Perspectives on Genetic Analysis of Plant Embryogenesis.

Abstract

Embryogenesis plays a central role in the life cycle of flowering plants. Ever since the process of double fertilization was documented at the turn of the century, plant embryologists have attempted to characterize the cellular and biochemical changes that occur within developing seeds (Maheshwari, 1950; Raghavan, 1976). For many years, the emphasis was on comparative morphology and the analysis of cell division patterns during early stages of embryo development (Johansen, 1950; Wardlaw, 1955). Attention then shifted to experimental studies of somatic embryogenesis, embryo culture, and haploid embryos derived from microspores (Raghavan, 1986). Manipulation of zygotic embryos was limited by the presence of surrounding maternal tissues. Electron microscopy provided additional details on cellular changes associated with embryogenesis but generally failed to identify the mechanisms responsible. Plant embryologists believed that genetic factors played an important role in morphogenesis, but mutants with altered patterns of embryo development were largely ignored (Meinke, 1986). Recent advances in molecular biology have led to a renewed interest in plant embryology and the underlying patterns of gene expression that occur throughout seed development (Goldberg et al., 1989). Many genes transcribed during embryonic maturation have now been examined at the molecular level. Genetics provides a complementary approach to the study of plant embryo development by allowing the identification of genes with essential functions during this critical stage of the life cycle (Meinke, 1986). The purpose of this review will be to explore the potential benefits and limitations of mutant analysis in relation to plant embryo development. Additional information can be obtained through recent reviews on plant development (Steeves and Sussex, 1989; Lyndon, 1990), experimental plant embryogenesis (Johri, 1984; Raghavan, 1986; Williams and Maheswaran, 1986), and plant developmental genetics (Sheridan, 1988; Meinke, 1991a, 1991b). Plant embryologists originally attempted to explain characteristic patterns of cell division observed early in development by establishing fundamental laws of embryogeny (Johansen, 1950). These laws of parsimony, numbers, origin, disposition, and destination were thought to reflect the fundamental organization of embryos from different species. This view has gradually been replaced by the realization that cell division patterns are determined more by genetic and biophysical factors than by laws of embryogeny. Examination of developmental pathways in different angiosperms has nevertheless revealed a number of common features. The most critical events appear to be the formation of apical meristems, the establishment of basic patterns of symmetry and cellular organization, and the transition from a heterotrophic zygote dependent upon nutrient reserves of surrounding maternal tissues to an autotrophic embryo capable of surviving desiccation and producing a viable seedling after germination. Early stages of plant embryo development are characterized by cell division and morphogenesis. This is followed by a period of cell specialization and embryonic maturation in preparation for dormancy and germination. Several features distinguish embryogenesis in angiosperms from related pathways in animal systems: (1) the process of double fertilization and subsequent interactions between embryo and endosperm tissues, (2) the apparently minor role played by maternal mRNAs stored in unfertilized eggs, (3) the absence of cellular migration during embryo development, (4) the absence of a germ line established early in development, (5) the activation of large numbers of zygotic genes during very early stages of embryogenesis, (6) the presence of a male gametophyte active in transcription that leads to elimination of many deleterious alleles before fertilization, (7) the establishment of relatively few specialized cell types, (8) the formation of apical meristems that ultimately produce the adult plant, and (9) the small size of the zygote and its location deep within maternal tissues. The zygote in flowering plants is also not unique; a wide range of somatic cells can be