Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1989 Nov;8(11):3177–3185. doi: 10.1002/j.1460-2075.1989.tb08476.x

The putative transposase of transposable element Ac from Zea mays L. interacts with subterminal sequences of Ac.

R Kunze 1, P Starlinger 1
PMCID: PMC401433  PMID: 2555157

Abstract

The Ac-specific ORFa protein, overexpressed in a baculovirus system, specifically binds to several subterminal fragments of Ac. The 11 bp long inverted repeats of the transposable element are not bound by the ORFa protein. Major ORFa protein-binding sites were delineated on 60 and 70 bp long sequence segments that lie 100 bp inside of the 5' Ac terminus and 40 bp inside of the 3' terminus respectively. Within all strongly bound fragments, and particularly in these 60 or 70 bp long segments, the hexamer motif AAACGG is repeated several times in direct or inverted orientation. The ORFa protein binds to synthetic concatemers of this motif, whereas the mutant motif AAAGGG is not complexed. Methylation of the cytosine residues in the AAACGG motif and/or its complementary strand has pronounced effects: whereas one of the two hemimethylated sequences has a higher affinity to the ORFa protein than both unmethylated and holomethylated DNAs, the other hemimethylated DNA is virtually not complexed at all. The native ORFa protein binding sites are more complex than the AAACGG sequence: certain Ac and Ds1 fragments devoid of AAACGG motifs (but containing several similar sequences) are weakly bound by the ORFa protein.

Full text

PDF
3177

Images in this article

3177Image
on p.3177
3178Image
on p.3178
3179Image
on p.3179
3179Image
on p.3179
3180Image
on p.3180
3181Image
on p.3181

