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First published online October 8, 2008; doi:10.3732/ajb.0800199 American Journal of Botany 95: 1349-1365 (2008) © 2008 Botanical Society of America, Inc. |
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Anatomy and Morphology |
2 Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK 3 Department of Botany, Natural History Museum, London, SW7 5BD, UK
Received for publication 17 June 2008. Accepted for publication 11 September 2008.
ABSTRACT
Duparquetia orchidacea (Caesalpinioideae-Cassieae-Duparquetiinae) is a monotypic liana from tropical West Africa. Its highly unusual, zygomorphic flowers, the unique pollen morphology, and the lack of vestured pits in the wood correspond with previous phylogenetic studies that resolved the position of the species to an isolated position among the early-branching Leguminosae. Here we present a detailed analysis of floral morphology and development to clarify open questions of its floral organization. We provide new data that can be useful in clarifying phylogenetic relationships among early branching Leguminosae and improve our understanding of floral evolution in this large and important plant family. For comparison, we also present developmental data for other Fabales. Our analysis reveals some unusual and in parts unique developmental patterns, such as strict acropetal organ formation, loss and suppression of floral organs, and early petal enlargement. We interpret alternating left-right symmetries in floral development as clues to a spiral organ formation in ancestral taxa. Early asymmetry of the young carpel helps to interpret enantiostyly of other Leguminosae as an example of imprinted shape. Finally, we show that cochlear-descending petal aestivation in Duparquetia and in Papilionoideae is based on different ontogenetic patterns and therefore is most probably nonhomologous.
Key Words: Caesalpinioideae • Duparquetia • enantiostyly • evolution • Fabaceae • Fabales • floral development • flower • Leguminosae • morphology
Despite several attempts to clarify relationships within the plant family Leguminosae (the bean or pea family), relationships among earliest-branching taxa are still not fully resolved and only partially understood (Fig. 1) (Lavin et al., 2005
; Bruneau et al., 2008). The West African monospecific genus Duparquetia apparently is a key taxon for resolving the deep nodes of the legumes. However, its relationships are uncertain, and basic structures such as its highly unusual flowers, which are unique in the family and which lead to the species epithet "orchidacea", are only superficially studied and poorly understood (Fig. 2A–C).
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, p. 305) remarked that the species is "perfectly isolated by its characters, combining those of very different [legume] tribes." Irwin and Barneby (1981) also recognized the uniqueness of Duparquetia and placed it in its own subtribe Duparquetiinae of tribe Cassieae, further commenting that they would "have awarded tribal rank to the five subtribes [of tribe Cassieae] if not dissuaded by others." Polhill (1994) and Lewis (2005) both followed Irwin and Barneby (1981) in retaining Duparquetia in its own subtribe.
Duparquetia is a liana with imparipinnate leaves, a racemose inflorescence, zygomorphic flowers, and a woody, elastically dehiscent pod (Fig. 2A–D). It lacks vestured pits in the wood vessels, a feature that is present in most members of the Leguminosae except for genera of the basally branching clade Cercideae and some members of the Dialiinae s.l. clade (Herendeen et al., 2003). Furthermore, in Duparquetia flowers the vexillary petal is exterior in bud, which is a characteristic otherwise associated with the subfamily Papilionoideae (e.g., Eichler, 1878). The pollen morphology, ultrastructure, and development of Duparquetia were studied by Graham et al. (1980), Graham and Barker (1981), Ferguson (1987), and Banks et al. (2006). These studies all confirmed that Duparquetia is a palynological oddity not only in the Leguminosae, but among the eudicots.
In this study our objectives are to (1) generate a complete floral developmental sequence of D. orchidacea, (2) clarify still open questions of organ identity, (3) compare the developmental sequence with the flower morphology of mature Duparquetia flowers, (3) compare the sequence with floral developmental sequences of putatively related genera and with other Fabales, and (4) make inferences about the evolution of the legume flower in the light of recent insights into legume radiation (Lavin et al., 2005; Bruneau et al., 2008).
Phylogenetic background
A phylogenetic analysis based on morphological characters (Chappill, 1995) placed Duparquetia in a trichotomy with subfamily Papilionoideae and a clade consisting of Caesalpinioideae plus Mimosoideae. In the analyses of Herendeen et al. (2003), Duparquetia was resolved as basally branching and sister to the Dialiinae s.l. clade, although with weak (53%) bootstrap support. In the most recent analyses by Bruneau et al. (2008), the genus is still found on a long branch in an unresolved position among early-branching Leguminosae together with the Cercideae clade, the Dialiinae clade, and a clade containing all other legumes (Fig. 1). Because of the unresolved systematic position of Duparquetia, it is timely to critically reinvestigate flower morphology and to study floral development in detail.
MATERIALS AND METHODS
Fresh material of Duparquetia orchidacea was fixed in 70% ethanol and stored in Kew mix (Cameroon: Polhill et al. 5217, Prenner and Ghogue 757; Gabon: Hawthorne s.n.; Nigeria: Coombe 177) and vouchers are stored in K. For scanning electron microscopy (SEM), material was dissected in 70% ethanol, dehydrated through an alcohol series to absolute ethanol, and critical-point-dried using an Autosamdri-815B critical-point dryer (Tousimis Research, Rockville, Maryland, USA) at the Royal Botanic Gardens, Kew (RBGK) and a Balzers CPD 030 (BAL-TEC AG, Liechtenstein) at the Natural History Museum, London (NHM). Dried material was further dissected and mounted onto specimen stubs using nail polish, coated with platinum using an Emitech K550 sputter coater (Emitech, Ashford, UK) at RBGK and a Cressington 208HR sputter coater (Cressington Scientific Instruments, Watford, UK) at the NHM, and examined using a Hitachi cold field emission SEM S–4700–II (Hitachi High Technologies, Tokyo, Japan) at RBGK, a Hitachi S-2500 SEM and a LEO 1455VP (Carl Zeiss SMT AG, Oberkochen, Germany) at the NHM. In total, more than 200 SEM micrographs were analyzed.
