Journal of Experimental Botany

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Journal of Experimental Botany, Vol. 53, No. 368, pp. 545-550, March 1, 2002
© 2002 Oxford University Press

Original Papers

The CO₂ response of Vicia guard cells acclimates to growth environment

Silvia Frechilla¹, Lawrence D. Talbott and Eduardo Zeiger²

Department of Organismal Biology, Ecology and Evolution, University of California, Los Angeles, CA 90024, USA

Received 4 June 2001; Accepted 24 October 2001

	Abstract

Top Abstract Introduction Materials and methods Results Discussion References

 
Stomata of growth chamber-grown Vicia faba leaves have an enhanced CO₂ response, measured as change in stomatal aperture, compared to stomata of greenhouse-grown leaves. Reciprocal transfer experiments showed that the stomatal response to CO₂ acclimated to the growing environment. Stomata of growth chamber-grown leaves transferred to a greenhouse lost their high CO₂ sensitivity within 2–3 d while stomata of greenhouse-grown leaves transferred to a growth chamber acquired a high CO₂ sensitivity within 5–7 d. Experiments measuring the CO₂ responses of stomata in detached epidermis showed that growth chamber and greenhouse-grown stomata have the same contrasting CO₂ sensitivity observed in the intact leaf, indicating that the responses reflect intrinsic guard cell properties. The acclimation properties of the CO₂ response of guard cells have implications for the understanding of stomatal function under the predicted increases in atmospheric CO₂.

Key words: Acclimation, carbon dioxide, stomata, Vicia faba.

	Introduction

Top Abstract Introduction Materials and methods Results Discussion References

 
Classical studies have shown that guard cells have an intrinsic response to CO₂ (Linsbauer, 1916; Heath and Russell, 1954; Mouravieff, 1956). It is well established that guard cells sense leaf intercellular CO₂ (Mott, 1988), but the sensory transducing cascade of the CO₂ signal is not well understood (Assmann, 1993, 1999; Zhu et al., 1998; Cousson, 2000). The study of the stomatal response to CO₂ has been complicated by the large variability of observed CO₂ responses, which range from complete CO₂ insensitivity in some species to high sensitivity in others (Morison, 1987, 2001). Furthermore, wide sensitivity ranges have been reported for the same species. For example, independent studies of maize and Xanthium have reported both high and low stomatal sensitivity to CO₂ within each species (Raschke et al., 1978; Mott, 1988; Farquhar et al., 1978; Sharkey and Raschke, 1981).

This variability in CO₂ response, particularly that reported within species, suggests that environmental factors are able to modify stomatal sensitivity to CO₂. An ABA-mediated enhancement of stomatal sensitivity to CO₂ in water-stressed plants is well established (Raschke, 1975). However, although different degrees of water availability might account for some of the observed variability under different experimental conditions, there remain numerous other environmental factors that may also stimulate acclimation responses.

The only well documented environmental condition causing acclimation in the stomatal CO₂ response under well-watered conditions is long-term growth under elevated CO₂ concentrations (antrcek and Sage, 1996). In these gas exchange studies, leaves grown at high [CO₂] have a lower response of stomatal conductance to CO₂, but respond over a wider range of [CO₂] than do plants grown under ambient CO₂ conditions. Plants have also been shown to acclimate to long-term changes in ambient [CO₂] by changing stomatal density (Wagner et al., 1996; Gray et al., 2000), and mesophyll photosynthetic properties (Sage, 1994).

A recent study found that growth conditions can alter the stomatal sensitivity to CO₂, even in well-watered plants grown under ambient CO₂ concentrations (Talbott et al., 1996). The study measured changes in stomatal aperture in response to short-term changes in CO₂ and found that stomata of growth chamber-grown, intact Vicia leaves had an enhanced sensitivity to CO₂ compared to stomata of greenhouse-grown leaves.

