MEMBRANE STRUCTURE AND FUNCTION

Communicating with Calcium

Correspondence to: Dale Sanders, ds10{at}york.ac.uk (E-mail), 44-1904-434317 (fax)

	INTRODUCTION

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Calcium as a Ubiquitous Signal in Plants
All living cells use a network of signal transduction pathways to conduct developmental programs, obtain nutrients, control their metabolism, and cope with their environment. A major challenge for cell biologists is to understand the "language" of these signaling systems. For simplicity, signaling pathways usually have been studied in isolation, with experimenters attempting to define a single pathway through which a given stimulus evokes a response. However, cells are not simple, and for any given stimulus (input), the final response (output) is likely to be the result of complex interaction, or cross-talk, between multiple pathways (Trewavas and Malhó, 1997; Jenkins 1998 ). Presumably, this cross-talk evolved as a mechanism to enable a relatively small number of messengers to help cells process a much larger array of potential stimuli in an appropriate fashion. In plant cells, the list of messengers used by signaling pathways includes Ca²⁺, lipids, pH, and cyclic GMP (cGMP). However, no single messenger has been demonstrated to respond to more stimuli than has cytosolic free Ca²⁺ ([Ca²⁺]_c). A partial list of stimuli that evoke changes in [Ca²⁺]_c is shown in Table 1.

Our knowledge of [Ca²⁺]_c in plant cell signaling has been markedly enhanced by the development of reliable techniques to measure free Ca²⁺ intracellularly (Read et al. 1993 ). Early studies (Brownlee and Wood 1986 ; Miller and Sanders 1987 ; Felle 1989 ) with Ca²⁺-selective microelectrodes yielded consistent estimates of [Ca²⁺]_c. However, electrodes are rather unwieldy and are unable to report detailed spatial information, so they have been largely supplanted by fluorescent dyes and the luminescent protein aequorin (Read et al. 1993 ). Ca²⁺-indicating fluorescent dyes usually are microinjected into the cell or sometimes loaded as the free acid at low pH. Their fluorescence yields are sufficient to enable ready imaging of heterogeneities in [Ca²⁺]_c,; for dyes in which an isosbestic point is present in the excitation or emission spectrum, ratiometric images allow quantification of the signal independent of dye concentration. Alternatively, changes in [Ca²⁺]_c can be visualized with the Ca²⁺-sensitive luminescent protein aequorin. The use of transgenic plants stably expressing apoaequorin—from which aequorin can be spontaneously reconstituted on addition of the luminophore coelenterazine—circumvents the requirement for microinjection, although low-intensity emission of aequorin so far has limited spatial resolution of [Ca²⁺]_c signals to the multicellular level (Knight et al. 1998 ).

Although calcium signals have been implicated in many stimulus–response phenomena, rigorous proof that a [Ca²⁺]_c transient is an essential intermediate has been difficult to obtain. A strong argument for a critical involvement of Ca²⁺ requires the demonstration not only that a stimulus evokes a change in [Ca²⁺]_c but also that two additional experimental criteria are met. First, a block of the [Ca²⁺]_c transient also should block the downstream response, and second, appropriate Ca²⁺-sensitive response elements should be present. Meeting these criteria represents a formidable technical challenge, but strong evidence exists to support a central role of [Ca²⁺]_c in a range of events, including phytochrome action (Shacklock et al. 1992 ; Bowler et al. 1994 ; Neuhaus et al. 1997 ), stomatal closure in response to a number of stimuli (MacRobbie 1997 ), and tip growth of root hairs, pollen tubes, and algal rhizoids (e.g., Brownlee and Wood 1986 ; Wymer et al. 1997 ; Holdaway-Clarke et al. 1998 ; Malho et al. 1998 ).

Why Calcium?
Metabolism in all cells requires the presence of orthophosphate (P_i) and phosphorylated organic compounds, particularly for cytosolic reactions associated with transduction of free energy. The low solubility product of Ca²⁺ with P_i would have required the early evolution of mechanisms for maintenance of [Ca²⁺]_c at a level that would certainly be well below the millimolar concentrations that prevail in seawater. Thus, transport systems that export Ca²⁺ from the cytosol are present in all cells to sustain steady state values of [Ca²⁺]_c in the submicromolar range. This homeostatic mechanism would have been ideal for subsequent evolution of Ca²⁺-based signaling pathways. Specifically, the elevation of [Ca²⁺]_c by a factor of 10 or 20 can occur more rapidly than would be possible for ions or solutes that are maintained at millimolar levels.

The chemistry of Ca²⁺ provides further favorable features for signal transduction. The ability of the ion to coordinate a considerable number (commonly six to eight) of uncharged oxygen atoms enables the evolution of protein conformations in which remote domains can participate in calcium binding (McPhalen et al. 1991 ). Calcium-induced conformational changes can in fact be exploited to elicit downstream events in signaling pathways.

Cytosolic Free Calcium, Buffering, and the Energization of Ca²⁺ Transport
The cytosolic free calcium concentration typically is maintained at ~200 nM (Bush 1995 ). However, the Ca²⁺ content of the cytosol is far higher than this because of the high affinity for Ca²⁺ to a range of binding proteins. Prominent among these proteins is calmodulin, which, by binding in turn to other proteins, serves as an adaptor of Ca²⁺ signals. Much of the calcium that enters the cytosol during signaling is rapidly bound. Estimates from neuronal cells suggest that only 0.1 to 1% of an imposed Ca²⁺ load remains free (Brinley et al. 1977 ; Gorman and Thomas 1980 ), with the rest being absorbed. The tendency for the majority of Ca²⁺ ions to associate with cytosolic proteins has the effect of markedly reducing the effective diffusion coefficient of Ca²⁺ in the cytosol (Thomas 1982 ). Restricted rates of diffusion in the cytosol underlie the occurrence of localized and spatially distinct patterns in Ca²⁺ signaling.

The presence of intracellular organelles that are able to accumulate Ca²⁺ effectively contributes to the buffering of a Ca²⁺ load, tending to dampen Ca²⁺ signals. Whereas the endoplasmic reticulum (ER), mitochondria, and even chloroplasts are all known to have the capacity to sequester Ca²⁺ (Bush 1995 ), it is vacuoles that, by virtue of their size and capacity for Ca²⁺ accumulation, represent the most prominent sink for Ca²⁺ in most cells. The relative contributions of biochemical and organellar buffering have not been estimated in plant cells. However, in the mycelial fungus Neurospora crassa, buffering of Ca²⁺ is extremely effective, with vacuolar sequestration probably playing the major role (Miller et al. 1990 ).

Ultimately, homeostasis of [Ca²⁺]_c must be achieved by export across the plasma membrane because both biochemical buffering and intracellular sequestration have finite capacities. Hence, a considerable electrochemical potential difference for Ca²⁺(_Ca) exists across all membranes in the cell, with the energized transport of Ca²⁺ invariably in a direction out of the cytosol. At the plasma membrane, the Ca²⁺ concentration ratio (inside/outside) is typically of the order of 10^-4, and the presence of a cytosolic negative electrical potential difference of approximately -150 mV yields a _Ca of approximately -50 kJ mol^-1. Although the potential difference across the membranes of organelles, such as the vacuole and ER, is likely to be less negative than that across the plasma membrane, large driving forces nevertheless prevail and require energized removal of Ca²⁺ from the cytosol. Efflux of Ca²⁺ from the cytosol is mediated by pumps powered by either ATP hydrolysis or a proton motive force. By contrast, the passive entry of Ca²⁺ into the cytosol is mediated by ion channels.

	ENCODING CALCIUM SIGNALS: AN ISSUE OF TRANSPORT

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Cytosolic Ca²⁺ signals can be thought of as the result of two opposing functions: influx into and efflux out of the cytosol. In theory, the characteristics of the transport systems catalyzing influx and efflux are the primary determinants of the dynamic form of a Ca²⁺ signal. However, Ca²⁺ binding proteins, by virtue of their buffer capacity, will in practice act as significant modifiers of [Ca²⁺]_c dynamics.

Research has emphasized the role of transporters in regulating [Ca²⁺]_c at the vacuolar, ER, and plasma membranes. Figure 1 gives an overview of the Ca²⁺ transport events at these membranes, which are the subject of more detailed discussion below. Additionally, Ca²⁺ fluxes across endomembranes, such as the chloroplast envelope, mitochondrial inner membrane, and nuclear membrane, might be equally important in determining the pattern or form of Ca²⁺ signals (Kreimer et al. 1985 ; Johnson et al. 1995 ; Santella and Carafoli 1997 ).

View larger version (121K): [in this window] [in a new window]   Figure 1. Schematic Representation of Major Identified Ca2+ Transport Pathways in Plant Cell Membranes. Energized transport systems are represented as blue circles. ACA1, ACA2, and ACA3 are Arabidopsis Ca2+ ATPases that have been localized to the membranes shown. The direction of Ca2+ pumping for ACA1 is hypothetical. ACAx refers to a plasma membrane ATPase that has been identified biochemically but not at a molecular level. BCA1 is a Brassica oleracea Ca2+ ATPase that localizes to the vacuolar membrane. CAX1 is a Ca2+/H+ antiporter from Arabidopsis, probably located at the vacuolar membrane. Red squares represent Ca2+-permeable ion channels, identified through electrophysiological approaches. None has been identified yet at a molecular level. BCC1, Brionica Ca2+ channel; InsP3R, putative InsP3 receptor; RyR, putative ryanodine receptor, activated by cADPR; SV channel, slowly activating vacuolar channel; VDCC2, voltage-dependent Ca2+ channel 2; VVCa channel, vacuolar voltage-gated Ca2+ channel. See text for further discussion and references.

