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Transcript
14 Comparative embryology of basal angiosperms William E Friedman Recent phylogenetic analyses of basal angiosperms have identified those lineages central to the study of the origin and early diversification of flowering plants. As we begin to understand the early evolution of endosperm developmental patterns in flowering plants, it is apparent that we know little about the other basic embryological features of basal angiosperms, such as the nature of the female gametophyte and even whether a process of double fertilization occurs. that little work remains to be done on the documentation and discovery of developmental patterns associated with the fertilization process, embryos, and endosperms. Yet, for all of the recent progress in analyzing the phylogenetic relationships of plants and deciphering molecular developmental programs in model systems, much of the organismic diversity of extant plants has yet to be studied, even at the most rudimentary level. Addresses Department of Environmental, Population and Organismic Biology, University of Colorado, Boulder, Colorado 80309, USA; e-mail: [email protected] This review focuses on our current understanding of the comparative embryology of basal angiosperms and examines the impact of recent advances in phylogenetic systematics on the area of early flowering plant evolution. In addition, the import of recent proposals to move beyond century-old typological schemes to a more evolutionary and developmental framework for the description of embryological process will be discussed. Current Opinion in Plant Biology 2001, 4:14–20 1369-5266/01/$ — see front matter © 2001 Elsevier Science Ltd. All rights reserved. Introduction Had Current Opinions in Plant Biology published its fourth volume in 1901 instead of 2001, the focus of a brief review/perspective of the previous few years of research in the area of comparative embryology would have been an enormous undertaking. Just over a century ago, international competition was keen to discover and document fertilization processes, and embryo and endosperm developmental patterns in a wide diversity of plants. In Japan in 1896, motile sperm were discovered in seed plants [1,2]. In Russia (1898) and France (1899), a second fertilization event (double fertilization) that initiates endosperm in flowering plants was reported [3,4]. Within months of the discovery of double fertilization in two species of lily, workers in France, Germany, Japan, Great Britain, and the United States raced to determine whether this phenomenon was a general feature of flowering plants and to interpret its evolutionary significance. The last half of the nineteenth century, as well as the first decade of the twentieth century was truly the golden age of comparative biology, a period dominated by evolutionary and developmental morphologists and anatomists, whose focus was on organisms and the variation inherent among plant life cycles. Of course, volume four of Current Opinions in Plant Biology will be published in 2001 and this review/perspective on the field of comparative embryology will necessarily differ from what might have been written a century ago. We live in a world in which molecular systematics and molecular developmental biology are dominant fields within biological research; where the focus has shifted from the organism and the breadth of organismic diversity to the genome and the more phylogenetically limited study of a small number of ‘model systems.’ The inference might be that, more than 150 years after comparative plant biology emerged as a major discipline, everything about the basic biology and variation in reproductive process in plants is known; and Phylogenetic context for basal angiosperms The importance of understanding the embryological features of early angiosperm lineages cannot be overemphasized because flowering plants are thought to be defined, in many ways, by their reproductive biology. Angiosperms, unlike all (or almost all) other groups of extant seed plants, possess a reduced male gametophyte (of three cells at maturity), a reduced female gametophyte (of seven cells and eight nuclei at maturity), a process of double fertilization, endosperm as an embryo-nourishing tissue, and a cellular pattern of embryogeny. In order to analyze the origin and early evolution of flowering plants, a clear formulation of the phylogenetic interrelationships of basal