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Department of Environmental, Population, and Organismic Biology, Campus Box 334, University of Colorado,Boulder, Colorado 80309
Received for publication January 5, 1999. Accepted for publication April 16, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: basal angiosperms • developmental evolution • embryology • endosperm development • eudicot • free nuclear endosperm • Platanaceae • Platanus racemosa.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Friedman, 1994
). However, despite intense interest in the origin of flowering plants as well as the considerable recent efforts of systematists to address questions of relationship among basal clades (Donoghue and Doyle, 1989
; Hamby and Zimmer, 1992
; Chase et al., 1993
; Qiu et al., 1993
; Doyle, Donoghue, and Zimmer, 1994
; Nixon et al., 1994
; Hoot, Magallón-Puebla, and Crane, 1997
; Qiu, 1997
; Nandi, Chase, and Endress, 1998
; Soltis et al., 1998
; Hoot, Magallón, and Crane, 1999
), there has been little comparative analysis of the embryological characters of primitive angiosperms. These include unique features such as a highly reduced female gametophyte, triple fusion, and endosperm. Thus, the origin and diversification of some of the most defining reproductive features of flowering plants have remained virtually ignored.
Although there have been a few recent embryological studies of basal angiosperms (Tobe et al., 1993
; Heo and Tobe, 1995
; Rudall and Furness, 1997
; Svoma, 1998
), much of the embryological literature describing these taxa dates to the early part of this century, lacks photographic documentation, and is fraught with inconsistencies and errors. In addition, important features of angiosperm reproductive biology, such as endosperm development, have been reduced to a handful of typological categories that lack any phylogenetic context. Furthermore, embryological developmental patterns in basal lineages have been classified into types that are almost always based on the study of derived taxa. This "top-down" approach seriously limits our ability to address fundamental questions of the origin and evolution of these characters. As a result, existing typological schemes provide little or no basis for understanding evolutionary transitions between the types.
An explicit goal of this study (and others in progress) is to characterize embryological development patterns in basal taxa (a "bottom-up" approach) in order to infer ontogenetic transitions that occurred during the early radiation of angiosperms. Indeed, a developmental and phylogenetically based approach to describing and comparing reproductive features in primitive flowering plants, without a priori assumptions of typological categorization, is essential if we are ever to make progress in solving Darwin's "abominable mystery."
Recent phylogenetic analyses (Donoghue and Doyle, 1989
; Hamby and Zimmer, 1992
; Chase et al., 1993
; Qiu et al., 1993
; Doyle, Donoghue, and Zimmer, 1994
; Nixon et al., 1994
; Hoot, Magallón-Puebla, and Crane, 1997
; Qiu, 1997
; Nandi, Chase, and Endress, 1998
; Hoot, Magallón, and Crane, 1999
) provide the following important insights into angiosperm phylogeny that help guide this analysis. Angiosperms are monophyletic. The monosulcate Magnoliidae (magnoliids) are a nonmonophyletic basal assemblage of angiosperms from which monophyletic monocot and eudicot clades evolved. The eudicot clade includes 75% of extant flowering plant species (Drinnan, Crane, and Hoot, 1994
). These phylogenetic findings indicate that in order to understand character evolution during the early radiation of angiosperms we must focus on magnoliids, basal monocots, and basal eudicots.
Platanus is the single extant genus representing one of the earliest branching eudicot clades, Platanaceae (Hufford and Crane, 1989
; Schwarzwalder and Dilcher, 1991
; Chase et al., 1993
; Hoot, Magallón-Puebla, and Crane, 1997
; Hoot, Magallón, and Crane, 1999
). The platanaceous lineage has a fossil record extending back to the early Cretaceous (Friis, Crane, and Pedersen, 1988
; Friis and Crane, 1989
; Friis, Pedersen, and Crane, 1994
). Thus this group holds a key, transitional position in angiosperm phylogeny and is critical to understanding reproductive character diversification during the origin of the largest clade of angiosperms (eudicots) from a magnoliid ancestor. However, Platanus is also a taxon for which embryology is incompletely known (Johri, Ambegaokar, and Srivastava, 1992
) and for which published reports (Brouwer, 1924
; Guseinova, 1976
) are contradictory. We have therefore undertaken an embryological study of P. racemosa in order to provide unequivocal data on defining angiosperm reproductive characters.
