Journal of Plant Physiology 171 (2014) 743–747

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Physiology

Organelle-localized potassium transport systems in plants夽 Shin Hamamoto, Nobuyuki Uozumi ∗ Department of Biomolecular Engineering, Graduate School of Engineering, Tohoku University, Aobayama 6-6-07, Sendai 980-8579, Japan

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Article history: Received 7 August 2013 Received in revised form 6 September 2013 Accepted 6 September 2013 Available online 3 March 2014 Keywords: Organelle potassium channels Vacuolar channels TPK Cyanobacteria

a b s t r a c t Some intracellular organelles found in eukaryotes such as plants have arisen through the endocytotic engulfment of prokaryotic cells. This accounts for the presence of plant membrane intrinsic proteins that have homologs in prokaryotic cells. Other organelles, such as those of the endomembrane system, are thought to have evolved through infolding of the plasma membrane. Acquisition of intracellular components (organelles) in the cells supplied additional functions for survival in various natural environments. The organelles are surrounded by biological membranes, which contain membrane-embedded K+ transport systems allowing K+ to move across the membrane. K+ transport systems in plant organelles act coordinately with the plasma membrane intrinsic K+ transport systems to maintain cytosolic K+ concentrations. Since it is sometimes difficult to perform direct studies of organellar membrane proteins in plant cells, heterologous expression in yeast and Escherichia coli has been used to elucidate the function of plant vacuole K+ channels and other membrane transporters. The vacuole is the largest organelle in plant cells; it has an important task in the K+ homeostasis of the cytoplasm. The initial electrophysiological measurements of K+ transport have categorized three classes of plant vacuolar cation channels, and since then molecular cloning approaches have led to the isolation of genes for a number of K+ transport systems. Plants contain chloroplasts, derived from photoautotrophic cyanobacteria. A novel K+ transport system has been isolated from cyanobacteria, which may add to our understanding of K+ flux across the thylakoid membrane and the inner membrane of the chloroplast. This chapter will provide an overview of recent findings regarding plant organellar K+ transport proteins. © 2014 Elsevier GmbH. All rights reserved.

Introduction K+ channels reside not only in the plasma membrane, but also in the membranes of intracellular organelles such as vacuoles, endoplasmic reticulum, mitochondria and chloroplasts. K+ channels in intracellular organelles participate in the regulation of cellular volume, pH, in cellular signaling and in the storage of nutrients (Lebaudy et al., 2007). Because of the large volume of the plant vacuole (Becker, 2007), K+ channels in the vacuole membrane are important contributors to cytosolic ion homeostasis. Early patchclamp studies identified three classes of vacuolar cation channels, slow-activating vacuolar (SV) channels, vacuolar K+ (VK) channels and fast-activating vacuolar (FV) channels (see also Ahmad and Maathuis, 2014; Pottosin and Dobrovinskaya, 2014). Subsequent molecular studies led to the isolation of genes encoding SV (Peiter

Abbreviations: SV, slow-activating vacuolar channel; VK, vacuolar K+ channel; FV, fast-activating vacuolar channel; CHO, Chinese hamster ovary cells; TPK, two-pore K+ channels; Snf1-related protein kinase 2, OST1/SnRK2E/SnRK2.6; ABA, abscisic acid; DGDG, digalactosyldiacylglycerol. 夽 This article is part of a Special Issue entitled “Potassium effect in plants”. ∗ Corresponding author. E-mail address: [email protected] (N. Uozumi). 0176-1617/$ – see front matter © 2014 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.jplph.2013.09.022

