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Ann Bot. Aug 2007; 100(2): 195–203.
Published online Jun 4, 2007. doi:  10.1093/aob/mcm109
PMCID: PMC2735322

Functional Utrastructure of Genlisea (Lentibulariaceae) Digestive Hairs

Abstract

Background and Aims

Digestive structures of carnivorous plants produce external digestive enzymes, and play the main role in absorption. In Lentibulariaceae, the ultrastructure of digestive hairs has been examined in some detail in Pinguicula and Utricularia, but the sessile digestive hairs of Genlisea have received very little attention so far. The aim of this study was to fill this gap by expanding their morphological, anatomical and histochemical characterization.

Methods

Several imaging techniques were used, including light, confocal and electron microscopy, to reveal the structure and function of the secretory hairs of Genlisea traps. This report demonstrates the application of cryo-SEM for fast imaging of whole, physically fixed plant secretory structures.

Key Results and Conclusion

The concentration of digestive hairs along vascular bundles in subgenus Genlisea is a primitive feature, indicating its basal position within the genus. Digestive hairs of Genlisea consist of three compartments with different ultrastructure and function. In subgenus Tayloria the terminal hair cells are transfer cells, but not in species of subgenus Genlisea. A digestive pool of viscous fluid occurs in Genlisea traps. In spite of their similar architecture, the digestive-absorptive hairs of Lentibulariaceae feature differences in morphology and ultrastructure.

Key words: Genlisea, Lentibulariaceae, carnivorous syndrome, carnivorous plant, digestive hairs, ultrastructure, cryo-scanning electron microscopy, morphology, cuticle, secretory glands, functional anatomy, digestive glands

INTRODUCTION

The Lentibulariaceae form the largest family of carnivorous plants, with three genera (Pinguicula, Utricularia, Genlisea) and about 300 species (Mabberley, 2000). According to molecular studies, the genus Genlisea is sister to Utricularia, and this pair is sister to the genus Pinguicula (Jobson and Albert, 2002; Jobson et al., 2003; Müller et al., 2004). Both Pinguicula and Utricularia develop active traps, but both the physiology and functioning of the traps differ much between these genera. Pinguicula are active ‘flypapers’ with slightly modified leaves for carnivory, but Utricularia form suction bladders (reviewed by Lloyd, 1942; Juniper et al., 1989; Legendre, 2000). In Genlisea a third special kind of trap has evolved – eel (lobster-pot) traps (Lloyd, 1942; Heslop-Harrison, 1975).

Genlisea species are small, rootless wetland plants which produce corkscrew-shaped subsoil traps of foliar origin for catching small soil organisms (Heslop-Harrison, 1975; Juniper et al., 1989; Reut, 1993). Barthlott et al. (1998) stated that Genlisea is highly specialized to trap protozoa; however, later it was experimentally shown that the prey caught depended on the kind of organisms available, and that the plants trapped both protozoa and metazoa (Płachno et al., 2005a; Studnička, 2003b). The basic structure of Genlisea traps is well known; each Genlisea trap consists of a stalk, a vesicle and a tubular channel (neck) which divides into two helically twisted arms (Fig. 1A). The digestive hairs have the same simple architecture consisting of three functional compartments: basal cell, middle cell, and a large head formed of four to eight terminal secretory cells (Goebel, 1891; Lloyd, 1942; Reut, 1993; Płachno, 2006). The details of its trap physiology and ultrastructure are still poorly recognized. So far only general observations of hair structure have been reported (Lloyd, 1942; Juniper et al., 1989; Reut, 1993; Müller et al., 2002). Juniper et al. (1989) found that these hairs resemble the sessile hairs of Byblis and Pinguicula, and suggested that their function and mechanism were also similar. For a proper understanding of the functions of the trap, detailed knowledge of the ultrastructure of these hairs is required. On that basis, comparison of digestive hair ultrastructure in Pinguicula, Utricularia and Genlisea, revealing structural and topographical differences and similarities, can shed light on the evolution of the carnivorous syndrome in Lentibulariaceae.

