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First published online April 14, 2004; 10.1105/tpc.017277
© 2004 American Society of Plant Biologists Developmental Evolution of the Sexual Process in Ancient Flowering Plant Lineages
a Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309 1 To whom correspondence should be addressed. E-mail ned{at}colorado.edu; fax 303-492-8699.
Recent investigations of ancient angiosperm lineages are yielding data critical to a fundamental reassessment of the origin and early evolution of flowering plants. To "reconstruct" the reproductive features of the earliest flowering plants, biological characters must be examined in an appropriate phylogenetic sampling of extant angiosperms, and their history must then be traced back through 130 million years of time. This task requires, first, a clear formulation of the phylogenetic interrelationships among basal angiosperms. Once robust phylogenetic hypotheses are available, comparative analyses can be used to infer and reconstruct the evolutionary history of a broad range of biological characters. Thus, the study of the origin and early evolution of flowering plants, like that of any group of organisms, relies on the interplay of phylogenetic and comparative biology. Incorrect (or vague) assessments of phylogenetic relationships, as well as misconstrued biological character data, will result in flawed evolutionary historical hypotheses. Both of these pitfalls have plagued the reconstruction of early angiosperm reproductive history for more than a century. After a long period of empirical and intellectual stagnation, critical new reproductive data coupled with more robust phylogenetic hypotheses are radically altering the conceptual landscape. Many of the century-old paradigms about the origin and early evolution of flowering plant reproductive features are in the midst of being substantially overthrown. For more than a century, the "defining" features of flowering plant reproductive biology have been thought to be well circumscribed. Typically, in angiosperms, the pollen grain (male gametophyte) is bicellular when it is shed from the anther and produces two sperm during the growth of the pollen tube within the tissues of the gynoecium. The female gametophyte is almost always monosporic in origin and usually develops into a seven-celled, eight-nucleate organism before fertilization. The fertilization process in flowering plants is marked by two separate gametic fusion events that produce a diploid embryo and a triploid embryo-nourishing endosperm. Finally, in most flowering plants, the embryo initiates a cellular pattern of development and the endosperm proceeds through a free nuclear (syncytial) phase of development (but eventually becomes cellularized) (Table 1). Although most angiosperms conform to this suite of reproductive characteristics, the widespread distribution of these features reveals nothing of their evolutionary origin and diversification. As we show here, new data derived from studies of ancient (extant) flowering plant lineages (Amborella, Nymphaeales, Austrobaileyales) indicate that the reproductive features of the first flowering plants differed significantly from the suite of gametophyte, embryo, and endosperm characteristics that are common to the overwhelming majority of extant flowering plants.
In this review, we examine the reproductive features of flowering plants associated with the fertilization process from an evolutionary developmental perspective. We address three basic questions. First, did the earliest flowering plants possess a process of double fertilization? The definitive answer (as of now) is maybe. As we show, after a century and a half of study of the plant fertilization process, a key taxon central to reconstructing the ancestral characteristics of extant flowering plants has yet to be examined for this process. Indeed, until two years ago (Williams and Friedman, 2002  ), there were no definitive studies demonstrating a process of double fertilization in any of the most ancient lineages of angiosperms (for a review of earlier studies, see Friedman and Floyd, 2001). Thus, the long-standing assumption that the first flowering plants expressed a second fertilization event that initiated a genetically biparental endosperm has yet to be proven.
