sign in sign up
<<
Home , Elmerrillia, Liriodendron, Magnoliaceae, Magnolia delavayi, Magnolia denudata, Pachylarnax

Pl. Syst. Evol. 258: 1–15 (2006) DOI 10.1007/s00606-005-0361-1

Comparative floral anatomy and ontogeny in

F. Xu1 and P. J. Rudall2

1South 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 , , . 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 and shrubs characterised by large organs are initiated in sequence, but ultimately form flowers with numerous and fertile parts a single ; thus their ontogeny is consistent with inserted separately on an elongated axis. More a interpretation. Tepals are initiated in whorls, than 80% of species of Magnoliaceae are and the 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 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 and Michelia isolated placement is also strongly supported montana (Van Heel 1981, 1983), and floral by analyses of nucleotide sequences in which ontogeny in 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 (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 existence of many 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 (). 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 (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 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 . The 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 apices (connective appendages) are short, and there is no distinct filament, so that the stamens cannot readily be differentiated into filament, anther, and connective. By contrast, in Liriodendron the sporangia are marginal in position and the filaments are thread-like. At anthesis, sporangia are introrse in Magnolia and Michelia but extrorse in Liriodendron. Shape of stamens in Liriodendron Figs. 1–6. Flowers of Magnoliaceae. Fig. 1. Magno- and several Magnolioideae was also studied by lia delavayi. Fig. 2. Magnolia championi. Fig. 3. Endress (1994b). Michelia crassipes. Fig. 4. Liriodendron tulipifera. . The total number of carpels in Fig. 5. Magnolia grandiflora. Fig. 6. Magnolia pae- a flower varies between species. In Magnolia netalauma 4 F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae the carpels, a -like stipe in Michelia subepidermally in Magnolia paenetalauma crassipes and all Magnolia species examined, (Fig. 12). Mature oil cells are filled with a but not in Liriodendron.InMagnolia champi- large vacuole and a cupule, which is a common oni, M. paenetalauma and Liriodendron the character of oil cells (Mariani et al. 1989), was carpels are glabrous, but pubescent in Magnolia observed in some slides (Figs. 15, 18). grandiflora, Magnolia delavayi and Michelia Dark-staining tanniniferous cells were crassipes. Each carpel possesses a single style present in most species, although they are with three vascular traces, a median and two sparse or absent in Michelia crassipes.In ventrals (Figs. 7, 17, 26, 32). Style shape and Magnolia championi (Figs. 18, 19, 25) they length varies from narrow, semi-erect, and are scattered throughout the carpel from style elongated in Magnolia paenetalauma to com- to ovary and also concentrated under the paratively stout and recurved in Magnolia epidermis to form a ring of tanniniferous cells. grandiflora.InLiriodendron the style is elon- In Magnolia paenetalauma, tanniniferous cells gate, broad, flattened and wing-like, and con- are only observed aggregated in the chalazal tains numerous aggregations of thick-walled region (Fig. 16) or scattered sparsely in the cells (Figs. 34, 40). The extent of the stigmatic ovary. In Liriodendron, tannins are present in epidermal papillae is variable between species. the outer integument and the distal portion of The stigma in Liriodendron differs from that of the inner integument (Fig. 35). species of subfamily Magnolioideae in that it is Numerous aggregations of thick-walled small and localized, formed of epidermal cells or solitary idioblastic sclereids were papillae (Fig. 38). Magnolia paenetalauma observed in all species except Michelia crassi- (Figs. 10, 11) has a small stigmatic crest of pes, also reported for Magnoliaceae by Can- unicellular epidermal papillae which are longer right (1960), and Igersheim and Endress (1997). than other epidermal cells, whereas in Magno- These cells have lamellar thickened walls, lia championi and Michelia crassipes the uni- obvious cytoplasm, large intercellular spaces cellular epidermal papillae resemble other and well-developed plasmodesmata (Figs. 13, epidermal cells (Fig. 24). The ventral suture 14). They are distributed from the style to the of the carpels is not closed in open flowers of ovary in Magnolia championi, Magnolia the Magnolia species examined here (Figs. 22, paenetalauma and Liriodendron chinense, 23), and only partially closed in Michelia although those of the latter possess compara- crassipes, in which the ventral suture is open tively thinner walls (Fig. 39). In the upper part at the upper part of style (Fig. 29) but firmly of the style of Magnolia championi, the group of fused at the lower part (Figs. 27, 28) so that thick-walled cells are associated with the the line of fusion completely disappears. In median veins, which is not connected in Liriodendron the ventral suture in the style is Magnolia paenetalauma. From the middle part completely closed (Figs. 32, 33). of style, they are associated with both the median Ovules are inserted at the inner edge of the and lateral veins in these two species. They are carpel margin (see also Erbar 1983). There are totally free from the veins in Liriodendron. two ovules per carpel in all species examined In confirmation of the observations of here. Crystals were not present in the integu- Canright (1960), carpel vasculature is similar ments of species examined here, in contrast to in Magnolia and Michelia; the apical carpels the material examined by Igersheim and En- are supplied entirely from the central vascular dress (1997). cylinder of the axis, while carpels from the Idioblasts and sclereids. Idioblastic (soli- middle to the base are all supplied by both the tary) oil cells were present in all species cortical and stelar systems. By contrast, in investigated here. They are circular and scat- Liriodendron, all carpels are supplied by tered in the carpel parenchyma from the style vasculature from both the cortex and central to the ovary, in the tissues (Figs. 15, 18) or vascular cylinder. F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae 5

