Pl. Syst. Evol. 258: 115 (2006) DOI 10.

1007/s00606-005-0361-1

Comparative oral anatomy and ontogeny in Magnoliaceae

F. Xu1 and P. J. Rudall2
1 2

South China Botanical Garden, Academia Sinica, Guangzhou, China Royal Botanic Gardens, Kew, Richmond, Surrey, UK

Received November 16, 2004; accepted June 9, 2005 Published online: March 8, 2006 Springer-Verlag 2006

Abstract. Floral anatomy and ontogeny are described in six species of Magnoliaceae, representing the two subfamilies Liriodendroideae (Liriodendron chinese and L. tulipifera) and Magnolioideae, including species with terminal owers (Magnolia championi, M. delavayi, M. grandiora, M. paenetalauma) and axillary owers (Michelia crassipes). The sequence of initiation of oral organs is from proximal to distal. The three distinct outermost organs are initiated in sequence, but ultimately form a single whorl; thus their ontogeny is consistent with a tepal interpretation. Tepals are initiated in whorls, and the stamens and carpels are spirally arranged, though the androecium shows some intermediacy between a spiral and whorled arrangement. Carpels are entirely free from each other both at primordial stages and maturity. Ventral closure of the style ranges from open in Magnolia species examined to partially closed in Michelia crassipes and completely closed in Liriodendron, resulting in a reduced stigma surface. Thick-walled cells and tannins are present in all species except Michelia crassipes. Oil cells are normally present. Floral structure is relatively homogeneous in this family, although Liriodendron diers from other Magnoliaceae in that the carpels are entirely closed at maturity, resulting in a relatively small stigma, in contrast to the elongate stigma of most species of Magnolia. The ower of Magnolia does not terminate in an organ or organ whorl but achieves determinacy by gradual diminution.

Key words: Floral development, Floral morphology, Liriodendron, Magnolia, Michelia.

Introduction Magnoliaceae are a well-dened and horticulturally important family of about 230 species of trees and shrubs characterised by large owers with numerous tepals and fertile parts inserted separately on an elongated axis. More than 80% of species of Magnoliaceae are distributed in subtropical and tropical regions of eastern Asia; the remainder occur in America, indicating a relictual tropical disjunction (Azuma et al. 2001). Renewed debate on the systematics of the family has been stimulated by several recent cladistic analyses, both morphological (Li and Conran 2003) and molecular (Shi et al. 2000), but several outstanding questions remain. Dandy (1927) proposed the rst comprehensive taxonomic treatment of Magnoliaceae, which recognised ten genera distributed in two tribes: Liriodendreae (sole genus Liriodendron) and Magnolieae, including Magnolia, Manglietia, Michelia, and six smaller genera. Subsequent authors have proposed several dierent infrafamilial taxonomic schemes, but

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

all of them divide the family into two subfamilies, of which one, Liriodendroideae, includes the sole genus Liriodendron, and the other, Magnolioideae, includes a variable number of genera. Laws (1984) Magnolioideae included two tribes: Magnolieae, with terminal owers, and Michelieae, with axillary owers. Nooteboom (1985) and Cheng and Nooteboom (1993) reduced genera of Magnolioideae rst to six genera (Chen and Nooteboom 1993) and later to two, and discarded all tribes and subtribes (Nooteboom 2000). Thus, there is no disagreement about the status of Liriodendroideae containing only Liriodendron; this isolated placement is also strongly supported by analyses of nucleotide sequences in which Liriodendron was consistently sister to all other Magnoliaceae (Qiu et al. 1995, Ueda et al. 2000, Shi et al. 2000, Kim et al. 2001). However, relationships within Magnolioideae remain equivocal; in all analyses, including chloroplast DNA sequence data from matK (Shi et al. 2000), and ndhF (Kim et al. 2001, 2004), the large genus Magnolia is paraphyletic with respect to the other smaller genera. Li and Conran (2003) recommended placement of the smaller genera of Magnolioideae within a broadly circumscribed Magnolia, but highlighted the need for more morphological data to improve phylogenetic resolution within this group. Many species of Magnoliaceae are known only from fossils (e.g. Frumin and Friis 1999, Kim et al. 2004), making combined morphological and molecular analysis highly desirable in this group. The large magnolia ower was once considered to represent the primitive oral type (the Ranalian hypothesis), based mainly on the existence of many fossil forms. However, recent improved understanding of phylogenetic relationships, together with new fossil discoveries, have demonstrated that small owers with relatively few organs predominate in earlydivergent angiosperms (magnoliids). The large owers of Magnoliaceae are now normally regarded as relatively specialised within this grade (for reviews see Crane et al. 1994, Endress 1994a). Here we examine oral