In the present study, reciprocal-transfer experiments were used to investigate whether the contrasting CO₂ sensitivity of stomata from greenhouse and growth chamber-grown plants is ontogenetically fixed or represents a plastic acclimation to different growth conditions. Studies of the CO₂ response in isolated stomata investigated whether the contrasting CO₂ sensitivity requires the presence of mesophyll tissue, or represents an intrinsic property of the guard cell. Measurements of the CO₂ response of growth chamber and greenhouse-grown stomata from intact leaves in an open-topped chamber built in a greenhouse, investigated whether the contrasting CO₂ sensitivities previously measured in a growth chamber could also be observed under the natural light, low humidity conditions prevailing in the greenhouse.

	Materials and methods

Top Abstract Introduction Materials and methods Results Discussion References

 
Plant material and growth conditions
Seeds of Vicia faba L. cv. Windsor Long Pod (Bountiful Gardens Seeds, Willits, CA, USA) were planted in pots with commercial potting mix (Sunshine mix No. 1, American Horticultural Supply, Camarillo, CA, USA). Plants were grown in a growth chamber (Conviron PGV-36, Asheville, NC, USA) at 85±3% RH, 12 h light 550 µmol m^-2 s^-1 (incandescent 40 W Philips; fluorescent: GTE Sylvania F96T12/CW/VHO) and 25/15 °C day/night air temperature, or in a greenhouse under natural light, 50–75% RH, 25–30/15–20 °C day/night air temperature. Plants were watered three times a day with an automatic watering system and fertilized once a week (20-10-20 mix, Grow-More Research and Manufacturing Co, Gardena, CA, USA).

Controlled CO₂ experiments with intact plants in a greenhouse
An open-topped enclosure was constructed over a 4'x8' greenhouse bench. Carbon dioxide levels in the plastic enclosure were manipulated by passing an air stream through a swamp cooler and into a plenum chamber underneath the enclosure that distributed it evenly over the floor of the enclosure. The air was then forced upward and out of the top of the enclosure. The CO₂ content of the air entering the enclosure was controlled by injecting 100% CO₂ gas from a cylinder into the air stream at the swamp cooler fan using a mass flow controller. Injection at this location ensured adequate CO₂ mixing before the air stream reached the plants. Carbon dioxide concentration in the enclosure was continuously monitored with an infrared gas analyser (EGM-1, PP systems, Hitchin, Herts, UK). Temperature in the chamber was 1 °C higher than the ambient temperature of the greenhouse. Relative humidity was within 2% of ambient, and light levels inside the chamber were 85% of ambient greenhouse levels. Plants were transferred to the enclosure in the morning and allowed to equilibrate for 2 h before an initial measurement of stomatal apertures was taken. Incident light was measured with a quantum sensor (Li-Cor Inc., Lincoln, NE, USA) and relative humidity was measured with a humidity sensor (model 2200, Lab-Line Instruments Inc., Melrose Park, IL, USA). Plants were kept for 1 h at each CO₂ concentration (400, 650 and 900 cm³ m^-3) before measurement of stomatal apertures (see below).

Carbon dioxide experiments with isolated stomata
The CO₂ response of stomata from detached epidermis was examined in darkness, and under red plus blue light. Two young, fully expanded leaves from the second and third internodes were harvested early in the morning. Epidermal peels from the abaxial side were carefully stripped by hand from the interveinal regions into 0.1 mM CaCl₂. The peels were then rinsed with distilled water and equilibrated for 1 h in a solution containing 1 mM MES–NaOH buffer (pH 6.0), 0.1 mM CaCl₂, and 1 mM KCl. The solution was aerated with 400 cm³ m^-3 CO₂ air. After equilibration, an initial aperture measurement was taken and the epidermal peels were divided into three portions for incubation under air containing 0, 400, or 900 cm³ m^-3 CO₂ for an additional 90 min. For the dark treatment, the 1 h preincubation and the 90 min incubation were carried out in darkness. For the experiments in the light, peels were simultaneously illuminated with 120 µmol m^-2 s^-1 red light (No. 2423 plexiglass, 50% cutoff 595 nm, Rohm and Haas, Hayward, CA, USA) and 10 µmol m^-2 s^-1 blue light (No. 2424 plexiglass, 470 nm maximum, half-band width 100 nm, Rohm and Haas) throughout the pre-incubation and CO₂ treatments. Light fluence rate was measured with a Li-Cor quantum sensor (Li-Cor Inc., Lincoln, NE, USA). The lights sources were Sylvania DAH 500 W incandescent projector bulbs for blue light and Sylvania 300 W 300PAR56/2MFL Cool Lux flood lamps for red light (GTE Products Corp., Winchester, KY, USA). In both treatments, temperature was maintained at 23 °C by placing the treatment dishes in a circulating water bath.

