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Anatomy and Morphology |
2Centro de Biotecnologia Vegetal, Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Bloco C2, Campo Grande, 1749-016 Lisboa, Portugal; 3Laboratório de Biotecnologia Vegetal, Instituto de Ciência Aplicada e Tecnologia, Faculdade de Ciências da Universidade de Lisboa, Edifício ICAT, Campo Grande, 1749-016 Lisboa, Portugal
Received for publication January 6, 2005. Accepted for publication March 31, 2005.
ABSTRACT
The morphology and anatomy of the labellar epidermal cells and the way in which they are arranged are described in an attempt to locate and characterize the osmophore in Ophrys fusca and O. lutea. The micromorphology of the labellum of these two species is similar. Four types of epidermal cells are present on the adaxial surface of the labellum. Long unicellular trichomes with straight tips cover the basal region of the labellum, whereas short unicellular trichomes with polygonal flattened bases form the reflective median speculum. The apical region of the labellum possesses a villous indumentum of long acuminate trichomes with bent or sinuate tips. Large smooth-walled, dome-shaped papillae occur on the margins and on the distal region of the abaxial surface of the labellum. These remarkable papillae have high polarity; the protoplasm at the apex of each cell contains several small vacuoles, while a prominent nucleus surrounded by numerous hypertrophied amyloplasts occurs at the opposite end of the cell. Positive reactions to Vogel's staining test and to Sudan black B enabled us to conclude that the osmophores of both species are composed of these peculiar secretory epidermal cells and by two or three subsecretory layers of parenchyma cells.
Key Words: anatomy • labellum • micromorphology • Ophrys • Orchidaceae • osmophore • Portugal • pseudocopulation
Ophrys orchids have developed a highly specialized pollination system involving sexual deception, a phenomenon regarded as exclusive to Orchidaceae (Nilsson, 1992
), but with a few exceptions, such as Guiera senegalensis (Combretaceae; Kullenberg, 1961
) and Gilliesia graminea (Alliaceae; Rudall et al., 2002
). Ophrys flowers mimic hymenopteran females in terms of shape, pilosity, and color patterns and thereby deceive their males for pollination (Kullenberg, 1961
; van der Pijl and Dodson, 1966
; Borg-Karlson, 1990
). In addition to these visual and tactile cues, the flowers also attract pollinators by means of olfactory stimuli involving synthesis of a complex mixture of volatile odoriferous compounds similar to the sex pheromones of the female (Kullenberg, 1961
; Borg-Karlson and Tengö, 1986
; Borg-Karlson, 1990
; Schiestl et al., 1999
). Hence, pollination by sexual deceit is highly specific; each Ophrys species is pollinated by only one or a few related species of hymenopterans (Kullenberg, 1961
; Paulus and Gack, 1981
; Schiestl et al., 1999
; Schiestl and Ayasse, 2002
; Ayasse et al., 2003
). Sexually excited male insects alight on an Ophrys labellum and try to copulate with it, a phenomenon known as pseudocopulation (Dafni, 1984
; Nilsson, 1992
; Delforge, 2001
). During these pre-copulatory movements, the pollinator touches the column of the flower and may remove pollinaria with the abdomen tip or the head (Kullenberg, 1961
; Delforge, 2001
). Transfer of pollinaria results in cross-pollination.
Volatiles released by flowers of Ophrys species include alkanes, alkenes, aliphatic alcohols, saturated hydroxy and oxo acids, aldehydes, ketones, esters, and oxygenated mono- and sesquiterpenes, combined in varying proportions (Borg-Karlson and Tengö, 1986
; Borg-Karlson, 1990
; Schiestl et al., 1999
, 2000
; Ayasse et al., 2000
, 2003
; Schiestl and Ayasse, 2002
). However, only a small subset of these compounds has been detected in the females of their pollinators and found to be active in stimulating mating behavior in the males (Schiestl et al., 1999
, 2000
; Schiestl and Ayasse, 2002
; Ayasse et al., 2003
). Despite the recent advances in chemical and ethological research on Ophrys pollination, the study of the specific site of biosynthesis and discharge of the volatile secretion has been neglected, and the fine structure of the Ophrys labellum has received little attention. Kullenberg (1961)
in his excellent and original survey of Ophrys pollination compared, even though superficially, the micromorphology of the flowers with that of their pollinator insects. More recently, the labellum micromorphology of six species from the O. bertolonii Moretti aggregate and of other related taxa was described (Servettaz et al., 1994
).
