Abstract
Calcium (Ca2+) represents very likely the most versatile ion in living organisms. It is involved in nearly all aspects of plant development and participates in a plethora of regulatory processes. Calcium is an important signaling compound, regulates cellular metabolism and is important for endocytosis and exocytosis. Calcium can easily form complexes with proteins, membranes and other organic acids rendering this ion a versatile signaling constituent and simultaneously a toxic cellular compound. Consequently, the required tight spatial and temporal control of intracellular Ca2+ levels provided the basis for the emergence of calcium signaling. It is this apparent antagonism between the obvious cellular abundance of Ca2+ as a structural important ion in the plant and its required rareness in the cytoplasm as well as the evident question how this simple ion can specifically function in such a myriad of distinct process that has sparked considerable interest and research. Here we will discuss new insights into the signaling function of Ca2+ in the context of its diverse cell biological roles.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
1 Introduction
Calcium (Ca2+) represents very likely the most versatile ion in living organisms. It is involved in nearly all aspects of plant development and participates in a plethora of regulatory processes. Calcium is an important signaling compound, regulates cellular metabolism and is important for endocytosis and exocytosis. Moreover, it is important for energy production within mitochondria and chloroplasts. Ca2+ is an ion that due to its specific properties can easily be dehydrated. Because of its flexibility in forming different coordination numbers and complex geometries, Ca2+ can easily form complexes with proteins, membranes and other organic acids like citrate and oxalate. This unique feature renders Ca2+ a toxic cellular compound because it can easily form insoluble complexes with phosphate (and consequently ATP), and also with DNA and RNA. However, on the other hand this property enabled the evolution of Ca2+ as an important signaling molecule because the required tight spatial and temporal control of intracellular Ca2+ levels provided the basis for the emergence of calcium signaling. It is this apparent antagonism between the obvious cellular abundance of Ca2+ as a structural important ion in certain organelles and cell structures and its required rareness in the cytoplasm as well as the yet not solved question how this simple ion can specifically function in such a myriad of distinct process that has sparked considerable interest and research. Several excellent reviews have in the past addressed the nutritional and signaling functions of Ca2+ (Hepler and Wayne 1985; Sanders et al. 2002; White and Broadley 2003; Hetherington and Brownlee 2004; Hirschi 2004). Here we will discuss new insights into the signaling function of Ca2+ in the context of its diverse cell biological roles.
2 Nutritional and Structural Functions of Ca2+
2.1 Nutritional Functions of Ca2+
Work in the late forties of the last century established that Ca2+ constitutes an important macronutrient for plant germination, growth and development (Mulder 1950; Helms 1971). Besides Mg2+, Ca2+ is the most abundant group two element in plants and in different plant species Ca2+ can reach concentrations between 0.02% (e.g., Poacea species) and ~5% of the plant dry weight, with higher concentrations generally found in dicotylous plants (Broadley et al. 2003). In general, plants are classified into calcifuges that grow on soil with low Ca2+ content, and calcicoles, growing on high calcareous soils that can tolerate a high soluble Ca2+ concentration like Brassicaceae (White and Broadley 2003). Some calcicoles plants are able to deposit large amounts of Ca2+ in trichomes to protect the stomata from excessive Ca2+ (De Silva et al. 1996). Within the plant, Ca2+ is unequally distributed, and reaches higher concentrations in leaves and stems than in underground tissues (Demarty et al. 1984). In aerial parts, young leaves and fruits contain lower Ca2+ concentrations than older leaves (Kirkby and Pilbeam 1984). Calcium uptake is confined to the root tip or to nodes of newly emerging lateral roots, indicating that Ca2+ does not cross the “casparian strip” and follows the apoplastic pathway to reach the xylem of the central cylinder (Kirkby and Pilbeam 1984).
Calcium deficiency affects every tissue and plant organ. Generally, it causes stunted plant growth and appearance of brown spots associated with polyphenol oxidation, necrosis of primarily meristematic cells and later on in older tissues, cracking of fruits and curling of the leaves (Bussler 1962; Simon 1978). Characteristic symptoms are “tipburn” mostly described in agricultural vegetables like lettuce, or “blossom-end rot” in fruits of tomato (Simon 1978; Ho and White 2005). Especially fast growing young tissues with a low transpiration rate and therefore insufficient supply of Ca2+ from the xylem are prone to deficiencies and exhibit symptoms early. This effect is further enhanced by the relative immobility of Ca2+ within the plant because Ca2+ is insufficiently redistributed from older leaves, which harbor a higher Ca2+ content (van Goor and Wiersma 1974; White and Broadley 2003).
Root growth and the development of the root system is also affected under Ca2+ deficiency leading to growth arrest and finally stalling of the root (Simon 1978). Ca2+ also affects the uptake of other ions into the root system. It improves the selective uptake of K+ in the presence of high Na+ concentrations (Epstein 1961,1998). Here Ca2+ concurrently blocks Na+-permeable channels and reduces Na+ uptake (Demidchik and Tester 2002) and inhibits Na+ induced K+ efflux (Shabala et al. 2006). In addition, it was suggested that Ca2+ reduces Na+ induced depolarization of the plasma membrane thereby minimizing K+ efflux by depolarization-activated channels (Shabala et al. 2006).
2.2 Structural Functions of Ca2+
The large ion radius of Ca2+ facilitates straightforward dehydration of the ion thereby enabling the binding of Ca2+ to several anionic headgroups of membrane-lipids like phosphatidylserine, phosphatidic acid or glycolipids and additionally to membrane proteins (Hauser et al. 1976; Jaiswal 2001). Consequently, Ca2+ represents an important regulator of different dynamic membrane processes. Within the cell, Ca2+ promotes the fusion of vesicles to their target membranes by cross-linking the lipids from the two different membranes (Williams 1970; Hauser et al. 1976). On the other hand, Ca2+ is a structure forming cation. It reduces the fluidity and therefore enables a tighter packaging of the membrane lipid bilayer, thereby reducing passive ion-fluxes of monovalent cations like H+, Na+ and K+ (Williams 1970; Jaiswal 2001; White and Broadley 2003; Plieth 2005). Therefore, Ca2+ deficiency induces membrane leakyness for monovalent cations rendering plants susceptible to damage by salt or low pH (Plieth 2005).
Calcium is also an abundant cell wall component critically regulating the strength and pH of the cell wall (Demarty et al. 1984). Here, Ca2+ bridges cell wall polymers like negatively charged galacturonanes or xylans (Brett and Waldron 1996) and influences the formation of the 1,3-β-glucan “callose”, which is an essential cell wall component in the cell plate of dividing cells, in growing pollen tubes, or is produced after wounding. Remarkably, the enzyme β-1,3 glucan synthase, which forms callose is directly activated by Ca2+ (Kauss 1987; Brett and Waldron 1996).
3 The Evolution of Ca2+ as a Signaling Molecule
Several physico-chemical features are unique to Ca2+ and predestinate this ion as potential signaling molecule. Due to the large ionic radius of a Ca2+ ion (99 pm) water molecules are less tightly bound to Ca2+ than to the smaller Mg2+ ion (65 pm). Therefore, less energy is required to remove the bound water to enable Ca2+ ligand interaction (Hepler and Wayne 1985). Consequently, Ca2+ ions are easily dehydrated, and can form complexes with high and variable coordination numbers (6–8, but also 5–10) and are flexible in coordination geometry and Ca2+-ligand distances. Ca2+ binds favorably to carboxylate oxygen, while Mg2+ or Zn2+ have higher affinity toward nitrogen-based ligands, associated with amino acids, which are not as common in proteins than glutamate and aspartate (Williams 1970; Ochiai 1991). Although other ions like Ba2+, Sr2+ and Zn2+ could substitute for Ca2+ function, they are less abundant than Ca2+ and other divalent cations like Cd2+ and Pb2+ are highly toxic (Jaiswal 2001).
On the other hand, these features of Ca2+ are also the reason why elevated levels of Ca2+ will react with inorganic phosphate, forming an insoluble precipitate. Therefore, high Ca2+ acts as a cytotoxin inhibiting the phosphate-based energy system (Hepler and Wayne 1985). Moreover, excess Ca2+ would compete with Mg2+ for binding sites on various proteins. Thus, during evolution, organisms were forced to evolve de-toxifying mechanisms that are effective in keeping Ca2+ at low levels in the cytoplasm. Importantly, Ca2+ pumps, which are responsible to extrude Ca2+ out of the cytoplasm, are themselves Ca2+-activated resulting in a time lag of efflux activation that follows the entry of Ca2+ into the cytoplasm. This facet of Ca2+ regulation mandatory leads to a transient Ca2+ elevation within the cell when Ca2+ permeable channels open (Ochiai 1991) thereby providing a unique system to evolve the extant Ca2+-regulated circuits in which Ca2+ itself activates Ca2+ channels within the cell. This Ca2+-dependent release of Ca2+ from external or internal stores now is responsible for a rapid, amplified (100 fold) but still transient Ca2+ increase and forms the mechanistic basis of many Ca2+ signaling events (Williams 2004).
Since the concentration of Ca2+ in the cytoplasm is kept at low levels, the concentration can be, rapidly and efficiently modulated. In contrast, due to physiological requirements, the cytosolic concentrations of Mg2+ or K+ are relatively high. Therefore, a 100 fold change of these ions in the cytosol would be more difficult to achieve: firstly the amount of ions to be transported would be much higher and secondly, the resulting dramatic change in cellular ion homeostasis would be detrimental while a 100 fold change of the Ca2+ concentration only marginally effects the osmotic balance of the cytoplasm (Hepler and Wayne 1985; Ochiai 1991). Finally, due to the unique properties of Ca2+, this ion can bind to and dissociate from proteins much faster than other ions (Ochiai 1991). This aspect of Ca2+, allows for transient interaction with calcium binding proteins and has enabled the evolution of a signaling system that can control fast and diverse reactions (Hepler and Wayne 1985).
4 Calcium Release in Response to Signals and Stimuli
4.1 Calcium Responses to Abiotic, Biotic Factors and Development
Cytoplasmic changes of Ca2+ concentration from resting concentrations of 100–300 nM up to 1 µM are observed after various signals or stimuli. Abiotic cues like salt (Lynch et al. 1989), osmotic stress (Takahashi et al. 1997; Cessna et al. 1998), drought (Knight et al. 1998), ozone (Clayton et al. 1999), anoxia (Subbaiah et al. 1994), CO2 (Webb et al. 1996), gravitation (Lee et al. 1983; Gehring et al. 1990; Fasano et al. 2002), mechanical injury and touch (Haley et al. 1995; Legue et al. 1997) all cause transient elevations in Ca2+ concentration. Different temperature regimes can also induce Ca2+ responses. Cold stress, especially the cooling rate, is reflected by specific increases of intracellular Ca2+ (Knight et al. 1991; Plieth et al. 1999). Development of freezing tolerance requires influx of extracellular Ca2+ and enhanced Ca2+-dependent exocytosis to enable resealing of the membrane after mechanical disruption provoked by cold (Schapire et al. 2008; Yamazaki et al. 2008). These membrane fusions are mediated by Ca2+ interaction with the sensor protein synaptotagmin to promote interaction with SNARE proteins (Kesavan et al. 2007; Schapire et al. 2008; Yamazaki et al. 2008). Furthermore, tobacco plants also respond with Ca2+ release to heat shock (Gong et al. 1998), while Ca2+ transients were recorded in Arabidopsis during the recovery from heat exposure (Larkindale and Knight 2002).
Also light responses in plants are accompanied by complex and specific patterns of Ca2+ transients. Changes in cytoplasmic Ca2+ concentration were observed after plant exposure to red but not far-red light implicating that this reaction is mediated by the photoreceptor phytochrome B (Shacklock et al. 1992; Neuhaus et al. 1993). Blue light Ca2+ responses depend on the phototropin photoreceptors but not on cryptochromes (Baum et al. 1999; Harada et al. 2003; Stoelzle et al. 2003). However, cryptochromes could fine tune a Ca2+ response (Long and Jenkins 1998), and cryptochrome signaling is mediated via the Ca2+- binding protein SUB1 (short under blue light), which in turn modulates phyotochrome function (Guo et al. 2001a). These observations exemplify the complexity and interconnection of Ca2+ responses that can occur in reaction to a single environmental cue like light. In addition, Ca2+ is also released in a circadian manner and responds distinctly to light intensity (Love et al. 2004).
Similar to abiotic stimuli, biotic factors like bacterial pathogens (Atkinson et al. 1990; Xu and Heath 1998; Blume et al. 2000), fungal elicitors (Knight et al. 1991), attacks by herbivores or symbiotic interactions with nitrogen-fixing bacteria or mycorrhizal fungi cause different and specific Ca2+ responses (Ehrhardt et al. 1996; Kosuta et al. 2008). Moreover, cell apoptosis during the hypersensitive response induced by a pathogen is mediated by a complex regulation of cellular Ca2+ dynamics. An initial transient increase of Ca2+ occurs after pathogen infection (Levine et al. 1996) and is then followed by a silent phase and a second, but sustained increase of cytoplasmic Ca2+ (Grant et al. 2000). Finally, a massive efflux of Ca2+ to the apoplast leads to cell collapse and death (Nemchinov et al. 2008).