Measurement of stomatal apertures
Stomatal apertures were determined from digitized video images of stomata in epidermal peels using an Olympus BH-2 microscope connected to a Javelin JE2362A digital imaging camera. Image processing was handled with an IBM PC-based MV-1 image analysis board (Metrabyte Corp., Taunton, MA, USA) and JAVA image analysis software (Jandel Scientific, Corte Madera, CA, USA) as described previously (Talbott et al., 1996). For each point within an experiment, mean aperture was determined from measurements of 30 stomata taken from three separate epidermal peels. Experiments were repeated four times and results are presented as averages of the mean aperture values from individual experiments.

Transfer experiments
Three-week-old Vicia faba plants, grown in the growth chamber or greenhouse conditions described above, were transferred to the alternative environment. The CO₂ response of stomata from intact leaves and from detached epidermis was measured in the morning of the day of the transfer and then daily during the subsequent 8–9 d, using recently mature, fully expanded leaves from the third and fourth internodes of the plant.

For quantification of stomatal CO₂ sensitivity in the growth chamber to greenhouse transfer experiments, a subset of growth chamber-grown plants transferred to the greenhouse were brought back to the growth chamber in the morning of each consecutive day and interspersed with non-transferred, growth chamber plants. After an equilibration time of 2 h, baseline stomatal apertures were measured as described earlier (Talbott et al., 1996) and the CO₂ concentration in the chamber was increased to 900 cm³ m^-3. Stomatal apertures of leaves were then measured after a 1 h exposure to the elevated concentration. The stomatal sensitivity to CO₂ was evaluated from the decrease in stomatal apertures in response to the elevated CO₂.

For the greenhouse-to-growth chamber transfer experiments, greenhouse-grown plants were interspersed with growth chamber-grown plants on the day of transfer. Measurements of the short-term stomatal response to elevated CO₂ were obtained in the morning of the day of the transfer and daily thereafter for 8–9 d, as described above.

Responses of stomata in epidermal peels were determined daily during the transfer experiments using the dark, and red plus blue light illumination protocols described in the section on experiments with isolated stomata.

	Results

Top Abstract Introduction Materials and methods Results Discussion References

 
The CO₂ response of stomata from intact, greenhouse and growth chamber-grown leaves measured in greenhouse conditions
The previous measurements of contrasting CO₂ sensitivity in stomata from growth chamber and greenhouse-grown leaves were obtained in a growth chamber under constant light, temperature and relative humidity (Talbott et al., 1996). That environment is significantly different from greenhouse conditions, particularly regarding light and relative humidity (see Materials and methods), and could affect the observed stomatal responses to CO₂. To address that question, the CO₂ response of stomata from greenhouse and growth chamber-grown Vicia plants was measured under greenhouse conditions in a open-topped enclosure which allowed adjustment of ambient CO₂ levels without major changes in other environmental parameters. To avoid baseline changes in stomatal apertures caused by natural fluctuations in incident light, the experiments were carried out at midday, under high and relatively constant levels of incident radiation (Fig. 1a, inset).

View larger version (24K): [in this window] [in a new window]   Fig. 1. The CO2 response of stomata from Vicia faba grown under greenhouse () and growth chamber (•) conditions. Aperture change in response to a 1 h exposure to 650 or 900 cm3 m-3 ambient CO2 is shown as a percentage of the initial aperture value (see Table 1). Data are the average of three experiments±SE. Error bars are contained within the symbol where not shown. Inset shows greenhouse light levels over the course of the experiment.

