Imprinting and Seed Development

Abstract

Imprinted genes are expressed predominantly from one allele in a parent-of-origin–specific manner. The endosperm, a seed tissue that mediates the transfer of nutrients from the maternal parent to the embryo, is an important site of imprinting in flowering plants. Imprinted genes have been identified in maize and Arabidopsis thaliana, but crosses in a variety of species suggest that the effect of imprinting on seed development is widespread throughout the angiosperms. The mechanism of imprinting in plants, as yet only partially understood, likely involves differences in DNA methylation and chromatin structure between differentially expressed maternal and paternal alleles. Seeds consist of three genetically distinct components: embryo, endosperm, and seed coat. In plants, mitosis follows meiosis to produce the haploid phase of the plant life cycle, the male and female gametophytes. The angiosperm female gametophyte, the site of fertilization, is completely embedded within the maternal sporophytic tissues of the ovule. The most prevalent type of mature female gametophyte is a seven-celled organism consisting of three antipodal cells, two synergid cells, an egg cell, and a diploid central cell. The function of the antipodal cells is unknown. The micropylar synergid cells help attract the pollen tube to the female gametophyte (Higashiyama et al., 2001). The egg cell lies adjacent to the synergid cells and is the progenitor of the embryo. The large central cell, the progenitor of the endosperm, contains two polar nuclei. These fuse before, or at the time of, fertilization to form a diploid central cell nucleus. The male gametophyte, or pollen, develops in the anther from microspores. A mature male gametophyte consists of two haploid sperm cells encased by a haploid vegetative cell. Seed development begins upon double fertilization. The pollen tube, formed from the vegetative cell of the male gametophyte, enters the female gametophyte through the micropylar end and releases two sperm into a synergid cell. One sperm fertilizes the egg cell and the other fertilizes the central cell. The resulting embryo and endosperm are genetically identical except for ploidy level: the embryo is diploid and the endosperm is triploid. Fertilization also initiates changes in maternal tissues. The ovary develops into a fruit and the ovule integuments differentiate to form the protective seed coat. The endosperm, a terminally differentiated tissue that nourishes the embryo during seed development, is the only known site of imprinting in plants. It has been known that the endosperm is a product of double fertilization for >100 years (reviewed by Sargant, 1900), but its evolutionary origin is still a puzzle. The endosperm might be derived from a supernumerary embryo that took on an embryo-nourishing function or from a female gametophyte that was later sexualized (Friedman, 2001). Diagram of the Embryo Sac of a Developing Arabidopsis Seed. The syncytial endosperm consists of three domains: the micropylar endosperm (MCE), which surrounds the base of the globular-stage embryo (EM), the peripheral endosperm (PEN), and the chalazal endosperm (CZE). Pink circles indicate endosperm nuclei, and gray areas indicate cytoplasm. Early endosperm development follows a similar pattern in maize. The endosperm, although not organized into distinct mitotic domains, divides synchronously as a syncytium for several days and then cellularizes from the periphery inward. Nuclear divisions continue asynchronously for several more days. Mitosis stops first at the base of the kernel. The cessation then spreads as a wave from the kernel apex downward and then out to the periphery (Kowles and Phillips, 1988). After the mitotic activity of the central region ceases, the cells increase in size and undergo extensive endoreduplication. Endoreduplication is asynchronous, and there is a large amount of heterogeneity in nuclear DNA content (Kowles and Phillips, 1988). The endosperm persists after embryo development is completed and constitutes the major portion of the mature kernel. It stores starch, lipids, and storage proteins and acts as a vital source of nutrients during germination and early seedling development (Lopes and Larkins, 1993). Imprinting exists in placental mammals as well as in angiosperms. Unsuccessful attempts to create mouse embryos from two female pronuclei first revealed parent-of-origin effects on embryogenesis in mammals (McGrath and Solter, 1984; Surani et al., 1984). Mammalian androgenetic and gynogenetic embryos fail to develop because of the failure of embryonic and extraembryonic tissues, respectively. These parent-of-origin effects suggested that imprinted genes might be essential for embryo development. Plant embryogenesis appears to be more flexible than mammalian embryogenesis. In addition to normal sexual reproduction, plant embryos can arise asexually from somatic tissue (Goldberg et al., 1994). Viable haploid embryos occasionally may