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. 1997 Oct;147(2):823–834. doi: 10.1093/genetics/147.2.823

The Ac-St2 Element of Maize Exhibits a Positive Dosage Effect and Epigenetic Regulation

T P Brutnell 1, B P May 1, S L Dellaporta 1
PMCID: PMC1208202  PMID: 9335617

Abstract

A novel derivative of the maize transposable element Ac, termed Ac-st2, that displays a positive dosage effect in maize has been identified. Although identical in sequence to other Ac elements, increasing the copy number of the element in the endosperm results in earlier and more frequent Ds excisions. Ac-st2 autonomously transposes and catalyzes somatic excisions of Ds elements. Germinal transpositions of either Ac-st2 or Ds, however, were not observed. The Ac-st2 phenotype includes a reduction in Ac transcript accumulation that is associated with increased methylation at specific sites in the promoter region of the major transcriptional start site within Ac (ORFa). This element differs from metastable (cycling) Ac derivatives in that Ac-st2 conditions a uniform transposition pattern throughout endosperm and plant development. Ac-st2 undergoes frequent increases in activity after its association with an active Ac element. This change in activity correlates with reduced levels of methylation in the ORFa promoter region. Using a competitive PCR assay, Ac transcript accumulation was followed through endosperm development. From these data, a model is proposed to explain the patterns of variegation associated with both ``wild type'' active Ac and Ac-st2 elements.

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Selected References

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  1. Alleman M., Kermicle J. L. Somatic variegation and germinal mutability reflect the position of transposable element Dissociation within the maize R gene. Genetics. 1993 Sep;135(1):189–203. doi: 10.1093/genetics/135.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bestor T. H., Chandler V. L., Feinberg A. P. Epigenetic effects in eukaryotic gene expression. Dev Genet. 1994;15(6):458–462. doi: 10.1002/dvg.1020150603. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Caldwell E. E., Peterson P. A. The Ac and Uq transposable element systems in maize: interactions among components. Genetics. 1992 Jul;131(3):723–731. doi: 10.1093/genetics/131.3.723. [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. Conrad M. N., Wright J. H., Wolf A. J., Zakian V. A. RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability. Cell. 1990 Nov 16;63(4):739–750. doi: 10.1016/0092-8674(90)90140-a. [DOI] [PubMed] [Google Scholar]
  7. Faugeron G., Rhounim L., Rossignol J. L. How does the cell count the number of ectopic copies of a gene in the premeiotic inactivation process acting in Ascobolus immersus? Genetics. 1990 Mar;124(3):585–591. doi: 10.1093/genetics/124.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Goyon C., Faugeron G. Targeted transformation of Ascobolus immersus and de novo methylation of the resulting duplicated DNA sequences. Mol Cell Biol. 1989 Jul;9(7):2818–2827. doi: 10.1128/mcb.9.7.2818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Henikoff S. Position-effect variegation after 60 years. Trends Genet. 1990 Dec;6(12):422–426. doi: 10.1016/0168-9525(90)90304-o. [DOI] [PubMed] [Google Scholar]
  12. Jones J. D., Carland F. M., Maliga P., Dooner H. K. Visual detection of transposition of the maize element activator (ac) in tobacco seedlings. Science. 1989 Apr 14;244(4901):204–207. doi: 10.1126/science.244.4901.204. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Leu J. Y., Sun Y. H., Lai Y. K., Chen J. A maize cryptic Ac-homologous sequence derived from an Activator transposable element does not transpose. Mol Gen Genet. 1992 Jun;233(3):411–418. doi: 10.1007/BF00265438. [DOI] [PubMed] [Google Scholar]
  16. Levine A., Yeivin A., Ben-Asher E., Aloni Y., Razin A. Histone H1-mediated inhibition of transcription initiation of methylated templates in vitro. J Biol Chem. 1993 Oct 15;268(29):21754–21759. [PubMed] [Google Scholar]
  17. Loo S., Rine J. Silencers and domains of generalized repression. Science. 1994 Jun 17;264(5166):1768–1771. doi: 10.1126/science.8209257. [DOI] [PubMed] [Google Scholar]
  18. Matzke M. A., Primig M., Trnovsky J., Matzke A. J. Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J. 1989 Mar;8(3):643–649. doi: 10.1002/j.1460-2075.1989.tb03421.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McCLINTOCK B. Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol. 1951;16:13–47. doi: 10.1101/sqb.1951.016.01.004. [DOI] [PubMed] [Google Scholar]
  20. McCLINTOCK B. The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A. 1950 Jun;36(6):344–355. doi: 10.1073/pnas.36.6.344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Pisabarro A. G., Martin W. F., Peterson P. A., Saedler H., Gierl A. Molecular analysis of the Ubiquitous (Uq) transposable element system of Zea mays. Mol Gen Genet. 1991 Nov;230(1-2):201–208. doi: 10.1007/BF00290669. [DOI] [PubMed] [Google Scholar]
  23. Schläppi M., Raina R., Fedoroff N. Epigenetic regulation of the maize Spm transposable element: novel activation of a methylated promoter by TnpA. Cell. 1994 May 6;77(3):427–437. doi: 10.1016/0092-8674(94)90157-0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Scofield S. R., English J. J., Jones J. D. High level expression of the Activator transposase gene inhibits the excision of Dissociation in tobacco cotyledons. Cell. 1993 Nov 5;75(3):507–517. doi: 10.1016/0092-8674(93)90385-4. [DOI] [PubMed] [Google Scholar]
  26. Scofield S. R., Harrison K., Nurrish S. J., Jones J. D. Promoter fusions to the Activator transposase gene cause distinct patterns of Dissociation excision in tobacco cotyledons. Plant Cell. 1992 May;4(5):573–582. doi: 10.1105/tpc.4.5.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Selker E. U., Cambareri E. B., Jensen B. C., Haack K. R. Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell. 1987 Dec 4;51(5):741–752. doi: 10.1016/0092-8674(87)90097-3. [DOI] [PubMed] [Google Scholar]
  28. Sheen J. Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell. 1991 Mar;3(3):225–245. doi: 10.1105/tpc.3.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Singh J., Klar A. J. Active genes in budding yeast display enhanced in vivo accessibility to foreign DNA methylases: a novel in vivo probe for chromatin structure of yeast. Genes Dev. 1992 Feb;6(2):186–196. doi: 10.1101/gad.6.2.186. [DOI] [PubMed] [Google Scholar]
  30. Spradling A. C., Rubin G. M. The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell. 1983 Aug;34(1):47–57. doi: 10.1016/0092-8674(83)90135-6. [DOI] [PubMed] [Google Scholar]
  31. Swinburne J., Balcells L., Scofield S. R., Jones J. D., Coupland G. Elevated levels of Activator transposase mRNA are associated with high frequencies of Dissociation excision in Arabidopsis. Plant Cell. 1992 May;4(5):583–595. doi: 10.1105/tpc.4.5.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Yoder J. I. Rapid proliferation of the maize transposable element Activator in transgenic tomato. Plant Cell. 1990 Aug;2(8):723–730. doi: 10.1105/tpc.2.8.723. [DOI] [PMC free article] [PubMed] [Google Scholar]

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