Second, what was the developmental pattern and mature structure of the ancestral angiosperm female gametophyte? We present an analysis of the very recent and surprising discovery that the female gametophyte in the earliest flowering plants probably was not of the Polygonum type (monosporic, seven celled, and eight nucleate) but rather was four celled and four nucleate at maturity (Friedman et al., 2003
Third, what were the ploidy and genetic constitution of early angiosperm endosperm? Because endosperm is initiated by the fertilization of the central cell, the ploidy and genetic constitution of endosperm are tied directly to the development and mature structure of the female gametophyte. Thus, any transition from a four-celled, four-nucleate female gametophyte with a haploid central cell to a seven-celled, eight-nucleate female gametophyte with a binucleate (diploid) central cell (Polygonum type) likely marks a transition from the diploid endosperms characteristic of the earliest angiosperms to the triploid endosperms found among most extant flowering plants (Friedman and Williams, 2003
Throughout the 20th century, the broad consensus on the reproductive characteristics of the earliest angiosperms derived from a general phylogenetic hypothesis that "Magnolia-like" plants and their relatives (magnoliids) constitute a plexus of ancient lineages (in essence, the paraphyletic wellspring) from which all other angiosperms evolved (Bessey, 1897 , 1915; Arber and Parkin, 1907; Takhtajan, 1969; Dahlgren, 1980; Cronquist, 1981; Walker and Walker, 1984; Donoghue and Doyle, 1989; Thorne, 1992). As a consequence, members of the Magnoliales and other groups, such as the Laurales and Winterales, frequently were studied to reconstruct the embryological features of the earliest flowering plants (Maneval, 1914; Earle, 1938; Hayashi, 1965; Sastri, 1969; Bhandari, 1971a, 1971b).
Embryological studies throughout the 20th century affirmed that a monosporic seven-celled, eight-nucleate female gametophyte (Polygonum type) is prevalent among magnoliids (Hayashi, 1965
Twentieth century embryological studies also affirmed that a second fertilization event that initiates an endosperm was ubiquitous among flowering plants, including magnoliids (Sargant, 1900
The twentieth century views of what characterized the "primitive" suite of angiosperm reproductive features were accepted with little dissent. Indeed, based on all of the generally accepted paradigms of flowering plant reproductive biology, evolutionary biologists could confidently report that "[d]ouble fertilization and the development of copious endosperm from a triple fusion nucleus [in a Polygonum-type female gametophyte] are clearly primitive characters within the angiosperms" (Cronquist, 1988
The long-standing assumptions about which lineages might contain taxa with ancient characteristics of flowering plants changed dramatically in 1999. At that time, a series of phylogenetic analyses converged on a set of relationships among basal angiosperms that indicated that most magnoliid lineages, although relatively ancient in origin, were not the most ancient lineages of flowering plants. These phylogenetic analyses (Mathews and Donoghue, 1999 ; Parkinson et al., 1999; Qiu et al., 1999, 2000; Soltis et al., 1999; Graham et al., 2000; Graham and Olmstead, 2000; Zanis et al., 2002, 2003; Borsch et al., 2003) revealed that the specific magnoliid clades Amborella, Nymphaeales (Nymphaeaceae and Cabombaceae), and Austrobaileyales (Illiciaceae, Schisandraceae, Trimeniaceae, and Austrobaileyaceae) constitute a basal grade of flowering plants (Figures 1 and 2). There is still ambiguity regarding the precise interrelationships of Amborella and Nymphaeales (Barkman et al., 2000; Graham and Olmstead, 2000; Angiosperm Phylogeny Group, 2003); in addition, the phylogenetic positions of other ancient angiosperm lineages, such as Chloranthaceae and Ceratophyllaceae, remain unresolved. However, there is good reason to believe that all angiosperms, to the exclusion of Amborella, Nymphaeales, and Austrobaileyales, share a more recent common ancestor (Figure 2). Thus, Amborella, Nymphaeales, and Austrobaileyales each originated (and had begun to evolve) before the origin of monocots, eudicots, and eumagnoliids (a clade that includes Magnoliales, Laurales, Piperales, and Winterales). The only recent phylogenetic analysis to suggest that any of these three lineages might not be basal among angiosperms (Goremykin et al., 2003) may suffer from subminimal taxon sampling, which is known to often yield spurious results.
It is now evident that the common ancestor of monocots and eudicots is not the common ancestor of extant angiosperms. Thus, comparative studies of monocots and eudicots (such as Zea and Arabidopsis) cannot be used to infer directly the ancestral characteristics of flowering plants (Figure 2). With the discovery that Amborella, Nymphaeales, and Austrobaileyales are the most ancient extant angiosperm lineages and might (or might not) retain some of the biological features of the earliest angiosperms (Friedman et al., 2003 ), it was evident that answers to Darwin's "abominable mystery" of the origin of flowering plants (Darwin, 1903) would have to be sought through direct study of these relictual groups (by the few remaining relictual embryologists). Only through careful comparisons of Amborella, Nymphaeales, and Austrobaileyales with early divergent lineages of monocots, eumagnoliids, and eudicots can robust hypotheses be formulated regarding the nature of the common ancestor of extant angiosperms.
