Abstract
We identified eight independent Tam3 copies residing in the same Antirrhinum majus genome. All the copies showed excision at 15 °C, but not at 25 °C. Under conditions promoting excision, each copy appeared to transpose in the leaves and flower lobes with a nearly constant frequency, whereas individual transposition abilities varied widely: the most active copy had an excision frequency more than 100-fold greater than that of the least active one. Despite the different transposition abilities, the structures of the eight Tam3 copies were almost identical. These results made it clear that the transpositional ability of Tam3 is regulated by chromosomal position, but they do not imply position-dependent transposase activity. The position effect of the Tam3 transposition was found to be correlated to the methylation state of the copy's end regions: DNA methylation in the Tam3 end regions tended to suppress the excision activity, and the degree of methylation was dependent on the chromosomal position. Our results also provide evidence of de novo methylation provoked by transposition of the endogenous element. We propose a mechanism of transpositional regulation of plant transposons that responds to the degree of methylation as determined by chromosomal position.
Similar content being viewed by others
References
Alleman, M. and Kermicle, J.L. 1993. Somatic variegation and germinal mutability reflect the position of transposable element Dissociation within the maize R gene. Genetics 135: 189–203.
Bancroft, I. and Dean, C. 1993. Factor affecting the excision fre-quency of the maize transposable element Ds in Arabidopsis thaliana. Mol. Gen. Genet. 240: 65–72.
Banks, J.A., Masson, P. and Fedoroff, N. 1988. Molecular mecha-nisms in the developmental regulation of the maize Suppressor-Mutator transposable element. Genes Dev. 2: 1364–1380.
Bennetzen, J.L. 1987. Covalent DNA modification and the regula-tion of Mutator element transposition in maize. Mol. Gen. Genet. 208: 45–51.
Berg, C. A. and Spradling, A.C. 1991. Studies on the rate and site-specificity of P element transposition. Genetics 127: 515–524.
Brown, J. and Sundaresan, V. 1992. Genetic study of the loss and restoration of Mutator transposon activity in maize: evi-dence against dominant-negative regulator associated with loss of activity. Genetics 130: 889–898.
Brutnell, T.P. and Dellaporta, S.L. 1994. Somatic inactivation and reactivation of Ac associated with changes in cytosine methyla-tion and transposase expression. Genetics 138: 213–225.
Calvi, B.R., Hong, T.J., Findley, S.D. and Gelbart, W.M. 1991. Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator, and Tam3. Cell 66: 465–471.
Carpenter, R., Martin, C. and Coen, E. 1987. Comparison of genetic behaviour of the transposable element Tam3 at two un-linked pigment loci in Antirrhinum majus. Mol. Gen. Genet. 207: 82–89.
Chandler, V.L., and Walbot, V. 1986. DNA modification of a maize transposable element correlates with loss of activity. Proc. Natl. Acad. Sci. USA 83: 1767–1771.
Chomet, P.S., Wessler, S. and Dellaporta, S.L. 1987. Inactivation of the maize transposable element Activator (Ac) is associated with its DNA modification. EMBO J. 6: 295–302.
Coen, E.S., Carpenter, R. and Martin, C. 1986. Transposable el-ements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell 47: 285–296.
Cubas, P., Vincent, C. and Coen, E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157–161.
Cuypers, H., Dash, S., Peterson, P.A., Saedler, H., and Gierl, A. 1988. The defective En-1102 element encodes a product reduc-ing the mutability of the En/Spm transposable element system of Zea mays. EMBO J. 7: 2953–2960.
Dennis, E.S. and Brettell, R.I. 1990. DNA methylation of maize transposable elements is correlated with activity. Phil. Trans. R. Soc. Lond. B Biol. Sci. 326: 217–229.
Doring, H.P. and Starlinger, P. 1986. Molecular genetics of trans-posable elements in plants. Annu. Rev. Genet. 20: 175–200.
Engels, W.R., Johnson-Schlitz, D.M., Eggleston, W.B. and Sved, J. 1990. High-frequency P element loss in Drosophila is homolog-dependent. Cell 62: 515–525.
Fedoroff, N.V. and Chandler, V. 1994. Inactivation of maize trans-posable elements. In: J. Paszkowski (Ed.) Homologous Re-combination and Gene Silencing in Plants, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 349–385.