For comparative purposes, additional developmental sequences are reported of the following taxa: Caesalpinioideae: Senna artemisioides (Gaudich. ex DC.) Randell (cult. BG Graz, Austria, leg. Prenner 372), Senna angustifolia Batka (cult. BG Graz, Austria, leg. Prenner 451); Mimosoideae: Inga feuillei DC. (cult. BG Graz, Austria, leg. Prenner 140); Papilionoideae: Cicer arietinum L. (cult. BG Graz, Austria, leg. Prenner 443); Polygalaceae: Polygala comosa Schk. (wild source, leg. Prenner 238). SEM technique was the same as described before, and the material was studied with a Philips XL30 ESEM microscope (FEI Electron Optics, Eindhoven, The Netherlands) at the Institute of Plant Sciences (University Graz, Austria).
Incomplete descriptions of Duparquetia orchidacea exist in various floras (e.g., Hutchinson and Dalziel [1928] in Flora of West Tropical Africa; Steyaert [1952] in Flore du Congo Belge; Aubréville [1968] in Flore du Gabon). However, Bois (1903) did have access to living material and carried out a thorough study of the vegetative and reproductive morphology of Duparquetia, even though he did not provide a complete description. The description in this paper is based on the herbarium material housed at the Natural History Museum, London (BM) and the Royal Botanic Gardens, Kew (K), the photos taken in Cameroon by van der Burgt (RBGK), Kirkup (RBGK), and Prenner (RBGK), the type material of Baillon’s Duparquetia orchidacea collected in Gabon in 1864 (Griffon du Bellay 4339, P), and Bentham’s Oligostemon pictus collected in Cameroon in 1863 (G. Mann 2210, K).
RESULTS
Species description
Duparquetia orchidacea is a scrambling, unarmed liana often climbing to the forest canopy, and with spiral phyllotaxy. The leaves are imparipinnate, petiolate, 3–9-foliolate. Leaflets are opposite to subopposite, petiolulate, 6–17 x 4–12 cm, ovate, obovate or elliptic, the base rounded or acute, the margin entire, the apex acuminate ending in a drip tip, the texture coriaceous, both surfaces lustrous and green. The stipules are caducous, c. 8 x 3 mm, narrowly triangular, the apex acuminate. The inflorescences are terminal, erect, 10–30-flowered racemes aggregated into heterothetic double racemes with 15–30 cm long inflorescence axes densely indumented with ferrugineous tomentum. The flower-subtending bract and the two lateral bracteoles are 2–3 x 1–1.5 mm, triangular, caducous, not enclosing the flower in bud with the indumentum similar to that of the inflorescence axis. The flowers are strongly zygomorphic (Fig. 2) and with 5–10 mm long pedicels. A hypanthium is completely lacking. The calyx is composed of four unequal sepals. The abaxial and adaxial sepals are 17–30 x 10–20 mm, ovate, cucullate. The abaxial/lower sepal is larger and enclosing the flower in bud. Its outer surface is ferrugineous with the indumentum similar to that of the inflorescence axis. The adaxial/upper sepal is only ferrugineous where not covered by the abaxial sepal. The covered parts are glabrous and white. The inner surface of both sepals is glabrous, white or pale pink. The two lateral sepals are petaloid, white or pale pink. One (i.e., the outer) is 23–25 x 12–14 mm, ovate, with a slightly lobed base and acute apex. The other (i.e., inner) sepal is 23–25 x 19–20 mm, distinctly bilobed, one lobe is ovate, the apex acute, the other obovate. The corolla is composed of five dimorphic petals. The adaxial and the two lateral petals are 19–20 x 6–7 mm, ovate, with highly visible red venation, their apices acute. The two abaxial/lower petals are 10–11 x 2–3 mm, strap-like, oblong, their apices rounded. All five petals are usually deep red, rarely white or pale pink like the sepals, with extrusions in the form of stalked gland-like structures along their margins or only along the basal parts of the organs. The androecium usually consists of four stamens (Fig. 2C, E, F) with 3–4 mm long, free filaments. The anthers are 15–17 x 3–4 mm, basifixed, oblong, robust, with long, pointed appendages. Each theca dehisces by a short, apical, poricidal slit. The anthers are postgenitally fused into a curving synandrium, rarely the lateral anthers remain free. The appendages remain consistently free (Fig. 2E, F). The gynoecium consists of a shortly stipitate, few-ovuled ovary with four ridges running along the length of the ovary, and a curved style. The pod is 6–15 x 2–4 cm, oblong, four-angled, woody, dark red turning brown at maturity, with an acute apex and 2–5 seeds. The seeds are c. 3 x 2 cm, oblong to ovoid, the testa thick and brown.
Duparquetia orchidacea occurs in the humid tropical forests of West Africa from the Ivory Coast in the west, through Liberia and Cameroon to Gabon, Nigeria, and the Republic of Congo.
