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Jasmonates trigger prey-induced
formation of ‘outer stomach’ in
carnivorous sundew plants
rspb.royalsocietypublishing.org
Yoko Nakamura1, Michael Reichelt2, Veronika E. Mayer3 and Axel Mithöfer1
1
Department of Bioorganic Chemistry, and 2Department of Biochemistry, Max Planck Institute for Chemical
Ecology, Hans Knöll Strasse 8, 07745 Jena, Germany
3
Department of Structural and Functional Botany, Faculty of Life Sciences, University of Vienna, Rennweg 14,
1030 Vienna, Austria
Research
Cite this article: Nakamura Y, Reichelt M,
Mayer VE, Mithöfer A. 2013 Jasmonates trigger
prey-induced formation of ‘outer stomach’ in
carnivorous sundew plants. Proc R Soc B 280:
20130228.
http://dx.doi.org/10.1098/rspb.2013.0228
Received: 31 January 2013
Accepted: 27 February 2013
Subject Areas:
plant science
Keywords:
carnivorous plants, Drosera, leaf movement,
auxin, jasmonate, chemonasty
Author for correspondence:
Axel Mithöfer
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2013.0228 or
via http://rspb.royalsocietypublishing.org.
It has been widely accepted that the growth-related phytohormone auxin is the
endogenous signal that initiates bending movements of plant organs. In 1875,
Charles Darwin described how the bending movement of leaves in carnivorous
sundew species formed an ‘outer stomach’ that allowed the plants to enclose and
digest captured insect prey. About 100 years later, auxin was suggested to be the
factor responsible for this movement. We report that prey capture induces both
leaf bending and the accumulation of defence-related jasmonate phytohormones. In Drosera capensis fed with fruitflies, within 3 h after prey capture and
simultaneous with leaf movement, we detected an increase in jasmonic acid
and its isoleucine conjugate. This accumulation was spatially restricted to the
bending segment of the leaves. The application of jasmonates alone was sufficient to trigger leaf bending. Only living fruitflies or the body fluids of
crushed fruitflies induced leaf curvature; neither dead flies nor mechanical treatment had any effect. Our findings strongly suggest that the formation of the
‘outer stomach’ in Drosera is a chemonastic movement that is triggered by
accumulation of endogenous jasmonates. These results suggest that in carnivorous sundew plants the jasmonate cascade might have been adapted to facilitate
carnivory rather than to defend against herbivores.
1. Introduction
Carnivorous plants of the worldwide genus Drosera (sundew) catch their prey by
using adhesive traps baited with sticky polysaccharide mucilage [1,2]. The glue is
produced by stalked glands (the so-called tentacles) on the leaves’ surface. The
glands also secrete enzymes to digest captured prey and to absorb the resulting
nutrients. Once the prey (mainly small insects) comes in contact with the sticky
glands, the lateral glandular tentacles bend towards the prey, which can no
longer escape, and move it to the centre of the leaf [1,2]. Mechanical and chemical
stimuli from the prey induce electric potentials in the glands that move towards the
base of the tentacles in the epidermal layer of the leaf [3]. After this first, fast tentacle movement, a second, slower movement of the whole leaf starts to enclose the
caught prey [1]. As a consequence, the prey comes in contact with numerous digestive glands. In Drosera capensis, the cape sundew that is indigenous to South Africa,
this curvature of the adaxial leaf surface is highly pronounced: because the leaf
almost completely encloses the prey, an ‘outer stomach’ is formed [4] (figure 1).
Although Darwin [1] described the leaf-bending phenomenon, real prey-induced
endogenous plant signals that direct this movement have so far not been identified.
Early studies of the endogenous plant signals in Drosera leaf movement
suggested a role for the phytohormone auxin, indole-3-acetic acid (IAA) [4,5].
Based on studies with the auxin transport inhibitor 2,3,5-triiodobenzoic acid
(TIBA), the authors concluded that captured prey induced an IAA flux from the
leaf tip downstream to the bending point. However, radio-labelled auxin,
3-indolyl-(2– 14C)-acetic acid, provided externally to the tip of a D. capensis leaf,
was not transported basipetally to the site of the prey [4]. In addition, the external
application of IAA induced only weak bending [5]. In a different experiment, an
anti-IAA antiserum-based enzyme immunoassay suggested the presence of
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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increased auxin at the site of the prey [4]. Unfortunately, a control for the presence of cross-reacting substances in the provided
‘prey’ (a piece of cheese) was missing. Moreover, false-positive
results by the anti-IAA antiserum owing to cross-reactivity
with structurally non-related compounds could not be ruled
out [6]. Thus, whether auxin represents the signal responsible
for outer stomach formation remained unknown.
