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19 Genetic and epigenetic processes in seed development Allan R Lohe* and Abed Chaudhury† Seed development has emerged as an important area of research in plant development. Recent research has highlighted the divergent reproductive strategies of the male and female genomes and interaction between genetic and epigenetic control mechanisms. Isolation of genes involved in embryo and endosperm development is leading to an understanding of the regulation of these processes at the molecular level. A thorough grasp of these processes will not only illuminate an important area of plant development but will also have an impact on agronomy by helping to facilitate food production. An understanding of seed development is also likely to clarify the molecular mechanisms of apomixis, a fascinating process of asexual seed production present in many plants. Addresses CSIRO Division of Plant Industry, PO Box 1600, Canberra, ACT 2601, Australia *e-mail: [email protected] † e-mail: [email protected] Current Opinion in Plant Biology 2002, 5:19–25 1369-5266/02/$ — see front matter © 2002 Elsevier Science Ltd. All rights reserved. Abbreviations AMP1 ALTERED MERISTEM PROGRAMMING1 ESC EXTRA SEX COMBS E(Z) ENHANCER OF ZESTE FIE FERTILIZATION INDEPENDENT ENDOSPERM FIS FERTILIZATION INDEPENDENT SEED MET1 METHYL TRANSFERASE1 MOM1 MORPHEUS’ MOLECULE1 PcG Polycomb group TTN TITAN YFP yellow fluorescent protein Introduction Seed development is central to the reproductive strategy of angiosperms. It is triggered by the process of double fertilization: the haploid egg is fertilized by one sperm cell and a homodiploid central cell of the ovule is fertilized by another sperm cell, leading to the formation of diploid embryo and triploid endosperm. Synchronized development of the embryo and the endosperm occurs inside the maternal ovule tissues, which are surrounded by inner and outer integuments. Thus, the interplay of different genome dosages encompassing the haploid and diploid generations participate in the ontogeny of seed. Among angiosperms, seed development in monocots and eudicots has important differences and similarities. Although both types of seed are produced by double fertilization, the relative development of embryo and endosperm is different in the two groups. In eudicots, the majority of the seed bulk is made up of embryo, whereas in monocots (such as rice and wheat), endosperm tissue constitutes the bulk of the grain. Although conventional Mendelian genetics held that the paternal and maternal genomes contribute equally to the zygote resulting from sexual reproduction, that view has been altered recently. Significant new results challenging this view have come from work on seed development. These results suggest that the paternal genome is probably less important in defining the early stages of seed development and that a number of genes show a parent-of-origin effect in their mode of action. The events of early seed development are modulated by epigenetic processes, such as DNA methylation and chromatin remodeling, that act on a large number of genes. The complex interplay of maternal and paternal genomes, involving genetic and epigenetic processes, makes seed development an exciting area of study. This complexity is also central to our understanding of an agronomically challenging branch of seed development: apomixis, this is, reproduction without fertilization. Although most plants use paternal and maternal genomes to produce a diploid organism sexually, in apomictic plants, functional seeds are produced without a female haploid reduction phase and without any contribution of the paternal parent. The key processes that trigger gametophytic apomixis are, first, an alteration of the female meiotic program that produces an unreduced embryo sac; second, the ability of the unreduced egg to develop parthenogenetically to produce a completely maternal diploid embryo; and, sometimes third, autonomous development of the endosperm to nourish the embryo. Thus, apomixis involves important alterations in the reproductive strategies of genes that control normal reproductive development. Knowledge gained from recent exciting research in seed development is likely to help the engineering of apomixis in agronomically important crop plants. Double fertilization Double fertilization constitutes two important events that initiate the process of seed development. Upon pollen maturation, two sperm cells are delivered via the pollen tube into the embryo