Flower initiation (Fig. 3)
Flowers are initiated in an acropetal, spiral sequence, and individual flowers are formed in the axils of flower-subtending bracts (Fig. 3A–C). The floral bract is the main protective structure during early development (Fig. 3G). Two lateral bracteoles are formed more or less simultaneously to the right and left of the floral primordium (Fig. 3B, C). The bracteoles remain small and apparently have only very limited protective function during early floral development (Fig. 3B–E).
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The two lateral sepals also enlarge distinctly, and their apices soon meet above the floral apex (Fig. 4A, C, G). At a height of c. 2 mm, basal abaxial lobes are formed on both lateral sepals (Fig. 5A). These lobes remain equal in size for a longer period (Fig. 5B, C). Only late in development, the lobe of the inner sepal enlarges distinctly, and finally the sepal appears bilobed with the two lobes equal in size (Figs. 2G, H, 5D). In the anthetic flower, this bilobed sepal becomes a landing platform for floral visitors, basally strengthened by the lesser-lobed outer sepal (Figs. 2B, C, G, H, 5D).
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Soon after initiation, petals enlarge and petal aestivation becomes cochlear descending with the adaxial median petal the outermost, followed in succession by the two adaxial lateral petals and finally the two abaxial/lower petals (Fig. 4I–L). The last formed adaxial petal, which is somewhat smaller at the beginning, becomes the innermost petal (Figs. 4K, L, 6D, F).
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Stamen formation and differentiation (Figs. 2, 5, 6)
Four alternipetalous stamens are formed more or less simultaneously, after a distinct plastochron during which the petals enlarge (Fig. 6A). The abaxial alternipetalous position remains free because there is no fifth stamen primordium initiated (Fig. 6A–C, E, G–I, K). The stamen primordia soon enlarge; the two lateral stamens more than the two adaxial stamens (Fig. 6B, C). Later in development, the apices of the young stamens become bilobed, and the two thecae are formed (Fig. 6H, J–L). The anthers fuse postgenitally and form a distinct column in the center of the young floral bud (Figs. 2H, 5I, K, L). In the anthetic flower, anther opening is introrse via slit-like pores (Fig. 2E, F).
Gynoecium formation and differentiation (figs. 6, 7)
A single central carpel is finally formed after a distinct plastochron during which the stamen primordia enlarged (Fig. 6C). The carpel appears to be formed exactly in the median plane, but the young initial soon turns either somewhat to the left or the right side of the flower (Fig. 6E, G, H, K). This asymmetry appears to be correlated with the position of the abaxial innermost petal. If the innermost petal lies on the right side, the carpel turns to the right and vice versa (Fig. 6D–G). The carpellary cleft is formed in median adaxial position, and it closes from the base toward the apex (Fig. 6J). Hairs are formed at the abaxial side of the carpel where a distinct free gap is visible; this gap indicates the position of the completely lost fifth stamen (Fig. 6H, I, K, L). The mature gynoecium is distinctly pilose on the abaxial side for about two-thirds from the base and has a papillate stigma (Fig. 7A). The stigmatic papillae protrude downward on the adaxial side of the carpel, along the carpellary cleft (Fig. 7B). Within the gynoecium, we found three ovules (Fig. 7A, C).
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Petal formation and development in Inga feuillei (Mimosoideae, Fig. 8G–I)
In Inga feuillei, petals are formed simultaneously (Fig. 8G). Probably as a result of variable petal numbers (5–7 petals were found), flower orientation appears to vary, so that one (aberrant) flower is found with a petal in adaxial/upper position (Fig. 8G). The two other flowers have the "normal" orientation of Mimosoideae with one petal in abaxial/lower position (Fig. 8H, I). Following their simultaneous initiation, the petals enlarge more or less synchronously, and they soon bend inward towards the organ-free floral apex (Fig. 8H). Soon after, the tips of the petals meet above the center of the young flower and petal aestivation becomes valvate, significantly strengthening early bud protection (Fig. 8I).
Petal development in Cicer arietinum (Papilionoideae, Fig. 8J–L)
In Cicer arietinum, petals are formed in a rapid unidirectional succession, starting on the abaxial side (details not shown). The petals enlarge very slowly, and the outer alternipetalous stamens and the central carpel soon overarch the petals in size (Fig. 8J). Bud protection is mainly provided by the calyx, which has been removed in all figures. This retarded petal enlargement prevails in later developmental stages in which the corolla significantly lags behind the development of the androecium and the gynoecium (Fig. 8K, L). Only very late in floral development, petals enlarge distinctly and form the typical papilionoid flag blossom (not shown).
Petal development in Polygala comosa (Polygalaceae, Fig. 8M–O)
In Polygala comosa, petal formation initially follows the spiral of the calyx, and the abaxial/lower petal is formed first (details not shown). This petal enlarges more or less in parallel with the stamens (Fig. 8M), while the two adaxial/upper petals lag behind in development (Fig. 8M, N). The two lateral petal initials stay in a more or less primordial stage (Fig. 8M). An older developmental stage shows that the abaxial/lower petal becomes concave, enclosing parts of the androecium and that appendages are formed just below its tip (Fig. 8O). The adaxial/upper petals are somewhat retarded in development, and the lateral petals are strongly reduced (Fig. 8O). The latter are hardly visible in the mature flower (not shown).
