Contribution to the Knowledge of the Floral Structure in Sabal palmetto (Walter) Lodd. Ex Schult. (Arecaceae: Coryphoideae)
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1 Article Contribution to the Knowledge of the Floral Structure in Sabal palmetto (Walter) Lodd. Ex Schult. (Arecaceae: Coryphoideae) CASTAÑO, F., CRÈVECOEUR, Michèle, STAUFFER, F.W. Abstract The floral structure of the neotropical palm Sabal palmetto is described. The species is characterized by the presence of hermaphrodite solitary flowers; congenitally united imbricate sepals and free imbricate petals. The six stamens are fertile, with filaments congenitally united towards the base. Contrary to previous reports indicating complete syncarpy, the three carpels are free in the basal region and postgenitally fused above the level of the septal nectary; they are ascidiate throughout the ovary and plicate from the style base up to the stigma. Our study supports the close relationships between Sabaleae and the rest of Cryosophileae. Reference CASTAÑO, F., CRÈVECOEUR, Michèle, STAUFFER, F.W. Contribution to the Knowledge of the Floral Structure in Sabal palmetto (Walter) Lodd. Ex Schult. (Arecaceae: Coryphoideae). Phytomorphology, 2009, vol. 59, no. 3/4, p Available at: Disclaimer: layout of this document may differ from the published version. [ Downloaded 06/05/2011 at 15:12:43 ]
2 F. Phytomorphology CASTANO et al. 59(3 Floral & 4) Anatomy 2009, in Sabal palmetto 85 Contribution to the Knowledge of the Floral Structure in Sabal palmetto (Walter) Lodd. Ex Schult. (Arecaceae: Coryphoideae) F. Castaño 1,2, M. Crèvecoeur 2 and F.W. Stauffer 1 1 Conservatoire et Jardin botaniques de la Ville de Genève. Université de Genève, Laboratoire de Systématique Végétale et Biodiversité, Chemin de l Impératrice 1, Case Postale 60, 1292 Chambésy-Genève, Switzerland 2 Département de Botanique et de Biologie végétale, Sciences III, Université de Genève. Quai Ernest-Ansermet 30, 1211 Genève 4, Switzerland ABSTRACT The floral structure of the neotropical palm Sabal palmetto is described. The species is characterized by the presence of hermaphrodite solitary flowers; congenitally united imbricate sepals and free imbricate petals. The six stamens are fertile, with filaments congenitally united towards the base. Contrary to previous reports indicating complete syncarpy, the three carpels are free in the basal region and postgenitally fused above the level of the septal nectary; they are ascidiate throughout the ovary and plicate from the style base up to the stigma. Our study supports the close relationships between Sabaleae and the rest of Cryosophileae. Key words: Anatomy, flowers, morphology, sabaleae Author for Correspondence: F.W. Stauffer, fred.stauffer@ville-ge.ch Introduction The palm family (Arecaceae) consists of approximately 252 genera and 2500 species, confined almost exclusively to the tropics (Dransfield et al., 2008). The family displays a huge morphological diversity and its monophyly has been supported by several molecular studies (Chase et al., 1995, 2000; Asmussen & Chase, 2001; Asmussen et al., 2006). The genus Sabal belongs to the subfamily Coryphoideae and is one of the most common palm genera in the Caribbean region and adjacent areas, with about sixteen species (Zona, 1990; Quero, 1991). It was traditionally placed as the sole member of tribe Corypheae, subtribe Sabalinae (Uhl& Dransfield, 1987). The members included in Corypheae are of special importance for palm systematics because their simple floral morphology, providing a microcosm of the structural diversity observed elsewhere in the family (Dransfield & Uhl, 1998). Based on the nature of the gynoecium, particularly on the degree of fusion of the carpels, the tribe Corypheae was first divided in four subtribes: Thrinacinae, Livistoninae, Coryphinae and Sabalinae (Dransfield et al., 1990). The monogeneric subtribe Sabalinae was characterized by the presence of three entirely united carpels, whereas carpels were reported as free or connate in different ways in