Comparative Floral Development in Lardizabalaceae (Ranunculales)

Botanical Journal of the Linnean Society, 2011, 166, 171–184. With 7 ﬁgures

Comparative ﬂoral development in Lardizabalaceae (Ranunculales)

XIAO-HUI ZHANG* and YI REN

Key Laboratory of Medicinal Plant Resource and Natural Pharmaceutical Chemistry of Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an, China 710062

Received 3 December 2010; revised 20 March 2011; accepted for publication 28 March 2011

Lardizabalaceae, one of seven families of Ranunculales, represent a monophyletic group. The family has functionally unisexual flowers with the organs in trimerous whorls, petaloid sepals and sometimes nectariferous petals. Among Ranunculales, Lardizabalaceae share several floral characters and climbing habit with Menispermaceae, but molecular analyses indicate that Circaeasteraceae and Lardizabalaceae form a strongly supported clade. Morphological and ontogenetic studies of flowers have proved to be a good complement to molecular data in clarifying relationships. Floral organogenesis has been studied in very few species of the family. This study investigates the comparative floral development of three species from three genera (Decaisnea, Akebia and Holboellia) of Lardizabalaceae using scanning electron microscopy. Flowers have a whorled phyllotaxis. Within each whorl, the organs are initiated either simultaneously or in a rapid spiral sequence. In Akebia, six sepals are initiated, but one to three sepals of the second whorl do not further develop. The presence of three sepals in Akebia is thus a developmentally secondary simplification. The petals (if present) are retarded in early developmental stages; stamens and petals are different in shape from the beginning of development. The retarded petals may not be derived from staminodes in Lardizabalaceae. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 171–184.

ADDITIONAL KEYWORDS: Akebia trifoliata – Decaisnea insignis – Holboellia grandiﬂora – petals – phyllotaxis – staminodes.

INTRODUCTION Lardizabalaceae, Berberidaceae and Ranunculaceae), Lardizabalaceae are similar to Menispermaceae in Lardizabalaceae are a small family with approxi- their climbing habit and several floral characters mately 50 species and have a disjunct distribution, [including trimerous, unisexual flowers, synandry, mainly in East Asia, but with two genera in Chile nectar leaves (nectariferous petals), gynoecium struc- (Chen, 2001). Plants are woody climbers or, rarely, ture and a comparable floral formula] (Endress & erect shrubs (Decaisnea Hook.f. & Thomson); inflores- Igersheim, 1999; Ronse De Craene, 2010), but molecu- cences are racemes. Flowers are functionally uni- lar phylogenetic analyses indicate a position for sexual by reduction and the whorled arrangement of Lardizabalaceae in core Ranunculales and Circaeast- floral organs is trimerous. Lardizabalaceae are gen- eraceae and Lardizabalaceae form a strongly erally considered to be monophyletic and part of supported clade (Wang et al., 2009b). Although Ranunculales, which belong to the early branching Lardizabalaceae have traditionally been placed eudicots (Hoot, Culham & Crane, 1995a, b; Hoot, among Ranunculales (Takhtajan, 1997), Takhtajan Magallón & Crane, 1999; Soltis, Soltis & Chase, 2000; (2009) elevated them to ordinal status, as Lardiza- APG III, 2009). balales, because he regarded them as basal in Ranun- Among Ranunculales (which include Eupteleaceae, culales and close to some magnoliids, a position not Papaveraceae, Menispermaceae, Circaeasteraceae, supported by molecular studies (APG III, 2009). The number of genera in Lardizabalaceae fluctuates from *Corresponding author. E-mail: [email protected] nine (Loconte, Campbell & Stevenson, 1995; Qin,

Figures 1–7. Mature flowers. Figures 1–2. Decaisnea insignis. Fig. 1. Male flower. Fig. 2. Female flower. Figures 3–5. Akebia trifoliata. Fig. 3. Female flower. Fig. 4. Male flower. Fig. 5. Male flower showing sterile carpels. Figures 6–7. Holboellia grandiflora. Fig. 6. Female flower. Fig. 7. Male flower. Scale bars, 1 cm (Figs 1, 3, 6); 8.5 mm (Fig. 2); 3.5 mm (Figs 4, 7); 2 mm (Fig. 5).

Figures 8–16. Floral development in Decaisnea insignis. Fig. 8. Young inflorescence. Fig. 9. Flower primordium with two bracteoles initiated, bract removed. Fig. 10. Flower with first three sepals initiated. Fig. 11. Initiation of the inner three sepals. Fig. 12. Six sepals arranged in two whorls. Fig. 13. Three stamens are initiated. Fig. 14. The stamens of the second whorl are formed. Fig. 15. Remaining floral apex triangular. Fig. 16. Three carpels are initiated. A, stamen; B, bract; Bl, bracteole; C, carpel; F, flower; L, leaf; S, sepal. Scale bars, 0.4 mm (Fig. 8); 50 mm (Fig. 9); 100 mm (Figs 10, 11, 14); 120 mm (Fig. 12); 150 mm (Figs 13, 15); 200 mm (Fig. 16).

1997) to ten (Takhtajan, 2009; Wang et al., 2009b) Kofuji et al., 1994; Hoot et al., 1995a, b, 1999; Soltis attributable to the uncertain systematic position of et al., 2000). However, Decaisnea has been suggested Sargentodoxa Rehder & E.H.Wilson (Stapf, 1925; to be elevated above the level of genus (Loconte et al., Hutchinson, 1964; Cronquist, 1981; Thorne, 1992; 1995; Wang et al., 2009a). According to Takhtajan

Figures 17–28. Stamen and carpel development in Decaisnea insignis. Fig. 17. Young flower, perianth removed. Fig. 18. The stamens differentiate into the anther and short filament. Fig. 19. Androecium of mature male flower. Fig. 20. Mature male flower, showing sterile carpels, four anthers removed. Fig. 21. Female flower bud, perianth removed. Fig. 22. Mature female flower with carpels and staminodes. Fig. 23. Magnification of the staminodes in Fig. 22, showing dehisced anther and pollen. Figures 24–27. Carpel development. Fig. 24. Young carpels. Figs 25–26. Carpels elongated. Fig. 27. Mature carpel. Fig. 28. Stigma of mature carpel. A, stamen; C, carpel; Fc, filaments connate into a tube; Sc, sterile carpel; St, staminode. Scale bars, 200 mm (Figs 17, 18); 1.25 mm (Figs 18, 20); 0.5 mm (Figs 21, 25, 26, 28); 1 mm (Figs 22, 27); 20 mm (Fig. 23); 100 mm (Fig. 24). ᭣

(2009), Lardizabalaceae consist of Decaisneoideae The materials were dehydrated in an alcohol series (Decaisnea), Sargentodoxoideae (Sargentodoxa) and and iso-amyl acetate series, critical-point dried in

Lardizabaloideae (Sinofranchetia Hemsl., Akebia carbon dioxide (CO2) and sputter-coated with gold. Decne., Archakebia C.Y.Wu, T.C.Chen & H.N.Qin, The SEM micrographs were taken with a Hitachi Holboellia Wall., Stauntonia DC., Parvatia Decne., S-570 scanning electron microscope at 15 KV. The Boquila Decne., Lardizabala Ruiz & Pav.). photographs of mature flowers were taken using a Morphological and ontogenetic studies of flowers Nikon Coolpix 990 digital camera. have been shown to be a useful complement to molecular data in clarifying organismal relationships (Endress, 2003; Ronse De Craene, 2004, 2007). Among RESULTS Ranunculales, flower development has been studied Unisexual flowers (Figs 1, 2) are grouped in compound in all families to various degrees and comparative racemes in D. insignis; racemes have one to three morphological and evolutionary aspects have been female flowers and approximately thirty male flowers discussed (Van Heel, 1983; Endress, 1987, 1995; in A. trifoliata (Figs 3–5); a corymbose raceme consists Ronse De Craene & Smets, 1995; Feng & Lu, 1998; of three to eight unisexual flowers in H. grandiflora Endress & Igersheim, 1999; Wang et al., 2006; Ren (Figs 6, 7). The development of the flowers in the et al., 2004, 2007, 2009; Ren, Chang & Endress, 2010; inflorescence is spiral and acropetal in Decaisnea and Zhao et al., 2011). Although studies of flower develop- Akebia, and more or less simultaneous in Holboellia. ment in Lardizabalaceae would be important to better understand the floral morphology and evolution in the family, and in Ranunculales in general, so far few FLORAL DEVELOPMENT IN DECAISNEA species have been studied (Wang, 2001; Shan et al., Decaisnea insignis has greenish functionally unisexual 2006; Zhang & Ren, 2008; Zhang, Ren & Tian, 2009). flowers consisting of six ovate–lanceolate sepals, six In this study, flower development of three genera was stamens (filaments connate into a slender tube, examined using scanning electron microscopy (SEM). anthers free with a broad connective apical appendage) The present knowledge on floral development in the and three carpels (Figs 1, 2). Each flower is subtended family is summarized and supplemented by new by a bract (Fig. 8); later, two lateral bracteoles (pro- information. We addressed the following questions: phylls) appear at the base of the floral primordium what patterns of floral phyllotaxis can be identified in (Fig. 9). In anthetic flowers, the subtending bract is Lardizabalaceae? Are petals similar to stamens in narrowly linear and two bracteoles are reduced. Six early development? How do species with different sepals are initiated in two whorls. The first three floral structure differ in development? sepals appear successively and form the first whorl. The first sepal is initiated on the adaxial or abaxial side of the floral apex. When the sepals of the first MATERIAL AND METHODS whorl enlarge (Fig. 10), the other three sepals appear Flower buds and young flowers of Decaisnea insignis successively to form the second whorl (Fig. 11). The (Griffith) Hook.f. & Thoms., Akebia trifoliata (Thunb.) young sepals are crescent-shaped (Figs 10, 11). Then Koidz. and Holboellia grandiflora Réaub. were they broaden with the outer three larger than the collected in Qinling Mountain (vouchers Zhang inner ones (Figs 12, 13, 15, 16). All sepals have 20060713, Zhang 200700425, Zhang 20080405, approximately the same size at anthesis (Figs 1, 2). SANU), Shaanxi Province, China, from April 2006 to When the sepals begin to cover the floral apex, December 2008. All materials were fixed in formali- three stamens originate simultaneously and each of n : acetic acid : ethanol (FAA) at a ratio of 5:5:90. them is opposite a sepal of the first whorl (Fig. 13). The buds were dissected in ethanol (70%) under a The three stamens of the second whorl appear alter- stereomicroscope before observation. nating with the stamens of the first whorl (Fig. 14).

