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First published online December 24, 2008; doi:10.3732/ajb.0800311 American Journal of Botany 96: 129-143 (2009) © 2009 Botanical Society of America, Inc. |
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Special Invited Papers |
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309 USA
Received for publication 16 September 2008. Accepted for publication 31 October 2008.
ABSTRACT
For more than a century, the common ancestor of flowering plants was thought to have had a seven-celled, eight-nucleate Polygonum-type female gametophyte. It is now evident that not one, but in fact three, patterns of female gametophyte development and mature structure characterize the common ancestors of the four most ancient clades of extant angiosperms: Amborella-type, Nuphar/Schisandra-type and Polygonum-type. The Amborella-type female gametophyte is restricted to a single extant species, Amborella trichopoda, and at maturity consists of eight cells and nine nuclei. Development of the Amborella-type gametophyte is essentially identical to the Polygonum-type except that there is an additional and asynchronous cell division at the micropylar pole prior to maturation that produces a third synergid and the egg cell. The Nuphar/Schisandra-type female gametophyte is four-nucleate and four-celled and at maturity contains a typical three-celled egg apparatus and a central cell with a single haploid polar nucleus. This type of gametophyte appears to be universal among extant members of the Nymphaeales (including Hydatellaceae) and Austrobaileyales. Based on explicit reconstruction of character distribution and evolution, the Polygonum-type female gametophyte is certain to be representative of the common ancestors of monocots, eudicots, magnoliids, Ceratophyllaceae, and Chloranthaceae. There are compelling biological reasons to suggest that the four-celled, four-nucleate female gametophyte (as found in Nymphaeales and Austrobaileyales) is ancestral among angiosperms, with transitions to Polygonum-type female gametophytes separately in the Amborellales and in the ancient angiosperm clade that includes all angiosperms except Amborella, Nymphaeales, and Austrobaileyales. Subsequent to the evolution of a seven-celled, eight-nucleate Polygonum-type female gametophyte in the Amborellales, we hypothesize that a peramorphic increase in egg apparatus cell number took place and led to the unique situation in which there are three synergids in Amborella trichopoda.
Key Words: Amborella • Austrobaileyales • double fertilization • endosperm • evo-devo • female gametophyte • Nymphaeales
For nearly a century, the common ancestor of flowering plants was thought to have had a seven-celled, eight-nucleate Polygonum-type female gametophyte (e.g., Porsch, 1907
; Maneval, 1914; Chiarugi, 1927; Schnarf, 1931; Maheshwari, 1950; Johri, 1963; Davis, 1966; Bhandari, 1971; Foster and Gifford, 1974; Stebbins, 1974; Palser, 1975; Takhtajan, 1976; Favre-Duchartre, 1984; Cronquist, 1988; Battaglia, 1989; Haig, 1990; Donoghue and Scheiner, 1992; Johri et al., 1992; Tobe et al., 2000). This conclusion was often reached through the erroneous assumption that "common" features of a clade are likely to be plesiomorphic (more than 80% of angiosperms produce a Polygonum-type female gametophyte; Palser, 1975). Moreover, the prevalence of Polygonum-type female gametophytes among Magnoliales, Laurales, and Winterales (Canellales), along with the phylogenetic assumption that these groups were among the most ancient of angiosperm lineages, was taken as prima facie evidence of the plesiomorphic ("primitive") nature of the monosporic eight-nucleate, seven-celled female gametophyte among angiosperms.
Beginning in the late 1990s, a series of molecular phylogenetic analyses fundamentally altered our thinking about the identities of the most ancient lineages of flowering plants (e.g., Mathews and Donoghue, 1999; Parkinson et al., 1999; Qiu et al., 1999, 2000, 2005, 2006; Soltis et al., 1999, 2000a, 2000b, 2007; Graham and Olmstead, 2000; Graham et al., 2000; Zanis et al., 2002; APG II, 2003; Kim et al., 2004; Soltis and Soltis, 2004; Leebens-Mack et al., 2005; Hansen et al., 2007; Jansen et al., 2007; Moore et al., 2007; Saarela et al., 2007; Doyle, 2008; Qiu and Estabrook, 2008). These diverse phylogenetic analyses continue to provide compelling evidence that Amborella trichopoda Baill., Nymphaeales sensu lato (Hydatellaceae, Cabombaceae, Nymphaeaceae), and Austrobaileyales (Austrobaileyaceae, Trimeniaceae, Illiciaceae, Schisandraceae) are three of the four most ancient extant lineages of angiosperms. For the record, the fourth most ancient lineage is the clade that includes all other angiosperms and is sister to Austrobaileyales (Arabidopsis (DC.) Hyhnh. and Zea L. are members of one of the four most ancient clades of flowering plants). Thus, after a century of concerted effort to study the biological features of Magnoliales, Laurales, and Winterales (Canellales) for the purposes of reconstructing early angiosperm evolutionary history, the focus shifted abruptly to the largely understudied members of the Amborellales, Nymphaeales, and Austrobaileyales. Evolutionary morphologists, anatomists, embryologists, and reproductive biologists interested in deciphering the evolutionary genesis of the currently dominant clade of photosynthetic life on earth began to look carefully at the biology of these newly identified most ancient angiosperm lineages.
The arrival of new (and potentially robust) phylogenetic hypotheses for the most ancient lineages of angiosperms specifically led to an intensive effort to examine the development of the female gametophyte (and other embryological features) in Amborella Baill., Nymphaeales and Austrobaileyales. Tobe et al. (2000) were the first to examine Amborella and concluded that the female gametophyte was, indeed, Polygonum-type, consistent with the established view that the first angiosperms produced a seven-celled, eight-nucleate female gametophyte. A survey of the embryological literature for Nymphaeales and Austrobaileyales also reported that Polygonum-type female gametophytes were characteristic of these newly identified most ancient angiosperm clades (Tobe et al., 2000). Thus, although a major shift had occurred in angiosperm phylogenetic hypotheses, the century-old hypothesis as to the plesiomorphic condition for the female gametophyte (Polygonum-type) remained unaltered at the turn of the millennium.
