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COMPARATIVE STRUCTURE of the OSMOPHORES in the FLOWER of Stanhopea Graveolens Lindley and Cycnoches Chlorochilon Klotzsch (ORCHIDACEAE)

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COMPARATIVE STRUCTURE of the OSMOPHORES in the FLOWER of Stanhopea Graveolens Lindley and Cycnoches Chlorochilon Klotzsch (ORCHIDACEAE) ACTA AGROBOTANICA Vol. 65 (2): 11–22 2012 COMPARATIVE STRUCTURE OF THE OSMOPHORES IN THE FLOWER OF Stanhopea graveolens Lindley AND Cycnoches chlorochilon Klotzsch (ORCHIDACEAE) 1Sebastian Antoń, 1Magdalena Kamińska, *1,2Małgorzata Stpiczyńska 1Department of Botany, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland 2University of Warsaw, Botanic Garden, Al. Ujazdowskie 4, 00-478 Warszawa, Poland *e-mail: [email protected] Received: 20.02.2012 Abstract common and widespread reward for pollinators is The structure of the osmophores in Stanhopea grave- nectar (van der Cingel, 2001). Moreover, some olens and Cycnoches chlorochilon was studied by means of representatives of Oncidiinae, e.g. Oncidium, Ornitho- light microscopy (LM), scanning electron microscopy (SEM) phora, Gomesa, reward pollinators with lipid-rich sub- and transmission electron microscopy (TEM). The scent glands stances (Stpiczyń ska and Davies, 2008; Ali- are located in the basal part of the labellum. The surface of the scioni et al. 2009). Some species offer both nectar osmophores is wrinkled or rugose, which increases the area of and fragrance reward, such as Cyclopogon elatus (Sw.) fragrance emission. On the surface of the epidermis, remnants of Schltr (Wiemer et al. 2009), or oil and fragrance, secretion are noticeable in S. graveolens, but these are absent in such as Grobya amherstiae Lindl. (Pansarin et al. C. chlorochilon. The osmophore tissue is composed of secretory 2009), whereas many other species offer exclusively epidermal cells and several layers of subepidermal parenchyma, floral fragrances as secondary floral attractants, e.g. and it is supplied by vascular bundles that run in ground paren- chyma. The secretory cells have large nuclei, a dense cytoplasm Gongora, Catasetum, Stanhopea, Cymbidium (Wil- with numerous ER profiles, lipid droplets, and plastids with a liams & Whitten, 1983; Stpiczyń ska, substantial amount of starch, which are probably involved in the 1993; Martini et al. 2003). synthesis of volatile substances. In the cell walls of the osmo- Floral fragrances are produced by the osmopho- phore cells, numerous pits with plasmodesmata occur that are li- res (scent glands) occurring in a large group of plants kely to take part in symplastic transport of the scent compounds. (Vogel, 1990; Dressler, 1993). In euglossino- The structure of the osmophores is similar in both investigated philous orchids scent is a combination of terpenes and species. Both S. graveolens and C. chlorochilon are pollinated aromatics (Williams & Whitten, 1983) and by euglossine bees, and such similarity results from adaptation functions as an attractant for male euglossine bees (tri- to effective scent emission and attraction of pollinators. be Euglossini, Apidae). It is collected from the flower surface and stored in specialized hind tibiae of these Key words: micromorphology, ultrastructure, histochemistry, sec- bees (Dressler, 1982). Fragrance is used as a pre- retory tissue, scent glands, Stanhopea, Cycnoches, cursor for a sex pheromone (Stern et al. 1987; V o - Epidendroideae gel, 1990; van der Cingel, 2001). Flowers of orchids are not the exclusive source of floral fragrance INTRODUCTION for euglossine bees, and this mutualistic relationship is not symmetric, as the bees can collect fragrances from Orchids expanded various adaptations to polli- the flowers of other genera such as Spathiphyllum, An- nation and their flowers provide several kinds of plant- thurium (Araceae), Drymonia and Gloxinia (Gesneria- -pollinator interactions (Dressler, 1993; van der ceae), Cyphomandra (Solanaceae), Dalechampia (Eu- Cingel, 2001). Since the pollen in Orchidaceae may phorbiaceae) (Williams & Whitten, 1983 and be used as food only in primitive species, e.g. Neu- references therein). Nevertheless, Pemberton and wiedia (Kocyan and Endress, 2001), the most Wheeler (2006) reported that an equally valuable 12 Sebastian Antoń, Magdalena Kamińska, Małgorzata Stpiczyńska source of essential oils for euglossine bees were leaves MATERIALS AND METHODS of Ocimum basilicum L., Pimenta dioica (L.) Merr or Melaleuca quinquenervia (Cav.) S.T. Blake. However, The plants of Stanhopea graveolens Lindl. and the reason why these bees collect fragrances is not en- Cycnoches chlorochilon Klotzsch used in this study tirely clear. are cultivated in the greenhouses of the Botanic Gar- In orchids, osmophores may be located on the den of the University of Warsaw. adaxial surface of sepals, petals, or part of the lip In the case of S. graveolens, osmophore tissue (Dressler, 1993). Such surface can be smooth or was sampled at the bud stage (buds 3-4 cm long, abo- covered by papillae, unicellular trichomes, as in Stan- ut one week before anthesis) and, additionally, on the hopea saccata Bateman (Curry et al. 1991), pear- second day of anthesis (Fig. 1 A-B), whereas from C. -shaped or spherical unicellular hairs with