© 2014 Scandinavian Plant Physiology Society, ISSN 0031-9317

Physiologia Plantarum 2014

MINIREVIEW

Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance Sergey Shabalaa,∗ and Igor Pottosina,b a b

School of Agricultural Science, University of Tasmania, Hobart, Tas 7001, Australia ´ ´ Centro Universitario de Investigaciones Biomedicas, Universidad de Colima, Colima, Mexico

Correspondence *Corresponding author, e-mail: [email protected] Received 14 October 2013; revised 15 December 2013 doi:10.1111/ppl.12165

Intracellular potassium homeostasis is a prerequisite for the optimal operation of plant metabolic machinery and plant’s overall performance. It is controlled by K+ uptake, efflux and intracellular and long-distance relocation, mediated by a large number of K+ -selective and non-selective channels and transporters located at both plasma and vacuolar membranes. All abiotic and biotic stresses result in a significant disturbance to intracellular potassium homeostasis. In this work, we discuss molecular mechanisms and messengers mediating potassium transport and homeostasis focusing on four major environmental stresses: salinity, drought, flooding and biotic factors. We argue that cytosolic K+ content may be considered as one of the ‘master switches’ enabling plant transition from the normal metabolism to ‘hibernated state’ during first hours after the stress exposure and then to a recovery phase. We show that all these stresses trigger substantial disturbance to K+ homeostasis and provoke a feedback control on K+ channels and transporters expression and posttranslational regulation of their activity, optimizing K+ absorption and usage, and, at the extreme end, assisting the programmed cell death. We discuss specific modes of regulation of the activity of K+ channels and transporters by membrane voltage, intracellular Ca2+ , reactive oxygen species, polyamines, phytohormones and gasotransmitters, and link this regulation with plantadaptive responses to hostile environments.

Introduction Potassium is an essential and the second most abundant mineral nutrient in plants. Potassium concentration in the bulk soil solution may vary several orders of magnitude ranging between approximately 0.025 and 5 mM (1 to 200 ppm) (Marschner 1995, Maathuis 2009). At the same time, plants usually accumulate between 2 and 10% of potassium per dry weight basis, or approximately

50–250 mM (Marschner 1995), and are capable to maintain rather constant cytosolic K+ content, typically within 100 to 200 mM range (Leigh and Wyn Jones 1984, Britto and Kronzucker 2008). This is achieved by the orchestrated regulation of a sophisticated network of potassium transport systems. These include the Shakertype and ‘two-pore’ potassium channels; various types of potassium-permeable non-selective cation channels; and KUP/HAK/KT, HKT and K+ /H+ transporters (V´ery

Abbreviations – ABA, abscisic acid; ABC, ATP-binding cassette; ER, endoplasmic reticulum; GORK, outward-rectifying depolarization-activated K+ channel; HO, haem oxygenase; H2 O2 , hydrogen peroxide; NOX, NADPH-oxidase; O2 – , superoxide radical; OH , hydroxyl radical; PAs, polyamines; PCD, programmed cell death; PIP, plasma membrane intrinsic proteins; PM, plasma membrane; QTL, quantitative trait loci; ROS, reactive oxygen species; ROSIC, ROS-induced ion conductance; sGC, soluble guanylate cyclase; SKOR, stelar K+ -selective outward rectifying channel. •

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and Sentenac 2003). The essentiality of potassium is related to its multiple roles in plants. Among these are cell maintenance of cell turgor pressure and cell elongation, osmoregulation, leaf and stomata movements, tropisms, enzyme activation, phloem solute transport, cation/anion balancing, control of membrane polarization, cytoplasmic pH regulation, chloroplast structure and functioning, protein and starch synthesis and energy conservation across membranes. As most of these processes are directly involved in plant adaptation to hostile environment, potassium uptake, transport and homeostasis play a central role in conferring abiotic and biotic stress tolerance in plants. In this work, we discuss molecular mechanisms and messengers mediating potassium transport and homeostasis focusing on four major environmental stresses: salinity, drought, flooding and biotic factors.

Potassium transport and homeostasis under stress conditions Drought Drought stress severely limits agricultural productivity worldwide and is the most critical threat to the world’s food security (Farooq et al. 2009). The severity of drought is unpredictable as it depends on many factors such as occurrence and distribution of rainfall, evaporative demands and moisture storing capacity of soils (Wery et al. 1994). Over 50% of the Earth’s surface area, including the vast majority of agricultural lands is vulnerable to drought. Based on FAO statistics, total Australia wheat yield in 2006 dropped by 46% (www.fao.org/docrep/017/aq191e/aq191e.pdf), costing economy over $6 billion. The same source has estimated that US retail food prices will increase between 3 and 4% in 2013 as a consequence of extreme drought in the United States wheat belt in 2012. Maintaining adequate K+ plant nutritional status is vital in adaptation to drought (Cakmak 2005), and there is increasing evidence that plants suffering from drought have a larger internal requirement for K+ (Cakmak and Engels 1999). At the same time, K+ uptake in plants is significantly reduced by the drought stress (Hu and Schmidhalter 2005). This reduction is attributed to both decreased mobility of K+ in the soil, reduced transpiration rate and impaired activity of root membrane transporters (Hu and Schmidhalter 2005, Hu et al. 2013). Numerous studies have shown that application of K+ fertilizer mitigates the adverse effects of drought on plant growth (reviewed in Hu and Schmidhalter 2005). Multiple mechanisms contribute to this mitigation. These include: (1) better stomata control and reduced transpiration under drought conditions,