In fact, the historical primary embryological literature is far from clear about the developmental and structural characteristics of the female gametophytes of members of the Nymphaeales and Austrobaileyales (see Friedman and Williams, 2003, for a review)—and this realization stimulated a series of new investigations of the embryology of these two clades. In Nuphar Sm. (Nymphaeaceae), Illicium L. (Illiciaceae), Kadsura Juss. (Schisandraceae), and Austrobaileya C. T. White (Austrobaileyaceae), mature female gametophytes were definitively shown to contain only four nuclei and four cells at maturity (Nuphar-type or Schisandra-type) (Williams and Friedman, 2002, 2004; Friedman et al., 2003; Tobe et al., 2007). Shortly after the surprising discovery in 2007 that members of the Hydatellaceae (Hydatella Diels and Trithuria Hook.f.) were not monocots, but rather, water lilies (Saarela et al., 2007), four-celled and four-nucleate female gametophytes were reported in this unusual clade of Nymphaeales (Friedman, 2008; Rudall et al., 2008). Finally, a new examination of the Amborella female gametophyte demonstrated that it is not Polygonum-type, but instead a unique nine-nucleate, eight-celled structure, now known as Amborella-type (Friedman, 2006a). Thus, only five years after the outset of a new wave of embryological studies of the ancient angiosperm clades Amborellales, Nymphaeales, and Austrobaileyales, it is clear that none of the representatives of these lineages produces a Polygonum-type female gametophyte—a dramatic reversal of a century of evolutionary thought about this key reproductive feature.
In light of the importance of Amborella to the reconstruction of early angiosperm evolutionary history, a thorough investigation of the developmental biology of its female gametophyte has been warranted and is herein presented. Moreover, given the absence of Polygonum-type female gametophytes among three of the most ancient lineages of extant flowering plants, careful analysis of the evolutionary implications of this new set of findings is required. Using recent insights into the developmental biology of the female gametophytes of flowering plants, we will reconstruct explicit hypotheses for the plesiomorphic condition for the angiosperm female gametophyte and the earliest phases of diversification of this egg- and central cell-producing structure that ultimately gave rise to the patterns of sexual reproduction that characterize the vast majority of flowering plants.
MATERIALS AND METHODS
Plant collections
Carpellate buds and open flowers of Amborella trichopoda were collected at Plateau de Dogny, New Caledonia (GPS coordinates = 21°37.253'S, 165°52.130'E) between the elevations of 601 m and 949 m a.s.l. (with permission from the Office of the Department of Natural Resources, Southern Province, New Caledonia) and from specimens growing in the University of Colorado greenhouses in Boulder, Colorado. Hand pollinations were performed on flowers in the field and in the greenhouse.
Bright field and fluorescence microscopy
Flowers were fixed for 24 h either in 3:1 (95% ethanol:acetic acid) and stored in 70% ethanol or in 4% glutaraldehyde in 50 mM PIPES buffer and stored in PIPES buffer. Specimens were dehydrated through an ethanol series, then infiltrated and embedded in glycol methacrylate (JB-4 embedding kit, Polysciences, Warrington, Pennsylvania, USA). Embedded flowers were serially sectioned into 4-µm thick ribbons. Sectioned flowers were first stained with 0.25 µg/mol of 4',6-diamidino-2-phenylindole (DAPI) in 0.05 Tris buffer (pH 7.2) and examined. Selected slides were later stained with Schiff’s reagent (Fisher Scientific, Fair Lawn, New Jersey, USA) and/or toluidine blue (0.1%) for additional examination under bright field conditions. Digital imaging was performed on a Zeiss Axiocam digital camera using brightfield and fluorescence optics. Fluorescence was viewed with an HBO 100 W burner (Carl Zeiss, Oberkochen, Germany) using a UV filter set (model 48702) with excitation filter (365 nm, band pass 12 nm), dichroic mirror (FT395), and barrier filter (LP397). Images were processed with Adobe (San Jose, California, USA) Photoshop 9.0. Image manipulations were restricted to operations applied to the entire image, except as noted in specific figure legends.
Transmission electron microscopy
Flowers were fixed for 24–48 h in a solution of 2% paraformaldehyde, 1% glutaraldehyde, and 2% acrolein in 50 mM PIPES buffer (pH 6.8) and were stored in PIPES buffer. Ovules were dissected from carpels and postfixed in 2% osmium tetroxide at 4°C for 2 h. Specimens were dehydrated through an ethanol series and infiltrated with propylene oxide for 1.5 h. Specimens were then infiltrated with and embedded in Spurr’s low viscosity embedding medium (Polysciences). Embedded ovules were sectioned 70 nm thick with a diamond knife and collected onto thin, bar square 200-mesh copper grids. Sections were stained with lead citrate and examined with a Philips CM 10 transmission electron microscope. Images were processed with Adobe Photoshop 9.0. Image manipulations were restricted to operations that were applied to the entire image, except as noted in specific figure legends.
RESULTS
Female gametophyte development in Amborella
A single megasporocyte is produced in the center of each ovule. The megasporocyte nucleus occupies the center of the cell, and a cytoplasmically dense zone forms between it and the chalazal wall (Fig. 1A). This cytoplasmically dense zone persists through the end of megasporogenesis. Meiosis I yields a dyad of two uninucleate cells, typically divided by a transverse cell wall (Fig. 1B). Meiosis II results in a linear tetrad of megaspore cells (Fig. 1C). The chalazal-most cell becomes the functional megaspore, and the other three megaspores degenerate before syncytial development of the female gametophyte is initiated. The functional megaspore has a large centrally placed nucleus that is surrounded by a vacuole. Cytoplasmic strands radiate from the nucleus to the lateral sides, but not the poles, of the cell (Fig. 1D).
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) that will contribute to the mature egg apparatus (Fig. 4). One of these two daughter cells is positioned chalazal to, and shares interfaces with, the other three cells of the egg apparatus. It also shares an interface with the central cell, but not with the wall of the female gametophyte. This cell will differentiate into the egg cell (described later).
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The three antipodal cells at the chalazal pole of the mature female gametophyte are densely cytoplasmic and contain rough endoplasmic reticulum and numerous plastids (Figs. 4B, C, 5D). The nuclei are small and retain their torpedo shape. Proliferation of antipodal cells, resulting in seven antipodals in an individual female gametophyte, was observed twice among 166 mature female gametophytes examined. The overall size of the mature eight-celled, nine-nucleate female gametophyte is significantly larger than that of the seven-celled, eight-nucleate stage.
Fertilization in Amborella
In Amborella, the pollen tube enters the ovule through the micropyle, proceeds between cells of the nucellus, and enters the egg apparatus via one of the synergids, which appears to be degenerated (Fig. 6). In two instances, we observed three extra nuclei (inferred to be the two sperm nuclei and the tube nucleus), in close proximity to one another, just outside of the tip of a pollen tube that had penetrated the egg apparatus of the female gametophyte (Fig. 7). Sperm nuclei were not observed fusing with the egg nucleus or the secondary nucleus. Nevertheless, circumstantial evidence indicates that Amborella appears to undergo double fertilization.
