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Introduction
Stomata plays an important role in signal sensing, transduction and driving environmental change. Stomatal morphology,
development, distribution and behavior respond to a spectrum of signals, from intracellular signaling to global climatic
change[1]. In addition to regulating stomatal movements, environmental signals also alter the number and density of stomata
formed during the development of the
leaf[2]. Drought stress could reduce stomatal density and stomatal
conductance[3]. When field water capacity reduced, stomatal density decreased, while the concentration of
abscisic acid (ABA) accumulation
increased[4]. Some soybean cultivars might respond to the increased levels of ultraviolet-B radiation by increasing
water-use efficiency and this response could be manifested through changes in stomatal development and
functioning[5]. Moreover, many signal transduction pathways are involved in stomatal acclimation process. It has been described as a
negative efficient between CO2 concentration and stomatal
density[6_8]. If the effects of
CO2 on stomatal aperture are brought about through a signaling network, then alterations in sensitivity to this signal should have effects on other
pathways[1]. Besides, stomata are influenced by rhythms, that either control stomatal aperture directly, or modulate the response of
stomata to other signals[1]. It has also been found that the complex signal network existed in the regulation of stomatal
movements[9]. Many environmental factors (eg, light,
CO2, soil water content, atmospheric water vapor pressure, temperature
and wind) can induce and regulate stomatal movements. Besides, the stomatal movements are regulated by
many factors including, vacuolar ion channels in guard cells,
Ca2+([Ca2+]cyt
oscillation), CaM, K+, Mg2+,
ABA, protein kinases, phosphatases and so
on[5,9,10_25].
The phytohormones play an important role in plant physiological processes. Although there is abundant evidence that
ABA closes stomata, ethylene and cytokinin are also both responsible for stomatal
response[26_30]. Stomatal opening is induced by
cytokinins[30]. Stomatal sensitivity to applied cytokinin varies widely according to the species the cytokinin
applied[27,28] and leaf
age[26]. Epidermal strip experiments showed that increasing ethylene synthesis (via application of Ethrel
or 1-aminocyclopropane-1-carboxylic acid (ACC) had variable effects on stomatal response of
Vicia faba)[26]. Phosphorus is not only a constituent of such key cell molecules as ATP, nucleic acids, and phospholipids, but also a pivotal regulator in
many metabolisms, including energy transfer, protein activation, and carbon and amino acid metabolic
processes[31]. In higher plants, Pi limitation enhanced Pi
use[32_34]. In plant cells, all the elements for a calcium-based messenger system
(includ-ing a highly regulated low level of
[Ca2+]cyt, plasma membrane and endomembrane calcium pumps and channels, and
spatially controlled calcium-dependent regulatory proteins and kinases) are contained, which could couple the external
stimuli of hormones to their physiological
response[35]. Calcium signaling in guard cells is one of the major pathways
regulating stomatal movement in which
Ca2+ may act as a second
messenger[2,9,14_18,36].
[Ca2+]cyt oscillation signals of the
guard cell are induced by many external stimuli, such as ABA, calcium,
H2O2, membrane voltage, drought and so on, and the
changes in [Ca2+]cyt regulate stomatal opening and
closing[8,13,14,19,37_47]. Moreover, CaM plays an important role in cell signal
transduction[36]. On the basis of our current knowledge of guard cell signaling, perhaps the best explanation for a hub in
stomatal development is the change in the concentration of guard cells
[Ca2+]cyt that have been induced by ABA, extracellular
calcium ion, and so on.
The known stomatal pattern mutants include the recessive mutations
too many mouths (tmm), four
lips (ftp), and R-558 in
Arabidopsis[48,49]. TMM controls stomatal initiation and spacing,
FLP may regulate guard mother cell fate, and the
R-558 gene product regulates stomatal density. The complexity of the mechanisms that regulate stomatal development was
beginning to be revealed by analyzing these mutant
phenotypes[49,50]. If guard cell signaling is organized as a network, then a
striking property of the network is that it acclimates to external
signals[1]. Acclimation to one signal leads to alterations in
sensitivity to another signal and are consistent with a network-based
organization[1]. Further efforts and more suitable
models from all research disciplines should be used to elucidate this topic. On the foundation of previous researches, we
considered that guard cell signals were recognized and organised by a system or a network in plants. We hypothesized that
stomatal index was controlled by multiple genes and these genes interacted with each other in a network. Therefore, we also
presumed that calcium signaling in guard cells might play a central and primary role in regulating stomatal development. The
purpose of the present study was to try to describe the regulation of signal network on stomatal developments in plants.
