Mutations in the FIE and MEA Genes That Encode Interacting Polycomb Proteins Cause Parent-of-Origin Effects on Seed Development by Distinct Mechanisms (original) (raw)
Related papers
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. Zhang, Y., LeRoy, G., Seelig, H.-P., Lane, W.S., and Reinberg, D.
Plant Epigenetics: MEDEA's Children Take Centre Stage Dispatch
2000
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.
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.
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.
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.
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.
Genes controlling fertilization-independent seed development in Arabidopsis thaliana
Proceedings of the National Academy of Sciences, 1999
We have cloned two genes, FIS1 and FIS2 , that control both fertilization independent seed development and postpollination embryo development in Arabidopsis . These genes confer female gametophytic phenotypes. FIS2 encodes a protein with a C 2 H 2 zinc-finger motif and three putative nuclear localization signals, indicating that it is likely to be a transcription factor. FIS1 encodes a protein with homology to the Drosophila Polycomb group gene Enhancer-of-zeste and is identical to the recently described Arabidopsis gene MEDEA . FIS1 is a protein with a number of putative functional domains, including the SET domain present in Enhancer-of-zeste-related proteins. Comparison of the position of the lesions in the fis1 and medea mutant alleles indicates that fis1 is a null allele producing a truncated polypeptide lacking all the protein domains whereas the deduced protein from medea lacks only the SET domain. We present a model of the role of FIS1 and FIS2 gene products in seed developm...
DNA Methylation Causes Predominant Maternal Controls of Plant Embryo Growth
PLoS ONE, 2008
The parental conflict hypothesis predicts that the mother inhibits embryo growth counteracting growth enhancement by the father. In plants the DNA methyltransferase MET1 is a central regulator of parentally imprinted genes that affect seed growth. However the relation between the role of MET1 in imprinting and its control of seed size has remained unclear. Here we combine cytological, genetic and statistical analyses to study the effect of MET1 on seed growth. We show that the loss of MET1 during male gametogenesis causes a reduction of seed size, presumably linked to silencing of the paternal allele of growth enhancers in the endosperm, which nurtures the embryo. However, we find no evidence for a similar role of MET1 during female gametogenesis. Rather, the reduction of MET1 dosage in the maternal somatic tissues causes seed size increase. MET1 inhibits seed growth by restricting cell division and elongation in the maternal integuments that surround the seed. Our data demonstrate new controls of seed growth linked to the mode of reproduction typical of flowering plants. We conclude that the regulation of embryo growth by MET1 results from a combination of predominant maternal controls, and that DNA methylation maintained by MET1 does not orchestrate a parental conflict.
Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation
Development, 2000
Some genes in mammals and flowering plants are subject to parental imprinting, a process by which differential epigenetic marks are imposed on male and female gametes so that one set of alleles is silenced on chromosomes contributed by the mother while another is silenced on paternal chromosomes. Therefore, each genome contributes a different set of active alleles to the offspring, which develop abnormally if the parental genome balance is disturbed. In Arabidopsis, seeds inheriting extra maternal genomes show distinctive phenotypes such as low weight and inhibition of mitosis in the endosperm, while extra paternal genomes result in reciprocal phenotypes such as high weight and endosperm overproliferation. DNA methylation is known to be an essential component of the parental imprinting mechanism in mammals, but there is less evidence for this in plants. For the present study, seed development was examined in crosses using a transgenic Arabidopsis line with reduced DNA methylation. C...