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First published online December 19, 2008; doi:10.3732/ajb.0800070 American Journal of Botany 96: 144-165 (2009) © 2009 Botanical Society of America, Inc. |
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Special Invited Papers |
Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996 USA
Received for publication 21 February 2008. Accepted for publication 22 August 2008.
ABSTRACT
A remarkable number of the defining features of flowering plants are expressed during the life history stage between pollination and fertilization. Hand pollinations of Amborella trichopoda (Amborellaceae) in New Caledonia show that when the stigma is first receptive, the female gametophyte is near maturity. Pollen germinates within 2 h, and pollen tubes with callose walls and plugs grow entirely within secretions from stigma to stylar canal and ovarian cavity. Pollen tubes enter the micropyle within 14 h, and double fertilization occurs within 24 h. Hundreds of pollen tubes grow to the base of the stigma, but few enter the open stylar canal. New data from Amborella, combined with a review of fertilization biology of other early-divergent angiosperms, show that an evolutionary transition from slow reproduction to rapid reproduction occurred early in angiosperm history. I identify increased pollen tube growth rates within novel secretory carpel tissues as the primary mechanism for such a shift. The opportunity for prezygotic selection through interactions with the stigma is also an important innovation. Pollen tube wall construction and substantial modifications of the ovule and its associated structures greatly facilitated a new kind of reproductive biology.
Key Words: Amborella • callose plug • carpel • double fertilization • evolution of development • heterochrony • novelty • origin of angiosperms • pollen tube growth • stigma
Many of the innovations that characterize angiosperms involve reproductive biology, and most of these function during the life history period between pollination and fertilization, the progamic phase. Novelties such as the closed carpel, stigma, internalized pollen tube transmitting tract, highly reduced male and female gametophytes, the process of double fertilization, callose-walled pollen tubes, rapid pollen tube germination and growth, and prezygotic mate selection systems have all at one time or another been linked to angiosperm ecological success and diversification (Stebbins, 1976
; Takhtajan, 1976; Doyle, 1978; Favre-Duchartre, 1979; Mulcahy, 1979; Willson and Burley, 1983; Zavada and Taylor, 1986; Bernhardt and Thien, 1987; Haig and Westoby, 1989; Friedman, 1990; Dajoz et al., 1991; Donoghue and Scheiner, 1992; Lloyd and Wells, 1992; Williams, 2008). Darwin (1859, pp. 98, 99) himself recognized the potential evolutionary importance of one novel aspect of the progamic phase—outcross pollen "prepotency" in the style—in the first volume of Origin of Species, and he subsequently performed many hand-pollination experiments testing the idea (e.g., Darwin, 1862).
Changes in rates, timing, and duration of ontogenies underlie the evolution of many novel aspects of the progamic phase. During the transition to angiospermy, the progamic phase is thought to have become greatly abbreviated (Maheshwari, 1950; Stebbins, 1976; Takhtajan, 1976; Doyle, 1978; Favre-Duchartre, 1979; Willson and Burley, 1983; Haig and Westoby, 1989; Friedman, 1990; Donoghue and Scheiner, 1992), although it is possible that abbreviation took place in the angiosperm stem lineage (Doyle and Donoghue, 1993). In either case, a shortened reproductive cycle is thought to have conferred many advantages in early angiosperm history (Stebbins, 1965, 1974, 1976; Queller, 1983; Doyle and Donoghue, 1986; Bond, 1989; Midgley and Bond, 1991). In gymnosperms, the period between pollination and fertilization is typically on the order of weeks to over a year (Singh, 1978; Willson and Burley, 1983).
The progamic phase in phylogenetically derived angiosperms involves a sophisticated orchestration of male and female gametophyte growth and development within female sporophytic tissues (stigma, pollen tube pathway, and ovule) as pollen tubes transport sperm from pollen grain to egg (Friedman, 1999; Herrero, 2003; Palanivelu et al., 2003; Tian et al., 2005). Angiosperms are strikingly diverse in both the physiology of such interactions and in the morphology of structures within which interactions occur. A goal of research into early angiosperm reproductive biology then is to understand the developmental origins and functional integration of these innovations as well as the underlying causes of their subsequent diversification. Toward that end, a consistent framework for understanding evolutionary transitions in the biology of the progamic phase in seed plants is needed.
A starting point is to identify the most general homologous features of developmental timing and growth that can undergo transformation within the group (Fig. 1). These must then be characterized in relevant fossil or extant lineages to reconstruct attributes of an ancestral and a descendant set of traits (Gould, 1977; Alberch et al., 1979; Reilly et al., 1997; Friedman and Carmichael, 1998). Novelties, developmental modifications, and heterochronies can then be identified and inferences can be made about altered relationships among the whole suite of ontogenies that interact between their common onset and offset landmarks.
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), (2) pollination (Herrero and Arbeloa, 1989), (3) pollen hydration (Honys and Twell, 2003), or (4) pollen germination (de Graaf et al., 2001). All agree the progamic phase ends with "fertilization," but ecological or agronomic studies (e.g., Fehr and Hadley, 1980) often record fertilization as the time when a pollen tube first enters the micropyle of the ovule, whereas model system studies (e.g., Higashiyama and Inatsugi, 2006) see fertilization as a process in itself, begining within the ovule and ending with completion of gamete fusion. In this paper, the term progamic phase is used to mean the period of development that begins with pollination (pollen adhesion to a sporophytic surface such as stigma or ovule) and ends with gamete fusion (e.g., Cresti et al., 1992), because these are absolute landmarks that encompass the entire series of interactions between male gametophyte and female sporophyte and gametophyte.