(2) efficient osmotic adjustment and maintenance of the turgor pressure, (3) prevention of droughtinduced accumulation of reactive oxygen species (ROS), (4) improved water use efficiency and control of long-distance water transport in plants and (5) maintaining optimal energy status, leaf photochemistry and intracellular ionic homeostasis and charge balance. Some of these aspects are discussed in more detail below. Rapid osmotic adjustment is absolutely critical to maintain cell turgor and support expansion growth of roots and shoots. In this context, accumulation of K+ plays a pivotal role in this process, contributing on average between 35 and 50% of the cell osmotic potential in crops (e.g. Shabala and Lew 2002, Chen et al. 2007b). In wheat, differences in shoot K+ content accounted for 84% of the difference in osmotic adjustment among K-sufficient genotypes, while for plants without K+ fertilization, K+ accumulation in leaves contributed only to 17–28% of osmotic adjustment (Damon et al. 2011). Potassium fertilization increased osmotic adjustment and improved water relations in a wide range of crop species (Pier and Berkowitz 1987, Ashraf et al. 2001, Sangakkara et al. 2000). Drought stress management requires the hydraulic uncoupling of guard cells from the surrounding mesophyll cells (Becker et al. 2003), and Shaker-like depolarization-activated outward rectifying K+ (GORK in Arabidopsis) channels at the guard cells plasma membrane play a crucial role in this process. Excised rosette leaves from Arabidopsis gork-1 mutant plants display increased transpirational water loss (Hosy et al. 2003), and adult akt1 plants displayed lower transpiration and less water consumption than wild-type plants (NievesCordones et al. 2012).Thus, it appears that the cells lacking a pathway for the rapid K+ release from the guard cells are not capable to close stomata when challenged by drought and, thus, are compromised. Consistent with this notion, the stress hormone abscisic acid (ABA) induced in plants under drought conditions was shown to upregulate both GORK channels’ activity and expression at transcriptional level (Jeannette et al. 1999, Becker et al. 2003). Interestingly, upregulation of GORK was manifested within 2 min of ABA application and persisted for 24–48 h following ABA removal. This indicates that even a very short pulse of ABA is sufficient to trigger ABA-signal transduction and optimize the stress response (Becker et al. 2003). Also, disruption of AKT1, a major route for K+ uptake by guard cells, enhanced stomatal closure in response to ABA and improved drought tolerance in plants (Nieves-Cordones et al. 2012). Another water-saving strategy enabling plant’s survival under drought condition is a concurrent downregulation of plant water channels – aquaporins Physiol. Plant. 2014

(Smart et al. 2001). The mRNA expression levels of plasma membrane intrinsic proteins (PIPs) and K+ channel/transporters such as AKT1, HAK1 and HKT1 responded similarly to water deprivation in rice (Liu et al. 2006). It was suggested that this downregulation may result in a reduced membrane water permeability and may promote cellular water conservation during periods of dehydration stress. Interestingly, root hydraulic conductivity was reduced in plants treated with K+ -channel blocker Cs+ , suggesting that fluxes of K+ are coupled to activity of water channels in the plasma membrane (Tazawa et al. 2001). Potassium availability also appears to be crucial for regulation of the hydraulic conductance of the xylem. It has been shown that the hydraulic conductance of xylem can be modulated by changes in the xylem sap cation concentration because of ion-mediated volume changes of pectins in pit membranes (Zwieniecki et al. 2001), and that K+ may be central to this process (Oddo et al. 2011, Trifilo et al. 2011). Change in the xylem sap K+ concentration from 3 to 12 mM has resulted in a 30 to 60% increase in stem hydraulic conductance in Laurus nobilis (Nardini et al. 2010), and increased xylem sap K+ in this species has resulted in a 45% increase in transpiration rate in this species (Oddo et al. 2011). Also, xylem cavitation is a common event in droughtstressed plants, and increased K+ availability was shown to reduce its occurrence (Trifilo et al. 2011). Production of ROS such as superoxide radical (O2 – ), hydrogen peroxide (H2 O2 ) and hydroxyl radical (OH ) increase dramatically in drought-affected plants (Cakmak 2005, Waraich et al. 2011). Several factors contribute to this process. First, drought inhibits or slows down photosynthetic carbon fixation by limiting the entry of CO2 into the leaf and causing disturbances to carbohydrate metabolism (Apel and Hirt 2004, Waraich et al. 2011), thus compromising plant’s ability to handle the full amount of the absorbed light. Drought stress may also directly activate superoxide-generating NADPHoxidases (NOXs) localized in the plasma membranes (Jiang and Zhang 2002). In addition, under drought conditions chloroplasts lose high amounts of K+ to further depress photosynthesis (Sen Gupta and Berkowitz 1987), further enhancing ROS formation. All these factors result in a severe oxidative damage to chloroplasts. Improvement of potassium nutritional status of plants can greatly lower the ROS production by reducing the activity of NADPH oxidases and maintaining photosynthetic electron transport (Cakmak 2005). To enable plants access to potassium, several types of K+ transporters were shown to be induced by the drought stress at the transcriptional level. KUP6, a high-affinity K+ transporter from the KUP/HAK/KT family, was recently •

