«Peristomatal Transpiration» and Stomatal Movement: A Controversial View

Institut fUr Botanik und Mikrobiologie der Technischen Universitat, MUnchen, Federal Republic of Germany

«Peristomatal Transpiration» and Stomatal Movement: A Controversial View II. Observation of Stomatal Movements under Different Conditions of Water Supply and Demand UTA MAIER-MAERCKER

With 11 figures Received July 30, 1978 . Accepted August 30, 1978

Summary Stomatal movement was observed under controlled cuvette conditions. When the humidity of the air was changed, stomatal response was linear or slightly curvilinear and exhibited hysteresis. While with detached Vicia faba plants the response became steeper with every succeeding day, curves obtained from rooted plants of Commelina communis had a common regression line during five consecutive days. The influence of air velocity and water supply to the roots were then studied. Increased air velocity (in the range of 0,3-1,3 m X sec-1 made impossible wide stomatal apertures while moderate stomatal opening) was not impeded. Restrictions of water supply (with mannitol solutions) resulted in depressions of opening relative to the humidity range; parallel graphs were obtained. After removing the mannitol from the roots, the original response was resumed. When potassium chloride was added to the water supply, maximum aperture was reached in high humidity. However, the response to changes in humidity was stronger. Rinsing the roots had no effect, but when in imitation of rain, the leaves were exposed to trickling water, the potassium effect was occasionally overcome. The results were discussed in the light of peristomatal transpiration. The view is held that the environmental variables (supply and demand) are cross-correlated and that stomatal response meets the supply-demand-relationship at the level of the subsidiary cell. Hysteresis is explained with the competition between water flux into the guard cell and transpiration of the subsidiary cell. Salt effects are seen in terms of local gradients between cell wall and cell vacuole. Following sudden illumination a steep gradient will enhance salt permeation into the guard cell and with it wide opening. On increased evaporative demand, the steep gradient assists in drawing water from the vacuole, increased closing tendency being the result.

Key words: Stomatal movement, peristomatal transpiration, evaporative demand.

Introduction

Stomatal response to air humidity - the subject of many papers - has led to conflicting views (HALL et ai., 1976). The general view holds that by the water Z. Pflanzenphysiol. Bd. 91. S. 157-172. 1979.

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saturation deficit of the air the bulk leaf water potential is reduced. This, via negative feedback system, controls stomatal aperture. In addition, experiments have proven that there is a direct response of stomata to evaporative demand, and it seems that this response is independent of the leaf tissue water content (LANGE et aI., 1971, 1975; SCHULZE et aI., 1972, 1974, 1975; HALL and KAUFMANN, 1975; HALL et aI., 1976; ASTON, 1976; LOSCH, 1977). Interactions between humidity and bulk leaf water status in determining stomatal resistance have been considered (SCHULZE, 1972, 1974, 1975; HALL et aI., 1976; KAUFMANN, 1976; ASTON, 1976; LOSCH, 1976; STERN et aI., 1977). Because of a discrepancy of stomatal aperture and actual leaf water potential it was concluded that «the effects of internal control mechanisms are overruled and/or modified by external climatic conditions» (SCHULZE, 1975). Since the mechanism of direct response is attributed to peristomatal transpiration this conclusion led to the belief that peristomatal transpiration «may exert an additional open-loop control over stomatal aperture» (RASCHKE, 1975, 1976). In this series the view is held that the environmental variables (supply and demand) are cross-correlated (MAIER-MAERCKER, 1979) and that the relationship of supply and demand is the determining factor. The following experiments were designed to provide information in support of this VIew. Materials and Methods Vicia Jaba and Commelina communis were grown from the seed in nutrient soil, outdoors during the summer, later in the year under normal greenhouse conditions. When the seedlings of Vicia faba had the first pair of fully expanded leaves, the stems were cut off under water and with the lower stem portion remaining in tap water. Commelina seedlings were dug out and the soil particles carefully removed by rinsing with tap water. The chamber (10.5 X 6 X 3.5 centimeters, built by Heinz Walz, £ffeltrich) provided sufficient space for the entire plant and a vial for water supply. The vial mouth was sealed around the stem of the plant using terostat (Terosone, Heidelberg). The vial was fixed in a horizontal position at the chamber bottom. Using Scotch-tape, one leaf with its abaxial side up, was firmly attached to a small aluminium stage. A square window cut into the heavy Plexiglass lid allowed microscope observation of the leaf surface through a coverslip which was cemented into the window frame. Through a hole in the side of the vial, a syringe could be inserted for replenishing or exchanging the liquid content, care being taken not to derange the set-up. Using a srew at the outside wall of the chamber the stage could be moved up right under the cover-slip window. For the sake of free air circulation, the stage was only raised for the brief periods of observation. Air was passed through the chamber with a flow rate of approx. 12.5 IIh, and the carbon dioxide content was kept normal. Humidity was controlled by a Siemens water vapour trap with the dew point temperatures adjusted to different values. Disregarding the dew point setting, the actual relative humidity of the air within the chamber was determined with the Hygroscope BT «rotronic» (Debrunner, Zurich), its sensor element in the chamber being in close vicinity of the leaf surface. Air circulation was provided by a built-in fan, the rotary velocity of which could be varied. Z. PJlanzenphysiol. Bd. 91. S. 157-172.1979.