Most of the traits involved in the fertilization process are not accessible in the fossil record, thus extant early-divergent lineages of angiosperms have been of great interest for reconstructing ancestral states of the group. In this study I provide details of the progamic phase of Amborella trichopoda Baill. (Amborellaceae), which has been placed as sister (with or without Nymphaeales) to all extant angiosperms by recent phylogenetic studies (Zanis et al., 2002; Leebens-Mack et al., 2005; Qiu et al., 2006; Jansen et al., 2007; Moore et al., 2007; Soltis et al., 2007). Previous work has documented structural features of the Amborella flower (Endress and Igersheim, 2000b; Buzgo et al., 2004), carpel and ovule (Endress and Igersheim, 1997, 2000a; Yamada et al., 2001), female gametophyte and endosperm (Tobe et al., 2000; Floyd and Friedman, 2001; Friedman, 2006), and some aspects of its pollination biology (Thien et al., 2003). Here I use hand pollinations and serial collections to describe structural aspects of the pollen tube pathway of Amborella, and the development of the pollen tube and female gametophyte through the time of formation of zygote and primary endosperm. I then compare these attributes with those of other early-divergent angiosperms and some gymnosperms to reconstruct early developmental transformations that led to a truly new reproductive biology.
MATERIALS AND METHODS
Amborella trichopoda (2n = 26) is an evergreen understory shrub or small tree endemic to New Caledonia (Jérémie, 1982). It is dioecious, both wind- and insect-pollinated (Thien et al., 2003), and flowers strongly during the transition from rainy to dry season in March and April. Pollinations were performed in early April 2001 in a population on the Plateau de Dogny, near Sarramea, New Caledonia (see Thien et al., 2003). Pollen was collected from male plants by cutting branches, placing them in water, and then transferring pollen directly from fresh dehiscing anthers to a stigma on a female plant in the population. Only fresh, same-day, pollen was used. Branches on female plants were bagged prior to flower opening and flowers were pollinated in situ by gently applying pollen to all stigmas in the apocarpous gynoecium with a toothpick. Pollinated flowers were kept bagged and then collected at various time intervals from 5 min to 6 d after pollination. I used the cut branch method for the majority of timed collections: bagged branches were cut about 50–80 cm below the tip several hours after pollination, placed in water, and kept in a natural environment where flowers could be collected and fixed at night.
Flowers were fixed for 24 h either in 3:1 (95% ethanol:acetic acid) or in FAA (1:2:7:10 glacial acetic acid:37% formaldehyde:H2O:95% ethanol) and stored in 70% ethanol. Carpels were infiltrated, embedded with glycol methacrylate (JB-4 embedding kit, Polysciences, Warrington, Pennsylvania, USA), and serially sectioned into 5-µm thick ribbons. Resin-embedded carpels were stained with either 0.1% toluidine blue (TBO) in H2O, with 0.005% aniline blue (AB) in 0.15 M K2HPO4, or with 0.25 mg/mL of 4'-6-diamidino-2-phenylindole (DAPI) in 0.05 M Tris buffer (pH 7.2). Other carpels were hand-cut along the median longitudinal line to expose the pollen tube pathway, then stained with 0.1% aniline blue in 0.1 M K3PO4.
Hand-sectioned carpels were viewed with a Zeiss (Thornwood, New York, USA) Stemi-SV11 stereoscope. Serial sections from resin-embedded carpels were viewed on a Zeiss Axioplan II light microscope with differential interference contrast (DIC) or fluorescence. On both microscopes, fluorescent light was filtered with (1) a UV filter set designed for DAPI visualization (Zeiss model no. 48702) with excitation filter (365 nm, band pass 12 nm), dichroic mirror (FT395), and barrier filter (LP397) or (2) a modification of that filter set to visualize both aniline blue and DAPI (substituting barrier filter LP397 with filter LP520). Micrographs were made with Zeiss Axiocam digital camera, and structures were measured using Zeiss Axiovision version 4.0 software. Images were processed with the program Photoshop 7.0 (Adobe, San Jose, California, USA). Image manipulations were restricted to operations applied to the entire image.
Pollen tube length in each carpel was measured at 16 time intervals as the distance from the tip of the stigma above the mouth of the stylar canal to the tip of the longest pollen tube (pollen tubes that could be traced to their pollen grain always originated from that area). Pollen tube pathway length was the longest pollen tube in the carpel plus the remaining distance along pollen tube pathway to the micropyle. Pollen tube growth rates were calculated using pollinated flowers from a single maternal tree as the length of the longest pollen tube divided by the time since pollination (N = 4 flowers/timepoint at 3, 5, 6.25, 9, 11, 13.7 h). I used the slope of the simple linear regression line in the program Excel 2003 (Microsoft, Redmond, Washington, USA) to estimate mean and standard deviation of leading pollen tube growth rate (3–13.7 h after pollination). For comparative purposes, I calculated the average sustained pollen tube growth rate necessary to achieve fertilization from many studies, taking the minimum pollen tube pathway length reported for a taxon and dividing by the earliest time at which a pollen tube was reported in the micropyle of that taxon.
To assess fertilization status, I scored female gametophytes as fertilized when there was evidence of pollen tube entry and/or presence of sperm nuclei within the female gametophyte, or if a zygote, primary endosperm nucleus (PEN) or multiple endosperm cells was present. Zygotes and PENs are distinctive and I confirmed this from material in which pollen tube entry into the female gametophyte could be seen. I also determined female gametophyte size in relation to fertilization status, although I never used this data alone to infer fertilization. Unfertilized female gametophytes were those in which there was no sign of pollen tube, sperm or zygote/PEN morphology.