sac. It has been suggested that sperm cells are taken to the embryo sac with the help of a cytoskeletal system [1]. One of the sperm cells then fuses with the egg cell and the other with the central cell, thereby initiating embryo and endosperm development (Figure 1). Whether an individual sperm cell is programmed to fertilize either the egg cell or the central cell is an issue that has not yet been resolved. Recent work suggests that sperm cell dimorphism exists in several species [2]. Similarly, a lot of new information regarding the early events of fertilization has been obtained from studies with isolated sperm cells and female gametes. The first detectable cellular event that 20 Growth and development Figure 1 A developing seed with embryo at the heart stage. clz, chalazal end of the embryo sac; em, embryo; en, endosperm; f, funiculus; mi, micropylar end of the embryo sac; s, suspensor. en em clz s mi f Current Opinion in Plant Biology takes place after gamete fusion is an increase in the concentration of cytosolic Ca2+, caused by an influx of cytosolic Ca2+. It is not clear, however, if this Ca2+ elevation is sufficient to trigger egg activation and the initiation of fertilization [3]. Embryo development Once the egg is fertilized, the unicellular zygote makes a progressive transition to become the embryo. The main body of the embryo that is elaborated includes the apical meristem, hypocotyl, cotyledons, root and shoot meristems, and a radial pattern including the epidermis and layers of conductive and vasculature tissues [4]. Mutational dissection has illuminated some of the early events of embryogenesis. Many genes affecting embryogenesis have been isolated, including LEAFY COTYLEDON2 (LEC2) [5], GNOM [6], SHOOT MERISTEMLESS (STM) [7], MONOPTEROS [8] and FACKEL [9]. LEC2 is likely to be a transcriptional regulator that provides the correct cellular environment for the initiation of embryo development. The first division of the embryo following fertilization is asymmetric and produces an apical and a basal cell. The smaller apical cell produces the bulk of the embryo and the larger basal cell forms part of the root and the suspensor. Among the pattern-formation mutants, only those that have mutations in GNOM/EMB30 have defective apical–basal polarity; the first division in these mutants appears to be symmetrical. GNOM encodes a guanine nucleotide exchange factor (GEF) that acts on an ADP ribosylation factor (ARF)-type G protein [6]. In contrast with mutations in GNOM/EMB30, a mutation in the FACKEL gene specifically reduces the hypocotyl, causing an embryo in which the roots seem to be attached to the cotyledons. The FACKEL gene product is a sterol reductase that is involved in lipid biosynthesis [9]. Another mutant, schlepperless, defines the gene that codes for a Chaperonin 60 alpha; the mutant phenotype indicates a role for this gene during proper seed development [10]. During the transition from the globular to the heart stage of embryo development, the cotyledon fate and number are elaborated giving rise to two cotyledons in the dicot embryo. In plants with mutations in the ALTERED MERISTEM PROGRAMMING1 (AMP1) gene, the cotyledon number is variable with up to 30% of the seedlings containing non-dicot seedlings. The mutant was found to have an elevated level of cytokinin and a number of other phenotypes, including partially de-etiolated growth, precocious flowering and an elevated level of cyclin D3. The AMP1 gene has recently been cloned [11•]. By homology, the gene is a putative glutamate carboxypeptidase. This result suggests that the product of the AMP1 gene modulates the level of a signaling molecule that acts to regulate a number of aspects of plant development. That signaling molecule could be an as yet unidentified small signal peptide. The altered cotyledon number and occasional formation of multiple embryos in the seeds of amp1 mutants suggest that AMP1 plays a critical role during pattern formation in plant embryogenesis. Genetic and epigenetic processes in seed development Lohe and Chaudhury Development of the endosperm Proper development of the endosperm is essential for growth of the embryo and the production of viable seed. The endosperm derives from a single precursor cell, the homodiploid central cell, which is the product of the fusion of the two haploid polar nuclei. After fertilization, the central cell nucleus continues to divide without cytokinesis, forming a syncytium. The diploid embryo and the triploid endosperm nuclei develop in