Annals of Botany 61, 343-351, 1988 343

The Ultrastructure of the Digestive Glands in

Pinguicula vulgaris L. {Lentibulariaceae) Relative to
their Function. II. The Changes on Stimulation
A. E. VASSILYEV and L. E. MURAVNIK
Komarov Botanical Institute, 197022 Leningrad, USSR

Accepted: 30 March 1988

ABSTRACT
The secretory cells of the digestive glands remain highly active during the entire period of prey digestion
and absorption of nutrients. They appear to play a major role in gland activity. A model of the digestive
gland's activity on stimulation is proposed. It is very similar to that suggested earlier for Dionaea muscipula.
After the digestion and absorption cycle, destructive processes are initiated in the glands. These appear
similar to those observed in the glands of the ageing, unstimulated leaf and are not associated with
feeding.

Key words: Pinguicula vulgaris L. carnivorous plant, digestive glands, ultrastructure, protein secretion,
absorption, senescence.

glands on stimulation. Unfortunately, the authors

INTRODUCTION
The carnivorous genus Pinguicula has been shown
to contain stores of digestive enzymes within the
head cells of the sessile leaf glands (Heslop-
Harrison and Knox, 1971; Heslop-Harrison, 1975,
1976 a, b; Heslop-Harrison and Heslop-Harrison,
1981). The major storage sites are the walls,
particularly the slime (spongy) layer, and to a
lesser extent, the vacuoles of the secretory head
cells. Hydrolases, along with water, are released
only by external stimulation. The mature unstimu-
lated digestive glands are almost completely dry.
The prey is captured by a sticky mucilage, produced
by the stalked glands of the leaf, and is digested
thereafter by fluid released abundantly by the
sessile glands in response to stimulation. As the
authors cited above clearly established, the absorp-
tion of the products of digestion, by the digestive
glands, starts very soon after stimulation. Less
convincing were these author's proposals on the
sequence of the fluid release and nutrient absorp-
tion, and the role of the different types of gland
cells, both in these processes and in stimulus
perception. Heslop-Harrison and Heslop-Harrison
(1981) claimed that, as the digestive glands mature,
their secretory cells undergo a type of total
autophagy and become sacs of enzymes. They play
therefore only a passive role in the activity of the
0305-7364/88/100343 + 09 $03.00
did not present convincing evidence of secretory
cell degeneration and they did not study the
ultrastructural changes the glands undergo after
stimulation. Heslop-Harrison (1976a) favours the
idea that absorption of nutrients begins only after
the cessation of enzyme secretion. However, this
conclusion remains entirely speculative.
In the first communication of this series (Vas-
silyev and Muravnik, 1988) we described the
ultrastructural changes of the sessile glands of P.
vulgaris from their initiation up to a fully mature
condition in unstimulated leaves. We showed that,
contrary to Heslop-Harrison and Heslop-
Harrison's (1981) opinion, the secretory cells of
the mature glands, ready for prey-capture, remain
intact. We also speculated about the nature of the
so-called spongy layer and the modes of enzyme
discharge into the storage sites. In the present
paper, an account of the ultrastructural changes of
the glands on stimulation will be given and the
model of gland functioning after the prey is
captured will be substantiated.
MATERIALS AND METHODS
Wild plants in the Leningrad region were taken
to the laboratory and the mature unactivated
leaves were caused to secrete small pieces of egg
© 1988 Annals of Botany Company

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 344 Vassilyev and Muravnik—Vltrastructure of Pinguicula vulgaris L.

albumin. The glands of the unactivated leaves of noted by Robins and Juniper (1980 a), in stimulated
the same age served as control. For electron secretory cells of Dionaea was found.
microscopy, pieces of leaves were fixed 0-5, 4,14 h, Coated Golgi vesicles increase in number at this
2 and 5 d after stimulation. The fixation and period and they are seen, not only in association
embedding were as described (Vassilyev and with the dictyosomes (Fig. 2 A), but also scattered
Muravnik, 1988). Ultrathin sections were viewed throughout the hyaloplasm. The mitochondria
under JEM-7A and Hitachi-600 electron micro- retain their condensed configuration (Fig. 2B).
scopes. The frequency of free ribosomes (approx. 300 in
1 /tm2) remains practically the same as in the
mature unstimulated glands (see Vassilyev and
Muravnik, 1988).
RESULTS In the barrier cells, 4 h after stimulation, a
The head cells of the glands became moist after moderately electron opaque periplasmic space
0-5 h contact with the egg albumin. The secretory appears at the junction of the upper and lateral cell
cells show some decrease in concentration of the walls (Fig. 3 A) and less thick along the upper
fibrillar-granular inclusions in the slime layer but periclinal wall. The formation of this space is
not in the specific densities in it. The gaps in the possible only in the uppermost part of the lateral
cuticle of the head cells are filled by osmiophilic walls since the other region is occupied by 'a
deposits and these also appear on the head surface. Casparian strip' in which the plasmalemma is
The vacuoles are obviously displaced towards the tightly adpressed to the cell wall.
plasmalemma. This movement may be a pre- In the leucoplasts of the barrier cells, the fine
requisite for the resumption of exocytosis of their granular inclusions, which earlier were incon-
contents, which was postulated for the cells during spicuous, begin to expand. Single short cisternae
maturation of the glands (Vassilyev and Muravnik, of ER lie near the mitochondria. The lipid droplets
1988). Vacuole exocytosis results in the discharge become more frequent. There is no apparent
of intracellular hydrolases into the periplasmic change in the ultrastructure of the reservoir (basal)
space and subsequently onto the head surface. cell.
The RER shows more stacks of parallel cisternae By 14 h, by which time the margins of the
(ergastoplasm) than the mature unstimulated stimulated leaf are folding towards the midribs;
glands. These stacks occasionally lie closely juxta- evidence for vacuole exocytosis is no longer
posed to the plasmalemma. The Golgi apparatus apparent. Cytosegresomes and multivesicular
activity remains low. There are no visible changes bodies appear in the cytoplasm of the secretory
in the nucleoli and mitochondria. cells. Groups of vesicles, similar to those of
After 4 h, by which time the volume of the the multivesicular bodies, can also be seen in
digestive fluid has notably increased, the secretion the periplasmic space. Myelin-like bodies are en-
droplets on the leaf surface can be distinguished by countered within the hyaloplasm and vacuoles. All
the naked eye. The reduction of the volume fraction the above formations can be seen in the secretory
of the vacuome, due to exocytosis of some vacuoles, cells of the glands in the control leaves. The
becomes apparent. The vacuolar volume of the vacuolar volume again increases, whereas the
secretory cells of Dionaea glands was also observed partial volume of the cytoplasm is decreased, due
by Robins and Juniper (1980 a) to fall substantially to the intensification of lytic processes. The RER is
after stimulation and it was also noted for P. fairly abundant as before, and regions of the
grandiflora by Heslop-Harrison (1975) in one of ergastoplasm are still visible. The periplasmic
her earlier reviews. The fibrils and granules in the space disappeared from the barrier cells by this
slime layer become less conspicuous than those in time.
unstimulated glands, and this distinguishes, in By day two, the leaf blade is fully unfolded and
sections, the intact vacuoles with denser content the surface of the heads of the stimulated glands
from those incorporated into the periplasmic space becomes as dry as prior to stimulation. The
(Fig. 1A). There are no visible changes in the contents of the slime layer appear mainly trans-
volume fraction of the slime layer and numerous parent; the slime being seen only in the vicinity
cytoplasmic evaginations are still apparent in it. of the primary wall. The outline of the plasma-
In the regions of the ergastoplasm, the RER lemma is still irregular. The local autophagy of
cisternae facing the plasmalemma show a loss of the cytoplasm progresses further (Fig. 3 B) and the
bound ribosomes (Fig. 1B). However, a distinct frequency of organelles, except mitochondria, is
membranous contact between the peripheral cister- reduced. Secretory cells with fewer organelles are
nae and the plasmalemma is observed very also characteristic of the unstimulated digestive
infrequently. No swelling of the ER cisternae, glands on leaves of similar age. Numerous

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 Vassilyev and Muravnik—Ultrastructure of Pinguicula vulgaris L. 345

FIG. I. A, A vacuole with a fibrillar content in contact with the plasmalemma (pi) of a secretory cell 4 h after
stimulation. Note the stack of RER, si, slime layer, x 39000. B, A portion of the ergastoplasm in the secretory cell
4 h after stimulation. Note the loss of ribosomes by the RER cisterna facing the plasmalemma (pi), x 105000.

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 346 Vassilyev and Muravnik—Ultrastructure o/Pinguicula vulgaris L.