angiosperms is essential [5••]. With robust phylogenetic hypotheses, evolutionary interpretation of the comparative biological features of angiosperms can be used to infer and reconstruct the diversification of plant reproductive patterns. For over a century, the identification of the earliest lineages of flowering plants was controversial and uncertain. Beginning in 1999, a series of independent analyses yielded a remarkable consensus on the most basal angiosperm lineages. These phylogenetic analyses [6••,7,8,9••,10•,11,12,13••,14,15•,16••] identify three monophyletic groups that comprise a basal (i.e. paraphyletic) grade of angiosperms: Amborella trichopoda, Nymphaeales (Nymphaeaceae plus Cabombaceae), and a clade that includes Illiciaceae, Trimeniaceae, Schisandraceae and Austrobaileyaceae. It is currently unclear whether Amborella, Nymphaeales, or Amborella plus Nymphaeales is the sister group to all other angiosperms (Figure 1). There have been additional recent phylogenetic findings about the major relationships among angiosperms. Although the term ‘dicots’ still (unfortunately) appears in the literature, flowering plants with two cotyledons in the Comparative embryology of basal angiosperms Friedman 15 Figure 1 (a) Amborellaceae (b) Nymphaeaceae (c) Cabombaceae Nymphaeaceae Cabombaceae Nymphaeaceae Cabombaceae Amborellaceae Amborellaceae Illiciaceae Illiciaceae Illiciaceae Schisandraceae Schisandraceae Schisandraceae Trimeniaceae Trimeniaceae Trimeniaceae Austrobaileyaceae Austrobaileyaceae Austrobaileyaceae All other angiosperms including eumagnoliids, eudicots and monocots All other angiosperms including eumagnoliids, eudicots and monocots All other angiosperms including eumagnoliids, eudicots and monocots Current Opinion in Plant Biology Hypothesized relationships of basal angiosperms. Recent phylogenetic analyses indicate that (a) Amborellaceae (Amborella trichopoda), (b) Nymphaeales (Nymphaeaceae plus Cabombaceae), or (c) Amborellaceae plus Nymphaeales is sister to all other angiosperms. All recent phylogenetic analyses conclude that Amborella trichopoda, Nymphaeales and a clade that includes the Illiciaceae, Schisandraceae, Trimeniaceae and Austrobaileyaceae comprise a grade of flowering plants that are basal. embryo clearly comprise a paraphyletic group that is no longer recognized by evolutionary biologists. Most (i.e. 95% of) dicotyledonous flowering plants, however, belong to a major monophyletic group [17], the eudicots (which are identified by the synapomorphy of tricolpate pollen). Another group, the eumagnoliids (comprising the Laurales, Magnoliales, Winterales, and Piperales), may constitute an additional monophyletic lineage of dicotyledonous flowering plants (this finding is currently weakly supported). Phylogenetic analyses of flowering plants continue to demonstrate that monocots are a robust monophyletic group. Currently, the relationships of monocots, eudicots and eumagnoliids are uncertain (Figure 2). there is little evidence (one way or the other) that double fertilization occurs in any of the most basal angiosperm lineages [5••,20••]. All basal angiosperms are known to produce an endosperm, but the question of its developmental origin remains unresolved. It is entirely possible that endosperm in Amborella and other basal angiosperms is developmentally derived from the central cell of the female gametophyte alone, and as such, is a genetically maternal tissue [20••]. Alternatively, a second fertilization event within the central cell of the female gametophyte, as has been definitively documented in derived monocots and eudicots, might initiate the formation of endosperm in Amborella. Only careful investigations of female gametophyte development and the fertilization process in the most basal angiosperms will reveal the developmental origin of endosperm in these taxa. The female gametophyte and double fertilization in basal angiosperms For the first time, we know which groups of plants are central to reconstructing the evolution of patterns of embryology among early angiosperms. The question is, what do we actually know about the nature of embryological features in basal angiosperms? Although Amborella may be the sister group to all other extant angiosperms and, as such, central to the determination of plesiomorphic character states for flowering plants, almost nothing is known of its embryology (see also Update). Embryo and endosperm development of Amborella are entirely unknown. Even