Changes In Guard Cell Turgor Research Articles

Acclimatisation of guard cell metabolism to long‐term salinity

Stomatal movements are enabled by changes in guard cell turgor facilitated via transient accumulation of inorganic and organic ions imported from the apoplast or biosynthesized within guard cells. Under salinity, excess salt ions accumulate within plant tissues resulting in osmotic and ionic stress. To elucidate whether (a) Na+ and Cl- concentrations increase in guard cells in response to long-term NaCl exposure and how (b) guard cell metabolism acclimates to the anticipated stress, we profiled the ions and primary metabolites of leaves, the apoplast and isolated guard cells at darkness and during light, that is, closed and fully opened stomata. In contrast to leaves, the primary metabolism of guard cell preparations remained predominantly unaffected by increased salt ion concentrations. Orchestrated reductions of stomatal aperture and guard cell osmolyte synthesis were found, but unlike in leaves, no increases of stress responsive metabolites or compatible solutes occurred. Diverging regulation of guard cell metabolism might be a prerequisite to facilitate the constant adjustment of turgor that affects aperture. Moreover, the photoperiod-dependent sucrose accumulation in the apoplast and guard cells changed to a permanently replete condition under NaCl, indicating that stress-related photosynthate accumulation in leaves contributes to the permanent closing response of stomata under stress.

On the origins of osmotically driven stomatal movements.

Contents Summary 84 I. Introduction 84 II. Stomatal form and biomechanics 85 III. Stomatal function 86 IV. Evolution of guard cell ion channels 87 V. Conclusions 88 Acknowledgements 88 Author contributions 88 References 88 SUMMARY: Stomatal pores with apertures that can be adjusted by changes in guard cell turgor have facilitated plant success in dry environments. We explore their evolutionary origins, considering recent findings from bryophytes. Unlike vascular plant stomata, which close to prevent water loss, bryophyte stomata become locked open to promote spore desiccation. We find that the families of ion channels, known to control stomatal movements in angiosperms, are ancient and represented across extant land plants. However, although angiosperm guard cells express specific ion channel genes, none appear specifically expressed in stomata-bearing moss tissues. Given the evolutionary shift in stomatal function from promotion to prevention of water loss, we postulate that ion channels adopted guard cell-specific functions after the divergence of bryophytes.

PHO1 expression in guard cells mediates the stomatal response to abscisic acid in Arabidopsis

Stomatal opening and closing are driven by ion fluxes that cause changes in guard cell turgor and volume. This process is, in turn, regulated by environmental and hormonal signals, including light and the phytohormone abscisic acid (ABA). Here, we present genetic evidence that expression of PHO1 in guard cells of Arabidopsis thaliana is required for full stomatal responses to ABA. PHO1 is involved in the export of phosphate into the root xylem vessels and, as a result, the pho1 mutant is characterized by low shoot phosphate levels. In leaves, PHO1 was found expressed in guard cells and up-regulated following treatment with ABA. The pho1 mutant was unaffected in production of reactive oxygen species following ABA treatment, and in stomatal movements in response to light cues, high extracellular calcium, auxin, and fusicoccin. However, stomatal movements in response to ABA treatment were severely impaired, both in terms of induction of closure and inhibition of opening. Micro-grafting a pho1 shoot scion onto wild-type rootstock resulted in plants with normal shoot growth and phosphate content, but failed to restore normal stomatal response to ABA treatment. PHO1 knockdown using RNA interference specifically in guard cells of wild-type plants caused a reduced stomatal response to ABA. In agreement, specific expression of PHO1 in guard cells of pho1 plants complemented the mutant guard cell phenotype and re-established ABA sensitivity, although full functional complementation was dependent on shoot phosphate sufficiency. Together, these data reveal an important role for phosphate and the action of PHO1 in the stomatal response to ABA.

Stomatal (mis)behaviour

When stomata first evolved they initiated the greening of terrestrial earth, and now more than 400 million years later these simple bi-cellular valves in the leaf surface regulate global fluxes of water and carbon. Despite their importance and superficial simplicity, the behaviour of stomata remains a great challenge to understand. Different approaches to studying stomatal control have yielded rather disparate models for how stomata respond to environmental stimuli. Much of this discord arises from the diversity of mechanisms apparently involved in changing guard cell turgor and hence the aperture of the stomatal pore. On the one hand, the physical tension produced by dragging water from the soil through the xylem to the leaves directly influences leaf and guard cell turgor, while on the other hand, phytohormone levels (most importantly abscisic acid), light, photosynthesis and atmospheric gases induce active changes in guard cell turgor by triggering ionic pumping. Each stomatal control mechanism has its own champion and no model has ever successfully integrated all components. In such an environment there is great value in examining how different parts of the stomatal control network interact, particularly the competition between 'hydraulic' signals related to leaf water content and 'metabolic' signals related to ambient photosynthetic conditions.

Guard cells

What are guard cells? A pair of guard cells surrounds each stoma on the leaf surface. Stomata are important because they regulate the uptake of CO2 from the atmosphere for photosynthesis and also the loss of water vapour from the plant during transpiration. The aperture of the stomatal pore is controlled by the two guard cells. When the guard cells are fully turgid the pore gapes open, whereas when they lose turgor the pore closes. Guard cells optimise leaf gas exchange in response to changing environmental conditions and their turgor is controlled by alterations in atmospheric CO2 concentration, light intensity, humidity and the drought hormone abscisic acid. Not to be confused with… Anything to do with the penal system or for that matter stigmata, although to the true believers guard cells are objects of considerable veneration. So are they a Johnny-come-lately arrival on the plant biology scene? Not at all. First described in the 17th century they were studied in the latter part of the 19th century and early 20th century by Francis Darwin and the great German plant physiologists of that era and have been subjected to intense investigation ever since. As a result we know quite a lot about how they work. So how do guard cells work? Changes in guard cell turgor are driven largely by fluxes of K+ ions. Underlying the fluxes is the co-ordinated activity of a battery of ion channels located at both the plasmalemma — the plant cell membrane — and tonoplast — the single membrane that bounds the vacuole in plant cells. The signal transduction pathways responsible for regulating these ion channels are being pieced together and there is good evidence that Ca2+, H+, cyclic ADP ribose, sphingosine-1-phosphate, inositol hexakisphosphate, phospholipases C and D and various protein kinases and phosphatases are all involved. Is it all just about the control of turgor? It certainly isn't. Guard cell development is also currently attracting great interest. Several guard cell development mutants have been isolated in Arabidopsis and two genes involved in the control of stomatal patterning — HIC and SDD1 — have recently been identified. HIC, for high carbon dioxide, encodes an enzyme involved in the synthesis of very-long-chain fatty acids, and is a negative regulator of stomatal development that responds to CO2. SDD1 encodes a subtilisin-like serine protease which may be involved in mediating a signal that controls the development of cell lineages that lead to guard cell formation. In addition, the observation that stomatal numbers on the leaf surface track atmospheric CO2 levels over the past 300 million years has prompted interest from the global climate change community. Don't say ‘You don't really work on holes in the leaf do you?’. Do say ‘I never knew I/V curves could be so interesting’. Where can I find out more?

Calcium ions as second messengers in guard cell signal transduction

Ca2+ is a ubiquitous second messenger in plant cell signalling. In this review we consider the role of Ca2+‐based signal transduction in stomatal guard cells focusing on three important areas: (1) the regulation of guard cell turgor relations and the control of gene expression in guard cells, (2) the control of specificity in Ca2+ signalling, (3) emerging technologies and new approaches for studying intracellular signalling. Stomatal apertures alter in response to a wide array of environmental stimuli as a result of changes in guard cell turgor. For example, the plant hormone abscisic acid (ABA) stimulates a reduction in stomatal aperture through a decrease in guard cell turgor. Furthermore, guard cells have been shown to be competent to relay an ABA signal from its site of perception to the nucleus. An increase in the concentration of cytosolic free Ca2+ ([Ca2+]1) is central to the mechanisms underlying ABA‐induced changes in guard cell turgor. We describe a possible model of Ca2+‐based ABA signal transduction during stomatal closure and discuss recent evidence which suggests that Ca2+ is also involved in ABA nuclear signal transduction. Many other environmental stimuli which affect stomatal apertures, in addition to ABA, induce an increase in guard cell [Ca2+]1) This raises questions regarding how increases in [Ca2+]1) can be a common component in the signal transduction pathways by which stimuli cause both stomatal opening and closure. We discuss several mechanisms of increasing the amount of information contained within the Ca2+ signal, including encoding information in a stimulus‐specific Ca2+ signal or Ca2+ signature', the concept of the ‘physiological address’ of the cell, and the use of other second messengers. We conclude by addressing the emerging technologies and new approaches which can be used in conjunction with guard cells to dissect further the molecular mechanisms of Ca2+‐mediated signalling in plants.

