Plant Epigenetics: MEDEA's Children Take Centre Stage Dispatch (original) (raw)
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Plant epigenetics: MEDEA's children take centre stage
Current Biology, 2003
The Arabidopsis Polycomb group gene MEDEA is imprinted in early development and regulates cell proliferation in seeds. A recent study identifies the first direct target of MEDEA regulation. This is an important step towards the genetic manipulation of seed development, and should help clarify the role of Polycomb-group proteins in imprinting in plants.
Bypassing genomic imprinting allows seed development
NATURE- …, 2007
In developing progeny of mammals the two parental genomes are differentially expressed according to imprinting marks, and embryos with only a uniparental genetic contribution die 1-3 . Gene expression that is dependent on the parent of origin has also been observed in the offspring of flowering plants, and mutations in the imprinting machinery lead to embryonic lethality, primarily affecting the development of the endosperm-a structure in the seed that nourishes the embryo, analogous to the function of the mammalian placenta 4 . Here we have generated Arabidopsis thaliana seeds in which the endosperm is of uniparental, that is, maternal, origin. We demonstrate that imprinting in developing seeds can be bypassed and viable albeit smaller seedlings can develop from seeds lacking a paternal contribution to the endosperm. Bypassing is only possible if the mother is mutant for any of the FIS-class genes, which encode Polycomb group chromatinmodifying factors. Thus, these data provide functional evidence that the action of the FIS complex balances the contribution of the paternal genome. As flowering plants have evolved a special reproduction system with a parallel fusion of two female with two male gametes, our findings support the hypothesis that only with the evolution of double fertilization did the action of the FIS genes become a requirement for seed development. Furthermore, our data argue for a gametophytic origin of endosperm in flowering plants, thereby supporting a hypothesis raised in 1900 by Eduard Strasburger.
Cell, 2002
et al., 1999). Thus, double fertilization generates a seed with a triploid endosperm and diploid embryo. The embryo generates organs (axis and cotyledon), tissues (protoderm, procambium, and ground meristem), and meristems (shoot and root). The fertilized central cell mediates the transfer of nutrients from maternal tissues to be absorbed by the embryo (Brown et al., 1999). Biology University of California, Los Angeles To gain insights into the maternal control of embryo and endosperm development, mutations in a small num-Los Angeles, California 90095 3 Section of Plant Biology ber of genes have been identified where seed viability depends upon the genotype of the maternal allele. For Division of Biological Sciences University of California, Davis example, these studies have shown that the female gametophyte provides the embryo with an MCM-related Davis, California 95616 4 Molecular Biology Institute protein, PROLIFERA (PRL), necessary for cytokinesis (Springer and Holding, 2002). Also, wild-type maternal University of California, Los Angeles Los Angeles, California 90095 alleles encoding Polycomb group proteins are necessary for proper female gametophyte and seed development. MEDEA (MEA), FERTILIZATION INDEPENDENT ENDOSPERM (FIE), and FERTILIZATION INDEPEN-Summary DENT SEED2 (FIS2) encode SET-domain, WD domain, and zinc finger Polycomb group proteins (Grossniklaus We isolated mutations in Arabidopsis to understand et al., 1998; Kiyosue et al., 1999; Luo et al., 1999; Ohad how the female gametophyte controls embryo and enet al., 1999; Birve et al., 2001). Polycomb group proteins dosperm development. For the DEMETER (DME) gene, repress gene transcription by forming complexes that seed viability depends only on the maternal allele. DME remodel chromatin structure at specific regions within encodes a large protein with DNA glycosylase and nuclear localization domains. DME is expressed pri-the genome (Francis and Kingston, 2001). One function marily in the central cell of the female gametophyte, of MEA, FIE, and FIS2 is to prevent the onset of central the progenitor of the endosperm. DME is required for cell proliferation and endosperm development prior to maternal allele expression of the imprinted MEDEA fertilization and to repress endosperm growth and devel-(MEA) Polycomb gene in the central cell and endoopment after fertilization (Kiyosue et al., 1999; Vinkesperm. Ectopic