Skip Navigation


JXB Advance Access originally published online on May 12, 2006
Journal of Experimental Botany 2006 57(9):2087-2092; doi:10.1093/jxb/erj165
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow Supplementary Data
Right arrow All Versions of this Article:
57/9/2087    most recent
erj165v1
Right arrow E-letters: Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when E-letters are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (3)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Kaiser, H.
Right arrow Articles by Grams, T. E. E.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kaiser, H.
Right arrow Articles by Grams, T. E. E.
Agricola
Right arrow Articles by Kaiser, H.
Right arrow Articles by Grams, T. E. E.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

© The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

RESEARCH PAPER

Rapid hydropassive opening and subsequent active stomatal closure follow heat-induced electrical signals in Mimosa pudica*

Hartmut Kaiser1,{dagger} and Thorsten E. E. Grams2

1Botanisches Institut der Christian-Albrechts-Universität zu Kiel, Olshausenstraße 40–60, D-42098 Kiel, Germany
2Ecophysiology of Plants, Technische Universität München, Am Hochanger 13, D-85354 Freising, Germany

{dagger}To whom correspondence should be addressed. E-mail: hkaiser{at}bot.uni-kiel.de

Received 27 September 2005; Accepted 16 February 2006


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 Supplementary data
 References
 
In Mimosa pudica L., heat stimulation triggers leaflet folding in local, neighbouring and distant leaves. Stomatal movements were observed microscopically during this folding reaction and electrical potentials, chlorophyll fluorescence, and leaf CO2/H2O-gas exchange were measured simultaneously. Upon heat stimulation of a neighbouring pinna, epidermal cells depolarized and the stomata began a rapid and pronounced transient opening response, leading to an approximately 2-fold increase of stomatal aperture within 60 s. At the same time, net CO2 exchange showed a pronounced transient decrease, which was followed by a similar drop in photochemical quantum yield at photosystem (PS) II. Subsequently, CO2-gas exchange and photochemical quantum yield recovered and stomata closed partly or completely. The transient and fast stomatal opening response is interpreted as a hydropassive stomatal movement caused by a sudden loss of epidermal turgor. Thus, epidermal cells appear to respond in a similar manner to heat-induced signals as the pulvinar extensor cells. The subsequent closing of the stomata confirms earlier reports that stomatal movements can be induced by electrical signals. The substantial delay (several minutes) of guard cell turgor loss compared with the immediate response of the extensor and epidermal cells suggests a different, less direct mechanism for transmission of the propagating signal to the guard cells.

Key words: Chlorophyll fluorescence, electrical signals, guard cells, Mimosa pudica, stomata


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 Supplementary data
 References
 
In Mimosa pudica, wounding by cutting or burning triggers the propagation of a signal, which causes upfolding of leaflets of neighbouring pinnae and distant leaves. Responsible for this folding is a rapid loss of turgor in the extensor cells in the pulvini of leaves, pinnae, and leaflets (Weintraub, 1952). The transmission of the stimulus is associated with systemic electric, hydraulic, and chemical responses (Braam, 2005). The nature of the primary signal, however, is still uncertain. An electrical signal with variable form and duration is propagated, which is involved in local (leaf level) and distant responses (Houwink, 1935; Sibaoka, 1953, 1966, 1969). However, propagation of the response may also occur through dead tissue (Houwink, 1935; Ricca, 1916), which points against an exclusive role of action potentials in long-distance signalling. In addition, distant responses could be elicited by hydraulic signals, which arise from a rapid release of xylem tension caused by release of water into the apoplast at the wounded site and by deflating extensor cells (Malone, 1994; Ricca, 1916). Such changes in xylem pressure are reported to cause local depolarizations similar to a propagating electrical signal (Stahlberg and Cosgrove, 1997). In this view, the electrical events are not the travelling stimulus but rather the effects of the hydraulic signals (Malone, 1994; Mancuso, 1999). The hydraulic dispersal of solutes released to the apoplast could also distribute chemical signals (Ricca, 1916) at a speed sufficient to explain the propagation of the leaf folding response (Malone, 1994; Rhodes et al., 1999).

The mechanism by which the extensor cells lose and recover their turgor is only partly understood (Braam, 2005). The cellular mechanisms of both processes are very similar to those responsible for guard cell swelling and shrinking. In pulvinar motor cells, Cl– efflux causes a rapid depolarization, outward rectifying K+-channels open and release K+, which then causes a loss of turgor (Allen, 1969; Stoeckel and Takeda, 1993). This basic process also causes guard cell turgor loss (MacRobbie, 1998). In Mimosa extensor cells, however, the velocity of water release is much higher than expected from known membrane permeabilities and, therefore, mechanisms such as solute-water co-transporters or aquaporins are suggested (Fleurat-Lessard et al., 1997a, b; MacRobbie, 1999; Morillon et al., 2001). The mechanisms of turgor build-up during the regeneration of extensor cells is analogous to the processes involved in turgor increase during stomatal opening. In brief, in both cases, proton pumping of an H+-ATPase (Fleurat-Lessard et al., 1997b; Serrano, 1989) is the driving force, which then promotes the uptake of K+ and an increase of the osmotic potential. Despite those similarities, the question if guard cells respond to the propagating heat-induced signal in a similar manner to extensor cells has not been examined.

This study was motivated by a previous study on chlorophyll fluorescence, gas exchange, and electrophysiological responses of M. pudica (Koziolek et al., 2004), where a strong decrease in assimilation rate during leaf folding and a concomitant decrease in photochemical quantum yield at PSII was observed. While net CO2 exchange dropped, leaf transpiration first rapidly increased, reaching a peak after approximately 150 s, and subsequently declined to a low level (Koziolek et al., 2004). The reason for this extraordinarily fast transient increase in water loss has not been commented on in previous work. With current knowledge, both a true stomatal opening response as well as a release of water into the extracellular spaces appeared possible. In this study this question was addressed by microscopic observation of stomatal aperture and the sequence of events in the lamina physiology upon heat-induced electrical signals is reported.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 Supplementary data
 References
 
Plant culture and experimental set-up
Plants were cultivated from seeds under standard greenhouse conditions and with optimal water and nutrient supply.

Stomatal aperture, chlorophyll fluorescence, electrical potential, and leaf gas exchange were recorded simultaneously on the same, attached pinna of Mimosa pudica plants (Fig. 1). In order to allow these simultaneous measurements, a gas exchange cuvette was designed into which one leaf of the plant was inserted. At the tip of an adjacent leaf outside the cuvette, heat stimulation using a flame was carried out. In order to allow for microscopic observation, assessment of chlorophyll fluorescence, and measurement of membrane potential it was necessary to fix most of the leaflets of one pinna with the adaxial side to a Perspex plate with double-sided transparent adhesive tape (Tesa 56661–2, Tesa, Hamburg, Germany). Some terminal leaflets of the same pinna were left unfixed to determine the timing of leaflet folding. Subsequently, the plate was mounted inside the cuvette, which allows observation of the lower leaf surface with a microscope lens mounted in the bottom of the gas-exchange cuvette (Kaiser and Kappen, 2001). Temperature and air humidity were set to 22 °C and a leaf–air mole fraction of water vapour ({Delta}W) of 5 mmol mol–1, respectively. Irradiance (PPFD of approximately 400 µmol photons m–2 s–1) was provided by a halogen light source (LS2, Hansatech, UK). After inserting one pinna into the gas-exchange cuvette, the whole plant was allowed to relax and adjust to measuring conditions for at least 24 h.


Figure 1
View larger version (44K):
[in this window]
[in a new window]
  		Fig. 1 Schematic plan of the experimental set-up allowing assessments of leaf gas exchange (CO2, H2O), chlorophyll fluorescence, epidermal electrical potential, and stomatal aperture at a pinna of a M. pudica plant.

 
Membrane potential
In the same experimental set-up (Fig. 1) and simultaneously with the other measurements, changes in the electric membrane potential of abaxial epidermal cells were monitored using glass microelectrodes with tip diameters of less than 1 µm, back-filled with 3 M KCl. These electrodes were inserted into the leaf epidermis using a micromanipulator. Electrical potential was recorded between the microelectrode and an Ag/AgCl reference electrode, which was connected to a cut end of another twig of the plant by immersion into artificial pond water (APW). Potentials were recorded by a FD23 electrometer (WPI Inc, USA) connected to a datalogger (CR10, Campbell Scientific, UK).