Fig. 1.
(A) Traps of very young hybrid Genlisea lobata × Genlisea violacea plant, the trap arms are very short (b, vesicle; n, neck; a, arm); (B) vesicle of Genlisea violacea; (C) vesicle of Genlisea sp. ‘Itacambira Beauty’; (D) vesicle ...

It is well known that chemical fixation of biological material often fails to rapidly stabilize all cell compartments, and may produce many artefacts (Mersey and McCully, 1978). To avoid these artefacts, several techniques have been employed to investigate nearly intact plant and animal tissues: various fluorophores, cryo-fixation, UV microscopy and environmental SEM (Lichtscheidl et al., 1990; Craig and Beaton, 1996; Pauluzzi et al., 1996; Hepler and Gunning, 1998; Walther and Müller, 1999). Recently, some of them have been used to study plant secretory structures (Turner et al., 2000, Kolb and Müller, 2004; Adlassnig et al., 2005; Sakamoto et al., 2006). In this paper the use of several imaging techniques, including light, confocal and electron microscopy, are described to distinguish the functional structure of the secretory hairs of Genlisea traps. The application of cryo-SEM for fast imaging of intact plant secretory structures without chemical fixation is highlighted.

MATERIALS AND METHODS

Plants of subgenus Genlisea (G. hispidula, G. aurea, G. pygmaea, G. repens, G. margaretae) and subgenus Tayloria (G. lobata, G. violacea f. Giant, G. uncinata, a species not yet described Genlisea sp. ‘Itacambira Beauty’, hybrid G. lobata × G. violacea f. Giant) were cultivated in the Department of Plant Cytology and Embryology, Jagiellonian University in Cracow. They were grown under a 16-h photoperiod in pots containing a mixture of wet peat and sand. The peat contained naturally occurring small organisms.

Cryo-scanning electron microscopy

For cryo-scanning microscopy, fresh trap parts of Genlisea hispidula were frozen in a mixture of solid and liquid nitrogen (‘slush’, − 210 °C) and transferred to a cryo-transfer system (Gatan) connected to the FE-SEM. Then the samples were fractured and the ice sublimated at − 95 °C for 5 min. The freshly prepared surfaces were observed in a Hitachi S-4800 scanning electron microscope at 3 kV. Finally, the same samples were sputter-coated with gold (approx. 5 nm thick) and observed again.

Light and transmission electron microscopy

Traps [mainly Genlisea hispidula (immature and mature traps), Genlisea lobata × Genlisea violacea f. Giant, but also Genlisea repens and Genlisea violacea f. Giant] were hand-sectioned with a razor blade and fixed in 2·5 % formaldehyde and 2·5 % glutaraldehyde in 0·05 m cacodylate buffer (pH 7·0) for 4 h at room temperature. The material was post-fixed in 1 % OsO4 in cacodylate buffer for 24 h at 4°C, rinsed in the same buffer, treated with 1 % uranyl acetate in distilled water for 1 h, dehydrated with acetone and embedded in Epon 812 (Fullam, Latham, NY, USA) or Spurr's resin. Semi-thin sections were stained with methylene blue/toluidine blue O and examined with an Olympus BX60 microscope. Ultrathin sections were cut on Leica Ultracut UCT and Sorvall MT 2B ultramicrotomes. After contrasting with uranyl acetate and lead citrate, the sections were examined in a Hitachi H500 or Philips CM 100 electron microscope.

Scanning electron microscopy

The procedures for preparing samples (G. hispidula, G. lobata, G. violacea f. Giant, G. uncinata, G. pygmaea, G. repens, Genlisea sp. ‘Itacambira Beauty’, G. margaretae, G. lobata × G. violacea f. Giant) for conventional SEM were as described earlier (Płachno et al., 2005b, c). Briefly, traps were hand-sectioned with a razor blade and fixed as for TEM. The material was later dehydrated in an ethanol and acetone series, and critical-point dried using liquid CO2. The dried tissues were sputter-coated with gold and viewed in a Hitachi S-4700 microscope.

