JXB Advance Access originally published online on December 12, 2003
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Journal of Experimental Botany, Vol. 55, No. 395, pp. 225-236, January 1, 2004
© 2004 Oxford University Press
Signalling in Abiotic Stress |
Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants
Received 4 June 2003; Accepted 18 July 2003
Department of Plant Sciences, University of Arizona, Tucson, AZ 85721, USA
* Present address: Water Technology Centre, Indian Agricultural Research Institute, New Delhi, India. To whom correspondence should be addressed. Fax: +1 520 621 7186. E-mail: jkzhu{at}ag.arizona.edu
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Abstract |
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Top
Abstract
IntroductionThe perception of abiotic stresses and signal transduction to switch on adaptive responses are critical steps in determining the survival and reproduction of plants exposed to adverse environments. Plants have stress-specific adaptive responses as well as responses which protect the plants from more than one environmental stress. There are multiple stress perception and signalling pathways, some of which are specific, but others may cross-talk at various steps. Recently, progress has been made in identifying components of signalling pathways involved in salt, drought and cold stresses. Genetic analysis has defined the Salt-Overly-Sensitive (SOS) pathway, in which a salt stress-induced calcium signal is probably sensed by the calcium-binding protein SOS3 which then activates the protein kinase SOS2. The SOS3–SOS2 kinase complex regulates the expression and activity of ion transporters such as SOS1 to re-establish cellular ionic homeostasis under salinity. The ICE1 (Inducer of CBF Expression 1)–CBF (C-Repeat Binding Protein) pathway is critical for the regulation of the cold-responsive transcriptome and acquired freezing tolerance, although at present the signalling events that activate the ICE1 transcription factor during cold stress are not known. Both ABA-dependent and -independent signalling pathways appear to be involved in osmotic stress tolerance. Components of mitogen-activated protein kinase (MAPK) cascades may act as converging points of multiple abiotic as well as biotic stress signalling pathways. Forward and reverse genetic analysis in combination with expression profiling will continue to uncover many signalling components, and biochemical characterization of the signalling complexes will be required to determine specificity and cross-talk in abiotic stress signalling pathways.
Key words: Abiotic stress, adaptive response, expression profiling, genetic analysis, signal transduction, stress perception.
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Introduction |
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Plants experience various environmental stresses including too little water (drought), too much salt (salinity), and extremes of temperature. Tolerance or susceptibility to these abiotic stresses is a very complex phenomenon, in part, because stress may occur at multiple stages of plant development and often more than one stress simultaneously affects the plant. Perception of stress cues and relay of the signals to switch on adaptive responses are the key steps leading to plant stress tolerance. As a result, differences in stress tolerance between genotypes or different developmental stages of a single genotype may arise from differences in signal perception and transduction mechanisms. Because stress sensors are not known and most of the signalling intermediates have not been identified, there is little definitive information regarding cross-talk between different stress signal transduction pathways in plants. The term ‘cross-talk’ is used here loosely to refer to situations where different signalling pathways share one or more intermediates/components or have some common outputs. Strictly speaking though, signalling pathways sharing common components may not necessarily cross-talk if the common components are scaffolded into distinct protein complexes (Park et al., 2003).
Various abiotic stresses result in both general and specific effects on plant growth and development. For example, drought limits plant growth due to photosynthetic decline, osmotic stress-imposed constraints on plant processes and interference with nutrient availability as the soil dries. Salinity interferes with plant growth as it leads to physiological drought and ion toxicity (Zhu, 2002). Chilling (temperatures below optimal but above freezing) and freezing temperatures can also cause osmotic stress in addition to their direct effect on metabolism (Thomashow, 1999). Therefore, osmotic stress and the associated oxidative stress appear to be common consequences of exposure to drought, salinity and low temperature. Prevention of osmotic stress caused by drought depends upon minimizing stomatal and cuticular water loss and maximizing water uptake (through root growth and osmotic adjustment). During salt stress, osmotic adjustment appears to play a major role in maintaining osmotic homeostasis, while survival during freezing-induced osmotic stress may depend upon prevention or delay of ice nuclei formation. As part of plant stress responses, regulation of gene expression also involves both universal and unique changes in transcript levels of certain plant genes (Shinozaki and Yamaguchi-Shinozaki, 2000). Based on the presence of these general and specific abiotic stress tolerance mechanisms, it is logical to expect plants to have multiple stress perception and signal transduction pathways, which may cross-talk at various steps in the pathways.
In this review, several abiotic stress signalling pathways and common signalling molecules that are important in stress responses are described. Specificity and potential points of cross-talk are discussed when evidence exists.
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Sensory kinases |
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Specificity in signalling is easy to envision if each stress signal has a sensor that can specifically transduce the signal to cellular targets. At present, few stress sensors have been identified and there is not enough information to assess whether cross-talk occurs at the level of sensors. Two-component systems, consisting of a sensory histidine kinase and a response regulator, function as stress sensors in bacteria and yeast. For example, the transmembrane two-component histidine kinases, HIK33 (cyanobacterium) and DesK (Bacillus subtilis) have been suggested as thermosensors (Suzuki et al., 2000; Aguilar et al., 2001). In yeast, an osmosensory histidine kinase, SLN1, senses osmotic stress and activates the HOG1 (high-osmolarity glycerol response 1) mitogen-activated protein kinase (MAPK) cascade (Maeda et al., 1994). Based on the stress-inducibility of its transcript and its ability to complement sln1-ts, a yeast mutant defective in osmosensing, the Arabidopsis thaliana histidine kinase, ATHK1, is thought to be a candidate osmosensor (Urao et al., 1999). ATHK1 gene expression is up-regulated during salt (250 mM NaCl) and low temperature (4 °C) stresses. When expressed in yeast, ATHK1 confers a high degree of osmolarity tolerance to the double mutant sln1
sho1 that lacks both yeast osmosensors, demonstrating that ATHK1 can activate the HOG1 MAPK pathway in yeast (Urao et al., 1999). Some receptor-like protein kinases have been implicated in abiotic stress responses. Transgenic analysis has shown that wound, salt and osmotic stresses induce C7 (NtC7) in tobacco and that this putative membrane-localized receptor-like protein may play an important role in osmotic stress tolerance (Tamura et al., 2003). Determination of the in vivo role of higher plant putative sensory kinases and the identification of signalling intermediates and targets will ultimately be required to determine whether sensor kinase signalling is specific or involved in cross-talk between stress signalling pathways.