In this study, we provided Drosophila melanogaster as prey
and subsequently analysed the induced phytohormone level
in the Drosera leaves upon prey capture. Leaf bending was a chemonastic movement initiated by a chemical signal derived from
the insect, not by simple mechanical treatments. Exogenously
applied phytohormones were used to trigger leaf bending
without prey. We correlate the leaf bending with the presence
of jasmonate, and suggest that the jasmonate signalling
pathway was involved when plants developed carnivory.
2. Results and discussion
Living fruitflies (D. melanogaster) were provided as prey
in order to observe the kinetics of the bending reaction in
D. capensis. Within a short time after prey capture, the leaves
started to bend at the exact site where the flies were placed;
after 3 h, bending was highly pronounced (figure 2a,b).
Analysis of the treated leaves showed that IAA levels did
not change, in contrast to the significant increase in oxylipin
phytohormones, namely jasmonic acid (JA) and its physiologically most active form, the isoleucine conjugate (JA-Ile;
figure 2c). Jasmonates are phytohormones that regulate plant
developmental processes as well as defences [7–9]. To further
investigate whether the accumulation of jasmonates was
restricted to the bending segment only, leaves challenged
by D. melanogaster were cut into three parts (non-curled
upper part, curled middle part and non-curled lower part;
figure 3a) and analysed. Compared with the control, after
3 h, only the curled tissue of the leaves showed the
Proc R Soc B 280: 20130228
Figure 1. Drosera capensis leaf 12 h after insect prey capture. Scale bar, 1 cm.
2
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1 cm
accumulation of JA and JA-Ile (1.67 versus 241.5 ng gFW21
and 0.1 versus 42.0 ng gFW21, respectively). Moreover, the
increase in jasmonate levels was drastic, whereas IAA
levels (6.13 versus 12.6 ng gFW21) increased only twofold
(figure 3b). The results strongly suggested that jasmonates at
the very least contributed to the leaves’ movement. Therefore,
an external application of these phytohormones should be sufficient to induce leaf bending without the presence of prey.
Indeed, as expected, JA-Ile induced bending at the site of application (figure 4). Moreover, the biosynthetic precursors of
jasmonates—12-oxo-phytodienoic acid (OPDA), JA and its synthetic mimic, coronalon [10]—were able to induce the same
reaction (see the electronic supplementary material, figure S1a).
The leaf curvature reaction was concentration-dependent (see
the electronic supplementary material, figure S2). Occasionally,
the leaf became completely rolled, which sometimes can also
be seen upon prey capture. Interestingly, the bending reaction
was observed only in the adaxial part of the leaf, regardless of
whether the stimulus was applied adaxially or abaxially,
indicating that leaf curvature in D. capensis is a nastic movement.
In contrast to jasmonates, IAA did not induce such leafbending reaction either at low (1 mM) or high concentrations
(1 mM; electronic supplementary material, figure S1b), supporting our results that auxin was not the only determining
factor for the leaf movement. However, the role of auxin in
the orchestration of plant movements is well established
[11]. Thus, we speculated that not a locally increased IAA
concentration but a local IAA gradient along the adaxial/
abaxial axis was involved. Such gradient might have been
induced by jasmonates. Because it was impossible to determine
phytohormone concentrations in both the upper and lower
epidermis independently, TIBA was used to inhibit auxin
transport. Therefore, the curvature of the leaves was determined in degrees [5]. In control plants, coronalon induced
leaf bending (119.38 + 72.9; n ¼ 14), whereas in the presence
of TIBA the coronalon-initiated bending (83.68 + 66.7;
n ¼ 11) was as often induced as inhibited, resulting in nonsignificant differences ( p ¼ 0.22; Mann–Whitney rank sum
U-test). This inconsistent result can be explained by the fact
that TIBA needs to interact directly with its target proteins localized in leaf lamina cells to execute its action; but in contrast to
the tentacles, some exogenously applied compounds hardly
penetrate the cuticle and enter the epidermal or mesophyll
cells, as shown for the fluorescent dyes Calcofluor White and
DAPI (see the electronic supplementary material, figure S3),
an observation that was also mentioned recently [12].
Jasmonates are induced by various stress factors such as
insect herbivory or tissue wounding [9,13]. In D. capensis,
there is no tissue wounding involved because the mouthparts
of D. melanogaster are spongy and unable to injure the plant.