Floral development (Figs. 44, 57, 65) to highly convex at later floral stages (Figs. 49, 60, 68, 74–76). The later Floral apex. At initiation, the floral apex is convex shape of the apex is maintained circular (Figs. 41, 53, 62, 71, 83) in all species through appendage initiations. Tepals, examined, and subsequently develops three stamens and carpels are initiated at slightly tepals surrounding a triangular floral primor- different levels around the periphery of the dium (Figs. 43, 54, 64). During subsequent apex. The members of each group of organs floral development the shape of the floral apex are initiated closely in time. varies from flat during perianth initiation

Figs. 7–16. Magnolia paenetalauma. Transverse sections of mature flower. 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. Oilcell(blackarrow).Fig. 16. Tanniniferous cells in chalazal region of ovule. All bars = 50 lm 6 F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Figs. 17–25 Magnolia championi. Transverse sections of mature flower. 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 7

Tepals. The three outer tepals are initiated initiated in spiral acropetal succession, but are in sequence (Figs. 42, 56, 59, 63) but ultimately trimerously whorled; the internodes between form a single whorl (Figs. 43, 54, 64). At this seldom elongate. There is a considerable stage, the shape of the floral primoridum difference in size between primordia of the first changes from circular to triangular (Figs. 43, and the second whorl during early stages 54, 64). The second whorl of three semicircular (Fig. 73). Following completion of tepal initi- tepal primordia are initiated at the tips of the ation, the central floral primordium is more or three angles formed by the triangular floral less circular (Figs. 47–49, 68, 74–76). primordium and alternate with the outer tepal Stamens. Stamen primordia are initiated whorl (Figs. 44, 57, 65). One of them is at the same time or slightly later than the third initiated slightly earlier than the other two whorl of perianth primordia. One or two (Figs. 65–67). Similarly, the innermost third stamen primordia arise opposite (in the same whorl of three perianth primordia differ sector as) the first tepal primordia (Figs. 46, slightly from one another in time of initiation 47, 68). Stamens are initiated acropetally, and alternate with those of the middle whorl successively and rapidly around the base of and hence are opposite those of the first whorl the apex (Figs. 48, 49, 60, 76, 77, 84). The (Figs. 45, 46, 68, 72, 73). Thus, the tepals are order of stamen initiation within each whorl is