the question of whether double fertilization occurs in Amborella has never been examined. Surprisingly, a century after it was ‘concluded’ that double fertilization is a defining feature of all angiosperms (except where it has been lost, as in the Podostemaceae [18,19]), The assumption, now more than a century old, that a seven-celled, eight-nucleate, female gametophyte is a defining feature of flowering plants, which evolved in their common ancestor, may also prove premature. The only recent work on female gametophyte development in the most basal angiosperm lineages involves members of the Nymphaeaceae and Cabombaceae [21–23]. Interestingly, these papers report that the mature female gametophyte in Nymphaea and Cabomba has four nuclei and four cells at maturity: one polar nucleus in a central cell, one egg cell, and two synergids. These findings contradict earlier studies that detected a more typical seven-celled, eight-nucleate female gametophyte in Nymphaeales [24–29]. It is possible that natural variation in female gametophyte structure exists in basal angiosperms, or that some of these studies are incorrect. 16 Growth and development Figure 2 Amborellaceae Cabombaceae Nymphaeaceae Illiciaceae Schisandraceae Trimeniaceae Austrobaileyaceae Ceratophyllum Monocots Winterales Laurales Eumagnoliids Piperales Magnoliales Chloranthaceae Current Opinion in Plant Biology Eudicots Major monophyletic groups of angiosperms. Although recent phylogenetic analyses have identified the earliest divergent lineages of extant angiosperms, there is much uncertainty about the phylogenetic relationships of other relatively basal angiosperm lineages. For example, the phylogenetic placement of monocots and eudicots is poorly resolved at present. The positions of Chloranthaceae and Ceratophyllum remain ambiguous and are highly variable between analyses. There is currently weak support for the monophyly of eumagnoliids, which include Piperales, Winterales, Laurales and Magnoliales. If members of the Nymphaeales do indeed produce a fourcelled female gametophyte, and if Nymphaeales should be resolved as sister to all other angiosperms, then a fourcelled, four-nucleate female gametophyte could be plesiomorphic for flowering plants. The implications of such a finding would be that a seven-celled, eight-nucleate female gametophyte might be derived (apomorphic) among angiosperms. Moreover, endosperm might be diploid in its plesiomorphic state (assuming that it actually arises from a second fertilization event [see above]) or even haploid, if it could be shown that no second fertilization event occurred! Although these evolutionary developmental scenarios may appear to be highly speculative, the fact is that we currently lack sufficient information about the reproductive biology of basal angiosperms to be confident about what constitutes a plesiomorphic condition and whether certain characters, long believed to be synapomorphies of flowering plants, are indeed so. Endosperm development and evolution in basal angiosperms Recently, there has been a concerted effort to study the developmental patterns expressed by endosperms in basal angiosperms [30••,31••]. The goals of these studies have been twofold: to determine the plesiomorphic pattern of endosperm development in flowering plants and to examine the evolutionary diversification of endosperm development among early divergent lineages. Flowering plant endosperm has long been characterized into three basic developmental patterns: free nuclear, (ab initio) cellular, and helobial. Free nuclear endosperm development always begins with a syncytial phase (i.e. mitosis without cytokinesis), which is usually followed by a process of cellularization (i.e. cytokinesis without mitosis) and additional cellular growth (i.e. mitosis coupled with cytokinesis). Cellular endosperm development is characterized by the coupling of cytokinesis with mitosis from the very first division of the endosperm. In helobial endosperm, the first division of the primary endosperm nucleus is immediately followed by a cell division to yield a two-celled endosperm. Syncytial development then occurs in one or both of these cellular compartments (and may later be followed by a process of cellularization). Although free nuclear endosperm has long been known to be the most common ‘type’ among flowering plants, this pattern of endosperm development does not occur among the most basal angiosperms. Rather, cellular