Advances of calcium signals involved in plant anti-drought

Hong-Bo Shao; Wei-Yi Song; Li-Ye Chu

doi:10.1016/j.crvi.2008.03.012

Biochemistry / Biochimie

Advances of calcium signals involved in plant anti-drought

Présenté par : Philippe Morat

Hong-Bo Shao ^1,^2,³ ; Wei-Yi Song ⁴ ; Li-Ye Chu ³

¹ Institute of Soil and Water Conservation, Chinese Academy of Sciences, Northwest A&F University, Yangling 712100, China
² Binzhou University, Binzhou 256603, China
³ Institute for Life Sciences, Qingdao University of Science & Technology, Qingdao 266042, China
⁴ Biology Department, Shangqiu Normal University, Shangqiu 47600, China

Comptes Rendus. Biologies, Volume 331 (2008) no. 8, pp. 587-596.

Résumé

Considerable progresses have taken place, both in the methodology available to study changes in intracellular cytosolic calcium and in our understanding of calcium signaling cascades, but how calcium signals function in plant drought resistance is questionable. In plant cells, calcium plays roles as a second messenger coupling a wide range of extracellular stimuli with intracellular responses. Different extracellular stimuli trigger specific calcium signatures: dynamics, amplitude and duration of calcium transients specify the nature, implication and intensity of stimuli. Calcium-binding proteins (sensors) play a critical role in decoding calcium signatures and transducing signals by activating specific targets and corresponding metabolic pathways. Calmodulin is a calcium sensor known to regulate the activity of many mammalian proteins, whose targets in plants are now being identified. Higher plants possess a rapidly growing list of calmodulin targets with a variety of cellular functions. Nevertheless, many targets appear to be unique to higher plants and remain characterized, calling for a concerted effort to elucidate their functions. To date, three major classes of plant calcium signals, including calcium permeable ion channels, Ca²⁺/H⁺ antiporters and Ca²⁺-ATPases, have been responsible for drought-stress signal transduction. This review summarizes the current knowledge of calcium signals involved in plant anti-drought and plant water use efficiency (WUE) and presents suggestions for future focus of study.

Métadonnées

Reçu le : 2008-01-21
Accepté le : 2008-03-31
Publié le : 2008-04-28

PMID

DOI : 10.1016/j.crvi.2008.03.012

Mots clés : Plant, Calcium signals, Calmodulin, Anti-drought, WUE, Guard cells, Breeding

Affiliations des auteurs :

Hong-Bo Shao ^{1, 2, 3} ; Wei-Yi Song ⁴ ; Li-Ye Chu ³

@article{CRBIOL_2008__331_8_587_0,
     author = {Hong-Bo Shao and Wei-Yi Song and Li-Ye Chu},
     title = {Advances of calcium signals involved in plant anti-drought},
     journal = {Comptes Rendus. Biologies},
     pages = {587--596},
     publisher = {Elsevier},
     volume = {331},
     number = {8},
     year = {2008},
     doi = {10.1016/j.crvi.2008.03.012},
     language = {en},
}

TY  - JOUR
AU  - Hong-Bo Shao
AU  - Wei-Yi Song
AU  - Li-Ye Chu
TI  - Advances of calcium signals involved in plant anti-drought
JO  - Comptes Rendus. Biologies
PY  - 2008
SP  - 587
EP  - 596
VL  - 331
IS  - 8
PB  - Elsevier
DO  - 10.1016/j.crvi.2008.03.012
LA  - en
ID  - CRBIOL_2008__331_8_587_0
ER  -

%0 Journal Article
%A Hong-Bo Shao
%A Wei-Yi Song
%A Li-Ye Chu
%T Advances of calcium signals involved in plant anti-drought
%J Comptes Rendus. Biologies
%D 2008
%P 587-596
%V 331
%N 8
%I Elsevier
%R 10.1016/j.crvi.2008.03.012
%G en
%F CRBIOL_2008__331_8_587_0

Hong-Bo Shao; Wei-Yi Song; Li-Ye Chu. Advances of calcium signals involved in plant anti-drought. Comptes Rendus. Biologies, Volume 331 (2008) no. 8, pp. 587-596. doi : 10.1016/j.crvi.2008.03.012. https://comptes-rendus.academie-sciences.fr/biologies/articles/10.1016/j.crvi.2008.03.012/

Version originale du texte intégral

1 Introduction

Calcium ion (Ca²⁺) has emerged as an important messenger mediating the actions of many hormone and environmental factors, including biotic and abiotic stresses in higher plants. More evidence implicates that Ca²⁺ is involved in regulating such diverse and fundamental processes such as cytoplasmic streaming, thigmotropism, gravitropism, cell division, cell elongation, cell differentiation, cell polarity, photomorphogenesis, plant defense and stress responses [1–26]. It is believed that calcium influx and cytoplasmic calcium increases are important for guard cell abscisic acid (ABA) transduction [27–39]. It is addressed that Ca²⁺-dependent and Ca²⁺-independent signaling processes in plants are related to certain putative parallels between initial guard cell signaling and both the initiation of defense responses and phytochrome-induced signaling [40–46]. It is generally accepted that a rapid increase in cytosolic calcium concentration is mediated by calcium channels located on the plasma membrane and endomembranes such as vacuolar and endoplasmic reticulum membranes [47–52]. Electrophysiological studies elucidated that plants have Ca²⁺ channels with different types of gating mechanisms: ligand, voltage, and stretch-activated [53–61]. However, only a limited number of genes encoding Ca²⁺ channels have been isolated and functionally expressed. Drought is one of the biggest stresses to agricultural production and quality [62–66]. Plants synthesize mainly the stress hormone ABA in response to drought, triggering a signaling cascade in guard cells that results in stomatal closure, thus reducing water loss that may influence WUE in plants. It was reported that ABA triggers an increase in cytosolic calcium in guard cells, having been proposed to include Ca²⁺ influx across the plasma membrane [67–71]. ABA is known to evoke increases in cytosolic-free [Ca²⁺], which is dependent on flux through Ca²⁺ channels in the plasma membrane and release from intracellular Ca²⁺ stores [72–79]. It was also reported that ABA induces an increase in cytosolic [Ca²⁺] in guard cells, which precedes the reduction in stomatal aperture [80–82]. Therefore, it is believed that such [Ca²⁺] leads to the reduction in stomatal aperture [83,84]. Calcium signal-encoding elements mainly include calcium-permeable ion channels, Ca²⁺/H⁺ antiporters and calcium ATPases. Calcium permeable channels have been investigated with electrophysiological, biochemical and molecular approaches [85–90]. It has been known that in guard cells, membrane hyperpolarization is directly associated with the elevation of cytosolic [Ca²⁺], which follows ABA application [91,92]. Specific patterns of Ca²⁺ elevation may be also involved in controlling both the stomatal closure response and the final steady state of stomatal aperture [93,94]. As a physiological trait of great importance regarding plant drought resistance and yield, much more attention is paid to WUE [95–101]. The molecular research regarding the enhancement of WUE plays important parts in the selection and cultivation of drought-resistant or drought-tolerant crop varieties. When breeding for drought tolerance, biomass productivity and water use efficiency are considered important agronomic characters. Guard cells represent the best characterized plant cell type with respect to ion transport and signal transduction. Stomatal closure can be triggered by raising the cytosolic Ca²⁺ concentration to approximately 1 μM or by drought stress due to ABA production [32,56]. It is clear that the possible relations between calcium signals and plant WUE are involved in the regulation of stomatal closure in guard cells [61,72,76,95,102].

2 Typical plant calcium signals

Plant calcium-signal-encoding elements mainly include calcium permeable ion channels, Ca²⁺/H⁺ antiporters and Ca²⁺-ATPases.

2.1 Calcium permeable ion channels in plants

The previous definition of a Ca²⁺-permeable channel, simply as a channel permeable to Ca²⁺, tacitly assumed that its physiological function was to mediate the Ca²⁺ influx from the apoplast into the cytoplasm [6,8,12,16,26,29,33]. Reports found that the importance of the cellular location of ion channels in determining stimulus specificity is emphasized by a study of Ca²⁺-mediated stomatal closure in tobacco [71,82,98–100]. Removal of extracellular Ca²⁺ with the chelator EGTA or blockage of the entry with a number of ion channel blockers suggested that low-temperature-induced closure involves primarily entry of Ca²⁺ across the plasma membrane, while intracellular mobilization appears to dominate if stomatal closure is initiated with ABA or mechanical stimulation. Another evidence showed that a wheat gene LCT1, encoding a low-affinity cation transporter, can complement yeast mutant with a disruption in the MIDI gene, which encodes a stretch-activated Ca²⁺-permeable non-selective cation channel. AtTPC1 (Arabidopsis two-pore voltage-gated channel1), encoding a two-pore voltage-gated channel with high affinity for Ca²⁺ permeation, was found to rescue the Ca²⁺ uptake activity of a yeast mutant cch1 (which encodes a homologous L-type Ca²⁺ channel) [42]. Cytosolic [Ca²⁺] was enhanced by overexpressing of AtTPC1 or suppressed by antisense expression of it under sucrose stress [72,89]. The molecular basis of plasma membrane Ca²⁺-permeable channel activity is only just becoming apparent, and there is a number of intriguing candidate genes. A unique gene in Arabidopsis, TPC1 (At4 g03560), encodes a channel with two Shaker-like domains (i.e., $2 \times 6$ transmembrane spans, each of which contains a putative ‘pore’ region) connected by a hydrophilic domain that includes two EF hands. The general structure resembles that of the pore-forming subunits of mammalian and yeast Ca²⁺ channels that contain four Shaker-like domains, and there is some sequence similarity. TPC1 expression enhances Ca²⁺ uptake in yeast Ca²⁺-channel mutant [92,97]. OsTPC1, the homolog of AtTPC1, was also identified and characterized [67,75]. TaTPC1 gene, a gene encoding a Ca²⁺ permeable channel, was cloned from wheat and located on the plasma membrane through the application of a TATPC1-GFP fusion protein [35,77]. Expression of TaTPC1 in the yeast mutant lacking CCH1 (homologous to the 1-subunit of a voltage-gated Ca²⁺ channel) can recover its growth through functional complementation, and TaTPC1-overexpression in transgenic plants could accelerate the stomatal closing in the presence of Ca²⁺ when compared with the control plants, indicating that the overexpression of TaTPC1 accelerated the stomatal closing in the presence of Ca²⁺ [99,102]. It was also found that hyperpolarization-activated Ca²⁺-permeable channels play a critical role in the response to ABA-induced stomatal closure through the production of reactive oxygen species, notably hydrogen peroxide [87,89,103–105]. In Arabidopsis guard cells, hydrogen peroxide stimulates hyperpolarization-activated Ca²⁺-permeable channels, thereby increasing cytosolic [Ca²⁺] [105]. Ca²⁺ channels involved in supplying the shoot with calcium are expected to be located primarily in the plasma membrane of root endodermal cells [106,107]. Plasma membrane Ca²⁺ channels from plant roots have been characterized both from calcium flux measurements in isolated vesicles and electrically, either after incorporating vesicles into planar lipid bilayers (PLB) or by patch-clamping root-cell protoplasts. All studies indicate the presence of depolarization-activated Ca²⁺ channels with contrasting pharmacologies. Two distinct Ca²⁺ channel activities have been observed when plasma membrane vesicles derived from rye or wheat roots were incorporated into PLB [108–110]. The inward Ca²⁺ flux through the maxi cation channel is inhibited by ruthenium red, but diltiazem, verapamil and quinine at micromolar concentrations and TEA⁺ at millimolar concentrations inhibited the outward K⁺ flux through this channel only. The second Ca²⁺ channel observed in PLBs has a lower unitary conductance and is termed voltage-dependent cation channel two (VDCC2). It is reported that plasma membrane calcium channels intracellular signaling and may exert effects on metabolism, gene expression and integrated physiological processes, including cell division and cell elongation through regulating cytosolic [Ca²⁺] [111]. It is thought that the inward Ca²⁺ current, which generates the cytosolic [Ca²⁺] gradient, is mediated by the clustering of catalytically active (perhaps mechanosensitive) Ca²⁺ channels at the apex of the root hair. This arrangement would be analogous to the apical clustering of mechanosensitive Ca²⁺ channels involved in osmoregulation and extension of hyphae of the oomycete Saprolegnia ferax or rhizoids of Fucus serratus [112–115]. It is noteworthy that these channels are inhibited by La³⁺, but not by nifedipine or verapamil. A model of calcium-permeable channels involving plant temperature sensing was established based on the fact that calcium influx into the cytoplasm is mediated by calcium-permeable channels, which are assumed to be solely dependent on the cooling rate ( $d T / d t$ ), whereas calcium efflux is mediated by calcium pumps, which have been shown to be dependent on the absolute temperature [116]. Such model suggests that the primary temperature sensor in plants might be a Ca²⁺-permeable channel [117,118]. A hyperpolarization-activated Ca²⁺-permeable channel, which can be suppressed by EGTA, trivalent cations, verapamil, nifedipine or diltiazem, was identified on the plasma membrane of Lilium davidii D pollen protoplasts with whole-cell patch-clamp recording. This primary evidence showed the presence of a voltage-dependent Ca²⁺-permeable channel, whose activity may be regulated by extracellular CaM, in pollen cells [119,120].