DISCUSSION
The floral groundplan: Some clarifications (Fig. 9A)
According to Baillon’s (1865) protologue of Duparquetia orchidacea, the calyx consists of only two median sepals. Baillon interpreted the two lateral organs as petals, which together with the three adaxial/upper petals form a pentamerous corolla. Furthermore, he interpreted the two vestigial abaxial/lower petals as petaloid staminodia, which in turn are part of a 10-merous androecium (because he interpreted the four stamens as two double stamens). This rather inventive but somewhat forced interpretation was never widely accepted (e.g., Bentham, 1865a, 1865b; Oliver, 1871; Bois, 1903), and we found no supporting evidence from our own observations. It is without doubt that the flower consists of four sepals (two median and two lateral), five petals of which the two abaxial are reduced in size, and four alternipetalous dithecous stamens. The fifth alternipetalous stamen in abaxial position, and the entire inner stamen whorl are lost. We base the assumption that the inner stamen whorl is lost on the widely accepted legume bauplan with five sepals, five petals, 10 stamens in two whorls of five, and a single terminal carpel (Fig. 9A; see also Eichler, 1878; Endress, 1994; Tucker, 2003a). We cannot confirm the existence of a fifth stamen ("Stamina 5, rarius 4") as mentioned by Bentham (1865a, 1865b). Furthermore, we cannot verify the existence of a "treble upper stamen," as mentioned by Bentham (1865a). The "treble upper stamen" could in fact be based on an erroneous observation because Bentham’s figures (1865a, figs. 6, 7 in plate 39) also only show two fused adaxial/upper stamens.
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, 2001a). Because of the rapid and distinct enlargement of the two first-formed sepals and the dome-like closure of the bud by the two lateral sepals, the calyx apparently provides a strong protective function for the inner floral organs. Considering that both the flower-subtending bract and the two lateral bracteoles have only a very limited protective function (see Fig. 3A–G), it makes sense for the calyx to provide the main protection for the inner floral organs.
In addition to this function, we also highlight the white petaloid appearance of the mature sepals, which make a marked contrast to the red petals (Fig. 2A–C). Finally, the distinctly bilobed inner lateral sepal apparently acts as a landing platform for floral visitors. This platform is additionally strengthened by the second (outer) lateral sepal, which is only basally lobed (Figs. 2B, C, G, H, 5D). Because the sole reward for floral visitors is pollen, which is released from the anthers via introrse apical slit-like pores (discussed later), the flowers are most probably visited by relatively large pollen-collecting and buzz-pollinating Xylocopa-like bees as described for other taxa with porate anthers (cf., Buchmann, 1983; Endress, 1994; Harder and Barclay, 1994; Lewis et al., 2000; Thorp, 2000; Marazzi et al., 2007).
We are aware that the red color of the petals is rather uncommon for entomophilous flowers and that it is normally a characteristic for bird-pollination (cf., Cronk and Ojeda, 2008; Thomson and Wilson, 2008). However, bird pollination can be ruled out because of the lack of nectar and the porose anther opening. It therefore seems plausible that the petaloid sepals have an important function in increasing insect attention and that both sepals and petals share attractive functions. The three adaxial/upper petals can also be interpreted as floral guides, leading pollinators toward the source of food (i.e., the pollen-providing stamens; cf. Dafni and Giurfa, 1999). The similarity with guide marks on the adaxial/upper petal(s) of Labichea lanceolata Benth. and Petalostylis labicheoides R.Br. (both early-branching Caesalpinioideae) is noteworthy (see Lewis, 2005). A "dark-dot" effect, which attempts to exploit mate seeking and aggregation behavior of insects (Dafni and Giurfa, 1999), seems less probable but cannot be ruled out at the present state of knowledge.
Comparing sepal size with the size of the petals, we have to consider the petals of D. orchidacea as reduced (even the three larger adaxial/upper petals). This reduction is further evidence for Ronse De Craene’s (2007) hypothesis that petaloid sepals are often correlated with reduced petal size. However, this correlation is not always true in Caesalpinioideae: in Delonix regia (Bojer) Raf., which has a normally developed corolla, the inner surface of the sepals is bright red (i.e., petaloid). The same is true for Amherstia nobilis Wall., in which the bracteoles are also petaloid. In both taxa, the petaloid sepals (and prophylls) are apparently "assisting" the corolla in pollinator attraction. Another example of petaloid sepals is found in Tamarindus indica L. for which Bentham (1865a, p. 305) also mentioned that "the veined petals [of Duparquetia] are nearly those of Tamarindus."
The shift and/or share of attractive functions between sepals and petals have apparently happened independently several times in caesalpinioid evolution. Within Fabales, another remarkable example of petaloid sepals paired with the reduction of some petals is found in Polygalaceae (cf., Bamert, 1990; Prenner, 2004b). The genetic background for sepaloid petals in Fabales remains to be studied (Bello et al., 2008), and it will be interesting to compare the genetic programs responsible for petaloid sepals in Polygalaceae and Caesalpinioideae.
The corolla: Protective, partly reduced, with an unusual aestivation pattern
The corolla of Duparquetia has special and, in parts, unique features throughout its development. A unique pattern of initiation and early enlargement is followed by a remarkable differentiation and specialization.
Protective function of early enlarging petals
The petals enlarge almost immediately after their initiation and they soon overarch the center of the flower (Fig. 4H–L). Therefore, petals, in addition to the sepals (as discussed before), provide protection for the inner floral organs (i.e., stamens and gynoecium). Furthermore, it is noteworthy that initially all five petals enlarge more or less equally and that the abaxial two petals only later in development lag behind and become reduced in size.