Stomatal aperture
Digital images of stomatal apertures on the lower leaf surfaces were recorded at a maximum rate of 1 image per 10 s during leaflet folding with a modified inverted microscope (Axiovert 25CFL, Zeiss; Kaiser and Kappen, 2001) equipped with a long-distance lens (x50) and a video camera. Subsequently, apertures (stomatal pore areas) were measured with custom image-analysis software.

Chlorophyll fluorescence
Simultaneously with the other measurements, fluorescence imaging of several leaflets covering the area of aperture and electrical measurements was used to assess the spatiotemporal variations of the photochemical quantum yield of energy conversion in PSII (Siebke and Weis, 1995) by means of an IMAGING-PAM Chlorophyll fluorimeter (Heinz Walz GmbH, Effeltrich, Germany). This system allows non-invasive determination of the photochemical quantum yield at PSII by the saturation pulse method (Genty et al., 1989; Schreiber et al., 1986). Saturation pulses were given every 12 s and photochemical quantum yield at PSII was calculated as (F'm – F)/F'm (for nomenclature, see Kooten and Snel, 1990).

Leaf gas exchange
Gas-exchange measurements allowing calculation of stomatal conductance (gh2o) and net CO2-exchange rate (JCO2) were either performed simultaneously with the other measurements by means of a modified gas-exchange system (Heinz Walz GmbH, Effeltrich, Germany, Fig. 1, for details see Kaiser and Kappen, 2001) or carried out independently using a Li-Cor 6400 system (Li-Cor, Nebraska, USA).


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 Supplementary data
 References
 
Approximately 40 s after heat stimulation of a neighbouring leaf at a distance of approximately 8–11 cm, the net CO2 gas exchange of the observed leaf started to decline transiently to nearly zero within 1 min. This transient reduction started at the instant of leaflet upfolding. Subsequently, net CO2 exchange recovered within the following 20 min to the initial levels (Fig. 2). Stomatal conductance rapidly increased during the first 2 min after heat stimulation and subsequently declined to approximately half of the values before the heat stimulation. Similar to the net CO2 gas exchange, stomatal conductance recovered in the following 20 min to values similar to the initial rates.


Figure 2
View larger version (12K):
[in this window]
[in a new window]
  		Fig. 2 Stomatal conductance (gH2O) and net CO2 exchange (JCO2) during leaflet folding. The measured leaflets were fixed and not allowed to fold. The vertical line (time zero) indicates the time of heat stimulation of an adjacent pinna.

 
Aperture measurements revealed a fast opening movement leading to a doubling of aperture. Although there was considerable variability in stomatal aperture between plants and experiments (cf. Figs 3, 4), the transient stomatal opening was consistently observed when leaves folded. This opening movement was completed within 1–2 min and followed by a pronounced closing movement approximately 1–2 min later (Fig. 3; a movie of these stomatal responses is available as supplemental material from http://jxb.oxfordjournals.org/). Four to five minutes after heat stimulation, observed stomata appeared completely closed. The sequence of reactions in electrical potential, leaflet upfolding, stomatal movement, and photochemical quantum yield at PSII is presented in Fig. 4. The measurements shown were conducted at the same spot of one leaflet as indicated in Fig. 5A. Within 1 min after stimulation of an adjacent leaf, the electrical potential dropped sharply at the observed leaflet, simultaneously with leaflet upfolding (which was prevented at the observed pinna by fixing of leaflets, see Materials and methods). At the same time, the opening response of the stomata started, leading to an increase of stomatal aperture of 80–100% within the next 60 s (cf. Fig. 3). However, a decline of photochemical quantum yield at PSII occurred only 2 min after heat stimulation, when the stomatal opening response was nearly completed (Fig. 5C) and 3.5 min after stimulation it reached a minimum of approximately 0.2. Chlorophyll fluorescence imaging revealed a high heterogeneity in photochemical quantum yield of 0.1 or lower (Fig. 5; a movie is available as supplemental material from http://jxb.oxfordjournals.org/). Recovery of photochemical quantum yield started in parallel with the recovery of electrical potential and was completed within 2 to 3 min (Figs 4, 5D).


Figure 3
View larger version (100K):
[in this window]
[in a new window]
  		Fig. 3 Time-course of stomatal apertures during leaf folding and images of stomata from the same experiment taken at three different times (A, B, C). Legend symbols in (A) mark three stomata whose responses are plotted in the graph. Time zero is the time of heat stimulation of an adjacent pinna.