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shown to be responsive to the drought stress (Osakabe et al. 2013). This transporter is expressed in the root epidermis and is believed to mediate K+ uptake under K+ -starvation conditions. KUP6 was also found to be upregulated in Arabidopsis suspension cells by ABA (Bohmer and Schroeder 2011). The protein kinase SNF1related protein kinases 2E (SRK2E), a key component of ABA signaling, interacted with and phosphorylated KUP6, suggesting that KUP functions are regulated directly via an ABA signaling complex (Osakabe et al. 2013). Drought stress has also resulted in an increased amount of transcript for AKT2 channel (Lacombe et al. 2000). AKT2 is known to be predominantly expressed in plant’s vasculature (V´ery and Sentenac 2003) and plays a critical role in long-distance K+ transport in plants. Salinity Nearly 10% of the land surface and 50% of all irrigated land in the world are affected by salinity, resulting in the annual losses in agricultural production being in excess of US$ 12 billion (Ruan et al. 2010, Flowers et al. 2010). Salinity problem is further exacerbated by the conversion of agricultural land into other uses in urban areas, increasing the competition between crops and energy plant species, and a requirement to increase global food production by about 70% to meet the 2050 challenge of feeding 9.3 billion population (Shabala 2013). As mentioned in the section Introduction, cytosolic potassium homeostasis is central to normal cell metabolism and functioning. At the same time, numerous studies have reported a dramatic decline in plant K+ content, both in roots and shoots, under saline conditions (Aziz and Khan 2001, Chen et al. 2005, Tavakkoli et al. 2011). Many studies have also suggested the existence of a strong positive correlation between shoot K+ content and plant salinity tolerance (e.g. Garthwaite et al. 2005, Chen et al. 2005), and roots ability to retain K+ was proven to be one of the key traits conferring salinity stress tolerance in barley (Chen et al. 2005, 2007a), wheat (Cuin et al. 2008, 2011) and lucerne (Smethurst et al. 2008). It was also shown that supply of K+ fertilizers has a beneficial impact on plant performance under saline conditions (Umar et al. 2011, Siringam et al. 2013). Detrimental effects of salinity are usually attributed to one of following three key factors: (1) reduced water availability due to osmotic effects caused by the presence of high salt concentrations in the soil solution, (2) Na+ toxicity to cell metabolism and (3) oxidative stress damage resulting from increased ROS production under saline conditions. Potassium appears to be ultimately involved in mitigating detrimental effects of each of these factors.

As previously commented on, potassium is a major osmoticum that is contributing on average between 35 and 50% of cell osmotic potential. In low Na+ accumulating wheat genotypes, osmotic adjustment was associated with maintenance of higher K+ levels (Rivelli et al. 2002). Mild salt treatments often result in an increased rate of K+ uptake (Chen et al. 2005), and halophytic species possess much better ability to maintain higher tissue K+ content under saline environments (Garthwaite et al. 2005). Halophytes are known to rely heavily on the use of inorganic ions (mainly Na+ and Cl− ) to maintain cell turgor pressure under hyperosmotic saline conditions (Flowers and Colmer 2008, Shabala and Mackay 2011); this is achieved by the efficient sequestration of these cytotoxic ions in vacuoles. Such sequestration, however, requires a concurrent increase in the osmotic potential of the cytosol, and cytosolic K+ retention appears to be absolutely essential for this process. If this condition is not met, plants then have to invest into production of various organic osmolytes (such as proline or glycine betaine) and face the consequences of yield penalties associated with high carbon cost of this process. In this context, salt-tolerant barley varieties had better root K+ retention ability and accumulated less organic osmolytes compared with their salt-sensitive counterparts (Chen et al. 2007b). The ability of a plant to maintain high cytosolic K+ /Na+ ratio has been repeatedly named as a key determinant of plant salt tolerance (Dubcovsky et al. 1996, Maathuis and Amtmann 1999, Shabala and Cuin 2008), and K+ /Na+ discrimination has been subject to quantitative trait loci (QTL) analysis for salt tolerance in many studies (Koyama et al. 2001, Lin et al. 2004, Lindsay et al. 2004). Several factors may explain this essentiality. First, owing to physical and chemical similarities between K+ and Na+ , the latter has a tendency to compete with K+ for major binding sites, including control of enzymatic activity. Flowers et al. (1977) have listed over 10 enzymes whose activity is suppressed more than 50% by physiologically relevant NaCl concentrations found in plant tissues. This inhibition occurs primarily as a result of a direct competition between Na+ and K+ that occurs at unfavorable cytosolic K+ /Na+ ratios. Hawker et al. (1974) have shown that K+ was four times more efficient in activating starch synthase which catalyzes the reaction of ADP glucose to starch, as compared with Na+ . Similarly, V max of pyruvate kinases in the presence of K+ was about 400 higher than without K+ (Oria-Hernandez et al. 2005) and could not be substituted by Na+ . Importantly, in vitro effects of NaCl on enzyme activity were

