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Temporal and Spatial Downregulation of Arabidopsis MET1 Activity Results in Global DNA Hypomethylation and Developmental Defects  

Kim, Minhee (Department of Biological Sciences, Seoul National University)
Ohr, Hyonhwa (Department of Biological Sciences, Seoul National University)
Lee, Jee Woong (Department of Biological Sciences, Seoul National University)
Hyun, Youbong (Department of Biological Sciences, Seoul National University)
Fischer, Robert L. (Department of Plant and Microbial Biology, University of California at Berkeley)
Choi, Yeonhee (Department of Biological Sciences, Seoul National University)
Publication Information
Molecules and Cells / v.26, no.6, 2008 , pp. 611-615 More about this Journal
Abstract
DNA methylation is an epigenetic mechanism for gene silencing. In Arabidopsis, MET1 is the primary DNA methyltransferase that maintains CG DNA methylation. Plants having an overall reduction of MET1 activity, caused by a met1 mutation or a constitutively expressed MET1 antisense gene, display genome hypomethylation, inappropriate gene and transposon transcription, and developmental abnormalities. However, the effect of a transient reduction in MET1 activity caused by inhibiting MET1 expression in a restricted set of cells is not known. For this reason, we generated transgenic plants with a MET1 antisense gene fused to the DEMETER (DME) promoter (DME:MET1 a/s). Here we show that DME is expressed in leaf primordia, lateral root primoridia, in the region distal to the primary root apical meristem, which are regions that include proliferating cells. Endogenous MET1 expression was normal in organs where the DME:MET1 a/s was not expressed. Although DME promoter is active only in a small set of cells, these plants displayed global developmental abnormalities. Moreover, centromeric repeats were hypomethylated. The developmental defects were accumulated by the generations. Thus, not maintaining CG methylation in a small population of proliferating cells flanking the meristems causes global developmental and epigenetic abnormalities that cannot be rescued by restoring MET1 activity. These results suggest that during plant development there is little or no short-term molecular memory for reestablishing certain patterns of CG methylation that are maintained by MET1. Thus, continuous MET1 activity in dividing cells is essential for proper patterns of CG DNA methylation and development.
Keywords
DEMETER; DNA methylation; FWA; METHYLTRANSERASE1; transposon;
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1 Cokus, S.J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, CD., Pradhan, S., Nelson, S.F., Pellegrini, M., and Jacobsen, S.E. (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452,215-219   DOI   ScienceOn
2 Doerner, P., Jorgensen, J.E., You, R., Steppuhn, J., and Lamb, C. (1996). Control of root growth and development by cyclin expression. Nature 380, 520-523   DOI   ScienceOn
3 Jullien, PE., Kinoshita, T., Ohad, N., and Berger, F. (2006). Maintenance of DNA methylation during the Arabidopsis life cycle Is essential for parental imprinting. Plant Cell 18, 1360-1372   DOI   ScienceOn
4 Kinoshita, T., Miura, A, Choi, Y., Kinoshita, Y., Cao, X., Jacobsen, S.E., Fischer, R.L., and Kakutani, T. (2004). One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303, 521-523   DOI   ScienceOn
5 Morales-Ruiz, T., Ortega-Galisteo, AP., Ponferrada-Marin, M.I., Martinez-Macias, R.R., Ariza, R.R., and Roldan-Arjona, T. (2006). DEMETER and REPRESSOR OF SILENCING1 encode 5methylcytosine DNA glycosylases. Proc. Natl. Acad. Sci. USA 103, 6853-6858
6 Ortega-Galisteo, AP., Morales-Ruiz, T., Ariza, R.R., and RoldanAriona, T. (2008). Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks. Plant Mol. BioI. 67, 671-681   DOI
