Floral structure and palynology of Podostemum weddellianum (Podostemaceae: Malpighiales

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The family Podostemaceae is exceptional among angiosperms because of its uncommon biology and morphology, the absence of double fertilisation and endosperm, and the obscure distinction between root, stem, and leaf. The highly modified morphology
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  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   Springer-Verlag 2010 Abstract  The family Podostemaceae is exceptionalamong angiosperms because of its uncommon biology andmorphology, the absence of double fertilisation and endo-sperm, and the obscure distinction between root, stem, andleaf. The highly modified morphology produced byreductions and specialisations is reflected in the multiplepositions that the Podostemaceae has occupied in differentclassification systems. In the family, structural studies aremainly related to the vegetative body. In the genus  Podo-stemum,  structural data are related to the developmentand embryology of   Podostemum ceratophyllum  Michx.,which, with  P. weddellianum , has pre-anthesis cleistogamy. P. weddellianum  is analysed for the first time with regardto floral structure and palynology. The presence of silica inthe spathella, the apical septum in the ovary, dyads andpseudomonads, unimodal embryo sac and chasmogamousflowers with the possibility of self-pollination contribute tothe characterisation of the Podostemoideae and the searchfor relationships among Podostemaceae and the clusioids. Keywords  Malpighiales    Podostemaceae    Podostemum   Flower structure    Anatomy    Palynology Introduction Podostemaceae are the largest family of strictly aquaticangiosperms, encompassing ca. 50 genera and approxi-mately 280 mainly pantropical species (Cook and Rutish-auser, 2007) of perennial or annual herbs. They occurfirmly attached on rocks in river rapids and waterfalls.Brazil is the area of greatest diversity, with 18 genera, sixof them endemic (Philbrick et al. 2010). Podostemaceae stand out among angiosperms becauseof their uncommon biology and morphology—the absenceof double fertilisation and endosperm (Haig 1990; Raghavan 2003) and the obscure distinction between root, stem, andleaf. The family diverges from other aquatic plants in theabsence of aerenchyma, the predominance of sexual overasexual reproduction, the high rate of endemism (Philbrick 1997), and the type of adhesion to the substrate, effected byhaptera on a sticky biofilm of slime-coated cyanobacteria(Ja¨ger-Zu¨rn and Grubert 2000). Flowering is mainly aerial,during the dry season when the low water level exposes theplant to the air (Philbrick  1984). The highly modified morphology produced by reduc-tions and specialisations is reflected in the multiple posi-tions that the Podostemaceae have occupied in differentclassification systems. Once recognised as monocotyle-donous, the family was related later to many differentgroups 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. 2000; Gustafsson et al. 2002; Tokuoka and Tobe 2006; Davis et al. 2005; Korotkova et al. 2009; Wurdack and Davis 2009; Angiosperm phylogeny group 2009) indicated a relationship between Podostemaceae and Hypericaceae.Although morphologically distinct, these taxa shareuncommon characters including the presence of specific 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-EstevesDepartamento de Botaˆnica, Museu Nacional/UFRJ,Rio de Janeiro, Brazile-mail: sahaiad@gmail.com  1 3 Plant Syst Evol (2010) 290:141–149DOI 10.1007/s00606-010-0356-4  idioblasts (resiniferous cells and channels), xanthones, andtenuinucellate ovules. Remarkably, several members of Hypericaceae have an herbaceous habit and live in a wethabitat,  Hypericum elodes  L. being a facultative aquaticspecies (Gustafsson et al. 2002). The diversity observed in Malpighiales is a result of therapid radiation, initiated in the tropical rainforests duringthe Upper Aptian (114 Mya), followed by lineage diver-sification; the Hypericaceae–Podostemaceae clade is themost recent, dating from the Upper Campanian (76 Mya)(Davis et al. 2005). Because of the high specialisation of  Podostemaceae, it is a major challenge to establish struc-tural homologies for them that justify their inclusion in theclusioid clade (Cook and Rutishauser 2007). Podostemum  Michx. consists of 11 species occurring inthe Americas . P. weddellianum  (Tul.) Philbrick and Novelo2004 is a well-represented species