Morphology and anatomy of the flower of Meliosma ... - Springer Link

Plant Systematics and Evolution

Pl Syst Evol 271: 79–91 (2008) DOI 10.1007/s00606-007-0618-y Printed in The Netherlands

Morphology and anatomy of the flower of Meliosma (Sabiaceae): implications for pollination biology L. P. Ronse De Craene,1 L. Wanntorp2 1 2

Royal Botanic Garden Edinburgh, Edinburgh, UK Swedish Museum of Natural History, Stockholm, Sweden

Received 29 June 2007; Accepted 9 October 2007; Published online 7 December 2007 Ó Springer-Verlag 2007

Summary. The structure and anatomy of mature flowers of four species of Meliosma is investigated using scanning electron and light microscopy. The vasculature of the flower, including the structure of the gynoecium, is described in detail. The mechanism of stamen maturation and pollen release is illustrated and discussed. The existence of an explosive pollination mechanism is questioned for at least part of the species. Flowers are proterandrous and fertile stamens are kept spatially separate from the style by a ring of large staminodes. Anthers are disporangiate by the loss of the adaxial pollen sacs. During maturation the filament bends progressively outwards and releases the pollen on the extension of the connective that acts as a secondary pollen presentation system. The nectary has five appendages topped with stomata secreting abundant nectar. The relationships of Sabiaceae are discussed relative to other early diverging eudicots. The significance of Sabiaceae as an isolated clade is highlighted, although some features point to a link with Menispermaceae. Keywords: Meliosma; Sabia; Sabiaceae; early diverging eudicots; disporangiate anthers; floral anatomy; staminodes; nectary; pollination

Introduction The Sabiaceae is a small family of three genera Sabia Colebr., Ophiocaryon Endl. and Meliosma Bl. distributed in Eastern and South Eastern Asia and tropical Central and South America. Meliosma with about 25–70 species has the widest distribution occurring both in Asia and America, while Sabia with about 19–50 species is restricted to Asia, and Ophiocaryon with about 7 species is only found in tropical South America (Chen 1943, van Beusekom 1971, Barneby 1972, Kubitzki 2007). Occasionally two separate families Sabiaceae and Meliosmaceae have been considered (e.g. Dahlgren 1981, Takhtajan 1997), although a unified Sabiaceae is to be preferred (e.g. Warburg 1895, Cronquist 1981, Stevens 2007). Earlier classifications placed Sabiaceae either in the Sapindales (e.g. Bentham and Hooker 1862, Dahlgren 1981, Takhtajan 1997), or in the Ranunculales close to Menispermaceae (e.g. Warburg 1895, Cronquist 1981). However, all recent phylogenetic studies based on molecular

Correspondence: Louis P. Ronse De Craene, Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK e-mail: [email protected]

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L. P. Ronse De Craene, L. Wanntorp: Floral anatomy and pollination mechanism in Meliosma

data have placed the family in the early diverging eudicots, but uncertainties remain about its position relative to Proteales and Buxales, or even core eudicots (e.g. Hilu et al. 2003; Soltis et al. 2003, 2005; Furness et al. 2007; Worberg et al. 2007). Wanntorp and Ronse De Craene (2007) investigated the floral development of selected species of Meliosma and found that the pentamerous flowers of Sabiaceae have a unique origin with a spiral initiation throughout, adding support to the hypothesis that pentamery has arisen independently in the family. The flowers of Meliosma are deceivingly complex (Wanntorp and Ronse De Craene 2007). They consist of four to five small sepals, five petals of two different sizes, three staminodes, two fertile stamens, and a superior, bicarpellate ovary. The staminodes are situated opposite the large petals and are basally adnate to them. The stamens are dorsally fused with a small petal. Stamens and staminodes are arranged in a closely coherent unit. Anthers consist of a broad basal platform, in some species extending into a crenulate rim, and bear two globular pollen sacs in an apical-adaxial position. The platform goes over into a narrow flattened filament. Staminodes form pouches in which the globular pollen sacs fit tightly when in bud. Two of the staminodes are asymmetrically built because only one pouch is developed, and the odd one has two pouches. The four pollen sacs fit with these four pouches. The staminodes form a tightly connected rim encircling the style. The gynoecium consists of two fused carpels with two connivent, occasionally twisted styles. The base of the ovary is surrounded by a conspicuous nectary with five prominent appendages alternating with the stamens and staminodes. A floral diagram illustrating the arrangement of floral parts is given in Wanntorp and Ronse de Craene (2007). Descriptions of the morphology of the flowers of Meliosma often lack detail and are inaccurate (e.g., Gagnepain 1950, see Discussion in Wanntorp and Ronse De Craene 2007). Little is known about the pollination of the tiny flowers and almost nothing is known regarding the anatomy