anatomy and ontogeny of a broad taxonomic range of species of Magnoliaceae in a systematic context. The oral morphology of Magnoliaceae has been investigated by several authors, including Baillon (1866), Howard (1948), Skvortsova (1958) and Melville (1969). Inuential studies of oral vasculature include those of Canright (1960), Tucker (1961), Skipworth and Philipson (1966), Skipworth (1970) and Ueda (1982, 1986). Earlier work on oral ontogeny in Magnoliaceae includes investigations of the oral apex and carpel of Michelia fuscata (Tucker 1960, 1961), carpel development in Magnolia stellata and Michelia montana (Van Heel 1981, 1983), and oral ontogeny in Liriodendron tulipifera and Magnolia denudata (Erbar and Leins 1994, Leins and Erbar 1994, Leins 2000). Materials and methods
Species examined were chosen as representatives of the taxa with terminal owers (species of Magnolia L.), those with axillary owers (species of Michelia T. Durand) and Liriodendron L. Specimens at a range of developmental stages were collected either from the Botanical Garden at the South China Institute of Botany, Chinese Academy of Sciences (SCBI), or the Living Collections, Royal Botanic Gardens, Kew (K). Voucher specimens of samples collected from South China Institute of Botany were deposited in SCBI. The following species were investigated: Magnolia championi Benth. (section Gwillimia) (SCBI: FX Xu 03011), M. delavayi Franch. (section Gwillimia) (SCBI: FX Xu 03019), M. grandiora L. (section Theorhodon) (SCBI: FX Xu 03008), M. paenetalauma Dandy (SCBI: FX Xu 03014), Michelia crassipes Y.W.Law (SCBI: FX Xu 03016), Liriodendron chinense Sargent (SCBI: FX Xu 03022) and L. tulipifera L. (K: 193977308). Material was xed in formalin acetic alcohol (FAA: 70% alcohol, formaldehyde and glacial acetic acid in a ratio of 85:10:5). For scanning electron microscope (SEM) examination, buds were dehydrated in an ethanol series. Dehydrated material was then critical-point-dried using a Baltec CPD 030 critical point drier, mounted onto SEM stubs using double-sided adhesive tape, coated with platinum using an Emitech K550 sputter coater,

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae and examined using a Hitachi cold eld emission SEM S-4700-II at 45 KV. For light microscope (LM) observations, material was embedded in resin prior to sectioning. Fixed owers and buds were dehydrated in an ethanol series to absolute ethanol, then transferred through an absolute ethanol : LR white resin series to absolute resin, and kept in a fridge for about a week, with daily changes of resin. Specimens were then moved to gelatine capsules and polymerized between 5862C at 600 mbar pressure for about 21 hours. Once cooled, the resin specimens were sectioned at 5lm thickness using a Leica microtome. Sections were stained in Toluidine Blue and mounted in DPX (Sigma-Aldrich Co., Gillingham, UK). Photomicrographs were taken using a Leitz Diaplan photomicroscope with a digital camera.

championi and Magnolia paenetalauma, the number is around ten; but over 90 are present in Magnolia delavayi (Fig. 1) and 4050 in Magnolia grandiora (Fig. 2). In material examined here, carpels were entirely separate from each other; no connection or adnation was observed at any position in any species examined here (Figs. 8, 9, 20, 21, 30, 31, 36, 37). The carpel-bearing region of the reproductive apex is cylindrical in Michelia crassipes, Magnolia championi and Magnolia paenetalauma to sub-ovoid in Magnolia delavayi and Magnolia grandiora. In Liriodendron the carpel-bearing region of the reproductive apex is more or less conical. This region of the ower is stipitate, formed by the sterile part of

