AOBPreview originally published online on September 27, 2004
Annals of Botany 2004 94(5):741-751; doi:10.1093/aob/mch199
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Annals of Botany 94/5, © Annals of Botany Company 2004; all rights reserved
Floral Development of Berberidopsis corallina: a Crucial Link in the Evolution of Flowers in the Core Eudicots
Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK
* E-mail l.ronsedecraene{at}rbge.org.uk
Received: 7 April 2004 Returned for revision: 9 June 2004 Accepted: 4 August 2004 Published electronically: 27 September 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and Aims On the basis of molecular evidence Berberidopsidaceae have been linked with Aextoxicaceae in an order Berberidopsidales at the base of the core Eudicots. The floral development of Berberidopsis is central to the understanding of the evolution of floral configurations at the transition of the basal Eudicots to the core Eudicots. It lies at the transition of trimerous or dimerous, simplified apetalous forms into pentamerous, petaliferous flowers.
• Methods The floral ontogeny of Berberidopsis was studied with a scanning electron microscope.
• Key Results Flowers are grouped in terminal racemes with variable development. The relationship between the number of tepals, stamens and carpels is more or less fixed and floral initiation follows a strict 2/5 phyllotaxis. Two bracteoles, 12 tepals, eight stamens and three carpels are initiated in a regular sequence. The number of stamens can be increased by a doubling of stamen positions.
• Conclusions The floral ontogeny of Berberidopsis provides support for the shift in floral bauplan from the basal Eudicots to the core Eudicots as a transition of a spiral flower with a 2/5 phyllotaxis to pentamerous flowers with two perianth whorls, two stamen whorls and a single carpel whorl. The differentiation of sepals and petals from bracteotepals is discussed and a comparison is made with other Eudicots with a similar configuration and development. Depending on the resolution of the relationships among the basalmost core Eudicots it is suggested that Berberidopsis either represents a critical stage in the evolution of pentamerous flowers of major clades of Eudicots, or has a floral prototype that may be at the base of evolution of flowers of other core Eudicots. The distribution of a floral Bauplan in other clades of Eudicots similar to Berberidopsidales is discussed.
Key words: Aextoxicon, Berberidopsidales, Berberidopsis, core Eudicots, Streptothamnus, bracteotepals, floral development, petals, phylogeny, phyllotaxis, scanning electron microscope
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Berberidopsis Hook. f. is a small genus with two disjunct species, B. beckleri (F.v.M.) Veldk. in Australia and B. corallina Hook. f. in Chile. Berberidopsis beckleri had originally been described by von Mueller (1862)
as Streptothamnus beckleri together with another species S. moorei F. v. M. The genus description is based on B. corallina which is known since the middle of the nineteenth century and has been cultivated for it scarlet flowers arising on twining stems. Berberidopsis was initially related to Berberidaceae and Lardizabalaceae (Hooker, 1862; Baillon, 1872). Baillon linked Berberidopsis with Erythrospermum Lamk., another genus considered to belong to Berberidaceae at that time. Both genera were transferred to Flacourtiaceae by Warburg (1893) and later by Gilg (1925) on the basis of a number of morphological characters, such as a trimerous ovary with parietal placentation and anthers with longitudinal dehiscence. Warburg maintained Berberidopsis and Erythrospermum in tribe Erythrospermeae, while Gilg placed both genera in tribe Oncobeae. The placement of Berberidopsis in Flacourtiaceae has been maintained in all premolecular systems of classification, although the isolated position of the genus in Flacourtiaceae was recognized and discussed on the basis of pollen (Keating, 1975; Van Heel, 1984) and wood anatomy (Miller, 1975; Baas, 1984). Compared with Flacourtiaceae, wood of Berberidopsis and its associated genus Streptothamnus (see below) is more primitive. Miller thought the wood of Berberidopsis was more similar to that of Dilleniaceae and Theaceae than Flacourtiaceae and suggested the creation of a family of its own. Van Heel (1977, 1979, 1984) studied the flower, fruit and seed anatomy of Berberidopsis and found that it differed in several features from Flacourtiaceae, such as the insertion of the ovules, the small embryo, endotestal seeds, a conspicuous notched cuticular layer and no differentiation of inner integuments. Van Heel (1984) also suggested that similarities with Erythrospermum are superficial and that the seed anatomy of the latter is more like other Flacourtiaceae. Hutchinson (1967) informally changed the name Erythrospermeae into Berberidopsideae, but this was validly published by Veldkamp only in 1984 (Veldkamp, 1984).
A study of seed anatomy, pollen and wood by van Heel (1984) and Baas (1984) demonstrated the close link between Streptothamnus beckleri and Berberidopsis corallina. Streptothamnus beckleri was formally transferred to Berberidopsis by Veldkamp (1984). The three species were grouped together into a tribe Berberidopsideae of Flacourtiaceae (Veldkamp, 1984) and later as a family Berberidopsidaceae by Takhtajan (1985). Although Streptothamnus moorei is dissimilar from Berberidopsis in several respects (e.g. pollen: Keating, 1975; Van Heel, 1984; wood anatomy: Baas, 1984), their association has not been questioned.
Berberidopsis was first linked with Aextoxicon on molecular evidence by Nandi et al. (1998) and this was supported by evidence from several genes (Savolainen et al., 2000a, b; Soltis et al., 2000, 2003). Aextoxicon and Berberidopsis had traditionally been placed widely apart. Aextoxicon was successively placed in Elaeagnaceae (Baillon, 1870), Euphorbiaceae (Pax, 1896) or in a family Aextoxicaceae (Engler and Gilg, 1919; Cronquist, 1981). The genus has been either considered to belong to Euphorbiales or Celastrales.
The association of Berberidopsis with Aextoxicon was formally recognized as an order Berberidopsidales by Savolainen et al. (2000a) and Soltis et al. (2000), and has since then been supported by other molecular evidence (Angiosperm Phylogeny Group, 2003; Hilu et al., 2003; Soltis et al., 2003). However, the relationship of Berberidopsidales to other core Eudicots is still uncertain (Fig. 1). Nandi et al. (1998) associated both genera with Asterids; Savolainen et al. (2000a) placed both families as sister to Caryophyllales with weak support, while Soltis et al. (2000) placed the clade as sister to Rosids and Saxifragales also with weak support. Hilu et al. (2003) and Soltis et al. (2003) found little resolution between the basal clades Berberidopsidales, Santalales, Asterids and Caryophyllales. Figure 1 gives an overview of current differences in the placement of Berberidopsidales.
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Flowers and vegetative parts of Aextoxicon look highly different from Berberidopsis. Flowers of Berberidopsis corallina are not differentiated into sepals and petals, but there is a gradual transition from smaller outer tepals to inner brightly coloured tepals. The androecium consists of a ring of stamens and there are three carpels with parietal placentation. The stamens are surrounded by a persistent receptacular nectary.
In contrast, Aextoxicon is described as having pentamerous unisexual flowers; staminate flowers have a well differentiated calyx and corolla, a haplostemonous androecium alternating with staminodial (?) glands and two sterile carpels (Baillon, 1870; Cronquist, 1981; Takhtajan, 1997). The perianth is enclosed in a saccate structure that ruptures irregularly at anthesis. Pistillate flowers have the same perianth but the number of parts is more variable; staminodes are well developed with or without a rudimentary anther. Placentation is parietal with two collateral ovules having an obturator (Baillon, 1870). Carlquist (2003) recently confirmed the close link between Berberidopsis and Aextoxicon on the basis of wood anatomy. The order is well circumscribed on the sharing of numerous primitive characters, rather than synapomorphies.