the other subtribes. In cladistic analysis based on morphological and molecular datasets (Uhl et al., 1990; Uhl et al., 1995; Asmussen et al., 2000; Asmussen & Chase, 2001), Sabalinae was resolved as sister to a clade consisting of all the neotropical apocarpous genera included in the subtribe Thrinacinae. Moreover, the most recent molecular phylogenetic analysis of the family (Asmussen et al., 2006) pointed out that Sabal forms a highly supported clade with the New World genera of Thrinacinae (Chelyocarpus, Coccothrinax, Cryosophila, Itaya, Schippia, Thrinax, Trithrinax and Zombia). Asmussen also provided the basis to the currently accepted classification of the palm family (i. e. Dransfield et al., 2005, 2008). In this new classification, Sabal is included as the sole member within the tribe Sabaleae and the New World genera of Thrinacinae represent the tribe Cryosophileae, which has also been found monophyletic in previous studies (i. e. Uhl et al., 1995; Baker et al., 1999; Asmussen & Chase, 2001; Hahn, 2002). Sabal palmetto (Walter) Lodd. ex Schult. is an emergent palm (ca. 20 m tall) widespread in the Bahamas, Cuba and the south eastern United States (Florida, Georgia, North Carolina and South Carolina). It has been found in coastal dunes and tidal flats to river banks and seasonally inundated savannas, often in disturbed
3 86 PHYTOMORPHOLOGY July-December 2009 vegetation, near sea level (Henderson et al., 1995; Zona, 1990). Most studies on the reproductive structures of Sabal have been superficial and the number of species relatively scant (i. e. Brown, 1976a, 1976b, 1982; Reddy & Kulkarni,1982; Zona & Judd, 1986). Hence, our current knowledge of the floral morphology and anatomy in Sabal is almost entirely based on the studies of Morrow (1965), who investigated three species: S. mexicana, S. minor and S. palmetto, and Uhl and Moore (1971), who briefly described the gynoecium in S. mexicana. According to previous studies and the more recent description of the world palm genera (Dransfield et al., 2008), the genus Sabal is primarily characterized by the presence of a trimerous tubular perianth, six fused stamens and three completely connate carpels. The aims of the present study are to: 1) contribute to the better knowledge of the floral structure in Sabal palmetto, critical for the understanding of the evolution of the gynoecium in the Coryphoid palm flower, and 2) explore the floral characters that could support the sister relationship between tribes Sabaleae and Cryosophileae. Material and methods The morphological and anatomical study was based on liquid-fixed and fresh flowers. Samples from living inflorescences of Sabal palmetto (Walter) Lodd. ex Schult. were collected from the greenhouses of the Conservatory and Botanical Garden of Geneva in November 2007 (Castaño and Stauffer 788-G). Additionally, flowers were obtained from the spirit collection of the Royal Botanic Gardens, Kew (Zona A). Observations on this palm were carried out during a visit to the Fairchild Tropical Botanic Garden (FTG) and the Montgomery Botanical Center (MBC), between October and November Flowers for morphological study were dissected under a stereomicroscope (Wild M3B). Some parts of the dissected specimens were chosen for scanning electron microscopy. They were dehydrated, criticalpoint-dried and sputter-coated with gold. Micrographs were obtained using a Zeiss DSM 940A Scanning electron microscope (Orion 6.60 Imaging System). For the anatomical investigations, flowers at or close to anthesis were chosen and fixed with standard FAA. Sepals and petals removed from some flowers were investigated in order to facilitate the observation and infiltration of the inner organs. The flowers were then dehydrated and embedded in the resin of Technovit 7100 [2-hidroxyethyl methacrylate (HEMA)] (Heraus Kulzer Gmbh) and sectioning was carried out using a rotary microtome (Leitz 1512) at 5-10 μm thickness. Further details on this technique are explained in Igersheim and Cichocki (1996) and Stauffer et al. (2002). The