of the flower. Warburg (1895) and van Beusekom (1971) argue that the flowers of Meliosma have an explosive pollination mechanism, whereas the stamens are held under tension by the staminodial appendages. In this study we analyze the floral anatomy and the mature morphology of selected species of Meliosma to understand the internal structure of the flower and clarify the pollination mechanism. Comparison is made with the flower of the sister genus Sabia. Knowledge of the floral morphology of families of the early diverging eudicots becomes increasingly important to understand the floral evolution of the angiosperms. This paper aims to contribute to that goal.

Materials and methods Flower buds of four species of Meliosma were used: M. veitchiorum Hemsl. (accession number 19521006), M. dilleniifolia (Wall.) Wall. aff. ssp. tenuis (Maxim.) Beus. (accession number 19632056; M. dilleniifolia (Wall.) Wall. ssp. cuneifolia (Franch.) Beus. (syn. M. cuneifolia Franch., also used by Wanntorp and Ronse De Craene 2007: accession number 19381038) in cultivation at the Royal Botanic Garden Edinburgh (RBGE), and M. pinnata (Roxb.) Walp. ssp. arnottiana (Walp.) Beus. var. oldhamii (Maxim.) Beus. (syn. M. oldhamii Maxim.) from Kyoto Botanical Garden (Japan). Floral buds were collected, fixed in FAA (5% acetic acid, 5% formaldehyde, 90% ethanol 70%), and subsequently stored in 70% alcohol. Additional observations were made on flowering trees of M. veitchiorum and M. alba (Schlechtend.) Walp. (syn. M. beaniana Rehd. & Wils.: accession number: 19081007) cultivated at RBGE. Meliosma veitchiorum and M. alba belong to subgenus Kingsboroughia, while M. dilleniifolia and M. pinnata belong to subgenus Meliosma. Buds and mature flowers were dissected and prepared using a Wild MZ8 stereomicroscope (Leica, Wetzlar, Germany), dehydrated in an ethanol–acetone series, and critical point dried with a K850 Critical Point dryer (Emitech Ltd, Ashford, Kent, UK). The dried material was later coated with platinum using an Emitech K575X sputter coater (Emitech Ltd, Ashford, Kent, UK) and examined with a Supra 55VP scanning electron microscope (LEO Electron Microscopy Ltd, Cambridge, UK). Reference material (in ethanol) (831 Led, 832 Led, 833 Led, 876 Led) is kept at RBGE.

L. P. Ronse De Craene, L. Wanntorp: Floral anatomy and pollination mechanism in Meliosma For light microscopy flower buds were embedded in Kulzer’s Technovit (2-hydroxyethyl methacrylate), as described in Igersheim and Cichocki (1996) and sectioned with a Leitz Minot 1212 rotary microtome fitted with metal blade. The sections (about 8 l thick) were stained with ruthenium red and toluidine blue and enclosed in DMX.

