Plant Cell Physiol. 45(11): 1709–1714 (2004)
JSPP © 2004
The Blue Light-Specific Response of Vicia faba Stomata Acclimates to Growth
Environment
Silvia Frechilla 1, Lawrence D. Talbott and Eduardo Zeiger 2
Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA 90024, U.S.A.
;
Stomata in epidermal strips from growth chambergrown Vicia faba leaves opened less in response to white
light than did stomata from greenhouse-grown leaves. Chlorophyll-mediated, red light-stimulated opening was similar
in stomata from the two growth conditions, but stomata
from the growth chamber environment had a severely
reduced response to blue light. Transfer of plants between
the two growth conditions resulted in an acclimation of the
stomatal blue light response. Stomata lost blue light sensitivity within 1 d of transfer to growth chamber conditions
and gained sensitivity to blue light over an 8 d period after
transfer to a greenhouse. Short-term transfer experiments
confirmed that the rapid loss of blue light sensitivity was an
acclimation response, requiring between 12 and 20 h exposure to growth chamber conditions. The acclimation of the
stomatal response to blue light was inversely related to a
previously reported acclimation response in which stomata
change between high CO2 sensitivity under growth chamber conditions and low CO2 sensitivity under greenhouse
conditions. The time courses of the blue light and CO2 acclimation responses were virtually identical, suggesting the
possibility of a common acclimation mechanism.
Keywords: Blue light — Carbon dioxide — Guard cells —
Stomatal acclimation — Vicia faba.
Abbreviations: PPFD, photosynthetic photon flux density; VPD,
vapor pressure difference.
Introduction
Extensive studies have shown that stomatal guard cells
have independent sensory transduction pathways for many
environmental signals such as light fluence, CO2 concentration, relative humidity/vapor pressure difference (VPD) and
temperature (Assmann 1999, Assmann and Shimazaki 1999,
Hetherington and Woodward 2003). Stomata use these signals
to adjust apertures so as to optimize gas exchange according to
prevailing conditions.
Acclimation is a change in the physiological responses of
an organism due to prior exposure to environmental conditions, as opposed to adaptation, which is the acquisition of a
1
2
response over multiple generations by a process of selection
(Taiz and Zeiger 2002). Recent studies indicate that stomata
can acclimate to at least some environmental conditions. Continuous growth at elevated CO2 results in stomata with altered
CO2 sensitivity (Šantrucek and Sage 1996) and diurnal time
courses of stomatal opening in a beech canopy seem to acclimate to light and VPD conditions (Kutsch et al. 2001). An
acclimation of the stomatal response to CO2 was also documented in recent studies (Talbott et al. 1996, Frechilla et al.
2002, Talbott et al. 2003). Stomata from growth chambergrown plants were shown to have a higher sensitivity to CO2 as
compared with stomata from greenhouse-grown plants. Transfer experiments showed that the difference in CO2 sensitivity
was an acclimation response, with stomata from greenhousegrown plants requiring 8 d to fully acquire the enhanced CO2
sensitivity characteristic of stomata from growth chambergrown plants. Loss of stomatal CO2 sensitivity in growth chamber-grown plants transferred to greenhouse conditions was
observed in 2 d (Frechilla et al. 2002). Relative humidity was
identified as a key environmental factor mediating this acclimation response (Talbott et al. 2003). Experiments with isolated
guard cells showed that the acclimation resulted from changes
in guard cell properties (Frechilla et al. 2002).
The signal transduction chain for CO2 is not well understood (Assmann 1999, Cousson 2000), although recent studies
have implicated photosynthetic carbon fixation in the guard cell
chloroplast as a site of sensing (Zhu et al. 1998, Zeiger et al.
2002). On the other hand, understanding of the sensory transduction chain for the blue light response is growing rapidly.
Blue light-stimulated opening results from increases in turgor
mediated by uptake of potassium and chloride ions. Ion uptake,
in turn, is driven by an increased electrochemical gradient
produced by activation of plasma membrane-localized protonpumping ATPases (Tallman 1992). Activation of the ATPase
requires phosphorylation of its C terminus by a serine-threonine
kinase, facilitated by binding of a 14-3-3 protein (Kinoshita
and Shimazaki 1999). Several lines of evidence have implicated the carotenoid pigment zeaxanthin as a blue light photoreceptor in guard cells (Zeiger et al. 2002, Talbott et al.
2003). Phototropin has also been postulated as a blue light photoreceptor in guard cells (Kinoshita et al. 2001), however, a
recent study in our laboratory has shown that guard cells of
Present address: Depto. Ciencias del Medio Natural, Universidad Publica de Navarra, 31006 Pamplona, Spain.
Corresponding author: E-mail, [email protected]; Fax, +1-310-825-9433.
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Acclimation of the stomatal blue light response
Results
Fig. 1 Light responses of isolated stomata from greenhouse- and
growth chamber-grown V. faba. Epidermal strips were given a pretreatment incubation in 1 mM KCl, 0.1 mM CaCl2 in the dark for 1 h,
then exposed for an additional hour to: darkness (Dark); 120 µmol m–2
s–1 red light (Red); a combination of 120 µmol m–2 s–1 red light and
10 µmol m–2 s–1 blue light (Red+Blue); 60 µmol m–2 s–1 white light
(White). Average aperture values at the end of the pre-treatment were
5.5 µm and 6.9 µm for greenhouse and growth chamber stomata,
respectively. Final aperture after light treatment is given in µm (A) and
expressed as a percentage of the final pre-treatment aperture (B) and
are the average of four experiments (n = 30 per experiment) ± standard error of the measurement.
phot1/phot2, a double mutant lacking phototropin, have a specific blue light response (Talbott et al. 2003).
The present study reports that isolated stomata from
greenhouse- and growth chamber-grown leaves differ in their
sensitivity to blue light as a result of an acclimation response to
the growth environment. Blue light sensitivity was inversely
related to the strength of the stomatal CO2 response and the
time courses for gain and loss of sensitivity are remarkably
similar, suggesting a link between the cellular response mechanism for CO2 and blue light. Study of these acclimation events
offers the opportunity to better understand stomatal adaptation
to specific environmental conditions and to gain insight into the
basic cellular mechanisms that guard cells use to sense and
integrate multiple environmental signals.
Blue light sensitivity of greenhouse and growth chamber stomata
In the present experiments, the light response of stomata
was tested in detached epidermal strips in order to eliminate
any mesophyll-related influences. The stomatal response to
light has two major components, one mediated by photosynthesis in the guard cell chloroplasts, and a specific blue light
response (Zeiger et al. 2002). The photosynthetic response can
be probed by red light, which does not activate the blue light
photoreceptor. Because chlorophyll absorbs both red and blue
light, the blue light-specific response is usually probed with a
dual-beam protocol using strong red light to saturate photosynthetically mediated opening and a second beam of blue light.
Any additional opening produced by the blue light can be
attributed to the blue light-specific response.
Steady-state aperture values of dark-adapted stomata averaged 5.5 µm in stomata isolated from greenhouse-grown plants
and 6.9 µm in stomata isolated from growth chamber plants.
The higher aperture values in growth chamber stomata probably result from the higher prevailing relative humidity conditions in the growth chamber environment (Talbott et al. 2003).
Stomata from greenhouse- and growth chamber-grown leaves
had similar photosynthesis-dependent opening when probed
under saturating (120 µmol m–2 s–1) red light (Fig. 1). Red light
treatment caused a net opening over dark aperture values of
0.7±0.1 µm and 0.6±0.2 µm in stomata from greenhouse and
growth chamber-grown plants, respectively (Fig. 1a). These
aperture increases represent a change of 113±2% and 110±2%
from initial dark aperture values at the start of the red light
treatment (Fig. 1b). In the dual-beam experiment, addition of
10 µmol m–2 s–1 blue light to the saturating red background produced an additional 1.0 µm increase in aperture in stomata
from greenhouse plants (Fig. 1a). This increased opening above
the level attained by red light-dependent stomatal opening is
typical of stomatal response to blue light (Schwartz and Zeiger
1984). In contrast, addition of blue light elicited an additional
increase of only 0.2 µm in stomata from growth chambergrown leaves (Fig. 1a). Since maximal apertures under growth
chamber conditions are typically 14–18 µm (Talbott et al.
1996), this small increase in aperture indicates that these
growth chamber-grown stomata had very poor blue light sensitivity. Under white light, stomata from both growth chamberand greenhouse-grown plants showed a level of response equivalent to that obtained with red plus blue light, confirming the
lack of a detectable blue-light response in the growth chambergrown stomata (Fig. 1a). Because of the higher initial apertures in stomata from growth chamber-grown plants, final
aperture values for red plus blue light treatments are similar
in stomata from the two environments. However, blue light
responses in the two environments can be easily compared
when results are expressed as the percentage change in aperture from the dark value (Fig. 1b). The red plus blue and white
Acclimation of the stomatal blue light response
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Fig. 2 Acclimation of the stomatal response to blue light probed in
transfer experiments. Plants were transferred from greenhouse to
growth chamber (open square) or from growth chamber to greenhouse
(closed square) environments on day 0. Stomatal aperture change in
response to 10 µmol m–2 s–1 blue light given in a background of
120 µmol m–2 s–1 red light was measured as described for Fig. 1. The
opening response is expressed as percentage change in aperture from
the final pre-treatment aperture on that day or as the absolute change in
µm (inset) and is the average of three experiments ± SE. Upper and
lower dotted lines represent the light response of control greenhouse
and growth chamber plants, respectively.
Fig. 3 Acclimation of the stomatal response to blue light probed in
short-term transfer experiments. Light response of stomata after shortterm exposure to growth chamber conditions. At hour 0, greenhousegrown plants were transferred to the growth chamber for 6, 12, 20 or
24 h then returned to the greenhouse. At 24 h intervals after the start of
transfer, the light response of stomata isolated from these plants was
tested as in Fig. 2. Data points are expressed as the percentage change
in aperture from the final pre-treatment aperture on that day and are
the average of three experiments ± SE. Upper and lower dotted lines
represent the average light response of control greenhouse and growth
chamber plants, respectively.
light treatments of stomata from greenhouse-grown plants can
be seen to produce substantial aperture increases over red light
alone, while response to these treatments in stomata from
growth chamber plants was indistinguishable from the increase
caused by red light alone.
the final aperture after addition of blue light is plotted as a percentage of the aperture under saturating red light, blue light
sensitivity in stomata of growth chamber-grown plants transferred to greenhouse conditions can be seen to undergo a sustained increase over the 8 d period (Fig. 2). In contrast, stomata
from greenhouse-grown plants transferred to the growth chamber display the lower sensitivity typical of growth chamber
conditions throughout the period from 1 to 8 d after transfer
(Fig. 2).
The rapid decline in stomatal blue light sensitivity upon
transfer of plants to the growth chamber environment raises the
question of whether the loss of sensitivity represents rapid
acclimation or reflects short-term inhibition of the blue light
response by some factor present in the growth chamber environment. To test these alternatives, short-term transfer experiments were carried out, in which greenhouse-grown plants
were transferred to the growth chamber for 6, 12, 20 or 24 h,
and then returned to the greenhouse. The blue light sensitivity
of these stomata was measured 24, 48 and 72 h after the start of
the transfer. Stomata kept in a growth chamber for 6 or 12 h
retained a blue light response typical of greenhouse-grown
plants when returned to a greenhouse (Fig. 3). In contrast, stomata from plants kept in the growth chamber for 20 or 24 h,
showed a loss of blue light sensitivity. This loss of sensitivity
persisted for at least 48 h after the plants were returned to
greenhouse conditions (Fig. 3), demonstrating that the loss of
Transfer experiments
Plants were transferred from the growth chamber to the
greenhouse and vice versa in order to test whether the observed
differences in stomatal blue light response reflected an acclimation similar to the acclimation previously observed with the
stomatal response to CO2 (Frechilla et al. 2002). Stomatal
sensitivity to blue light in the two populations was tested daily
in isolated epidermal strips treated with blue light given in a
background of saturating red light. In stomata from growth
chamber-grown leaves transferred to a greenhouse, blue lightstimulated opening increased from a value of 1.2 µm typical of
stomata from growth chamber-grown plants to 2.4 µm in about
8 d (Fig. 2 inset). In contrast, blue light-stimulated stomatal
opening of greenhouse-grown plants transferred to a growth
chamber declined from 2.1 µm to 1.1 µm within 1 d after transfer (Fig. 2 inset). Aperture values under saturating red light
were lower for stomata from greenhouse-grown plants than for
stomata from growth chamber-grown plants, as shown in Fig.
1. During the transfer experiments, this aperture attained under
red light changed smoothly to values typical of the new growth
conditions in both transfer directions (data not shown). When
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Acclimation of the stomatal blue light response
Fig. 4 Comparison of the time course for the acclimation of the stomatal responses to blue light and CO2. Time course of the gain (a) and
loss (b) of sensitivity to blue light (closed circle) and CO2 (open circle) responses are shown. Values represent percentage change from
initial apertures. Note that since stomata close in response to CO2, the
final apertures of responding stomata will have values lower than
100%. Data from Fig. 2 (blue light response) and Frechilla et al. 2002
(CO2 response).
blue light sensitivity was rapid acclimation of the stomatal
response to blue light to growth chamber conditions.
A comparison of the time courses for the acclimation of
the stomatal responses to blue light and CO2 reveals a remarkable similarity. Development of full blue light and CO2 sensitivity (seen as increased closure in response to elevated CO2) in
stomata occurs over an 8 d time course in a response characterized by a gradual increase in sensitivity over the course of the
acclimation period (Fig. 4a). In contrast, loss of sensitivity in
both responses occurs much more rapidly than gain of sensitivity, being completed 20–48 h after exposure to the new conditions (Fig. 4b).
Discussion
In contrast to the stomatal response to CO2, for which a
wide range of sensitivities has been reported (Morison 1987,
Morison 2001), variability in stomatal sensitivity to light has
been given much less consideration. There are, however, some
indications in the literature that such variability exists. In some
studies, stomata of growth chamber-grown Zea mays were
found to have low sensitivity to light (Raschke et al. 1978). On
the other hand, Z. mays stomata were shown to have high sensi-
tivity to light in a gas exchange analysis using greenhousegrown plants (Farquhar et al. 1978). Stomatal responses in a
beech forest canopy were found to acclimate in response to the
preceding photosynthetic photon flux density (PPFD) and VPD
conditions (Kutsch et al. 2001).
In earlier studies, we demonstrated that stomata of plants
grown under growth chamber conditions have high sensitivity
to CO2 whereas stomata of plants grown under greenhouse conditions have low CO2 sensitivity (Talbott et al. 1996). When
Vicia faba plants are transferred from greenhouse to growth
chamber conditions or vice versa, stomata show an acclimation
of the stomatal CO2 response in which guard cells acquire CO2
sensitivity typical of the new environment (Frechilla et al.
2002).
Taken together, the reported acclimation of the CO2
response and the data reported here show a reciprocal relationship between the blue light and CO2 responses, such that stomata are primarily sensitive to either blue light or CO2 but not
to both factors simultaneously. The time courses of the CO2
and blue light acclimations are strikingly similar (Fig. 4). In
both cases, the gain in sensitivity is a slow, gradual process that
is completed in 8 d while loss of sensitivity occurs much more
quickly. Short-term transfer experiments (Fig. 3) indicate that
the rapid loss of blue light sensitivity is an acclimation requiring a minimum of 12 h exposure to growth chamber conditions
and is not readily reversible by transferring the plants back to
greenhouse conditions. The slow gain and rapid loss of sensitivity appears consistent with a mechanism in which the acclimation to high sensitivity requires an elaborate synthesis of
sensory transduction chain components, while the loss of sensitivity can be achieved by relatively rapid degradation events.
Detailed investigations involving manipulation of light
intensity, light quality, temperature and relative humidity, both
between and within greenhouse and growth chamber environments, have shown that relative humidity is the major environmental factor eliciting the acclimation of the CO2 response
(Talbott et al. 2003). The reciprocal nature and close correlation between the time courses of the CO2 and the blue light
acclimation responses presented in this paper strongly suggest
that changes in relative humidity also mediate the acclimation
of the stomatal response to blue light. Confirmation of the role
of humidity in the blue light response awaits detailed humidity
experiments.
The reciprocal relationship between stomatal sensitivity to
blue light and CO2, and the similarity of the acclimation time
courses of the two responses could be explained by a functional link between the sensory transduction mechanisms of the
two responses. Previous studies have established a tight, positive relationship between light intensity, aperture and guard cell
content of the blue light-absorbing pigment, zeaxanthin, a postulated blue light photoreceptor of guard cells (Srivastava and
Zeiger 1995, Frechilla et al. 2000, Talbott et al. 2003). In addition, stomatal aperture and guard cell zeaxanthin content have
been shown to decrease as a function of increasing ambient
Acclimation of the stomatal blue light response
CO2 concentration (Zhu et al. 1998). Like their mesophyll
counterparts, guard cells have a functional xanthophyll cycle
(Srivastava and Zeiger 1995, Zeiger and Zhu 1998, Zhu et al.
1998). However, on a chlorophyll basis, guard cell chloroplasts
have very high rates of electron transport (Shimazaki and
Zeiger 1987), which could, through increased lumen acidification, result in increased zeaxanthin content and explain the high
sensitivity of the light-dependent zeaxanthin metabolism in
guard cells (Srivastava and Zeiger 1995, Zhu et al. 1998).
Guard cells also fix CO2 photosynthetically (Gotow et al. 1988)
and increases in CO2 concentration have been shown to
decrease guard cell lumen acidity by increasing ATP and
NADPH consumption (Cardon and Berry 1992). These opposing effects on lumen pH could help explain interactions
between stomatal light and CO2 responses and provide a basis
for the reciprocal relationship between the acclimation of stomatal sensitivity to blue light and CO2.
The present study shows for the first time that the blue
light response of guard cells acclimates to growth conditions
with a time course identical to that previously reported for an
acclimation of the guard cell response to CO2. These guard cell
properties are likely to have functional and ecophysiological
implications that warrant further study.
Materials and Methods
Plant material and growth conditions
Seeds of V. faba L. cv Windsor Long Pod (Bountiful Gardens
Seeds, Willits, CA, U.S.A.) were planted in pots with commercial potting mix (Sunshine mix #1, American Horticultural Supply, Camarillo,
CA, U.S.A.). Plants were grown in a growth chamber (Conviron PGV36, Asheville, NC, U.S.A.) at 85% relative humidity (RH), 12 h light
550 µmol m–2 s–1 (incandescent 40 W Philips; fluorescent: GTE Sylvania F96T12/CW/VHO), 25°C/12 h dark, 15°C, or in a greenhouse
under natural light, 50–75% RH, 25–30°C day/15–20°C night. 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 Company, Gardena, CA, U.S.A.).
Measurements of stomatal response to light
Two leaves 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 in the dark for 60 min in a solution containing 1 mM MES-NaOH buffer (pH 6.0), 0.1 mM CaCl2 and
1 mM KCl. After this dark preincubation, an initial aperture measurement was taken and the epidermal peels were kept in the dark or
exposed to: 120 µmol m–2 s–1 red light, 10 µmol m–2 s–1 blue light plus
120 µmol m–2 s–1 red light, or 60 µmol m–2 s–1 white light. A final
aperture measurement was taken after a 60 min light treatment period.
The solution was aerated with 400 cm3 m–3 CO2 air throughout the preincubation and light treatment periods. Red light was provided by a red
filter (No. 2423 plexiglass, 50% cut-off 595 nm; Rohm and Haas, Hayward, CA, U.S.A.) using Sylvania 300-W 300PAR56/2MFL Cool Lux
flood lamps (GTE Products Corp., Winchester, KY, U.S.A.) as the
light source. Blue light was provided by a blue filter (No. 2424 plexiglass, 470 nm maximum, half-band width 100 nm; Rohm and Haas)
using Sylvania DAH 500 W incandescent projector bulbs as the light
source. White light was provided by Sylvania DAH 500 W projector
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bulbs attenuated with neutral density filters. Light intensity was measured with a Li-Cor quantum sensor (Li-Cor Inc., Lincoln, NE, U.S.A.).
In all treatments, the 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, U.S.A.) and JAVA image analysis software (Jandel Scientific, Corte Madera, CA, U.S.A.). At each
time point, aperture values from at least 30 stomata from at least three
separate epidermal peels were used to determine average aperture for
that experiment. Experiments were repeated at least three times.
Transfer experiments
V. faba plants were grown for 21 d under either growth chamber
or greenhouse conditions, then transferred to the alternative environment. At intervals after the transfer, stomatal response to red plus blue
light was tested as described above.
Short-term transfer experiments
A set of short-term transfer experiments was undertaken in order
to determine whether the rapid loss of blue light sensitivity upon transfer of plants to the growth chamber represented an acclimation
response or an immediate inhibition of the response by some factor in
the growth chamber environment. Greenhouse-grown V. faba plants
were transferred to the growth chamber at the beginning of a light
cycle and subjected to growth chamber conditions for 6, 12, 20 or
24 h. At the end of this period, the plants were returned to the greenhouse. The blue light sensitivity of stomata from these plants was
determined 24 h after the start of the transfer and at the beginning of
the two subsequent daily cycles as described above.
Acknowledgments
This work was supported by U.S. Department of Energy grant
#90ER20011 and National Science Foundation grant #DCB 8904254.
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(Received June 21, 2004; Accepted September 10, 2004)