et al., 2005) and VK channels (Gobert et al., 2007), as described below, but the genes encoding FV channels have not yet been identified. Fifteen genes encoding K+ channels have been identified in the Arabidopsis thaliana genome (Mäser et al., 2001; Véry and Sentenac, 2003; Dreyer and Uozumi, 2011; Uozumi and Dreyer, 2012; see also Anschütz et al., 2014; Demidchik, 2014) and these channels were originally classified in three groups (TPK, Kir and voltage dependent K+ channels as described below), based on their protein structure (Uozumi et al., 1998; Durell et al., 1999). The seven voltage dependent K+ channels consist of six transmembrane spanning segments and are localized to the plasma membrane, whereas the five two-pore K+ channels (TPK) are integral to organellar membranes, with exception of the plasma membrane-localized TPK4 (Becker et al., 2004; Maîtrejean et al., 2011). One gene encoding a Kir (K+ inward rectifier)-like K+ channel is present in the Arabidopsis genome (Voelker et al., 2010). However, this channel homolog is unlikely to function as a channel due to a partial deletion of the pore and transmembrane domains required for activity in canonical TPK channels (Rocchetti et al., 2012; Sharma et al., 2013). To understand machinery and function of photosynthesis performed in chloroplasts in higher plant cells, unicellular photoheterotrophic cyanobacteria provide an important model for chloroplasts because plastids arose from an internalized ancestral

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cyanobacterium; a process referred to as symbiogeneses (Cavalier-Smith, 2000). Cyanobacteria contain intracellular thylakoids for oxygenic photosynthesis, similar to those of the chloroplasts in higher plants and algae. Synechocystis sp. PCC 6803 was the first photosynthetic organism for which the complete genome sequence was determined (Kaneko et al., 1996). The existence of various K+ transport proteins in Synechocystis indicates that they are likely to perform distinct physiological roles. In this they contribute to the organism’s survival and its adaptation to the frequently changing environment experienced by photosynthetic bacteria with their dependence on the light/dark cycle accompanied by temperature shifts and dry/wet phases. For details on the role of K+ in photosynthetic reactions see Zörb et al. (2014).

Modulation of VK in guard cells The phytohormone abscisic acid (ABA) triggers an increase of cytosolic Ca2+ in guard cells and initiates a signaling cascade that results in stomatal closure (Ache et al., 2000;Fig. 1; see also Blatt et al., 2014). Stomatal closure is mediated by the release of K+ alongside with anions from the vacuole into the cytoplasm via vacuolar membrane-localized K+ channels followed by the extrusion of K+ across the plasma membrane of the guard cells (Becker et al., 2003). This leads to a decrease in osmotic pressure inside the cells and water is released from the guard cell. The resulting decrease in turgor pressure causes shrinking of the guard cells, which leads to stomatal closure. Early patch-clamp experiments on guard cell vacuoles from several plants identified the voltageindependent K+ channel conductance as VK channel activity (Ward and Schroeder, 1994; Pottosin et al., 2003). The K+ current was highly selective for K+ and activated by cytosolic Ca2+ . The ubiquitously expressed vacuolar TPK channel in A. thaliana, TPK1, was electrophysiologically characterized using tpk1 knockout plants, tpk1-overexpressing plants and heterologous expression in yeast (Gobert et al., 2007). Their ion selectivity features and activation manner are consistent with the previously observed VK channel current (Fig. 1). Moreover, ABA-treated tpk1 knockout mutant plants exhibited a much slower decrease in leaf conductance compared to wild type, which can be explained by a delayed response of stomatal closure (Gobert et al., 2007). In contrast, the wild-type plants and the TPK1-overexpressers showed a faster decrease in leaf conductance, indicating that the stomata were properly closing. Taken together, these results are consistent with TPK1 being involved in the enhancement of stomatal closure via K+ release from the vacuole in guard cell. In guard cells, several kinases and phosphatases play a crucial role in stomatal opening/closure. One of the primary de/phosphorylation targets are ion channels since they are effector molecules controlling stomatal aperture. In in vivo assays, the guard cell-specific ABA-dependent kinase, OST1/SnRK2E/SnRK2.6 (Snf1-related protein kinase 2) activates an S-type slow anion channel called SLAC1 (slow anion channel associated 1) in the plasma membrane by phosphorylating an N-terminal serine at position 120 (Mustilli et al., 2002; Yoshida et al., 2002; Vahisalu et al., 2010). SnRK2.6 is also potentially able to phosphorylate the threonine at position 306 in the C-terminal cytosolic region of the plasma membrane K+ channel KAT1, resulting in the shutdown of KAT1mediated K+ uptake (Sato et al., 2009). Two calcium dependent protein kinases, CPK3 and CPK6 have also been identified as activators of SLAC1 (Mori et al., 2006; Brandt et al., 2012; Scherzer et al., 2012). Similarly, the vacuole-localized K+ channel TPK1 is a target of phosphorylation by CPK3 (Latz et al., 2013;Fig. 1). The 14-3-3 proteins can associate with phosphorylated serines and threonines in their target consensus binding motif (Latz et al., 2007). Phosphorylation of Ser42 in the cytosolic N-terminus of