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The primary endosperm nucleus is always found in the chalazal region of the female gametophyte. The first division of the primary endosperm nucleus produces a pseudotransverse wall at the chalazal end of the female gametophyte, creating two domains of endosperm. Endosperm development in Amborella has been described in Floyd and Friedman (2001) .
DISCUSSION
The Amborella female gametophyte produces eight cells and nine nuclei. This stands in marked contrast with the four-celled, four-nucleate female gametophytes (Nuphar/Schisandra-type) found in Nymphaeales (Batygina et al., 1982; Galati, 1985; Winter, 1987, 1993; Titova, 1990; Winter and Shamrov, 1991a, b; Van Miegroet and Dujardin, 1992; Shamrov, 1998; Williams and Friedman, 2002; Friedman and Williams, 2003; Friedman, 2008; Rudall et al., 2008) and Austrobaileyales (Yoshida, 1962; Swamy, 1964; Solntseva, 1981; Battaglia, 1986, 1989; Friedman et al., 2003; Williams and Friedman, 2004; Tobe et al., 2007) and differs from the seven-celled, eight-nucleate Polygonum-type common to most monocots, magnoliids, and eudicots (Friedman and Williams, 2003). The absence of Polygonum-type female gametophytes in the most ancient angiosperm lineages is a startling reversal of a century of thought in which it had been universally concluded that this type of female gametophyte characterized the first angiosperms as well as extant members of the most ancient lineages.
Female gametophyte development in Amborella
As with the overwhelming majority of angiosperms (Maheshwari, 1950) including Nymphaeales and Austrobaileyales, the female gametophyte of Amborella is derived from the chalazal-most megaspore. After the first mitotic division of the functional megaspore, the two resulting nuclei migrate to opposite poles of the cell, as is also characteristic in Polygonum-type female gametophytes, but not in the four-nucleate, four-celled female gametophytes of Nymphaeales and Austrobaileyales (Fig. 10). At each pole in the binucleate female gametophyte of Amborella, the nucleus undergoes two rounds of mitosis to produce four nuclei. One nucleus from each pole migrates toward the center of the syncytium, after which cellularization of the remaining three nuclei at each pole occurs. After cellularization, a final cell division occurs within the micropylar region of the female gametophyte (Fig. 10). It is this final division that produces the egg cell and a third synergid and represents the final step necessary to prepare the female gametophyte of Amborella for fertilization.
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), that reported a seven-celled, eight-nucleate Polygonum-type female gametophyte with antipodals that degenerate before fertilization. However, it is likely that FAA (formalin, acetic acid, ethanol) fixation, coupled with paraffin embedding is unable to provide sufficient resolution to observe the extra cell in the egg apparatus or detect the small antipodals. We conclude, as did Rudall (2006), that the differing results of these two embryological studies, with respect to the number of synergids and persistence of antipodals, are not due to teratology or polymorphic conditions in Amborella. Beyond our extensive sampling with light and fluorescence microscopy (over 160 female gametophytes from many genetically distinct plants in the field and greenhouse were observed) to document the developmental basis for the mature structure of the female gametophyte of Amborella, serially sectioned female gametophytes prepared for transmission electron microscopy are definitive; the egg apparatus contains four cells (three synergids and an egg cell), and the antipodals are persistent (Fig. 5).
It is worth noting that the potential for teratological or polymorphic structures associated with the female gametophytes of Amborella does exist. We found two instances, among over 160 mature female gametophytes examined, of antipodal proliferation. Antipodal proliferation has been reported in numerous basal eudicots, magnoliids, and monocots (Johri et al., 1992; Williams and Friedman, 2004; Holloway and Friedman, 2008).
Comparative aspects of female gametophyte development in Amborella and other ancient angiosperm lineages
It is now evident that not one, but in fact three, patterns of female gametophyte development and mature structure (Fig. 10) characterize the common ancestors of the four most ancient clades of extant angiosperms (Amborellales, Nymphaeales, Austrobaileyales, and the clade that includes all other angiosperms): Amborella-type, Nuphar/Schisandra-type, and Polygonum-type (Friedman, 2006a, b). The Amborella-type female gametophyte is restricted to a single extant species, Amborella trichopoda. The Nuphar/Schisandra-type appears to be universal in the Nymphaeales and Austrobaileyales (Williams and Friedman, 2002, 2004; Friedman et al., 2003; Friedman, 2006b, 2008; Tobe et al., 2007; Rudall et al., 2008), and this specifically includes members of the Hydatellaceae (Friedman, 2008; Rudall et al., 2008), which have recently been discovered to be part of the Nymphaeales (and not monocots, as long believed). Based on explicit reconstruction of character distribution and evolution, the Polygonum-type is certain to be representative of the common ancestor of monocots, eudicots, magnoliids, Ceratophyllaceae, and Chloranthaceae (Friedman and Williams, 2003).
Comparative evolutionary developmental analyses of the four-nucleate, four-celled female gametophytes in the ancient angiosperm lineages Nymphaeales and Austrobaileyales led to the key insight that the female gametophytes of all flowering plants are fundamentally modular entities (Friedman and Williams, 2003, 2004; Friedman et al., 2008) composed of iterative sets of quartets of nuclei (sensu Porsch, 1907; Schnarf, 1936; Cocucci, 1973; Favre-DuChartre, 1976; Battaglia, 1989; Haig, 1990). Development of a standard angiosperm female gametophyte module involves three basic ontogenetic stages: (1) positioning of a single nucleus within a developmentally autonomous cytoplasmic domain of the female gametophyte; (2) two free-nuclear mitoses to yield four nuclei within that domain; and (3) partitioning of three uninucleate cells adjacent to the pole such that the fourth nucleus is confined to the central cell of the female gametophyte (Fig. 11; Friedman and Williams, 2003; Friedman et al., 2008). Angiosperm female gametophytes are formed from one (e.g., Nymphaeales and Austrobaileyales), two (e.g., Polygonum-type) or four (e.g., Penaea-type) developmental modules.