Figures 29–37. Floral development in Akebia trifoliata. Fig. 29. Young inflorescence. Fig. 30. Somewhat older inflorescence. Fig. 31. Flowers with initiation of the first three sepals. Fig. 32. Initiation of the second whorl of three sepals (asterisks). Fig. 33. Six sepals initiated, reduced subtending bract visible. Fig. 34. The first three stamens initiated, one of the inner sepals visible (arrow). Fig. 35. Slightly older stage and one of the inner sepals visible (arrow). Figures 36–37. Young flowers, outer three sepals removed, showing the inner three reduced sepals (asterisks). A, stamen; B, bract; S, sepal. Scale bars, 0.4 mm (Fig. 29); 0.5 mm (Fig. 30); 50 mm (Fig. 31); 100 mm (Figs 32, 33, 34, 35, 36, 37).

The stamens begin to differentiate into an apical tip, with a short filament (Figs 4, 5, 40). Three to nine anther and filament (Fig. 17) and the filaments carpels are initiated successively, with a massive become connate into a tube (Figs 18–20). The anther remnant of the floral apex in the centre (Figs 38, 39). tip develops into a broad, flattened, horn-like append- The young flowers are morphologically bisexual, age (Fig. 20). This is also the case in the staminodes but either the stamens or the carpels stop develop- of the female flowers (Fig. 21). ment early and the flowers become functionally The remaining floral apex forms a triangular pro- unisexual. In female flowers, carpels become condu- tuberance after initiation of the six stamens plicate (Figs 41–43) and at anthesis they are straight (Fig. 14) and three carpels are initiated simulta- or slightly curved (Figs 3, 44) with a round stigma neously (Figs 14–16). There is a massive remnant of (Fig. 45) and the androecial organs are small stami- the floral apex in the centre after carpel initiation nodes (Fig. 44). In male flowers, the carpels are (Fig. 17). The carpel is hemispherical in early devel- reduced and sterile (Fig. 40). opment (Fig. 16) and elongates later (Fig. 17). A lon- gitudinal depression appears on the ventral side of each young carpel (Fig. 24). The slit deepens, the FLORAL DEVELOPMENT IN HOLBOELLIA carpel becomes conduplicate and forms a ventral slit Holboellia grandiflora has pale greenish–white or (Fig. 25). The top of the carpel becomes flattened pale purple unisexual flowers, with six narrowly (Fig. 26) and develops into a horseshoe-shaped, obovate sepals, six ovate petals, six stamens (connec- oblique stigma (Figs 27, 28). tive protrusion small, apiculate) and three carpels The flowers appear bisexual in early development, (Figs 6, 7). but they become functionally unisexual. In male Each flower is subtended by a broad bract (Figs 51, flowers (Figs 1, 19), the carpels stop growing early 52). Six sepals are initiated in two whorls (Figs 52, (Fig. 20). In female flowers, stamens form petaloid 53). Within each whorl, the sepals are initiated suc- staminodes. The connate androecial tube formed by cessively. The first sepal appears on the adaxial side the staminode filaments is shorter than the tube of of the floral apex. The sepal primordium is crescent- the male flower (Fig. 22). The way of anther dehis- shaped (Fig. 53). cence and pollen morphology of the staminodes in the Six petals arise in two whorls when the first three female flowers are the same as in the stamens of the sepals cover the floral apex, with the first three petals male flowers (Figs 19, 22, 23). initiated successively, each opposite the sepals of the first whorl (Figs 54, 55). Three additional petals form a second whorl (Fig. 56). After stamen initiation, the FLORAL DEVELOPMENT IN AKEBIA further development of the petals is suppressed Akebia trifoliata has purple unisexual flowers consist- (Fig. 57) and petals can now be seen in the lateral ing of three to five broadly elliptic sepals, six stamens views of the floral bud because the stamens enlarge and three to nine carpels (Figs 3–5). At the base of the significantly (Figs 58–62). The petals of the second racemes there are one to three female flowers; the whorl even stop developing shortly after initiation upper flowers are male. and are inconspicuous (Fig. 59). Petals are minute Each flower is subtended by a bract, which develops and spathulate in anthetic flowers (Figs 67, 68). only slowly during flower development (Figs 29–30) The androecium has six stamens in two whorls. and is reduced in older stages. The first sepal usually When the sepals cover the floral apex, the first three forms on the adaxial side of the floral apex. The first stamens appear opposite the petals of the first whorl three sepals are initiated successively (Fig. 31) and (Fig. 57) simultaneously before the initiation of the form the first whorl (Fig. 32). Three additional sepals three stamens of the second whorl (Figs 58, 61). The form the second whorl (Figs 32, 33). The sepals of the stamens develop into a long filament and an anther first whorl enlarge normally (Figs 34, 35), whereas with a small apiculate connective protrusion those of the second whorl remain small (Figs 34, 37, (Figs 62–64, 67). 46, 47) or only one or two enlarge (Fig. 48). Thus, at When the six stamens are already large, three anthesis there are only three to five conspicuous carpels arise successively (Fig. 62). They become con- sepals (Figs 49, 50). duplicate (Figs 65, 66, 69–73). The anthetic carpels Six stamens are initiated successively when the have a short inconspicuous style and oblique stigma first three sepals begin to cover the floral apex (Figs 68, 72, 73). (Figs 34, 35) and they are arranged in two whorls The male and female flowers are homomorphic in (Figs 35–37), each opposite one of the sepals. The early developmental stages. In the male flowers, the young stamens are hemispherical (Figs 34, 35) before sterile carpels are shorter than the stamen filaments they differentiate into the anther and filament (Fig. 67). In the female flowers, the staminodes are (Figs 38, 39). At anthesis, the anthers are incurved minute, subsessile (Fig. 68).