Figs. 26–31. Michelia crassipes. Transverse sections of mature flower. Fig. 26. Single carpel, with three vascular traces (black arrows); thickwalledcellsabsent;theventral 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 8 F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Figs. 32–40. Liriodendron chinense. Transverse sections of mature flower. 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 flower, 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 9

Figs. 41–52. Magnolia paenetalauma. Floral development (SEM). Figs. 41–43. Differentiation of three outer tepals surrounding the triangular floral apex. Fig. 44. Differentiation of second tepal whorl, one tepal slightly earlier than the other two. Fig. 45. Initiation of three outer and three middle tepals, and first tepal of inner whorl. Figs. 46–48. Differentiation of third tepal whorl and stamens. Fig. 49. Acropetal initiation of stamens. At this stage the floral apex reaches its greatest height and diameter. Fig. 50. Differentiation of carpels, showing carpel primordia larger than those of stamens. Fig. 51. Differentiation of carpels, showing the carpel primordia initiated alternately and in series of four to five. Fig. 52. Older stage. Abbreviations: c =carpel;f = floral apex; s =stamen;t1 = tepal of first whorl; t2 = tepal of second whorl; t3 = tepal of third whorl. All bars = 100 lm 10 F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae not determined. During stamen development, 86). Carpel primordia are free and are initiated the floral apex displays its greatest height and in acropetal succession (Figs. 50, 51, 58, 69, 70, diameter. In Liriodendron tulipifera and Mag- 79, 87). During carpel initiation, the floral apex nolia delavayi the outermost stamens are gradually diminishes in height and diameter. broader and petaloid at older stages (Figs. 61, At the middle or late stage of ontogeny, the 88). margins of each carpel are incurved, forming a Carpels. When all stamen primordia have deep ventral groove which extends to the tip been initiated and begun to broaden, the (Figs. 51, 55, 58, 79–82, 87, 88). There is no remaining floral apex becomes slightly flatter. differentiation of stigma and style at this stage. Some rounded bulges are initiated in series of In older buds of all species examined here, four to five, which are larger than the stamen stamens and carpels are arranged irregularly primordia (Figs. 50, 51, 55, 69, 78, 80, 81, 85, on the floral axis (Figs. 52, 61, 70, 82, 88).

Figs. 53–61. Magnolia delavayi. Floral development (SEM). Figs. 53, 56, 59. Differentiation of outer tepals. Fig. 54. Three outer tepals initiated surrounding triangular floral primordium. Fig. 55. Differentiation of carpels, showing carpel primordia initiated in series of four to five. Fig. 57. Initiation of three middle tepals. Fig. 58. Differentiation of carpels, showing deep ventral groove extending to the tip of each carpel. Fig. 60. Initiation of stamens. Fig. 61. Older stage of flower bud, showing arrangement of stamens and carpels, and outermost petaloid stamens. Abbreviations: c =carpel;f = floral apex; s =stamen;ps = petaloid stamens; t1 = tepal of first 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 Rather, the floral meristem achieves determi- nacy by gradual diminution (Tucker 1960, Our observations correspond with those of 1979), as with the indeterminate apex of other investigations, such as Tucker’s (1961) racemose inflorescences. observations on Michelia fuscata, that apical Floral ontogeny in Magnoliaceae is remark- growth continues during floral development in ably homogeneous throughout the family, with Magnoliaceae, but the floral apex gradually tepals arranged in a more or less whorled diminishes in diameter and height during pattern surrounding more or less irregularly carpel initiation. Thus, the flower of Magnoli- arranged fertile organs. Erbar and Leins (1994) aceae is not a ‘‘true’’ determinate structure, observed an intermediate organisation in since it does not terminate in an organ or and Liriodendron tulipifera, organ whorl, as in typical eudicot flowers.

