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
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
Ó 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 flowers (Magnolia
championi, M. delavayi, M. grandiflora, M. paenetalauma) and axillary flowers (Michelia crassipes).
The sequence of initiation of floral 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
differs 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
flower 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-defined and horticulturally important family of about 230 species
of trees and shrubs characterised by large
flowers 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 first 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
different infrafamilial taxonomic schemes, but
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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. Law’s (1984) Magnolioideae
included two tribes: Magnolieae, with terminal
flowers, and Michelieae, with axillary flowers.
Nooteboom (1985) and Cheng and Nooteboom (1993) reduced genera of Magnolioideae
first 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 flower was once considered to represent the primitive floral 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 flowers with
relatively few organs predominate in earlydivergent angiosperms (magnoliids). The large
flowers of Magnoliaceae are now normally
regarded as relatively specialised within this
grade (for reviews see Crane et al. 1994,
Endress 1994a). Here we examine floral
anatomy and ontogeny of a broad taxonomic
range of species of Magnoliaceae in a systematic context. The floral morphology of Magnoliaceae has been investigated by several
authors, including Baillon (1866), Howard
(1948), Skvortsova (1958) and Melville (1969).
Influential studies of floral vasculature include
those of Canright (1960), Tucker (1961), Skipworth and Philipson (1966), Skipworth (1970)
and Ueda (1982, 1986). Earlier work on floral
ontogeny
in
Magnoliaceae
includes
investigations of the floral apex and carpel of
Michelia fuscata (Tucker 1960, 1961), carpel
development in Magnolia stellata and Michelia
montana (Van Heel 1981, 1983), and floral
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 flowers (species of Magnolia
L.), those with axillary flowers (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. grandiflora 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: 1939–77308).
Material was fixed 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 field emission
SEM S-4700-II at 4–5 KV. For light microscope
(LM) observations, material was embedded in resin
prior to sectioning. Fixed flowers 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 58–62C 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.
3
championi and Magnolia paenetalauma, the
number is around ten; but over 90 are present
in Magnolia delavayi (Fig. 1) and 40–50 in
Magnolia grandiflora (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 grandiflora. In Liriodendron
the carpel-bearing region of the reproductive
apex is more or less conical. This region of the
flower 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 flower; 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 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 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
and several Magnolioideae was also studied by
Endress (1994b).
Gynoecium. The total number of carpels in
a flower varies between species. In Magnolia
Figs. 1–6. Flowers of Magnoliaceae. Fig. 1. Magnolia delavayi. Fig. 2. Magnolia championi. Fig. 3.
Michelia crassipes. Fig. 4. Liriodendron tulipifera.
Fig. 5. Magnolia grandiflora. Fig. 6. Magnolia paenetalauma
4
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
grandiflora, 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
grandiflora. In Liriodendron the style is elongate, broad, flattened 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 differs 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 flowers 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 firmly
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 filled 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 confirmation 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 floral apex is
circular (Figs. 41, 53, 62, 71, 83) in all species
examined, and subsequently develops three
tepals surrounding a triangular floral primordium (Figs. 43, 54, 64). During subsequent
floral development the shape of the floral apex
varies from flat during perianth initiation
5
(Figs. 44, 57, 65) to highly convex at later
floral stages (Figs. 49, 60, 68, 74–76). The later
convex shape of the apex is maintained
through appendage initiations. Tepals,
stamens and carpels are initiated at slightly
different levels around the periphery of the
apex. The members of each group of organs
are initiated closely in time.
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. Oil cell (black arrow). Fig. 16. Tanniniferous cells in chalazal region of
ovule. All bars = 50 lm
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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
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 floral 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 floral
primordium and alternate with the outer tepal
whorl (Figs. 44, 57, 65). One of them is
initiated slightly earlier than the other two
(Figs. 65–67). Similarly, the innermost third
whorl of three perianth primordia differ
slightly from one another in time of initiation
and alternate with those of the middle whorl
and hence are opposite those of the first whorl
(Figs. 45, 46, 68, 72, 73). Thus, the tepals are
7
initiated in spiral acropetal succession, but are
trimerously whorled; the internodes between
petals seldom elongate. There is a considerable
difference in size between primordia of the first
and the second whorl during early stages
(Fig. 73). Following completion of tepal initiation, the central floral primordium is more or
less circular (Figs. 47–49, 68, 74–76).
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 first 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. 26–31. Michelia crassipes. Transverse sections of mature flower. 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
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,
the floral 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 floral apex becomes slightly flatter.
Some rounded bulges are initiated in series of
four to five, 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 floral 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, 79–82, 87, 88). There is no
differentiation of stigma and style at this stage.
In older buds of all species examined here,
stamens and carpels are arranged irregularly
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
Discussion
Our observations correspond with those of
other investigations, such as Tucker’s (1961)
observations on Michelia fuscata, that apical
growth continues during floral development in
Magnoliaceae, but the floral apex gradually
diminishes in diameter and height during
carpel initiation. Thus, the flower of Magnoliaceae is not a ‘‘true’’ determinate structure,
since it does not terminate in an organ or
organ whorl, as in typical eudicot flowers.
11
Rather, the floral meristem achieves determinacy by gradual diminution (Tucker 1960,
1979), as with the indeterminate apex of
racemose inflorescences.
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. 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 = floral apex; 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
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 floral 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
differ from other Magnoliaceae in that the
13
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 conflicts with our data, but
indicates that some late fusion or concrescence
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 = floral apex; 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
style, so that the stigmatic region is relatively
short. Michelia crassipes also differs from the
other species examined in the absence of thickwalled cells and tannins. Wider sampling is
necessary to determine the significance 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:
[email protected]), South China Botanical Garden,
Academia Sinica, Guangzhou, 510650, China.
Paula J. Rudall (e-mail: [email protected]),
Royal Botanic Gardens, Kew Richmond, Surrey,
TW9 3AB, UK.