Early petal enlargement is a rare phenomenon in Caesalpinioideae. Other caesalpinioids with early enlarging petals are Senna and Delonix, in which two different patterns of petal enlargement (quick and slow) were reported by Endress (1994) and Marazzi and Endress (2008) (see also Fig. 8A–F; Tucker, 1996b). In Delonix regia petals enlarge fairly rapidly, even though they do not fully enclose the carpel (see Fig. 8.26 in Endress, 1994). Within Leguminosae, early petal enlargement is a characteristic of Mimosoideae. In this subfamily the calyx stops growing early, and the sole protective structure of the enlarging bud is provided by the valvately aestivated petals (Fig. 8G–I; see also Gemmeke, 1982; Ramírez-Domenech and Tucker, 1989; Prenner, 2004c; Gómez-Acevedo et al., 2007).
Most other Caesalpinioideae studied so far show a more or less distinct retarded petal enlargement (e.g., Tucker, 1998, 2000a, b, 2001b, 2002a, b). Other Fabales with retarded petal development are Papilionoideae (Fig. 8J–L; see also Tucker, 1987; Klitgaard, 1999; Prenner, 2003, 2004a, d), Quillajaceae and Surianaceae (Bello et al., 2007). In these taxa, the protective function for the inner floral organs is mainly provided by the sepals and/or to a variable degree by the floral prophylls. Polygala has a mixed pattern, because the abaxial/lower petal enlarges fairly early compared to the two adaxial/upper petals (Fig. 8M–O; see also Bamert, 1990; Prenner, 2004b). The two lateral petals stop growing soon after their initiation, and they are strongly reduced in the mature flower.
Unique petal differentiation and aestivation
Considering the sequence of petal initiation, it is noteworthy that either the abaxial left or the abaxial right petal is formed last (Fig. 4D–F) and that this last-formed petal is in the innermost position (Figs. 4K, L, 6D, F). This in turn affects the symmetry of the young carpel, which is turned either to the left (when the last-formed petal lies on the left) or to the right (when the last-formed petal lies on the right) (Fig. 6D–H). Analogous to findings in Polygala myrtifolia (Prenner, 2004b), these distinct left–right symmetries could be interpreted as remnants of an ancestral helical organ formation, which is frequently found in other Caesalpinioideae (reviewed in Tucker, 2003a). The early asymmetry of the young carpel does not prevail until anthesis, and we interpret it as "imprinted shape" caused by the pressure of contiguous organ(s) (cf., Endress, 2008) which in Duparquetia apparently is the innermost petal.
Duparquetia differs from most other Caesalpinioideae in that the adaxial/upper petal is the outermost (i.e., it shows cochlear-descending petal aestivation instead of the typical caesalpinioid cochlear-ascending aestivation in which the adaxial/upper petal is the innermost) (Figs. 4K, L, 5K, 6D, F, 9A; Eichler, 1878). Cochlear-descending petal aestivation, characteristic of most Papilionoideae, is only occasionally reported in Caesalpinioideae. However, past studies showed that in some putatively early-branching Papilionoideae petal aestivation is variable (e.g., van der Maesen, 1970; Mansano et al., 2002; Tucker, 2002b). For Caesalpinioideae, Eichler (1878) mentioned that — besides Duparquetia — in Tamarindus sometimes the adaxial/upper petal can be the outermost.
Marazzi and Endress (2008) described two patterns of petal aestivation in different species of the caesalpinioid genus Senna. In addition to the typical cochlear-ascending aestivation, they found quincuncial aestivation as a second pattern (see also Fig. 8B–F). They speculated that these patterns are probably the result of different growth rates among the petals. Early enlarging petals maintain the pattern of their spiral initiation sequence, resulting in a quincuncial aestivation (Fig. 8B, C). Late enlarging petals in contrast are influenced by the developing floral monosymmetry, which results in a cochlear-ascending aestivation (Fig. 8D–F). Our study of Senna angustifolia furthermore reveals a modified pattern of ascending petal aestivation in which the adaxial petal is innermost, covered by the two lateral petals, which also cover the two abaxial/lower petals (Fig. 8F). Our study further suggests that the sequence of petal initiation (i.e., pronouncedly following the spiral of the sepals vs. almost simultaneous petal initiation) also plays a role in further petal development and aestivation (Fig. 8A–F). Armstrong and Douglas (1989) found that in Scrophulariaceae a similar phenomenon of differing petal enlargement is responsible for different patterns of their aestivation.
Analogous to these examples, the cochlear-descending petal aestivation in Duparquetia is apparently also the result of the sequence of petal initiation and early petal enlargement. The two lateral-adaxial petals are formed slightly earlier, and they seem to enlarge somewhat more rapidly than the median-adaxial petal (Fig. 4D–F). In this way the adaxial/upper petal is forced in an outer position and petal aestivation becomes cochlear-descending (Figs. 4H, I, K, L). However, it is remarkable that in Papilionoideae cochlear-descending petal aestivation becomes discernible much later in floral development. Here, as discussed earlier, petal enlargement is generally retarded, and the petals consequently aestivate much later in floral development (Fig. 8J–L; see also Tucker, 1989, 1994; Klitgaard, 1999; Prenner, 2004a). Hence we want to highlight that the developmental basis for the cochlear-descending petal aestivation differs distinctly between Duparquetia and Papilionoideae and that it is most probably not a homologous feature.