Figs. 62–70. Magnolia cha (SEM). Fig. 62. Floral apex. Fig. 63. Differentiation of first tepal of outer whorl. Fig. 64. Subsequent differentiation of outer tepal whorl surrounding the triangular floral primordium. Fig. 65– 67. Differentiation of middle tepal whorl, one tepal slightly earlier than the other two. Fig. 68. Initiation of stamens (arrow). Fig. 69. Differentiation of carpels, showing the carpel primordia initiated in series of four to five. Fig. 70. Older stage, showing irregular arrangement of stamens and carpels. Abbreviations: c =carpel;f = floral apex; s =stamen;t1 = tepal of first whorl; t2 = tepal of second whorl; t3 = tepal of third whorl. All bars = 100 lm 12 F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae

Figs. 71–82. Magnolia grandiflora. Floral development (SEM). Fig. 71. Floral apex. Figs. 72–73. Initiation of three tepal whorls. Fig. 74–76. Initiation of third tepal whorl and stamens. At this stage the floral 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. 79–81. Differentiation of carpels, showing carpel primordia initiated alternately, and in series of four to five. A deep ventral groove extends to the tip of each carpel. The floral apex gradually diminishes in height and diameter. Fig. 82. Older stage of flower bud, showing irregular arrangement of stamens and carpels. Abbreviations: c =carpel;f =floralapex;s =stamen;t1 = tepal of first 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 carpels are entirely closed at maturity, resulting derived from a spiral one in angiosperms in a relatively small stigma, in contrast to the (Erbar 1983, 1988; Erbar and Leins 1982, 1983, elongate stigma of most species of Magnolia. 1994). In some Magnolioideae not examined No carpel fusion was observed here in species of here, such as , Dugandiodendron, Magnolioideae, either in primordial or mature and Woonyoungia (Li and Conran 2003) carpel structures. In some other early-diverging an- number is reduced to less than ten. Van Heel giosperms, including the ANITA grade and (1983) described early carpel formation in some magnoliids (Endress and Igersheim 2000), Michelia montana, which is unusual in possess- carpel closure is entirely by secretion rather ing only two to four stalked carpels arranged in than by postgenital fusion. However, this char- pairs. acter may be variable in Magnoliaceae, and One outstanding question of floral mor- requires further investigation. Nooteboom phology in Magnoliaceae is whether the out- (1985) reported carpel fusion in some of the ermost organs represent bracts, as indicated by smaller genera of Magnolioideae, such as Tal- their mature structure, or tepals, as Ueda auma, Aromadendron and Tsoongiodendron, in (1986) proposed. The three distinct outermost which the is a syncarp. Li and Conran organs are initiated in sequence, but ultimately (2003) reported that in all Magnoliaceae the form a single whorl; thus their ontogeny is carpels are connate to varying degrees before consistent with a tepal interpretation. dehiscence; this conflicts with our data, but Both species of Liriodendron examined here indicates that some late fusion or concrescence differ from other Magnoliaceae in that the may occur. In Michelia crassipes, the ventral