Cytochemical observations and confocal microscopy

For cytochemical observations, both fresh and fixed sectioned hairs were used. The PAS reaction was used for detection of water-insoluble polysaccharides with 1,2-glycol groups (Wędzony, 1996). Auramine 0 was used for cutin and lipid localization (Wędzony, 1996). Hairs were incubated with the membrane-permeable fluorophore DIOC6(3) (dihexaoxacarbocyanine iodide) to label mitochondria and endoplasmic reticulum (Terasaki, 1994). Living hairs in DIOC6(3) solution were observed with a confocal microscope (ICS Leica Microsystem Heidelberg, Mannheim, Germany).

RESULTS

Distribution and general morphology of hairs

Three patterns of digestive hair distribution were observed in Genlisea vesicles (Fig. 1B–D and Table 1). In subgenus Genlisea the hairs are densely clustered; thus the heads are flattened to a more cube-like shape. Genlisea vesicle hairs are mushroom-shaped, with a short stalk and a globular head (Fig. 2A). The terminal cells usually have a radial arrangement (Fig. 2B), but this pattern is disrupted in some hairs.

Fig. 2.
(A) Fractured hair of Genlisea hispidula (cryo-SEM) (BC, basal cell; MC, middle cell; TC, terminal cell; IN, vacuolar inclusion; V, vacuole; N, nucleus); (B) radial arrangement of terminal cells in Genlisea uncinata hair; (C) part of section through middle ...
Table 1.
Comparison of some fine-structural features of digestive hairs in subgenera Genlisea and Tayloria

Structure of hairs

The basic structure of the digestive hairs is uniform throughout the genus. Some fine structural differences of the subgenera Genlisea and Tayloria are compared in Table 1.

Basal cell and middle cell

The cylindrical basal cell is laterally linked with epidermal cells, and below with parenchyma cells. In some hairs the basal cell is in direct contact with a tracheary element. It is highly vacuolated; the cytoplasm with organelles is concentrated towards the middle cell. The middle cell is more or less cylindrical, with broadened terminal parts. The part of this cell that supports terminal cells is especially large and more or less conical. The lateral wall is impregnated with electron-translucent material – cutin (Casparian strip). This wall is thickened especially at the base of the cell, where the middle cell is linked with the basal cell. The lateral wall apparently is brittle, because it fractures easily during material processing. The cell is strongly polarized. The vacuole occupies the middle and basal parts of the cell and contains highly osmiophilic material. In TEM, the vacuole consists of both electron-translucent and solidly electron-dense osmiophilic compartments. In cryo-SEM, homogenous material fills the whole vacuole (Fig. 2A). During preparation for TEM, probably some of this material was washed out from the vacuole. The hairs readily absorb Auramine 0, which is accumulated in the middle cell. The vacuole is polymorphic, consisting of Auramine-positive and Auramine-negative parts. Most of the cytoplasm with the nucleus, mitochondria, ER and plastids with osmiophilic inclusions lies near the terminal cells (Fig. 2C). All mitochondria within the hairs exhibit well-developed cristae. The transverse wall between the stalk and the basal cell is thin and penetrated by numerous plasmodesmata. The transverse wall between the stalk and the terminal cell is also thin, but the wall surface is larger than that between the stalk and the basal cell.