Calcium Efflux through H⁺/Ca²⁺ Antiporters and Calcium ATPases
The transport systems that energize efflux from the cytosol are proposed to provide three critical housekeeping functions. First, they restore [Ca²⁺]_c to resting levels, thereby terminating Ca²⁺ signals. Second, they load Ca²⁺ into compartments such as the ER and vacuole to be used as sources for regulated Ca²⁺ release. Third, they supply Ca²⁺ to various organelles to support specific biochemical functions. For example, high levels of Ca²⁺ in the ER are required for proper protein processing through the secretory pathway (Rudolph et al. 1989 ; Gill et al. 1996 ).

A fundamental question is whether, in addition to their housekeeping functions, any of these efflux pathways help shape the dynamic form of a calcium signal and thereby help define the information encoded in calcium release. If efflux is subject to regulation, then elucidating the signals that control these efflux systems will be equally important in identifying the signals that open various calcium channels. Pioneering work in two nonplant systems (Xenopus oocytes and Dictyostelium) has demonstrated that increasing the abundance or activity of a Ca²⁺ pump can indeed alter signal transduction (Camacho and Lechleiter 1993 ; Cubitt et al. 1998 ; Lechleiter et al. 1998 ). Thus, the potential signaling importance of efflux systems in plants must be seriously considered.

Carriers
H⁺/Ca²⁺ antiporters can in principle drive "uphill" transport of Ca²⁺ in which a proton motive force is maintained, although in plants this usually requires a H⁺/Ca²⁺ stoichiometry of at least three (Blackford et al. 1990 ). The first plant H⁺/Ca²⁺ antiporter to be cloned and functionally expressed was CAX1p (Calcium exchanger 1; Hirschi et al. 1996 ). The gene was identified by its ability to restore growth on high-Ca²⁺ media to a yeast mutant defective in vacuolar Ca²⁺ transport. CAX1p appears to transport Ca²⁺ at low concentrations (K_m is ~13 µM), consistent with kinetic studies on H⁺/Ca²⁺-antiport activity conducted with oat root vacuoles (e.g., Schumaker and Sze 1986 ). Although it is reasonable to speculate that CAX1p is localized to the plant vacuole, there is evidence for H⁺/Ca²⁺ antiporters in other membranes, such as the plasma membrane (Kasai and Muto 1990 ). Thus, the localization of various antiporters may require careful evaluation at the whole-cell level.

Pumps
Calcium pumps belong to the superfamily of P-type ATPases that directly use ATP to drive ion translocation. Two distinct Ca²⁺ pump families have been proposed, based on protein sequence identities (Axelsen and Palmgren 1998 ). Members of the type IIA and IIB families, respectively, include the ER-type and plasma membrane–type Ca²⁺ pumps first identified in animal cells. Previously, ER- and plasma membrane–type pumps were distinguished by three criteria: (1) localization to either the ER or plasma membrane, respectively; (2) differential sensitivity to inhibitors (e.g., ER-type inhibition by cyclopiazonic acid and thapsigargin); and (3) direct activation of plasma membrane–type pumps by calmodulin (Evans and Williams 1998 ).

Several genes encoding type IIA (ER-type) pumps have been cloned from plants, including LCA1 from tomato (Wimmers et al. 1992 ), OCA1 from rice (for OsCa–ATPase; Chen et al. 1997 ), and ECA1/ACA3 from Arabidopsis (for ER-type Ca²⁺–ATPase/Arabidopsis Ca²⁺–ATPase isoform 3; Liang et al. 1997 ). There is evidence that ECA1p/ACA3p is located in the ER. However, in contrast to the animal prototypes, non-ER locations have been suggested for other isoforms. For example, immunodetection of LCA1-related pumps in membrane fractionation experiments identified ER-type pumps in both tonoplast and plasma membrane locations (Ferrol and Bennett 1996 ).

Three plant genes encoding type IIB (plasma membrane–type) pumps have been reported: ACA1 and ACA2 from Arabidopsis (Huang et al. 1993 ; Harper et al. 1998 ) and BCA1 from Brassica oleracea (Malmstrom et al. 1997 ). The corresponding plant proteins are distinguished from animal plasma membrane–type pumps by (1) localization at membranes other than the plasma membrane, and (2) a unique structural arrangement with putative autoinhibitory domains at the N terminus instead of the C terminus. Evidence suggests that ACA1p is in a plastid inner envelope membrane, based on membrane fractionation and immunodetection with an anti-ACA1 polyclonal antibody (Huang et al. 1993 ). BCA1p appears to be in the vacuolar membrane, based on correspondence with a peptide sequence obtained from a purified vacuolar ATPase (Malmstrom et al. 1997 ). ACA2p was shown to fractionate with the ER, as indicated by immunodetection of ACA2p in membrane fractions and confirmed by cytological visualization of an ACA2p tagged with a C-terminal green fluorescent protein (Harper et al. 1998 ; Hong et al. 1999 ).

Functional Overlap?
The vacuole and ER provide two examples in which multiple efflux pathways have been identified in the same organelle. In vacuoles, there is evidence for both a H⁺/Ca²⁺ antiporter (like CAX1p) and a pump (like BCA1p). In the ER, there is evidence for two different types of calcium pumps, a type IIA (like ACA3p/ECA1p) and type IIB (like ACA2p). It is not clear what unique functional properties are provided by the different efflux pathways.

Regulation
It is expected that the Ca²⁺ efflux pathways are regulated in plants, by analogy to fungal and animal systems. The yeast Ca²⁺ exchanger (VCX1p) is inhibited by calcineurin, a calmodulin-activated phosphatase (Cunningham and Fink 1996 ). In animals, both ER- and plasma membrane–type Ca²⁺ pumps appear to be regulated by multiple signal transduction pathways, including calmodulin and multiple kinases (e.g., CaMKII and protein kinase C; Carafoli 1997 ; Stokes 1997 ; Penniston and Enyedi 1998 ). The ER-type pumps can be regulated in response to cytoplasmic signals as well as a feedback system that senses the Ca²⁺ load within the ER lumen (Bhogal and Colyer 1998 ; Mogami et al. 1998 ). In plants, the clearest example of regulation is the direct activation of at least some type IIB pumps by Ca²⁺/calmodulin (e.g., ACA2p and BCA1p).

Calcium Influx through Ca²⁺-Permeable Ion Channels
Calcium-permeable channels have yet to be definitively identified at a molecular level in plants. Nevertheless, a wheat cDNA clone, LCT1 (for low-affinity cation transporter 1), complements yeast mutants defective in Ca²⁺ influx (Schachtman et al. 1997 ; Clemens et al. 1998 ). Although the sequence of LCT1 provides no clues to its likely relationship to previously identified ion channels, an exciting possibility is that LCT1p provides a physiologically significant pathway for Ca²⁺ uptake in plants.

Despite the paucity of molecular detail, electrophysiological and biochemical studies have resulted in a considerable body of information on the permeability, gating, and pharmacological properties of Ca²⁺-permeable channels, especially at the vacuolar and plasma membranes. In some cases, especially with respect to ligand-gated channels, insights are emerging into their roles in cell signaling.

Plasma Membrane
At least two major classes of Ca²⁺ channels reside in the plasma membrane (White 1998 ). Those that are relatively nonselective with respect to cation and possess a high single-channel conductance are known as maxi-cation channels (White 1993 , White 1994 ). The second class is relatively more selective for cation, exhibits a smaller single-channel conductance, and is known as voltage-dependent cation channel 2 (White 1994 ; Pineros and Tester 1995 , Pineros and Tester 1997 ). Although both classes of ion channel have been characterized most thoroughly in cereal roots, it is clear that Ca²⁺-permeable channels exist in a variety of other cell types and tissues, including carrot and parsley suspension cultures (Thuleau et al. 1993 ; Zimmermann et al. 1997 ) and Arabidopsis mesophyll and root cells (Ping et al. 1992 ; Thion et al. 1996 ).

A common feature of most such channels is their capacity for activation by membrane depolarization. It is thought that such voltage gating might comprise the critical factor responsible for channel activation during signaling (Ward et al. 1995 ). Thus, a number of signals, including blue light (Spalding and Cosgrove 1989 ), red light (Ermolayeva et al. 1996 ), nodulation (Nod) factors (Ehrhardt et al. 1992 ), and fungal elicitors (Kuchitsu et al. 1993 ), evoke rapid (<1 min) membrane depolarization, probably through initial activation of anion channels (Cho and Spalding 1996 ; Ermolayeva et al. 1997 ). The resultant increase in Ca²⁺ channel activity could then facilitate an increase in [Ca²⁺]_c. However, additional regulators of Ca²⁺ channel activity are likely to be required to preclude initiation of Ca²⁺ signals by the many factors (e.g., inorganic and organic nutrients) that have been shown to depolarize plant plasma membranes. The demonstration that the activity of depolarization-activated Ca²⁺ channels is apparently suppressed by direct or indirect interaction with microtubules (Thion et al. 1996 ) is in accord with the notion of voltage-independent control.

Evidence favors the presence of additional Ca²⁺ entry pathways into plant cells. In guard cells, for example, it is likely that abscisic acid (ABA) induces Ca²⁺ influx by activation of nonselective and voltage-independent cation channels (Schroeder and Hagiwara 1990 ; Thiel et al. 1992 ). The inhibition of instantaneous current by okadaic acid (Thiel and Blatt 1994 ) suggests that the activities of the channels that underlie the current might be regulated by protein phosphatase type 1 or 2A.

Endomembranes
At least four different Ca²⁺-permeable channel types have been identified at vacuolar membranes (Allen and Sanders 1997 ). Two of these channels are ligand gated, one by inositol 1,4,5-trisphosphate (InsP₃; Schumaker and Sze 1987 ; Alexandre et al. 1990 ), the other by cyclic ADP-ribose (cADPR; Allen et al. 1995 ). The pharmacological properties of plant cADPR-gated channels resemble those of ryanodine receptors (Muir and Sanders 1996 ), which, along with InsP₃ receptors, are responsible for mobilization of ER-based Ca²⁺ pools during signaling in animal cells. Microinjection of both InsP₃ and cADPR into guard cells has revealed that both compounds have the capacity to elevate [Ca²⁺]_c, thereby demonstrating that InsP₃- and cADPR-gated channels are functional in Ca²⁺ release in plants (Gilroy et al. 1990 ; Leckie et al. 1998 ).