DME expression in endosperm actinoog et al., 2000). Thus, to date, no genes have been vates expression of the normally silenced paternal discovered that function primarily prior to fertilization in MEA allele. In leaf, ectopic DME expression induces the female gametophyte to control processes essential MEA and nicks the MEA promoter. Thus, a DNA glycofor subsequent embryo and endosperm development sylase activates maternal expression of an imprinted after fertilization. gene in the central cell. Because only the maternal allele is required for seed viability, loss-of-function mea, fie, fis2, and prl mutations Jiricny, J. (2002). An APE that proofreads. Nature 415, 593-594. Mutations in the FIE and MEA genes that encode interacting poly-M., and Jost, Y.-C. (2001). 5-methylcytosine DNA glycosylase particcomb proteins cause parent-of-origin effects on seed development ipates in the genome-wide loss of DNA methylation occurring during by distinct mechanisms. Plant Cell 12, 2367-2381. mouse myoblast differentiation. Nucleic Acids Res 29, 4452-4461. Kakutani, T., Jeddeloh, J.A., Flowers, S.K., Munakata, K., and Rich-Accession Numbers ards, E.J. (1996). Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc. Natl. Acad. The DME cDNA sequence has been deposited in GenBank as acces-Sci. USA 93, 12406-12411. sion number AF521596. Kasinsky, H.E., Lewis, J.D., Dacks, J.B., and Ausio, J. (2001). Origin of H1 linker histones. FASEB J. 15, 34-42.
Plant Journal, 2017
Endosperm cellularization is essential for embryo development and viable seed formation. Loss of function of the FERTILIZATION INDEPENDENT SEED (FIS) class Polycomb genes, which mediate trimethylation of histone H3 lysine27 (H3K27me3), as well as imbalanced contributions of parental genomes interrupt this process. The causes of the failure of cellularization are poorly understood. In this study we identified PICKLE RELATED 2 (PKR2) mutations which suppress seed abortion in fis1/mea by restoring endosperm cellularization. PKR2, a paternally expressed imprinted gene (PEG), encodes a CHD3 chromatin remodeler. PKR2 is specifically expressed in syncytial endosperm and its maternal copy is repressed by FIS1. Seed abortion in a paternal genome excess interploidy cross was also partly suppressed by pkr2. Simultaneous mutations in PKR2 and another PEG, ADMETOS (ADM), additively rescue the seed abortion in fis1 and in the interploidy cross, suggesting that PKR2 and ADM modulate endosperm cellularization independently and reproductive isolation between plants of different ploidy is established by imprinted genes. Genes upregulated in fis1 and downregulated in the presence of pkr2 are enriched in glycosyl-hydrolyzing activity, while genes downregulated in fis1 and upregulated in the presence of pkr2 are enriched with microtubule motor activity, consistent with the cellularization patterns in fis1 and the suppressor line. The antagonistic functions of FIS1 and PKR2 in modulating endosperm development are similar to those of PICKLE (PKL) and CURLY LEAF (CLF), which antagonistically regulate root meristem activity. Our results provide further insights into the function of imprinted genes in endosperm development and reproductive isolation.
Genomic Imprinting and Endosperm Development in Flowering Plants
Molecular Biotechnology, 2003
Genomic imprinting, the parent-of-origin-specific expression of genes, plays an important role in the seed development of flowering plants. As different sets of genes are imprinted and hence silenced in maternal and paternal gametophyte genomes, the contributions of the parental genomes to the offspring are not equal. Imbalance between paternally and maternally imprinted genes, for instance as a result of interploidy crosses, or in seeds in which imprinting has been manipulated, results in aberrant seed development. It is predominantly the endosperm, and not or to a far lesser extent the embryo, that is affected by such imbalance. Deviation from the normal 2m:1p ratio in the endosperm genome has a severe effect on endosperm development, and often leads to seed abortion. Molecular expression data for imprinted genes suggest that genomic imprinting takes place only in the endosperm of the developing seed. Although far from complete, a picture of how imprinting operates in flowering plants has begun to emerge. Imprinted genes on either the maternal or paternal side are marked and silenced in a process involving DNA methylation and chromatin condensation. In addition, on the maternal side, imprinted genes are most probably under control of the polycomb FIS genes.