 
For the measurement of stomatal aperture in intact leaves, epidermal strips were quickly removed from attached leaves and stomatal apertures were determined within 2 min of dissection (Talbott et al., 1996). Average apertures of stomata from greenhouse-grown plants were 11.9±0.4 µm under the ambient [CO₂] prevailing at the onset of the experiments. A 1 h exposure to 650 and 900 cm³ m^-3 resulted in stomatal apertures of 11.9±0.4 and 11.5±0.5 µm, respectively. Thus, as observed in the growth chamber measurements (Talbott et al., 1996), stomata from greenhouse-grown leaves were insensitive to changes in [CO₂] in the 400–900 cm³ m^-3 range. By contrast, average stomatal apertures of growth chamber-grown leaves were 12.7±0.5 µm under ambient [CO₂], and 9.8±0.5 and 7.5±0.4 µm after a 1 h exposure to 650 and 900 cm³ m^-3 CO₂, respectively. Thus, apertures decreased to about 60% of their initial value when [CO₂] was increased to 900 cm³ m^-3 (Fig. 1). It was therefore concluded that the environment in which the measurements were carried out had no effect on the contrasting CO₂ sensitivity of stomata from growth chamber and greenhouse-grown leaves.

View this table: [in this window] [in a new window]   Table 1. Initial aperture values in µm for the CO2 response experiments with stomata from intact leaves, and isolated stomata after a 1 h equilibration Values are the average of four experiments±SE.

 
The CO₂ response of isolated stomata from greenhouse and growth chamber-grown leaves
Stomatal responses in the intact leaf can be markedly influenced by interactions with the mesophyll tissue (Raschke et al., 1978; Mansfield et al., 1990; Mott, 1990). CO₂ treatments applied to isolated stomata in epidermal strips were used to test whether the contrasting CO₂ sensitivity of stomata from greenhouse and growth chamber-grown leaves requires the presence of mesophyll, or whether it is an intrinsic property of guard cells. In addition, the experiments with isolated stomata made it possible to extend the tested [CO₂] to the 0–900 cm³ m^-3 range. Because of reported differences in the CO₂ response of stomata in the light and in darkness (Zhu et al., 1998), both conditions were investigated.

For the experiments in darkness, isolated stomata in epidermal strips were incubated for 1 h in the dark under air containing 400 cm³ m^-3 CO₂. This preincubation was followed by a 90 min treatment under CO₂-free air, or under air containing 400 cm³ m^-3 or 900 cm³ m^-3 CO₂. Average apertures at the end of the preincubation were 5.6±0.1 and 9.5±0.2 µm for greenhouse and growth chamber stomata, respectively. No aperture change was observed in stomata isolated from either greenhouse or growth chamber-grown plants after the 90 min treatment in 400 cm³ m^-3 CO₂ (Fig. 2a). Incubation of stomata from growth chamber-grown plants with CO₂-free air resulted in an aperture increase to 11.4±0.2 µm (120% of initial aperture), whereas incubation with 900 cm³ m^-3 CO₂ yielded average apertures of 8.0±0.1 µm (84% of initial aperture, Fig. 2a). By contrast, stomata isolated from greenhouse-grown stomata were insensitive to either CO₂ treatment.

View larger version (19K): [in this window] [in a new window]   Fig. 2. The CO2 response of isolated stomata from Vicia faba. Epidermal strips were isolated from greenhouse- () or growth chamber-grown (•) leaves and incubated in darkness (a) or 120 µmol m-2 s-1 red light/10 µmol m-2 s-1 blue light (b) at 400 cm3 m-3 CO2. After equilibration, guard cells were treated for 1 h with air containing 0, 400 or 900 cm3 m-3 CO2. Changes in stomatal aperture are reported as a percent of the initial aperture value (see Table 1). Points are the average of four experiments±SE. Error bars are contained within the symbol where not shown.

