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Regulation of ion homeostasis under salt stress
Jian-Kang Zhu
When under salt stress, plants maintain a high concentration of K and a low concentration of Na in the cytosol. They do this by regulating the expression and activity of K and Na transporters and of H pumps that generate the driving force for transport. Although salt-stress sensors remain elusive, some of the intermediary signaling components have been identied. Evidence suggests that a protein kinase complex consisting of the myristoylated calcium-binding protein SOS3 and the serine/ threonine protein kinase SOS2 is activated by a salt-stresselicited calcium signal. The protein kinase complex then phosphorylates and activates various ion transporters, such as the plasma membrane Na/H antiporter SOS1.
Addresses Department of Plant Sciences, University of Arizona, Tucson, Arizona 85721, USA e-mail: jkzhu@ag.arizona.edu

Current Opinion in Plant Biology 2003, 6:441–445 This review comes from a themed issue on Cell signalling and gene regulation Edited by Kazuo Shinozaki and Elizabeth Dennis 1369-5266/$ – see front matter 2003 Elsevier Ltd. All rights reserved. DOI 10.1016/S1369-5266(03)00085-2

case for understanding the general regulation of ion homeostasis in plant cells. In addition, understanding how plants cope with excessive Na in the environment is of great agricultural importance as soil salinity accounts for large yield losses in crops worldwide. Na stress disrupts K uptake by root cells [1]. When Na enters cells and accumulates to high levels, it becomes toxic to enzymes [1]. To prevent growth cessation or cell death, excessive Na has to be extruded or compartmentalized in the vacuole [1]. Unlike animal cells, plant cells do not have Na-ATPases or Na/K-ATPases, and they rely on H-ATPases and H-pyrophosphatases to create a proton-motive force that drives the transport of all other ions and metabolites [1]. Many of the transporters of H, K and Na have now been identied. The regulatory mechanisms that control the expression and activity of the transporters are beginning to be elucidated. This review focuses on recent progress in understanding the cellular transduction of the salt-stress signal to regulate Na transport in plants.

Sensing salt stress
Presumably, both hyperosmolarity and ion-specic signals of salt stress are sensed by plant cells. Although ionspecic signals are probably more important than hyperosmolarity in the regulation of Na transport, osmotic stress also plays a role (Figure 1). Osmotic stress activates the synthesis of abscisic acid (ABA), which can upregulate the transcription of AtNHX1, the gene encoding the vacuolar Na/H exchanger [2]. Osmotic stress may be sensed in part by stretch-activated channels and by transmembrane protein kinases, such as twocomponent histidine kinases [3] and wall-associated kinases [4]. At present, genetic evidence to support the role of any of these proteins in plant osmotic-stress responses is lacking. Little is known about how Na is sensed in any cellular system. Theoretically, Na can be sensed either before or after entering the cell, or both. Extracellular Na may be sensed by a membrane receptor, whereas intracellular Na may be sensed either by membrane proteins or by any of the many Na-sensitive enzymes in the cytoplasm. The plasma-membrane Na/H antiporter SOS1 (SALT OVERLY SENSITIVE1) is a possible Na sensor [5]. The SOS1 protein has 10–12 transmembrane domains and a long tail (of more than 700 amino acids) that is predicted to reside in the cytoplasm [5]. SOS1 has Na/ H exchanger activity, and this transport activity is essential for Na efux from Arabidopsis cells [6,7]. However, the unusually long cytoplasmic tail of SOS1 suggests that this protein may not only transport Na but
Current Opinion in Plant Biology 2003, 6:441–445

Abbreviations ABA abscisic acid abi1 ABA-insensitive1 HKT high afnity K transporter NHX Na/H exchanger Snf3 Sucrose non-fermenting3 SOS1 SALT OVERLY SENSITIVE1

Introduction
The homeostasis of intracellular ion concentrations is fundamental to the physiology of living cells. Proper regulation of ion ux is necessary for cells to keep the concentrations of toxic ions low and to accumulate essential ions. Plant cells employ primary active transport, mediated by H-ATPases, and secondary transport, mediated by channels and co-transporters, to maintain characteristically high concentrations of K and low concentrations of Na in the cytosol. Intracellular K and Na homeostasis is important for the activities of many cytosolic enzymes, and for maintaining membrane potential and an appropriate osmoticum for cell volume regulation. Under salt stress, the maintenance of K and Na homeostasis becomes even more crucial. Thus, the regulation of ion transport by salt-stress signaling provides a model
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442 Cell signalling and gene regulation