To establish the maximum size of the female gametophyte (central cell) before fertilization and to describe the growth rate of the primary endosperm cell after fertilization, I analyzed central cell size and primary endosperm cell size as a function of time after pollination. I used an upper boundary analysis method (Blackburn et al., 1992; Zhang et al., 2005) to fit an ordinary least squares regression line to fertilized and to unfertilized female gametophyte size data. Upper boundary analysis is appropriate for estimating growth rate because sizes at each timepoint are underestimated when ovules are abortive or obliquely sectioned. Furthermore, sizes of late-fertilized primary endosperm cells will be smaller than those that were fertilized earlier, and because fertilization time cannot be known, the largest primary endosperm cells at each time will best reflect growth from a common fertilization time. I arbitrarily selected time intervals of 10 h and removed all but the maximum size female gametophyte from each interval before each regression analysis.
RESULTS
Pollen tube pathway
Stigmas in newly opened flowers are a translucent whitish-green and are often, but not always visibly wet. When wet, the stigmatic exudate often forms a single mass covering all stigmas of separate carpels within the flower. Stigmas on unpollinated flowers become dry and white after several days. Stigmas on pollinated flowers turn rose-red within 8 h and become drier and darker afterward.
The pollen tube pathway in a mature Amborella carpel is divided into three distinct regions: (1) the stigmatic crest consisting of long, densely packed multicellular, uni- to multiseriate papillae (Figs. 2–5; Endress and Igersheim, 2000a); (2) the stylar canal, which functions as a relatively undifferentiated, secretory transmitting tract formed by the incompletely sealed ascidiate carpel (Figs. 5, 6); and (3) the ovarian cavity, which is almost completely filled by a single downward-facing ovule at maturity (Fig. 5).
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Pollen tube walls stained strongly with aniline blue, from pollen grain intine to near the tip, indicating they are callosic (Stone and Clarke, 1992) in all areas except the tip (Fig. 4). The first callose plug, initiated from one side of the callosic inner wall (Williams, 2008), was not seen until pollen tubes were at least 9 h old, usually within the stylar canal. Pollen tubes grow between stigmatic hairs directly to the base of the stigma, and upon reaching carpel ground tissue, either arrest growth or are deflected (Figs. 3, 7, 8). Pollen tubes do not grow between the tightly packed cells of the carpel ground tissue (Fig. 9) and only enter the stylar canal through its open mouth (Fig. 10).
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Rod-shaped bacteria invaded the stigmatic region of one carpel in which the female gametophyte had already been fertilized (Fig. 11). In this case, there was an unbroken band of carpel ground tissue cells with unusually thick cell walls beneath the base of the stigma (Fig. 11A, C). Aniline blue staining revealed these thickenings to be strongly callosic (Fig. 11B). This sealing of the carpel also extended across the mouth of the stylar canal (Fig. 11A), where bacteria would have most direct access to the inner carpel. Bacteria were not seen within secretions in the stylar canal or any other area below this substigmatic barrier (over 70 serial sections were viewed). The callosic barrier was not present in uninfected carpels (compare Figs. 5 and 9 with Fig. 11).
In the area near the mouth of the stylar canal, stigmatic hairs grade into a zone of densely staining cells several layers thick that form the appressed inner surfaces of the ascidiate carpel. There is no single distinct, organized epidermal layer bounding these inner surfaces (Figs. 5, 6), but cells in the region adjacent to the canal are densely cytoplasmic, indicative of high metabolic activity associated with secretory activity (Evert, 2006), and their apparently high water demands are supplied by a nearby massive dorsal vascular tissue consisting mostly of tracheoids (Figs. 7, 8, 12, and 13).
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). Pollen tubes entering the micropyle were significantly smaller in diameter than those within the transmitting tract or stigmatic tissues: mean ± SD diameter within the micropyle was 4.75 ± 0.67 µm (N = 18), whereas in the stylar canal, the mean was 7.52 ± 1.36 µm (N = 18) (t-test, P < 0.0001). Usually only a single callose plug was seen along the entire length of pollen tube, about half the distance from stigma to micropyle (Fig. 13) but another often formed in the micropyle (Figs. 15, 17). A callose spot can be seen in the penetrated synergid (Fig. 15). In most cases, only a single pollen tube penetrated the micropyle, the underlying nucellus, and a synergid of the female gametophyte. Of 30 carpels that had at least one pollen tube in the ovarian cavity, 10 had micropyles that had been reached by more than one pollen tube (Figs. 16, 17), and eight of these had multiple entry. In two cases, a pollen tube grew past a micropyle that had already been penetrated by a pollen tube (Fig. 16). Several times, one or two pollen tubes curled up between the inner integument and the nucellus, while another entered the nucellus (Figs. 17, 18A). The nucellus is only two to three cell layers thick, and pollen tubes passed through it without disrupting cell walls (Fig. 18B).
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Female gametophyte before fertilization
The Amborella female gametophyte ultimately produces eight cells and nine nuclei, and thus the egg apparatus comprises three synergids and an egg cell (Friedman, 2006). In this unique form of development, cellularization occurs at the eight-nucleate stage to form three antipodal cells and a polar nucleus at the chalazal pole and three undifferentiated cells plus a polar nucleus at the micropylar pole. Subsequently, two of the three undifferentiated cells become synergids, and the third undergoes cell division to give rise to an egg cell and a third synergid (Friedman, 2006). All unfertilized female gametophytes, where the number of cells or nuclei in the micropylar domain could be determined, had three synergids subtending a prominent egg cell (Figs. 19, 20).