restricted to the biomesof the Atlantic rainforest and cerrado in the states of MinasGerais, Espı´rito Santo, Rio de Janeiro, and Sa˜o Paulo inBrazil.In this family, structural studies are mainly related to thevegetative regions (Schnell 1967; Rutishauser 1997; Cusset and Cusset 1988; Ancibor 1990; Imaichi et al. 1999; Hiyama et al. 2002; Suzuki et al. 2002; Fujinami and Imaichi 2009). The development and structure of vegetative andreproductive shoots were recently studied in the Neotropicalspecies  Diamantina lombardii  Novelo, Philbrick & Irgang(Rutishauser et al. 2005), and the African species  Stonesiaghoguei  E. Pfeifer & Rutishauser (Pfeifer et al. 2009) and  Djinga felicis  C. Cusset (Ghogue et al. 2009). Embryological data are increasingly included in phylo-genetic studies, especially at the family level (Simpson2006). In Podostemaceae, such data, mainly embryo sacdevelopment, are used in the infrafamiliar classification(Razi 1949; Mukkada 1969; Battaglia 1971; Nagendran et al. 1977, 1980; Ja ¨ger-Zu¨rn 1997; Murguı ´a-Sa´nchez et al.2002; Sikolia and Ochora 2008; Sikolia and Onyango 2009). Characters from microsporangia, microspores, pol-len grains, ovules, megaspores, and seeds may also beuseful in analyses at several taxonomic levels (Simpson2006). Microsporogenesis was analysed in the context of the subfamily systematics (Ja¨ger-Zu¨rn et al .  2006) andembryology and floral anatomy were studied in  Zeylani-dium subulatum  (Gardner) C. Cusset (referred to as  Podo-stemum subulatum  Gardner in Nagendran et al. 1980), in  Weddellina squamulosa  Tul. (Ja¨ger-Zu¨rn et al. 2006),and in  Vanroyenella plumosa  Novelo & C. T. Philbrick (Murguı´a-Sa´nchez and Ma´rquez-Guzma´n 2001).In the genus  Podostemum,  structural data are related tothe development and embryology of   P. ceratophyllum Michx., (Hammond 1937), which, together with  P. wed-dellianum , has pre-anthesis cleistogamy (Philbrick andVomela 2006).Palynological studies are rare in Podostemaceae, consid-ering the large number of taxa (Erdtman 1952; Bezuidenhout1964; Nair 1965; Lobreau-Callen et al. 1998; Osborn et al. 2000; Passarelli et al. 2002).  Podostemum  species werestudied by O’Neill et al. (1997) and Passarelli et al. (2010). Herein,  P. weddellianum  is analysed with regard tofloral and pollen structure. Materials and methods The plants of   P. weddellianum  (Tul.) C. T. Philbrick &Novelo were collected by the authors. Voucher specimenswere deposited in the Herbarium of the Museu Nacional,Universidade Federal do Rio de Janeiro (R). For anatomi-cal analysis C. Torres, B. Sa´ & M. Ribeiro 1 was used, forpalynological analysis C. P. Bove & C. B. Moreira 856.Flowers and buds were measured for length, fixed in 4%formaldehyde  ?  2.5% glutaraldehyde in 0.05 M sodiumphosphate buffer, pH 7.2 (Gahan 1984), dehydrated in anethanol series, embedded in Historesin  (Leica) in accor-dance with the manufacturer’s recommended procedure,and sectioned with glass knives at 1–3  l m on an AmericanOptical rotary microtome. The sections were stained withtoluidine blue O (Feder and O’brien 1968). For observationof the pollen tubes, sections were stained with aniline blue(0.1%) in 0.15 M K  2 HPO 4  (Martin, 1959), kept at 4  C for2 h, and observed under UV. Measurements and photo-micrographs were obtained by use of an Olympus BX-51microscope with the image-capture system Q color5 andImage-Pro Express software.Histochemical tests were performed to detect the pres-ence of starch, using Lugol (Langeron 1949), and silica,using phenol and clove oil (Johansen 1940). The chemical nature of crystals was determined by differential solubilitytests in acetic acid and hydrochloric acid (Maclean andIvimey-Cook  1952).Palynological analysis was performed in acetolysedmaterial (Erdtman 1960), described, measured up to sevendays later (Salgado-Labouriau 1973) and photographed byuse of an Olympus CX-31 microscope. Non-acetolisedgold-coated material was examined by means of a ZeissDSM 960 scanning electron microscope on carbon-tapedstubs. Twenty-five measurements were taken from dyads infrontal view and from isolated pollen grains from dyads inequatorial view. Apertures and exine thickness values werearithmetical means from ten measurements. The resultspresented in the text are the arithmetic mean and the rangeof variation. Palynological terminology is in accordancewith Punt et al. (2007), taking into account the size, shape, number of apertures, and the pattern of ornamentation of the sexine.All images were processed with Adobe  Photoshop  7.0. 