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From a comparative perspective, the ontogeny of the Amborella-type female gametophyte is most similar to that of the common Polygonum-type. In Amborella and in angiosperms with a Polygonum-type female gametophyte, the uninucleate functional megaspore divides mitotically to produce two daughter nuclei that migrate to opposite poles (developmental domains). Each nucleus then initiates an independent developmental module that produces four free nuclei (for a total of eight free nuclei). At the eight-nucleate stage, cytokinesis partitions three nuclei into three cells at each pole, while the remaining free nucleus from each of the two modular quartets is contributed to the common cytoplasm of the central cell. Thus, following cellularization of the syncytium, both Amborella-type and Polygonum-type female gametophytes are seven-celled and eight-nucleate (Fig. 10).
In contrast to angiosperms with Polygonum-type female gametophytes, cellularization of the eight-nucleate syncytium into seven cells in Amborella does not constitute the terminus of somatic and sexual ontogeny. After cellularization in Polygonum-type female gametophytes, an egg apparatus with two synergids and one egg cell differentiates (Maheshwari, 1950). However, in Amborella, formation of an egg cell and final differentiation of an egg apparatus does not occur until a subsequent cell division yields a nine-nucleate, eight-celled female gametophyte with a four-celled egg apparatus (three synergids and an egg cell). Importantly, the egg cell is formed from this final asynchronous division (Friedman, 2006a). Thus the key (and only) developmental difference between Polygonum-type and Amborella-type female gametophytes involves either the developmental addition of a terminal ontogenetic stage (peramorphosis), assuming that the Amborella-type egg apparatus is apomorphic, or the developmental advancement of sexual maturation (i.e., the formation of an egg) accompanied by truncation of ontogeny (paedomorphosis), assuming that the Polygonum- and Nuphar/Schisandra-type three-celled egg apparatus is apomorphic (Fig. 10).
Development of the Amborella-type female gametophyte differs critically from the Nuphar/Schisandra-type at two key points of ontogeny. In Nymphaeales (Hydatellaceae, Cabombaceae, and Nymphaeaceae) and Austrobaileyales (Austrobaileyaceae, Trimeniaceae, Illiciaceae, and Schisandraceae) after the first mitotic division of the functional megaspore, the two resulting nuclei do not migrate to opposite poles of the female gametophyte to establish two developmental modules. Instead, both nuclei at the two-nucleate stage in Nymphaeales and Austrobaileyales remain in the micropylar region (Fig. 10). As such, only a single developmental module is initiated in the Nuphar/Schisandra-type of female gametophyte. This produces a quartet of nuclei at the micropylar end of the female gametophyte (Friedman and Williams, 2003; Friedman et al., 2008).
The second point of ontogenetic divergence between the Amborella-type and Nuphar/Schisandra-type female gametophyte involves the number of cells and process of differentiation of the egg apparatus (as is the case with the Polygonum-type described earlier). In Amborella, the egg apparatus contains four cells and the egg cell is formed by a terminal asynchronous cell division. In members of the Nymphaeales and Austrobaileyales, the egg apparatus is three-celled, and the egg differentiates directly from one of the three cells at the micropylar end of the female gametophyte formed during cellularization (Fig. 10).
Hypothesized plesiomorphic states and character transitions: Analysis of evolutionary history
Female gametophytes of angiosperms, as with any organisms, are an amalgam of biological traits. For the purposes of our analysis, there are two key features of female gametophyte development that vary among ancient lineages of angiosperms: the number of developmental modules initiated (one or two) and the number of cells present in the egg apparatus (three or four).
It is equally parsimonious to hypothesize either character state for the egg apparatus (three-celled or four-celled) as plesiomorphic (Fig. 12). As such, the unique (among angiosperms) asynchronous cell division to form an egg and a third synergid may be viewed as a derived condition that evolved somewhere along the 130 million year long branch that leads to Amborella trichopoda. Alternatively, the four-celled egg apparatus could represent the original condition for angiosperms (Friedman, 2006a).
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Beyond parsimony
Simple parsimony analysis of the distribution and evolution of female gametophyte types among ancient lineages of angiosperms does not appear to provide any resolution of the ancestral condition. Thus, it is worth asking whether insights into the biological consequences (correlates) of the three alternative gametophyte structures can help to resolve this issue. Endosperm in flowering plants is initiated by the fertilization of the central cell of the female gametophyte during the process of double fertilization. For this reason, the genetic constitutions of endosperms among flowering plants are specifically determined by (and vary according to) the nuclear complement of the central cell. Variations in female gametophyte development and mature structure have direct consequences on endosperm function and fitness (Friedman et al., 2008).
Selection is hypothesized to favor endosperms with higher ploidy, higher heterozygosity, higher maternal to paternal genome ratios, and reduced opportunity for genetic (interparental and/or parent–offspring) conflict (see Friedman et al., 2008 for a review of this extensive and fascinating literature). Stebbins (1974, 1976) was the first to suggest that higher levels of endosperm ploidy should enable higher rates of transcription in support of the active physiological role of endosperm and, hence, should be adaptive and evolutionarily favored. Thus, transitions from female gametophytes that produce diploid endosperms (Nuphar/Schisandra-type) to those that yield triploid endosperms (e.g., Polygonum-type and Amborella-type) are predicted to be beneficial (Friedman et al., 2008).
A trend toward higher ratios of maternal to paternal genomic contributions to endosperm has also been predicted by theoretical analyses of the potential roles of interparental and/or parent-offspring conflict associated with seed provisioning (Charnov, 1979; Cook, 1981; Westoby and Rice, 1982; Queller, 1983, 1989, 1994; Willson and Burley, 1983; Law and Cannings, 1984; Bulmer, 1986; Haig, 1986; Haig and Westoby, 1989a, b; Friedman, 1995; Friedman et al., 2008). According to these analyses, conflict between pollen- and ovule-bearing parents over optimal investment of nutrients in the embryo-nourishing tissues of seeds of a maternal sporophyte and/or conflict between sibling embryos for resources from the maternal sporophyte should favor increases in the maternal genomic contribution to endosperm.
The triploid endosperms derived from Amborella-type and Polygonum-type female gametophytes are genetically equivalent (a sperm and two genetically identical polar nuclei participate in the second fertilization event). When compared with the diploid endosperms derived from Nuphar/Schisandra-type female gametophytes (a sperm and one polar nucleus participate in the second fertilization event), predicted levels of interparental and/or parent-offspring conflict are significantly reduced in the triploid endosperms derived from both Amborella-type and Polygonum-type female gametophytes (see Friedman et al., 2008 for specific calculations associated with different plant mating systems).