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Sperm were not seen in the female gametophyte until 23.5 hap, adjacent to the egg cell and associated with degenerate synergid material (Fig. 22A). Before fertilization, polar nuclei were positioned in the central region but never at the chalazal pole (Table 1). Polar nuclei were first seen adjacent to the egg at 14.5 hap and also when sperm were present at 23.5 hap (Fig. 22). The first zygote was also seen at 23.5 hap, and the primary endosperm nucleus (PEN) was positioned within the chalazal domain at this and later times (Table 1; Fig. 23). Primary endosperm nuclei are distinctly different from polar nuclei or the polar fusion (secondary) nucleus: they are much larger, they have a larger nucleolus (or three small nucleoli), they fluoresce brighter with DAPI, and after they become situated at the extreme chalazal pole, they have a distinct star-shaped pattern of cytoplasmic strands connecting to the edges of the coenocyte (Fig. 23). A free sperm nucleus was seen in the primary endosperm cell as well (Fig. 23 inset). Zygotes usually possessed a distinctive circular cell wall with a large nucleus situated in the center of a vacuolate cell and connected by cytoplasmic strands to its cell wall. Egg cells were small and without a large vacuole or larger and vacuolate with a small nucleus positioned at the chalazal edge of the cell. The first division of the zygote or PEN was never observed before 83 hap. At 138 hap, the endosperm had become multicellular, and in one case a 4-celled embryo was accompanied by a ca. 5-celled endosperm.
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Most flowering plants share a suite of unique developmental innovations associated with the fertilization process, thus a number of changes to progamic phase biology must have occurred during the early history or prehistory of angiosperms compared to the situation in ancestral seed plants. Amborella is only one surviving lineage among many that diverged early in angiosperm history. However, the data from Amborella and from other early-diverging lineages, when taken together, may provide insights into the likely plesiomorphic states of the many characters that comprise the highly integrated fertilization syndrome of flowering plants. In this discussion, I use "basal grade angiosperms" for Amborella, Nymphaeales, and Austrobaileyales; and "early-divergent angiosperms" to include these plus Ceratophyllum, Chloranthales, eumagnoliids, the monocot lineages Acorus and Alismatales, and several groups of early-diverging eudicots: Ranunculales, Sabiales, Proteales, Trochodendrales, and Buxales.
Structural features of the pollen tube pathway and their bearing on the origin of carpel closure
In Amborella, pollen is received on a well-developed multicellular, multiseriate stigma (Endress and Igersheim, 2000a), and pollen often germinates on secretions without contacting papillae. Pollen tubes with callose walls grow within secretions toward the stigma base. They do not penetrate the substigmatic ground tissue but are deflected or grow laterally toward the mouth of the stylar canal. Because pollen tubes occasionally arrived on stigmas from adjacent free carpels, Amborella seems to be yet another apocarpous basal grade angiosperm with some form of intercarpellary pollen tube growth (Williams et al., 1993; Endress, 2001; Wang et al., 2002). In this study, hand pollinations probably provided many more pollen grains than would normally occur on a stigma, and as such, successful pollen tubes always originated from pollen just above the mouth of the stylar canal. The stylar canal is formed from the unfused inner margins of an ascidiate carpel (Endress and Igersheim, 2000a), and the stigmatic hairs near its mouth are continuous with multiple files of densely cytoplasmic cells that form the more or less defined secretory canal. Because the stylar canal is generally not bounded by a distinct epidermal layer, the Amborella transmitting tract is characterized as semiclosed (Hanf, 1936). Pollen tubes exit the stylar canal at the top of the ovarian cavity, grow around the single pendant ovule, and enter its downward-facing micropyle. They grow between cells of a very thin nucellar apex before entering a degenerate synergid that subtends the egg cell.
The stigma
All extant early-divergent angiosperms studied to date have a well-developed stigma formed from the tip or margins of the carpel (Endress, 2001), and the fossil record also indicates stigmas are ancient (Zavada and Taylor, 1986; Friis et al., 2000, 2005). Amborella has a wind/insect pollination syndrome (Thien et al., 2003), and its stigma is similar in structure to that of wind- or wind/insect pollinated early-divergent angiosperms such as Trimenia, Hedyosmum, Ascarina, and Brasenia (Endress and Igersheim, 1997; Endress, 2001, 2005; Bernhardt et al., 2003). The stigma has a primary role as an early mediator of pollen–carpel interactions (Zavada and Taylor, 1986; Lloyd and Wells, 1992), and it appears to be the site of self-sterility in the basal grade angiosperm, Trimenia (Bernhardt et al., 2003).
A remarkable aspect of many angiosperm pollen tube pathways is that, though they initially support growth of many pollen tubes, often only a single pollen tube approaches each ovule (Maheshwari, 1950; Spielman and Scott, 2008). Such sorting is mediated by a hierarchy of molecular signaling cascades from stigma to egg in model angiosperms (Hulskamp et al., 1995; Ray et al., 1997; Higashiyama et al., 2001; Huck et al., 2003; Palanivelu and Preuss, 2006). In Amborella, the primary reduction of the pollen tube cohort occurred within the stigmatic region: only one or two pollen tubes ever entered the open stylar canal. Those that did enter had a high probability of reaching the ovule (as also reported for Illicium; Williams et al., 1993). These observations suggest that in Amborella pollen competition for access to the single ovule occurs primarily within the stigma and that gamete selection is strongest at the pollen germination and early tube growth stages of development. However, selection for fast early development might have been slow to have an effect if early angiosperms were pollen limited. Thien et al. (2003) found fewer than half of Amborella flowers received pollen, and those that did typically had zero to five pollen grains per carpel.