A property of both the InsP₃ receptors and the ryanodine receptors of animal cells is their capacity for activation by [Ca²⁺]_c. This response is thought to underlie Ca²⁺-induced Ca²⁺ release (CICR), which can be fundamental to the amplification of Ca²⁺ signals (Taylor and Traynor 1995 ). Curiously, neither InsP₃- nor cADPR-gated currents across the vacuolar membrane of plants are activated by [Ca²⁺]_c (Allen and Sanders 1994b ; Leckie et al. 1998 ), despite the presence of waves, oscillations, and spikes of [Ca²⁺]_c (see below), which are suggestive of CICR.

The remaining two Ca²⁺-permeable channel types at the vacuolar membrane are both voltage gated, one by membrane hyperpolarization (Johannes et al. 1992 ; Gelli and Blumwald 1993 ; Allen and Sanders 1994a ) and the other by membrane depolarization (Ward and Schroeder 1994 ; Schultz-Lessdorf and Hedrich 1995 ; Allen and Sanders 1996 ). The second of these channel types is known as the slowly activating vacuolar (SV) channel, and it also is activated by [Ca²⁺]_c above ~600 nM (Hedrich and Neher 1987 ). It has been proposed that SV channel activation might comprise a route for CICR (Ward and Schroeder 1994 ), with Ca²⁺ provided by the opening of one or both of the ligand-gated channels acting as the "trigger" for SV activation. This proposal has been contested as a result of the finding that the open probability of the SV channel is highly dependent on _Ca and that, at values of _Ca favoring mobilization of Ca²⁺ from the vacuole, the open probability of the SV channel becomes vanishingly small (Pottosin et al. 1997 ). However, this debate might need to be reassessed as a result of the finding that the open probability of the SV channel is markedly enhanced by the presence of cytosolic Mg²⁺ ions (Cantu et al. 1998 ), which were not present in the experiments of Pottosin et al. 1997 .

Despite the prominence of the vacuole as an intracellular store of Ca²⁺ in mature cells, the possibility that other intracellular compartments participate in Ca²⁺ signaling should not be ignored. Indeed, imaging studies have demonstrated intracellular Ca²⁺ mobilization from regions of pollen tubes and root hairs in which no vacuole is apparent (Ehrhardt et al. 1996 ; Franklin-Tong et al. 1996 ), and it is not surprising that Ca²⁺ channels have been described at nonvacuolar membranes. A voltage-sensitive Ca²⁺ channel has been identified in the ER from Brionica dioica tendrils and functionally characterized in planar lipid bilayers (Klusener et al. 1995 ). Calcium release elicited by InsP₃ furthermore has been demonstrated in sucrose gradient-fractionated vesicles from cauliflower florets, which were considerably denser than the vacuolar fraction and were possibly associated with cortical ER (Muir and Sanders 1997 ).

Physiological roles for both InsP₃- and cADPR-gated channels are emerging. Microinjection studies and metabolite measurements have suggested roles for InsP₃ in stomatal closure (Gilroy et al. 1990 ), osmoregulation (Srivastava et al. 1989 ; Cho et al. 1993 ), modulation of turgor in the motor cells of leaf pulvini by red light (Kim et al. 1996 ), and cessation of pollen tube growth, possibly during the self-incompatibility response (Franklin-Tong et al. 1996 ). There is clear evidence for a role of cADPR-induced Ca²⁺ signaling in ABA responses. Wu et al. 1997 showed that cADPR levels are upregulated by ABA and used a microinjection strategy to demonstrate that cADPR evokes expression of two ABA-regulated genes. Although gene expression is activated by a range of treatments thought to increase [Ca²⁺]_c, such as InsP₃ microinjection, the ABA response is blocked selectively by the cADPR antagonist 8-amino-cADPR but not by heparin. Conversely, Ca²⁺-responsive cab gene expression is enhanced by neither cADPR nor InsP₃ microinjection. These results suggest considerable specificity in the cADPR-signaling pathway, implying either that cADPR uses a specified pool of Ca²⁺ or that the dynamic properties of the resultant [Ca²⁺]_c signal are critical for the given response. In a separate study (Leckie et al. 1998 ), ABA-induced stomatal closure was shown to be both evoked by cADPR and partially blocked by inhibitors of ADP–ribosyl cyclase.

	TARGETS OF CALCIUM SIGNALS

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The targets of Ca²⁺ signal transduction pathways can be divided into two categories: primary sensors and downstream substrates. Some downstream substrates represent the end point for the signaling pathway and include ion channels. In guard cells, anion channels involved in salt loss during stomatal closure are activated by [Ca²⁺]_c and by phosphorylation (Schroeder and Keller 1992 ; Schmidt et al. 1995 ). In the case of Ca²⁺ activation of SV channels (discussed above), the effects of Ca²⁺ are mediated by calmodulin (Bethke and Jones 1994 ; Schultz-Lessdorf and Hedrich 1995 ).

Calcium-dependent protein kinases (CDPKs) are a unique family of kinases, distinguished by a C-terminal calmodulin-like regulatory domain with four calcium binding EF hands. They are likely to be important primary sensors of Ca²⁺ signals and were first identified in plants and protozoa (Harper et al. 1991 ; Suen and Choi 1991 ; Zhao et al. 1993 ). CDPKs have been found in neither yeast nor animal systems, throughout the course of genome-sequencing projects (J.F. Harper and A.C. Harmon, unpublished results). In plants, on the other hand, divergent subfamilies have been identified with one or more degenerate EF hands (e.g., Lindzen and Choi 1995 ; Patil et al. 1995 ). In Arabidopsis, >12 members of the CDPK superfamily have been identified (Hrabak et al. 1996 ).

The plethora of CDPK isoforms, along with the comparable paucity of potential gene homologs that encode calmodulin-dependent kinase or protein kinase C–like proteins, has led to the speculation that most calcium-regulated protein kinase activity in plants occurs through CDPK pathways (Satterlee and Sussman 1998 ). Some CDPK isoforms appear to regulate distinct signaling pathways. For example, in a transient expression system, only two of eight CDPK isoforms induced expression from the ABA/stress regulated promoter HVA-1 (Sheen 1996 ). Biochemical studies, moreover, show distinct substrate specificities for different isoforms (Lee et al. 1998 ). In addition, different isoforms are activated by different threshold concentrations of calcium, raising the possibility that specific isoforms will decode different Ca²⁺ signals. Although the subcellular localization of specific isoforms has not been completed, it is clear that there are multiple isoforms widely distributed in both soluble and membrane-associated locations (Roberts and Harmon 1992 ).

The identification of potential substrates of CDPKs remains a major challenge. Based on in vitro assays, there is a growing list of potential CDPK targets, including chloride and potassium channels in guard cells (Pei et al. 1996 ; J. Li et al. 1998 ), the nodulin 26 channel in soybean root nodules (Lee et al. 1995 ), sucrose phosphate synthase (McMichael et al. 1995 ), EF1-/phosphatidylinositol 4-kinase (Yang and Boss 1994 ), the plasma membrane proton pump (Lino et al. 1998 ; Camoni et al. 1998 ), nitrate reductase (Bachmann et al. 1996 ), and bZIP-type transcripting factors (Meshi et al. 1998 ). However, the more difficult task is to demonstrate that a putative substrate is regulated by a particular CDPK pathway within the organism.

A role for phosphatases as primary sensors of Ca²⁺ signals also is emerging. Inward K⁺ currents in guard cells, which are downregulated during stomatal closure, are inhibited by calcineurin (protein phosphatase 2B) but activated by immunosuppressants, which antagonize calcineurin activity (Luan et al. 1993 ). Similarly, SV channels are inactivated by calcineurin, and it has been proposed that if SV channels are involved in CICR, then the physiological significance of this inactivation might be as a negative feedback mechanism to prevent the cytosol from being flooded by the vacuolar Ca²⁺ pool (Allen and Sanders 1995 ) or as a regulator of [Ca²⁺]_c oscillation frequency (McAinsh and Hetherington 1998 ). A more defined role for calcineurin is hinted at by the finding (Liu and Zhu 1998 ) that the SOS3 gene of Arabidopsis encodes a homolog of the calcineurin B subunit from yeast (as well as neuronal calcium sensors from animals). sos3 mutants are hypersensitive to Na⁺, and the phenotype is partially suppressed by increasing extracellular Ca²⁺ concentration (Liu and Zhu 1997 ). Because salt stress is known to elicit rapid changes in [Ca²⁺]_c (Knight et al. 1997 ), SOS3p might be the primary Ca²⁺ sensor in a salt stress signal transduction pathway. However, it should be noted that although the sos3 phenotype is specific to salt stress, the changes in free Ca²⁺ are not and also are induced by water stress (Knight et al. 1997 ).

Other signaling components are likely to form primary sensors of Ca²⁺ signals. The finding that plants possess Ca²⁺-activated phosphoinositide-specific phospholipase C (PI-PLC) activity (e.g., Huang et al. 1995 ) suggests a role for InsP₃ in CICR, because Ca²⁺ mobilization by InsP₃ would then trigger further InsP₃ production. The recent cloning of plant PI-PLCs has confirmed that they are both Ca²⁺ activated and closely related to the mammalian PLC isoforms (Kopka et al. 1998 ). In accord with the notion that PI-PLCs participate in Ca²⁺ signaling, Ca²⁺ waves in pollen tubes and ABA-induced oscillations in [Ca²⁺]_c in guard cells are inhibited by PI-PLC inhibitors (Franklin-Tong et al. 1996 ; Staxen et al. 1999 ). In both of these systems, Ca²⁺ appears to participate in determining the dynamics of its own signal.