Secretory cells

The cytoplasm of the terminal cell is concentrated mostly towards its base and radial walls (Fig. 2A). Here the prominent nucleus is localized, as well as dictyosomes, numerous mitochondria (Fig. 3A), and plastids with small starch grains and plastoglobules (Fig. 3B). A large vacuole occupies most of the cell, and is surrounded by a thin peripheral layer of cytoplasm in which there are ribosomes, mitochondria, and dictyosomes (not hypertrophied) with small electron-translucent vesicles (Fig. 3C) and ER. In the vacuole is a large spherical inclusion visible by light microscopy and cryo-SEM (Fig. 2A) but not by TEM. By cryo-SEM this inclusion appears homogenous. In hairs from immature traps of G. hispidula, rough endoplasmic reticulum (rER) profiles are situated mainly along the outer walls of the terminal cells. Portions of rER elements (Fig. 3D) and electron-translucent vesicles are in close association with the plasmalemma. Sometimes the rER membrane seems to be anastomosed with the plasmalemma (Fig. 3D). Multivesicular and paramural bodies are also observed (Fig. 3E). The latter seem to be in close contact with rER membranes (Fig. 3F). The surfaces of both the outer and radial walls are irregular; however, a wall labyrinth sensu stricto is not formed. Similar observations were made in mature hairs of this species (Fig. 3G). In contrast to Genlisea hispidula (Fig. 2A) and G. repens, G. violacea × G. lobata and G. violacea feature radial and outer walls ingrowths (the terminal cells are transfer cells). The wall ingrowths are of reticular type and consist of two different structural regions: a dense core, and peripheral electron-translucent substance surrounding it. The wall ingrowths are PAS-positive; they branch and anastomose to form the wall labyrinth. There are many mitochondria (Fig. 3H), rER and some microbodies in close proximity to the invaginated plasma membrane. Unlike in the walls between terminal and stalk cells (Fig. 4A), plasmodesmata were not observed in the radial walls of the secretory cells (Fig. 4B), indicating the absence of a symplastic connection between these cells. The cuticle of the terminal cells is clearly seen in TEM as an electron-dense layer having discontinuities manifest as bright areas (Fig. 4C). The discontinuities are developed as pores, and are especially visible above a thick pectic layer continuous with the common middle lamella of anticlinal cell walls. In unimpregnated wall material, separate cutin cystoliths also occur. Cuticular pores were detected by various techniques, both in chemically fixed and in frozen material (for more details, see Płachno et al., 2005b).

Fig. 3.
(A) In vivo labelling of mitochondria, endoplasmic reticulum and nuclear envelope, using DIOC6(3), in terminal cells of Genlisea violacea f. Giant, Scale bar = 10 µm. (B) Part of terminal cell cytoplasm with mitochondria (M), plastid (P) and rough ...
Fig. 4.
(A) Part of transverse wall between stalk and terminal cell penetrated by numerous plasmodesmata, Genlisea lobata × Genlisea violacea: MC, middle cell; TC, terminal cell; In, wall ingrowth; scale bar = 500 nm. (B) Part of the radial wall between ...

DISCUSSION

Hair architecture in Lentibulariaceae

Besides having a similar architecture (basal cell, middle cell and secretory cells), the digestive-absorptive hairs of the Lentibulariaceae present morphological and ultrastructural differences (Table 2). For example, the middle cell in all three genera has a Casparian strip-like lateral wall, which is an apoplastic barrier, but this cell has a highly developed wall labyrinth only in Utricularia. This is associated with rapid water transport during removal of water from Utricularia bladders (Fineran and Lee, 1975; Fineran, 1985). The terminal cells of Genlisea share similarities with those of both Utricularia and Pinguicula. For example, the large vacuole, which is the dominant organelle, is also characteristic of the arms – the distal parts of quadrifid and bifid terminal cells of Utricularia (Fineran and Lee, 1975). One of the main functions of this vacuole in both genera is enlargement of the cell (contact between the cell surface and external environment), which is important for secretion and absorption processes.

Table 2.
Comparison of some fine-structural features of digestive hairs in Lentibulariaceae (after Vintéjoux, 1974; Beltz, 1975; Fineran and Lee, 1975; Fineran, 1985; Heslop-Harrison and Heslop-Harrison,1981; Juniper et al., 1989; Płachno, 2006 ...