Unlike members of the Magnoliales, Laurales, Winterales, and many other magnoliids, Amborella and taxa within the Austrobaileyales were rarely examined embryologically during the 20th century (Friedman et al., 2003
After the recent identification of the most ancient lineages of angiosperms, it rapidly became apparent that there was little substantive evidence of a second fertilization event in any of the constituent members of the Amborella, Nymphaeales, and Austrobaileyales clades (Friedman and Floyd, 2001 ). Until 2 years ago, there were just four reports of a fusion of a second sperm nucleus with the two polar nuclei (or their fusion product, the secondary nucleus) of the female gametophyte in the most basal angiosperm lineages: Brasenia (Khanna, 1965), Nymphaea (Khanna, 1967), Cabomba (Galati, 1985), and Illicium (Hayashi, 1963a). In contradistinction to these claims, there were reports that some early angiosperm lineages might not have a second fertilization event (e.g., Nymphaea [Cook, 1909] and the ancient monocot lineage Acorus [Buell, 1938]). Regrettably, none of these studies included photomicrographic evidence in support of their conclusions.
In the last 2 years, the first robust photomicrographic and cell biological evidence of a second fertilization event in basal angiosperms has been published (Williams and Friedman, 2002
The G1 karyogamy pattern in basal angiosperms is fundamentally similar to that of all nonplant eukaryotes that have been studied (reviewed by Friedman, 1999 ; Corellou et al., 2001) but differs from the cell cycle behavior of Arabidopsis (Friedman, 1999) and several other derived angiosperms (Ermakov et al., 1980). These plants, found scattered in Brassicaceae, Asteraceae, and Poaceae, appear to be unique among eukaryotes: the synthesis phase of the cell cycle is expressed in gametes before fertilization (G2 karyogamy). Even though a second fertilization event has now been documented conclusively in the Nymphaeales and Austrobaileyales, the determination of whether this process was a feature of the common ancestor of extant flowering plants still depends on an assessment of the condition in Amborella. To date, the fertilization event in Amborella has not been observed. If Amborella is eventually shown to initiate an endosperm from a sexual process, it can be confidently concluded that double fertilization was present in the common ancestor of all extant flowering plants. However, if Amborella lacks a second fertilization event, explanations include the possibilities that the first flowering plants lacked a sexual (biparental) endosperm and that double fertilization evolved in the common ancestor of all extant flowering plants other than Amborella or that a second fertilization process was present in the first angiosperms but was lost in the lineage that produced Amborella.
If double fertilization is eventually shown to be a feature of the common ancestor of flowering plants, this still will not reveal where this process came from and how it evolved. Double fertilization processes, defined as two fertilization events in a single female gametophyte by two sperm from a single pollen tube, also occur in nonflowering seed plants, particularly among members of the Gnetales and possibly some conifers (Friedman, 1990
From 1985 through 1998 (Crane, 1985
Subsequent to the 1999 revelation of the basal phylogenetic positions of Amborella, Nymphaeales, and Austrobaileyales, Tobe and colleagues (2000) reported that the female gametophyte of Amborella produces seven cells and eight nuclei. This finding initially seemed to indicate that although there had been a shift in hypothesis regarding what constituted the most ancient flowering plant lineages, the century-old paradigm that the first angiosperms had a Polygonum-type female gametophyte remained unaltered. Based on a review of the secondary literature (Padmanabhan, 1970; Johri et al., 1992), Tobe et al. (2000) also noted that members of the Nymphaeales and Austrobaileyales had Polygonum-type female gametophytes, thus perpetuating the long-standing appraisal of the embryological characters of these poorly studied taxa.
