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Magazine R718

Primer tissues. These form multicellular The first gametophytic division -like structures, each of which is asymmetric, producing one develops into a leafy . The large and one small cell. In C. mature produce richardii, the large cell divides male and female sexual organs, again asymmetrically to produce development the antheridia and archegonia, another small cell, which later respectively. The gametophyte is develops into the , a - often sexually distinct, and like structure. The small cell from Wuxing Li and Hong Ma are either male or female. the first division becomes the Each has an outer protonemal initial, which divides Unlike animals, which produce layer that encloses and protects further to form a linear three- single-celled directly thousands of motile , which celled . The middle cell from meiotic products, plants swim through available external then undergoes a transition in have generations which alternate water layer to the . Fertilization divisional plane, forming a two- between the diploid at the base of the cylindrical dimensional structure. During and haploid gametophyte (Figure produces a diploid development, a 1A). The diploid sporophytic which develops into an is formed in the two- generation develops from the unbranched sporophyte. The dimensional plane and gives rise zygote, the fusion product of sporophyte consists of a thin stalk to the male antheridia and the haploid gametes. Sporophytic attached to the gametophyte, and female archegonia. In the male cells undergo to produce a that encloses the gametophyte, most cells, except haploid , which divide sporophytic meiotic cells. the apical and basal cells, will mitotically to form the In recent years, the develop into antheridia. multicellular gametophyte. Certain and In C. richardii, each antheridium cells in the gametophyte Funaria hygrometrica have contains an outer sterile subsequently differentiate into emerged as attractive model and an inner spermatogeneous gametes. systems for studying gene cell, which undergoes five rounds Land plants are divided into function in non-vascular plants of to produce 32 small four groups (Figure 1B). The most because of the relative ease of spermatocytes. Further basal group, the , molecular manipulation by differentiation of the including mosses and liverworts, homologous recombination. spermatocytes generates lack vascular tissues. Plants of Mutants affecting gametophyte functional sperm cells, each with the second group, including development have been isolated a coil structure and a . In and horsetails, have a vasculature and their analysis should provide the flask-shaped archegonium, a but lack . insights into the molecular basis highly cytoplasmic egg is formed and angiosperms both produce of gametophyte development in near the interior base. During seeds. Angiosperms produce mosses. fertilization, the archegonium and include most of the opens a channel allowing direct familiar plants. Although land Gametophyte development in access of the sperm to the egg. plants in all four groups share a ferns The differences between male common life cycle (Figure 1A), the Unlike bryophytes, in vascular and hermaphrodite gametophyte relative sizes of, and nutritional plants the sporophyte generation development allow screening for relationship between, the is macroscopic but the C. richardii mutants that have sporophyte and gametophyte gametophyte generation is altered determination. Studies vary greatly among different microscopic. gametophytes of such mutants have led to a groups of land plants. are free living and they require model for sexual determination in Gametophyte development also moist conditions for reproduction. fern gametophyte development. varies among these groups. Most ferns, such as Ceratopteris richardii — an attractive genetic Gametophyte development in Gametophyte development in model system — are gymnosperms mosses homosporous, producing only one In plants, the sporophytic In bryophytes, the sporophyte is kind of . In isolation, a C. generation is dominant and free- minute and dependent on the richardii spore develops into a living, and the gametophytes are relatively prominent and hermaphrodite gametophyte, very small and dependent on the nutritionally independent producing both and sperm. sporophyte for nutrients. Among gametophyte for resources. The The gametophyte becomes a gymnosperms, have male gametophyte looks like a male if exposed to enough of the and female cones on the same miniature herb, with tiny -like pheromone during . Other gymnosperms bear photosynthetic organs. The its early development. After this male and female reproductive gametophyte generation begins initial period, the gametophyte is structures on different individuals. as a dormant spore, which insensitive to antheridiogen and In all gymnosperms, the male germinates under appropriate develops into a hermaphrodite, gametophyte ( grain) reaches conditions to produce filamentous which produces and secretes the female reproductive structure and branching protonemal antheridiogen. helped by wind or animals. Magazine R719