Taking together previously published work on Lentibulariaceae hairs (Fineran and Lee, 1975; Heslop-Harrison and Heslop-Harrison, 1981; Fineran, 1985) and the present results, it is clear that the most complicated terminal cell in the digestive hairs of this family has evolved in Utricularia. In contrast to the sessile hairs in Pinguicula and Genlisea, in Utricularia the quadrifid and bifid terminal cells not only play a role in secretion and absorption but also partially take over the function of the middle cell. According to Heslop-Harrison and Heslop-Harrison (1981), in Pinguicula digestive hairs the radial walls of terminal cells have wall ingrowths. This is similar to the present observation in the Genlisea hybrid studied and G. violacea. In both genera they consist mainly of polysaccharides with 1,2-glycol groups (pectins). It should be added that Heslop-Harrison (1976) reported finding transfer cells in G. africana but did not describe the ultrastructure of the hairs. In the present study it was found that the wall ingrowths of Genlisea are similar to the reticular wall ingrowths described in other plants (Gunning and Pate, 1969). Transfer cells are developed for intensive short-distance transport between the symplast and apoplast (Gunning and Pate, 1974; Offler et al., 2003). In Genlisea the wall labyrinth is well developed and transport should also be very intensive and active, because the complexity of wall ingrowths is directly correlated with the intensity of transport by the transfer cell (Gunning and Pate, 1969). In interpreting the present results and the findings from a molecular study by Jobson et al. (2004), it should be borne in mind that the concentration of hairs along vascular bundles in species of subgenus Genlisea may be inherited from an ancestor (subgenus Genlisea is most probably the basal lineage; Jobson et al. 2004; present results). According to Jobson et al. (2004), active water pumping might have occurred in the Genlisea ancestor trap. In recent Genlisea species, active transport of water with organisms into traps has not been observed; prey entered the traps unaided and later moved inside (Adamec, 2003; Płachno et al., 2005a). In summary, the functional specialization and degree of complexity of Lentibulariaceae traps and digestive hairs are strongly correlated with differences in the rates of their molecular evolution (Jobson and Albert, 2002; Jobson et al., 2004; Müller et al., 2004).

Mode of secretion

The presence of well-developed rER and numerous mitochondria in terminal cells of Genlisea showed that these cells are active and have the essential apparatus for enzyme biosynthesis, as in digestive glands of other carnivorous plant (reviewed by Juniper et al., 1989). In the closely related Pinguicula, it has been suggested that the main synthesis of digestive enzymes occurs on membrane-bound ribosomes of the rER (Schnepf, 1961; Vassilyev and Muravnik, 1988). The present observations may suggest the mode of secretion. Multivesicular bodies are connected with both secretion and endocytosis (e.g. Tanchak and Fowke, 1987; Tse et al., 2004). Paramural bodies probably are also connected with transport of synthesized material, as in Claceolaria trichomes (Sacchetti et al., 1999). In Genlisea, we suggest that digestive enzymes may also be transported directly from ER to the cell wall via connecting ER membranes with the plasmalemma. This mechanism was previously suggested for Dionaea (Robins and Juniper, 1980) and Pinguicula (Vassilyev and Muravnik, 1988). Using a high-pressure freezing complex of actin and ER, which is associated with organelles and the cell wall, stalk cells of Drosera capensis were observed in emergences (Lichtscheidl et al., 1990). Cortical ER may play a key role in anchoring the cytoskeleton, in facilitating seretion, and also in the communication of signals between cytoplasm and the exterior of the cell (reviewed by Lichtscheidl and Hepler, 1996). Phosphatase activity is connected with the outer and radial walls of mature Genlisea digestive hairs (Płachno, et al., 2006; Fig. 1). In other carnivorous plants (Nepenthes, Dionaea, Pinguicula), synthesis of digestive enzymes in the prematuration stage of gland development has been suggested (Vassilyev, 1977; Robins and Juniper, 1980; Heslop- Harrison and Heslop-Harrison, 1981; Vassilyev and Muravnik, 1988; Owen et al., 1999). In Drosophyllum lusitanicum there is continuous enzyme (acid hydrolase) secretion in both immature and mature unstimulated digestive glands (Vassilyev, 2005). In mature traps of Genlisea, digestive hairs are stimulated continuously, because prey enter opened traps all the time. Enzyme secretion occurs in the absence of prey in plants from in vitro sterile culture (Płachno, 2006; Płachno et al., 2006). For these reasons, we suggest that digestive enzymes are continuously secreted to the trap interior (continuous digestive activity). Mucilage has been observed inside Genlisea traps (Studnička, 2003a; Płachno et al., 2005b). Thus, digestive pools of viscous fluid occur in Genlisea. However, unlike in the secretory cells of mucilage glands of Drosophyllum, Drosera, Utricularia and Pinguicula (Schnepf, 1961, 1963; Vintéjoux and Shoar-Ghafari, 1997, 2005) hypertrophy of dictyosomes and large vesicles containing mucilage were not observed in Genlisea.