Transient changes in cellular Ca2+ concentration have also extensively been observed during tightly regulated developmental processes. Oscillatory, tip-localized gradients of Ca2+ are important for proper growth of pollen tubes and expansion of root hairs by enabling high exocytotic turnover at the growing tip (Rathore et al. 1991; Miller et al. 1992; Rudd and Franklin-Tong 1999). In contrast, the self-incompatibility response during pollination is mediated by a rise of Ca2+ originating from the nuclear region, potentially regulating gene expression to inhibit pollen tube growth (Franklin-Tong et al. 1993). Ca2+ is also essential for fertilization (Faure et al. 1994), and a Ca2+ transient lasting for several minutes has been observed during the sperm-egg fusion event (Digonnet et al. 1997).
4.2 Calcium Responses to Hormones
Calcium release and subsequent signal transduction events are important after perception of phytohormones like cytokinin (Hahm and Saunders 1991), salicylic acid (Kawano et al. 1998) and ethylene (Raz and Fluhr 1992). Jasmonic acid (Sun et al. 2006) and its precursor 12-oxophytodienoic acid (OPDA) induce a large increase of cytoplasmic Ca2+ (Walter et al. 2007). Giberellic acid (GA) causes a long sustained increase of cytosolic Ca2+ at the cell periphery by influx of extracellular Ca2+ (Gilroy and Jones 1992), but the release of intracellular Ca2+ is also important for induction of α-amylase transcription (Chen et al. 1997). GA mediated calcium influx also precedes and is important for the secretion of α-amylase (Bush 1996) and can be accounted to the effect that Ca2+ enhances exocytosis (Homann and Tester 1997) by promoting membrane fusion (Bhalla et al. 2006; Martens et al. 2007). Additionally, GA also increases Ca2+ within the endoplasmic reticulum (ER), which is important for the maturation of α-amylase (Bush et al. 1989a, b). On the other hand, GA induced Ca2+ release in aleurone cells can be reversed by ABA (Gilroy and Jones 1992), and Ca2+ uptake into the ER is also inhibited by ABA (Bush et al. 1993).
Auxin induces an oscillatory Ca2+ release and thereby promotes stomatal opening (Felle 1988; Irving et al. 1992). Abscisic acid (ABA) also induces oscillatory Ca2+ transients resulting in closure of the stomata and being essential to keep them closed in the long term (McAinsh et al. 1990; Allen et al. 1999, 2000, 2001; Staxen et al. 1999). In another study, spontaneous Ca2+ oscillations were terminated by ABA in some guard cells (Klusener et al. 2002). These findings suggest that ABA can have positive and negative effects on the cellular Ca2+ level. Moreover, since Ca2+ levels in the cytosol exhibit circadian oscillation, these different levels of cytoplasmic calcium could also differentially prime the guard cells and other cell types to the effect of ABA, which then leads to a different final outcome (Dodd et al. 2005). Indeed, MacRobbie (1989) found out that the stimulatory effect of ABA is stronger in the afternoon than in the morning (MacRobbie 1989). Moreover, the parameters of Ca2+ oscillations which lead to stomatal closure could depend on the physiological condition of the plant (Klusener et al. 2002).
These examples clearly illustrate the universality and complexity of Ca2+ responses as well as their intricate and often confusing interconnection with various cellular or hormonal processes. They also highlight a continuing dilemma of plant Ca2+ research in which a further accumulation of descriptive data linking Ca2+ responses to certain biological processes will not likely advance our understanding of the underlying functional principles and causalities.
4.3 Interconnection of Ca2+ Dynamics with other Second Messengers
A similar complex situation applies to the interconnection of Ca2+ with other second messenger components. Various second messengers induce Ca2+ release, and their generation itself is often regulated by Ca2+. Diacylglycerol (DAG), Cyclic nucleotides like cAMP and cGMP (Volotovski et al. 1998), cyclic Adenosine-diphospho-Ribose (cADPR) (Allen et al. 1995), Inositol-3-phosphate (InsP3) (Alexandre 1990; Gilroy et al. 1990) or its derivate myo-Inositol-Hexakisphosphate (InsP6) (Lemtiri-Chlieh et al. 2003), Nicotinic Acid-Adenine Dinucleotidphosphate (NAADP) (Navazio et al. 2000), Sphingosine-1-phosphate (S1P) (Ng et al. 2001), extracellular Glutamate (Dennison and Spalding 2000) and extracellular ATP (Demidchik et al. 2003, 2009; Jeter et al. 2004) can mobilize Ca2+ either from intracellular or extracellular stores, respectively. Reactive oxygen species (ROS), generated by plasma membrane NADPH oxidases, cause a Ca2+ influx into the cytosol (Price et al. 1994; Pei et al. 2000; Foreman et al. 2003). Moreover, different types of ROS can differentially activate Ca2+ permeable channels in different root tissues (Demidchik et al. 2007). Like ROS, the Ca2+ releasing second messenger cADPR is also produced after application of ABA (Wu et al. 1997; Leckie et al. 1998), and is also synthesized in a circadian manner which could be important for the observed circadian Ca2+ oscillations (Dodd et al. 2007). These observations point to a further level of complexity interconnecting Ca2+ simultaneously with second messengers, hormonal responses and reactions to environmental cues.
5 Organelles and Ca2+
Calcium can rapidly enter the cell (106 molecules/sec. per channel) but diffusion within the cytoplasm is very limited (up to 0.5 µm) and Ca2+ is rapidly bound by Ca2+ binding proteins or buffered by cell organelles (within 50 µsec) (Clapham 1995; Lecourieux et al. 2002). Indeed, near membrane Ca2+ concentrations in the vicinity of Ca2+ channels are estimated to be 10–100 fold higher than the measured cytoplasmic Ca2+ concentrations (Etter et al. 1996; Demuro and Parker 2006). Therefore, local Ca2+ signals at specific microdomains are assumed to be the basis of differential Ca2+ signals, which can promote different responses to various signals (Berridge 2006).
Various organelles and compartments are implicated in different Ca2+ responses, and moreover, several compartments can act in concert to shape a Ca2+ signal and to establish a correct response to the signal. The major Ca2+ store of the cell is the apoplast which supplies extracellular Ca2+ (1–10 mM). From the apoplast, Ca2+ is released by Ca2+ channels which are activated by changes of the plasma membrane voltage, or by ligand activated channels (Fig. 1a).
Intracellular Ca2+ is stored mainly in the vacuole and ER, and released by voltage dependent and ligand gated channels. Within the vacuole, Ca2+ functions as counterion of inorganic and organic anions (White and Broadley 2003). Additionally, different types of vesicles, like Golgi or endosomal vesicles are potential mobile calcium stores (Wagner and Rossbacher 1980; Wick and Hepler 1980; Sakai-Wada and Yagi 1993; Trewavas 1999; Li et al. 2008), or transport excess calcium and other cations out of the cytoplasm either to the apoplast or to the vacuole (Fig. 1b) (Menteyne et al. 2006). Other organelles, like chloroplast and mitochondria, store Ca2+ also and are important to maintain the cellular Ca2+ and ATP homeostasis (Plieth 2005).
5.1 Calcium Signaling within the Nucleus
High levels of calcium are observed in the nucleus and the nuclear envelope (Wick and Hepler 1980). The nucleus can respond specifically and independently of the cytoplasm to a signal by specific temporal changes in Ca2+ concentration (van Der Luit et al. 1999; Pauly et al. 2001). Bacterial elicitors induce a Ca2+ release in the cytosol and nucleus. However, the nitric oxide (NO) signal following elicitor application is important for the Ca2+ release in the cytosol, but it does not trigger a nuclear Ca2+ response (Lamotte et al. 2004). The nucleus also exhibits specific calcium signals in response to different elicitors. Harpin and flagellin resulted in a different Ca2+ release than observed in response to carbohydrate elicitors like oligogalacturonides. Remarkably, the cytosolic Ca2+ response to these elicitors was comparable (Lecourieux et al. 2005).
These observations suggest that the nucleus does indeed harbor an independent Ca2+ machinery which could involve P-ATPases and nucleotide gated channels located at the inner membrane of the nucleus to regulate the nuclear Ca2+ reservoir (Mazars et al. 2009). Although it was reported that nuclei are Ca2+ impermeable (Xiong et al. 2004), inhibition of Ca2+ entry from the extracellular milieu prevented nuclear Ca2+ rises (Pauly et al. 2001; Mazars et al. 2009). In additon, it was reported that the nuclear membrane can take up Ca2+ in an ATP-dependent manner, which then can be released into the nucleus, implicating that nuclei harbor autonomous Ca2+ machineries (Bunney et al. 2000).
In legumes, Nod factor-mediated perinuclear oscillations of Ca2+ that occur 10-30 minutes after the initial Ca2+ rise in the cytosol (Ehrhardt et al. 1996; Felle et al. 1999), are mediated by the proteins CASTOR and POLLUX, which resemble bacterial potassium channels. However, the exact function of these proteins has remained unclear (Charpentier et al. 2008).
5.2 Calcium Regulation by the ER
Especially due to its large surface within the cell the ER is likely to represent an important intracellular Ca2+ store. The ER contains different types of Ca2+ channels and transporters, to regulate cytoplasmic and luminal Ca2+ levels. However, no ER-localized Ca2+ channel from plants has been identified at the molecular level and our understanding of the contribution of the ER to cellular dynamics of Ca2+ is much less advanced than in animal systems. Considering the absence of channels that exhibit recognizable similarity to animal InsP3 and Ryanodine-receptors in plants (with the exception of Chlamydomonas and Volvox (Wheeler and Brownlee 2008)) the interconnection of the ER with the cellular Ca2+ homeostasis in plants may be fundamentally different than in animals cells.
The ER is loosely associated with the mitotic apparatus, and Ca2+ levels regulated by the ER could be therefore important to control cell division (Hepler 2005). Within the lumen of the ER, calcium is important for the maturation of proteins (Bush et al. 1989b). Ca2+ concentration within the lumen of the ER is tightly controlled by Calreticulin (CRT), a high capacity calcium binding protein (25 calcium ions/protein) (Persson et al. 2001). Overexpression or reducing the expression either enhances resistance to Ca2+ depletion or leads to increased sensitivity to low Ca2+, respectively (Persson et al. 2001). Moreover, increasing the Ca2+ buffer capacity by overexpressing CRT also enhances the stimulus induced Ca2+ release from the ER (Persson et al. 2001).
5.3 Mitochondrial Calcium Dynamics
Mitochondria have to retain high concentrations of Ca2+ to maintain the activity of enzymes like the NADH dehydrogenase (Moore and Åkerman 1984). Moreover, mitochondria are able to take up enormous amounts of Ca2+ from the cytosol (Dieter and Marme 1980). The resting concentration of Ca2+ in mitochondria has been estimated to be around 200 nM (Subbaiah et al. 1998; Logan and Knight 2003), and the mitochondrial Ca2+ content increases dramatically in response to cytoplasmic Ca2+ rises (Logan and Knight 2003). Therefore, mitochondria represent important cellular Ca2+ sinks that can contribute to the reduction of cytosolic Ca2+ levels after a stimulus induced elevation of cytoplasmic Ca2+ concentration (Bygrave 1978; Dieter and Marme 1980, 1983).
In addition, specific stimuli like touch or hydrogen peroxide induce a transient increase of mitochondrial Ca2+ concentration that was suggested to occur independently of the cytosolic rise of Ca2+, pointing to a semi-autonomous mitochondrial calcium signaling pathway (Logan and Knight 2003). Moreover, mitochondria can also contribute to the cytosolic rise of Ca2+ by release of Ca2+ during anoxic conditions (Subbaiah et al. 1998).
5.4 The Role of Chloroplasts in Cellular Calcium Homeostasis
Chloroplasts can accumulate Ca2+ in the millimolar range and thereby can contribute to the cellular Ca2+ homeostasis (Portis and Heldt 1976). The level of Ca2+ in chloroplasts can rise upon illumination by light (Moore and Åkerman 1984; Miller and Sanders 1987; Kreimer et al. 1988) or after dark transition (Sai and Johnson 2002), and can follow a circadian rhythm (Johnson et al. 1995), but does not respond to mechanical stress or cold (van Der Luit et al. 1999). Within the chloroplast, Ca2+ is required for the electron flow at photosystem II (Kauss 1987), stabilizes the high redox potential form of cytochrome b-559 (McNamara and Gounaris 1995) and is an important co-factor and activity-regulator of enzymes like NAD kinase (Moore and Åkerman 1984). Indeed, the differential distribution of Ca2+ and Mg2+ between the stroma and thylakoid lumen during the dark and light phase has been shown to contribute to the regulation of the “on-off” state of chloroplasts (Ettinger et al. 1999).