Figure 1

Salt stress Hyperosmolarity Na+ ABA

AKT1 K+

Sensor

Receptor ABI1

SOS3

Ca2+

Na+ AtNHX1 H+

Vacuole

Na+

SOS2 H+ Na+ SOS1
Current Opinion in Plant Biology

AtHKT1

Signaling pathways that regulate the expression and activities of ion transporters to maintain a low cytoplasmic concentration of Na under salt stress. Excessive Na and hyperosmolarity are each perceived by unknown sensors. The Ca2-responsive SOS3–SOS2 protein kinase pathway mediates Na regulation of the expression and activities of Na transporters. Hyperosmolarity is proposed to induce the synthesis of ABA, which in turn upregulates the transcription of AtNHX1 and other ion-transporter genes. The potential negative regulation of AtHKT1 by SOS3–SOS2 and of AKT1 by intracellular Na is also indicated by broken lines ending in t-bars.

also sense this ion. Several transporters with long cytoplasmic tails or loops have been demonstrated to be sensors. For example, the glucose transporters Snf3 (Sucrose non-fermenting 3) and Rgt2 (Regulator of glucose transporter 2) in yeast function as low- and highglucose sensors, respectively [8]. Although the yeast proteins Snf3 and Rgt2 do not have a signicant glucosetransport activity [8], studies of other proteins have demonstrated that sensing and transport are not mutually exclusive functions. For instance, the sugar permease BglF in Escherichia coli has a dual role in sensing and transporting b-glucosides [9]. The yeast ammonium transporter Mep2p also functions in both sensing ammonium and transporting it into cells, initiating nutritional signals that regulate lamentous growth [10,11]. It is conceivable, therefore, that SOS1 may be both a transporter and a sensor of Na.

unknown. Na currents that are mediated by non-selective cation channels are partially sensitive to calcium, and this correlates with the inhibition of Na entry into roots by calcium [16]. It is unclear whether calcium's regulation of the activity of non-selective cation channels is direct or indirect via intracellular regulatory proteins. The Arabidopsis AtHKT1 protein mediates Na inux when expressed in heterologous systems such as Xenopus oocytes and yeast [17]. A screen for suppressor mutations of the salt-hypersensitive Arabidopsis mutant sos3 identied mutant alleles of AtHKT1 [12]. athkt1 suppression of sos3 is due to reduced Na accumulation. In wheat, the K–Na co-transporter HKT1 also functions in Na inux under salt stress [18]. It is possible that in wildtype cells the Na-inux activity of AtHKT1 is negatively regulated by SOS3 (a calcium-binding protein) and by other components of the SOS regulatory pathway (Figure 1). Alternatively, the SOS pathway may not regulate AtHKT1 and the suppressive effect of athkt1 may be due simply to reduced Na entry. An intriguing question is why Na-inux transporters such as AtHKT1 have been maintained during evolution, given the toxic effect of intracellular Na. athkt1 mutants do not have obvious growth or developmental defects. They are more tolerant of Na stress than wildtype plants when grown in culture media but are more sensitive when grown in soil. The essential role of AtHKT1 in saline soil is likely explained by its potential involvement in long-distance Na transport between the root and the shoot [13].
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NaR entry
The enormous negative membrane potential across the plasma membrane of plant cells favors the passive transport of Na into cells. Na enters plant cells through the high-afnity K transporter HKT1 [12,13] and through non-selective cation channels [14]. Additionally, in some plant species such as rice, Na leakage into the transpiration stream via the apoplast can account for a major part of Na entry into plants [15]. Na uptake through the apoplastic pathway is affected by root development and silica deposition in the cell wall. The precise molecular identities of non-selective cation channels are still
Current Opinion in Plant Biology 2003, 6:441–445