indistinguishable between halophytes and highly sensitive glycophyte crops (Flowers et al. 1977), emphasizing essentiality of maintaining low cytosolic Na+ levels. Another important aspect related to essentiality cytosolic K+ homeostasis comes from the fact that high K+ concentrations are required to determine the cell fate and its transition to the programmed cell death (PCD). The loss of potassium has been shown to play a primary role in cell shrinkage, caspase activation and nuclease activity during apoptosis (one of the forms of PCD) in mammalian systems (Bortner and Cidlowski 2007, Hughes and Cidlowski 1999). Similar mechanism has been postulated to exist in plant systems (Shabala 2009). Two major lines of evidence support this notion. First, expression of mammalian anti-apoptotic CED-9 gene in tobacco leaf mesophyll has improved both K+ retention and overall salinity stress tolerance of plants (Shabala et al. 2007). Second, activity of caspase-like proteases and endonucleases under saline stress conditions was much lower in Arabidopsis gork mutant lacking a functional K+ efflux channel and thus retaining more K+ in the cytosol when exposed to salinity (Demidchik et al. 2010). This suggest that not only a cytosolic K+ /Na+ ratio but also absolute concentrations of K+ are essential to confer salinity stress tolerance. Plants exposure to salinity also results in an increased ROS production. This production is observed in both roots and leaves and is critically dependent on potassium availability. It is well documented that K+ deficient plants are more susceptible to high light intensity, with higher incidents of photo-oxidative damage reported (Marschner and Cakmak 1989). Increases in the severity of K+ deficiency were associated with enhanced activity of enzymes involved in detoxification of H2 O2 (e.g. ascorbate peroxidase) and utilization of H2 O2 in oxidative processes (guaiacol peroxidase), and K+ deficiency also caused an increase in NADPH-dependent O2 – generation in root cells (Cakmak 2005). Thus, optimizing the K+ nutritional status of plants can reduce this detrimental build-up of ROS either by enhancing photosynthetic electron transport or by inhibiting the membrane-bound NADPH oxidases. Indeed, an increase in NADPH oxidation was up to eightfold higher in plants with low K supply than in K-sufficient plants (Cakmak 2005). A rapid (within minutes; Shabala et al. 2006) and pronounced (by as much as 50 mM; Hajibagheri et al. 1988) decline in the cytosolic K+ concentration is observed in plant cells exposed to salinity. As a result, cytosolic K+ concentration in salinized tissues may be as low as 15–20 mM (Cuin et al. 2003 – in leaves; Shabala et al. 2006 – in roots). Three major factors contribute to this decline (Fig. 1). First, Na+ transport across the plasma •

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Salinity Cytosol Na+ raises Membrane depolarization

O2– produced in MX Cytosol Ca2+ raises NADPH activation H2O2 production

GORK activation

OH• formation

K+ leak

NSCC activation

Protease activation

Damage to key structures

PCD

Necrosis

Fig. 1. Salinity stress signal transduction networks resulting operating in plant cells. GORK, outward-rectifying depolarization-activating K+ channels; MX, mitochondria; NSCC, non-selective cation channels.

membrane results in significant membrane depolarization (by 60–80 mV; Shabala et al. 2003, 2005, 2006) enabling K+ efflux via outward-rectifying depolarizationactivated K+ channel (Shabala and Cuin 2008) encoded by GORK gene in Arabidopsis (V´ery and Sentenac 2003). Second, Na+ accumulation in the cytosol leads to an increase in the cytosolic Ca2+ levels, activating plasma membrane NOX (Lecourieux et al. 2006) and leading to apoplastic H2 O2 production. By interacting with transition metals in cell walls, H2 O2 may form highly reactive hydroxyl radical (Rodrigo-Moreno et al. 2013a), directly activating both GORK (Demidchik et al. 2010) and K+ permeable non-selective (Demidchik et al. 2003) cation channels and further contributing to K+ leak. Apoplastic H2 O2 may also enter the cell via aquaporins (Bienert et al. 2007) and interact with the superoxide formed in mitochondria under saline conditions (Cakmak 2005). This will result in generation of the hydroxyl radicals (via Fenton reaction) in the cytosolic compartment, with a consequent activation of NSCC from the cytosolic site (Rodrigo-Moreno et al. 2013b). As long as plants can control these three potential pathways for K+ leak from Physiol. Plant. 2014