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Calcium—a ubiquitous messenger |
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In plant cells, calcium (Ca2+) serves as a second messenger during abiotic stress signalling (Sanders et al., 1999; Knight, 2000). Calcium is a major point of signalling cross-talk because it can be elicited by numerous abiotic as well as developmental, hormonal and biotic stress cues. Specific Ca2+ signatures (e.g. oscillations) have been implicated in numerous physiological processes, such as stomatal regulation where oscillations in cytosolic Ca2+ led to stomatal closure. Further evidence for the importance of Ca2+ in the regulation of stomatal aperture came from studies in which closure was prevented by steady and sustained or non-oscillating cytosolic Ca2+ signals (Allen et al., 2000). The Ca2+ signature changes depending on the particular stress (Kiegle et al., 2000), the rate of stress development (Plieth et al., 1999), previous exposure to stress conditions (Knight et al., 1997), and the tissue type (Kiegle et al., 2000). The mechanisms giving rise to the changes in cytosolic Ca2+ levels are just beginning to be identified. Recent studies have implicated Ca2+ channels in the regulation of cytosolic Ca2+. For example, pharmacological studies have shown that membrane fluidity and reorganization of the cytoskeleton are essential for cold-induced cytosolic Ca2+ oscillations in alfalfa and Brassica napus, respectively (Orvar et al., 2000; Sangwan et al., 2001) suggesting the involvement of stretch/mechanosensitive Ca2+ channels. Pharmacological studies have also shown that cADPR-gated Ca2+ channels are involved in abscisic acid (ABA)-induced expression of cold-regulated genes in tomato (Wu et al., 1997) and B. napus (Sangwan et al., 2001). Inositol 1,4,5-tris phosphate (IP3)-gated Ca2+ channels have been implicated in dehydration- and salt stress-induced cytosolic Ca2+ elevations (DeWald et al., 2001; Takahashi et al., 2001). Genetic analysis of the FRY1 locus of Arabidopsis suggested the involvement of IP3 (which in turn is expected to generate cytosolic Ca2+ oscillations) in ABA, salt and cold stress signalling. FRY1 encodes an inositol polyphosphate 1-phosphatase, which catabolizes IP3. An ABA-induced IP3 transient is altered in the fry1 mutant, which leads to a more sustained accumulation of IP3 and a plant that is hypersensitive to ABA, cold and salt stresses (Xiong et al., 2001b).
Although involvement of a heterotrimeric GTP-binding (G)- protein has been demonstrated in ABA signal transduction during guard cell regulation (Wang et al., 2001), the role of G-protein-associated receptors or classical stress sensors in eliciting Ca2+ signatures during abiotic stress has yet to be shown in plants. Specificity and/or cross-talk in Ca2+ signalling may depend upon the magnitude, duration and subcellular localization of the Ca2+ oscillation as well as Ca2+ sensor diversity. Experimentally induced increases in cytoplasmic Ca2+ (via microinjection, the use of Ca2+ ionophores or Ca2+ channel agonists/antagonists) have been shown to mediate hormone/stress responses (Sheen, 1996; Wu et al., 1997; Orvar et al., 2000; Sangwan et al., 2001). Because these artificial changes in Ca2+ may not exactly mimic stress-induced Ca2+ oscillations, but, nevertheless, were sufficient to regulate stress-specific responses, specificity in signalling might arise downstream of Ca2+, for example, from the presence or absence of a specific Ca2+ responsive signalling complex.
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The SOS pathway regulates ion homeostasis |
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Regulation of cellular ion homeostasis during salinity stress is critical for plant salt tolerance. One of the responses of plant cells to salt stress is the generation of a cytosolic Ca2+ transient (Knight et al., 1997) and the subsequent activation of Ca2+ sensor protein expression and/or activity. Until recently, little was known about the in vivo targets and downstream outputs of salt stress signalling pathways; however, the identification of the Salt-Overly-Sensitive (SOS) pathway in Arabidopsis has begun to reveal components and mechanisms involved in the plant’s response to ionic stress. Molecular analysis of sos mutants of Arabidopsis led to the identification of components (SOS1, SOS2 and SOS3) of a pathway that transduce a salt stress-induced Ca2+ signal to reinstate cellular ion homeostasis (Fig. 1; Zhu, 2002).
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SOS3 is a Ca2+ sensor essential for transducing the salt stress-induced Ca2+ signal and for salt tolerance in Arabidopsis. SOS3 encodes a Ca2+ binding protein with an N-myristoylation motif and three Ca2+-binding EF hands. The amino acid sequence of SOS3 shows significant similarity to the regulatory subunit of yeast calcineurin and animal neuronal Ca2+ sensors (Liu and Zhu, 1998; Ishitani et al., 2000). A loss-of-function mutation that reduces the Ca2+ binding capacity of SOS3 (sos3-1) renders the mutant hypersensitive to salt (Ishitani et al., 2000); a defect that can be partially rescued by high levels of Ca2+ in the growth medium (Liu and Zhu, 1998). SOS3 binds Ca2+ with low affinity when compared to other Ca2+-binding proteins like caltractin and calmodulin (Ishitani et al., 2000). The differences in the affinity of these Ca2+ sensors may ultimately be useful in distinguishing variations in Ca2+ signals.
The search for salt-tolerant determinants also led to the identification of the SOS2 locus in Arabidopsis; the sos2 mutant is also hypersensitive to NaCl stress. SOS2 encodes a serine/threonine protein kinase with an N-terminal kinase catalytic domain similar to SNF1/AMPK, and a unique C-terminal regulatory domain (Liu et al., 2000). Under normal cellular conditions, the catalytic and regulatory domains interact with each other, probably preventing substrate phosphorylation by blocking substrate access. In the presence of Ca2+, SOS3 activates the SOS2 kinase (Halfter et al., 2000). A FISL-motif in the regulatory domain of SOS2 is necessary and sufficient for interaction with SOS3 and deletion of this FISL-motif constitutively activates the SOS2 kinase (Guo et al., 2001). Replacement of Thr168 in the kinase domain by Asp also led to the production of a constitutively active SOS2 kinase. Overexpression of active forms of SOS2 under the control of the CaMV 35S promoter rescued the salt-sensitive phenotype of both sos2 and sos3, supporting the idea that SOS3 and SOS2 are functioning in the same Ca2+-signalling pathway during salt stress (Zhu, 2002).