	DECODING CALCIUM SIGNALS: THE PROBLEM OF SPECIFICITY

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The involvement of Ca²⁺ in a wide variety of stimulus– response pathways in plant cells raises several questions concerning how different responses can be regulated by the same messenger. Moreover, a variety of graded Ca²⁺-mediated responses to stimuli of varying strengths is a hallmark of plant responses to environmental changes (McAinsh et al. 1997 ; Malho et al. 1998 ; McAinsh and Hetherington 1998 ). Which features of the Ca²⁺ signaling machinery are relevant to understanding how a single messenger can carry multiple messages? Key considerations include amplitude, duration, frequency, and location of the Ca²⁺ signal, as well as the interactions with other cellular components and signaling pathways that reflect the "physiological address" of the given cell (McAinsh et al. 1997 ).

In animal cells, differential responses to Ca²⁺ signals varying in amplitude, duration, frequency, and localization have been clearly demonstrated. The amplitude and duration of a Ca²⁺ signal in B lymphocytes, for instance, induce differential activation of transcription factors (Dolmetsch et al. 1997 ). Changes in the frequency of electrically induced Ca²⁺ spikes, moreover, differentially affect nerve cell differentiation (Gu and Spitzer 1995 ). Using a membrane-permeant form of caged InsP₃, W.H. Li et al. 1998 showed that the frequency of Ca²⁺ spikes can determine the degree of gene expression via a nuclear factor of T cells, lending support to the hypothesis that information can be encoded into the frequency of repetitive Ca²⁺ signals (Tang and Othmer 1995 ; Berridge 1997 ). Additionally, in mouse pituitary cells, elevations of nuclear [Ca²⁺] can elicit changes in gene expression via cAMP response elements, whereas changes in [Ca²⁺]_c affect gene expression by means of serum response elements (Hardingham et al. 1997 ). The recent demonstration that a human transcriptional repressor is directly modulated by Ca²⁺ indicates that Ca²⁺ can regulate gene expression without involving protein phosphorylation cascades (Carrion et al. 1999 ).

Calcium Transients and Downstream Responses
Evidence that different types of Ca²⁺ signal can differentially influence gene expression is less direct for plant cells. There are several examples of single Ca²⁺ transients in response to defined stimuli. These include rapid rises in [Ca²⁺]_c in response to touch or cold shock, involving both vacuolar and plasma membrane Ca²⁺ fluxes (Knight et al. 1991 , Knight et al. 1996 ), and transient increases in [Ca²⁺] of varying duration in response to oxidative stress (Price et al. 1994 ), elicitors (Knight et al. 1991 ), systemin (Moyen et al. 1998 ), and hypo-osmotic treatments (Tazawa et al. 1995 ; Taylor et al. 1996 ; Takahashi et al. 1997 ).

The simplest hypothesis linking Ca²⁺ signals to graded downstream responses is that the magnitude of the Ca²⁺ transient reflects the magnitude of the stimulus and determines the degree of the response. Malho et al. 1998 have collated Ca²⁺ transient data pertaining to 11 different stimuli and point out that with respect to lag phase, rise time, and duration, each [Ca²⁺]_c signal possesses distinct characteristics that could be viewed as an identifying fingerprint of the stimulus. For example, the lag phase in response to wind/touch is imperceptible, the rise time is <1 sec, and the duration of the transient only 15 sec, whereas hypo-osmotic shock in tobacco cells produces a lag phase of 30 sec, followed by a rise time of 60 sec and signal duration of 150 sec. The magnitude of hypo-osmotically induced Ca²⁺ transients has been shown to depend on the size of the hypo-osmotic shock (Takahashi et al. 1997 ; Brownlee et al. 1999 ). In tobacco, the hypo-osmotic Ca²⁺ transient showed biphasic behavior with a slow, small elevation preceding a larger, faster transient elevation. Both phases were dependent on the presence of extracellular Ca²⁺, although they showed differential sensitivities to the vacuolar-type H⁺-ATPase inhibitor bafilomycin and the protein kinase inhibitor K-252a, suggesting the involvement of different mechanisms for elevating Ca²⁺. The data also suggested that Ca²⁺-independent phosphorylation was required as part of the osmosensing mechanism. Recently, it was shown that the initial phase resulted from influx from the external medium, whereas the larger transient elevation reflected release of Ca²⁺ from intracellular stores (Cessna et al. 1998 ). In Arabidopsis, the magnitude of Ca²⁺ transients arising from drought or oxidative stress could be influenced by prior drought or oxidative treatments (Knight et al. 1997 , Knight et al. 1998 ). These different Ca²⁺ signals correlated well with changes in osmotic stress–induced patterns of gene expression and the acquisition of osmotic stress tolerance.

However, a more complex relationship appears to exist between Ca²⁺ signals and the downstream responses in plants. Thus, osmotic (mannitol) and salt stress can each induce Ca²⁺ transients of similar magnitude and duration, with different levels of expression of the p5cs gene, which encodes for an enzyme involved in proline synthesis (Knight et al. 1997 ). These findings suggest that factors other than Ca²⁺ are involved in discriminating between the two response pathways. A further complication in interpreting Ca²⁺ signals in terms of a simple response has been demonstrated in soybean in response to UV and red light. Specifically, phytochrome control of the gene encoding chalcone synthase is regulated positively by cGMP and negatively by Ca²⁺/calmodulin, whereas the response to UV light was regulated positively by Ca²⁺/calmodulin (Frohnmeyer et al. 1998 ). An explanation as to how Ca²⁺/calmodulin could have opposing effects on the expression of the same gene in the same cell appears to lie in the observation that the responses to UV and red light were temporally separated.

Ca²⁺ Oscillations and Repetitive Spikes
Several plant cell types respond to a variety of physiological and nonphysiological stimuli with repetitive increases in [Ca²⁺]_c (oscillations) (Subbaiah et al. 1994 ; McAinsh et al. 1995 ; Ehrhardt et al. 1996 ; Bauer et al. 1997 , Bauer et al. 1998 ; Schonknecht et al. 1998 ). Whether these represent true Ca²⁺ signals or are the result of perturbations of normal Ca²⁺ homeostasis requires the demonstration of clear downstream responses dependent on the frequency, duration, or amplitude of the oscillations. Downstream responses to repetitive Ca²⁺ signals have been characterized in only a few cases in plants. Repetitive elevations in root hair [Ca²⁺] occur in response to Nod factors (Ehrhardt et al. 1996 ). Anoxic gene expression is preceded by repetitive Ca²⁺ spikes in Arabidopsis roots in anaerobic conditions (Subbaiah et al. 1994 ). Oscillations in the tip-focused Ca²⁺ gradient correlate with growth rate in pollen tubes (see below). In guard cells, Ca²⁺-induced oscillations can be induced by treatments such as changes in external [Ca²⁺] and ABA (McAinsh et al. 1995 ; Staxen et al. 1996 ). The frequency and magnitude of Ca²⁺ oscillations have been shown to influence the stomatal aperture. Both the amplitude and dynamics of the Ca²⁺ transients, moreover, were dependent on the magnitude of the imposed external Ca²⁺ concentration. Transfer to high concentrations of Ca²⁺ (1.0 mM) produced large (up to 859 nM) elevations in [Ca²⁺], whereas lower external [Ca²⁺] gave rise to smaller symmetrical elevations up to 600 nM with a shorter period.

A mechanism for generating specificity from different patterns of Ca²⁺ oscillations has been proposed (Goldbeter et al. 1990 ; McAinsh and Hetherington 1998 ) that involves the action of a Ca²⁺-dependent phosphatase and a Ca²⁺-independent protein kinase. Changes in the pattern of Ca²⁺ oscillations would be reflected in the degree of phosphorylation of target proteins leading to different responses.

Spatially Localized Ca²⁺ Signals
A further mechanism by which Ca²⁺ signals can exert specific effects, and one that is poorly understood in many aspects of plant signal transduction, involves the localization of the signal to a specific subcellular region. Repetitive Ca²⁺ signals elicited by Nod factors localized to the nuclear region of root hairs (Ehrhardt et al. 1996 ), thereby revealing spatial separation from the apical Ca²⁺ signals involved in root hair growth (see below). The use of aequorin, targeted separately to the chloroplast or cytosol, has revealed the presence of circadian oscillations of chloroplast and cytosolic Ca²⁺ after transfer from light to darkness (Johnson et al. 1995 ). In contrast, heat shock was shown to induce prolonged elevations of cytosolic, but not chloroplast, [Ca²⁺] in tobacco (Gong et al. 1998 ).

In animal cells, many Ca²⁺ signals have been shown to propagate as waves of elevated [Ca²⁺]. These initiate at a defined location and propagate as release of Ca²⁺ from intracellular stores (Jaffe 1995 ). In contrast, there are few examples of Ca²⁺ waves in plants. The hypo-osmotically induced Ca²⁺ transient in Fucus rhizoid cells propagates as a wave of elevated [Ca²⁺] that initiates at the extreme rhizoid apex and involves Ca²⁺ influx at apical regions and Ca²⁺ release from subapical intracellular stores (Taylor et al. 1996 ). The rate of propagation is at least 5 to 10 µm sec^-1, comparable to the propagation velocities of waves of intracellular Ca²⁺ release observed in a variety of animal systems (Jaffe 1995 ). No similar physiologically induced Ca²⁺ waves have been characterized yet in other plant systems, although a wave of intracellular Ca²⁺ release can be induced in Papaver pollen tubes in response to photorelease of caged InsP₃. Preliminary evidence also exists for the occurrence of a centripetally directed Ca²⁺ wave in electrically stimulated guard cells (Grabov and Blatt 1998 ). The activation voltage, threshold amplitude, and duration of this Ca²⁺ signal were affected by the presence of ABA. In animal cells, Ca²⁺ waves propagate via release of Ca²⁺ from the ER. The domination of many higher plant cells by a large central vacuole might be one reason why few Ca²⁺ waves have been observed. Accordingly, in both Fucus and pollen tubes, Ca²⁺ waves propagate through regions that contain ER but no large vacuole. Evidence for the involvement of different intracellular Ca²⁺ pools that may reflect spatially distinct Ca²⁺ signals comes from pharmacological studies of aequorin-transformed plants and the use of aequorin targeted to different cellular locations. As seen in Figure 2, for example, both vacuolar and plasma membrane Ca²⁺ fluxes are implicated in cold shock and drought Ca²⁺ signals. In contrast, a different Ca²⁺ pool appears to be involved in response to oxidative signals (Price et al. 1994 ). Figure 2 provides additional examples in which the source or location of a specific Ca²⁺ signal is known.