The stylar canal and ovarian cavity
Carpels can develop as leaf-like (plicate) or tube-like (ascidiate) structures, and in many angiosperms carpel closure occurs late in development by a process of fusion of inner margins (Endress, 1994, 2001; Tucker and Kantz, 2001). Amborella and many other early-divergent angiosperms lack such postgenital fusion—their ascidiate carpels are open at maturity and are sealed by secretions, not fused tissues (Endress and Igersheim, 2000a). Results reported here show that the pollen tube pathway of Amborella follows a continuous line of secretions from stigma to open stylar canal and ovarian cavity. There was no evidence of true intercellular pollen tube growth in which pollen tubes pass through solid ground tissue between cells that are joined by middle lamellae.
Open, ascidiate carpels sealed with secretions have been reconstructed as ancestral in angiosperms (Doyle and Endress, 2000; Endress, 2001). Early-divergent angiosperms with such plesiomorphic carpel morphology and in which pollen tube growth follows the open secretory pathway include Amborella, Austrobaileya (Williams, 2008) and Kadsura (Lyew et al., 2007). Other taxa with plesiomorphic open carpels have different patterns. In Sarcandra and Chloranthus (Chloranthaceae; Hristova et al., 2005), pollen tubes do not to penetrate substigmatic ground tissue, but in contrast to Amborella, they grow between tightly packed epidermal papillae of stigma and stylar canal. Trimenia (Bernhardt et al., 2003) and Brasenia and Cabomba (Taylor and Williams, in press) have a different pattern in which pollen tubes grow directly into solid substigmatic ground tissue to reach the stylar canal. Finally, a few basal grade angiosperms have postgenital fusion of a peripheral portion of their carpels, and in these (Nymphaea; Orban and Bouharmont, 1995; Nuphar and Illicium; J. H. Williams, unpublished data) pollen tubes grow through a short substigmatic region of developmentally fused ground tissues to reach the stylar canal.
Parsimony favors the hypothesis that the ancestral state of pollen tube growth through the carpel was along an entirely open, secretory pathway as occurs in Amborella, Austrobaileya, Kadsura, and probably Hedyosmum (J. H. Williams, unpublished data) and Hydatellaceae (Rudall et al., 2008). Different forms of intercellular pollen tube growth—such as within secretions between tightly appressed tissues (Amborella) or densely packed epidermal papillae (Sarcandra), within a short region of developmental fused cells (Nymphaea), or in the extreme case, within ground tissues in which pollen tubes must digest middle lamellae (Trimenia, Brasenia)—can be viewed as early experiments in pollen tube pathway anatomy. It is notable that carpel closure by developmental fusion evolved independently in several early-diverging lineages and occurs late in development along the carpel margins only. True carpel closure, and hence, long solid transmitting tracts, is not known within basal grade angiosperms.
The nucellus
In all early-divergent angiosperms studied to date, including Amborella (this study); Nymphaea, Nuphar, Cabomba, and Brasenia (Nymphaeales; Orban and Bouharmont, 1995; Taylor and Williams, in press); Trithuria (Hydatellaceae; Friedman, 2008); Austrobaileya, Trimenia, and Illicium (Austrobaileyales; Bernhardt et al., 2003; Koehl et al., 2004; J. H. Williams, unpublished data); and Hedyosmum, Sarcandra, and Chloranthus (Chloranthaceae; Hristova et al., 2005; J. H. Williams, unpublished data), pollen tubes grow between cells of the nucellus to reach the female gametophyte. However, the nucellar covering through which pollen tubes pass is also quite thin in early-divergent angiosperms, consisting of only about three cell layers in Amborella and only a single layer in many Nymphaeales (Johri et al., 1992). The nucellar apex of gymnosperms, other than Ephedra, is much thicker, ranging from a few hundred microns up to about 3 mm (Appendix 1).
Nondestructive pollen tube growth between nucellar cells is a feature that distinguishes angiosperms from gymnosperms and likely evolved a single time, given its ubiquity in early-divergent lineages. It remains to be seen whether pollen tube growth through various carpel ground tissues is fundamentally similar to growth through nucellar tissue.
Carpel closure
True carpel closure may have been advantageous in early angiosperm history because it provided mechanical protection against pathogens and a site in which maternal signaling and provisioning as well as pollen competition were intensified (Stebbins, 1974; Mulcahy, 1979; Haig and Westoby, 1989; Lloyd and Wells, 1992; Endress, 2001). The finding that many basal grade angiosperms do not have true carpel closure (and solid pollen tube pathways) raises the possibility that an ancestrally secretory pollen tube pathway might also have been a conduit for pathogen infection. Wet, montane cloud forests are permissive environments for microorganisms, and the sugars needed for pollen tube growth are also attractive to fungi and bacteria.
Amborella possesses two mechanisms for sealing carpels after pollination. Amborella stigmas showed signs of senescence within 8 hap, and rapid senescence has been shown to protect against pathogen invasion in other species (Valdivia et al., 2006). Second, Amborella may also effectively seal the inner carpel from bacterial infection by secretion of callose into cell walls across the entire substigmatic region. Callose is known to be synthesized quickly during plant–pathogen interactions (Stanghellini and Aragati, 1966; Dumas and Knox, 1983; Stone and Clarke, 1992). Rapid stylar senescence and callose secretion are two solutions to the problem of having open, secretory pollen tube pathways. Pathogens may have been a driving force for the repeated evolution of partial carpel closure, but pollen tube innovations that enabled growth through developmentally fused tissues must have already been present or evolved concurrently.
