Most differentiation events in higher plants occur continuously in the postembryonic adult phase of the life cycle. Embryogenesis in plants, therefore, is concerned primarily with establishing the basic shoot-root body pattern of the plant and accumulating food reserves that will be used by the germinating seedling after a period of embryonic dormancy within the seed. Recent genetics studies in Arabidopsis have identified genes that provide new insight into how embryos form during plant development. These studies, and others using molecular approaches, are beginning to reveal the underlying processes that control plant embryogenesis.
Higher plant reproduction is unique because 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 that replicates to generate the endosperm, a tissue that supports embryo development. To understand mechanisms that initiate reproduction, we isolated a mutation in Arabidopsis, f644, that allows for replication of the central cell and subsequent endosperm development without fertilization. When mutant f644 egg and central cells are fertilized by wild-type sperm, embryo development is inhibited, and endosperm is overproduced. By using a map-based strategy, we cloned and sequenced the F644 gene and showed that it encodes a SETdomain polycomb protein. Subsequently, we found that F644 is identical to MEDEA (MEA), a gene whose maternal-derived allele is required for embryogenesis [Grossniklaus, U., VielleCalzada, J.
Position-dependent regulation of growth is important for shaping organs in multicellular organisms. We have characterized the role of JAGGED, a gene that encodes a protein with a single C2H2zinc-finger domain, in controlling the morphogenesis of lateral organs in Arabidopsis thaliana. Loss of JAGGED function causes organs to have serrated margins. In leaves, the blade region is most severely affected. In sepals, petals and stamens, the strongest defects are seen in the distal regions. By monitoring cell-cycle activity in developing petals with the expression of HISTONE 4, we show that JAGGED suppresses the premature differentiation of tissues, which is necessary for the formation of the distal region. The localization of defects overlaps with the expression domain of JAGGED, which is restricted to the growing regions of lateral organs. JAGGED expression is notably absent from the cryptic bract, the remnant of a leaf-like organ that subtends the flower in many species but does not normally develop in wild-type Arabidopsis. If misexpressed, JAGGED can induce the formation of bracts, suggesting that the exclusion of JAGGED from the cryptic bract is a cause of bractless flowers in Arabidopsis.
A fundamental problem in biology is to understand how fertilization initiates reproductive development. Higher plant reproduction is unique because two fertilization events are required for sexual reproduction. First, a sperm must fuse with the egg to form an embryo. A second sperm must then fuse with the adjacent central cell nucleus that replicates to form an endosperm, which is the support tissue required for embryo and/or seedling development. Here, we report cloning of the Arabidopsis FERTILIZATION-INDEPENDENT ENDOSPERM ( FIE ) gene. The FIE protein is a homolog of the WD motif-containing Polycomb proteins from Drosophila and mammals. These proteins function as repressors of homeotic genes. A female gametophyte with a loss-of-function allele of fie undergoes replication of the central cell nucleus and initiates endosperm development without fertilization. These results suggest that the FIE Polycomb protein functions to suppress a critical aspect of early plant reproduction, namely, endosperm development, until fertilization occurs. INTRODUCTIONThe higher plant life cycle alternates between multicellular haploid (i.e., gametophyte) and diploid (i.e., sporophyte) generations. In Arabidopsis, the ovule generates the female gametophyte, which is composed of egg, central, synergid, and antipodal cells ( Figure 1A). Surrounding and protecting the female gametophyte are maternal cell layers, which are called the integuments ( Figure 1A). Double fertilization within the female gametophyte activates four reproductive developmental programs. (1) The fertilized egg initiates embryogenesis ( Figure 1D). (2) The fertilized central cell generates the primary triploid endosperm nucleus that replicates to form the endosperm ( Figure 1D), which is the tissue that supports the development of the embryo. (3) The maternal integument cell layers of the ovule become the seed coat ( Figures 1D and 1H). (4) The ovary differentiates and elongates to form the fruit, or silique ( Figure 1F).The two products of fertilization, embryo and endosperm, display distinct patterns of development. In Arabidopsis, the embryo proceeds through a series of stages that have been defined morphologically as preglobular, globular ( Figure 1D), heart, cotyledon, and maturation ( Figure 1H). During these stages, an axis of polarity is fixed, shoot and root meristems are formed, and storage organs are generated (Goldberg et al., 1994). In contrast, the fertilized central cell (i.e., the primary endosperm nucleus) divides mitotically to produce a syncytium of nuclei that fills an expanding central cell (Figure 1D). After cytokinesis occurs, endosperm cells produce storage proteins, starch, and lipids (Lopes and Larkins, 1993).Ultimately, the endosperm is absorbed by the developing embryo ( Figure 1H). It is thought that endosperm evolved from a supernumerary fertilization event that originally produced multiple embryos and may represent a highly modified embryo that enhances the fitness of its sister embryo (Friedman, 1992(Friedman, , 1995.To understand t...