 

Figure 4
View larger version (12K):
[in this window]
[in a new window]
  		Fig. 4 Heat stimulation of an adjacent leaf caused the following responses: (a) changes of membrane potential measured with a microelectrode inserted into an epidermal cell on the abaxial leaf surface. Measurements were performed a few millimetres apart from the site of stomata observation, (b) aperture response of three stomata, and (c) photochemical quantum yield at PSII. Assessment of chlorophyll fluorescence was performed on the same spot as the aperture measurements. The vertical lines mark the times of heat stimulation (dotted) and leaf folding (dashed). Letters indicate the times of the yield measurements shown in Fig. 5.

 

Figure 5
View larger version (110K):
[in this window]
[in a new window]
  		Fig. 5 Images of photochemical quantum yield at PSII in the moment of stimulation (A) and after 72 s (B), 156 s (C), and 228 s (D) in the experiment shown in Fig. 4. The circle in (A) indicates the spot where the fluorescence and aperture measurements shown in Fig. 4 were performed.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
Supplementary data
 References
 
In the leaf of Mimosa pudica, not only the pulvinar motor cells respond to heat-induced signals, but the physiology of the entire leaf lamina is strongly affected (Fig. 5). When the electrical signal arrived at the observed leaf area, net CO2 exchange started to decline transiently (Fig. 2). Approximately 1 min later, photochemical quantum yield at PSII was also decreased to values of 0.1–0.2 (Figs 4, 5). This observed transient knockout of the dark and light reactions of photosynthesis are in accordance with a previous report (Koziolek et al., 2004) and are similar to recently published observations in poplar (Lautner et al., 2005).

Koziolek et al. (2004) also reported a rapid transient increase of transpiration when leaves were prevented from reducing their transpiring area by overlapping their leaflets during the upfolding reaction. From the gas-exchange measurements alone, Koziolek et al. (2004) could not identify the reason for the transient increase in water loss. In this work, direct evidence for a fast and substantial stomatal response triggered by heat stimulation of distant leaves is presented. This stomatal response is complex and consists of two phases, (i) a fast opening response which is followed by (ii) a pronounced reduction of stomatal aperture. In principle, stomata can open for two reasons: an increase in guard cell turgor or a decrease in epidermal turgor. An increase in guard cell turgor requires energy and is inherently slow. By contrast, ‘hydropassive’ stomatal movements are caused by an epidermal turgor loss without any energy-dependent osmotic increases of guard cell turgor and, thus, can be quite fast. The best known example for such hydropassive movements is the Iwanoff-effect (Iwanoff, 1928), which occurs after cutting a transpiring leaf, and the transient stomatal opening caused by a sudden increase in leaf-to-air mole fraction water difference (Kappen et al., 1987; Kappen and Haeger, 1991). Due to the quickness of the opening movement (phase 1), it is concluded that it is not osmotically driven but caused by a sudden loss of epidermal turgor. The sequence of events supports this interpretation. Stomatal opening started exactly when epidermal cells depolarized and leaflets folded. The most likely explanation for the initial opening response (phase 1) is that epidermal cells, similar to the pulvinar motor cells, respond with depolarization and a decrease of turgor. Another possible explanation for passive stomatal movements might be the hydraulic pressure wave which travels through the mimosa plant (Hooke, 1667; Malone, 1994). However, an increase in pressure should result in stomatal closure rather than opening because it would increase epidermal backpressure on guard cells. In fact, Malone's measurements (1994) give evidence that the pressure wave leads to a transient increase of leaf thickness. However, during leaf folding this initial increase of leaf thickness was reversed and followed by a sharp decline of leaf thickness (by approximately 16 %). Although Malone did not interpret these measurements in this functional manner, they are in accordance with the proposition of epidermal turgor loss.

During the second phase of stomatal response following the initial opening, aperture declined at various rates (cf. Fig 3, 4). In some cases, an extremely fast response led to full closure of previously widely opened stomata within 1.5 min (Fig. 3). As far as is known, such fast closing responses have not previously been reported. Stomatal closure can be caused either by a decrease in guard cell turgor or a recovery of epidermal turgor and it is difficult to differentiate between these two mechanisms. However, since stomata closed further than their initial aperture before the heat stimulation, it is likely that guard cell osmotic potential decreased.