Our goals were (1) to provide an analysis of embryological development in Platanus that moves beyond the century-old typologies that have dominated the embryological literature; and (2) to explore the evolutionary implications of our results. First, we report on the development of the female gametophyte (embryo sac), embryo, and endosperm. We then discuss the new contributions of this work and briefly compare our results to previous studies of Platanus. Finally, we compare Platanus embryological development with published data for other basal eudicots and more distantly related angiosperms in order to examine the developmental implications of the multiple evolutionary origins of free nuclear endosperm patterns among flowering plants.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), was harvested weekly from 17 March 1997 through 29 July 1997 from several trees in a wild population growing near Mentone, California. In addition, one dried inflorescence from the previous year was collected. Two voucher specimens were deposited at the University of Colorado Herbarium (COLO; Floyd and Swan 97-47). Inflorescences were placed in plastic bags, kept cool, and shipped for overnight delivery to the laboratory in Boulder, Colorado. Flowers are unisexual and clustered tightly on unisexual, spherical heads (Figs. 1–2) that are arranged in a compound inflorescence of two to seven heads on a peduncle. The plants are monoecious and are wind pollinated. Occasionally an entire inflorescence will have morphologically bisexual flowers (Fig. 3). Female flowers consist of seven to nine free carpels surrounded by staminodes (Fig. 4) and diminutive sepals.
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Fixed flowers were dehydrated through an ethanol series to 95% ethanol, infiltrated with monomer A of the JB-4 embedding kit (Polysciences, Warrington, Pennsylvania), and embedded in an oxygen-free environment. More than 1000 ovules were serially sectioned to 5-µm thickness on either a MICROM (Walldorf, Germany) or a Leica (Nussloch, Germany) rotary microtome using glass knives. Slides with acrolein or glutaraldehyde-fixed material were stained in 0.1% toluidine blue, examined, and photographed on a Zeiss (Carl Zeiss, Jena, Germany) Axiophot microscope using both bright field and differential interference contrast (DIC) optics. Slides with 3:1 fixed material were stained in a solution of 0.25 µg/mL 4',6-diamidino-2-phenylindole (DAPI) and 0.1 mg/mL phenylenediamine in 0.05 mol/L TRIZMA (Sigma Chemical Co., St. Louis, Missouri) buffer, pH 7.2, for 45 min followed by 5 min in a solution of 0.01% aniline blue in 0.1 mol/L TRIZMA buffer to visualize sperm nuclei and callose in pollen tubes. Sections were examined and photographed on a Zeiss Axiophot microscope equipped with epifluorescence (HBO 50 W burner; Carl Zeiss, Jena, Germany).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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50 µm long) differentiates deep within the nucellus (Fig. 8) 2 wk after pollination and meiosis (Figs. 9, 10) results in a linear tetrad of megaspores (Fig. 11). The chalazal-most spore, always larger and more vacuolate than the other three, develops into the functional megaspore. The other three megaspores are small, cytoplasmically dense, and they quickly degenerate (Figs. 11, 12). Thus, female gametophyte development is monosporic.
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100 µm in length before the second mitotic division occurs. At the four-nucleate stage (Fig. 15) it is similar in size and cytoplasmic appearance to the two-nucleate stage (Fig. 14). The female gametophyte continues to grow, and by the time it has differentiated into an eight-nucleate, seven-celled structure it is 300–400 µm in length (Fig. 16).
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Within the egg apparatus of the female gametophyte, the synergids are densely cytoplasmic and exhibit an obvious filiform apparatus (Fig. 19). The egg cell protrudes somewhat farther into the female gametophyte, and its nucleus is usually centrally positioned (Fig. 20). In recently fertilized ovules one synergid is collapsed and the other intact, but it is not known whether the degenerate synergid breaks down prior to fertilization. Following fertilization, the female gametophyte elongates to 500–800 µm before division of the primary endosperm nucleus occurs.