Figs. 83–88. 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 five. Fig. 87. Carpel differentiation, showing a deep ventral groove extending to the tip of each carpel; the floral apex gradually diminishes in height and diameter. Fig. 88. Older stage of flower bud, showing arrangement of stamens and carpels, and outermost petaloid stamens. Abbreviations: c =carpel;f =floralapex;ps =petaloid stamen; s = stamen. All bars = 100 lm 14 F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae carpel suture is closed in the lower part of the Endress P. K., Igersheim A. (2000) Gynoecium style, so that the stigmatic region is relatively structure and evolution in basal angiosperms. short. Michelia crassipes also differs from the Int. J. . Sci. 161 (6 Suppl.): S211–S223. other species examined in the absence of thick- Erbar C. (1983) Zum Karpellbau einiger Magnoli- walled cells and tannins. Wider sampling is iden. Bot. Jahrb. Syst. 104: 3–31. necessary to determine the significance of these Erbar C. (1988) Early developmental patterns in flowers and their value for systematics. In: characters. However, we concur with Noote- Leins P., Tucker S. C., Endress P. K. (eds.) boom (1985) that concrescence of the carpels Aspects of floral development J. Cramer, Berlin, alone is not a reliable character for delimitation pp. 7–23. of genera in Magnoliaceae. Erbar C., Leins P. (1982) Zur Spirale in Magnolien- blu¨ten. Beitr. Biol. Pflanzen 56: 225–241. We thank Chrissie Prychid (Royal Botanic Gar- Erbar C., Leins P. (1983) Zur Sequenz von dens, Kew) for help in the laboratory. The project Blu¨tenorganen bei einigen Magnoliiden. Bot. was supported by the National Sciences Founda- Jahrb. Syst. 103: 433–449. tion of China (grant number 30000011, 30370108) Erbar C., Leins P. (1994) Flowers in Magnoliidae and the National Sciences Foundation of Guang- and the origin of flowers in other subclasses of dong province, China (grant number 000991). We the angiosperms. I. The relationships between are grateful to Peter Endress and an anonymous flowers of Magnoliidae and Alismatidae. Pl. reviwer for their comments on the manuscript. Syst. Evol. Suppl. 8: 193–208. Frumin S., Friis E. M. (1999) Magnoliid reproduc- References tive organs from the Cenomanian-Turonian of north-western Kazakhstan: Magnoliaceae and Azuma H., Garcia-Franco J. G., Rico-Gray V., Illiciaceae. Pl. Syst. Evol. 216: 265–288. Thien L. B. (2001) Molecular phylogeny of the Howard R. A. (1948) The morphology and sys- Magnoliaceae: The biogeography of tropical and tematics of the West Indian Magnoliaceae. Bull. temperate disjunctions. Amer. J. Bot. 88: 2275– Torr. Bot. Club 75: 335–357. 2285. Igersheim A., Endress P.K. (1997) Gynoecium Baillon H. E. (1866) Sur la famille des Magno- diversity and systematics of the liace´es. Adansonia 1: 133–192. and winteroids. Bot. J. Linn. Soc. 124: 213–271. Canright J. E. (1952) The comparative morphology Kim S., Soltis D. E., Soltis P. S., Suh Y. (2004) and relationships of the Magnoliaceae I. Trends DNA sequences from Miocene fossils: an ndhF of specialization in the stamens. Amer. J. Bot. sequence of Magnolia latahensis (Magnoliaceae) 39: 484–497. and an rbcL sequence of Persea pseudocarolin- Canright J. E. (1960) The comparative morphology ensis (). Amer. J. Bot. 91: 615–620. and relationships of the Magnoliaceae III. Car- Kim S., Park C. W., Kim Y. D., Suh Y. (2001) pels. Amer. J. Bot. 47: 145–155. Phylogenetic relationships in family Magnolia- Chen B. L., Nooteboom H. P. (1993) Notes on ceae inferred from ndhF sequences. Amer. J. Bot. Magnoliaceae III: the Magnoliaceae of China. 88: 717–728. Ann. Missouri Bot. Gard. 80: 999–1104. Law Y. W. (1984) A preliminary study on the Crane P. R., Friis E. M., Pedersen K. R. (1994) of the family Magnoliaceae. Acta Paleobotanical evidence on the early radiation of Phytotax. Sin. 22: 80–109. magnoliid angiosperms. Pl. Syst. Evol. s8: 51–72. Leins P. (2000) Blu¨te und Frucht. Schweizerbart: Dandy J. E. (1927) The genera of Magnoliaceae. Stuttgart. Kew Bull. 1927: 275–264. Leins P., Erbar C. (1994) Flowers in Magnoliidae Endress P. K. (1994a) Floral structure and evolu- and the origin of flowers in other subclasses of tion of primitive angiosperms: recent advances. the angiosperms. II. The relationships between Pl. Syst. Evol. 192: 79–97. flowers of Magnoliidae, Dilleniidae, and Caryo- Endress P. K. (1994b) Shapes, sizes and evolution- phyllidae. Pl. Syst. Evol. Suppl 8: 208–218. ary trends in stamens of Magnoliidae. Bot. Li J., Conran J. G. (2003) Phylogenetic relation- Jahrb. Syst. 115: 429–460. ships in Magnoliaceae subfam. Magnolioideae: a F. Xu and P. J. Rudall: Floral morphology of Magnoliaceae 15