The cones bear scale-like male A B Seedless vascular or female organs, called Bryophytes plants Gymnosperms Angiosperms microsporophylls and megasporophylls, respectively. In Sporophyte (2n) , the microsporophyll has Mitosis Fertilization Meiosis two , sac-like LivewortsHornwortsMosses Club mossesHorsetailsFerns ConifersGnetales Angiosperms structures filled with many diploid Sperm cells + eggs Spores mother cells, which undergo meiosis to produce Mitosis haploid . The Gametophyte (1n) megasporophyll has two , each containing a single Current Biology mother cell which produces four meiotic products, Figure 1. The life cycle and phylogenetic tree of land plants. one of which becomes the (A) The life cycle. From the diploid (2n; red) sporophyte generation, sporocytes undergo functional megaspore. The meiosis and produce haploid spores (1n; green). Mitoses then form gametophytes, microspore and megaspore then which produce gametes, sperm cells and eggs. The fertilization of an egg with a sperm develop into male and female cell produces a zygote. (B) A phylogenetic tree of major land plants, showing the rela- gametophytes, respectively. tionships of the groups of plants discussed here. In the west white Pinus monticola, male gametophyte Male gametophyte development in completely envelopes the development involves a series of angiosperms generative cells. In contrast, the asymmetric cell divisions. First, Angiosperms are defined by generative nucleus is more tightly the microspore divides to produce having seeds in the enclosing organized and less active in a large central cell and a small derived from the of a . transcription. The generative cell first primary prothallial cell. The The flower consists of primarily later undergoes a second mitosis central cell divides to produce a sporophytic tissues, with both to produce two sperm cells. second primary prothallial cell and male and female gametophytes Pollen development depends on an antheridial initial. Another which are highly reduced in size in the function of a surrounding unequal division of the antheridial comparison to all other land sporophytic tissue called . initial results in a large tube cell plants. Angiosperms also have the The pollen dehydrates during and a small antheridial cell. The unique property of double maturation; after , the small antheridial cell divides to fertilization, producing a usually pollen grain rehydrates and form a sterile cell and a generative triploid in addition to germinates to produce a pollen cell, which divides later to form the . The male tube. This tube grows towards the two sperm cells. gametophyte is formed in the , providing a passageway for In the female cone of P. anthers of the , and the the sperm cells to reach the monticola, the megaspore female gametophyte is located in female gametophyte. Because the undergoes multiple mitoses, the ovules within the pistil. female gametophyte is within the followed by cellularization, to In the anther, four pollen sacs female reproductive organ of the produce about 2000 primary (locules) contain numerous sporophyte, the must prothallial cells. Three to five microspore mother cells, each of extend considerable distances — primary prothallial cells near the which undergoes meiosis to many times the size of the pollen micropyle, an opening of the produce four microspores in a grains — to reach the egg. ovule, enlarge and develop into tetrad (Figure 2A). The male archegonial initial cells. Each gametophyte generation begins Female gametophyte development initial cell divides and develops with the microspore. Initially, the in angiosperms into an archegonium containing microspore has a uniformly The female reproductive organ, an egg and other supportive distributed cytoplasm with a the ovary, completely encloses cells. centrally located haploid nucleus. one or more ovules, the location After pollen lands on the A large later forms at the of the female gametophyte, female cone, it germinates to center, displacing the nucleus to commonly called the embryo sac. produce a pollen tube that grows the side. In many flowering plants, The ovule is attached to the inner towards the female gametophyte, including the model species surface of the ovary, with a often over two consecutive Arabidopsis and maize, two micropyle at the distal end. Each growth seasons. One sperm cell mitotic divisions occur during ovule contains a single from each pollen grain fertilizes a pollen development. The first megaspore mother cell which is single egg, while the other division produces a large surrounded by integuments, the degenerates. Typically, the egg vegetative cell and a much smaller protective and nutritive layers of cells of all archegonia of a female generative cell. The vegetative cell sporophytic cells. The megaspore gametophyte are fertilized and inherits most of the cytoplasm mother cell undergoes meiosis to begin embryo development, but from the microspore cell, has a generate four haploid products. usually only one of the relatively loose nucleus that is Three of the haploid products develops to maturity. active in transcription, and degenerate and only the one near Current Biology Vol 12 No 21 R720