The fertilization process in Amborella
During the time between pollination and fertilization, female gametophyte differentiation and pollen tube growth must be synchronized such that sperm and egg are fully differentiated when they meet (Friedman, 1999; Herrero, 2003). At the time of pollination, Amborella female gametophytes were near maturity—they had become cellularized and were near their maximum unfertilized size (Fig. 24). Most had degenerate synergid(s), polar nuclei initiating fusion in the center of the central cell, and degenerated antipodals. Nearer the time of fertilization (about 24 hap), the two polar nuclei or the secondary fusion nucleus became positioned in the central cell directly adjacent to a highly vacuolated egg cell with its apically positioned nucleus (Fig. 22; Table 1). This sequence of events is typical of the fertilization process in other angiosperms (see reviews in Russell, 1992; Reiser and Fischer, 1993; Williams and Friedman, 2004).
There is good evidence that double fertilization occurs in Amborella. A pollen tube released two sperm in degenerate synergid material, and a free sperm nucleus was seen within the central cell. In female gametophytes that were entered by pollen tubes, the central cell (putative primary endosperm cell) often had grown beyond the mature size of central cells in unfertilized female gametophytes. The putative primary endosperm nucleus (PEN) was also larger than a secondary nucleus (formed from fusion of two polar nuclei) in unfertilized material. Finally, the PEN was most often seen in a novel chalazal position, and commonly possessed three nucleoli, indicative of the presence of three sets of chromosomes. Fusion of two polar nuclei just before or during their fusion with a sperm has been shown to produce a PEN with three nucleoli in other early-divergent angiosperms, such as Butomus (Roper, 1952), Chloranthus (Yoshida, 1959), and Sarcandra (Yoshida, 1960). These data strongly suggest that Amborella has a triploid endosperm with one paternal and two maternal genomic components.
Reconstructing developmental timing of the ancestral seed plant progamic phase
There is good reason to think that the time between pollination and fertilization in the earliest seed plants was quite long. Seed plant outgroups have long-lived gametophytes, and the portion of their life history that is comparable to the progamic phase of seed plants is also long. Ferns, lycophytes, and bryophytes all have an interval on the order of weeks to years between spore dispersal to the environment and the release of sperm from a mature gametophyte (Hauke, 1968; Lloyd and Klekowski, 1970; Whittier, 2003; D. K. Smith, University of Tennessee, personal communication). The shortest known time from spore dispersal to first reproduction of the gametophyte in such groups seems to be restricted to derived lineages of aquatics, such as the lycophyte Isoetes (about two weeks; Bierhorst, 1971) and the ferns, Ceratopteris (10–14 d; L. Hickok, University of Tennessee, personal communication) and Marsileaceae (after sporocarps release spores, gametophytes mature within a day; Bierhorst, 1971).
Male gametophyte ontogeny, mature structure, and the functional biology of the pollen tube of cycads and Ginkgo are more comparable to gametophytes of seed plant outgroups than to those of male gametophytes of Gnetales and angiosperms (Singh, 1978; Friedman, 1993). Thus, the 4–12 mo interval between pollination and sperm release in cycads, Ginkgo and most conifers (Appendix 1) can be seen as a plesiomorphic life history character.
Reconstructing developmental timing of the ancestral angiosperm progamic phase
In Amborella, stigmas are receptive in newly opened flowers and female gametophytes are cellularized (i.e., egg cell present) and near their maximum unfertilized size (Appendix 1; Fig. 24). Virtually all basal grade and most other early-divergent angiosperms are similar (Appendix 1 and Endress and Igersheim, 1997, 1999, 2000a; Igersheim and Endress, 1997, 1998; Igersheim et al., 2001). Exceptions occur within Piperales (Hydnora, Piper, and Thottea; Igersheim and Endress, 1998), Laurales (Cassytha, Doryphora, and Sparattanthelium; Endress and Igersheim, 1997), and several early-divergent eudicots (Appendix 1; Endress and Igersheim, 1999; Sogo and Tobe, 2006).
Because the Amborella female gametophyte is near maturity at the time pollen tube growth begins, fertilization must occur shortly thereafter unless eggs have long receptive periods. In this study stigmatic receptivity lasted less than three days (see also, Thien et al., 2003), and ovules appeared viable for only a few days. Thus, the window for pollen tubes to reach eggs is short. Consistent with this prediction, Amborella pollen tubes first reached the micropyle in less than 14 h, gamete fusion was first observed at about 24 h, and nearly 100% of gametophytes were fertilized within 55 h.
Other early-divergent angiosperms in which the egg cell has formed before pollination generally have an interval of 
2–48 h between pollination and fertilization (Appendix 1). Schnarf (1929) and Maheshwari (1950) found that most angiosperms have intervals in this range, and parsimony analysis supports such an interval as the ancestral state (Williams, 2008). Isolated occurrences of long gymnosperm-like progamic phases within early-divergent angiosperms such as in Platanus and Euptelea (Appendix 1) are most likely apomorphic, though little is known about their fertilization biology.
The developmental origins of short reproductive cycles in gymnosperms and angiosperms
Rapid reproduction is rare among nonflowering seed plant groups and is said to have played a role in the origin and ecological success of early angiosperms (Stebbins, 1965, 1974, 1976; Takhtajan, 1976; Queller, 1983; Haig and Westoby, 1989; Doyle and Donoghue, 1993). Gymnosperms generally have both a long progamic phase and a long period of seed maturation and time to seed germination (Singh, 1978; Willson and Burley, 1983). Basal grade angiosperms have very short progamic phases, but they do not have particularly fast seed development. Though the ancestral angiosperm seed is reconstructed as very small relative to gymnosperm seeds (Moles et al., 2005), early-divergent angiosperm seeds contain underdeveloped embryos (Baskin and Baskin, 1998; Forbis et al., 2002), and those of Amborella, Austrobaileya, many Nymphaeaceae, Cabombaceae, and Chloranthaceae develop slowly and have months-long germination times (Feild, 2008; J. H. Williams, personal observation). Thus, heterochronic changes to the reproductive cycle during the origin of angiosperms appear to have been heavily concentrated on the pollination to fertilization period.