In contrast to Amborella and what was assumed to be the case in Nymphaeales and Austrobaileyales, there were interesting hints that the female gametophytes in Nymphaeales and Austrobaileyales might not be of the Polygonum type. Beginning with work by Yoshida (1962)
It is now evident that earlier reports of Polygonum-type female gametophytes in Nymphaeales and Austrobaileyales almost certainly are in error (Friedman and Williams, 2003
Many embryologists, assuming that the particular magnoliid taxon under study had a Polygonum-type female gametophyte (in essence because ancient lineages of flowering plants must have this type of female gametophyte), concluded that they had missed a transitory seven-celled, eight-nucleate stage in their developmental series. Thus, female gametophytes in Cabombaceae, Nymphaeaceae, Austrobaileyaceae, Trimeniaceae, Schisandraceae, and Illiciaceae usually were characterized as possessing "ephemeral antipodals" and undergoing rapid fusion of the two polar nuclei within the central cell (Davis, 1966 ; Johri et al., 1992; Tobe et al., 2000).
The mature female gametophytes of members of the Nymphaeales and Austrobaileyales are monosporic and now have been shown conclusively to contain four cells and four nuclei at maturity: a haploid uninucleate central cell, an egg cell, and two synergids (Figure 5). When the DNA content of the central cell nucleus is assayed, it is shown to be haploid and to occupy the G1 phase of the cell cycle (Williams and Friedman, 2002
The female gametophyte of angiosperms is best viewed as a fundamentally modular structure in which individual developmental modules consist of "quartets" of nuclei (Porsch, 1907 ; Schnarf, 1936; Maheshwari, 1950; Swamy and Krishnamurthy, 1975; Favre-DuChartre, 1976; Battaglia, 1989; Friedman and Williams, 2003). Each module can be characterized by a common developmental pattern: (1) positioning of a single nucleus within a cytoplasmic domain (pole) 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 (Figure 6) (Friedman and Williams, 2003).
There are only two known female gametophyte ontogenetic sequences present in the most ancient clades of extant angiosperms: the monosporic four-celled, four-nucleate sequence characteristic of Nymphaeales and Austrobaileyales (Friedman et al., 2003 ; Friedman and Williams, 2003; Williams and Friedman, 2004); and the monosporic seven-celled, eight-nucleate sequence of Amborella (Tobe et al., 2000). Although the polarity of evolutionary transition is, on strict grounds of parsimony, unresolved, we have argued that four-celled, four-nucleate female gametophytes may be plesiomorphic among angiosperms (Friedman and Williams, 2003). If this hypothesis is correct, the first angiosperm female gametophytes were composed of a single four-celled, four-nucleate module (Friedman and Williams, 2003). Early in angiosperm history, ectopic expression of this basic developmental module resulted in the initiation of a second developmental module within the female gametophyte. In basal angiosperm taxa with four-celled female gametophytes, all nuclei are confined to the micropylar domain during free nuclear development, and this yields a single modular quartet (Figure 7). In Amborella and other angiosperms with Polygonum-type female gametophytes, the migration of one of the nuclei to the chalazal pole at the two-nucleate stage results in the establishment of a chalazal developmental module (in addition to the micropylar module) that ultimately forms three antipodal cells and a polar nucleus (Figure 7).
We have hypothesized that the establishment of a duplicate module in the angiosperm female gametophyte was accomplished initially at the two-nucleate stage through the developmental insertion of a cytoskeletal apparatus that separates the nuclei into distinct cytoplasmic domains at opposite poles of the female gametophyte (Figure 7). The net effect of this novel nuclear migration process was the creation of two cytoplasmic/developmental domains in the female gametophyte and the parallel initiation of two modular quartets. The result was the formation of a seven-celled, eight-nucleate Polygonum-type female gametophyte (Friedman and Williams, 2003 ).
The transition to a two-module seven-celled, eight-nucleate female gametophyte from a one-module four-nucleate, four-celled female gametophyte appears to have occurred twice: once in the Amborella lineage and once in the common ancestor of the monocots, eudicots, and eumagnoliids (Figure 8). Given that the oldest known angiosperm pollen has been dated to 132 million years before the present (Friis et al., 1999
If the modular duplication hypothesis is correct, the chalazal module (or quartet) of monocots, eudicots, and eumagnoliids represents a developmental novelty that arose during the earliest phases of the diversification of angiosperms. Thus, the second polar nucleus and the three antipodal cells of the seven-celled, eight-nucleate female gametophyte are angiosperm innovations and are not strictly homologous with any part of the female gametophyte of nonflowering seed plants. This conclusion stands in marked contrast to the long-standing hypothesis that the antipodal cells of the seven-celled, eight-nucleate female gametophyte are homologous with (and a highly reduced vestige of) the large somatic body (prothallus) of nonflowering seed plant female gametophytes (Sargant, 1900 ; Battaglia, 1951; Favre-DuChartre, 1984).