Regulation of ion homeostasis under salt stress Zhu 443

The role of cellular efux of Na is not intuitive in multicellular plants, as Na transported out of one cell would present a problem for neighboring cells. So the role of Na efux has to be considered in specic tissues and in the context of whole plants. In Arabidopsis, Na efux is catalyzed by the plasma-membrane Na/H antiporter encoded by the SOS1 gene [5,6,7,19]. SOS1 activity is detected in salt stressed but not in unstressed plants [6]. It is an electroneutral Na/H exchanger that is specic for Na and cannot transport Li or K [6,20]. Activity of the SOS1 promoter is detected ubiquitously in virtually all tissues, but its greatest activity is found in root epidermal cells (particularly in epidermal cells at the root tip) and in cells bordering the vascular tissue throughout the plant [19]. This SOS1 expression pattern, together with the results of ion analysis in sos1 mutant plants, suggests that SOS1 has several roles. First, Na efux into the root medium; second, buying time for Na storage in the vacuole by slowing down Na accumulation in the cytoplasm; and third controlling long-distance Na transport between roots and leaves by loading Na into and unloading Na from the xylem and phloem. SOS1's role in longdistance transport is important for coordination between transpirational Na ow and the vacuolar sequestration of Na in leaves. Increased expression of SOS1 results in improved salt tolerance in transgenic Arabidopsis [21]. The transcript level of SOS1 is upregulated by salt stress [5]. This upregulation appears to be at the posttranscriptional level, as SOS1 promoter activity is not upregulated by salt stress but SOS1 expression driven by the constitutive Cauliower mosaic virus 35S promoter is [21]. The salt-stress upregulation of SOS1 is partly under the control of SOS2 and SOS3 [5]. Plasma-membrane H-ATPases generate the driving force for Na transport by SOS1. Disruption of the root-endodermis-specic plasma-membrane H-ATPase, AHA4, in mutant Arabidopsis plants causes increased salt sensitivity [22]. The transcript levels of some H-ATPases have been shown to increase in response to salt stress [23]. Overexpression of the Arabidopsis H-pyrophosphatase, AVP1, was shown to improve salt as well as drought tolerance [24]. Whether SOS3 and SOS2 are involved in this regulation is not known. Activation of the Na/H antiport activity of SOS1 by salt stress is controlled by SOS3 and SOS2 ([6,7]; Figure 1). SOS3 is a myristoylated calcium-binding protein that is capable of sensing the cytosolic calcium signal elicited by salt stress [25,26]. SOS2 is a serine/threonine protein kinase that has a unique carboxy-terminal regulatory domain and an amino-terminal catalytic domain similar to that of the yeast protein SNF1 and animal AMP-activated kinase (AMPK) [27]. The amino-terminal kinase catalytic domain of SOS2 interacts with the carboxy-terminal regulatory domain [28]. The carboxy-terminal regulatory domain of SOS2 also interacts with SOS3,
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NaR efux

and this interaction is mediated by a 21-amino-acid sequence, the FISL motif [28]. In the presence of calcium, SOS3 activates the substrate phosphorylation activity of SOS2 [29]. The FISL motif is autoinhibitory and its deletion results in constitutive activation of SOS2 [6,28]. Constitutive activation of SOS2 can also be achieved by introducing mutations into the kinase activation loop [28,30]. These mutations substitute Ser-156, Thr-168 or Tyr-175 with the acidic Asp to mimic phosphorylated residues [30]. The data suggest that in vivo SOS2 may be activated by phosphorylation in the activation loop by an upstream protein kinase. In sos3 or sos2 mutant plants, SOS1 activity cannot be induced by salt stress [6]. In-vitro addition of constitutively active SOS2 recombinant protein to plasmamembrane vesicles that were isolated from sos2 or sos3 mutant plants restores SOS1 activity to near the wildtype level [6]. The activation of SOS1 by SOS3 and SOS2 has also been demonstrated in yeast, in which co-expression of the three genes could restore salt tolerance to a mutant that was defective in all endogenous Na transporters [7]. Yeast cells with the reconstituted SOS pathway were used to show that SOS1 could be phosphorylated by the SOS3–SOS2 protein kinase complex [7]. Vacuolar sequestration of Na not only lowers Na concentration in the cytoplasm but also contributes to osmotic adjustment to maintain water uptake from saline solutions. Other organelles, such as plastids and mitochondria, may also accumulate some Na and thus contribute to the overall subcellular compartmentation of Na. In Arabidopsis, the AtNHX family of Na/H antiporters function in Na compartmentation [31]. AtNHX1 and AtNHX2 are localized in the tonoplast membrane, and their transcript levels are upregulated by ABA or osmotic stress [32]. The transcript levels of vacuolar HATPase components also increase in response to salt stress [33]. Overexpression of AtNHX1 in various plants [34], of an Atriplex homolog of AtNHX1 in rice [35] or of the vacuolar H-pyrophosphatase in Arabidopsis [36] was reported to enhance plant salt tolerance substantially. Salt-stress regulation of AtNHX1 expression is not impaired in the Arabidopsis sos1, sos2 or sos3 mutants. However, mutations that cause ABA deciency or the ABA-insensitive1 (abi1) (but not the abi2) mutation partially disrupt AtNHX1 upregulation by salt stress [2,32]. This suggests that an SOS-independent, ABA-dependent pathway regulates the expression of the vacuolar antiporter in response to salt stress (Figure 1). However, the SOS pathway appears to regulate the activity of vacuolar Na/H antiporters [37].