The plesiomorphic progamic phase in seed plants is long because pollen reception occurs before or early in megagametogenesis and fertilization occurs much later, after a large female gametophyte develops (Fig. 25; Appendix 1; Singh, 1978). Pollen tube development is correspondingly slow. In virtually all gymnosperms pollen hydration, germination, and tube growth takes several weeks or more, and there may also be periods of dormancy (Appendix 1; Owens et al., 1995; Fernando et al., 2005). Notably, in vitro and in vivo pollen tube growth rates are slow in all gymnosperms, ranging from 1 to 20 µm/h (Appendix 1; Hoekstra, 1983; de Win et al., 1996; Yatomi et al., 2002; Lazzaro et al., 2005). Thus, slow pollen germination and pollen tube growth are plesiomorphic features of seed plants (Fig. 25).
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). Ephedra (Gnetales), in which fertilization takes place about 10–16 hap, is the extreme example, except that the large female gametophyte is conserved (Fig. 25) and pollen tube growth rate remains very slow (Appendix 1).
The short progamic phases of early-divergent angiosperms have a strikingly different developmental origin relative to those of gymnosperms such as Ephedra. Most considerations of the origin of the angiosperm fertilization process have accepted that female gametophytes underwent a process of reduction (Stebbins, 1976; Takhtajan, 1976; Favre-Duchartre, 1979). The evolutionary transition from a months-long to a day-long progamic phase in the common ancestor of extant angiosperms involved precocious maturation of the egg, perhaps at a 4-, 8-, or 9-celled stage of ontogeny (Williams and Friedman, 2002; Friedman and Williams, 2003; Friedman, 2006), and consequently the shifting of fertilization from late to early megagametogenesis (Fig. 25). Progenesis of the female gametophyte would have necessitated shortening the period of pollen tube development because pollination timing was not similarly displaced to an earlier time (Fig. 25). Amborella and other early-divergent angiosperms have much faster pollen germination schedules and shorter periods of pollen tube growth than most living gymnosperms (Appendix 1; Fig. 25). Importantly, and in contrast to Ephedra and all other gymnosperms, shortening of the pollen tube growth period in angiosperms occurred in concert with innovations that facilitated much faster pollen tube growth.
The origin of rapid pollen tube growth in angiosperms
The in vivo pollen tube growth rate of Amborella of about 100 µm/h is comparable to that of many other early-divergent angiosperms, yet from 5 to >200-fold faster than that of any gymnosperm (Appendix 1). However, Amborella pollen tubes are among the slowest in angiosperms, which typically grow at rates of 600 to more than 10000 µm/h (Maheshwari, 1950; d’Eckenbrugge, 1990; Taylor and Hepler, 1997). These data suggest that ancient angiosperms originated with very slow pollen tube growth rates, even though they already possessed a number of innovations that were essential to the subsequent evolution of faster growth rates.
Early seed plant male gametophytes inherited a rhizoid-like pattern of haustorial pollen tube growth (such as occurs in extant cycads and Ginkgo), and sperm swam independently to the egg (Friedman, 1993). Siphonogamy, in which pollen tubes function to carry nonmotile sperms to eggs, may have evolved once in a recent common ancestor of conifers, Gnetales and angiosperms, or independently in angiosperms and Gnetales plus conifers (Friedman and Floyd, 2001; Rudall and Bateman, 2007), depending on seed plant relationships (Hajibabaei et al., 2006; Burleigh and Mathews, 2007). In either case, pollen tubes of Gnetales and conifers retain a number of plesiomorphic seed plant features that appear to limit their growth rates, including a growth mode in which tubes cause cell death of adjacent (usually nucellar) cells in order to advance, the need to maintain cytoplasmic continuity between growing pollen tube tip(s) and pollen grain, and the thick, cellulose-based primary wall structure of pollen tube and tip (Dumas and Knox, 1983; Derksen et al., 1999; Fernando et al., 2005).
Amborella and other basal grade angiosperms have narrow pollen tubes that grow without causing cell death, within novel carpellar secretions or tissues. All studies of early-divergent angiosperms report pollen tube walls to be constructed predominantly from 1,3-β-glucan (callose), and most also show that callosic inner wall thickenings act to plug the tube in distal areas (see Williams, 2008). Studies of model system angiosperms indicate pollen tubes have thin pectic tips (Li et al., 1994; Geitmann and Steer, 2006). Based on the reconstruction of the ancestral pollen tube pathway described above, these distinguishing features of angiosperm pollen tubes were initially linked to free growth within secretions of an open carpel.
Two observations suggest there would have been strong selection for the buildup of callose in lateral tube walls of pollen tubes growing within a secretory environment. Pollen tubes grown in thick media or in solid tissues produce thinner callosic walls than those grown in less viscous media, presumably because of the mechanical support provided by thicker media or tightly packed cells (Parre and Geitmann, 2005). Callosic pollen tube walls are also much less permeable than cellulose-based walls (Cresti and van Went, 1976) and thus better maintain osmotic conditions in a secretory environment.
