Female Gametophyte Development

Abstract

Early in their evolution, plants acquired a life cycle that alternates between a multicellular haploid organism, the gametophyte, and a multicellular diploid organism, the sporophyte. Angiosperms have both female and male gametophytes. The female gametophyte is critical to many steps of the angiosperm reproductive process, including pollen tube guidance, fertilization, the induction of seed development upon fertilization, and maternal control of seed development after fertilization. Genetic analysis in Arabidopsis and maize has revealed mutants defective in almost all stages of female gametophyte development, and analysis of these mutants is beginning to reveal features of the female gametophyte developmental program. In addition, mutants defective in female gametophyte function have revealed 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. Gametophytes and sporophytes differ morphologically and functionally. The major function of diploid sporophyte generation is to produce haploid spores, which are the products of meiosis. Spores undergo cell proliferation and differentiation to develop into gametophytes. The major function of gametophyte generation is to produce haploid gametes. The fusion of egg and sperm gives rise to the zygote, which is the beginning of diploid sporophyte generation, thereby completing the life cycle (Gifford and Foster, 1989). The Arabidopsis Female Gametophyte. (A) Ovule. (B) Female gametophyte. The view in (B) is perpendicular to that in (A). The mature female gametophyte in Arabidopsis is ∼105 μm long and ∼25 μm wide. The gray areas represent cytoplasm, the white areas represent vacuoles, and the black areas represent nuclei. ac, antipodal cells; cc, central cell; ch, chalazal region of the ovule; ec, egg cell; f, funiculus; mp, micropyle; sc, synergid cell; sn, secondary nucleus. The angiosperm gametophytes are essential for the reproductive process. During sexual reproduction in angiosperms, the male gametophyte is transferred from the anther to the carpel's stigma, whereupon it forms a pollen tube that grows great distances through the carpel's internal tissues to deliver its two sperm cells to the female gametophyte. One sperm cell fertilizes the egg cell and the second sperm cell fuses with the central cell. After fertilization, the ovule gives rise to a seed; the seed's embryo, endosperm, and seed coat are derived from the fertilized egg cell, fertilized central cell, and ovule integuments, respectively (Maheshwari, 1950). The female gametophyte plays a critical role in essentially every step of the reproductive process. During pollen tube growth, the female gametophyte participates in directing the pollen tube to the ovule (Higashiyama, 2002; Johnson and Preuss, 2002; Higashiyama et al., 2003). During fertilization, cytoskeletal components within the female gametophyte direct the sperm cells to the egg cell and the central cell (Russell, 1992, 1993; Lord and Russell, 2002). Upon fertilization, female gametophyte–expressed genes control the initiation of seed development (Chaudhury et al., 2001). During seed development, female gametophyte–expressed gene products play a role in controlling embryo and endosperm development (Ray, 1997; Chaudhury and Berger, 2001). In this review, we describe angiosperm female gametophyte structure and development, summarize the female gametophyte's reproductive functions, and discuss the molecular and genetic approaches that are being used to understand these processes at the molecular level. Comprehensive reviews of the female gametophyte have been published previously (Maheshwari, 1950; Willemse and van Went, 1984; Haig, 1990; Huang and Russell, 1992; Russell, 2001). Patterns of Female Gametophyte Development Exhibited by Angiosperms. Genera exhibiting these patterns are indicated in parentheses. More comprehensive descriptions of the variation among angiosperms can be found in several reviews (Maheshwari, 1950; Willemse and van Went, 1984; Haig, 1990; Huang and Russell, 1992; Russell, 2001). In this figure, the chalazal end of the female gametophyte is up and the micropylar end is down. FG, female gametophyte. During megasporogenesis, the diploid megaspore mother cell undergoes meiosis and gives rise to four haploid nuclei. Angiosperms exhibit three main patterns of megasporogenesis, referred to as monosporic, bisporic, and tetrasporic. These three patterns are summarized in Figure 2. The three types differ mainly in whether cell plate formation occurs after these divisions, thus determining the number of meiotic products that contribute to the formation of the mature female gametophyte. In the monosporic pattern, both meiotic divisions are accompanied by cell plate formation, resulting in four one-nucleate megaspores. Subsequently, three megaspores, generally the micropylar-most megaspores