Endosperm is an absorptive structure that supports embryo development or seedling germination in angiosperms. The endosperm of cereals is a main source of food, feed, and industrial raw materials worldwide. However, the genetic networks that regulate endosperm cell differentiation remain largely unclear. As a first step toward characterizing these networks, we profiled the mRNAs in five major cell types of the differentiating endosperm and in the embryo and four maternal compartments of the maize (Zea mays) kernel. Comparisons of these mRNA populations revealed the diverged gene expression programs between filial and maternal compartments and an unexpected close correlation between embryo and the aleurone layer of endosperm. Gene coexpression network analysis identified coexpression modules associated with single or multiple kernel compartments including modules for the endosperm cell types, some of which showed enrichment of previously identified temporally activated and/or imprinted genes. Detailed analyses of a coexpression module highly correlated with the basal endosperm transfer layer (BETL) identified a regulatory module activated by MRP-1, a regulator of BETL differentiation and function. These results provide a high-resolution atlas of gene activity in the compartments of the maize kernel and help to uncover the regulatory modules associated with the differentiation of the major endosperm cell types.
The plant life cycle alternates between a diploid sporophyte generation and a haploid gametophyte generation. The angiosperm female gametophyte is critical to the reproductive process. It is the structure within which egg cell production and fertilization take place. In addition, the female gametophyte plays a role in pollen tube guidance, the induction of seed development, and the maternal control of seed development. Genetic analysis in Arabidopsis has uncovered mutations that affect female gametophyte development and function. Mutants defective in almost all stages of development have been identified, and analysis of these mutants is beginning to reveal features of the female gametophyte developmental program. Other mutations that affect female gametophyte function have uncovered regulatory genes required for the induction of endosperm development. From these studies, we are beginning to understand the regulatory networks involved in female gametophyte development and function. Further investigation of the female gametophyte will require complementary approaches including expression-based approaches to obtain a complete profile of the genes functioning within this critical structure.
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. INTRODUCTIONFlowering plant reproduction involves fertilization of two cells (reviewed in van Went and Willemse, 1984). Within the Arabidopsis ovule, the female gametophyte consists of an egg cell and two synergid cells at the micropylar end, a central cell in the middle, and three antipodal cells at the chalazal end. All are haploid except for the central cell, which contains two polar nuclei that fuse to form a diploid nucleus. Reproduction is initiated when an entering pollen tube discharges two genetically identical haploid sperm cells. Fertilization of the egg generates the diploid embryo, which passes through morphologically defined stages (globular, heart, torpedo, walking stick, early maturation, and maturation) (Goldberg et al., 1994;Jurgens and Mayer, 1994). During embryo development, two organ systems (axis and cotyledon) and three tissue layers (protoderm, procambium, and ground meristem) are specified (Lindsey and Topping, 1993;Jurgens, 1994;Meinke, 1994).Fertilization of the central cell generates the triploid endosperm, for which the pattern of development differs dramatically from that of the embryo. Arabidopsis endosperm development is characteristic of nuclear endosperm development in angiosperms (Mansfield and Briarty, 1990a;Webb and Gunning, 1991;Berger, 1999;Brown et al., 1999). The Arabidopsis primary endosperm nucleus replicates without cytokinesis to form a syncytium of nuclear-cytoplasmic domains that migrate to the periphery of the expanding central cell (Brown et al., 1999). When the embryo is at the globular/heart transi...
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