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The Female Gametophyte of Flowering Plants Venkatesan Sundaresan1,2,* and Monica Alandete-Saez1,2

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The Female Gametophyte of Flowering Plants Venkatesan Sundaresan1,2,* and Monica Alandete-Saez1,2 REVIEW 179 Development 137, 179–189 (2010) doi:10.1242/dev.030346 Pattern formation in miniature: the female gametophyte of flowering plants Venkatesan Sundaresan1,2,* and Monica Alandete-Saez1,2 Summary Plant reproduction involves gamete production by a haploid Box 1. Glossary generation, the gametophyte. For flowering plants, a defining Angiosperms. Flowering plants, in which seeds are produced within characteristic in the evolution from the ‘naked-seed’ plants, or the female reproductive organs. Anthers. The anther, which carries the pollen grain (the male gymnosperms, is a reduced female gametophyte, comprising gametophyte), sits on top of a filament to form the stamen or male just seven cells of four different types – a microcosm of pattern organ of a flower. formation and gamete specification about which only little is Embryo sac. The female gametophyte of flowering plants, which known. However, several genes involved in the differentiation, produces the two female gametes – the egg cell and central cell – for fertilization and post-fertilization functions of the female double-fertilization by the two sperm cells of the male gametophyte gametophyte have been identified and, recently, the (pollen grain). morphogenic activity of the plant hormone auxin has been Eudicots. The term means, literally, ‘true dicotyledons’, as this group found to mediate patterning and egg cell specification. This contains the majority of plants that have been considered article reviews recent progress in understanding the pattern dicotyledons and have typical dicotyledonous characters. formation, maternal effects and evolution of this essential unit Filiform apparatus. Structure formed at the micropylar (distal) pole of the synergid cell wall that is thickened, forming finger-like of plant reproduction. projections into the synergid cell cytoplasm. Gametophyte. The haploid generation of a plant produced by Key words: Embryo sac, Gametophyte, Flowering plant, meiosis from the sporophyte. The mature gametophyte produces Reproduction, Gametes male or female gametes (or both in lower plants). The fusion of male and female gametes produces a diploid zygote that develops into a Introduction new sporophyte. The life cycle of land plants involves an alternation of generations Gymnosperms. Group of seed-bearing plants from which the between a haploid gametophyte (see Glossary, Box 1) and a diploid angisoperms are presumed to have descended. The name comes sporophyte (see Glossary, Box 1). Whereas animal gametes are from the Greek word gymnospermos, meaning ‘naked seeds’, as formed directly after meiosis, plant gametes are produced only after seeds are found unenclosed on the scales of a cone or similar structure. growth of the multicellular haploid gametophyte. The morphological Ovule. The ovule, which carries the female gametophyte, is located complexity of the haploid generation ranges from the macroscopic in the part of the carpel (the female organ of a flower) known as the moss gametophytes, which dwarf the sporophyte, to the three-celled ovary, which ultimately becomes the fruit. Depending on the plant, male gametophyte (pollen) and seven-celled female gametophyte flowers can have one or multiple ovules per ovary. (embryo sac) that are characteristic of most flowering plants Sporophyte. The diploid generation of a plant, which is initiated (Maheshwari, 1950). The latter evolved through an extreme with the zygote. reduction from the female gametophytes of the gymnosperms (see Stigma. In a flower, the stigma is the terminal portion of the carpel, Glossary, Box 1), which frequently contain over a thousand cells, which has no epidermis and is meant to receive pollen grains. and is considered a key innovation in the evolution of flowering plants (reviewed by Friedman and Williams, 2003). These ‘stripped down to essentials’ female gametophytes confer two major defining Despite the crucial importance of the female gametophyte of characteristics of the flowering plants. First, they are small enough flowering plants, much remains to be learnt about its development to be packaged within an ovary. Second, they generate two gametes and overall biology, partly because it is a highly inaccessible that undergo double-fertilization to produce the nutritive tissue structure. The past few years, however, have seen some exciting called endosperm concordantly with the embryo, which allows more progress in the field. Here, we focus primarily on the female efficient resource allocation to fertilized seeds (reviewed by gametophyte of the model plant Arabidopsis, which has been Raghavan, 2003). The reduced female gametophyte of flowering studied more extensively than that of other plants, and review recent plants enabled much more rapid seed setting (i.e. the production of advances in the understanding of the patterning, the maternal effects seeds during reproductive growth) than is possible in gymnosperms, and the evolution of the female gametophyte. allowing for habitat adaptations