Reduced levels of genetic conflict (as a consequence of increased maternal genomic contributions to endosperm) in a population of seeds on a maternal sporophyte should lead to preferential provisioning (under resource-limited conditions) of a subset of the most fit embryos/seeds (this maximizes maternal fitness through her progeny). Conversely, higher ratios of paternal to maternal genomes in endosperm are predicted to result in more "selfish" behavior in individual endosperms with respect to the acquisition of nutrients for their compatriot embryos; the result being that paternal genetic interests may lead to the abortion of other embryos with greater overall fitness. There is critical experimental evidence to suggest that when paternal genome dosage or expression in endosperm (in Zea and Arabidopsis) is increased, the endosperms and embryos of these seeds are larger and aggressively acquire nutrients from the maternal sporophyte (Lin, 1982, 1984; Scott et al., 1998; Adams et al., 2000; see Gehring et al., 2004, and Baroux et al., 2007, for excellent summaries of this literature), potentially at the expense of seeds with more fit embryos.
Assuming the predictions of the endosperm ploidy hypothesis and genetic conflict hypotheses are correct, increases in the number of female gametophyte developmental modules should have been favored over the course of angiosperm evolutionary history. The benefits of higher module number (for example, two vs. one) will be manifest in trends toward increased endosperm ploidy, increased maternal to paternal genomic ratios, increased relatedness of the maternal sporophyte to the endosperms contained within its seeds, and diminished conflict through decreased ratios of relatedness of endosperm to its compatriot embryo vs. other embryos (Friedman et al., 2008).
For these reasons, the most plausible reconstruction of early-angiosperm female gametophyte character evolution is one that begins with a single-module female gametophyte with a haploid central cell that yields a diploid endosperm with a 1:1 maternal to paternal genome ratio and high levels of genetic conflict. This stands in marked contrast to the hypothesis that either a Polygonum-type or Amborella-type female gametophyte (with a diploid central cell) is plesiomorphic because this hypothesis requires two independent transitions from triploid endosperm to diploid endosperm (which run counter to the theoretical predictions of Stebbins’s ploidy hypothesis and the genetic conflict hypotheses).
We also hypothesize that the common ancestor of angiosperms had a three-celled egg apparatus. If the original (plesiomorphic) female gametophyte module produced four parietal cells and contributed a fifth nucleus to the central cell, it would seem likely that upon modular duplication, an ectopically expressed chalazal module in Amborella-type and Polygonum-type female gametophytes would have had four antipodal cells rather than three. If correct, the Nuphar/Schisandra-type, with its three-celled egg apparatus gave rise to the unique Amborella-type female gametophyte through module duplication (to create a seven-celled, eight-nucleate structure) and a subsequent peramorphic addition of an asynchronous cell division to yield a four-celled egg apparatus (Fig. 14). Thus, the ancestors of Amborella trichopoda are likely to have had Polygonum-type female gametophytes at some point in their evolutionary history.
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; and this is likely to be a conservative estimate). Thus, triploid endosperm (derived from a sperm and two genetically identical polar nuclei) appears to have evolved twice: once in the ancestor of Amborella and once in the common ancestor of monocots, eudicots, and magnoliids. Of course, should future phylogenetic analyses alter the best hypotheses for relationships among the most ancient lineages of angiosperms (and particularly the position of Amborella as sister to all other extant flowering plants), careful reexamination of the evolutionary developmental history of the female gametophyte will be required.
Concluding remarks
For over a century, a specific set of paradigms concerning the origin and early diversification of flowering plant reproductive features was dominant. The first flowering plants were long hypothesized to have had large showy flowers with many parts, conduplicately folded carpels and laminar stamens. At the level of the fertilization process, the female gametophyte was believed to be Polygonum-type (seven cells and eight nuclei) with a second fertilization event that yielded a triploid endosperm. Most workers thought that the endosperm of the earliest flowering plants was free nuclear. Finally, it has long been a matter of "fact" that angiosperms were unique among seed plants in deferring maternal allocation of resources to the seed until after fertilization. In the last five years alone, each of these paradigms appears to have fallen or is poised to do so.
We now know that the flowers of the first angiosperms were extremely small, with ascidiate carpels and nonlaminar stamens (Endress, 2001, 2006; Friis et al., 2006). None of the members of the earliest extant angiosperm clades (specifically Amborellales, Nymphaeales, and Austrobaileyales) produces a Polygonum-type female gametophyte and, as we have argued, the four-nucleate, four-celled Nuphar/Schisandra-type is very likely to be plesiomorphic. With the exception of Amborella, members of early-divergent angiosperm lineages, including Hydatella (Trithuria), form diploid (not triploid endosperm, as had been universally assumed) genetically biparental endosperms from the fertilization of a haploid uninucleate central cell. It is clear that the plesiomorphic pattern of endosperm development is ab initio cellular (not syncytial; Floyd and Friedman, 2000; Holloway and Friedman, 2008). Most recently, with the discovery that maternal plants of Hydatella (Trithuria) provision ovules/seeds with embryo-nourishing reserves prior to fertilization (Friedman, 2008), yet another angiosperm-defining biological feature may well be overturned. Only time, and further study of the embryological features of the ancient angiosperm lineages, will tell how many additional longstanding assumptions (dogmas) concerning the earliest flowering plants will fall.
In the roughly ten years since our phylogenetic understanding of the relationships of ancient lineages of angiosperms changed radically, the focus on the biology of Amborella, Nymphaeales (including Hydatellaceae), Austrobaileyales, magnoliids, early divergent monocots, and early divergent eudicots has provided an entirely new set of perspectives on the earliest phases of the diversification of flowering plants. The sudden shift in accepted hypotheses governing our understanding of early angiosperm evolution was essentially unexpected; not one of these new hypotheses was even remotely anticipated a decade ago. The paradigm shift has occurred in the blink of an eye.
There is cause for considerable optimism that our understanding of the patterns of early angiosperm diversification will continue to unfold at a remarkable pace. The extraordinary expansion of knowledge of the early flowering plant fossil record over the last thirty years shows no signs of abating. Our current phylogenetic insights into the deeper relationships of angiosperms that began in the late 1990s have been strengthened with further and more comprehensive analyses. Finally, the few extant (perhaps even relictual) morphologists, embryologists, and anatomists have made the study of early-divergent angiosperm lineages a remarkably active field. In so doing, they have uncovered tremendous and heretofore unknown biological diversity among the most ancient clades of flowering plants, have themselves been intellectually energized and may even live to witness a resurgence of these disciplines. Not since the golden age of organismic structural plant biology in the first half of the twentieth century has there been so much to look forward to in terms of discovery and its potential impact on our understanding of one of the most complicated and interesting evolutionary stories in the history of photosynthetic life, the origin and early diversification of flowering plants.