A direct influence of the chloroplast on the cytoplasmic Ca2+ dynamics was revealed by the analysis of the Ca2+ -binding protein CAS (Ca2+ sensing receptor) (Han et al. 2003; Nomura et al. 2008; Weinl et al. 2008). CAS has originally been reported as an extracellular Ca2+-sensing receptor, exhibting a high capacity to bind calcium (10–12 calcium ions per molecule) (Han et al. 2003). However, several studies revealed that the protein is exlusively localized in chloroplasts (Nomura et al. 2008; Vainonen et al. 2008; Weinl et al. 2008). Within the chloroplast, CAS is targeted to the thylakoid membrane, and is light-dependent phosphorylated (Vainonen et al. 2008; Weinl et al. 2008). CAS knock-out plants exhibit retarded growth, however, activity of the photosystem is not affected in these plants (Vainonen et al. 2008). When grown under low Ca2+ conditions, CAS knock-down plants display delayed bolting and are not able to induce flowering (Han et al. 2003). Ca2+-induced cytoplasmic Ca2+ release is impaired in CAS knock-down and knock-out plants and these lines are impaired in Ca2+-induced stomatal closure responses (Han et al. 2003; Nomura et al. 2008; Weinl et al. 2008). However, CAS knock-out plants can respond to externally imposed Ca2+ oscillations and then display normal stomatal closure reactions, indicating that the ability to respond to cytoplasmic Ca2+ elevations in mutant plants is not affected. This points to a function of CAS in the generation of cytoplasmic Ca2+ transients that are required for stomatal closure (Weinl et al. 2008) and indicates that the chloroplast targeted Ca2+ sensor protein CAS somehow connects cytoplasmic and chloroplast Ca2+ dynamics. This function somewhat resembles that of the Ca2+ buffer protein CRT in the ER. Similarly, loss of CAS could lead to a reduced buffer capacity of the chloroplasts, implicating that less Ca2+ can be allocated from the chloroplasts to the transient cytoplasmic increase of Ca2+. These recent findings surprisingly highlighted the interconnection and importance of chloroplasts for the cellular Ca2+ machinery.
6 Channels and Transporters shaping Ca2+ Signals
6.1 Influx of Ca2+
Several different Ca2+ permeable channel activities were reported to exist at the plasma membrane of plants that can mediate the influx of Ca2+ into the cytosol and have the potential to modulate the cellular Ca2+ signature depending on their specific activation properties (White et al. 2002; Demidchik and Maathuis 2007). In general, Ca2+ permeable channels can be classified as voltage dependent and voltage independent/ligand dependent channels (White et al. 2002). Additionally, stretch activated calcium channels exist at the plasma membrane (Cosgrove and Hedrich 1991; Dutta and Robinson 2004; Nakagawa et al. 2007). These different channel types can co-exist in certain cell types, allowing the cells to respond to a wide range of signals and to differentiate between nutrient and signaling requirements (Miedema et al. 2001; Miedema et al. 2008). Variability in the specific abundance of the different channel types could contribute to the specific needs of a cell type or tissue (Demidchik et al. 2002). However, it should be noted that the molecular identification and characterization of true Ca2+ – specific channels from plants has still not been reported.
6.1.1 Voltage Dependent Channels
Voltage dependent channels are separated in to depolarization activated Ca2+ permeable channels (DACCs) and hyperpolarization activated Ca2+ permeable channels (HACCs) (White et al. 2002). Depolarization activated channels contribute to the short transient influx of Ca2+ during signal responses, since they enter a quiescent state at constant depolarized membrane voltage (Thion et al. 1998). Hyperpolarization activated channels exhibit a large Ca2+ conductance and could contribute to a sustained Ca2+ influx regulating signaling and nutrition in fast growing tissues or cell types (Miedema et al. 2001, 2008), but are inactivated by increased levels of intracellular Ca2+ (Hamilton et al. 2000). Consequently, both channel types could function interdependently. Hyperpolarization of the membrane could activate HAC channels. Influx of Ca2+ would inhibit HACC activity and depolarize the membrane which then would activate DAC channels (Hamilton et al. 2000; Miedema et al. 2001). In addition, voltage dependent K+ channels could also contribute to the influx of Ca2+ (Fairley-Grenot and Assmann 1992; Wegner and De Boer 1997; White et al. 2002).
Plant annexins are small proteins capable of Ca2+-dependent membrane binding and insertion and appear to create Ca2+ influx pathways especially during stress responses involving acidosis (Mortimer et al. 2008). Some annexins were recently shown to assemble into Ca2+-permeable channels in the plasma membrane and endomembranes of plant cells, which could be activated by Ca2+, hyperpolarization and ROS (Demidchik and Maathuis 2007; Mortimer et al. 2008). In addition, annexins from Zea mays were reported to create Ca2+ permeable transport pathways and to regulate cytoplasmic Ca2+ concentration (Laohavisit et al. 2009).
6.1.2 Ligand Gated Channels
While the molecular identity of voltage dependent channels is still of uncertainty, ligand gated channels are nonselective cation channels represented by Cyclic nucleotide gated channels (CNGCs) and Glutamate receptors, which are important for ion homeostasis of Ca2+ and different other cations like K+, Na+ and others (Hua et al. 2003a; Ali et al. 2006). Individual CNGCs harbor different selectivity filters, indicating that certain CNGCs exhibit distinct selectivity for cations (Kaplan et al. 2007). Indeed, tobacco plants overexpressing a CNGC gene were hypersensitive to Pb2+, while Arabidopsis plants harboring a T-DNA insertion within the respective CNGC1 gene were more tolerant to Pb2+ (Arazi et al. 1999; Sunkar et al. 2000). In Arabidopsis 20 CNGC were identified which are expressed in different tissues of the plant (White et al. 2002). In general, CNGCs are activated by cAMP and cGMP and harbor a binding site for Calmodulin which partially overlaps with the binding domain for cNMPs. Therefore, binding of Ca2+/Calmodulin results in inactivation of CNGCs, due to blocking of the cNMP binding domain (Hua et al. 2003b; Ali et al. 2006). Moreover, for CNGC2 it was also suggested that the channel is blocked by high external Ca2+ concentrations (Hua et al. 2003a). CNGC2 was originally identified as the “defence no death” (dnd) 1 mutant, which fails to induce the Ca2+ mediated hypersensitive response to an avirulent strain of the pathogen Pseudomonas syringae and exhibits enhanced resistance to pathogens (Yu et al. 1998; Clough et al. 2000). Interestingly, mutants of CNGC2 are specifically hypersensitive to external Ca2+, but have a normal Ca2+ content. Therefore, it was suggested that CNGC2 contributes to calcium signaling (Chan et al. 2003). In addition to CNGC2, CNGC4 (Balague et al. 2003), CNGC11 and CNGC12 (Yoshioka et al. 2006; Urquhart et al. 2007) were also implicated in mediating pathogen responses, while CNGC18 mediates tip growth of pollen (Frietsch et al. 2007).
Similar to CNGCs, Glutamate receptors (GLR) are also non-selective cation channels and 20 genes encoding GLRs were identified in Arabidopsis (White et al. 2002). GLRs are activated by Glutamate and Glycine as well as by other amino acids and mediate increases of cytosolic Ca2+ concentration (Qi et al. 2006). It is assumed that GLRs are important for plant Ca2+ nutrition (Demidchik and Maathuis 2007) but also have a role in calcium dependent photomorphogenesis. Application of GLR antagonists impaired plant light-signal transduction and resulted in enlarged hypocotyls and reduced chlorophyll accumulation (Lam et al. 1998; Brenner et al. 2000).
6.1.3 Vacuolar and ER Ca2+ Channels
Electrophysiological analyzes of the vacuolar membrane identified currents that are indicative for the function of voltage dependent channels and ligand gated channels. Among these, the “Two-pore channel” 1 (TPC1) appears to encode the depolarization activated slow vacuolar (SV) channel of the tonoplast (Hedrich and Neher 1987; Peiter et al. 2005). Plants lacking TPC1 are deficient in SV channel activity (Peiter et al. 2005). Remarkably, although the SV channel is the most abundant vacuolar channel, loss of SV channel function does not or only marginally impair calcium signaling events mediated by ABA or different biotic and abiotic factors which partially rely on influx of Ca2+ from intracellular stores (Peiter et al. 2005; Ranf et al. 2008). These observations suggest that SV-channels contribute only modestly to the modulation of cytoplasmic Ca2+ concentration by Ca2+ influx from the vacuole (Perez et al. 2008). Therefore, the exact functional role of TPC1 is still uncertain (Pottosin and Schonknecht 2007). Moreover, it needs to be considered that further not well characterized voltage dependent channels, that have been described as a fast vacuolar channel (FV) (Hedrich and Neher 1987) and as a Ca2+ insensitive vacuolar channel (CIVC) (Ranf et al. 2008), are likely to contribute to Ca2+ fluxes across the vacuolar membrane (Allen and Sanders 1994).
The identity and characterization of plant vacuolar ligand-gated Ca2+ channels is even less advanced than that of ligand-gated channels from the plasma membrane. By applying either caged compounds, or by direct patch clamp techniques, it was revealed that InsP3/InsP6 and cADPR mediated Ca2+ release, suggesting the existence of ligand-gated channels (Schumaker and Sze 1987; Alexandre 1990; Gilroy et al. 1990; Allen et al. 1995; Lemtiri-Chlieh et al. 2003). However, considering the paucity of molecular data confirming the existence of such channels, it remains possible that these compounds may indirectly activate channels by binding to receptors which subsequently activate voltage dependent channels like SV and FV channels (Lemtiri-Chlieh et al. 2003).
Similarly, it was also suggested that the ER contributes to InsP3/InsP6 and cADPR mediated Ca2+ release (Muir and Sanders 1997; Martinec et al. 2000; Navazio et al. 2001). Besides these two types of channels, a unique ligand gated channel appears to exist at the ER which is activated by NAADP (Navazio et al. 2000).
6.2 Efflux of Calcium
After release of Ca2+ into the cytosol, Ca2+ is actively transported out of the cytoplasma against the electro-chemical gradient to restore the normal cytoplasmic Ca2+ level. This finally leads to the observed Ca2+ transient and it should be emphasized that a tight regulation of Ca2+ efflux is as equally important for Ca2+ signaling as the more intensively studied influx mechanisms.
Extrusion of calcium is achieved by P-type calcium-ATPases and by Ca2+/H+ antiporter systems. While pumps mediate high-affinity low-turnover Ca2+ export, antiporter provoke low-affinity high-capacity export. Therefore, antiporter reduce the Ca2+ cytoplasmic level to a few micromolar after signal mediated influx of Ca2+, while calcium-ATPases further lessen the cytoplasmic Ca2+ concentration to the resting level and maintain the Ca2+ homeostasis (Bush 1993; Hirschi 1999).
Ca2+ efflux transport activity appears to be coordinatively regulated with the influx of Ca2+ and specific regulation in response to defined stimuli has been reported (Bush et al. 1993; Gao et al. 2004). However, the underlying principles of Ca2+ efflux regulation are still poorly understood. Specific hormones can differentially activate the transporter systems of the ER or tonoplast. After a Ca2+ transient, Ca2+ released by GA seems to be mainly transported out of the cytoplasma via the ER transporters. In contrast, ABA activates transport activity at the ER and the tonoplast (Bush et al. 1993).
6.2.1 Calcium-Proton Antiporter
In the Arabidopsis genome 6 genes encode for putative Ca2+/H+ antiporters, designated as cation exchangers (CAX) (Maser et al. 2001; Shigaki et al. 2006) that contribute to the regulation of Ca2+ (Catala et al. 2003; Cheng et al. 2003; Zhao et al. 2008). In addition, five cation calcium exchanger (CCX) proteins (also termed CAX7-11), related to K+ dependent Na+/Ca2+ antiporters are encoded in the Arabidopsis genome (Shigaki et al. 2006). Moreover, four putative antiporters are encoded in the genome of Arabidopsis, which exhibit EF hand Ca2+ binding motifs suggesting that they are directly regulated by Ca2+ (Shigaki et al. 2006).
