Calcium-Mediated Abiotic Stress Signaling in Roots

Abstract

Roots are subjected to a range of abiotic stresses as they forage for water and nutrients. Cytosolic free calcium is a common second messenger in the signaling of abiotic stress. In addition, roots take up calcium both as a nutrient and to stimulate exocytosis in growth. For calcium to fulfill its multiple roles must require strict spatio-temporal regulation of its uptake and efflux across the plasma membrane, its buffering in the cytosol and its sequestration or release from internal stores. This prompts the question of how specificity of signaling output can be achieved against the background of calcium’s other uses. Threats to agriculture such as salinity, water availability and hypoxia are signaled through calcium. Nutrient deficiency is also emerging as a stress that is signaled through cytosolic free calcium, with progress in potassium, nitrate and boron deficiency signaling now being made. Heavy metals have the capacity to trigger or modulate root calcium signaling depending on their dose and their capacity to catalyze production of hydroxyl radicals. Mechanical stress and cold stress can both trigger an increase in root cytosolic free calcium, with the possibility of membrane deformation playing a part in initiating the calcium signal. This review addresses progress in identifying the calcium transporting proteins (particularly channels such as annexins and cyclic nucleotide-gated channels) that effect stress-induced calcium increases in roots and explores links to reactive oxygen species, lipid signaling, and the unfolded protein response.

Introduction

Plant roots are exposed to a variety of abiotic stresses as they navigate the soil, foraging for nutrients and water. Cytosolic free calcium ([Ca²⁺]_cyt) is central to the response to these stresses, acting as a second messenger but also driving exocytosis (Carroll et al., 1998). Specificity of [Ca²⁺]_cyt signaling is determined by the amplitude and duration (and possible oscillation) of the [Ca²⁺]_cyt increase, often referred to as the “signature”’ (McAinsh and Pittman, 2009), that is elicited by the stimulus. This signature would be driven by the opening of plasma membrane (PM) and endomembrane Ca²⁺-permeable channels and terminated by the activity of Ca²⁺ efflux transporters in those membranes, plus Ca²⁺-binding proteins, to restore the resting [Ca²⁺]_cyt of 100–200 nM. Use of organelle-targeted Ca²⁺ reporting proteins has shown that the Ca²⁺ content of the endoplasmic reticulum (ER) and Golgi increases after stress-induced transient increases in [Ca²⁺]_cyt, strongly suggesting that Ca²⁺ is sequestered there to terminate the [Ca²⁺]_cyt signal (Ordenes et al., 2012; Bonza et al., 2013). Transport of Ca²⁺ into organelles is catalyzed by Ca²⁺-ATPases. There are two distinct families: The Auto-inhibited Ca²⁺-ATPases, ACA (that also operate at the PM) and the ER Ca²⁺-ATPases, ECA; reviewed by Bonza et al., 2016). The lower affinity CAX (Cation/H⁺ Exchangers) appear to be restricted to endomembranes but also facilitate Ca²⁺ sequestration (Connorton et al., 2012). Changes in organelle free Ca²⁺ in roots could also play a part in signaling, most notably in the formation of symbioses and cell death (Stael et al., 2012; Zhao et al., 2013; Wagner et al., 2015). Decoding the [Ca²⁺]_cyt signature will be effected by specific Ca²⁺-binding proteins. Calmodulins (CaMs) and Calmodulin-like proteins (CMLs) are encoded by multi-gene families in plants. They lack kinase domains, suggesting these proteins must target others with enzymatic activity. CaMs modulate transcription by binding to Calmodulin-binding Transcription Activators (CAMTAs) (Virdi et al., 2015). Other multi-gene families are also evident for Ca²⁺-Dependent Protein Kinases (CPKs) and Calcineurin-B Like proteins (CBLs). The latter target CBL-Interacting Protein Kinases (CIPKs) to effect cellular responses (Thoday-Kennedy et al., 2015). Changes in [Ca²⁺]_cyt also have the potential to activate lipid signaling pathways. A somewhat forgotten aspect of Ca²⁺ signaling is the Ca²⁺ activation of members of the Phospholipase C and Phospholipase D families (Qin et al., 1997; Hunt et al., 2004; Dressler et al., 2014; Ruelland et al., 2015; Hou et al., 2016). Phospholipase C catalyses production of diacylglycerol and inositol trisphosphate (InsP₃) while Phospholipase D catalyses production of phosphatidic acid, thus [Ca²⁺]_cyt would have the capacity to trigger distinct lipid signals depending on the location and Ca²⁺-sensitivity of the phospholipases. Targets of lipid signals have been reviewed recently by Hou et al. (2016).

The vast majority of [Ca²⁺]_cyt measurements are from Arabidopsis thaliana seedlings and guard cells, achieved using the luminescent Ca²⁺-interacting aequorin protein. Far fewer studies have focused specifically on roots or utilized the greater sensitivity and spatial resolution of ratiometric fluorescent dyes. The genetically encoded YC3.6 Ca²⁺ reporter is now being used for both Arabidopsis and rice roots (Behera et al., 2015), holding much promise for the future. It is now clear that an identical stimulus can elicit markedly different root [Ca²⁺]_cyt signatures depending on genus. So far, rice root [Ca²⁺]_cyt signals have been found to be lower in amplitude but of longer duration than those of Arabidopsis (Behera et al., 2015).

Electrophysiological studies of root cell plasma membrane (PM) have advanced our understanding of the Ca²⁺ influx routes that could generate [Ca²⁺]_cyt signatures. There is a central role for PM voltage in [Ca²⁺]_cyt signaling, as individual stresses can hyperpolarize (render it more negative) or depolarize (render it less negative). Manipulating PM voltage elicits distinct [Ca²⁺]_cyt signatures and resultant transcriptional responses (Whalley et al., 2011; Whalley and Knight, 2013). Studies on root epidermal and root hair PM have shown that this membrane harbors channels that are activated by hyperpolarized voltage (Hyperpolarization-Activated Ca²⁺ Channels (HACCs); Véry and Davies, 2000; Demidchik et al., 2002, 2009; Ma et al., 2012), Depolarization-Activated Ca²⁺Channels (DACCS); Demidchik et al., 2002; Miedema et al., 2008) and Voltage-Independent Ca²⁺Channels (VICCs) (Demidchik et al., 2002). Thus changes in voltage would activate specific suites of channels to generate a signature. An additional tier of regulation of the PM Ca²⁺ influx routes is afforded by reactive oxygen species (ROS) that are produced during development and stress responses (Figure 1). This regulation depends on the specific ROS, its position, the cell type and the cell’s developmental state. In Arabidopsis roots, sensitivity of PM Ca²⁺ channel activation by extracellular H₂O₂ decreases as epidermal cells mature but is still greater than that of the cortex (Demidchik et al., 2007). A similar picture emerges for extracellular hydroxyl radicals, which elicit greater PM Ca²⁺ influx currents in the epidermis and root hairs than the pericycle (Demidchik et al., 2003; Foreman et al., 2003). In epidermal PM of the elongation zone, extracellular hydroxyl radicals elicit different Ca²⁺ channel activity to extracellular H₂O₂ (Demidchik et al., 2003, 2007). Thus, ROS will play a significant part of generating cell-specific [Ca²⁺]_cyt signatures in response to stress.

FIGURE 1

Demidchik et al., 2007). Extracellular hydroxyl radicals activate Annexin 1 (pink) (Demidchik et al., 2003; Foreman et al., 2003; Laohavisit et al., 2012). Ca²⁺ influx would depolarise the PM and if unopposed this could activate DACCs (yellow) (Demidchik et al., 2002). Increased [Ca²⁺]_cyt could further activate RBOH.