Early embryogenesis
The zygote remains undivided until the endosperm begins cellularization. However, during this time the zygote elongates toward the chalazal end of the endosperm and develops a large vacuole. The zygote nucleus occupies the apical region of the cell (Fig. 21). The first cell division is transverse and produces a basal cell, which includes the vacuole, and a smaller apical cell (Fig. 22). Transverse divisions result in a uniseriate, linear proembryo of four to six cells (Figs. 23, 24). Based on comparison of two-celled proembryos with four-celled proembryos, we believe that both the basal and apical cells divide at least once transversely. However, stages of mitosis in the two-celled proembryo were never observed.
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Embryos often become dislodged and are displaced from the micropylar end of the endosperm. Approximately 25% of the globular proembryos observed were located in the center of the early cellular endosperm (Fig. 29). All embryos ultimately produce a shoot apex, a root apex, and two well-developed cotyledons (Fig. 28). At maturity the embryo fills most of the cavity initially occupied by the inner endosperm, with a thin layer of densely cytoplasmic, outer endosperm surrounding it. Cells of the mature embryo are filled with storage products including protein bodies and lipids (determined by Sudan IV and naphthol blue-black staining).
Endosperm development
Endosperm development is depicted in Fig. 30. The primary endosperm nucleus divides in the center of the female gametophyte (Figs.30 A–B, 31–33). No permanent cell wall is formed following mitosis, although an incipient cell plate was observed between two recently separated daughter nuclei (Fig. 32). The two endosperm nuclei migrate to opposite ends of the central cell before the second mitotic division occurs. Endosperm nuclei proceed through numerous rounds of free nuclear mitosis until >1000 nuclei are formed (Figs. 30B–G, 34–37). Initially, the nuclei are evenly spaced around a large central vacuole in a thin, parietal layer of cytoplasm (Figs. 30E, 34, 37). Differentiation of the free nuclear endosperm eventually produces two cytoplasmically distinct zones. Fewer than 50 nuclei aggregate at the extreme chalazal end of the endosperm. This region of endosperm is cytoplasmically dense, lacks a central vacuole, and will hereafter be referred to as the "chalazal zone" (Figs. 30F, 35, 36). At the same time a "micropylar zone" of endosperm forms and comprises a large central vacuole with a parietal layer of cytoplasm and nuclei. As will be seen, these two free nuclear zones exhibit very different patterns of further development. The entire endosperm continues to elongate during free nuclear development to 900 µm in length.
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Following cellularization of the chalazal zone, anticlinal walls are established within the micropylar zone of the endosperm. Initially these anticlinal cell walls form between adjacent nuclei and end freely in the coenocyte (Figs. 30H, 40). Anticlinal wall formation is first manifest at the chalazal end of the micropylar zone and is associated with the final round of mitotic divisions in the coenocyte. This process, including nuclear division and associated cell wall formation, occurs in a wave that begins at the chalazal end of the micropylar zone and proceeds toward the micropylar end of the endosperm.
Independent anticlinal walls of the micropylar zone quickly fuse with adjacent walls to form uninucleate alveoli that surround the central vacuole (Fig. 41). At the end of this wall initiation phase, the endosperm has a completely cellularized chalazal zone and a single layer of uninucleate open alveoli and some closed cells surrounding the central vacuole of the micropylar zone (Figs. 30I, 42). The cells and alveoli in this layer are of varying sizes, and the anticlinal walls are not all perpendicular to the central cell wall (Fig. 42). Cell plates were observed that formed at oblique angles to the central cell wall. This process may be responsible for the formation of closed cells in the first layer of alveoli and the irregular angles and sizes of the cells and alveoli. Centripetal cellularization then proceeds rapidly, resulting in a completely compartmentalized micropylar zone of endosperm composed of large, irregularly shaped, thin-walled, uninucleate, vacuolate cells (Figs. 30J, 43). No consistent pattern of cell formation is evident in either transverse or longitudinal sections and regular layers of cells are not produced in the process of centripetal cellularization. The entire endosperm, when cellularization is complete, is 4000 µm long.