Results Floral morphology and anatomy Flowers are solitary, bisexual, and haplomorphic, i.e. with spirally arranged organs inserted separately onto an elongated axis. A ring of three bract-like structures surrounds the ower; 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. 16). Androecium. In all species except Liriodendron, the stamens have long slender nonmarginal 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 lament, so that the stamens cannot readily be dierentiated into lament, anther, and connective. By contrast, in Liriodendron the sporangia are marginal in position and the laments are thread-like. At anthesis, sporangia are introrse in Magnolia and Michelia but extrorse in Liriodendron. Shape of stamens in Liriodendron and several Magnolioideae was also studied by Endress (1994b). Gynoecium. The total number of carpels in a ower varies between species. In Magnolia

Figs. 16. Flowers of Magnoliaceae. Fig. 1. Magnolia delavayi. Fig. 2. Magnolia championi. Fig. 3. Michelia crassipes. Fig. 4. Liriodendron tulipifera. Fig. 5. Magnolia grandiora. Fig. 6. Magnolia paenetalauma

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

the carpels, a petiole-like stipe in Michelia crassipes and all Magnolia species examined, but not in Liriodendron. In Magnolia championi, M. paenetalauma and Liriodendron the carpels are glabrous, but pubescent in Magnolia grandiora, Magnolia delavayi and Michelia crassipes. Each carpel possesses a single style with three vascular traces, a median and two ventrals (Figs. 7, 17, 26, 32). Style shape and length varies from narrow, semi-erect, and elongated in Magnolia paenetalauma to comparatively stout and recurved in Magnolia grandiora. In Liriodendron the style is elongate, broad, attened and wing-like, and contains numerous aggregations of thick-walled cells (Figs. 34, 40). The extent of the stigmatic epidermal papillae is variable between species. The stigma in Liriodendron diers from that of species of subfamily Magnolioideae in that it is small and localized, formed of epidermal papillae (Fig. 38). Magnolia paenetalauma (Figs. 10, 11) has a small stigmatic crest of unicellular epidermal papillae which are longer than other epidermal cells, whereas in Magnolia championi and Michelia crassipes the unicellular epidermal papillae resemble other epidermal cells (Fig. 24). The ventral suture of the carpels is not closed in open owers of the Magnolia species examined here (Figs. 22, 23), and only partially closed in Michelia crassipes, in which the ventral suture is open at the upper part of style (Fig. 29) but rmly fused at the lower part (Figs. 27, 28) so that the line of fusion completely disappears. In Liriodendron the ventral suture in the style is completely closed (Figs. 32, 33). Ovules are inserted at the inner edge of the carpel margin (see also Erbar 1983). There are two ovules per carpel in all species examined here. Crystals were not present in the integuments of species examined here, in contrast to the material examined by Igersheim and Endress (1997). Idioblasts and sclereids. Idioblastic (solitary) oil cells were present in all species investigated here. They are circular and scattered in the carpel parenchyma from the style to the ovary, in the tissues (Figs. 15, 18) or

subepidermally in Magnolia paenetalauma (Fig. 12). Mature oil cells are lled with a large vacuole and a cupule, which is a common character of oil cells (Mariani et al. 1989), was observed in some slides (Figs. 15, 18). Dark-staining tanniniferous cells were present in most species, although they are sparse or absent in Michelia crassipes. In Magnolia championi (Figs. 18, 19, 25) they are scattered throughout the carpel from style to ovary and also concentrated under the epidermis to form a ring of tanniniferous cells. In Magnolia paenetalauma, tanniniferous cells are only observed aggregated in the chalazal region (Fig. 16) or scattered sparsely in the ovary. In Liriodendron, tannins are present in the outer integument and the distal portion of the inner integument (Fig. 35). Numerous aggregations of thick-walled cells or solitary idioblastic sclereids were observed in all species except Michelia crassipes, also reported for Magnoliaceae by Canright (1960), and Igersheim and Endress (1997). These cells have lamellar thickened walls, obvious cytoplasm, large intercellular spaces and well-developed plasmodesmata (Figs. 13, 14). They are distributed from the style to the ovary in Magnolia championi, Magnolia paenetalauma and Liriodendron chinense, although those of the latter possess comparatively thinner walls (Fig. 39). In the upper part of the style of Magnolia championi, the group of thick-walled cells are associated with the median veins, which is not connected in Magnolia paenetalauma. From the middle part of style, they are associated with both the median and lateral veins in these two species. They are totally free from the veins in Liriodendron. In conrmation of the observations of Canright (1960), carpel vasculature is similar in Magnolia and Michelia; the apical carpels are supplied entirely from the central vascular cylinder of the axis, while carpels from the middle to the base are all supplied by both the cortical and stelar systems. By contrast, in Liriodendron, all carpels are supplied by vasculature from both the cortex and central vascular cylinder.