sections were stained with toluidine blue and red ruthenium and mounted in Assistent-Histokitt mounting medium. Flowers were sectioned from the base towards the apex. Therefore, consecutive levels in the sections refer to an acropetal sequence in the flowers. Photos of the anatomical sections were obtained, using a microscope Leica DMIRE2 and a camera Leica DC 300F. The collections and the permanent slides of the microtome sections are deposited at the Laboratory of Micromorphology of the Conservatory and Botanical Garden of Geneva. Results Inflorescence The inflorescence is interfoliar, arcuate, cm long, with 3 branching orders; peduncle up to 30 cm long, 1.5 cm diameter, dorsiventrally compressed and glabrous; the prophyll is 20 cm long, slightly striate, glabrous and tubular; the peduncular bracts were not seen. The rachis is cm long, dorsiventrally compressed, glabrous; rachis bracts papyraceous, 3-4 cm long, cm wide, tubular; rachillae 15-17, progressively shorter towards the distal part of the rachis, inserted at approximately 45-90, 5-25 cm long, glabrous, sterile portion cm long; subtended by a bicarinate bract of 3-4 cm long. Flower morphology and anatomy The flowers are mm long, hermaphrodite and sessile (Fig. 1A). They are solitary and spirally arranged on the rachillae (Fig. 1D). Each flower is subtended by two short bracts, which are lanceolate, acute and directly adnate to the rachilla (Fig. 1A, D). The calyx is formed by three imbricate sepals, which are congenitally united from the base up to 2/3 their length, and forming a 2 mm long shallow cup. The three free sepal lobes are acute and slightly crenate in the margins (Fig. 1A, E). The corolla is formed by 3 petals, which are imbricate, 6-7 mm long, oblong, concave, with the margin involute, the apex obtuse and the adaxial face papillose (Fig. 1F); they are basally adnate to the androecium (Fig. 2A). Stamens 6, 4-5 mm long, all fertile and attached at the same level, slightly reflexed and spread at anthesis (Fig. 1A, G). Three of them are antesepalous and three
4 F. CASTANO et al. Floral Anatomy in Sabal palmetto 87 antepetalous (Fig. 1B). The filaments are congenitally united, forming a shallow tube up to ½ their length (Fig. 1G); the latter is slightly adnate to the gynoecium at the base. The connectives are short and fragile. Anthers are exerted, versatile, sagittate, mm long, dorsifixed (Fig. 1A, G). Their dehiscence is extrorse and longicidal (Fig. 1B). The gynoecium is formed by 3 carpels of mm in length (Fig. 1H, 2C). Carpels are ascidiate towards the ovary and plicate from the base of the style up to the stigmatic branches. The gynoecium is characterized by the presence of three regions: the first, towards the base, is almost completely apocarpic (Fig. 2A); the second, located between the septal nectary and the base of the style is synascidiated (Fig. 2C); the third, towards the distal portion, where the carpels are postgenitally fused throughout their flanks, is synplicate (Fig. 2E, F). All the carpels have an ovary region slightly broader than the elongated style (Fig. 1H). At anthesis, all of them become receptive. The styles are postgenitally fused and their ventral slits are confluent from the stigma downwards to the ovary region. The stigma is trilobed, capitate and conspicuously papillose (Fig. 1C); it appears to be of the wet type (following terminology of Heslop- Harrison and Shivanna, 1977). All three lobes are short, reflexed and equally developed. The papillae covering the branches are 1-3 celled, projected in all directions. The compitum, where the large and folded inner surfaces of the three carpels are confluent, differentiates from the base of the style and extends up to the stigmatic region. Despite its large inner surface, a small lumen is formed (Fig. 2F). The pollen tube transmitting tract (PTTT) separates downwards in three branches, one for each locule (Fig. 2E). It reaches the ovule by surrounding the funiculus throughout the continuous papillate epidermis (Fig. 2C). A septal nectary is