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Floral Structure and Palynology of Podostemum Weddellianum (Podostemaceae: Malpighiales)

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Floral Structure and Palynology of Podostemum Weddellianum (Podostemaceae: Malpighiales) Plant Syst Evol (2010) 290:141–149 DOI 10.1007/s00606-010-0356-4 ORIGINAL ARTICLE Floral structure and palynology of Podostemum weddellianum (Podostemaceae: Malpighiales) B. de Sa´-Haiad • C. A. Torres • V. H. R. de Abreu • M. R. Gonc¸alves • C. B. F. Mendonc¸a • L. D. R. de Santiago-Fernandes • C. P. Bove • V. Gonc¸alves-Esteves Received: 30 May 2010 / Accepted: 6 September 2010 / Published online: 5 October 2010 Ó Springer-Verlag 2010 Abstract The family Podostemaceae is exceptional Introduction among angiosperms because of its uncommon biology and morphology, the absence of double fertilisation and endo- Podostemaceae are the largest family of strictly aquatic sperm, and the obscure distinction between root, stem, and angiosperms, encompassing ca. 50 genera and approxi- leaf. The highly modified morphology produced by mately 280 mainly pantropical species (Cook and Rutish- reductions and specialisations is reflected in the multiple auser, 2007) of perennial or annual herbs. They occur positions that the Podostemaceae has occupied in different firmly attached on rocks in river rapids and waterfalls. classification systems. In the family, structural studies are Brazil is the area of greatest diversity, with 18 genera, six mainly related to the vegetative body. In the genus Podo- of them endemic (Philbrick et al. 2010). stemum, structural data are related to the development Podostemaceae stand out among angiosperms because and embryology of Podostemum ceratophyllum Michx., of their uncommon biology and morphology—the absence which, with P. weddellianum, has pre-anthesis cleistogamy. of double fertilisation and endosperm (Haig 1990;Raghavan P. weddellianum is analysed for the first time with regard 2003) and the obscure distinction between root, stem, and to floral structure and palynology. The presence of silica in leaf. The family diverges from other aquatic plants in the the spathella, the apical septum in the ovary, dyads and absence of aerenchyma, the predominance of sexual over pseudomonads, unimodal embryo sac and chasmogamous asexual reproduction, the high rate of endemism (Philbrick flowers with the possibility of self-pollination contribute to 1997), and the type of adhesion to the substrate, effected by the characterisation of the Podostemoideae and the search haptera on a sticky biofilm of slime-coated cyanobacteria for relationships among Podostemaceae and the clusioids. (Ja¨ger-Zu¨rn and Grubert 2000). Flowering is mainly aerial, during the dry season when the low water level exposes the Keywords Malpighiales Á Podostemaceae Á Podostemum Á plant to the air (Philbrick 1984). Flower structure Á Anatomy Á Palynology The highly modified morphology produced by reduc- tions and specialisations is reflected in the multiple posi- tions that the Podostemaceae have occupied in different classification systems. Once recognised as monocotyle- donous, the family was related later to many different groups of monocots or dicots (Van Royen 1951) and is currently included in the order Malpighiales (Soltis et al. 1999). Later studies (Soltis et al. 2000; Savolainen et al. B. de Sa´-Haiad (&) Á C. A. Torres Á V. H. R. de Abreu Á 2000; Gustafsson et al. 2002; Tokuoka and Tobe 2006; M. R. Gonc¸alves Á C. B. F. Mendonc¸a Á Davis et al. 2005; Korotkova et al. 2009; Wurdack and L. D. R. de Santiago-Fernandes Á C. P. Bove Á Davis 2009; Angiosperm phylogeny group 2009) indicated V. Gonc¸alves-Esteves a relationship between Podostemaceae and Hypericaceae. Departamento de Botaˆnica, Museu Nacional/UFRJ, Rio de Janeiro, Brazil Although morphologically distinct, these taxa share e-mail: [email protected] uncommon characters including the presence of specific 123 142 B. de Sa´-Haiad et al. idioblasts (resiniferous cells and channels), xanthones, and Palynological studies are rare in Podostemaceae, consid- tenuinucellate ovules. Remarkably, several members of ering the large number of taxa (Erdtman 1952;Bezuidenhout Hypericaceae have an herbaceous habit and live in a wet 1964; Nair 1965; Lobreau-Callen et al. 1998;Osbornetal. habitat, Hypericum elodes L. being a facultative aquatic 2000; Passarelli et al. 2002). Podostemum species were species (Gustafsson et al. 2002). studied by O’Neill et al. (1997) and Passarelli et al. (2010). The diversity observed in Malpighiales is a result of the Herein, P. weddellianum is analysed with regard to rapid radiation, initiated in the tropical rainforests during floral and pollen structure. the Upper Aptian (114 Mya), followed by lineage diver- sification; the Hypericaceae–Podostemaceae clade is the most recent, dating from the Upper Campanian (76 Mya) Materials and methods (Davis et al. 2005). Because of the high specialisation of Podostemaceae, it is a major challenge to establish struc- The plants of P. weddellianum (Tul.) C. T. Philbrick & tural homologies for them that justify their inclusion in the Novelo were collected by the authors. Voucher specimens clusioid clade (Cook and Rutishauser 2007). were deposited in the Herbarium of the Museu Nacional, Podostemum Michx. consists of 11 species occurring in Universidade Federal do Rio de Janeiro (R). For anatomi- the Americas. P. weddellianum (Tul.) Philbrick and Novelo cal analysis C. Torres, B. Sa´ & M. Ribeiro 1 was used, for 2004 is a well-represented species restricted to the biomes palynological analysis C. P. Bove & C. B. Moreira 856. of the Atlantic rainforest and cerrado in the states of Minas Flowers and buds were measured for length, fixed in 4% Gerais, Espı´rito Santo, Rio de Janeiro, and Sa˜o Paulo in formaldehyde ? 