The first target of the SOS3–SOS2 pathway was identified by molecular genetic analysis of the sos1 mutant of Arabidopsis. As with sos2 and sos3, sos1 is hypersensitive to salt and all three mutants accumulate higher levels of Na+ than is found in wild-type plants. Genetic analysis confirmed that SOS3, SOS2, and SOS1 function in a common pathway of salt tolerance (Zhu et al., 1998). SOS1 encodes a plasma membrane Na+/H+ exchanger (antiporter) with a very long predicted cytoplasmic tail (Shi et al., 2000). The SOS3–SOS2 kinase complex appears to control both the expression and activity of SOS1 (Fig. 1). During salt stress, up-regulation of SOS1 transcript levels is diminished in the sos3 and sos2 mutants (Shi et al., 2000). The Na+/H+ antiport activity of SOS1 was demonstrated in comparisons of activity in plasma membrane vesicles isolated from wild-type and sos1 plants; where activity in sos1 was significantly lower than that in the wild type. A demonstration that SOS1 is a target of the SOS2–SOS3 regulatory pathway and that the antiport activity of SOS1 is regulated by the SOS2 kinase came from experiments in which plasma membrane Na+/H+ antiport activity was compared in vesicles isolated from sos2 and sos3 plants; activity was reduced in both mutants compared to that in wild-type plants and activity in these two mutants could be restored when activated SOS2 protein kinase was added in vitro (Qiu et al., 2002). The SOS3–SOS2 kinase complex was found to phosphorylate SOS1 directly (Quintero et al., 2002). The myristoylation of SOS3 has been shown to be critical for salt tolerance; a mutation in SOS3 that disrupts myristoylation (G2A) causes salt hypersensitivity (Ishitani et al., 2000). One interpretation of these data is that the constitutive myristoylation of SOS3 allows it to recruit SOS2 to the plasma membrane, helping to bring SOS2 to its target SOS1 (Quintero et al., 2002). Recent studies in which the SOS pathway has been functionally reconstituted in Saccharomyces cerevisiae further demonstrate that a salt stress-induced Ca2+ signal is transduced by the SOS3–SOS2 kinase complex to activate SOS1 and to re-establish cellular ion homeostasis (Quintero et al., 2002). Together these experiments suggest that Na+ efflux from root cells experiencing salinity stress may be achieved by the activation of SOS1 by the SOS3–SOS2 complex and that SOS1 probably also retrieves Na+ from the xylem, thereby preventing excess Na+ accumulation in the shoot (Shi et al., 2002, 2003).
Additional targets of the SOS regulatory pathway are emerging. For example, in Arabidopsis, Na+ entry into root cells during salt stress appears to be mediated by AtHKT1, a low affinity Na+ transporter (Uozumi et al., 2000). The athkt1 mutation suppresses the sos3 mutation (Rus et al., 2001), suggesting that the SOS3–SOS2 kinase complex may prevent Na+ influx by inactivating the HKT1 protein or down-regulating HKT1 gene expression during salt stress (Zhu, 2002). In addition, the activity of vacuolar Na+/H+ antiporters may also be activated by SOS3–SOS2 (Fig. 1) (Qiu et al., 2003). Available evidence suggests that the SOS pathway is specific for ion homeostasis responses under salt stress (Fig. 1; Zhu, 2002). Future investigations will determine whether it controls other plant processes and cross-talk with other pathways.
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SOS3-like calcium-binding proteins (SCaBPs) |
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The Arabidopsis genome encodes at least eight SOS3-like Ca2+-binding proteins (SCaBPs) and 23 SOS2-like protein kinases (PKSs, Guo et al., 2001). Since Ca2+ acts as a second messenger in a number of signalling pathways including those initiated by abiotic stresses and hormones, one interesting question is whether the SOS3- and SOS2-like proteins are components of these signalling pathways. Genetic studies to ‘knock-down’ SCaBP and PKS levels using RNA interference (RNAi) have revealed that scabp5 and pks3 mutants are impaired in their response to ABA and that the SCaBP5–PKS3 complex specifically senses and transduces ABA-specific Ca2+ signals (Guo et al., 2002). In these mutants, germination, seedling growth, stomatal regulation, and gene expression were hypersensitive to ABA. ABA-induced expression levels of the cold and drought-responsive genes COR47, COR15A and RD29A were substantially higher in the scabp5 and pks3 mutants when compared with their expression in the wild type, and these mutants expressed higher levels of COR47 and COR15A even without exogenous ABA. In the scabp5pks3 double mutant, ABA sensitivity was not additive, supporting a role for these two proteins in the same ABA signalling pathway. SCaBP5 and PKS3 are specific to ABA-induced Ca2+ signalling, as scabp5 and pks3 were defective in their response to ABA but not in their response to salt and cold stresses or to other plant hormones including auxin, cytokinin, brassinolides, and gibberellins (Guo et al., 2002). As was found for SOS2, PKS3 also contains an autoinhibitory FISL motif, deletion of which (PKS3
F) constitutively activated PKS3; transgenic Arabidopsis ectopically expressing PKS3F showed ABA insensitivity. In yeast two-hybrid assays, SCaBP5 physically interacts with PKS3 which, in turn, strongly interacts with the 2C-type protein phosphatase ABA-insensitive 2 (ABI2) and to a lesser extent with the homologous ABA-insensitive 1 (ABI1) protein. Genetic studies have shown that abi1-1 and abi2-1 are suppressors of the scabp5 and pks3 mutations. The current model is that SCaBP5–PKS3 and ABI2 form part of a Ca2+-responsive negative regulatory loop controlling ABA sensitivity (Fig. 2; Guo et al., 2002).
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Calcium-dependent protein kinases (CDPKs) |
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Besides the PKS family of protein kinases that are responsive to Ca2+ via the SCaBPs, plants also contain a large family of Ca2+-dependent protein kinases (CDPKs). CDPKs have been implicated in signalling pathways in response to stresses such as drought, wounding and cold. Transgenic analyses, studies of stress-responsive gene expression and characterization of CDPK activation suggest that some stress-induced Ca2+ signals are perceived and transduced by CDPKs (Table 1). The involvement of CDPKs in stress-induced gene transcription was demonstrated using a maize leaf protoplast transient expression system (Sheen, 1996). In these studies, a constitutively active form of an Arabidopsis CDPK (AtCDPK1) activated the expression of a barley ABA-responsive promoter fusion (HVA1::LUC; Sheen, 1996). Ectopic expression of CDPK induced the expression of a rice stress-responsive gene, RAB16 (Saijo et al., 2000) and HVA1 in the maize protoplasts (Sheen, 1996). RAB16 and HVA1 have a G-box type ABA-responsive cis element (ABRE), which can be activated by a bZIP transcription factor (Leung and Giraudat, 1998). Overexpression of the catalytic domain of ABI1 inhibited ABA- and AtCDPK1-induced HVA1 transcription (Sheen, 1996). These results suggest that the up-regulation of RAB16 and HVA1 may be mediated by CDPKs, which are under the negative control of ABI1. In the common ice plant Mesembryanthemum crystallinum, CDPK substrate protein 1 (CSP1) has been identified as a substrate protein for McCDPK1. McCDPK1 phosphorylates CSP1 in vitro in a Ca2+-dependent manner and salt stress induces co-localization of McCDPK1 and CSP1 in the nucleus of ice plants (Patharkar and Cushman, 2000). While many more CDPKs exist in the plant genome, little is known about the targets or specificity of most of these kinases.