present in the mid-region of the three carpels; it differentiates as a triradiate cavity formed by three confluent carpel flanks, specifically located between the base and mid-length of the ovary. An epithelium is formed by elongate cells of the columnar type. Other kind of non-secretory cells, mostly isodiametric, form the nectarial conducts that lead to the openings and are located near mid-length of the ovary (Fig. 2B). The ovule is anatropous, bitegmic and crassinucellate; it is basally attached towards the ventral side of the locule (Fig. 2C, D) and does not fill the entire locule. The ventral walls of the locule are covered with numerous papillae, which connect directly with those of the ventral slits forming the PTTT. Towards the micropyle the outer and the inner integuments are 7 and 4 cell layers thick, respectively. At mid-length of the ovule, the thickness of the integuments remains constant. The nucellus is 2-3 cell layers thick and the micropyle is straight and narrow (Fig. 2D). The short floral base consists of two regions: one external, formed by large parenchymatic cells with thin walls, and another internal composed by short cells, the basal vasculature, some tannin idioblasts and a high density of raphides. The vascular supply consists of one ring in the middle, and a second ring in the transition between the two regions above mentioned. The first ring consists of 9 vascular bundles, that will serve the gynoecium and the androecium, whereas the second consists of vascular bundles that will supply the perianth organs. There are 3 vascular bundles at the base of each petal. Upwards, there are 4-5 vascular bundles and 1-2 procambial strands. Each stamen has one vascular bundle, which could be observed from the base of the filaments up to the connective. Each carpel has 3 ventral and 2-3 dorsal vascular bundles. At mid-length of the ovary, each carpel has one dorsal and two lateral vascular bundles. Vascular bundles could not be observed in the ovule. Each style has one dorsal vascular bundle and two lateral bundles that reach the basal stigmatic region. Raphide idioblasts are present in large amounts in all floral organs, except of the stigma and the ovule. In the perianth, they are present throughout the sepals, whereas restricted to the base in the petals. Raphides are also frequent throughout the staminal tube, the free portion of the filaments (Fig. 2F), the endothecium and the tapetum. In the gynoecium, they were dispersed at the base of the carpels, the ovary walls and throughout the style (Fig. 2A, D, F). Tannins were mostly present towards the apex of the sepals, where they almost completely fill the mesophyll. A few tannins idioblasts were observed in the apical part of the filaments and the connective. In the style tannins are restricted to the transitional zone with the stigma, where they form a continuous layer towards the epidermis. Tannin idioblasts concentrate towards the periphery of the 3 stigmatic lobes. Towards the chalaza, some tannins idioblasts form a 2-3-celled layer (Fig. 2D); they were also scattered in the funicle. Discussion Regarding the general morphology of the flower, there is relative concordance between our results and previous studies (i.e. Morrow, 1965; Uhl & Moore, 1971). However, our findings differ from the published reports especially with respect to the gynoecium structure. In spite of the deep implications for modern taxonomy of Coryphoid palms, the degree of fusion of the carpels
5 88 PHYTOMORPHOLOGY July-December 2009 Figure 1. General morphology of the rachillae and the flower in Sabal palmetto. A. Flower at anthesis (lateral view), arrow pointing to the stigmas, scale bar= 1 mm; B. Flower at anthesis (upper view), scale bar= 1 mm; C. Stigma, arrow pointing to the densely papillate stigmas, scale bar= 120 μm; D. Portion of rachillae (lateral view), scale bar= 2 mm; E. Calyx, scale bar= 1 mm; F. Isolated petal, scale bar= 1 mm; G. Flower without perianth (lateral view), scale bar= 1 mm; H. Gynoecium (lateral view), scale bar= 1 mm.