Figures 38–50. Stamen and carpel development in Akebia trifoliata. Fig. 38. Flower (sepals removed) with five carpels initiated. Fig. 39. Slightly older stage. Fig. 40. Young male flower, showing sterile carpels. Figures 41–43. Carpel development in female flowers. Fig. 41. Young carpels. Fig. 42. Carpel partly closed. Fig. 43. Carpel closed, conduplicate. Fig. 44. Young female flower, showing carpels and staminodes. Fig. 45. Stigma of carpel of an anthetic flower. Fig. 46. Young male flower, from lateral, showing two reduced sepals of inner whorl (white arrows). Fig. 47. Young male flower, from below; arrowheads show three reduced sepals of inner whorl. Fig. 48. One of the reduced sepals of the inner whorl slightly larger than the other two. Fig. 49. Four well-developed sepals in a young female flower. Fig. 50. Five differently enlarged sepals in a young female flower (reduced sepal marked with arrowhead). A, stamen; C, carpel; S, sepal; Sc, sterile carpel; St, staminode. Scale bars, 100 mm (Figs 38, 46); 150 mm (Fig. 39); 0.6 mm (Figs 40, 47); 0.4 mm (Figs 41, 43, 45); 200 mm (Figs 42, 48); 1 mm (Figs 44, 49, 50). ᭣

DISCUSSION cially obvious: sepals range from four to nine and VARIABILITY OF FLORAL ORGAN NUMBER IN petals from five to seven. Carpels range from ten to 80 in bisexual flowers and only a few sterile carpels to LARDIZABALACEAE none at all in male flowers (Zhang & Ren, 2008). In The double perianth is a key evolutionary innovation Berberidaceae, the complete reduction of the perianth that led to large radiations in angiosperms (Endress, is related to the chaotic floral phyllotaxis in Achlys 2006, 2010). In Lardizabalaceae, the number of sepals DC. (Endress, 1989). In Menispermaceae, flowers are is relatively constant (mostly six, three to five in also mostly trimerous, but with many incidences of Akebia); double perianth (six sepals and six nectarif- increase or decrease of organ number; male flowers erous petals) occurs in Sargentodoxa, Sinofranchetia, usually have a different number of carpels than Holboellia, Parvatia, Stauntonia, Lardizabala and female flowers; a single carpel in female flowers of Boquila (Qin, 1997; Takhtajan, 2009), but petals are Stephania dielsiana Wu may be the results of reduc- absent in the other genera. tion (Kessler, 1993; Endress, 1995; Wang et al., 2006). The perianth has diverse functions (Endress, 2008) and a differentiated perianth has apparently evolved multiple times (Zanis et al., 2003). The biseriate peri- FLORAL PHYLLOTAXIS anth is a matter of progressive readjustment by a Changes in floral phyllotaxis appear to have played a strict arrangement of tepals (Ronse De Craene, 2004) major role in angiosperm evolution, and more in-depth and their nearly simultaneous initiation through studies allow us to trace evolutionary changes in floral shorter plastochrons. Loss of petals in certain families phyllotaxis in ever more detail. The two main patterns has been compensated by petaloidy of the sepals, of floral phyllotaxis are spiral and whorled (Endress, which has occurred before or after total petal loss 1987, 2006). Whorled patterns have often been misin- (Ronse De Craene, 2007). Petaloidy of sepals evolved terpreted as spiral on the basis of the presence of multiple times in Ranunculales (Rasmussen, Kramer parastichies or spiral initiation of organs in basal & Zimmer, 2009). Sepals are all petaloid and are angiosperms, and Endress & Doyle (2007) reviewed relatively attractively coloured, and they could func- the patterns of floral phyllotaxis, including spiral, tion in both protection and optical attraction in whorled and irregular or chaotic phyllotaxis. In early Lardizabalaceae. Shan et al. (2006) reported that diverging angiosperms, floral phyllotaxis is more flex- petaloidy of the perianth is caused by the expression ible and whether the ancestral floral phyllotaxis in of class B genes in Akebia trifoliata. In angiosperms, angiosperms was spiral or whorled is equivocal if the diversification of the B-class gene family has optimized in phylogenetic trees (Endress & Doyle, resulted in the evolution of petaloidy and perianth 2007). dimorphism (Specht & Bartlett, 2009). The present and previous studies show that the Evolution toward secondary simplification is floral phyllotaxis is mostly whorled in Lardizabal- common in angiosperms (Endress, 2006; Endress & aceae, and within each whorl the organs are initiated Doyle, 2009). In Akebia (this study), although six either simultaneously or in a rapid spiral sequence sepals are initiated, all or some of the inner three (Akebia, Sinofranchetia, Sargentodoxa) (this study; sepals are reduced; thus, there are only three to Shan et al., 2006; Zhang & Ren, 2008; Zhang et al., five sepals in mature flowers. In contrast, in Lardiza- 2009). Chaotic patterns tend to occur when floral balaceae, a secondary increase in organ number organs are numerous and their primordia are small occurs in the gynoecium. Three carpels are present in (Endress & Doyle, 2007), and the unordered sequence most of the genera, but three to nine in Akebia,and of carpel initiation in Sargentodoxa may be the result more than 90 in female flowers of Sargentodoxa (Shan of the large number. In Decaisnea, stamens and carpels et al., 2006; Zhang & Ren, 2008; this study). In Sar- are initiated in whorls, whereas the initiation gentodoxa, the variability of organ number is espe- sequence of sepals is spiral, but later they are arranged

