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Comparative Floral Anatomy and Ontogeny in Magnoliaceae

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Comparative Floral Anatomy and Ontogeny in Magnoliaceae Pl. Syst. Evol. 258: 1–15 (2006) DOI 10.1007/s00606-005-0361-1 Comparative floral anatomy and ontogeny in Magnoliaceae F. Xu1 and P. J. Rudall2 1South China Botanical Garden, Academia Sinica, Guangzhou, China 2Royal Botanic Gardens, Kew, Richmond, Surrey, UK Received November 16, 2004; accepted June 9, 2005 Published online: March 8, 2006 Ó Springer-Verlag 2006 Abstract. Floral anatomy and ontogeny are de- Key words: Floral development, Floral morphology, scribed in six species of Magnoliaceae, representing Liriodendron, Magnolia, Michelia. the two subfamilies Liriodendroideae (Liriodendron chinese and L. tulipifera) and Magnolioideae, including species with terminal flowers (Magnolia Introduction championi, M. delavayi, M. grandiflora, M. pae- netalauma) and axillary flowers (Michelia crassipes). Magnoliaceae are a well-defined and horticul- The sequence of initiation of floral organs is from turally important family of about 230 species proximal to distal. The three distinct outermost of trees and shrubs characterised by large organs are initiated in sequence, but ultimately form flowers with numerous tepals and fertile parts a single whorl; thus their ontogeny is consistent with inserted separately on an elongated axis. More a tepal interpretation. Tepals are initiated in whorls, than 80% of species of Magnoliaceae are and the stamens and carpels are spirally arranged, though the androecium shows some intermediacy distributed in subtropical and tropical regions between a spiral and whorled arrangement. Carpels of eastern Asia; the remainder occur in Amer- are entirely free from each other both at primordial ica, indicating a relictual tropical disjunction stages and maturity. Ventral closure of the style (Azuma et al. 2001). Renewed debate on the ranges from open in Magnolia species examined to systematics of the family has been stimulated partially closed in Michelia crassipes and completely by several recent cladistic analyses, both closed in Liriodendron, resulting in a reduced stigma morphological (Li and Conran 2003) and surface. Thick-walled cells and tannins are present molecular (Shi et al. 2000), but several out- in all species except Michelia crassipes. Oil cells are standing questions remain. normally present. Floral structure is relatively Dandy (1927) proposed the first compre- Liriodendron homogeneous in this family, although hensive taxonomic treatment of Magnoliaceae, differs from other Magnoliaceae in that the which recognised ten genera distributed in two carpels are entirely closed at maturity, resulting in a relatively small stigma, in contrast to the tribes: Liriodendreae (sole genus Liriodendron) elongate stigma of most species of Magnolia. The and Magnolieae, including Magnolia, Mang- flower of Magnolia does not terminate in an organ lietia, Michelia, and six smaller genera. Sub- or organ whorl but achieves determinacy by gradual sequent authors have proposed several diminution. different infrafamilial taxonomic schemes, but 2 F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae all of them divide the family into two anatomy and ontogeny of a broad taxonomic subfamilies, of which one, Liriodendroideae, range of species of Magnoliaceae in a system- includes the sole genus Liriodendron, and the atic context. The floral morphology of Mag- other, Magnolioideae, includes a variable noliaceae has been investigated by several number of genera. Law’s (1984) Magnolioideae authors, including Baillon (1866), Howard included two tribes: Magnolieae, with terminal (1948), Skvortsova (1958) and Melville (1969). flowers, and Michelieae, with axillary flowers. Influential studies of floral vasculature include Nooteboom (1985) and Cheng and Noote- those of Canright (1960), Tucker (1961), Skip- boom (1993) reduced genera of Magnolioideae worth and Philipson (1966), Skipworth (1970) first to six genera (Chen and Nooteboom 1993) and Ueda (1982, 1986). Earlier work on floral and later to two, and discarded all tribes and ontogeny in Magnoliaceae includes subtribes (Nooteboom 2000). Thus, there is no investigations of the floral apex and carpel of disagreement about the status of Liriodend- Michelia fuscata (Tucker 1960, 1961), carpel roideae containing only Liriodendron; this development in Magnolia stellata and Michelia isolated placement is also strongly supported montana (Van Heel 1981, 1983), and floral by analyses of nucleotide sequences in which ontogeny in Liriodendron tulipifera and Mag- Liriodendron was consistently sister to all other nolia denudata (Erbar and Leins 1994, Leins Magnoliaceae (Qiu et al. 1995, Ueda et al. and Erbar 1994, Leins 2000). 