A Generative Nucleus Vegetative cell cell

Sperm Vegetative cells nucleus

Microspore Microspores Vacuolization First, asymmetric Second mitotic division mother cell mitotic division and pollen tube growth

Antipodal Antipodal B Functional cells cells megaspore

Central nuclei Nuclei Central nuclei

Degenerated Synergid Synergid cells cells Egg cell

Megaspore Female Eight-nucleate Cellularization Nuclei migration mother cell meiosis stage cell Current Biology

Figure 2. Male and female gametophyte development in angiosperms. (A) Male gametophyte. Meiosis produces four microspores; vacuolization is accompanied by nuclear migration. The microspore divides asymmetrically to form a large vegetative cell and a small generative cell. The generative cell then produces two sperm cells, which later move toward the ovule through the growing pollen tube. (B) Female gametophyte. Meiosis in the megaspore mother cell produces four haploid products; one becomes the megaspore. During development, three rounds of mitosis form two clusters of four nuclei at the two ends of the female gametophyte. Cellularization generates seven cells: one egg cell and two synergid cells form the egg apparatus at the distal end, and three antipodal cells at the proximal end. In the large central cell, two nuclei migrate toward the center and fuse together. the proximal end becomes the Angiosperms exhibit double flowers and protective fruit are all functional megaspore. fertilization. When the pollen tube thought to have contributed to the Depending on the pattern of reaches the distal end of the success of angiosperms. subsequent cell divisions, four ovule, it grows into the micropyle types of female gametophyte and penetrates into one of the two Genetic studies of gametophyte development have been synergids. The two sperm cells development in angiosperms described. In most flowering are released: one fuses with the Because the angiosperm species, including egg cell to produce the zygote; gametophytes are microscopic Arabidopsis and maize, the the other fuses with the central and dependent on the megaspore undergoes a cell, giving rise to the precursor of sporophyte, genetic studies polygonum-type pathway that the endosperm. In a polygonun- usually involve mutagenesis of the results in a seven-celled female type embryo sac, the endosperm sporophyte generation. Mutations gametophyte (Figure 2B). During is a triploid organ. But in the water that cause defects in sporophytic this type of embryo sac lily Nuphar polysepalum, and tissues resulting in sterility or development, three rounds of several other basal angiosperms, reduced fertility are described by mitotic divisions occur without the embryo sac is produced by several reviews cited in the cytokinesis. The resulting eight two rounds of mitosis following references and will not be nuclei are separated by a large meiosis, and contains four haploid discussed here. Examples of central vacuole into two groups, cells, including the egg and gametophytic mutations that each of which contains four central cells. Consequently, both affect gametophyte development nuclei and is located near one products of the double are discussed below. Because the end of an elongated embryo sac. fertilization, the zygote and the gametophyte is haploid, even The embryo sac then undergoes endosperm, are diploid. recessive mutations in essential cellularization, producing three Regardless of , the genes will not be transmitted to antipodal cells at the proximal endosperm is a unique the next generation. Thus, a end and two synergid cells and angiosperm organ which is an heterozygous sporophyte with a one egg cell at the distal end. important nutritional structure that female gametophytic mutation is The remaining two nuclei, and supports embryo and/or seedling semi-sterile, because half of the much of the cytoplasm at the development. The presence of embryo sacs will carry the mutant center, form a large central cell. endosperm, animal-attracting allele and fail to develop. A similar Magazine R721 heterozygous plant with a male the two-nucleate stage seems to dimorphism of reproductive gametophytic mutation is still be lost; in addition, the second structures may represent an fertile, because half of the pollen and third rounds of mitosis are not evolutionary trend that might have is normal and can successfully synchronized, and sometimes provided increasing fitness to land pollinate the pistil. Such mutations only the distal nucleus undergoes plants. can be detected by their failure to the second mitosis. Furthermore, Molecular and genetic studies transmit via the pollen. after cellularization, some distal have begun to reveal genes that Several mutations in cells undergo extra divisions, control several aspects of Arabidopsis and maize have been resulting in an indeterminate gametophyte development, identified that