Stress-induced [Ca²⁺]_cyt elevation in roots remains poorly understood in terms of the genes encoding the PM or endo membrane Ca²⁺ channels involved. Plants have multi-gene families of Glutamate Receptor-Like channels (GLR; activated by a range of extracellular nitrogenous ligands) and Cyclic Nucleotide-Gated channels (CNGC; activated by intracellular cyclic nucleotides), with each gene encoding a potential subunit of a potentially tetrameric channel. Some members have been characterized as having Ca²⁺ channel forming ability (reviewed by Swarbreck et al., 2013 and Weiland et al., 2016). Membrane residency has yet to be determined for all proteins and while the majority tested are in the PM, in Arabidopsis GLR3.5 has been localized to both mitochondria and chloroplast, depending on its splicing variant (Teardo et al., 2015), CNGC19 to the vacuole (Yuen and Christopher, 2013) and CNGC20 potentially to both PM and vacuole (Fischer et al., 2013; Yuen and Christopher, 2013). Mechanosensitive Ca²⁺ channels of the PM have also been identified (Nakagawa et al., 2007; Hou et al., 2014; Yuan et al., 2014; Kamano et al., 2015), as has a vacuolar Ca²⁺ efflux channel TPC1 (Two Pore Channel1; Peiter et al., 2005). Root cells will express specific complements of these genes and their transcription can change under abiotic stress (Dinneny et al., 2008; Roy et al., 2008), with the implication that stress resets the [Ca²⁺]_cyt signaling system.

The threat of abiotic stress is global. Drought threatens plant productivity across continents, with water shortage not only imposing an osmotic challenge but also leading to soil hardness that roots must overcome. Changing weather patterns are bringing greater rainfalls to some areas (particularly Northern Europe) thus leading to the threat of hypoxic challenge from waterlogged soil (Shabala et al., 2014). Salinity stress arising from sodic soils is made worse by irrigation and counteracting nutritional deprivation by fertilizer application comes with an increasing economic and environmental cost. In this review, the effects of salinity, water availability (including soil hardness), nutritional deprivation, heavy metals and cold on root [Ca²⁺]_cyt will be addressed. The candidate channels for elevating [Ca²⁺]_cyt in roots will be introduced and the downstream consequences of the signal will be reviewed.

Salinity Stress from Channel to Transcription

The transporters for Na⁺ influx into the root are not fully known but include the PM cyclic nucleotide-gated channels CNGC3 (Gobert et al., 2006) and CNGC10 (Guo et al., 2008; Jin et al., 2015) in Arabidopsis. Na⁺ ingress is opposed by the Annexin1 protein and the AGB1 heterotrimeric G protein subunit in Arabidopsis roots (Laohavisit et al., 2013; Yu and Assmann, 2015). The mechanisms for sensing the increase in cytosolic Na⁺ remain obscure (Maathuis, 2014; Shabala et al., 2015) however what is clear is that Na⁺ entry depolarizes the root epidermal PM voltage (Maathuis, 2014). This is significant in that it implicates depolarization-activated and voltage-independent PM Ca²⁺-permeable channels in generating the transient [Ca²⁺]_cyt increases observed in roots in response to NaCl (Figure 2). Both channels types are present in Arabidopsis root epidermal PM (Demidchik et al., 2002). However, involvement of hyperpolarization-activated PM Ca²⁺ channels should not be dismissed because increasing [Ca²⁺]_cyt shifts their activation voltage to more depolarized values (Véry and Davies, 2000; Demidchik et al., 2002) and they are implicated in the Arabidopsis root response to NaCl (Ma et al., 2012; Laohavisit et al., 2013). Critically, hyperosmotic stress hyperpolarizes root epidermal PM voltage (Maathuis, 2014) and this would potentially be a basis for generating a component of the [Ca²⁺]_cyt signal specific to the hyperosmotic component of NaCl stress.

FIGURE 2

DeWald et al., 2001; Tracy et al., 2008; Zhang Y. et al., 2015; Zhang X. et al., 2015). ARP2/3 restricts mitochondrial Ca²⁺ efflux (Zhao et al., 2013). [Ca²⁺]_cyt activation of RBOH NADPH oxidase activity would promote extracellular hydroxyl radical formation and activation of Annexin1-mediated Ca²⁺ influx (pink) (Laohavisit et al., 2013). We hypothesize that these are held in a microdomain (red). This leads to SOS1 transcription (Laohavisit et al., 2013). CaM activation would restrict CNGC-mediated Ca²⁺ influx and promote efflux by ACA Ca²⁺-ATPase activation (Boursiac and Harper, 2007). [Ca²⁺]_cyt elevation activates CBL4 and CIPK24 (purple) leading to SOS1-mediated Na⁺ extrusion (Liu et al., 2000). CIPK24 activates vacuolar V-ATPase to provide the driving force for NHX1 and CAX1 to sequester Na⁺ and Ca²⁺ respectively, also activated by CIPK24 (Cheng et al., 2004; Batelli et al., 2007; Quintero et al., 2011).

Ca²⁺ Influx across the PM

Application of NaCl can cause a heterogeneous increase in Arabidopsis and rice root [Ca²⁺]_cyt that depends on cell type, external [Ca²⁺], and the bathing medium’s effect on PM voltage (Kiegle et al., 2000; Tracy et al., 2008; Laohavisit et al., 2013; Choi et al., 2014; Zhang Y. et al., 2015). Pericycle cells of Arabidopsis have a lower amplitude of [Ca²⁺]_cyt increase and a more variable recovery phase than the surrounding tissues (Kiegle et al., 2000), suggesting a cell-specific transporter complement. Block of NaCl-induced [Ca²⁺]_cyt increase by lanthanides implicates PM Ca²⁺ influx channels in the response of both Arabidopsis and rice roots (Tracy et al., 2008; Zhang Y. et al., 2015). The anti-apoptotic protein Bcl-2 mimics lanthanides in that its overexpression impairs the NaCl-induced [Ca²⁺]_cyt increase in rice roots (Kim et al., 2014). Clearly, the [Ca²⁺]_cyt increase could lead to cell death if it were great enough and Bcl-2 may interact directly with PM channels. The genetic identities of the PM Ca²⁺ influx channels initiating the NaCl-induced [Ca²⁺]_cyt increase remain unknown. It has been suggested that they may be Ca²⁺-permeable CNGCs (Shabala et al., 2015) as salinity stress increased cytosolic cGMP in Arabidopsis seedlings within seconds (Donaldson et al., 2004). The source of cGMP may prove to be critical as only the [Ca²⁺]_cyt response to low NaCl (50 mM) was sensitive to inhibition of soluble guanylyl cyclase activity and the signal evoked by an equivalent osmotic stress was insensitive (Donaldson et al., 2004). It remains feasible that neither the ionic nor osmotic components of the [Ca²⁺]_cyt increase in response to high [NaCl] require cGMP. The osmotic component of NaCl stress could increase [Ca²⁺]_cyt in Arabidopsis roots through the PM mechanosensitive Ca²⁺-permeable channel OSCA1 (Reduced Hyperosmolality-Induced [Ca²⁺]_I increase1). This channel mediates the [Ca²⁺]_cyt response to hyperosmotic stress (Yuan et al., 2014). Its discovery through a screen of aequorin-expressing mutants (Yuan et al., 2014) highlights the potential of this approach for identification of channels (and their families) involved in stress-induced [Ca²⁺]_cyt elevation.

The initial increase in [Ca²⁺]_cyt could be amplified by the production of ROS sourced ultimately by PM NADPH oxidases (encoded by Respiratory Burst Oxidase Homolog genes), with [Ca²⁺]_cyt activating these enzymes through their EF hands (Figure 2). In accordance with this, Arabidopsis root cortical cells lacking RBOHD and F have much lower PM hyperpolarization-activated Ca²⁺ activity in response to NaCl challenge than wild type (Ma et al., 2012). Mutant seedlings have an impaired [Ca²⁺]_cyt response. Arabidopsis RBOHD can be activated by CIPK26/CBL1/9 (Drerup et al., 2013) but a direct link to stress has not been shown. Extracellular hydroxyl radicals are likely to be the ROS involved in [Ca²⁺]_cyt elevation (Chung et al., 2008; Demidchik et al., 2010; Laohavisit et al., 2013; Richards et al., 2015). The extracellular superoxide anions produced by NADPH oxidases are readily converted to H₂O₂ and wall Fe/Cu act as Fenton catalysts to generate hydroxyl radicals (Richards et al., 2015). Their production by Arabidopsis roots is significantly increased under NaCl stress (Demidchik et al., 2010) and RBOHC is implicated as a driver for production (Chung et al., 2008). Extracellular hydroxyl radicals activate a PM Ca²⁺ influx in Arabidopsis root epidermis (Demidchik et al., 2003; Foreman et al., 2003) that has now been shown to be mediated by Annexin1 (Laohavisit et al., 2012).