Stomatal Responses to Light and Leaf-Air Water Vapor Pressure Difference Show Similar Kinetics in Sugarcane and Soybean

Stomatal responses to light and humidity (vapor pressure difference, VPD) are important determinants of stomatal conductance. Stomatal movements induced by light are the result of a transduction of the light stimulus into modulated ion fluxes in guard cells and concomitant osmotic adjustments and turgor changes. It is generally assumed that this transduction process is a general stomatal property, with different environmental stimuli integrated into guard cell metabolism through their modulation of ion fluxes. In contrast with this notion, the VPD response, which is unique because both its triggering signal and the turgor changes required for aperture modulations involve water molecules, has been considered to be hydropassive and thus independent of guard cell metabolism. We used a kinetic approach to compare the light and VPD responses in order to test the hypothesis that hydropassive changes in guard cell turgor could be faster than the metabolism-dependent light responses. Changes in stomatal conductance in intact leaves of sugarcane and soybean were measured after application of step changes in VPD and in light. In spite of a 5-fold difference in overall rates between the two species, the response rates following light or VPD steps were similar. Although a coincidental kinetic similarity between two mechanistically different responses cannot be ruled out, the data suggest a common mechanism controlling stomatal movements, with the VPD stimulus inducing metabolic modulations of ion fluxes analogous to other stomatal responses.

Cell Potentials and Turgor Pressures in Epidermal Cells of Tradescantia and Commelina

Cell Potentials and Turgor Pressures in Epidermal Cells of Tradescantia and Commelina

Stomatal responses to light and CO2 are dependent on KCI concentration

Abstract. The responses of stomata on detached epidermis of Commelina communis to light and CO2 have been shown to be strongly dependent on the concentration of KCI in the incubation medium. There was a high sensitivity to the two stimuli in 50 mM KCI, but there were much reduced responses at lower and higher concentrations. It is considered that an appropriate choice of medium is essential if useful physiological studies of stomata are to be made using epidermal strips. At lower KCI concentrations, the ability of the stomata to open is thought to be limited by the availability of K+ ions, and at higher concentrations their ability to close may be affected because of an inhibition of the net efflux of K+. The production of malate was related to KCI concentration, and was largest in the medium containing zero KCI which supported poor stomatal responses to light and CO2It is concluded that malate metabolism is unlikely to play a central part in the changes in guard cell turgor that are brought about by light and CO2.

FURTHER OBSERVATIONS OF CATION‐STIMULATED STOMATAL OPENING IN ISOLATED EPIDERMIS

SummaryMeasurements of apparent osmotic pressures of guard cells in isolated epidermis of Commelina communis indicate a considerable rise (up to 26.3 bars) when K+ ions are added to the incubation medium. This rise in apparent osmotic pressure appears to be the major cause of the stomatal opening that is stimulated by K+ ions, but reduction in turgor of the epidermal cells, owing to the solutes in the incubation medium, may also contribute to the wide stomatal apertures. Histochemical tests on epidermis taken from leaves with stomata that were closed in darkness, or that were open in light, suggest that K+ accumulates in guard cells when stomata open in response to light. No movements of K+ or Na+ from epidermis to mesophyll could be detected and it is concluded that ion movements associated with changes in guard cell turgor are probably confined to the epidermis in C. communis. Ion uptake (indicated by 86Rb and 24Na) into epidermis was stimulated by light but not by a reduction in CO2 concentration, whereas stomatal apertures were affected by these environmental factors to approximately the same extent. It is tentatively concluded that active transport of monovalent cations into guard cells might explain the CO2‐independent light responses of stomata, but not their light‐independent CO2 responses.