affect different number of eggs and polar nuclei. including sexual determination, stages of male gametophytic In Arabidopsis gf and fem cell polarity establishment, cell development. Arabidopsis gemini mutants, female development is fate determination and the control pollen1 pollen grains show an arrested at different stages. of cell division. We can look incompletely penetrant These studies suggest that forward to a rapid expansion in phenotype; the mutant pollen many genes may be involved in the knowledge of gametophyte grains exhibit equal, unequal or regulating rounds of mitoses, cell development, with the use of partial division for the first mitosis, polarity, and nuclear position genetic, genomic, and possibly because of an inability to during gametophyte development. evolutionary approaches to establish a polar nuclear position. Cell-cycle control and identify both conserved and So GEMINI POLLEN1 may be cytoskeleton function are likely specialized components of required for proper nuclear important for these processes. regulatory networks. migration before the first mitosis. These mutants and others should In maize mutant gaMS-2 pollen, provide valuable insights into the Acknowledgements the first mitosis produces two regulation of gametophyte We thank D. Zhao, L. Zahn, H. similar cells; most pollen grains development. In addition, Kong for helpful comments on this are blocked after the first mitosis. genomic projects in combination manuscript. The work in our lab is Maize gaMS-1 mutant with reverse genetic tools should supported by NSF, NIH, and microspores develop into non- also be very informative. USDA grants to H.M. and by funds functional pollen grains with from the Biology Department and reduced sizes, usually arrested Conclusions the Life Sciences Consortium at after the first mitosis. The genes The gametophyte generation in the Pennsylvania State University. gaMS-1 and gaMS-2 may be land plants has evolved from a required for normal progression free-living and relatively complex Key References through the first mitosis. organism into microscopic Anderson, E.D. and Owens, J.N. In the Arabidopsis mutant structures dependent on the (2000). Microsporogenesis, pollination, pollen and limpet pollen (lip) pollen, the sporophyte. The strong male gametophyte development in generative cell fails to migrate vasculature, sporophyte- Taxus brevifolia. Ann. Bot.-London inward after the first mitosis. In supported gametophytes and 86, 1033–1042. another Arabidopsis mutant, drought-resistant pollen are likely Banks, J.A. (1999). Gametophyte development in ferns. Annu. Rev. sidecar pollen (scp), pollen grains to have contributed to the Plant Physiol. Plant Mol. Biol. 50, often contain an extra vegetative success of seed plants. The 163–186. cell. The extra vegetative cell is protective ovary/fruit and the Cove, D. (2000). The moss, produced before the asymmetric triploid endosperm most likely Physcomitrella patens. J. Plant Growth Regul. 19, 275–283. division, suggesting that SCP is further increased the reproductive Grossniklaus, U. and Schneitz, K. an important negative regulator fitness of flowering plants, making (1998). The molecular and genetic that prohibits the microspore from them the most successful group basis of ovule and dividing symmetrically. of plants. megagametophyte development. Several female gametophytic Understanding the evolution of Semin. Cell Dev. Biol. 9, 227–238. McCormick, S. (1993). Male mutants exhibit defects at gametophytic gametophyte development. Plant different stages. The maize lethal is an important aspect in the Cell 5, 1265–1275. ovule2 mutation results in study of gametophytes. Mosses Owens, J.N. and Bruns, D. (2000). gametophytes arrested at one-, generally produce Western white pine (Pinus monticola Dougl.) reproduction: I. two- and four-nucleate stages, morphologically uniform Gametophyte development. Sex. suggesting this gene may function gametophytes which differ only in Plant Reprod. 13, 61–74. in regulating female nuclear sexual organs, whereas ferns Williams, J.H. and Friedman, W.E. division cycles. Similarly, the produce sexually dimorphic (2002). Identification of diploid endosperm in an early angiosperm development of Arabidopsis gametophytes generally from a lineage. Nature 415, 522–526. hadad mutant embryo sacs single type of spore. The arrests after one or two mitotic gametophytes in seed plants, Department of Biology and the Life divisions, and there may be a both gymnosperms and Sciences Consortium, the Intercollege defect in nuclear migration. In angiosperms, are genetically pre- Graduate Program in , another maize mutant, determined and structurally the Pennsylvania State University, indeterminate gametophyte1 (ig), dimorphic from the first mitosis. University Park, Pennsylvania 16802, the polarity of the embryo sac at Progressively determined sexual USA.