NaR compartmentation

KR homeostasis

A high cytosolic K/Na ratio is important for maintaining cellular metabolism. Under salt stress, Na competes
Current Opinion in Plant Biology 2003, 6:441–445

444 Cell signalling and gene regulation

with K for uptake into roots. The transcript levels of several K transporter genes are either down- or upregulated by salt stress, probably reecting the different capacities of plants to maintain K uptake under salt stress. Salt stress increases the transcript level of the Arabidopsis root K-transporter gene AtKC1 [38]. In the common ice plant, salt stress upregulates the expression of KMT1 (a AKT/KAT family member) and various HAK/ KUP (high afnity K transporter/K uptake transporter)-type genes, whereas it downregulates the expression of MKT1 (another AKT/KAT family member) [39,40]. The signicance of this transcript-level regulation is difcult to determine because the transport characteristics and in-vivo roles of the transporters are unclear. At the activity level, K channels are regulated by protein kinases [41] and phosphatases [42]. Whether salt stress regulates the activities of K-uptake transporters through these or other protein kinases or phosphatases remains to be determined. A particularly novel mode of activity regulation has been found for two HKT1 homologs from Eucalyptus camaldulensis [43]. These Na–K co-transporters display intrinsic osmosensing capabilities when expressed in Xenopus oocytes. Their Na- and K-transport activities are enhanced by a downshift in extracellular osmolarity. The Arabidopsis sos mutants have a growth defect under K-limiting conditions [44]. Athkt1 mutations suppress not only the salt-hypersensitivity but also the K-acquisition defect of the sos3 mutant [12]. The involvement of the SOS pathway could be indirect. A defect in Na efux in the sos mutant may lead to excessive cytoplasmic Na that is inhibitory to K-uptake transporters such as AKT1 (E Spalding, personal communication; Figure 1). Under K-limiting conditions, inhibitory levels of cytoplasmic Na may arise in the sos mutants, even when grown in media that is not supplemented with extra NaCl.

Acknowledgements
Work in my laboratory has been supported by grants from US Department of Agriculture's National Research Initiative, by the National Science Foundation and by the National Institute of Health.

References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest 1. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ: Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 2000, 51:463-499. Shi H, Zhu JK: Regulation of expression of the vacuolar NaR/HR antiporter gene AtNHX1 by salt stress and ABA. Plant Mol Biol 2002, 50:543-550. Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K: A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 1999, 11:1743-1754. Kohorn BD: WAKs: cell wall associated kinases. Curr Opin Cell Biol 2001, 13:529-533. Shi H, Ishitani M, Kim C, Zhu JK: The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative NaR/HR antiporter. Proc Natl Acad Sci USA 2000, 97:6896-6901.

2.

3.

4. 5.

Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK: Regulation of SOS1, a plasma membrane NaR/HR exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 2002, 99:8436-8441. The authors assayed Na/H exchange activity in plasma-membrane vesicles from wildtype Arabidopsis plants and from sos1, sos2 and sos3 Arabidopsis mutants. The results demonstrate that SOS1 is a plasma membrane Na/H antiporter, and that its activity depends on the SOS3– SOS2 protein kinase complex. Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM: Reconstitution in yeast of the Arabidopsis SOS signaling pathway for NaR homeostasis. Proc Natl Acad Sci USA 2002, 99:9061-9066. The rst time that a plant signaling pathway has been functionally reconstituted in yeast. This work shows that SOS1 is phosphorylated by the SOS3–SOS2 protein kinase complex, and that its transport activity requires its activation by SOS3 and SOS2. The authors also show that myristoylated SOS3 recruits SOS2 to the plasma membrane. 8. ¨ Ozcan S, Dover J, Johnston M: Glucose sensing and signaling by two glucose receptors in the yeast. EMBO J 1998, 17:2566-2573. Chen Q, Arents JC, Bader R, Postma PW, Amster-Choder O: BglF, the sensor of the E. coli bgl system, uses the same site to phosphorylate both a sugar and a regulatory protein. EMBO J 1997, 16:4617-4627. 7.