Mode of absorption

The pores in the cuticle are involved in both secretion of enzymes and absorption of the products of digestion. The present ultrastructural observations confirm earlier reports on cuticular discontinuities in Genlisea hairs seen by SEM and vital staining (Płachno et al., 2005b). In carnivorous plants, true cuticular pores have been detected only in Drosera (Williams and Pickard, 1969, 1974 after Juniper et al., 1989; Ragetli et al., 1972; Heslop-Harrison, 1975) and recently in Roridula (Anderson, 2005).

In the present study, cryo-SEM was found to be a very useful method for visualizing not only the morphology but also the cytomorphology of whole plant secretory structures.

ACKNOWLEDGEMENTS

The first author is grateful to Dr Elena Gorb and Dr Stanislav Gorb (Evolutionary Biomaterials Group, MPI for Metals Research, Stuttgart, FRG) for their hospitality and for providing the opportunity to use the cryo-SEM, and to Prof. Irene K. Lichtscheidl and her group (Department of Cell Physiology and Scientific Films, University of Vienna, Austria) for the use of confocal microscopy facilities and for hosting the author's stay at the University of Vienna. We thank Kamil Pásek (http://www.bestcarnivorousplants.com), Dr Gerfield Deutsch, Andreas Fleischman and Dr Lubomir Adamec for providing plants for this study. This work was supported in part by a grant from the Jagiellonian University, Cracow (DBN-414/CRBW/18/2006).