The Plant Cell, 2000
In flowering plants, two cells are fertilized in the haploid female gametophyte. Egg and sperm nuclei fuse to form the embryo. A second sperm nucleus fuses with the central cell nucleus, which replicates to generate the endosperm, a tissue that supports embryo development. The FERTILIZATION-INDEPENDENT ENDOSPERM (FIE) and MEDEA (MEA) genes encode WD and SET domain polycomb proteins, respectively. In the absence of fertilization, a female gametophyte with a loss-of-function fie or mea allele initiates endosperm development without fertilization. fie and mea mutations also cause parent-of-origin effects, in which the wild-type maternal allele is essential and the paternal allele is dispensable for seed viability. Here, we show that FIE and MEA polycomb proteins interact physically, suggesting that the molecular partnership of WD and SET domain polycomb proteins has been conserved during the evolution of flowering plants. The overlapping expression patterns of FIE and MEA are consistent with their suppression of gene transcription and endosperm development in the central cell as well as their control of seed development after fertilization. Although FIE and MEA interact, differences in maternal versus paternal patterns of expression, as well as the effect of a recessive mutation in the DECREASE IN DNA METHYLATION1 (DDM1) gene on mutant allele transmission, indicate that fie and mea mutations cause parent-of-origin effects on seed development by distinct mechanisms.
Maternal control of seed development
Seminars in Cell & Developmental Biology, 2001
Maternal control of higher plant seed development is likely to involve female sporophytic as well as female gametophytic genes. While numerous female sporophytic mutants control the production of the ovule and the embryo sac true maternal effect mutations affecting embryo and endosperm development are rare in plants. A new class of female gametophytic mutants has been isolated that controls autonomous development of endosperm. Molecular analyses of these genes, known as FIS class genes, suggest that they repress downstream seed development genes by chromatin remodelling. Expression of the FIS genes in turn is modulated by parent specific expression or genomic imprinting which in turn is controlled by DNA methylation. Thus maternal control of seed development is a complex developmental event influenced by both genetic and epigenetic processes.
The Plant Cell, 2000
In flowering plants, two cells are fertilized in the haploid female gametophyte. Egg and sperm nuclei fuse to form the embryo. A second sperm nucleus fuses with the central cell nucleus, which replicates to generate the endosperm, a tissue that supports embryo development. The FERTILIZATION-INDEPENDENT ENDOSPERM (FIE) and MEDEA (MEA) genes encode WD and SET domain polycomb proteins, respectively. In the absence of fertilization, a female gametophyte with a loss-of-function fie or mea allele initiates endosperm development without fertilization. fie and mea mutations also cause parent-of-origin effects, in which the wild-type maternal allele is essential and the paternal allele is dispensable for seed viability. Here, we show that FIE and MEA polycomb proteins interact physically, suggesting that the molecular partnership of WD and SET domain polycomb proteins has been conserved during the evolution of flowering plants. The overlapping expression patterns of FIE and MEA are consistent with their suppression of gene transcription and endosperm development in the central cell as well as their control of seed development after fertilization. Although FIE and MEA interact, differences in maternal versus paternal patterns of expression, as well as the effect of a recessive mutation in the DECREASE IN DNA METHYLATION1 (DDM1) gene on mutant allele transmission, indicate that fie and mea mutations cause parent-of-origin effects on seed development by distinct mechanisms.