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5000 µm (5 mm) at this stage. In the mature seed the nucellus is reduced to a thin, crushed layer, except at the extreme chalazal and micropylar ends. The integuments develop into a thin seed coat, and only the outer endosperm remains, surrounding the large, well-developed embryo. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Bretzler, 1924
; Brouwer, 1924
; Guseinova, 1976
). All report a monosporic pattern of female gametophyte development, with some variability in the descriptions of size, structure, and phenology. Our findings are in basic agreement with these previous reports of female gametophyte development. Only one study claimed to have observed early endosperm, which was described as ab initio cellular (Guseinova, 1976
). Very little has been reported of embryogenesis in Platanus (Bretzler, 1924
; Guseinova, 1976
).
Platanus embryology: new contributions
Cell division patterns associated with early embryo development are variable in P. racemosa. The same embryonic form was produced through a variable sequence of cell divisions in early embryogenesis. This has been noted before in other angiosperm taxa (Burgess, 1985
; Gifford and Foster, 1989
; Kaplan and Cooke, 1997
) and argues against the use of embryological classification systems based solely on patterns of cell division and lineage. We therefore do not assign an "embryological type" (sensu Johansen or Souèges) to Platanus, but prefer to describe the developmental process based on the model proposed by Kaplan and Cooke (1997)
. Embryogenesis in Platanus proceeds through six phases: (1) zygotic polarization (Fig. 21); (2) zygotic cell division (Fig. 22); (3) filamentous, uniseriate growth (Figs. 23, 24); (4) differentiation into a three-dimensional (globular) proembryo and linear suspensor (Figs. 25, 26); (5) histogenesis/organogenesis; and (6) growth of the embryo proper (Figs. 27, 28). Although cell division patterns do not precisely correlate with the genesis of form in the embryo, the initial division of the zygote does establish two regions of the proembryo with distinct developmental fates. The basal cell will contribute only to part of the suspensor while most of the derivatives of the apical cell will form the embryo proper. The suspensor plays almost no role in embryogenesis, in contrast to many angiosperms.
Although the only previous study of early endosperm stages in Platanus reported an ab initio cellular pattern of development (Guseinova, 1976
), we clearly observed that endosperm in P. racemosa begins with a free nuclear phase. However, endosperm development in Platanus involves much more than simple free nuclear proliferation followed by cellularization. Rather, it occurs in four primary stages: (1) free nuclear proliferation; (2) cellularization of the chalazal zone; (3) centripetal cellularization of the micropylar zone; and (4) cellular proliferation and differentiation. Within each of these stages, a complex series of events occurs, involving regional zonation and differentiation of the developing embryo-nourishing tissue. It is this complex pattern of endosperm development that will form the basis for much of the following discussion.
Evolutionary implications: multiple origins of free nuclear endosperm
The objective of our work is not only to describe embryological development in Platanus, but to use this information to examine and interpret the origin and evolution of defining angiosperm reproductive characters such as endosperm. Our results show that free nuclear endosperm cannot be viewed as "a relatively simple and amorphous tissue marked by the presence of only a few differentiated cell types" (Raghavan, 1997
, p. 322) as is sometimes mistakenly claimed in the literature. We have chosen to focus on endosperm development because it is a complex process with several distinct stages that provide many points of comparison.
Ab initio cellular endosperm is the most common developmental pattern among basal angiosperm lineages and phylogenetically based analyses of character distribution indicate that it almost certainly represents the plesiomorphic condition in flowering plants (Donoghue and Scheiner, 1992
; Friedman, 1992
). Platanus endosperm is clearly derived relative to the plesiomorphic condition in angiosperms in that it has a free nuclear phase of development.