Results Floral anatomy. Floral anatomy was investigated in flower buds of Meliosma veitchiorum, M. pinnata, and M. dilleniifolia ssp. cuneifolia. No separate descriptions are given for individual species as anatomy was generally found to be similar. A closed vascular system is found at the base of the flower. Traces for sepals and bracts arise at different levels corresponding to their initiation sequence. The five sepals are supplied by a single vascular trace that divides into one median and two laterals higher in the sepal (Fig. 1). Five common stamen–petal traces are given off at a higher level following the departure of sepal traces (Fig. 2). Stamens/staminodes and the corresponding petals are detached as common organs and the vascular bundles branch off into the respective organs (Figs. 3, 4). The division of bundles to the stamens occurs below that of the staminodes. At this level a nectary is visible as small-celled tissue and two traces diverge from the central stele (Fig. 4, arrows). The gynoecium is delimited from the nectary and the two traces differentiate as the two dorsal bundles of the carpels (Figs. 4, 5). While the locules are visible the central vascular tissue becomes reorganized in two areas, each becoming the ventral traces for the respective ovules of each carpel by halving (Figs. 5, 6, 12). The ventral traces are used up in supplying the ovules. At the top of the ovary the dorsals fade out and no traces run into the styles. Ovules are initially inserted parallelly (only one of a pair visible in Fig. 10) but in older buds they become superposed and a septum separates the two locules (Figs. 11–13, 15). The ovules fill the ovarian cavity completely. The placenta is covered with darkly staining secretory trichomes (Fig. 13) and secretion extends along the whole stylar canal (Fig. 16). In M. pinnata and M. dilleniifolia the ovules have a single integument (Figs. 11, 12, 15, 16). In M. veitchiorum

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two integuments are formed as a rim around the nucellus (Figs. 6, 14, 17). We occasionally found that the outer integument is incompletely developed, suggesting that the single integument is the inner one in M. pinnata and M. dilleniifolia. The styles extend beyond the ring of staminodes (Figs. 8, 9, 18). Styles are weakly to strongly appressed but not fused (Figs. 9, 18, 39–42). In M. pinnata and M. dilleniifolia the two styles are erect and terminate in a common slit-like stigmatic area (Figs. 9, 39, 40, 42). Styles are not closely appressed to each other and are often intertwined in M. veitchiorum (Fig. 27). No vascular tissue runs in the styles but the two stylar canals are filled with a secretion (Fig. 18). At the top of the styles the stylar canals open adaxially into a broad slit. Anther development has been described in Wanntorp and Ronse De Craene (2007). Ovule development corresponds with microsporogenesis (Fig. 25). In young anthers the anther wall is composed of an epidermis, an endothecium which is one cell thick, a few intermediate layers, and an inner secretory tapetum layer of the secretory type (Figs. 19, 20). In older anthers the tapetum layer is partly resolved and the endodermis shows tangential thickenings (Figs. 21–23). The ovary wall, as well as the anthers, contains cells with a broad prismatic calcium oxalate crystal. In the anthers these are mainly situated in the area of the vascular bundle (Figs. 23, 24). By disintegration of the anther wall, the crystals become intermingled with the pollen. Pollen grains are tricolporate, about 15 l in size, and with a reticulate exine. Flowering process. Flowers are proterandrous. There is a difference to the extent of development of the style between different species. In M. veitchiorum and M. pinnata the styles grow between the tightly connivent staminodes before the buds opens (Figs. 18, 27). In M. dilleniifolia ssp. cuneifolia the development of the style lags behind and the closely interconnected styles emerge when the anthers are already open (Figs. 28, 30, 36). In young flower buds the staminodes surround the young styles in a coherent unit and the young anthers fit in adaxial folds formed by the staminodes (Figs. 9, 27, 36). At this stage the filaments are abruptly bent inwards in the middle