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The leaf received light through the chamber window while the roots were kept in the dark. Total radiation, measured at the level of the leaf was approx. 30 Wxm- 2 with an illumination level of 16,000 Ix (mercury vapour lamp: HQI E 400 W). The air above the chamber was ventilated. For temperature control the whole chamber was placed in a water bath. Water flow through a Siemens water vapour trap (here used as a thermostate) kept the chamber temperature at a constant 24°C. Variations never exceeded 0.25°C. Leaf temperature was 0.8 °C above the air temperature on the average. Relative humidity of the air and its temperature were determined inside the chamber and continuously recorded with a Siemens Compensograph. For determining stomatal aperture the chamber was taken out of the water bath and placed under a microscope equipped with incident light (Leitz Ultropak). A micrometerstage assisted in finding the reference area of the leaf surface throughout the experiment. Before the experiments were started a rough sketch of this area was made. Certain characteristics of the epidermis, such as peculiarities of cell pattern, anomalous cells, hair distribution etc. made it possible that the same porus could be located within seconds and its aperture measured with an eyepiece graticule using a magnification of X 656. Since the chamber was made of aluminium (wall diameter 10 mm) the temperature of the air inside did not vary within the short time of measurement. Heating of the air space above the leaf by the incident light was kept at a tolerable level by the use of a heat absorption filter and by working as fast as possible. When everything was set for the experiment, the mounted plant was allowed a period of 18 hours for adjustment in a relative humidity of 75 0/0. Measurements were taken at steps of approx. 10 0/0 in the humidity range. Decreases occurred at a very slow rate (in steps of twO degrees dew point setting). When the desired level was reached humidity was kept constant for one hour before stomatal aperture was determined. Stomatal aperture was plotted against the water saturation deficit of the air. Any graph shown in this paper is representative of at least twenty similar experiments.

Results I. Stomatal responses to changes in humidity a) Vi cia faba

Even within small leaf areas the width of the porus varied greatly no matter how long the leaf had spent in a given constant humidity atmosphere. Aperture of stomata, in general, was found to increase with their proximity to a leaf vein. Table 1 features average stomatal widths; the measurements were taken in close proximity and in some distance from the vein and were arranged accordingly. The Table 1: Vida Jaba: Stomatal apertures (per cent of maximum) in air of different water saturation deficit (average of 25 measurements).

3.052 7.63 9.81 13.09

(86 (65 (55 (40

Ofo RH) Ofo RH) Ofo RH) Ofo RH)

proximal to a vein

distant from vein

100 Ofo 75 Ofo 72.3 Ofo 53.75 Ofo

100 Ofo 68.3 Ofo 50.5 Ofo 27.5 Ofo

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table revealed of how little reliability results can be when a small number of stomata are taken at random «for statistics». It was, therefore, decided to record the aperture of individual stomata through the full range of relative humidity. With increasing water saturation deficit of the air the aperture of any of the stomata decreased in a linear or slightly curvilinear manner. The slope of the graphs varied considerably (fig. 1).