unison, with each appearing to be dependent on the other for correct developmental progression. Unlike the embryo, which progresses through several morphologically distinct stages as it develops from a fertilized egg cell, the endosperm nuclei form a syncytium without readily identifiable features. With the exception of nuclei at the chalazal (posterior) pole, cellularization of the endosperm has occurred by the time the embryo reaches the heart stage [12]. Endosperm polarity The embryo sac forms within the ovule and is the product of the meiosis of the megaspore mother cell, from which a single cell of four survives. This cell undergoes three mitotic divisions to form a seven-celled, eight-nucleus embryo sac (the central cell contains two polar nuclei) (see [13] for review). The positions of the haploid nuclei within the embryo sac are highly ordered, possibly to facilitate the double fertilization event and subsequent development. These positions may also provide the initial cues for the development of endosperm polarity. The cellularized endosperm has a substructure consisting of different types of tissue. Analysis of a histone 2B::YFP (yellow fluorescent protein) gene fusion during early seed development showed that the syncytium is organized into three distinct mitotic domains along the anterior–posterior axis [14•]. The domains are characterized by synchronously dividing nuclei whose mitotic activity is independent of the mitotic activity in other domains. From the intensity of labeling, it was suggested that nuclei in the chalazal domain undergo endoreduplication, in contrast to the other nuclei in the endosperm. Mutations in any of the three FERTILIZATION INDEPENDENT SEED (FIS) genes (see next section) disrupt endosperm polarization as well as proliferation of endosperm nuclei [15•]. Mutational analyses are being supplemented with molecular genetics to assist in the identification of genes that are active in the endosperm and therefore in seed germination. Screening of more than 10 000 Arabidopsis transgenic lines carrying a β-glucuronidase (GUS) gene trap identified a line in which GUS expression was restricted to the micropylar end of the germinating seed [16]. A T-DNA insertion into the TITAN (TTN) gene alters mitosis and cell cycle control during endosperm development. Some ttn alleles form giant polyploid nuclei with enlarged nucleoli. TITAN is related to ADP ribosylation factors and is a member of the RAS family of small GTP-binding proteins, which regulate many eukaryote cell functions [17]. 21 A common emerging theme in plant development is that hypothetical ancestral representatives of gene families with a broad expression pattern may be co-opted for specialized functions. These genes may include representatives of multigene families, such as the MADS-box family, some of which are expressed in the endosperm and in the developing male and female gametophytes [18]. Similarly, in maize, a member of the RbAp (retinoblastoma-associated protein) sub-family of WD-repeat proteins is abundant during endosperm formation and is also expressed in the shoot apical meristem and leaf primordia of the embryo [19]. Gametophytic maternal-effect mutations Mutations that affect endosperm proliferation have been isolated in screens that looked for seed development without pollination. Three mutations belonging to the FIS class are female gametophyte mutations that result in the spontaneous initiation of endosperm development in the absence of fertilization. Each of the FIS genes (i.e. FIS1/MEDEA, FIS2 and FIS3/FERTILIZATION INDEPENDENT ENDOSPERM [FIE]) controls at least three functions in the developing endosperm: repression of genes required for the initiation of endosperm development, organization of the endosperm anterior–posterior axis, and the number of divisions of the endosperm nuclei [15•]. In addition, embryos inheriting a maternal copy of fis1 or fis2 rarely develop past the heart stage, and there is no embryo development in fis3 mutants. As a result, seeds carrying a maternal copy of a fis mutation shrivel and are rarely viable. The fis mutants mimic at least some of the apomictic processes, such as autonomous endosperm development, but the mutations are not sufficient for progression to full apomictic seed development. The FIS genes have several interesting properties in common. They all encode proteins that belong to the Polycomb group (PcG) of general transcriptional repressors, which were originally described in Drosophila. A multiplicity of PcG complexes exists