Very few studies have dealt with the morphology of the flower of Berberidopsis. The only other study dealing with the development of Berberidopsis is by Baillon (1876). However, his observations are highly biased by the assumption of an underlying trimerous groundplan in the flower relating the genus to Berberidaceae. A study of the floral development of Berberidopsis imposes itself, because of the limited knowledge of the floral structure and because Berberidopsis lies at the transition of basal Eudicots to core Eudicots. Most basal Eudicots are dimerous or trimerous, with only occasionally pentamerous types (Sabiaceae, Ranunculaceae) which represent homoplasious trends (Ronse De Craene et al., 2003; Soltis et al., 2003). The basal sister group of other core Eudicots is the Gunnerales with small dimerous flowers (Soltis et al., 2003) and, although this order may be basal to the transition to the common pentamerous, petaliferous flowers of core Eudicots, other taxa remain plausible candidates. The canalization of merosity resulting in the pentamerous condition in the core Eudicots followed the divergence of Gunnerales from the rest of the core Eudicots. However, despite the fact that several possibilities have been presented elsewhere (e.g. Ronse De Craene et al., 2003; Soltis et al., 2003), no substantial evidence exists of the actual transition process. Depending on the availability of a stable molecular phylogeny of the root of the major clades of the core Eudicots (cf. Fig. 1), the information obtained from Berberidopsidales can help in answering whether there is a single or several origins in the evolution of pentamerous, petaliferous flowers, and how the evolutionary transition has occurred. The transition of basal Eudicots to core Eudicots in terms of floral morphology remains a mystery, and a thorough study of the floral development of the Berberidopsidaceae and Aextoxicaceae can give support for understanding the direction of evolution of the flowers of core Eudicots, given the obtainment of a well-supported phylogeny.
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MATERIALS AND METHODS |
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Flowering material of Berberidopsis corallina cultivated at the Royal Botanic Garden Edinburgh (coll. Number 820 Led – 1996.1386 – collected in Chile, Region VIII [Biobío] by Instituto de Investigaciónes Ecológicas Chiloé (IIECH) and Royal Botanic Garden Edinburgh (1996) 660) was collected during the summer of 2002 and spring 2003. Material was immediately fixed in FAA and stored in 70 % alcohol. Buds were dissected with a Leitz Wild MZ8 stereomicroscope, dehydrated in an ethanol–acetone series, and critical point dried with an Emitech K850 Critical point dryer. Material was coated with platinum using an Emitech K575X sputter coater and observed with a Leo 55VP scanning electron microscope.
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RESULTS |
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Berberidopsis corallina is a twining vine with spirally arranged leaves. Flowers emerge on terminal racemes and are subtended by small bracts (Fig. 2). The lowermost flowers are occasionally situated in the axil of vegetative leaves. Inflorescences often have variable growth, regularly ending with a larger top flower (Fig. 3A and B), or the inflorescence may become vegetative again after producing a number of flowers. One occasionally finds smaller inflorescences at the base of the main inflorescence; these consist of a few to a single flower (Figs 3C and 5G). Lower buds on the inflorescence may develop as vegetative apices.
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Leaf and bract margins, as well as stems, are covered with uniseriate, multicellular hairs. Mature flower buds are situated at the end of a stout pedicel (Figs 2, 5G and 6F). This pedicel may be up to six times the length of the flower. All flowers are subtended by a bract and two bracteoles (Figs 2 and 3). The bract is inserted at the base of the pedicel, while the position of the bracteoles is highly variable. They can be inserted at the base of the pedicel with the bract, at different levels on the pedicel (Fig. 5G), or just below the tepals (Figs 3C and D, 4A and D).
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Mature flowers are scarlet without clear differentiation between bracteoles, sepals or petals (tepals) (Fig. 2). In my material the tepal number was almost constantly 12 (Fig. 8). The inner tepals are longer than the intermediate tepals and outer tepals at maturity (Fig. 2); The five outer tepals range in size from approx. 3 mm long (tepal one) to about 7 mm long (tepal 5); intermediate tepals (from tepal 6 on) to inner tepals (tepals 11 and 12) range in size from 9 to 11 mm.