View larger version (71K): [in this window] [in a new window]   Figure 2. Schematic Representation of the Origins and Locations of Calcium Signals in Response to Specific Stimuli. Signals originate from the external medium, ER, mitochondrion, chloroplast, and vacuole and can be localized or global, cytosolic, nuclear and perinuclear, or chloroplastic. Red arrows indicate the principal Ca2+ fluxes. See the text and Table 1 for discussion and references.

Gradients in Apically Growing Systems
Tip-focused Ca²⁺ gradients have been described in several types of pollen tubes (Rathore et al. 1991 ; Miller et al. 1992 ; Franklin-Tong et al. 1997 ), root hairs (Hermann and Felle 1995 ; Felle and Hepler 1997 ; Wymer et al. 1997 ), and algal rhizoids (Brownlee and Wood 1986 ; Brownlee and Pulsford 1988 ; Shaw and Quatrano 1996 ; Taylor et al. 1996 ). Ca²⁺ at the growing apex can reach micromolar levels. The Ca²⁺ gradient in pollen tubes correlates closely with growth (Rathore et al. 1991 ; Miller et al. 1992 ). Accordingly, microinjection of the Ca²⁺ buffer dibromoBAPTA into pollen tubes prevented growth and concomitantly abolished the Ca²⁺ gradient (Miller et al. 1992 ). Agapanthus undulatus pollen tubes could be oriented according to localized elevations of [Ca²⁺] induced by treatments such as photorelease of caged Ca²⁺ at the pollen tube apex (Malho et al. 1994 , 1996). Tip-localized Ca²⁺ pulses were shown to coincide with oscillations in growth rate (Messerli and Robinson 1997 ). It is tempting to speculate that the magnitude and frequency of the Ca²⁺ oscillations provide information that regulates growth rate (Holdaway-Clarke et al. 1997 ). Oscillatory increases in growth rate were accompanied by in-phase increases in Ca²⁺ at the pollen tube apex. However, measurements of Ca²⁺ influx at the growing apex, by using an extracellular Ca²⁺-selective microelectrode, showed that oscillations in Ca²⁺ influx occurred with the same frequency as, but out of phase with, growth and [Ca²⁺]_c. This could reflect Ca²⁺ influx associated with the refilling of a store, such as the ER, although the ER of pollen tubes is not particularly concentrated at the apex (Lancelle and Hepler 1992 ). Alternatively, the observed Ca²⁺ influx could reflect changes in Ca²⁺ binding to different cell wall components laid down during oscillatory growth pulses (Holdaway-Clarke et al. 1997 ). The significance of Ca²⁺ oscillations and pulsatile pollen tube growth is not clear inasmuch as pollen tubes can grow normally without manifesting Ca²⁺ oscillations (Holdaway-Clarke et al. 1997 ; Messerli and Robinson 1997 ).

Indirect evidence for the involvement of Ca²⁺-permeable channels in facilitating Ca²⁺ influx at the pollen tube apex comes from the use of the Mn²⁺-quench technique (Malho et al. 1995 ), whereby entry of Mn²⁺ through putative Ca²⁺-permeable channels quenches Ca²⁺ dye fluorescence. Unfortunately, attempts to apply the patch–clamp technique to pollen tubes for definitive demonstration of Ca²⁺-permeable channels so far have been unsuccessful, because protoplasts from the pollen tube apex remain hypersecretory, thereby preventing Giga-ohm seal formation between the membrane and the patch–clamp electrode. Vibrating Ca²⁺-selective microelectrode studies also have shown preferential Ca²⁺ influx at the root hair apex (Hermann and Felle 1995 ; Jones et al. 1995 ). Both the apically localized [Ca²⁺] elevation and root hair growth were prevented by verapamil, suggesting that Ca²⁺-permeable channels might be involved in maintenance of the gradient (Wymer et al. 1997 ). Moreover, Mn²⁺-quench experiments indicated that a significant component of the apical Ca²⁺ gradient was due to Ca²⁺ influx. The root hair system should be more tractable than is the pollen tube for patch–clamp studies of Ca²⁺ channels and signaling. Ca²⁺ influx in Fucus rhizoids, which might involve the activity of mechanosensitive Ca²⁺-permeable channels, is involved in maintaining the apical Ca²⁺ gradient (Taylor et al. 1996 ). The apical Ca²⁺ gradient in Fucus correlates well with the presence of actin and calmodulin at the rhizoid apex (Henry et al. 1996 ; Love et al. 1997 ). Moreover, actin has been shown to localize to sites of attachment of the plasma membrane to the cell wall (Henry et al. 1996 ). Whereas earlier Ca²⁺ imaging experiments suggested that [Ca²⁺] becomes elevated at the rhizoid pole before germination of the rhizoid cell (Berger and Brownlee 1993 ), it was not clear whether this occurred before or during fixation of the polar axis. A potential problem with imaging Ca²⁺ gradients during the early stages of polarization is the buffering of small localized Ca²⁺ elevations by the dye. Pu and Robinson 1998 used an indirect method to investigate early Ca²⁺ gradients in polarizing Pelvetia zygotes by ratio imaging of zygotes injected with low concentrations of the nonratiometric indicator Calcium Crimson against images of zygotes loaded with rhodamine B. [Ca²⁺] elevations could be detected within 1 hr of illumination with unilateral light, suggesting that the Ca²⁺ gradient could form before polar axis fixation.

The Ca²⁺ gradient in root hairs could be detected only during growth and not during root hair initiation (Wymer et al. 1997 ), implying a role for Ca²⁺ in growth after initiation. Although pollen tube orientation can be manipulated by treatments that cause asymmetric distribution of Ca²⁺, root hairs tend to extend along a predefined polar axis. Perturbations in growth direction induced by asymmetric photorelease of a caged Ca²⁺ ionophore (A23187) induced only transient changes in the direction of growth, after which elongation resumed along the original axis (Bibikova and Gilroy 1997 ). Cytoskeletal architecture might underlie the inherent polarity and morphogenesis of the extending root hair. In contrast to the pollen tube (Miller et al. 1996 ), actin localizes to the growing root hair apex (Jiang et al. 1997 ). However, it is also clear that root hairs tend to grow at fixed angles relative to the main root, indicating that some reference signal is used to monitor the position of the growing tip with respect to the main root axis.

	FUTURE PROSPECTS

TOP INTRODUCTION ENCODING CALCIUM SIGNALS: AN... TARGETS OF CALCIUM SIGNALS DECODING CALCIUM SIGNALS: THE... FUTURE PROSPECTS REFERENCES

Research is still needed to identify and clone the different carriers and pumps involved in Ca²⁺ efflux from the cytosol. For example, there is biochemical evidence for a calmodulin-regulated Ca²⁺ pump in the plasma membrane (e.g., Askerlund 1997 ; Hwang et al. 1997 ), but the corresponding gene has not been identified. An even larger gap in our knowledge concerns the absence of insight into the molecular identity of plant Ca²⁺-permeable channels. The low abundance and (probable) large size of Ca²⁺ channels make them poor candidates for identification from cDNA libraries. However, candidate genes for both Ca²⁺ transporters and channels that are both expected and novel will likely emerge from genome-sequencing projects in the near future.

The greatest challenge ahead is to understand the isoform-specific functions of different transporters and channels. We have entered the era of "pathway quantification" (Koshland 1998 ), where fundamental advances will require a detailed investigation into how Ca²⁺ fluxes are controlled in specific regions of the cell. Toward that goal, research is needed to determine the subcellular location, biochemical activity, and regulatory properties of each transporter and channel.

It is clear that genetics will be required to achieve an integrated understanding of each transporter in cellular and whole-plant physiology. Two important genetic strategies already have begun. The first is a "reverse genetic" approach to identify mutations in known Ca²⁺ transporters in Arabidopsis. This approach has yielded the first genetic mutation of a Ca²⁺ transporter in higher plants, identified as a T-DNA insertion into the ACA3/ECA1 gene (Krysan et al. 1996 ). The second approach is to engineer transgenic plants with altered transporters designed to activate or block specific Ca²⁺ transport pathways. For example, the ACA2p pump has been engineered with a mutation that makes it constitutively active (Harper et al. 1998 ). Such genetic tools are providing us with new strategies to modify specific transport pathways in transgenic plants, without the inherent problems associated with modifying calcium transients with potentially nonspecific inhibitors. The use of fluorescent indicators and nontargeted aequorin to monitor global changes in [Ca²⁺]_c can provide only limited data on the spatiotemporal characteristics of Ca²⁺ signals. Information about localized [Ca²⁺] changes can come only from highly resolved confocal imaging studies or the use of targeted indicators. The application of new indicators, such as ratioable fluorescent cameleons (Miyawaki et al. 1997 ), is likely to provide much-needed information on Ca²⁺ signaling. This indicator offers exciting possibilities for combined studies of gene expression and interaction of Ca²⁺ signals with specific components of signaling pathways.

	ACKNOWLEDGMENTS

We thank Dr. Helen V. Coombs for assistance with manuscript preparation.

