Luan S. (ed.) Coding and Decoding of Calcium Signals in Plants [Signaling and Communication in Plants]
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elevations simply act as threshold-based switches, with their complex dynamics
simply reflecting features of the Ca
2+
homeostatic system and not carrying signifi-
cant information (Scrase-Field and Knight 2003). Alternatively, unique Ca
2+
signatures monitored at the whole plant level could actually reflect cell-type
specific signals, with particular tissues or cells eliciting distinct spatial and/or
temporal changes in Ca
2+
that then lead to cell-type specific response. For example,
when monitored at a whole plant level using the Ca
2+
-sensitive luminescent
photoprotein aequorin ubiquitously expressed in all cell types, cold stress leads to
a characteristic temporal Ca
2+
signature (Fig. 3a, 35S data). However, when the
same Ca
2+
reporter was monitored using transactivation lines to drive cell-type
specific expression of the sensor, distinct differences in this signature were seen
between cell types (Kiegle et al. 2000). Indeed, such cell type specificity of
Fig. 3 Comparison of the calcium response of entire organs compared to individual cell types,
and of a population of cells compared to a single cell.(a) Cytoplasmic calcium changes over time
as reported by aequorin in an Arabidopsis root (35S::aequorin) or in specific cell types of the root
in response to either cold, osmotic, or salt stress. Note the differences in kinetics that are revealed
when observing the calcium response in only the epidermis (red) or endodermis (blue) instead of
the entire organ (grey). Redrawn from Kiegle et al. 2000.(b) Simulated and actual Arabidopsis
guard cell cytoplasmic calcium dynamics in response to cold shock in either a population or a
single cell. The simulation (left panel) is an average of 5,000 individual oscillating cells (inset )
showing an initial synchronous peak followed by a broader peak that represents an amalgamation
of asynchronous oscillations. Actual aequorin measurements of the calcium signature in a guard
cell population responding to cold shock (right panel) match the simulation, and the more sensitive
ratiometic fluorescent calcium indicator yellow cameleon reveals oscillations in a single guard cell
after cold shock (inset). Inset axis labels are the same as those on the outset graph, unless otherwise
marked. Redrawn from Dodd et al. (2006) and Allen et al. (2000)
52 W.-G. Choi et al.
response was seen to a range of stimuli (Fig. 3a). Work in animal cells shows that
even in the same cell, different magnitudes of Ca
2+
elevation can lead to different
suites of response elements being triggered (Dolmetsch et al. 1997). Thus, the same
stimulus could be driving very different responses in different cell types and
averaging the Ca
2+
change over the whole organism may provide a misleading
idea of the kinetics of the response at the cellular level. This point was highlighted
by modeling the kinetics of Ca
2+
change expected from stomatal guard cells
responding to low temperature. When assayed at the single cell level using imaging
of a Ca
2+
-sensitive GFP (Cameleon YC2.1), oscillations were detected in cold
stressed stomatal guard cells (Fig. 3b, right panel insert; Allen et al. 2000), whereas
at the whole plant level using aequorin, which averaged response of many stomata,
a spike and then shoulder of elevated Ca
2+
was recorded (Fig. 3b, right panel; Dodd
et al. 2006). Modeling showed that the initial spike in the whole plant aequorin
measurements likely reflected a synchronous response from the cells, whereas the
shoulder was produced by averaging of the subsequent oscillations exhibited at the
single cell level slowly falling out of phase with each other (Fig. 3b, left panel;
Dodd et al. 2006).
Alternatively, the same cell type could be generating unique Ca
2+
signatures to
different stimuli. In this case there would need to be a mechanism to decode the
spatial and temporal characteristics of these changes to trigger unique outcomes.
Thus, for spatial encoding/decoding, the localization of Ca
2+
-regulated proteins and
Ca
2+
change within the cell could have profound effects on what downstream
changes a spatially localized change in Ca
2+
could elicit. An obvious example
would be Ca
2+
changes elicited in the nucleus where no equivalent simultaneous
cytosolic change occurs, as observed, for example, in the Ca
2+
spiking localized to
the nucleus of root hair cells responding to NOD factors (Ehrhardt et al. 1996). NOD
factors are signaling compounds produced by symbiotic bacteria such as rhizobia as
part of the nodulation signaling pathway of nitrogen fixing symbiosis (Stacey et al.
2006). In this case, only nuclearly localized Ca
2+
-dependent response factors would
be triggered to elicit nuclear response pathways, despite a host of Ca
2+
-dependent
factors also being present in the cytosol. There is evidence that such spatially
localized encoding of response can be extended to even subtler localizations.
Perhaps one of the best examples is seen in mammalian neurons where Ca
2+
influx
through L-type channels in the plasma membrane triggers activation of the CREB
transcription factor. Even though Ca
2+
entry through non-L-type channels can elicit
aCa
2+
increase similar to that of the L-type channel it fails to trigger the signaling
cascade leading to CREB activation (Dolmetsch et al. 2001; West et al. 2001). This
specificity appears to reside in a CaM molecule bound via an “IQ” motif to the inner
surface of the L-type channel. Activation of this specific CaM is needed to activate
the signaling cascade to CREB and only Ca
2+
passing through the L-type channel
has access to this protein. There are numerous examples of spatially localized Ca
2+
changes in response to myriad signals in plants, suggesting this kind of “hard wired”
signal processing could be widespread.