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baker B., Coupland G., Fedoroff N., Starlinger P., Schell J. Phenotypic assay for excision of the maize controlling element Ac in tobacco. EMBO J. 1987 Jun;6(6):1547–1554. doi: 10.1002/j.1460-2075.1987.tb02399.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker B., Schell J., Lörz H., Fedoroff N. Transposition of the maize controlling element "Activator" in tobacco. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4844–4848. doi: 10.1073/pnas.83.13.4844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Chandler V. L., Walbot V. DNA modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1767–1771. doi: 10.1073/pnas.83.6.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coupland G., Baker B., Schell J., Starlinger P. Characterization of the maize transposable element Ac by internal deletions. EMBO J. 1988 Dec 1;7(12):3653–3659. doi: 10.1002/j.1460-2075.1988.tb03246.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coupland G., Baker B., Schell J., Starlinger P. Characterization of the maize transposable element Ac by internal deletions. EMBO J. 1988 Dec 1;7(12):3653–3659. doi: 10.1002/j.1460-2075.1988.tb03246.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Craigie R., Arndt-Jovin D. J., Mizuuchi K. A defined system for the DNA strand-transfer reaction at the initiation of bacteriophage Mu transposition: protein and DNA substrate requirements. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7570–7574. doi: 10.1073/pnas.82.22.7570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dooner H. K., English J., Ralston E. J. The frequency of transposition of the maize element Activator is not affected by an adjacent deletion. Mol Gen Genet. 1988 Mar;211(3):485–491. doi: 10.1007/BF00425705. [DOI] [PubMed] [Google Scholar]
  11. Döring H. P., Starlinger P. Molecular genetics of transposable elements in plants. Annu Rev Genet. 1986;20:175–200. doi: 10.1146/annurev.ge.20.120186.001135. [DOI] [PubMed] [Google Scholar]
  12. Fedoroff N. The heritable activation of cryptic Suppressor-mutator elements by an active element. Genetics. 1989 Mar;121(3):591–608. doi: 10.1093/genetics/121.3.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fried M., Crothers D. M. Equilibria and kinetics of lac repressor-operator interactions by polyacrylamide gel electrophoresis. Nucleic Acids Res. 1981 Dec 11;9(23):6505–6525. doi: 10.1093/nar/9.23.6505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. García-Blanco M. A., Clerc R. G., Sharp P. A. The DNA-binding homeo domain of the Oct-2 protein. Genes Dev. 1989 Jun;3(6):739–745. doi: 10.1101/gad.3.6.739. [DOI] [PubMed] [Google Scholar]
  15. Garner M. M., Revzin A. A gel electrophoresis method for quantifying the binding of proteins to specific DNA regions: application to components of the Escherichia coli lactose operon regulatory system. Nucleic Acids Res. 1981 Jul 10;9(13):3047–3060. doi: 10.1093/nar/9.13.3047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gierl A., Lütticke S., Saedler H. TnpA product encoded by the transposable element En-1 of Zea mays is a DNA binding protein. EMBO J. 1988 Dec 20;7(13):4045–4053. doi: 10.1002/j.1460-2075.1988.tb03298.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Hauser C., Fusswinkel H., Li J., Oellig C., Kunze R., Müller-Neumann M., Heinlein M., Starlinger P., Doerfler W. Overproduction of the protein encoded by the maize transposable element Ac in insect cells by a baculovirus vector. Mol Gen Genet. 1988 Nov;214(3):373–378. doi: 10.1007/BF00330469. [DOI] [PubMed] [Google Scholar]
  20. Jensen E. Ø, Marcker K. A., Schell J., Bruijn F. J. Interaction of a nodule specific, trans-acting factor with distinct DNA elements in the soybean leghaemoglobin Ibc(3) 5' upstream region. EMBO J. 1988 May;7(5):1265–1271. doi: 10.1002/j.1460-2075.1988.tb02940.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kemler I., Schreiber E., Müller M. M., Matthias P., Schaffner W. Octamer transcription factors bind to two different sequence motifs of the immunoglobulin heavy chain promoter. EMBO J. 1989 Jul;8(7):2001–2008. doi: 10.1002/j.1460-2075.1989.tb03607.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Leung P. C., Teplow D. B., Harshey R. M. Interaction of distinct domains in Mu transposase with Mu DNA ends and an internal transpositional enhancer. Nature. 1989 Apr 20;338(6217):656–658. doi: 10.1038/338656a0. [DOI] [PubMed] [Google Scholar]
  24. Martin C., Prescott A., Lister C., MacKay S. Activity of the transposon Tam3 in Antirrhinum and tobacco: possible role of DNA methylation. EMBO J. 1989 Apr;8(4):997–1004. doi: 10.1002/j.1460-2075.1989.tb03466.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McKown R. L., Waddell C. S., Arciszewska L. K., Craig N. L. Identification of a transposon Tn7-dependent DNA-binding activity that recognizes the ends of Tn7. Proc Natl Acad Sci U S A. 1987 Nov;84(22):7807–7811. doi: 10.1073/pnas.84.22.7807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Pereira A., Cuypers H., Gierl A., Schwarz-Sommer Z., Saedler H. Molecular analysis of the En/Spm transposable element system of Zea mays. EMBO J. 1986 May;5(5):835–841. doi: 10.1002/j.1460-2075.1986.tb04292.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Phadnis S. H., Berg D. E. Identification of base pairs in the outside end of insertion sequence IS50 that are needed for IS50 and Tn5 transposition. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9118–9122. doi: 10.1073/pnas.84.24.9118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pohlman R. F., Fedoroff N. V., Messing J. Correction: nucleotide sequence of Ac. Cell. 1984 Dec;39(2 Pt 1):417–417. doi: 10.1016/0092-8674(84)90020-5. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Potter S. S. DNA sequence of a foldback transposable element in Drosophila. Nature. 1982 May 20;297(5863):201–204. doi: 10.1038/297201a0. [DOI] [PubMed] [Google Scholar]
  32. Reed R. R., Young R. A., Steitz J. A., Grindley N. D., Guyer M. S. Transposition of the Escherichia coli insertion element gamma generates a five-base-pair repeat. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4882–4886. doi: 10.1073/pnas.76.10.4882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rio D. C., Rubin G. M. Identification and purification of a Drosophila protein that binds to the terminal 31-base-pair inverted repeats of the P transposable element. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8929–8933. doi: 10.1073/pnas.85.23.8929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  36. Saluz H., Jost J. P. A simple high-resolution procedure to study DNA methylation and in vivo DNA-protein interactions on a single-copy gene level in higher eukaryotes. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2602–2606. doi: 10.1073/pnas.86.8.2602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schiefelbein J. W., Raboy V., Fedoroff N. V., Nelson O. E., Jr Deletions within a defective suppressor-mutator element in maize affect the frequency and developmental timing of its excision from the bronze locus. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4783–4787. doi: 10.1073/pnas.82.14.4783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Schwartz D. Gene-controlled cytosine demethylation in the promoter region of the Ac transposable element in maize. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2789–2793. doi: 10.1073/pnas.86.8.2789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Schwarz-Sommer Z., Gierl A., Cuypers H., Peterson P. A., Saedler H. Plant transposable elements generate the DNA sequence diversity needed in evolution. EMBO J. 1985 Mar;4(3):591–597. doi: 10.1002/j.1460-2075.1985.tb03671.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Streck R. D., Macgaffey J. E., Beckendorf S. K. The structure of hobo transposable elements and their insertion sites. EMBO J. 1986 Dec 20;5(13):3615–3623. doi: 10.1002/j.1460-2075.1986.tb04690.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Van Sluys M. A., Tempé J., Fedoroff N. Studies on the introduction and mobility of the maize Activator element in Arabidopsis thaliana and Daucus carota. EMBO J. 1987 Dec 20;6(13):3881–3889. doi: 10.1002/j.1460-2075.1987.tb02728.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wiater L. A., Grindley N. D. Gamma delta transposase and integration host factor bind cooperatively at both ends of gamma delta. EMBO J. 1988 Jun;7(6):1907–1911. doi: 10.1002/j.1460-2075.1988.tb03024.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yin J. C., Reznikoff W. S. dnaA, an essential host gene, and Tn5 transposition. J Bacteriol. 1987 Oct;169(10):4637–4645. doi: 10.1128/jb.169.10.4637-4645.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. van Bergen B. G., van der Ley P. A., van Driel W., van Mansfeld A. D., van der Vliet P. C. Replication of origin containing adenovirus DNA fragments that do not carry the terminal protein. Nucleic Acids Res. 1983 Apr 11;11(7):1975–1989. doi: 10.1093/nar/11.7.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES