JIPB

Journal of Integrative Plant Biology

Transport, signaling, and homeostasis of potassium and sodium in plants Eri Adams and Ryoung Shin* RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa 230‐0045, Japan

Abstract Potassium (Kþ) is an essential macronutrient in plants and a lack of Kþ significantly reduces the potential for plant growth and development. By contrast, sodium (Naþ), while beneficial to some extent, at high concentrations it disturbs and inhibits various physiological processes and plant growth. Due to their chemical similarities, some functions of Kþ can be undertaken by Naþ but Kþ homeostasis is severely

INTRODUCTION

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(ATK1) (Sentenac et al. 1992; Daram et al. 1997; Ros et al. 1999; Urbach et al. 2000). KT/KUP/HAKs are also known to function as high‐affinity and/or low‐affinity Hþ/Kþ symporters (Santa‐ Maria et al. 1997; Ahn et al. 2004; Qi et al. 2008; Kobayashi et al. 2010; Haro et al. 2013). The Arabidopsis outward‐rectifying Kþ channel, STELAR Kþ OUTWARD RECTIFIER (SKOR), has been indicated to play a major role in xylem loading (Gaymard et al. 1998; Harada and Leigh 2006). Tonoplast‐localized tandem‐pore Kþ (TPK)‐type (KCO‐type) channels have been demonstrated as being involved in Kþ retrieval from the vacuole (Czempinski et al. 1997, 2002; Becker et al. 2004; Bihler et al. 2005; Voelker et al. 2006, 2010; Hamamoto et al. 2008). Stomatal movement is also known to be regulated by Kþ channels such as Kþ CHANNEL IN ARABIDOPSIS THALIANA1 (KAT1) (Anderson et al. 1992a; Schachtman et al. 1992; Ache et al. 2000; Schroeder et al. 2001; Ivashikina et al. 2005; Lebaudy et al. 2010). On the other hand, several cation channels, including HIGH‐AFFINITY Kþ TRANSPORTERs (HKTs), non‐selective cation channels (NSCCs), and a low‐affinity cation transporter (LCT1), are reported to be involved in Naþ uptake from the soil, whereas other channels, including NAþ/Hþ EXCHANGERs (NHXs) and an Naþ/Hþ antiporter, SALT OVERLY SENSITIVE1 (SOS1), are suggested to function in salt tolerance and Naþ homeostasis in plants (Barkla et al. 1994; Schachtman et al. 1997; Berthomieu et al. 2003; Apse and Blumwald 2007; Liu et al. 2010; Bassil et al. 2011a, 2011b; Baluska and Mancuso 2013). In Kþ‐deficiency signaling, reactive oxygen species (ROS), calcium (Ca2þ), and phytohormones have been reported as March 2014 | Volume 56 | Issue 3 | 231–249

Free Access

Potassium (Kþ) is the most abundant essential cation in almost all organisms and it plays a pivotal role in the fundamental physiological processes in plants (Hastings and Gutknecht 1978; Maathuis and Amtmann 1999; Very and Sentenac 2003; Amtmann et al. 2006). Cytosolic Kþ concentrations are sustained at approximately 100 mmol/L in the plant cell whereas vacuolar Kþ concentrations are variable depending on the external Kþ concentrations (Rodriguez‐Navarro 2000). Sodium (Naþ) is a beneficial element in plants and low levels of Naþ are essential for some plants such as C4 species. By contrast, high concentrations of cytosolic Naþ are toxic to plants. The tolerable cytosolic Naþ concentrations in plants are thought to be 10–30 mmol/L (Carden et al. 2003; Corratge‐ Faillie et al. 2010). Sodium is known to be capable of replacing part of the Kþ functions in plants such as osmotic adjustment, membrane potential regulation, cell growth, enzyme activity, and protein synthesis. However, the major role of Naþ is considered to be regulation of turgor pressure and cell expansion (Maser et al. 2002a; Rodriguez‐Navarro and Rubio 2006; Haro et al. 2010; Kronzucker and Britto 2011; Kronzucker et al. 2013). Potassium is either actively or passively transported from the soil to the plant cell (Maathuis and Sanders 1992, 1994; Very and Sentenac 2003; Harada and Leigh 2006). Although not much is known about active Kþ transport, passive Kþ transport has been shown to be mediated by inward‐rectifying voltage‐ gated Kþ channels such as ARABIDOPSIS Kþ TRANSPORTER1

Keywords: Homeostasis; potassium; signaling; sodium; transport Citation: Adams E, Shin R (2014) Transport, signaling, and homeostasis of potassium and sodium in plants. J Integr Plant Biol 56: 231–249. doi: 10.1111/jipb.12159 Edited by: Leon V. Kochian, Cornell University, USA Received Oct. 29, 2013; Accepted Dec. 31, 2013 Available online on Jan. 7, 2014 at www.wileyonlinelibrary.com/ journal/jipb © 2014 Institute of Botany, Chinese Academy of Sciences

Invited Expert Review

Ryoung Shin *Correspondence: [email protected]

affected by salt stress, on the other hand. Recent advances have highlighted the fascinating regulatory mechanisms of Kþ and Naþ transport and signaling in plants. This review summarizes three major topics: (i) the transport mechanisms of Kþ and Naþ from the soil to the shoot and to the cellular compartments; (ii) the mechanisms through which plants sense and respond to Kþ and Naþ availability; and (iii) the components involved in maintenance of Kþ/Naþ homeostasis in plants under salt stress.

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regulatory signals (Shin and Schachtman 2004; Amtmann et al. 2006; Amtmann and Armengaud 2007; Schachtman and Shin 2007; Wang and Wu 2010, 2013; Shin 2011). These signals are also known to play a role when a plant responds to salinity (Blumwald 2000; Munns and Tester 2008). Maintenance of intracellular Kþ/Naþ homeostasis is a crucial mechanism for plant growth and development, which is presumably tightly regulated through these signaling mechanisms (Walker et al. 1996a; Kim et al. 2007; Bassil et al. 2012; Jiang et al. 2013). This review offers an overview of the latest knowledge on Kþ and Naþ transport, sensing, and signaling. In addition, the components involved in the regulation of Kþ and Naþ homeostasis are discussed.

POTASSIUM SENSING AND TRANSPORT IN PLANTS Plants operate various Kþ transport mechanisms upon sensing Kþ availability. These Kþ sensing mechanisms in plants still remain largely unknown. Transport of exogenous Kþ through the plasma membrane into, and its allocation within the plant are mediated by diverse Kþ channels and transporters. Although the mechanism of Kþ transport mediated by Shaker‐type channels has been intensively investigated using electrophysiological approaches and heterologous expression systems, knowledge of the KT/KUP/HAK transporters is still limited (Schachtman et al. 1989; Maathuis and Sanders 1992, 1994; Schachtman and Schroeder 1994; Amtmann et al. 2006; Schachtman and Shin 2007; Wang and Wu 2013). Potassium transport by membrane transporters is comprised of the following processes: uptake into the root, movement out/into the xylem/phloem, and cellular compartmentalization. Most of the current knowledge on these processes in plants has been obtained from studies using Arabidopsis thaliana as the model. In this section, the mechanisms in which plants sense Kþ, transport it from the soil to the shoot and respond to it are discussed focusing on recent progress in Arabidopsis. Kþ sensing The Kþ sensing process is a key step for the regulation of Kþ homeostasis. However, sensors for Kþ in plants have not yet been identified. In bacteria, a P‐type ATPase, Kþ‐dependent growth (Kdp) serves as a Kþ entry point as well as a sensor but its homolog in plants has not been reported (Polarek et al. 1988, 1992). The most promising candidate for a Kþ sensor would be AKT1, a Shaker‐type inward‐rectifying Kþ channel. The akt1‐1 mutant has a clear phenotype in Kþ‐ starved conditions and the AKT1‐mediated Kþ influx and the resultant cytosolic Kþ concentrations are influenced by external Kþ concentrations (Gierth and Maser 2007). Because AKT1 is known to be regulated by the CALCINEURIN B‐LIKE PROTEINs (CBLs)‐CBL‐INTERACTING PROTEIN KINASE23 (CIPK23) complexes (Wang and Wu 2013), post‐translational regulation may be involved in Kþ sensing by AKT1, although more evidence is required to prove AKT1 as being a Kþ sensor. Some other channels, such as HIGH‐AFFINITY Kþ TRANSPORTER5 (HAK5), GUARD CELL OUTWARDLY‐RECTIFYING Kþ CHANNEL (GORK), and Kþ UPTAKE PERMEASE4 (KUP4), have also been suggested as Kþ sensors but none of their sensory March 2014 | Volume 56 | Issue 3 | 231–249

