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Comparative Floral Development in Lardizabalaceae (Ranunculales)

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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 function- ally 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, © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 171–184 171 172 X.-H. ZHANG and Y. REN 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). © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 171–184 FLORAL DEVELOPMENT OF LARDIZABALACEAE 173 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 © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 171–184 174 X.-H. ZHANG and Y. REN © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 171–184 FLORAL DEVELOPMENT OF LARDIZABALACEAE 175 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
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