7 Penterman, J., Zilberman, D., Huh, J.H., Ballinger, T., Henikoff, S., and Fischer, R.L. (2007). DNA demethylation in the Arabidopsis genome. Proc. Natl. Acad. Sci. USA 104,6752-6757
8 Scott, R.J., and Spielman, M. (2006). Genomic imprinting in plants and mammals: how life history constrains convergence. Cytogenet Genome Res. 113,53-67   DOI   ScienceOn
9 Sutherland, D., Coe, L., and Raleigh, E.A. (1992). McrBC: A Multisubunit GTP-dependent restriction endonuclease. J. Mol. BioI. 225, 327-348   DOI
10 Yadegari, R., Kinoshita, T., Lotan, 0., Cohen, G., Katz, A, Choi, Y., Katz, A, Nakashima, K., Harada, J.J., Goldberg, R.B., et al. (2000). Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms. Plant Cell 12, 2367-2381   DOI
11 Zilberman, D., Gehring, M., Tran, RK, Ballinger, T., and Henikoff, S. (2007). Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39, 61-69   DOI   ScienceOn
12 Henderson, I.R., and Jacobsen, SE. (2007). Epigenetic inheritance in plants. Nature 447, 418-424   DOI   ScienceOn
13 Lister, R., O'Malley, R.C., Tonti-Filippini, J., Gregory, an, Berry, C.C., Millar, AH., and Ecker, J.R. (2008). Highly integrated Single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523-536   DOI   ScienceOn
14 Ronemus, M.J., Galbiati, M., Ticknor, C., Chen, J., and Dellaporta, S.L. (1996). Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273, 654-657   DOI   ScienceOn
15 Lippman, Z., May, B., Yordan, C., Singer, T., and Martienssen, R. (2003). Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS BioI. 1, E67   DOI
16 Saze, H., SCheid, O.M., and Paszkowski, J. (2003). Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat. Genet. 34, 65-69   DOI   ScienceOn
17 Bender, J. (2004). DNA Methylation and Epigenetics. Annu. Rev. Plant BioI. 55, 41-68   DOI   ScienceOn
18 Xiao, w., Gehring, M., Choi, Y., Margossian, L., Pu, H., Harada, J.J., Goldberg, R.B., Pennell, R.I., and Fischer, R.L. (2003). Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev. Cell 5, 891-901   DOI   ScienceOn
19 Barkoulas, M., Galinha, C., Grigg, S.P., and Tsiantis, M. (2007). From genes to shape: regulatory interactions in leaf development. Curro Opin. Plant BioI. 10, 660-666   DOI   ScienceOn
20 Ferreira, P.C., Hemerly, A.S., Engler, JD., van Montagu, M., Engler, G., and Inze, D. (1994). Developmental expression of the arabidopsis cyclin gene cyc1At. Plant Cell 6, 1763-1774   DOI
21 Matzke, M.A., and Birchler, J.A. (2005). RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6, 24-35   DOI   ScienceOn
22 Chan, S.w., Henderson, I.R., and Jacobsen, S.E. (2005). Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat. Rev. Genet. 6,351-360   DOI   ScienceOn
23 Gehring, M., Huh, J.H., Hsieh, T.F., Penterman, J., Choi, Y., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (2006). DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124, 495-506   DOI   ScienceOn
24 Kankel, M.W., Ramsey, DE., Stokes, T.L., Flowers, SK, Haag, J.R., Jeddeloh, J.A., Riddle, N.C., Verbsky, M.L., and Richards, E.J. (2003). Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163, 1109-1122
25 Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J.J., Goldberg, R.B., Jacobsen, S.E., and Fischer, R.L. (2002). DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110,33-42   DOI   ScienceOn
26 Finnegan, E.J., Peacock, w.J., and Dennis, E.S. (1996). Reduced DNA methylation in Arabidopsis results in abnormal plant development. Proc. Natl. Acad. Sci. USA 93, 8449-8454
27 Rabinowicz, p.o., Palmer, L.E., May, B.P., Hemann, M.T., Lowe, SW., McCombie, W.R., and Martienssen, R.A. (2003). Genes and transposons are differentially methylated in plants, but not in mammals. Genome Res. 13,2658-2664   DOI   ScienceOn
28 Zhu, J.Q., Liu, J.H., Liang, X.w., Xu, B.Z., Hou, Y., Zhao, XX, and Sun, Q.Y. (2008). Heat stress causes aberrant DNA methylation of H19 and Igf-2r in mouse blastocysts. Mol. Cells 25, 211-215