for the transposase, whereas binding to inactive ends is strongly reduced. These results provide strong evidence for the above-mentioned model. Moreover, in the absence of DNA methylation, replication enhances Ds transposition in petunia protoplasts >8-fold and promotes formation of a predominant excision footprint. Accordingly, replication also has a methylation-independent regulatory effect on transposition.

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Selected References

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  1. Atkinson P. W., Warren W. D., O'Brochta D. A. The hobo transposable element of Drosophila can be cross-mobilized in houseflies and excises like the Ac element of maize. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9693–9697. doi: 10.1073/pnas.90.20.9693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Banks J. A., Masson P., Fedoroff N. Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element. Genes Dev. 1988 Nov;2(11):1364–1380. doi: 10.1101/gad.2.11.1364. [DOI] [PubMed] [Google Scholar]
  3. Becker H. A., Kunze R. Maize Activator transposase has a bipartite DNA binding domain that recognizes subterminal sequences and the terminal inverted repeats. Mol Gen Genet. 1997 Apr 16;254(3):219–230. doi: 10.1007/s004380050410. [DOI] [PubMed] [Google Scholar]
  4. Chatterjee S., Starlinger P. The role of subterminal sites of transposable element Ds of Zea mays in excision. Mol Gen Genet. 1995 Nov 27;249(3):281–288. doi: 10.1007/BF00290528. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Chen J., Greenblatt I. M., Dellaporta S. L. Transposition of Ac from the P locus of maize into unreplicated chromosomal sites. Genetics. 1987 Sep;117(1):109–116. doi: 10.1093/genetics/117.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Colot V., Haedens V., Rossignol J. L. Extensive, nonrandom diversity of excision footprints generated by Ds-like transposon Ascot-1 suggests new parallels with V(D)J recombination. Mol Cell Biol. 1998 Jul;18(7):4337–4346. doi: 10.1128/mcb.18.7.4337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Essers L., Adolphs R. H., Kunze R. A highly conserved domain of the maize activator transposase is involved in dimerization. Plant Cell. 2000 Feb;12(2):211–224. doi: 10.1105/tpc.12.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Feldmar S., Kunze R. The ORFa protein, the putative transposase of maize transposable element Ac, has a basic DNA binding domain. EMBO J. 1991 Dec;10(13):4003–4010. doi: 10.1002/j.1460-2075.1991.tb04975.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fontes E. P., Eagle P. A., Sipe P. S., Luckow V. A., Hanley-Bowdoin L. Interaction between a geminivirus replication protein and origin DNA is essential for viral replication. J Biol Chem. 1994 Mar 18;269(11):8459–8465. [PubMed] [Google Scholar]
  11. Gorbunova V., Levy A. A. Analysis of extrachromosomal Ac/Ds transposable elements. Genetics. 2000 May;155(1):349–359. doi: 10.1093/genetics/155.1.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Heinlein M., Brattig T., Kunze R. In vivo aggregation of maize Activator (Ac) transposase in nuclei of maize endosperm and Petunia protoplasts. Plant J. 1994 May;5(5):705–714. doi: 10.1111/j.1365-313x.1994.00705.x. [DOI] [PubMed] [Google Scholar]
  14. Houba-Hérin N., Becker D., Post A., Larondelle Y., Starlinger P. Excision of a Ds-like maize transposable element (Ac delta) in a transient assay in Petunia is enhanced by a truncated coding region of the transposable element Ac. Mol Gen Genet. 1990 Oct;224(1):17–23. doi: 10.1007/BF00259446. [DOI] [PubMed] [Google Scholar]
  15. Houba-Hérin N., Domin M., Pédron J. Transposition of a Ds element from a plasmid into the plant genome in Nicotiana plumbaginifolia protoplast-derived cells. Plant J. 1994 Jul;6(1):55–66. doi: 10.1046/j.1365-313x.1994.6010055.x. [DOI] [PubMed] [Google Scholar]
  16. Kennedy A. K., Guhathakurta A., Kleckner N., Haniford D. B. Tn10 transposition via a DNA hairpin intermediate. Cell. 1998 Oct 2;95(1):125–134. doi: 10.1016/s0092-8674(00)81788-2. [DOI] [PubMed] [Google Scholar]