TPK1 is strongly induced by salt stress, and the open probability is increased by interaction of the cytoplasmic N-terminal region with 14-3-3 proteins (Latz et al., 2007; Voelker et al., 2010; Latz et al., 2013). Interestingly, tpk1 and cpk3 knockout plants exhibit decreased germination rates compared with wild-type plants and a reintroduction of TPK1 into tpk1 knockout plants complements the loss of function phenotype (Latz et al., 2013). In rice, OsTPKa and OsTPKb are found in the membranes of different vacuoles even though their overall amino acid sequence is highly similar (Isayenkov et al., 2011). TPKa is localized mainly in the membranes of the large central lytic vacuoles and TPKb is expressed in the membranes of smaller protein storage vacuoles. The targeting information of TPKa and TPKb is contained in the sequence of their C-terminus. The SV channel in the vacuole membrane encoded by AtTPC1 (tandem pore calcium channel 1) shows slowly activated K+ and Ca2+ transport activity after an increase in cytosolic Ca2+ (Peiter et al., 2005). The existence of two EF-hand motifs in the C-terminal regions likely accounts for its Ca2+ dependence. TPC1 plays a role in calcium release from the vacuole into the cytoplasm (DadaczNarloch et al., 2011). TPC1 appears to be involved in responses to elevated extracellular Ca2+ (Islam et al., 2010). In addition, a TPC1 loss of function mutant, attpc1 is less sensitive to inhibition of seed germination by ABA (Peiter et al., 2005). In contrast, a different study concluded that ABA and methyl jasmonate are not involved in AtTPC1 function (Islam et al., 2010). Exposure of plants to abiotic stress conditions like hyperosmotic shock, cold or heat treatment, which trigger an elevation of cytosolic Ca2+ concentration, weakly induces phosphorylation of TPK1. Sequence analysis of Arabidopsis TPK channel proteins shows one or two EF hand motifs in the cytoplasmic C-terminal domain of AtTPK1, AtTPK2 and AtTPK3. In contrast, AtTPK4 lacks EF hands and AtTPK5 exhibits only low similarity to the consensus sequence of the canonical EF hand motif (Gobert et al., 2007). The presence of this motif indicates an ability to bind cytoplasmic Ca2+ at physiological concentrations (0.05–1 ␮M).

Functional characterization of VK In higher plants, patch-clamp recordings made it possible to evaluate the activities of three different channels, SV, FV, and VK, in the guard cell vacuolar membrane (see also Ahmad and Maathuis, 2014; Pottosin and Dobrovinskaya, 2014). The cation current profiles were initially determined in situ in the presence of interfering background conductance or “ionic noise”. In such cases, heterologous expression in Xenopus oocytes, which possess few endogenous ion channels, is a powerful tool for recording ion channels. However, vacuolar membrane-localized membrane proteins are not always sorted into the oocyte plasma membrane, due to the existence of sorting signals that are responsible for localization to the vacuolar membrane. An alternative strategy for the characterization of plant channels is expression in Escherichia coli. Since bacteria like E. coli have no organelles, the heterologously expressed plant membrane proteins must be sorted into the plasma membrane. An E. coli mutant that is deficient in K+ uptake has been used as a functional expression system for K+ uptake channels and transporters (Uozumi et al., 1998; Uozumi, 2001). By use of this system, the K+ uptake activity of tobacco NtTPK1 and Arabidopsis AtTPK1, 2, 3 and 5 has been elucidated (Hamamoto et al., 2008a; Isayenkov and Maathuis, 2013). Yeast resembles plant cells with respect to the presence of a vacuole. Hence, a number of vacuolar proteins including transporters from plant cells have been characterized using the budding yeast Saccharomyces cerevisiae (Gaxiola et al., 1999; Liu et al., 2003; Yamaguchi et al., 2003). Budding yeast have a large central vacuole, which occupies more than 80% of the cellular