In addition to the spatial component of signal processing, plants also are capable
of generating complex temporal changes in Ca
2+
levels that could also carry
Calcium, Mechanical Signaling, and Tip Growth 53
information to trigger unique responses. In stomatal guard cells many stimuli elicit
Ca
2+
changes linked to stomatal closure (Kim et al. 2010). These Ca
2+
signals are
often seen to oscillate and by experimentally manipulating cytosolic Ca
2+
it has
been possible to impose Ca
2+
transients with a range of frequencies. These
experiments have revealed two mechanisms behind Ca
2+
-dependent signals:
short-term Ca
2+
-reactive closure and long-term Ca
2+
-programmed closure. Ca
2+
-
reactive closure is a threshold phenomenon where Ca
2+
increases to above a critical
level and induces response. The tempor al character of the Ca
2+
spiking in this case
is not relevant. However, Ca
2+
-programmed closure is dependent on the “signature”
of the Ca
2+
change, being sensitive to the frequency and duration of the Ca
2+
spiking. These are genetically separable elements of Ca
2+
signal processing; for
example, a double mutant in the downstr eam Ca
2+
-regulated protein kinases CPK3
and CPK6 show impaired Ca
2+
-reactive closure but unaltered Ca
2+
-programmed
closure. Con versely overexpression of the glutamate receptor homolog AtGLR3.1,
disrupts Ca
2+
programmed closure but not the rapid Ca
2+
-reactive closure (Cho
et al. 2009).
Thus, it appears tha t, at least in the case of the guard cell, there should be
information about the stimulus encoded in the temporal characteristics of the Ca
2+
signal. How then might a c ell take such information and decode it into a bio chemi-
cal change in a signaling pathway? In animal cells, a similar Ca
2+
-dependent
frequency-encoding element has been observed and a possible biochemically
based decoding system has been defined in the characteristics of CaM-dependent
kinase II. Here the kinetics of association and dissociation of Ca
2+
with CaM and
of Ca
2+
-activated CaM with the kinase leads to a bistable switch where only when
Ca
2+
transients are of sufficient magnitude and of sufficient frequency is the kinase
activity switched on (De Koninck and Schulman 1998). Different subunit isoforms
show different frequency responses allowing the cell to tune to the signal it wishes
to decode. Although this mechanism was initially defined in animals, it may well
play a similar role in NOD factor s ignaling where the Ca
2+
/CaM-dependent kinase
(DMI3 or CCaMK) is known to be an important downstream component taking the
Ca
2+
signal elicited by NOD factor perception and then translating this to tran-
scription al activation in the nucleus (Ane et al. 2004; Gleason et al. 2006;
Levy et al. 2004; Mitra et al. 2004a, b; Tirichine et al. 2006). CCaMKs have an
autoinhibitory domain that negatively regulates the kinase (Patil et al. 1995)and
deletion of this domain in DMI3 leads to constitutive nodulation signaling
(Gleason et al. 2006; Tirichine et al. 2006), reinforcing the idea that Ca
2+
-
dependent activation of t his kinase is critica l to NOD factor signaling. Interest-
ingly, the evidence suggests that this system is able to c ount the number of Ca
2+
spikes rather than utilize in formation in the freque ncy domain. Thus, when moni-
toring induction of the N od factor respon sive ENOD11 pr omoter, it was observed
that a threshold of 36 transients was required to trigger response and that the
frequency component of the response was not as critical as absolute number of
transients (Miwa et al. 2006).
54 W.-G. Choi et al.
9 Role of CaM and CDPKs in Growth
There is evidence that these kinds of Ca
2+
-dependent response components might
also play similar roles in translating Ca
2+
signals to the modulation of growth. For
example, proteins such as CaM and calcium-dependent protein kinases (CPKs or
CDPKs) are thought to play important roles during tip growth. Thus, CaM exhibits
a tip-focused gradient in pollen and utilizing a fluorescent indi cator of CaM
activity, Rato and collea gues found this apically localized CaM pulsed in its state
of activation with a period of 40–80 s (Rato et al. 2004). Intracellular activation of a
CaM inhibitory peptide caused reorientation of growth, suggesting CaM may play a
role in the tip growth guidance system. The pollen-specific Arabidopsis protein
NPG1 (No Pollen Germination 1) appears to be a target for three CaM isoforms
(CaM2, 4, and 6) and genetic, histological, and pollen germinat ion analyses
suggests it plays an important role in pollen germination (Golovkin and Reddy
2003).
In addition, several studies have characterized an important role for CDPKs in
the tip growth of pollen tubes and root hairs (reviewed in Kudla et al. 2010 ). It
appears that the spatio-temporal patterns of expression and accumulation of CDPKs
are important in regulating tip growth. For example, using a fluorescent probe for
CDPK activity, Moutinho and collea gues reported CDPK activit y to show a tip-
focused gradient and increases in activation were seen to accompany redirection of
pollen tube growth, suggesting a role in the apical growth machinery (Moutinho
et al. 1998). In maize, ZmCDPK showed pollen specific expression (Estruch et al.