FOOTNOTES
1 The authors thank P. Diggle for suggestions that improved the manuscript. This research was supported by a grant from the National Science Foundation (IOB 0446191). 
2 Author for correspondence (e-mail: ned{at}colorado.edu)
LITERATURE CITED
Adams, S., R. Vinkenoog, M. Spielman, H. G. Dickinson, AND R. J. Scott. 2000. Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation. Development 127: 2493–2502.[Abstract]
Angiosperm Phylogeny Group II. 2003. Classification for the orders and families of flowering plants. Botanical Journal of the Linnean Society 141: 399–436.[CrossRef][Web of Science]
Baroux, C., A. Pecinka, J. Fuchs, I. Schubert, AND U. Grossniklaus. 2007. The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization. Plant Cell 19: 1782–1794.
Battaglia, E. 1986. Embryological questions: 7. Do new types of embryo sac occur in Schisandra? Annals of Botany 44: 69–82.
Battaglia, E. 1989. Embryological question: 14. The evolution of the female gametophyte of angiosperms: An interpretative key. Annals of Botany 47: 7–144.
Batygina, T. B., I. I. Shamrov, AND G. E. Kolesova. 1982. Embryology of the Nymphaeales and Nelumbonales. II. The development of the female embryonic structures. Botanicheskii Zhurnal 67: 1179–1195.
Bhandari, N. N. 1971. Embryology of the Magnoliales and comments on their relationships. Journal of the Arnold Arboretum 52: 1–39, 285–304.[Web of Science]
Bulmer, M. G. 1986. Genetic models of endosperm evolution in higher plants. In S. Karlin, and E. Nevo [eds.], Evolutionary process and theory, 743–763. Academic Press, New York, New York, USA.
Charnov, E. L. 1979. Simultaneous hermaphroditism and sexual selection. Proceedings of the National Academy of Sciences, USA 76: 2480–2484.
Chiarugi, A. 1927. Il gametofito femmineo delle angiosperme nei suoi vari tipi di construzione e di sviluppo. Nuovo Giornale Botanico Italiano Nuova Serie 34: 1–133.
Cocucci, A. E. 1973. Orchid embryology—Membrane systems and pollen-tube growth. Caryologia 25 (Supplement): 201–206.[Web of Science]
Cook, K. E. 1981. Plant parenthood. Natural History 90: 31–35.
Cronquist, A. 1988. The evolution and classification of flowering plants. Houghton Mifflin, Boston, Massachusetts, USA.
Davis, G. L. 1966. Systematic embryology of the angiosperms. Wiley, New York, New York, USA.
Donoghue, M. J., AND S. M. Scheiner. 1992. The evolution of endosperm: A phylogenetic account. In R. Wyatt [ed.], Ecology and evolution of plant reproduction. Chapman and Hall, New York, New York, USA.
Doyle, J. A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169: 816–843.[CrossRef][Web of Science]
Endress, P. K. 2001. The flowers in extant basal angiosperms and inferences on ancestral flowers. International Journal of Plant Sciences 162: 1111–1140.[CrossRef][Web of Science]
Endress, P. K. 2006. Angiosperm floral evolution: Morphological developmental framework. Advances in Botanical Research 44: 1–61.[CrossRef]
Favre-DuChartre, M. 1976. Interprétations de l’albumen et des éléments des sacs embryonaires selon divers auteurs. Bulletin de la Societé Botanique de France 123: 17–32.
Favre-Duchartre, M. 1984. Homologies and phylogeny. In B. M. Johri [ed.], Embryology of angiosperms 679–734. Springer-Verlag, Berlin, Germany.
Floyd, S. K., AND W. E. Friedman. 2000. Evolution of endosperm developmental patterns among basal flowering plants. International Journal of Plant Sciences 161: S57–S81.[CrossRef][Web of Science]
Floyd, S. K., AND W. E. Friedman. 2001. Developmental evolution of endosperm in basal angiosperms: Evidence from Amborella (Amborellaceae), Nuphar (Nymphaeaceae), and Illicium (Illiciaceae). Plant Systematics and Evolution 228: 153–169.[CrossRef][Web of Science]
Foster, A. S., AND E. M. Gifford. 1974. Comparative morphology of vascular plants. Freeman, San Francisco, California, USA.
Friedman, W. E. 1995. Organismal duplication, inclusive fitness theory and altruism: Understanding the evolution of endosperm and the angiosperm reproductive syndrome. Proceedings of the National Academy of Sciences, USA 92: 3913–3917.
Friedman, W. E. 2006a. Embryological evidence for developmental lability during early angiosperm evolution. Nature 441: 337–340.[CrossRef][Medline]
Friedman, W. E. 2006b. Sex among the flowers. Natural History 115: 48–53.
Friedman, W. E. 2008. Hydatellaceae are water lilies with gymnospermous tendencies. Nature 453: 94–97.[CrossRef][Web of Science][Medline]
Friedman, W. E., W. N. Gallup, AND J. H. Williams. 2003. Female gametophyte development in Kadsura: Implications for Schisandraceae, Austrobaileyales, and the early evolution of flowering plants. International Journal of Plant Sciences 164 (Supplement): S293–S305.[CrossRef][Web of Science]
Friedman, W. E., E. N. Madrid, AND J. H. Williams. 2008. Origin of the fittest and survival of the fittest: Relating female gametophyte development to endosperm genetics. International Journal of Plant Sciences 169: 79–92.[CrossRef][Web of Science]
Friedman, W. E., AND J. H. Williams. 2003. Modularity of the angiosperm female gametophyte and its bearing on the early evolution of endosperm in flowering plants. Evolution 57: 216–230.[Web of Science][Medline]
Friedman, W. E., AND J. H. Williams. 2004. Developmental evolution of the sexual process in ancient flowering plant lineages. Plant Cell 16 (Supplement): S119–S132.
Friis, E. M., K. R. Pedersen, AND P. R. Crane. 2006. Cretaceous angiosperm flowers: Innovation and evolution in plant reproduction. Palaeogeography, Palaeoclimatology, Palaeoecology 232: 251–293.[CrossRef]
Galati, B. G. 1985. Estudios embriológicos en Cabomba australis (Nymphaeaceae). I. La esporogenesis y las generaciones sexuadas. Boletín de la Sociedad Argentina de Botánica 24: 29–47.
Gehring, M., Y. Choi, AND R. L. Fischer. 2004. Imprinting and seed development. Plant Cell 16: S203–S213.