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Diverse signals converge at MAPK cascades |
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Perhaps some of the strongest evidence for cross-talk during abiotic stress signalling in plants comes from studies of MAPK cascades. The Arabidopsis genome encodes approximately 60 MAPKKKs, 10 MAPKKs and 20 MAPKs. Signals perceived by the 60 MAPKKKs have to be transduced through 10 MAPKKs to 20 MAPKs which offer scope for cross-talk between different stress signals. MAPKs are implicated in developmental, hormonal, biotic, and abiotic stress signalling (Ligterink and Hirt, 2000). Members of MAPK cascades are activated by more than one types of stress, which suggests that MAPK cascades act as points of convergence in stress signalling (Table 2). Two-hybrid analysis and the use of Arabidopsis kinases for complementation studies in yeast led to the identification of a putative Arabidopsis MAPK cascade consisting of AtMEKK1, AtMEK1/AtMKK2, and AtMPK4 (Ichimura et al., 1998). Salt stress induces the expression and activity of AtMEKK1 (Ichimura et al., 2000), which activates AtMPK4 in vitro (Huang et al., 2000). AtMPK4 is activated by cold, low humidity, osmotic stress, touch, and wounding (Ichimura et al., 2000). The Arabidopsis mutant atmpk4 is insensitive to jasmonic acid, accumulates high levels of salicylic acid and shows constitutive Systemic Acquired Resistance (SAR, Peterson et al., 2000). The identification of a MAPK phosphatase 1 mutant (mkp1) in Arabidopsis further demonstrated the complexity of the AtMPK4 signalling cascade. mkp1 is resistant to salinity but hypersensitive to genotoxic stress induced by UV-C. A yeast two-hybrid screen showed that MKP1 could interact with AtMPK4 (Ulm et al., 2002). Although the inputs and outputs of the AtMPK4 pathway have yet to be defined, microarray analysis of mkp1 indicated that the transcript level of a putative Na+/H+-antiporter (AT4G23700) is negatively regulated by AtMKP1 (Ulm et al., 2002). Reactive oxygen species have been shown to activate a MAPK cascade in Arabidopsis that appears to include ANP1 (a MAPKKK), AtMPK3 and AtMPK6 and its positive regulator, Nucleoside Diphosphate Kinase 2 (Kovtun et al., 2000; Moon et al., 2003). Transient expression studies in Arabidopsis mesophyll protoplasts showed that MPK3 and MPK4 function downstream of the flagellin receptor FLS2 (Asai et al., 2002). Studies from alfalfa and tobacco also showed that a MAPK cascade is a node of cross-talk in biotic and abiotic stress signalling (Table 2). Thus biotic and abiotic stress signals converge at the level of MAPK cascades.
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The ICE1 pathway regulates cold-stress-responsive genes |
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Many plant species with origins in temperate regions can acquire tolerance to freezing temperatures by a prior exposure to low non-freezing temperatures, a process called cold acclimation. The expression of COR (cold responsive) genes has been shown to be critical in plants for both chilling tolerance and cold acclimation (Thomashow, 1999; Xiong et al., 2002b). Arabidopsis COR genes (COR78/RD29A, COR47, COR15a, COR6.6) encode LEA-like stress proteins. These genes are induced by cold, dehydration (due to water deficit/high salt/freezing) or ABA. Promoter analysis of the COR genes showed that they contain dehydration responsive elements (DRE) or C-Repeats (CRT) and some of them contain ABREs as well (Yamaguchi-Shinozaki and Shinozaki, 1994; Stockinger et al., 1997). The expression of COR genes is regulated by both ABA-dependent and -independent pathways (Ishitani et al., 1997; Shinozaki and Yamaguchi-Shinozaki, 2000). A family of transcription factors known as C-Repeat binding factors (CBFs) or dehydration responsive element binding factors (DREBs) that control ABA-independent expression of COR genes in response to cold stress has recently been identified. These transcription factors belong to the ethylene-responsive element binding protein/APETELA2 (EREBP/AP2) family (Stockinger et al., 1997; Liu et al., 1998). Ectopic expression of CBFs/DREB1s in transgenic plants turns on downstream cold-responsive genes even at warm temperatures and confers improved freezing, drought and salt tolerance (Jaglo-Ottosen et al., 1998; Liu et al., 1998; Kasuga et al., 1999). An RNA helicase mutant of Arabidopsis, los4 (low expression of osmotically responsive genes), is impaired in the cold-regulated expression of CBF genes and their downstream target genes and, consequently, is sensitive to chilling stress (Gong et al., 2002).
The CBF/DREB1 genes are transiently induced by cold stress, and this induction precedes that of downstream genes with the DRE/CRT cis-element (Thomashow, 1999). Three cold-inducible CBF genes (CBF1/DREB1B, CBF2/DREB1C and CBF3/DREB1A) have been identified in Arabidopsis. The CBF cold-response pathway appears to be conserved in B. napus, wheat, rye, and tomato (Jaglo et al., 2001; Hsieh et al., 2002), suggesting that regulation of the CBF transcriptional cascade during cold stress is an important strategy for plant cold tolerance. Molecular genetic analysis of the HOS1 (high expression of osmotically responsive genes) locus of Arabidopsis showed that cold-signalling components upstream of the CBFs might be regulated by specific ubiquitin-mediated degradation (Lee et al., 2001). The hos1 mutation results in sustained and super-induction of CBF2, CBF3, and their target regulon genes specifically during cold stress. Therefore, HOS1 negatively regulates the COR genes by modulating the expression level of the CBFs. HOS1 encodes a ring finger protein, which has been implicated as an E3 ubiquitin-conjugating enzyme. HOS1 is constitutively expressed but drastically down-regulated within 10 min of cold stress and recovers to basal levels by 1 h of cold stress. HOS1 protein is present in the cytoplasm at normal growth temperatures and accumulates in the nucleus upon cold stress. Thus a positive regulator of CBF expression is probably tagged by HOS1 for protein degradation during cold stress (Fig. 3; Lee et al., 2001).
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Since CBF transcripts begin accumulating within 15 min of plant exposure to cold, it has been proposed that there is a transcription factor already present in the cell at normal growth temperatures that recognizes the CBF promoters and induces CBF expression upon exposure to cold stress (Gilmour et al., 1998). The unknown activator(s) has been called ‘ICE’ (Inducer of CBF Expression) protein(s) and it has been suggested that, upon exposing a plant to cold, modification of either ICE or an associated protein would allow ICE to bind to the CBF promoter and to activate CBF transcription (Gilmour et al., 1998). In order to identify ICE proteins, systematic forward genetic analysis using a reporter gene (CBF3::LUC, the luciferase gene under the transcriptional control of the CBF3 promoter)-based genetic screen was performed in Arabidopsis. Several mutants identified from the screen showed abnormal cold regulation of CBF3::LUC expression as determined by bioluminescence imaging. Molecular genetic analysis of one of the mutants led to the identification of ICE1 (inducer of CBF expression 1), a transcriptional activator of the CBF genes (Chinnusamy et al., 2003). ice1 mutant plants are impaired in cold acclimation and defective in cold-regulated expression of CBF3 and its target COR genes. ICE1 encodes a constitutively expressed and nuclear localized MYC-like basic helix-loop-helix transcription factor. DNA binding assays showed that ICE1 specifically bound to the MYC recognition sequences on the CBF3 promoter, but not to a putative MYB recognition sequence. Transient expression assays indicated that ICE1 is a transcriptional activator. Transgenic lines constitutively overexpressing ICE1 did not express CBF3 at warm temperatures but showed a higher level of CBF3 expression, as well as enhanced expression of the target genes RD29A and COR15A at cold temperatures, suggesting that cold-induced modification of ICE1 protein is necessary for it to act as a transcriptional activator of CBF3 in planta. Taken together, these studies suggest that cold-stress-activated ICE1 binds to the MYC cis-elements of the CBF promoter and induces CBF expression, which, in turn, regulates target COR genes and cold acclimation (Fig. 3; Chinnusamy et al., 2003). The signalling components that transduce the cold stress signal to ICE1 remain to be identified. It is also unclear whether ICE1 also functions in other abiotic stress response pathways.