1994) and using the pharmacological CaM and CDPK inhibitors calmidazolium
and W-7, and ZmCDP K mRNA antisense oligonucleotides, In vitro pollen germi-
nation and tube growth were shown to be dependent on CaM/ZmCDPK action. In
addition, Yoon and colleagues showed that Petunia inflata CDPK1 (PiCDPK1) and
PiCDPK2 play distinct roles in pollen tube growth polarity (Yoon et al. 2006).
Transient expression of PiCDPK1 and PiCDPK2 showed that these proteins local-
ize to different subcellular compartments: the plasma membrane for PiCDPK1 and
unknown internal compartment for PiCDPK2. Expression of a catalytically inactive
and a calcium-independent (constitutively active) version of these enzymes caused
disruption of pollen tube elongation and of the tip-focused Ca
2+
gradient showing
that the function of the PiCDPKs is associated with the regulation of pollen tube
growth, possibly involving maintenance of Ca
2+
homeostasis. A requirement for the
function of CDPKs has also been shown in the model plant Arabidopsis (Myers
et al. 2009). Thus, both AtCPK17 and AtCPK34 are targeted to the plasma
membrane during pollen tube germination and tube growth. Homozygous double
knockout mutants of AtCPK17 and AtCPK34 showed a near-sterile phenotype
which was rescued by expression of AtCPK34, suggesting that the functions of
the CPK17 and CPK34 proteins are redundant and essential to pollen tube growth.
Taken together, these observat ions suggest that the function of the CDPKs
is important for pollen tube growth, most likely by decoding the Ca
2+
gradient
generated during pollen tube growth. This role appears conserved in root hair
Calcium, Mechanical Signaling, and Tip Growth 55
elongation as well. A RNA interference line of Medicago truncatula directed
against MtCDPK1 showed both a reduced number of root hairs and root cell
length, resulting in reduction of rhizobial and mycorrhizal symbiotic colonization
(Ivashuta et al. 2005). According to microarray analysis of these plants, silencing of
MtCDPK1 led to altered expression of genes relating to cell wall formation and
defense. These findings are consistent with the idea that the function of MtCDPK1
is to modulate cell expansion or cell wall synthesis of Medicago during plant and
microbe symbioti c interactions.
10 Conclusions and Perspectives
The above discussion highlights a role for Ca
2+
as a ubiquitous regulat or of growth.
There also appears a close connection between Ca
2+
, ROS, and proton fluxes that
may be linked in a conserved response cassette. For tip growth we are beginning to
amass a series of molecularly identified components of this response system from
identified Ca
2+
channels generating the tip-focused Ca
2+
gradient sustaining
growth, to elements of the monomeric G-protein complex, to response components
such as the CDPKs that integrate Ca
2+
change to cellular response. There are strong
parallels to the mechanical signaling system elsewhere in the plant but here we are
currently lack ing equivalent molecular resolution of the signaling components.
Thus, identification of mechanically responsive Ca
2+
permeable channels and
response components such as potentially afforded by CaM or the CPKs is a pressing
need for the field. Interestingly, some of the earliest touch-inducible transcripts
identified, the TCH genes, encode for CaM or CaM-like proteins (McCormack et al.
2005), suggesting touch may be able to remodel its own Ca
2+
response network.
Indeed, in general these classes of Ca
2+
-responsive proteins are known to play roles
in many different processes ranging from the regulation of trichome development
(through modulation of kinesin interacting Ca
2+
-binding protein by cml42; Dobney
et al. 2009), to transcriptional regulation during defense signaling (CaM-binding
transcription factor 3; Du et al. 2009; Galon et al. 2008). One unexpected recent
finding was that Arabidopsis CaM7 can even function directly as a transcription
factor specifically binding to the cis-acting Z-/G-Box (A
TACGTGT/CACGTA)
light-responsive element in promoters o f light-inducible genes, suggesting that
AtCaM7 may regulate expression of genes in response to light signals (Kushwaha
et al. 2008). As such functions continue to be discovered and the spectrum of Ca
2+
binding proteins in plants (such as the CaMs, CaM-like, CDPKS, CBL/CIPKs,
CaMTAs; Dodd et al. 2010; Kudla et al. 2010) become better defined we can
anticipate the molecular mechanisms behind the pervasive role of Ca
2+
in plant
regulation to become more clear. The possibility of a Ca
2+
signal being transduced
through many simultaneous Ca
2+
response networks, each tuned to a specific
component of the Ca
2+
signal, holds the potential to explain in part how plants
56 W.-G. Choi et al.
can integrate such a wide spectrum of stimuli to establish the plastic development
that is a hallmark of plant responses to an ever-changing world.
Acknowledgements This work was supported by grants from the National Science Foundation,
National Aeronautics and Space Administration and United State Department of Agriculture.
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