irregular chlorochilon this tissue was sampled exclusively from cuticle in Cymbidium tracyanum Rolfe (Stpiczyń - male flowers on the 7th-10th day of anthesis. The osmo- ska, 1993), dome-shaped papillae in Ophrys lutea phores were examined with light microscopy (LM), (Ascensãno et al. 2005), or papillose cells with scanning electron microscopy (SEM) and transmission smooth cuticle in Acianthera (de Melo et al. 2010). electron microscopy (TEM). Freshly cut pieces of se- Stanhopea graveolens Lindley (Stanhopeinae) cretory tissue (about 3×3 mm) were fixed with 2.5% and Cycnoches chlorochilon Klotzsch (Catasetinae) are glutaraldehyde in 0.1 M phosphate buffer at a pH of fragrant orchids pollinated exclusively by male euglos- 7.4 at room temperature for 2 h, and then washed in sine bees (Williams & Whitten, 1983). Dura- phosphate buffer. Afterwards, the material was post-fi- tion of flowering and the period of fragrance secretion xed in 1.5% osmium tetroxide for 1.5 h and washed in are significantly diverse in both species. In Cycnoches, distilled water. The fixed material was dehydrated in a anthesis lasts weeks, as long as the pollinia remain in- graded ethanol series, infiltrated and embedded in LR tact, whereas in Stanhopea flowers last only three days White resin. The embedded material was cut at 60 nm (Vogel, 1990). Cycnoches is well known for produ- for TEM using a Reichert Ultracut-S ultramicrotome cing sexually dimorphic flowers and non-functional and a glass knife, stained with uranyl acetate and post- intermediate flowers are occasionally formed as well -stained in lead citrate (Reynolds, 1963). Then, the (Dressler, 1993). The lip in Cycnoches is upper sections were examined with an FEI Technai G2 Spirit due to the fact that these flowers are not resupinated Bio TWIN transmission electron microscope, at an ac- (Bechtel et al. 1980). The hypochile is separated celerating voltage of 120 kV. TEM images were taken from the epichile by dark green waxy callus. Also, the using a Megaview G2 Olympus Soft Imaging Solution labellum of Cycnoches has an enormous thickness (up camera. to 9 mm thick) and represents the most voluminous For light microscopy, pieces of osmophores osmophore in Orchidaceae (V ogel, 1990). were prepared as described for TEM, but resin blocks In Orchidaceae, the structure of osmophores were cut into semi-thin sections (0.9-1.0 μm thick) has been studied with light microscopy (Vogel, and stained with 1% (w/v) aqueous methylene blue- 1990; Pansarin et al. 2009) and both scanning and -Azur B solution for general histology. The presence transmission electron microscopy (Stern et al. 1987; of insoluble polysaccharides was tested with PAS sta- Curry et al. 1991; Stpiczyń ska, 1993; Stpi- ining (Jensen, 1962). Additionally, hand-cut sec- czyń ska, 2001; Wiemer et al. 2009; d e Melo tions were made using a razor blade and then tested et al. 2010). In the literature there are some detailed for starch presence with Lugol’s iodine solution (IKI). data on the structure of osmophores in several spe- For lipids, the tissue was stained with alcoholic Sudan cies of Stanhopea (Stern et al. 1987; Curry et al. III (in hand-cut sections) and Auramine O (in semi- 1991), but up to now the studies on the structure of the -thin sections); in the latter, the staining reaction was large and elaborated osmophore gland in Stanhopea examined by means of a Nikon Eclipse 90i microscope graveolens has been neglected. Also, there have been equipped with a fluorescein isothiocyanate filter. Also, no anatomical studies of the osmophores in Cycnoches the autofluorescence of chlorophyll in plastids was te- chlorochilon at all. sted in C. chlorochilon using a Nikon Eclipse 90i flu- The purpose of this study was to investigate orescence microscope with a UV-2B filter. and compare the micromorphology and ultrastructure For the observations of the surface of the se- of the osmophores in Stanhopea graveolens and Cyc- cretory epidermis, pieces of osmophore tissue were noches chlorochilon using light microscopy, scanning dehydrated in acetone, then subjected to critical-point and transmission electron microscopy. We selected drying using liquid CO2, sputter-coated with gold and these species because of significant differences in the examined by means of a TESCAN/VEGA LMU scan- flower life-span and, at the same time, the difference in ning electron microscope, at an accelerating voltage of the functioning of these secretory glands. 30 kV. Comparative structure of the osmophores in the flower of Stanhopea graveolens Lindley and Cycnoches chlorochilon... 13 RESULTS In the flowers of S. graveolens, the surface of the osmophores is rugose (Fig. 1C-F) at the two sta- Stanhopea graveolens ges investigated. In buds, the cuticle covering the epi- The labellum of Stanhopea graveolens is com- dermal cells is slightly wrinkled (Fig. 1C), whereas in posed of three parts: basal hypochile, mesochile and open flowers it is highly sculptured, mainly at the tip distal epichile. The hypochile bears osmophore. The parts of the rugae (Fig. 1D). On the surface of the epi- petals and sepals are faintly orange to yellow, while dermis, remnants of secretion and a distended cuticle the hypochile is strongly orange (Fig.
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