CAX proteins harbor a N-terminal regulatory/autoinhibitory domain, which binds to an adjacent region within the N-terminus (Pittman et al. 2002a; Mei et al. 2007). It has been observed that individual CAX proteins can have different transport capacities, metal selectivity and transcriptional regulation (Hirschi et al. 2000; Pittman et al. 2002b). Although individual CAX proteins can function specifically in distinct responses to definite stimuli (Zhao et al. 2008), CAX1 and CAX3 could also form functional heteromers (Cheng et al. 2005; Zhao et al. 2009). Additionally, different regulatory proteins could interact with CAX proteins to modulate their transport activity (Cheng and Hirschi 2003; Cheng et al. 2004a, b). CAX1-CAX4 are localized to the vacuole (Hirschi et al. 2000; Cheng et al. 2002a, 2003, 2005), but anti-porter activity was also reported to reside at the plasma membrane (Kasai and Muto 1990; Luo et al. 2005).
Several attempts were performed to change the cellular calcium levels of plants by overexpressing CAX proteins, either to improve plant tolerance against various stress regimes or to improve the availability of calcium for human nutrition. Overexpression of the truncated version (lacking the regulatory domain) of the vacuolar antiporter CAX1 from Arabidopsis in tobacco leads to an altered Ca2+ homeostasis. Although plants contained more total Ca2+, plants showed Ca2+ deficiency symptoms. In accordance with this, plants also displayed hypersensitivity to Mg2+, Na+ and to cold shock (Hirschi 1999). It was discussed that overexpression of AtCAX1 resulted in over-accumulation of Ca2+ in the vacuole and, therefore, by simultaneous reduction of the cytoplasmic Ca2+ concentration caused the deficiency symptoms.
6.2.2 Phosphorylated-type ATPases
Classical Ca2+ P-ATPases belong to the second subclass (II) of Phosphorylated(P)-type ATPases. Two different types of PII ATPases are found in plants. PIIB ATPases contain an autoinhibtory N-terminal region (autoinhibited calcium ATPases, ACAs; 10 members), which is absent in PIIA type proteins (ER type calcium ATPases, ECA, 4 members) (Sze et al. 2000). The autoinhibitory domain in PIIB type proteins can be relieved by the binding of Calmodulin, which results in activation of the pump (Harper et al. 1998). On the other hand, the activity of the PIIB type Ca2+-ATPase ACA2, is inhibited by phosphorylation within the N-terminal regulatory domain. Interestingly, this regulatory function is mediated by an another Ca2+ binding protein, a CDPK (Hwang et al. 2000). PIIA type ATPases are found at the ER (ECA1) (Liang et al. 1997), the Golgi (ECA3) (Mills et al. 2008) and endosomes (also ECA 3) (Li et al. 2008). Besides being Ca2+ transporters, ECAs are also important for regulating the Mn2+ homeostasis of plants, transporting excess Mn2+ out of the cytoplasm (Wu et al. 2002; Li et al. 2008; Mills et al. 2008). The existence of ECAs at the Golgi and/or Endosomes could also be important for exocytotic processes as, for example, the vacuolar sorting receptor PV72 interacts with target proteins in a Ca2+ dependent manner (Shimada et al. 2002; Watanabe et al. 2002).
PIIB type ATPases are found at the ER (ACA2) (Harper et al. 1998), the vacuole (ACA4, ACA11) (Geisler et al. 2000; Lee et al. 2007), the plasma membrane (ACA8, ACA9, ACA10) (Bonza et al. 2000; Schiott et al. 2004; George et al. 2008) and also at the plastid envelope (ACA1) (Huang et al. 1993). Transcript levels of ACAs are stress regulated (Carena et al. 2006). The importance of a PIIa type Ca2+-ATPase activity in regulating the cytoplasmic Ca2+ level is exemplified by an analysis of a Ca2+-ATPase loss-of-function mutant in the moss Physcomitrella patens. While wildtype plants exhibit a transient Ca2+ release after applying Na+ stress, loss of function mutant lines exhibit a sustained elevation of Ca2+ (Qudeimat et al. 2008). Interestingly, the sustained increase of Ca2+ concentration impaired the expression of salt stress-induced genes and rendered mutant plants less tolerant to Na+ stress (Qudeimat et al. 2008), implicating a direct causal relation between the proper formation of a Ca2+ signature and stress tolerance. In Arabidopsis, analyses of loss-of-function mutations of ACA9 and ACA10 implicate these pumps in specific functions, like in pollen tube growth and in inflorescence development of plants, respectively (Schiott et al. 2004; George et al. 2008)
Moreover, several PI type proteins, which are mainly heavy metal transporters are also implicated in Ca2+ transport. AtHMA1 (heavy metal ATPase), a heavy metal transporter supposed to function in detoxification processes for heavy metals is a PI-ATPase that localizes to the chloroplast envelope. In addition to heavy metals like Cu2+, AtHMA1 transports Ca2+ with high affinity and is specifically inhibited by thapsigargin like SERCA (sarcoplasmic/endoplasmic reticulum Ca2+ATPase)-pumps from animals (Seigneurin-Berny et al. 2006; Moreno et al. 2008).
7 Signal Response Coupling of Calcium
Diverse stimuli specifically induce changes in cellular and apoplastic Ca2+ concentration (Cessna et al. 1998; Pauly et al. 2001; Lecourieux et al. 2002, 2005; Rentel and Knight 2004; Kosuta et al. 2008). The specific signatures of such Ca2+ transients can be unique to a defined cue but different stimuli can also induce similar Ca2+ responses. Typical examples of such Ca2+ signature are presented in Fig. 1c, and below we discuss only selected representative instances to illustrate this facet of Ca2+ signaling.
7.1 Differences in Salt and Mannitol Responses
Several reports showed that specific Ca2+ transients can be detected after salt or drought stress (imposed by mannitol application) in different cell types of the root, which, however, exhibited similar response signatures (Knight et al. 1997; Kiegle et al. 2000). Therefore, the existence of a Ca2+ independent factor was suggested that would allow to discriminate between the Ca2+ signatures evoked by drought and salt stress (Knight et al. 1997). In contrast, aleurone cells of barley responded differentially to either mannitol or sodium, leading to decrease and increase of cytosolic Ca2+, respectively (Bush 1996). A detailed study by Gao et al. (2004) addressing the interconnection of cytoplasmic and apoplastic dynamics of Ca2+concentration in roots of Arabidopsis provides new insights how Ca2+ could function as a specific signal in these different stress responses (Gao et al. 2004). Here, the Ca2+ elevation within the cytosol was simultaneously recorded to the changes of apoplastic Ca2+. The response to mannitol resulted only in a minor transient cytoplasmic Ca2+ elevation. In contrast, sodium stress resulted in a transient cytoplasmic Ca2+ spike which was more pronounced than after mannitol application (Pauly et al. 2001; Gao et al. 2004). However, after this initial spike a slow but constant rise of cytoplasmic Ca2+ concentration was observed (see Fig. 1c) (Gao et al. 2004). Additionally, apoplastic Ca2+ elevation was also observed under sodium stress (Gao et al. 2004), which could result from enhanced exocytosis (Homann and Tester 1997; Belan et al. 1998). As sodium ions can exchange Ca2+ from the membrane or from cell wall components this apoplastic rise in Ca2+ concentration may contribute to membrane protection (Williams 1970; Hauser et al. 1976; Brett and Waldron 1996). An apoplastic calcium rise was not observed under drought stress, most likely since mannitol does not exchange calcium from membrane and cell wall components (Gao et al. 2004).
7.2 Differences in Symbiotic Calcium Responses
Symbiotic plants can interact with nitrogen-fixing rhizobial bacteria or with arbuscular mycorrhizal fungi that aid nutrient uptake of the plant. Although both signals (Nod factor, or mycorrhizal factors) require the same machinery for Ca2+ signaling, the outcome is quite different. While Nod factors induce nodulation, interaction with symbiotic fungi does not induce nodulation (Kosuta et al. 2008). Although both factors induce Ca2+ oscillations, their signatures are remarkably different. Initial, Ca2+ spiking triggered by Nod factor perception induces a subsequent large rise of cytoplasmic Ca2+ in regard of duration and amplitude. After a descent of cytoplasmic Ca2+ to basal levels, immediate and recurrent increases of calcium occur which finally result in repetitive and periodic spiking. This is in contrast to the oscillations induced by the mycorrhizal factor. Here, the transient is shorter and lower in amplitude (only 17% of the Nod factor spike). After the drop to basal level, there is a gap of different length of low Ca2+ before the next spike is recorded which can differ in duration and amplitude from the previous spike (see Fig. 1c) (Kosuta et al. 2008). These differences could result in the different observed symbiotic outcomes.
8 Calcium Binding Proteins
Different classes of Ca2+ binding proteins represent the cellular “currency” to translate Ca2+ signals into defined downstream response reactions. Here we will focus on three main classes of Ca2+ binding proteins, which all harbor EF hands for Ca2+ binding. These are the Calmodulins (CaMs) and their related Calmodulin like proteins (CMLs), the Calcium-dependent protein kinases (CDPKs) and the calcineurin-B like (CBL) proteins which form a network with CBL-interacting protein kinases (CIPKs).
8.1 Calmodulin
Calmodulins are small proteins of about 148 amino acids, composed of four Ca2+-binding EF hands which are arranged in a dumbbell structure in that EF hands 1/2 and 3/4 are separated by a alpha-helical handle (Strynadka and James 1989). Upon Ca2+ binding, CaMs undergo a structural change, from a closed to an open conformation which enables binding to target proteins (Chin and Means 2000).
In Arabidopsis, 7 genes encode for only 4 Calmodulin isoforms because 3 Calmodulins share an identical amino acid sequence (CaMs 2, 3 and 5) (McCormack et al. 2005). Additionally, Arabidopsis contains 50 CaM-like proteins, which harbor variable numbers (between 2 and 6) of EF hands that could account for different Ca2+ binding affinities (McCormack and Braam 2003).
CaMs are generally cytoplasmic proteins, which can translocate into the nucleus or to cellular membranes upon binding to different target proteins (Deisseroth et al. 1998; Chung et al. 2000). Additionally, Ca2+ binding proteins related to Calmodulin can be secreted into the apoplastic space, potentially regulating cell wall regeneration (Sun et al. 1995) and the growth of pollen by affecting activity of hyperpolarization activated channels (Ma et al. 1999; Shang et al. 2005). CML18 has been reported to localize within the vacuole here regulating the function of the Na+/H+ antiporter NHX1 (Yamaguchi et al. 2005).
About 170 different target proteins of CaMs were identified up to now (Jun et al. 1996; Reddy et al. 2002; Yang and Poovaiah 2003; Popescu et al. 2007). CaMs/CMLs are important regulators of metabolism, cell structure proteins, proteins of the phyotohormone signal network, ion transporters, heat shock proteins and proteins regulating translation and transcription (Reddy et al. 2002; Du and Poovaiah 2005; Popescu et al. 2007; Du et al. 2009). CaM or CMLs are directly implicated in fine tuning the hypersensitivity response after pathogen infection. While NO production is mediated by CaMs or CMLs, like CML24 (Ma et al. 2008), the channel which is important for Ca2+ release, which then results in NO production, is also inhibited by CaMs (Ali et al. 2007). This could be important to prevent excess accumulation of Ca2+, and would lead to the observed transient increase of Ca2+. CaMs are also supposed to have an important role during photomorphogenesis (Neuhaus et al. 1993) and a specific function in light dependent development of seedlings was assessed for CaM7 that can act as a transcriptional regulator by binding to Z- and G-box light responsive promoter elements (Kushwaha et al. 2008).
Different mechanisms contribute to the specificity of responses mediated by individual CaMs and CMLs. In the tobacco plant Nicotiana plumbaginifolia, individual CaMs are differentially transcriptionally regulated. While NpCaM1 is upregulated by wind and cold, the expression of NpCaM2 is unaffected (van Der Luit et al. 1999). In Arabidopsis, one CaM and different CMLs are induced by touch (Braam et al. 1997). Additionally, CML expression can be tissue specific and can be modulated by stress, hormones and light (McCormack et al. 2005; Magnan et al. 2008). Post-transcriptional regulation of protein stability by methylation or phosphorylation could also play an important role (Oh and Roberts 1990; Leclerc et al. 1999; Kushwaha et al. 2008). An additional layer of functional diversification results from differential target protein regulation by CaM/CMLs (Lee et al. 2000; Popescu et al. 2007). Remarkably, it has been reported that targets can be activated by one CaM/CML and reciprocally inactivated by another CaM/CML (Lee et al. 1997; Leclerc et al. 1999; Kushwaha et al. 2008).
8.2 CDPKs
Calcium dependent protein kinases (CDPKs) evolutionary arose by fusion of a N-terminal serine/threonine kinase with a C-terminal Calmodulin EF hand Ca2+ binding domain, separated by an autoinhibitory junction domain. Classical CDPKs contain four EF hands, while “CDPK-related kinases” (CRKs) harbor three or less functional EF hands (Harper et al. 2004).
The junction domain functions as a pseudosubstrate. When no Ca2+ is bound to the Calmodulin domain, the junction domain interacts with the kinase domain and blocks phosphorylation of target proteins. Upon Ca2+ binding, the Calmodulin domain binds the junction domain displacing it from the kinase domain and thereby leading to activation of the kinase (Hrabak et al. 2003).
