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(Platanaceae), a Basal Eudicot1 American Journal of Botany 86(11): 1523±1537. 1999. A DEVELOPMENTAL AND EVOLUTIONARY ANALYSIS OF EMBRYOLOGY IN PLATANUS (PLATANACEAE), A BASAL EUDICOT1 SANDRA K. FLOYD,2 VERONICA T. L ERNER, AND WILLIAM E. FRIEDMAN Department of Environmental, Population, and Organismic Biology, Campus Box 334, University of Colorado, Boulder, Colorado 80309 The Platanaceae are an early derived eudicot lineage and therefore occupy a key position for understanding reproductive character diversi®cation associated with the early evolutionary radiation of ¯owering plants. We conducted an embryological study of Platanus racemosa in order to provide critical data on de®ning angiosperm reproductive characters for this important group. Female gametophyte development is monosporic. Embryogenesis occurs in a series of stages including zygote elongation and division, development of a linear proembryo, formation of the embryo proper, histogenesis, organogenesis, and growth. Endosperm development is a complex process that includes four distinct phases: free nuclear proliferation, cellularization of the chalazal zone, centripetal cellularization of the micropylar zone, and cellular differentiation and growth. Only the outer endosperm layer persists at seed maturity. Our ®ndings differ signi®cantly from previously published reports for Platanus, in which endosperm development was described as ab initio cellular. A comparison of endosperm development in Platanus with several closely and distantly related free nuclear taxa reveals considerable developmental variability, consistent with a hypothesis of multiple origins of free nuclear endosperm in angiosperms. Our analysis indicates that much remains to be learned about embryology in basal angiosperms. Additional developmental and comparative studies will likely reveal critical insights into the early evolution of ¯owering plants. Key words: basal angiosperms; developmental evolution; embryology; endosperm development; eudicot; free nuclear endosperm; Platanaceae; Platanus racemosa. Within the last two decades Darwin's ``abominable ing reproductive features of ¯owering plants have re- mystery,'' concerning the origin and early evolutionary mained virtually ignored. history of the angiosperms, has been the focus of much Although there have been a few recent embryological attention. Determining patterns of character distribution studies of basal angiosperms (Tobe et al., 1993; Heo and and evolution in basal angiosperms is critical to under- Tobe, 1995; Rudall and Furness, 1997; Svoma, 1998), standing the origin and diversi®cation of ¯owering plants much of the embryological literature describing these (Doyle and Donoghue, 1993; Friedman, 1994). However, taxa dates to the early part of this century, lacks photo- despite intense interest in the origin of ¯owering plants graphic documentation, and is fraught with inconsisten- as well as the considerable recent efforts of systematists cies and errors. In addition, important features of angio- to address questions of relationship among basal clades sperm reproductive biology, such as endosperm devel- (Donoghue and Doyle, 1989; Hamby and Zimmer, 1992; opment, have been reduced to a handful of typological Chase et al., 1993; Qiu et al., 1993; Doyle, Donoghue, categories that lack any phylogenetic context. Further- and Zimmer, 1994; Nixon et al., 1994; Hoot, MagalloÂn- more, embryological developmental patterns in basal lin- Puebla, and Crane, 1997; Qiu, 1997; Nandi, Chase, and eages have been classi®ed into types that are almost al- Endress, 1998; Soltis et al., 1998; Hoot, MagalloÂn, and ways based on the study of derived taxa. This ``top- Crane, 1999), there has been little comparative analysis down'' approach seriously limits our ability to address of the embryological characters of primitive angiosperms. fundamental questions of the origin and evolution of These include unique features such as a highly reduced these characters. As a result, existing typological schemes female gametophyte, triple fusion, and endosperm. Thus, provide little or no basis for understanding evolutionary the origin and diversi®cation of some of the most de®n- transitions between the types. An explicit goal of this study (and others in progress) is to characterize embryological development patterns in 1 Manuscript received 5 January 1999; revision accepted 16 April basal taxa (a ``bottom-up'' approach) in order to infer 1999. ontogenetic transitions that occurred during the early ra- The authors thank Sharon Swan for collecting and shipping all ¯oral materials used in this study; Dan Dvorkin for assistance with sectioning; diation of