FIG. 2. A, Dictyosomes with coated vesicles (arrows), 4 h stimulation x 62000. B, condensed mitochondria, 4 h after
stimulation, x 60000. C, orthodox mitochondria, 5d, x 55000.

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 Vassilyev and Muravnik—Ultrastructure of Pinguicula vulgaris L. 347

FIG. 3. For legend see p. 348.

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 348 Vassilyev and Muravnik—Ultrastructure o/Pinguicula vulgaris L.

'fenestrae' appear in the ER cisternae sheathing absorption of nutrients after stimulation. The
the leucoplasts (Fig. 3C). The Golgi apparatus release of the digestive fluid is accompanied, at the
again appears inactive. ultrastructural level, by a decrease in the concen-
In the leucoplasts of the barrier cell stimulated tration of the granules and fibrils within the slime
glands, one or two finely granular inclusions, layer. There also appear osmiophilic deposits,
occupy by day two the main volume of the presumably proteins, within cuticular interrup-
organelles. They are delimited by a membrane tions of the gland heads and also outside the
(Fig. 3D). Lipid droplets become a common cuticle. Exocytosis of the contents of some vacuoles
component of the barrier cells. into the slime layer is resumed, resulting in enzyme
By day five the volume of the cytoplasm in the addition to the digestive fluid. This process has
secretory cells is markedly reduced, due to cell been described (Vassilyev and Muravnik, 1988) as
vacuolation during the course of the autophagic one of the possible ways of the hydrolase discharge
process. The larger vacuoles appear transparent during the period of gland maturation. It is
while the smaller ones contain electron opaque pertinent to note in this regard the speculation of
deposits. The latter seem to originate from the Heslop-Harrison and Knox (1971), that enzymes
cytosegresomes after lysis of their contents. In the held in the head cell vacuoles are somehow
cytoplasm, which takes the form of the inter- 'pumped' into the periplasmic space. In Dionaea
vacuolar strands, organelles become infrequent. glands Robins and Juniper (1980 a) also observed
In the still lobed nucleus, the nucleolus appears the decrease in the volume fraction of the vacuoles
small and devoid of its granular component. The and the loss of hydrolases out of them. Somewhat
zones of the ergastoplasm disappear and the ER later, Rea, Joel and Juniper (1983) proposed that
now takes the form of single long cisternae the decrease in vacuolar volume observed upon
scattered throughout the cytoplasm. Dictyosomes stimulation results from the fusion of the vacuoles
are sparse and their activity is low. The mito- containing hydrolases and ions to the plasma-
chondria acquires an orthodox configuration lemma in the Dionaea glands.
(Fig. 2C) and the size of the plastoglobuli in the On stimulation in P. vulgaris, regions of the
leucoplasts increases. The surface density of free ergastoplasm appeared at the periphery of the
ribosomes by day 5 has notably decreased, and is protoplast in the secretory cells. This may indicate
now on average, about 100 in 1 /im2. The protein the enhanced synthesis of digestive enzymes.
crystals characteristic of the nuclei of the barrier Robins and Juniper (1980c) presented autoradio-
and reservoir cells are as large as before and their graphic evidence that, in Dionaea, the additional
number in some glands even increased up to four. protein is also synthesized and secreted into
In the leucoplasts of the reservoir cell, the finely digestive fluid after stimulation. However, in P.
granular inclusions appear similar to those of the vulgaris, the nucleolus remains segregated and
plastids in the barrier cells. does not show any signs of reactivation.
The digestive glands of old unstimulated leaves The frequent stacking of the ER close to the
are very similar in their ultrastructure to those of plasmalemma is probably related to its involve-
glands after 5 d stimulation. The main difference is ment in a direct discharge of stored and newly
that, in the secretory cells of the unstimulated synthesized hydrolases into the slime layer. We
glands, the slime and cytoplasmic evaginations in failed to find a direct fusion of the ER cisternae
the periplasm are replaced by homogenous with the plasmalemma. Nevertheless, the possi-
material similar to that of the typical cell wall and bility can not be excluded that the membranes of
apparently corresponding to the secondary wall. the ER form the transient anastomoses with the
plasmalemma (Vassilyev and Muravnik, 1988). In
Dionaea, Robins and Juniper (1980a, b) consider
DISCUSSION the formation of junctions between the ER and the
Contrary to the conclusion reached by Heslop- plasmalemma as the principal mode of hydrolase
Harrison and Heslop-Harrison (1981) that the release.
secretory cells of the digestive glands are, in the The Golgi apparatus of the secretory cells
species of Pinguicula they studied, ephemeral, in appears to undergo only slight activation, which is
our material they remained intact throughout the reflected both by the increase in the number of
entire period of secretion of digestive fluid and coated vesicles in the vicinity of the dictyosomes