Annexins are Ca²⁺-binding proteins that can bind to or insert into membranes and are implicated in stress reactions (Laohavisit and Davies, 2011; Davies, 2014). Critically, when root epidermal protoplasts are challenged with NaCl, the resultant PM hyperpolarization-activated Ca²⁺ influx is lost in the annexin1 loss of function mutant and the [Ca²⁺]_cyt signal is impaired (Laohavisit et al., 2013). Hydroxyl radicals are potent but short-lived so their effects must be close to the site of production (Richards et al., 2015). As NADPH oxidases can be held in lipid rafts it may be that hydroxyl radicals target co-resident channels. Finally, extracellular ATP levels of Arabidopsis roots increase in response to NaCl (Dark et al., 2011). Extracellular ATP activates root epidermal PM hyperpolarization-activated Ca²⁺ influx channels via RBOHC (Demidchik et al., 2009), suggesting the involvement of extracellular ROS in channel activation. Whether these channels involve Annexin1 remains to be determined but both the annexin1 and rbohc loss of function mutants are impaired in [Ca²⁺]_cyt-dependent transcriptional responses under NaCl stress (Chung et al., 2008; Laohavisit et al., 2013).

Calcium Release from Stores

Although not demonstrated in roots, the Arabidopsis Actin-Related Protein2/3 (ARP2/3) acts to limit NaCl-induced [Ca²⁺]_cyt increase, partly by limiting Ca²⁺ release from mitochondria. In the arp2/3 mutant, the [Ca²⁺]_cyt increase is greater than wild type and so is the extent of mitochondrial-driven cell death (Zhao et al., 2013). Release of vacuolar Ca²⁺ to the cytosol in Arabidopsis roots may be by a Na⁺/Ca²⁺ exchanger encoded by AtNCL (Na⁺/Ca²⁺ Exchanger-Like; Wang et al., 2012; Li P.H. et al., 2016). This tonoplast protein is thought to sequester Na⁺ into the vacuole, coupled to the release of vacuolar Ca²⁺. The concomitant increase in [Ca²⁺]_cyt could provide a negative feedback mechanism to limit further transport as Ca²⁺ binding to the exchanger’s EF hands has been shown to be inhibitory in vitro (Li P.H. et al., 2016). Pharmacological approaches have also implicated internal stores in the NaCl-induced [Ca²⁺]_cyt increase in roots of both Arabidopsis and rice. Inhibitors of store release of Ca²⁺ by cADPR (cyclic ADP ribose) and inositol trisphosphate (InsP₃) suggested involvement of the InsP₃ pathway in Arabidopsis roots (Tracy et al., 2008). Moreover, salt and hyperosmotic stress in Arabidopsis roots caused an InsP₃ accumulation that correlated well with [Ca²⁺]_cyt increase (DeWald et al., 2001). The rice [Ca²⁺]_cyt signal was also sensitive to disruption of putative InsP₃-gated store release whilst impairment by thapsigargin implicated the ER as a participating store (Zhang Y. et al., 2015). However, using ER-targeted YC3.6, Bonza et al. (2013) detected an increase in Arabidopsis root ER [Ca²⁺] in response to salt stress. This followed the salt-induced [Ca²⁺]_cyt increase and critically, a drop in ER [Ca²⁺] prior to the [Ca²⁺]_cyt increase was never observed. Therefore, with the level of resolution available, it appears that in this system the ER does not contribute to the [Ca²⁺]_cyt signal through store release but acts to return [Ca²⁺]_cyt to resting levels. Studies on Populus euphratica cultured cells identified the vacuole as the site of InsP₃ and cADPR action (Zhang X. et al., 2015). Certainly, Phospholipase C isoforms (as the source of InsP₃) are firmly implicated in salt stress responses (reviewed by Ruelland et al., 2015).

The genetic identities of the endomembrane Ca²⁺-permeable channels implicated by pharmacological studies remain elusive. GLRs have recently been postulated to be involved in ER Ca²⁺ release (Weiland et al., 2016). The TPC1 vacuolar channel of Arabidopsis would be capable of releasing Ca²⁺ to the cytosol and recent analyses of its crystal structure has thrown greater light on its regulation by voltage and EF hands (Guo et al., 2016; Kintzer and Stroud, 2016). At current resolution afforded by YC3.6, its loss does not appear to have a significant impact on the magnitude of the Arabidopsis root [Ca²⁺]_cyt increase to salt, rather it slightly delays the response (Choi et al., 2014). However, TPC1 has a significant part to play in the propagation of a [Ca²⁺]_cyt wave that travels from the root apex through the cortical and endodermal tissue to signal the NaCl challenge to the shoots and elicit a transcriptional response. ROS also relay a salinity stress signal (reliant on RBOHD) in Arabidopsis leaves (Miller et al., 2009) but whether this occurs in roots and is involved in propagating the [Ca²⁺]_cyt wave remains to be tested.

Decoding, Na⁺ Clearance, Transcription and the Unfolded Protein Response

Salinity-induced [Ca²⁺]_cyt elevation in roots drives a transcriptional response (Laohavisit et al., 2013; Zhang Y. et al., 2015) and post-translational modifications. The proteins sensing the NaCl-induced [Ca²⁺]_cyt increase are now being elucidated. For example, the Arabidopsis vacuolar Two Pore K⁺ channel 1 (TPK1) would bind Ca²⁺, and open to release K⁺ to the cytosol to maintain a favorable Na⁺/K⁺ ratio (Latz et al., 2013). This could be further enhanced by phosphorylation by CPK3, which requires micromolar [Ca²⁺] for activity. CPK3 is present at both the PM and vacuole. It does not appear to contribute to a transcriptional response under salt stress but has a discrete set of protein targets to phosphorylate (Mehlmer et al., 2010). On prolonged salt stress, CPK29 expression is induced. This protein can phosphorylate TPK1 at sub-micromolar [Ca²⁺] and is envisaged to be part of longer-term K⁺ homeostasis in adapted roots (Latz et al., 2013). Also in Arabidopsis, CPK27 (present at the root PM) acts to promote Na⁺ efflux (Zhao et al., 2015). Intriguingly, CPK7 acts to limit water transport in Arabidopsis roots through lowering PIP1 aquaporin abundance (Li et al., 2015) but whether this is relevant to salinity or osmotic stress is not yet known. It can be readily envisaged that calmodulins will bind Ca²⁺ and as these are negative regulators of CNGC channels (Hua et al., 2003), would act to limit further Na⁺ or Ca²⁺ influx at the PM. Further, CaM activation of ACAs (Autoinhibited Ca²⁺ATPases) would restore [Ca²⁺]_cyt to pre-stimulus levels (Boursiac and Harper, 2007). Expression of ACAs varies with salt stress and, as shown by rice roots, can relate to salt tolerance (Yamada et al., 2014).

The Salt Overly Sensitive (SOS) pathway lies downstream of the root [Ca²⁺]_cyt increase. Delineated in Arabidopsis and now acknowledged as operating in crops and trees (Thoday-Kennedy et al., 2015), the SOS pathway leads to Na⁺ efflux from the cytosol. Efflux across the PM is mediated by the SOS1 Na/H⁺ antiporter. Salt stress induction of SOS1 transcription lies downstream of Annexin1 in Arabidopsis roots and as SOS1 is required for adaptive adventitious root formation, the annexin1 loss of function mutant accordingly produces fewer of these than wild type (Laohavisit et al., 2013). Additionally, the stability of salt stress-induced SOS1 transcript requires RBOHC (Chung et al., 2008), further suggesting that this NADPH oxidase and Annexin1 may be in the same pathway. In Arabidopsis roots, increased [Ca²⁺]_cyt is sensed at the PM by CBL4 (SOS3) which can then react with the serine/threonine protein kinase CIPK24 (SOS2) (Liu et al., 2000). The resultant CBL/CIPK complex phosphorylates the PM Na/H⁺ antiporter SOS1 at its auto-inhibitory C-terminus to achieve activation of Na⁺ efflux (Quintero et al., 2011). Activation of SOS1 can also be achieved in Arabidopsis by Mitogen Activated Protein Kinase6 (MPK6) and loss of MPK6 function impairs root growth under salt stress (Yu et al., 2010). MPK6 is activated by a phosphatidic acid produced under salt stress by Phospholipase Dα1 (PLDα1) (Yu et al., 2010). As this PLD isoform contains a Ca²⁺-binding C2 domain for its activation it is feasible that salt-induced [Ca²⁺]_cyt increase could activate SOS1 through this lipid-mediated pathway via MPK6 (Yu et al., 2015). This may help explain the importance of activation of PLDs in salt-stressed crop roots such as barley (Meringer et al., 2016). SOS2 may also promote activity of the vacuolar V-type H⁺-ATPase to provide the driving force for Na⁺ sequestration (Batelli et al., 2007). The NHX1 Na⁺-H⁺ exchanger may also be regulated by SOS2 to aid vacuolar Na⁺ sequestration (Qiu et al., 2004) and SOS2 activation of the vacuolar CAX1 Ca²⁺/H⁺ antiporter would help terminate a [Ca²⁺]_cyt signature through Ca²⁺ sequestration (Cheng et al., 2004). Other CAX are involved in root tolerance of salt stress and the pathways to their induction and regulation now need to be identified (Yamada et al., 2014).

Salt exposure puts the plant’s ER under stress, leading to an accumulation of unfolded or misfolded proteins that could lead to cell death (Liu et al., 2007, 2011). Such ER stress triggers upregulation of a suite of responses termed the “Unfolded Protein Response” (UPR), in which folding capacity is upregulated (including by Ca²⁺-regulated chaperones), translation is curtailed and the ER-associated degradation pathway acts to lower the aberrant protein load (Deng et al., 2013; Ruberti et al., 2015; Hossain et al., 2016; Wan and Jiang, 2016). Expression of the ER Ca²⁺-binding chaperones Calnexin and Calreticulin has been shown to upregulated in the Arabidopsis UPR (Christensen et al., 2008; Liu et al., 2011) and it would now be interesting to test whether these are involved in regulating levels of Ca²⁺ in the ER under stress. However, expression of rice’s only calnexin gene is decreased under salt stress (Sarwat and Naqvi, 2013). It is not yet clear whether the salt-induced [Ca²⁺]_cyt signal in roots (or other parts of the plant) helps initiate or regulate the UPR. It is feasible that the salt-induced [Ca²⁺]_cyt increase activates the root PM Phospholipase C2 (Hunt et al., 2004) because the Arabidopsis loss of function mutant is hypersensitive to tunicamycin, which can induce the UPR (Kanehara et al., 2015). With IP₃ as the product of Phospholipase C activity, this would implicate IP₃-mediated release of Ca²⁺ from stores. Indeed, for Arabidopsis seedlings the application of 2-aminoethoxydiphenyl borate as an inhibitor of IP₃-mediated Ca²⁺ release prevented salt stress-induced transcription of BIP1/2 (encoding an ER chaperone) as a diagnostic of a UPR response (Liu et al., 2011). Intriguingly, application of La³⁺ as a blocker of PM Ca²⁺ influx prevented the upregulation of UPR gene expression which was produced by application of spermine to Arabidopsis seedlings (Sagor et al., 2015). Exogenous spermine (as with salt) can depolarise the root epidermal PM (Pottosin et al., 2014) and can also attenuate hydroxyl radical-induced cation fluxes at root epidermal PM (Zepeda-Jazo et al., 2011). Whether spermine and salt stress share a common pathway to the UPR response merits further investigation.

Water Availability is Signaled Through [Ca²⁺]_cyt

The hyperosmotic challenge in [Ca²⁺]_cyt determinations is acute and does not mimic the chronic, progressive drought conditions that roots may face. Nevertheless, such studies have proved fruitful. As described above, the Arabidopsis OSCA1 PM Ca²⁺ influx channel drives the root’s initial hyperosmotic stress [Ca²⁺]_cyt signal (Yuan et al., 2014). In an elegant study, heterologous expression of Arabidopsis genes in Chinese Hamster Ovary (CHO) cells containing the Fura-2 Ca²⁺-reporting dye lead to the identification of Calcium-permeable Stress-gated cation Channel1 (CSC1; Hou et al., 2014), a close relative of OSCA1. CSC1 has been characterized in CHO cells as a PM Ca²⁺-permeable channel that is activated by hyperosmotic stress. It is resident in plant PM (Hou et al., 2014) and is expressed in roots but to date an in planta role remains unreported. Targeting aequorin to the cytosolic face of the Arabidopsis vacuolar membrane has revealed the capacity of the vacuole to release Ca²⁺ in response to acute hyperosmotic stress, with pharmacological intervention suggesting an involvement of InsP₃ (Knight et al., 1997). As with salt stress, hyperosmotic stress-induced [Ca²⁺]_cyt increase could activate Phospholipases and initiate lipid signaling. Osmotic stress activates PLD in barley roots (Meringer et al., 2016). Although not tested directly, phosphatidic acid downstream of PLD could be involved in the activation of two sucrose non-fermenting-1 related protein kinase 2 proteins (SnRK2.4 and 2.10) in Arabidopsis roots under hyperosmotic stress. These SnRK2s are also activated under salt stress and relocate from the root epidermal cytosol to the PM; loss of function impairs root growth (McLoughlin et al., 2012). Work using Golgi-targeted aequorin in Arabidopsis seedlings has shown that an increase in Golgi [Ca²⁺] follows the [Ca²⁺]_cyt increase induced by hyperosmotic stress, suggesting that this organelle helps terminate the [Ca²⁺]_cyt signal (Ordenes et al., 2012).

The ABA produced under drought stress inhibits primary root growth and [Ca²⁺]_cyt is likely to play a role in the signaling pathway as exogenous ABA elevates root [Ca²⁺]_cyt, which in Arabidopsis roots is controlled by the PM Proline-rich Extensin-like Receptor Kinase4 (PERK4) (Bai et al., 2009). PERK4’s extracellular domain is wall associated and its intracellular domain has kinase activity. PM HACCs lie downstream of ABA and PERK4. The perk4 mutant is not only impaired in ABA-induced HACC activity and [Ca²⁺]_cyt activation but also in ABA inhibition of primary root elongation (Bai et al., 2009). This implies that [Ca²⁺]_cyt elevation acts to arrest growth. RBOHD/F may lie downstream of PERK4 and upstream of HACCs in the root ABA pathway if the HACCs were ROS-activated. The rbohd/f mutant is impaired in both ABA-induced HACC activation and [Ca²⁺]_cyt elevation (Jiao et al., 2013). Another possibility is that CNGCs are involved as ABA can increase cGMP levels (Isner et al., 2012.). GLRs are firmly implicated in the drought response; overexpression of rice GLR1 and GLR2 enhances drought tolerance of both rice and Arabidopsis (Lu et al., 2014). The [Ca²⁺]_cyt increase is likely to lead to a transcriptional response as Ca²⁺-sensing proteins are activated. ABA increases abundance and activity of Arabidopsis CPK4 and CPK11 leading to phosphorylation of the ABA-responsive transcription factors ABF1 and ABF4 and induction of drought stress genes (Zhu et al., 2007). Drought leads to CAMTA1 activity and the regulation of discrete gene sets including those for drought recovery (Pandey et al., 2013). In maize roots, drought stress triggers activity of CIPK8 (which interacts with CBL1, 4, and 9) and likely leads to adaptive transcription (Tai et al., 2016).

Hypoosmotic stress also elevates [Ca²⁺]_cyt and is relevant to waterlogged soils. In Arabidopsis, root PM harbors two mechanosensitive Ca²⁺-permeable channels, MCA1 and MCA2 (Mid1-Complementing Activity; Kamano et al., 2015). MCA1 responds to hypoosmotic stress to elevate [Ca²⁺]_cyt (Nakagawa et al., 2007). Rice only harbors an MCA1 in the PM. It is present in the root and mediates hypoosmotic shock-induced [Ca²⁺]_cyt expression in cultured cells, probably lying upstream of NADPH oxidase activity (Kurusu et al., 2012). Abundant water not only exposes roots to potential hypoosmotic stress but also risks limiting their oxygen supply, the consequences of which are reviewed in the following section.

Mechanistic Basis of [Ca²⁺]_cyt Response to O₂ Deficiency Remains Poorly Understood

Oxygen deficiency (hypoxia) or absence (anoxia) causes transient increases in root [Ca²⁺]_cyt but the signature is organ- and species-dependent (reviewed by Shabala et al., 2014). For example, when challenged by anoxia, root protoplasts from hypoxia-tolerant rice display a greater [Ca²⁺]_cyt signature than hypoxia-intolerant wheat root protoplasts (Yemelyanov et al., 2011). The location of the Ca²⁺ influx also varies; use of pharmacological blockers showed that the rice signature was generated by both PM influx and store release whilst wheat appeared to rely solely on stores (Yemelyanov et al., 2011). The types of Ca²⁺ channels mediating the [Ca²⁺]_cyt increase have yet to be identified in any species. However, those activated by PM voltage depolarization are implicated. As O₂ deficiency lessens ATP production, activity of the PM H⁺-ATPase can be compromised thus resulting in a less negative (depolarized) PM voltage as H⁺ efflux is curtailed. The extent and duration of membrane depolarization varies with sensitivity to O₂ deprivation and cell type. Values of -70 to -80 mV have been reported for O₂-deprived barley root cells (Zeng et al., 2014) and theoretically these would be sufficient to activate PM depolarization-activated Ca²⁺ influx channels (Miedema et al., 2008) to contribute to an hypoxia/anoxia [Ca²⁺]_cyt signature. Downstream of the [Ca²⁺]_cyt signature, it is likely that CaM and ROPs (Rho GTPase) are activated (reviewed by Shabala et al., 2014). In Arabidopsis roots, hypoxia causes rapid upregulation of CML38 expression and this protein appears to require Ca²⁺ to associate with the cytosolic stress granules that form and store messenger RNA ribonucleoproteins (Lokdarshi et al., 2016).

RBOH activity is firmly implicated in the response to low O₂. In Arabidopsis, RBOHD expression is induced by hypoxia and is required for transcription of hypoxia-induced genes (Yang and Hong, 2015). Hypoxia also induces ethylene production and in wheat roots this causes RBOH induction (Yamauchi et al., 2014). A further level of regulation has been found in Arabidopsis; the Hypoxia Responsive Universal Stress Protein 1 (HRU1) interacts with GTP-bound ROP2 and RBOHD (Gonzali et al., 2015). HRU1 is one of 44 putative universal stress proteins in Arabidopsis. It exists as a cytosolic dimer but anoxia promotes monomer formation and increased association with the PM. There it is thought to be part of a mobile complex with ROP2 and AtRBOHD leading to activation of that NADPH oxidase (Gonzali et al., 2015). Although RBOH activity has been linked to PM Ca²⁺ channel activation in several abiotic stress scenarios, hypoxia and anoxia have yet to be tested.

Ethylene has been shown to activate PM Ca²⁺-permeable channels (with a weak voltage dependence) in tobacco suspension cells (Zhao et al., 2007) and it remains a possibility that these may play a part in the root hypoxia [Ca²⁺]_cyt signal with RBOH as an intermediary. Oxygen deprivation (and also sulfur and phosphate, Pi, deprivation) triggers programmed cell death (PCD) in mid-cortical cells for aerenchyma formation (Fagerstedt, 2010). This PCD is stimulated by ethylene and ROS and involves Ca²⁺ (Xu et al., 2013; Petrov et al., 2015). In wheat roots, anoxia causes mitochondria to release their Ca²⁺ and high [Ca²⁺]_cyt causes cytochrome c release (Virolainen et al., 2002). The abnormal mitochondrial ultrastructure in Arabidopsis caused by hypoxia is partially phenocopied by loss of GLR3.5 from the inner mitochondrial membrane, suggesting that this channel must be deactivated during PCD (Teardo et al., 2015). Further channels must now be identified to understand the hypoxic/anoxic response. Recent work on Arabidopsis roots has shown distinct, cell-specific levels of [Ca²⁺]_cyt after 24 h of hypoxia and highlighted the importance of CAX11 in controlling meristem [Ca²⁺]_cyt (Wang et al., 2016). Loss of CAX4 function resulted in lower tolerance of hypoxia thus further demonstrating the importance of Ca²⁺ sequestration in this stress response (Wang et al., 2016).

Ca²⁺ Signaling in Nutrient Deprivation is an Emerging Area

Investigating [Ca²⁺]_cyt elevation in response to nutrient deprivation or resupply is technically challenging, particularly if using aequorin. Nevertheless it is now clear that nutrient levels can induce [Ca²⁺]_cyt changes and that downstream Ca²⁺ sensors regulate appropriate responses. The nutritional status of the root will have a part to play in determining the [Ca²⁺]_cyt signatures, particularly of the endodermis as the extent of suberization is set by nutrition (Barberon et al., 2016) and suberin lamellae determine endodermal [Ca²⁺]_cyt responses (Moore et al., 2002). To date, potassium, nitrate and boron have been studied.

Potassium

Plants must maintain cytosolic K⁺ at around 80 mM for optimal growth even though soil concentration may be sub-millimolar and they deploy a multigene family of K⁺ transporters in homeostatic control (Shabala and Pottosin, 2014). As extracellular K⁺ decreases, the root epidermal PM hyperpolarizes and [Ca²⁺]_cyt increases (Demidchik et al., 2002). This increase can be abolished by gadolinium, implicating PM Ca²⁺ influx. The genetic identities of the PM Ca²⁺-permeable channels that would effect the [Ca²⁺]_cyt increase remain unknown. The hyperpolarised PM correlates with induction of HAK5 expression in tomato root (Nieves-Cordones et al., 2008). HAK5 encodes the PM High Affinity K⁺ transporter that facilitates K⁺ uptake from low external concentrations that are thermodynamically unfavorable for channel-mediated influx. In Arabidopsis roots, low K⁺-induction of HAK5 expression (and other K⁺-deprivation genes) has been shown to depend on RBOHC activity and ROS (Shin and Schachtman, 2004). At present it is unclear whether the hyperpolarization of the PM directly activates RBOHC (which as an electron exporter may be voltage-dependent) or whether ROS-activated PM Ca²⁺ channels are involved in the K⁺-deprivation [Ca²⁺]_cyt signal. HAK5 activity in Arabidopsis roots is regulated by CIPK23-mediated phosphorylation, downstream of CBL1, CBL8, CBL9, and CBL10 (Ragel et al., 2015). The extent to which the transcriptional response to low K⁺ availability is governed by [Ca²⁺]_cyt is unclear but deficiency does result in upregulation of transcripts of Ca²⁺ signaling proteins (CaM, CBL, CIPK) in Arabidopsis seedlings (Armengaud et al., 2004) and sugarcane roots (Zeng et al., 2015). At higher external [K⁺], the AKT1 channel (Arabidopsis K⁺Transporter1) facilitates uptake and its activity is promoted by CIPK23-mediated phosphorylation, downstream of CBL1 and CBL9 (Li et al., 2006; Cheong et al., 2007). This regulation is recapitulated in rice roots where CIPK23/CBL1 activate AKT1 (Li et al., 2014).

Nitrate

Nitrate is the most important form of nitrogen for agriculture and deprivation triggers significant transcriptional and developmental responses. The effect of nitrate withdrawal on [Ca²⁺]_cyt has yet to be reported but recently it was shown that nitrate-starved Arabidopsis roots responded to nitrate resupply with a rapid, monophasic transient increase in [Ca²⁺]_cyt that was sensitive to lanthanides and phospholipase C (PLC) inhibition (Riveras et al., 2015). Lanthanum also blocked nitrate-induced InsP₃ production, suggesting that Ca²⁺ influx across the PM activated a PLC. The [Ca²⁺]_cyt and InsP₃ increases were entirely dependent on the PM nitrate influx transporter NRT1.1 (Nitrate Transporter1.1; Riveras et al., 2015). By using the nrt1.1 mutant and pharmacological blockers, nitrate-induced gene transcription was also found to lie downstream of NRT1.1, and [Ca²⁺]_cyt elevation from PM influx and InsP₃-gated store release. Calcium is also key to the regulation of nitrate uptake capacity as CIPK23, which is activated by CBL9 and CBL1, and dephosphorylated by ABI2 (a member of the PP2C protein phosphatase family; Léran et al., 2015,), phosphorylates NRT1.1 under low nitrate condition, thus converting it from a low to high affinity transporter (Ho et al., 2009). By contrast CIPK8 positively regulates the low-affinity phase of the nitrate primary response which includes transcriptional regulation, but its regulation of primary root elongation is concentration independent in Arabidopsis (Hu et al., 2009). CBL7, which is upregulated under nitrate deprivation, positively regulates the nitrate-dependent induction of NTR2.4 and NTR2.5 gene expression (Ma Q. et al., 2015). Given the lack of a [Ca²⁺]_cyt reporter line available in crops up until recently for rice, little is known about nitrate deficiency-induced [Ca²⁺]_cyt signaling but CaM protein abundance of wheat roots declines under nitrate deficiency, suggesting a remodeling of signaling systems (Jiang et al., 2015).