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Fig. 1. Schematic model of ion channels involved in stomatal closure (left) and topology of the interaction between TPK1 and 14-3-3 proteins (right).

volume, and performs similar functions to the vacuole in plant cells. Furthermore, in order to decrease ionic noise, specific endogenous genes can be easily inactivated in a targeted manner. One limitation of using yeast in patch-clamp experiments is the small size of the haploid yeast cells. To overcome this problem, the much larger cells of a S. cerevisiae tetraploid strain were successfully used for patchclamp recording of the yeast vacuole cation conductance (Bertl and Slayman, 1990), and of AtTPK1 expressed in the yeast vacuolar membrane (Bihler et al., 2005). As an alternative method to patchclamp recording of ion channels in the yeast vacuole, (Yabe et al., 1999) developed the yeast enlargement procedure, which resulted in haploid S. cerevisiae cells of approximately 20 ␮m diameter. They used this method to evaluate the V-type ATPase in yeast vacuole membranes (Yabe et al., 1999). These giant yeast cells were also used for the characterization of plant vacuole-associated protonpumping pyrophosphatase of mung bean (Vigna radiata; Nakanishi et al., 2003). The giant yeast cell method was applied to study the tobacco vacuolar-localized K+ channel NtTPK1 from N. tabacum cv. SR1 (Hamamoto et al., 2008a, 2008b). NtTPK1 is strongly activated at acidic cytosolic pH and slightly activated by elevated cytosolic Ca2+ , a novel property for plant K+ channels. Tobacco BY-2 culture cells are a useful system to study physiological processes and responses. Multiple alleles of TPK1 were isolated from BY-2 cells, some of which contained amino acid changes in the GYG signature of the second pore region, but are still functional (Hamamoto et al., 2008a). Additional genes encoding K+ channels have been cloned from tobacco; the plasma membrane-localized outwardly rectifying K+ channel NTORK, and the vacuolar membrane-located K+ channel NtTPK1, which is different from the NtTPK1 characterized by Hamamoto et al. (2008b). Both are synchronously induced during cell division (Sano et al., 2009). During cell elongation, an increase of K+ uptake occurs to generate turgor pressure in the cell, whereas K+ uptake is not required for cell division (Sano et al., 2009). Ktr transporter-mediated osmoregulation in cyanobacteria as a chloroplast model Synechocystis is a moderately halotolerant cyanobacterium, so suitable for studying the acclimation mechanism and process of

Fig. 2. The cyanobacterium Synechocystis sp. PCC 6803 and chloroplasts in Arabidopsis thaliana contain K+ channels and transporters.

osmoadaptation as well as intracellular ion homeostasis. Because it is a unicellular organism, Synechocystis cells are exposed directly to defined environmental stress conditions, which is very difficult to duplicate in chloroplast studies in plants (Fig. 2). Comparison of the genomes of Synechocystis and E. coli shows that three types of K+ transport systems, Kdp, Ktr (=Trk/HKT) and K+ channels including SynK are found in both microorganisms (Uozumi and Dreyer, 2012). Synechocystis possesses all types of them except for Kup (K+ uptake transporter), which is present in plants like A. thaliana. All Kdp, Ktr (=Trk/HKT) and K+ channels share a common basic membrane structure and ion selective pore formation (for more details on plant HKTs see also Benito et al., 2014; Nieves-Cordones et al., 2014; Véry et al., 2014).

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Cyanobacteria can adapt to high NaCl concentrations and to daily fluctuations of the osmolarity in its environment. A K+ transport system in cyanobacteria is involved in the early steps of this osmoadaptation. The Ktr system mediates K+ uptake and its activity is induced by an increase in the concentration of Na+ outside the cell (Matsuda et al., 2004; Fig. 2). The crucial subunit, KtrB (slr1509) belongs to the family of Trk/Ktr/HKT, Kdp and K+ channels. The Ktr system consists of the cytosolic components of KtrA and KtrE together with KtrB. KtrA encodes an NAD-binding peripheral membrane protein, while the KtrE protein has digalactosyldiacylglycerol (DGDG) synthase activity (Awai et al., 2007; Sakurai et al., 2007). Ktr has a fourfold-repeated membrane-pore-membrane motif and several residues help to reinforce its structure and function (Kato et al., 2001). The well-conserved His residue located in the second pore region is essential for the K+ uptake activity (Zulkifli and Uozumi, 2006). A positively-charged residue (R262) helps to sustain the transport by electrostatic interaction with two negatively-charged residues (E247 and D261; Zulkifli et al., 2010). The best-conserved positively-charged residues occur in the middle of the last transmembrane segment of Ktr/Trk/HKT-type transporters. Removal of the positive charge of Synechocystis KtrB results in loss of K+ transport activity. This demonstrates the necessity of the positive charge at this site for function (Kato et al., 2007). Since the positivelycharged residue is absent in K+ channels, it may be one of the determinants for the nature of the transporters. However, conversion from transporter to channel through neutralization of the positive residue in vivo was not successful for KtrABE or wheat HKT (Kato et al., 2007). The positive charge may be required for the electric interaction with the conserved negatively-charged residue in the fourth pore region. The possible electrostatic interactions between conserved charged residues in Ktr/Trk/HKT transporters predicted from the atomic-scale model developed by Durell et al. (1999) contribute to the stabilization of the conformation of the proteins.

Functional identification of K+ channels in cyanobacteria The Synechocystis genome contains at least five copies of K+ channel homologous genes. Two channels, SynK (KchC) and SynCaK have been functionally characterized and their expression pattern determined. SynK (slr0498) is a Shaker-type K+ channel, with six membrane-spanning segments containing a voltage sensing domain (Zanetti et al., 2010; Checchetto et al., 2012; Fig. 2). Expression in E. coli and in the mammalian CHO (Chinese Hamster Ovary) cells revealed that SynK functions as a K+ selective channel. SynK resides both in the thylakoid and in the plasma membrane in Synechocystis. Interestingly, the sequence of the pore forming region of SynK is homologous to the first half of the pore region of TPK3, and immunodetection with an anti-TPK3 antibody showed the presence of TPK3 in the thylakoid membrane of chloroplasts in Arabidopsis. This indicates that there is a common ancestry of K+ channels in cyanobacteria and higher plants. The SynCaK (sll0993) channel shows sequence homology to MthK, a Ca2+ -activated K+ channel of Methanobacterium thermoautotrophicum (Genbank accession no. O27564). This channel possesses a unique carboxyl-terminal cytosolic domain called RCK (regulator of the conductance of K+ ), which is a regulatory component for Ca2+ binding and unbinding (Jiang et al., 2002). Carraretto et al., 2013 determined by patch-clamp recording using the animal CHO cell expression system, that Ca2+ -activation of the K+ conductance of SynCaK from Synechocystis is similar to that of MthK (Fig. 2). A major amount of SynCaK protein was isolated from the plasma membrane fraction in Synechocystis. The activity of SynCaK is likely to be unaffected by osmotic or salt stress, but probably plays a role in the

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Organelle-localized potassium transport systems in plants.

Some intracellular organelles found in eukaryotes such as plants have arisen through the endocytotic engulfment of prokaryotic cells. This accounts fo...
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