FIG. 3. A, The emergence of a periplasmic space (ps) in the barrier cell at the junction of the lateral and upper
periclinal walls, 4h after stimulation, cs, a portion of the 'Casparian strip', pi, plasmalemma, x 59000. B, Local
autophagy in the secretory cell, 2 d, ct, cytosegresome, x 30 000. C, The appearance of the' fenestrae' in the ER sheath
of the leucoplasts (1), 2 d, x 70000. D, Osmiophilic inclusions in the leucoplasts of the barrier cell, 2 d, x 30000.

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 Vassilyev and Muravnik—Ultrastructure of Pinguicula vulgaris L. 349

and scattered in the cytoplasm. These vesicles may in the capturing slime (Heslop-Harrison, 1975). It
participate in secretion of additional hydrolases is also affected by trace amounts of enzymes on the
into the slime layer rather than being involved in surface of the digestive glands. The resulting
the endocytotic uptake of digestion products. products of hydrolysis enter the head cells of the
After stimulation, ultrastructural features digestive glands and interact with the receptors
characterize the secretory cells of P. vulgaris as the present in the plasmalemma of the secretory cells.
most active, compared with the other cells of the The secretion of the digestive fluid is initiated.
digestive glands. The secretory cells remain highly Solutes present in the fluid spread the stimulus to
active during the whole of the secretion-absorption more and more glands. This spread of activity is
cycle. Thus, they play a major role in the perception restricted, as Heslop-Harrison and Knox (1971)
of the stimulus in the release of digestive fluid suggested, by the gradient in the concentration of
and absorption of nutrients. This conclusion nutrients around the digested prey. Bulk flow of
is in contrast to the view of Heslop-Harrison fluid back to the glands is evidently blocked by the
and Heslop-Harrison (1981) who claim that, in Casparian strip of the barrier cells. This barrier
P. grandiflora, when the secretory cells are mature function of the strip in glands was convincingly
they undergo a total autolysis and are transformed shown by Heslop-Harrison (19766).
into a non-living sac of enzymes. These authors Digestive enzymes in solution leak on to the
conclude that these cells can play only a passive surface from the slime layer of the secretory cells
role, whereas the active roles in perception, of the sessile glands. The enzymes are then leached
secretion and absorption are taken by the barrier out through the gaps in the cuticle of the gland
(endodermal) cell of the gland. The discrepancy, in heads where, briefly, they are concentrated and
our opinion, arises from the incorrect inter- become visible there in the ultrathin sections as the
pretation of the electron micrographs by the osmiophilic inclusions. Slime apparently, also
authors. Close examination of their electron leaks out and makes the digestive fluid viscous.
micrographs shows no difference between the Then the exocytosis of the vacuolar hydrolases
species, nor of the environmental conditions. into the slime layer starts. The protein-synthesizing
Ultrastructural changes noted in the P. vulgaris system of the secretory cells is evidently activated
glands some days after stimulation include the and adds a small amount of hydrolases to the fluid
reduction of the size of the nucleolus, and of the through the transient fusion of the ER with the
frequency of the free ribosomes, the accumulation plasmalemma and the coalescence of coated
of the plastoglobuli in the leucoplasts, the pro- vesicles to this membrane.
gressive fenestration of the ER sheath, an increase As Heslop-Harrison and Heslop-Harrison (1980)
in the number of the multivesicular bodies and the showed, the driving force for this movement is the
appearance of myelin-like bodies. These changes active transport of ions, particularly Cl". These
are accompanied by the reduction of the number ions accumulate in the reservoir gland cells, prior
of all the organelles and are characteristic of to stimulation, then are pumped through the
senescent cells. They are not directly associated barrier cell into the secretory cells and out of the
with stimulation because they are also observed in glands. Here, Cl", as in Dionaea, serves as the
the secretory cells of the unstimulated glands of principal free anion which ensures the appropriate
the same age. The above changes may be explained osmolarity and activity of the digestive fluid (Rea,
by the genetically programmed ephemeral nature Joel and Juniper, 1983).
of leaves in Pinguicula. In P. vulgaris, the duration The highly active appearance of the secretory
of the life-cycle of the leaves is about 10-15 d, and cells in the stimulated glands of P. vulgaris implies
in P. grandiflora (Heslop-Harrison, 19766) even that ion pumps are present in the plasmalemma of
shorter, about 5 d. This short period of whole leaf these cells, .whose surface area is greatly extended
activity, rather than autolysis of the secretory cells, by its irregular outline and by the presence of
explains why the digestive glands in Pinguicula can numerous cytoplasmic evaginations within the
perform only one secretion-absorption cycle in slime layer. The high osmotic concentraion in the
contrast to Dionaea, where the digestive glands are apoplast of the secretory cells by the active efflux
capable of repeated reaction (Scala, Schwab and of ions from the cytoplasm partly explains the fact
Simmons, 1968; Schwab, Simmons and Scala, that the volume fraction of the slime layer is
1969). maintained at approximately the same level during
From the ultrastructural data obtained and on the whole secretion and absorption cycle, not-
the analysis of the published information, the withstanding the leakage of slime.
following putative model of digestive gland opera- Heslop-Harrison and Heslop-Harrison (1980)
tion in P. vulgaris, after stimulation, is proposed. believe that the pumps operate in the plasmalemma
A trapped insect is attacked by hydrolases present of the barrier cell. We feel that this is unlikely.