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Fig. 1: Detached plant (Vicia faba): Response of three different stomata to changes humidity.

III

air

Even completely closed stomata opened immediately when the humidity of the air was increased. But when a plant was left for only a few hours in an atmosphere of high water saturation deficit (less than 30 Ofo RH), it took the stomata more than 24 hours to achieve opening even in very high relative humidity. However, when this aftereffect was overcome, stomata reached the same apertures as before. The response of the same stoma to decreases in air humidity was higher with every succeeding day of experiment (one run per day). The graphs obtained gradually became steeper (fig. 2). The response was different when humidity was decreased or increased in a stepwise manner. The resulting graph reveals the characteristics of a typical hysteresis (fig. 3). This phenomenon is not accounted for by a different speed of adjustment. The readings were the same for several hours. When in the second run, step decreases in humidity were changed into step increases before the minimum of aperture was reached, readings were on different curves (fig. 3).

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'/, 100 80

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Fig. 2: Detached plant (Vicia faba): Response of one stoma to changes in air humidity during 3 succeeding days. x-x first day, 0-8 second day, Ii:" ... Ii:" third day. '/, 100 80

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Fig. 3: Detached plant (Vicia faba): Response of one stoma to increasing and decreasing water deficit of the air. x-x step decreases of air humidity, @-@ step increases of air humidity, 0---0 Second run. Increase in humidity beginning before the minimum aperture is reached (8--G). Ii:"-Ii:,, Decrease in air humidity before the maximum aperture is reached.

b) Commelina communis

In contrast to Vi cia faba, whole plants of Commelina communis were used with their roots dipped in tap water. Curves obtained from one individual stoma were almost straight and had a common regression line during five consecutive days (fig. 4). It occurred quite often that the highest value of aperture did not coincide with the

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.,. 100 80

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Fig. 4: Rooted plant (Commelina communis): Response of one stoma during 4 succeeding days. Vertical arrows represent opening in response to reillumination after a dark period of 8 hours. Oblique arrow in downward direction indicates high response to decrease in humidity after this dark-light treatment.

highest value of the humidity range; maximum aperture was reached at around 85 0 /0 RH. This width was taken as 100 010. Stomata could not be brought to complete closure by decreasing humidity below 30 Ofo RH. When the stomatal pore had narrowed to about 25010 (of the max. aperture) stomata apparently started to oscillate. Hysteresis of stomatal response is not a characteristic of detached stems or leaves. Entire plants with intact roots showed the same phenomenon (fig. 5). Overshoots of 20 Ofo were usual when humidity was increased in the low range. Ascending and descending curve branches always have more or less corresponding curvature (fig. 6). That means that stomata which were less sensitive to decreases in humidity were able to open wider when humidity was increased (fig. 6). Such behaviour was the usual for the stomata in close vicinity of a leaf vein. When in an atmosphere of high humidity stomata with wide apertures were darkened for several hours they closed but partially (20-50 Ofo of max. aperture). When light was again switched on, they opened within minutes to the maximum. Stomata with small apertures hardly opened upon reillumination when the preceding dark period was in a dry atmosphere (30010 RH). A small overshoot was observed (fig. 4). At medium humidity stomata opened moderateiy in response to reillumination. About one hour after the onset of light they had reached about the aperture they had before the light was switched off. During several hours the opening proceeded up to very high (sometimes maximum) readings. But when at this point humidity of the air was lowered, the response of the stomata was extremely high (fig. 4).

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Fig. 5: Rooted plant (Commelina communis): Response of one stoma to increasing and decreasing water deficit of the air. x-x step decreases of air humidity, ®-® step increases of air humidity, R:,-R:, decrease in air humidity before the maximum aperture is reached, e-e step increases in air humidity before minimum aperture is reached.

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Fig. 6: Graphs illustrating the response of twO stomata to changes in air humidity. The dotted lines represent a stoma in close vicinity of a vein.