angiosperms. Indeed, a developmental and and John Herr and Andrew Douglas for thoughtful suggestions for im- phylogenetically based approach to describing and com- proving the manuscript. This work was funded by grants from the Na- paring reproductive features in primitive ¯owering plants, tional Science Foundation (DEB 9701210, IBN 9696013, BSR without a priori assumptions of typological categoriza- 9158182) and equipment grants-in-aid of research from Apple Com- tion, is essential if we are ever to make progress in solv- puter, Carl Zeiss, Compaq Computer, Fisher Scienti®c, Lasergraphics, Leica Instruments, Olympus America, and Research and Manufacturing ing Darwin's ``abominable mystery.'' Company. Recent phylogenetic analyses (Donoghue and Doyle, 2 Author for correspondence (e-mail: ¯[email protected]). 1989; Hamby and Zimmer, 1992; Chase et al., 1993; Qiu 1523 1524 AMERICAN JOURNAL OF BOTANY [Vol. 86 et al., 1993; Doyle, Donoghue, and Zimmer, 1994; Nixon et al., 1994; Hoot, MagalloÂn-Puebla, and Crane, 1997; Qiu, 1997; Nandi, Chase, and Endress, 1998; Hoot, Ma- galloÂn, and Crane, 1999) provide the following important insights into angiosperm phylogeny that help guide this analysis. Angiosperms are monophyletic. The monosul- cate Magnoliidae (magnoliids) are a nonmonophyletic basal assemblage of angiosperms from which monophy- letic monocot and eudicot clades evolved. The eudicot clade includes 75% of extant ¯owering plant species (Drinnan, Crane, and Hoot, 1994). These phylogenetic ®ndings indicate that in order to understand character evolution during the early radiation of angiosperms we must focus on magnoliids, basal monocots, and basal eu- dicots. Platanus is the single extant genus representing one of the earliest branching eudicot clades, Platanaceae (Huf- ford and Crane, 1989; Schwarzwalder and Dilcher, 1991; Chase et al., 1993; Hoot, MagalloÂn-Puebla, and Crane, 1997; Hoot, MagalloÂn, and Crane, 1999). The platana- ceous 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 diversi®cation during the origin of the largest clade of angiosperms (eudicots) from a magnoliid ances- Figs. 1±4. In¯orescences of Platanus racemosa. 1. Female in¯ores- tor. However, Platanus is also a taxon for which embry- cence with numerous female ¯owers tightly clustered on spherical head. ology is incompletely known (Johri, Ambegaokar, and Scale bar 5 0.5 cm. 2. Male in¯orescence prior to anthesis. Scale bar 5 0.5 cm. 3. Morphologically bisexual in¯orescence with both male Srivastava, 1992) and for which published reports (Brou- ¯owers releasing pollen and female ¯owers. Scale bar 5 0.5 cm. 4. wer, 1924; Guseinova, 1976) are contradictory. We have Higher magni®cation view of a female in¯orescence. A single ¯ower, therefore undertaken an embryological study of P. ra- consisting of nine free carpels and surrounding staminodes, is indicated cemosa in order to provide unequivocal data on de®ning by the arrow. Scale bar 5 0.25 cm. angiosperm reproductive characters. Our goals were (1) to provide an analysis of embryo- cally bisexual ¯owers (Fig. 3). Female ¯owers consist of seven to nine logical development in Platanus that moves beyond the free carpels surrounded by staminodes (Fig. 4) and diminutive sepals. century-old typologies that have dominated the embryo- logical literature; and (2) to explore the evolutionary im- HistologyÐClusters of carpels were cut from in¯orescences and plications of our results. First, we report on the devel- placed into vials containing either 50 mmol/L Pipes buffer (also 5 opment of the female gametophyte (embryo sac), em- mmol/L EGTA and 1 mmol/L MgSO4) at pH 6.8, 100 mmol/L Pipes bryo, and endosperm. We then discuss the new contri- buffer (also 10 mmol/L EGTA and 2 mmol/L MgSO4) at pH 6.8, or a butions of this work and brie¯y compare our results to solution of 3:1 ethanol: acetic acid (3:1 solution). Acrolein or glutar- previous studies of Platanus. Finally, we compare Pla- aldehyde was added to the vials with Pipes buffer to a concentration of tanus embryological development with published data for 4%. Specimens were left in ®xative a minimum of 48 h, then rinsed other basal eudicots and more distantly related angio- and stored in Pipes buffer or 75% ethanol (the 3:1 ®xed specimens) at sperms in order to examine the developmental implica- 48C until needed. tions of the multiple evolutionary origins of free nuclear Fixed ¯owers were dehydrated through an ethanol series to 95% eth- endosperm patterns among ¯owering plants. anol, in®ltrated with monomer A of the JB-4 embedding kit (Polysci- ences, Warrington, Pennsylvania), and embedded in an oxygen-free en- MATERIALS AND METHODS vironment. More than
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