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 350 Vassilyev and Muravnik—infrastructure o/Pinguicula vulgaris L.

However, in the Utricularia digestive glands, the This is consistent with the terminal character of
barrier (pedestal) cells, rather than secretory cells, such gland activity in this species.
remove the excess water from the trap and absorb Most of the nutrients taken up through the
the digestion products (Fineran, 1985). A feature plasmalemma of the secretory cells are transported
of the pedestal cells of this genus is the highly along the concentration gradient into the barrier
developed labyrinthine wall. and then into the reservoir cell, through, it is
The efflux of Cl~ ions from the secretory cells supposed, the numerous plasmodesmata which
of the Pinguicula glands may be coupled to the traverse the periclinal walls of the gland cells.
active secretion of H+ ions. The accumulation of Considerably less nutrient reaches the Casparian
H+ ions in the digestive fluid lowers its pH and strip, moving within the apoplast. The strip is an
thus favours the activity of acid hydrolases. A effective barrier for free diffusion and the nutrients
similar suggestion has been made by Robins and enter the barrier cell through its plasmalemma in
Juniper (1980c) for the digestive glands of Dionaea. the region of its upper periclinal wall.
Thus, the different components of the digestive The significance of the fairly wide periplasmic
fluid in P. vulgaris are secreted from the head cells space filled by the electron opaque material
by different pathways. Ions and water are released observed in the barrier cell 4 h after stimulation
through the entire plasmalemma surface (eccrine when absorption was at its maximum, remains
secretion) while the hydrolytic enzymes add to the to be established. There is still no explanation
slime layer components by exocytosis of vacuoles for the fact of the retention and even the additional
and coated vesicles (granulocrine secretion) or by formation of protein crystals in the nucleus of the
the transient fusion of ER with the plasmalemma. barrier cell and of the expansion of the osmiophilic
This conclusion agrees with the suggestion made inclusions in the leucoplasts in this cell, nor of the
earlier by Robins (1976) for Dionaea that the appearance of similar inclusions in the leucoplasts
release of water and proteins occurs by different of the reservoir cell in both stimulated and
mechanisms. unstimulated glands with age.
We believe that, as in Dionaea (Robins and Thus, from the above evidence, the activity of
Juniper, 1980rf), the absorption of the digestion the digestive glands on stimulation appears to
products by the sessile glands in Pinguicula starts have much in common with that of Dionaea
very shortly after the onset of secretion and that glands. The major difference is in the rate of
both activities proceed simultaneously. This bi- digestion and absorption, which proceeds much
directional flow is under the control of the secretory more rapidly in Pinguicula.
cells. The active secretion of H+ ions from the
cytoplasm is accompanied by their absorption ACKNOWLEDGEMENTS
along a concentration gradient. Such an inward We are grateful to Professor P. Bell for his
passive uptake of protons is obviously coupled to encouragement, helpful discussion and corrections
the eccrine absorption of aminoacids, sugars, of the manuscript.
peptides and other low molecular substances
which are formed as a result of the hydrolysis of LITERATURE CITED
insect tissue on the leaf surface. The secretory cells, FINERAN, B. A., 1985. Glandular trichomes in Utricu-
with their extended plasmalemma surface, secrete laria: a review of their structure and function. Israel
ions and absorb nutrients as true transfer cells. Rea Journal of Botany 34, 295-330.
and Whatley (1983) also follow the idea of the HESLOP-HARRISON, Y. 1975. Enzyme release in carni-
H+-amino acid co-transport in the secretory cells vorous plants, pp. 525-78. In Lysosomes in Biology
and Pathology, eds J. T. Dingle and R. T. Dean, vol.
of the Dionaea glands. The one-way mechanism of 4, 614 pp. Biological Press, B.V., North Holland
absorption, suggested by Heslop-Harrison and Division, Amsterdam.
Knox (1971) and Heslop-Harrison (1976a), ap- , 1976 a. Enzyme secretion and digest uptake in
pears less attractive than the hypothesis supported carnivorous plants, pp. 463-76. In Perspectives in
above. Experimental Biology, ed. N. Sunderland, vol 2,
523 pp. Pergamon Press, Oxford.
The highly active mitochondria of the secretory
cells of the P. vulgaris glands, during the whole , 19766. Carnivorous plants a century after Darwin.
secretion and absorption phase, provide the Endeavour 35, 114-22.
and HESLOP-HARRISON, J. 1980. Chloride ion
energy required for increasing gland activity. movement and enzyme secretion from the digestive
However, unlike Robins and Juniper'sfindingsin glands of Pinguicula. Annals of Botany 45, 729-31.
Dionaea (1980o, c) we did not note any changes , 1981. The digestive glands of Pinguicula:
in structure and number of the mitochondria structure and cytochemistry. Annals of Botany 47,
consistent with increased respiration in P. vulgaris. 293-319.