Graham, S. W., AND R. G. Olmstead. 2000. Utility of 17 chloroplast genes fro inferring the phylogeny of the basal angiosperms. American Journal of Botany 87: 1712–1730.
Graham, S. W., P. A. Reeves, A. C. E. Burns, AND R. G. Olmstead. 2000. Microstructural changes in noncoding chloroplast DNA: Interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference. International Journal of Plant Sciences 161 (Supplement): S83–S96.[CrossRef][Web of Science]
Haig, D. 1986. Conflicts among megaspores. Journal of Theoretical Biology 123: 471–480.[CrossRef][Web of Science]
Haig, D. 1990. New perspective on the angiosperm female gametophyte. Botanical Review 56: 236–274.[CrossRef]
Haig, D., AND M. Westoby. 1989a. Inclusive fitness, seed resources, and maternal care. In J. Lovett-Doust, and L. Lovett-Doust [eds.], Plant reproductive ecology patterns and strategies, 60–79. Oxford University Press, Oxford, UK.
Haig, D., AND M. Westoby. 1989b. Parent-specific gene expression and the triploid endosperm. American Naturalist 134: 147–155.[CrossRef][Web of Science]
Hansen, D. R., S. G. Dastidar, Z. Cai, C. Penaflor, J. V. Kuehl, J. L. Boore, AND R. K. Jansen. 2007. Phylogenetic and evolutionary implications of complete chloroplast genome sequences of four early-diverging angiosperms: Buxus (Buxaceae), Chloranthus (Chloranthaceae), Dioscorea (Dioscoreaceae), and Illicium (Schisandraceae). Molecular Phylogenetics and Evolution 45: 547–563.[CrossRef][Medline]
Holloway, S. J., AND W. E. Friedman. 2008. Embryological features of Tofieldia glutinosa and their bearing on the early diversification of monocotyledonous plants. Annals of Botany 102: 167–182.
Jansen, R. K., Z. Cai, L. A. Raubeson, H. Daniell, C. W. dePamphilis, J. Leebens-Mack, K. F. Müller et al.. 2007. Analysis of 81 genes from 64 chloroplast genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proceedings of the National Academy of Sciences, USA 104: 19369–19374.
Johri, B. M. 1963. Female gametophyte. In P. Maheshwari [ed.], Recent advances in the embryology of angiosperms, 69–103. International Society of Plant Morphology, Delhi, India.
Johri, B. M., K. B. Ambegaokar, AND P. S. Srivastava. 1992. Comparative embryology of angiosperms. Springer-Verlag, Berlin, Germany.
Kim, S., D. E. Soltis, P. S. Soltis, M. J. Zanis, AND Y. Suh. 2004. Phylogenetic relationships among early-diverging eudicots based on four genes: Were the eudicots ancestrally woody? Molecular Phylogenetics and Evolution 31: 16–30.[CrossRef][Web of Science][Medline]
Law, R., AND C. Cannings. 1984. Genetic-analysis of conflicts arising during development of seeds in the Angiospermophyta. Proceedings of the Royal Society of London, B, Biological Sciences 221: 53–70.
Leebens-Mack, J., L. A. Raubeson, L. Y. Cui, J. V. Kuehl, M. H. Fourcade, T. W. Chumley, J. L. Boore et al.. 2005. Identifying the basal angiosperm node in chloroplast genome phylogenies: Sampling one’s way out of the Felsenstein zone. Molecular Biology and Evolution 22: 1948–1963.
Lin, B. Y. 1982. Association of endosperm reduction with parental imprinting in maize. Genetics 100: 475–486.
Lin, B. Y. 1984. Ploidy barrier to endosperm development in maize. Genetics 107: 103–115.
Maheshwari, P. 1950. An introduction to the embryology of angiosperms. McGraw-Hill, New York, New York, USA.
Maneval, W. E. 1914. The development of Magnolia and Liriodendron, including a discussion of the primitiveness of the Magnoliaceae. Botanical Gazette (Chicago, Ill.) 57: 1–31.[CrossRef]
Mathews, S., AND M. J. Donoghue. 1999. The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286: 947–950.
Moore, M. J., C. D. Bell, P. S. Soltis, AND D. E. Soltis. 2007. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proceedings of the National Academy of Sciences, USA 104: 19363–19368.
Palser, B. F. 1975. The bases of angiosperm phylogeny: Embryology. Annals of the Missouri Botanical Garden 62: 621–646.[CrossRef][Web of Science]
Parkinson, C. L., K. L. Adams, AND J. D. Palmer. 1999. Multigene analyses identify the three earliest lineages of extant flowering plants. Current Biology 9: 1485–1488.[CrossRef][Web of Science][Medline]
Porsch, O. 1907. Versuch einer phylogenetischen Erklärung des Embryosackes und der doppelten Befruchtung der Angiospermen. Gustav Fisher, Jena, Germany.
Qiu, Y. L., O. Dombrovska, J. H. Lee, L. B. Li, B. A. Whitlock, F. Bernasconi-Quadroni, J. S. Rest et al.. 2005. Phylogenetic analyses of basal angiosperms based on nine plastid, mitochondrial, and nuclear genes. International Journal of Plant Sciences 166: 815–842.[CrossRef][Web of Science]
Qiu, Y.-L., AND G. F. Estabrook. 2008. Inference of phylogenetic relationships among key angiosperm lineages using a compatibility method on a molecular data set. Journal of Systematics and Evolution 46: 130–141.[Web of Science]
Qiu, Y. L., J. H. Lee, F. Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zanis, E. A. Zimmer et al.. 1999. The earliest angiosperms: Evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404–407.[CrossRef]
Qiu, Y. L., J. H. Lee, F. Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zanis, E. A. Zimmer et al.. 2000. Phylogeny of basal angiosperms: Analyses of five genes from three genomes. International Journal of Plant Sciences 161 (Supplement): S3–S27.[CrossRef][Web of Science]
Qiu, Y. L., L. B. Li, T. A. Hendry, R. Q. Li, D. W. Taylor, M. J. Issa, A. J. Ronen et al.. 2006. Reconstructing the basal angiosperm phylogeny: Evaluating information content of mitochondrial genes. Taxon 55: 837–856.[Web of Science]
Queller, D. 1983. Kin selection and conflict in seed maturation. Journal of Theoretical Biology 100: 153–172.[CrossRef][Web of Science]
Queller, D. 1989. Inclusive fitness in a nutshell. In P. H. Harvey, and L. Partridge [eds.], Oxford surveys in evolutionary biology, 73–109. Oxford University Press, Oxford, UK.