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Flowers tend to follow a strongly regular developmental pattern. Bracts are initiated acropetally on the racemose inflorescence, or below the terminal flower (Fig. 3A–C). An elliptical primordium is formed in the axil of each bract (Fig. 3A and B). Soon two lateral bracteoles arise in succession, either from left to right (Fig. 3A, B and E) or more rarely from right to left (Figs 3D, F and 4A). The bracts and bracteoles stop growing in early stages and are minute at anthesis (Fig. 2). The sequence of initiation of the tepals is spiral throughout, following a 2/5 phyllotactic pattern. The divergence angle was constant around 135°. The first tepal arises abaxially and is inserted towards the first bracteole (Fig. 3A, B and E). Four other tepals follow in a rapid 2/5 sequence (Figs 3E and F and 4A) forming an outer pentamerous whorl. The sequence continues with five more tepals arising between the five first-formed tepals (Fig. 4B). Two more tepals arise on the centrally expanding apex; tepal 11 is inserted between tepals 6 and 8, opposite tepal 3, and tepal 12 is inserted between tepals 7 and 9 opposite tepal 4 (Figs 4C–G and 5C–F). All tepals show a constant growth and the inner tepals eventually overtop the outer tepals in size (Figs 2 and 6F). When the last tepal has been initiated the floral apex expands as a broadly flattened platform (Fig. 4C–F). Stamen primordia emerge on the periphery in a rapid sequence, almost simultaneously (Fig. 4E–G). The pattern of arrangement of the stamens was found to be conservative. Stamens are more or less positioned opposite the eight inner tepals in a single whorl (Fig. 5D and F). However, older stamens have a different size, and smaller stamens are situated opposite the last-formed tepals (Figs 5C–F and 6A–E). The number of stamens fluctuates between eight (Figs 5D–F and 6C and E), ten or 11 (Figs 5A–C and 6A). The stamens opposite tepals 10–12 are slightly displaced relative to the centre of the tepals, along short parastichial curves (Fig. 5E-curves, D and F and Fig. 6A). The size of the stamens reflects their spiral initiation sequence following the 2/5 sequence of the tepals. The stamens appear to be placed on a low mound (Fig. 4F).
When the number of stamens exceeds eight, some stamens appear split and grouped as pairs or occasionally as triplets (Fig. 5A–C, asterisks, and Fig. 6A). These stamens always alternate with the carpels and are clearly the result of dédoublement, as two or more stamens tend to be laterally connected (Figs 5B and 6A, arrow). Three stamens are situated more or less opposite the three carpels; these are the stamens opposite tepals 10–12. The other stamens are positioned against the flanks of the carpels, the stamen opposite tepal 7 stands isolated, while the other flanks are taken up by two stamens (Figs 5D and F and 8).
The stamen primordia differentiate from globular primordia into elliptic appendages of differing size (Figs 5G and 6A and B). They become progressively rectangular and flattened with a crestlike apical appendage (Fig. 6C–E, G and H). Anther tissue develops on the adaxial and lateral surface of the anther. The apical crest becomes differentiated as an elongated connective appendage; a filament is very short to inexistent (Fig. 6H). At maturity the filaments are basally fused (Figs 6G and 7E).
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Three carpel primordia emerge at the same time as the stamen primordia on the central area of tissue (Figs 4G and 5A and D). The boundaries between individual carpels are inconspicuous or even not discernable, and rapidly a continuous rim with three globular protuberances is formed (Fig. 5A–F). The protuberances differentiate as three carpels by the formation of a central depression; the carpel wall forms three invaginating loops alternating with the carpel primordia (Fig. 6A and B). These invaginations represent placental outgrowths and they extend towards the centre, enclosing the central hole into a triangular slit (Fig. 6B–E). The gynoecium extends upwards as a long saccate primordium overtopping the stamen primordia (Fig. 5G). The three zones alternating with the invaginations extend apically as three lobes that act as a long stylar structure (Figs 6D and 7A and B). Ovules are initiated on the middle of the saccate ovary on each side of the invaginating placenta; eight to ten ovules develop basipetally in two rows ending in a single ovule at the base (Fig. 7A–E). The ovules of each row face away from each other and two integuments are differentiated (Fig. 7D). Ovules are anatropous at maturity (Fig. 7E).
Between the androecium and the inner tepals the receptacle extends into a lobed ring-like nectary (Figs 6D, E and G and 7E). Open nectarostomata are scattered over its surface (Fig. 7F).