Boron

Boron deficiency is widespread worldwide and particularly prevalent in China (Shorrocks, 1997). As B plays a dominant role in co-ordinating cell wall structure (Kobayashi et al., 1996), changes in cell wall stability are likely to influence the signal relayed into the cell upon B deprivation and indeed a rapid change in cell wall modulus has been observed (Goldbach et al., 2001). Early work in Vicia faba showed a release of membrane-bound Ca²⁺ into the apoplast (Mühling et al., 1998), raising the possibility of Ca²⁺ signaling during the early stages of B deficiency. Increased levels of both [Ca²⁺]_cyt and ROS have been suggested to lead to the increased root hair growth known to occur under B deprivation (González-Fontes et al., 2016). In cultured tobacco cells, transcriptional changes in response to short-term B deprivation (1 h) were abolished when withdrawing Ca²⁺ from the growth medium or upon treatment with the Ca²⁺ channel blocker lanthanum, thus implicating PM Ca²⁺ influx channels in generating a [Ca²⁺]_cyt signal (Koshiba et al., 2010). However, a transient [Ca²⁺]_cyt signal in direct response to B withdrawal has yet to be reported. Rather, work has focused on the possible remodeling of Ca²⁺ transport and signaling as a consequence of B deprivation.

Challenging cultured tobacco cells with Ca²⁺ resulted in a higher amplitude of [Ca²⁺]_cyt transient in B-deprived cells (1 h deprivation) than those grown under replete conditions (Koshiba et al., 2010). This suggests that B deprivation rapidly “resets” the PM’s Ca²⁺ transport systems to generate altered [Ca²⁺]_cyt responses. The [Ca²⁺]_cyt response of B-deprived cells was sensitive to lanthanum and diphenyleneiodonium, pointing to the involvement of PM Ca²⁺ channels and NADPH oxidases respectively (Koshiba et al., 2010). Arabidopsis roots expressing the YC3.6 [Ca²⁺]_cyt reporter exhibited higher levels of [Ca²⁺]_cyt at the apex than controls after 6 and 24 h of B deprivation (Quiles-Pando et al., 2013). This time course of B deprivation also resulted in significant upregulation of CNGC19 (encoding a vacuolar channel), four genes of the ACA family of P_IIB-type Ca²⁺-ATPases (ACA1,10,12,13) and CAX3 encoding a vacuolar cation-H⁺ antiporter (Quiles-Pando et al., 2013). This suite of transporters could effect Ca²⁺ efflux from the vacuole (CNGC19) to increase [Ca²⁺]_cyt with clearance to the apoplast by ACA10-13 and sequestration to the vacuole by CAX3. How they are regulated remains to be determined, as does the involvement of the structurally compromised wall and the consequence of this higher level of apical [Ca²⁺]_cyt. The area of higher [Ca²⁺]_cyt reported appears to correspond with the zone of inhibition of primary root elongation and the induction of cell death (Oiwa et al., 2013; Camacho-Cristobal et al., 2015). Once again, ethylene production appears to be upstream of NADPH oxidase-driven ROS production in growth arrest and death (Oiwa et al., 2013; Camacho-Cristobal et al., 2015).

Eight CML genes were also significantly upregulated after a day’s B deprivation of Arabidopsis roots (CML11,12,23,24, 30.37,45.47), as were three CPK genes (CPK1,28,29) all suggesting a distinct change in intracellular Ca²⁺ signaling (Quiles-Pando et al., 2013). This B deprivation also caused upregulation of WRKY transcription factors (TF) (WRKY38,40,46), two three MYB family TF (MYB14,15,78) and downregulation of two BZIP family TFs (bZIP34,61) (González-Fontes et al., 2016). B deprivation has also been found to promote the senescence-associated WRKY6 TF in the root tip (Kasajima et al., 2010). It has been suggested that the CMLs and CPKs upregulated by B deprivation are part of the chain of events leading to TF activation in the nucleus (González-Fontes et al., 2016) and this now requires direct testing. CIPK8 also positively regulates nitrate induced up-regulation of BOR1, a gene encoding a boron transporter responsible for xylem loading (Hu et al., 2009), suggesting that root signaling results in preservation of shoot B supply.

Heavy Metal Stress has the Capacity to Distort Ca²⁺ Signaling

At the opposite end of nutritional deprivation is heavy metal stress. Industrial activity, mining and modern agricultural practices can lead to soil contamination by heavy metals (defined here as 7 g/cm³ and above). Although some of these metals (such as Zn, Cu) are required as micronutrients they can be damaging in excess whilst others (such as Cd) have no physiological role and can be deleterious even at low concentrations, often impairing mineral nutrition. The consequences of heavy metal exposure have been reviewed recently by Singh et al. (2016) and these authors explore signaling pathways (although not explicitly addressing Ca²⁺), intersects with hormonal responses and detoxification.

Cadmium

Cadmium is a particular threat to Ca²⁺-based processes because of its similar size. A recent review by Chmielowska-Bak et al. (2014) summarized the effects of Cd on ROS accumulation, NO accumulation, MAP kinase activation and downstream responses in a wide range of plant systems and, importantly, did this as a function of Cd exposure. With regards to Ca²⁺ a key question is whether Cd (as a Ca²⁺ “substitute”) generates a signal in its own right or whether its impairment of Ca²⁺ homeostasis will be, in effect, the signal. Certainly Cd depolarises the rice root epidermal PM, which would impair Ca²⁺ influx and results in inhibition of root elongation (Li et al., 2012). Cd can permeate guard cell PM Ca²⁺ channels (Perfus-Barbeoch et al., 2002) and may compete with Ca²⁺ for entry into rice root hairs through PM HACC, thus limiting Ca²⁺ influx (Li et al., 2012). Competitive effects appear likely given the ability of exogenous Ca²⁺ addition to alleviate Cd inhibition of root growth of both terrestrial and aquatic plants, implying competition for uptake (Zhang et al., 2012; Rodriguez-Hernandez et al., 2015). Additionally, competitive inhibition by Cd of Ca²⁺ uptake through the wheat LCT1 transporter expressed in yeast has been observed (Clemens et al., 1998). Root hair growth in Arabidopsis is inhibited by Cd; it inhibits Ca²⁺ influx and so dissipates the apical [Ca²⁺]_cyt gradient needed for growth (Fan et al., 2011). This could reflect block of root hair Ca²⁺ influx channels or Cd outcompeting Ca²⁺ for that influx pathway. However, Yeh et al. (2007) observed an increase in rice root [Ca²⁺]_cyt following 15 min of Cd exposure, with a more tolerant variety sustaining a greater increase than a sensitive variety. In roots of the aquatic plant Typha latifolia, Cd exposure increases transcription of TPC1 which suggests that vacuoles might release Ca²⁺ to the cytosol (Rodriguez-Hernandez et al., 2015). Inhibitor treatments indicated involvement of NADPH oxidases, hydroxyl radicals and CIPK upstream of a MAP kinase induction that linked to tolerance (Yeh et al., 2007). Cd stimulates expression and activity of NADPH oxidases in cucumber roots but it is not known if these responses are Ca²⁺-dependent (Jakubowska et al., 2015). It is worth noting that it is not only an increase in [Ca²⁺]_cyt that could stimulate NADPH oxidase activity but that also the restriction of Ca²⁺ entry to the cytosol could cause stimulation (Mortimer et al., 2008). It seems likely that in Arabidopsis roots it would be CAXs predominating in terminating a Cd-induced increase in [Ca²⁺]_cyt. CAX4 mediates Cd and Ca²⁺ transport into Arabidopsis thaliana vacuoles and is needed for correct growth under Cd stress (Mei et al., 2009). CAX1 expression is higher in roots of the Cd-tolerant A. halleri compared to the sensitive A. thaliana (Baliardini et al., 2015).

