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Developmental Morphology of Branching Flowers in Nymphaea

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Developmental Morphology of Branching Flowers in Nymphaea J Plant Res (2006) 119:561–570 DOI 10.1007/s10265-006-0021-8 REGULAR PAPER Developmental morphology of branching flowers in Nymphaea prolifera Valentin Grob Æ Philip Moline Æ Evelin Pfeifer Æ Alejandro R. Novelo Æ Rolf Rutishauser Received: 16 March 2006 / Accepted: 29 May 2006 / Published online: 5 October 2006 Ó The Botanical Society of Japan and Springer-Verlag 2006 Abstract Nymphaea and Nuphar (Nymphaeaceae) Introduction share an extra-axillary mode of floral inception in the shoot apical meristem (SAM). Some leaf sites along Water lilies have attracted botanical systematists for at the ontogenetic spiral are occupied by floral primordia least 200 years. Nymphaeales (Nymphaeaceae and lacking a subtending bract. This pattern of flower ini- Cabombaceae) comprise eight genera and approxi- tiation in leaf sites is repeated inside branching flowers mately 70 species of aquatic plants, with a worldwide of Nymphaea prolifera (Central and South America). distribution in tropical to temperate regions. Whereas Instead of fertile flowers this species usually produces the stem lineage of Nymphaeales is old based on fossil sterile tuberiferous flowers that act as vegetative evidence (125–115 million years ago), molecular dating propagules. N. prolifera changes the meristem identity indicates that the extant nymphaealean genera diver- from reproductive to vegetative or vice versa repeat- sified relatively recently, i.e., not earlier than approxi- edly. Each branching flower first produces some peri- mately 46 million years ago (Gandolfo et al. 2004; Yoo anth-like leaves, then it switches back to the vegetative et al. 2005). Features like scattered vascular bundles, meristem identity of the SAM with the formation of embryological data, cotyledonary and floral structure foliage leaves and another set of branching flowers. have linked them to monocots, especially to the Alis- This process is repeated up to three times giving rise to matidae (Les and Schneider 1995). Molecular data more than 100 vegetative propagules. The develop- corroborate the recent morphological understanding of mental morphology of the branching flowers of N. the relationship among basal angiosperms: Amborella prolifera is described using both microtome sections as the basal-most angiosperm is sister to all extant and scanning electron microscopy. angiosperms, with Nymphaeales being the first branch after Amborella (Zanis et al. 2002; APG II 2003;Lo¨ hne Keywords AGAMOUS Æ Floral reversion Æ and Borsch 2005; Qiu et al. 2005; Soltis et al. 2005). All Homeosis Æ Meristem identity Æ Nymphaea prolifera Æ Nymphaeales share several morphological characters, Proliferated flowers e.g., rhizomatous stems, solitary flowers, acropetal initiation of floral organs, radial floral symmetry, simultaneous initiation of the carpels in a whorl, and formation of a vascular plexus at the base of the flower. Floral characters vary extensively among genera, & V. Grob Æ P. Moline Æ E. Pfeifer Æ R. Rutishauser ( ) ranging from the small, simple monocot-like flowers of Institut fu¨ r Systematische Botanik, Universita¨tZu¨ rich, Zollikerstrasse 107, 8008 Zurich, Switzerland Cabomba to the large, showy, elaborate flowers of e-mail: [email protected] Nymphaea and Victoria (Les et al. 1999; Ronse De Craene et al. 2003; Schneider et al. 2003; Soltis and A. R. Novelo Soltis 2004; Yoo et al. 2005). Departamento de Bota´nica, Instituto de Biologı´a, Universidad Nacional Auto´ noma de Me´xico, Most angiosperms show axillary branching, where a Mexico, D.F. 04510, Mexico lateral bud is subtended by a leaf or bract. Nymphae- 123 562 J Plant Res (2006) 119:561–570 ales, however, show various deviating patterns with completely white flowers that have sepals that are respect to flower positioning at the shoot apex. For usually shorter and narrower than the outer petals, and example, flowers of Victoria and Euryale arise in carpellary appendages with tips that are mostly less nonmedian axillary positions to the associated leaf or than 1.5 mm thick (Wiersema 1987). seemingly so (Cutter 1961; Weidlich 1980), whereas in The purpose of this paper is to explore the devel- Nuphar and Nymphaea each flower replaces a leaf in opmental morphology of the repeatedly branching the ontogenetic spiral of the shoot apex (Cutter 1961; flowers of N. prolifera using both microtome sections Chassat 1962; Weidlich 1976a, 1976b; Les et al. 1999; and scanning electron microscopy: Schneider et al. 2003). 