On the other hand, despite the pioneer studies of Vogel in the 1960s on Orchidaceae, Aristolochiaceae, Araceae, and Asclepiadaceae (Vogel, 1990
), our knowledge of the anatomy and cytology of the osmophores of Ophrys remains poor. In the last 20 years, most research on the anatomy and ultrastructure of orchid osmophores has concentrated on tropical species (Pridgeon and Stern, 1983
, 1985
; Curry, 1987
; Stern et al., 1987
; Curry and Stern, 1991
; Curry et al., 1991
). By contrast, studies of European species are still relatively rare (Stpiczy
ska, 1993
, 2001
).
Within the framework of a wider project involving speciation of Ophrys in Portugal, we have undertaken cytological studies on the flower. In this paper, we compare the structure of the labella of O. fusca and O. lutea and describe the epidermal cell types and their distribution pattern in an attempt to locate and characterize the osmophore.
MATERIALS AND METHODS
Flowers from natural populations of O. fusca Link and O. lutea (Gouan) Cav. occurring throughout central-western Portugal were collected. Flowers prior to and at anthesis were fixed for scanning electron microscopy (SEM), with 2.5% glutaraldehyde in 0.1 M sodium phosphate buffer at pH 7.2. Samples were kept in fixative under vacuum at room temperature for 20 min, followed by 48–72 h at 4°C. The material was then washed in the fixative buffer, dehydrated in a graded acetone series, critical-point dried with CO2 and coated with gold. Observations were carried out on a JEOL T220 scanning electron microscope (JEOL Ltd., Tokyo, Japan) at an accelerating voltage of 15 or 20 kV.
For light microscopy, pieces of labella from buds just before anthesis and flowers at anthesis were processed in two ways. Some were fixed as described for SEM, but after the washes in the fixative buffer and dehydration through an ethanol series, the material was infiltrated with and embedded in Leica Historesin (Leica Microsystems, Nussloch/Heidelberg, Germany). Sections (2 µm thick) were cut using a Leica RM 2155 microtome (Leica Microsystems, Nussloch, Germany) and sequentially stained with periodic acid–Schiff's (PAS) reagent/toluidine blue O (Feder and O'Brien, 1968
) for polysaccharides and for general histology. Sections were tested for starch with Lugol's iodine solution (IKI; Johansen, 1940
) and for lipids with Sudan black B (Bronner, 1975
) using appropriate controls. Other pieces of labella (namely, portions of the margins) were fixed with 2.5% glutaraldehyde in 0.1 M sodium phosphate buffer at pH 7.2 for 12 h at 4°C, rinsed in the fixative buffer, and postfixed with 2% osmium tetroxide in the same buffer for 1 h at room temperature. After washes in distilled water, specimens were dehydrated in a graded acetone series and embedded in Epon-Araldite resin (Electron Microscopy Sciences, Fort Washington, Pennsylvania, USA). Semithin sections (approximately 0.5 µm thick) were cut with a Sorvall MT-1 ultramicrotome (Sorvall Inc., Norwalk, USA) and stained with Sudan black B as described for the sections embedded in Leica Historesin. Sections were observed with a Leitz (Wetzlar, Germany) Dialux microscope.
Vogel's staining method was used for the macroscopic observation of osmophores (Stern et al., 1986
). Whole fresh buds, just prior to anthesis, and flowers at anthesis were immersed in 0.1% (w/v) aqueous neutral red for 2– 24 h. After staining, flowers were rinsed in tap water and examined.
RESULTS
Labellum micromorphology
The Ophrys labellum has one central lobe flanked by two lateral lobes. The central lobe can be divided along its length into three main regions: basal (near the stigmatic cavity), median, and apical (Fig. 1).
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A key morphological feature of the apical part of the labellum of O. fusca and O. lutea is the presence of a central notch (Figs. 10, 12, arrows). In both orchids, the adaxial surface of the apical part of the labellum and lateral lobes is covered to a variable extent by a dense villous indumentum of long acuminate unicellular trichomes with swollen bases and narrow tips that are bent or sinuate (Figs. 8, 9). The trichome cell walls, like those of the other trichomes found in these two species, also show cuticular striations. In O. fusca, such a villous indumentum covers the entire portion of the labellum that surrounds the speculum as well as the entire apical portion, with the exception of the glabrous border (Figs. 10, 11). By contrast, in O. lutea, the area of the villous indumentum is smaller and is restricted to the proximal zone of the apical part of the labellum and to the lateral lobes, which are in contact with the speculum (Fig. 12). Otherwise, the distal zone of the labellum is composed of large, smooth, dome-shaped papillae, which strongly resemble the cells of the border and the abaxial epidermal cells from the apical region of the labella of both species (Figs. 11, 13). Furthermore, a marked cell gradient is visible extending from the glabrous margin of the labellum to the area covered by the villous indumentum. The dome-shaped papillae gradually acquire a conical shape with pointed or round tips, which tend to become more hairlike as they approach the villous indumentum (Fig. 11).