2.2 Ca²⁺/H⁺ antiporters in plants

The Ca²⁺/H⁺ antiporter plays a key role, together with Ca²⁺-ATPase, in the accumulation of Ca²⁺ in vacuoles that constitute the primary pool of Ca²⁺ among several organelles of plants. The Ca²⁺/H⁺ antiporter is driven by a pH gradient generated by vacuolar proton pumps. Molecular cloning of the antiporters from Saccharomyces cerevisiae, Arabidopsis thaliana and mung bean revealed that the antiporter is a highly hydrophobic protein with an acidic motif in the centre [35–39,88]. The Ca²⁺-transport activity and intracellular localization of the translation product of cDNA for mung bean Ca²⁺/H⁺ antiporter (VCAX1) were examined. When the cDNA was expressed in Saccharomyces cerevisiae that lacked its own genes for vacuolar Ca²⁺-ATPase and the antiporter, VCAX1 complemented the active Ca²⁺ transporters, and the microsomal membranes from the transformant showed high activity of the Ca²⁺/H⁺ antiporter [121,122]. Ca²⁺/H⁺ antiporters may play an important role in specifying the duration and amplitude of specific cytosolic Ca²⁺ fluctuations through regulating Ca²⁺ efflux. The plant Ca²⁺/H⁺ antiporters were cloned by their ability to suppress the Ca²⁺-hypersensitive phenotype of a Saccharomyces cerevisiae mutant. These genes have been termed as cation exchangers (CAX). CAX1 from Arabidopsis thaliana is a high-capacity and low-affinity Ca²⁺ transporter, which has been shown to be localized to the plant vacuole; its activity appears to be regulated by an N-terminal autoinhibitory domain. Arabidopsis has up to 12 putative Ca²⁺/H⁺ cation antiporters (CAX1–11 and MHX), in which CAX1 is a high-capacity and low-affinity Ca²⁺ transporter [123–125]. When heterologously expressed in yeast, CAX1 is unable to suppress the Ca²⁺ hypersensitivity of yeast vacuolar Ca²⁺ transporter mutants due to an N-terminal autoinhibition mechanism that prevents Ca²⁺ transport. Several results suggest that CAX1 is regulated by several signaling molecules that converge on the N-terminus of CAX1 to regulate H⁺/Ca²⁺ antiporter [62,68,72]. Through using site-directed mutagenesis, 31 mutations in the repeats of the Oryza sativa CAX were generated, which translocates Ca²⁺ and Mn²⁺. Mutant exchangers were expressed in a Saccharomyces cerevisiae strain that is sensitive to Ca²⁺ and Mn²⁺ because of the absence of vacuolar Ca²⁺-ATPase and the Ca²⁺/H⁺ exchanger. Such Ca²⁺/H⁺ exchangers have 11 predicted transmembrane domains (TMs) and an acidic residue-rich region between TM6 and TM7. In CAX1, the 9-amino acid calcium domain exists in the hydrophilic loop between TM1 and TM2. This domain is thought to be involved in the selection of Ca²⁺; however, the sequence has not been found in other CAXs. The C domain located in TM4 may be involved in the selection of Mn²⁺ by Arabidopsis CAX2, which is the only plant CAX known to be capable of Mn²⁺ transport. Based on results from the TMpred program 2, the 451-amino acid protein OsCAX1a was predicted to have 11 TMs, like other CAX proteins [67,92,98].

2.3 Ca²⁺-ATPases in plants

Calcium pumps (Ca²⁺-ATPases) belong to the superfamily of P-type ATPases that directly use ATP to drive ion translocation. Two distinct Ca²⁺ pump families have been proposed based on protein sequence identities [45–47,98,100]. Members of the type IIA and IIB families, respectively, include the ER-type calcium ATPases (ECAs) and the autoinhibited Ca²⁺-ATPases (ACAs). In Arabidopsis, there are four ECA- and ten ACA-type calcium pumps. Isoform ECA1 appears to be located in the ER, as determined by membrane fractionation and immunodetection [78,105,109]. However, the potential for other isoforms targeting to non-ER locations must be considered. In tomato, there is evidence from membrane fractionation and immunodetection, suggesting that related ER-type calcium pumps (LCA1-related) are present in the vacuolar and plasma membranes [110,111]. It is concluded that activity and stability of Ca²⁺-ATPase under 2 °C low temperature are the key factors in the development of cold resistance of winter wheat. It is also suggested that the cold-resistant agent CR-4 plays an important role in stabilizing plasma membrane calcium pump (Ca²⁺-ATPase) under low temperature stress through the electron microscopical observations using the cytochemical method of cerium phosphate precipitation, which indicated that the Ca²⁺-ATPase activity was mainly localized at the plasma membrane in wheat seedling cells growing at normal temperatures. Therefore, it can be inferred that Ca²⁺-ATPase is involved in plant responses to drought, salt and water deficits [125–130].

3 Calcium signals and molecular genetics of plant WUE

Plant WUE is an important index for measuring plant drought resistance and yield. In recent years, numerous progresses have been made in the investigation of plant WUE, especially at the molecular level. The ABA-responsive barley gene HVA1, a member of group-3 late embryogenesis abundant (LEA) protein genes, was introduced into spring wheat (Triticum aesti6um L.) cv. Hi-Line using the biolistic bombardment method [36,83,96]. Two homozygous lines and one heterozygous transgenic line expressing the HVA1 gene had significantly (PB0.01) higher WUE values, i.e. 0.66–0.68 g kg⁻¹, as compared to 0.57 and 0.53 g kg⁻¹, respectively, for the non-expressing transgenic and non-transgenic controls under moderate water deficit conditions. The two homozygous transgenic plant lines also had significantly greater total dry weight, root fresh and dry weight, and shoot dry weight compared to the two controls under soil water deficit conditions. Results of this study indicate that growth characteristics were improved in transgenic wheat plants constitutively expressing the barley HVA1 gene in response to soil water deficit [76,79,92,95]. A T-DNA insertion mutant for the Arabidopsis ABA-transporter AtMRP5 (mrp5-1) was isolated. Guard cells from mrp5-1 mutant plants were found to be intensive to the sulfonylurea compound glibenclamide, which in the wild type induces stomatal opening in the dark. The knockout in AtMRP5 affects several signaling pathways controlling stomatal movements. Stomatal apertures of mrp5-1 and wild-type Ws-2 were identical in the dark. In contrast, opening of stomata of mrp5-1 plants were reduced in the light. In the light, stomatal closure of mrp5-1 was insensitive to external calcium and ABA, a phytohormone responsible for stomatal closure during drought stress [126–130]. In contrast to Ws-2, the phytohormone auxin could not stimulate stomatal opening in the mutant in darkness. All stomatal phenotypes were complemented in transgenic mrp5-1 plants. Both whole-plant and single-leaf gas exchange measurements demonstrated a reduced transpiration rate of mrp5-1 in the light. Excised leaves of mutant plants exhibits reduced water loss, and water uptake was strongly decreased at the whole-plant level. If plants were not watered, mrp5-1 plants survived much longer, due to reduced water use. Analysis of CO₂ uptake and transpiration showed that mrp5-1 plants have increased the WUE.ERECTA gene, encoding a putative leucine-rich repeat receptor-like kinase (LRR-RLK) and known for its effects on inflorescence development, which was isolated and discovered as a major contributor to a locus, called D on Arabidopsis chromosome 2 [87]. Its mechanisms include, but are not limited to, effects on stomatal density, epidermal cell expansion, mesophyll cell proliferation and cell–cell contact. What is more, the results also indicate that the ERECTA gene can change both the stomatal number and structure of a leaf, thus regulating plant transpiration rate and WUE (biomass/amount of water used), which demonstrates excellent prosperities in improving crop drought resistance and high WUE [89,123].

