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415 Calcium oscillations in higher plants Nicola H Evans*, Martin R McAinsh† and Alistair M Hetherington‡ There is considerable interest in the possibility that stimulusinduced oscillations in cytosolic free calcium encode information that is used to specify the outcome of the final response in calcium-based signalling pathways in plants. Recent results provide conclusive evidence that plant cells can decipher complex calcium signatures. Addresses Department of Biological Sciences, University of Lancaster, Lancaster LA1 4YQ, UK *e-mail: [email protected] † e-mail: [email protected] ‡ e-mail: [email protected] Current Opinion in Plant Biology 2001, 4:415–420 1369-5266/01/$ — see front matter © 2001 Elsevier Science Ltd. All rights reserved. Abbreviations ABA abscisic acid AtCBL Arabidopsis calcineurin-B-like protein [Ca2+]cyt concentration of free calcium ions in the cytosol [Ca2+]ext concentration of calcium ions outside the cell NF Nod factor PLC phospholipase C S1P sphingosine-1-phosphate Introduction The calcium ion is firmly established as an important component of a diverse array of plant signal transduction pathways [1–3]. In fact, it is the very ubiquity of this intracellular second messenger that has prompted investigations into how specificity is controlled in calcium-based signalling systems [1,4]. It has been suggested that information encrypted in the stimulusinduced increase in the concentration of free calcium ions in the cytosol ([Ca2+]cyt) helps to define the outcome of the response. Stimulus-specific increases in [Ca2+]cyt are called calcium signatures [5]. Of the different calcium signatures that have been recorded in plants, stimulusinduced oscillations in [Ca2+]cyt are currently attracting the greatest interest. The purpose of this short review is to provide an introduction to oscillations in [Ca2+]cyt and the way in which they are generated. We follow with a discussion of three signalling pathways in which [Ca2+]cyt oscillations are well documented. The review concludes with a discussion of the prospects for the future in this branch of signal transduction research. Oscillations in [Ca2+]cyt and their generation Table 1 provides a survey of the occurrence and characteristics of stimulus-induced oscillations in [Ca2+]cyt, which have been observed in many different cell types and are induced by a wide range of stimuli. A knowledge of the way in which [Ca2+]cyt oscillations are generated is one key to understanding how specificity is encoded in calcium-based signalling systems. Changes in the rate at which calcium enters and exits the cytosol are likely to form the basis of any mechanism that generates [Ca2+]cyt oscillations. These fluxes include influx and efflux across the plasma membrane and release and uptake into intracellular stores [2], including a contribution from the nucleus [6,7]. Accordingly, it is likely that oscillations in [Ca2+]cyt reflect the coordinated operation of plasma membrane calcium-permeable channels, secondmessenger-mediated calcium release from internal stores, the plasma membrane H+/Ca2+ antiporter, endomembrane Ca2+-ATPases and H+-ATPases. The stomatal guard cell is the most extensively studied model in investigations of the generation of [Ca2+]cyt oscillations. Using calcium imaging and the manganese quench technique, McAinsh et al. [8] showed that plasma membrane calcium-permeable channels were involved in the generation of [Ca2+]ext-induced oscillations in [Ca2+]cyt (i.e. oscillations induced by the concentration of calcium ions outside the cell) in this cell type. Other evidence highlighting the importance of plasma membrane calcium-permeable channels has been provided by a series of important experiments by Blatt and co-workers [9–11]. Using Vicia faba, they showed that calcium influx through a hyperpolarisation-activated channel was coupled to oscillations in the potential of the guard cell plasma membrane [12,13] and this led to pulsatile increases in [Ca2+]cyt. Abscisic acid (ABA) has been shown to increase the probability of the opening of this hyperpolarisation-activated Ca2+-permeable channel [11], which suggests that it may be involved in the generation of the [Ca2+]cyt oscillations that frequently accompany ABAinduced stomatal closure [14]. Schroeder and colleagues, working with Arabidopsis, showed that ABA and H2O2 stimulated a hyperpolarisation-induced calcium channel [15]. These results show clearly that calcium-permeable channels are involved in the generation of oscillations in [Ca2+]cyt and highlight the importance of membrane voltage in the regulation of these fluxes. Although Ca2+ influx through a calcium-permeable plasma membrane channel may trigger the onset of oscillations under some circumstances [16], in ABA-induced [Ca2+]cyt