6.

Conclusions
Many of the transporters for H , K and Na have been identied from various plant species. It is clear that salt stress regulates the expression level as well as the activities of some of these transporters. Evidence suggests that the SOS pathway plays a central role in coordinating the activities of several of the transport systems (Figure 1). Future efforts should be directed towards discovering the elusive salt-stress sensors and identifying additional signaling components that mediate the salt-stress regulation of the expression and activities of ion transporters.


9.

10. Marini AM, Soussi-Boudekou S, Vissers S, Andre B: A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 1997, 17:4282-4293. 11. Lorenz MC, Heitman J: The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J 1998, 17:1236-1247. 12. Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM: AtHKT1 is a salt tolerance determinant that controls NaR entry into plant roots. Proc Natl Acad Sci USA 2001, 98:14150-14155. 13. Maser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami M, Yamaguchi K, Nishimura M, Uozumi N et al.: Altered shoot/root NaR distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the NaR transporter AtHKT1. FEBS Lett 2002, 531:157-161. The authors show that the Na inux carrier AtHKT1 has a necessary role in plant salt tolerance. Such a function probably involves a role for the transporter in the long-distance transport of Na from root to shoot. 14. Amtmann A, Sanders D: Mechanisms of NaR uptake by plant cells. Adv Bot Res 1999, 29:75-112. www.current-opinion.com

Update
Berthomieu et al. [45] have recently shown that Arabidopsis sas2 mutations, which cause overaccumulation of Na in the shoot, are allelic to AtHKT. On the basis of AtHKT's strong expression in phloem tissues, they propose that AtHKT1 is involved in Na recirculation from shoots to roots.
Current Opinion in Plant Biology 2003, 6:441–445

Regulation of ion homeostasis under salt stress Zhu 445

15. Yeo AR, Flowers SA, Rao G, Welfare K, Senanayake N, Flowers TJ: Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass ow. Plant Cell Environ 1999, 22:559-565. 16. Tester M, Davenport R: NaR tolerance and NaR transport in higher plants. Ann Bot (Lond) 2003, 91:503-527. A valuable comprehensive review of salt tolerance mechanisms in plants. 17. Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker EP, Nakamura T, Schroeder JI: The Arabidopsis HKT1 gene homolog mediates inward NaR currents in Xenopus laevis oocytes and NaR uptake in Saccharomyces cerevisiae. Plant Physiol 2000, 122:1249-1259. 18. Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA: A role for HKT1 in sodium uptake by wheat roots. Plant J 2002, 32:139-149. Using an antisense approach, the authors show that reducing the expression of the wheat HKT1 gene decreases Na accumulation and increases salt tolerance. The data support a role for HKT1 in Na inux in wheat roots. 19. Shi H, Quintero FJ, Pardo JM, Zhu JK: The putative plasma membrane NaR/HR antiporter SOS1 controls long-distance NaR transport in plants. Plant Cell 2002, 14:465-477. The authors found strong expression of SOS1 in epidermal cells surrounding the root tip and in parenchyma cells bordering the xylem and phloem. On the basis of this expression pattern and of ion analysis in the sos1 mutant, the authors propose roles for SOS1 in the long-distance transport of Na as well as in expelling Na to the soil medium. 20. Qiu QS, Barkla BJ, Vera-Estrella R, Zhu JK, Schumaker KS: NaR/HR exchange activity in the plasma membrane of Arabidopsis thaliana. Plant Physiol 2003, 132:1041-1052. 21. Shi H, Lee BH, Wu SJ, Zhu JK: Overexpression of a plasma membrane NaR/HR antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 2003, 21:81-85. 22. Vitart V, Baxter I, Doerner P, Harper JF: Evidence for a role in growth and salt resistance of a plasma membrane HR-ATPase in the root endodermis. Plant J 2001, 27:191-201. 23. Niu X, Zhu JK, Narasimham ML, Bressan RA, Hasegawa PM: Plasma membrane HR-ATPase gene expression is regulated by NaCl in halophyte (Atriplex nummularia L.) cell cultures. Planta 1993, 190:433-438. 24. Gaxiola RA, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR: Drought- and salt-tolerant plants result from overexpression of the AVP1 HR-pump. Proc Natl Acad Sci USA 2001, 98:11444-11449. 25. Liu J, Zhu JK: A calcium sensor homolog required for plant salt tolerance. Science 1998, 280:1943-1945. 26. Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK: SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 2000, 12:1667-1677. 27. Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK: The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 2000, 97:3730-3734. 28. Guo Y, Halfter U, Ishitani M, Zhu JK: Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 2001, 13:1383-1400. 29. Halfter U, Ishitani M, Zhu JK: The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calciumbinding protein SOS3. Proc Natl Acad Sci USA 2000, 97:3735-3740.