the cytosol, or are capable to compensate K+ loss from the vacuolar K+ pool, root cells are able to survive saline stress. Once the latter avenue is exhausted, cytosolic K+ declines below accepted threshold, triggering PCD via the mechanism described above. Hydroxyl radicals may also cause lipid peroxidation and direct damage to cellular structure, resulting in tissue necrosis. Another key player mediating potassium homeostasis under saline conditions are tonoplast NHX exchangers. These exchangers were originally described as Na+ /H+ antiporters (Apse et al. 1999). Overexpressing NHX genes in transgenic plants resulted in improved salt tolerance in a range of crop species (Apse et al. 1999, Zhang and Blumwald 2001), presumably due to improved vascular Na+ sequestration. However, several later reports failed to find the anticipated correlation between increased salt tolerance and enhanced accumulation of Na+ by NHX proteins (Leidi et al. 2010 and references within). Instead, the role of NHX proteins was attributed to K+ /H+ exchange and discussed in the context of regulation of a vacuolar K+ content (Rodriguez-Rosales et al. 2008, Barragan et al. 2012). Indeed, tomato plants overexpressing LeNHX2 gene showed no difference in Na+ content compared with untransformed plants but had higher K+ content in both roots and shoots and grew much better under saline stress conditions (Huertas et al. 2013). Arabidopsis hhx1nxh2 double mutants showed similar sensitivity and even greater rates of Na+ sequestration than the wild type (Barragan et al. 2012) but lacked an ability to create the vacuolar K+ pool, impairing osmoregulation and compromising turgor generation for cell expansion. Thus, it appears that the role of NHX exchanger as a mediator of K+ transport between cytosol and vacuole, and its implications for plant salinity stress tolerance, remain to be elucidated in more details in the future experiments. Waterlogging Shoot potassium content declines substantially (e.g. several fold) in plants exposed to prolonged waterlogging (Close and Davidson 2003, Smethurst et al. 2005, Board 2008). Reports for roots are more controversial, ranging from significant decline (Pezeshki et al. 1999, Smethurst et al. 2005) to no change or even increase (Ashraf and Rehman 1999, Teakle et al. 2010) in root K+ content. The most likely explanation for the latter controversy comes from the complexity of root to shoot nutrient translocation in flooded plants, and its strong dependence on the duration of the treatment and species specificity. Waterlogging treatment induces a ‘physiological drought’, reducing stomatal conductivity

by several fold (Pang et al. 2004, Ou et al. 2011, Polacik and Maricle 2013) thus affecting nutrients delivery to the shoot. This may result in an increase in the xylem sap osmolality and K+ concentration during prolonged flooding (Jackson et al. 1996). On a shorter time scale, root growth is arrested immediately upon onset of hypoxia, while shoot growth still persists (Malik et al. 2002). This may result in a significant reallocation of root K+ toward the expending shoot and, in the light of reduced root capacity to take up K+ (see below), may lead to severe K+ deficiency in the root. Consistent with this notion, extracellular supply of K+ in the form of a foliar spray alleviates detrimental effects of waterlogging (Ashraf et al. 2001, Wang et al. 2013). Under conditions of oxygen deprivation, root K+ uptake is markedly reduced (reviewed in Elzenga and van Veen 2010). Under hypoxia, this effect seems to be reversible, as strong reduction in K+ uptake by nodal and seminal roots of wheat has stopped upon plants transfer from hypoxia to air (Kuiper et al. 1994). Moreover, 6 h after re-oxygenation K+ uptake exceeded that of continuously aerated roots in these experiments. More severe anoxia treatments often entail net K+ release from plant roots (Morard et al. 2004). The above reversibility and the extent of oxygen deprivation effect on net K+ fluxes may be explained by the rapid alteration in the metabolic pool and, specifically, ATP availability required to maintain membrane potential and facilitate low-affinity K+ uptake. Mancuso and Marras (2006) have compared electrophysiological and biochemical responses of two Vitis species: anoxia-sensitive Vitis rupestris and anoxia-tolerant Vitis riparia. In sensitive V. rupestris, anoxia led to energy deficit and ATP imbalance, together with the subsequent disruption of ion homeostasis and cell death. In V. riparia, a strong decrease in K+ membrane permeability allowed cells to avoid severe ion imbalances during prolonged anoxic episodes. The same group has investigated effects of hypoxic acclimation on anoxia tolerance in Vitis roots (Mugnai et al. 2011). Among reported findings, the maintenance of a better cytosolic K+ homeostasis and K+ channel functionality was named as an essential component of such acclimation mechanism. Microelectrode ion flux measurements on hypoxic barley roots have revealed high tissue- and timedependent specificity of K+ transport in plant roots (Pang et al. 2006). In mature zone, onset of hypoxia has resulted in an immediate (within few minutes) reduction in net K+ uptake in a waterlogging-sensitive Naso Nijo cultivar. In a tolerant TX9425 variety, this reduction was only temporary, and net K+ fluxes were recovered 10 min later. The situation was rather different in the root apex, where hypoxia treatment has actually reduced