Stomata of M. pudica apparently do not respond directly to the depolarization of the epidermal membrane potential as their closing response was delayed for several minutes. This is not surprising, when considering the fact that they are electrically isolated by the lack of plasmodesmata to the adjacent epidermal cells (Palevitz and Hepler, 1985). Therefore, guard cell deflation is most likely not triggered directly by the electrical signal traveling through the leaf tissue, but by indirect factors. These could include apoplastic factors as well as an increased intercellular CO2-concentration due to the inhibition of photosynthesis. Although substantially delayed, the closing response is, nevertheless, a stomatal response, which is ultimately triggered by propagating heat-induced signals. These results underline the possible involvement of electrical signals in long-distance signalling for co-ordinating leaf gas exchange on the whole plant level (Fromm, 1998; Fromm and Eschrich, 1993; Van Sambeek and Pickard, 1976).

When the heat-induced signal reaches a Mimosa leaf, both the pulvinar and epidermal cells lose turgor at the same time. This demonstrates that, although pulvinar motor cells are specialized to perform a very fast and substantial turgor loss upon depolarization, this ability is also present in epidermal cells. In addition to the evidence from chlorophyll fluorescence and gas-exchange measurements, these results underline that the entire leaf and not only the pulvini undergo intense physiological responses. These results present evidence that the heat-induced signal causes (i) a rapid, hydropassive stomatal opening response as a result of turgor loss of the surrounding epidermal cells, and (ii) an active stomatal closure concomitant with a loss of net CO2 uptake.


   Supplementary data
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Supplementary data
References
 
Supplemental material to this paper is available at http://jxb.oxfordjournals.org/


   Acknowledgements
 
We want to thank Heike Scholz for taking sympathetic care of these sensitive plants.


   Footnotes
 
* This paper is dedicated to Professor Ludger Kappen. Back


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Supplementary data
 References
 
Allen RD. (1969) Mechanism of the seismonastic reaction in Mimosa pudica. Plant Physiology 44:1101–1107.[Abstract/Free Full Text]

Braam J. (2005) In touch: plant responses to mechanical stimuli. New Phytologist 165:373–389.[CrossRef][Web of Science][Medline]

Fleurat-Lessard P, Bouche-Pillon S, Leloup C, Bonnemain JL. (1997a) Distribution and activity of the plasma membrane H+-ATPase in Mimosa pudica L. in relation to ionic fluxes and leaf movements. Plant Physiology 113:747–754.[Abstract]

Fleurat-Lessard P, Frangne N, Maeshima M, Ratajczak R, Bonnemain JL, Martinoia E. (1997b) Increased expression of vacuolar aquaporin and H+-ATPase related to motor cell function in Mimosa pudica L. Plant Physiology 114:827–834.[Abstract]

Fromm J. (1998) Electrical signaling and gas exchange in maize plants of drying soil. Plant Science 132:203–213.[CrossRef]

Fromm J and Eschrich W. (1993) Electric signals released from roots of willow (Salix viminalis L.) change transpiration and photosynthesis. Journal of Plant Physiology 141:673–680.

Genty B, Briantais J-M, Baker NR. (1989) The relationship between the quantum yield of of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990:87–92.

Hooke R. (1667) Micrografia , London.

Houwink AL. (1935) The conduction of excitation in Mimosa pudica. Recueil des Travaux Botaniques Neerlandais 32:51–91.

Iwanoff L. (1928) Zur Transpirationsbestimmung am Standort. Berichte der Deutschen Botanischen Gesellschaft 46:306–310.

Kaiser H and Kappen L. (2001) Stomatal oscillations at small apertures: Indications for a fundamental imperfection of stomatal feedback-control inherent in the stomatal turgor mechanism. Journal of Experimental Botany 52:1303–1313.[Abstract/Free Full Text]

Kappen L, Andresen G, Lösch R. (1987) In situ observations of stomatal movements. Journal of Experimental Botany 38:126–141.[Abstract/Free Full Text]

Kappen L and Haeger S. (1991) Stomatal responses of Tradescantia albiflora to changing air humidity in light and in darkness. Journal of Experimental Botany 42:979–986.[Abstract/Free Full Text]

Koziolek C, Grams TEE, Schreiber U, Matyssek R, Fromm J. (2004) Transient knockout of photosynthesis mediated by electrical signals. New Phytologist 161:715–722.[CrossRef]

Lautner S, Grams TEE, Matyssek R, Fromm J. (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiology 138:2200–2209.[Abstract/Free Full Text]

MacRobbie EAC. (1998) Signal transduction and ion channels in guard cells. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 353:1475–1488.