Figures 51–62. Floral development in Holboellia grandiflora. Fig. 51. Young inflorescence. Fig. 52. Young flower with initiation of the first three sepals. Fig. 53. The three sepals of the second whorl initiated. Fig. 54. The first three petals initiated (asterisks). Fig. 55. Flower with petals of first whorl. Fig. 56. Initiation of the second three petals (asterisks). Fig. 57. Flower with the first three stamens initiated. Fig. 58. Flower, from the side, one sepal removed, showing one petal of the first whorl with retarded development. Fig. 59. Young flower, from the side, showing one of the inconspicuous petals of the second whorl (arrow). Fig. 60. Young flower, from the side, with enlarged stamen and retarded petals. Fig. 61. Six stamens arranged in two whorls. Fig. 62. Three carpels initiated. A, stamen; C, carpel; P, petal; S, sepal. Scale bars, 0.3 mm (Fig. 51); 100 mm (Figs 52, 57, 58, 59); 50 mm (Figs 53, 54, 55, 56); 120 mm (Figs 60, 61, 62). ᭣ in whorls (this study). In Sinofranchetia, the initiation cally by the androecium and show retarded develop- sequence of the floral organs is spiral, but they are ment (Hiepko, 1965; Kosuge, 1994; Endress, 1995; arranged in whorls in the mature flowers. In Sargento- Ronse De Craene & Smets, 1995). In Ranunculaceae, doxa, the initiation sequence of sepals and petals is petals show obvious characteristics of staminodes spiral, stamens are initiated in two whorls and carpels (Tamura, 1965; Erbar, Kusma & Leins, 1998). In are initiated in whorls or in an unordered manner Berberidaceae, petals are retarded in development to (Zhang & Ren, 2008). The initiation sequence of peri- the extent that they had become strongly linked with anth and carpels of Holboellia is spiral, but stamens the stamens in forming ‘stamen–petal common pri- are initiated in whorls (this study). mordia’; petals probably are evolutionarily heteroge- At the level of Ranunculales, floral phyllotaxis is neous, they may be derived from bracts, tepals or also relatively plastic: whorled phyllotaxis occurs stamens, or a combination of these two (Terabayashi, in Ranunculaceae, Menispermaceae, Berberidaceae, 1983; DeMaggio & Wilson, 1986; Endress, 1987, 1995; Lardizabalaceae and Papaveraceae; spiral phyllotaxis Feng, 1998; Feng & Lu, 1998). In Menispermaceae, does not occur at all in Papaveraceae, and only in six petals are initiated in two whorls or petals Ranunculaceae is it present in a relatively large pro- reduced to two (Wang et al., 2006). Papaveraceae portion of the genera (Endress, 1995). The floral mostly have a multistaminate androecium of many organs have a spiral phyllotaxis in Circaeasteraceae whorls, and three perianth whorls are differentiated (Ren et al., 2004; Tian, Zhang & Ren, 2006). In Ber- into sepals and petals, presumably derived from beridaceae, the initiation of the floral organs is of the bracts (Ronse De Craene, 2003). trimerous whorled pattern, whereas phyllotaxis is Retarded nectariferous petals (nectar leaves) are spiral in the terminal flowers of the inflorescences of often bilobed in Lardizabalaceae (Endress, 1995). Berberis L. (Berberidaceae) (Endress, 1987; Feng, According to the floral development of Sargentodoxa, 1998; Feng & Lu, 1998). In Menispermaceae, floral Sinofranchetia and Holboellia, petals (nectar leaves) phyllotaxis is mostly whorled, but is spiral in a few and stamens are different in shape from the begin- genera (Endress, 1995, 2010; Wang et al., 2006). ning of development (petals flat and rectangular, stamens hemispherical). In Sargentodoxa petals (nectar leaves) show complicated morphology: some ORIGIN OF PETALS petals are staminode-like and some are sepal-like Petals evolved several times in early diverging eud- (Zhang & Ren, 2008). In Holboellia, the petals show icots and were lost several times (Kramer & Irish, greatly retarded development and those of the second 1999, 2000; Kramer, Di Stilio & Schluter, 2003; Zanis whorl even stop developing soon after initiation. et al., 2003; Irish, 2009; Specht & Bartlett, 2009). It has been discussed repeatedly that petals have been CONCLUSIONS derived either from bracts or from sterile stamens (Hiepko, 1965; Takhtajan, 1997; Ronse De Craene, In Lardizabalaceae, sepals are all petaloid (coloured) 2007). B-gene expression plays a role in the develop- and function in both protection and optical attraction. ment of the petals, but it does not clarify petal homol- Secondary simplification is present in Akebia: ogy (Kramer & Irish, 1999; Kramer et al., 2003; Ronse although six sepals are initiated in the early stages, all De Craene, 2007). Arguments used for the identifica- or part of the inner three sepals are reduced later in tion of ‘andropetals’ as opposed to ‘bracteopetals’ are development. In contrast, in Akebia and Sargentodoxa, the vascular arrangement, the ontogeny, teratological the carpel number is secondarily increased. Floral cases and the spatial relation between stamens and phyllotaxis is whorled in Lardizabalaceae and, within petals; however, a strict distinction is not clear each whorl, the organs are initiated either simulta- (Hiepko, 1965; Ronse De Craene, Soltis & Soltis, 2003). neously (e.g. stamens and carpels of Decaisnea, Petals in Ranunculales represent modified stamens stamens of Holboellia) or in a rapid spiral sequence and the petals are strongly influenced morphogeneti- (Akebia, Sinofranchetia, Sargentodoxa, perianth of