Fedroff, N., and Schlappi, M. and Raina, R. 1995. Epigenetic regulation of the maize Spm transposon. Bioessays 17: 291–297.
Garza, D., Medhora, M., Koga, A. and Hartl, D.L. 1991. Intro-duction of the transposable element mariner into the germline of Drosophila melanogaster. Genetics 128: 303–310.
Gloor, G.B., Nassif, N.A., Johnson-Schlitz, D.M., Preston, C.R. and Engels, W.R. 1991. Targeted gene replacement in Drosophila via P element-induced gap repair. Science 253: 1110–1117.
Haring, M., Gao, H.G., Volbeda, T., Rommens, T. H.J., Nijkamp, J. and Hille, J. 1989. A comparative study of Tam3 and Ac transpo-sition in transgenic tobacco and petunia plants. Plant Mol. Biol. 13: 189–201.
Harrison, B.J. and Fincham, J.R.S. 1964. Instability at the pal locus in Antirrhinum majus.I. Effects of environment on frequencies of somatic and germinal mutation. Heredity 19: 237–258.
Harrison, B.J. and Fincham, J.R.S. 1968. Instability at the pal locus in Antirrhinum majus. III. A gene controlling mutation frequency. Heredity 23: 67–72.
Hehl, H., Nacken, W.K.F., Krause, A., Saedler, H. and Sommer, H. 1991. Structural analysis of Tam3, a transposable element from Antirrhinum majus, reveals homologies to the Ac element from maize. Plant Mol. Biol. 16: 369–371.
Jeddelho, J.A., Stokes, T.L. and Richards, E.J. 1999. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nature Genet. 22: 94–97.
Kidwell, M.G. 1994. The evolutionary history of the P family of transposable elements. J. Hered. 85: 339–346.
Kidwell, M.G. and Lisch, D. 1997. Transposable elements as sources of variation in animals and plants. Proc. Natl. Acad. Sci. USA 94: 7704–7711.
Kishima, Y., Yamashita, S., Martin, C. and Mikami, T. 1999. Struc-tural conservation of the transposon Tam3 family in Antirrhinum majus and estimation of the number of copies able to transpose. Plant Mol. Biol. 39: 299–308.
Kishima, Y., Yamashita, S. and Mikami, T. 1997. Immobilized copies with a nearly intact structure of the transposon Tam3 in Antirrhinum majus: implications for the cis-element related to the transposition. Theor. Appl. Genet. 95: 1246–1251.
Kunze, R. and Starlinger, P. 1989. The putative transposase of trans-posable element Ac from Zea mays L. interacts with subterminal sequences of Ac. EMBO J. 8: 3177–3185.
Kunze, R., Starlinger, P. and Schwartz, D. 1988. DNA methyla-tion of the maize transposable element Ac interferes with its transcription. Mol Gen Genet 214: 325–327.
Kunze, R., Stochaj, U., Laufs, J. and Starlinger, P. 1987. Tran-scription of transposable element Activator (Ac) of Zea mays L. EMBO J. 6: 1555–1563.
Laski, F.A., Rio, D.C. and Rubin, G.M. 1986. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44: 7–19.490
Levy, A.A., and Walbot, V. 1990. Regulation of the timing of trans-posable element excision during maize development. Science 248: 1534–1537.
Li, E., Bestor, T.H. and Jaenisch, R. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915–926.
Lisch, D., Chomet, P. and Freeling, M. 1995. Genetic characteriza-tion of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line. Genetics 139: 1777–1796.
Lohuis, M., Müller, A., Heidmann, I., Niedenhof I. and Meyer, P. 1995. A repetitive DNA fragment carrying a hot spot for de novo methylation enhances expression variegation in tobacco and petunia. Plant J. 8: 919–932.
Lozovskaya, E.R., Hartl, D.L. and Petrov, D.A. 1995. Genomic regulation of transposable elements in Drosophila.Curr.Opin. Genet. Dev. 5: 768–773.
Luff, B., Pawlowski, L. and Bender, J. 1999. An inverted repeat trig-gers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 4: 505–511.
Martin, C., Carpenter, R., Sommer, H., Saedler, H. and Coen, E. 1985. Molecular analysis of instability in flower pigmentation of Antirrhinum majus following isolation of the pallida locus by transposon tagging. EMBO J. 4: 1625–1630.