in Drosophila, and each complex contains about 30 proteins that maintain a repressed transcriptional state throughout the lifetime of the organism [20•]. FIS1/MEDEA has sequence similarity with the protein encoded by the Drosophila gene ENHANCER OF ZESTE (E[Z]) and FIS3/FIE with that encoded by EXTRA SEX COMBS (ESC) (see [21] for review). Although it was originally proposed that FIS2 may correspond functionally to the Drosophila protein HUNCHBACK [22,23], FIS2 shares sequence similarity with the Drosophila protein SU(Z)12 [21]. In the yeast two-hybrid assay, the Drosophila E(Z) and ESC proteins interact physically [24,25]. It has recently been shown that FIS1/MEDEA and FIS3/FIE also interact physically, but FIS2 does not interact with either FIS1/MEDEA or FIS3/FIE [26,27••,28]. The Drosophila E(Z) and ESC proteins are members of a multiprotein PcG complex that is distinct from other complexes containing PcG proteins [29]. PcG complexes have not yet been identified in plants, and it has not yet been determined whether FIS1/MEDEA and FIS3/FIE are also restricted to a subset of PcG complexes in Arabidopsis. 22 Growth and development Figure 2 Current Opinion in Plant Biology Scanning electron microscope image of a silique containing seeds resulting from the crossing of a FIS3/fis3 heterozygote with pollen carrying a METHYL TRANSFERASE1 (MET1) antisense construct. The picture shows rescued large seeds carrying maternal fis3 and small seeds carrying maternal FIS3. The FIS genes share two additional properties. First, there is no phenotypic effect on seed development when fis mutations are introduced to the zygote paternally, in contrast to the shrunken seed phenotype caused by the maternal inheritance of fis mutations. A possible reason for this is that the paternal genome is repressed in early seed development (see section on ‘Epigenetic effects in endosperm development’ below). Second, each of the FIS genes is expressed in the developing endosperm. The finding that genes in Arabidopsis encode proteins that are homologous to the PcG class of transcriptional repressors suggests that global control of gene repression evolved before the separation of lines leading to plants and animals. Elucidating the function of PcG proteins is continuing to be an important topic in Drosophila research, and may help us to understand the functions of Arabidopsis PcG proteins such as FIS. Recently, two Arabidopsis homologs of the trithorax-group (trxG) of transcriptional activators have been discovered [30], suggesting that the similarities in global transcriptional activation are conserved between plants and animals. Epigenetic effects in endosperm development Before fertilization, the egg and central cell (i.e. the endosperm precursor) can express only maternal genes because they originate from female tissue. After fertilization, the zygote and endosperm contain both maternal and paternal genomes. Gene expression in both embryo and endosperm is largely, if not entirely, maternal in origin until three to four days after fertilization. The activity of 20 paternal genes was first detected only after that time [31••]. The reasons for the delayed activation of the paternal genome, and the molecular mechanisms that govern that delay, are unknown. It seems unlikely that suppression of the male genome is necessary for correct gene dosage because in apomicts the unreduced embryo sac has two maternal genomes and develops normally. The transient silencing of the male genome has similarities to whole-genome imprinting by inactivation of the male genome in mealybugs [32]. Acetylation levels of histone H4 in the chromatin of mealybugs have been implicated in the control of the differential activity of the male and female genomes [32]. Evidence is emerging, however, that not all genes from the paternal genome are inactive in early embryo and endosperm development. Springer et al. [33] found that the PROLIFERA gene is expressed early in development in both the embryo and endosperm. Similarly, paternally inherited FIS1/MEDEA is expressed in the embryo but not in the endosperm [34]. Further work is needed to establish whether the transitory inactivation of the paternal genome includes all genes whose maternal counterparts are expressed before about 80 hours of development. The three FIS genes are active in the central cell before fertilization and so are expressed maternally. FIS::GUS fusions that are inherited paternally are not expressed in the early endosperm [27••], supporting evidence that the male genome