Control of male gametophyte development.

In a previous review of male gametophyte development (McCormick, 1993), it was noted that the two areas posed by Mascarenhas (1975) as fruitful areas for future research were the following. What are the differences in the two cytoplasms that determine the different cell fates of the generative and vegetative cells? And what are the functions of pollen-specific proteins? Now, 10 years later, the genome sequences of Arabidopsis and rice have been completed. There are extensive EST databases for many plants and several data sets from microarray hybridizations. There are extensive resources for disrupting the functions of genes. The pollen research community has made significant progress toward a deeper understanding of pollen development using community resources as well as novel techniques developed specifically for the analysis of pollen. This reviewwill provide an overview of these advances and prospects for the future, focusing on male gametophyte development, strictly defined as postmeiosis development, after the formation of the haploid microspores. Meiosis will not be discussed in detail. Anther development and the role of the tapetum in pollen development are discussed by Dickinson and Scott in this issue. The main features of pollen development are shown in Figure 1, which is based on an ultrastructural analysis of microsporogenesis in Arabidopsis thaliana (Owen and Makaroff, 1995). The male gametophyte, or pollen grain, is a three-celled organism that is derived by stereotypical cell divisions. Our story starts inside the anther, when sporogenous initial cells, also called pollen mother cells, undergo meiosis to form a tetrad of cells. Figure 2 shows Arabidopsis tetrads that have been extruded from one anther. Each tetrad is enclosed in a thick callose wall. The microspores in each tetrad are freed from their meiotic brothers by the action of callase, an enzyme produced by the tapetum. The tapetum is a nutritive cell layer that lines the locule containing the developing microsporocytes. The tapetum disintegrates in the later stages of pollen development. The microspores enlarge and then each undergoes an asymmetric mitosis. The mitosis is asymmetric because the dividing nucleus is adjacent to the wall, and the spindle orientation is such that after cytokinesis, one cell is much smaller than the other. The two cells of this bicellular pollen grain have strikingly different fates. The larger cell is called the vegetative cell, and the smaller cell is called the generative cell. The larger vegetative cell does not divide again but eventually will form the pollen tube. The generative cell is engulfed inside the cytoplasm of the vegetative cell. The generative cell undergoes mitosis, sometimes termed a second or pollen mitosis, to form the two sperm cells. The timing of this second pollen mitosis varies in different plant families, sometimes occurring within the anther (as in grasses and crucifers), although more commonly it occurs during pollen tube growth. In most plants, mature pollen grains are released from the anthers in a partially dehydrated state. Once on the stigma, the pollen grains hydrate and the vegetative cell extends a tube that grows by tip growth. As the tube extends, the vegetative cell nucleus and the two closely associated sperm cells move into the tube. Eventually, the entire vegetative cell exits the pollen grain and travels at the tip of the rapidly growing pollen tube. Pollen development is complete when the sperm cells are released into the embryo sac.