activities have been confirmed in plants (Grabov 2007) (Figure 1A). Kþ influx at the soil‐plant interface In Arabidopsis, AKT1 and a KT/KUP/HAK‐type transporter, HAK5, both of whose expression is mainly observed in roots, are considered to function dominantly in Kþ uptake from the soil (Walker et al. 1996b; Hirsch et al. 1998; Ahn et al. 2004; Gierth et al. 2005; Wang and Wu 2013). ATK1 mediates ammonium (NH4þ)‐insensitive Kþ transport (Hirsch et al. 1998; Spalding et al. 1999; Qi et al. 2008), in contrast to HAK5 (Hirsch et al. 1998; Spalding et al. 1999; Qi et al. 2008). It has been shown that AKT1 is activated upon phosphorylation by CIPK23, which forms complexes with CBLs such as CBL1, CBL9, and CBL10. ATK1 activated by the CBLs–CIPK23 complexes induces Kþ uptake under the Kþ‐limited condition (Xu et al. 2006). Two members of the protein phosphatase 2C (PP2C) family, AIP1 and AIP1H, have been indicated to interact with the CBLs– CIPKs (CIPK6, CIPK16, and CIPK23) complexes through a direct binding with the kinase domain of CIPKs and to indirectly deactivate AKT1 through inhibition of phosphorylation. Inactivation of PP2Cs, therefore, results in activation of the AKT1 channel. Moreover, it has been demonstrated that specific CBLs directly interact with and inactivate PP2Cs, and consequently activate AKT1 (Lan et al. 2011). Another member of the Shaker family, Kþ CHANNEL1 (KC1), has been shown to form a heterocomplex with AKT1 (Duby et al. 2008; Geiger et al. 2009; Wang et al. 2010; Jeanguenin et al. 2011). The AKT1 homocomplex is known to play a role in Kþ efflux under Kþ‐ deficient conditions. It has been reported that KC1 inhibits the AKT1‐mediated Kþ efflux via heterocomplex formation. AKT1 as well as the AKT1–KC1 complex are assumed to be a unique mechanism whose activity is highly sensitive to a decline in external Kþ concentrations. Although KC1 is not a direct target of CIPK23, inactivation of KC1 results in diminished function of CBLs–CIPK23‐activated AKT1. Additionally, the AKT1–KC1 complex has been reported to function at a much more negative membrane potential than the AKT1 homocomplex (Geiger et al. 2009). This provides the electrophysiological support for higher Kþ channel activity of the AKT1–KC1 heterocomplex compared with the homocomplex. A soluble N‐ethylmaleimide‐sensitive factor attachment protein receptor (SNARE) family protein, SYP121, has also been suggested to be involved in the regulation of AKT1 via physical interaction with KC1 (Honsbein et al. 2009). The plant KT/KUP/HAK family proteins have been isolated as homologs of Escherichia coli KUP and soil yeast HAK proteins (Epstein and Kim 1971; Banuelos and Rodriguez‐Navarro 2001). The KT/KUP/HAK transporters facilitate high‐affinity (cluster I) and/or low‐affinity (cluster II) Kþ transport. The members of this family discriminate poorly among monovalent cations such as Kþ, Rbþ, and Csþ (Very and Sentenac 2003). Arabidopsis HAK5 has been confirmed as a plasma membrane‐localized high‐ affinity transporter which belongs to the cluster I along with rice OsHAK1 and barley HvHAK1 (Rubio et al. 2000; Banuelos et al. 2002; Gierth et al. 2005). HAK5 is mainly expressed in Kþ‐ deprived roots and its function is inhibited by NH4þ (Qi et al. 2008). In the akt1 mutant, the level of HAK5 expression has been shown to be higher than the wild type, possibly due to reduced Kþ uptake in the absence of AKT1 (Hirsch et al. 1998). Most of the other Arabidopsis KUPs do not exhibit differential www.jipb.net

Figure 1. Overview of potassium (Kþ) and sodium (Naþ) transport and signaling in plants (A) Summary of known Kþ and Naþ channels/transporters in the plant. (B) Schematic diagram of Kþ deficiency signaling in the cell. (C) Simplified cartoon of the SALT OVERLY SENSITIVE (SOS) signal pathway. M, myristoylation; P, phosphorylation.

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expression in response to Kþ deficiency (Ahn et al. 2004), suggesting that these KUPs may be regulated post‐transcriptionally and/or post‐translationally. On the other hand, Arabidopsis KUP2, KUP3, KUP4, and barley HvHAK2 have been characterized as low‐affinity (cluster II) Kþ transporters (Quintero and Blatt 1997; Kim et al. 1998; Rubio et al. 2000; Ashley et al. 2006) and Arabidopsis KUP1 as a dual‐affinity transporter (Fu and Luan 1998). Some KT/KUP/HAKs are known to localize at the tonoplast and suggested to function in Kþ transport from the vacuole to the cytosol (Banuelos et al. 2002). By contrast, moss (Physcomitrella patens) PpHAK2 has been reported to localize at the endomembrane and function either as a Hþ/Kþ symporter or an antiporter (Haro et al. 2013). The first plant HKT isolated was from wheat by complementation of the yeast Kþ transporter mutant and was recently named TaHKT2;1 (formerly known by HKT1) and it has been shown to transport Kþ as well as Naþ (Schachtman and Schroeder 1994; Rubio et al. 1995). The plant HKT‐type transporters are categorized into two major subfamilies. Class I family members, that exist both in monocotyledonous and dicotyledonous plants, only transport Naþ whereas class II family members, that are found typically in monocotyledonous plants, mediate both Naþ and Kþ (Garciadeblas et al. 2003; Rodriguez‐Navarro and Rubio 2006; Gierth and Maser 2007; Corratge‐Faillie et al. 2010; Kronzucker and Britto 2011). Therefore, it can be expected that at least some of the class II HKTs in monocotyledonous plants are involved in Kþ influx from the soil. CYCLIC NUCLEOTIDE‐GATED CHANNELs (CNGCs) are one of the largest channel families in plants (Demidchik et al. 2002). The various roles of CNGCs have been previously described to include the control of biotic and abiotic stresses (Demidchik et al. 2002). Of the 20 members in Arabidopsis, CNGC1, CNGC2, CNGC4, and CNGC10 have been confirmed for their Kþ inward‐rectifying channel activities. CNGC2 shows preferential Kþ selectivity over Naþ whereas CNGC4 is similarly permeable to Kþ and Naþ (Leng et al. 1999, 2002; Ma et al. 2006). It has also been shown that CNGC18, which controls the directional pollen tube growth and localizes at the plasma membrane of the pollen tube, also regulates Kþ homeostasis but probably not Naþ homeostasis (Frietsch et al. 2007). Due to their similarity with Kþ channels, glutamate‐ activated channels, GLUTAMATE RECEPTORs (GLRs) have been considered as possible Kþ channels. Of those, GLR1.1 and GLR1.4, whose transcripts are expressed in the roots, are shown to absorb Kþ (Chiu et al. 2002; Tapken and Hollmann 2008). The Arabidopsis genome encodes as many as 28 members of CATION/Hþ EXCHANGERs (CHXs), which are homologous to the mammalian CHXs. Some of them are suggested to be involved in Naþ transport in plants whereas CHX13, CHX17, CHX20, CHX21, and CHX23 have been shown to function in Kþ accumulation and homeostasis (Cellier et al. 2004; Grabov 2007; Padmanaban et al. 2007; Zhao et al. 2008; Lu et al. 2011). CHX13 has been suggested to play a role in Kþ acquisition and to promote Kþ uptake. The chx13 mutants are sensitive to Kþ deficiency and expression of CHX13 is induced in the Kþ‐starved roots (Zhao et al. 2008). Recently, two moss (P. patens) CHXs, PpCHX1 and PpCHX2, have been shown to mediate Kþ transport as a Kþ/Hþ antiporter (Mottaleb et al. 2013). Additionally, the wheat low‐affinity transporter, March 2014 | Volume 56 | Issue 3 | 231–249

LCT1, has been reported to mediate Kþ, Naþ, Ca2þ as well as Cd2þ (Schachtman et al. 1997; Clemens et al. 1998). Although a homolog has been identified in rice, this OsLCT1 does not mediate Naþ (Uraguchi et al. 2011). It has been suggested that GORK plays a role in Kþ efflux at the root hair tip and may function as a Kþ sensor in the root hairs (Ivashikina et al. 2001). However, the mechanisms of Kþ efflux and radial movement in the roots are largely unknown. Long‐distance transport of Kþ Potassium absorbed via Kþ channels and transporters in the roots must be loaded into the xylem for translocation to the shoots. SKOR has first been identified as a Shaker‐like outward‐ rectifying Kþ channel in plants. SKOR mediates Kþ transport from the stelar cells to the xylem in the roots, which is a key step for the long‐distance Kþ distribution from the root to the shoot. The C‐terminal non‐transmembrane region of SKOR has been demonstrated as being required for the intracellular Kþ sensing process (Liu et al. 2006). The expression of SKOR is inhibited by abscisic acid (ABA), suggesting that decreased Kþ transport to the shoots may be a form of water stress response (Gaymard et al. 1998). Although Kþ EFFLUX ANTIPORTERs (KEAs) are considered to be Hþ/Kþ antiporters and to play a role in Kþ efflux into the xylem sap, their molecular functions are not well characterized (Yao et al. 1997; Maser et al. 2001). The exception is Arabidopsis KEA2, which has recently been shown to be a functional Hþ/Kþ antiporter and to modulate monovalent cation and pH homeostasis in chloroplasts or plastids (Aranda‐Sicilia et al. 2012). An inward‐rectifying channel, KAT2, is phloem‐associated and localized in the cotyledons and the apical part of the hypocotyl and its expression is induced by auxin (Philippar et al. 2004). It is possible that KAT2 functions in Kþ homeostasis in the phloem of Arabidopsis. AKT2/3 is a member of the weakly voltage‐dependent Kþ channels. They have been shown to be regulated by extracellular protons and Ca2þ and to function as the photosynthate‐induced phloem channels (Hoth et al. 2001; Deeken et al. 2002, 2003; Ivashikina et al. 2005). The Kþ channel function of AKT2/3 is blocked by proton, regulated independently of voltage change and their expression is in the vascular tissues, predominantly in the phloem of the aerial parts of the plant. An Arabidopsis mutant, akt2/3‐1, displays reduced Kþ contents and reduced Kþ dependency of the phloem potential relative to the wild type. It is, therefore, suggested that AKT2/3 regulates phloem loading and long‐distance transport via modification of phloem potential (Deeken et al. 2002). Interestingly, AKT2/3 functions as both a Kþ efflux channel and an influx channel. AKT2/3, unlike the other Shaker channels (AKT1, KAT1, KAT2, and KC1), has been reported to physically interact with ABA‐regulated PP2CA. Moreover, AKT2/3 and PP2CA are shown to be co‐ expressed. These findings suggest that AKT2/3 and PP2CA coordinately regulate Kþ current and membrane potential for phloem loading and long‐distance transport of Kþ (Cherel et al. 2002). Intracellular movement of Kþ In order to maintain constant cytosolic Kþ concentrations in the cell, Kþ influx into and efflux out of the vacuole is a crucial mechanism for plant survival. NHXs are known to be involved www.jipb.net

Kþ and Naþ transport and signaling in sequestration of Naþ and Kþ into the vacuoles. Arabidopsis NHX1 and NHX2 function as a Naþ/Hþ and Kþ/Hþ antiporters at the tonoplast depending on the Naþ concentrations (Venema et al. 2002; Rodriguez‐Rosales et al. 2009; Barragan et al. 2012). NHX3 has also been indicated as being localized in the vacuolar membrane as well as the endoplasmic reticulum (ER) and to function as a Kþ/Hþ antiporter required for Kþ‐deficiency tolerance during the early developmental stage of the plant (Liu et al. 2010). On the other hand, the TPK family, which is comprised of five members in Arabidopsis, is suggested in regulation of Kþ efflux from the vacuole. TPKs, with the exception of TPK4, have been shown to localize at the vacuolar membrane (Hedrich 2012). It has been demonstrated that TPK1 is regulated through 14‐3‐3 protein binding as well as Ca2þ binding on the EF‐hand motif and functions in a voltage‐ independent manner. TPK1 has been considered to play a role in Kþ homeostasis through vacuolar Kþ release (Bihler et al. 2005; Latz et al. 2007, 2013). A tonoplast‐localized KT/ KUP/HAK, OsHAK10, is also known to mediate Kþ release from the vacuole to the cytosol (Banuelos et al. 2002) and this suggests that the other tonoplast‐localized KT/KUP/HAK may be involved in this process. However, information on the cellular localization of the plant KT/KUP/HAKs is scarce and further studies are required. In terms of stomatal regulation, Kþ is one of the major players in osmotically driven guard cell movement (Schroeder et al. 2001). It has been shown that the activation of Hþ‐ATPase at the guard cell membrane results in membrane hyperpolarization and sequential activation of inward‐rectifying Kþ channels such as KAT1 and KAT2; this increase in Kþ influx leads to stomatal opening. By contrast, depolarization of the guard cell membrane through inhibition of Hþ‐ATPase leads to activation of outward‐rectifying Kþ channels such as GORK, an increase in Kþ efflux and subsequent closure of the stomata (Ache et al. 2000; Pilot et al. 2001; Schroeder et al. 2001; Lebaudy et al. 2010). Arabidopsis KAT1 has been cloned (Schachtman et al. 1992) and confirmed as a Kþ channel using the Kþ channel blockers TEA and Ba2þ (Anderson et al. 1992a, b). An ABA‐activated kinase, OPEN STOMATA1 (OST1), has been shown to phosphorylate the C‐terminal region of KAT1 at Thr306 and Thr308 and modification of Thr306 diminishes its activity (Sato et al. 2009). It also has been revealed that the N terminus of KAT1 is required for voltage sensitivity by contributing to the electric field sensed by the voltage sensor and the KAT1 properties are not affected by the extracellular Kþ concentrations (Marten et al. 1996; Marten and Hoshi 1998). KAT2 is also expressed in the guard cell and its product controls stomatal opening. KAT1 and KAT2 have been shown to preferentially heteromerize to form inward Kþ channel in the guard cells (Pilot et al. 2001; Lebaudy et al. 2010). A similar heterocomplex OsKAT2–OsKAT3 in rice has been observed in the guard cells, although the function of two proteins is antagonistic (Hwang et al. 2013a, 2013b). Yet another component, Arabidopsis CHX20 has also been suggested to localize at the endomembrane of guard cells and to regulate stomatal opening (Padmanaban et al. 2007). On the other hand, GORK has been shown to be activated in a voltage‐ and Kþ‐dependent manner and to mediate depolarization‐induced Kþ efflux from the guard cell. ABA induces both depolarization of the guard cell plasma membrane and GORK expression and GORK‐mediated Kþ efflux out of the guard cell is also induced www.jipb.net

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(Ache et al. 2000; Becker et al. 2003). As described here, Kþ influx for stomata opening and Kþ efflux for stomata closing are tightly regulated by the Shaker‐type Kþ channels. A mitochondria‐localized Kþ channel (mitoKATP channel) has also been isolated as a Kþ uniporter (Pastore et al. 1999, 2007, 2013). It has been indicated that Kþ concentrations in the mitochondrial matrix are regulated by the mitoKATP channel and subsequent Kþ entry into the mitochondria results in depolarization of the membrane (Jarmuszkiewicz et al. 2010). However, the information of mitochondria‐localized plant Kþ channels is still limited compared to those of mammalian (Jarmuszkiewicz et al. 2010). Therefore, further characterization is required to understand their roles in plants. Response to Kþ availability Plant roots constantly monitor external Kþ concentrations and sense Kþ availability. When plants sense Kþ deficiency, a short‐ term deficiency response is turned on and the high‐affinity Kþ uptake system is activated within a few hours (Shin and Schachtman 2004; Schachtman and Shin 2007; Wang and Wu 2013). The high‐affinity Kþ uptake mechanism in plants is mediated by the high‐affinity channels such as Arabidopsis HAK5 and AKT1, which are activated by ROS within 6 h of a deficiency being detected (Shin and Schachtman 2004). ROS produced by nicotinamide adenine dinucleotide phosphate oxidases is known to play a key role in Kþ‐deficiency signaling as well as in other macronutrient (nitrogen, phosphorus, and sulfur) deficiency signal pathways (Shin and Schachtman 2004; Shin et al. 2005; Schachtman and Shin 2007). Potassium‐ deficiency‐induced ROS is mainly accumulated in the elongation zone of the root hair and acts to stimulate elongation (Jung et al. 2009) and also modulates gene expression, including HAK5 (Shin and Schachtman 2004) and the downstream signaling components (Shin and Schachtman 2004; Jung et al. 2009; Kim et al. 2010, 2012). It has also been reported that an ethylene signal is required for Kþ‐deficiency‐ induced ROS accumulation and consequent gene expression, root hair elongation as well as high‐affinity Kþ uptake (Jung et al. 2009; Kim et al. 2012) (Figure 1B). Calcium is another important molecule in Kþ‐deficiency signaling and in Kþ/Naþ homeostasis. Cytoplasmic Ca2þ serves as a secondary signal and regulates the downstream transcriptional and post‐translational response to the external Kþ availability (Wang and Wu 2013). When plants experience Kþ deficiency, the cytosolic Ca2þ levels are immediately elevated resulting in the activation of AKT1 via phosphorylation by CIPK23 (Hirsch et al. 1998; Xu et al. 2006; Lan et al. 2011). It has been reported that the known Ca2þ sensors, CBL1, CBL9, and CBL10 interact with CIPK23 to activate AKT1 and that CBL4 interacts with CIPK6 for AKT2/3 activation in the Kþ‐deficient conditions (Hirsch et al. 1998; Ros et al. 1999; Spalding et al. 1999; Xu et al. 2006; Geiger et al. 2009; Wang et al. 2010; Lan et al. 2011). Because AKT1 is the major channel for uptake of Kþ from the soil under the Kþ‐deficient conditions, the Ca2þ‐ regulated CBLs–CIPK23 complex is the crucial component for Kþ‐deficiency signaling. The cipk23 mutant shows impaired growth and lower Kþ content under Kþ deficiency relative to the wild type, reinforcing the importance of CBLs–CIPK23. A recent report has indicated that CBL2 and CBL3 also play a role in regulation of the putative tonoplast‐localized outward Kþ channel phosphorylated by CIPK9 (Liu et al. 2013). In contrast March 2014 | Volume 56 | Issue 3 | 231–249