is not activated until later in development [31••]. These results could explain why a wildtype FIS gene introduced via pollen does not rescue a maternal fis mutation. Interestingly, the absence of paternal rescue of fis1, fis2 and fis3 mutations can be overridden when methylation is disturbed, either by a mutation in DECREASE IN DNA METHYLATION1 (DDM1), a gene that encodes a SWI2/SNF2-like chromatin remodeling factor [35,36], or with a DNA METHYL TRANSFERASE1 (MET1) antisense construct (Figure 2; [27••,28,37,38,39•]). These mutations decrease methylation over most of the genome, although the MET1 antisense construct does increase methylation in some regions [40,41]. Rescue of fis1 and fis2 mutations most likely results from the early activation of one or more genes in the paternal genome. The paternal genes that rescue fis ovules are not the wildtype FIS alleles because rescue also occurs in the presence of a paternally inherited fis mutation [27••,42]. Parent-of-origin effects such as these suggest the occurrence of genomic imprinting [43]. Usually, such effects are manifested early in development, and they can occur in both plants and animals. Epigenetic mechanisms such as DNA methylation or chromatin remodeling may be responsible for imprinting because the effects can be modified by genes that affect methylation (e.g. MET1) [37], histone deacetylation (e.g. HISTONE DEACETYLASE COMPLEX [HDAC]) [44–46] or chromatin remodeling (e.g. DDM1 and MORPHEUS’ MOLECULE1 [MOM1]) [35,36,47••]; (see [48] for a recent review). Genetic and epigenetic processes in seed development Lohe and Chaudhury Epigenetic regulation may also play an important role in silencing some genes in polyploids. Arabidopsis suecica is an allotetraploid derived from A. thaliana and Cardaminopsis arenosa. At least ten genes are silenced by hypermethylation in A. suecica, and it has been suggested that epigenetic regulation may be advantageous in the evolution of polyploid species [49•]. In F1 hybrids between diploid species of wheat and in the derived allotetraploids, alterations to cytosine methylation occurred in about 13% of the loci examined [50]. Apomixis Several thousand plant species can reproduce asexually to generate seeds that are clones of the female parent. The apomictic process begins in the ovule with a modified meiotic division that results in an unreduced embryo sac and an egg cell with an unreduced chromosome number. Development of the egg into an embryo begins spontaneously (i.e. by parthenogenesis), even though fertilization has not occurred. Alternatively, another unreduced cell can take on the role of the egg cell, either in the embryo sac (diplospory) or a sporophytic cell (apospory). Depending on the type of apomixis, fertilization of the central cell can occur normally and development of a triploid endosperm is initiated (pseudogamy, the most common type of apomixis). Alternatively, spontaneous endosperm development can occur without fertilization and independently of embryo development (see [51,52]). Apomixis would be a particularly useful trait to introduce into crop plants, primarily because of its ability to propagate seeds clonally. The genes that repress embryo and endosperm development until fertilization are of interest in understanding how apomictic systems function at the molecular level. Sexually reproducing Arabidopsis thaliana has been studied intensively to identify genes that, when mutated, allow seed production without fertilization. Although it has not been possible to generate an apomictic mutant of Arabidopsis to date, mutations in each of the three FIS genes described above result in endosperm proliferation in the absence of fertilization. Spontaneous endosperm development is a characteristic of some modes of apomictic reproduction. Even if fertilized, however, a fis mutant embryo fails to develop, and upon maturity, the seeds of these mutants shrivel and are usually inviable. Normal seed development also requires the coordinated growth of the silique tissues surrounding the ovule. An enhancer insertion has been isolated that hyperactivates the cytochrome P450 gene CYP78A9, resulting in large and seedless fruit in the absence of pollination [53]. Another gene that is essential for development of the silique is FRUIT WITHOUT FERTILIZATION (FWF) [54]. Mutation of this gene results in enhanced cell division, expansion of the silique mesocarp layer and increased lateral vascular bundle development in the absence of fertilization. These genes are of interest in understanding the molecular events of apomixis because, in apomicts, both silique and seed development occur spontaneously without fertilization. 