Thus, the question remained: what was responsible for the
induction of jasmonate biosynthesis and the subsequent leaf
bending—contact with the tentacles and the leaf surface, or
chemical stimuli? This issue has never been investigated systematically. When provided as prey, living D. melanogaster
induced movement in leaves, unlike dead flies or small
stones (figure 5). These results suggested that the movement
of flies struggling to escape the adhesive trap elicited the
response. However, the stimulation of the tentacles and the
leaves with a small brush could not induce leaf bending,
which argues against the response being a thigmonastic reaction. When we observed that the presence of dead, crushed
flies caused a strong leaf-bending reaction (figure 5), we
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(a)
3
1.5 h
3h
45 min
1.5 h
3h
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45 min
Proc R Soc B 280: 20130228
(b)
(c)
*
150
n.s.
60
JA (ng gFM–1)
IAA (ng gFM–1)
80
n.s.
40
n.s.
20
0
*
*
100
50
0
0
50
100
time (min)
150
200
0
50
100
time (min)
150
200
JA-Ile (ng gFM–1)
30
*
25
20
15
10
5
n.s.
*
0
0
50
100
time (min)
150
200
Figure 2. Kinetics of leaf bending in Drosera capensis. (a) Control leaves and (b) leaves after capture of two living Drosophila melanogaster. Arrows indicate the
position of the flies. Scale bars, 1 cm. (c) Phytohormone concentrations (ng per g fresh weight; 3 – 5 leaves were collected for one single measurement) in
D. capensis leaves treated with (white circle) and without (black circle) D. melanogaster after 45, 90 and 180 min (mean + s.d.; n ¼ 5). Asterisks indicate significant differences between treatments; n.s., not significant (ANOVA, SNK-test, p , 0.001). Five leaves were collected for each single time point. All phytohormones
were analysed in parallel from the same samples. IAA, indole-3-acetic acid; JA, jasmonic acid; JA-Ile, jasmonic acid – isoleucine conjugate. (Online version in colour.)
concluded that certain insect-derived compounds, recognized
as chemical signals by the plant, were inducing the response.
However, such chemical cues might be released as well
during the effort by captured, living flies to escape but not
by dead, intact flies. Darwin [1] observed the leaf edge of
Drosera rotundifolia bending 24 h after challenge with dead
prey, and dead fruitflies induced leaf curvature in D. capensis
after 1 day [14]. In fact, this does not contradict our hypothesis because once the digestion of dead insect prey has
started, chemical signals are released and available, although
delayed by several hours. Thus, we argue that prey-derived
material serves as a signal for the plant to generate jasmonates and, eventually, to induce the chemonastic movement
of D. capensis leaves to form the ‘outer stomach’. Up to
now, only one other example is known where jasmonates
are involved in plant movements, namely tendril coiling in
Bryonia dioica [6,15]; but in contrast to Drosera, tendril coiling
is a thigmonastic reaction induced only by touch as external
stimulus. However, in B. dioica also exogenously applied
auxin can induce tendril coiling [15].
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(a)
4
m
u
(b) 500
JA-Ile
*
420
x - fold increase
300
200
100
*
145
n.s.
2.8 4.1 0.9
0
upper
*
2.0
middle
n.s.
1.7 3.0 1.1
lower
phytohormones
Figure 3. (a) Definition of Drosera capensis leaf segments observed 3 h after
fruitfly capture; u, upper; m, middle; l, lower. (b) Phytohormone analyses of
the various segments (9–12 leaves were collected for each single measurement);
indicated is the increase in the respective phytohormone 3 h after capture of two
Drosophila melanogaster compared with the control. From left to right: jasmonic
acid (black bar), jasmonic acid–isoleucine conjugate (grey bar), indole-3-acetic
acid (white bar); exact values are given above the bars (n ¼ 3). Asterisks indicate
significant differences between treatments; n.s., not significant (ANOVA, SNK-test,
p , 0.001 for JA and JA-Ile, p , 0.003 for IAA).
The exact nature of the chemical signals in Drosera–insect–
prey interaction remains to be elucidated. The signals could
simply be any kind of nutrient that is valuable for the plant.
However, other types of stress besides herbivory and wounding can induce jasmonate accumulation in plants; for example,
pathogen-derived elicitors that eventually induce plant defences in cell suspension cultures [16,17]. Similarly, in some
plant–insect interactions, fatty acid–glutamine conjugates
from feeding herbivores have been shown to actively induce
jasmonates and, subsequently, direct and indirect defences
[18,19]. Conceivably, the molecule that is recognized by
D. capensis and initiates the formation of the ‘stomach’ could
be any defence-activating signalling compound as defined by
herbivore-associated molecular patterns [20]. Specifically, in
carnivorous sundew, the jasmonate cascade, which is typically
involved in plant defence against insect herbivores, might be
used to facilitate prey capture.