LITERATURE CITED

  • Adamec L. Zero water flows in the carnivorous genus. Genlisea. Carnivorous Plant Newsletter. 2003;32:46–48.
  • Adlassnig W, Peroutka M, Lang I, Lichtscheidl IK. Glands of carnivorous plants as a model system in cell biological research. Acta Botanica Gallica. 2005;152:111–124.
  • Anderson B. Adaptation to foliar absorption of faeces: a pathway in plant carnivory. Annals of Botany. 2005;95:757–761. [PubMed]
  • Barthlott W, Porembski S, Fischer E, Gemmel B. First protozoa-trapping plant found. Nature. 1998;392:447.
  • Beltz C. The influence of natural environmental conditions on the growth, distribution, and morphological expression of the carnivorous aquatic plant Utricularia macrorhiza Le Conte, with light and electron microscopic observation of bladder ontogeny. Ames, USA: Iowa State University; 1975. PhD Thesis.
  • Craig S, Beaton CD. A simple cryo-SEM method for delicate plant tissues. Journal of Microscopy. 1996;182:102–105.
  • Fineran BA. Glandular trichomes in Utricularia: a review of their structure and function. Israel Journal of Botany. 1985;34:295–330.
  • Fineran BA, Lee MSL. Organization of quadrifid and bifid hairs in the trap of. Utricularia monanthos. Protoplasma. 1975;84:43–70.
  • Goebel K. Genlisea. Lentibulariaceae. Pflanzenbiologische Schilderungen. 1891;2:121–127. Tab. 15–16.
  • Gunning BES, Pate JS. ‘Transfer cells’ plant cells with wall ingrowths, specialized in relation to short distance transport of solutes – their occurrence, structure, and development. Protoplasma. 1969;68:107–133.
  • Gunning BES, Pate JS. Transfer cells. In: Robards AW, editor. Dynamic aspects of plant ultrastructure. London: McGraw-Hill; 1974. pp. 441–476.
  • Hepler PK, Gunning BES. Confocal fluorescence microscopy of plant cells. Protoplasma. 1998;201:121–157.
  • Heslop-Harrison Y. Enzyme release in carnivorous plants. In: Dingle JT, Dean RT, editors. Lysozymes in biology and pathology. Vol. 4. Amsterdam: North Holland Publishing Company; 1975. pp. 525–578.
  • Heslop-Harrison Y. Enzyme secretion and digest uptake in carnivorous plants. In: Sunderland Y, editor. Perspectives in experimental biology. Vol. 2. Oxford: Pergamon Press; 1976. pp. 463–476.
  • Heslop-Harrison Y, Heslop-Harrison J. The digestive glands of Pinguicula: structure and cytochemistry. Annals of Botany. 1981;47:293–319.
  • Jobson RW, Albert VA. Molecular rates parallel diversification contrasts between carnivorous plant sister lineages. Cladistics. 2002;18:127–136.
  • Jobson RW, Playford J, Cameron KM, Albert VA. Molecular phylogenetics of Lentibulariaceae inferred from plastid rps16 intron and trnL-F DNA sequences: implications for character evolution and biogeography. Systematic Botany. 2003;28:157–171.
  • Jobson RW, Nielsen R, Laakkonen L, Wikström M, Albert VA. Adaptive evolution of cytochrome c oxidase: infrastructure for a carnivorous plant radiation. Proceeding of the National Academy of Sciences of the USA. 2004;101:18064–18068. [PMC free article] [PubMed]
  • Juniper BE, Robins RJ, Joel JM. The carnivorous plants. London: Academic Press; 1989.
  • Kolb D, Müller M. Light, conventional and environmental scanning electron microscopy of the trichomes of Cucurbita pepo subsp. pepo var. styriaca and histochemistry of glandular secretory products. Annals of Botany. 2004;94:515–526. [PubMed]
  • Legendre L. The genus Pinguicula L. (Lentibulariaceae): an overview. Acta Botanica Gallica. 2000;147:77–95.
  • Lichtscheidl IK, Hepler PK. Smallwood M, Knox J P, Bowles DJ. Membranes: specialised functions in plants. New York: BIOS Scientific Publishers; 1996. Endoplasmic reticulum complex in the cortex of plant cell; pp. 383–402.
  • Lichtscheidl IK, Lancelle SA, Hepler PK. Actin-endoplasmic reticulum complex in Drosera.: their structural relationship with the plasmalemma, nucleus, and organelles in cells prepared by high pressure freezing. Protoplasma. 1990;155:116–126.
  • Lloyd FE. The carnivorous plants. Waltham, MA: Chronica Botanica Company; 1942.
  • Mabberley WJ. The plant book. Cambridge: Cambridge University Press; 2000.
  • Mersey B, McCully ME. Monitoring the course of fixation of plant cells. Journal of Microscopy. 1978;114:49–76.
  • Müller K, Borsch T, Legendre L, Theisen I, Barthlott W. Evolution of carnivory in Lentibulariaceae: considerations based on molecular, morphological, and physiological evidence. Proceedings the 4th International Carnivorous Plant Conference; 2002; Tokyo, Japan: pp. 63–73.
  • Müller K, Borsch T, Legendre L, Porembski S, Theisen I, Barthlott W. Evolution of carnivory in Lentibulariaceae and the Lamiales. Plant Biology. 2004;6:477–490. [PubMed]
  • Offler CE, McCurdy DW, Patrick JW, Talbot MJ. Transfer cells: cells specialized for a special purpose. Annual Review of Plant Biology. 2003;54:431–454. [PubMed]
