Nuclear Endosperm Development in Cereals and Arabidopsis thaliana

Abstract

The nuclear endosperm of monocots, including the cereal species maize, rice, barley, and wheat, represents humankind's most important renewable source of food, feed, and industrial raw materials. In addition, the endosperm is an attractive system for developmental biology studies. Similar to the embryo, the endosperm is the result of a fertilization process and therefore may be considered an organism in its own right. Endosperm development has been the subject of several recent reviews (DeManson, 1997; Becraft et al., 2000; Becraft, 2001; Olsen, 2001; Brown et al., 2002; Berger, 2003). This review emphasizes the main developmental aspects of nuclear endosperm development in cereals and Arabidopsis thaliana, including evolutionary origin, coenocyte development, endosperm cellularization, cell fate specification, and differentiation. After fertilization in what is the most common type of endosperm development, the nuclear type, the initial endosperm nucleus divides repeatedly without cell wall formation, resulting in a characteristic coenocyte-stage endosperm. Cellularization occurs via the formation of radial microtubule systems (RMS) and alveolation. Many dicot species, including commercially important crop plants such as soybean, cotton, and Arabidopsis, also have a nuclear endosperm, although the endosperm is consumed in part by the embryo during seed maturation. During its development, striking similarities exist between the endosperm in these groups, particularly with respect to the cellularization phase. Insight into the genetic specification of the different processes in endosperm development (e.g., coenocyte formation, alveolation, cell fate specification, and differentiation) may ultimately reveal how developmental subprograms are integrated into a master program specifying the entire endosperm body plan. This knowledge will not only benefit basic science but also strengthen efforts to improve cereal grain quality. Development and Structure of the Polygonum-Type Embryo Sac of Maize and Arabidopsis. (A) The embryo sac develops from the surviving haploid megaspore resulting from female meiosis. (B) After three rounds of mitosis without cell wall formation between sister nuclei, two groups of four nuclei form at the micropylar (mp) and chalazal (cz) poles of the young megagametophyte. (C) Three of the nuclei at each pole are walled off and become the egg cell (e), the synergids (sy), and the antipodal cells (ap). One nucleus from each pole migrates to the center (polar nuclei; pn) of the megagametophyte. (D) The haploid polar nuclei of maize remain separate until fertilization. The shaded area of the megagametophyte represents the central cell that develops into the endosperm after fertilization. One of the haploid male nuclei (m) from the pollen tube (pt) enters the central cell, and the three nuclei fuse to form the triploid primary endosperm nucleus. (E) The two polar nuclei of the Arabidopsis central cell fuse before fertilization. The antipodal cells are eliminated by programmed cell death. Figure modified from Drews et al. (1998). Definitions of Terms The figure citations are to the first mentions of each term in the text. Definitions of Terms The figure citations are to the first mentions of each term in the text. The Endosperm Coenocyte of Cereals and Arabidopsis. (A) to (D) Cereals. (E) to (H) Arabidopsis. (A) The triploid endosperm nucleus (en) is located in the basal cytoplasm of the central cell. A large central vacuole (cv) fills up most of the volume, surrounded by a thin line of cytoplasm (cy). (B) The central cell nucleus divides without the formation of a functional interzonal phragmoplast, and no cell wall is formed between sister nuclei. (C) After three rounds of nuclear divisions, eight endosperm nuclei are located in a single plane in the basal endosperm coenocyte. (D) The complete endosperm coenocyte contains evenly spaced nuclei in the entire peripheral cytoplasm. (E) The Arabidopsis endosperm coenocyte has nuclei migrating from the micropylar region (mp) toward the chalazal end (cz), eventually covering the entire periphery of the coenocyte. (F) and (G) As development progresses, the endosperm coenocyte develops three distinct regions: the region surrounding the embryo (MCE), the central or peripheral endosperm (PEN), and the region of the chalazal endosperm (CZE), which contains the chalazal cyst (cz). (H) At the end of the globular embryo stage, the embryo becomes completely surrounded by cytoplasm. Not surprisingly, genetic evidence shows that mutants affecting maternal ovule tissues also affect endosperm development. A priori, these maternal effects are expected to be of two types, gametophytic (effects expressed in the megagametophyte itself) and sporophytic (effects expressed in maternal plant tissues) (for an overview and references, see Drews et al., 1998; Grossniklaus and Schneitz, 1998; Chaudhury and Berger, 2001). A special group of Arabidopsis female-gametophytic mat