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				I. Y. Perera, C.-Y. Hung, C. D. Moore, J. Stevenson-Paulik, and W. F. Boss Transgenic Arabidopsis Plants Expressing the Type 1 Inositol 5-Phosphatase Exhibit Increased Drought Tolerance and Altered Abscisic Acid Signaling PLANT CELL, October 1, 2008; 20(10): 2876 - 2893. [Abstract] [Full Text] [PDF]

				J. S. Busse, S. Ozgen, and J. P. Palta Influence of Root Zone Calcium on Subapical Necrosis in Potato Shoot Cultures: Localization of Injury at the Tissue and Cellular Levels J. Amer. Soc. Hort. Sci., September 1, 2008; 133(5): 653 - 662. [Abstract] [Full Text] [PDF]

				K. Lee, E. H. Song, H. S. Kim, J. H. Yoo, H. J. Han, M. S. Jung, S. M. Lee, K. E. Kim, M. C. Kim, M. J. Cho, et al. Regulation of MAPK Phosphatase 1 (AtMKP1) by Calmodulin in Arabidopsis J. Biol. Chem., August 29, 2008; 283(35): 23581 - 23588. [Abstract] [Full Text] [PDF]

				X. Li, S. Chanroj, Z. Wu, S. M. Romanowsky, J. F. Harper, and H. Sze A Distinct Endosomal Ca2+/Mn2+ Pump Affects Root Growth through the Secretory Process Plant Physiology, August 1, 2008; 147(4): 1675 - 1689. [Abstract] [Full Text] [PDF]

				R. F. Mills, M. L. Doherty, R. L. Lopez-Marques, T. Weimar, P. Dupree, M. G. Palmgren, J. K. Pittman, and L. E. Williams ECA3, a Golgi-Localized P2A-Type ATPase, Plays a Crucial Role in Manganese Nutrition in Arabidopsis Plant Physiology, January 1, 2008; 146(1): 116 - 128. [Abstract] [Full Text] [PDF]

				S. H. Hung, C. C. Wang, S. V. Ivanov, V. Alexieva, and C. W. Yu Repetition of Hydrogen Peroxide Treatment Induces a Chilling Tolerance Comparable to Cold Acclimation in Mung Bean J. Amer. Soc. Hort. Sci., November 1, 2007; 132(6): 770 - 776. [Abstract] [Full Text] [PDF]

				S.-Y. Zhu, X.-C. Yu, X.-J. Wang, R. Zhao, Y. Li, R.-C. Fan, Y. Shang, S.-Y. Du, X.-F. Wang, F.-Q. Wu, et al. Two Calcium-Dependent Protein Kinases, CPK4 and CPK11, Regulate Abscisic Acid Signal Transduction in Arabidopsis PLANT CELL, October 1, 2007; 19(10): 3019 - 3036. [Abstract] [Full Text] [PDF]

				H. Mei, J. Zhao, J. K. Pittman, J. Lachmansingh, S. Park, and K. D. Hirschi In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1 J. Exp. Bot., September 26, 2007; (2007) erm190v1. [Abstract] [Full Text] [PDF]

				X. Pang, T. Halaly, O. Crane, T. Keilin, A. Keren-Keiserman, A. Ogrodovitch, D. Galbraith, and E. Or Involvement of calcium signalling in dormancy release of grape buds J. Exp. Bot., September 1, 2007; 58(12): 3249 - 3262. [Abstract] [Full Text] [PDF]

				J. Ishijima, N. Nagasaki, M. Maeshima, and M. Miyano RVCaB, a Calcium-binding Protein in Radish Vacuoles, is Predominantly an Unstructured Protein with a Polyproline Type II Helix J. Biochem., August 1, 2007; 142(2): 201 - 211. [Abstract] [Full Text] [PDF]

				Y. Xiang, Y. Huang, and L. Xiong Characterization of Stress-Responsive CIPK Genes in Rice for Stress Tolerance Improvement Plant Physiology, July 1, 2007; 144(3): 1416 - 1428. [Abstract] [Full Text] [PDF]

				H. C. Park, M. L. Kim, S. M. Lee, J. D. Bahk, D.-J. Yun, C. O. Lim, J. C. Hong, S. Y. Lee, M. J. Cho, and W. S. Chung Pathogen-induced binding of the soybean zinc finger homeodomain proteins GmZF-HD1 and GmZF-HD2 to two repeats of ATTA homeodomain binding site in the calmodulin isoform 4 (GmCaM4) promoter Nucleic Acids Res., June 28, 2007; 35(11): 3612 - 3623. [Abstract] [Full Text] [PDF]

				L. L. Ge, H. Q. Tian, and S. D. Russell Calcium function and distribution during fertilization in angiosperms Am. J. Botany, June 1, 2007; 94(6): 1046 - 1060. [Abstract] [Full Text] [PDF]

				A. T. Fuglsang, Y. Guo, T. A. Cuin, Q. Qiu, C. Song, K. A. Kristiansen, K. Bych, A. Schulz, S. Shabala, K. S. Schumaker, et al. Arabidopsis Protein Kinase PKS5 Inhibits the Plasma Membrane H+-ATPase by Preventing Interaction with 14-3-3 Protein PLANT CELL, May 1, 2007; 19(5): 1617 - 1634. [Abstract] [Full Text] [PDF]

				W. R. Swindell The Association Among Gene Expression Responses to Nine Abiotic Stress Treatments in Arabidopsis thaliana Genetics, December 1, 2006; 174(4): 1811 - 1824. [Abstract] [Full Text] [PDF]

				Y. Leshem, N. Melamed-Book, O. Cagnac, G. Ronen, Y. Nishri, M. Solomon, G. Cohen, and A. Levine Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance PNAS, November 21, 2006; 103(47): 18008 - 18013. [Abstract] [Full Text] [PDF]

				T. Hewezi, M. Leger, W. El Kayal, and L. Gentzbittel Transcriptional profiling of sunflower plants growing under low temperatures reveals an extensive down-regulation of gene expression associated with chilling sensitivity J. Exp. Bot., September 1, 2006; 57(12): 3109 - 3122. [Abstract] [Full Text] [PDF]

				N. FEDOROFF Redox Regulatory Mechanisms in Cellular Stress Responses Ann. Bot., August 1, 2006; 98(2): 289 - 300. [Abstract] [Full Text] [PDF]

				J. Liu, S. S. Miller, M. Graham, B. Bucciarelli, C. M. Catalano, D. J. Sherrier, D. A. Samac, S. Ivashuta, M. Fedorova, P. Matsumoto, et al. Recruitment of Novel Calcium-Binding Proteins for Root Nodule Symbiosis in Medicago truncatula Plant Physiology, May 1, 2006; 141(1): 167 - 177. [Abstract] [Full Text] [PDF]

				M. E. Maffei, A. Mithofer, G.-I. Arimura, H. Uchtenhagen, S. Bossi, C. M. Bertea, L. S. Cucuzza, M. Novero, V. Volpe, S. Quadro, et al. Effects of Feeding Spodoptera littoralis on Lima Bean Leaves. III. Membrane Depolarization and Involvement of Hydrogen Peroxide Plant Physiology, March 1, 2006; 140(3): 1022 - 1035. [Abstract] [Full Text] [PDF]

				I. Y. Perera, C.-Y. Hung, S. Brady, G. K. Muday, and W. F. Boss A Universal Role for Inositol 1,4,5-Trisphosphate-Mediated Signaling in Plant Gravitropism Plant Physiology, February 1, 2006; 140(2): 746 - 760. [Abstract] [Full Text] [PDF]

				X.-C. Yu, M.-J. Li, G.-F. Gao, H.-Z. Feng, X.-Q. Geng, C.-C. Peng, S.-Y. Zhu, X.-J. Wang, Y.-Y. Shen, and D.-P. Zhang Abscisic Acid Stimulates a Calcium-Dependent Protein Kinase in Grape Berry Plant Physiology, February 1, 2006; 140(2): 558 - 579. [Abstract] [Full Text] [PDF]

				Y.-J. Wang, J.-N. Yu, T. Chen, Z.-G. Zhang, Y.-J. Hao, J.-S. Zhang, and S.-Y. Chen Functional analysis of a putative Ca2+ channel gene TaTPC1 from wheat J. Exp. Bot., December 1, 2005; 56(422): 3051 - 3060. [Abstract] [Full Text] [PDF]

				S. H. Ok, H. J. Jeong, J. M. Bae, J.-S. Shin, S. Luan, and K.-N. Kim Novel CIPK1-Associated Proteins in Arabidopsis Contain an Evolutionarily Conserved C-Terminal Region That Mediates Nuclear Localization Plant Physiology, September 1, 2005; 139(1): 138 - 150. [Abstract] [Full Text] [PDF]

				Y.-s. Hwang, P. C. Bethke, Y. H. Cheong, H.-S. Chang, T. Zhu, and R. L. Jones A Gibberellin-Regulated Calcineurin B in Rice Localizes to the Tonoplast and Is Implicated in Vacuole Function Plant Physiology, July 1, 2005; 138(3): 1347 - 1358. [Abstract] [Full Text] [PDF]

				Z.-l. Shang, L.-g. Ma, H.-l. Zhang, R.-r. He, X.-c. Wang, S.-j. Cui, and D.-y. Sun Ca2+ Influx into Lily Pollen Grains Through a Hyperpolarization-activated Ca2+-permeable Channel Which Can be Regulated by Extracellular CaM Plant Cell Physiol., April 1, 2005; 46(4): 598 - 608. [Abstract] [Full Text] [PDF]

				R. S. Tegg, L. Melian, C. R. Wilson, and S. Shabala Plant Cell Growth and Ion Flux Responses to the Streptomycete Phytotoxin Thaxtomin A: Calcium and Hydrogen Flux Patterns Revealed by the Non-invasive MIFE Technique Plant Cell Physiol., April 1, 2005; 46(4): 638 - 648. [Abstract] [Full Text] [PDF]

				T. Asano, N. Tanaka, G. Yang, N. Hayashi, and S. Komatsu Genome-wide Identification of the Rice Calcium-dependent Protein Kinase and its Closely Related Kinase Gene Families: Comprehensive Analysis of the CDPKs Gene Family in Rice Plant Cell Physiol., February 1, 2005; 46(2): 356 - 366. [Abstract] [Full Text] [PDF]