MacRobbie EAC. (1999) Vesicle trafficking: a role in trans-tonoplast ion movements? Journal of Experimental Botany 50:925–934.[Abstract]

Malone M. (1994) Wound-induced hydraulic signals and stimulus transmission in Mimosa pudica L. New Phytologist 128:49–56.[CrossRef]

Mancuso S. (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera. Australian Journal of Plant Physiology 26:55–61.

Morillon R, Lienard D, Chrispeels MJ, Lassalles JP. (2001) Rapid movements of plants organs require solute-water cotransporters or contractile proteins. Plant Physiology 127:720–723.[Free Full Text]

Palevitz BA and Hepler PK. (1985) Changes in the coupling of stomatal cells of Allium and Commelina communis demonstrated by microinjection of Lucifer yellow. Planta 164:473–479.[CrossRef][Web of Science]

Rhodes JD, Thain JF, Wildon DC. (1999) Evidence for physically distinct systemic signalling pathways in the wounded tomato plant. Annals of Botany 84:109–116.[Abstract/Free Full Text]

Ricca JC. (1916) Soluzione d'un problema di fisiologia. La propagazione di stimulo nella Mimosa. Nuove Giornale Botanico Italiano 23:51–170.

Schreiber U, Schliwa U, Bilger W. (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorimeter. Photosynthesis Research 10:51–62.

Serrano R. (1989) Structure and function of plasma membrane ATPase. Annual Review of Plant Physiology and Plant Molecular Biology 40:61–84.[CrossRef][Web of Science]

Sibaoka T. (1953) Some aspects of on the slow conduction of stimuli in the leaf of Mimosa pudica. Science Report, Tohoku University (Biological) 20:72–88.

Sibaoka T. (1966) Action potentials in plant organs. Symposium of the Society for Experimental Biology 20:49–74.

Sibaoka T. (1969) Physiology of rapid movements in plants. Annual Review of Plant Physiology 20:165–184.

Siebke K and Weis E. (1995) Assimilation images of leaves of Glechoma hederacea: analysis of non-synchronous stomata related oscillations. Planta 196:155–165.[Web of Science]

Stahlberg R and Cosgrove DJ. (1997) The propagation of slow wave potentials in pea epicotyls. Plant Physiology 113:209–217.[Abstract]

Stoeckel H and Takeda K. (1993) Plasmalemmal, voltage-dependent ionic currents from excitable pulvinar motor cells of Mimosa pudica. Journal of Membrane Biology 131:179–192.[Medline]

Van Kooten O and Snel JFH. (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research 25:147–150.[CrossRef]

Van Sambeek JW and Pickard BG. (1976) Mediation of rapid electrical, metabolic, transpirational, and photosynthetic changes by factors released from wounds. III. Measurements of CO2 and H2O flux. Canadian Journal of Botany 54:2662–2671.

Weintraub M. (1952) Leaf movements in Mimosa pudica. New Phytologist 50:357–382.[CrossRef]


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 ANN BOT (LOND)Home page
A. Pavlovic, V. Demko, and J. Hudak
Trap closure and prey retention in Venus flytrap (Dionaea muscipula) temporarily reduces photosynthesis and stimulates respiration
Ann. Bot., November 3, 2009; (2009) mcp269v1.
[Abstract] [Full Text] [PDF]

Home page
 Plant Physiol.Home page
H. Kaiser and N. Legner
Localization of Mechanisms Involved in Hydropassive and Hydroactive Stomatal Responses of Sambucus nigra to Dry Air
Plant Physiology, February 1, 2007; 143(2): 1068 - 1077.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow Supplementary Data
Right arrow All Versions of this Article:
57/9/2087    most recent
erj165v1
Right arrow E-letters: Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when E-letters are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (3)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Kaiser, H.
Right arrow Articles by Grams, T. E. E.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kaiser, H.
Right arrow Articles by Grams, T. E. E.
Agricola
Right arrow Articles by Kaiser, H.
Right arrow Articles by Grams, T. E. E.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?