6 F. CASTANO et al. Floral Anatomy in Sabal palmetto 89 Figure 2. Anatomy of the flower in Sabal palmetto. A. Transverse section of the flower showing the septal nectary (basal level of the ovary, calyx removed), scale bar= 400 μm; B. Detail of the septal nectary, arrow pointing to the epithelium, scale bar= 100 μm; C. Transverse section of the flower showing a completely syncarpous gynoecium (upper level of the ovary), scale bar= 400 μm; D. Detail of the ovule in longitudinal section, arrow pointing to the micropyle region (remaining of the funicle also shown), scale bar= 100 μm. E. Detail of the style and the compitum in transverse section, arrow pointing to a raphide containing idioblast, scale bar= 100 μm; F. Transverse section of the flower (level of the style, calyx removed), scale bar= 200 μm.
7 90 PHYTOMORPHOLOGY July-December 2009 (apocarpy vs. syncarpy) has been for a long time poorly understood. The case of the genus Sabal is an example in which we have found interesting features related to this aspect. According to our study, the three carpels in the gynoecium of Sabal palmetto are not completely connate. They are free in the basal region and then fused above the level of the septal nectary. Our observations are neither congruent with those presented by Morrow (1965), nor with those of Dransfield et al. (2008), who pointed out the presence of three carpels united throughout their length. Morrow (1965) stressed the fact that the carpels appeared partially free due to the occurrence of septal nectaries. Meanwhile, Uhl and Moore (1971) described the three carpels as completely connate except from the nectary region. Although, Morrow (1965) analyzed material of three different species, he considered his report as inadequate to characterize the genus. He found considerable variation in features such as the degree of connation of the carpels and closure of the gynoecium, the occurrence of raphides in the gynoecium and the development of the septal nectaries. Such variation was attributed by him to the different species studied and to the difference in the physiological age within the same species. According to Stauffer et al., 2009, the postgenital union of the carpels from the top of the ovaries up to the stigmas in Licuala peltata (Coryphoideae: Trachycarpeae: Livistoninae) and the recent observations of postgenital apical union in the carpels of Rhapis (Coryphoideae: Trachycarpeae: Rhapidinae, Giddey et al., (2009), could suggest that the carpel fusion in the tribe may be a liable character and therefore, represented by transitional character states. Regarding the structure of the ovule, it was described as campylotropous by Uhl and Moore (1971), but it is anatropous according to the studies of Morrow (1965), Uhl and Dransfield (1987), and the present contribution. The presence of a funicular aril was reported by Uhl and Moore (1971) and Morrow (1965), but this could not be confirmed by our results. Relationships between sabaleae and cryosophileae The clade, consisting of members of the recently described tribe Cryosophileae, with the genus Sabal as sister group, has been resolved and highly supported in different morphological and molecular phylogenetic studies (Uhl et al., 1995; Asmussen et al., 2000, 2006; Asmussen & Chase, The close relationship between Sabal and Cryosophileae is supported in our study by the presence of the following group of shared characters: hermaphrodite flowers, fused floral organs and basally ascidiate carpels. Acknowledgements We would like to thank Dr. R. Spichiger for permanent support to this investigation. FC is grateful to the Swiss Confederation Scholarship and the Hans Wilsdorf Foundation for financial support. Thanks go to Dr. Pierre-André Loizeau and Dr. Daniel Jeanmonod (Conservatoire et Jardin Botaniques de la Ville de Genève) for continuous support to this study and Dr. André Piuz (Muséum d Histoire Naturelle, Genève) for the SEM work. The Augustin Lombard foundation grant from the Geneva SPHN Society and the Swiss Academy of Sciences kindly granted field work of FC. Finally, we want to acknowledge the team of gardeners, the library and the herbarium of the Conservatory for providing permanent access to their collections. Dr. Larry Noblick (MBC) and Dr. Scott Zona (FTG) kindly welcomed and gave us access to the collections at their respective institutions. We thank an anonymous reviewer for constructive criticism on the manuscript. References Asmussen, C.B. & Chase, M.W Coding and non coding plastid DNA in palm systematics. 