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Floral development Floral apex. At initiation, the oral apex is circular (Figs. 41, 53, 62, 71, 83) in all species examined, and subsequently develops three tepals surrounding a triangular oral primordium (Figs. 43, 54, 64). During subsequent oral development the shape of the oral apex varies from at during perianth initiation

(Figs. 44, 57, 65) to highly convex at later oral stages (Figs. 49, 60, 68, 7476). The later convex shape of the apex is maintained through appendage initiations. Tepals, stamens and carpels are initiated at slightly dierent levels around the periphery of the apex. The members of each group of organs are initiated closely in time.

Figs. 716. Magnolia paenetalauma. Transverse sections of mature ower. Fig. 7. Floral apex, showing three fully developed carpels in the last tier, each with 3 vascular bundles (white arrows). Fig. 8. Carpellary region, showing carpels closely appressed, but not fused. Fig. 9. detail of Fig. 9, showing carpels closely appressed. Fig. 10. Stigmatic epidermal papillae. Fig. 11. Detail of Fig. 10. Fig. 12. Subepidermal oil cell. Fig. 13. Upper carpels, showing aggregations of thick-walled cells in each carpel. Fig. 14. Detail of thick-walled cells in Fig. 13, free from the vascular bundles. Fig. 15. Oil cell (black arrow). Fig. 16. Tanniniferous cells in chalazal region of ovule. All bars = 50 lm

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Figs. 1725 Magnolia championi. Transverse sections of mature ower. Fig. 17. Single carpel, showing three vascular traces (black arrows) interspersed with regions of thick-walled cells. Fig. 18. Oil cell and tanniferous cells. Fig. 19. Single carpel, showing aggregations of thick-walled cells and subepidermal tannins. Fig. 20. Carpels including ovules; carpels closely appressed but not fused to each other; note insertion to axis. Fig. 21. Detail of Fig. 20, showing carpels closely appressed. Fig. 22. Carpel below ovule, showing ventral suture. Fig. 23. Detail of Fig. 22, showing open ventral suture. Fig. 24. Stigma, showing unicellar epidermal papillae. Fig. 25. Tanniniferous cells (arrowed) in chalazal region of ovule. All bars = 50 lm

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Tepals. The three outer tepals are initiated in sequence (Figs. 42, 56, 59, 63) but ultimately form a single whorl (Figs. 43, 54, 64). At this stage, the shape of the oral primoridum changes from circular to triangular (Figs. 43, 54, 64). The second whorl of three semicircular tepal primordia are initiated at the tips of the three angles formed by the triangular oral primordium and alternate with the outer tepal whorl (Figs. 44, 57, 65). One of them is initiated slightly earlier than the other two (Figs. 6567). Similarly, the innermost third whorl of three perianth primordia dier slightly from one another in time of initiation and alternate with those of the middle whorl and hence are opposite those of the rst whorl (Figs. 45, 46, 68, 72, 73). Thus, the tepals are

initiated in spiral acropetal succession, but are trimerously whorled; the internodes between petals seldom elongate. There is a considerable dierence in size between primordia of the rst and the second whorl during early stages (Fig. 73). Following completion of tepal initiation, the central oral primordium is more or less circular (Figs. 4749, 68, 7476). Stamens. Stamen primordia are initiated at the same time or slightly later than the third whorl of perianth primordia. One or two stamen primordia arise opposite (in the same sector as) the rst tepal primordia (Figs. 46, 47, 68). Stamens are initiated acropetally, successively and rapidly around the base of the apex (Figs. 48, 49, 60, 76, 77, 84). The order of stamen initiation within each whorl is