Martin, C., Prescott, A., Lister, C. and MacKay, S. 1989. Activity of the transposon Tam3 in Antirrhinum and tobacco: possible role of DNA methylation. EMBO J. 8: 997–1004.
Martienssen, R. and Baron, A. 1994. Coordinate suppression of mutations caused by Robertson's Mutator transposons in maize. Genetics 136: 1157–1170.
Meyer, P. and Heidmann, I. 1994. Epigenetic variants of a trans-genic petunia line show hypermethylation in transgene DNA: an indication for specifc recognition of foreign DNA in transgenic plants. Mol. Gen. Genet. 243: 390–399.
McDonald, J.F. 1993. Evolution and consequences of transposable elements. Curr. Opin. Genet. Dev. 3: 855–864.
Ochman, H. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120: 621–623.
O'Kane, C.J. and Gehring, W.J. 1987. Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl. Acad. Sci. USA 84: 9123–9127.
Okano, M., Bell, W.D., Haber, D.A. and Li, E. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247–257.
Peterson, P.W. and Yoder, J.I. 1995. Amplification of Ac in tomato is correlated with high Ac transposition activity. Genome 38: 265–276.
Reik, W., Kelsey, G. and Walter, J. 1999. Dissecting de novo methylation. Nature Genet. 23: 380–382.
Rio, D.C. 1991. Regulation of Drosophila P element transposition. Trends Genet. 7: 282–287.
Roberts, D., Hoopes, B.C., McClure, W.R. and Kleckner, N. 1985. IS10 transposition is regulated by DNA adenine methylation. Cell 43: 117–130.
Saedler, H. and Gierl, A. 1996. Transposable Elements. Current Topics in Microbiology and Immunology 204. Springer-Verlag, Berlin/Heidelberg.
Schläppi, M., Raina, R. and Fedoroff, N. 1994. Epigenetic regula-tion of the maize Spm transposable element: novel activation of a methylated promoter by TnpA. Cell 77: 427–437.
Schwartz, D. and Dennis, E. 1986. Transposase activity of the Ac controlling element in maize is regulated by its degree of methylation. Mol. Gen. Genet. 205: 476–482.
Smit, A.F. and Riggs, A.D. 1996. Tiggers and DNA transposon fossils in the human genome. Proc. Natl. Acad. Sci. USA 93: 1443–1448.
Smith, D., Yanai, Y., Liu, Y.G., Ishiguro, S., Okada, K., Shi-bata, D., Whittler, R.F. and Fedoroff, N. 1994. Characterization and mapping of Ds-GUS-T-DNA lines for targeted insertional mutagenesis. Plant J. 10: 721–732.
Sommer, H., Carpenter, R., Harrison, B.J. and Saedler, H. 1985. The transposable element Tam3 of Antirrhinum majus generates a novel type of sequence alterations upon excision. Mol. Gen. Genet. 199: 225–231.
Stam, M., Viterbo, A., Mol, J.N.M. and Kooter, J.M. 1998. Position-dependent methylation and transcriptional silencing of transgenes in inverted T-DNA repeats: implications for posttran-scriptional silencing of homologous host genes in plants. Mol. Cell Biol. 18: 6165–6177.
Wang, L., Heinlein, M. and Kunze, R. 1996. Methylation pattern of Activator transposase binding sites in maize endosperm. Plant Cell 4: 747–758.
Wang, L. and Kunze, R. 1998. Transposase binding site methylation in the epigenetically inactivated Ac derivative Ds-cy. Plant J. 13: 577–582.
Yamashita, S., Mikami, T. and Kishima, Y. 1998. Tam3 in Antir-rhinum majus is an exceptional transposon resistant to alteration by abortive gap repair: identification of nested transposons. Mol. Gen. Genet. 259: 468–474.
Yamashita, S., Shimizu-Takano, T., Kitamura, K., Mikami, T. and Kishima, Y. 1999. Resistance to gap repair of the transposon Tam3 i n Antirrhinum majus: a role of the end regions. Genetics 153: 1899–1908.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kitamura, K., Hashida, Sn., Mikami, T. et al. Position effect of the excision frequency of the Antirrhinum transposon Tam3: implications for the degree of position-dependent methylation in the ends of the element. Plant Mol Biol 47, 475–490 (2001). https://doi.org/10.1023/A:1011892003996
Issue Date:
DOI: https://doi.org/10.1023/A:1011892003996