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.2011 Sep 13;108(37):15492-7.
doi: 10.1073/pnas.1112535108. Epub 2011 Sep 6.

A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap

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A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap

María Escalante-Pérez et al. Proc Natl Acad Sci U S A..

Abstract

Venus flytrap's leaves can catch an insect in a fraction of a second. Since the time of Charles Darwin, scientists have struggled to understand the sensory biology and biomechanics of this plant, Dionaea muscipula. Here we show that insect-capture of Dionaea traps is modulated by the phytohormone abscisic acid (ABA) and jasmonates. Water-stressed Dionaea, as well as those exposed to the drought-stress hormone ABA, are less sensitive to mechanical stimulation. In contrast, application of 12-oxo-phytodienoic acid (OPDA), a precursor of the phytohormone jasmonic acid (JA), the methyl ester of JA (Me-JA), and coronatine (COR), the molecular mimic of the isoleucine conjugate of JA (JA-Ile), triggers secretion of digestive enzymes without any preceding mechanical stimulus. Such secretion is accompanied by slow trap closure. Under physiological conditions, insect-capture is associated with Ca(2+) signaling and a rise in OPDA, Apparently, jasmonates bypass hapto-electric processes associated with trap closure. However, ABA does not affect OPDA-dependent gland activity. Therefore, signals for trap movement and secretion seem to involve separate pathways. Jasmonates are systemically active because application to a single trap induces secretion and slow closure not only in the given trap but also in all others. Furthermore, formerly touch-insensitive trap sectors are converted into mechanosensitive ones. These findings demonstrate that prey-catching Dionaea combines plant-specific signaling pathways, involving OPDA and ABA with a rapidly acting trigger, which uses ion channels, action potentials, and Ca(2+) signals.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
(A) ABA (50 μM) desensitizes traps. Forty-eight hours after ABA application, more than two trigger-hair displacements are required for trap closure (n = 60). (B) Upon drought stress (soil water content below 70%) more than two hair stimulations are required to elicit trap closure (n = 12). (C) Quantification of ABA levels (pmol ABA/gFW) in the trap lobes of well watered and of water deficientDionaea at 50% soil water content (FW, fresh weight,n = 6 ± SD).
Fig. 2.
Fig. 2.
(A) Insect (ant) capture results in OPDA synthesis. Note that OPDA levels increased already more than twofold 30 min after prey capture. Maximal levels (sixfold) were measured after 1 wk (n = 4, one-way ANOVA, Tukey HSD test,P < 0.05).
Fig. 3.
Fig. 3.
COR mimics an eatable prey. Spray application ofDionaea lobes with 1 mM COR induced transient opening of the trap, followed by secretion onset, slow trap closure, and external stomach formation. Time (in hours) is shown inside the boxes (n = 5).
Fig. 4.
Fig. 4.
Quantification of COR-induced secretion. (A) The lobe of aDionaea trap was divided in six sectors (A to F), and the number of glands were counted. (B andC) Close-up view of nonsecreting glands (B) in comparison with COR-stimulated secreting glands (C). (D) Quantification of gland surfaces of nonsecreting and COR-stimulated (48 h, 100 μM COR) secretingDionaea traps divided into sectors as illustrated inA (n = 20 traps ± SD). (E–G) Quantification of the volume (E,n = 10 ± SE), protein content (F,n = 6 ± SE), and pH (G,n = 12 ± SE) of secreted fluids plotted against the time after COR application. (H) Exogenous application of 1 mM COR increased endogenous OPDA levels in COR-treated traps (local) as well as in nonstimulated traps (systemic;n = 4, one-way ANOVA, Tukey HSD test,P < 0.05).
Fig. 5.
Fig. 5.
(A) View on the inner leaflet of a trap lobe. (Inset) FURA-2 loaded iontophoretically into a gland cell complex via a micropipette impaled into a secretory cell. (B) AP in responses to single trigger hair displacements in the presence (red) and absence (black) of 1 mM COR. (C) Quantification of APs shown in A. (Inset) AP amplitude (Upper) and duration (at 50% of amplitude,Lower). The columns represent the average of at least six independent measurements; the bars are ± SD (t test,P ≤ 0.001 indicated by an asterisk). (D) Spontaneous APs (relative values) leading to a trap closure 8.5 h after COR exposure. Four of the six examined plants generated a series of APs after trap closure. (E) Calcium transient elicited by 3 APs. APs were elicted by individual mechanical stimulation of single trigger hairs. ADionaea gland cell was impaled with a double-barrelled microelectrode and iontophoretically loaded with the calcium sensitive dye FURA-2 as shown inA Inset. Plasma-membrane potential (lower trace) monitored simultaneously with the FURA-2 F345/390 fluorescence ratio (upper trace). In 7 of 14 cells, the AP was accompanied by a calcium transient. (F) Scheme for the involvement of ABA and jasmonates (OPDA) in the prey capture byD. muscipula. When trigger hairs of the Venus flytrap are mechanically stimulated by a prey, mechanosensitive ion channels are activated and generate receptor potentials, which in turn induce APs and the lobes of the trap abruptly close. A successful prey capture leads to consecutive touching of the trigger hairs by the struggling prey, which stimulates the synthesis of OPDA and the rise of cytosolic [Ca2+]. These chemical factors herald the start of the second phase of trap closure, which is accompanied by secretion of lytic enzymes from the glands and the hermetically sealing of the trap (stomach formation). In addition, the synthesis of OPDA systemically presensitizes other traps of the carnivore and positively feeds back on trap excitability. In contrast, drought stress (ABA) decreases the excitability of traps because prey digestion is accompanied by an enormous consumption of water.
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References

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