Abstract
Genetic approaches to identify molecular components of transcriptional gene silencing (TGS) in plants have yielded several Arabidopsis thaliana mutants and identified the first genes involved. All mutations found affect the maintenance of silencing and reactivate silent genes in trans. The mutations fall into two categories: ddm1 and hog release silencing in association with decreased levels of DNA methylation, while sil and mom reactivate genes without changing the methylation state. While plants homozygous over several generations for hog, sil or mom exhibit no morphological changes, ddm1-type mutants accumulate developmental abnormalities. The mutants indicate that TGS in plants is controlled by several genetic components and possibly by multiple independent pathways. The DDM1 gene was assigned to the SWI2/SNF2 gene family of chromatin-remodelling proteins, the MOM gene is a novel protein and the other loci have not yet been characterized.
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Amedeo, P., Habu, Y., Afsar, K., Mittelsten Scheid, O. and Paszkowski, J. 2000. Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature, in press.
Armstrong, J.A. and Emerson, B.M. 1998. Transcription of chromatin: these are complex times. Curr. Opin. Genet. Dev. 8: 165–172.
Bender, J. and Fink, G.R. 1995. Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83: 725–734.
Cubas, P., Vincent, C. and Coen, E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157–161.
Davies G.J., Sheikh, M.A., Ratcliffe, O.J., Coupland, G. and Furner I.J. 1997. Genetics of homology-dependent gene silencing in Arabidopsis: a role for methylation. Plant J. 12: 791–804.
Ehrenhofer-Murray, A.E., Kamakaka, R.T. and Rine, J. 1999. A role for the replication proteins PCNA, RF-C, Polymerase ∈ and Cdc45 in transcriptional silencing in Saccharomyces cerevisiae. Genetics 153: 1171–1182.
Ehrlich, M. and Wang, R.Y.H. 1981. 5–Methylcytosine in eucaryotic DNA. Science 212: 1350–1357.
Finnegan, E.J., Bretell, R.I.S. and Dennis, E.S. 1993. The role of DNA methylation in the regulation of plant gene expression. In: J.P. Jost and H.P. Saluz (Eds.) DNA Methylation: Molecular Biology and Biological Significance, Birkhäuser Verlag, Basel, pp. 218–261.
Finnegan, E.J., Peacock, W.J. and Dennis, E.S. 1996. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl. Acad. Sci. USA 93: 8449–8454.
Furner, I.J., Sheikh, M.A. and Collett, C.E. 1998. Gene silencing and homology-dependent gene silencing in Arabidopsis: genetic modifiers and DNA methylation. Genetics 149: 651–662.
Hirochika, H., Okamoto, H. and Kakutani, T. 2000. Silencing of retrotransposons in Arabidopsis and reactivation by ddm1 mutation. Plant Cell, 12: 357–369.
Jacobsen, S.E. and Meyerowitz, E.M. 1997. Hypermethylated superman epigenetic alleles in Arabidopsis. Science 277: 1100–1103.
Jeddeloh, J.A., Bender, J. and Richards, E.J. 1998. The DNA methylation locus DDM1 is required for maintenance of gene silencing in Arabidopsis. Genes Dev. 12: 1714–1725.
Jeddeloh, 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.
Kakutani, T. 1997. Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis thaliana. Plant J 12: 1447–1451.
Kakutani, T., Jeddeloh, J.A. and Richards, E.J. 1995. Characterization of an Arabidopsis thaliana DNA hypomethylation mutant. Nucl. Acids Res 23: 130–137.
Kakutani, T., Jeddeloh, J.A. Flowers, S.K., Munakata, K. and Richards, E.J. 1996. Developmental abnormalities and epimutations associated with DNA hypermethylation mutations. Proc. Natl. Acad. Sci. USA 93: 12406–12411.
Kakutani, T., Munakata, K., Richards, E.J. and Hirochika, H. 1999. Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics 151: 831–838.
Kilby, N.J., Leyser, H.M.O. and Furner, I.J. 1992. Promoter methylation and progressive transgene inactivation in Arabidopsis. Plant. Mol. Biol. 20: 103–112.
Kooter, J.M., Matzke, M.A. and Meyer, P. 1999. Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci. 4: 340–347.
Li, E., Bestor, T.H. and Jaenisch, R. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915–926.
Matzke, M.A., Primig, M., Trnovsky, J. and Matzke, A.J.M. 1989. Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J. 8: 643–649.
Meyerowitz, E.M. 1994. Structure and organization of the Arabidopsis thaliana nuclear genome. In: E.M. Meyerowitz and C.R. Somerville (Eds.) Arabidopsis, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 21–36.
Meyerowitz, E.M. and Somerville, C.R. (Eds.). 1994. Arabidopsis, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Mittelsten Scheid, O., Paszkowski, J. and Potrykus, I. 1991. Reversible inactivation of a transgene in Arabidopsis thaliana. Mol. Gen. Genet. 228: 104–112.
Mittelsten Scheid, O., Jakovleva, L., Afsar, K., Maluszynska Y. and Paszkowski, J. 1996. A change of ploidy can modify epigenetic silencing. Proc. Natl. Acad. Sci. USA 35: 7114–7119.
Mittelsten Scheid, O., Afsar, K. and Paszkowski, J. 1998. Release of epigenetic gene silencing by trans-acting mutations in Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 632–637.
Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N. and Bird, A. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386–389.
Ng, H.H., Zhang, Y., Hendrich, B., Johnson, C.A., Turner, B.M., Erdjument-Bromage, H., Tempst, P., Reinberg, D. and Bird A. 1999. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nature Genet. 23: 58–61.
Park, Y.D., Papp, I., Moscone, E.A., Iglesias, V.A., Vaucheret, H., Matzke, A.J. and Matzke, M.A. 1996. Gene silencing mediated by promoter homology occurs at the level of transcription and results in meiotically heritable alterations in methylation and gene activity. Plant J. 9: 183–194.
Pazin, M.J. and Kadonaga, J.T. 1997. SWI2/SNF2 and related proteins: ATP-driven motors that disrupt protein-DNA interactions? Cell 88: 737–740
Pollard, K.J. and Peterson, C.L. 1998. Chromatin remodeling: a marriage between two families? Bioessays 20: 771–780.
Ronemus, M.J., Galbiati, M., Ticknor, C., Chen, J. and Dellaporta, S.L. 1996. Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273: 654–657.
Smith, J.S., Caputo, E. and Boeke, J.D. 1999. A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol. Cell Biol. 19: 3184–3197.
Vielle-Calzada, J.P., Thomas, J., Spillane, C., Coluccio, A., Hoeppner, M.A. and Grossniklaus, U. 1999. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 13: 2971–2982.
Vongs, A., Kakutani, T., Martienssen, R.A. and Richards, E.J. 1993. Arabidopsis thaliana DNA methylation mutants. Science 260: 1926–1928.
Wade, P.A., Gegonne, A., Jones, P.L., Ballestar, E., Aubry, F. and Wolffe, A.P. 1999. Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nature Genet. 23: 62–66.
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Mittelsten Scheid, O., Paszkowski, J. Transcriptional gene silencing mutants. Plant Mol Biol 43, 235–241 (2000). https://doi.org/10.1023/A:1006487529698
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DOI: https://doi.org/10.1023/A:1006487529698