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ABA-dependence of stress responsive gene expression |
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ABA regulates several aspects of plant development including seed development, desiccation tolerance of seeds and seed dormancy and plays a crucial role in the plant’s response to abiotic (drought, salinity, cold, and hypoxia) and biotic stresses. Although the phenomenon of ABA biosynthesis up-regulation in response to osmotic stress is well known, the signalling pathway by which ABA biosynthetic genes are up-regulated is unknown. A Ca2+-dependent signalling pathway appears to regulate the expression of ABA biosynthetic genes such as ZEP (zeaxanthin epoxidase), NCED (9-cis-epoxycarotenoid dioxygenase), AAO (ABA-aldehyde oxidase), and MCSU (molybdenum cofactor sulphurase) (Xiong et al., 2002b). Genetic analysis of ABA-deficient mutants established the necessity of ABA signalling in stomatal control of water loss from plants (Schroeder et al., 2001). Here the focus is on ABA-mediated stress-responsive gene expression during abiotic stresses. Stress-responsive genes have been proposed to be regulated by both ABA-dependent and ABA-independent signalling pathways (Fig. 2; Shinozaki and Yamaguchi-Shinozaki, 2000; Zhu, 2002). Genetic analysis of the ABA-deficient mutants los5/aba3 and los6/aba1 of Arabidopsis showed that ABA plays a pivotal role in osmotic stress-regulated gene expression. The expression of stress-responsive genes such as RD29A, RD22, COR15A, COR47, and P5CS was severely reduced or completely blocked in the los5 mutant (Xiong et al., 2001a), while in los6, the expression of RD29A, RD19, COR15A, COR47, KIN1, and ADH was lower than in wild-type plants (Xiong et al., 2002a). Therefore, although ABA-independent pathways may exist, an ABA-dependent signalling pathway plays an essential role in stress-responsive gene expression during osmotic stress (Xiong et al., 2001a). Stress-responsive genes contain DRE, ABRE, MYC recognition sequence (MYCRS), and MYB recognition sequence (MYBRS) cis-elements in their promoters (Zhu, 2002). ABA-dependent signalling activates basic leucine zipper transcription factors called ABFs/AREBs to induce stress-responsive gene expression (Xiong et al., 2002b). Recently, Narusaka et al. (2003) showed that the DRE and ABRE elements are interdependent in the expression of the RD29A gene.
Overexpression of a soybean cold- and ABA-inducible C2H2-type zinc finger protein (SCOF1) in Arabidopsis resulted in constitutive expression of stress-responsive genes and freezing tolerance. Although SCOF1 is unable to directly bind to ABRE or DRE/CRT motifs, it enhances the DNA binding activity of SGBF1, a bZIP transcription factor, to ABRE cis-elements of stress-responsive genes (Kim et al., 2001). Thus SCOF1-SGBF1 appears to regulate the ABA-dependent pathway of stress-responsive gene expression through ABRE during cold stress (Kim et al., 2001). ABI5-related (bZIP) transcription factors, AREB1 and AREB2 were found to promote ABA-activation of target gene expression which was repressed by either protein kinase inhibitor treatment of wild-type cells or a dominant-negative abi1-1 mutation (Fig. 2; Uno et al., 2000).
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ABA-independent pathways of stress-responsive gene expression |
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ABA-independent stress-responsive gene expression has been thought to be regulated through DRE cis-elements, while ABA-dependent pathways activate gene expression through ABRE cis-elements. In ABA-independent pathways during osmotic stress signalling, AP2-type transcription factors, DREB2A and DREB2B, trans-activate the DRE cis-element of stress-responsive genes (Fig. 2; Liu et al., 1998). However, cloning and transgenic analysis of a DREB1-related transcription factor, CBF4 in Arabidopsis, showed that regulation of DRE elements may also be mediated by an ABA-dependent pathway. CBF4 gene expression is up-regulated by drought and ABA, but not by cold stress. Overexpression of CBF4 in Arabidopsis resulted in constitutive expression of CRT/DRE containing stress-responsive genes and enhanced tolerance to drought and freezing stresses (Fig. 2; Haake et al., 2002).
Arabidopsis stress-responsive genes may also be regulated by a zinc finger transcriptional repressor STZ/ZAT10 (Lee et al., 2002). Arabidopsis los2, a chilling-sensitive mutant, is impaired in stress-responsive gene expression during cold but not under ABA, salt or osmotic (PEG) stress treatment. However, no apparent difference in CBF expression was observed between the wild type and los2. Cold stress up-regulates LOS2 expression, with LOS2 encoding an enolase that is localized in both the cytoplasm and nucleus. In animals, enolase functions as transcriptional repressor of the c-myc gene (Subramanian and Miller, 2000). Electromobility shift assays showed that the Arabidopsis LOS2 binds to the promoter element of STZ/ZAT10. STZ/ZAT10 expression is induced rapidly and transiently by cold in the wild type, and this induction is stronger and more sustained in the los2 mutant, suggesting that LOS2 acts as a repressor of STZ/ZAT10 expression during cold stress (Lee et al., 2002). Thus stress-responsive proteins act as effectors of cold, drought and salt tolerance, but different signalling pathways control the expression of stress-responsive genes during cold and osmotic stresses. The components of both ABA-dependent and -independent signalling pathways that activate the transcription factors need to be genetically defined in order to assess whether a signalling pathway is specific to a stress or is involved in cross-talk with other pathways.