Figures 63–73. Stamen and carpel development in Holboellia grandiflora. Fig. 63. Young male flower, from above. Fig. 64. Reduced carpels in a young male flower. Fig. 65. Young female flower, from above. Fig. 66. Carpels, staminodes and petals in a young female flower. Fig. 67. Mature male flower, sepals removed. Fig. 68. Mature female flower, sepals removed. Figures 69–71. Carpel development of female flower. Fig. 69. Young carpel. Fig. 70. Carpel, conduplicate, partly closed. Fig. 71. Carpel closed. Fig. 72. Carpel at anthesis. Fig. 73. Anthetic stigma, enlarged. A, stamen; C, carpel; P, petal; S, sepal; Sc, sterile carpel; St, staminode. Scale bars, 0.6 mm (Figs 63, 66, 73); 0.3 mm (Fig. 64); 200 mm (Figs 65, 70); 1 mm (Figs 67, 68, 72); 50 mm (Figs 69, 71).

Holboellia). The unordered initiation sequence of the Endress PK. 2003. Morphology and angiosperm systematics carpels in Sargentodoxa may be the results of high in the molecular era. The Botanical Review 68: 545– organ number. 570. Petals (nectar leaves) and stamen shapes are dif- Endress PK. 2006. Angiosperm floral evolution: morphologi- ferent from the beginning of development: petals are cal developmental framework. Advances in Botanical flat and rectangular, stamens are hemispherical. Research 44: 1–61. Lardizabalaceae share some floral developmental Endress PK. 2008. Perianth biology in the basal grade of characters with Menispermaceae: flowers are actino- extant angiosperms. International Journal of Plant Sciences 169: 844–862. morphic and trimerous; male and female flowers Endress PK. 2010. Flower structure and trends of evolution have similar organ positions; organs are initiated in eudicots and their major subclades. Annals of the Mis- more or less simultaneously within whorls; the male souri Botanical Garden 97: 541–583. and female flowers are almost homomorphic in early Endress PK, Doyle JA. 2007. Floral phyllotaxis in basal developmental stages (except for few genera, e.g. angiosperms: development and evolution. Current Opinion Stephania of Menispermaceae, Sargentodoxa of in Plant Biology 10: 52–57. Lardizabalaceae). Lardizabalaceae and Berberi- Endress PK, Doyle JA. 2009. Reconstructing the ancestral daceae are similar in retarded petals and the trim- angiosperm flower and its initial specialization. American erous whorled initiation of the floral organs; Journal of Botany 96: 22–66. however, ‘stamen–petal common primordia’ is a Endress PK, Igersheim A. 1999. Gynoecium diversity and general character in Berberidaceae, where petals systematics of the basal eudicots. Botanical Journal of the are retarded in development to the extent that they Linnean Society 130: 305–393. became strongly linked with the stamens in forming Erbar CP, Kusma SK, Leins P. 1998. Development and ‘common primordia’. interpretation of nectary organs in Ranunculaceae. Flora 194: 317–332. ACKNOWLEDGEMENTS Feng M. 1998. The family Berberidaceae: floral development