Before maturity several flowers drop off below the terminal larger flower. Tepals are similar to leaves in having three main traces; inner tepals only have two or a single trace. After anthesis the perianth and stamens fall off, leaving a fleshy disc around the young fruit. The fruit inflates into a berry. More details of fruit and seed anatomy are given in Van Heel (1977, 1979, 1984).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The floral development of Berberidopsis corallina is highly regular and conservative in number and arrangement of parts, compared with other spiral flowers. The number of stamens and other floral parts is relatively constant, although authors give fluctuating numbers of tepals and stamens for Berberidopsis (e.g. Gilg, 1925
: perianth 9–15, stamens 7–10; Veldkamp, 1984: perianth 13–15, stamens 6–10). These fluctuations may reflect inherent variability, the confusion in identifying bracts, bracteoles and tepals in some flowers, and dédoublement affecting the androecium. Baillon (1876) similarly observed increased numbers but linked this to two trimerous stamen whorls. The basic number of stamens is eight, although Veldkamp counted six to ten stamens for B. corallina and 12 or 13 stamens for B. beckleri. Carpels are constantly three in B. corallina and five in B. beckleri.
Berberidopsis differs from Streptothamnus in several respects (see Keating, 1975; Baas, 1984; Van Heel, 1984; Veldkamp, 1984). These differences include interesting floral morphological features in Streptothamnus, such as cyclic flowers with usually five persistent calyx lobes and five caducous petals, the absence of the persistent extrastaminal disc, four placentae, numerous stamens with long filaments and an inconspicuous connective. The pentamerous construction and presence of petals is reminiscent of Aextoxicon. However, Keating (1975) found the pollen of Streptothamnus moorei to be indistinguishable from Erythrospermum. More studies of the flower of Streptothamnus, as well as a study of the molecular architecture of the genus are essential to understand its position relative to Berberidopsis, Aextoxicon and Flacourtiaceae.
The numbers of carpels (three), stamens (eight) and tepals (13 if one includes one of the bracteoles) are clear Fibonacci numbers (Fig. 8). The sequence of initiation of the flower follows a 2/5 pattern with constant divergence angles. This means that the flower of Berberidopsis shows a predisposition for pentamery. The development up to the five first-formed tepals (Figs 3F and 4A) is not different from sepal initiation in regular pentamerous flowers. Seven tepals and eight stamens follow in a regular sequence, and almost with a regular alternation. At an intermediate stage of development the pattern of initiation is a clear 2/5 with two whorls of tepals (Fig. 4B). The five carpels of B. beckleri complete the pentamerous regularity of the flower.
Floral organs in Berberidopsis arise along a divergence angle approaching the golden divergence angle of 137·5°, which is the ‘golden’ divergence angle. The change in plastochron between successive whorls is almost inexistent and there is no sudden change in primordium size. As such, Berberidopsis is a classic example of a spiral flower. However, the arrangement of organs in alternating groups of five is important and one could indicate that pentamery is incipient in Berberidopsis. The tepals appear in alternating whorls and this may be due to space restrictions and the large diameter of the central flattened apical meristem. There is no obvious break in the initiation of the stamens and carpels.
Could pentamerous flowers of core Eudicots be derived from predecessors such as the flower of Berberidopsis? Evidence for a pivotal position of flower types such as Berberidopsis in the differentiation of pentamerous cyclic flowers with petals and sepals is, on the one hand, linked with the position of Berberidopsis in a phylogenetic framework (Fig. 1) and, on the other, from morphological evidence presented by the flower. The lower branches of the core eudicots currently have little support (e.g. Angiosperm Phylogeny Group, 2003; Hilu et al., 2003; Soltis et al., 2003) and an understanding of the position of Berberidopsidales is crucial for understanding the evolution of floral characters and the solving of the dilemma of sepal and petal origins.
Berberidopsis shows the possibility of a scenario for the differentiation of pentamerous, diplostemonous flowers from acyclic spiral flowers by a progressive reduction in number of parts, and a flattening of the central meristem, linked with differences in size. This transition is not restricted to Berberidopsis, but may have arisen within several clades of the core Eudicots (see below).