Materials and methods
Plant material Arabidopsis thaliana lines used in this study were Columbia wild-type ((Nottingham Arabidopsis Stock
Centre (NASC)) and 10 mutants (cin3-1, ein3-1, ein4, era1-2, gca2, E1, E2, E3, PG1, RW1, phr1) (Table 1). The wild-type
background of these mutants was Columbia.
Growth conditions The 1/2 strength Murashige and Skoog
medium[60] supplemented with 10 g/L sucrose, was used for
seed germination and as basal medium. The pH of the medium was adjusted to 5.7 before agar (Difco, 0.8% agar) was added.
All media were autoclaved for 20 min at
121 °C. Seeds were surface sterilized by soaking in 75% alcohol for 30 s and followed by 15% Clorox for 15 min. The seeds
were then rinsed five times in sterilized water prior to transfer into prepared culture medium. Then the
Arabidopsis seeds, after germinating in the culture medium for seedling development at 4 °C in the dark for 48 h, were placed under 15 h
photoperiod [125
µmol·m-2·s-1, provided by tissue culture chamber (CU-36L5, Percival Scientific, Iowa, USA)] at 20 °C. After
about two weeks, samples were transfered into 11-cm diameter pots with perlite, which has a vermiculite base. Vernalized
seeds of Arabidopsis
thaliana[34] were grown hydroponically in nutrient solution containing 5 mmol/L
KNO3, 2.5 mmol/L
KH2PO4, 2 mmol/L
MgSO4, 2 mmol/L
Ca(NO3)2, 50 µmol/L Fe-EDTA, 70 µmol/L
H3BO4, 14 µmol/L
MnCl2, 0.5 µmol/L CuSO4,
1µmol/L ZnSO4, 0.2 µmol/L
Na2MoO4 and 0.01 µmol/L
CoCl2, pH 5.7[61]. Plants were grown in growth chambers (AR-75L,
Percival Scientific, Boone, IA) under the light of a photosynthetic photon flux density of 125
µmol·m-2·s-1 in a 15-h light/9-h
dark photoperiod. The temperature and humidity were controlled at 22 °C and 70%, respectively. After the pots were covered
with plastic film for 3 d, plants were watered with nutrient solution thoroughly from below, twice each week.
Determination of stomatal index for 20 plants of each mutant and the wild type, all rosette mature leaves were removed
from each plant. After lower epidermis surface of mature rosette leaves was dealt with the methods of nail enamel
printing[62], stomatal density (number of stomata per unit area) and epidermal cell density (number of epidermal cell per unit area) were
measured with microscope eclipse E600W (Japan, NIKON). We measured the stomatal density and epidermal cell density in
five positions per leaf, including tip, middle, and base, the part near to tip, the part near to base.
The epidermal cell density (non-stomatal cells) and stomatal density enabled calculation of the stomatal index as
follows[63]:
Stomatal index=100×stomatal density/(stomatal density+epidermal cell density)
Statistical analyses of data Means of the stomatal indices in wild type and 10 mutants were calculated and stomatal
indices were comparable among different leaf locations (tip, middle, base, the part near to tip, the part near to base) on lower
epidermis surface within each plant type by using ANOVA. Moreover, stomatal indices in wild type and 10 mutants were
compared using ANOVA among the different plant types. LSD (least significant difference) test at the 0.05 significance level
was used to determine differences between mutants
(n=100).
Potential relative effect of genes Consequently, on the basis of the hypothesis that stomatal development is controlled
by a signal network, we used potential relative effect of genes (PREG) to describe the difference between two mutants. The
calculation of the PREG was as follows:
PREG = _(Im_Imi)/Im
Where Im is the stomatal index of certain type, and Imi is the stomatal index of relative types. PREG is negative (when
Imi<Im) or positive (when Imi>Im).
Results
Stomatal distribution and stomatal index In the wild type and 10 mutants, stomatal indices did not differ with respect to
location (tip, middle, base, the part near to tip, the part near to base) on the lower epidermis (LSD test,
P>0.05). The distribution pattern of stomata on the lower epidermis was not affected significantly in all types of mutants used in our
research. Compared mutants with wild type, the stomatal indices of 10 mutants decreased significantly (LSD test,
P<0.05) (Figure1), that of ein4 (ethylene-insensitive mutant 4) was the most obvious change in 10 mutants, and that of RW1 (35s
intervention of Arabidopsis Pi-starvation induced CaM mutant 3) was the least obvious change in 10 mutants.
Potential relative effect of genes We found that significant change existed between some mutants by ANOVA (LSD test,
P<0.05) (Figure 2). PREG describing the difference between two mutants is shown in Figure 2 and Figure 3. PG1 had a positive
effect on ein and cin, while a negative effect on RW1 and phr1; phr1 had a positive effect on ein, cin, era1-2, E, PG1; ein had
a negative effect on phr1, PG1, RW1, E, era1-2, and cin; cin had a positive effect on ein, while a negative effect on phr1, PG1,
and RW1; era1-2 had a positive effect on ein, while a negative effect on phr1 and RW1; E had a positive effect on ein, while
a negative effect on phr1, PG1, and RW1; RW1 had a positive effect on PG1, ein, cin, era1, E. Therefore, significant changes
and interactions might exist between some mutant genes.