  17. Kheyr-Pour A., Bendahmane M., Matzeit V., Accotto G. P., Crespi S., Gronenborn B. Tomato yellow leaf curl virus from Sardinia is a whitefly-transmitted monopartite geminivirus. Nucleic Acids Res. 1991 Dec 25;19(24):6763–6769. doi: 10.1093/nar/19.24.6763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kunze R., Behrens U., Courage-Franzkowiak U., Feldmar S., Kühn S., Lütticke R. Dominant transposition-deficient mutants of maize Activator (Ac) transposase. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7094–7098. doi: 10.1073/pnas.90.15.7094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kunze R., Starlinger P. The putative transposase of transposable element Ac from Zea mays L. interacts with subterminal sequences of Ac. EMBO J. 1989 Nov;8(11):3177–3185. doi: 10.1002/j.1460-2075.1989.tb08476.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Laufs J., Traut W., Heyraud F., Matzeit V., Rogers S. G., Schell J., Gronenborn B. In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3879–3883. doi: 10.1073/pnas.92.9.3879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Laufs J., Wirtz U., Kammann M., Matzeit V., Schaefer S., Schell J., Czernilofsky A. P., Baker B., Gronenborn B. Wheat dwarf virus Ac/Ds vectors: expression and excision of transposable elements introduced into various cereals by a viral replicon. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7752–7756. doi: 10.1073/pnas.87.19.7752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McElroy D., Louwerse J. D., McElroy S. M., Lemaux P. G. Development of a simple transient assay for Ac/Ds activity in cells of intact barley tissue. Plant J. 1997 Jan;11(1):157–165. doi: 10.1046/j.1365-313x.1997.11010157.x. [DOI] [PubMed] [Google Scholar]
  23. Nagar S., Pedersen T. J., Carrick K. M., Hanley-Bowdoin L., Robertson D. A geminivirus induces expression of a host DNA synthesis protein in terminally differentiated plant cells. Plant Cell. 1995 Jun;7(6):705–719. doi: 10.1105/tpc.7.6.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Roberts D., Hoopes B. C., McClure W. R., Kleckner N. IS10 transposition is regulated by DNA adenine methylation. Cell. 1985 Nov;43(1):117–130. doi: 10.1016/0092-8674(85)90017-0. [DOI] [PubMed] [Google Scholar]
  25. Roth D. B., Menetski J. P., Nakajima P. B., Bosma M. J., Gellert M. V(D)J recombination: broken DNA molecules with covalently sealed (hairpin) coding ends in scid mouse thymocytes. Cell. 1992 Sep 18;70(6):983–991. doi: 10.1016/0092-8674(92)90248-b. [DOI] [PubMed] [Google Scholar]
  26. Saedler H., Nevers P. Transposition in plants: a molecular model. EMBO J. 1985 Mar;4(3):585–590. doi: 10.1002/j.1460-2075.1985.tb03670.x. [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. Shen W. H., Das S., Hohn B. Mechanism of Ds1 excision from the genome of maize streak virus. Mol Gen Genet. 1992 Jun;233(3):388–394. doi: 10.1007/BF00265435. [DOI] [PubMed] [Google Scholar]
  29. Sugimoto K., Otsuki Y., Saji S., Hirochika H. Transposition of the maize Ds element from a viral vector to the rice genome. Plant J. 1994 Jun;5(6):863–871. doi: 10.1046/j.1365-313x.1994.5060863.x. [DOI] [PubMed] [Google Scholar]
  30. Wang L., Heinlein M., Kunze R. Methylation pattern of Activator transposase binding sites in maize endosperm. Plant Cell. 1996 Apr;8(4):747–758. doi: 10.1105/tpc.8.4.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wang L., Kunze R. Transposase binding site methylation in the epigenetically inactivated Ac derivative Ds-cy. Plant J. 1998 Feb;13(4):577–582. doi: 10.1046/j.1365-313x.1998.00060.x. [DOI] [PubMed] [Google Scholar]
  32. Weil C. F., Kunze R. Transposition of maize Ac/Ds transposable elements in the yeast Saccharomyces cerevisiae. Nat Genet. 2000 Oct;26(2):187–190. doi: 10.1038/82827. [DOI] [PubMed] [Google Scholar]
  33. Wirtz U., Osborne B., Baker B. Ds excision from extrachromosomal geminivirus vector DNA is coupled to vector DNA replication in maize. Plant J. 1997 Jan;11(1):125–135. doi: 10.1046/j.1365-313x.1997.11010125.x. [DOI] [PubMed] [Google Scholar]
  34. van Gent D. C., Mizuuchi K., Gellert M. Similarities between initiation of V(D)J recombination and retroviral integration. Science. 1996 Mar 15;271(5255):1592–1594. doi: 10.1126/science.271.5255.1592. [DOI] [PubMed] [Google Scholar]

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