oscillations for example, calcium release from internal stores is undoubtedly involved also. Staxen et al. [14] found that an inhibitor of phospholipase C (PLC) interfered with the ability of ABA to generate oscillations in guard-cell [Ca2+]cyt. This observation suggests that inositol 1,4,5triphosphate (Ins[1,4,5]P3)-gated calcium-release channels are involved in the generation of ABA-induced [Ca2+]cyt oscillations. Interestingly, the same inhibitor had no effect on [Ca2+]ext-induced [Ca2+]cyt oscillations, indicating the differential involvement of the Ins(1,4,5)P3–PLC pathway in the generation of ABA and [Ca2+]ext-induced [Ca2+]cyt oscillations. Further work from this group has shown that 416 Cell signalling and gene regulation Table 1 Oscillations in [Ca2+]cyt in plants. Cell type Stimulus Method Characteristics Reference(s) Guard cells [Ca2+]ext fura-2 0.1 mM: period, 8.3 ± 0.8 min; amplitude, 300–560 nM 1.0 mM: period, 13.6 ± 0.6 min; amplitude, 400–850 nM 750 µM: period, 5.8 ± 0.1 min; amplitude, <60 nM 10 mM: period, 6.7 ±0.2 min; amplitude, >120 nM 1 mM: period, 161 ± 20 s; amplitude ~160 nM 10 mM: period, 396 ± 23 s; amplitude, ~1020 nM [8,14,29] fura-2 Cameleon [19••,30••,46] Caged Ca2+ fura-2 Period, 4.5 ± 0.3 min [8] ABA fura-2 10 nM: period, 11.0 ± 0.9 min; amplitude, 200–600 nM 1 µM: period, 18.0 ± 0.9 min; amplitude, 200–600 nM Transients: period, 468 ± 41 s; amplitude, ~500 nM Oscillations: period, 333 ± 35 s; amplitude, ~500 nM [14] [30••] Cameleon Seedlings [45] [19••,30••,46] H2O2 Cameleon Repetitive transients: amplitude, ~700 nM Cold Cameleon Repetitive transients: period, 154 ± 11 s; amplitude, ~125 nM [30••] Hyperpolarisation fura-2 fura-2 Cameleon Membrane hyperpolarisation: oscillations and 'waves' Low [K+]ext: oscillations in 30% cells Low [K+]ext: transients and oscillations [10] [14] [19••,30••,46] Cyclic ADP-ribose fura-2 Period, ~3.75 min; amplitude, ~200 nM [17] S1P 6 µM: period, 3.8 ± 0.4 min; amplitude, 30–50 nM 50 µM: period, 2.8 ± 0.2 min; amplitude, 50–100 nM [18•] fura-2 Circadian Recombinant aequorin Period, ~22 h; amplitude, 400–550 nM [47,48] Cold Recombinant aequorin Frequency, ~100 s [49] Roots Mannitol Targeted aequorin Oscillations in the endodermis and pericycle [50] NaCl Targeted aequorin Oscillations in the endodermis and pericycle Root hairs Nod factors Ca Green-/fura-2-dextran Spiking: period, ~60 s Oregon Green-dextran Spiking: period, 102 ± 24 s Oregon Green-dextran Spiking: period, 1–2 min; amplitude, ~200 nM [21] [22•] [23•] Staminal hairs Mastorporan Ca Green-dextran [51] Pollen tubes Caged Ins(1,4,5)P3 Ca Green 'Waves': period, 6–10 min [52] Caged Ca2+ Ca Green-dextran Period, 30–45 s [53] Growth Indo-1-dextran fura-2-dextran fura-2-dextran Recombinant aequorin Period, ~80 s; amplitude, >1 µM Period, 15–46 s; amplitude, 0.55–1.2 µM Period, ~23 s; amplitude, 0.75–3.0 µM Period, 38.7 ± 1.8 s; amplitude, 3–10 µM [53] [25] [54] [26,27•] Red/far-red light Quin-2-AM Frequency, 0.017–0.05 s–1; amplitude, <0.15 µM [55,56] Maize epidermal cells Auxin Microelectrodes Indole acetic acid: period, ~36 min [57] Unicellular green algae Strontium fura-2-dextran Spiking: frequency, 0.8–0.2 min–1; period, 35 ± 8 s; amplitude, 367 ± 71 nM [58,59] fura-2-dextran Spiking: frequency, 1.0 ± 0.4 min–1; period, 30 ± 2 s [58] Oat protoplasts Caffeine Ins(1,4,5)P3, inositol (1,4,5) triphosphate; [K+]ext, Period, ~3 min; amplitude, ~500 nM [50] concentration of free potassium outside the cell. the messengers cyclic adenosine diphosphoribose [17] and S1P (sphingosine-1-phosphate) [18•] are involved in ABA signalling and are capable of generating [Ca2+]cyt oscillations. These data illustrate two important points: first, multiple pathways are available for the generation of oscillations in [Ca2+]cyt; and second, different stimuli can access different mechanisms for generating [Ca2+]cyt oscillations. A recent paper demonstrates that mechanisms for the removal of calcium from the cytosol are as important to the generation of [Ca2+]cyt oscillations as those for influx. Allen et al. [19••] observed that [Ca2+]ext- and hydrogen-peroxideinduced [Ca2+]cyt oscillations in Arabidopsis guard cell [Ca2+]cyt were abolished in the det3 mutant — which exhibits reduced expression of a subunit of the V-type ATPase. As the sequestration of calcium into internal stores is an active process that is reliant on the electrochemical gradient for H+, Allen et al. conclude that the reduction in endomembrane energisation in the mutant disrupted the ability to generate [Ca2+]cyt oscillations. Interestingly, neither ABA- nor cold-induced [Ca2+]cyt oscillations were disrupted in the det3 mutant. This observation underlines the point that different stimuli can access different mechanisms for generating [Ca2+]cyt oscillations. The involvement of oscillations in [Ca2+]cyt