Discussion
Stomatal distribution In the wild type and 10 mutants, stomatal indices did not differ with respect to locations. In
endogen, there was regularity in the distribution of stomata on the surface of rice leaves; generally, the stomata arranged
vertically in rows between veins, and were also well-distributed near the veins, the edge and the tip of a
leaf[64]. We conferred that dissimilarity might exist between dicot and endogen, and these mutations in
Arabidopsis did not influence stomatal distribution.
Stomatal index: the negative effect of these mutants on stomatal index in
Arabidopsis thaliana Comparing mutants with
wild type, we found that the stomatal indices of 10 mutants decreased obviously, and significant difference existed between
wild type and 10 mutants by ANOVA (LSD test,
P<0.05; Figure 1). The results were consistent with evolutionism that these
mutants had the negative effects on stomatal index (SI) in
Arabidopsis thaliana. From an evolutional point of view, most
mutations have negative effects on plant growth. For newly arisen mutations, these effects will most likely be harmful
because prevailing genotypes are generally well adapted for their particular environments, and most changes are unlikely to
improve them further[65]. Therefore, we could consider that ethylene, cytokinin, ABA and
AtPsiCaM (Pi-starvation induced CaM) and Pi-starvation-response had something to do with regulating stomatal development; different signal transduction
pathway could influence the same plant process.
Why did the stomatal indices in all of the tested mutants change so significantly? The genome of
Arabidopsis is nearly the smallest one in high plants, and it is
haploidy[54], furthermore, it is easy to get an
Arabidopsis mutant. Thus, combining the results, we could speculate that the stomata intensity in
Arabidopsis might be highly sensitive to most mutations in
genome, while the effects of many gene mutations on the stomatal index might be negative. Moreover, we also could presume
that the stomatal development was regulated by a signal network in which one signal transduction pathway change might
influence the stomatal development more or less; and the stomata intensity could be used as an index of the relative
regulation in the genome transcription signal and metabolic networks.
According to the result, regardless of natural over-expression or intervention in CaM mutant, stomatal indices all
decrease compared with wild type (Figure 1). Whether the expression of CaM was enhanced or intervened, both induced the
decreased change of stomatal index. These showed that CaM was very sensitive to stomatal develop-ment. Therefore, we
considered that whether the expression of CaM was enhanced or intervened, both influence the calcium signal transduction.
Therefore, the calcium signal transduction was possibly a hub in the stomatal development regulation network.
The decrease of the stomatal indices in ethylene insensitive mutants is most obvious compared with that of wild type
(Figure 1). The results showed that ethylene signal made the change of stomatal index decrease and ethylene signal
transduction was sensitive to stomatal development, which could be influenced by calcium signal transduction.
The gene network The network of gene interactions may be obtained among that of calcium signal transduction, Pi
signaling pathway, ETH signaling pathway, CK signaling pathway and ABA signaling pathway based on our findings
(Figure 4).
Calcium signal transduction The role of calcium in various signal transduction pathways is well
known[66,67]. Several studies have implicated
Ca2+ in ethylene signal
transduction[68]. Evidence was presented earlier that
Ca2+ participates in cytokinin signaling in
Amaranthus[67,69]. Organic acids are secreted to calcium cations, which increases mobilization of Pi
from both acidic and calcareous
soils[70]. CaM, a key calcium sensor in all eukaryotes, regulates diverse cellular processes by
interacting with other proteins[36,68]. CaM join in the process of controlling
Ca2+ signal speciality[36]. Calcium, through CaM,
could regulate the activity of EICBP (ethylene-induced CaM-binding protein), which is an ethylene inducible
gene[68]. The proposed cytokinin-induced rise in intracellular calcium may be affected in part by the activation of
CaM[71]. Cytokinin-regulated responses is inhibited by CaM-binding
compounds[72]. CaM-binding proteins are also involved in ethylene signal
transduction[68] .
Pi signaling pathway Vicente Rubio et
al considered that this protein PHR1 acted downstream in the Pi starvation
signaling pathway[33]. Pi starvation-responsive genes appear to be involved in multiple metabolic pathways, implying a
complex Pi regulation system in
plants[34]. Phosphorus regulated almost every signal transduction pathway by a constituent
of such key cell molecules and a pivotal regulator in many metabolisms (including energy transfer, protein activation, and
carbon and amino acid metabolic process-es)[35,36,67,73,74].