patterns of endosperm development are prevalent among basal angiosperms and parsimonious character optimization onto the most recent angiosperm phylogenies indicates that cellular endosperm development is likely to be plesiomorphic among flowering plants [31••]. It is clear that both helobial and free nuclear endosperms have originated many times over the course of flowering plant evolution [31••]. It is unclear whether cellular endosperm development has ever evolved from a free nuclear or helobial pattern. Interestingly, helobial endosperm development, a pattern common among monocots, also evolved within the Nymphaeales in the common ancestor of the Cabombaceae [31••]. Although free nuclear endosperm is not present in any of the most basal angiosperms, free nuclear development is found in several basal monocots [32] (however, most of these reports are extremely old and could be erroneous descriptions of helobial development), eudicots [30••] and some members of the eumagnoliids (specifically, derived Lauraceae [33]). Free nuclear endosperms of basal eudicots have recently been studied in Platanus [30••], Papaver [34,35] and Ranunculus [36–38]. When analyzed within a phylogenetic context, free nuclear endosperm development has likely evolved at least four separate times within the eudicots [30••], perhaps several times within the monocots, and once within the Lauraceae [33]. An important point is that the free nuclear endosperms of model system taxa such as Arabidopsis (a eudicot) and Zea (a monocot) clearly represent derived developmental patterns among angiosperms; thus they are homoplasious (i.e. have evolved separately) with respect to each other, as well as to the free nuclear endosperms of various basal eudicots. Comparative embryology of basal angiosperms Friedman Recently, both Olsen et al. [39] and Brown et al. [40] have called attention to the high degree of overall similarity, at the cell biological level, of the processes of free nuclear development and centripetal cellularization in the endosperms of Arabidopsis and grasses such as Zea. Moreover, both groups of workers have suggested that the development of free nuclear endosperms in these highly derived angiosperms is at least superficially similar to the free nuclear and centripetal cellularization patterns expressed by the female gametophytes of nonflowering seed plants. Clearly, the free nuclear and centripetal cellularization patterns of development found in the endosperms of highly nested eudicots (e.g. Arabidopsis), basal eudicots (e.g. Platanus and Ranunculus) and monocots (e.g. Zea), and the female gametophytes of most nonflowering seed plants [41] are all strictly homoplasious. Given this important evolutionary context, it is intriguing to imagine that ancient developmental programs for syncytial growth and subsequent cellularization might have been recruited each time a free nuclear pattern of endosperm evolved from a cellular (or helobial) ancestral pattern. Alternatively, specific patterns of cell biological development and gene expression associated with the free nuclear phase and the process of cellularization in these diverse syncytial systems might be expected to differ. For example, the developmental origin of anticlinal walls in free nuclear endosperms has long been controversial [42,43•], with various workers describing cytoskeleton and cellplate patterns during the initial cellularization of the syncytial stage that appear to differ among taxa. An evolutionary perspective that has not been explicitly considered by cell and molecular developmental biologists is that some of the reported pattern-level differences may be real and indeed reflect the independent evolution of syncytial endosperm in diverse angiosperm lineages. It is essential to remember that although the cellular endosperms of flowering plants may all be homologous (at the level of developmental pattern), free nuclear endosperms are not, from an evolutionary perspective, all one ‘thing’ (the same is true of helobial endosperms). It would be most useful if future cellular and molecular studies of free nuclear endosperms explicitly compared the endosperms of groups that have independently acquired this pattern of development. The bipolar nature of endosperm A recent study of a broad selection of basal angiosperms reveals an important underlying developmental commonality that is expressed during endosperm development [31••]. Endosperms of basal angiosperms, whether