II. Stomatal response to air velocity

If the seedlings of Commelina communis had an intact root system and illumination was continuous, stomatal response to humidity changes of the air remained practically unaltered for a period of up to five days (fig. 4). One full scale experiment (with only the humidity changed) was then compared to readings Z. PJlanzenphysiol. Bd. 91. S. 157-172. 1979.

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obtained when the rotary velocity of the fan was increased in stepwise manner. In the initial experiment the operating voltage of the fan was kept at 0,8 V (standard voltage in all experiments was 1 V, the actual air velocity at the level of the leaf being approx. 0.15 m X sec-I). With the power increased to 3 V (air velocity: 0.775 m X sec-I) stomatal aperture drastically decreased at any given humidity. Oscillations were evidently suppressed. In general, wide apertures were more affected than smaller ones. When humidity was decreased in a stepwise manner and the velocity of the air kept constant, curvilinear graphs were obtained. They became gradually steeper in the high humidity range when air velocity was increased (fig. 7). This means that windspeed (in the range of 0.3-1.3 m X sec-I) prohibits wide stomatal apertures but may not impede stomata to open moderately. "/. 100 80

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Fig. 7: Rooted plant (Commelina communis): Response of one stOma to changing humidity and velocity of the air x-x zero m/sec, . - - 0,3 m/sec, 8-8 0,425 m/sec [:=:J-[:=:J 0,775 m/sec b-b 1,3 m/sec.

Ill. Stomatal response to changes in air humidity with water supply limited After the stomatal response to changes in humidity was recorded, the tap water around the roots of the plant was replaced by a 15 mM (tap water) solution of mannitol. The plant was allowed to adjust to an atmosphere of 75 % RH for 12 hours. Thereafter the humidity was raised almost to the saturation point and stomatal aperture was measured two hours later. Stomata did not reach maximum aperture. Gradually reduced air humidity caused the same relative response. The graph based on this response turned out to be parallel to the initial curve which was obtained while the roots were in water (fig. 8). The response to step increases in humidity (hysteresis!) showed the same opening depression. Further decreases in solute potential of the supply resulted in further depressions of stomatal apertures. A set of parallel graphs was obtained (fig. 9). Z. P/lanzenphysiol. Bd. 91. S. 157-172. 1979.

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"Ie 100 80

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Fig. 8: Rooted plant (Commelina communis): Response of one stoma to changes in air humidity with unrestricted and restricted water supply. x-x plant with roots in tap water, G-G in a 15 mM solution of mannitol 0--0 in tap water after repeated rinsing of the rOOt. +--0-- and +--&--readings of each of the ascending curve branches.

Fig. 9: Rooted plant (Commelina communis): Response of one stoma to changes in air humidity; water supply increasingly restricted; x-x plant with the roots in tap water, G-G in 10 mM mannitol, &::,-& 20 mM, Q-Q 30mM, 0 - 0 in water after repeated rinsing of the roots.

After mannitol was carefully removed from the roots (by at least 20 changes of tap water) and the plant was allowed a 12 hours' period of adjustment to the tap water, the original response was resumed in all but a few cases (fig. 8).

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IV. Stomatal response to changes in humidity when potassium chloride was added to the water supply Potassium chloride was dissolved in the tap water supply to make a 5 mM solution (inc!. 0.05 mM Ca++). In contrast to the mannitol treatment, maximum aperture was reached in high humidity. However, the responses to changes in humidity were higher in both directions (figs. 10, 11). This effect was greatly enhanced by 48 hours of

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Fig. 10: Rooted plant (Commelina communis): Response of one stoma to changes in air humidity with 5 mM potassium chloride (tap water); feeding time 12 hours (&) and 48 hours (8); x-x no potassium added.

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Fig. 11: Rooted plant (Commelina communis): Response of one stoma to changes in air humidity with 5 mM potassium chloride (tap water) (e); feeding time 48 hours; x-x no potassium added; b after rinsing the leaf. Z. PJlanzenphysiol. Bd. 91. S. 157-172. 1979.

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feeding (fig. 10). Rinsing the roots had no revoking effect. After 24 hours of feeding the stomata, a higher response to changes in humidity was shown even when the solution was replaced by water. Rinsing the leaf with dist. water had no visible effect either. However, when in imitation of a persistent rain, a trickle of tap water was for 12 hours kept running over the leaf surface, the potassium effect was usually overcome (fig. 11).