In Arabidopsis 34 CDPKs are encoded in the genome. All CDPKs harbor a N-terminal “variable domain” upstream of the kinase domain, which can differ in sequence and length (Cheng et al. 2002b). The “variable domain” can determine CDPK localization and can represent a docking site for regulatory 14-3-3 proteins (Lu and Hrabak 2002). CDPKs are differentially localized, and have been found to reside in the cytoplasma and nucleoplasma, but are also associated with the cytoskeleton, plasma membrane, ER or peroxisomes (Putnam-Evans et al. 1989; Martin and Busconi 2000; Lu and Hrabak 2002; Dammann et al. 2003; Choi et al. 2005).
Regulation of CDPK kinase activity is achieved by a complex interplay of membrane translocation, phosho-lipid binding and auto- as well as trans-phosphorylation (Schaller et al. 1992; Farmer and Choi 1999; Szczegielniak et al. 2000, 2005). Some CDPKs are transcriptionally regulated (Hrabak et al. 2003) and could be regulated by their protein stability (Satterlee and Sussman 1998; Zhu et al. 2007). Since each CDPKs display distinct composition of various EF hands with different affinities to calcium, differential activation of CDPKs depending on the respective cellular Ca2+ concentration may occur. Certain CDPKs display a very low activation requirement suggesting that these kinases are already constitutively active at resting cytoplasmic Ca2+ levels (Lee et al. 1998).
Functional analysis of two CDPKs from Arabidopsis that are strongly expressed in guard cells (CPK3 and CPK6), revealed that loss-of-function mutants of CPK3 and/or CPK6 are impaired in Ca2+ and ABA-dependent activation of S-type anion channels (Schroeder and Hagiwara 1989; Mori et al. 2006) and in the ABA-dependent activation of Ca2+ channels (Hamilton et al. 2000; Pei et al. 2000; Mori et al. 2006). Consequently, these mutant plants exhibited reduced stomatal closure after application of ABA or after artificially imposing Ca2+ oscillations (Mori et al. 2006). However, long term stomatal closure in these mutants as well as ABA-mediated inhibition of seed germination were not affected, implicating that CPK3/CPK6 are specifically regulating the rapid stomatal closure (Mori et al. 2006). In contrast, loss of function of CPK4/CPK11, two highly related cytoplasmic/nucleoplasmic localized CDPKs, reduces the sensitivity of mutant plants to ABA in seedling germination and growth, and stomatal closure is partially impaired in response to ABA (Zhu et al. 2007). CPK4 and CPK11 interact and phosphorylate ABA-responsive transcription factors ABF1 and ABF4 in the presence of ABA (Uno et al. 2000; Zhu et al. 2007). However, ABFs also interact and are phosphorylated by other CDPKs, implicating further kinases in regulating ABA responses in Arabidopsis (Choi et al. 2005).
Phosphorylation of the transcriptional activator “Repression of shoot growth” (RSG) by CDPK1 from tobacco enables binding of 14-3-3 proteins and represses the function of RSG during GA responses (Ishida et al. 2008). CDPK2 from tobacco is transiently activated by phosphorylation specifically after pathogen infection (Romeis et al. 2000, 2001), and is triggering different stress response pathways within the cell (Ludwig et al. 2005). Furthermore, CDPKs are implicated in root development (Ivashuta et al. 2005), wound response (Szczegielniak et al. 2005), secretion and vacuolar function in response to GA (McCubbin et al. 2004), pollen tube growth and pollen tube polarity (Estruch et al. 1994; Yoon et al. 2006), response to salt, drought stress and potassium homeostasis (Saijo et al. 2000; Ma and Wu 2007). These findings illustrate the functional diversity of CDPKs in various biological processes.
8.3 CBLs and CIPKs
The third class of Ca2+ binding proteins is represented by the group of Calcineurin-B like (CBL) proteins (Kudla et al. 1999; Batistic and Kudla 2004). Similar to CaMs, CBLs contain four EF hands to bind Ca2+ (Nagae et al. 2003; Kolukisaoglu et al. 2004; Sanchez-Barrena et al. 2005), but contain an unconventional first EF hand, which encompasses 14 aminoacids instead of 12 aminoacids typical for a canonical EF hand (Nagae et al. 2003). Nevertheless, this unique EF hand is still able to bind Ca2+ (Nagae et al. 2003; Sanchez-Barrena et al. 2005, 2007), and could play an important role in the selective interaction with CBL-partner proteins. In Arabidopsis 10 genes encode for CBL proteins (Kolukisaoglu et al. 2004). CBL1, CBL4, CBL5 and CBL9 are N-terminal myristoylated proteins (Ishitani et al. 2000; Batistic et al. 2008) that, in addition, harbor further cysteine residues in the vicinity of the myristoylated glycine suggesting further acylation. Indeed, CBL1 has been shown to undergo modification by palmitate or stearate, and together with the myristoyl modification, these lipid modifications are important for correct plasma membrane targeting and function of the CBL1 protein in stress response (Batistic et al. 2008). CBL2, CBL3, CBL6 and CBL10 lack a classical N-myristoylation site. Instead, these proteins harbor an extended N-terminal region that is important for correct sub-cellular targeting of the proteins (Batistic et al. 2009).
CBL proteins interact and regulate the activity of a certain class of protein kinases, designated as CBL-interacting protein kinases (CIPKs) (Shi et al. 1999). In Arabidopsis, 26 genes encode for CIPKs, which belong to the third subgroup of SNF-related protein kinases (SnRK3) (Hrabak et al. 2003; Batistic and Kudla 2009). It has been suggested that binding of CBLs to the CIPKs via the conserved NAF domain of these kinases (Albrecht et al. 2001) relieves autoinhibition of the kinase, which then results in kinase activation and target phosphorylation (Guo et al. 2001b; Fujii and Zhu 2009). Moreover, CIPKs can interact with PP2Cs (Ohta et al. 2003) and crystallization studies implicate that CIPK24 either interacts with CBLs or PP2Cs, excluding the formation of a trimeric complex (Sanchez-Barrena et al. 2007). Therefore, the on-off state of the CIPKs may be regulated by the interaction with CBLs (on state) or type 2C protein phosphatases (off state).
Several mechanisms contribute to generating signaling specificity within the CBL-CIPK network. Preferential complex formation between certain CBLs and CIPKs enable a focused signal transmission of signals from the calcium sensor proteins to the kinases (Albrecht et al. 2001). Additionally, certain pairs of CBL-CIPK complexes are localized at different cellular compartments, and are differentially expressed in different tissues or in response to stresses, thereby enabling spatial and temporal regulation of the network. For example, CBL4 is mainly expressed in roots, while CBL10 is mainly expressed in leaves (Kim et al. 2007). Both calcium sensor proteins can interact with CIPK24, which is expressed in both tissues. However, CBL4/CIPK24 complexes are localized at the plasma membrane while CBL10/CIPK24 complexes accumulate at the tonoplast thereby creating a dual functioning kinase (Fig. 1d). The alternative formation of CBL/CIPK24 complexes may enable simulatenous Ca2+-dependent regulation of Na+ extrusion in the root and Na+ sequestration into the vacuole in the shoot of salt stressed plants (Kim et al. 2007). In general, CBL and CIPK proteins are critical for controlling the response to different stress situations like salt and osmotic stress (Albrecht et al. 2003; Cheong et al. 2003; D’Angelo et al. 2006; Tripathi et al. 2009), response to and regulation of ABA synthesis (Kim et al. 2003; Pandey et al. 2004), nitrate homeostasis (Hu et al. 2009) root development (Tripathi et al. 2009) and stomatal movement (Cheong et al. 2007). CIPK11 negatively regulates the plasma membrane Arabidopsis H+-ATPase 2 (AHA2), which mediates hyperpolarization of the plasma membrane (Fuglsang et al. 2007). CBL4 together with its interacting protein kinase CIPK24 form the specific “Salt overly sensitive” (SOS) pathway, which regulate the sodium/proton antiporter SOS1 at the plasma membrane (Fig. 1d). During salt stress, calcium influx is detected by CBL4, which activates CIPK24 and subsequently activates SOS1, to extrude excess sodium out of the cell (Halfter et al. 2000; Qiu et al. 2002; Quintero et al. 2002). CBL1 and CBL9 target CIPK23 to the plasma membrane to activate the potassium channel AKT1 to maintain K+ homeostasis under low potassium conditions (Li et al. 2006; Xu et al. 2006; Cheong et al. 2007) (Fig. 1d). The identification of further targets fo CBL/CIPK complexes currently remains one of the main challenges to further our understanding of this complex signaling network.
9 Conclusions
Beginning in the middle of the last century plant biologists uncovered the crucial nutritional and structural role of Ca2+ for plants. However, in this regard Ca2+ never attracted as much attention as for example K+. It was the surprising notion, that only a tiny fraction of the bio-available calcium, namely the free cytoplasmic Ca2+ pool and its regulated dynamics, modulates a plethora of biological processes that sparked an immense interest in this ion. Consequently, during the following decades of the last century an immense amount of observations accumulated that linked changes in cellular Ca2+ concentration and distribution to the regulation of many diverse processes of plant growth and development.
The extensive involvement of Ca2+ frequently leads to the vexing question: how can one ion specifically control so many events? Current research is beginning to provide answers. Ca2+ regulation in plants involves many facets that can define and adjust responses in both time and space. The unequal distribution of Ca2+ in the cell provides the basis for rapid Ca2+ fluxes and the resulting concentration changes. Influx channels on the plasma membrane and release channels from internal stores provide several ways to generate rapid ion elevations or to create local gradients. The frequency as well as amplitude modulation, provide means of generating signals that have unique properties. Once these signals are generated, then a wide variety of Ca2+-decoding components interpret and relay these signals. Complex signaling networks, prominently involving CDPKs and CIPKs translate this information into phosphorylation events thereby simultaneously amplifying and specifying response reactions. It is an emerging picture that plants possess myriad ways in which Ca2+ can operate as the intermediary in transducing stimuli into the appropriate responses. The challenge for the near future lies in characterizing the underlying functional principles of signal response coupling and in identifying the prime targets of Ca2+ regulated phosphorylation events.