Free nuclear endosperm is the most common developmental type reported among angiosperms (Dahlgren, 1991
; Johri, Ambegaokar, and Srivastava, 1992
), and it is generally discussed within the traditional typological framework as if it were a single phenomenon with a few unusual variants (Vijayaraghavan and Prabhakar, 1984
; Johri, Ambegaokar, and Srivastava, 1992
). However, when cellular, free nuclear, and helobial types are mapped as character states onto published cladograms that resolve relationships among basal eudicot lineages (Chase et al. 1993
; Hoot, Magallón, and Crane, 1999
), parsimonious character optimization indicates that free nuclear endosperm has evolved three times independently among the lower eudicots and once in the ancestor of higher eudicots (Fig. 46). This implies that free nuclear endosperm in the monocots was also derived independently. Multiple origins of free nuclear endosperm development among dicots and monocots were also predicted by Dahlgren (1991)
. Given this hypothesis of multiple origins of free nuclear endosperm development, we would expect to find variability among taxa representing independent origins and greater similarity among taxa that share a common origin of free nuclear endosperm.
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2 mo after fertilization (Fig. 5). Centripetal cellularization does not produce regular layers of cells, but appears to be irregular (Fig. 43). The cellular endosperm differentiates into inner and outer layers (Figs. 30, 44). The embryo grows into and replaces the inner endosperm, whereas the outer endosperm persists and stores protein and oil at seed maturity (Figs. 30, 45). Most of these features are summarized in Table 1.
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; Drinnan, Crane, and Hoot, 1994
; Hoot, Magallón-Puebla, and Crane, 1997
; Soltis et al., 1998
; Stevenson and Douglas, 1998
; Hoot, Magallón, and Crane, 1999
), a surprising result given the morphological disparity of the three groups. If this hypothesis of relationship is correct, a reasonable prediction would be the presence of similar, evolutionarily homologous patterns of endosperm development in these three taxa.
Incomplete and conflicting embryological reports have been published for Nelumbo (Khanna, 1965
; Padmanabhan, 1970
; Batygina, Kolesova, and Vasiljeva, 1983
). Endosperm development was described as both free nuclear (Khanna, 1965
; Padmanabhan, 1970
) and ab initio cellular (Batygina, Kolesova, and Vasiljeva, 1983
), demonstrating the need for thorough reinvestigation of this important basal taxon.
More work has been done on the Proteaceae (Kausik, 1938a, b, 1941;
Venkata Rao, 1965, 1967, 1969, and others
), although largely with genera such as Grevillea which appear to be nested well within the family (Hoot and Douglas, 1998
) and exhibit highly derived endosperm developmental patterns (Venkata Rao, 1967
). All members of the Proteaceae exhibit free nuclear endosperm development (Johri, Ambegaokar, and Srivastava, 1992
). While derived taxa have been studied extensively, there is a single report of endosperm development in the basal genus Bellendena (Hoot and Douglas, 1998
). This taxon shares many embryological features with Platanus: an orthotropous ovule, micropyle formed by the inner integument only, distinct chalazal and micropylar zones in the free nuclear endosperm, and a large embryo in the mature seed (Venkata Rao, 1967
). However, Bellendena reportedly has micropylar-to-chalazal initiation of endosperm cellularization (Venkata Rao, 1967
), the opposite of Platanus. The similarities between Platanus and Bellendena are consistent with the hypothesis that they share a single evolutionary origin of free nuclear endosperm in a common ancestor. A more complete analysis of endosperm development in basal Proteaceae and Nelumbo is needed to provide a broader basis for comparison within this intriguing clade. It is also clear that comparative embryology has great potential to address questions of relationship in the Platanaceae/Proteaceae/Nelumbonaceae clade, which is otherwise difficult given the highly specialized and apomorphic nature of the sporophyte phase in these three families.