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b Figs. 1–14. Transverse and longitudinal sections of the flower of Meliosma. 1, 7, 8, 10–13 M. dilleniifolia ssp. cuneifolia; 2–6, 9, 14 M. veitchiorum. 1 TS at base of flower with departure of traces to each sepal (arrows). 2, 3 Successive TS with departure of common petal–stamen traces (arrows). 4 Division of stamen petal traces and separation of respective organs. Note nectary and departure of two dorsals (arrows) from the central stele. 5 TS through the upper part of the nectary. 6 TS through the middle of the ovary with ovule attachment. 7 TS through the upper part of the ovary. 8 TS through the base of the style. Note the connected staminodes. 9 TS through the stylar and anther regions. 10 Young ovary showing one of the developing ovules. 11 Section of older ovary showing two ovules within a locule. 12 TS in the lower part of the ovary showing two ovules and the nectary. 13 TS through the middle of the ovary with placental tissue. The arrow points to secretory trichomes. 14 TS of one locule showing an ovule with two integuments and attachment to the placenta. 1–3, 5–9 Bar 50 lm, 4 12, 13 = 20 lm; 10, 11 = 100 lm. Af fertile stamen, As sterile stamen, D dorsal trace, Ii inner integument, N nectary, Nu, nucellus, Oi outer integument, Ow ovary wall, P petal or petal trace, S sepal, St style, V ventral trace. Asterisks point to the adaxial side of the flower

and the anthers are hidden from view (Fig. 27). One of the three staminodes is symmetrically developed and encapsulates one pollen sac of each anther; the two other staminodes have only a single lobe that encloses the other pollen sac (Figs. 6, 8, 26, 36). In this way the androecium forms a tightly closed dome covering disc and ovary. When the flowers open, the style protrudes between the staminodes before the stamens are clearly visible. By pressing on the filament with a needle, the anthers pop out of the pouch formed by the staminodes (Figs. 27–30). When the flower expands, the filaments bend outwards and the anthers become detached from the tight grip of the staminodes. This is a progressive process in M. veitchiorum and M. alba, as we could not see the explosive mechanism described by van Beusekom (1971) and Warburg (1895). In M. dilleniifolia we often found fewer stamens in opened flowers (Figs. 28, 30), suggesting that they drop off at an early stage, possibly by an explosive mechanism. While the filaments curve outwards the pollen sacs dehisce by a slit situated on the inner surface (Figs. 27, 28, 30, 34, 35). The single pollen sacs open inward out; the anther wall curves outwards and exposes the pollen grains that are collected in clumps on the broad connective expansion (Figs. 29, 34, 35). This broad dish-like area differs in shape between different species, being shallow and extending as flaps next to the pollen sacs in M. veitchiorum (Figs. 9, 27), and forming two ventral auricles in M. dilleniifolia (Figs. 31–33) and M. pinnata (Fig. 34). The sticky pollen remains in clumps on

the protuberance for the insect visitor to collect (Figs. 29, 34). When pollen is released the anthers continue their outward curve (Fig. 30). Soon after pollen release the stamens and staminodes drop off with the petals. The pollination mechanism might explain the heteromorphy of the petals; the broad erect petals enclose the bud and hold the staminodes erect (Figs. 27, 28), while the smaller often bifid petals do allow for the filament to curve outwards (Figs. 32, 33). After the flower has dropped its petals and stamens the ovary continues its development sheathed by the nectary. The ovary wall is covered with uniseriate multicellular trichomes (Fig. 44). The nectary in Meliosma is a broad disc surrounding the superior ovary. There is no vascular tissue but the secretory cells are small with large nuclei (Figs. 4, 12, 18, 25, 38). At maturity the nectary is either developed in the shape of a tire or a buoy with weak crenellations (Fig. 41), or it resembles a crown bearing five prominent appendages topped with one to three stomata (Figs. 39, 40, 43). Both types were observed in M. dilleniifolia (Figs. 40, 41), while in the other species only the crenulate disk was found. Abundant secretion occurs through these distal stomata (Figs. 45, 46). The appendages are not equidistant, but four are grouped in pairs, while the odd one is situated at the other end of the disc (Figs. 40, 43). The arrangement of appendages corresponds with the insertion of the stamens—the pairs are close to the fertile stamen in the median plane of the flower. As the staminodes tightly