4 Calcium signals and aquaporins involved in plant drought resistance

Plant aquaporins play an important role in water uptake and movement, which open and close a gate that regulates water movement in and out of the cells. Some plant aquaporins also play an important role in response to water stress. Since their discovery, advancing knowledge of their structures and properties led to an understanding of the basic features of the water transport mechanism and increased illumination to plant water relations. Meanwhile, molecular and functional characterization of aquaporins has revealed the significance of their regulation in response to the adverse environments such as drought and salinity [34,53,75,125].

Aquaporins, or Major Intrinsic Proteins (MIPs), are channel-forming membrane proteins with the extraordinary ability to combine a high flux with a high specificity for water across biological membranes. They belong to a well-conserved and ancient family of proteins called the major intrinsic proteins (MIPS), with molecular weights in the range of 26–34 kDa, with members found in nearly all living organisms. The aquaporin family in plants is large, indicating complex and regulated water transport within the plant in order to adapt to different environmental conditions, which includes more than 150 membrane channel proteins. Regulation of aquaporin-mediated water flow, through indirect or direct means, appears to be a mechanism by which plants can control cellular and tissue water movement. All aquaporin isoforms probably work together in an orchestrated manner, where each individual aquaporin isoform displays a specific localization pattern, substrate specificity, and regulatory mechanism [6,46,79,91,130].

Terrestrial plants have evolved to cope with rapid changes in the availability of water by regulating all aquaporins that lie within the plasma membrane [30,43,56,68]. Regulation of aquaporin trafficking may also represent a way to modulate membrane water permeability, and the factors affecting and regulating aquaporin behaviors involve phosphorylation, heteromerization, pH, Ca²⁺, pressure, solute gradients, drought, flooding and so on, which suggests that aquaporins are involved in a versatile and dynamic regulation of water movement [20,32,50,57]. The abundance and activity of aquaporins in the plasma membrane and tonoplast may be regulated, hence enabling the plant to tightly control water fluxes into and out of its cells, as well as within the cells [5,6,19,50].

Currently, powerful evidence indicates that cellular biochemistry and physiology of a living organism is seriously affected by ion homeostasis [32–41,56,98]. Mercury (Hg²⁺) has been used extensively to provide evidence for the involvement of aquaporins in water transport process in animal and plant cells [67]. Due to mercury-induced conformational changes and identification of conserved surface loops in plasma membrane aquaporins from higher plants, mercury is thought to bind to sulphydryl groups of the aquaporin proteins, physically blocking the channels and reducing their hydraulic conductivity [9,111]. Partial recovery of the water flow rate following the application of mercuric chloride was also observed in tomato and aspen root systems, implying the presence of aquaporins as the regulators of plant water status [85,96]. However, the inhibition of water flow with mercurial reagents is not completely understood, and is not a general characteristic of aquaporins [28,38]. Some mercurial reagents, especially mercuric chloride, are highly membrane-permeate and are powerful metabolic inhibitors. That is why the effect of HgC1₂ on water permeation across the living cells should be interpreted with caution, since a possible outcome of HgC1₂ application could be the reduced phosphorylation of water channels [9–12]. Mercury can also induce conformational changes in the plasma membrane aquaporins of higher plants [87].

Calcium signaling is a common pathway in the response of plants to environmental stresses or hormones and cell-specific fluctuations in cytosolic Ca²⁺ occur in the epidermis, endodermis and pericycle of Arabidopsis roots in response to drought and salt [88,98,112]. Aquaporins in plant membranes can undergo Ca²⁺-dependent phosphorylation, which can raise their water-channel activity [19,29,35]. On the other hand, calcium showed a clear effect on aquaporin activity, with two distinct ranges of sensitivity to free Ca²⁺ concentration [72,79]. Since the normal cytoplasmic free Ca²⁺ sits between these ranges, it allows for the possibility of changes in Ca²⁺ to finely up- or down-regulate water channel activity [72,79,89]. Ca²⁺ decreased the osmotic water permeability of PM vesicles from Arabidopsis, suggesting a potential relevance to intracellular Ca²⁺ signaling and further influencing plant WUE [14,92,93,102–106]. At the whole plant's level, Ca²⁺ has also been shown to ameliorate the reduction of root hydraulic conductivity produced by salinity [81,97]. The effect of calcium is predominantly on the cytoplasmic side, and inhibition corresponds to an increase in the activation energy for water transport. However, a link between these observations and cell signaling and/or calcium-dependent water channel gating remains to be established [52,63,67,78,121–130].

5 Conclusions

The calcium signal metabolism performs a pivotal function in the whole multiple signaling networks that mediate a variety of cellular events, including proliferation, differentiation, and cell survival. The presence of it in mammalian cells and plant cells is no longer in any doubt, and this has been corroborated by the detection of the enzymes responsible for phosphoinositide metabolism, phosphoinositide kinases and phosphatases in animals and plants, which is directly linked with calcium signals. Plants have evolved multiple traits that provide resistance against a range of biotic and abiotic stress factors. The majority of studies on plant resistance have focussed on one particular trait and its effect on one particular stress factor. However, plants usually employ multiple lines of resistance against multiple stress factors simultaneously. For instance, in response to herbivore attack, plants both express traits that have a direct negative impact on the herbivore, and traits that enhance the efficacy of the herbivore's natural enemies. In order to better understand the functioning of plant resistance, we study how plants integrate the expression of multiple (inducible) resistance traits in response to various combinations of biotic and abiotic stress factors.

ABA is an endogenous anti-transpirant that induces stomatal closure, thereby leading to water conservation and change of WUE. There is more than 95% of the water that passes through plants exits via the stomatal pores, through which the vast majority of carbon dioxide required for photosynthesis enters. Stomata operate as a miniature homeostatic sensor and effector system that senses a number of stimuli to induce guard cell swelling or shrinking, resulting in stomatal opening or closing, and thus optimization of WUE, a measure of the efficiency with which plants facilitate CO₂ influx at the expense of water loss. Therefore, ABA-induced stomatal closure is closely related with WUE. From the above descriptions, we found out that the changes in cytosolic Ca²⁺ concentration, especially such changes in guard cells, can be regulated by ABA production, thus leading to the change of the stomatal aperture. Moreover, cytosolic Ca²⁺ concentration can be regulated by Ca²⁺ transporters such as calcium-permeable ion channels, Ca²⁺/H⁺ antiporters and Ca²⁺-ATPases, which are also called calcium-signal-encoding elements. We can conclude that the latter, activated by ABA-induced signaling, are involved in regulating WUE through control of the influx and efflux of Ca²⁺ from guard cells. These elements may be involved in the midway process of ABA-induced stomatal closure. The above three kinds of calcium-signal-encoding elements have similar motifs in their molecular structure. We can think that calcium-permeable channels and Ca²⁺/H⁺ antiporters may also be involved in plant stress resistance as Ca²⁺-ATPases do. In addition, we also found out that some genes, seemingly having nothing to do with WUE, can actually directly or indirectly regulate plant WUE, and that some of these genes can even regulate stomatal aperture and stomatal density, which are crucial to the change of WUE. Hence, we can equally conclude that calcium-signal-encoding elements are also involved in the change of plant anti-drought properties and plant WUE. In the presence of Ca²⁺, the overexpression of TaTPC1 (functioning in Ca²⁺ import in wheat cytosol) accelerated stomatal closure. Therefore, it is easy to reach the conclusion that calcium-signal-encoding elements (including calcium permeable ion channels, Ca²⁺/H⁺ antiporters and Ca²⁺-ATPases) can regulate plant WUE through involving in the midway process of ABA-induced stomatal closure and the change of plant WUE; such process can be illustrated as:

ABA signaling transduction → activation of calcium-signal-encoding elements → change of cytosolic Ca²⁺ concentration [Ca²⁺]_cyt → Ca²⁺ signaling transduction → change of the stomatal aperture → change of plant WUE and plant anti-drought properties

The above is our hypothesis about the relations between calcium-signal-encoding elements and WUE in plants. Many more details concerning its molecular mechanism need to be further studied and clarified.

Acknowledgements

The National Science & Technology Supporting Project (2007BAD69B01) and National 863 Water saving of Important Item (2006AA100201) are gratefully acknowledged for supporting this work.

Bibliographie

[1] A.B. Elizabeth Genes commonly regulated by water-deficit stress in Arabidopsis, J. Exp. Bot., Volume 55 (2004), pp. 2331-2341

[2] S. Nobuhiro; R. Mittler Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction, Physiol. Plant., Volume 126 (2006), pp. 45-51

[3] B. Chow; P. McCourt Hormone signaling from a developmental context, J. Exp. Bot., Volume 55 (2004), pp. 247-251

[4] A. Hodge Plastic plants and patchy soils, J. Exp. Bot., Volume 57 (2006), pp. 401-411

[5] N.A. Eckardt; H.T. Cho; R.M. Perrin; M.R. Willmann Plant biology, Plant Cell, Volume 13 (2001), pp. 2165-2173

[6] S. Nishimoto; E. Nishida MAPK signaling: ERK5 versus ERK1/2, EMBO Rep., Volume 7 (2006), pp. 782-786

[7] C.K.Y. Ng; T. Kinoshita; S. Pandey et al. ABA induces rapid subnuclear reorganization in guard cells, Plant Physiol., Volume 134 (2004), pp. 1327-1331

[8] G.M. Pastori; C.H. Foyer Common components, networks, and pathways of cross-tolerance to stress. The central role of ‘Redox’ and ABA-mediated controls, Plant Physiol., Volume 129 (2002), pp. 460-468

[9] J.M. Kwak; V. Nguyen; J. Schroeder The role of reactive oxygen species in hormonal responses, Plant Physiol., Volume 141 (2006), pp. 323-329

[10] L.A. del Rio; L.M. Sandalio; F.J. Corpas et al. Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling, Plant Physiol., Volume 141 (2006), pp. 330-335

[11] C. Gapper; L. Dolan Control of plant development by reactive oxygen species, Plant Physiol., Volume 141 (2006), pp. 341-345

[12] P.M. Mullineaux; S. Karpinski; N.R. Baker Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants, Plant Physiol., Volume 141 (2006), pp. 346-350

[13] M. Sagi; R. Fluhr Production of reactive oxygen species by plant NADPH oxidases, Plant Physiol., Volume 141 (2006), pp. 336-340

[14] H.Y. Zhu; H.K. Choi; D.R. Cook; R.C. Shoemaker Bridging model and crop legumes through comparative genomics, Plant Physiol., Volume 137 (2005), pp. 1189-1196

[15] R. Munns Genes and salt tolerance: bringing them together, New Phytol., Volume 167 (2005), pp. 645-663

[16] A.G. Condon; R.A. Richards; G.J. Rebetzke; G.D. Farquhar Breeding for high water-use efficiency, J. Exp. Bot., Volume 55 (2004), pp. 2447-2460

[17] V. Andjelkovic; R. Thompson Changes in gene expression in maize kernel in response to water and salt stress, Plant Cell Rep., Volume 25 (2006), pp. 71-79

[18] M.A. Rabbani; K. Maruyama; H. Abe et al. Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and ABA application using cDNA microarry and RNA gel-blot analysis, Plant Physiol., Volume 133 (2003), pp. 1755-1767

[19] M.A. Torres; J.D.G. Jones; J.L. Dangl Reactive oxygen species signaling in response to pathogens, Plant Physiol., Volume 141 (2006), pp. 373-378

[20] F. Zaninotton; S. La Camera; A. Polverari; M. Delledonne Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response, Plant Physiol., Volume 141 (2006), pp. 379-383

[21] Y. Soeda; M.C.J.M. Konings; O. Vorst et al. Gene expression programs during Brassica oleracea seed maturation, osmopriming, and germination are indicators of progression of the germination process and the stress tolerance level, Plant Physiol., Volume 137 (2005), pp. 354-368

[22] V. Shulaev; D.J. Oliver Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research, Plant Physiol., Volume 141 (2006), pp. 367-372

[23] D.M. Rhoads; A.L. Umbach; C.C. Subbaiah; J.N. Siedow Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling, Plant Physiol., Volume 141 (2006), pp. 357-366

[24] M.Y. Jiang; J.H. Zhang Abiscisic acid and antioxidant defense in plant cells, Acta Bot. Sin., Volume 46 (2004), pp. 1-9

[25] H.L. Luo; F.M. Song; H. Zheng Overexpression in transgenic tobacco reveals different roles for the rice homeodomain gene OsBIHD1 in biotic and abiotic stress responses, J. Exp. Bot., Volume 56 (2005), pp. 2673-2682

[26] M. Balota; S. Cristescu; W.A. Payne et al. Ethylene production of two wheat cultivars exposed to desiccation, heat, and paraquat-induced oxidation, Crop Sci., Volume 44 (2004), pp. 812-818