The variable petal aestivation in the papilionoid Cadia purpurea is caused by a rather different developmental and genetic base (cf., van der Maesen, 1970; Tucker, 2002a; Citerne et al., 2006). Citerne et al. (2006) showed that the uniform petals of the radially symmetric Cadia are apparently the result of "dorsalization" of the flower. This dorsalization is the result of additional expression of LegCYC genes (normally found only in the adaxial/dorsal region of the flower) in lateral and abaxial positions. In this way, in Cadia all five petals have acquired the identity of the adaxial/dorsal standard petal of a "normal" papilionoid flower, resulting in a random aestivation of petals (see also Feng et al., 2006 on the control of petal shape in Lotus japonicus and Wang et al., 2008 on Pisum sativum). Using molecular data, Boatwright et al. (2008) showed that Cadia, which was formerly grouped in Sophoreae, is a monophyletic sister to Podalyrieae. The authors therefore proposed transference of the genus to Podalyrieae and interpreted the unusual actimorphic flowers as an apomorphy for the genus, which otherwise shares many characters with Podalyrieae.
Together, these examples demonstrate the importance of careful and rigorous investigation of the sequence of organ initiation, the pattern of organ enlargement and the developmental genetic background of the described phenomenon. Only a rigorous comparative approach can finally lead to a better understanding of superficially similar but nonhomologous morphologies.
Gland-like structures on petal margins
We found gland-like structures along the entire margins of the two vestigial abaxial/lower petals and along basal margins of the other three petals (Fig. 5E–L). These structures resemble stalked, club-shaped hairs as found on different organs in Caesalpinia s.l. and related genera (Rudall et al., 1994). To our knowledge, however, in this group, hairs (if present) are restricted to the base of the petals, and no report of evenly distributed hairs along the entire petal margin is known. In Duparquetia this unusual pattern could be the result of petal reduction, and we argue that the two abaxial/lower vestigial petals in Duparquetia could be homologous to the petal bases of other caesalpinioids.
Concerning possible functions of these elaborate structures, further studies in the field and/or on cultivated material are necessary. The gland-like structures could (1) provide tactile stimulants for floral visitors, (2) function as pseudonectaries (analogous to similar structures in flowers of Parnassia; cf., Matthews and Endress, 2005), (3) act as scent-emitting osmophores (Vogel, 1990; Endress, 1994), or (4) represent food bodies providing nourishing tissue for visiting insects (analogous to similar structures in flowers of e.g., some Annonaceae; cf. Endress, 1994).
The androecium: Reduced and specialized
The androecium of Duparquetia has to be considered as highly elaborate. It is reduced (only four stamens initiate), it forms a synandrium due to postgenital fusion of the anthers, and pollen is released via poricidal slits. Because of the fused anthers, the androecium appears in the anthetic flower almost like a shield bending over the center of the flower (Fig. 2C). Due to the loss of both the abaxial/lower stamen and the entire inner stamen whorl, there is plenty of space in the abaxial/lower position for the protrusion of the carpel. Because of the poricidal anther opening (Fig. 2E, F; see also Harris, 1906) and the lack of nectar as a floral reward, we suggest that larger pollen-collecting, Xylocopa-like bees buzz-pollinate the flowers (see Lewis et al., 2000, and earlier discussion).
Due to its porate anthers, Duparquetia was included in tribe Cassieae in which porate anther opening is a common character (Bentham, 1865b; Irwin and Barneby, 1981; Tucker, 1996a; Marazzi et al., 2007). However, recent studies show that Cassieae is not monophyletic (Fig. 1; Herendeen et al., 2003; Lewis et al., 2005; Bruneau et al., 2008) and a close relationship between Duparquetia and other Cassieae is not supported by the most recent phylogenetic analyses. Consequently, porate anthers appear to have evolved independently several times within Caesalpinioideae.
The gynoecium: Does the last-formed organ provide a clue to the evolution of enantiostyly in Caesalpinioideae?
The gynoecium is the last-formed organ terminating the flower. This late formation of the carpel is rather unusual among legumes because it is precocious in most other studied taxa (Fig. 9B). Another remarkable feature is the early asymmetry of the young carpel, which we interpret as the result of "imprinted shape" sensu Endress (2008) (see earlier discussion). Depending on the position of the innermost abaxial/lower petal, the tip of the young carpel is forced either to the left or to the right of the median plane.
Is enantiostyly (i.e., the deflection of the style to the left or right of the median plane) in Senna the result of an analogous phenomenon of imprinted shape? As reported by Marazzi and Endress (2008) the direction of the style depends in Senna on the direction of the spiral of the calyx (i.e., a spiral to the right results in the style turned to the right and vice versa). We argue that the spiral of the calyx often determines the position of the first-formed abaxial/lower petal, which in most enantiostylous species enlarges early (Fig. 8B) and which later becomes strongly heteromorphic (see Marazzi and Endress, 2008). Analogous to the circumstances in Duparquetia, the style could be forced off the median plane by this heteromorphic petal. We speculate that mature flowers of Duparquetia are not enantiostylous because mechanical forces on the carpel are less strong due to the vestigial nature of the abaxial/lower petals, the retarded formation of the carpel and the reduced androecium. This leaves more available space within the bud and mechanical forces therefore cannot act as strongly on the carpel as in enantiostylous Senna species. Enantiostylous Senna species in which the two abaxial/lower petals are equal in size and shape (i.e., "symmetry pattern two" in Marazzi and Endress, 2008), and in which these petals initiate and enlarge almost simultaneously (Fig. 8D–F; see also Tucker, 1996b) apparently argue against the hypothesis that enantiostyly is the result of imprinted shape. Therefore, it will be interesting to carefully investigate these enantiostylous taxa with monosymmetric corolla searching for mechanical power that could force the carpel out of the median plane.