It has been hypothesized that the novel callosic pollen tube wall structure of angiosperms originated as a consequence of selection for rapid pollen tube growth rate (Knox, 1984), which caused callose synthase complexes to be displaced laterally from the tip (Derksen et al., 1999). Conifer pollen tubes secrete callose at the tip only (Derksen et al., 1999). Such a model assumes angiosperms have modified conifer-like pollen tubes. The data reported here suggest callosic walls may have originated in response to selection for rapid pollen germination coupled with growth in a novel secretory environment. Callosic walls do not seem to have been a prerequisite for achieving the growth rates seen in Amborella and some other early-divergent angiosperms. For example, root hairs, which have cellulosic primary walls comparable to those of gymnosperm pollen tubes, have growth rates similar to Amborella: 100 µm/h in Arabidopsis (Schiefelbein, 2000) and 35–144 µm/h in other angiosperms (Hepler et al., 2001; Evert, 2006).
The modest, initial increases in pollen tube growth rates that occurred during the evolutionary transition to angiospermy were associated with the transition from a destructive mode of tube growth through a solid obstructing nucellar tissue, such as in the conifer Cedrus (Chowdhury, 1961), to a mode in which growth occurred along a secretory pathway and through a very thin nucellus, as in Amborella (Fig. 26). This novel mode of nondestructive pollen tube growth probably allowed a modest initial growth rate increase prior to the origin of extant angiosperms. Within living lineages, at least three early-divergent aquatic lineages, including Nymphaeales, had the capacity to independently evolve much faster pollen tube growth rates, comparable to those of derived monocots and eudicots (Appendix 1). The pollen tube pathways of taxa in these lineages vary widely in composition and length, implying a common set of pollen tube innovations that could support the evolution of rapid growth rates was already present in their common ancestor, prior to the radiation of extant angiosperms. Structural aspects of angiosperm pollen tube walls are implicated because they provide the biomechanical support, maintenance of turgor pressure, and rapid biosynthesis of wall materials needed to support tremendous increases in growth rates. It is notable that some fungal hyphae also have callose walls and achieve fast tip growth rates (Shapiro and Mullins, 2002).
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), angiosperm pollen tube growth rates seem to be limited primarily by the nature of the maternal tissues they interact with (Fig. 26). Indeed, the apparent evolutionary boundary represented by the high sustained pollen tube growth rate of maize (Fig. 26), is far exceeded by short-term growth rates on the stigma of one early-divergent eudicot (Stone et al., 2004). Complementary changes in maternal and paternal provisioning and signaling as well as the development of solid or semisolid pollen tube pathways that provided mechanical support and guidance for pollen tubes underlie a great diversification of carpel structure and physiology. There remains much to be learned about the historical and/or present-day forces that have shaped the tremendous diversity in reproductive timing, pollen tube growth rates, and pollen tube pathway lengths present in angiosperms relative to gymnosperms.
Conclusions
Carpel closure, or angiospermy, has long been seen as a central defining feature of flowering plants, and its origin and early evolution is closely tied to its role in transmitting pollen tubes rapidly from stigma to ovule (Stebbins, 1974; Endress, 1994). In Amborella, pollen germinates within 2 h, and pollen tubes grow entirely through secretions from stigma to ovule. Double fertilization occurs within 24 h of pollination. Relative to derived monocots and eudicots, the pollen tube pathway of Amborella is very short, and pollen tube growth rates are very slow. However, Amborella pollen tubes are quite similar to those of derived angiosperms: they are narrow, have callosic walls, one or more callose plugs, and lack callose in the growing tip.
A review of studies of early-divergent angiosperms indicates that the ancestral pollen tube pathway was short and secretory, and pollen tubes must have evolved their novel callosic structure and mode of facilitated (nondestructive) growth while developing within secretions. Pollen tubes may have first evolved the ability to grow within ground tissues when an ancient, but novel, stigmatic region surrounding the mouth of the stylar canal began expanding to cover more distant carpellar surfaces. Nondestructive pollen tube growth through ground tissues in turn allowed the new possibility of true carpel closure by developmental fusion of carpel walls. The spectacular and geologically recent diversification of flowering plants that so intrigued Darwin must have come about by an accumulation and integration of a multitude of novel traits during their early history. Structural aspects of pollen tube growth found in Amborella and other early-divergent angiosperms clearly preceded elaborate carpel forms that changed the length and composition of the pollen tube pathway in derived lineages of monocots and eudicots. Such carpel innovations include true carpel closure as well as the joining of free carpels (syncarpy) to form a common style with an internal transmitting tract and increases in stigma to ovule distances through elongation of the style and/or addition of ovules to an ancestrally shallow ovary.
Characteristics of the progamic phase of early-divergent angiosperms and selected gymnosperms. Superscripts "a–d" are used in the references and notes section to refer to the corresponding column of the table: (a) Earliest time pollen tubes were observed in micropyle (mp) or female gametophyte (fert). (b) Minimum distance from stigma to first ovule along pollen tube pathway, from fresh material or from published photos (n, number of maternal plants). (c) Average sustained leading pollen tube growth rate to first ovule (column b divided by column a, except for gymnosperms, in which only the active period of pollen tube growth was used). (d) Leading pollen tube growth rate measured before fertilization [mean (m) ± standard deviation, range (r)].
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FOOTNOTES
1 The author thanks T. Jaffré (L’Institut de Recherche pour le Développement, Noumea, New Caledonia) for logistical support and T. Arias and M. L. Taylor for laboratory assistance. H. G. Dickinson, A. N. Doust, T. S. Feild, W. E. Friedman, and L. Hufford provided many helpful comments. Funding was provided by the University of Tennessee and the National Science Foundation (DEB 0640792). The author especially thanks W. E. Friedman for encouragement and for travel support in New Caledonia. 
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