23 Identification of the genes controlling the decision between the sexual and apomictic pathways is difficult because most apomicts are polyploid and recombinants are difficult to obtain and analyze. Recent studies have indicated that apomixis may be the product of one or a small number of genetic factors that are closely linked. The three essential components of apomixis in Hieracium (i.e. apospory, and autonomous embryo and endosperm development) segregate as a single dominant Mendelian factor [55]. It is unclear whether the factor is a single gene or a co-adapted gene complex that is maintained by an absence of crossing over. From crosses between sexual and apomictic dandelions (Taraxacum) and analysis of the progeny, it was concluded that diplospory and parthenogenesis (two ‘elements of apomixis’) can be uncoupled [56]. Similarly, in Erigeron annuus, factors controlling diplospory and parthenogenesis are unlinked and inherited independently [57]. The authors of this work on Erigeron annuus further concluded that the parthenogenetic locus is likely to be a gametophyte recessive lethal, and that the region responsible for diplospory appears to be inherited on a univalent chromosome. Conclusions Proper development of an ovule into a mature seed depends on the coordinated expression of many genes over a short period of time. Discovering the identities of these genes and elucidating their roles will require a combination of genetics, and molecular and cell biology. The most exciting recent development has been the complete sequencing of the Arabidopsis genome [58], which will facilitate enormously the identification of seed development genes and the genetic pathways that they control. Sometimes the homologies of an unknown Arabidopsis gene with a known gene in well-studied organism can provide clues to its function. For example, each of three FIS genes that suppress endosperm proliferation in the absence of fertilization has a clear homolog in the Drosophila PcG class of genes. The PcG proteins function as global repressors of gene activity by altering chromatin structure. Chromatin remodeling genes, in addition to the PcG FIS class, play a key role in seed development. These genes include histone deacetylases, genes in the SWI2/SNF2 class and methyl transferase genes (see [59]). Recently, a new plant genome research project entitled ‘Functional genomics of plant chromatin genes’ has been initiated to identify, mutate, and functionally analyze the several hundred plant chromatin genes in maize and Arabidopsis that contribute to chromatin-level control of gene expression [60•]. Epigenetic effects are also involved in early embryo and seed development. Study of epigenetic effects, best carried out in Arabidopsis and maize, may lead to new insights into the genetic mechanisms that control seed development. Acknowledgements We thank Aneta Ivanova for the photograph of the embryo in Figure 1. The financial support of the Graingene organization to ARL is gratefully acknowledged. 24 Growth and development References and recommended reading 17. Papers of particular interest, published within the annual period of review, have been highlighted as: • of special interest •• of outstanding interest 1. Cheung AY: Pollen–pistil interactions in compatible pollination. Proc Natl Acad Sci USA 1995, 92:3077-3080. 2. Saito C, Nagata N, Sakai A, Mori K, Kuroiwa H, Kuroiwa T: Unequal distribution of DNA-containing organelles in generative and sperm cells of Erythrina crista-galli (Fabaceae). Sex Plant Reprod 2000, 12:296-301. 3. Antoine AF, Faure JE, Cordeiro S, Dumas C, Rougier M, Feijo JA: A calcium influx is triggered and propagates in the zygote as a wavefront during in vitro fertilization of flowering plants. Proc Natl Acad Sci USA 2000, 97:10643-10648. 4. Jürgens G, Mayer U, Busch M, Lukowitz W, Laux T: Pattern formation in the Arabidopsis embryo: a genetic perspective. Philos Trans R Soc London B Biol Sci 1995, 350:19-25. 5. Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ: LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 2001, 98:11806-11811. 6. Grebe M, Gadea J, Steinmann T, Kientz M, Rahfeld JU, Salchert K, Koncz C, Jürgens G: A conserved domain of the Arabidopsis GNOM protein mediates subunit interaction and cyclophilin 5 binding. Plant Cell 2000, 12:343-356. 7. Long J, Barton MK: Initiation of axillary and floral meristems in Arabidopsis. Dev Biol 2000, 218:341-353. 