The developmental and functional behavior of antipodals and the chalazal polar nucleus in basal monocots and basal eudicots suggests that the chalazal module of the Polygonum-type female gametophyte originally consisted of two components: (1) three persistent antipodal cells that lacked conspicuous postfertilization development (Williams and Friedman, 2004
Evidence for the generality of the modular hypothesis for the angiosperm female gametophyte derives from its ability to account for much of the diversity of mature structures among flowering plant female gametophytes. All angiosperms initiate a micropylar module (which contains an egg). Ninety-nine percent of angiosperms initiate a chalazal developmental module in addition to the micropylar module. In Penaea, two additional "equatorial" modules supplement the micropylar and chalazal modules: each module produces three peripheral cells and contributes a nucleus to the central cell. In some angiosperms (e.g., Plumbago with two modules and Plumbagella with four modules [Gifford and Foster, 1989
The key to transitions between angiosperm female gametophytes with different numbers of modules lies in the modification of early development to position nuclei within one, two, or four cytoplasmic and developmentally autonomous domains (Friedman and Williams, 2003 ). The gain of nuclear migration to opposite poles at the early two-nucleate stage can account for the transition from a four-nucleate to an eight-nucleate female gametophyte in the common ancestor of monocots, eumagnoliids, and eudicots. Conversely, the loss of nuclear migration at the two-nucleate stage can account for the origin of the four-celled, four-nucleate female gametophyte from an eight-nucleate ancestor, as is the case in Onagraceae (parsimony analysis indicates that the ancestors of Onagraceae had a Polygonum-type female gametophyte [Tobe and Raven, 1983; Conti et al., 1996, 1997]). Onagraceae is not the only group in which the chalazal module has been lost. In grasses (tribes Paniceae and Andropogoneae), the chalazal module appears to have been lost repeatedly, and in each case this correlates with a shift from sexual reproduction (seven-celled, eight-nucleate female gametophyte) to apomixis (four-celled, four-nucleate female gametophyte) (Warmke, 1954; Brown and Emery, 1958; Battaglia, 1991).
The monosporic seven-celled, eight-nucleate Polygonum-type female gametophyte has long served as the baseline for analysis of the origin and subsequent evolution of the angiosperm female gametophyte (Schnarf, 1931 ; Maheshwari, 1950; Johri, 1963; Davis, 1966; 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). It is now evident that this type of female gametophyte is rare among basal angiosperms (occurring in only a single extant species, Amborella trichopoda), whereas the four-celled, four-nucleate type of female gametophyte typifies the ancient angiosperm lineages Nymphaeales and Austrobaileyales and may be plesiomorphic for flowering plants as a whole. Given that the genetic constitution of endosperm is related directly to the genetic constitution of the central cell of the female gametophyte, changes in female gametophyte development have the potential to directly alter the ploidy and maternal-to-paternal genomic ratios of endosperm. We believe that major transitions in the modular construction of female gametophytes may have little, if anything, to do with the functional biology of the gametophyte per se. Rather, selection has acted primarily to preserve female gametophyte developmental mutants that have created advantageous alterations in the genetics and ploidy of endosperm. If true, the critical classes of mutants associated with evolutionary transitions in endosperm genetics and ploidy will be those that alter the distribution of free nuclei during the early stages of female gametophyte development and hence the number of developmental modules that are established.