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Conclusions and perspectives |
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Several abiotic stress signalling pathway components have been identified based on mutant analysis or their stress induction, ability to complement the growth of relevant yeast mutants and ectopic expression studies. Genetic analysis has been successfully exploited to define the SOS pathway of ion homeostasis during salt stress. Some of the events involved in the regulation of freezing tolerance by the ICE1–CBF pathway and osmotic stress tolerance by ABA-dependent and -independent pathways are becoming clearer. However, there is still only a fragmentary view of abiotic stress signalling pathways. Forward and reverse genetics approaches will continue to be imperative to dissect these complex pathways. Although conventional genetic screens have yielded valuable insight into stress signal transduction, this approach may ultimately be limited because of the functional redundancy of components within the signalling pathways. Reporter gene-based molecular screens offer a way systematically to identify upstream signalling components that control subsets of responses, which may not manifest as visible tolerance phenotypes. Thorough characterization of mutant phenotypes will provide an indication whether a signalling component functions in a specific pathway or is involved in multiple pathways. Cell biological analysis of spatial and temporal expression patterns, combined with biochemical characterization of the components, particularly identification of signalling complexes, will be required to firmly establish specificity or cross-talk of the signalling pathways.
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Acknowledgements |
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Our work has been supported by grants from USDA-NRI, BARD, SWC, NSF, and NIH.
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References |
|---|
Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D. 2001. Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO Journal 20, 1681–1691.[CrossRef][Web of Science][Medline]
Allen G, Chu SP, Schumacher K, et al. 2000. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289, 2338–2342.
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983.[CrossRef][Medline]
Baluska F, Ovecka M, Hirt H. 2000. Salt stress induces changes in amounts and localization of the mitogen-activated protein kinase SIMK in alfalfa roots. Protoplasma 212, 262–267.[CrossRef]
Cardinale F, Jonak C, Ligterink W, Niehaus K, Boller T, Hirt H. 2000. Differential activation of four specific MAPK pathways by distinct elicitors. Journal of Biological Chemistry 275, 36734–36740.
Cardinale H, Meskiene I, Ouaked F, Hirt H. 2002. Convergence and divergence of stress-induced mitogen-activated protein kinase signalling pathways at the level of two distinct mitogen-activated protein kinase kinases. The Plant Cell 14, 703–711.
Chinnusamy V, Ohta M, Kanrar S, Lee B-H, Hong X, Agarwal M, Zhu J-K. 2003. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes and Development 17, 1043–1054.
DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, Thompson JE, Prestwich GD, Hama H. 2001. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiology 126, 759–769.
Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF. 1998. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. The Plant Journal 16, 433–443.[CrossRef][Web of Science][Medline]
Gong Z, Lee H, Xiong L, Jagendorf A, Stevenson B, Zhu J-K. 2002. RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proceedings of the National Academy of Sciences, USA 99, 11507–11512.
Guo Y, Halfter U, Ishitani M, Zhu J-K. 2001. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. The Plant Cell 13, 1383–1400.
Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu J-K. 2002. A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signalling in Arabidopsis. Development Cell 3, 233–244.
Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ. 2002. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiology 130, 639–648.
Halfter U, Ishitani M, Zhu J-K. 2000. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proceedings of the National Academy of Sciences, USA 97, 3735–3740.
Hoyos ME, Zhang S. 2000. Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiology 122, 1355–1364.
Hsieh TH, Lee LT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT. 2002. Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiology 129, 1086–1094.
Huang Y, Li H, Gupta R, Morris PC, Luan S, Kieber JJ. 2000. ATMPK4, an Arabidopsis homolog of mitogen-activated protein kinase, is activated in vitro by AtMEK1 through threonine phosphorylation. Plant Physiology 122, 1301–1310.
Ichimura K, Mizoguchi T, Irie K, Morris P, Giraudat J, Matsumoto K, Shinozaki K. 1998. Isolation of ATMEKK1 (a MAP kinase kinase kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. Biochemical and Biophysical Research Communications 253, 532–543.[CrossRef][Web of Science][Medline]
Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K. 2000. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. The Plant Journal 24, 655–665.[CrossRef][Web of Science][Medline]
Ishitani M, Liu J, Halfter U, Kim C-S, Shi W, Zhu J-K. 2000. SOS3 function in plant salt tolerance requires N-myristoylation and calcium-binding. The Plant Cell 12, 1667–1677.
Ishitani M, Xiong L, Stevenson B, Zhu J-K. 1997. Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis thaliana: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. The Plant Cell 9, 1935–1949.[Abstract]
Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF. 2001. Components of the Arabidopsis C-repeat/dehydration responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiology 127, 910–917.
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF. 1998. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280, 104–106.
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1999. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17, 287–291.
Kiegerl S, Cardinale F, Siligan C, et al. 2000. SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress induced MAPK, SIMK. The Plant Cell 12, 2247–2258.
Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR. 2000. Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. The Plant Journal 23, 267–278.[Medline]
Kim JC, Lee SH, Cheng YH, et al. 2001. A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. The Plant Journal 25, 247–259.[CrossRef][Web of Science][Medline]
Knight H. 2000. Calcium signalling during abiotic stress in plants. International Review of Cytology 195, 269–325.[Web of Science][Medline]
Knight H, Trewavas AJ, Knight MR. 1997. Calcium signalling in Arabidopsis thaliana responding to drought and salinity. The Plant Journal 12, 1067–1078.[CrossRef][Web of Science][Medline]
Kovtun Y, Chiu W-L, Tena G, Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proceedings of the National Academy of Sciences, USA 97, 2940–2945.
Lee H, Guo Y, Ohto M, Xiong L, Stevenson B, Zhu J-K. 2002. LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO Journal 21, 2692–2702.[CrossRef][Web of Science][Medline]
Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu J-K. 2001. The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes and Development 15, 912–924.
Leung J, Giraudat J. 1998. Abscisic acid signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 49, 199–222.[CrossRef][Web of Science][Medline]
Ligterink W, Hirt H. 2000. MAP kinase pathways in plants: versatile signalling tools. International Review of Cytology 201, 209–258.
Liu J, Ishitani M, Halfter U, Kim C-S, Zhu J-K. 2000. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proceedings of the National Academy of Sciences, USA 97, 3730–3734.
Liu J, Zhu J-K. 1998. A calcium sensor homolog required for plant salt tolerance. Science 280, 1943–1945.
Liu Q, Sakuma Y, Abe H, Kasuga M, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain, separate two cellular signal transduction pathways in drought- and low temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell 10, 1391–1406.
Maeda T, Wurgler-Murphy SM, Saito H. 1994. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369, 242–245.[CrossRef][Medline]
Mikolajczyk M, Awotunde OS, Muszyska G, Klessig DF, Dobrowolska G. 2000. Osmotic stress induces rapid activation of a salicylic acid–induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. The Plant Cell 12, 165–178.
Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K. 1996. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 93, 765–769.
Moon H, Lee B, Choi G, et al. 2003. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proceedings of the National Academy of Sciences, USA 100, 358–363.