in signalling pathways Nod-factor signalling In the legume–Rhizobium symbiosis, Nod factors (NFs) are lipochitooligosaccharide signals synthesised by the bacteria Calcium oscillations in higher plants Evans et al. that are involved in the signal transduction pathway leading to nodule formation [20]. Long and co-workers [21] observed oscillations in [Ca2+]cyt in alfalfa root hairs three to six minutes after NF application. More recently, this work has been extended to the model legume Medicago truncatula. The choice of this species enabled Long and co-workers to make use of the dmi1 and dmi2 mutants, which fail to form nodules in response to the bacteria. Both DMI1 and DMI2 have been proposed to encode proteins that act early in NF perception and signal transduction. In marked contrast to the wild type, the dmi1 and dmi2 mutants failed to exhibit any [Ca2+]cyt oscillations in response to NF [22•]. Similarly in pea, when the nodulation-defective mutants sym8, sym10 and sym19 were challenged with NF, no [Ca2+]cyt oscillations were observed [23•]. These results show that there is a strong correlation between NF-induced [Ca2+]cyt oscillations and nodule formation. Recent data indicate a role for PLC and phospholipase D in this signalling pathway [24]. However, as noted by Long and co-workers [22•], it is not known whether [Ca2+]cyt oscillations are on the main signalling pathway leading to nodulation or are on a separate spur. Pollen-tube growth It is well documented that the growth of root hairs and rhizoids requires a gradient of [Ca2+]cyt, with the highest [Ca2+]cyt found at the growing apex [1].The same is true for growing pollen tubes, but there the situation is more complicated because the [Ca2+]cyt in the tip region oscillates. The oscillations in [Ca2+]cyt have been found to be approximately in phase with the oscillations of growth [25,26]. Although it would be tempting to suggest that the oscillations in [Ca2+]cyt are responsible for driving or setting growth rates, the most recent data show that, in fact, the [Ca2+]cyt oscillations lag slightly behind oscillations in the elongation rate of lily pollen [27•]. Messerli et al. [27•] also observed that the relative peak tube growth rate during the growth oscillations is predictive of the relative magnitude of the peak of the nearest lagging [Ca2+]cyt oscillation. The most up-to-date model [27•] indicates that oscillations in [Ca2+]cyt have an important role in controlling the periodic secretion of new material required for pollen-tube growth but suggests that these oscillations are a component in the overall system rather than the master player. 417 from multiple [Ca2+]cyt-oscillation-inducing stimuli (such as external Ca2+ and external K+, external Ca2+ and ABA, or external Ca2+ and mannitol) to formulate the appropriate calcium signature and final stomatal aperture [29]. These data suggest that the guard cell is capable of reading or decoding the pattern of [Ca2+]cyt. Recent work provides additional evidence that oscillations in [Ca2+]cyt play an important role in guard-cell signalling. In their experiments on the det3 mutant of Arabidopsis, Allen et al. [19••] observed that [Ca2+]ext and hydrogen peroxide — both of which cause stomatal closure — failed to induce oscillations in [Ca2+]cyt. They also noted that the stomata of the mutant failed to close in response to these stimuli. In a further experiment, they asked whether the det3 mutant could be rescued by artificially inducing [Ca2+]cyt oscillations. Using an ingenious protocol, Allen et al. found that the answer to this question was ‘yes’. The results from these experiments showed conclusively that [Ca2+]cyt oscillations are important in directing the outcome of signalling pathways. One of the most striking observations regarding guard-cell [Ca2+]cyt oscillations is that they are relatively slow (Table 1) and continue after the cell has finished adjusting its turgor relations. This raises the important question of the functions of the long-term oscillations. One possibility is that they are responsible for holding the guard cell in a steady, low-turgor state while protecting it from extended periods of exposure to elevated [Ca2+]cyt [14]. Recent data from the Schroeder group [30••] not only support this suggestion but show that, in fact, the situation is more complex. It turns out that the degree of decrease in steadystate aperture is programmed by the frequency, number, duration and amplitude of [Ca2+]cyt oscillation. These authors extended their work to include the Arabidopsis ABA-insensitive gca2 mutant. Although ABA induces [Ca2+]cyt oscillations in this mutant, they are markedly different from those in the wild type and stomatal closure is not observed. By artificially inducing steady-state closureinducing [Ca2+]cyt oscillations, the authors