Labellum anatomy and histochemistry
Anatomically, the labella of O. fusca and O. lutea flowers are similar. They consist of multilayered parenchyma supplied by vascular strands and delimited by an upper and a lower epidermis. These differ from each other and comprise several types of cell depending upon which region is examined. The labellar parenchyma cells range from isodiametric to slightly elongated and are characterized by a large central vacuole and a thin layer of peripheral cytoplasm with relatively few organelles (Figs. 14–18). Elliptical crystalliferous idioblasts containing raphides of calcium oxalate are frequent among parenchyma cells (Fig. 25). Close to the border of the labellum, the parenchyma cells, especially those from the subepidermal layer, are less vacuolated and contain abundant small plastids (Figs. 18, 20, 22, 25).
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In both species, the abaxial epidermis of the distal part of the apical region of the labellum has characteristic anatomical features, especially near the central notch. This region comprises smooth-walled large papillae that appear spherical, reniform, or pyriform in section and that have an obvious polarity (Figs. 19–24). The distal region of the cell possesses several small vacuoles that become confluent, giving rise to a single large vacuole. In contrast, the proximal region of the cell contains dense cytoplasm with a prominent enlarged nucleus, rich in chromatin, surrounded by numerous hypertrophied plastids. These organelles, identified as amyloplasts by PAS and IKI staining, are larger than those observed within parenchyma cells (Fig. 22). This peculiar papillate epidermis extends throughout the entire border of the labellum, from the apical to the basal region (Figs. 25, 26). In O. lutea, this type of epidermis occurs on the well-defined peripheral area of both the abaxial and adaxial surfaces of the labellum next to the margins and corresponds on the adaxial surface to the glabrous, yellow zone of the labellum.
In semithin sections stained with Sudan black B, the vacuoles of the epidermal and parenchyma cells at the margins of the labellum contain Sudan-positive material (Figs. 27–30). In the cytoplasm of some epidermal cells are dark blue droplets (Fig. 29). An exudate that is often present outside the epidermal cell walls is also Sudan-positive (Figs. 27, 29). However, in Leica Historesin sections stained with Sudan black B, only the cuticles gave a positive reaction.
With Vogel's method for locating the osmophores, the labellar margin of both species stained light red. The staining, already visible after only 2 h in neutral red, did not change significantly after 24 h.
DISCUSSION
Labellum micromorphology and pollination
The similarity in labellum micromorphology between O. fusca and O. lutea flowers found in the present study supports the inclusion of both species in section Pseudophrys, which was stated by Godfery (1928)
and upheld by Devillers and Devillers-Terschuren (1994)
. Species from this section (O. fusca, O. lutea, and O. omegaifera H. Fleischmann aggregates) differ from the other section, Euophrys, in several morphological features of the stigmatic cavity, the structure of the labellum, and the speculum configuration. Also, the type of pseudocopulation performed by the insect pollinators is different in both sections: abdominal in section Pseudophrys and cephalic in section Euophrys (Godfery, 1928
; Devillers and Devillers-Terschuren, 1994
; Delforge, 2001
). Molecular phylogenetic analysis data also have shown that the O. fusca–O. lutea clade is well separated from the other Ophrys species (Pridgeon et al., 1997
; Soliva et al., 2001
). The different position adopted by pollinators upon the labellum during pseudocopulation is probably determined by particular features of the adaxial indumentum. As we have described, this indumentum is composed of unicellular trichomes that vary greatly in shape and size. In contrast, the abaxial part of the labellum, which plays no functional role in insect tactile stimulation, possesses an epidermis of slightly elongated flattened cells that become papillate at the margin, especially in the apical region.
The long trichomes present on the basal part of the labellum of O. fusca and O. lutea flowers may play a crucial role in the orientation of the excited male on the labellum. These trichomes probably guide the abdomen tip along the basal groove toward the stigmatic cavity (Kullenberg, 1961
; Devillers and Devillers-Terschuren, 1994
).
The well-defined speculum occurring on the central median region of the labellum of Ophrys may provide a secondary stimulus as insects approach the labellum, reinforcing the effect of the odor that acts as the primary attractive factor (Kullenberg, 1961
). Indeed, the color and intense brightness of the speculum contrast with the darker background of the adjacent regions of the labellum so that it resembles the wings of an insect (Moore, 1980
; Delforge, 2001
). The short unicellular trichomes of the speculum of O. fusca and O. lutea are similar to those observed on the speculum of O. garganica O. Danesch & E. Danesch and O. promontorii O. Danesch & E. Danesch, species included in O. sphegodes Miller aggregate (Servettaz et al., 1994
). Their large flattened bases and short tips with cuticular striations running from base to apex may explain, at least partially, the intense brightness of the speculum. In fact, the expanded bases of the speculum cells may act as a planar epidermis, which reflects most incident radiation. In addition, cuticular striations on lateral walls of trichomes may scatter emergent light, thereby increasing and maintaining the brightness of the speculum, regardless of the direction of viewing and the angle of incident light, as occurs on petal papillate cells (Kay et al., 1981
).