30. Gong D, Guo Y, Jagendorf AT, Zhu JK: Biochemical characterization of the Arabidopsis protein kinase SOS2 that functions in salt tolerance. Plant Physiol 2002, 130:256-264. 31. Blumwald E: Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 2000, 12:431-434. 32. Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM: Differential expression and function of Arabidopsis thaliana NHX NaR/HR antiporters in the salt stress response. Plant J 2002, 30:529-539. 33. Dietz KJ, Tavakoli N, Kluge C, Mimura T, Sharma SS, Harris GC, Chardonnens AN, Golldack D: Signicance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot 2001, 52:1969-1980. 34. Apse MP, Blumwald E: Engineering salt tolerance in plants. Curr Opin Biotechnol 2002, 13:146-150. A review of transgenic approaches to improving salt tolerance in plants, most notably by enhanced expression of Na and H transporters. 35. Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T: Introduction of a NaR/HR antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett 2002, 532:279-282. 36. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR: Drought- and salt-tolerant plants result from overexpression of the AVP1 HR-pump. Proc Natl Acad Sci USA 2001, 98:11444-11449. 37. Qiu Q, Schumaker KS, Zhu JK: Regulation of vacuolar membrane NaR/HR exchange activity in Arabidopsis thaliana by the SOS pathway. Abstract 200, Plant Biology 2002, 3–7 August 2002, Denver, Colorado, USA. 38. Pilot G, Gaymard F, Mouline K, Cherel I, Sentenac H: Regulated expression of Arabidopsis shaker KR channel genes involved in KR uptake and distribution in the plant. Plant Mol Biol 2003, 51:773-787. 39. Su H, Golldack D, Katsuhara M, Zhao C, Bohnert HJ: Expression and stress-dependent induction of potassium channel transcripts in the common ice plant. Plant Physiol 2001, 125:604-614. 40. Su H, Golldack D, Zhao C, Bohnert HJ: The expression of HAK-type K(R) transporters is regulated in response to salinity stress in common ice plant. Plant Physiol 2002, 129:1482-1493. 41. Li J, Lee YRJ, Assmann SM: Guard cells possess a calciumdependent protein kinase that phosphorylates the KAT1 potassium channel. Plant Physiol 1998, 116:785-795. 42. Cherel I, Michard E, Platet N, Mouline K, Alcon C, Sentenac H, Thibaud JB: Physical and functional interaction of the Arabidopsis KR channel AKT2 and phosphatase AtPP2CA. Plant Cell 2002, 14:1133-1146. 43. Liu W, Fairbairn DJ, Reid RJ, Schachtman DP: Characterization of two HKT1 homologues from Eucalyptus camaldulensis that display intrinsic osmosensing capability. Plant Physiol 2001, 127:283-294. 44. Zhu JK, Liu J, Xiong L: Genetic analysis of salt tolerance in Arabidopsis thaliana: evidence of a critical role for potassium nutrition. Plant Cell 1998, 10:1181-1192. 45. Berthomieu P, Conejero G, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oiki S, Yamada K, Cellier F, Gosti F et al.: Functional analysis of AtHKT1 in Arabidopsis shows that NaR recirculation by the phloem is crucial for salt tolerance. EMBO J 2003, 22:2004-2014.

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Current Opinion in Plant Biology 2003, 6:441–445

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