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8 F. CASTANO et al. Floral Anatomy in Sabal palmetto 91 W.J., Sullivan, S., Joseph, J., Molvray, M., Kores, P.J., Givnish, T.J., Sytsma, K.J. & Pires, J.C Higher level systematics of the monocotyledons: an assessment of current knowledge and a new classification. In: Systematics and Evolution of Monocots. K.L. Wilson and D.A. Morrison, eds. CSIRO, Melbourne, pp Dransfield, J. & Uhl, N.W Palmae. In: The Families and Genera of Vascular Plants. Vol. IV. Flowering plants- Monocotyledons. K. Kubitzki, ed. Springer, Berlin, Germany, pp Dransfield, J., Ferguson, I.K. & Uhl, N.W The Coryphoid palms: patterns of variation and evolution. Annals of the Missouri Botanical Garden, 77: Dransfield, J., Uhl, N.W., Asmussen, C.B., Baker, W.J., Harley, M. & Lewis, C.E A new phylogenetic classification of the palm family, Arecaceae. Kew Bulletin, 60: Dransfield, J., Uhl, N.W., Asmussen, C.B., Baker, W.J., Harley, M.M. & Lewis, C.E Genera palmarum: the evolution and classification of palms. Kew Publishing, Royal Botanic Gardens, Kew, UK, 744pp. Giddey, A., Spichiger, R.E. & Stauffer, F.W Comparative floral structure and systematics in the Asian palm genus Rhapis (Arecaceae, Coryphoideae). Flora, 204: Hahn, W.J A molecular phylogenetic study of the Palmae (Arecaceae) based on atpb, rbcl, and 18S nrdna sequences. Systematic Biology, 51: Henderson, A., Galeano, G. & Bernal, R Field Guide to the Palms of the Americas. Princeton University Press, Princeton, New Jersey, USA, 376pp. Heslop-Harrison, Y. & Shivanna, K.R The receptive surface of the angiosperm stigma. Annals of Botany, 41: Igersheim, A. & Cichocki, O A simple method for microtome sectioning of prehistoric charcoal specimens, embedded in 2- hydroxyethyl methacrylate (HEMA). Review of Paleobotany and Palynology, 92: Morrow, L.O Floral morphology and anatomy of certain Coryphoideae (Palmae). Ph.D. Dissertation, Cornell University, Ithaca, New York, USA, 371pp. Quero, H Sabal gretheriae, a new species of palm from the Yucatan Peninsula, Mexico. Principes, 35: Reddy, G.N. & Kulkarni, A.R Developmental fruit anatomy of some coryphoid palms. Geophytology, 12: Stauffer, F.W., Rutishauser, R. & Endress, P.K Morphology and development of the female flowers in Geonoma interrupta (Arecaceae). American Journal of Botany, 89: Stauffer F.W., Barfod A. & Endress P.K Floral structure in Licuala peltata (Arecaceae: Coryphoideae) with special reference to the architecture of the unusual labyrinthine nectary. Botanical Journal of the Linnean Society, 161: Uhl, N.W. & Dransfield, J Genera Palmarum. Allen Press, Lawrence, Kansas, 610 pp. Uhl, N.W. & Moore, H.E The palm gynoecium. American Journal of Botany, 58: Uhl, N.W., Dransfield, J., Hansen, K.S. & Doyle, J.C Phylogenic analyses within Coryphoideae (Palmae). Supplement to American Journal of Botany, 77: Uhl, N.W., Dransfield, J., Davis, J.I., Luckow, M.A., Hansen, K.S. & Doyle, J.J Phylogenetic relationships among palms: Cladistic analysis of morphological and chloroplast DNA restriction site variation. In: Monocotyledons, Systematics and Evolution. P.J. Rudall, P.J. Cribb, D.F. Cutler and C.J. Humphries, eds. Royal Botanic Gardens, Kew, UK, pp Zona, S A monograph of Sabal (Arecaceae: Coryphoideae). Aliso, 12: Zona, S. & Judd, W Sabal etonia (Palmae): Systematics, distribution, ecology, and comparisons to other Florida scrub endemics. Sida, 11:
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