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American Society of Plant Biologists Hypersensitivity of Abscisic Acid–Induced Cytosolic Calcium Increases in the Arabidopsis Farnesyltransferase Mutant era1-2Cell and Developmental Biology Section, Division of Biology and Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093-0116 2 To whom correspondence should be addressed. E-mail julian{at}biomail.ucsd.edu; fax 858-534-7108
Cytosolic calcium increases were analyzed in guard cells of the Arabidopsis farnesyltransferase deletion mutant era1-2 (enhanced response to abscisic acid). At low abscisic acid (ABA) concentrations (0.1 µM), increases of guard cell cytosolic calcium and stomatal closure were activated to a greater extent in the era1-2 mutant compared with the wild type. Patch clamping of era1-2 guard cells showed enhanced ABA sensitivity of plasma membrane calcium channel currents. These data indicate that the ERA1 farnesyltransferase targets a negative regulator of ABA signaling that acts between the points of ABA perception and the activation of plasma membrane calcium influx channels. Experimental increases of cytosolic calcium showed that the activation of S-type anion currents downstream of cytosolic calcium and extracellular calcium-induced stomatal closure were unaffected in era1-2, further supporting the positioning of era1-2 upstream of cytosolic calcium in the guard cell ABA signaling cascade. Moreover, the suppression of ABA-induced calcium increases in guard cells by the dominant protein phosphatase 2C mutant abi2-1 was rescued partially in era1-2 abi2-1 double mutant guard cells, further reinforcing the notion that ERA1 functions upstream of cytosolic calcium and indicating the genetic interaction of these two mutations upstream of ABA-induced calcium increases.
Farnesyltransferases (FTases) are heterodimeric enzymes in eukaryotes that catalyze the attachment of farnesyl lipids to the C-terminal region of target proteins (Schafer and Rine, 1992  ; Zhang and Casey, 1996; Nambara and McCourt, 1999). Farnesylation occurs at a conserved CaaX domain, where "C" is a Cys, "aa" are most often alipathic amino acids, and "X" is usually Cys, Met, Ser, Ala, or Gln. Farnesylated proteins play central roles in cell signaling in yeast and animal cells and include Ras, GTP binding proteins, nuclear lamin B, yeast mating factors, and protein kinases (Glomset and Farnsworth, 1994; Schmitt et al., 1996; Yalovsky et al., 1997). Attachment of a farnesyl lipid to these proteins allows targeting to a membrane surface or facilitates protein–protein interactions and therefore is essential in the construction of functional signaling complexes.
In plants, FTases have been identified at the molecular level in tomato, pea, and Arabidopsis (Yang et al., 1993
An Arabidopsis mutant carrying a fast neutron–induced deletion in the
ABA reduces water loss from plants during drought stress via a signal transduction network in guard cells that leads to stomatal closure (MacRobbie, 1998
Enhanced ABA sensitivity in era1-2 guard cells leads to reduced rates of water loss from era1-2 plants compared with wild-type plants under drought stress (Pei et al., 1998
Increases in cytosolic calcium concentration ([Ca2+]cyt) in guard cells have been shown to be early events in the signaling cascade that results in ABA-induced stomatal closure in a number of plant species (McAinsh et al., 1990
These data suggest that [Ca2+]cyt increases function as a second messenger in a wide variety of ABA signal transduction cascades. Recently, signaling mutants in Arabidopsis and other species are being defined and "mapped" with respect to their effects on stimulus-induced [Ca2+]cyt signals with mutations acting either upstream or downstream of [Ca2+]cyt (Allen et al., 1999a
In this study, we used Arabidopsis plants expressing the calcium indicator yellow cameleon 2.1 (YC2.1) (Allen et al., 1999b
Hypersensitivity of ABA-Induced [Ca2+]cyt Increases in era1-2 Guard Cells ABA elicits repetitive transients, or oscillations, in [Ca2+]cyt in stomatal guard cells maintained in low (5 mM) extracellular KCl buffers (Grabov and Blatt, 1998 ; Allen et al., 1999b, 2000; Staxén et al., 1999). In 75% (n = 36 from 48 cells) of wild-type (Columbia) guard cells expressing the green fluorescent protein–based calcium indicator YC2.1 (Allen et al., 1999b; Miyawaki et al., 1999), application of 10 µM ABA induced repetitive transients in [Ca2+]cyt, with an average peak-to-peak period of 7.6 ± 0.3 min and an amplitude increase of 0.42 ± 0.021 ratio units (n = 36), as shown in Figure 1A . However, in wild-type guard cells, application of only 0.1 µM ABA elicited no, or only small, [Ca2+]cyt increases (change in ratio units of 0.04 ± 0.01; n = 46) (Figure 1B).
As a positive control, 10 mM extracellular calcium ([Ca2+]ext) was applied to these cells at the end of the experiment and elicited large [Ca2+]cyt increases, indicating that they were viable to report [Ca2+]cyt changes (Figure 1B). However, when era1-2 guard cells expressing YC2.1 were treated with 0.1 µM ABA, repetitive [Ca2+]cyt transients were induced in 67% of cells (n = 29 from 43 cells; Figure 1C). Increases in [Ca2+]cyt in era1-2 guard cells induced by 0.1 µM ABA had a mean transient peak-to-peak period of 9.1 ± 0.9 min, an amplitude increase of 0.17 ± 0.033 ratio units, and mean and modal (most common) numbers of transients of 2.5 and 3, respectively (n = 29), within a recording period of up to 45 min. No significant differences in resting [Ca2+]cyt were apparent between wild-type and era1-2 guard cells (P > 0.61 for the wild type [n = 36] versus era1-2 [n = 43]).
The era1-2 mutant shows ABA-hypersensitive stomatal closure (Pei et al., 1998
Calcium Influx Mediated by Calcium-Permeable Currents Shows ABA-Hypersensitive Activation in era1-2
S-Type Anion Channel Activation by [Ca2+]cyt in era1-2 Guard Cells To determine whether the era1-2 mutation also can affect signal transduction mechanisms downstream of [Ca2+]cyt in guard cells, we measured S-type anion channel activation by [Ca2+]cyt. S-type anion currents can be activated by both ABA (Grabov et al., 1997 ; Pei et al., 1997, 1998; Leonhardt et al., 1999; Li et al., 2000) and [Ca2+]cyt (Schroeder and Hagiwara, 1989; Allen et al., 1999a) and are central components of stomatal closure (Schmidt et al., 1995). Unexpectedly, we found that [Ca2+]cyt activation of S-type anion channels in patch-clamped Arabidopsis guard cell protoplasts was dependent on the protoplasts being preincubated with high [Ca2+]ext concentrations, as illustrated in Figure 3 . When protoplasts were preincubated in a solution containing 1 mM [Ca2+]ext, no significant cytosolic calcium activation of S-type anion currents was measured when [Ca2+]cyt was buffered to 280 nM (n = 9) (Figures 3A and 3C) or 2 µM (n = 26) (Figures 3B and 3C). After 1 h of preincubation with 40 mM [Ca2+]ext, only small S-type anion channel currents were recorded when [Ca2+]cyt was buffered to 280 nM (n = 13) (Figures 3D and 3F), but they were activated when [Ca2+]cyt was buffered to 2 µM (Figures 3E and 3F) (n = 8; P < 0.001 for 2 µM versus 280 nM [Ca2+]cyt at -145 mV).
Consistent with these findings, [Ca2+]cyt activation of anion currents measured previously in Arabidopsis guard cell protoplasts followed gigaohm seal formation in a bath solution containing 40 mM CaCl2 (Allen et al., 1999a ). In the experiments represented in Figures 3A to 3F, protoplasts were sealed and recorded in bath solution containing 1 mM CaCl2 after preincubation in either 1 or 40 mM [Ca2+]ext, indicating that the continued presence of high [Ca2+]ext per se is not essential for [Ca2+]cyt activation of anion currents, although a previous exposure to high [Ca2+]ext is required.
Calcium activation of S-type anion currents was compared in wild-type and era1-2 guard cell protoplasts at 1 mM [Ca2+]ext after preincubation in 40 mM [Ca2+]ext, as shown in Figure 4
. S-type anion currents were similar in the wild type and era1-2 at [Ca2+]cyt levels of 500 nM (P > 0.79) or 2 µM (P > 0.58) (Figure 4). Because the activation of anion currents occurs downstream of [Ca2+]cyt (Schroeder and Hagiwara, 1989
The era1-2 Mutation Reduces Inwardly Rectifying K+ Current Channel Activity in Guard Cells To determine if the era1-2 mutation affects other ion channels involved in stomatal movements, inwardly rectifying K+ (K+in) currents were measured in guard cell protoplasts. As shown in Figure 5 , K+in currents were reduced significantly (2.8-fold lower at -180 mV; P < 0.0001; n = 26) in era1-2 guard cells compared with the wild type. K+in channels provide an important route for K+ uptake during stomatal opening (Schroeder et al., 1987 ; Thiel et al., 1992; Kwak et al., 2001). To determine whether lower K+in currents affected stomatal movements in era1-2, stomatal opening was measured in low and high extracellular K+ (Figure 5D). In low K+ (5 mM KCl and 50 µM CaCl2), stomatal opening was similar in the wild type and era1-2 (Figure 5D, left bars; P > 0.46; see also Figure 1D).
However, when extracellular K+ was increased (50 mM KCl and 50 µM CaCl2), wild-type stomata opened farther than those in era1-2 (Figure 5D, right bars). Similarly, at 20 mM KCl, stomatal apertures were smaller in era1-2 compared with the wild type in the absence of ABA (Pei et al., 1998 ). These data suggest that the era1-2 mutation can act as a limiting factor on K+in channel activity in guard cells, reducing stomatal opening.
Epistatic Interaction between abi2-1and era1-2 in [Ca2+]cyt Signaling in Guard Cells
A recent study showed that the abi2-1 mutation disrupts calcium signaling downstream of ABA perception but upstream of ICa activation (Murata et al., 2001
To determine whether the hypersensitivity of ABA-induced [Ca2+]cyt signals in era1-2 (Figure 1C) or the insensitivity of ABA-induced [Ca2+]cyt increases in abi2-1 (Figure 6B) was epistatic in relation to ABA-induced [Ca2+]cyt signals, we measured [Ca2+]cyt and stomatal closure in the era1-2 abi2-1 double mutant in response to low levels of ABA (0.1 µM). (Note that Landsberg erecta/Columbia cross-controls did not show any significant variation from either ecotype in ABA sensitivity in seed germination assays [data not shown].) In the majority of double mutant guard cells (69%; n = 29 from 42 cells tested), there was no induction of [Ca2+]cyt transients after the application of 0.1 µM ABA (Figure 6C), although subsequent application of 10 mM [Ca2+]ext as a control was able to induce [Ca2+]cyt transients. However, in some era1-2 abi2-1 guard cells (31%; n = 13 from 42 cells tested), 0.1 µM ABA induced a transient increase in [Ca2+]cyt (Figure 6D). In these responsive guard cells of the double mutant, a single [Ca2+]cyt transient was induced in all cells that responded to 0.1 µM ABA (n = 13). Therefore, [Ca2+]cyt signaling in guard cells of the double mutant showed a phenotype that was intermediate between those of the two mutant phenotypes (cf. Figures 1C and 6B).
The partial recovery of the abi2-1 [Ca2+]cyt signaling phenotype is reflected in ABA-induced stomatal closure in the double mutant. Under the same experimental conditions used for [Ca2+]cyt imaging here, ABA-induced closure in era1-2 abi2-1 was significantly greater than in abi2-1 (Figure 6E) but less than in the wild type or in era1-2 alone (Figures 1D and 6E) (see Pei et al. [1998] To test this finding further, [Ca2+]cyt activation of S-type anion currents and [Ca2+]ext-induced stomatal closure were measured in the era1-2 abi2-1 double mutant, as illustrated in Figure 7 . S-type anion currents were activated (after a 40 mM [Ca2+]ext preincubation, as in Figures 3 and 4) by [Ca2+]cyt at 500 nM and 2 µM (Figure 7A), and activation was not significantly different from that in the wild-type or era1-2 guard cell protoplasts (Figure 7B) (n = 13 era1-2 abi2-1 guard cells; P > 0.58).
The addition of [Ca2+]ext to preopened stomates can cause [Ca2+]cyt increases and oscillations (McAinsh et al., 1995 ; Allen et al., 1999a, 2000) that cause stomatal closure. Stomatal closure induced by [Ca2+]ext showed no dramatic differences between the wild type, era1-2, and the era1-2 abi2-1 double mutant (Figure 7C), although interestingly, at 0.1 mM [Ca2+]ext, stomatal apertures in the era1-2 mutant were consistently larger than at 0.01 or 1 mM (Figure 7C). The signaling mechanism underlying this phenotype is not known, but this finding suggests additional points of action of the FTase. Together, the [Ca2+]ext-induced stomatal closure in the wild type, era1-2, and the era1-2 abi2-1 double mutant (Figure 7C) and the calcium activation of anion currents (Figures 7A and 7B) reinforce the finding that the era1-2 and abi2-1 mutations both affect guard cell signaling upstream of [Ca2+]cyt.
The role of cytosolic calcium in controlling plant cell signal transduction is becoming more fully understood with the application of new molecular genetic and imaging techniques (Sanders et al., 1999 ; Rudd and Franklin-Tong, 2001). In particular, the ability to map the positions of various mutants in relation to the calcium signal is revealing interactions and relationships in defined signaling cascades (Allen and Schroeder, 2001). However, the identities of many signaling components remain to be identified, and their interactions with calcium-based signaling pathways remain unknown.
To date, five Arabidopsis mutants have been shown to affect guard cell calcium signaling. These mutants fall into three categories: the mutants abi1-1 and abi2-1 impair ABA-induced calcium oscillations (Allen et al., 1999a
In this study, we investigated the effect of the FTase deletion mutant era1-2 on calcium signaling in guard cells. This mutation renders stomatal closure hypersensitive to the hormonal stimulus ABA (Pei et al., 1998
Recent studies have suggested that calcium influx into guard cells across the plasma membrane plays a critical role in ABA-induced stomatal closure (Hamilton et al., 2000
Hyperpolarization-activated calcium channels that mediate Ca2+ influx have been identified in tomato suspension cells (Gelli and Blumwald, 1997
Our data do not exclude additional effects of ERA1 in modulating intracellular calcium release mechanisms (reviewed in Schroeder et al., 2001a
The activation of S-type anion currents by an increase of cytosolic calcium has been shown to be a component of guard cell turgor reduction (Schroeder and Hagiwara, 1989
A previous report has shown that S-type anion current activation in era1-2 guard cell protoplasts was hypersensitive to ABA (Pei et al., 1998
These data suggest two possible explanations for the ABA-hypersensitive anion channel phenotypes observed previously (Pei et al., 1998
Interestingly, a new component of the regulation of S-type anion currents by calcium was revealed in this study (Figure 3). Cytosolic calcium activated S-type currents most effectively when guard cells were preincubated in high external calcium. High extracellular calcium concentrations are known to cause [Ca2+]cyt oscillations in guard cells (McAinsh et al., 1995
Another new effect of the era1-2 mutant on guard cell K+in channel activity also was characterized here (Figure 5). K+in currents were significantly lower in era1-2 compared with wild-type guard cells. This was not observed to have an effect on stomatal aperture under the imposed conditions of low extracellular K+ and Ca2+ concentrations (Figure 1D), but it led to reduced apertures relative to those in the wild type in era1-2 at higher extracellular K+ (Figure 5) (Pei et al., 1998
The idea that ERA1 acts upstream of [Ca2+]cyt was further strengthened by analyzing era1-2 and abi2-1 interactions. The hypersensitivity of ABA-induced cytosolic calcium increases in era1-2 guard cells could partly rescue the impairment of ABA-induced calcium increases in the abi2-1 protein phosphatase type 2C mutant (Figure 6). These data correlate with the intermediate ABA-induced stomatal closing phenotype in the era1 abi2 double mutant (Pei et al., 1998 Overall, the data presented in this study demonstrate how a combination of genetics and a multifaceted cell biological approach can be a powerful tool for dissecting signal transduction pathways and placing mutations at specific points in defined signaling networks. For the era1-2 mutant, this analysis has placed the action of this mutant in guard cells at a point downstream of ABA perception and upstream of plasma membrane calcium influx channel activation.
Plant Growth Arabidopsis thaliana plants were grown in soil (Redi-Earth Peat-Lite Mix; Scotts, Marysville, OH) in a controlled-environment growth chamber (Conviron model E15; Controlled Environments, Asheville, NC) under a 16-h-light/8-h-dark cycle at a photon fluence rate of 75 µmol·m-2·s-1 and a temperature of 20°C. Pots were watered every 2 to 3 days with deionized water. The wild-type background was Columbia for the era1-2 mutant and Landsberg erecta for abi2-1. The era1-2 mutant line used in this study had been backcrossed previously into the wild type (Columbia) three times (Cutler, 1995 ). All mutants and wild types were transformed with yellow cameleon 2.1 (YC2.1) by direct Agrobacterium tumefaciens transformation using floral dip (Allen et al., 1999b). At least three independent YC2.1-transformed lines were used for each wild type and mutant, except for the era1-2 abi2-1 double mutant, for which only two lines were available.
Calcium Imaging
Aperture Measurements
Electrophysiology
To measure calcium influx currents (ICa), the pipette solution contained 10 mM BaCl2, 0.1 mM DTT, 4 mM EGTA, and 10 mM Hepes-Tris, pH 7.1, and the bath solution contained 100 mM BaCl2, 0.1 mM DTT, and 10 mM Mes-Tris, pH 5.6. NAD(P)H (1 mM) was added to the pipette for the measurement of ABA-activated ICa activity. The addition of 5 mM NAD(P)H to the pipette (Pei et al., 2000
To measure S-type anion currents, the pipette solution contained 150 mM CsCl, 2 mM MgCl2, 6.7 mM EGTA, 5 mM MgATP, 10 mM Hepes-Tris, pH 7.1, and a concentration of CaCl2 calculated to give the desired free Ca2+ concentration. Free calcium concentrations were calculated with the program CALCIUM (Foehr et al., 1993
The standard voltage protocol stepped the voltage from a holding potential of +30 mV to -145 mV for 40 s. Subsequent voltage steps were reduced by 30 mV per pulse. The interpulse period was 12 s. No leak subtraction was made. All recordings were made 7 to 10 min after access to the whole cell configuration. There was no preincubation of protoplasts with ABA in these experiments (in contrast to the procedure reported by Pei et al. [1997] To measure inwardly rectifying K+ currents, the pipette solution contained 30 mM KCl, 70 mM K-glutamate, 2 mM MgCl2 6.7 mM EGTA, 3.35 mM CaCl2, 5 mM Mg-ATP, and 10 mM Hepes-Tris, pH 7.1. The bath solution contained 30 mM KCl, 1 mM CaCl2, 2 mM MgCl2, and 10 mM Mes-Tris, pH 5.6. From a holding potential of 0 mV, the voltage was stepped to -180 mV in -20-mV increments for 5 s each. Steady state current was sampled in the last 100 ms of these voltage steps.
We dedicate this work to the memory of our friend Gethyn Allen and his pioneering research in plant Ca2+ signaling. We thank Roger Tsien for the use of a CALCIUM imaging setup for some experiments, Peter McCourt (University of Toronto) for providing the era1-2 and era1-1 mutants, Shaul Yalovsky (Tel Aviv University) for providing the complemented era1-2 lines, and Justin Borevitz (Salk Institute) for Landsberg erecta/Columbia crosses. This research was supported by grants from the National Institutes of Health (Grant GM60396-1P42ES10337), the U.S. Department of Energy (Grant 94ER201807), the National Science Foundation (Grant MCB 0077791), the Torry Mesa Research Institute Syngenta, and the U.S.–Israel Binational Agricultural Research and Development Fund to J.I.S.
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010448. Received October 12, 2001; accepted March 21, 2002.
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Abstract
INTRODUCTION
-subunit of a FTase has been isolated from a screen to identify mutants with an enhanced response to abscisic acid (ABA) (Cutler et al., 1996
-hydroxyfarnesylphosphonic acid, indicating that FTases may function in the guard cell ABA signal transduction pathway (Pei et al., 1998
30% of all guard cells exhibited spontaneous oscillations in [Ca2+]cyt. These cells were not included in the analysis; only cells exhibiting a stable resting [Ca2+]cyt level were used to analyze stimulus-induced [Ca2+]cyt increases. (Note that because measurements of [Ca2+]cyt in this study were collected from two different microscopes that used charge-coupled device cameras with different 480-nm sensitivities, the 535:480-nm ratios were normalized by dividing all measured ratios in any given recording by the initial, steady state ratio from that recording that represents prestimulus [Ca2+]cyt). The yellow fluorescent protein of YC2.1 bleaches at a faster rate than the cyan fluorescent protein, leading to a slow decline in baseline 535:480-nm ratios. Baseline decline was eliminated by a linear correction factor that was calculated from the rate of decrease in baseline ratio before the application of a stimulus. 
