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The Giant Extra-Floral Nectaries of Carnivorous Heliamphora Folliculata: Architecture and Ultrastructure

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The Giant Extra-Floral Nectaries of Carnivorous Heliamphora Folliculata: Architecture and Ultrastructure ACTA BIOLOGICA CRACOVIENSIA Series Botanica 49/2: 91–104, 2007 THE GIANT EXTRA-FLORAL NECTARIES OF CARNIVOROUS HELIAMPHORA FOLLICULATA: ARCHITECTURE AND ULTRASTRUCTURE BARTOSZ J. PŁACHNO1*, PIOTR ŚWIĄTEK2, AND ANDREAS WISTUBA3 1Department of Plant Cytology and Embryology, Jagiellonian University, ul. Grodzka 52, 31–044 Cracow, Poland, 2Department of Animal Histology and Embryology, University of Silesia, ul. Bankowa 9, 40–007 Katowice, Poland 3Maudauer Ring 227, 68259 Mannheim, Germany Received September 15, 2007; revision accepted December 7, 2007 Extra-floral nectaries commonly occur in carnivorous plants, forming pitfall traps to attract nectar-feeding insects. Although they are not connected with pollination, extra-floral nectaries promote the reproductive func- tions of carnivorous plants by increasing the supply of animal-sourced nutrients and thereby increasing the plant's vigor. Our main purpose here was to study the functional ultrastructure of the giant nectaries in Heliamphora, focusing on nectar production and secretion. We wanted to determine whether specialization of the shape and struc- ture of Heliamphora nectar spoons has an influence on nectary structure. Heliamphora folliculata, with its unique nectar storage chamber, may also have specialized giant nectaries differing from other species in the genus. In Heliamphora folliculata the largest nectaries occur in a nectar storage chamber. Regardless of their size, the nec- taries have similar ultrastructure. Key features of their cells are ER-sheathed leucoplasts and vacuoles with large osmiophilic phenolic inclusions. The former is characteristic for cells producing monoterpenes; indeed, the giant nectaries produce volatile compounds and may have a function similar to osmophores. Nectary cells are isolated from ordinary parenchyma cells by cutinized walls lacking plasmodesmata (endodermis). Symplastic transport is possible only between nectary cells and special parenchyma cells that have wall thickenings. Between them are many plasmodesmata; thus the nectary is a symplastic and apoplastic field. These specialized parenchyma cells are similar to the flange cells described in parasitic plants. Why has a special spoon with a nectar chamber evolved in Heliamphora folliculata? One answer given is that it protects nectar against being washed away by frequent rain- falls so that the plant produces less nectar and saves energy. Also, when nectar is not easily accessible the insects have to spend more time near the trap entrance to look for it, and they are more likely to be trapped. Regardless of the shape and structure of Heliamphora nectar spoons (pitcher appendages), giant nectaries apparently have the same architecture throughout the genus. So far as is known, pollinator-prey conflict does not exist in Heliamphora; nectaries in this genus are formed only for nectar-feeding prey. Key words: Heliamphora, Sarraceniaceae, extra-floral nectaries, nectar, carnivorous plants, ultra- structure, symplastic field, osmophores, leucoplasts, carnivorous syndrome, tepui. INTRODUCTION 2006). Like other pitcher plants (Cephalotus, Nepenthes, Darlingtonia, Sarracenia), Heliamphora The family Sarraceniaceae, with three genera possesses extra-floral nectaries on the pitcher trap (Darlingtonia, Heliamphora, Sarracenia), groups surface. Nectar-feeding insects are attracted and carnivorous plants from the New World forming trapped (Jaffe et al., 1995). Their carcasses are a mainly pitfall traps (excepting Sarracenia psittacina source of nutrients for the plants (Lloyd, 1942; with a lobster-type trap; Studnièka, 1984). According Juniper et al., 1989; Jaffe et al., 1992). The anatomy to recent molecular studies, the genus Sarracenia is of nectaries of a few species of Heliamphora were first sister to Heliamphora, and this pair is sister to the described by Kraft (1896, after Lloyd, 1942) and later genus Darlingtonia (Bayer et al., 1996; Neyland and in detail by Lloyd (1942). Nectary morphology has Merchant, 2006). The genus Heliamphora comprises been studied by SEM in only two Heliamphora about 13 species and is restricted to tepuis and species (H. heterodoxa, H. nutans), by Adams and plateaus of Venezuela, Brazil and Guyana (Rice, Smith (1977) and Juniper et al. (1989); they report- *e-mail: [email protected] PL ISSN 0001-5296 © Polish Academy of Sciences, Cracow 2007 92 Płachno et al. Fig. 1. (a) Heliamphora folliculata in its natural habitat in southern Venezuela, (b) Upper part of pitcher with nectar spoon (nectar chamber damaged), southern Venezuela, (c) Upper part of pitcher of juvenile plant, lacking the spoon; note glabrous triangular