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b Figs. 15–26. Transverse and longitudinal sections of the flower of Meliosma. 15, 16, 18 M. pinnata; 17, 19–26 M. veitchiorum. 15 LS showing two superposed ovules. In the upper ovule an embryo sac is visible (arrow). 16 TS through locule. Note the single integument and secretory hairs on the placenta (arrow). 17 TS with detail of ovule with two integuments. 18 LS through young flower. Note the style filled with secretion reaching into the ovary (arrow). 19 LS of anther at meiosis. 20 LS of anther wall. 21 LS of mature anther. 22 TS of anther wall. 23 TS through the middle of mature anther. Arrow points to the position of calcium oxalate crystals. 24 Detail of cells in the connective area. 25 LS of part of the flower showing two superposed ovules. 26 Adaxial view of staminode with two interconnected petals. 18, Bar = 50 lm, Figs. 19, 21, 23 = 10 lm, 15–17, 20, 22, 24 = 20 lm, 26 = 200 lm. Af fertile stamen, As sterile stamen, En endodermis, Ep epidermis, Ii inner integument, N nectary, Nu, nucellus, Oi outer integument, P petal, Ta tapetum, V ventral trace

cover the nectary as a lid (Figs. 6–8,38), nectar is produced and accumulates between the broad disc lobes. Access to nectar is only possible through slits between the staminodial lobes—this induces the pollinating insects to wander close to the anther tissue. Discussion Anther dehiscence. The broad dish-like appendage of the anthers has been described as an expanded connective by various authors (e.g. Baillon 1874, Warburg 1895, Takhtajan 1997). However, the fact that the anthers are disporangiate has been overlooked by most authors (except for brief mentions in the literature (e.g. Warburg 1895, Baillon 1874; Chen 1943, Kubitzki 2007). Sabiaceae were left out in the global review of anthers of Endress and Stumpf (1990). Sabia shares the disporangiate anthers with Meliosma (Ronse De Craene unpubl. obs.; van de Water 1980). One tricky question is whether the adaxial or the abaxial pair of pollen sacs is reduced. Developmentally it is not possible to observe any traces of the second set of pollen sacs (Wanntorp and Ronse De Craene 2007). The normal dehiscence pattern for tetrasporangiate anthers in most angiosperms is laterally with the lobes curving towards the exterior (Fig. 47A). When dehiscing, the anther walls of Meliosma curve inward out, exposing the pollen on the broad connective. A plausible explanation for this pattern is that the adaxial (ventral) pollen sacs have been lost and that the broadened connective has pushed the two remaining pollen sacs towards each other (Fig. 47B). In the case of

tetrasporangiate anthers opening in a similar fashion one would expect the abaxial pollen sacs to curve out in the same way as in Meliosma. Van de Water (1980) described a similar dehiscence pattern for Sabia. Sabia has a broad connective; the anthers open along the connection with the connective at the adaxial side and the wall turns inside out. When fully opened the anthers give the impression of being extrorse. Disporangiate anthers are fairly common in basal angiosperms (e.g. Lauraceae, Monimiaceae, Hernandiaceae) and their location is difficult to assess. They have been correlated with a specialized floral biology such as a secondary pollen presentation on the gynoecium or a precise deposition of pollen linked to the dehiscence of the thecae by narrow slits (Endress and Stumpf 1990). In the case of Meliosma the anthers are set widely apart and separated by the broad staminodes; pollen is not deposited on the gynoecium, but on the extended connective appendage. It appears that Meliosma shows a unique pattern of secondary pollen presentation by accumulating pollen on the extensive connective-dish. The gradual movement of the anthers exposes the dish to visiting insects. However, more experimental work needs to be carried out in other species to verify the statement of van Beusekom whether an explosive mechanism can be invoked. In that case the broad connective can act as a container catapulting the pollen on the insect. Zhilin (1981) suggested that the explosive mechanism is restricted to subgenus Meliosma to which M. dilleniifolia and M. pinnata belongs. Subgenus Kingsboroughia containing M. veitchiorum and M. alba is said to lack the explosive mechanism