cellular, free nuclear, or helobial, are distinctly bipolar and express independent patterns of development in what have been termed the ‘chalazal domain’ and the ‘micropylar domain’ [31••]. Even when the entire endosperm is initially free nuclear, as in Platanus (a basal eudicot), the cytological 17 organization of endosperm in the chalazal domain (which is densely cytoplasmic with no large vacuoles) has been reported to be radically different from that in the micropylar domain (where a parietal band of cytoplasm surrounds a large central vacuole). Moreover, the process of cellularization in each domain in Platanus is temporally separate and cell biologically distinct. Cell walls are formed simultaneously throughout the chalazal domain, but centripetally in the micropylar domain [20••]. It is interesting to note that in Arabidopsis, a densely cytoplasmic free nuclear chalazal region forms, and at the time when the rest of the endosperm cellularizes this chalazal cytoplasm remains free nuclear [40,43•,44,45,46••]. Other highly derived free nuclear taxa in which chalazal endosperm development differs from that of the rest of the tissue include Zea, Glycine, and Helianthus [47–51]. As might be expected, differential patterns of gene expression in the micropylar and chalazal regions in Arabidopsis [45] and Zea [52–55] have recently been documented. Unfortunately, little, if anything, is known of gene expression in endosperms of basal angiosperms or any angiosperms with either a cellular or a helobial pattern of endosperm development. Among basal angiosperms with helobial endosperms, the chalazal domain and the micropylar domain are defined by the first cell division, which yields a two-celled endosperm. The micropylar domain initiates a free nuclear pattern of development. The chalazal domain may, however, undergo free nuclear development, cellular development, or no further nuclear or cellular proliferation at all [31••]. Thus, the bipolar nature and independence of developmental fate between micropylar and chalazal domains has produced at least three basic patterns among basal angiosperms with helobial endosperms [31••,56]. Among angiosperms with a cellular pattern of endosperm development, the chalazal and micropylar domains are not always defined or tightly correlated with the first cell division. Rather, a chalazal region with limited cell proliferation and a micropylar region with more extensive cell proliferation emerge during the early development of the endosperm [31••]. Clearly, the developmental independence of micropylar and chalazal domains among basal angiosperms may be general to all angiosperm endosperms. A most intriguing aspect of the underlying bipolar nature of endosperm, whether free nuclear, cellular or helobial, is that this pattern is strongly reminiscent of the morphogenetic principles that govern the organization of flowering plant embryos [5••,20••,31••] (principles of embryo development have been recently reviewed [57]). Both embryos and endosperms (at least plesiomorphic endosperms) undergo an initial, unequal partitioning of the first cell, and this is followed by differential patterns of development at the two poles. Indeed, some of the recently published [31••] and yet to be published (SK Floyd, personal 18 Growth and development communication) micrographs of basal angiosperm endosperms are remarkably embryo-like. Kranz et al. [51,58] have also called attention to the highly embryo-like organization of in-vitro-formed endosperms of Zea, in which one pole is globular with smaller cells and the other pole is roughly filamentous with larger cells, much like a suspensor. The embryo-like nature of endosperms among basal angiosperms may have important implications for the analysis of the evolutionary homology of endosperm. For over a century, a debate has focused on whether endosperm represents a highly modified supernumerary embryo or a sexualized modification of a component of female gametophyte development [20••,59,60]. Although many basal angiosperm endosperms (and even some derived angiosperm endosperms, such as in vitro Zea) are embryo-like, comparative information on the underlying molecular programs of endosperm and embryos among basal angiosperms will be critical to the evaluation of these alternative hypotheses. One final caveat relating to endosperm development among basal angiosperms: although many basal angiosperms have been categorized into one of the three basic