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to the cipk23 mutant, Kþ contents are unchanged in the Kþ‐ starved cipk9 mutant compared with the wild type (Pandey et al. 2007). Because the Kþ‐deficiency symptom is known to be initiated in the old leaves, the authors have suggested that CIPK9 may be involved in Kþ reallocation from the old leaves to the young leaves during Kþ deficiency (Figure 1B). Some of the genes encoding Arabidopsis Kþ transporters such as KEA5, KC1, and CHX17 in addition to HAK5 have been shown to be induced by Kþ deficiency (Ahn et al. 2004; Cellier et al. 2004; Shin and Schachtman 2004; Zhao et al. 2008). A similar response has been observed in a variety of plant species including tomato (LeHAK5), hot pepper (CaHAK1), and rice (OsHAK1) (Banuelos et al. 2002; Wang et al. 2002; Martinez‐ Cordero et al. 2005). Some of the transcription factors regulating these Kþ channels also have been identified and characterized (Kim et al. 2012; Hong et al. 2013). Expression of Arabidopsis high‐affinity transporter, HAK5, is known to be dramatically induced by Kþ deprivation and quickly reduced to the basal levels on Kþ resupply (Ahn et al. 2004). For this reason, HAK5 has been extensively studied as it is considered a positive regulator of Kþ‐deficiency signaling (Ahn et al. 2004; Schachtman and Shin 2007; Qi et al. 2008; Amtmann and Blatt 2009; Kim et al. 2012; Hong et al. 2013). Many transcription factors that activate the expression of HAK5 have been isolated using the HAK5promoter::luciferase plants (Kim et al. 2012; Hong et al. 2013). Among the many, five transcription factors (RAP2.11, DDF2, JLO, bHLH121, and transcription factor II_A) have been confirmed for their responsiveness to Kþ deficiency and their direct binding ability to the HAK5 promoter. Overexpression of these transcription factors results in the enhanced root growth under the Kþ‐deficient conditions, presumably via induction of HAK5 expression (Kim et al. 2012; Hong et al. 2013). Activation of an AP2/ERF‐type transcription factor, RAP2.11, leads to the induction of HAK5 expression through binding on the ERE motif and the GCC‐box of the HAK5 promoter. It also has been reported that expression of RAP2.11 is induced by ROS, ethylene, and Kþ deficiency and that RAP2.11 is involved in root growth and Kþ uptake. This suggests that RAP2.11 plays a crucial role in the ethylene‐ and ROS‐mediated Kþ‐deficiency signal pathway (Kim et al. 2012). In addition to these transcription factors, a type III peroxidase, RARE COLD INDUCIBLE GENE3 (RCI3), has been identified as a positive regulator of HAK5 expression. Overexpression of RCI3 influences primary root growth under normal conditions and results in higher ROS production in the roots under Kþ deficiency but does not alter tolerance to Kþ deficiency (Kim et al. 2010). In addition to the transcription factors which directly regulate the Kþ channels, those that are involved in Kþ deficiency have been identified by various approaches (Armengaud et al. 2004; Shin and Schachtman 2004; Shin et al. 2007; Kim et al. 2009; Shin 2011; Kim et al. 2012; Hong et al. 2013). Armengaud and co‐workers have shown that expression of various types of transcription factors such as bHLH, WRKY, NAM, AP2, and E2F is regulated by Kþ availability according to the microarray analysis (Armengaud et al. 2004). This microarray analysis also suggested the involvement of jasmonates (JAs) in Kþ‐deficiency signaling. It has been shown that expression of a series of genes involved in JA biosynthesis is differentially regulated by Kþ availability (Armengaud et al. 2004). A key protein of JA signaling, CORONATINE INSENSITIVE1 (COI1) is an F‐box E3 ligase that functions as a March 2014 | Volume 56 | Issue 3 | 231–249

component of the JA receptor complex. It has been indicated that responsiveness to Kþ availability, especially gene expression, is attenuated in the coi1‐16 mutant and Kþ‐deficiency‐ induced JA production confers increased resistance against pathogens and insects to the wild‐type plants (Armengaud et al. 2010). In addition to the levels of JA, oxylipin and glucosinolate contents are shown to be increased by Kþ deficiency in the wild type but this increase is absent in coi1‐16 (Troufflard et al. 2010). It has been proposed that Kþ deficiency induces glucosinolate and oxylipin biosynthesis to enhance survival of the plants in the Kþ‐deficient conditions (Troufflard et al. 2010). Lateral root growth is inhibited upon Kþ deficiency. It has been reported that the Arabidopsis R2R3‐MYB transcription factor, MYB77, which is involved in auxin‐mediated lateral root growth, participates in this response (Shin et al. 2007). In response to Kþ deficiency, the free indole‐3‐acetic acid levels and MYB77 expression are reduced, resulting in reduction of the lateral root numbers (Shin and Schachtman 2004; Shin et al. 2007). Potassium transport through Arabidopsis KUP4 also may be coupled with auxin transport (Rigas et al. 2001; Desbrosses et al. 2003; Vicente‐Agullo et al. 2004). It has been shown that auxin induces expression of maize ZMK1, a homolog of Arabidopsis AKT1, presumably leading to an increase in a Kþ channel density (Philippar et al. 2006). These findings point to the notion that auxin is involved in Kþ‐ deficiency response as well as Kþ uptake. A nucleus‐localized protein, NUCLEAR PROTEIN X1 (NPX1), in Arabidopsis has been demonstrated to be upregulated in response to Kþ deficiency (Shin and Schachtman 2004). It has been shown further that NPX1 interacts with an NAC transcription factor, TIP, to inactivate the downstream ABA pathway, suggesting the involvement of ABA signaling in Kþ‐ deficiency response (Kim et al. 2009). In support of this, higher levels of ABA are seen in Kþ‐starved shoots and roots (Kim et al. 2009). It is predicted that Kþ deficiency activates ABA biosynthesis and signaling through inactivation of NPX1. Cytokinins are also suggested to play a role in Kþ‐deficiency response. Upon Kþ deficiency, levels of cytokinins have been shown to decrease, resulting in ROS accumulation, root hair growth, and HAK5 expression in Arabidopsis (Nam et al. 2012). As described, the Kþ‐deficiency signal pathway is mediated by a various phytohormones including ethylene, JAs, auxin, ABA, and cytokinins. More than 60 enzymes are reported to be regulated in a Kþ availability‐dependent manner, many of which are involved in sugar and nitrogen metabolism (Wyn Jones and Pollard 1983; Amtmann et al. 2006). Potassium deficiency also modifies the levels of various metabolites including amino acids, pyruvate, organic acids, and sugars. Most of the changes in response to deficiency are known to be reversed by Kþ resupply (Armengaud et al. 2009). It has been reported that pyruvate kinases are activated by Kþ binding and the levels of pyruvate decrease in Kþ‐starved plants (Smith et al. 2000; Turner and Plaxton 2000). A dramatic decline in acidic amino acid (glutamate and aspartate) levels has also been demonstrated in Kþ‐starved plants. The alteration of glutamate contents may be associated with a cation channel, GLRs (Lacombe et al. 2001; Amtmann and Armengaud 2009). A classic report has shown an alteration of araginase activity and an increase of proline contents in finger‐millet and groundnut under Kþ deficiency www.jipb.net

Kþ and Naþ transport and signaling (Nageswara Rao et al. 1981). It can be assumed that glutamate plays a role in Kþ‐deficiency signaling, leading to the modification of proline metabolism. In order to survive in limited Kþ conditions, plants promptly sense Kþ deprivation and turn on an emergency Kþ‐deficiency signaling mechanism. As described above, Kþ‐deficiency signaling is very elaborate and fine‐tuned. Although intensive studies on Kþ‐deficiency signaling have been conducted over the past decade, further elucidation of the sensing mechanisms is required.

SODIUM TRANSPORT AND SIGNALING IN PLANTS Sodium is categorized as a “beneficial element” for plants. This means, by definition, that Naþ is not required by all plants but can promote plant growth and may be essential for particular taxa (Pilon‐Smits et al. 2009). Although there is a tendency to focus on its negative effect in creating salt stress at high concentrations, Naþ is known to compensate for some of the functions of Kþ owing to its chemical similarity, particularly when Kþ availability is limited. On the other hand, soil salinity is a major drawback for plant growth and crop production, and according to an Food and Agriculture Organization of the United Nations report published in 2000, more than 800 million hectares of the total global land area is affected by salinity. Because of this, plants have developed the specific mechanisms to transport, sense, and respond to a variety of Naþ conditions. In this section, how plants absorb Naþ from the soil, transport it across the plant body, and respond to it when there is an excess will be discussed focusing on recent progress in the understanding of these mechanisms. Beneficial functions of Naþ are also described. Naþ influx at the soil‐plant interface The largest proportion of Naþ influx from the soil into plant cells occurs across the plasma membrane of the root hair epidermal cells through passive transport. Several candidates have been reported as responsible for Naþ uptake in plants including NSCCs, HKTs, and LCT1 (Apse and Blumwald 2007; Craig Plett and Moller 2010). NSCCs typically mediate the passive influx of a wide range of cations through the plasma membrane. Two families of NSCCs, CNGCs and GLRs, are suggested as being involved in Naþ uptake (Apse and Blumwald 2007; Craig Plett and Moller 2010). In the genome of Arabidopsis, the glycophytic (salt‐sensitive) model plant, 20 each of CNGCs and GLRs are predicted. Of those, CNGC1, CNGC3, and CNGC4 have been reported to conduct Naþ as well as Kþ (Balague et al. 2003; Hua et al. 2003; Gobert et al. 2006); however, CNGC2 has been shown to preferentially conduct Kþ over Naþ (Hua et al. 2003). CNGC10 also has been suggested as conducting Kþ and Naþ; however, it may also contribute to Naþ uptake at the seedling stage and Naþ recirculation in mature plants, suggesting a complicated regulatory mechanism (Guo et al. 2008). Expression of CNGC19 and CNGC20 has been found to be induced in response to the ionic, not osmotic, portion of salt stress. However, this induction occurs only in the shoots and cngc19 and cngc20 mutants show no difference in Naþ or Kþ contents in the shoots compared with the wild type; therefore, the authors reporting this predict that CNGC19 www.jipb.net

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and CNGC20 are involved in reallocation of Naþ in plants in response to salt stress rather than Naþ uptake from the soil (Kugler et al. 2009). Of the GLRs, conductance of GLR1.1 and GLR1.4 for Naþ, Kþ, and Ca2þ, and GLR3.7 for Naþ, Ca2þ, and Ba2þ has been reported (Roy et al. 2008; Tapken and Hollmann 2008). Because the function of the majority of the other NSCC members remain elusive, it is possible that many more are acting in parallel for Naþ uptake. Some of the class II HKTs are also suggested as being responsible for Naþ uptake at the soil‐plant interface (Corratge‐Faillie et al. 2010; Hauser and Horie 2010). The first member of HKTs isolated, TaHKT2;1, has been suggested to function as a high‐affinity Naþ/Kþ symporter and, under salt stress, to function as a low‐affinity Naþ uniporter (Corratge‐ Faillie et al. 2010; Hauser and Horie 2010). Later, it was found that HKTs could be categorized into two major subfamilies, class I and class II (Platten et al. 2006). Class I HKTs have the first glycine replaced by a serine at the highly conserved four glycine residues in the first p‐loop region (SGGG type) whereas class II HKTs have all four glycine residues (GGGG type). This amino acid change is important for the selectivity of ions to which each HKT is permeable: the SGGG‐type HKTs are permeable to Naþ only while the GGGG‐type HKTs are permeable to both Naþ and Kþ (Maser et al. 2002b). In rice, two of the nine members of the HKT family, OsHKT2;1 and OsHKT2;2 (formerly known by HKT1 and HKT2) have been reported to mediate Naþ uptake from the soil. OsHKT2;1 is an atypical class II HKT which possesses the SGGG‐type p‐loop and mediates high‐affinity Naþ uptake, but little Kþ (Horie et al. 2001; Yao et al. 2010). Expression of OsHKT2;1 is induced in response to Kþ deficiency, while oshkt2;1 mutants accumulate less Naþ, but not less Kþ, suggesting that OsHKT2;1 contributes to Naþ uptake in a Kþ availability‐dependent manner. The mutants also show severe growth retardation under the low Naþ and Kþ conditions, suggesting that Naþ can compensate, to some extent, for the nutritional value of Kþ under Kþ deficiency (Horie et al. 2001, 2007). By contrast, OsHKT2;2, so far only found in a salt‐tolerant indica variety, Pokkali, transports both Naþ and Kþ, but only transports Naþ under salt stress, as in the case of TaHKT2;1 (Horie et al. 2001; Yao et al. 2010). In barley, a relatively salt‐tolerant species, HvHKT2;1 (formerly known by HKT1) transports both Naþ and Kþ. Overexpression of HvHKT2;1 increases Naþ concentrations in the shoots and renders the plants tolerant to salinity, indicating the salt‐including behavior of barley (Mian et al. 2011), which contrasts with the salt‐excluding behavior of wheat (discussed in the later section). Class II HKTs are generally found in monocotyledonous species and no class II HKT homologs exists in Arabidopsis (Corratge‐Faillie et al. 2010). Another candidate transporter, LCT1, has been isolated from wheat and shown to conduct a number of cations including Naþ, Rbþ, Ca2þ, Liþ, and Csþ (Schachtman et al. 1997; Amtmann et al. 2001; Uraguchi et al. 2011). LCT1 contains 8–10 transmembrane helices and a hydrophilic N terminus; however, this Naþ uptake function may be unique to wheat (Schachtman et al. 1997). Radial transport of Naþ in the root Once it is inside the epidermis, radial transport of Naþ to the xylem across the root radius occurs through apoplastic and/or March 2014 | Volume 56 | Issue 3 | 231–249

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symplastic routes. Part of the Naþ becomes bound to the root apoplast but the rest is thought to move somewhat freely across the apoplast until it gets to the Casparian band of the endodermis which serves as the physical barrier for Naþ entry. Generally, at this point, Naþ needs to be transported across the plasma membrane into the cytoplasm for further radial movement; however, it can in some cases pass the Casparian band through apoplastic bypass flow (Craig Plett and Moller 2010). The extent of the contribution of this bypass pathway to net Naþ influx depends on the plant species but it is not believed to be significant in Arabidopsis (Essah et al. 2003). In rice, in which a significant amount of Naþ is transported through the bypass pathway, silicon supplementation can partially block the apoplastic transpirational bypass flow of Naþ into the shoot (Yeo et al. 1999; Shi et al. 2013). It has been suggested that another structural barrier to apoplastic Naþ movement is the phi cell layers, which exist in a small number of species such as Brassica. Phi cells show cell wall thickening and accumulate Naþ; therefore, preventing the Naþ flow into the xylem (Fernandex‐Garcia et al. 2009). Apoplast is believed to withstand relatively high concentrations of Naþ because apoplastic enzymes have been shown to be more salt tolerant than cytoplasmic enzymes in both halophytes (salt‐tolerant species) and glycophytes (Thiyagarajah et al. 1996). On another front, Naþ once having entered into the cytoplasm through transporters/channels (as mentioned in the earlier section) moves swiftly to the xylem via a symplastic route connected by plasmodesmata. It is not known whether this process is regulated in any way for Naþ (Craig Plett and Moller 2010). A classic report depicts this process in tomato as a passive flow depending on the transpiration rate (Maas and Ogata 1972). Although no transporter has been reported to be involved in root radial transport of Naþ, a member of the CHX family, Arabidopsis CHX21, is a possible candidate. The chx21 mutant shows reduced Naþ concentrations in xylem and leaf sap under salt stress and CHX21 is detected in root endodermal cells, suggesting that CHX21 may be responsible for transporting Naþ across the endodermal cell membrane into the stele (Hall et al. 2006). An Arabidopsis mutant sodium overaccumulation in shoot1 (sas1) was reported to be impaired in control of the root radial transport of Naþ; however, up to now the mutation has not yet been associated with a gene (Nublat et al. 2001). Cell‐ specific ion profiles in the roots of durum wheat and sunflower have revealed that epidermis and cortex provide a preferential storage for Naþ (Lauchli et al. 2008; Ebrahimi and Bhatla 2012). Long‐distance transport of Naþ When Naþ reaches the stele, it needs to be loaded to the xylem across the plasma membrane from where it goes through long‐ distance transport from root to shoot via the transpiration stream. It is believed that xylem loading of Naþ is active under mild salinity and passive under severe salt stress (Apse and Blumwald 2007; Craig Plett and Moller 2010). An Arabidopsis mutant of a plasma membrane Naþ/Hþ antiporter, sos1, accumulates less Naþ in the shoots under mild salt stress and SOS1 is localized in the xylem‐symplast boundary (Shi et al. 2000, 2002). Therefore, SOS1 is thought to mediate the active loading of Naþ to the xylem under mild salinity. However, the same reports have indicated that at high salt stress, expression of SOS1 is induced and SOS1 functions in retrieval of Naþ from the xylem, conferring salt tolerance to March 2014 | Volume 56 | Issue 3 | 231–249

plants (Shi et al. 2000, 2002). This notion remains speculative and is discussed later in this section. It has been shown in Arabidopsis that, in response to salinity, ROS accumulates in root vasculature and controls xylem loading of Naþ to inhibit a toxic accumulation of Naþ in the shoots (Jiang et al. 2012). There is also an indication that inositol may promote uptake and xylem loading of Naþ in ice plant (Mesembryanthemum crystallinum), a halophyte (Nelson et al. 1999). Sodium loaded in the xylem of the root is transported to the shoot by the transpiration stream. Because Naþ exerts most toxicity in the shoot where it inhibits a various metabolic processes, plants have developed some strategies to counteract this. One way is the accumulation of Naþ in the older leaves in order to protect the young growing leaves from salt stress. This phenomenon has been reported in a wide variety of plant species (Craig Plett and Moller 2010). Multiple studies have reported on removal of Naþ from the xylem but this process is unlikely to be mediated by a Naþ/Hþ antiporter such as SOS1 because its operation “in reverse” under high Naþ conditions is thermodynamically unfavorable (Apse and Blumwald 2007; Craig Plett and Moller 2010). Instead, class I HKTs have been shown to be involved in xylem unloading of Naþ. HKT1;1 from Arabidopsis is localized at the plasma membrane of xylem parenchyma cells and responsible for passive xylem unloading of Naþ (Sunarpi et al. 2005; Davenport et al. 2007; Xue et al. 2011). Consequently, hkt1;1 mutants show increased concentrations of Naþ in the shoot and xylem sap and decreased concentrations in the phloem sap compared with the wild type, conferring hypersensitivity to Naþ (Berthomieu et al. 2003; Sunarpi et al. 2005; Davenport et al. 2007). Conversely, retrieval of Naþ from the xylem to avoid Naþ transport into the shoot via HKT1 is thought to be a primary salt‐tolerance mechanism in glycophytes (Rus et al. 2004). Moreover, it has been shown that cell type‐ specific expression, but not constitutive expression, of HKT1;1 in the root epidermis and cortex or stele decreases Naþ accumulation in the shoot and improves salinity tolerance, providing a clue to improve salt tolerance in crops (Moller et al. 2009; Plett et al. 2010). HKT1;1 was once reported to be also involved in phloem loading and recirculation of Naþ (Berthomieu et al. 2003) but this notion was refuted by the later report (Davenport et al. 2007). Class I HKTs responsible for Naþ unloading from the xylem have also been identified in rice and wheat, OsHKT1;5, TmHKT1;4 and TmHKT1;5 (Ren et al. 2005; James et al. 2006). It has been shown that a significant amount of Naþ recirculation through the phloem back to the root may occur in some plant species, especially halophytes, as a form of a salt‐ tolerance mechanism (Craig Plett and Moller 2010). Arabidopsis CNGC10 has been reported to be involved, not only in Naþ uptake from the soil as described in the earlier section, but also in phloem loading and/or xylem unloading of Naþ because Naþ is highly accumulated in the shoot of the CNGC10 antisense lines relative to the wild type (Guo et al. 2008). Naþ efflux from the root It is important that plants maintain low cytoplasmic Naþ concentrations for growth and survival under saline conditions. Plants have developed a direct mechanism to exclude Naþ from the cells across the plasma membrane to the soil or apoplast. This process has been well characterized in www.jipb.net

Kþ and Naþ transport and signaling Arabidopsis. SOS1, a Naþ/Hþ antiporter involved in xylem loading as mentioned earlier, is also localized at the plasma membrane of epidermis in the root tip as well as the root stele (Shi et al. 2002) and considered to play a major role in active Naþ efflux under the high Naþ conditions. SOS1 remains inactive due to a C‐terminal auto‐inhibitory domain under non‐ stress conditions and is activated through phosphorylation of the auto‐inhibitory domain by the SOS2–SOS3 complex upon salinity (Qiu et al. 2002; Quintero et al. 2011). SOS2 (CIPK24) is a serine/threonine protein kinase that directly phosphorylates and activates SOS1 (Liu et al. 2000; Quintero et al. 2002). SOS2 itself is autophosphorylated and this phosphorylation is important for activation of SOS1 in salt tolerance (Fujii and Zhu 2009). SOS3 (CBL4) is a Ca2þ sensor which escorts SOS2 to plasma membrane‐bound SOS1 to interact and activate (Liu and Zhu 1998; Liu et al. 2000). Calcium binding and N‐ myristoylation of SOS3 are required for its function in salt tolerance (Ishitani et al. 2000). It has been revealed recently that SOS2 physically interacts with a flowering time regulator, GIGANTEA (GI), and this interaction inhibits SOS2 from interacting with SOS3 therefore preventing phosphorylation of SOS1 in the absence of salt stress (Kim et al. 2013). Upon salinity, GI dissociates from SOS2 and is degraded, consequently rendering SOS2 available for interaction with SOS3 to activate the downstream response and retarding flowering, a common response to stress conditions (Kim et al. 2013). The SOS3 homolog SOS3‐LIKE CALCIUM BINDING PROTEIN8 (SCABP8/CBL10) has been implicated in the SOS pathway (Kim et al. 2007; Quan et al. 2007). One group has reported that Ca2þ‐bound SCABP8 interacts with SOS2 and activates SOS1 in response to salinity mainly in the shoot and SOS3 functions primarily in the root (Quan et al. 2007). SCABP8 has further been shown to be phosphorylated by SOS2 in a Ca2þ‐ independent manner upon salt stress and this phosphorylation stabilizes the SCABP8–SOS2 interaction but SOS2 does not phosphorylate SOS3, reinforcing the non‐redundancy of their functions (Lin et al. 2009). Another group, on the other hand, has suggested that the SOS3–SOS2 complex functions in the plasma membrane and the SCABP8–SOS2 complex functions at the vacuole, possibly involved in vacuolar sequestration of Naþ (Kim et al. 2007). In support of this, indirect evidence has shown that tonoplast Naþ/Hþ antiport activity is induced by SOS2 (Qiu et al. 2004). SOS2 is also known to interact with other vacuolar transporters, a Hþ/Ca2þ antiporter CATION EXCHANGER1 (CAX1) and Hþ‐ATPase, suggesting a complicated ion homeostasis adjustment that takes place in response to salt stress (Cheng et al. 2004; Batelli et al. 2007) (Figure 1C). Recently, SCABP8 has also been indicated to directly interact with AKT1 to regulate Kþ influx (Ren et al. 2013). Vacuolar sequestration of Naþ Another important mechanism for salt tolerance in plants is compartmentalization of Naþ into vacuole to reduce the cytosolic Naþ concentrations. Vacuolar NHXs are believed to be the key regulator of this process. The first plant NHX identified is Arabidopsis NHX1 and overexpression of this confers salt tolerance to the plants (Apse et al. 1999; Gaxiola et al. 1999), although there is a contradictory report (Yang et al. 2009). NHX1 and NHX2 are the most abundant and widely distributed NHX transcripts in Arabidopsis (Yokoi et al. 2002; www.jipb.net

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Aharon et al. 2003) and recent reports have indicated that they redundantly regulate Kþ uptake into the vacuole, vacuolar pH as well as Naþ sequestration to control cell expansion, stomatal function, and flower development (Leidi et al. 2010; Bassil et al. 2011b; Barragan et al. 2012). Induction of NHX1 and NHX2 in response to salinity is ABA‐dependent (Shi and Zhu 2002; Yokoi et al. 2002). NHX1 is also regulated by a vacuolar calmodulin‐like protein, CaM15, through modification of Naþ/Kþ selectivity of NHX1 upon binding to reduce Naþ/Hþ exchange activity in a Ca2þ‐ and pH‐dependent manner (Yamaguchi et al. 2005). NHX3 is also predominantly localized at the vacuolar membrane and is involved in Kþ sequestration (Liu et al. 2010). NHX4 is reported to be localized to the vacuole and involved in salt tolerance but its direct function in Naþ sequestration is still obscure (Li et al. 2009). NHX5 and NHX6, on the other hand, are localized to endosomal compartments associated with the Golgi and trans‐Golgi network and have a redundant role in salt tolerance, protein processing, and trafficking of intracellular cargo through regulation of endosomal pH and Kþ (and possibly Naþ) homeostasis (Bassil et al. 2011a). Activity of NHXs is reported to be either dependent or independent of the SOS pathway (Yokoi et al. 2002; Qiu et al. 2004). It is generally accepted that the activity of NHXs is, transcriptionally, translationally, or post‐ translationally, increased upon salt stress and this increase accounts for salinity tolerance in a variety of plant species (Silva and Geros 2009). In order to maintain the function of Naþ/Hþ antiporters for moving Naþ into the vacuole in exchange for Hþ, a Hþ gradient across the tonoplast generated by Hþ‐ATPase and Hþ‐pyrophosphatase (Hþ‐ PPiase) is necessary. In Arabidopsis, Hþ‐PPiase is encoded by a single gene, AVP1, and overexpression of this gene enhances the vacuolar Hþ gradient resulting in salt tolerance, presumably due to activation of Naþ/Hþ antiporters (Gaxiola et al. 2001). A recent report has shown that salt tolerance conferred by AVP1 overexpression is impaired in the sos1 mutant, suggesting that this pathway is SOS1 dependent (Undurraga et al. 2012). Another class of cation transporters, CATION/CA2þ EXCHANGERs (CCXs), may be involved in vacuolar sequestration of Naþ. It has been suggested that Arabidopsis CCX3 (formerly known by CAX9) and possibly CCX4 exhibit Naþ/Kþ transport ability (Morris et al. 2008). CCX3 is primarily localized in the endomembrane of flowers and CCX4 throughout the plant. Overexpression of CCX3 induces accumulation of Naþ in the leaves but whether these CCXs take part in compartmentalization of Naþ in the vacuole is elusive (Morris et al. 2008). CCX5 (formerly known by CAX11), in contrast, has been reported to be localized in the plasma membrane and nuclear periphery and to mediate high‐affinity Kþ uptake and Naþ transport in yeast (Zhang et al. 2011b). Another component suggested to be involved in sequestration is NAþ‐ AND Kþ‐SENSITIVE1 (NKS1) in Arabidopsis, an endomembrane‐localized protein of unknown function. The nks1‐1 mutant exhibits enhanced sensitivity to NaCl and KCl but not to LiCl or mannitol and accumulates Naþ (Choi et al. 2011). Some plants, especially halophytes, are known to use Naþ as a “cheap” osmolite. Although NSCCs are predicted to be likely candidates, no transporter has yet been reported as responsible for Naþ transport out of the vacuole into the cytosol. March 2014 | Volume 56 | Issue 3 | 231–249

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Salt tolerance Salinity tolerance in plants is well studied and reviewed elsewhere so this section is restricted to the general concept and interspecies difference of tolerance. Salt stress can be divided into osmotic stress and ionic stress. Osmotic stress initiates immediately after the roots encounter increased concentrations of salt and results in a reduced rate of shoot growth, whereas ionic stress initiates once Naþ accumulates to toxic levels in the shoots and results in senescence and death of old leaves (Munns and Tester 2008). Osmotic stress is perceived in the plant by an osmosensor, HISTIDINE KINASE1 (HK1) in the case of Arabidopsis and is transmitted to an mitogen‐activated protein kinase cascade (Silva and Geros 2009). In response to osmotic stress, a series of physiological changes take place such as transient water loss in leaf cells, long‐term reduction in cell expansion and division and stomatal closure, all of which lead to a decline in the rate of photosynthesis (Munns and Tester 2008). These changes are mainly mediated through the ABA and cytosolic Ca2þ signals, increased production of ROS and the concomitant increase of detoxifying enzyme activity (Munns and Tester 2008). Although the mechanism of Naþ sensing is largely unknown, tolerance to ionic Naþ is considered to be achieved by two major strategies: Naþ extrusion and Naþ compartmentalization (Munns and Tester 2008). Net Naþ concentrations in the cytoplasm of the shoot, where it exerts the major toxicity, is determined by the rates of influx into the root, efflux out of the root, xylem loading and unloading for long‐distance transport into the shoot, phloem loading for long‐distance transport back into the root, and influx into the vacuole for compartmentalization. Once Naþ is sequestrated (mainly into the vacuole, although the apoplast, ER, and Golgi bodies are the alternatives), “compatible solutes” such as sugars, proline, and glycine betaine are accumulated in the cytoplasm to maintain the osmotic balance (Kader and Lindberg 2010). Elevated levels of cytosolic Ca2þ and a pH increase in response to salinity‐induced ionic stress, rather than osmotic stress, are assumed to contribute to the activation of the SOS pathway for ionic homeostasis and consequent enhanced tolerance through extrusion and possibly sequestration of Naþ (Kader and Lindberg 2010). The mechanisms in plants to overcome salt stress vary considerably between species. Thellungiella halophila, a close relative of Arabidopsis, is a halophyte in contrast to Arabidopsis and has been reported to accumulate less Naþ during salt stress compared with Arabidopsis (Volkov et al. 2003). This has been explained by less influx of Naþ, not more efflux of Naþ, and the greater Kþ uptake selectivity over Naþ, resulting in better Naþ/Kþ ratios in T. halophila compared with Arabidopsis (Wang et al. 2006; Ghars et al. 2008). A similar trend in salt‐tolerance mechanisms has been observed in salt‐ tolerant and salt‐sensitive cultivars of rice (Horie et al. 2001; Malagoli et al. 2008). As described earlier, barley, a relatively salt‐tolerant species, has been reported to enhance salt tolerance through induction of HvHKT2;1 and the concomitant increase of Naþ translocation into the shoot, instead of reducing Naþ uptake (Mian et al. 2011). A halophytic ice plant has been evolved to develop specialized trichome cells called epidermal bladder cells and to sequestrate Naþ there under salt stress (Agarie et al. 2007). By contrast, it has been shown that a tropical halophyte Theobroma cacao positively absorbs Naþ under saline conditions and that increased Naþ/ March 2014 | Volume 56 | Issue 3 | 231–249

Kþ ratios result in increased plant performance (Gattward et al. 2012). Beneficial function of Naþ Sodium is known to be essential for plants which perform C4 or crassulacean acid metabolism (CAM) photosynthesis. The ionic effect, rather than the osmotic effect, of Naþ induces phosphoenolpyruvate carboxylase‐kinase (PEPCase‐k), which is involved in activation of the enzyme required for the first step of atmospheric CO2 fixation in Sorghum (Garcia‐Maurino et al. 2003). Similarly, a halophytic C3‐CAM species, ice plant, obtains carbon solely through C3 photosynthesis where it does not encounter salinity or drought; in contrast, salinity induces carbon acquisition through CAM photosynthesis in the dark (Winter and Holtum 2007). Moreover, a recent report has indicated that salinity induces photoprotective strategies through activation of nicotinamide adenine dinucleotide phosphate‐dependent malate dehydrogenase (NADP‐MDH) and NADP‐malic enzyme (NADP‐ ME), and that absence of salinity increases susceptibility to high light in ice plant (Gawronska et al. 2013). Induction of pyruvate uptake into plastids by Naþ in C4 plants has long been known (Ohnishi and Kanai 1987; Ohnishi et al. 1990) and a Naþ‐dependent pyruvate transporter, BILE ACID:SODIUM SYMPORTER FAMILY PROTEIN2 (BASS2), has been identified relatively recently (Furumoto et al. 2011). Pyruvate is an important metabolite for many biological processes in plants including the C4 photosynthesis and the methyl erythritol phosphate (MEP) pathway. BASS2 is localized at the chloroplast envelope membrane and although it is highly abundant in C4 plants, the orthologs are found in all of the land plants (Furumoto et al. 2011). This Naþ influx via BASS2 is coupled with NAþ/Hþ ANTIPORTER1 (NHD1) which exchanges Naþ with Hþ across the chloroplast envelop to establish an Naþ gradient necessary for pyruvate uptake (Furumoto et al. 2011). Although a certain function of Kþ is known to be replaceable by Naþ even in glycophytes such as enzymatic and osmotic regulation (Pilon‐Smits et al. 2009), some halophytic species positively use Naþ instead of Kþ to grow optimally under moderate salinity. It has been reported that Sesuvium portulacastrum accumulates a large amount of Naþ and this functions more effectively than Kþ in terms of cell expansion, leaf succulence, and shoot development in this halophyte (Wang et al. 2012). Another woody halophyte, Zygophyllum xanthoxylum, also accumulates Naþ and uses it for osmotic adjustment, which in turn improves photosynthetic activity (Ma et al. 2012). A specialized aquatic halophyte, Zostera marina, has been shown to utilize Naþ in order to transport nitrate and inorganic phosphate (Garcia‐Sanchez et al. 2000; Rubio et al. 2005).

Kþ AND Naþ HOMEOSTASIS Salt stress significantly influences various ion homeostasis such as Ca2þ, Kþ, NO3– as well as Naþ and results in reallocation of these ions to create a new and adjusted homeostasis. Due to the chemical similarity between Naþ and Kþ, Kþ homeostasis is severely influenced during salt stress. High Naþ concentrations in plants often cause Kþ‐deficiency symptoms and interrupt many physiological processes mediated by Kþ such as protein synthesis and enzymatic reaction, although the turgor function of Kþ can be largely replaced by Naþ. Maintenance of adequate www.jipb.net

Kþ and Naþ transport and signaling Naþ/Kþ ratios is considered to be vital for plant survival. One major cause of disturbed Naþ/Kþ ratios under salinity is that Naþ competes with Kþ for uptake sites in the plasma membrane‐localized transporters such as NSCCs and HKTs. In addition, membrane depolarization caused by Naþ results in decreased Kþ uptake through inward‐rectifying Kþ channels,

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making it thermodynamically unfavorable, and increased Kþ efflux through outward‐rectifying channels. Moreover, synthesis of compatible solutes in response to salt stress consumes a large amount of adenosine triphosphate (ATP) and leads to inhibited high‐affinity Kþ uptake, all of which result in increased Naþ/Kþ ratios (Shabala and Cuin 2007).

Figure 2. HAK5 expression and potassium (Kþ) and sodium (Naþ) accumulation in Arabidopsis under various NaCl concentrations (A) Chemiluminescence imaging of HAK5promoter::luciferase plants grown on indicated concentrations of NaCl in Kþ‐deficient (10 mmol/L KCl) and Kþ‐sufficient (1.75 mmol/L KCl) conditions. Three day old seedlings germinated on the control medium (1.75 mmol/L KCl) were transferred onto each medium and grown for 11 d prior to imaging. (B) Kþ concentrations in Kþ‐deficient and (C) Kþ‐sufficient conditions. (D) Naþ concentrations in Kþ‐deficient and (E) Kþ‐sufficient conditions. The wild‐type (Col‐0) plants were germinated and grown on each medium for 11 d, dried and extracted with HNO3 at 125 °C. Potassium and Naþ concentrations were determined on a flame atomic absorption spectrometer; refer to Adams et al. (2013) for more details. Statistically significant differences (P < 0.05) compared with the control conditions, according to one‐way ANOVA with the Bonferroni’s multiple comparison post‐test, are indicated as asterisks. DW, dry weight. www.jipb.net

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In order to improve Naþ/Kþ ratios under salinity, plants respond promptly to the increased concentrations of Naþ. In Arabidopsis, expression of several Kþ channels (KUP6, KUP11, SKOR, and AKT2/3) has been reported as salt‐responsive (Maathuis 2006). A Kþ transporter gene, CHX17, is also known to be induced in response to salinity, Kþ deficiency, and ABA (Cellier et al. 2004), suggesting that the Naþ signal regulates Kþ transporters for redistribution of Kþ and the improved Naþ/ Kþ ratio in plants. Monocotyledonous plants are generally known to have larger numbers of HKT transporters compared with dicotyledonous plants. Some of them such as rice OsHKT2;1 exhibit diverse modes of action including Naþ/Kþ symport and Naþ uniport according to the external concentrations of Naþ and Kþ. It is possible that HKT proteins significantly contribute to Kþ/Naþ homeostasis at least in monocotyledons (Jabnoune et al. 2009). A key signal to ameliorate the negative effects caused by salinity appears to be Ca2þ. Calcium has been shown to inhibit NSCCs, a major port of Naþ entry (Demidchik and Tester 2002) and Naþ‐induced Kþ efflux (Shabala et al. 2006), resulting in improved Naþ/Kþ ratios. It is speculated that the Ca2þ‐ dependent CBL–CIPK network may play a role in connecting Kþ uptake and Naþ homeostasis under salinity (Luan et al. 2009). That is, as described in the earlier sections, the CBLs–CIPK23 complexes activate AKT1 to induce Kþ uptake and the analogous CBL4/SOS3–CIPK24/SOS2 complex activates SOS1 to mediate Naþ efflux (Amtmann and Armengaud 2007). Synthesized compatible solutes and polyamines are also suggested to improve Naþ/Kþ ratios by inhibition of NSCCs and a consequent decline in membrane depolarization and Kþ efflux (Shabala and Cuin 2007). A few other factors have recently been reported and assumed to be involved in Kþ/Naþ homeostasis under salinity stress. An AAA‐type ATPase, SUPPRESSOR OF Kþ TRANSPORT GROWTH DEFECT1 (SKD1), has been identified in the halophyte ice plant as being involved in salt tolerance (Jou et al. 2004). SKD1 is considered to function in protein sorting and to be a positive regulator of salinity tolerance via maintenance of Kþ/ Naþ homeostasis in both ice plant and Arabidopsis (Jou et al. 2006; Ho et al. 2010). A recent report has proposed a potential regulatory mechanism of SKD1 (Chiang et al. 2013); however, the mechanism of SKD1‐dependent salt tolerance awaits further elucidation. Ethylene has also been suggested to contribute to the mechanism for soil‐salinity tolerance. It has been demonstrated previously that salinity induces ethylene signaling and causes developmental defects through DELLA proteins (Achard et al. 2006). Another line of support for the involvement of ethylene comes from the finding that an ethylene‐related transcription factor, ETHYLENE‐INSENSITIVE3 (EIN3), activates an ERF transcription factor ETHYLENE AND SALT INDUCIBLE1 (ESE1) by direct binding and that subsequent binding of ESE1 to salt‐related genes enhances salt tolerance in Arabidopsis (Zhang et al. 2011a). Recent reports have indicated that the salt‐induced ethylene signal promotes DELLA‐ independent RBOHF‐dependent ROS accumulation in the root stele, which, in turn, reduces Naþ concentrations in xylem sap and results in salt tolerance due to reduced levels of Naþ in the shoot (Jiang et al. 2012, 2013). Simultaneously, ethylene‐induced, RBOHF‐independent (RBOHC‐dependent) ROS accumulation induces HAK5 expression and Kþ accumulation, leading to an improved Naþ/Kþ ratio (Jiang et al. 2013). March 2014 | Volume 56 | Issue 3 | 231–249

As described, maintenance of Kþ/Naþ homeostasis in an environment of salinity is important for plant development and survival. In order to assess the gene expression of a high‐ affinity Kþ transporter, Arabidopsis HAK5, under salinity, HAK5promoter::luciferase plants were grown in various concentrations of NaCl and the luciferase activity was observed (Figure 2A). Expression of HAK5 is known to be induced in response to Kþ deficiency in the root (Qi et al. 2008). Interestingly, strong luciferase activity was also observed in the aerial part of the Kþ‐deficient plants and this aerial activity gradually decreased with the increasing concentrations of NaCl whereas the root activity was constant, or possibly intensified. By contrast, a dramatic increase in luciferase activity was observed in the Kþ‐sufficient plants upon NaCl treatment and the activity was restricted, almost exclusively, in the root at NaCl concentrations below 50 mmol/L. Although quantification of the endogenous HAK5 levels is required to draw a conclusion, these data imply that high concentrations of Naþ cause seeming Kþ deficiency to induce HAK5 expression. These data also imply that the Kþ requirement under Kþ deficiency in the aerial part of the plant decreases with increased concentrations of Naþ, possibly due to compensation. This inhibitory effect of NaCl on Kþ‐deficiency‐induced HAK5 expression has previously been reported in the root of hydroponically grown adult Arabidopsis plants (Nieves‐ Cordones et al. 2010). Potassium and Naþ concentrations were also determined in these nutritional conditions. Potassium concentrations decreased upon NaCl treatment and this decrease was observed as low as 10 mmol/L NaCl in the Kþ‐ sufficient plants (Figure 2C), whereas it was not statistically significant until 50 mmol/L NaCl in the Kþ‐deficient plants (Figure 2B). Similarly, Naþ accumulation was observed at lower NaCl concentrations in the Kþ‐sufficient plants (Figure 2E) than in the Kþ‐deficient plants (Figure 2D). Sodium concentrations were similar between Kþ‐sufficient and ‐deficient plants in the absence of NaCl. This contrasts with a finding in rice that Kþ‐ deficient plants accumulate more Naþ than Kþ‐sufficient plants (Shankar et al. 2013), suggesting the existence of species‐ dependency. Taken together, these results seem to highlight that there are multiple phases in the regulation of salinity responses depending on Kþ availability that cannot be simply explained by mere external Naþ concentrations or a standardized Naþ/Kþ ratio. Future investigation on Kþ and Naþ concentrations at the organ and cellular levels would provide further insight into the finer points of regulation of Kþ/ Naþ homeostasis in plants.

ACKNOWLEDGEMENTS We thank Dr. Aya Hayaishi and Ms. Takae Miyazaki for technical assistance. Special thanks go to Dr. Michael Adams for comments and discussion on the manuscript. This work was supported by funding from RIKEN.

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