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b Figs. 27–38. Anthesis and anatomy of staminodes in Meliosma. 27, 29, 38 M. veitchiorum; 28, 30–33, 35–37: M. dilleniifolia ssp. cuneifolia; 27, 34: M. pinnata. 27. Lateral view of flower at anthesis, two petals and two staminodes removed. The right anther starts dehiscing (arrow). 28 Apical view of flower at the onset of dehiscence. 29 Pollen grains on the exposed anther wall. 30 Flower with recurved filament. 31–33 adaxial, lateral, and abaxial views of young anthers and their associated petals. 34 Dehisced anther with pollen grains on the basal appendage. 35 TS of dehisced anther with pollen grains and the connective. 36 TS of staminodes surrounding the style. 37 TS of two connected staminodes. 38 LS of nectary partly covered by staminodial appendage. 35, 37, Bar = 20 lm, 36, 38 = 50 lm, 34 = 100 lm, 30–33 = 200 lm, 29–31 = 500 lm, 28 = 1 mm. Af fertile stamen, As sterile stamen, N nectary, P petal. Asterisks point to the adaxial side of the flower

and the flowers remain open for a longer time. This corresponds with our observations. Floral anatomy. The ovary is syncarpous but the styles are postgenitally united. The ovules are initially positioned side by side in each locule but they become superposed by the restricted space for their further development. The embryology of Sabiaceae has been briefly described by Mauritzon (1936), Raju (1952), and Sharanina (1996). They mention that the ovules are unitegmic and have no micropyle. We report the presence of two integuments in Meliosma veitchiorum, contrary to descriptions of unitegmy in textbooks obviously taken over from earlier studies (e.g. Cronquist 1981, Takhtajan 1997). However, the other species studied were unitegmic. Endress and Igersheim (1999) briefly described the gynoecium structure of Sabia and reported the presence of mucilage in style and ovary. We report the presence of intraovarian secretory trichomes situated on the placenta. These trichomes produce ovarian mucilage which is also found in the pollentransmitting tract of the style and play an obvious role in facilitating pollen tube growth (Rudall et al. 1998). Secretory intra-ovarian trichomes are rare in the eudicots, but are found more regularly in the monocots and some basal angiosperms. There is no discussion on crystals in anthers, but Raju (1952) mentions crystals in the ovary wall cells. We found that calcium oxalate crystals were often present in open anthers mixed with pollen grains. D’Arcy et al. (1996) studied the presence of calcium oxalate in anthers of different families, not including Sabiaceae. Contrary to species where calcium oxalate occurs in packages at the level of anther dehiscence, in Meliosma

calcium oxalate occurs scattered in idioblasts around the connective area. D’Arcy et al. (1996) discussed several hypotheses for the presence of calcium oxalate packages, including a role in anther dehiscence, as a metabolic sink, discouragement of herbivores or as a food source. It is possible that the association of calcium oxalate with pollen in Meliosma is accidental without the significance of the packages associated with specialized flowers found in the asterids. The apical stomata on the nectary have been overlooked by most authors, who describe disc and glands, and nectaries as separate entities (e.g. Chen 1943). The whole disc-like structure with appendages needs to be described as a nectary, as it contains densely staining tissue responsible for nectar secretion. Chen (1943) and van de Water (1980) observed a similar variation in the nectary of Sabia as in Meliosma in the extent of development of the appendages, as well as presence of glandular tissue on top of the appendages. Systematic considerations. The flower morphology of Meliosma is reminiscent of Sabia in many ways and supports the recognition of a single family (Chen 1943, van de Water 1980, Kubitzki 2007, Wanntorp and Ronse De Craene 2007). Sabia and Meliosma share several floral characters including the filaments adhering to the base of the petals, disporangiate anthers with a similar pollen morphology, the five-lobed nectary, and similar ovary and ovules. The connective in Sabia is thick, although not developed to the extent found in Meliosma. A comparative study including the polarization of character evolution will only be possible by including the third genus of Sabiaceae,