Few developmental analyses of endosperm are available for other basal eudicot taxa. However, several recent reports describe aspects of endosperm development for two taxa in the other two putative "free nuclear" basal eudicot clades (Fig. 46): Ranunculus (Ranunculaceae) (Chitralekha and Bhandari, 1993
; XuHan and Van Lammeren, 1993, 1997)
and Papaver (Papaveraceae) (Olson, 1981
). It should be noted that neither Ranunculus nor Papaver are basal genera within Ranunculaceae and Papaveraceae (Hoot et al., 1997
; Ro, Keener and McPheron, 1997
). Our comparison is thus limited to taxa nested within the two lineages and thus with potentially more derived characteristics. Fortunately, there do not appear to be widely deviant patterns of endosperm development within these two families as has been observed in the Proteaceae (see discussion above) (Johri, Ambegaokar, and Srivastava, 1992
, and references therein). In addition, the Menispermaceae represent a more basal branch in the ranunculid free nuclear clade than the Ranunculaceae (Fig. 46), yet embryological reports for taxa in the Menispermaceae (Sastri, 1964
), although somewhat lacking in detail, appear to show congruence with descriptions for the Ranunculaceae. Thus, the use of Papaver and Ranunculus as representatives of the two putative free nuclear clades should provide useful information.
Endosperm development in Papaver (Papaveraceae) (Olson, 1981
; Johri, Ambegaokar, and Srivastava, 1992
) differs in several respects (for which information is available) from Platanus and Ranunculus (Chitralekha and Bhandari, 1993
; XuHan and Van Lammeren, 1993, 1997
) except for the storage of protein and oil (Table 1). Papaver does show endosperm wall initiation at the filamentous embryo stage (Olson, 1981
) as does Platanus, but differs from Platanus in some other embryological features including having a micropyle formed by both integuments and a small embryo surrounded by abundant endosperm in the mature seed (Johri, Ambegaokar, and Srivastava, 1992
).
Ranunculus shares some features of endosperm development with Platanus including chalazal-to-micropylar polarity of anticlinal cell wall initiation, wall initiation associated with mitosis, and the storage of oil and protein. However, Ranunculus also differs from Platanus in the duration of cellularization, embryo developmental stage at endosperm anticlinal wall initiation, and mode of centripetal wall formation. In Platanus, some anticlinal walls in the micropylar zone appear to converge as they grow in toward the central vacuole, closing some of the alveoli formed when anticlinal walls are initiated (Fig. 42). Centripetal cellularization continues to form cells of varying size and with no distinct layering ("irregular" in Table 1) (Fig. 43). In contrast, anticlinal walls in Ranunculus grow inward without converging (Chitralekha and Bhandari, 1993
). Periclinal walls form after rounds of mitosis so that regular layers of cells are produced centripetally ("regular" in Table 1) (Chitralekha and Bhandari, 1993
). In addition to the characters compared in Table 1, Platanus embryos are large and well developed at seed maturity and are surrounded by a thin layer of endosperm. In Ranunculus, embryos only reach an early cotyledon stage and are surrounded by copious amounts of endosperm at seed maturity (XuHan and Van Lammeren, 1997)
. Clearly there is variability among these three basal eudicot taxa (Platanus, Ranunculus, and Papaver) (Fig. 46).
An even greater degree of developmental variability is evident among free nuclear endosperms when comparisons are made with higher eudicot taxa, represented here by legumes (Fabaceae) (Yeung and Cavey, 1988
; Dute and Peterson, 1992
; Chamberlin, Horner, and Palmer, 1994
; XuHan and Van Lammeren, 1994;
Algan and Bakar, 1996
), Stellaria (Caryophyllaceae) (Newcomb and Fowke, 1973
), and Helianthus (Asteraceae) (Newcomb, 1973
) (Fig. 47). These three lineages all have two similar features: micropylar-to-chalazal anticlinal wall initiation and irregular centripetal cellularization (Table 1). In general, these higher eudicot taxa have less extensive free nuclear development prior to cellularization than the free nuclear basal eudicots, although there is variability in this feature. Cellularization begins when fewer than ten free nuclei are present in Helianthus (Newcomb, 1973
), whereas many free nuclei are produced before walls form in Stellaria (Newcomb and Fowke, 1973
) and legumes (Algan and Bakar, 1996
). Endosperm cell wall initiation in the higher eudicots appears to occur at a relatively advanced embryo stage, but this feature also varies among the higher eudicots. The embryo reaches the heart-shaped stage before walls are initiated in Stellaria (Newcomb and Fowke, 1973
), but wall formation begins at the globular embryo stage in legumes (Yeung and Cavey, 1988
; Dute and Peterson, 1992
; Chamberlin, Horner, and Palmer, 1994
) and Helianthus (Newcomb, 1973
). In each of these cases, the onset of endosperm cellularization occurs at a much more advanced embryo stage than in Platanus where the embryo is in an early filamentous phase when walls begin to form in the chalazal zone (Table 1).
