Imprinting of the MEA Polycomb Gene Is Controlled by Antagonism between MET1 Methyltransferase and DME Glycosylase

Xiao, Wenyan; Gehring, Mary; Choi, Yeonhee; Margossian, Linda; Pu, Hong; Harada, John J.; Goldberg, Robert B.; Pennell, Roger I.; Fischer, Robert L.

doi:10.1016/s1534-5807(03)00361-7

Cited by 203 publications

(191 citation statements)

References 46 publications

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“…2 K-T). Recent data indicate that various transcriptional-regulatory mechanisms, including PcG-mediated mechanisms, contribute to establishing this pattern of expression (35)(36)(37)(38)(39). In contrast, SWN is localized in the nucleus at all stages of development except in pollen grains and during endosperm development (Figs.…”

Section: Discussionmentioning

confidence: 99%

Partially redundant functions of two SET-domain polycomb-group proteins in controlling initiation of seed development in Arabidopsis

Wang

Tyson

Jackson

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

125

107

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In Arabidopsis, a complex of Polycomb-group (PcG) proteins functions in the female gametophyte to control the initiation of seed development. Mutations in the PcG genes, including MEDEA (MEA) and FERTILIZATION-INDEPENDENT SEED 2 (FIS2), produce autonomous seeds where endosperm proliferation occurs in the absence of fertilization. By using a yeast two-hybrid screen, we identified MEA and a related protein, SWINGER (SWN), as SET-domain partners of FIS2. Localization data indicated that all three proteins are present in the female gametophyte. Although single-mutant swn plants did not show any defects, swn mutations enhanced the mea mutant phenotype in producing autonomous seeds. Thus, MEA and SWN perform partially redundant functions in controlling the initiation of endosperm development before fertilization in Arabidopsis.chromatin ͉ endosperm ͉ female gametophyte ͉ fertilization ͉ gene silencing I n angiosperms, seed development is initiated by a doublefertilization event within the female gametophyte (FG). The pollen tube delivers two sperm cells that fuse with the haploid egg cell and the typically homodiploid central cell to initiate the development of two distinct organs, an embryo and an endosperm, respectively (1). The diploid embryo forms the next generation, whereas the typically triploid endosperm is a shortlived nutritive tissue that supports embryogenesis or seedling development. In most angiosperms, including Arabidopsis, the endosperm undergoes a nuclear-type development that includes an initial period of coenocytic development in which the primary endosperm nucleus undergoes mitosis without cytokinesis followed by cellularization. In Arabidopsis, the cellularized endosperm is gradually absorbed by the developing embryo, and only an aleurone layer remains at seed maturity (2, 3).Recent evidence indicates that the FG controls the initiation of seed development in Arabidopsis. Mutations in genes encoding the Polycomb-group (PcG) proteins FERTILIZATION-INDEPENDENT ENDOSPERM (FIE), MEDEA (MEA), FERTILIZATION-INDEPENDENT SEED 2 (FIS2), and the Arabidopsis homologue of MULTICOPY SUPPRESSOR OF IRA 1 (MSI1) cause the development of autonomous seeds in the absence of fertilization due mainly to proliferation of the diploid central cell nucleus. Molecular and genetic evidence indicates that these proteins are expressed in the FG and function to repress downstream genes required for normal endosperm proliferation before fertilization (4-11). The FIE, MEA, FIS2, and MSI1 genes encode proteins that are highly similar to components of the Polycomb repressive complex 2͞3 (PRC2͞3) that include the Drosophila Esc, E(z), Su(z)12, and p55 and the mammalian EED, EZH2, SUZ12, and RbAp48͞46, respectively (12). PRC2͞3 and the larger PRC1 complex function to silence and maintain epigenetic silencing of target genes involved in regulation of early development, cell growth, and proliferation. At least part of the gene-silencing function of PRC2͞3 is likely mediated through its intrinsic histone H3 methylation activity (13, 1...