Figs. 2631. Michelia crassipes. Transverse sections of mature ower. Fig. 26. Single carpel, with three vascular traces (black arrows); thick walled cells absent; the ventral suture is closed. Fig. 27. Lower part of style. Fig. 28. Detail of Fig. 27, showing closed ventral suture. Fig. 29. Upper part of style, showing open ventral suture. Fig. 30. Carpellary region, showing free carpels. Fig. 31. Detail of Fig. 30. All bars = 50 lm

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Figs. 3240. Liriodendron chinense. Transverse sections of mature ower. Fig. 32. Single carpel, with three vascular traces (black arrows); thick-walled cells absent. Fig. 33. Detail of Fig. 32, showing closed ventral suture. Fig. 34. Middle part of mature ower, showing carpel arrangement. Fig. 35. Ovule, showing tannins present in outer integument and distal portion of inner integument. Fig. 36. Detail of Fig. 37. Fig. 37. Carpellary region, showing free carpels. Fig. 38. Stigma, showing localized epidermal papillae. Fig. 39. Detail of Fig. 40, showing thick-walled cells. Fig. 40. Winged styles, each containing a group of thick-walled cells, free from vascular bundles. All bars = 50 lm, except in 35 = 200 lm

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Figs. 4152. Magnolia paenetalauma. Floral development (SEM). Figs. 4143. Dierentiation of three outer tepals surrounding the triangular oral apex. Fig. 44. Dierentiation of second tepal whorl, one tepal slightly earlier than the other two. Fig. 45. Initiation of three outer and three middle tepals, and rst tepal of inner whorl. Figs. 4648. Dierentiation of third tepal whorl and stamens. Fig. 49. Acropetal initiation of stamens. At this stage the oral apex reaches its greatest height and diameter. Fig. 50. Dierentiation of carpels, showing carpel primordia larger than those of stamens. Fig. 51. Dierentiation of carpels, showing the carpel primordia initiated alternately and in series of four to ve. Fig. 52. Older stage. Abbreviations: c = carpel; f = oral apex; s = stamen; t1 = tepal of rst whorl; t2 = tepal of second whorl; t3 = tepal of third whorl. All bars = 100 lm

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F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

not determined. During stamen development, the oral apex displays its greatest height and diameter. In Liriodendron tulipifera and Magnolia delavayi the outermost stamens are broader and petaloid at older stages (Figs. 61, 88). Carpels. When all stamen primordia have been initiated and begun to broaden, the remaining oral apex becomes slightly atter. Some rounded bulges are initiated in series of four to ve, which are larger than the stamen primordia (Figs. 50, 51, 55, 69, 78, 80, 81, 85,

86). Carpel primordia are free and are initiated in acropetal succession (Figs. 50, 51, 58, 69, 70, 79, 87). During carpel initiation, the oral apex gradually diminishes in height and diameter. At the middle or late stage of ontogeny, the margins of each carpel are incurved, forming a deep ventral groove which extends to the tip (Figs. 51, 55, 58, 7982, 87, 88). There is no dierentiation of stigma and style at this stage. In older buds of all species examined here, stamens and carpels are arranged irregularly on the oral axis (Figs. 52, 61, 70, 82, 88).

Figs. 5361. Magnolia delavayi. Floral development (SEM). Figs. 53, 56, 59. Dierentiation of outer tepals. Fig. 54. Three outer tepals initiated surrounding triangular oral primordium. Fig. 55. Dierentiation of carpels, showing carpel primordia initiated in series of four to ve. Fig. 57. Initiation of three middle tepals. Fig. 58. Dierentiation of carpels, showing deep ventral groove extending to the tip of each carpel. Fig. 60. Initiation of stamens. Fig. 61. Older stage of ower bud, showing arrangement of stamens and carpels, and outermost petaloid stamens. Abbreviations: c = carpel; f = oral apex; s = stamen; ps = petaloid stamens; t1 = tepal of rst whorl; t2 = tepal of second whorl; t3 = tepal of third whorl. All bars = 100 lm

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

11

Discussion Our observations correspond with those of other investigations, such as Tuckers (1961) observations on Michelia fuscata, that apical growth continues during oral development in Magnoliaceae, but the oral apex gradually diminishes in diameter and height during carpel initiation. Thus, the ower of Magnoliaceae is not a true determinate structure, since it does not terminate in an organ or organ whorl, as in typical eudicot owers.