When carefully observing the sequence of arrangement of the stamens, it is clear that there is no rigorous alternation of primordia. There is an overlap of positions by the inner organs relative to the outer. Subtle shifts in size of primordia, linked with almost imperceptible changes in plastochron lead to a clear alternation of whorls. For example, stamens 13, 14 and 15 are placed closer to tepals 8, 9 and 10, respectively. Reduction in size of tepals 6–8 could lead to a displacement of stamens 13–15 opposite tepals 1–3. The initiation of ten stamens (linked with replacement of tepals 11 and 12 by stamens) approaches a diplostemonous flower.
The differentiation of sepals and petals is not clear in Berberidopsis; there is rather a progressive differentiation of outer and inner tepals. It is interesting to note that the ‘calyptra’ of Aextoxicon appears to be two-parted (as two fused bracteoles) and that the ‘petals’ are irregular and with progressively smaller sizes (L. P. Ronse De Craene, unpubl. res.), suggesting a homology with the perianth of Berberidopsis. Depending on obtaining adequate material, the floral development of Aextoxicon is to be compared with that of Berberidopsis in the understanding of flower evolution and perianth differentiation within Berberidopsidales.
The question of homology of the petals in the core Eudicots is central to this discussion, as petals can either be derived from tepals by a differentiation of an outer sepaline whorl and an inner petaline whorl, or from stamens by sterilization of anther tissue (see Takhtajan, 1991; Albert et al., 1998; Ronse De Craene and Smets, 2001). This question is currently investigated in the context of evolutionary developmental genetics (e.g. Albert et al., 1998; Ronse De Craene, 2003). However, depending on the position of Berberidopsidales, different interpretations remain plausible. It is interesting to note that in the core Eudicots the same pattern of floral development as in Berberidopsis is occasionally found. Several characteristics of Berberidopsis are encountered in the Dilleniaceae, including the acyclic perianth with differentiation of inner/outer tepals, relatively low carpel numbers, and comparable wood anatomy. In Dillenia five sepals and five petals arise in a spiral, the petals with a shorter plastochron than the sepals. A total of eight inner stamens are initiated before more stamens emerge centrifugally (Endress, 1997). In Hibbertia there is a trend for the petals to arise nearly simultaneously, and this is associated with their smaller size and a shorter plastochron (Tucker and Bernhardt, 2000). However, in Dilleniaceae there have been several phases of subsequent increases and reductions (Endress, 1997; Tucker and Bernhardt, 2000). The floral development of several Camellioideae (Theaceae) up to the androecium is highly similar to Berberidopsis (Tsou, 1998). Organs arise in a spiral sequence with a 2/5 divergence in each category of organs. There is much similarity in some Camellia with up to 12 perianth parts and a differentiation in size of inner and outer perianth parts (e.g. Tsou, 1998: fig. 14). Subtle changes in plastochron lead to alternation of sepals and petals and the attainment of alternating pentamerous whorls of sepals and petals (Erbar, 1986; Tsou, 1998). Similar patterns are found in Actinidiaceae and Lecythidaceae (Endress, 1994; L. P. Ronse De Craene, unpubl. res.). Other cases include Clusiaceae (Leins and Erbar, 1991; Gustafsson, 2000), Bonnetiaceae (Dickison and Weitzman, 1998), Achariaceae (former Flacourtiaceae: Bernhard and Endress, 1999) in Malpighiales, and Paeoniaceae (Hiepko, 1964; Leins and Erbar, 1991) in Saxifragales. In most cases these patterns of sequential initiation are associated with a secondary centrifugal stamen increase.
It is important to understand how the pattern of differentiation of sepals and petals has evolved in the core Eudicots, petals having either a strictly staminodial origin, or having arisen as a derivation from bracteopetals. Multiple origins linked with a secondary loss or developmental changes through genetic mutations can have affected the nature of the petals, and this remains an exciting topic to be explored.
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ACKNOWLEDGEMENTS |
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I thank Frieda Christie for technical assistance with the scanning electron microscope and the horticultural staff of RBGE for help with collecting the specimens. The Royal Botanic Garden of Edinburgh is acknowledged for a photograph of Berberidopsis corallina taken by Debbie White and growing at RBGE (© RBG Edinburgh 19687146b).
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LITERATURE CITED |
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