part with numerous nectaries, (d) Part of leaf of juvenile plant; on the external wings are long, straight, nonsecretory hairs together with numerous glands, (e,f) Small nectaries among downward-directed, unicellu- lar, nonsecretory epidermal hairs, in adult plant. n – nectary. Giant nectaries of Heliamphora 93 Fig. 2. (a) Section through nectar spoon. H – nectar chamber; CH – nectar channel; B – base, (b) Numerous small nec- taries on glabrous spoon base, (c) Small nectary with four apical cells and remnants of secretion, (d) Part of section through nectar chamber; giant nectaries visible (*). Note strong fluorescence of cutinized walls. Bar = 300 μm, (e) Section through nectar chamber; numerous giant nectaries visible. ed two kinds of nectaries in Heliamphora: large ones Sarraceniaceae are restricted to Heliamphora. There restricted to the pitcher appendage (spoon), and have been no ultrastructure studies of nectaries in small ones occurring on the outer and partly on the this genus. Vogel (1998) pointed to the need for work inner pitcher surface. The small nectaries have a on the detailed ultrastructure of the nectaries of other basic construction very similar to that of the extra-flo- members of Sarraceniaceae. To date, the only group ral nectaries of Sarracenia, "Sarracenia-type" (Lloyd, of carnivorous plants to be studied in detail in terms 1942; Vogel, 1998). The giant extra-floral nectaries in of nectary ultrastructure and nectar production is 94 Płachno et al. Nepenthes (Vassilyev, 1977; Juniper et al, 1989; SCANNING ELECTRON MICROSCOPY Merbach et al., 2001). The procedures for preparing samples for conven- Heliamphora folliculata Wistuba, Harbarth & tional SEM were as described earlier (Płachno et al., Carow was described only recently, in 2001, from the 2005a,b). Briefly, traps were hand-sectioned with a Los Testigos table mountains in southern Venezuela. razor blade and fixed as for TEM or in 70% ethanol This endemic species is unique not only among with 1% glycerine. The material was later dehydrat- Heliamphora species but also in the Sarraceniaceae ed in an ethanol and acetone series, and critical- family, in that its pitcher appendage (spoon) forms a point dried using liquid CO . The dried tissues were chamber to store nectar (Fig. 1a,b; Wistuba et al., 2 sputter-coated with gold and viewed in a HITACHI 2001). The structure and shape of pitcher appendages S–4700 microscope (Scanning Microscopy with nectaries is one of the most valuable characters Laboratory of Biological and Geological Sciences, for interpreting Heliamphora relationships (Wistuba Jagiellonian University). To study pit distribution et al., 2001, 2002 and Carow et al., 2005). and cell wall architecture, we extracted cytoplasm. One of our aims here is to study nectar cham- Nectar spoons were hand-sectioned and fresh tissue ber anatomy and the distribution of nectaries in was placed in commercial bleach (sodium hypochlo- Heliamphora folliculata. The main purpose is to rite) diluted 1:10 in water. After 2 h the material was examine the ultrastructure of the giant nectaries of washed in water and fixed in 2.5% glutaraldehyde in Heliamphora, focusing on nectar secretion. Another cacodylate buffer. Later procedures for preparing important aim was to determine whether specializa- samples for SEM were as above. tion of the shape and structure of Heliamphora nec- tar spoons has an influence on nectary structure. Perhaps Heliamphora folliculata, with its unique HISTOCHEMISTRY nectar storage chamber, also has specialized giant Autofluorescence (chlorophyll a, cutinized walls) nectaries differing from other species in the genus. observations of fresh sectioned tissue were made in an epifluorescence microscope (Nikon Eclipse E 400 with UV–2A and B–2A filters). For some samples MATERIALS AND METHODS DAPI was added to label DNA. Documentation was PLANT MATERIAL made on Sensia 200 and 100 slide film. Juvenile and adult plants of Heliamphora folliculata, originated from seeds collected by Andreas Wistuba RESULTS during a field trip in 2001 (Wistuba et al., 2001) from Aparaman Tepui and Murosipan Tepui, were exam- SPOON ANATOMY AND NECTARY DISTRIBUTION ined. Additionally, Heliamphora folliculata plants Leaves of juvenile plants lack the spoon; only the from the Murosipan Tepui and plants of Heliamphora apex of the pitcher is slightly curved and forms a minor (Auyan Tepui) and Heliamphora heterodoxa small appendix at the tip (Fig. 1c). There are only were obtained from the collection of Kamil Pásek of small nectaries scattered on the glabrous inner sur- Dobroslavice, Czech Republic. face of the apex, the glabrous triangular part of the upper inner pitcher wall, and the glabrous pitcher margins. As in mature traps, nectaries occur also on LIGHT AND TRANSMISSION ELECTRON MICROSCOPY the inner pitcher wall among downward-directed, uni- The procedures for preparing samples for TEM
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