				V. Chinnusamy, A. Jagendorf, and J.-K. Zhu Understanding and Improving Salt Tolerance in Plants Crop Sci., January 31, 2005; 45(2): 437 - 448. [Abstract] [Full Text] [PDF]

				Y.-F. Wang, L.-M. Fan, W.-Z. Zhang, W. Zhang, and W.-H. Wu Ca2+-Permeable Channels in the Plasma Membrane of Arabidopsis Pollen Are Regulated by Actin Microfilaments Plant Physiology, December 1, 2004; 136(4): 3892 - 3904. [Abstract] [Full Text] [PDF]

				E. Karita, H. Yamakawa, I. Mitsuhara, K. Kuchitsu, and Y. Ohashi Three Types of Tobacco Calmodulins Characteristically Activate Plant NAD Kinase at Different Ca2+ Concentrations and pHs Plant Cell Physiol., October 15, 2004; 45(10): 1371 - 1379. [Abstract] [Full Text] [PDF]

				C. R. Jeter, W. Tang, E. Henaff, T. Butterfield, and S. J. Roux Evidence of a Novel Cell Signaling Role for Extracellular Adenosine Triphosphates and Diphosphates in Arabidopsis PLANT CELL, October 1, 2004; 16(10): 2652 - 2664. [Abstract] [Full Text] [PDF]

				K. D. Hirschi The Calcium Conundrum. Both Versatile Nutrient and Specific Signal Plant Physiology, September 1, 2004; 136(1): 2438 - 2442. [Full Text] [PDF]

				X. Cai and J. Lytton The Cation/Ca2+ Exchanger Superfamily: Phylogenetic Analysis and Structural Implications Mol. Biol. Evol., September 1, 2004; 21(9): 1692 - 1703. [Abstract] [Full Text] [PDF]

				G. K. Pandey, Y. H. Cheong, K.-N. Kim, J. J. Grant, L. Li, W. Hung, C. D'Angelo, S. Weinl, J. Kudla, and S. Luan The Calcium Sensor Calcineurin B-Like 9 Modulates Abscisic Acid Sensitivity and Biosynthesis in Arabidopsis PLANT CELL, July 1, 2004; 16(7): 1912 - 1924. [Abstract] [Full Text] [PDF]

				A. K. Azad, Y. Sawa, T. Ishikawa, and H. Shibata Phosphorylation of Plasma Membrane Aquaporin Regulates Temperature-Dependent Opening of Tulip Petals Plant Cell Physiol., May 1, 2004; 45(5): 608 - 617. [Abstract] [Full Text] [PDF]

				M. Brault, Z. Amiar, A.-M. Pennarun, M. Monestiez, Z. Zhang, D. Cornel, O. Dellis, H. Knight, F. Bouteau, and J.-P. Rona Plasma Membrane Depolarization Induced by Abscisic Acid in Arabidopsis Suspension Cells Involves Reduction of Proton Pumping in Addition to Anion Channel Activation, Which Are Both Ca2+ Dependent Plant Physiology, May 1, 2004; 135(1): 231 - 243. [Abstract] [Full Text] [PDF]

				E. Cholewa and C. A. Peterson Evidence for Symplastic Involvement in the Radial Movement of Calcium in Onion Roots Plant Physiology, April 1, 2004; 134(4): 1793 - 1802. [Abstract] [Full Text] [PDF]

				D. Gao, M. R. Knight, A. J. Trewavas, B. Sattelmacher, and C. Plieth Self-Reporting Arabidopsis Expressing pH and [Ca2+] Indicators Unveil Ion Dynamics in the Cytoplasm and in the Apoplast under Abiotic Stress Plant Physiology, March 1, 2004; 134(3): 898 - 908. [Abstract] [Full Text] [PDF]

				A. P. Yamniuk and H. J. Vogel Structurally Homologous Binding of Plant Calmodulin Isoforms to the Calmodulin-binding Domain of Vacuolar Calcium-ATPase J. Biol. Chem., February 27, 2004; 279(9): 7698 - 7707. [Abstract] [Full Text] [PDF]

				J. H. Yoo, M. S. Cheong, C. Y. Park, B. C. Moon, M. C. Kim, Y. H. Kang, H. C. Park, M. S. Choi, J. H. Lee, W. Y. Jung, et al. Regulation of the Dual Specificity Protein Phosphatase, DsPTP1, through Interactions with Calmodulin J. Biol. Chem., January 9, 2004; 279(2): 848 - 858. [Abstract] [Full Text] [PDF]

				H. Yamakawa, S. Katou, S. Seo, I. Mitsuhara, H. Kamada, and Y. Ohashi Plant MAPK Phosphatase Interacts with Calmodulins J. Biol. Chem., January 9, 2004; 279(2): 928 - 936. [Abstract] [Full Text] [PDF]

				T. Kamiya and M. Maeshima Residues in Internal Repeats of the Rice Cation/H+ Exchanger Are Involved in the Transport and Selection of Cations J. Biol. Chem., January 2, 2004; 279(1): 812 - 819. [Abstract] [Full Text] [PDF]

				V. Chinnusamy, K. Schumaker, and J.-K. Zhu Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants J. Exp. Bot., January 2, 2004; 55(395): 225 - 236. [Abstract] [Full Text] [PDF]

				L. Rubio, A. Rosado, A. Linares-Rueda, O. Borsani, M. J. Garcia-Sanchez, V. Valpuesta, J. A. Fernandez, and M. A. Botella Regulation of K+ Transport in Tomato Roots by the TSS1 Locus. Implications in Salt Tolerance Plant Physiology, January 1, 2004; 134(1): 452 - 459. [Abstract] [Full Text] [PDF]

				R. Catala, E. Santos, J. M. Alonso, J. R. Ecker, J. M. Martinez-Zapater, and J. Salinas Mutations in the Ca2+/H+ Transporter CAX1 Increase CBF/DREB1 Expression and the Cold-Acclimation Response in Arabidopsis PLANT CELL, December 1, 2003; 15(12): 2940 - 2951. [Abstract] [Full Text] [PDF]

				M. K. Alsheikh, B. J. Heyen, and S. K. Randall Ion Binding Properties of the Dehydrin ERD14 Are Dependent upon Phosphorylation J. Biol. Chem., October 17, 2003; 278(42): 40882 - 40889. [Abstract] [Full Text] [PDF]

				N. Mitsuda, T. Isono, and M. H. Sato Arabidopsis CAMTA Family Proteins Enhance V-PPase Expression in Pollen Plant Cell Physiol., October 15, 2003; 44(10): 975 - 981. [Abstract] [Full Text] [PDF]

				P. J. WHITE and M. R. BROADLEY Calcium in Plants Ann. Bot., October 1, 2003; 92(4): 487 - 511. [Abstract] [Full Text] [PDF]

				C. K.-Y. NG and M. R. MCAINSH Encoding Specificity in Plant Calcium Signalling: Hot-spotting the Ups and Downs and Waves Ann. Bot., October 1, 2003; 92(4): 477 - 485. [Abstract] [Full Text] [PDF]

				V. Vanoosthuyse, G. Tichtinsky, C. Dumas, T. Gaude, and J. M. Cock Interaction of Calmodulin, a Sorting Nexin and Kinase-Associated Protein Phosphatase with the Brassica oleracea S Locus Receptor Kinase Plant Physiology, October 1, 2003; 133(2): 919 - 929. [Abstract] [Full Text] [PDF]

				Y. H. Cheong, K.-N. Kim, G. K. Pandey, R. Gupta, J. J. Grant, and S. Luan CBL1, a Calcium Sensor That Differentially Regulates Salt, Drought, and Cold Responses in Arabidopsis PLANT CELL, August 1, 2003; 15(8): 1833 - 1845. [Abstract] [Full Text] [PDF]

				A. Harada, T. Sakai, and K. Okada phot1 and phot2 mediate blue light-induced transient increases in cytosolic Ca2+ differently in Arabidopsis leaves PNAS, July 8, 2003; 100(14): 8583 - 8588. [Abstract] [Full Text] [PDF]

				H.-T. Liu, B. Li, Z.-L. Shang, X.-Z. Li, R.-L. Mu, D.-Y. Sun, and R.-G. Zhou Calmodulin Is Involved in Heat Shock Signal Transduction in Wheat Plant Physiology, July 1, 2003; 132(3): 1186 - 1195. [Abstract] [Full Text] [PDF]

				L. V. Nazarenko, I. M. Andreev, A. A. Lyukevich, T. V. Pisareva, and D. A. Los Calcium release from Synechocystis cells induced by depolarization of the plasma membrane: MscL as an outward Ca2+ channel Microbiology, May 1, 2003; 149(5): 1147 - 1153. [Abstract] [Full Text] [PDF]

				M. R. Broadley, H. C. Bowen, H. L. Cotterill, J. P. Hammond, M. C. Meacham, A. Mead, and P. J. White Variation in the shoot calcium content of angiosperms J. Exp. Bot., May 1, 2003; 54(386): 1431 - 1446. [Abstract] [Full Text] [PDF]

				V. S. Anil, A. C. Harmon, and K. S. Rao Temporal Association of Ca2+-Dependent Protein Kinase with Oil Bodies during Seed Development in Santalum album L.: Its Biochemical Characterization and Significance Plant Cell Physiol., April 15, 2003; 44(4): 367 - 376. [Abstract] [Full Text] [PDF]

				S. L. Shaw and S. R. Long Nod Factor Elicits Two Separable Calcium Responses in Medicago truncatula Root Hair Cells Plant Physiology, March 1, 2003; 131(3): 976 - 984. [Abstract] [Full Text] [PDF]

				N.-H. Cheng, J. K. Pittman, B. J. Barkla, T. Shigaki, and K. D. Hirschi The Arabidopsis cax1 Mutant Exhibits Impaired Ion Homeostasis, Development, and Hormonal Responses and Reveals Interplay among Vacuolar Transporters PLANT CELL, February 1, 2003; 15(2): 347 - 364. [Abstract] [Full Text] [PDF]