morphology, embryology and systematics. Unpublished D. We sincerely thank two anonymous reviewers for Phil. Thesis, Institute of Botany, Chinese Academy of providing valuable comments and helpful suggestions. Sciences. We would like to thank Ms. Lauren Schewe and Dr. Feng M, Lu AM. 1998. Floral organogenesis and its system- Guosheng Liu (Department of Biology, University of atic significance in the genus Nandina (Berberidaceae). Acta Saskatchewan) for editing the English. We acknowl- Botanica Sinica 40: 102–108. edge Dr. Liang Zhao for his photographs (Figs 1, 2). Hiepko P. 1965. Vergleichend–morphologische und entwick- This work was supported by the Foundation of Key lungsgeschichtliche Untersuchungen über das Perianth bei Laboratory of Medicinal Plant Resource and Natural den Polycarpicae. Botanische Jahrbücher für Systematik 84: Pharmaceutical Chemistry of Ministry of Education of 359–508. China. Hoot SB, Culham A, Crane PR. 1995a. The utility of atpB gene sequences in resolving relationships in the Lardizaba- REFERENCES laceae, including comparisons with rbcL and 18S ribosomal DNA sequences. Annals of the Missouri Botanical Garden APG III. 2009. An update of the Angiosperm Phylogeny 82: 194–207. Group classification for the orders and families of flowering Hoot SB, Culham A, Crane PR. 1995b. Phylogenetic rela- plants: APG III. Botanical Journal of the Linnean Society tionships of the Lardizabalaceae and Sargentodoxaceae: 161: 105–121. chloroplast and nuclear DNA sequence evidence. Plant Sys- Chen DZ. 2001. Lardizabalaceae. In: Ying TS, ed. Flora tematics and Evolution 9: 195–199. reipublicae popularis sinicae. Vol. 29. Beijing: Science Press, Hoot SB, Magallón S, Crane PR. 1999. Phylogeny of basal 2–50. eudicots based on three molecular data sets: atpB, rbcL and Cronquist A. 1981. An integrated system of classification of 18S nuclear ribosomal DNA sequences. Annals of the Mis- flowering plants. New York: Columbia University Press. souri Botanical Garden 86: 1–32. DeMaggio AE, Wilson CL. 1986. Floral structure and orga- Hutchinson J. 1964. The genera of flowering plants nogenesis in Podophyllum peltatum (Berberidaceae). Ameri- (Angiospermae). Vol. 1. Oxford: Clarendon Press. can Journal of Botany 73: 21–32. Irish VF. 2009. Evolution of petal identity. Journal of Experi- Endress PK. 1987. Floral phyllotaxis and floral evolution. mental Botany 60: 2517–2527. Botanische Jahrbücher für Systematik 108: 417–438. Kessler PJA. 1993. Menispermaceae. In: Kubitzki K, Rohwer Endress PK. 1989. Chaotic floral phyllotaxis and reduced JG, Bittrich V, eds. The families and genera of vascular perianth in Achlys (Berberidaceae). Botanica Acta 102: 159– plants II. Berlin: Springer, 402–418. 163. Kofuji R, Udea R, Yamaguchi K, Shimizu T. 1994. Molecu- Endress PK. 1995. Floral structure and evolution in Ranun- lar phylogeny in the Lardizabalaceae. Journal of Plant culanae. Plant Systematics and Evolution 9: 47–61. Research 107: 339–348.