1. We ask if the meristem of branching flowers of N. The genus Nymphaea consists of approximately 45 prolifera mirrors the pattern of the SAM of other species of aquatic herbs with perennial rhizomes, Nymphaea spp. such as N. alba mostly floating leaves and showy flowers. The bractless 2. We search for comparable patterns in the Nymp- flowers have mostly tetramerous calyces, whereas the haeaceae and other vascular plants other flower organs occur in whorls or rings of many 3. We discuss the observed patterns in the light of members. The petals are white, blue, red or yellow in developmental genetic findings various shades (Wiersema 1987). Nymphaea prolifera Wiersema belongs to the neo- tropic and night-flowering subgenus Hydrocallis, which Materials and methods according to molecular data is a basal division of the genus (Borsch et al. 1998). This species was originally The material of N. prolifera Wiersema used for this described by Wiersema (1984, 1987) from Argentina study was collected in the Reserva de la Biosphera (Corrientes). Since then it has also been found in ‘‘Pantanos de Centla,’’ Estado de Tabasco, Mexico (1 Brazil: Mato Grosso and Mato Grosso do Sul (Pott November 1998). The material of N. alba L. was col- 1998), and in Paraguay (Ritter et al. 2001), Ecuador lected from plants cultivated in the Botanical Garden (Cornejo and Bonifaz 2003), and Mexico (Olvera and of the University of Zurich (Switzerland). The material Lot 1991). Fruits and seeds are rarely, if ever, produced was fixed and preserved in 70% ethanol. For scanning in N. prolifera. Propagation seems to rely mostly, if not electron microscopy, the dissected material was critical exclusively, on the tuberiferous (sterile) flowers. In- point dried and sputter coated (Au). The micrographs stead of sexual reproduction, these flowers are tubers, were taken with scanning electron microscopes Cam- giving rise to another set of leaves and tuberiferous bridge S4 and JEOL. For microtome sections, speci- flowers. The floral meristem, which starts with the mens were embedded in Kulzer’s Technovit (2- development of the perianth, switches back to an hydroethyl methacrylate), as described by Igersheim indeterminate, vegetative meristem. This ‘‘sleeping’’ and Cichocki (1996), and sectioned with a MICROM shoot apical meristem (SAM) starts the establishment HM 355 rotary microtome and conventional micro- of a new rhizome as soon as the detached flower has tome knife types C and D. The mostly 7-lm thick dropped to the ground. This is an effective way of sections were stained with ruthenium red and toluidine asexual propagation, as hundreds of tiny tubers, al- blue (Weber and Igersheim 1994). The permanent ready complete with juvenile leaves and roots, can be slides of the microtome sections are deposited at the released from a single individual (Wiersema 1987). N. Institute of Systematic Botany, University of Zurich prolifera seems to occur with a disjunct pattern within (Z). Fixed and dry voucher specimens (Novelo 3347) of the species area of Nymphaea amazonum, a close rel- N. prolifera are housed in the Herbarium of Zurich ative of N. prolifera. Overall, the morphology of N. Universities (Z/ZT); dry material is also deposited in the amazonum and that of N. prolifera are very similar. Herbarium of UNAM (Mexico). The authorities of Cornejo and Bonifaz (2003) even observed N. additional species names mentioned in the text are amazonum individuals with tuberiferous flowers. equivalent to the species and author names given by Wiersema (1987) found potential hybrids in Argentina, Wiersema (1987). propagating entirely via tuberiferous flowers. They were triploid (3n=27) compared with the diploid (2n=18) mother species. Wiersema (1984, 1987) sepa- rated the two species in that N. prolifera lacks pubes- Results cence on the petioles. Moreover, N. prolifera usually has a few inconspicuous green sepaloid organs instead The measurements in the following description are of white petals. Rarely, N. prolifera produces based on our own observations in the field (Tabasco, 123 J Plant Res (2006) 119:561–570 563 Mexico). They may deviate to some degree from the leaves arising from this rooted tuber consist of cylin- measurements given by Wiersema (1987). drical stalks (petioles) up to 1.2 m long. Their base is provided with two attached lateral stipules that are Leaves and branching flowers arising from rooted fused to some degree along the adaxial leaf insertion tubers zone (Figs. 2a, 4e, f). Stipules of mature leaves are attached to a slightly broadened leaf sheath 4–7 cm N. prolifera is a perennial aquatic herb, as typical for long. The suborbicular to reniform leaf blades are up to most Nymphaeaceae (Fig. 1a–d). The rhizome of this 20 cm wide with a slight tendency towards peltation species consists of an erect and nearly spherical tuber (Fig. 1d). The rooted tubers (rhizomes) also produce or caudex 2–2.5 cm in diameter. Its lower side is fixed flowers on stalks up to 80 cm long. This first set of to the muddy soil by several contractile roots. Mature branching flowers will be called here mother flowers, Fig. 1 Nymphaea prolifera. Plants photographed in the field: (arrow). This mother flower gives rise to seven daughter flowers Reserva de la Biosphera ‘‘Pantanos de Centla,’’ Estado de (F, one removed) and three stalked leaves (L). One daughter Tabasco, Mexico (1st November 1998, photographs by R. flower already with outgrowing granddaughter flowers (F¢). c Rutishauser). a Mother flower (F) with daughter flowers (F¢) The only flower (F) found to have an increased number and granddaughter flowers (F†).
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