142 B. de Sa´-Haiad et al.  1 3  Results P .  weddellianum  flowers are hermaphroditic, zygomorphic,pedicellate, solitary, axillary or terminal, small (6 mm),and greenish. All organs consist of a one-layered epidermisand a few layers of parenchyma, and vasculature, absent intepals, is composed of undifferentiated elements. Whenpresent, tracheary elements (observed in the pedicel,andropodium, filament, and placenta vasculature) exhibitonly annular thickening.Thepedicel,fromthestageoffloralbudonward(Fig. 1a),has a central vascular unit and starch-rich parenchyma cells(Fig. 1b). The spathella is a non-vascularised lamina, club-shaped, consisting of a one-layered epidermis and one layerof parenchyma at its apex, reaching four layers at the base.Both tissues consist of polygonal, vacuolated, thick-walledcells, which may contain silica bodies (Fig. 1c).Departing from the andropodium, which is plano-con-vex, anatomically similar to the pedicel, and with theadaxial side facing the gynoecium (Fig. 1d), the tepalsemerge: two at each side of the andropodium base and oneon top of the andropodium in the fork between the twofilaments. They are linear, have a loose parenchyma, andlack vascular tissue.The androecium has two stamens. The filament has astarch-rich parenchyma (Fig. 1e) and one central vascularunit (Fig. 1f). The anthers (Fig. 1g) are bithecate, tetral- ocular, introrse, or latrorse and dehisce by means of alongitudinal slit. At anthesis, their wall is composed by onelayer of epidermis, the endothecium with bar thickeningsand a degraded secretory tapetum. Ubisch bodies arepresent in both the tapetum and on the surface of the pollengrains (Fig. 1h). These have a circular outline and densecytoplasm, and are released in dyads (Fig. 1i) or pseudo-monads (Fig. 1i; 2e), because of degeneration of one of the grains. Dyads are acalymmate (Fig. 2a–d) with a mean sizeof (37.5–(45.6)–50.0  l m). Pollen grains are suboblate,medium-sized (DP  =  17.5–(22.9)–25.0  l m; DE  =  25.0–(26.4)–30.0  l m),3-colpatewithspinuloseexine(ca.1.2  l m);and short wide colpi (ca. 7.6  9  3.4  l m). The membrane isdensely ornamented, impeding observation of aperture bor-ders by means of light microscopy. The sexine is almost asthick as the nexine.The ovary is superior, bicarpellate, bilocular and syn-carpous with a circular outline and two multiovulateunequal locules (Fig. 2g, k). The ovary wall (Fig. 2f) is composed of epidermis and three or four parenchyma celllayers, all of them rich in starch grains.The ovarian septum is slender and formed, for the mostpart, by the epidermis of carpels (Fig. 2h). The ovarycontains an apical septum (Fig. 3a). The stigmas are ram-ified, with loose papillae. In flower buds they are adjacentto the anthers (Fig. 3b); dyads (Fig. 3c) and pollen tubes (Fig. 3d) are present on their surface. The transmittingtissue extends from the stigma base to the depressed style(Fig. 3e). The axial placenta is protruding, located at themiddle of the septum, rich in starch grains (Fig. 2i) andvascularised (Fig. 2 j) by a set of elements with walls of variable thickness.Ovules are anatropous, tenuinucellate, and bitegmic. Theinner integument is two cell layers thick, rich in phenoliccompounds, and barely reaches the middle of the embryosac (Fig. 3f). The outer integument is three cell layersthick. Both integuments are rich in starch. The micropyle isexostomal. The embryo sac is surrounded by the nucellarepidermis and protrudes, with the egg apparatus and polarcell, beyond the inner integument. Antipodals are absent(Fig. 3g). The nucellar cells in the chalazal pole have theirwalls degraded, forming the nucellar plasmodium. Discussion In the subfamily Podostemoideae, each floral bud is pro-tected by the spathella, a unique and characteristic struc-ture, generally of uniform thickness, composed of epidermis and 2–3 (–5) layers of parenchyma cells (Ja¨ger-Zu¨rn 2005). The growth of the bud and its frequent uprightposition, coupled with pedicel elongation, lead to spathellarupture at anthesis, as in  P. weddellianum.  