  • Owen TP, Lennon KA, Santo MJ, Anderson AN. Pathways for nutrient transport in the pitcher of the carnivorous plant. Nepenthes alata. Annals of Botany. 1999;84:459–466.
  • Pauluzzi I, Lichtscheidl IK, Url WG. Ultra-violet microscopy. Proceedings of the Royal Microscopical Society. 1996;31:155–160.
  • Płachno BJ. Evolution and anatomy of traps and evolution of embryo sac nutritive structures in the Lentibulariaceae family members. Kraków, Poland: Jagiellonian University; 2006. PhD Thesis.
  • Płachno BJ, Adamus K, Faber J, Kozłowski J. Feeding behaviour of carnivorous Genlisea plants in the laboratory. Acta Botanica Gallica. 2005a;152:159–164.
  • Płachno BJ, Faber J, Jankun A. Cuticular discontinuities in glandular hairs of Genlisea St.-Hil. in relation to their functions. Acta Botanica Gallica. 2005b;152:125–130.
  • Płachno BJ, Jankun A, Faber J. Development of the wall labyrinth in pavement epithelium hairs of some Utricularia species. Acta Biologica Cracoviensia series Botanica. 2005c;47:109–113.
  • Płachno BJ, Adamec L, Lichtscheidl IK, Peroutka M, Adlassnig W, Vrba J. Fluorescence labelling of phosphatase activity in digestive glands of carnivorous plants. Plant Biology. 2006;8:813–820. [PubMed]
  • Ragetli HWJ, Weintraub M, Lo E. Characteristic of Drosera tentacles. I. Anatomical and cytological detail. Canadian Journal of Botany. 1972;50:159–168.
  • Reut MS. Trap structure of the carnivorous plant Genlisea (Lentibulariaceae) Botanica Helvetica. 1993;103:101–111.
  • Robins RJ, Juniper BE. The secretory cycle of Dionea muscipula Ellis. I. Fine structure and the effect of stimulation on the fine structure of the glands. New Phytology. 1980;86:279–296.
  • Sacchetti G, Romagnoli C, Nicoletti M, Fabio AD, Bruni A, Poli F. Glandular trichomes of Calceolaria adscendens Lidl. (Scrophulariaceae): histochemistry, development and ultrastructure. Annals of Botany. 1999;83:87–92.
  • Sakamoto K, Sayama H, Nakamoto H, Matsushima H, Kaneko Y. Sapporo, Japan: 2006. Ultrastructural changes during digestion and aborption in the aquatic plant Aldrovanda vesiculosa. 16th International Microscopy Congress, 3–8 September 2006,
  • Schnepf E. Licht- und Elektronmikroskopische Beobachtungen an Insektivoren-Drüsen über die Sekretion des Fangschleimes. Flora. 1961;151:73–87.
  • Schnepf E. Zur Cytologie und Physiologie pflanzlicher Drüsen. I. Über der Fangschleim der Insektivoren. Flora. 1963;153:1–22.
  • Studnička M. Further problem in Genlisea trap untangled. Carnivorous Plant Newsletter. 2003a;32:40–45.
  • Studnička M. Observations on life strategies of Genlisea, Heliamphora and Utricularia in natural habitats. Carnivorous Plant Newsletter. 2003b;32:57–61.
  • Tanchak MA, Fowke LC. The morphology of the multivesicular bodies in soybean protoplasts and their role in endocytosis. Protoplasma. 1987;138:173–182.
  • Terasaki M. Labeling of endoplasmic reticulum with DiOC6(3) In: Celis J, editor. Cell biology: a laboratory handbook. Vol. 2. Orlando, FL: Academic Press; 1994. pp. 381–386.
  • Tse YC, Mo B, Hillmer S, Zhao M, Lo SW, Robinson DG, et al. Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. The Plant Cell. 2004;16:672–693. [PMC free article] [PubMed]
  • Turner GW, Gershenzon J, Croteau RB. Development of peltate glandular trichomes of peppermint. Plant Physiology. 2000;124:665–680. [PMC free article] [PubMed]
  • Walther P, Müller M. Biological ultrastructure as revealed by high resolution cryo-SEM of block faces after cryo-sectioning. Journal of Microscopy. 1999;196:279–287. [PubMed]
  • Wędzony M. Department of Plant Physiology Monographs 5. Kraków, Poland [in Polish]: 1996. Fluorescence microscopy for botanists.
  • Vassilyev AE. Dynamics of ultrastructural characters of Drosophyllum lusitanicum Link (Droseraceae) digestive glands during maturation and after stimulation. Taiwania. 2005;50:167–182.
  • Vassilyev AE. Functional morphology of plant secretory cells. Leningrad, Russia: Nauka Press [in Russian]; 1977.
  • Vassilyev AE, Muravnik LE. The ultrastructure of the digestive glands in Pinguicula vulgaris L. (Lentibulariaceae) relative to their function. I. The changes during maturation. Annals of Botany. 1988;62:329–341.
  • Vintéjoux C. Ultrastructural and cytochemical observations on the digestive glands of Utricularia neglecta L. (Lentibulariaceae): distribution of protease and acid phosphatase activities. Portugaliae Acta Biologica Series A. 1974;14:463–474.
  • Vintéjoux C, Shoar-Ghafari A. Sécrétion de mucilages par une plante aquatique carnivore: l'Utricularia neglecta L. (Lentibulariaceae) Acta Botanica Gallica. 1997;144:347–352.
  • Vintéjoux C, Shoar-Ghafari A. Mucigenic cells in carnivorous plants. Acta Botanica Gallica. 2005;147:5–20.

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