 
For the experiments with illuminated stomata, both the preincubation and the CO₂ treatments were carried out under 120 µmol m^-2 s^-1 red and 10 µmol m^-2 s^-1 blue light, conditions that activate the two major guard cell photoreceptor systems (Schwartz and Zeiger, 1984). Illumination did not change the basic pattern of contrasting sensitivity to CO₂ observed with intact leaves and with epidermal peels in the dark (Fig. 2b). Stomata isolated from greenhouse-grown plants showed negligible differences in aperture across all CO₂ treatments, while stomata from growth chamber plants had a change in average aperture of -1.3 µm and +1.5 µm under the high and low CO₂ treatments, respectively. Light treatment did result in altered initial aperture values (Table 1) and a minor (5%) variation in the magnitude of response.

Initial aperture values (Table 1) and the magnitude of aperture changes differed between growth environments (growth chamber and greenhouse) and experimental conditions (intact leaf and isolated stomata in epidermal peels), however, the differential CO₂ sensitivities (Figs 1, 2) and the acclimation responses (described below) were similar under all conditions.

Acclimation of the stomatal response to CO₂ characterized in transfer experiments
The acclimation properties of the stomatal response to CO₂ was studied in transfer experiments in which growth chamber-grown plants were transferred to a greenhouse, and vice versa. Control plants were kept in their original growth environment. The stomatal response to high CO₂ was tested daily in intact leaves, and in isolated stomata kept in darkness or in the light.

Acclimation responses were observed in all conditions (Figs 3, 4). In intact leaves, stomata from transferred greenhouse plants, which initially showed an aperture increase of 1.2 µm in response to short-term elevation of CO₂, responded with a 6.9 µm decrease of aperture by the end of the 8 d period. By contrast, stomata of transferred growth chamber plants, which initially responded to increased CO₂ with a 4.2 µm decrease in aperture, displayed a 0.4 µm increase in aperture by the end of the transfer period. Similar transitions in CO₂ sensitivity were seen when the responses of isolated stomata were tested (Fig. 4). The absolute change in aperture of CO₂-responsive stomata was -2.1 µm and -1.7 µm in dark and light-treated preparations, respectively. These values are similar to the aperture changes found in the experiments shown in Fig. 2.

View larger version (22K): [in this window] [in a new window]   Fig. 3. Acclimation of the stomatal response to CO2 in intact leaves. Plants were transferred from a greenhouse to a growth chamber () or from a growth chamber to a greenhouse (•) on day 0. Aperture changes in response to 900 cm3 m-3 CO2 were measured on subsequent days and is shown as a percentage of initial aperture. Points are the average of four experiments±SE. Upper and lower dotted lines at day 8 indicate the aperture change of control plants maintained under greenhouse and growth chamber conditions, respectively.

 

View larger version (22K): [in this window] [in a new window]   Fig. 4. Acclimation of the CO2 response of isolated stomata. Stomata were isolated from plants transferred from a greenhouse to a growth chamber () or from a growth chamber to a greenhouse (•) on day 0. Aperture changes in response to 900 cm3 m-3 CO2, either in darkness (a) or in 120 µmol m-2 s-1 red light/10 µmol m-2 s-1 blue light (b), were measured on subsequent days and are shown as a percentage of initial aperture. Points are the average of four experiments±SE. Upper and lower dotted lines at day 9 indicate the aperture change of control plants maintained under greenhouse and growth chamber conditions, respectively.

 
The time-course of acclimation was similar in both the intact leaf and isolated stomata experiments. Growth chamber-grown stomata lost their high CO₂ sensitivity 2–3 d after the transfer. Greenhouse-grown stomata displayed the enhanced CO₂ sensitivity typical of growth chamber-grown plants 5 d after the transfer in the intact leaf experiments and 6–7 d after transfer in the measurements with isolated stomata. In all cases the acclimation was gradual, with changes in the sensitivity of the CO₂ response observed as early as 1 d after the transfer.