the extent of K+ efflux measured from normoxic roots (Pang et al. 2006). The latter findings were surprised and counter-intuitive. The following explanation can be given. First, the membrane potential of epidermal cells in the elongation zone is usually 10 to 15 mV less negative than in the mature zone (Bose et al., unpublished), favoring thermodynamically passive K+ efflux through depolarization-activated outward-rectifying (KOR) K+ channels under conditions of experiment. At the same time, 2 h of hypoxia has caused a 26-fold decline in the rate of O2 uptake in mature zone (20 mm from root tip) but only a 12-fold decline in the root meristem (0.2 mm from root tip; Fig 2 in Pang et al. 2006). Thus, it is plausible to suggest that available oxygen may be rapidly redistributed within the root bulk, with a higher proportion being allocated to the metabolically more active root apex. Importance of longitudinal gas-phase O2 diffusion within roots has been frequently emphasized in the literature (e.g. Armstrong and Beckett 1987, Colmer and Greenway 2011), and given the relatively small cell volume of apical cells as compared with the bulk of the root, it is possible to suggest that the partial O2 concentration in this region may even transiently increase during initial hours of hypoxia. Such increase would result in a temporarily upregulation of H+ -ATPase activity, reducing K+ loss via KOR channels. This hypothesis should be validated in direct experiments. Another factor that strongly impacts root K+ homeostasis under flooded condition is the elemental soil toxicity resulting from the changes in the soil redox potential (Khabaz-Saberi and Rengel 2010, Shabala 2011). A massive increase in the amount of available Mn and Fe in the soil solution was observed within a few days of onset of waterlogging, often to above toxic levels (Marschner 1995, Zeng et al. 2013). For example, a fivefold increase in Fe content in WL-treated Eucalyptus nitens plants was reported by Close and Davidson (2003), and root Fe level in lucerne has also increased by about fivefold, from 121 to 585 mg kg−1 DW (Smethurst et al. 2005). Being a transition metal, Fe is highly redox active and, in the presence of H2 O2 , can mediate production of the hydroxyl radical through the Fenton reaction (Rodrigo-Moreno et al. 2013a). The hydroxyl radical is considered to be highly reactive and most detrimental of all ROS species, casing lipid peroxidation, damage to DNA and proteins, pigment breakdown and impairment of enzymatic activity. Hydroxyl radicals are also known to directly activate both K+ -selective outward rectifying (Demidchik et al. 2010) and non-selective K+ permeable (Zepeda-Jazo et al. 2011) channels, resulting in a massive K+ leak from the cytosol. In addition to inorganic phytotoxins such as Fe2+ , Mn2+ or H2 S, a significant accumulation of organic Physiol. Plant. 2014

substances (e.g. ethanol, acetaldehyde and various short-chain fatty acids and phenolics), also occurs in waterlogged soils, as a result of anaerobic metabolism in both plants and rhizosphere microorganisms (Armstrong and Armstrong 1999, Shabala 2011). These secondary metabolites were shown to have detrimental effects on K+ uptake and accumulation, both at the whole plant (Glass 1974) and cell-specific levels (Pang et al. 2007). The molecular identity of K+ transporters involved in responses to oxygen deprivation and plants adaptation to elemental and metabolic toxins remains a matter of conjecture. Net K+ efflux induced by physiological concentrations of hydroxybenzoic and acetic acids was strongly inhibited in barley roots by TEA+ (Pang et al. 2007), a known blocker of voltage-gated Shaker type K+ channels. A similar blocking effect of TEA+ was also reported for hypoxia-induced K+ fluxes (Pang et al. 2006). Along with substantial membrane depolarization (by 50 to 70 mV; Zhang and Tyerman 1997, Pang et al. 2007, Zeng et al. 2013), it implies that KOR channels could be downstream targets for both secondary metabolites and hypoxia signaling. While observed K+ leak measured in flooded roots is certainly detrimental for overall plant nutrition and is responsible for K+ deficiency that has been reported in crops grown in waterlogged soils (Marschner 1995), it may also play a possible beneficial role in aerenchyma formation by eliminating cortical cells via PCD mechanism. This PCD may be triggered by the increased caspase-like activity in K+ -depleted cells, similar to the model suggested for salinity stress. The ethylene-independent pathway of aerenchyma formation has been suggested earlier (Shabala 2011) but has to be validated in direct experiments. Biotic factors Superoxide-generating NOXs are also activated by pathogenic attacks (Lamb and Dixon 1997, Bolwell and Wojtaszek 1997), and potassium nutritional status has a strong impact on plant susceptibility to pathogen. High K+ status in crops decreases the incidence of diseases (Prabhu et al. 2007). K+ deficiency results in early defense signaling (Amtmann et al. 2008), and it was suggested that K+ supply early in the growth season followed by K+ depletion at a later growth stage could be a mean to strengthen the inherent defense potential of plants to pathogens (Romheld and Kirkby 2010). Hypersensitive response is a type of PCD, initiated by pathogen or pathogen-generated elicitors. This response is beneficiary for the host in case of the attack by biotrophic pathogen, because it helps to localize the infection. There is circumvented evidence that Physiol. Plant. 2014