[27] G.P. Miles; M.A. Samuel; A.M. Jones; B.E. Ellis Mastoparan rapidly activates plant MAP kinase signaling independent of heterotrimeric G proteins, Plant Physiol., Volume 134 (2004), pp. 1332-1336

[28] V. Demidchik; C. Nichols; M. Oliynyk et al. Is ATP a signaling agent in plants?, Plant Physiol., Volume 133 (2003), pp. 456-461

[29] J.L. Carrasco; G. Ancillo; M.J. Castello; P. Vera A novel DNA-binding motif, hallmark of a new family of plant transcription factors, Plant Physiol., Volume 137 (2005), pp. 602-606

[30] Y. Sakuma; K. Maruyama; Y. Osakabe et al. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression, Plant Cell, Volume 18 (2006), pp. 1292-1309

[31] R. Desikan; J.T. Hancock; J. Bright et al. A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells, Plant Physiol., Volume 137 (2005), pp. 831-834

[32] R. Gupta; S. Luan Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants, Plant Physiol., Volume 132 (2003), pp. 1149-1152

[33] M. Boudsocq; C. Laurière Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families, Plant Physiol., Volume 138 (2005), pp. 1185-1194

[34] J.C. Jang; P. Leon; L. Zhou; J. Sheen Hexokinase as a sugar sensor in higher plants, Plant Cell, Volume 9 (1997), pp. 5-19

[35] J. Hughes; T. Lamparter Prokaryotes and phytochrome. The connection to chromophores and signaling, Plant Physiol., Volume 121 (1999), pp. 1059-1068

[36] P. Bauer; Z. Bereczky Gene networks involved in iron acquisition strategies in plants, Agronomie, Volume 23 (2003), pp. 447-454

[37] J.E. Malamy Intrinsic and environmental response pathways that regulate root system architecture, Plant Cell Environ., Volume 28 (2005), pp. 67-77

[38] U. Bechtold; S. Karpinski; P.M. Mullineaux The influence of the light environment and photosynthesis on oxidative signaling responses in plant-biotrophic pathogen interactions, Plant Cell Environ., Volume 28 (2005), pp. 1046-1055

[39] M.F. Covington; S.L. Harmer The circadian clock regulates auxin signaling and responses in Arabidopsis, PLoS Biol., Volume 5 (2007), pp. 1773-1784

[40] R.D. Hall Plant metabolomics: from holistic hope, to hype, to hot topic, New Phytol., Volume 169 (2006), pp. 453-468

[41] S. de la F. van Bentem; E. Roitinger; D. Anrather et al. Phosphoproteomics as a tool to unravel plant regulatory mechanisms, Physiol. Plant., Volume 126 (2006), pp. 110-119

[42] E. Huq Degradation of negative regulators: a common theme in hormone and light signaling networks?, Trends Plant Sci., Volume 11 (2006), pp. 4-7

[43] P.D. Hare; W.A. Cress; J. Van Staden Dissecting the roles of osmolyte accumulation during stress, Plant Cell Environ., Volume 21 (1998), pp. 535-553

[44] G. Noctor Metabolic signaling in defence and stress: the central roles of soluble redox couples, Plant Cell Environ., Volume 29 (2006), pp. 409-425

[45] S.W. Yu; K.X. Tang MAP kinase cascades responding to environmental stress in plants, Acta Bot. Sin., Volume 46 (2004) no. 2, pp. 127-136

[46] K. Nakashima; K. Yamaguchi-Shinozaki Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants, Physiol. Plant., Volume 126 (2006), pp. 62-71

[47] M. Cvetkovska; C. Rampitsch; N. Bykova; T. Xing Genomic analysis of MAP kinase cascades in Arabidopsis defense responses, Plant Mol. Biol. Rep., Volume 23 (2005), pp. 331-343

[48] D. Lecourieux; R. Ranjeva; A. Pugin Calcium in plant defence-signaling pathways, New Phytol., Volume 171 (2006), pp. 249-269

[49] B. Chow; P. McCourt Hormone signaling from a developmental context, J. Exp. Bot., Volume 55 (2004), pp. 247-251

[50] N.G. Halford; S. Hey; D. Jhurreea et al. Highly conserved protein kinases involved in the regulation of carbon and amino acid metabolism, J. Exp. Bot., Volume 55 (2004), pp. 35-42

[51] N. Geldner The plant endosomal system-its structure and role in signal transduction and plant development, Planta, Volume 219 (2004), pp. 547-560

[52] A.H. Millar; V. Mittova; G. Kiddle et al. Control of ascorbate synthesis by respiration and its implications for stress responses, Plant Physiol., Volume 133 (2003), pp. 443-447

[53] D. Lee; D.H. Polisensky; J. Braam Genome-wide identification of touch-and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes, New Phytol., Volume 165 (2005), pp. 429-444

[54] A. Garcia-Brugger; O. Lamotte; S. Bourque et al. Early signaling events induced by elicitors of plant defenses, Mol. Plant-Microb. Interact., Volume 19 (2006), pp. 711-724

[55] S. Badr; A. Bahiedin; B. Abdelgawad et al. Construction of a dehydrin gene cassette for drought tolerance from wild origin for wheat transformation, Int. J. Bot., Volume 1 (2005), pp. 175-182

[56] D. Fu; M. Lu The structural basis of water permeation and proton exclusion in aquaporins, Mol. Membr. Biol., Volume 24 (2007), pp. 366-374

[57] C. Dutilleul; M. Garmier; G. Noctor et al. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation, Plant Cell, Volume 15 (2003), pp. 1212-1226

[58] C.G. Bartoli; J.-J. Guiamet; G. Kiddle et al. Ascorbate content of wheat leaves is not determined by maximal l-galactono-1,4-lactone dehydrogenase (GalLDH) activity under drought stress, Plant Cell Environ., Volume 28 (2005), pp. 1073-1081

[59] A. Yamamoto; Md.N.H. Bhuiyan; R. Waditee et al. Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants, J. Exp. Bot., Volume 56 (2005), pp. 1785-1796

[60] Q. Gao; M. Yu; X.S. Zhang et al. Modelling seasonal and diurnal dynamics of stomatal conductance of plants in a semiarid environment, Funct. Plant Biol., Volume 32 (2005), pp. 583-598

[61] B. Kohler; A. Hills; M.R. Blatt Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways, Plant Physiol., Volume 131 (2003), pp. 385-388

[62] J. Samaj; F. Baluska; B. Voigt et al. Endocytosis, actin cytoskeleton, and signaling, Plant Physiol., Volume 135 (2004), pp. 1150-1161

[63] H.B. Wang; D.C. Liu; J.Z. Sun; A.M. Zhang Asparagine synthetase gene TaASN1 from wheat is up-regulated by salt stress, osmotic stress and ABA, J. Plant Physiol., Volume 162 (2005), pp. 81-89

