Summary
Tissue cultures were initiated from embryos with an inactive form of Ac in the wx-m9 Ds-cy allele. Plants regenerated from the cultures showed a high frequency of activation of Ac. That activation was shown to be associated with reduced methylation of cytosine residues at the 5′ end of the transposable element. An examination of Ac activity and methylation status of the Ac element in progenies of the regenerant plants demonstrated transmission of the altered epigenotype through two sexual generations. In these progenies no evidence for trans activation of inactive, partially methylated, Ac elements was obtained. These results confirm that in certain instances altered methylation patterns can be inherited through the germ line.
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References
Armstrong CL, Phillips RL (1988) Genetic and cytogenetic variation in plants regenerated from organogenic and friable, embryogenic tissue cultures of maize. Crop Sci 28:363–369
Banks JA, Fedoroff N (1989) Patterns of developmental and heritable change in methylation of the Suppressor-mutator transposable element. Dev Genet 10:425–437
Banks JA, Masson P, Fedoroff N (1988) Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element. Genes Dev 2:1364–1380
Benzion G, Phillips RL (1988) Cytogenetic stability of maize tissue cultures: a cell line pedigree analysis. Genome 30:318–325
Bestor T, Landano A, Mattaliano R, Ingram V (1988) Cloning and sequencing of a cDNA encoding DNA methyl transferase of mouse cell. The carboxyl terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J Mol Biol 202:971–983
Brettell RIS, Dennis ES, Scowcroft WR, Peacock WJ (1986) Molecular analysis of a somaclonal mutant of maize alcohol dehydrogenase. Mol Gen Genet 202:235–239
Brown PTH (1989) DNA methylation in plants and its role in tissue culture. Genome 31:717–729
Chandler VL, Walbot V (1986) DNA modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci USA 83:1767–1771
Chomet PS, Wessler S, Dellaporta SL (1987) Inactivation of the maize transposable element Activator (Ac) is associated with DNA modification. EMBO J 6:295–302
Chu CC, Wang CC, Sun CS, Hsü C, Yin KC, Chu CY, Bi FY (1975) Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Sci Sin 18:659–668
D'Amato F (1985) Cytogenetics of plant cell and tissue cultures and their regenerates. CRC Crit Rev Plant Sci 3:73–112
Dennis ES, Brettell RIS (1990) DNA methylation of maize transposable elements is correlated with activity. Philos Trans R Soc Lond [Biol] 326:217–229
Dennis ES, Sachs MM, Gerlach WL, Finnegan EJ, Peacock WJ (1985) Molecular analysis of the alcohol dehydrogenase 2 (Adh2) gene of maize. Nucleic Acids Res 13:727–743
Dennis ES, Brettell RIS, Peacock WJ (1987) A tissue culture induced Adh1 null mutant of maize results from a single base change. Mol Gen Genet 210:181–183
Fedoroff N, Wessler S, Shure M (1983) Isolation of the transposable maize controlling elements Ac and Ds. Cell 35:235–242
Holliday R (1990) Mechanisms for the control of gene activity during development. Biol Rev 65:431–471
Holliday R, Pugh JE (1975) DNA modification mechanisms and gene activity during development. Science 187:226–232
James MG, Stadler J (1989) Molecular characterization of Mutator systems in maize embryogenic callus cultures indicates Mu element activity in vitro. Theor Appl Genet 77:383–393
Kunze R, Stochaj U, Laufs J, Starlinger P (1987) Transcription of the transposable element Activator (Ac) of Zea mays L. EMBO J 6:1555–1563
Kunze R, Starlinger P, Schwartz D (1988) DNA methylation of the maize transposable element Ac interferes with its transcription. Mol Gen Genet 214:325–327
Larkin PJ, Scowcroft WR (1981) Somaclonal variation — a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214
Larkin PJ, Ryan SA, Brettell RIS, Scowcroft WR (1984) Heritable somaclonal variation in wheat. Theor Appl Genet 67:443–455
McCoy TJ, Phillips RL (1982) Chromosome stability in maize (Zea mays) tissue cultures and sectoring in some regenerated plants. Can J Genet C 24:559–565
Müller E, Brown PTH, Hartke S, Lörs H (1990) DNA variation in tissue culture-derived rice plants. Theor Appl Genet 80:673–679
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 15:473–497
Peschke VM, Phillips RL (1991) Activation of the maize transposable element Suppressor-mutator (Spm) in tissue culture. Theor Appl Genet 81:90–97
Peschke VM, Phillips RL, Gengenbach BG (1987) Discovery of transposable element activity among progeny of tissue culture-derived maize plants. Science 238:804–807
Phillips RL, Kaeppler SM, Peschke VM (1990) Do we understand somaclonal variation? In: Nijkamp HJJ, Van der Plas LHW, VanAartrijk J (eds) Progress in plant cellular and molecular biology. Kluwer Academic Publications, Dordrecht, Boston, London, pp 131–141
Planckaert F, Walbot V (1989) Molecular and genetic characterization of Mu transposable elements in Zea mays: behaviour in callus culture and regenerated plants. Genetics 123:567–578
Pohlman RF, Fedoroff NV, Messing J (1984) The nucleotide sequence of the maize controlling element Activator. Cell 37:635–642
Riggs AD (1975) X inactivation, differentiation and DNA methylation. Cytogenet Cell Genet 14:9–25
Sano H, Kamada I, Youssefian S, Katsumi M, Wabiko H (1990) A single treatment of rice seedlings with 5-azacytidine induces heritable dwarfism and undermethylation of genomic DNA. Mol Gen Genet 220:441–447
Schwartz D (1989) Gene-controlled cytosine demethylation in the promoter region of the Ac transposable element in maize. Proc Natl Acad Sci USA 86:2789–2793
Schwartz D, Dennis ES (1986) Transposase activity of the Ac controlling element in maize is regulated by its degree of methylation. Mol Gen Genet 205:476–482
Sutton WD, Gerlach WL, Schwartz D, Peacock WJ (1984) Molecular analysis of Ds controlling element mutations of the Adh1 locus of maize. Science 223:1265–1268
Wessler SR, Varagona MJ (1985) Molecular basis of mutations at the waxy locus of maize: correlation with the fine structure genetic map. Proc Natl Acad Sci USA 82:4177–4181
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Communicated by H. Saedler
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Brettell, R.I., Dennis, E.S. Reactivation of a silent Ac following tissue culture is associated with heritable alterations in its methylation pattern. Molec. Gen. Genet. 229, 365–372 (1991). https://doi.org/10.1007/BF00267457
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DOI: https://doi.org/10.1007/BF00267457