Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1996 Apr;8(4):747–758. doi: 10.1105/tpc.8.4.747

Methylation pattern of Activator transposase binding sites in maize endosperm.

L Wang 1, M Heinlein 1, R Kunze 1
PMCID: PMC161134  PMID: 8624445

Abstract

The maize transposable element Activator (Ac) transposes after replication from only one of the two daughter chromatids. It has been suggested that DNA methylation in conjunction with methylation-sensitive transposase binding to DNA may control the association of Ac transposition and replication. We present here a detailed genomic sequencing analysis of the cytosine methylation patterns of the transposase binding sites within both Ac ends in the wx-m9::Ac allele, where Ac is inserted into the tenth exon of the Waxy gene. The Ac elements in wx-m9::Ac kernels exhibit intriguing methylation patterns and fall into two distinct groups. Approximately 50% of the elements are fully unmethylated at cytosine residues through the 256 nucleotides at the 5' end (the promoter end). The other half is partially methylated between Ac residues 27 and 92. In contrast, at the 3' end, all Ac molecules are heavily methylated between residues 4372 and 4554. The more internally located Ac sequences and the flanking Waxy DNA are unmethylated. Although most methylated cytosines in Ac are in the symmetrical CpG and CpNpG arrangements, nonsymmetrical cytosine methylation is also common in the hypermethylated regions of Ac. These results suggest a model in which differential activation of transposon ends by hemimethylation controls the chromatid selectivity of transposition and the association with replication.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

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

  1. Becker D., Lütticke R., Li M., Starlinger P. Control of excision frequency of maize transposable element Ds in Petunia protoplasts. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5552–5556. doi: 10.1073/pnas.89.12.5552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bird A. P. CpG-rich islands and the function of DNA methylation. Nature. 1986 May 15;321(6067):209–213. doi: 10.1038/321209a0. [DOI] [PubMed] [Google Scholar]
  3. Brandeis M., Frank D., Keshet I., Siegfried Z., Mendelsohn M., Nemes A., Temper V., Razin A., Cedar H. Sp1 elements protect a CpG island from de novo methylation. Nature. 1994 Sep 29;371(6496):435–438. doi: 10.1038/371435a0. [DOI] [PubMed] [Google Scholar]
  4. Brettell R. I., Dennis E. S. Reactivation of a silent Ac following tissue culture is associated with heritable alterations in its methylation pattern. Mol Gen Genet. 1991 Oct;229(3):365–372. doi: 10.1007/BF00267457. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. Coupland G., Plum C., Chatterjee S., Post A., Starlinger P. Sequences near the termini are required for transposition of the maize transposon Ac in transgenic tobacco plants. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9385–9388. doi: 10.1073/pnas.86.23.9385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dash S., Peterson P. A. Frequent loss of the En transposable element after excision and its relation to chromosome replication in maize (Zea mays L.). Genetics. 1994 Feb;136(2):653–671. doi: 10.1093/genetics/136.2.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Döring H. P., Nelsen-Salz B., Garber R., Tillmann E. Double Ds elements are involved in specific chromosome breakage. Mol Gen Genet. 1989 Oct;219(1-2):299–305. doi: 10.1007/BF00261191. [DOI] [PubMed] [Google Scholar]
  14. English J. J., Harrison K., Jones JDG. Aberrant Transpositions of Maize Double Ds-Like Elements Usually Involve Ds Ends on Sister Chromatids. Plant Cell. 1995 Aug;7(8):1235–1247. doi: 10.1105/tpc.7.8.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. English J., Harrison K., Jones J. D. A genetic analysis of DNA sequence requirements for Dissociation state I activity in tobacco. Plant Cell. 1993 May;5(5):501–514. doi: 10.1105/tpc.5.5.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fedoroff N., Masson P., Banks J. A. Mutations, epimutations, and the developmental programming of the maize Suppressor-mutator transposable element. Bioessays. 1989 May;10(5):139–144. doi: 10.1002/bies.950100502. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Geiser M., Weck E., Döring H. P., Werr W., Courage-Tebbe U., Tillmann E., Starlinger P. Genomic clones of a wild-type allele and a transposable element-induced mutant allele of the sucrose synthase gene of Zea mays L. EMBO J. 1982;1(11):1455–1460. doi: 10.1002/j.1460-2075.1982.tb01337.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. 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]
  22. 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]
  23. Greenblatt I. M. The mechanism of modulator transposition in maize. Genetics. 1968 Apr;58(4):585–597. doi: 10.1093/genetics/58.4.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hehl R., Nacken W. K., Krause A., Saedler H., Sommer H. Structural analysis of Tam3, a transposable element from Antirrhinum majus, reveals homologies to the Ac element from maize. Plant Mol Biol. 1991 Feb;16(2):369–371. doi: 10.1007/BF00020572. [DOI] [PubMed] [Google Scholar]
  25. Herrmann A., Schulz W., Hahlbrock K. Two alleles of the single-copy chalcone synthase gene in parsley differ by a transposon-like element. Mol Gen Genet. 1988 Apr;212(1):93–98. doi: 10.1007/BF00322449. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Keller J., Jones J. D., Harper E., Lim E., Carland F., Ralston E. J., Dooner H. K. Effects of gene dosage and sequence modification on the frequency and timing of transposition of the maize element Activator (Ac) in tobacco. Plant Mol Biol. 1993 Jan;21(1):157–170. doi: 10.1007/BF00039626. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Lacour M., Vidal P. P., Xerri C. Early directional influence of visual motion cues on postural control in the falling monkey. Ann N Y Acad Sci. 1981;374:403–411. doi: 10.1111/j.1749-6632.1981.tb30886.x. [DOI] [PubMed] [Google Scholar]
  30. Macleod D., Charlton J., Mullins J., Bird A. P. Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev. 1994 Oct 1;8(19):2282–2292. doi: 10.1101/gad.8.19.2282. [DOI] [PubMed] [Google Scholar]
  31. Martienssen R., Baron A. Coordinate suppression of mutations caused by Robertson's mutator transposons in maize. Genetics. 1994 Mar;136(3):1157–1170. doi: 10.1093/genetics/136.3.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Meyer P., Niedenhof I., ten Lohuis M. Evidence for cytosine methylation of non-symmetrical sequences in transgenic Petunia hybrida. EMBO J. 1994 May 1;13(9):2084–2088. doi: 10.1002/j.1460-2075.1994.tb06483.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Murray M. G., Thompson W. F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980 Oct 10;8(19):4321–4325. doi: 10.1093/nar/8.19.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Peleman J., Cottyn B., Van Camp W., Van Montagu M., Inzé D. Transient occurrence of extrachromosomal DNA of an Arabidopsis thaliana transposon-like element, Tat1. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3618–3622. doi: 10.1073/pnas.88.9.3618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rhodes P. R., Vodkin L. O. Organization of the Tgm family of transposable elements in soybean. Genetics. 1988 Oct;120(2):597–604. doi: 10.1093/genetics/120.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Theres N, Scheele T, Starlinger P. Cloning of the Bz2 locus of Zea mays using the transposable element Ds as a gene tag. Mol Gen Genet. 1987 Aug;209(1):193–197. doi: 10.1007/BF00329858. [DOI] [PubMed] [Google Scholar]
  38. 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]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES