Guard Cell: Electronically linked
Pascal Mäsera, Nathalie Leonhardtb,c and Julian I. Schroederb1
aInstitute of Cell Biology, University of Berne, CH-3012 Bern, Switzerland
bDivision of Biological Sciences, Cell and Developmental Biology Section and Center for Molecular Genetics,
University of California, San Diego, La Jolla CA92093-0116, USA
cDepartement d'ecophysiologie vegetale et de microbologie, CEA Cadarache, F-13180 St Paul Lez
1Corresponding author, e-mail: juilan at biomail dot ucsd dot edu, phone: 858-534-7759, fax: 858-534-7108
The Arabidopsis Book, eds. C. R. Somerville
& E. Meyerowitz, ASPB
• Figure 1 is linked to explanations that appear upon mouse-over.
A model for roles of ion channels in ABA signalling.
Light-induced stomatal opening.
ABA-induced stomatal closing.
Being rooted in one place plants must respond to changes in environmental conditions and stresses. Hormone and light signal transduction pathways form complex networks that control plant responses to the environment. In spite of their importance for plant growth and development, these signaling pathways remain "grey boxes", with many major players and their interactions remaining unknown. In guard cells, a network of signal transduction mechanisms integrates water status, hormone responses, light, CO2 and other environmental conditions to regulate stomatal movements in leaves for optimization of plant growth and survival under diverse conditions. Stomatal guard cells have become one of the well-developed model systems for understanding how various signaling components can interact within a network in a single plant cell. Guard cells allow quantitative dissection of the functions of individual genes and proteins within signaling cascades because:
1. Guard cells respond cell-autonomously to physiological stimulation, allowing cell biological analyses of stomatal opening and closing in response to various stimuli.
The roles of ion channels in ABA signaling
The hormone ABA triggers a signalling cascade in guard cells that results in stomatal closure and inhibits stomatal opening. Stomatal closure is mediated by turgor reduction in guard cells, which is caused by efflux of K+ and anions from guard cells, sucrose removal, and a parallel conversion of the organic acid malate to osmotically inactive starch (MacRobbie, 1998). Figure 1 shows an extension of early models for the roles of ion channels in ABA-induced stomatal closing (Schroeder and Hedrich, 1989; McAinsh et al., 1990).
|Figure 1. A model for roles of ion
channels in ABA signaling.
Mouse-over for explanations or see text below (mouse-over does not work on Mac browsers and some PC browsers) .
|ABA triggers cytosolic calcium ([Ca2+]cyt)
increases (McAinsh et al., 1990; Fig. 1, left panel). [Ca2+]cyt elevations activate two different types
of anion channels: Slow-activating sustained (S-type; Schroeder and Hagiwara, 1989) and rapid transient (R-type; Hedrich et
al., 1990) anion channels. Both mediate anion release from guard cells,
causing depolarization (Fig. 1, left panel). This change in membrane potential
deactivates inward-rectifying K+ (K+in)
channels and activates outward-rectifying K+ (K+out)
channels (Schroeder et al., 1987), resulting in K+ efflux from
guard cells (Fig. 1,
left panel). In addition,
ABA causes an alkalization of the guard cell cytosol (Blatt and Armstrong,
1993) which directly enhances K+out channel activity (Blatt and Armstrong, 1993;
Ilan et al., 1994; Miedema and Assmann, 1996) and down-regulates the transient
R-type anion channels (Schulz-Lessdorf et al., 1996). The sustained efflux
of both anions and K+ from guard cells via anion and K+out channels contributes to loss of guard cell
turgor, which leads to stomatal closing (Fig. 1).
As vacuoles can take up over 90% of the guard cell’s volume, over 90% of the ions exported from the cell during stomatal closing must first be transported from vacuoles into the cytosol (MacRobbie, 1998; MacRobbie, 1995). [Ca2+]cyt elevation activates vacuolar K+ (VK) channels proposed to provide a pathway for Ca2+-induced K+ release from the vacuole (Ward and Schroeder, 1994). At resting [Ca2+]cyt, K+ efflux from guard cell vacuoles can be mediated by fast vacuolar (FV) channels, allowing for versatile vacuolar K+ efflux pathways (Allen and Sanders, 1996). The pathways for anion release from vacuoles remain elusive.
Stomatal opening is driven by plasma membrane proton-extruding H+-ATPases. H+-ATPases can drive K+ uptake via K+in channels (Fig. 1, right panel; Kwak et al., 2001). Cytosolic Ca2+ elevations in guard cells down-regulate both K+in channels (Schroeder and Hagiwara, 1989) and plasma membrane H+-ATPases (Kinoshita et al., 1995), providing a mechanistic basis for ABA and Ca2+ inhibition of K+ uptake during stomatal opening (Fig. 1, right panel).
|Light-induced stomatal opening
Guard cells respond to a multitude of signals including temperature, partial CO2 pressure, light, humidity, and hormonal stimuli. For the majority of signals the molecular identity of the sensors is not known, with the notable exception of blue light: The phototropins PHOT1 and PHOT2 were shown to be the blue light receptors in Arabidopsis guard cells (Kinoshita et al., 2001). Figure 2 illustrates the signaling cascade from activation of PHOT1,2 to stomatal opening in terms of known genes and their relative position in the signal transduction pathway.
|ABA-induced stomatal closing
One of the best understood plant signaling networks is the one triggered by ABA in guard cells, causing stomatal closure. As shown in Figure 3, many genes encoding for positive as well as negative regulators of guard cell ABA signaling have been identified in Arabidopsis. The gene(s) encoding the ABA receptor(s), however, remained elusive. Most of the ABA signal transduction components were found by classic "forward" genetic screens for either increased or reduced sensitivity to ABA.
We thank Annual Reviews for permission to use the review by Schroeder et al. (2001) for this electronic model. We thank Dr. June Kwak for help in preparing figure 1 and Guillaume Leonhardt for help with figures 2 and 3. Preparation of this article and research from the authors' laboratory was supported by NSF (MCB 0077791) and NIH (R01GM060396) grants to J.I.S., Human Frontiers Science Program fellowships to N.L. and P.M., and in part by a grant from DOE (DE-FG02-03ER15449) and NSF (DBI 0077378) to J.I.S.
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