References
Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20:1051–1063
Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu U, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470
Alexandre J (1990) Opening of Ca2+ channels in isolated red beet root vacuole membrane by inositol 1, 4, 5-trisphosphate. Nature 343:567–570
Ali R, Zielinski RE, Berkowitz GA (2006) Expression of plant cyclic nucleotide-gated cation channels in yeast. J Exp Bot 57:125–138
Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA (2007) Death don’t have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19:1081–1095
Allen GJ, Sanders D (1994) Two Voltage-Gated, Calcium Release Channels Coreside in the Vacuolar Membrane of Broad Bean Guard Cells. Plant Cell 6:685–694
Allen GJ, Muir SR, Sanders D (1995) Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science 268:735–737
Allen GJ, Kwak JM, Chu SP, Llopis J, Tsien RY, Harper JF, Schroeder JI (1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J 19:735–747
Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342
Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057
Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J 20:171–182
Atkinson MM, Keppler LD, Orlandi EW, Baker CJ, Mischke CF (1990) Involvement of Plasma Membrane Calcium Influx in Bacterial Induction of the K/H and Hypersensitive Responses in Tobacco. Plant Physiol 92:215–221
Balague C, Lin B, Alcon C, Flottes G, Malmstrom S, Kohler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365–379
Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924
Batistic O, Kudla J (2009) Plant calcineurin B-like proteins and their interacting protein kinases. Biochim Biophys Acta 1793:985–992
Batistic O, Sorek N, Schultke S, Yalovsky S, Kudla J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20:1346–1362
Batistic O, Waadt R, Steinhorst L, Held K, Kudla J (2009) CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J, doi: 10.1111/j.1365-1313X.2009.04045.x
Baum G, Long JC, Jenkins GI, Trewavas AJ (1999) Stimulation of the blue light phototropic receptor NPH1 causes a transient increase in cytosolic Ca2+. Proc Natl Acad Sci USA 96:13554–13559
Belan P, Gardner J, Gerasimenko O, Gerasimenko J, Mills CL, Petersen OH, Tepikin AV (1998) Isoproterenol evokes extracellular Ca2+ spikes due to secretory events in salivary gland cells. J Biol Chem 273:4106–4111
Berridge MJ (2006) Calcium microdomains: organization and function. Cell Calcium 40:405–412
Bhalla A, Chicka MC, Tucker WC, Chapman ER (2006) Ca2+-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat Struct Mol Biol 13:323–330
Blume B, Nurnberger T, Nass N, Scheel D (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12:1425–1440
Bonza MC, Morandini P, Luoni L, Geisler M, Palmgren MG, De Michelis MI (2000) At-ACA8 encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiol 123:1495–1506
Braam J, Sistrunk ML, Polisensky DH, Xu W, Purugganan MM, Antosiewicz DM, Campbell P, Johnson KA (1997) Plant responses to environmental stress: regulation and functions of the Arabidopsis TCH genes. Planta 203:S35–S41
Brenner ED, Martinez-Barboza N, Clark AP, Liang QS, Stevenson DW, Coruzzi GM (2000) Arabidopsis mutants resistant to S(+)-beta-methyl-alpha, beta-diaminopropionic acid, a cycad-derived glutamate receptor agonist. Plant Physiol 124:1615–1624
Brett C, Waldron K (1996) Physiology and biochemistry of plant cell walls, second editionth edn. Chapman & Hall, London
Broadley MR, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, Mead A, White PJ (2003) Variation in the shoot calcium content of angiosperms. J Exp Bot 54:1431–1446
Bunney TD, Shaw PJ, Watkins PA, Taylor JP, Beven AF, Wells B, Calder GM, Drobak BK (2000) ATP-dependent regulation of nuclear Ca2+ levels in plant cells. FEBS Lett 476:145–149
Bush DS (1993) Regulation of cytosolic calcium in plants. Plant Physiol 103:7–13
Bush DS (1996) Effects of gibberellic acid and environmental factors on cytosloic calcium in wheat aleurone cells. Planta 199:89–99
Bush DS, Biswas AK, Jones RL (1989a) Gibberellic-acid-stimulated Ca2+ accumulation in endoplasmic reticulum of barley aleurone: Ca2+ transport and steady-state levels. Planta 178:411–420
Bush DS, Sticher L, van Huystee R, Wagner D, Jones RL (1989b) The calcium requirement for stability and enzymatic activity of two isoforms of barley aleurone alpha-amylase. J Biol Chem 264:19392–19398
Bush DS, Biswas AK, Jones RL (1993) Hormonal regulation of Ca2+ transport in the endomembrane system of the barley aleurone. Planta 189:507–515
Bussler W (1962) Die Entwicklung von Calcium-Mangelsymptomen. Z Pflanzenernahr Dung Bodenkde 100:53–58
Bygrave FL (1978) Mitochondria and the control of intracellular calcium. Biol Rev Camb Philos Soc 53:43–79
Carena M, Bonza MC, Harris R, Sanders D, De Michelis MI (2006) Abscisic acid stimulates the expression of two isoforms of plasma membrane Ca2+-ATPase in Arabidopsis thaliana seedlings. Plant Biol 8:572–578
Catala R, Santos E, Alonso JM, Ecker JR, Martinez-Zapater JM, Salinas J (2003) Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940–2951
Cessna SG, Chandra S, Low PS (1998) Hypo-osmotic shock of tobacco cells stimulates Ca2+ fluxes deriving first from external and then internal Ca2+ stores. J Biol Chem 273:27286–27291
Chan CW, Schorrak LM, Smith RK, Bent AF, Sussman MR (2003) A cyclic nucleotide-gated ion channel, CNGC2, is crucial for plant development and adaptation to calcium stress. Plant Physiol 132:728–731
Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M (2008) Lotus japonicus CASTOR and POLLUX Are Ion Channels Essential for Perinuclear Calcium Spiking in Legume Root Endosymbiosis. Plant Cell 20:3467–3479
Chen X, Chang M, Wang B, Wu B (1997) Cloning of a Ca2+-ATPase gene and the role of cytosolic Ca2+ in the gibberellin-dependent signaling pathway in aleurone cells. Plant J 11:363–371
Cheng NH, Hirschi KD (2003) Cloning and characterization of CXIP1, a novel PICOT domain-containing Arabidopsis protein that associates with CAX1. J Biol Chem 278:6503–6509
Cheng NH, Pittman JK, Shigaki T, Hirschi KD (2002a) Characterization of CAX4, an Arabidopsis H+/cation antiporter. Plant Physiol 128:1245–1254
Cheng SH, Willmann MR, Chen HC, Sheen J (2002b) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485
Cheng NH, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347–364
Cheng NH, Liu JZ, Nelson RS, Hirschi KD (2004a) Characterization of CXIP4, a novel Arabidopsis protein that activates the H+/Ca2+ antiporter, CAX1. FEBS Lett 559:99–106
Cheng NH, Pittman JK, Zhu JK, Hirschi KD (2004b) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922–2926
Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138:2048–2060
Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845
Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:223–239
Chin D, Means AR (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10:322–328
Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750–1761
Chung WS, Lee SH, Kim JC, Heo WD, Kim MC, Park CY, Park HC, Lim CO, Kim WB, Harper JF, Cho MJ (2000) Identification of a calmodulin-regulated soybean Ca2+-ATPase (SCA1) that is located in the plasma membrane. Plant Cell 12:1393–1407
Clapham DE (1995) Calcium signaling. Cell 80:259–268
Clayton H, Knight MR, Knight H, McAinsh MR, Hetherington AM (1999) Dissection of the ozone-induced calcium signature. Plant J 17:575–579
Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328
Cosgrove DJ, Hedrich R (1991) Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L. Planta 186:143–153
D’Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schultke S, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J (2006) Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 48:857–872
Dammann C, Ichida A, Hong B, Romanowsky SM, Hrabak EM, Harmon AC, Pickard BG, Harper JF (2003) Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol 132:1840–1848
De Silva DLR, Hetherington AM, Mansfield TA (1996) Where does all the calcium go? Evidence of an important regulatory role for trichomes in two calcicoles. Plant Cell Environ 19:880–886
Deisseroth K, Heist EK, Tsien RW (1998) Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392:198–202
Demarty M, Morvan C, Thellier M (1984) Calcium and the cell wall. Plant Cell Environ 7:441–448
Demidchik V, Maathuis FJ (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404
Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–387
Demidchik V, Bowen HC, Maathuis FJ, Shabala SN, Tester MA, White PJ, Davies JM (2002) Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. Plant J 32:799–808
Demidchik V, Nichols C, Oliynyk M, Dark A, Glover BJ, Davies JM (2003) Is ATP a signaling agent in plants? Plant Physiol 133:456–461
Demidchik V, Shabala SN, Davies JM (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. Plant J 49:377–386
Demidchik V, Shang Z, Shin R, Thompson E, Rubio L, Laohavisit A, Mortimer JC, Chivasa S, Slabas AR, Glover BJ, Schachtman DP, Shabala SN, Davies JM (2009) Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. Plant J 58:903–913
Demuro A, Parker I (2006) Imaging single-channel calcium microdomains. Cell Calcium 40:413–422
Dennison KL, Spalding EP (2000) Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol 124:1511–1514
Dieter P, Marme D (1980) Ca2+ transport in mitochondiral and microsomal fraction from higher plants. Planta 150:1–8
Dieter P, Marmé D (1983) The effect of calmodulin and far-red light on the kinetic properties of the mitochondrial and microsomal calcium-ion transport system from corn. Planta 159:277–281
Digonnet C, Aldon D, Leduc N, Dumas C, Rougier M (1997) First evidence of a calcium transient in flowering plants at fertilization. Development 124:2867–2874
Dodd AN, Love J, Webb AA (2005) The plant clock shows its metal: circadian regulation of cytosolic free Ca2+. Trends Plant Sci 10:15–21
Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J, Assie JM, Robertson FC, Jakobsen MK, Goncalves J, Sanders D, Webb AA (2007) The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318:1789–1792
Du L, Poovaiah BW (2005) Ca2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature 437:741–745
Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy AS, Poovaiah BW (2009) Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–1158
Dutta R, Robinson KR (2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135:1398–1406
Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681
Epstein E (1961) The essential role of calcium in selective cation transport by plant cells. Plant Physiol 36:437–444
Epstein E (1998) How calcium enhances plant salt tolerance. Science 280:1906–1907
Estruch JJ, Kadwell S, Merlin E, Crossland L (1994) Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci USA 91:8837–8841
Etter EF, Minta A, Poenie M, Fay FS (1996) Near-membrane Ca2+ transients resolved using the Ca2+ indicator FFP18. Proc Natl Acad Sci USA 93:5368–5373
Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1386
Fairley-Grenot KA, Assmann SM (1992) Permeation of Ca2+ through K+ channels in the plasma membrane of Vicia faba guard cells. J Membr Biol 128:103–113
Farmer PK, Choi JH (1999) Calcium and phospholipid activation of a recombinant calcium-dependent protein kinase (DcCPK1) from carrot (Daucus carota L.). Biochim Biophys Acta 1434:6–17
Fasano JM, Massa GD, Gilroy S (2002) Ionic signaling in plant responses to gravity and touch. J Plant Growth Regul 21:71–88
Faure JE, Digonnet C, Dumas C (1994) An in Vitro System for Adhesion and Fusion of Maize Gametes. Science 263:1598–1600
Felle H (1988) Auxin causes oscillation of cytosolic free calcium and pH in Zea mays coleoptiles. Planta 174:495–499
Felle HH, Kondorosi E, Kondorosi A, Schultze M (1999) Elevation of the cytosolic free Ca2+ is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiol 121:273–280
Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446
Franklin-Tong VE, Ride JP, Read ND, Trewavas A, Franklin FCH (1993) The self-incompatibiity response in Papaver rhoeas is mediated by cytosolic free calcium. Plant J 4:163–177
Frietsch S, Wang YF, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI, Harper JF (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104:14531–14536
Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG, Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634
Fujii H, Zhu JK (2009) An autophosphorylation site of the protein kinase SOS2 is important for salt tolerance in Arabidopsis. Mol Plant 2:183–190
Gao D, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C (2004) Self-reporting Arabidopsis expressing pH and Ca2+ indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 134:898–908
Gehring CA, Williams DA, Cody SH, Parish RW (1990) Phototropism and geotropism in maize coleoptiles are spatially correlated with increases in cytosolic free calcium. Nature 345:528–530
Geisler M, Frangne N, Gomes E, Martinoia E, Palmgren MG (2000) The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol 124:1814–1827
George L, Romanowsky SM, Harper JF, Sharrock RA (2008) The ACA10 Ca2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol 146:716–728
Gilroy S, Jones RL (1992) Gibberellic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc Natl Acad Sci USA 89:3591–3595
Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346:769–771
Gong M, van der Luit AH, Knight MR, Trewavas AJ (1998) Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116:429–437
Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23:441–450
Guo H, Mockler T, Duong H, Lin C (2001a) SUB1, an Arabidopsis Ca2+-binding protein involved in cryptochrome and phytochrome coaction. Science 291:487–490
Guo Y, Halfter U, Ishitani M, Zhu JK (2001b) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383–1400
Hahm SH, Saunders MJ (1991) Cytokinin increases intracellular Ca2+ in Funaria: detection with Indo-1. Cell Calcium 12:675–681
Haley A, Russell AJ, Wood N, Allan AC, Knight M, Campbell AK, Trewavas AJ (1995) Effects of mechanical signaling on plant cell cytosolic calcium. Proc Natl Acad Sci USA 92:4124–4128
Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740
Hamilton DW, Hills A, Kohler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967–4972
Han S, Tang R, Anderson LK, Woerner TE, Pei ZM (2003) A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature 425:196–200
Harada A, Sakai T, Okada K (2003) Phot1 and phot2 mediate blue light-induced transient increases in cytosolic Ca2+ differently in Arabidopsis leaves. Proc Natl Acad Sci USA 100:8583–8588
Harper JF, Hong B, Hwang I, Guo HQ, Stoddard R, Huang JF, Palmgren MG, Sze H (1998) A novel calmodulin-regulated Ca2+-ATPase (ACA2) from Arabidopsis with an N-terminal autoinhibitory domain. J Biol Chem 273:1099–1106
Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263–288
Hauser H, Levine BA, Williams RJP (1976) Interaction of ions with membranes. Trends Biochem Sci 1:278–281
Hedrich R, Neher E (1987) Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329:833–836
Helms K (1971) Calcium Deficiency of Dark-grown Seedlings of Phaseolus vulgaris L. Plant Physiol 47:799–804
Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155
Hepler PK, Wayne RO (1985) Calcium and plant development. Ann Rev Plant Physiol 36:397–439
Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401–427
Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122
Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442
Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133
Ho LC, White PJ (2005) A cellular hypothesis for the induction of blossom-end rot in tomato fruit. Ann Bot (Lond) 95:571–581
Homann U, Tester M (1997) Ca2+-independent and Ca2+/GTP-binding protein-controlled exocytosis in a plant cell. Proc Natl Acad Sci USA 94:6565–6570
Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680
Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278
Hua BG, Mercier RW, Leng Q, Berkowitz GA (2003a) Plants do it differently. A new basis for potassium/sodium selectivity in the pore of an ion channel. Plant Physiol 132:1353–1361
Hua BG, Mercier RW, Zielinski RE, Berkowitz GA (2003b) Functional interaction of calmodulin with a plant cyclic nucleotide gated cation channel. Plant Physiol Biochem 41:945–954
Huang L, Berkelman T, Franklin AE, Hoffman NE (1993) Characterization of a gene encoding a Ca2+-ATPase-like protein in the plastid envelope. Proc Natl Acad Sci USA 90:10066–10070
Hwang I, Sze H, Harper JF (2000) A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc Natl Acad Sci USA 97:6224–6229
Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA 89:1790–1794
Ishida S, Yuasa T, Nakata M, Takahashi Y (2008) A tobacco Calcium-dependent protein kinase, CDPK1, regulates the transcription factor REPRESSION OF SHOOT GROWTH in response to gibberellins. Plant Cell 20:3273–3288
Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667–1678
Ivashuta S, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17:2911–2921
Jaiswal JK (2001) Calcium - how and why? J Biosci 26:357–363
Jeter CR, Tang W, Henaff E, Butterfield T, Roux SJ (2004) Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis. Plant Cell 16:2652–2664
Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A, Trewavas A (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269:1863–1865
Jun T, Wu S, Bai J, Sun D (1996) Extracellular calmodulin-binding proteins in plants: purification of a 21-kDa calmodulin-binding protein. Planta 198:510–516
Kaplan B, Sherman T, Fromm H (2007) Cyclic nucleotide-gated channels in plants. FEBS Lett 581:2237–2246
Kasai M, Muto S (1990) Ca2+ pump and Ca2+/H+ antiporter in plasma membrane vesicles isolated by aqueous two-phase partitioning from corn leaves. J Membr Biol 114:133–142
Kauss H (1987) Some aspects of Calcium-dependent regulation in plant metabolism. Ann Rev Plant Physiol 38:47–72
Kawano T, Sahashi N, Takahashi K, Uozumi N, Muto S (1998) Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: the earliest events in salicylic acid signal transduction. Plant Cell Physiol 39:721–730
Kesavan J, Borisovska M, Bruns D (2007) v-SNARE actions during Ca2+-triggered exocytosis. Cell 131:351–363
Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23:267–278
Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423
Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, Schultke S, Lee SC, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473–484
Kirkby EA, Pilbeam DJ (1984) Calcium as a plant nutrient. Plant Cell Environ 7:397–405
Klusener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugouvieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130:2152–2163
Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526
Knight H, Trewavas AJ, Knight MR (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12:1067–1078
Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16:681–687
Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol 134:43–58
Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105:9823–9828
Kreimer G, Melkonian M, Holtum JA, Latzko E (1988) Stromal Free Calcium Concentration and Light-Mediated Activation of Chloroplast Fructose-1, 6-Bisphosphatase. Plant Physiol 86:423–428
Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci USA 96:4718–4723
Kushwaha R, Singh A, Chattopadhyay S (2008) Calmodulin7 plays an important role as transcriptional regulator in Arabidopsis seedling development. Plant Cell 20:1747–1759
Lam HM, Chiu J, Hsieh MH, Meisel L, Oliveira IC, Shin M, Coruzzi G (1998) Glutamate-receptor genes in plants. Nature 396:125–126
Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 135:516–529
Laohavisit A, Mortimer JC, Demidchik V, Coxon KM, Stancombe MA, Macpherson N, Brownlee C, Hofmann A, Webb AA, Miedema H, Battey NH, Davies JM (2009) Zea mays Annexins Modulate Cytosolic Free Ca2+ and Generate a Ca2+-Permeable Conductance. Plant Cell 21:479–493
Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695
Leckie CP, McAinsh MR, Allen GJ, Sanders D, Hetherington AM (1998) Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc Natl Acad Sci USA 95:15837–15842
Leclerc E, Corti C, Schmid H, Vetter S, James P, Carafoli E (1999) Serine/threonine phosphorylation of calmodulin modulates its interaction with the binding domains of target enzymes. Biochem J 344(Pt 2):403–411
Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14:2627–2641
Lecourieux D, Lamotte O, Bourque S, Wendehenne D, Mazars C, Ranjeva R, Pugin A (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38:527–538
Lee JS, Mulkey TJ, Evans ML (1983) Reversible Loss of Gravitropic Sensitivity in Maize Roots After Tip Application of Calcium Chelators. Science 220:1375–1376
Lee SH, Seo HY, Kim JC, Heo WD, Chung WS, Lee KJ, Kim MC, Cheong YH, Choi JY, Lim CO, Cho MJ (1997) Differential activation of NAD kinase by plant calmodulin isoforms. The critical role of domain I. J Biol Chem 272:9252–9259
Lee JY, Yoo BC, Harmon AC (1998) Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean. Biochemistry 37:6801–6809
Lee SH, Johnson JD, Walsh MP, Van Lierop JE, Sutherland C, Xu A, Snedden WA, Kosk-Kosicka D, Fromm H, Narayanan N, Cho MJ (2000) Differential regulation of Ca2+/calmodulin-dependent enzymes by plant calmodulin isoforms and free Ca2+ concentration. Biochem J 350(Pt 1):299–306
Lee SM, Kim HS, Han HJ, Moon BC, Kim CY, Harper JF, Chung WS (2007) Identification of a calmodulin-regulated autoinhibited Ca2+-ATPase (ACA11) that is localized to vacuole membranes in Arabidopsis. FEBS Lett 581:3943–3949
Legue V, Blancaflor E, Wymer C, Perbal G, Fantin D, Gilroy S (1997) Cytoplasmic free Ca2+ in Arabidopsis roots changes in response to touch but not gravity. Plant Physiol 114:789–800
Lemtiri-Chlieh F, MacRobbie EA, Webb AA, Manison NF, Brownlee C, Skepper JN, Chen J, Prestwich GD, Brearley CA (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci USA 100:10091–10095
Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol 6:427–437
Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625–12630
Li X, Chanroj S, Wu Z, Romanowsky SM, Harper JF, Sze H (2008) A distinct endosomal Ca2+/Mn2+ pump affects root growth through the secretory process. Plant Physiol 147:1675–1689
Liang F, Cunningham KW, Harper JF, Sze H (1997) ECA1 complements yeast mutants defective in Ca2+ pumps and encodes an endoplasmic reticulum-type Ca2+-ATPase in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:8579–8584
Logan DC, Knight MR (2003) Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133:21–24
Long JC, Jenkins GI (1998) Involvement of plasma membrane redox activity and calcium homeostasis in the UV-B and UV-A/blue light induction of gene expression in Arabidopsis. Plant Cell 10:2077–2086
Love J, Dodd AN, Webb AA (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 16:956–966
Lu SX, Hrabak EM (2002) An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum. Plant Physiol 128:1008–1021
Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JD, Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 102:10736–10741
Luo GZ, Wang HW, Huang J, Tian AG, Wang YJ, Zhang JS, Chen SY (2005) A putative plasma membrane cation/proton antiporter from soybean confers salt tolerance in Arabidopsis. Plant Mol Biol 59:809–820
Lynch J, Polito VS, Lauchli A (1989) Salinity Stress Increases Cytoplasmic Ca Activity in Maize Root Protoplasts. Plant Physiol 90:1271–1274
Ma SY, Wu WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol 65:511–518
Ma L, Xu X, Cui S, Sun D (1999) The presence of a heterotrimeric G protein and its role in signal transduction of extracellular calmodulin in pollen germination and tube growth. Plant Cell 11:1351–1364
Ma W, Smigel A, Tsai YC, Braam J, Berkowitz GA (2008) Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol 148:818–828
MacRobbie EA (1989) Calcium influx at the plasmalemma of isolated guard cells of Commelina communis. Planta 178:231–241
Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud JP, Aldon D (2008) Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J 56:575–589
Martens S, Kozlov MM, McMahon HT (2007) How synaptotagmin promotes membrane fusion. Science 316:1205–1208
Martin ML, Busconi L (2000) Membrane localization of a rice calcium-dependent protein kinase (CDPK) is mediated by myristoylation and palmitoylation. Plant J 24:429–435
Martinec J, Feltl T, Scanlon CH, Lumsden PJ, Machackova I (2000) Subcellular localization of a high affinity binding site for D-myo-inositol 1, 4, 5-trisphosphate from Chenopodium rubrum. Plant Physiol 124:475–483
Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667
Mazars C, Bourque S, Mithofer A, Pugin A, Ranjeva R (2009) Calcium homeostasis in plant cell nuclei. New Phytol 181:261–274
McAinsh MR, Brownlee C, Hetherington AM (1990) Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure. Nature 343:186–188
McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phyt 159:585–598
McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389
McCubbin AG, Ritchie SM, Swanson SJ, Gilroy S (2004) The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of the barley aleurone through regulation of vacuolar function. Plant J 39:206–218
McNamara VP, Gounaris K (1995) Granal photosystem II complexes contain only the high redox potential form of cytochrome b-559 which is stabilized by the ligation of calcium. Biochim Biophys Acta 1231:289–296
Mei H, Zhao J, Pittman JK, Lachmansingh J, Park S, Hirschi KD (2007) In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Bot 58:3419–3427
Menteyne A, Burdakov A, Charpentier G, Petersen OH, Cancela JM (2006) Generation of specific Ca2+ signals from Ca2+ stores and endocytosis by differential coupling to messengers. Curr Biol 16:1931–1937
Miedema H, Bothwell JH, Brownlee C, Davies JM (2001) Calcium uptake by plant cells–channels and pumps acting in concert. Trends Plant Sci 6:514–519
Miedema H, Demidchik V, Very AA, Bothwell JH, Brownlee C, Davies JM (2008) Two voltage-dependent calcium channels co-exist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytol 179:378–385
Miller AJ, Sanders D (1987) Depletion of cytosolic free calcium induced by photosynthesis. Nature 326:397–400
Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101:7–12
Mills RF, Doherty ML, Lopez-Marques RL, Weimar T, Dupree P, Palmgren MG, Pittman JK, Williams LE (2008) ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol 146:116–128
Moore AL, Åkerman KEO (1984) Calcium and plant organelles. Plant Cell Environ 7:423–429
Moreno I, Norambuena L, Maturana D, Toro M, Vergara C, Orellana A, Zurita-Silva A, Ordenes VR (2008) AtHMA1 is a thapsigargin-sensitive Ca2+/heavy metal pump. J Biol Chem 283:9633–9641
Mori IC, Murata Y, Yang Y, Munemasa S, Wang Y-F, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLOS Biology 4:1749–1762
Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, Battey NH, Davies JM (2008) Annexins: multifunctional components of growth and adaptation. J Exp Bot 59:533–544
Muir SR, Sanders D (1997) Inositol 1, 4, 5-trisphosphate-sensitive Ca2+ release across nonvacuolar membranes in cauliflower. Plant Physiol 114:1511–1521
Mulder EG (1950) Mineral nutrition of plants. Annu Rev Plant Physiol 1:1–24
Nagae M, Nozawa A, Koizumi N, Sano H, Hashimoto H, Sato M, Shimizu T (2003) The crystal structure of the novel calcium-binding protein AtCBL2 from Arabidopsis thaliana. J Biol Chem 278:42240–42246
Nakagawa Y, Katagiri T, Shinozaki K, Qi Z, Tatsumi H, Furuichi T, Kishigami A, Sokabe M, Kojima I, Sato S, Kato T, Tabata S, Iida K, Terashima A, Nakano M, Ikeda M, Yamanaka T, Iida H (2007) Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc Natl Acad Sci USA 104:3639–3644
Navazio L, Bewell MA, Siddiqua A, Dickinson GD, Galione A, Sanders D (2000) Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate. Proc Natl Acad Sci USA 97:8693–8698
Navazio L, Mariani P, Sanders D (2001) Mobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol 125:2129–2138
Nemchinov LG, Shabala L, Shabala S (2008) Calcium efflux as a component of the hypersensitive response of Nicotiana benthamiana to Pseudomonas syringae. Plant Cell Physiol 49:40–46