morphological cladistic analysis. Pl. Syst. Evol. Skvortsova N. T. (1958) On the flower anatomy of 242: 33–47. Magnolia grandiflora L. Bot. Zhurn. 43: 401– Mariani P., Cappeletti E. M., Campoccia D., 408. [in Russian] Baldan B. (1989) Oil cell ultrastructure and Tucker S. (1960) Ontogeny of the floral apex of development in Liriodendron tulipifera L. Bot. Michelia fuscata. Amer. J. Bot. 47: 266–277. Gaz. 150: 391–396. Tucker S. (1961) Phyllotaxis and vascular organi- Melville R. (1969) Studies in floral structure and zation of the carpels in Michelia fuscata. Amer. evolution. I. Magnoliales. Kew Bull. 23: 133– J. Bot. 48: 60–71. 180. Tucker S. (1979) Ontogeny of the inflorescence of Nooteboom H. P. (1985) Notes on Magnoliaceae, Saururus cernuus (Saururaceae). Amer. J. Bot. with a revision of Pachylarnax and 66: 227–236. and the Malesian species of Manglietia and Ueda K. (1982) On the fundamental vascular Michelia. Blumea 31: 65–121. pattern in the flowers of the Magnoliales. Acta Nooteboom H. P. (2000) Different looks at the Phytotax. Geobot. 33: 383–391. [in Japanese] classification of the Magnoliaceae. In: Liu Y. H, Ueda K. (1986) Vascular systems in the Magnoli- Fan H. M., Chen Z. Y., Wu Q. G., Zeng Q. W. aceae. Bot. Mag. Tokyo 99: 333–349. (eds.) Proceedings of the international sympo- Ueda K., Yamashita J., Tamura M. N. (2000) sium of the family Magnoliaceae 26–37. Science Molecular phylogeny of the Magnoliaceae. In: Press, Beijing, China. Liu Y. H., Fan H. M., Chen Z. Y., Wu Q. G., Qiu Y. L., Chase M. W., Parks C. R. (1995) A Zeng Q. W. (eds.) Proceedings of the chloroplast DNA phylogenetic study of the international symposium of the family Magnoli- eastern Asia–eastern disjunct aceae 205-209. Science Press, Beijing, China. section Rytidospermum of Magnolia (Magnolia- van Heel W. A. (1981) A SEM investigation on the ceae). Amer. J. Bot. 82: 1582–1588. development of free carpels. Blumea 27: 499–522. Shi S., Jin H., Zhong Y., He X., Huang Y., Tan F., van Heel W. A. (1983) The ascidiform early Boufford D. E. (2000) Phylogenetic relationships development of free carpels, a SEM investiga- of the Magnoliaceae inferred from cpDNA matK tion. Blumea 28: 231–270. sequences. Theor. Appl. Genet. 101: 925–930. Skipworth J. P. (1970) Development of floral vasculature in the Magnoliaceae. Phytomorphol- Addresses of the authors: Fengxia Xu (e-mail: ogy 20: 228–236. [email protected]), South China Botanical Garden, Skipworth J. P., Philipson W. R. (1966) The Academia Sinica, Guangzhou, 510650, China. cortical vascular system and the interpretation Paula J. Rudall (e-mail: [email protected]), of the Magnolia flower. Phytomorphology 16: Royal Botanic Gardens, Kew Richmond, Surrey, 463–469. TW9 3AB, UK.