Downloaded from https://academic.oup.com/aob/article-abstract/62/4/343/546268

by University of Durham user
on 24 March 2018
 Vassilyev and Muravnik—infrastructure
and KNOX, R. B., 1971. A cytocheraical study of the
leaf-gland enzymes of insectivorous plants of the
genus Pinguicula. Planta 96, 183-211.
REA, P. A., JOEL, D. M. and JUNIPER, B. E., 1983.
Secretion and redistribution of chloride in the
digestive glands of Dionaea muscipula Ellis (Venus's
flytrap) upon secretion stimulation. New Phylologisi
94, 359-66.
and WHATLEY, F. R., 1983. The influence of
secretion elicitors and external pH on the kinetics of
D-alanine uptake by the trap lobes of Dionaea
muscipula Ellis (Venus's flytrap). Planta 158,
312-9.
ROBINS, R. J., 1976. The nature of the stimuli causing
digestive juice secretion in Dionaea muscipula Ellis
(Venus's flytrap). Planta 128, 263-5.
and JUNIPER, B. E., 1980a. The secretory cycle of
Dionaea muscipula Ellis. I. The fine structure and the
effect of stimulation on the fine structure of the
digestive gland cells. New Phytologist 86, 279-96.
, 19806. The secretory cycle of Dionaea
Downloaded from https://academic.oup.com/aob/article-abstract/62/4/343/546268
by University of Durham user
on 24 March 2018
of Pinguicula vulgaris L. 351
muscipula Ellis. II. Storage and synthesis of the
secretory proteins. New Phytologist 86, 297-311.
, 1980 c. The secretory cycle of Dionaea
muscipula Ellis. III. The mechanism of release of
digestive secretion. New Phytologist 86, 313-27.
, 1980rf. The secretory cycle of Dionaea
muscipula Ellis. V. The absorption of nutrients. New
Phytologist 86,413-22.
SCALA, J., SCHWAB, D. and SIMMONS, E., 1968. The fine
structure of the digestive gland of Venus's flytrap.
American Journal of Botany 55, 649-57.
SCHWAB, D. W., SIMMONS, E. and SCALA, J., 1969. Fine
structure changes during function of the digestive
gland of Venus's flytrap. American Journal of
Botany 56, 88-100.
VASSILYEV, A. E. and MURAVNIK, L. E., 1988. The
ultrastructure of the digestive glands in Pinguicula
vulgaris (Lentibulariaceae) relative to their function.
I. The changes during the maturation. Annals of
Botany (in press).