endosperm typologies (i.e. cellular, free nuclear, or helobial), it is probable that a significant number of these reports contain serious errors. For example, several recent studies of endosperm development in basal angiosperms show that previous reports were incorrect: Lactoris and Drimys (both magnoliids) were originally reported to be free nuclear, but are, in fact, cellular [61,62]; Platanus (a basal eudicot) was originally reported to be cellular, but is, in fact, free nuclear [30••]; and Mahonia (a basal eudicot) was reported to be free nuclear, but is definitely cellular (SK Floyd, WE Friedman, unpublished data). In many other basal angiosperm taxa, conflicting reports of endosperm developmental patterns remain unresolved [30••]. Conclusions In just the past year alone, more papers have appeared on the molecular phylogenetics of basal angiosperms than on the actual biology of basal angiosperms. In the past three years, more review articles have appeared on the molecular genetics of female gametophytes, embryos and endosperms of ‘model system’ flowering plants than primary papers on these basic life-cycle components in all of the basal angiosperms. These comments are not intended as a slight of the recent advances of molecular systematics and model system molecular developmental biology. The remarkable and important advances in these disciplines have fundamentally recast the nature of inquiry in modern biology. Rather, as Endress [63] and others have argued recently, what is needed is a balance between the molecular sciences and the organismic sciences. If we are to ultimately gain deeper insights into the origin and evolution of flowering plants from both phylogenetic and molecular developmental perspectives, documentation of the still largely unknown organismic diversity of structure and pattern in these critical organisms will be essential. Update Recently, research on the embryology of Amborella was published by Tobe et al. [64]. For the first time, data are presented that describe diverse reproductive features including anther anatomy, ovule anatomy and morphology, female gametophyte development (eight-nucleate, sevencelled) and endosperm development (cellular). No data were presented that bears on the question of whether a second fertilization event initiates endosperm in Amborella, and thus, this remains a question that is open for investigation. Tobe et al. also analyzed embryological character distribution within basal angiosperms in order to suggest the nature of plesiomorphic reproductive character states for angiosperms as a whole. Acknowledgements I thank Sandra Floyd for helpful discussions about the evolution of embryological features of basal angiosperms; Joe Williams and Pam Diggle for helpful comments for the improvement of the manuscript; and the National Science Foundation (USA) for support of my research. References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: • of special interest •• of outstanding interest 1. Hirase S: On the spermatozoid of Ginkgo biloba. Bot Mag Tokyo 1896, 10:325-328. 2. Ikeno MS: Spermatozoid of Cycas revoluta. Bot Mag Tokyo 1896, 10:367-368. 3. Nawaschin SG: Resultate einer Revision der Befruchtungsvorgange bei Lilium martagon und Fritillaria tenella. Bull Acad Sci St Petersburg 1898, 9:377-382. [Title translation: Results of a revision of the fertilization process in the Lilium martagon and Fritillaria tenella.] 4. Guignard L: Sur les antherozoides et la double copulation sexuelle chez les vegetaux angiosperms. Comptes Rendues Acad Sci, Paris 1899, 128:864-871. [Title translation: On the sperm and sexual double fertilization in flowering plants.] 5. •• Friedman WE, Floyd SK: The origin of flowering plants and their reproductive biology: a tale of two phylogenies. Evolution 2001, in press. This paper deals explicitly with the character evolution implications of the new angiosperm and seed plant phylogenetic hypotheses. The focus is on issues associated with the origin of double fertilization and the evolutionary homology of endosperm. 6. •• Mathews S, Donoghue MJ: The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 1999, 286:947-950. One of the first papers to identify Amborella, Nymphaeales and Illiciales as the most basal angiosperms. 7. Mathews S, Donoghue MJ: Basal angiosperm phylogeny inferred from duplicate phytochromes A and C. Int J Plant Sci 2000, 161:in press. 