Neuhaus G, Bowler C, Kern R, Chua NH (1993) Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 73:937–952
Ng CK, Carr K, McAinsh MR, Powell B, Hetherington AM (2001) Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410:596–599
Nomura H, Komori T, Kobori M, Nakahira Y, Shiina T (2008) Evidence for chloroplast control of external Ca2+-induced cytosolic Ca2+ transients and stomatal closure. Plant J 53:988–998
Ochiai E-I (1991) Why Calcium? J Chem Educ 68:10–12
Oh SH, Roberts DM (1990) Analysis of the State of Posttranslational Calmodulin Methylation in Developing Pea Plants. Plant Physiol 93:880–887
Ohta M, Guo Y, Halfter U, Zhu JK (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci USA 100:11771–11776
Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D’Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924
Pauly N, Knight MR, Thuleau P, Graziana A, Muto S, Ranjeva R, Mazars C (2001) The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells. Cell Calcium 30:413–421
Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734
Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408
Perez V, Wherrett T, Shabala S, Muniz J, Dobrovinskaya O, Pottosin I (2008) Homeostatic control of slow vacuolar channels by luminal cations and evaluation of the channel-mediated tonoplast Ca2+ fluxes in situ. J Exp Bot 59:3845–3855
Persson S, Wyatt SE, Love J, Thompson WF, Robertson D, Boss WF (2001) The Ca2+ status of the endoplasmic reticulum is altered by induction of calreticulin expression in transgenic plants. Plant Physiol 126:1092–1104
Pittman JK, Shigaki T, Cheng NH, Hirschi KD (2002a) Mechanism of N-terminal autoinhibition in the Arabidopsis Ca2+/H+ antiporter CAX1. J Biol Chem 277:26452–26459
Pittman JK, Sreevidya CS, Shigaki T, Ueoka-Nakanishi H, Hirschi KD (2002b) Distinct N-terminal regulatory domains of Ca2+/H+ antiporters. Plant Physiol 130:1054–1062
Plieth C (2005) Calcium: just another regulator in the machinery of life? Ann Bot (Lond) 96:1–8
Plieth C, Hansen UP, Knight H, Knight MR (1999) Temperature sensing by plants: the primary characteristics of signal perception and calcium response. Plant J 18:491–497
Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci USA 104:4730–4735
Portis AR Jr, Heldt HW (1976) Light-dependent changes of the Mg2+ concentration in the stroma in relation to the Mg2+ dependency of CO2 fixation in intact chloroplasts. Biochim Biophys Acta 449:434–436
Pottosin II, Schonknecht G (2007) Vacuolar calcium channels. J Exp Bot 58:1559–1569
Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ, Knight MR (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301–1310
Putnam-Evans C, Harmon A, Palevitz BA, Fechheimer M, Cormier MJ (1989) Calcium-dependent protein kinase is localized with F-actin in plant cells. Cell Motil Cytoskel 12:12–22
Qi Z, Stephens NR, Spalding EP (2006) Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol 142:963–971
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441
Qudeimat E, Faltusz AM, Wheeler G, Lang D, Brownlee C, Reski R, Frank W (2008) A PIIB-type Ca2+-ATPase is essential for stress adaptation in Physcomitrella patens. Proc Natl Acad Sci USA 105:19555–19560
Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA 99:9061–9066
Ranf S, Wunnenberg P, Lee J, Becker D, Dunkel M, Hedrich R, Scheel D, Dietrich P (2008) Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. Plant J 53:287–299
Rathore KS, Cork RJ, Robinson KR (1991) A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. Dev Biol 148:612–619
Raz V, Fluhr R (1992) Calcium Requirement for Ethylene-Dependent Responses. Plant Cell 4:1123–1130
Reddy VS, Ali GS, Reddy AS (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277:9840–9852
Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479
Romeis T, Piedras P, Jones JD (2000) Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12:803–816
Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. Embo J 20:5556–5567
Rudd JJ, Franklin-Tong VE (1999) Calcium signaling in plants. Cell Mol Life Sci 55:214–232
Sai J, Johnson CH (2002) Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell 14:1279–1291
Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327
Sakai-Wada A, Yagi S (1993) Ultrastructural studies on the Ca2+ localization in the dividing cells of the maize root tip. Cell Struct Funct 18:389–397
Sanchez-Barrena MJ, Martinez-Ripoll M, Zhu JK, Albert A (2005) The structure of the Arabidopsis thaliana SOS3: molecular mechanism of sensing calcium for salt stress response. J Mol Biol 345:1253–1264
Sanchez-Barrena MJ, Fujii H, Angulo I, Martinez-Ripoll M, Zhu JK, Albert A (2007) The structure of the C-terminal domain of the protein kinase AtSOS2 bound to the calcium sensor AtSOS3. Mol Cell 26:427–435
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417
Satterlee JS, Sussman MR (1998) Unusual membrane-associated protein kinases in higher plants. J Membr Biol 164:205–213
Schaller GE, Harmon AC, Sussman MR (1992) Characterization of a calcium- and lipid-dependent protein kinase associated with the plasma membrane of oat. Biochemistry 31:1721–1727
Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, Botella MA (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20:3374–3388
Schiott M, Romanowsky SM, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101:9502–9507
Schroeder JI, Hagiwara S (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338:427–430
Schumaker KS, Sze H (1987) Inositol 1, 4, 5-trisphosphate releases Ca2+ from vacuolar membrane vesicles of oat roots. J Biol Chem 262:3944–3946
Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J, Richaud P, Rolland N (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281:2882–2892
Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+ -permeable channels. Plant Physiol 141:1653–1665
Shacklock PS, Read ND, Trewavas A (1992) Cytosolic free calcium mediates red light-induced photomorphogenesis. Nature 358:753–755
Shang ZL, Ma LG, Zhang HL, He RR, Wang XC, Cui SJ, Sun DY (2005) Ca2+ influx into lily pollen grains through a hyperpolarization-activated Ca2+-permeable channel which can be regulated by extracellular CaM. Plant Cell Physiol 46:598–608
Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393–2405
Shigaki T, Rees I, Nakhleh L, Hirschi KD (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815–825
Shimada T, Watanabe E, Tamura K, Hayashi Y, Nishimura M, Hara-Nishimura I (2002) A vacuolar sorting receptor PV72 on the membrane of vesicles that accumulate precursors of seed storage proteins (PAC vesicles). Plant Cell Physiol 43:1086–1095
Simon EW (1978) The symptoms of calcium deficiency in plants. New Phytol 80:1–15
Staxen II, Pical C, Montgomery LT, Gray JE, Hetherington AM, McAinsh MR (1999) Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc Natl Acad Sci USA 96:1779–1784
Stoelzle S, Kagawa T, Wada M, Hedrich R, Dietrich P (2003) Blue light activates calcium-permeable channels in Arabidopsis mesophyll cells via the phototropin signaling pathway. Proc Natl Acad Sci USA 100:1456–1461
Strynadka NC, James MN (1989) Crystal structures of the helix-loop-helix calcium-binding proteins. Annu Rev Biochem 58:951–998
Subbaiah CC, Bush DS, Sachs MM (1994) Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. Plant Cell 6:1747–1762
Subbaiah CC, Bush DS, Sachs MM (1998) Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells. Plant Physiol 118:759–771
Sun DY, Bian YQ, Zhao BH, Zhao LY (1995) The effects of CaM on cell wall regeneration and cell division of protoplasts. Plant Cell Physiol 36:133–138
Sun QP, Guo Y, Sun Y, Sun DY, Wang XJ (2006) Influx of extracellular Ca2+ involved in jasmonic-acid-induced elevation of [Ca2+]cyt and JR1 expression in Arabidopsis thaliana. J Plant Res 119:343–350
Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke IN, Maathuis FJ, Sanders D, Bouchez D, Fromm H (2000) Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J 24:533–542
Szczegielniak J, Liwosz A, Jurkowski I, Loog M, Dobrowolska G, Ek P, Harmon AC, Muszynska G (2000) Calcium-dependent protein kinase from maize seedlings activated by phospholipids. Eur J Biochem 267:3818–3827
Szczegielniak J, Klimecka M, Liwosz A, Ciesielski A, Kaczanowski S, Dobrowolska G, Harmon AC, Muszynska G (2005) A wound-responsive and phospholipid-regulated maize calcium-dependent protein kinase. Plant Physiol 139:1970–1983
Sze H, Liang F, Hwang I, Curran AC, Harper JF (2000) Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51:433–462
Takahashi K, Isobe M, Knight MR, Trewavas AJ, Muto S (1997) Hypoosmotic Shock Induces Increases in Cytosolic Ca2+ in Tobacco Suspension-Culture Cells. Plant Physiol 113:587–594
Thion L, Mazars C, Nacry P, Bouchez D, Moreau M, Ranjeva R, Thuleau P (1998) Plasma membrane depolarization-activated calcium channels, stimulated by microtubule-depolymerizing drugs in wild-type Arabidopsis thaliana protoplasts, display constitutively large activities and a longer half-life in ton 2 mutant cells affected in the organization of cortical microtubules. Plant J 13:603–610
Trewavas A (1999) Le calcium, C’est la vie: calcium makes waves. Plant Physiol 120:1–6
Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plant. Plant J 58:778–790
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637
Urquhart W, Gunawardena AH, Moeder W, Ali R, Berkowitz GA, Yoshioka K (2007) The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner. Plant Mol Biol 65:747–761
Vainonen JP, Sakuragi Y, Stael S, Tikkanen M, Allahverdiyeva Y, Paakkarinen V, Aro E, Suorsa M, Scheller HV, Vener AV, Aro EM (2008) Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. Febs J 275:1767–1777
van Der Luit AH, Olivari C, Haley A, Knight MR, Trewavas AJ (1999) Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiol 121:705–714
van Goor BJ, Wiersma D (1974) Redistribution of potassium, calcium, magnesium, and manganese in the plant. Physiol Plant 31:163–168
Volotovski ID, Sokolovsky SG, Molchan OV, Knight MR (1998) Second messengers mediate increases in cytosolic calcium in tobacco protoplasts. Plant Physiol 117:1023–1030
Wagner G, Rossbacher R (1980) X-ray microanalysis and chlorotetracycline staining of calcium vesicles in the green alg Mougeotia. Planta 149:298–305
Walter A, Mazars C, Maitrejean M, Hopke J, Ranjeva R, Boland W, Mithofer A (2007) Structural requirements of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells. Angew Chem Int Ed Engl 46:4783–4785
Watanabe E, Shimada T, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2002) Calcium-mediated association of a putative vacuolar sorting receptor PV72 with a propeptide of 2S albumin. J Biol Chem 277:8708–8715
Webb AAR, McAinsh MR, Mansfield TA, Hetherington AM (1996) Carbon dioxide induces increases in guard cell cytosolic free calcium. Plant J 9:297–304
Wegner LH, De Boer AH (1997) Properties of Two Outward-Rectifying Channels in Root Xylem Parenchyma Cells Suggest a Role in K+ Homeostasis and Long-Distance Signaling. Plant Physiol 115:1707–1719
Weinl S, Held K, Schlucking K, Steinhorst L, Kuhlgert S, Hippler M, Kudla J (2008) A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179:675–686
Wheeler GL, Brownlee C (2008) Ca2+ signalling in plants and green algae–changing channels. Trends Plant Sci 13:506–514
White PJ, Broadley MR (2003) Calcium in plants. Ann Bot (Lond) 92:487–511
White PJ, Bowen HC, Demidchik V, Nichols C, Davies JM (2002) Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochim Biophys Acta 1564:299–309
Wick SM, Hepler PK (1980) Localization of Ca2+-containing antimonate precipitates during mitosis. J Cell Biol 86:500–513
Williams RJP (1970) The biochemistry of sodium, potassium, magnesium, and calcium. Quart Rev Chem Soc 24:331–365
Williams RJ (2004) Signalling: basics and evolution. Acta Biochim Pol 51:281–298
Wu Y, Kuzma J, Marechal E, Graeff R, Lee HC, Foster R, Chua NH (1997) Abscisic acid signaling through cyclic ADP-ribose in plants. Science 278:2126–2130
Wu Z, Liang F, Hong B, Young JC, Sussman MR, Harper JF, Sze H (2002) An endoplasmic reticulum-bound Ca2+/Mn2+ pump, ECA1, supports plant growth and confers tolerance to Mn2+ stress. Plant Physiol 130:128–137
Xiong TC, Jauneau A, Ranjeva R, Mazars C (2004) Isolated plant nuclei as mechanical and thermal sensors involved in calcium signalling. Plant J 40:12–21
Xu H, Heath MC (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell 10:585–598
Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360
Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E (2005) Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner. Proc Natl Acad Sci USA 102:16107–16112
Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-Dependent Freezing Tolerance in Arabidopsis Involves Membrane Resealing via Synaptotagmin SYT1. Plant Cell 20:3389–3404
Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512
Yoon GM, Dowd PE, Gilroy S, McCubbin AG (2006) Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity. Plant Cell 18:867–878
Yoshioka K, Moeder W, Kang HG, Kachroo P, Masmoudi K, Berkowitz G, Klessig DF (2006) The chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18:747–763
Yu IC, Parker J, Bent AF (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci USA 95:7819–7824
Zhao J, Barkla BJ, Marshall J, Pittman JK, Hirschi KD (2008) The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659–669
Zhao J, Shigaki T, Mei H, Guo YQ, Cheng NH, Hirschi KD (2009) Interaction between Arabidopsis Ca2+/H+ Exchangers CAX1 and CAX3. J Biol Chem 284:4605–4615
Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2010 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Batistič, O., Kudla, J. (2010). Calcium: Not Just Another Ion. In: Hell, R., Mendel, RR. (eds) Cell Biology of Metals and Nutrients. Plant Cell Monographs, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10613-2_2
Download citation
DOI: https://doi.org/10.1007/978-3-642-10613-2_2
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-10612-5
Online ISBN: 978-3-642-10613-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)