Recently, in Dionaea muscipula, the venus flytrap, it was
shown that application of the Pseudomonas syringae-derived
phytotoxin coronatine, a structural mimic of jasmonates,
induced leaf lobes to close, thereby forming the ‘outer stomach’
of this carnivorous plant [21]. However, this movement took
several hours, whereas the natural closing induced by prey is
accomplished within a second [22,23]. Why in those experiments only the phytotoxin was active but jasmonates failed
remained an unsolved question. Moreover, even upon prey
capture, only after several hours could an increase in OPDA
be measured, and then less than twofold, but no increase in
JA and JA-Ile was detected. These results prevent us from concluding that jasmonates have a role in the prey capture
mechanism in Dionaea as well. In carnivorous plants,
D. m.
D. m. †
stone
brush
D. m., crushed
Figure 5. Drosera capensis leaves treated with different modes of prey: two
living individuals of Drosophila melanogaster (D. m.); two dead individuals of
D. melanogaster (D. m. †); a small stone with the size of two fruitflies; challenge with a brush for 15 min; freshly crushed D. melanogaster (D. m.,
crushed). The leaves shown represent three different plants. Each single
photo was taken after 12 h, immediately after cutting off the leaves. Arrows
indicate the position of the prey. Scale bars, 1 cm. (Online version in colour.)
Proc R Soc B 280: 20130228
Figure 4. Three Drosera capensis leaves treated with three 10 ml-drops JA-Ile
( jasmonic acid – isoleucine conjugate, 100 mM) at the same time in the
centre of the adaxial site of the intact leaf. The leaves shown represent
three different plants. Photograph taken after 12 h, immediately after cutting
off the leaves. Scale bar, 1 cm.
400
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l
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(a) Plant material and treatment
Drosera capensis L. plants were grown in the greenhouse at 22–248C
(day) and 20–228C (night), 60–70 per cent humidity, and light
from 6.00 to 22.00. Plants were kept wet the entire time with collected rain water. All treatments were performed with the intact
leaves of the plants for the time indicated in the particular
experiments. Applications were done in the centre of adult leaves.
For treatment with Drosophila melanogaster (reared on conventional cornmeal agar), either two living or two dead flies (frozen
at 2208C) were placed on the same leaf site with a distance of
approximately 5 mm between them. Living flies were cooled
on ice for 30 min before being used. In the signal compound
treatment, three 10 ml drops (100 mM, if not indicated otherwise)
or water for the control were applied side by side. For inhibitor
(250 mM) experiments, 10 ml drops were applied 2 h before
jasmonates (100 mM) were added at the same site for 6 h. Fluorescent dye (Calcofluor White M2R 1 mg ml21 for cell wall
staining; DAPI 10 mg ml21 for DNA staining) uptake was documented by an Olympus BX 41 reflecting fluorescence microscope
equipped with a colour view soft imaging system.
JA was synthesized from commercially available methyl-JA
(Sigma) by saponification; JA-Ile, coronalon and OPDA were synthesized according to [26 – 28]; IAA, TIBA and fluorescent dyes
were purchased (Calcofluor White: Fluka, DAPI: Sigma), respectively. All experiments were performed independently at least
three times.
(b) Quantification of jasmonic acid, JA-Ile, OPDA and
indole acetic acid in sundew leaves
Five leaves were collected for each single measurement of phytohormones. Plant material of individually treated leaves was
The work was supported by the Max Planck Society. Special thanks
to W. Boland and J. Gershenzon for continuous support,
I. Lichtscheidl for valuable advice with the fluorescent staining,
and A. Lehr, C. Lembke, B. Arnold, T. Krügel, S. Trautheim,
J. Vadassery and A. Bellaire for help in the laboratory, growing
plants, providing fruitflies and stimulating discussions. We thank
E. Wheeler, Boston, for editorial assistance.
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Zorbax Eclipse XDB-C18 column (50 4.6 mm, 1.8 mm, Agilent).
Formic acid (0.05%) in water and acetonitrile was used as mobile
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injection volume was 2 ml. An API 5000 tandem mass spectrometer (Applied Biosystems) equipped with a Turbospray ion
source was operated in the negative ionization mode. The instrument parameters were optimized by infusion experiments with
pure standards, where available. The ion spray voltage was maintained at 24500 eV. The turbo gas temperature was set at 7008C.
Nebulizing gas was set at 60 psi, curtain gas at 25 psi, heating
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rspb.royalsocietypublishing.org
jasmonates might be involved in chemonastic reactions rather
than in thigmonastic movements.
As already known, jasmonates are part of a network of
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studies will analyse how phytohormones cross-talk to initiate
leaf movement in Droseraceae and other plants. Insights into
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In addition, our findings suggest that jasmonates, in addition
to auxin, might be involved in growth-dependent plant
movements such as in phototropism or gravitropism [11].
The availability of highly sensitive analytical methods for
phytohormone analyses will allow a deeper understanding of
the roles and networking of various phytohormones.
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