the efflux of K+ , anions, and water not only assisted cell shrinkage but positively regulated the cell death machinery (Garcia-Brugger et al. 2006). K+ homeostasis and K+ transport systems also appear to be important for plant responses to viral infection and, specifically, to the process of the virus-host recognition. Recently we have shown that, unlike in other plant–pathogen interactions, Ca2+ signaling appears to be non-essential in recognition of the early stages of viral infection. Instead, we observed significant changes in K+ fluxes as early as 10 min after inoculation (Shabala et al. 2010). Results of pharmacological experiments and membrane potential measurements pointed out that a significant part of these fluxes may be mediated by KOR channels, and it was suggested that these channels may be formed as a result of incorporation of some viral K+ -efflux channel into the plasma membrane of host cells. The physiological rationale behind this may be reduced cell turgor pressure, facilitating the ejection of viral DNA into the host cells, as suggested for Paramecium bursari chlorella virus, PBCV-1 (Neupartl et al. 2008).

Factors controlling intracellular K+ homeostasis in plants Membrane potential and cytosolic Ca2+ High cytosolic K+ levels that are required for optimal cell metabolism are achieved primarily by the maintenance of a large (–120 to –180 mV) negative voltage difference across the plasma membrane (PM). This resting potential is set by the PM H+ -ATPase and is normally kept close to the equilibrium potential for K+ , EK (Hirsch et al. 1998). A decrease of the resting potential below EK leads to the activation of inward rectifying K+ channels (encoded by AtAKT1 in Arabidopsis thaliana roots), which may contribute to the K+ uptake, providing external K+ is not very low. At low (micromolar) external K+ its uptake is mediated by H+ gradient-coupled transporters, most importantly by HAK5 (Hirsch et al. 1998, Rubio et al. 2008). Therefore, H+ -ATPase controls K+ uptake in two ways: by creating a driving force for the channel-mediated K+ uptake via control of membrane potential difference and by generation of the H+ gradient, fuelling the cotransporter-mediated high affinity K+ uptake. Moreover, hyperpolarization may be directly involved in the induction of HAK5 expression (Nieves-Cordones et al. 2008). Depending on stress type, membrane potential may go down or up, inducing K+ uptake or efflux (Shabala and Cuin 2008). In case of voltage-dependent K+ -selective channels these changes effectively (functionally) eliminate either outward-rectifying K+ channels (which are closed at hyperpolarized potentials), or inward rectifying K+ channels (closed at depolarized potentials).

Decrease of external K+ causes the immediate membrane hyperpolarization due to a decrease of the EK (Wang and Wu 2013). At moderate decreases of the external K+ , passive uptake via inward rectifying K+ channels would be feasible. At lower external K+ (70% of its normal level) decrease of intracellular K+ (Roeflsema and Hedrich 2005, Chen et al. 2005, Shabala et al. 2006). For the sake of electroneutrality, such a massive loss has to be accompanied by an equivalent efflux of intracellular anions (Zhang et al. 2001b, Roeflsema and Hedrich 2005, Garcia-Brugger et al. 2006), whereas under salt stress intracellular K+ is partly exchanged for external Na+ . K+ loss in the latter case can be reduced by Cl – uptake across the PM, which electrically compensates the equivalent part of Na+ uptake (Shabala et al. 2005, Teakle and Tyerman 2010). K+ loss, induced by a variety of stresses, can be remediated by an appropriate readjustment of the plasma membrane transport properties or buffered by mobilization of K+ from vacuoles. However, in some cases, exaggerated K+ loss may be beneficiary, like in the case of the hypersensitive response to a pathogen attack. In addition to membrane potential difference, many ion transporters are regulated by the cytosolic Ca2+ . Elevation in cytosolic Ca2+ was shown to mediate a variety of responses to abiotic and biotic stresses such as cold and heat, salt, osmotic, oxidative and anoxia, K+ deficiency, and pathogen attack/elicitors (Lecourieux et al. 2006, Ranf et al. 2008, Wang and Wu 2013). It should be noted that in most of cases H+ -ATPase transcripts do not change at stress, but there are substantial changes in the H+ -ATPase activity, either positive or negative, due to a post-translational control (Gaxiola et al. 2007). Salt-tolerant barley varieties have several-fold higher activity of PM H+ -ATPase in roots as compared with salt-sensitive ones, while showing no significant difference at the protein level. Such intrinsically higher H+ -ATPase activity helps salt-tolerant varieties to better withstand depolarization challenge,