Munnik T, Ligterink W, Meskiene I, Calderini O, Beyerly J, Musgrave A, Hirt H. 1999. Distinct osmosensing protein kinase pathways are involved in signalling moderate and severe hyper-osmotic stress. The Plant Journal 20, 381–388.[CrossRef][Web of Science][Medline]
Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. The Plant Journal 34, 137–148.[CrossRef][Web of Science][Medline]
Orvar BL, Sangwan V, Omann F, Dhindsa R. 2000. Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. The Plant Journal 23, 785–794.[CrossRef][Web of Science][Medline]
Park SH, Zarrinpar A, Lim WA. 2003. Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms. Science 299, 1061–1064.
Patharkar OR, Cushman JC. 2000. A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator. The Plant Journal 24, 679–691.[CrossRef][Web of Science][Medline]
Peterson M, Brodersen P, Naested H, et al. 2000. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111–1120.[CrossRef][Web of Science][Medline]
Plieth C, Hansen, U-P, Knight H, Knight MR. 1999. Temperature sensing by plants: the primary characteristics of signal perception and calcium response. The Plant Journal 18, 491–497.[CrossRef][Web of Science][Medline]
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu J-K. 2002. Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proceedings of the National Academy of Sciences, USA 99, 8436–8441.
Qiu QS, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, Zhu JK. 2003. Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the SOS pathway. Journal of Biological Chemistry: 10.1074Jbc.M307982200.
Quintero FJ, Ohta M, Shi H, Zhu, J-K, Pardo JM. 2002. Reconstitution in yeast of the Arabidopsis SOS signalling pathway for Na+ homeostasis. Proceedings of the National Academy of Sciences, USA 99, 9061–9066.
Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee B-H, Matsumoto TK, Koiwa H, Zhu J-K, Bressan RA, Hasegawa PM. 2001. AtHKT1 is a salt-tolerance determinant that controls Na+ entry into plant roots. Proceedings of the National Academy of Sciences, USA 98, 14150–14155.
Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K. 2000. Over-expression of a single Ca2+ dependent protein kinase confers both cold and salt/drought tolerance on rice plants. The Plant Journal 23, 319–327.[CrossRef][Web of Science][Medline]
Sanders D, Brownlee C, Harper JF. 1999. Communicating with calcium. The Plant Cell 11, 691–706.
Sangwan V, Foulds I, Singh J, Dhindsa RS. 2001. Cold-activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx. The Plant Journal 27, 1–12.[CrossRef][Web of Science][Medline]
Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D. 2001. Guard cell signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 52, 627–658.[CrossRef][Web of Science][Medline]
Sheen J. 1996. Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274, 1900–1902.
Shi H, Ishitani M, Kim C-S, Zhu J-K. 2000. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences, USA 97, 6896–6901.
Shi H, Lee B-H, Wu S-J, Zhu J-K. 2003. Overexpression of a plasma membrane Na+/H+ antiporter improves salt tolerance in Arabidopsis. Nature Biotechnology 21, 81–85.[CrossRef][Web of Science][Medline]
Shi H, Quintero FJ, Pardo JM, Zhu J-K. 2002. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. The Plant Cell 14, 465–477.
Shinozaki K, Yamaguchi-Shinozaki K. 2000. Molecular response to dehydration and low temperature: differences and cross-talk between two stress signalling pathways. Current Opinion in Plant Biology 3, 217–223.[Web of Science][Medline]
Stockinger EJ, Gilmour SJ, Thomashow MF. 1997. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcription activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences, USA 94, 1035–1040.
Subramanian A, Miller DM. 2000. Structural analysis of alpha-enolase. Mapping the functional domains involved in down-regulation of the c-myc proto-oncogene. Journal of Biological Chemistry 275, 5958–5965.
Suzuki I, Dmitry AL, Kanesaki Y, Mikami K, Murata N. 2000. The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO Journal 19, 1327–1334.[CrossRef][Web of Science][Medline]
Takahashi S, Katagiri T, Hirayama T, Yamaguchi-Shinozaki K, Shinozaki K. 2001. Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidopsis cell culture. Plant and Cell Physiology 42, 214–222.
Tamura T, Hara K, Yamaguchi Y, Koizumi N, Sano H. 2003. Osmotic stress tolerance of transgenic tobacco expressing a gene encoding a membrane-located receptor-like protein from tobacco plants. Plant Physiology 131, 454–462.
Thomashow MF. 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571–599.[CrossRef][Web of Science][Medline]
Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T, Wang X, Shinozaki K, Paszkowski J. 2002. Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO Journal 21, 6483–6493.[CrossRef][Web of Science][Medline]
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid dependent signal transduction pathway under drought and high-salinity conditions. Proceedings of the National Academy of Sciences, USA 97, 11632–11637.
Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker EP, Nakamura T, Schroeder JI. 2000. The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiology 122, 1249–1259.
Urao T, Katagiri T, Mizoguchi T, Yamaguchi-Shinozaki K, Hayashida N, Shinozaki K. 1994. Two genes that encode Ca2+-dependent protein kinases are induced by drought and high-salt stress in Arabidopsis thaliana. Molecular and General Genetics 244, 331–340.
Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K. 1999. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. The Plant Cell 11, 1743–1754.
Wang X-Q, Ullah H, Jones A, Assmann S. 2001. G protein regulation of ion channels and abscisic acid signalling in Arabidopsis guard cells. Science 292, 2070–2072.
Wu Y, Kuzma J, Marechal E, Graeff R, Lee HC, Foster R, Chua N-H. 1997. Abscisic acid signalling through cyclic ADP-ribose in plants. Science 278, 2126–2130.
Xiong L, Ishitani M, Lee H, Zhu J-K. 2001a. The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. The Plant Cell 13, 2063–2083.
Xiong L, Lee B-H, Ishitani M, Lee H, Zhang C, Zhu J-K. 2001b. FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signalling in Arabidopsis. Genes and Development 15, 1971–1984.
Xiong L, Lee H, Ishitani M, Zhu J-K. 2002a. Regulation of osmotic stress responsive gene expression by LOS6/ABA1 locus in Arabidopsis. Journal of Biological Chemistry 277, 8588–8596.
Xiong L, Schumaker KS, Zhu J-K. 2002b. Cell signalling for cold, drought, and salt stresses. The Plant Cell 14, S165–S183.
Xiong L, Yang Y. 2003. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. The Plant Cell 15, 745–759.
Yamaguchi-Shinozaki K, Shinozaki K. 1994. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. The Plant Cell 6, 251–264.[Abstract]
Yuasa T, Ichimura K, Mizoguchi T, Shinozaki K. 2001. Oxidative stress activates ATMPK6, an Arabidopsis homologue of MAP kinase. Plant and Cell Physiology 42, 1012–1016.
Zhu J-K. 2002. Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.[CrossRef][Medline]
Zhu J-K. Liu J, Xiong L. 1998. Genetic analysis of salt tolerance in Arabidopsis thaliana: evidence of a critical role for potassium nutrition. The Plant Cell 10, 1181–1192.