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Section: Discussionmentioning

confidence: 99%

Partially redundant functions of two SET-domain polycomb-group proteins in controlling initiation of seed development in Arabidopsis

Wang

Tyson

Jackson

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

125

107

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“…Growth conditions are as described in ref. 16. PCR was used to genotype plants, and the PCR conditions are in SI Methods.…”

Section: Methodsmentioning

confidence: 99%

“…Three targets of DME are MEDEA (MEA), FWA, and FIS2. In vegetative tissue, the default state for these genes is methylated (14)(15)(16). However, in the reproductive central cell, DME excises 5-methylcytosine at MEA and presumably FWA and FIS2, establishing hypomethylated, transcriptionally active alleles of these genes (9, 10, 14, 15).…”

mentioning

confidence: 99%

DNA demethylation in the Arabidopsis genome

Penterman

Zilberman

Huh

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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459

470

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Cytosine DNA methylation is considered to be a stable epigenetic mark, but active demethylation has been observed in both plants and animals. In Arabidopsis thaliana, DNA glycosylases of the DEMETER (DME) family remove methylcytosines from DNA. Demethylation by DME is necessary for genomic imprinting, and demethylation by a related protein, REPRESSOR OF SILENCING1, prevents gene silencing in a transgenic background. However, the extent and function of demethylation by DEMETER-LIKE (DML) proteins in WT plants is not known. Using genome-tiling microarrays, we mapped DNA methylation in mutant and WT plants and identified 179 loci actively demethylated by DML enzymes. Mutations in DML genes lead to locus-specific DNA hypermethylation. Reintroducing WT DML genes restores most loci to the normal pattern of methylation, although at some loci, hypermethylated epialleles persist. Of loci demethylated by DML enzymes, >80% are near or overlap genes. Genic demethylation by DML enzymes primarily occurs at the 5 and 3 ends, a pattern opposite to the overall distribution of WT DNA methylation. Our results show that demethylation by DML DNA glycosylases edits the patterns of DNA methylation within the Arabidopsis genome to protect genes from potentially deleterious methylation. DNA glycosylase ͉ epigenetics ͉ genome maintenanceA rabidopsis is a eukaryotic model for DNA methylation studies. In Arabidopsis cytosine methylation is found in all sequence contexts (CG, CNG, and CNN) and is important for genomic imprinting and genome defense against transposable elements (1). Most DNA methylation is located at transposonrich heterochromatic regions (2-4). However, genome-wide mapping of methylation has showed that a significant fraction (20-33%) of genes are methylated (3-5). In general, methylation within Arabidopsis genes is concentrated in the middle and distributed away from 5Ј and 3Ј ends, suggesting that 5Ј and 3Ј methylation is detrimental to gene function (3, 4). The mechanisms that maintain gene ends relatively free of methylation are not known.DNA methylation is often considered a stable epigenetic mark, but enzymatic DNA demethylation is known to occur. In mammals, the paternal pronucleus is actively demethylated immediately after fertilization (6, 7) but the enzymes responsible are unknown (8). In Arabidopsis, DNA demethylation is mediated by the DEMETER (DME) family of bifunctional helixhairpin-helix DNA glycosylases that have both DNA glycosylase and apurinic/apyrimidinic (AP) lyase activities (9-13). The DNA glycosylase initiates the base excision repair process by specifically excising 5-methylcytosine through cleavage of the N-glycosylic bond. AP lyase subsequently nicks the DNA, and an AP endonuclease generates a 3Ј-hydroxyl to which a DNA repair polymerase adds an unmethylated cytosine. DNA ligase completes the repair process by sealing the nick.Demethylation by DME is one step in a developmental pathway that establishes genomic imprinting in the Arabidopsis endosperm (9,10,14). Three targets of DME are MEDEA (MEA),...

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“…PcG proteins act in complexes that apply H3K27me3 on their target genes, causing gene repression by not well understood mechanisms . Although activity of the maternal MEA allele depends on DME-mediated DNA demethylation (Choi et al, 2002;Xiao et al, 2003), the DNA methylation status of the paternal MEA allele seems to be irrelevant for its expression (Gehring et al, 2006). Rather, repression of the paternal MEA allele requires the activity of the FERTI-LIZATION INDEPENDENT SEED (FIS) PcG complex with MEA itself being a subunit of this complex (Baroux et al, 2006;Gehring et al, 2006;Jullien et al, 2006b).…”

Section: Imprinting Mechanismsmentioning

confidence: 99%