8. Hardtke CS, Berleth T: The Arabidopsis gene MONOPTEROUS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 1998, 17:1405-1411. 9. Schrick K, Mayer U, Horrichs A, Kuhnt C, Bellini C, Dangl J, Schmidt J, Jürgens G: FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis. Genes Dev 2000, 14:1471-1484. 10. Apuya NR, Yadegari R, Fischer RL, Harada JJ, Zimmerman JL, Goldberg RB: The Arabidopsis embryo mutant schlepperless has α gene. Plant Physiol 2001, a defect in the chaperonin-60α 126:717-730. 11. Helliwell C, Chin-Atkins AN, Wilson I, Chapple R, Dennis ES, • Chaudhury A: The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell 2001, 13:1-12. Mutants that are defective in the AMP1 gene exhibit many different phenotypes that are seemingly unrelated. The AMP1 protein is similar to the glutamate carboxypeptidases. It is proposed that the AMP1 gene product modulates the level of a small signaling molecule, which in turn regulates diverse developmental processes. 12. Berger F: Endosperm development. Curr Opin Plant Biol 1999, 2:28-32. 13. Olsen O-A: Endosperm development: cellularization and cell fate specification. Annu Rev Plant Mol Biol 2001, 52:233-267. 14. Boisnard-Lorig C, Colon-Carmona A, Bauch M, Hodge S, Doerner P, • Bancharel E, Dumas C, Haseloff J, Berger F: Dynamic analyses of the expression of the HISTONE::YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell 2001, 13:449-451. A histone 2B::YFP fusion protein enabled the observation of mitotic activity in living syncytial endosperm. The syncytium is organized into three polar mitotic domains in which nuclei divide simultaneously with a specific time course. 15. Sørensen MB, Chaudhury AM, Robert H, Bancharel E, Berger F: • Polycomb group genes control pattern formation in plant seed. Curr Biol 2001, 11:277-281. Using a green fluorescent protein (GFP) marker that is expressed in the posterior pole of the endosperm, it is shown that mutations in each of the MEDEA/FIS1, FIS2 and FIE/FIS3 genes disrupt the establishment of the anterior–posterior polar axis in the endosperm. 16. Dubreucq B, Berger N, Vincent E, Boisson M, Pelletier G, Caboche M, Lepiniec L: The Arabidopsis AtEPR1 extensin-like gene is specifically expressed in endosperm during seed germination. Plant J 2000, 23:643-652. McElver J, Patton D, Rumbaugh M, Liu C, Yang LJ, Meinke D: The TITAN5 gene of Arabidopsis encodes a protein related to the ADP ribosylation factor family of GTP binding proteins. Plant Cell 2000, 12:1379-1392. 18. Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF: MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 2000, 24:457-466. 19. Rossi V, Varotto S, Locatelli S, Lanzanova C, Lauria M, Zanotti E, Hartings H, Motto M: The maize WD-repeat gene ZmRbAp1 encodes a member of the MSI/RbAp1 sub-family and is differentially expressed during endosperm development. Mol Genet Genomics 2001, 265:576-584. 20. Saurin AJ, Shao Z, Erdjument-Bromage H, Tempst P, Kingston RE: • A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 2001, 412:655-660. A major PcG complex of proteins from Drosophila was purified and fractionated into 30 proteins. For the first time, a direct physical connection was demonstrated among proteins that bind to specific regulatory DNA sequences, PcG proteins and transcription machinery proteins. 21. Chaudhury AM, Koltunow A, Payne T, Luo M, Tucker MR, Dennis ES, Peacock WJ: Control of early seed development. Annu Rev Cell Dev Biol 2001, 17:677-699. 22. Grossniklaus U, Spillane C, Page DR, Köhler C: Genomic imprinting and seed development: endosperm formation with and without sex. 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Curr Biol 2000, 10:1535-1538. 27. •• Luo M, Bilodeau P, Koltunow A, Dennis E, Peacock WJ, Chaudhury AM: Expression and parent-of-origin effects for FIS2, MEA and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci USA 2000, 97:10637-10642. The expression patterns of the three genes, MEDEAA/FIS1, FIS2 and FIE/FIS3, in the developing seed are described. MEDEA/FIS1 and FIS2 have similar expression patterns in endosperm before cellularization. FIE/FIS3 is also expressed in the endosperm, and also in other tissues. Each of the three genes shows a parent-of-origin effect that is not dependent on DNA methylation 28. Yadegari R, Kinoshita T, Lotan O, Cohen G, Katz A, Kazuo N, Harada JJ, Goldberg RB, Fischer RL, Ohad N: 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 2000, 12:2367-2382. 29. 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