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Figs. 39–46. Nectary and gynoecium in Meliosma. 39, 42, 43 M. pinnata; 40–41 M. dilleniifolia ssp. cuneifolia; 44 M. veitchiorum; 45–46 M. dilleniifolia ssp. aff. tenuis. 39 Lateral view of flower without petals or stamens. 40 Apical view of ovary with nectary and appendages. 41 Apical view of ovary with nectary. Note the small, almost undeveloped appendages. 42 Stigmatic hole. 43 View of nectary from above—ovary removed. 44 Detail of trichomes on the ovary wall. 45 Nectary appendage with one of the apical stomata visible. 46 Nectary appendage covered with secretion. 42, 44, Bar = 20 lm, 45, 46 = 50 lm, 43 = 100 lm, 39 = 200 lm, 40, 41 = 500 lm. Asterisks point to the adaxial side of the flower

Ophiocaryon, for which material is currently not available. Affinities of Sabiaceae are still unclear. Table 1 compares Sabiaceae with other potentially related families in a number of characters. A closer link with Menispermaceae (cf. Cronquist 1981) cannot be excluded based on pollen, embryological and ovary characters. Some Meni-

spermaceae share dithecal anthers with Sabiaceae (Endress and Stumpf 1990) but details of their arrangement are not known. Interestingly some Menispermaceae and Ranunculaceae have unitegmic ovules with a rudimentary outer integument (reported in Endress and Igersheim 1999). Sabiaceae share the presence of hemianatropous ovules with Menispermaceae and some


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Fig. 47. Diagrammatic presentation of anther dehiscence of common tetrasporangiate anthers (A) and disporangiate anthers of Sabiaceae (B). The adaxial side below, the abaxial side up Table 1.

Comparison of Sabiaceae with other early diverging eudicots on a number of selected floral characters

Characters

Sabiaceae

Common stamen– + petal (tepal) trace Carpel number 2 Nectary position Intrastaminal disc Oxalate crystals in + ovary wall Ovary syncarpous + Stigma shape Restricted to carpel tip Bundles per carpel 3 Dorsal bundles Not reaching style Secretory hairs in + ovary Ovules two per + carpel and superposed Ovules bitegmic +/– Ovule structure Hemianatropous Anthers disporangiate Endothecium Presence of endoapertures

Menispermaceae Proteaceae

Buxaceae

Trochodendraceae

?

+

–

+

(1)2–6 Petal

4/6-17 Ovary

+

1 2–3 Intrastaminal disc Pistillode or lobes ovary + –

– Restricted to carpel tip 5 ?

– Restricted to carpel tip 3–5 Reaching stigma

+ Decurrent

+ Decurrent 5 Reaching stigma

–

–

3 Reaching stigma –a

+

+/–

+

–

–

–

+ Anatropous

+

+ (–) + + Hemianatropous Ortho-, Anatropous hemianatropous +/– – –

One-layered

?

One-layered

One-layered

+

+/–

–

One-twolayered +

–

–

Data from Endress (1995), Endress and Stumpf (1990, 1991), Endress and Igersheim (1999), Furness et al. (2007), Nast and Bailey (1945), von Balthazar and Endress (2002), Wang et al. (2006), and this study a Pachysandra has non-secretory hairs at the transition of the ventral slit and the placenta (Endress and Igersheim 1999)

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Proteaceae (Endress and Igersheim 1999). Pollen grains are of a generalized type (tricolporate, subprolate and reticulate, with endoapertures: Erdtman 1952; Furness et al. 2007). Sabiaceae share endoapertures only with two other families of early-diverging eudicots, Buxaceae and Menispermaceae. Recent molecular evidence (Worberg et al. 2007) supports the monophyly of Sabiaceae and places the family as the second branch in the basal eudicot grade with inconclusive support. This places the family in an isolated position in relation to the other early diverging eudicots as might be expected from the unusual floral morphology which evolved clearly separately with little evidence of a close association with other families (Wanntorp and Ronse De Craene 2007). We thank Frieda Christie and Dr. Chris Jeffree for assistance with the SEM. We are also grateful to Dr. Toru Tokuoka for collecting flower buds of Meliosma pinnata. Travel for LW to RBGE was possible through SYNTHESYS grant GB-TAF 1626. Helpful comments by Dmitry Sokoloff and an anonymous reviewer are gratefully acknowledged.

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