Discussion The results presented in this paper show that many factors interfere with stomatal response to changes in air humidity (i. e. the effect of air velocity identified here; see fig. 7). While most workers make a point of their using a fan, no consideration is given the possible interference of air velocity with stomatal movement. Given, the employed air velocities have been different ones in each ecophysiological study, the results by necessity must contradict each other. Conflicting evidence was actually presented (see HALL and KAUFMANN, 1975; HALL et aI., 1976; LOSCH, 1977 for reference). When the effect of humidity on a process is to be assessed, great importance is attached to good air circulation in order that uniform humidity be provided. However, considering peristomatal transpiration the mechanism of primary response, it should be kept in mind that this process, like cuticular transpiration of any cell, depends on the boundary layer resistance. The closing reaction occurs in response to a difference in water saturation at the guard cell-atmosphere-interphase. Therefore the reaction must be intense when the surface layer is removed by air turbulences, less so if this happens more slowly by convection. ASHENDEN and MANSFIELD (1977) found the difference in boundary layer resistance to be greatest in the range of 0.16 m X sec- 1 and 0.41 m X sec- 1 (7.97 s X cm- 1 and 0.89 s X cm ool respectively). In this very same range (0.15-0.425 m X sec-I) the difference of stomatal response was also found to be greatest (see fig. 7). There is evidence on record that overall transpiration hardly increased on account of stomatal closure (GRACE, 1974) or even diminished with increasing wind speed (RASCHKE, 1958; WHITEHEAD, 1963; KALMA and KUIPER, 1966; DRAKE et aI., 1970; O'LEARY and KNECHT, 1974). RASCHKE (1960) calculated that the reaction of wind depended on the prevailing stomatal width: While the humidity term in transpiration increased with wind, transpiration remained constant if stomatal resistance was high (RASCHKE, 1960). This is consistent with the results presented here. It is concluded, that stomatal reaction is not a function of relative humidity but a response to evaporative demand. The results of the mannitol treatment (see chapter III) indicate that stomata may tolerate a higher evaporative demand if the supply with water is unlimited (fig. 8 and 9). So, if supply to a plant which has its roots in soil is decreasing during an Z. Pflanzenphysiol. Bd. 91. S. 157-172. 1979.

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experiment, an increasing slope of the curve would be the result (ASTON, 1976, interpreting the results of HALL and KAUFMANN, 1975). Transpiration of an adjacent branch which was left outside the chamber may also limit the supply (RICHTER, 1973). A linear response to changes in air humidity was also reported by ASTON (1976) and LOSCH (1977). The former author used whole plants which were «adequately supplied» with nutrient solution, the latter worked with isolated epidermal strips above a water saturated artificial substomatal cavity. This linear response could not be sensibly explained if the result of peristomatal transpiration were only «turgor loss of the guard cells without reduction of the solute content» (= response in the sense of RASCHKE, 1976). Such responses cannot be lasting ones because a rising transpiration rate is after a time-lag followed by a flow rate of matching capacity (KRAMER, 1937; SKIDMORE and STONE, 1964; EHRLER et aI., 1965; LANG et aI., 1969; SHERIFF, 1974; SHERIFF and SINCLAIR, 1973; JARVIS, 1976). But if the solute contents of the guard cells were reduced in a «follow - up» system (CRAM, 1976), then the quasi steady-state response could easily be explained as follows: Before the subsidiary cells are resaturated after the time lag of absorption, guard cells would have decreased their osmotic pressure and adjust their demand to a lower rate (STALFELT, 1963). Hysteresis would be the consequence. On account of the particularly high transpiration rate of the subsidiary cell, the guard cell «feels» the water state of the leaf as the actual water potential of the subsidiary cell (see MAIER-MAERCKER, 1979). This water potential in turn, determines the water flux into the guard cell. The prerequisite for a flux of water into the guard cell is that 'ljJS - 1jJG > 0 where 'Ips is the water potential of the subsidiary cell and 'ljJG that of the guard cell. If 'ljJG is increased by lower solute content 'ljJs must go up accordingly to provide an additional water flux to the guard cell which is necessary for opening the pore. Since the water potential of the subsidiary cell is decreased by cuticular transpiration, humidity of the air must be higher in order to allow this additional water potential to be built up. Stomata which had closed their pores in response to dry air did not open again when the water status of the leaf had improved, but opened, when humidity of the air was allowed to increase (SCHULZE et aI., 1972). This result can easily be explained with hysteresis. There is no need to postulate two mechanisms of response. Stomatal response to the supply-demand-relationship is complicated by additional factors which interfere with guard cell reaction: 1. What EDWARDS et al. (1976) term «mechanical advantage of the subsidiary cell over the guard cell» may be the reason that the maximum stomatal aperture does not coincide with the highest humidity. Epidermal cells might absorb water from the atmosphere and exert pressure upon the guard cell, the result being a hydropassive closing tendency. Hydropassive movements in this original meaning (STALFELT, 1955) may also be the cause for the observed oscillations when stomatal apertures are small