Rather, the oral meristem achieves determinacy by gradual diminution (Tucker 1960, 1979), as with the indeterminate apex of racemose inorescences. Floral ontogeny in Magnoliaceae is remarkably homogeneous throughout the family, with tepals arranged in a more or less whorled pattern surrounding more or less irregularly arranged fertile organs. Erbar and Leins (1994) observed an intermediate organisation in Magnolia denudata and Liriodendron tulipifera,

Figs. 6270. Magnolia cha (SEM). Fig. 62. Floral apex. Fig. 63. Dierentiation of rst tepal of outer whorl. Fig. 64. Subsequent dierentiation of outer tepal whorl surrounding the triangular oral primordium. Fig. 65 67. Dierentiation of middle tepal whorl, one tepal slightly earlier than the other two. Fig. 68. Initiation of stamens (arrow). Fig. 69. Dierentiation of carpels, showing the carpel primordia initiated in series of four to ve. Fig. 70. Older stage, showing irregular arrangement of stamens and carpels. Abbreviations: c = carpel; f = oral apex; s = stamen; t1 = tepal of rst whorl; t2 = tepal of second whorl; t3 = tepal of third whorl. All bars = 100 lm

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F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Figs. 7182. Magnolia grandiora. Floral development (SEM). Fig. 71. Floral apex. Figs. 7273. Initiation of three tepal whorls. Fig. 7476. Initiation of third tepal whorl and stamens. At this stage the oral apex reaches its greatest height and diameter. Fig. 77. Acropetal initiation of stamens. Fig. 78. Initiation of carpels, showing carpel primordia larger than stamen primordia. Figs. 7981. Dierentiation of carpels, showing carpel primordia initiated alternately, and in series of four to ve. A deep ventral groove extends to the tip of each carpel. The oral apex gradually diminishes in height and diameter. Fig. 82. Older stage of ower bud, showing irregular arrangement of stamens and carpels. Abbreviations: c = carpel; f = oral apex; s = stamen; t1 = tepal of rst whorl; t2 = tepal of second whorl; t3 = tepal of third whorl. All bars = 100 lm

F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

13

and suggested that a whorled condition is derived from a spiral one in basal angiosperms (Erbar 1983, 1988; Erbar and Leins 1982, 1983, 1994). In some Magnolioideae not examined here, such as Pachylarnax, Dugandiodendron, and Woonyoungia (Li and Conran 2003) carpel number is reduced to less than ten. Van Heel (1983) described early carpel formation in Michelia montana, which is unusual in possessing only two to four stalked carpels arranged in pairs. One outstanding question of oral morphology in Magnoliaceae is whether the outermost organs represent bracts, as indicated by their mature structure, or tepals, as Ueda (1986) proposed. The three distinct outermost organs are initiated in sequence, but ultimately form a single whorl; thus their ontogeny is consistent with a tepal interpretation. Both species of Liriodendron examined here dier from other Magnoliaceae in that the

carpels are entirely closed at maturity, resulting in a relatively small stigma, in contrast to the elongate stigma of most species of Magnolia. No carpel fusion was observed here in species of Magnolioideae, either in primordial or mature structures. In some other early-diverging angiosperms, including the ANITA grade and some magnoliids (Endress and Igersheim 2000), carpel closure is entirely by secretion rather than by postgenital fusion. However, this character may be variable in Magnoliaceae, and requires further investigation. Nooteboom (1985) reported carpel fusion in some of the smaller genera of Magnolioideae, such as Talauma, Aromadendron and Tsoongiodendron, in which the fruit is a syncarp. Li and Conran (2003) reported that in all Magnoliaceae the carpels are connate to varying degrees before dehiscence; this conicts with our data, but indicates that some late fusion or concrescence may occur. In Michelia crassipes, the ventral