[64] M.J. Haydon; C.S. Cobbett Transporters of ligands for essential metal ions in plants, New Phytol., Volume 174 (2007), pp. 499-506

[65] O. Lamotte; C. Courtois; L. Barnavon et al. Nitric oxide in plants: the biosynthesis and cell signaling properties of a fascinating molecule, Planta, Volume 221 (2005), pp. 1-4

[66] N. Etheridge; B.P. Hall; G.E. Schaller Progress report: ethylene signaling and responses, Planta, Volume 223 (2006), pp. 387-391

[67] O. Batistic; J. Kudla Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network, Planta, Volume 219 (2004), pp. 915-924

[68] S. Ramanjulu; D. Bartels Drought- and desiccation-induced modulation of gene expression in plants, Plant Cell Environ., Volume 25 (2002), pp. 141-151

[69] R.E. Sharp; V. Poroyko; L.G. Hejiek et al. Root growth maintenance during water deficits: physiology to functional genomics, J. Exp. Bot., Volume 55 (2004), pp. 2343-2351

[70] C. Bolle The role of GRAS proteins in plant signal transduction and development, Planta, Volume 218 (2004), pp. 683-692

[71] D.Y. Zhou; Q.Y. Tian; L.H. Li; W.H. Zhang Nitric oxide in involved in nitrate-induced inhibition of root elongation in Zea mays, Ann. Bot., Volume 100 (2007), pp. 497-503

[72] Y.L. Shang; X.Y. Li; H.T. Cui et al. RAR1, a central player in plant immunity, is targeted by Pseudomonas syringae effector AvrB, Proc. Natl Acad. Sci., Volume 103 (2006), pp. 19200-19205

[73] M.G. Zhao; Q.Y. Tan; W.H. Zhang Ethylene activates a plasma membrane Ca²⁺-permeable channel in tobacco suspension cells, New Phytol., Volume 174 (2007), pp. 507-515

[74] X.G. Liu; Y.L. Xue; B. Li et al. A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid, Science, Volume 315 (2007) no. 5819, pp. 1712-1716

[75] W.M. Xing; Y. Zou; Q. Liu et al. The structural basis for activation of plant immunity by bacterial effector protein AvrPto, Nature, Volume 449 (2007) no. 7159, pp. 243-247

[76] H.D. Chen; V.J. Karplus; H. Ma; X.W. Deng Plant biology research comes of age in China, Plant Cell, Volume 18 (2006), pp. 2856-2864

[77] D. Bartels; R. Sunkar Drought and salt tolerance in plants, Crit. Rev. Plant Sci., Volume 24 (2005), pp. 23-58

[78] X.L. Hu; M.Y. Jiang; J.H. Zhang et al. Calcium-calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H₂O₂ production in leaves of maize plants, New Phytol., Volume 173 (2007), pp. 27-38

[79] O. Postaire; L. Verdoucq; C. Maurel Aquaporins in plants: from molecular structure to integrated functions, Adv. Bot. Res., Volume 46 (2008), pp. 76-136

[80] M. Fiers; K.L. Ku; C.M. Liu CLE peptide ligands and their roles in establishing meristems, Curr. Opin. Plant Biol., Volume 10 (2007), pp. 39-43

[81] W.H. Cao; J. Liu; X.J. He; R.L. Mu et al. Modulation of ethylene responses affects plant salt-stress response, Plant Physiol., Volume 143 (2007), pp. 707-719

[82] M.B. Bogeat-Triboulot; M. Brosche; J. Renaut et al. Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions, Plant Physiol., Volume 143 (2007), pp. 876-892

[83] Y. Goldgur; S. Rom; R. Rodolfo et al. Desiccation and zinc binding induces transition of tomato abscisic stress ripening1, a water stress- and salt stress-regulated plant-specific protein, from unfolded to folded state, Plant Physiol., Volume 143 (2007), pp. 617-628

[84] K.M. Liu; L. Wang; Y.Y. Xue et al. Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced praline level in rice, Planta, Volume 226 (2007), pp. 1007-1016

[85] W. Zhang; L.M. Fan; W.H. Wu Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics, Plant Physiol., Volume 143 (2007), pp. 1140-1151

[86] X.Y. Dai; Y.Y. Xu; Q.B. Ma et al. Overexpression of a R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis, Plant Physiol., Volume 143 (2007), pp. 1-13

[87] A.J. Thompson; J. Andrews; B.J. Mulholland et al. Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion, Plant Physiol., Volume 143 (2007), pp. 1905-1917

[88] S. Munemasa; K. Oda; M. Watanabe-Sugimoto et al. The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abiscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production, Plant Physiol., Volume 143 (2007), pp. 1398-1407

[89] N. Navrot; V. Collin; J. Gualberto et al. Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses, Plant Physiol., Volume 142 (2006), pp. 1364-1379

[90] R. Jorgensen 21st century plant biology: Viva la Revolucion?, Plant Cell, Volume 19 (2007), pp. 389-390

[91] C.R. Blanding; S.J. Simmons; P. Casati et al. Coordinated regulation of maize genes during increasing exposure to ultraviolet radiation: identification of ultraviolet-responsive genes, functional processes and associated potential promoter motifs, Plant Biotech. J., Volume 5 (2007), pp. 677-695

[92] C.-H. Foyer; G. Noctor Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context, Plant Cell Environ., Volume 28 (2005), pp. 1056-1071

[93] A.J. Trewavas; R. Malho Ca²⁺ signaling in plant cells: the big network, Curr. Opin. Plant Biol. (1998), pp. 428-433

[94] A.S.N. Reddy Calcium: silver bullet in signaling, Plant Sci., Volume 160 (2000), pp. 381-404

[95] R.E. Zielinski Calmodulin and calmodulin-binding proteins in plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., Volume 49 (1998), pp. 697-725

[96] M. John Ward; Z.M. Pei; J.I. Schroeder Roles of ion channels in initiation of signal transduction in higher plants, Plant Cell, Volume 7 (1995), pp. 833-834

[97] T. Furuichi; W.K. Cunningham; S. Muto A putative two pore channel AtTPC1 mediates Ca²⁺ flux in Arabidopsis leaf cells, Plant Cell Physiol., Volume 42 (2001), pp. 900-905

[98] M. Piñeros; M. Tester Calcium channels in higher plant cells: selectivity, regulation and pharmacology, J. Exp. Bot., Volume 48 (1997), pp. 551-577

[99] Z.M. Pei; Y. Murata; G. Benning Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells, Nature, Volume 406 (2000), pp. 731-734

[100] M.R. McAinsh; C. Brownlee; A.M. Hetherington Abscisic acid-induced elevation of guard cell cytoplasmic Ca²⁺ precedes stomatal closure, Nature, Volume 343 (1990), pp. 186-188

