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

Abstract

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...

Endosperm and Nucellus Develop Antagonistically in Arabidopsis Seeds

“…As a positive control, we hybridized ovule sections with a HISTONE4 (HIS4) antisense probe and observed its characteristic patchy expression pattern in actively dividing cells (Figures 3J and 3K) (Blein et al, 2008). Consistent with these results, MEA and FIS2, the other FIS genes specifically expressed in the central cell (Luo et al, 2000;Wang et al, 2006), do not affect seed coat development (Roszak and Köhler, 2011). We showed that fis2/+ unfertilized ovules do not undergo nucellus degeneration at 6 DAF (Supplemental Figure 5).…”

“…All four FIS genes, MEDEA (MEA), FIS2, FERTILIZATION INDEPENDENT ENDOSPERM (FIE), and MULTICOPY SUPPRESSOR OF IRA1 (MSI1), are expressed in the ovule central cell and repress its division before fertilization Kiyosue et al, 1999;Luo et al, 1999;Ohad et al, 1999;Yadegari et al, 2000;Hennig et al, 2003;Köhler et al, 2003;Guitton et al, 2004;Wang et al, 2006). By contrast, only FIE and MSI1 are also expressed in sporophytic tissues and repress seed coat development (Ohad et al, 1999;Hennig et al, 2003;Köhler et al, 2003;Roszak and Köhler, 2011).…”

An E3 ligase complex regulates SET-domain polycomb group protein activity in Arabidopsis thaliana

“…5), suggesting that CLF competes with MEA in the formation of PRC2 complexes. This is consistent with the fact that both CLF and MEA are able to interact in vitro with the same Su(z) homologs, including FIS2, that are expressed in endosperm (18,36). So, the question arises, how is CLF and MEA function separated during endosperm development when their respective RNA expression patterns and ability to interact with PcG proteins overlap?…”

Regulation of imprinted gene expression in Arabidopsis endosperm

“…PcG proteins related to MEA (SWINGER and CURLY LEAF) and FIS2 (VERNALIZATION 2 and EM-BRYONIC FLOWER 2) are expressed in endosperm (http:// seedgenenetwork.net). These proteins can interchangeably form PRC2 complexes (36) and might provide redundant PRC2 functionality in a dme mutant background.…”