Figs. 8388. Liriodendron tulipifera. Floral development (SEM). Fig. 83. Floral apex. Fig. 84. Initiation of stamens. Figs. 85, 86. Initiation of carpels, showing carpel primordia initiated in series of four to ve. Fig. 87. Carpel dierentiation, showing a deep ventral groove extending to the tip of each carpel; the oral apex gradually diminishes in height and diameter. Fig. 88. Older stage of ower bud, showing arrangement of stamens and carpels, and outermost petaloid stamens. Abbreviations: c = carpel; f = oral apex; ps = petaloid stamen; s = stamen. All bars = 100 lm

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F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae Endress P. K., Igersheim A. (2000) Gynoecium structure and evolution in basal angiosperms. Int. J. Plant. Sci. 161 (6 Suppl.): S211S223. Erbar C. (1983) Zum Karpellbau einiger Magnoliiden. Bot. Jahrb. Syst. 104: 331. Erbar C. (1988) Early developmental patterns in owers and their value for systematics. In: Leins P., Tucker S. C., Endress P. K. (eds.) Aspects of oral development J. Cramer, Berlin, pp. 723. Erbar C., Leins P. (1982) Zur Spirale in Magnolienblu ten. Beitr. Biol. Panzen 56: 225241. Erbar C., Leins P. (1983) Zur Sequenz von Blu tenorganen bei einigen Magnoliiden. Bot. Jahrb. Syst. 103: 433449. Erbar C., Leins P. (1994) Flowers in Magnoliidae and the origin of owers in other subclasses of the angiosperms. I. The relationships between owers of Magnoliidae and Alismatidae. Pl. Syst. Evol. Suppl. 8: 193208. Frumin S., Friis E. M. (1999) Magnoliid reproductive organs from the Cenomanian-Turonian of north-western Kazakhstan: Magnoliaceae and Illiciaceae. Pl. Syst. Evol. 216: 265288. Howard R. A. (1948) The morphology and systematics of the West Indian Magnoliaceae. Bull. Torr. Bot. Club 75: 335357. Igersheim A., Endress P.K. (1997) Gynoecium diversity and systematics of the Magnoliales and winteroids. Bot. J. Linn. Soc. 124: 213271. Kim S., Soltis D. E., Soltis P. S., Suh Y. (2004) DNA sequences from Miocene fossils: an ndhF sequence of Magnolia latahensis (Magnoliaceae) and an rbcL sequence of Persea pseudocarolinensis (Lauraceae). Amer. J. Bot. 91: 615620. Kim S., Park C. W., Kim Y. D., Suh Y. (2001) Phylogenetic relationships in family Magnoliaceae inferred from ndhF sequences. Amer. J. Bot. 88: 717728. Law Y. W. (1984) A preliminary study on the taxonomy of the family Magnoliaceae. Acta Phytotax. Sin. 22: 80109. Leins P. (2000) Blu te und Frucht. Schweizerbart: Stuttgart. Leins P., Erbar C. (1994) Flowers in Magnoliidae and the origin of owers in other subclasses of the angiosperms. II. The relationships between owers of Magnoliidae, Dilleniidae, and Caryophyllidae. Pl. Syst. Evol. Suppl 8: 208218. Li J., Conran J. G. (2003) Phylogenetic relationships in Magnoliaceae subfam. Magnolioideae: a

carpel suture is closed in the lower part of the style, so that the stigmatic region is relatively short. Michelia crassipes also diers from the other species examined in the absence of thickwalled cells and tannins. Wider sampling is necessary to determine the signicance of these characters. However, we concur with Nooteboom (1985) that concrescence of the carpels alone is not a reliable character for delimitation of genera in Magnoliaceae.
We thank Chrissie Prychid (Royal Botanic Gardens, Kew) for help in the laboratory. The project was supported by the National Sciences Foundation of China (grant number 30000011, 30370108) and the National Sciences Foundation of Guangdong province, China (grant number 000991). We are grateful to Peter Endress and an anonymous reviwer for their comments on the manuscript.

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Addresses of the authors: Fengxia Xu (e-mail: xfx@scib.ac.cr), South China Botanical Garden, Academia Sinica, Guangzhou, 510650, China. Paula J. Rudall (e-mail: p.rudall@rbgkew.org.uk), Royal Botanic Gardens, Kew Richmond, Surrey, TW9 3AB, UK.