Jesson and Barrett (2002b) showed that enantiostyly is genetically inherited in the monocots Heteranthera multifolia (Griseb.) C. N. Horn (Pontederiaceae) and Wachendorfia paniculata L. (Haemodoraceae). Both taxa are dimorphic enantiostylous with right- and left-styled flowers on separate individuals (see also Barrett, 2002; Jesson and Barrett, 2002a; Jesson et al., 2003), and in both taxa enantiostyly becomes evident very late in development (Jesson et al., 2003). Strange et al. (2004) found in Monocharia (Pontederiaceae) that an elliptical or linear appendage on the abaxial outer stamen is probably correlated with enantiostyly. According to the authors, it is not clear if the position of the appendage facilitates the asymmetric displacement of the style (i.e., enantiostyly could be an imprinted shape) or if the appendage assists the release of pollen onto pollinators (see also Rudall and Bateman, 2004). As we have mentioned, the direction of the style can already be predicted by the direction of the helix of the calyx. Consequently, we argue that the study of earliest developmental stages can prove critical and could lead to a better understanding of the developmental basis of enantiostyly in other angiosperms.
The stigmatic surface of Duparquetia appears "grooved" because the papillae protrude to a certain extend downward along the adaxial side of the carpel (see also Owens and Lewis, 1996). Therefore, the stigma is not typical for buzz-pollinated taxa, which frequently have point-tipped stigmas (e.g., Endress, 1994; Marazzi et al., 2007). Finally, our finding of three-ovulate gynoecia differs from Bentham (1865a, b) and Baillon (1865) who described the ovary as biovulate. Our study of mature pods showed that Duparquetia apparently has 2–5 ovules (seeds) per ovary (pod) (see also Bois, 1903).
Loss and suppression of floral organs and its impact on floral symmetry
Duparquetia is intriguing because we found both organ loss (one sepal and six stamens are lost) and organ reduction (i.e., the two abaxial/lower petals are reduced in size). Tucker (1998) highlighted that organ loss can profoundly affect subsequent organogeny, leading to a "chaotic" floral development in some Caesalpinioideae such as Gleditsia, Ceratonia, and Labichea (see also Tucker, 1988, 1991, 1992, 1999, 2000d).
Duparquetia differs considerably from these examples. Even the complete loss of one sepal does not significantly affect further organogeny or the symmetry of the young flower, which remains zygomorphic throughout its development. We speculate that this stability is the result of the distinct plastochrons that we observed during sepal initiation. Because of this, the floral apex has the form of an isosceles trapezoid before the first petal is initiated (Fig. 4B), and petal initiation therefore becomes canalized. Four petals (have to) arise in the four corners of the trapezoid, and a fifth petal is formed in adaxial/upper position where space allows another primordium. Loss of the fifth alternipetalous stamen and the entire inner antepetalous stamen whorl also does not affect organogeny but strengthens the zygomorphic appearance of the young flower. Here again it is noteworthy that stamen initiation does not start until all petals are initiated and enlarged to a certain degree (i.e., after a certain plastochron; Figs. 6, 9B). The same factor (initiation after all stamens have formed and somewhat enlarged) holds true for the carpel, which finally terminates the flower (Figs. 6B, C, 9B).
This strict acropetal sequence of organ formation is found only rarely (or is possibly even unique) within Leguminosae, where in most cases the carpel is formed precociously and the formation of other organs can overlap (Fig. 9B; see also Tucker, 1989, 2003a). Early carpel formation with overlapping organ whorls is apparently in conflict with the ABC model of floral organ identity, which is based on model organisms (mainly Arabidopsis and Anthirrhinum) in which organs of the different whorls arise simultaneously and in a strict acropetal pattern (i.e., from outside toward the center of the flower) (cf., Coen and Meyerowitz, 1991). Adjustments of the ABC model will be necessary for a clarification of the particular circumstances in Leguminosae (cf., Benlloch et al., 2003; Berbel et al., 2005; Citerne et al., 2006). Considering the position of Duparquetia orchidacea among early-branching legumes and its particular floral groundplan, in depth studies of its genetics of organ identity and floral development could be highly rewarding.
Is this just another "awkward" caesalpinioid flower?
After unraveling the developmental background of the highly unusual flowers of Duparquetia, we have to ask if this is just another awkward Caesalpinioideae with unusual floral features. Duparquetia indeed combines several developmental features that are rare or even unique within legumes (i.e., combination of loss and suppression of organs, organ formation in a strict acropetal sequence, distinct, and in parts long plastochrons both within and between whorls) and which finally result in a highly specialized zygomorphic flower.