The initial aperture of transferred plants changed to a value characteristic of the new growth environment, and the time-course of this shift matched the acclimation time-course of the CO₂ response (data not shown). This suggests a functional relationship between the mechanism(s) controlling the range of stomatal opening and the stomatal response to CO₂.

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
The results from the epidermal peel experiments clearly showed that isolated stomata from epidermal strips retain the differential CO₂ sensitivity seen in the intact leaf. Thus, isolated stomata from growth chamber-grown leaves exhibited an enhanced CO₂ sensitivity whereas stomata from greenhouse-grown leaves were largely insensitive to changes in ambient [CO₂]. It was therefore concluded that the contrasting CO₂ sensitivity of stomata grown in the two different environments reflects intrinsic guard cell properties.

Stomata have independent responses to light and CO₂ (Mouravieff, 1956; Zeiger and Hepler, 1977), and a recent study has implicated zeaxanthin-dependent and independent mechanisms mediating CO₂ sensing in guard cells (Zhu et al., 1998). Therefore whether the contrasting CO₂ sensitivity under investigation was affected by light conditions was investigated. Results showed that isolated stomata from greenhouse-grown plants remained insensitive to CO₂ both in the light and in darkness, whereas stomata from growth chamber-grown plants showed an enhanced CO₂ sensitivity under both conditions. Initial apertures and absolute aperture changes, however, were larger in the light. These aperture differences support the concept of a different sensory transducing cascade regulating the stomatal response to CO₂ in illuminated guard cells (Zhu et al., 1998).

This is the first report of an acclimation of the stomatal response to CO₂ shown to be reversible upon changes in growth conditions. Both greenhouse and growth chamber-grown stomata acclimated to the reciprocal environment, although the time-course of the acclimation involving a loss of CO₂ sensitivity, observed in the growth chamber-to-greenhouse transfer, was substantially shorter than the time required for the reciprocal acclimation. If the sensitivity changes involve structural changes in a sensory transduction cascade, the contrasting time-courses might reflect longer times required for the assembly of new components required for an increase in CO₂ sensitivity. Alternatively, the longer time-courses required for an enhanced CO₂ sensitivity, which is associated with higher stomatal apertures, might be part of an adaptive strategy aimed at preventing large fluctuations in stomatal apertures, and potential water loss, in response to short-term, transient changes in environmental conditions.

The acclimation time-courses measured in the experiments with isolated stomata support the conclusion that the acclimation process is intrinsic to the guard cell. The time-course was similar to that observed in the experiments with intact leaves, although acquisition of full CO₂ sensitivity took 1–2 d longer than observed in the intact leaf. The longer apparent acclimation time and generally lower aperture changes seen with isolated stomata could be due to factors such as the stress of isolation and treatment. Stomatal, light, CO₂, and osmoregulatory responses have been found to be consistent between the isolated and intact preparations (Talbott and Zeiger, 1993, 1996; Zhu et al., 1998).

An important direction for further research is the identification of the environmental factor(s) mediating the acclimation response. As discussed in a previous study (Talbott et al., 1996), light intensity and quality, daily fluctuations in ambient CO₂ concentration, and relative humidity are key environmental variables warranting further studies.

Stomata are receiving increasing attention in climate change models (Sellers et al., 1996), and understanding of the acclimation properties of the stomatal response to CO₂ should be valuable for future modelling work. A detailed characterization of the relationship between growth conditions and stomatal sensitivity to CO₂ should also be valuable for future studies of CO₂ sensing in stomata.

	Acknowledgments

 
This work was supported by DOE grant No. 90ER20011 and NSF grant No. DCB 8904254.

	Notes

 
¹ Present address: Departamento Ciencias del Medio Natural, Universidad Publica de Navarra, 31006 Pamplona, Spain.

² To whom correspondence should be addressed. Fax: +1 310 825 9433. E-mail: zeiger{at}biology.ucla.edu

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