Download Calcium oscillations in higher plants Nicola H Evans*, Martin R

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