Ethylene signaling pathway Ethylene could negatively regulate ABA
synthesis[75]. A calmodulin binding protein from
Arabidopsis is induced by
ethylene[68]. It is likely that ethylene mediates specific aspects of Pi signaling in vascular
plants[70].
Cytokinin signaling pathway Cytokinin, which may involve different classes of
Ca2+ channel[76], increases intracellular
Ca2+ in Funaria[77] and in moss
protoplasts[78]. Cytokinins can elevate ethylene biosynthesis in etiolated
Arabidopsis seedlings via ACC
synthase[51]. It is likely that cytokinin mediates specific aspects of Pi signaling in vascular
plants[70,79]. Under Pi-starvation conditions, Pi regulation system is regulated by
cytokinin[80].
Abscisic acid signaling pathway ABA has been shown to increase the probability of the opening of
hyperpolarization-activated Ca2+-permeable channels. It has also been established that ABA induced
[Ca2+]cyt oscillations in guard
cells[74]. Under Pi-starvation conditions, Pi regulation system is regulated by
ABA[80].
Two signaling pathways interaction Chang et al
have provided evidence that the regulation of flower senescence
involves the interaction of cytokinins, ethylene, and
ABA[81]. Ethylene-mediated cross-talk between calcium-dependent
protein kinase and mitogen-activated protein kinases (MAPK) signaling controls stress responses in
plants[82]. Ethylene is involved in the cytokinin signal transduction, or that ethylene and cytokinins both participate a conjunct approach or
composition[54,83]. ABA signaling is regulated by the ethylene response pathway in
Arabidopsis[75]. Unlike several other hormone interactions involving ethylene, cross-talk between ABA and ethylene appears to occur at many levels and is
dependent on the tissue and the process being
assayed[75,84_86]. Reducing the ethylene response could induce ABA synthesis,
which in turn could increase the dormancy of the
seed[75].
The hypothesis: a network regulate stomatal
development Each cell is a production of multiple signal
transduction programs involving expression of thousands of
genes[87]. In addition, the presence of intracellular signaling components that
feature in multiple signal pathways suggests that the existence of truly stand-alone pathways are highly unlikely, and the
architecture must become increasingly
reticulate[1,87]. The eukaryotic cellular functions are highly connected through
networks[87], the hub of signal transduction that regulate other signal transduction. It is possible that these signal transduction
pathways are modified as guard cells progress through the cell cycle, in response to changes in environment, and during
stomatal development.
Is there any evidence that guard cell signaling is organized as a network and specifically as a type of network known as
a scale-free network? The multiple transcriptional regulators within each category were able to bind to genes encoding
regulators that are responsible for control of other cellular
processes[1]. Recent works show that the control of stomatal
aperture by environmental signals depends on coordinated alterations to guard cell turgor (ionic fluxes and sugars),
cytoskeleton organization, membrane transport, and gene expression and multiple cellular
processes[1]. The action of hormones (auxin and abscisic acid) on guard cells and the organic anions enhanced by changes in apoplastic
K+, Cl_and Ca2+ can alter
their response to light to modulate stomatal
opening[25]. It has also been revealed that a bifurcating signaling pathway directs
ABA effects on stomatal movement[88]. If the effects of
CO2 on stomatal aperture and development might be brought about
through a signaling network, then alterations in sensitivity to this signal should have effects on other
pathways[1,89].
Moreover, during the process of evolution, a plant repairs the original signal transduction pathway to acclimatize oneself
to new environmental change or something else. We speculated that the signal transduction pathway interaction, which
could regulate other morphology, distribution and behavior in plants (eg, roots) responds to a spectrum of signal pathways
in plants, but were also able to regulate stomatal development. In this network, one signal transduction pathway could
regulate stomatal development indirectly, that is, it could act on other signal transductions that might influence stomatal
development directly by an existing pathway. The stand-alone, stimulus-specific signaling pathways might be an inadequate
means of controlling stomatal development. We speculated that the existing regulation network was also able to regulate
stomatal development. Moreover, we presumed the relation existed between mutants; consequently, we constructed a
simplified model (Figure 2, 3) for the
Arabidopsis stomatal development regulatory network upon these data in this paper.
Comparing the two figures (Figure 3, Figure 4), we found similarity between them. We could hypothesize that calcium as a
hub, play an important role in regulating stomatal development in the network; calcium signaling exerted more influence on
regulating stomatal development than ethylene, cytokinin, ABA and Pi signal transduction pathway; the other signal
transduction pathways all regulated stomtal development by influencing calcium signal transduction pathways or being
influenced by calcium signal transduction pathways. Therefore, the presence of multiple cellular processes might interact to
regulate stomatal development, and the architecture might be reticulate.
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