2.5% glutaraldehyde in 0.05 M sodium Brazil. phosphate buffer, pH 7.2 (Gahan 1984), dehydrated in an In this family, structural studies are mainly related to the ethanol series, embedded in HistoresinÒ (Leica) in accor- vegetative regions (Schnell 1967; Rutishauser 1997; Cusset dance with the manufacturer’s recommended procedure, and Cusset 1988; Ancibor 1990; Imaichi et al. 1999; and sectioned with glass knives at 1–3 lm on an American Hiyama et al. 2002; Suzuki et al. 2002;FujinamiandImaichi Optical rotary microtome. The sections were stained with 2009). The development and structure of vegetative and toluidine blue O (Feder and O’brien 1968). For observation reproductive shoots were recently studied in the Neotropical of the pollen tubes, sections were stained with aniline blue species Diamantina lombardii Novelo, Philbrick & Irgang (0.1%) in 0.15 M K2HPO4 (Martin, 1959), kept at 4°C for (Rutishauser et al. 2005), and the African species Stonesia 2 h, and observed under UV. Measurements and photo- ghoguei E.Pfeifer&Rutishauser(Pfeiferetal.2009)and micrographs were obtained by use of an Olympus BX-51 Djinga felicis C. Cusset (Ghogue et al. 2009). microscope with the image-capture system Q color5 and Embryological data are increasingly included in phylo- Image-Pro Express software. genetic studies, especially at the family level (Simpson Histochemical tests were performed to detect the pres- 2006). In Podostemaceae, such data, mainly embryo sac ence of starch, using Lugol (Langeron 1949), and silica, development, are used in the infrafamiliar classification using phenol and clove oil (Johansen 1940). The chemical (Razi 1949; Mukkada 1969; Battaglia 1971; Nagendran nature of crystals was determined by differential solubility et al. 1977, 1980;Ja¨ger-Zu¨rn 1997; Murguı´a-Sa´nchez et al. tests in acetic acid and hydrochloric acid (Maclean and 2002; Sikolia and Ochora 2008; Sikolia and Onyango Ivimey-Cook 1952). 2009). Characters from microsporangia, microspores, pol- Palynological analysis was performed in acetolysed len grains, ovules, megaspores, and seeds may also be material (Erdtman 1960), described, measured up to seven useful in analyses at several taxonomic levels (Simpson days later (Salgado-Labouriau 1973) and photographed by 2006). Microsporogenesis was analysed in the context of use of an Olympus CX-31 microscope. Non-acetolised the subfamily systematics (Ja¨ger-Zu¨rn et al. 2006) and gold-coated material was examined by means of a Zeiss embryology and floral anatomy were studied in Zeylani- DSM 960 scanning electron microscope on carbon-taped dium subulatum (Gardner) C. Cusset (referred to as Podo- stubs. Twenty-five measurements were taken from dyads in stemum subulatum Gardner in Nagendran et al. 1980), frontal view and from isolated pollen grains from dyads in in Weddellina squamulosa Tul. (Ja¨ger-Zu¨rn et al. 2006), equatorial view. Apertures and exine thickness values were and in Vanroyenella plumosa Novelo & C. T. Philbrick arithmetical means from ten measurements. The results (Murguı´a-Sa´nchez and Ma´rquez-Guzma´n 2001). presented in the text are the arithmetic mean and the range In the genus Podostemum, structural data are related to of variation. Palynological terminology is in accordance the development and embryology of P. ceratophyllum with Punt et al. (2007), taking into account the size, shape, Michx., (Hammond 1937), which, together with P. wed- number of apertures, and the pattern of ornamentation of dellianum, has pre-anthesis cleistogamy (Philbrick and the sexine. Vomela 2006). All images were processed with AdobeÒ PhotoshopÒ 7.0. 123 Floral structure and palynology 143 Results (Fig. 3d) are present on their surface. The transmitting tissue extends from the stigma base to the depressed style P. weddellianum flowers are hermaphroditic, zygomorphic, (Fig. 3e). The axial placenta is protruding, located at the pedicellate, solitary, axillary or terminal, small (6 mm), middle of the septum, rich in starch grains (Fig. 2i) and and greenish. All organs consist of a one-layered epidermis vascularised (Fig. 2j) by a set of elements with walls of and a few layers of parenchyma, and vasculature, absent in variable thickness. tepals, is composed of undifferentiated elements. When Ovules are anatropous, tenuinucellate, and bitegmic. The present, tracheary elements (observed in the pedicel, inner integument is two cell layers thick, rich in phenolic andropodium, filament, and placenta vasculature) exhibit compounds, and barely reaches the middle of the embryo only annular thickening. sac (Fig. 3f). The outer integument is three cell layers The pedicel, from the stage of floral bud onward (Fig.
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