[101] Y. Murata; Z.M. Pei; I.C. Mori; J. Schroeder Abscisic acid activation of plasma membrane Ca²⁺ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1–1 and abi2–1 protein phosphatase 2C mutants, Plant Cell, Volume 13 (2000), pp. 2513-2523

[102] D. Sanders; J. Pelloux; C. Brownlee; J.F. Harper Calcium at the crossroads of signaling, Plant Cell (2002), p. S401-S417

[103] A. Grabov; M.R. Blatt Membrane voltage initiates Ca²⁺ waves and potential Ca²⁺ increases with abscisic acid in stomatal guard cells, Proc. Natl Acad. Sci., Volume 95 (1998), pp. 4778-4783

[104] G.J. Allen; S.P. Chu; C.L. Harrington et al. A defined range of guard cell calcium oscillation parameters encodes stomatal movements, Nature, Volume 411 (2001), pp. 1053-1057

[105] J.I. Schroeder; G.J. Allen; V. Hugouvieux; J.M. Kwak; D. Waner Guard cell signal transduction, Annu. Rev. Plant Physiol. Plant Mol. Biol., Volume 52 (2001), pp. 627-658

[106] A. Amtmann; M. Fischer; E.L. Marsh et al. The wheat cDNA LCT1 generates hypersensitivity to sodium in a salt-sensitive yeast strain, Plant Physiol., Volume 126 (2001), pp. 1061-1071

[107] K. Hashimoto; M. Saito; H. Matsuka et al. Functional analysis of a rice putative voltage-dependent Ca²⁺ channel, OSTPC1, expressed in yeast cells lacking its homologous gene CCH1, Plant Cell Physiol., Volume 45 (2004), pp. 496-500

[108] Z.M. Pei; Y. Murata; G. Benning et al. Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells, Nature, Volume 406 (2000), pp. 731-734

[109] X. Zhang; L. Zhang; F.C. Dong et al. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba, Plant Physiol., Volume 126 (2001), pp. 1438-1448

[110] P.J. White Calcium channels in the plasma membrane of root cells, Ann. Bot., Volume 81 (1998), pp. 173-183

[111] P.J. White Characterization of a high-conductance, voltage-dependent cation channel from the plasma membrane of rye roots in planar lipid bilayers, Planta, Volume 191 (1993), pp. 541-551

[112] P.J. White Specificity of ion channel inhibitors for the maxi cation channel in rye root plasma membranes, J. Exp. Bot., Volume 47 (1996), pp. 713-716

[113] P.J. White Cation channels in the plasma membrane of rye roots, J. Exp. Bot., Volume 48 (1997), pp. 499-514

[114] D.S. Bush Calcium regulation in plant cells and its role in signaling, Annu. Rev. Plant Physiol. Plant Mol. Biol., Volume 46 (1995), pp. 95-122

[115] C. Plieth Temperature sensing by plants: Calcium-permeable channels as primary sensors – A model, J. Membr. Biol., Volume 172 (1999), pp. 121-127

[116] Z.L. Shang; L.G. Ma; H.L. Zhang et al. Ca²⁺ Influx into lily pollen grains through a hyperpolarization-activated Ca²⁺-permeable channel which can be regulated by extracellular CaM, Plant Cell Physiol., Volume 46 (2005), pp. 598-608

[117] N.H. Cheng; J.Z. Liu; R.S. Nelson; K.D. Hirschi Characterization of CXIP4, a novel Arabidopsis protein that activates the H⁺/Ca²⁺ antiporter, CAX1, FEBS Lett., Volume 559 (2004), pp. 99-106

[118] T. Kamiya; M. Maeshima Residues in internal repeats of the rice cation/H⁺ exchanger are involved in the transport and selection of cations, J. Biol. Chem., Volume 279 (2004), pp. 812-819

[119] M. Geisler; K.B. Axelsen; J.F. Harper; M.G. Palmgren Molecular aspects of higher plant P-type Ca²⁺-ATPases, Biochim. Biophys. Acta, Volume 1465 (2000), pp. 52-78

[120] K.B. Axelsen; M.G. Palmgren Inventory of the superfamily of P-type ion pumps in Arabidopsis, Plant Physiol., Volume 126 (2001), pp. 696-706

[121] N. Ferrol; A.B. Bennett A single gene may encode differentially localized Ca²⁺-ATPases in tomato, Plant Cell, Volume 8 (1996), pp. 1159-1169

[122] M. Klein; L. Perfus-Barbeoch; A. Frelet et al. The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signaling and water use, Plant J., Volume 33 (2003), pp. 119-129

[123] J. Masle; R.S. Gilmore; R. Graham et al. The ERECTA gene regulates plant transpiration efficiency in Arabidopsis, Nature, Volume 436 (2005) no. 7052, pp. 866-870

[124] K.Q. Ye; J.Y. Ahn Nuclear phophoinositide signaling, Front. Biosci., Volume 13 (2008), pp. 540-548

[125] S. Eisenberg; Y.I. Henis Interactions of Ras proteins with the plasma membrane and their roles in signaling, Cell Signal., Volume 20 (2008), pp. 31-39

[126] H.B. Shao; L.Y. Chu; Z.H. Lu; C.M. Kang Primary oxidant scavenging and redox signaling in higher plants, Int. J. Biol. Sci., Volume 4 (2008), pp. 8-14

[127] H.B. Shao; L.Y. Chu Plant molecular biology in China: Opportunities and challenges, Plant Mol. Biol. Rep., Volume 23 (2005), pp. 345-358

[128] H.B. Shao; L.Y. Chu; M.A. Shao; C.X. Zhao Advances in functional regulation mechanisms of plant aquaporins: their diversity, gene expression, localization, structure and roles in plant water relations, Mol. Membr. Biol., Volume 25 (2008), pp. 1-12

[129] H.B. Shao; X.Y. Chen; L.Y. Chu et al. Investigation on the relationship of Proline with wheat anti-drought under soil water deficits, Biointerfaces, Volume 53 (2006), pp. 113-119

[130] H.B. Shao; Z.S. Liang; M.A. Shao Dynamic changes of anti-oxidative enzymes of 10 wheat genotypes at soil water deficits, Biointerfaces, Volume 42 (2005), pp. 187-194

Commentaires - Politique

Ces articles pourraient vous intéresser

The dynamic changing of Ca²⁺ cellular localization in maize leaflets under drought stress

Yuan-yuan Ma; Wei-yi Song; Zi-hui Liu; ...

C. R. Biol (2009)

RNA-Seq analysis of the wild barley (H. spontaneum) leaf transcriptome under salt stress

Ahmed Bahieldin; Ahmed Atef; Jamal S.M. Sabir; ...

C. R. Biol (2015)

Carbon dioxide signalling in plant leaves

Ulrich Lüttge

C. R. Biol (2007)