Queller, D. 1994. Male–female conflict and parent–offspring conflict. American Naturalist 144: S84.[CrossRef][Web of Science]
Rudall, P. J. 2006. How many nuclei make and embryo sac in flowering plants? BioEssays 28: 1067–1071.[CrossRef][Medline]
Rudall, P. J., M. V. Remizowa, A. S. Beer, E. Bradshaw, D. W. Stevenson, T. D. Macfarlane, R. E. Tuckett et al.. 2008. Comparative ovule and megagametophyte development in Hydatellaceae and water lilies reveal a mosaic of features among the earliest angiosperms. Annals of Botany 101: 941–956.
Saarela, J. M., H. S. Rai, J. A. Doyle, P. K. Endress, S. Mathews, A. D. Marchant, B. G. Briggs, AND S. W. Graham. 2007. Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446: 312–315.[CrossRef][Medline]
Schnarf, K. 1931. Vergleichende embryologie der angiospermen. Bornträger, Berlin, Germany.
Schnarf, K. 1936. Contemporary understanding of embryo sac development among angiosperms. Botanical Review 2: 565–585.[CrossRef]
Scott, R. J., M. Spielman, J. Bailey, AND H. G. Dickinson. 1998. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125: 3329–3341.[Abstract]
Shamrov, I. I. 1998. Formation of hypostase, podium and postament in the ovule of Nuphar lutea (Nymphaeaceae) and Ribes aureum (Grossulariaceae). Botanicheskii Zhurnal 83: 3–14.
Solntseva, M. P. 1981. Illiciales. In M. S. Yakovlev [ed.], Comparative embryology of flowering plants, 51–54. Nauka, Leningrad, Russia [in Russian].
Soltis, D. E., M. A. Gitzendanner, AND P. S. Soltis. 2007. A 567-taxon data set for angiosperms: The challenges posed by Bayesian analyses of large data sets. International Journal of Plant Sciences 168: 137–157.[CrossRef][Web of Science]
Soltis, D. E., P. S. Soltis, M. W. Chase, M. E. Mort, D. C. Albach, M. Zanis, V. Savolainen et al.. 2000b. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society 133: 381–461.[CrossRef][Web of Science]
Soltis, P. S., AND D. E. Soltis. 2004. The origin and diversification of angiosperms. American Journal of Botany 91: 1614–1626.
Soltis, P. S., D. E. Soltis, AND M. W. Chase. 1999. Angiosperm phylogeny inferred from multiple genes as a research tool for comparative biology. Nature 402: 402–404.[CrossRef]
Soltis, P. S., D. E. Soltis, M. J. Zanis, AND S. Kim. 2000a. Basal lineages of angiosperms: Relationships and implications for floral evolution. International Journal of Plant Sciences 161 (Supplement): S97–S107.[CrossRef][Web of Science]
Stebbins, G. L. 1974. Flowering plants: Evolution above the species level. Harvard University Press, Cambridge, Massachusetts, USA.
Stebbins, G. L. 1976. Seeds, seedlings, and the origin of angiosperms. In C. B. Beck [ed.], Origin and early evolution of angiosperms, 300–311. Columbia University Press, New York, New York, USA.
Swamy, B. G. L. 1964. Macrogametophytic ontogeny in Schisandra chinensis. Journal of the Indian Botanical Society 43: 391–396.
Takhtajan, A. 1976. Neoteny and the origin of flowering plants. In C. B. Beck [ed.], Origin and early evolution of angiosperms, 207–219. Columbia University Press, New York, New York, USA.
Titova, G. E. 1990. The development of the female generative structures in Cabomba caroliniana A. Gray (Cabombaceae). In T. Batygina [ed.], Proceedings of the XI International Symposium on Embryology and Seed Reproduction, 1990, Leningrad, Russia. Nauka, Leningrad, Russia.
Tobe, H., T. Jaffre, AND P. H. Raven. 2000. Embryology of Amborella (Amborellaceae): Descriptions and polarity of character states. Journal of Plant Research 113: 271–280.[CrossRef][Web of Science]
Tobe, H., Y. Kimoto, AND N. Prakash. 2007. Development and structure of the female gametophyte in Austrobaileya scandens (Austrobaileyaceae). Journal of Plant Research 120: 431–436.[CrossRef][Medline]
Van Miegroet, F., AND M. Dujardin. 1992. Cytologie et histology de la reproduction chez le Nymphaea heudelottii. Canadian Journal of Botany 70: 1991–1996.[CrossRef]
Westoby, M., AND B. Rice. 1982. Evolution of seed plants and inclusive fitness of plant tissues. Evolution 36: 713–724.[CrossRef][Web of Science]
Williams, J. H., AND W. E. Friedman. 2002. Identification of diploid endosperm in an early angiosperm lineage. Nature 415: 522–526.[CrossRef][Medline]
Williams, J. H., AND W. E. Friedman. 2004. The four-celled female gametophyte of Illicium (Illiciaceae; Austrobaileyales): Implications for understanding the origin and early evolution of monocots, eumagnoliids, and eudicots. American Journal of Botany 91: 332–357.
Willson, M. F., AND N. Burley. 1983. Mate choice in plants: Tactics, mechanisms, and consequences. Princeton University Press, Princeton, New Jersey, USA.
Winter, A. N. 1987. Embryology of the family Hydrostemma (Barclaya) with respect to its systematic position. Institute Biological Science, Leningrad, Russia [in Russian].
Winter, A. N. 1993. Some aspects of the reproductive biology of Hydrostemma longifolium (Barclaya longifolia) (Barclayaceae). Botanicheskii Zhurnal 78: 69–83.
Winter, A. N., AND I. I. Shamrov. 1991a. Development of the ovule and embryo sac in Nuphar lutea (Nymphaeaceae). Botanicheskii Zhurnal 76: 378–390.
Winter, A. N., AND I. I. Shamrov. 1991b. Megasporogenesis and embryo sac development in representatives of the genera Nymphaea and Victoria (Nymphaeaceae). Botanicheskii Zhurnal 76: 1716–1728.
Yoshida, O. 1962. Embryologische studien über Schisandra chinensis Bailey. Journal of the College of Arts and Sciences of Chiba University 3: 459–462.
Zanis, M. J., D. E. Soltis, P. S. Soltis, S. Mathews, AND M. J. Donoghue. 2002. The root of the angiosperms revisited. Proceedings of the National Academy of Sciences, USA 99: 6848–6853.
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