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(COWAN, 1972). Oscillations are interpreted «as a consequence of a discrepancy between the photoactive and the hydroactive system» (ANDERSON et al., 1954). Supporting evidence for this view is that oscillations occurred only when the light response was saturated while the hydroresponse was limiting. If humidity terms were increased by wind, the oscillations stopped perhaps by overruling the light effects. 2. Stomatal response is further affected by salts which by the transpiration stream are carried to the evaporating surfaces and accumulate there. The transpiration stream to the evaporation sites is primarily a bulk flow along the cell walls (WEATHERLEY, 1970, 1976). Clearly, salt accumulation in the Donnan space would reduce the vapour concentration gradient between leaf and air. Here an explanation is offered for the low rate of peristomatal transpiration from the surface of the guard cells during pore closure (MAERCKER, 1965; MAIER-MAERCKER, 1979). Especially when salt uptake into the guard cell vacuole is limited or salts even leak from it, the apoplast around the guard cell must be flooded with salts trapping water in consequence. Salt accumulation during the dark phase may explain wide openings in response to reillumination. However, not the absolute rate of transpiration accounts for stomatal reaction, but a change in evaporative demand. Fluctuations of transpiration rate will be reflected initially in a change of the hydraulic potential of the solution in the cell wall (COWAN and MILTHORPE, 1968). Steep local gradients will result. The drying wall will absorb water from wherever it is most readily available, the more efficiently, the higher its ion content. Water is not only drawn from the guard cell vacuole but also attracted from the on-coming water supply. Thus, salt in the transpiration stream may have a closing effect on stomata (see chapter IV in this paper). SQUIRE and MANSFIELD (1972) have already pointed out that potassium influx into guard cells of detached epidermal strips was restricted even when the subsidiary cells were intact. Great caution must be exercised when data of stomatal behaviour from detached epidermal strips are applied to the stomatal mechanism of intact plants (WILLMER and MANSFIELD, 1969, 1970). 3. Stomatal responses to changes in air humidity are obscured by a third factor, the after-effect of a period of dryness mediated by abscisic acid (ABA). In this study this after-effect was observed in Vicia faba but not in rooted plants of Commelina communis. ABA may contibute to the hysteresis effect by imposing a ceiling on the extent to which stomata can open (MANSFIELD et aI., in press). However, an indirect control of immediate stomatal responses by ABA would be less sensitive than peristomatal transpiration and would destroy the sensitivity of individual stomatal complexes to their microclimate. DITTRICH and RASCHKE (1977) feel, that guard cells would «blind themselves to the signal of a need for CO 2 if they produced assimilates by themselves». How much rather would the guard cell be blinded to the signal of subtile turgor changes by an influx of ions mediated by ABA somewhere in the mesophyll. Ion fluxes can therefore only be the consequence of the guard cell's turgor changes (MAIER-MAERCKER, 1979).

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Acknow ledgemen ts I am greatly indepted to Prof. Dr. H. ZIEGLER. Thanks are also due to Prof. Dr. W. KOCH. This work has been supported by the Deutsche Forschungsgemeinschaft.

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