that require short reproductive cycles and facilitating the expansion of flowering plants into diverse Female gametophyte development ecological niches. In angiosperms (see Glossary, Box 1), the male gametophytes (the pollen grains) develop within the anthers (see Glossary, Box 1) and the female gametophytes (megagametophytes or embryo sacs) 1Department of Plant Biology and 2Department of Plant Sciences, University of develop within the ovule (see Glossary, Box 1). There has been over California, 1 Shields Avenue, Davis, CA 95616, USA. a century of developmental studies on gametophyte development in *Author for correspondence ([email protected]) a large number of diverse plant species (Friedman et al., 2008). In DEVELOPMENT 180 REVIEW Development 137 (2) A C Fig. 1. Cell types and reproductive functions of Outer Central cell the female gametophyte (embryo sac). integuments Chalazal end (A)Sketch of a seven-celled embryo sac 2n ( -type), based on the model plant Egg cell n Polygonum Sperm nuclei Central Arabidopsis, that shows the four cell types within vacuole n the maternal tissues of the ovule: the synergid cells, Antipodal cells n the egg cell, the central cell and the antipodal cells. Central cell Degenerated (B)Wild-type Arabidopsis ovule showing a mature synergid Inner integuments embryo sac (FG7 stage, green dashed) with the Egg cell two synergid cell nuclei (yellow), the egg cell Sperm cells nucleus (red) and the central cell nucleus (purple). (C)Sketch of pollen tube reception within a Inner Pollen tube degenerated synergid cell in the micropylar end of integuments Synergid cells the embryo sac. Two sperm cells (violet) are Micropylar end released upon pollen tube reception. One sperm nucleus (dark blue) fuses to the egg cell nucleus BD (n), and a second sperm nucleus fuses to the central cell nucleus (2n) during double fertilization. (D) Sketch of a fertilized seed, with an embryo (2n) Endosperm nuclei (3n) at the globular stage and with endosperm nuclei (3n) before cellularization occurs. Egg cell nucleus Central cell nucleus Embryo (2n) Synergid cell nuclei most flowering plants, including Arabidopsis and maize, the embryo leaving only the proximal (chalazal) megaspore as the functional sac has a characteristic organization called the Polygonum-type megaspore [FM stage or female gametophyte stage 1 (FG1); Fig. (Maheshwari, 1950), containing seven cells of four distinct cell 2C] in each ovule. The megaspore then undergoes three sequential types (Fig. 1A,B). These four cell types are, first, the egg cell, which mitotic nuclear divisions, designated as stages FG2 to FG5 gives rise to the embryo, second, two accessory cells called synergid (Christensen et al., 1997), to generate the eight nuclei that will cells, which are important for pollen tube attraction, third, the central contribute to the differentiated embryo sac, four at each pole (Fig. cell, which gives rise to the endosperm, and fourth, three cells of 2D,E). Subsequent cellularization results in the formation of seven unknown function called antipodal cells. The entire embryo sac is cells owing to the nuclear migration of two of these nuclei called the enclosed within diploid sporophytic tissues called integuments, polar nuclei (Fig. 2E), which will constitute the central cell nucleus. which will constitute the seed coat in the mature seed. When pollen In the seven-celled embryo sac, the micropylar (distal) end of the lands on the stigma (see Glossary, Box 1), it forms a structure called ovule is adjacent to the egg cell and the two synergid cells, whereas the pollen tube that penetrates the embryo sac through an opening in the chalazal (proximal) end of the ovule is adjacent to the three the integuments called the micropyle and delivers two sperm cells antipodal cells. The homo-diploid (2n) central cell occupies much by entering a synergid cell, which subsequently degenerates (Fig. of the embryo sac and contains a large central vacuole. All of the 1C). Eventually, the other synergid cell will also degenerate. The cells within the embryo sac are highly polarized and possess two gametic cells of the embryo sac, the egg cell and the central cell, distinctive morphologies (Huang and Russell, 1992). will undergo double-fertilization by the two sperm cells of the pollen The precise migration and positioning of the nuclei at the eight- (Fig. 1C). The fertilization of the egg cell within the embryo sac by nucleate FG5 stage marks the distinction between these nuclei in one of the sperm cells delivered by the pollen tube results in the their cell-fate specification (Huang and Sheridan, 1994; Webb and diploid zygote, which will initiate the next sporophyte generation Gunning, 1994). At the micropylar pole, the two most distal nuclei (Fig. 1C,D). The fertilization of the central cell by the second sperm will form the future synergids. Of the remaining two nuclei, the cell results in the triploid endosperm, which functions as a nutritive more distal nucleus of the pair will form the future egg cell, whereas source for the embryo or the germinating seedling (Fig. 1C,D). the more central nucleus will become one of the two polar nuclei of A schematic outline of the development of a seven-celled embryo the central cell.
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