From this perspective, the key "functional" component of the original chalazal module was the chalazal polar nucleus that participated in a second fertilization event and altered the original genetic constitution and ploidy of endosperm. Thus, the set of three antipodals, in their original manifestation in the earliest Polygonum-type female gametophytes, can be viewed as an evolutionary "spandrel" (sensu Gould and Lewontin, 1979
A trend toward higher endosperm ploidy and increases in the ratio of maternal to paternal genomic contributions is consistent with and predicted by theoretical analyses of the potential roles of intersexual conflict and kin conflict during the early evolution of endosperm (Westoby and Rice, 1982
For more than a century, the question of what endosperm is, from an evolutionary/homological point of view, has confounded plant embryologists and evolutionary biologists. The prevalence of the diploid condition of early angiosperm endosperms may help to address this difficult question. From an evolutionary-historical perspective, there are only three possible answers to the question of what endosperm is, all of which have been known for more than a century (Sargant, 1900
If double fertilization is a feature of the common ancestor of angiosperms, the fact that diploid endosperms predominate among basal angiosperms and are likely to be plesiomorphic strongly suggests that before the acquisition of embryo-nourishing behavior, the ancestral second fertilization product was diploid. A diploid ancestral condition is congruent with an embryo homology for endosperm, because (obviously) embryos are diploid. Although double fertilization events in Gnetales may not be evolutionarily related to those of flowering plants, it is certainly notable that the second fertilization product in Ephedra and Gnetum is a diploid embryo (Friedman, 1992a
Imprinting and parent-of-origin effects in the endosperms of Arabidopsis and Zea (Kermicle, 1970
A comparative analysis, based on the most recently published phylogenies of angiosperms, supports the following evolutionary developmental hypothesis (Friedman and Williams, 2003 ; Williams and Friedman, 2004). The earliest angiosperms possessed a four-celled, four-nucleate female gametophyte that lacked antipodals and a second polar nucleus. The developmental reduction of the large gymnosperm female gametophyte (thousands of cells with multiple archegonia) to the four-celled condition of the first angiosperms involved the loss of archegonial structure, the reduction of the number of eggs from many to one (per female gametophyte), and the complete elimination of the somatic body (prothallus). This condition still is to be found among Nymphaeales and Austrobaileyales. Approximately 10 million years after the origin of angiosperms, ectopic duplication of the basic modular quartet that produces the egg apparatus and a uninucleate haploid central cell generated a second developmental module expressed in the chalazal domain of the female gametophyte of the common ancestor of monocots, eumagnoliids, and eudicots (modular duplication also occurred in an ancestor of Amborella trichopoda). Thus, the antipodals of the seven-celled, eight-nucleate female gametophyte (Polygonum type) represent a duplicated and sterilized egg apparatus. Because the ploidy and genetic constitution of endosperm is always tied directly to the development and mature structure of the female gametophyte, the transition from a monosporic four-celled, four-nucleate female gametophyte with a haploid central cell to a monosporic seven-celled, eight-nucleate female gametophyte with a binucleate (diploid) central cell also marked the transition from the diploid genetically biparental endosperms of the earliest angiosperms to the triploid genetically biparental endosperms found among most extant flowering plants, including Arabidopsis, Antirrhinum, and Zea. Finally, although the issue of whether the first angiosperms possessed a process of double fertilization remains unresolved, the answer will be revealed as soon as the condition is investigated in Amborella. If double fertilization is found to be a defining feature of the first angiosperms, this should refocus attention on the century-old question of the evolutionary origin of double fertilization and, most importantly, the homology of endosperm. More than a century after the beginning of intensive study of the reproductive biology of flowering plants, much remains to be discovered about the basic features of the sexual process in angiosperms in general and, more specifically, in the most ancient lineages of this remarkable clade of plants. Nevertheless, a new understanding of the evolutionary developmental basis for the diversification of flowering plant gametophyte structure, fertilization process, and endosperm genetics is beginning to emerge from studies propelled by recent insights into angiosperm phylogeny and a more developmentally dynamic sense of how plant structure evolves.
We thank Larry Hufford, Robert Robichaux, and Pamela Diggle for critical feedback and suggestions to improve the manuscript and William Gallup for assistance with histology and digital imaging. This research was supported by a grant from the National Science Foundation to W.E.F. (IBN-9816107) and by a grant from the University of Colorado Committee on Research and Creative Works.
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.017277. Received September 11, 2003; accepted January 9, 2004.
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INTRODUCTION
TWENTIETH CENTURY VIEWS OF...
10 million years after the origin of flowering plants (Williams and Friedman, 2004