				K.-N. Kim, Y. H. Cheong, J. J. Grant, G. K. Pandey, and S. Luan CIPK3, a Calcium Sensor-Associated Protein Kinase That Regulates Abscisic Acid and Cold Signal Transduction in Arabidopsis PLANT CELL, February 1, 2003; 15(2): 411 - 423. [Abstract] [Full Text] [PDF]

				C. C. SUBBAIAH and M. M. SACHS Molecular and Cellular Adaptations of Maize to Flooding Stress Ann. Bot., January 2, 2003; 91(2): 119 - 127. [Abstract] [Full Text] [PDF]

				A. H. Knoll and A. H. Knoll Biomineralization and Evolutionary History Reviews in Mineralogy and Geochemistry, January 1, 2003; 54(1): 329 - 356. [Full Text] [PDF]

				B. Klusener, J. J. Young, Y. Murata, G. J. Allen, I. C. Mori, V. Hugouvieux, and J. I. Schroeder Convergence of Calcium Signaling Pathways of Pathogenic Elicitors and Abscisic Acid in Arabidopsis Guard Cells Plant Physiology, December 1, 2002; 130(4): 2152 - 2163. [Abstract] [Full Text] [PDF]

				P. J. White and R. J. Davenport The Voltage-Independent Cation Channel in the Plasma Membrane of Wheat Roots Is Permeable to Divalent Cations and May Be Involved in Cytosolic Ca2+ Homeostasis Plant Physiology, November 1, 2002; 130(3): 1386 - 1395. [Abstract] [Full Text] [PDF]

				D. Lecourieux, C. Mazars, N. Pauly, R. Ranjeva, and A. Pugin Analysis and Effects of Cytosolic Free Calcium Increases in Response to Elicitors in Nicotiana plumbaginifolia Cells PLANT CELL, October 1, 2002; 14(10): 2627 - 2641. [Abstract] [Full Text] [PDF]

				B. J. Heyen, M. K. Alsheikh, E. A. Smith, C. F. Torvik, D. F. Seals, and S. K. Randall The Calcium-Binding Activity of a Vacuole-Associated, Dehydrin-Like Protein Is Regulated by Phosphorylation Plant Physiology, October 1, 2002; 130(2): 675 - 687. [Abstract] [Full Text] [PDF]

				J. K. Pittman, C. S. Sreevidya, T. Shigaki, H. Ueoka-Nakanishi, and K. D. Hirschi Distinct N-Terminal Regulatory Domains of Ca2+/H+ Antiporters Plant Physiology, October 1, 2002; 130(2): 1054 - 1062. [Abstract] [Full Text] [PDF]

				Z. Wu, F. Liang, B. Hong, J. C. Young, M. R. Sussman, J. F. Harper, and H. Sze An Endoplasmic Reticulum-Bound Ca2+/Mn2+ Pump, ECA1, Supports Plant Growth and Confers Tolerance to Mn2+ Stress Plant Physiology, September 1, 2002; 130(1): 128 - 137. [Abstract] [Full Text] [PDF]

				T. K. Matsumoto, A. J. Ellsmore, S. G. Cessna, P. S. Low, J. M. Pardo, R. A. Bressan, and P. M. Hasegawa An Osmotically Induced Cytosolic Ca2+ Transient Activates Calcineurin Signaling to Mediate Ion Homeostasis and Salt Tolerance of Saccharomyces cerevisiae J. Biol. Chem., August 30, 2002; 277(36): 33075 - 33080. [Abstract] [Full Text] [PDF]

				I. Y. Perera, J. Love, I. Heilmann, W. F. Thompson, and W. F. Boss Up-Regulation of Phosphoinositide Metabolism in Tobacco Cells Constitutively Expressing the Human Type I Inositol Polyphosphate 5-Phosphatase Plant Physiology, August 1, 2002; 129(4): 1795 - 1806. [Abstract] [Full Text] [PDF]

				J. K. Pittman, T. Shigaki, N.-H. Cheng, and K. D. Hirschi Mechanism of N-terminal Autoinhibition in the Arabidopsis Ca2+/H+ Antiporter CAX1 J. Biol. Chem., July 12, 2002; 277(29): 26452 - 26459. [Abstract] [Full Text] [PDF]

				G. J. Allen, Y. Murata, S. P. Chu, M. Nafisi, and J. I. Schroeder Hypersensitivity of Abscisic Acid-Induced Cytosolic Calcium Increases in the Arabidopsis Farnesyltransferase Mutant era1-2 PLANT CELL, July 1, 2002; 14(7): 1649 - 1662. [Abstract] [Full Text] [PDF]

				A. L. O. Facanha, H. Appelgren, M. Tabish, L. Okorokov, and K. Ekwall The endoplasmic reticulum cation P-type ATPase Cta4p is required for control of cell shape and microtubule dynamics J. Cell Biol., June 10, 2002; 157(6): 1029 - 1040. [Abstract] [Full Text] [PDF]

				S.-H. Cheng, M. R. Willmann, H.-C. Chen, and J. Sheen Calcium Signaling through Protein Kinases. The Arabidopsis Calcium-Dependent Protein Kinase Gene Family Plant Physiology, June 1, 2002; 129(2): 469 - 485. [Abstract] [Full Text] [PDF]

				J. Sai and C. H. Johnson Dark-Stimulated Calcium Ion Fluxes in the Chloroplast Stroma and Cytosol PLANT CELL, June 1, 2002; 14(6): 1279 - 1291. [Abstract] [Full Text] [PDF]

				C. Plieth and A. J. Trewavas Reorientation of Seedlings in the Earth's Gravitational Field Induces Cytosolic Calcium Transients Plant Physiology, June 1, 2002; 129(2): 786 - 796. [Abstract] [Full Text] [PDF]

				M. C. Kim, S. H. Lee, J. K. Kim, H. J. Chun, M. S. Choi, W. S. Chung, B. C. Moon, C. H. Kang, C. Y. Park, J. H. Yoo, et al. Mlo, a Modulator of Plant Defense and Cell Death, Is a Novel Calmodulin-binding Protein. ISOLATION AND CHARACTERIZATION OF A RICE Mlo HOMOLOGUE J. Biol. Chem., May 24, 2002; 277(22): 19304 - 19314. [Abstract] [Full Text] [PDF]

				B.-C. Yoo, J.-Y. Lee, and W. J. Lucas Analysis of the Complexity of Protein Kinases within the Phloem Sieve Tube System. CHARACTERIZATION OF CUCURBITA MAXIMA CALMODULIN-LIKE DOMAIN PROTEIN KINASE 1 J. Biol. Chem., May 3, 2002; 277(18): 15325 - 15332. [Abstract] [Full Text] [PDF]

				L. Xiong, K. S. Schumaker, and J.-K. Zhu Cell Signaling during Cold, Drought, and Salt Stress PLANT CELL, May 1, 2002; 14(90001): S165 - 183. [Full Text] [PDF]

				S. Luan, J. Kudla, M. Rodriguez-Concepcion, S. Yalovsky, and W. Gruissem Calmodulins and Calcineurin B-like Proteins: Calcium Sensors for Specific Signal Response Coupling in Plants PLANT CELL, May 1, 2002; 14(90001): S389 - 400. [Full Text] [PDF]

				D. Sanders, J. Pelloux, C. Brownlee, and J. F. Harper Calcium at the Crossroads of Signaling PLANT CELL, May 1, 2002; 14(90001): S401 - 417. [Full Text] [PDF]

				F. Rutschmann, U. Stalder, M. Piotrowski, C. Oecking, and A. Schaller LeCPK1, a Calcium-Dependent Protein Kinase from Tomato. Plasma Membrane Targeting and Biochemical Characterization Plant Physiology, May 1, 2002; 129(1): 156 - 168. [Abstract] [Full Text] [PDF]

				D. Gong, Z. Gong, Y. Guo, and J.-K. Zhu Expression, Activation, and Biochemical Properties of a Novel Arabidopsis Protein Kinase Plant Physiology, May 1, 2002; 129(1): 225 - 234. [Abstract] [Full Text] [PDF]

				V. S. Reddy, G. S. Ali, and A. S. N. Reddy Genes Encoding Calmodulin-binding Proteins in the Arabidopsis Genome J. Biol. Chem., March 15, 2002; 277(12): 9840 - 9852. [Abstract] [Full Text] [PDF]

				C. Garcia-Mata and L. Lamattina Nitric Oxide and Abscisic Acid Cross Talk in Guard Cells Plant Physiology, March 1, 2002; 128(3): 790 - 792. [Full Text] [PDF]

				A. S. N. Reddy, I. S. Day, S. B. Narasimhulu, F. Safadi, V. S. Reddy, M. Golovkin, and M. J. Harnly Isolation and Characterization of a Novel Calmodulin-binding Protein from Potato J. Biol. Chem., February 1, 2002; 277(6): 4206 - 4214. [Abstract] [Full Text] [PDF]

				T. Shigaki, N.-h. Cheng, J. K. Pittman, and K. Hirschi Structural Determinants of Ca2+ Transport in the Arabidopsis H+/Ca2+ Antiporter CAX1 J. Biol. Chem., November 9, 2001; 276(46): 43152 - 43159. [Abstract] [Full Text] [PDF]

				Y. Saijo, N. Kinoshita, K. Ishiyama, S. Hata, J. Kyozuka, T. Hayakawa, T. Nakamura, K. Shimamoto, T. Yamaya, and K. Izui A Ca2+-Dependent Protein Kinase that Endows Rice Plants with Cold- and Salt-Stress Tolerance Functions in Vascular Bundles Plant Cell Physiol., November 1, 2001; 42(11): 1228 - 1233. [Abstract] [Full Text] [PDF]

				J. K. Pittman and K. D. Hirschi Regulation of CAX1, an Arabidopsis Ca2+/H+ Antiporter. Identification of an N-Terminal Autoinhibitory Domain Plant Physiology, November 1, 2001; 127(3): 1020 - 1029. [Abstract] [Full Text] [PDF]

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