The nature of the spathella, however, has been the subject of discussion.Considered as an arillus (Ja¨ger-Zu¨rn 2005) possibly because of the small and coriaceous fruit similar to a seed,the spathella is now interpreted as fused modified bracts,although leaf features are not evident (no vascular tissue ormidrib) in  P. weddellianum  or in  Marathrum foeniculace-um  Humb. & Bonpl. and  M. utile  Tul., Central and SouthAmerican taxa of Podostemoideae. In these species of   Marathrum,  the occurrence of two tips in the youngspathella supports the view that the spathella is formedfrom two fused bracts. It is noteworthy that the decussateposition of the tips is perpendicular to the distichousfoliation of the leaves (Ja¨ger-Zu¨rn 2005). The shoots of   Diamantina  lombardii Novelo, Philbrick & Irgang, a Bra-zilian podostemoid, produce two-flowered units, each onewith a terminal flower surrounded by a tubular spathellaand a lateral flower subtended by an open bract-likespathella (Rutishauser et al. 2005). This genus seems to be one of the most basal in the New World podostemoids(Ruhfel et al. in prep.). So the open bract-like spathella canbe derived from a foliage leaf and should be taken as aplesiomorphic character state within the subfamily Podos-temoideae. In other clusioids, for example the familyClusiaceae, bracts are often in close contact with theperianth parts and do not differ very much from them inform and size. In  Clusia valerioi  Standl., however, these Floral structure and palynology 143  1 3  organs can be differentiated on the basis of their phyllo-taxy. The opposite arrangement can be taken as an indi-cation of bracts, and the spiral order can be taken as typicalof sepals (Hochwallner and Weber 2006). This is also true for  Clusia gundlachii  A. Stahl., in which, based on theirposition, the lowermost pair of organs below the flower istermed bracteoles, although these organs are anatomicallysimilar to the floral organs distal to them (Gustafsson2000). In  Garcinia brasiliensis  Mart., also of the familyClusiaceae, young flower buds are also wrapped by a cup-shaped persistent bracteole that breaks irregularly withgrowth, the fragments being persistent and arranged in thesame decussate phyllotaxy of leaves (D. O. Leal, personalobservation). The presence and arrangement of foliaceousprotective structures, that emerge united or not, may beunderstood,inourview,asa homologyfor theclusioidclade.The presence of amorphous silica bodies in the spathellaof   P. weddellianum  is described here for the first time. Fig. 1 a  line drawing of floralbud without the spathella; b  longitudinal section of thepedicel;  c  cross section of thespathella showing silica bodies( arrows );  d  cross section of thespathella, andropodium, andtepals;  e  longitudinal section of the filament;  f   detail of thefilament vasculature;  g  obliquesection of a dehiscing anther( arrows );  h  longitudinal sectionof the anther locule, showingUbisch bodies on both thetapetum and the microsporesurface;  i  longitudinal section of the anther locule showing dyadsand pseudomonads.  Bars : a  0.5 mm;  f   1  l m;  e  5  l m;  c ,  h , i  10  l m;  d ,  g  20  l m;  b  100  l m; adp , andropodium;  p , pedicel;  sp ,spathella;  tp , tepal. Line drawingby Camila Torres144 B. de Sa´-Haiad et al.  1 3  Deposits of silica can occur from the beginning of devel-opment in all tissues of the plant body, internally orexternally to cells (Prychid et al. 2004). They seem to be related to the reduction of biotic or abiotic stress byreducing transpiration and light transmission, aidingthe maintenance of tissue stiffness, and protecting fromherbivores and pathogens by being a biologically activeelement capable of triggering a broad spectrum of naturaldefences (Currie and Perry 2007). In  P. weddellianum  andother taxa of Podostemaceae it is likely that silica bodies,besides protection, also confer greater strength against theimpactofthestrongcurrentstowhichtheplantsaresubjected.Anatomically, except for the presence of silica bodies, thespathella of   P. weddellianum  resembles those described byJa¨ger-Zu¨rn (2005) for  M. utile  Tul. and  M. foeniculatum Humb. and Bonpl. The observed lack of clear differentiationbetween phloem and xylem is characteristic of the family(Cook and Rutishauser 2007; Ghogue et al. 2009). Fig. 2 a – c  dyad:  a  opticalsection (LM);  b  different focalplanes of the sexine (LM); c  general view (SEM);  d  surfacedetail (SEM);  e  pseudomonad(aborted pollen grain); f   longitudinal section of theovary wall;  g ,  i ,  k  cross sectionsof the ovary:  g  proximal portion i  mid-level portion  k  distalportion;  h  detail of the slenderseptum;  j  detail of the singlecentral vascular bundle thatoccurs in the axial placenta.  Bars :  d  1  l m;  a ,  b ,  c  5  l m;  e ,  f  , h ,  j  10  l m;  g ,  i ;  k  100  l mFloral structure and palynology 145  1 3
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