A key point for future studies is the intersect between Cd and hormones in relation to [Ca²⁺]_cyt. Exogenous Ca²⁺ can ameliorate Cd’s inhibition of Arabidopsis root growth by counteracting effects of NO on auxin homeostasis (Hu et al., 2013; Li P. et al., 2016; Yuan and Huang, 2016). Cd also interferes with auxin homeostasis in barley roots (Zelinova et al., 2015). Auxin itself can increase Arabidopsis root [Ca²⁺]_cyt and this increase is mediated by CNGC14 at the PM, downstream of an unidentified auxin receptor (Shih et al., 2015). This begs the question of whether CNGC14 is an entry route for Cd and the pathway to disrupted auxin homeostasis. Additionally, Cd has been described as a “metallohormone” in that it triggers expression of brassinosteroid-regulated genes in Arabidopsis roots (Villiers et al., 2012). Brassinosteroids are themselves capable of transiently elevating [Ca²⁺]_cyt in Arabidopsis roots (through PM Ca²⁺ influx) and activate a possible DACC in wheat root PM (Straltsova et al., 2015). Again this raises the question of channel identity to help elucidate the relationship between Cd and brassinosteroid signaling and combat the effects of this potent soil contaminant.

Copper, Gadolinium and Lead

In contrast to Cd, transition heavy metals could be capable of generating ROS directly and so perturb [Ca²⁺]_cyt signaling. Transition metals can catalyze production of hydroxyl radicals from superoxide anion and hydrogen peroxide through the Haber-Weiss reaction, with Cu⁺ and Fe²⁺ catalyzing hydroxyl radical production from hydrogen peroxide through the Fenton reaction (Richards et al., 2015). Unless levels of these catalytic metals are tightly controlled, production of hydroxyl radicals (the most potent of the ROS) could inflict significant oxidative damage. Taking Cu as the exemplar, it plays a positive role in hydroxyl radical-activated cell wall loosening for root elongation (Fry et al., 2002) and this could be coupled in Arabidopsis roots to hydroxyl radical-activation of PM Annexin1-mediated Ca²⁺ influx to stimulate exocytosis and growth (Foreman et al., 2003; Laohavisit et al., 2012). This model proposes regulation by extracellular hydroxyl radicals while Rodrigo-Moreno et al. (2013) have proposed that Cu⁺ binding at the intracellular face of the PM in Arabidopsis root tips catalyzes hydroxyl radical production to regulate ion flux. This would allow coupling of Cu transport into the root to regulation of PM Ca²⁺ influx channels. Certainly, low levels of Cu can promote elongation of Arabidopsis primary root and this effect is diminished by blocking PM Ca²⁺ influx channels (Demidchik et al., 2003). The effects of extracellular Cu on PM Ca²⁺ channels and therefore on [Ca²⁺]_cyt signaling are likely to be complex. Electrophysiological analysis of Arabidopsis root epidermal PM has shown that Cu not only activates Ca²⁺ channels through ROS production (Annexin 1; Laohavisit et al., 2012) but also blocks channels, the molecular identity of which remains unknown (Demidchik et al., 2003).

Catalytic production of ROS by Cu is not the only route to modulating [Ca²⁺]_cyt. Longer-term exposure to Cu can stimulate exocytosis-mediated ROS production. Lin et al. (2013) found that inhibiting vesicle traffic with brefeldin also inhibited Cu-stimulated ROS production in rice roots. Whether this involved NADPH oxidase or other ROS generators remains to be determined. Rice root [Ca²⁺]_cyt increases in response to Cu addition and could link to NADPH oxidases and CIPK activity leading to MAP kinase activation (Yeh et al., 2007). It triggers oxidative stress in Populus roots that leads to regulation of CaM genes, implicating perturbation of [Ca²⁺]_cyt (Guerra et al., 2009).

In common with Cd, excess Cu also alters auxin homeostasis in roots and interferes with NO signaling (Lequeux et al., 2010; Kolbert et al., 2012). In excess, Cu stunts Arabidopsis root and root hair elongation and can inhibit lateral root outgrowth (Kolbert et al., 2012). Accumulation of lignin has been observed in both Arabidopsis and rice roots (Lequeux et al., 2010; Liu et al., 2015) and in the former accumulation is associated with the endodermis. It would now be interesting to ascertain whether such wall modification changes [Ca²⁺]_cyt signals in central cells or affects [Ca²⁺]_cyt propagative signaling to the shoot. Root tip cell death has also been observed (Huang et al., 2007; Lequeux et al., 2010; Rodrigo-Moreno et al., 2013). Cu-induced cell death in rice roots was attenuated by chelating extracellular Ca²⁺ thus implicating Ca²⁺ influx across the PM (Huang et al., 2007) while in Arabidopsis roots cell death was attenuated by addition of Gd³⁺ or verapamil as PM Ca²⁺ channel blockers (Rodrigo-Moreno et al., 2013).

Gd³⁺ is routinely used as a PM Ca²⁺ channel blocker, for example with proven efficacy against Arabidopsis root epidermal and root hair HACC, DACC and VICC (Véry and Davies, 2000; Demidchik et al., 2002; Miedema et al., 2008). It is also effective against the root PM hydroxyl radical-activated and H₂O₂-activated Ca²⁺ influx channels (Demidchik et al., 2003, 2007) and the Annexin1-mediated pathway (Laohavisit et al., 2012). As a consequence Gd³⁺ lowers Ca²⁺ influx (measured with ⁴⁵Ca; Demidchik et al., 2002). From this it can be anticipated that Gd³⁺ would have the capacity to dampen stress-induced [Ca²⁺]_cyt signaling in roots, including that mediated by oxidative stress (Demidchik et al., 2003, 2007) and elicited by NaCl (Laohavisit et al., 2013). Pb is less well studied in terms of [Ca²⁺]_cyt. Exogenous Ca²⁺ can protect against root Pb accumulation, suggesting competitive uptake (Rodriguez-Hernandez et al., 2015). However, Pb was found to evoke Ca²⁺ accumulation and diphenyleneiodinium-sensitive ROS increase in rice roots, the latter leading to MAPK activation (Huang and Huang, 2008). Entry of Pb into Arabidopsis roots involves CNGC1 as its deletion confers greater tolerance but whether Pb permeates this channel is unknown (Sunkar et al., 2000). Pb has also been shown to increase expression of TPC1 in Typha roots (Rodriguez-Hernandez et al., 2015) but whether this results in increased [Ca²⁺]_cyt in this or other roots is not known yet.

Mechanical Stress

Roots experience a range of mechanical stimuli, induced as they encounter soil particles or neighboring roots. An increase in [Ca²⁺]_cyt together with an apoplastic alkanisation are early effects induced by mechanical stimuli. One of the known downstream events from the increase in [Ca²⁺]_cyt is the upregulation of touch-sensitive genes such as CML12 and CML24 (Braam, 1992). Mechanically triggered [Ca²⁺]_cyt changes are dependent on the type of stimulus and the responding tissue (Legue et al., 1997; Monshausen et al., 2009). For example, manually bending an Arabidopsis root induces a rapid, biphasic increase in [Ca²⁺]_cyt on the convex side of the roots where cells are stretched (Monshausen et al., 2009) while previously compressed cells on the concave side of the roots show a monophasic and less intense increase in [Ca²⁺]_cyt upon return to their resting position. The source of Ca²⁺ is likely to be extracellular (Monshausen et al., 2009; Richter et al., 2009; Kurusu et al., 2012); with internal stores being mobilized to amplify the response (Chehab et al., 2009; Toyota and Gilroy, 2013).