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; Algan and Bakar, 1996
) and Helianthus (Newcomb, 1973
) store protein and oil, like Platanus, Ranunculus, and Papaver, although in some legumes the endosperm does not acquire any storage compounds (Chamberlin, Horner, and Palmer, 1994
). There has been no report of endosperm storage products in Stellaria. Endosperm development patterns vary greatly among this sample of higher eudicots (legumes, Helianthus, Stellaria); and they all differ in many ways from basal eudicots (Table 1).
Finally, we can extend the comparison of free nuclear endosperms to include the group most distantly related to Platanus, i.e., the monocots (Figs. 46, 47). The basal monocot Acorus (Chase et al., 1993
; Duvall et al., 1993a, b
; Nandi, Chase, and Endress, 1998
) is reported to have ab initio cellular endosperm (Buell, 1938
). This, along with parsimonious interpretation of character distribution (Fig. 46), indicates that at some point during the separate radiations of monocot and eudicot clades from magnoliid ancestors, free nuclear endosperms were also derived independently from the ab initio cellular pattern of development in the monocot clade.
Cereal endosperm development has been well studied and characterized (Mares, Norstog, and Stone, 1975
; Morrison and O'Brien, 1976
; Mares et al., 1977
; Fineran, Wild, and Ingerfeld, 1981
; Van Lammeren, 1988
; Engell, 1989
; Bosnes, Weideman, and Olsen, 1992
; Olsen, Potter, and Kalla, 1992
; Brown, Lemmon, and Olsen, 1994,
1996
; Olsen, Brown, and Lemmon, 1995
) and exhibits a unique combination of features (Table 1). Extensive free nuclear development occurs, as in Platanus, but cellularization is completed rapidly after 1 wk rather than 2 mo (Olsen, Brown, and Lemmon, 1995
). Cereals are the only group of the eight compared in Table 1 to store abundant starch in the endosperm. Another unusual feature of cereal endosperm is a regular centripetal cellularization, which is shared only with Ranunculus (XuHan and Van Lammeren, 1993)
among the eight taxa compared. However, unlike Ranunculus, cereal endosperms exhibit differentiation into aleurone and starchy layers that store hydrolytic protein and starch, respectively (Olsen, Potter, and Kalla, 1992
; Olsen, Brown, and Lemmon, 1995
). This pattern is unique among free nuclear taxa. There are some similarities in the endosperm of cereals and several other free nuclear taxa, such as micropylar-to-chalazal cellularization (Johri, Ambegaokar, and Srivastava, 1992
) (present in all taxa except Platanus and Ranunculus) and wall initiation at the globular proembryo phase (shared with legumes and Helianthus) (reviewed in Olsen, Brown, and Lemmon, 1995
).
Comparison of free nuclear endosperm development among taxa also reveals that Platanus endosperm exhibits some features that are unique or at least unusual. These include a distinct chalazal zone that cellularizes first, differential cellularization patterns of the chalazal and micropylar zones, a multinucleate cellular stage in the chalazal zone, chalazal-to-micropylar cellularization, and differentiation into an inner endosperm that is consumed by the embryo and a persistent outer endosperm that is filled with storage products.