Thanks to the extensive work of Shirley Tucker (reviewed in Tucker, 2003a), we have access to a wealth of developmental data of a broad array of legume taxa. For the current study, we have extracted data of the potentially related Cercis canadensis, Labichea lanceolata, Petalostylis labicheoides, and Dialium guineense from Tucker (1998, 2002b). We also include Tamarindus indica, which has a similar floral bauplan to Duparquetia (i.e., mature flowers with a four-lobed calyx, only three petals and three functional stamens; see Tucker, 2000c). Because the timing of organ formation (strictly acropetal with distinct plastochrons) in Duparquetia is rather remarkable, we restrict our comparative analysis to the relative timing of organ formation (Fig. 9B). This analysis clearly shows the tendency to precocious initiation of the carpel and different patterns of organ loss and reduction among the sampled taxa. It is intriguing that Tamarindus indica differs considerably in its developmental timing and its floral structure even though it has a similar groundplan to Duparquetia. In Tamarindus the tetramery of the calyx is the result of fusion of two sepals (not organ loss as in Duparquetia), two abaxial/lower petals are strongly reduced (as in Duparquetia), and only one stamen in adaxial/upper position is entirely lost, while four outer and two inner stamens are initiated but reduced. The carpel in Tamarindus is formed precociously together with the petals (Fig. 9B; Tucker, 2000c).
Among early-branching Leguminosae, it seems plausible that there was a distinct experimental phase with different developmental pathways leading to the highly canalized and specialized flag blossom of the majority of Papilionoideae. Lavin et al. (2005) found evidence for a rapid familywide diversification in Leguminosae. The authors (Lavin et al., 2005, p. 544) note that "the profusion of basally branching and morphologically diverse crown clades within legumes reveals that the paraphyletic grade of caesalpinioid lineages harbor neither the oldest diversifications nor some other quality of legume antiquity." Bruneau et al. (2008) focused their study on the relationships and diversification in the caesalpinioid legumes, but were unable to solve relationships among early branching legume lineages. The authors emphasize that the position of Duparquetia remains unresolved and that Duparquetia is one of the main causes for the persisting lack of resolution among the first-diverging legume lineages.
These new insights into legume evolution have to be carefully considered when discussing evolutionary trends in floral morphology and development of Leguminosae. Looking for parallels between subfamilies we can for example see that both, loss and reduction/suppression of organs occurred in caesalpinioids (e.g., Tucker, 1988, 1998, 2000a, 2001b; Marazzi and Endress, 2008) and in papilionoids (e.g., Tucker, 1988, 1990, 2003b; Pennington et al., 2000; Prenner, 2004e; McMahon, 2005; McMahon and Hufford, 2005). The same is true for spiral sepal initiation, which is pronounced in several Caesalpinioideae (Tucker, 2003a) but can also be rudimentary in papilionoids (e.g., Klitgaard, 1999; Prenner, 2004e) and for which we showed some evidence in Duparquetia. Finally, it is intriguing that petal heteromorphism, which is an important key character in the papilionoid flag blossom, also exists in the flowers of Duparquetia.
Analogous circumstances can be stated if we consider the legume flower as a pollination unit: the pronounced zygomorphy, elaborate landing platform, fused and porate anthers, petaloid sepals, and heteromorphic corolla with elaborate gland-like hairs make the flower of Duparquetia a highly specialized unit. Consequently, we argue that the degree of floral specialization in Duparquetia is comparable with that of the highly elaborate and well-known flag blossom of Papilionoideae (cf. Westerkamp, 1997). Several authors have put forward hypotheses as to why the papilionoid flag blossom became so highly successful in terms of species number (e.g., Westerkamp, 1997; Pennington et al., 2000; Sprent, 2001, 2007; Schrire et al., 2005). Their arguments include (1) adaptation to bees as important pollen vectors and (2) symbiosis with nitrogen-fixing bacteria, which gave the papilionoids a competitive edge and enabled them to colonize nutrient-poor soils. Why Duparquetia, with its highly elaborate flowers remained a monotypic genus, is an outstanding question. What role did geography and ecology play in the evolutionary history of this enigmatic taxon And how important is the fact that Duparquetia is apparently lacking nitrogen-fixing bacteria (Sprent, 2001; Diabate et al., 2005)?
Concluding remarks
Neither the exact systematic position of Duparquetia orchidacea, nor its closest relatives among early-branching legumes are currently known. Molecular phylogenies may be hampered by the rapid radiation of Leguminosae (Lavin et al., 2005; Bruneau et al., 2008). Therefore it seems important to enlarge the existing data sets with additional data (morphological and molecular) and taxa. The current study can be seen as one attempt in tackling questions of legume evolution. Our investigation of the morphology and development of Duparquetia orchidacea reveals a wealth of new data, which lead to a better understanding of this enigmatic species. Furthermore, these data result in new ideas on different aspects of floral evolution in Leguminosae (e.g., evolution of enantiostyly, zygomorphy, and petal heteromorphism). And they can potentially help to resolve the systematic position of Duparquetia and the systematic relationships among the early-branching taxa of Leguminosae.
FOOTNOTES
1 The authors thank D. Kirkup and X. van der Burgt for making their beautiful photos available to us, W. Hawthorne and X. van der Burgt for collecting Duparquetia in the field; A. Bruneau, G. Lewis, P. Rudall, and D. Sokoloff for fruitful discussions; P. Herendeen and L. Ronse de Craene for valuable comments in their reviews. B.K. is grateful to the Royal Botanic Gardens, Kew (K) and the Natural History Museum in Paris (P) for making typus material available on loan to the NHM and for financial support from National Science Foundation grant no. DEB-0316375. G.P. thanks M. Cheek for the opportunity to join a fieldtrip to Cameroon, during which material was collected, J.-P. Ghogue for assistance in the field, and the Austrian Science Fund for financial support (FWF, project J2504). 
4 Author for correspondence (e-mail: g.prenner{at}kew.org)
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