Over-expressing MCA1 in Arabidopsis lead to an enhanced [Ca²⁺]_cyt transient post mechanical stimulation by the addition of a membrane crenator, however, the mca1 mutant showed no difference from the wild type (Nakagawa et al., 2007). Accordingly, Shih et al. (2014) showed no change in mca1 apoplastic alkalinisation following root bending, which is closely related to the [Ca²⁺]_cyt signature. Thus some levels of compensation occur in mutants deficient in mechanosensitive Ca²⁺ channels. In contrast to the MCAs, MSLs (MscS-Like) were identified in Arabidopsis due to their sequence similarity to the bacterial Mechanosensitive channels of small conductance (MscS) (Haswell et al., 2008). These are encoded by a multiple gene family of 10 members, with MSL9 and MSL10 found in the PM of root cells and required for a mechanosensitive channel activity. They are predominantly anion channels and their relationship to mechano-stimulated [Ca²⁺]_cyt increase has yet to be shown but may be through PM voltage regulation. At this point, it is unclear whether these channels represent mechano-sensors or act downstream of yet unknown mechano-sensors.

Recently, the PM receptor-like kinase FERONIA has been implicated in regulating the Arabidopsis mechano-stimulated [Ca²⁺]_cyt increase and downstream transcriptional regulation (Shih et al., 2014). feronia mutants lack the second peak of the biphasic increase in [Ca²⁺]_cyt elicited in stretched cells by manual bending. However, the mechanism by which FERONIA can regulate [Ca²⁺]_cyt remains unclear as its kinase activity is not essential and targets are unknown. As far as we know, this study was the first in which a mutant with an aberrant mechano-stimulated [Ca²⁺]_cyt increase also showed a root skewing phenotype. Root skewing (deviation from the vertical when grown on vertical or inclined agar) may be influenced by mechano-sensing. At this point, it is unclear whether FERONIA also plays a role in the mechanical induction of lateral root formation (Richter et al., 2009).

Cold Stress

Cold plays a key role in the regulation of physiology and development; the signaling processes relaying non-stressful temperatures (12°C and above) have been reviewed by Wigge (2013). The signaling cascades activated by cold stress (typically 4°C experimentally) and their relations with hormonal signaling have been reviewed by Knight and Knight (2012), Jeon and Kim (2013), Shi et al. (2015) and Eremina et al. (2016). Most studies on the effect of cold stress on [Ca²⁺]_cyt report on seedlings or leaves. From these it is well established that [Ca²⁺]_cyt elevation involves both Ca²⁺ influx across the PM and release from predominantly vacuolar stores (e.g., Knight et al., 1996; Mazars et al., 1997; Knight and Knight, 2000: Zhu et al., 2013). By using an extracellular Ca²⁺-reporting microelectrode, Sulaiman et al. (2012) confirmed that Ca²⁺ influx from the extracellular space is a component of the Arabidopsis root response to cold stress. For Arabidopsis roots, the [Ca²⁺]_cyt response to cold stress measured using aequorin is lower in amplitude and of much shorter duration than leaves (Zhu et al., 2013). Using aequorin Plieth et al. (1999) determined that the faster the rate of cooling Arabidopsis roots, the greater the [Ca²⁺]_cyt response. Sensitivity and magnitude of the [Ca²⁺]_cyt cooling response were enhanced by low temperature but repeated exposure to cold lead to desensitizing of the response. These results imply the existence of Ca²⁺ transport systems that could be regulated at the post-translational and possibly transcriptional levels. In Arabidopsis, cold-induced [Ca²⁺]_cyt elevation would activate a root PM calcium/calmodulin-regulated receptor-like kinase (CRLK1; Yang et al., 2010). This would then activate a specific mitogen-activated protein kinase kinase kinase (MEKK1) that then targets protein kinase kinase2 (MKK2; Furuya et al., 2013). This pathway leads to gene activation and freezing tolerance (Furuya et al., 2014). [Ca²⁺]_cyt elevation would also activate CIPK3, that acts an intersect with ABA signaling (Kim et al., 2003). Part of the transcriptional response to cold in Arabidopsis could be activated by increased [Ca²⁺]_cyt through CAMTA3 regulation of the transcriptional regulator CBF2 (C-Repeat/Dehydration Responsive Element Binding Factor2) (Doherty et al., 2009).

Cold stress has been found to depolarise the PM of root cells from cucumber and Triana bogotensis (Lyalin and Ktitorova, 1969; Minorsky and Spanswick, 1989), consistent with the effect of Ca²⁺ influx across the PM. A modeling exercise revealed the possible importance of a PM DACC in cold stress-induced [Ca²⁺]_cyt elevation of roots (White, 2009). Cold has been shown to activate a PM DACC in leaf protoplasts (Carpaneto et al., 2007) but this has not yet been shown for roots. As microtubule destabilization activates the Arabidopsis root PM DACC (Thion et al., 1998), this could link to the increased cold-induced [Ca²⁺]_cyt signal observed when microtubules are disrupted in Nicotiana plumbaginifolia leaf protoplasts (Mazars et al., 1997). Actin depolymerization is implicated in cold-induced Ca²⁺ influx across the PM into Medicago sativa suspension cells (Orvar et al., 2000). This in turn could relate to the cold-induced activation of pear pollen PM HACC that involves actin depolymerization (Wu et al., 2012). It would be timely therefore to investigate root PM for cold effects on HACC and DACC, exploring also the involvement of the cytoskeleton. In common with mechanical stress, cold stress could perturb the PM bilayer sufficiently to change Ca²⁺ channel activity. Work on M. sativa suspension cells showed that increasing membrane fluidity at 4°C prevented the Ca²⁺ influx across the PM that is necessary to trigger gene expression for freezing tolerance (Orvar et al., 2000). Conversely, imposing membrane rigidity at normal temperature triggers activation of the Ca²⁺-dependent MEKK1-MKK2-MPK4 pathway in Arabidopsis seedlings (Furuya et al., 2014). The possibility that mechanosensitive channels are involved in cold-induced [Ca²⁺]_cyt signaling merits investigation. However, recent work on rice roots indicates another route to Ca²⁺ influx. COLD1 has been identified as a PM activator of the heterotrimeric G protein subunit α (Ma Y. et al., 2015). It is required for cold-activated Ca²⁺ influx to roots (measured using extracellular Ca²⁺-reporting microelectrode) and elevation of root [Ca²⁺]_cyt (aequorin and cameleon determinations). This indicates that heterotrimeric G proteins lie upstream of PM Ca²⁺ channels in the cold response. In common with other stress responses, NADPH oxidase activity also appears in cold stress and needs to be placed in relation to Ca²⁺ channels. Arabidopsis roots exposed to cold stress use AtSRC2 (Soybean gene Regulated by Cold2) to enhance Ca²⁺ activation of the AtRBOHF NADPH Oxidase (Kawarazaki et al., 2013). This suggests that NADPH oxidase activity can lie downstream of Ca²⁺ channel activity. Curtailing cold-induced [Ca²⁺]_cyt elevation could involve vacuolar CAX1 activity in Arabidopsis (Catala et al., 2003).

Conclusion and Future Prospects

A repeated message from this review is how incomplete our knowledge is of the channels mediating stress-induced [Ca²⁺]_cyt increases, and by extension those of organelles. Many members of channel gene families still await characterization. The identification of new families of channels is challenging and will require different approaches linking forward and reverse genetics to electrophysiology. Targets of Ca²⁺-binding and interacting proteins also require further study. Components common to different abiotic stresses are emerging such as Arabidopsis CIPK23 in K⁺ and nitrate deprivation. These common regulatory components are likely to represent critical steps where complex stress signals encountered in the soil are integrated in unified responses. Receptor like kinases such as FERONIA or PERK4 have emerged as new components in [Ca²⁺]_cyt signaling and perhaps other related proteins will be found to have a role in abiotic stress signaling. Remodeling of calcium signaling machinery after stress is also apparent with the possibility of components common to different stresses. For example, Arabidopsis CNGC19 is upregulated under B limitation and salinity stress (Kugler et al., 2009). Finally, [Ca²⁺]_cyt-dependent transcriptional responses can be delineated and future work could include the impact of stress-induced calcium signaling on epigenetic inheritance (Sani et al., 2013; Probst and Scheid, 2015).

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