8. Qiu Y-L, Lee J, Bernasconi-Quadroni R, Soltis DR, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW: The earliest angiosperms: evidence from mitochondrial, plastid, and nuclear genomes. Nature 1999, 402:404-407. 9. •• Qiu Y-L, Lee J, Bernasconi-Quadroni R, Soltis DR, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW: Phylogeny of basal angiosperms: analyses of five genes from three genomes. Int J Plant Sci 2000, 161(suppl):3-27. A thorough analysis of basal angiosperm phylogeny that was published in a special issue of the International Journal of Plant Sciences on basal Comparative embryology of basal angiosperms Friedman angiosperms. The authors conclude that Amborella, Nymphaeales and a clade that includes the Illiciales comprise a basal grade of angiosperms. 10. Soltis PS, Soltis DE, Chase MW: Angiosperm phylogeny inferred • from multiple genes as a research tool for comparative biology. Nature 1999, 402:402-404. One of the first papers to identify Amborella, Nymphaeales and Illiciales as the most basal grade of angiosperms on the basis of gene sequence. 11. Soltis PS, Soltis DE, Zanis MJ, Kim S: Basal lineages of angiosperms: relationships and implications for floral evolution. Int J Plant Sci 2000, 161(suppl):97-107. 12. Parkinson CL, Adams KL, Palmer JD: Multigene analyses identify the three earliest lineages of extant flowering plants. Curr Biol 1999, 9:1485-1488. 13. Graham SW, Reeves PA, Burns ACE, Olmstead RG: Microstructural •• changes in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference. Int J Plant Sci 2000, 161(suppl):83-96. This phylogenetic analysis finds support for the Nymphaeales as sister to all other angiosperms on the basis of an indel. 14. Graham SW, Olmstead RG: Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. Am J Botany 2001, 87:1712-1730. 15. Doyle JA, Endress PK: Morphological phylogenetic analysis of • basal angiosperms: comparison and combination with molecular data. Int J Plant Sci 2000, 161(suppl):121-153. A comparative examination of molecular data and morphological data relating to the phylogenetic relationships of basal angiosperms, and more importantly, to several aspects of character evolution among early angiosperm lineages. 27. Cook MT: Development of the embryo sac and embryos of Castalia odorata, Nymphaea advena. Bull Torrey Bot Club 1902, 29:211-220. 28. Cook MT: The embryogeny of some Cuban Nymphaeaceae. Bot Gaz 1906, 42:376-392. 29. Ramji MN, Padmanabhan DP: Developmental studies on Cabomba caroliniana Gray. I. Ovule and carpel. Proc Indian Acad Sci 1965, 62:215-223. 30. Floyd SK, Lerner VT, Friedman WE: A developmental and •• evolutionary analysis of embryology in Platanus (Platanaceae), a basal eudicot. Am J Botany 1999, 86:1523-1537. The free nuclear endosperm of Platanus, a basal eudicot, is examined from a developmental perspective. For the first time, the homoplasious nature of free nuclear endosperms among flowering plants is analyzed within a comparative and phylogenetic context. 31. Floyd SK, Friedman WE: Evolution of endosperm developmental •• patterns among basal flowering plants. Int J Plant Sci 2000, 161(suppl):57-81. A comparative study of endosperm development in 13 basal angiosperms. The plesiomorphic features of endosperm development in flowering plants are analyzed. 32. Johri BM, Ambegaokar KB, Srivastava PS: Comparative Embryology of Angiosperms. Berlin: Springer-Verlag; 1992. 33. Heo K, van der Werff H, Tobe H: Embryology and relationships of Lauraceae (Laurales). Bot J Linn Soc 1998, 126:295-322. 34. Olson AR: Embryo and endosperm development in ovules of Papaver nudicaule after in vitro placental fertilization. Can J Bot 1981, 59:1738-1748. 16. Barkman TJ, Chenery G, McNeal JR, Lyons-Weiler J, dePamphilis CW: •• Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. Proc Natl Acad Sci USA 2001, in press. A phylogenetic analysis that suggests that Amborella is sister to Nymphaeales and that this clade is sister to all other angiosperms. 35. Bhandari NN, Bhargava M, Chitralekha P: Cellularization of freenuclear endosperm of Papaver somniferum L. Phytomorphology 1986, 36:357-366. 17. 37. Doyle JA, Hotton CL: Diversification of early angiosperm pollen in a cladistic context. In Pollen and Spores: Patterns of Diversification. Edited by Blackmore S, Barnes SH. Oxford: Clarendon Press; 1991:169-195. 19 36. Chitralekha P, Bhandari NN: Cellularization of free-nuclear endosperm in Ranunculus sceleratus Linn. Phytomorphology 1993, 43:165-183. 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