When features of development are compared, it is clear that free nuclear endosperms are not all the same. There are differences in almost every aspect of developmental timing, patterning, and structure among the three basal eudicot lineages with free nuclear endosperm (represented by Platanus, Papaver, and Ranunculus). An even greater degree of variability is evident when comparisons with Platanus are extended to include more distantly related, free nuclear taxa in the higher eudicots (represented by legumes, Stellaria, and Helianthus) and monocots (represented by cereals) (Figs. 46, 47; Table 1). These findings are congruent with the hypothesis that free nuclear endosperm has evolved independently within basal eudicots, higher eudicots, and monocots.
The cellular-to-free nuclear transition: developmental perspective
An intriguing feature observed in Platanus was the presence of an incipient cell plate between daughter nuclei derived from the primary endosperm nucleus (Fig. 32). Although interzonal phragmoplasts that fail to form cell plates have been observed during free nuclear mitosis of cereal endosperm (Olsen, Brown, and Lemmon, 1995
), this is the first report of this kind of phenomenon in a more basal angiosperm. Both of these structures are suggestive of an ab initio cellular ancestry for free nuclear endosperm, and this is in turn consistent with the hypothesis that ab initio cellular development is plesiomorphic for angiosperms (Donoghue and Scheiner, 1992
; Friedman, 1992
). The evolutionary transition to a free nuclear condition would have involved a developmental disruption of normal cytokinesis. The point of disruption appears to be different in Platanus and cereals: in Platanus cytokinesis is interrupted at a point after cell plate initiation but before cell wall completion; in cereals cytokinesis is interrupted after phragmoplast formation but before a cell plate is formed. This again is consistent with the hypothesis of independent origins of free nuclear endosperm in these two groups. It would be interesting to know whether vestiges of cytokinesis are evident in taxa, other than Platanus and cereals, with free nuclear endosperm.
Conclusions
Our analysis of embryology in Platanus reveals much more complexity than traditional typological designations suggest, particularly for endosperm. By carefully examining the entire developmental process, we have observed a number of endosperm features that have not been explicitly reported in basal taxa before, such as a transitory cell plate during free nuclear mitosis, chalazal and micropylar zones with distinct modes of cellularization, and unique patterns of cellular differentiation.
The initial stage of endosperm development in Platanus (free nuclear) is completely different from what was previously reported (ab initio cellular). Two other basal angiosperm taxa, Drimys winteri (Johri, Ambegaokar, and Srivastava, 1992
) and Lactoris (Tobe et al., 1993
), have recently been shown to be ab initio cellular in contrast to earlier reports of free nuclear development. This demonstrates the critical need for modern reevaluation of embryological characters for key basal angiosperm taxa. Incorrect data will lead to erroneous conclusions about character evolution and relationship.
Comparison of embryology in Platanus with limited published data for basal Proteaceae indicates possible evolutionary homologies, congruent with the hypothesis of recent shared ancestry and a common origin of free nuclear endosperm development in the clade including Platanaceae and Proteaceae. In contrast, comparison of endosperm developmental characters in Platanus with other free nuclear taxa reveals many significant differences. This is consistent with the hypothesis that free nuclear endosperms have evolved numerous times within angiosperms, including three times during the early radiation of the eudicot clade.
Comparative analysis of endosperm development within the appropriate phylogenetic context has the potential to yield insight into reproductive character evolution, particularly at the base of the eudicot clade where there is considerable variability. However, analyses with the necessary level of detail are mostly restricted to phylogenetically derived groups such as cereals and legumes that are distantly related to each other and to Platanus. Without comparable data sets for other basal taxa, a full exploration of the evolutionary history of the features we have reported is not possible. Future embryological investigations must include additional basal eudicots, basal monocots, and magnoliids in order to permit broad, comparative analyses of these defining angiosperm reproductive characters. The results are likely to reveal important new insights into the early evolutionary radiation of flowering plants.
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FOOTNOTES |
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2
Author for correspondence (floyds{at}colorado.edu
).
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LITERATURE CITED |
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