The border of the labellum of both species and the entire distal part of the apical region of the labellum of O. lutea are considered to be the main sites of light reflection due to the presence of large, smooth, spherical papillae. Such remarkable epidermal papillae, already reported by Pais (1976)
, are similar to those described for the deflexed edge of the labellum of O. garganica and other related taxa (Servettaz et al., 1994
).
Ophrys fusca and O. lutea attract and seem to be pollinated by Andrena male bees in general (Kullenberg, 1961
; van der Pijl and Dodson, 1966
; Borg-Karlson and Tengö, 1986
). However, in a recent paper, Schiestl and Ayasse (2002)
reported A. nigroaenea as the specific pollinator of O. fusca. The micromorphological similarities between the O. fusca and O. lutea's labella allow us to conclude, as did Kullenberg (1961)
, that the ability to stimulate the insect males, sexually excited by the odor, by means of tactile cues is probably similar in both species. As a result, the biologically isolating key factor between these two Ophrys species may be differences in the scents that they produce, which were identified by Borg-Karlson (1990)
.
Labellum anatomy and histochemistry
Anatomically, the most remarkable labellar structure in O. fusca and O. lutea is the border, particularly at the apical region near the central notch, where large spherical to dome-shaped papillae occur. Such cells, besides their high polarity, have features typical of secretory cells, namely, an enlarged nucleus with dense chromatin areas and abundant organelles.
Papillae considered on histochemical grounds to be osmophores (floral scent glands) are often located on the upper surface of the perianth and comprise a single secretory layer of well-differentiated epidermal cells and two to three layers of starch-rich parenchyma, which form a subsecretory tissue (Vogel, 1990
). The staining reaction observed when living floral tissue was subjected to Vogel's test enabled us to identify presumed osmophores, although neutral red does not specifically stain this tissue (Stern et al., 1986
). The large dome-shaped papillae on the marginal surface of the labella of O. fusca and O. lutea fulfill many of the criteria that characterize osmophore cells, such as considerable cell polarity, smooth convex outer tangential walls, large nuclei of the secretory epidermis, and abundant amyloplasts of the subsecretory parenchyma cells. Like the osmophores described for most orchids (Pridgeon and Stern, 1983
, 1985
; Stern et al., 1987
; Curry, 1987
; Curry and Stern, 1991
; Curry et al., 1991
; Stpiczyska, 1993
), the osmophores of these two species, apparently comprise a secretory layer of epidermal cells and a subsecretory parenchyma tissue, which are located, in O. fusca and O. lutea, on both adaxial and abaxial surfaces of margins of the labellum. However, the major quantity of starch-rich plastids is found in epidermal cells, which contrasts with the typical distribution of starch on subepidermal tissue. Similar osmophore structure also occurs in some Ophrydeae spp. (Vogel, 1990
).
The presence of lipophilic material inside vacuoles of both epidermal and parenchyma cells in the borders of the labella of O. fusca and O. lutea provides evidence for the involvement of these tissues in the secretory process, thereby constituting the osmophore in both species. However, some lipoidal material, owing to its low molecular mass and high volatility, is immediately discharged into the atmosphere or easily extracted from its storing sites, the vacuoles, probably following dehydration of the specimens. Black-stained interfaces between small vacuoles occurring in some epidermal cells may be the result of this leaching process. The lipids were not preserved in specimens fixed only with glutaraldehyde and infiltrated with Historesin, a hydrophilic embedding material. More complex lipids with higher molecular masses may accumulate within and even outside the cells, forming an exudate (Vogel, 1990
).
The large amount of starch in the numerous amyloplasts in the secretory and subsecretory cells may be used as a source of energy or carbon for the biosynthesis of fragrant metabolites. Generally, following secretion, the osmophores cells develop a larger vacuome, which is accompanied by a marked depletion in starch (Stern et al., 1987
). We do not, however, know whether this sequence of cellular events occurs in O. fusca and O. lutea. Ultrastructural studies are under way to obtain more detailed information on these peculiar osmophores.
In conclusion, the labella of O. fusca and O. lutea present an adaxial surface consisting of four different types of epidermal cells arranged into well-defined color areas. Unlike the abaxial epidermis, the adaxial indumentum may provide important tactile and visual stimulation to the pollinator insects. Moreover, the entire border and the abaxial surface from the distal part of the apical region of the labellum together constitute the osmophore. In both species, it consists of a secretory papillate epidermis and two or three subsecretory parenchyma layers.
FOOTNOTES
4 Author for correspondence (e-mail: lia.ascensao{at}fc.ul.pt
) 
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