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 A. Boyko, P. Kathiria, F. J. Zemp, Y. Yao, I. Pogribny, and I. Kovalchuk Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (Virus-induced plant genome instability) Nucleic Acids Res., March 12, 2007; 35(5): 1714 - 1725. [Abstract] [Full Text] [PDF]
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P.-C. Lin, S.-G. Hwang, A. Endo, M. Okamoto, T. Koshiba, and W.-H. Cheng Ectopic Expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis Promotes Seed Dormancy and Stress Tolerance Plant Physiology, February 1, 2007; 143(2): 745 - 758. [Abstract] [Full Text] [PDF]
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J. J. Burke Evaluation of Source Leaf Responses to Water-Deficit Stresses in Cotton Using a Novel Stress Bioassay Plant Physiology, January 1, 2007; 143(1): 108 - 121. [Abstract] [Full Text] [PDF]
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 W. R. Swindell The Association Among Gene Expression Responses to Nine Abiotic Stress Treatments in Arabidopsis thaliana Genetics, December 1, 2006; 174(4): 1811 - 1824. [Abstract] [Full Text] [PDF]
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 A. M. Burza, I. Pekala, J. Sikora, P. Siedlecki, P. Malagocki, M. Bucholc, L. Koper, P. Zielenkiewicz, M. Dadlez, and G. Dobrowolska Nicotiana tabacum Osmotic Stress-activated Kinase Is Regulated by Phosphorylation on Ser-154 and Ser-158 in the Kinase Activation Loop J. Biol. Chem., November 10, 2006; 281(45): 34299 - 34311. [Abstract] [Full Text] [PDF]
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 W. F. XU and W. M. SHI Expression Profiling of the 14-3-3 Gene Family in Response to Salt Stress and Potassium and Iron Deficiencies in Young Tomato (Solanum lycopersicum) Roots: Analysis by Real-time RT-PCR Ann. Bot., November 1, 2006; 98(5): 965 - 974. [Abstract] [Full Text] [PDF]
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A. Rosado, A. L. Schapire, R. A. Bressan, A. L. Harfouche, P. M. Hasegawa, V. Valpuesta, and M. A. Botella The Arabidopsis Tetratricopeptide Repeat-Containing Protein TTL1 Is Required for Osmotic Stress Responses and Abscisic Acid Sensitivity Plant Physiology, November 1, 2006; 142(3): 1113 - 1126. [Abstract] [Full Text] [PDF]
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J.-G. Chen, H. Ullah, B. Temple, J. Liang, J. Guo, J. M. Alonso, J. R. Ecker, and A. M. Jones RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis J. Exp. Bot., August 1, 2006; 57(11): 2697 - 2708. [Abstract] [Full Text] [PDF]
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A. Maggio, J.-K. Zhu, P. M. Hasegawa, and R. A. Bressan Osmogenetics: Aristotle to Arabidopsis PLANT CELL, July 1, 2006; 18(7): 1542 - 1557. [Full Text] [PDF]
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G. W. Owttrim RNA helicases and abiotic stress Nucleic Acids Res., June 21, 2006; 34(11): 3220 - 3230. [Abstract] [Full Text] [PDF]
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S. Ma, Q. Gong, and H. J. Bohnert Dissecting salt stress pathways J. Exp. Bot., March 1, 2006; 57(5): 1097 - 1107. [Abstract] [Full Text] [PDF]
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 Y. Zhang, M. A. R. Mian, and J. H. Bouton Recent Molecular and Genomic Studies on Stress Tolerance of Forage and Turf Grasses Crop Sci., February 1, 2006; 46(2): 497 - 511. [Abstract] [Full Text] [PDF]
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A. D'ARCY-LAMETA, R. FERRARI-ILIOU, D. CONTOUR-ANSEL, A.-T. PHAM-THI, and Y. ZUILY-FODIL Isolation and Characterization of Four Ascorbate Peroxidase cDNAs Responsive to Water Deficit in Cowpea Leaves Ann. Bot., January 1, 2006; 97(1): 133 - 140. [Abstract] [Full Text] [PDF]
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E. A. Ottow, M. Brinker, T. Teichmann, E. Fritz, W. Kaiser, M. Brosche, J. Kangasjarvi, X. Jiang, and A. Polle Populus euphratica Displays Apoplastic Sodium Accumulation, Osmotic Adjustment by Decreases in Calcium and Soluble Carbohydrates, and Develops Leaf Succulence under Salt Stress Plant Physiology, December 1, 2005; 139(4): 1762 - 1772. [Abstract] [Full Text] [PDF]
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C. He, J. Yan, G. Shen, L. Fu, A. S. Holaday, D. Auld, E. Blumwald, and H. Zhang Expression of an Arabidopsis Vacuolar Sodium/Proton Antiporter Gene in Cotton Improves Photosynthetic Performance Under Salt Conditions and Increases Fiber Yield in the Field Plant Cell Physiol., November 1, 2005; 46(11): 1848 - 1854. [Abstract] [Full Text] [PDF]
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Z. Xin, Y. Zhao, and Z.-L. Zheng Transcriptome Analysis Reveals Specific Modulation of Abscisic Acid Signaling by ROP10 Small GTPase in Arabidopsis Plant Physiology, November 1, 2005; 139(3): 1350 - 1365. [Abstract] [Full Text] [PDF]
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M. Boudsocq and C. Lauriere Osmotic Signaling in Plants. Multiple Pathways Mediated by Emerging Kinase Families Plant Physiology, July 1, 2005; 138(3): 1185 - 1194. [Full Text] [PDF]
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 V. Levchenko, K. R. Konrad, P. Dietrich, M. R. G. Roelfsema, and R. Hedrich Cytosolic abscisic acid activates guard cell anion channels without preceding Ca2+ signals PNAS, March 15, 2005; 102(11): 4203 - 4208. [Abstract] [Full Text] [PDF]
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 I. Kameshita, T. Nishida, S. Nakamura, Y. Sugiyama, N. Sueyoshi, Y. Umehara, M. Nomura, and S. Tajima Expression Cloning of a Variety of Novel Protein Kinases in Lotus japonicus J. Biochem., January 1, 2005; 137(1): 33 - 39. [Abstract] [Full Text] [PDF]
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A. Kelner, I. Pekala, S. Kaczanowski, G. Muszynska, D. G. Hardie, and G. Dobrowolska Biochemical Characterization of the Tobacco 42-kD Protein Kinase Activated by Osmotic Stress Plant Physiology, October 1, 2004; 136(2): 3255 - 3265. [Abstract] [Full Text] [PDF]
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T. J. Panikulangara, G. Eggers-Schumacher, M. Wunderlich, H. Stransky, and F. Schoffl Galactinol synthase1. A Novel Heat Shock Factor Target Gene Responsible for Heat-Induced Synthesis of Raffinose Family Oligosaccharides in Arabidopsis Plant Physiology, October 1, 2004; 136(2): 3148 - 3158. [Abstract] [Full Text] [PDF]
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