were able to induce steady-state closure in the gca2 mutant. These data provide conclusive evidence that guard cells are able to decipher the information encoded in [Ca2+]cyt oscillations. Conclusions Guard-cell turgor relations Calcium ions are well-established second messengers in the signal transduction pathways responsible for the control of guard-cell turgor [28]. When investigating the response to [Ca2+]ext, McAinsh and co-workers [8] observed that different concentrations of [Ca2+]ext brought about strikingly different patterns of [Ca2+]cyt oscillation (Figure 1). They found that for [Ca2+]ext, and subsequently ABA [14], it was possible to correlate the strength of the external stimulus with both the pattern of [Ca2+]cyt oscillation and the magnitude of stomatal closure. The same group found that guard cells can integrate information The past 12 months have seen considerable advances in our understanding of the role of [Ca2+]cyt oscillations in plants. Although the theoretical benefits of signalling through oscillations in [Ca2+]cyt have been considered in the context of the pollen tube [31•], perhaps the next key question is how they are read or decoded. This issue has received considerable attention in animal cells and several models have been published that are based on calciumdependent protein kinases, phosphoprotein phosphatases [32,33], and protein kinase C [34]. In plants, calciumdependent protein kinases [35] are obvious candidates for primary decoders of [Ca2+]cyt oscillations. Calmodulin is 418 Cell signalling and gene regulation Figure 1 (a) A schematic representation of the mechanism by which signalling information is encoded in the guard-cell calcium signature. (a) The strength of the stimulus ([Ca2+]ext, ABA, S1P) has been correlated directly with the pattern of [Ca2+]cyt oscillations (i.e. their period, frequency and amplitude) [8,14,18•], which, in turn, dictates the resultant steady-state stomatal aperture [8,14,18•,30••]. (b) Guard cells are able to integrate signalling information from a number of stimuli, which induce oscillations in [Ca2+]ext applied simultaneously to generate a novel calcium signature when formulating the final stomatal aperture [29]. Response III is the novel calcium signature produced as a result of applying stimuli A and B simultaneously. Open stoma: turgid guard cells Stimulus ([Ca2+]ext, ABA, S1P) [High] [Ca2+]cyt [Medium] [Ca2+]cyt [Ca2+]cyt [Low] Time Time Time Response I Response II Response III Open stoma: no change in guard cell turgor Partially closed stoma Closed stoma: flaccid guard cells (b) Stimulus B [Ca2+]cyt [Ca2+]cyt Stimulus A Time Response A Response B [Ca2+]cyt Time Time Response C Current Opinion in Plant Biology another obvious candidate [36]. Unlike animal calmodulin, there are isoforms of plant calmodulin that exhibit different calcium-binding affinities [37]. This suggests that, in plants, calmodulin could serve as a highly versatile interpreter of [Ca2+]cyt oscillations. Another family of calcium sensors in plants are the Arabidopsis calcineurin-B-like proteins (AtCBLs). Recent data indicate that individual members of the AtCBL family interact with groups of novel protein kinases from the CIPKS (calcineurin-B-like-interacting protein kinase)/SIP family [38,39]. As AtCBL proteins are known to be involved in salt tolerance and are induced in response to other stresses [40,41], it is likely Calcium oscillations in higher plants Evans et al. 419 that this family of proteins will emerge as key interpreters of [Ca2+]cyt oscillations. 15. Pei ZM, Murata Y, Benning G, Phomine S, Klusener B, Allen GJ, Grill E, Schroeder JI: Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 2000, 406:131-134. Another exciting area for investigation will be calciumregulated proteolysis. This could control the abundance of other signal transduction components such as transcription factors. Data supporting this suggestion have come from recent work on eEF1A (eukaryotic elongation factor 1α) [42•]. Finally, the role of the cytoskeleton in calcium signalling deserves increased consideration. It is becoming clear that this dynamic structure has a major role to play in generating calcium signatures [43] and as a platform on which calcium response components are located [44]. 16. MacRobbie EAC: ABA activates multiple Ca2+ fluxes in stomatal guard cells, triggering vacuolar K+ (Rb+) release. Proc Natl Acad Sci USA 2000, 97:12361-12368. Acknowledgements The authors’ work is supported by the UK Biotechnology and Biological Sciences Research Council. MRM is grateful to the Royal Society of London for the award of a University Research Fellowship. The authors would like to thank Gethyn Allen and Julian Schroeder for making available data prior to full publication. 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