Electrical and chemical signals in short-term systemic photosynthetic responses of tobacco plants to local burning

Department of Experimental Physics, Laboratory of Biophysics, Palacký University, tr. Svobody 26, 771 46 Olomouc, Czech Republic.
Planta (Impact Factor: 3.26). 01/2007; 225(1):235-44. DOI: 10.1007/s00425-006-0325-x
Source: PubMed


Short-term (up to 1 h) systemic responses of tobacco (Nicotiana tabacum cv. Samsun) plants to local burning of an upper leaf were studied by measuring the following variables in a distant leaf: extracellular electrical potentials (EEPs); gas exchange parameters; fast chlorophyll fluorescence induction; and endogenous concentrations of three putative chemical signaling compounds-abscisic (ABA), jasmonic (JA), and salicylic (SA) acids. The first detected response to local burning in the distant leaves was in EEP, which started to decline within 10-20 s of the beginning of the treatment, fell sharply for ca. 1-3 min, and then tended to recover within the following hour. The measured gasometric parameters (stomatal conductance and the rates of transpiration and CO(2) assimilation) started to decrease 5-7 min after local burning, suggesting that the electrical signals may induce stomatal closure. These changes were accompanied by systemic increases in the endogenous ABA concentration followed by huge systemic rises in endogenous JA levels started after ca. 15 min, providing the first evidence of short-term systemic accumulation of these plant hormones in responses to local burning. Furthermore, JA appears to have an inhibitory effect on CO(2) assimilation. The correlations between the kinetics of the systemic EEP, stomatal, photosynthetic, ABA, and JA responses suggest that (1) electrical signals (probably induced by a propagating hydraulic signal) may trigger chemical defense-related signaling pathways in tobacco plants; (2) both electrical and chemical signals are interactively involved in the induction of short-term systemic stomatal closure and subsequent reductions in the rate of transpiration and CO(2) assimilation after local burning events.