Kosuge K. 1994. Petal evolution in Ranunculaceae. Plant Specht CD, Bartlett ME. 2009. Flower evolution: the origin Systematics and Evolution 8: 185–191. and subsequent diversification of the angiosperm flower. Kramer EM, Irish VF. 1999. Evolution of genetic mecha- Annual Review of Ecology, Evolution, and Systematics 40: nisms controlling petal development. Nature 399: 144–148. 217–243. Kramer EM, Irish VF. 2000. Evolution of the petal and Stapf O. 1925. Sargentodoxa cuneata. Curtis’s Botanical stamen developmental programs: evidence from compara- Magazine 151: 9111–9112. tive studies of the lower eudicots and basal angiosperms. Takhtajan A. 1997. Diversity and classification of flowering International Journal of Plant Sciences 161: S29–S40. plants. New York: Columbia University Press. Kramer EM, Di Stilio VS, Schluter PM. 2003. Complex Takhtajan A. 2009. Flowering plants, 2nd edn. New York: patterns of gene duplication in the APETALA3 and PISTIL- Springer. LATA lineages of the Ranunculaceae. International Journal Tamura M. 1965. Morphology, ecology, and phylogeny of the of Plant Sciences 164: 1–11. Ranunculaceae IV. Science Reports, Osaka University 14: Loconte H, Campbell LM, Stevenson DM. 1995. Ordinal 53–71. and familial relationships of ranunculid genera. Plant Sys- Terabayashi S. 1983. Studies in the morphology and system- tematics and Evolution 9: 99–118. atics of Berberidaceae. VI. Floral anatomy of Diphylleia Qin HN. 1997. A taxonomic revision of the Lardizabalaceae. Michx., Podophyllum L. and Dysosma Woodson. Acta Phy- Cathaya 8-9: 1–214. totaxonomica et Geobotanica 34: 27–47. Rasmussen DA, Kramer EM, Zimmer EA. 2009. One size Thorne RF. 1992. Classification and geography of the flow- fits all? Molecular evidence for a commonly inherited petal ering plants. Botanical Review 58: 225–348. identity program in Ranunculales. American Journal of Tian XH, Zhang L, Ren Y. 2006. Development of flowers and Botany 96: 96–109. inflorescences of Circaeaster (Circaeasteraceae, Ranuncula- Ren Y, Li ZJ, Chang HL, Lei YJ, Lu AM. 2004. Floral les). Plant Systematics and Evolution 256: 89–96. development of Kingdonia (Ranunculaceae s.l., Ranuncula- Van Heel WA. 1983. The ascidiform early development of free les). Plant Systematics and Evolution 247: 145–153. carpels. A SEM investigation. Blumea 28: 231–270. Ren Y, Li HF, Zhao L, Endress PK. 2007. Floral morpho- Wang F. 2001. Phylogeny and Biogeography of the Lardiza- genesis in Euptelea (Eupteleaceae, Ranunculales). Annals of balaceae. Unpublished D. Phil. Thesis, Kunming Institute of Botany 100: 185–193. Botany, The Chinese Academy of Sciencies. Ren Y, Chang HL, Tian XH, Song P, Endress PK. 2009. Wang HC, Meng AP, Li JQ, Feng M, Chen ZD, Wang W. Floral development in Adonideae (Ranunculaceae). Flora 2006. Floral organogenesis of Cocculus orbiculatus and 204: 506–517. Stephania dielsiana (Menispermaceae). International Ren Y, Chang HL, Endress PK. 2010. Floral development Journal of Plant Sciences 167: 951–960. in Anemoneae (Ranunculaceae). Botanical Journal of the Wang HF, Friedman CR, Zhu ZX, Qin HN. 2009a. Early Linnean Society 162: 77–100. reproductive developmental anatomy in Decaisnea and its Ronse De Craene LP. 2003. The evolutionary significance of systematic implications. Annals of Botany 104: 1243–1253. homeosis in flowers: a morphological perspective. Interna- Wang W, Lu AM, Ren Y, Endress ME, Chen ZD. 2009b. tional Journal of Plant Sciences 164: S225–S235. Phylogeny and classification of Ranunculales: evidence from Ronse De Craene LP. 2004. Floral development of Berberi- four molecular loci and morphological data. Perspectives in dopsis corallina: a crucial link in the evolution of flowers in Plant Ecology, Evolution and Systematics 11: 81–110. the core eudicots. Annals of Botany 94: 741–751. Zanis MJ, Soltis PS, Qiu YL, Zimmer E, Soltis DE. 2003. Ronse De Craene LP. 2007. Are petals sterile stamens or Phylogenetic analyses and perianth evolution in basal bracts? The origin and evolution of petals in the core eud- angiosperms. Annals of the Missouri Botanical Garden 90: icots. Annals of Botany 100: 621–630. 129–150. Ronse De Craene LP. 2010. Floral diagrams: an aid to Zhang XH, Ren Y. 2008. Floral morphology and development understanding flower morphology and evolution. New York: of Sargentodoxa (Lardizabalaceae). International Journal of Cambridge University Press. Plant Sciences 169: 1148–1158. Ronse De Craene LP, Smets EF. 1995. Evolution of the Zhang XH, Ren Y, Tian XH. 2009. Floral morphogenesis in androecium in the Ranunculiflorae. Plant Systematics and Sinofranchetia (Lardizabalaceae) and its systematic signifi- Evolution 9: 63–70. cance. Botanical Journal of the Linnean Society 160: 82– Ronse De Craene LP, Soltis PS, Soltis DE. 2003. Evolu- 92. tion of floral structures in basal angiosperms. International Zhao L, Liu P, Che X-F, Wang W, Ren Y. 2011. Floral Journal of Plant Sciences 164: S329–S363. organogenesis of Helleborus thibetanus and Nigella dama- Shan HY, Su KM, Lu WL, Kong HZ, Chen ZD, Meng Z. scena (Ranunculaceae) and its systematic significance. 2006. Conservation and divergence of candidate class B Botanical Journal of the Linnean Society. DOI: 10.1111/ genes in Akebia trifoliata (Lardizabalaceae). Development j.1095-8339.2011.01142.x (in press). Genes and Evolution 216: 785–795. Soltis DE, Soltis PS, Chase MW. 2000. Angiosperm phylogeny inferred from 18S rDNA and atpB sequences. Botanical Journal of Linnean Society 133: 381–461.

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