2000, Shi et al. 2000, Kim et al. 2001). How- ever, relationships within Magnolioideae Materials and methods remain equivocal; in all analyses, including chloroplast DNA sequence data from matK (Shi et al. 2000), and ndhF (Kim et al. 2001, Species examined were chosen as representatives of 2004), the large genus Magnolia is paraphyletic the taxa with terminal flowers (species of Magnolia with respect to the other smaller genera. Li and L.), those with axillary flowers (species of Michelia Conran (2003) recommended placement of the T. Durand) and Liriodendron L. Specimens at a smaller genera of Magnolioideae within a range of developmental stages were collected either from the Botanical Garden at the South China broadly circumscribed Magnolia, but high- Institute of Botany, Chinese Academy of Sciences lighted the need for more morphological data (SCBI), or the Living Collections, Royal Botanic to improve phylogenetic resolution within this Gardens, Kew (K). Voucher specimens of samples group. Many species of Magnoliaceae are collected from South China Institute of Botany known only from fossils (e.g. Frumin and were deposited in SCBI. The following species were Friis 1999, Kim et al. 2004), making combined investigated: Magnolia championi Benth. (section morphological and molecular analysis highly Gwillimia) (SCBI: FX Xu 03011), M. delavayi desirable in this group. Franch. (section Gwillimia) (SCBI: FX Xu 03019), The large magnolia flower was once con- M. grandiflora L. (section Theorhodon) (SCBI: FX sidered to represent the primitive floral type Xu 03008), M. paenetalauma Dandy (SCBI: FX Xu (the Ranalian hypothesis), based mainly on the 03014), Michelia crassipes Y.W.Law (SCBI: FX Xu Liriodendron chinense existence of many fossil forms. However, recent 03016), Sargent (SCBI: FX Xu 03022) and L. tulipifera L. (K: 1939–77308). improved understanding of phylogenetic rela- Material was fixed in formalin acetic alcohol tionships, together with new fossil discoveries, (FAA: 70% alcohol, formaldehyde and glacial have demonstrated that small flowers with acetic acid in a ratio of 85:10:5). For scanning relatively few organs predominate in early- electron microscope (SEM) examination, buds were divergent angiosperms (magnoliids). The large dehydrated in an ethanol series. Dehydrated mate- flowers of Magnoliaceae are now normally rial was then critical-point-dried using a Baltec regarded as relatively specialised within this CPD 030 critical point drier, mounted onto SEM grade (for reviews see Crane et al. 1994, stubs using double-sided adhesive tape, coated with Endress 1994a). Here we examine floral platinum using an Emitech K550 sputter coater, F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae 3 and examined using a Hitachi cold field emission championi and Magnolia paenetalauma, the SEM S-4700-II at 4–5 KV. For light microscope number is around ten; but over 90 are present (LM) observations, material was embedded in resin in Magnolia delavayi (Fig. 1) and 40–50 in prior to sectioning. Fixed flowers and buds were Magnolia grandiflora (Fig. 2). dehydrated in an ethanol series to absolute ethanol, In material examined here, carpels were then transferred through an absolute ethanol : LR entirely separate from each other; no connec- white resin series to absolute resin, and kept in a tion or adnation was observed at any position fridge for about a week, with daily changes of resin. Specimens were then moved to gelatine capsules in any species examined here (Figs. 8, 9, 20, 21, and polymerized between 58–62C at 600 mbar 30, 31, 36, 37). The carpel-bearing region of pressure for about 21 hours. Once cooled, the resin the reproductive apex is cylindrical in Michelia specimens were sectioned at 5lm thickness using a crassipes, Magnolia championi and Magnolia Leica microtome. Sections were stained in Tolui- paenetalauma to sub-ovoid in Magnolia dela- dine Blue and mounted in DPX (Sigma-Aldrich vayi and Magnolia grandiflora.InLiriodendron Co., Gillingham, UK). Photomicrographs were the carpel-bearing region of the reproductive taken using a Leitz Diaplan photomicroscope with apex is more or less conical. This region of the a digital camera. flower is stipitate, formed by the sterile part of Results Floral morphology and anatomy Flowers are solitary, bisexual, and haplomor- phic, i.e. with spirally arranged organs inserted separately onto an elongated axis. A ring of three bract-like structures surrounds the flow- er; these are normally interpreted as bracts, but sometimes as sepals. The perianth consists of normally nine free tepals which surround numerous free stamens and carpels respectively (Figs. 1–6). Androecium. In all species except Lirioden- dron, the stamens have long slender non- marginal sporangia which are embedded in the adaxial surface of the microsporophyll. In Magnolia and Michelia species examined here, the stamen apices (connective appendages) are short, and there is no distinct filament,
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