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    • "The link between electrical signalling and jasmonate accumulation is now well recognized [29], [48], [49], [50]. Jasmonates are lipid-derived compounds acting as key signaling molecules in plant stress responses [51]. "
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    ABSTRACT: The trap of the carnivorous plant Venus flytrap (Dionaea muscipula) catches prey by very rapid closure of its modified leaves. After the rapid closure secures the prey, repeated mechanical stimulation of trigger hairs by struggling prey and the generation of action potentials (APs) result in secretion of digestive fluid. Once the prey's movement stops, the secretion is maintained by chemical stimuli released from digested prey. We investigated the effect of mechanical and chemical stimulation (NH4Cl, KH2PO4, further N(Cl) and P(K) stimulation) on enzyme activities in digestive fluid. Activities of β-D-glucosidases and N-acetyl-β-D-glucosaminidases were not detected. Acid phosphatase activity was higher in N(Cl) stimulated traps while proteolytic activity was higher in both chemically induced traps in comparison to mechanical stimulation. This is in accordance with higher abundance of recently described enzyme cysteine endopeptidase dionain in digestive fluid of chemically induced traps. Mechanical stimulation induced high levels of cis-12-oxophytodienoic acid (cis-OPDA) but jasmonic acid (JA) and its isoleucine conjugate (JA-Ile) accumulated to higher level after chemical stimulation. The concentration of indole-3-acetic acid (IAA), salicylic acid (SA) and abscisic acid (ABA) did not change significantly. The external application of JA bypassed the mechanical and chemical stimulation and induced a high abundance of dionain and proteolytic activity in digestive fluid. These results document the role of jasmonates in regulation of proteolytic activity in response to different stimuli from captured prey. The double trigger mechanism in protein digestion is proposed.
    PLoS ONE 08/2014; 9(8):e104424. DOI:10.1371/journal.pone.0104424 · 3.23 Impact Factor
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    • "They confirmed the electrical nature of the heat-induced wound signal, showing a signal with variation-potential character to spread via the phloem systemically within the plant. Interference of electrical signals with plant photosynthesis has now been demonstrated for a wide range of species, for example, from the green algae genus Chara, tobacco, maize and Venus flytrap or soybean (Hlavackova et al. 2006; Grams et al. 2007; Krupenina & Bulychev 2007; Pavlovic, Demko & Hudak 2010; Pavlovic 2012; Gallé et al. 2013). Despite the recent progress that has been achieved in understanding heat-induced electrical and hydraulic signal transduction and their effects on photosynthesis and stomatal aperture, mechanisms underlying the phenomenon of the transient knockout of net CO2 uptake still require further clarification. "
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    ABSTRACT: Leaf photosynthesis of the sensitive plant Mimosa pudica displays a transient knockout in response to electrical signals induced by heat stimulation. This study aims at clarifying the underlying mechanisms, in particular, the involvement of respiration. To this end, leaf gas exchange and light reactions of photosynthesis were assessed under atmospheric conditions largely eliminating photorespiration by either elevated atmospheric CO2 or lowered O2 concentration (i.e. 2000 μmol mol-1 or 1 %, respectively). In addition, leaf gas exchange was studied in the absence of light. Under darkness, heat stimulation caused a transient increase of respiratory CO2 release simultaneously with stomatal opening, hence reflecting direct involvement of respiratory stimulation in the drop of the net CO2 uptake rate. However, persistence of the transient decline in net CO2 uptake rate under illumination and elevated CO2 or 1% O2 makes it unlikely that photorespiration is the metabolic origin of the respiratory CO2 release. In conclusion, the transient knockout of net CO2 uptake is at least partially attributed to an increased CO2 release through mitochondrial respiration as stimulated by electrical signals. Putative CO2 limitation of Rubisco due to decreased activity of carbonic anhydrase was ruled out as the photosynthesis effect was not prevented by elevated CO2.
    Plant Cell and Environment 06/2013; 37(1). DOI:10.1111/pce.12150 · 6.96 Impact Factor
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    • "In the case of the sensitive plant Mimosa pudica, reduction of net CO 2 exchange and F PSII in a neighbouring leaf is much stronger than observed in other plant species, and stomatal conductance rapidly increases during the first 2 min after heat stimulation, and subsequently declines to approximately half of the initial value before heat stimulation (Koziolek et al., 2003; Kaiser and Grams, 2006). A rapid decline in stomatal conductance and photosynthesis in neighbouring leaves after heat stimulation also occurs in tobacco (Hlaváčková et al., 2006). In our experiment with Dionaea, no reactions of stomata after mechanical stimulation were observed; therefore, we can exclude stomatal limitation of photosynthesis (Fig. 1C "
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    ABSTRACT: The carnivorous plant Venus flytrap (Dionaea muscipula) produces a rosette of leaves: each leaf is divided into a lower part called the lamina and an upper part, the trap, with sensory trigger hairs on the adaxial surface. The trap catches prey by very rapid closure, within a fraction of a second of the trigger hairs being touched twice. Generation of action potentials plays an important role in closure. Because electrical signals are involved in reduction of the photosynthetic rate in different plant species, we hypothesized that trap closure and subsequent movement of prey in the trap will result in transient downregulation of photosynthesis, thus representing the energetic costs of carnivory associated with an active trapping mechanism, which has not been previously described. Traps were enclosed in a gas exchange cuvette and the trigger hairs irritated with thin wire, thus simulating insect capture and retention. Respiration rate was measured in darkness (RD). In the light, net photosynthetic rate (AN), stomatal conductance (gs) and intercellular CO2 concentration (ci) were measured, combined with chlorophyll fluorescence imaging. Responses were monitored in the lamina and trap separately. Irritation of trigger hairs resulted in decreased AN and increased RD, not only immediately after trap closure but also during the subsequent period when prey retention was simulated in the closed trap. Stomatal conductance remained stable, indicating no stomatal limitation of AN, so ci increased. At the same time, the effective quantum yield of photosystem II (PSII) decreased transiently. The response was confined mainly to the digestive zone of the trap and was not observed in the lamina. Stopping mechanical irritation resulted in recovery of AN, RD and PSII. We put forward the first experimental evidence for energetic demands and carbon costs during insect trapping and retention in carnivorous plants, providing a new insight into the cost/benefit model of carnivory.
    Annals of Botany 11/2009; 105(1):37-44. DOI:10.1093/aob/mcp269 · 3.65 Impact Factor
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