induced by high salt, hence minimizing NaCl-induced K+ leak (Chen et al. 2007a). H+ -ATPase can be directly regulated by the intracellular K+ , which at high (normal) concentration partly uncouples ATP-hydrolysis from the H+ transport, resulting in coupling rates H+ /ATP < 1 (Buch-Pedersen et al. 2006). This implies that H+ pumping will be stimulated by K+ deficiency, supporting energization of the PM for secondary transports, including transporter-mediated K+ uptake. Several papers have also reported the PM H+ -ATPase inhibition by the intracellular Ca2+ (Kinoshita et al. 1995, Brault et al. 2004). This inhibition is indirect and likely to be mediated by the CBL/CIPK network (Fig. 2), where CIPK is a CBL-interacting protein kinase and CBL stays for calcineurin B-like protein. Indeed, phosphorylation of H+ -ATPase by PKS5, a member of the SOS2-like kinase family, has interacted with CBL2 to induce a dissociation of 14-3-3 proteins, causing inactivation of the H+ -ATPase pump (Fuglsang et al. 2007). One of the earliest events in plant responses to K+ deficiency is an activation of the inward rectifying K+ channels in plant roots (AKT1 in A. thaliana). AKT1 requires phosphorylation by CIPK23 (upregulated at K+ deficiency), which is activated due to an interaction with CBL1 or CBL9 (Xu et al. 2006). There also appear to be a redundancy in the action of CBL1 and CBL9, so only double mutants displayed altered nutrient absorption by root hairs and altered stomata function (Cheong et al. 2007). Loading of K+ to xylem may be mediated by SKOR, a stelar K+ -selective outward rectifying channel (Gaymard et al. 1998). Another contributing channel is NORC (outward rectifying non-selective current), which is equally permeable for monovalent cations (K+ ) and anions. SKOR channel is downregulated by an increase in cytosolic Ca2+ , and NORC is upregulated by high cytosolic Ca2+ . It was hypothesized that NORC can participate in the xylem loading under stress conditions, characterized by an overall increase in intracellular Ca2+ , so that it will depolarize membrane potentials to values, close to zero, mediating simultaneous efflux of cations and anions (Wegner and De Boer 1997). At the same time, in guard cells GORK activity seems to be independent on Ca2+ , where GORK-mediated K+ efflux is electrically coupled and driven by anion efflux via a slow anion channel, SLAC1. This anion channel is upregulated by a variety of Ca2+ -dependent protein kinases, CPKs (Fig. 2). Some CPK also participates in a downregulation of KAT1 channel, facilitating stomata closure (Berkowitz et al. 2000). Tissue K+ /Na+ relations are regulated by several transporters and channels, which control long distance K+ and Na+ transport and vacuolar sequestration (Fig. 2). Vacuolar Na+ sequestration is thought to be controlled Physiol. Plant. 2014

Fig. 2. Calcium as a master key in controlling ion transport in plant cells. 1. The parallel activation of K+ and nitrate uptake. 2. Activation of anion efflux, inhibition of K+ influx and depolarization resulting in electroneutral loss of salt and mediating processes such as volume/turgor regulation and xylem loading. 3. Regulation of vacuolar Na+ and K+ transport and tonoplast Na+ /K+ selectivity by cytosolic and vacuolar Ca2+ . 4. Na+ extrusion and vacuolar sequestration, K+ mobilization from vacuole, and their long-distance transport. 5. ROS-induced cation conductance (comprised of hyperpolarization-activated Ca2+ influx, annexin1-mediated cation current, and weakly voltage-dependent non-selective conductance, ROSIC) is positively feedbacked by inflowing Ca2+ . CAM, calmodulin; CBL, calcineurin B-like protein; CIPK (SIP4), CBL-interacting protein-kinase; EF (hand), Ca2+ -binding domain; ACA, plasma membrane Ca2+ ATPase; AHA, plasma membrane H+ ATPase CAX1, Ca2+ /H+ exchanger; NHX1, SOS1, Na+ /H+ exchangers; NRT1.1, nitrate transporter; AKT1, KAT1, AKT2, Shaker-type inward or weakly rectifying K+ channels; GORK/SKOR, Shaker-type outward rectifying guard-cell or stellar K+ channels; FV, fast vacuolar channel; SV (TPC1), slow vacuolar channel; VK (TPK1), vacuolar K+ channel; NOX, NADPH oxidase.

by NHX1 Na+ /H+ antiporters, which, however, display a very significant K+ /H+ exchange activity (Apse and Blumwald 2007). Yet, Na+ /K+ selectivity of the NHX1 is regulated by vacuolar calmodulin in both Ca2+ and pH-dependent manner (Yamaguchi et al. 2005). Physical interaction of AKT2 channels with CIPK6 kinase, activated by CBL4 without channel protein phosphorylation, recruits these weakly rectifying K+ channels from the endoplasmic reticulum (ER) to the plasma membrane (Held et al. 2011). AKT2 channels control K+ recirculation from and to the phloem. On the other hand, K+ mobilization from the vacuole (most likely via K+ /H+ symport) at K+ deficiency is upregulated by CIPK9-CBL2/3 (Liu et al. 2013). Vacuole is central to Ca2+ and K+ storage, and possesses a set of three different K+ -permeable channels, which are differentially regulated by cytosolic and luminal Ca2+ . One of them is VK, a highly K+ selective channel which is voltage-independent and is activated by the increase in the cytosolic Ca2+ (Ward Physiol. Plant. 2014

and Schroeder 1994, Pottosin et al. 2003). This channel is encoded by TPK1 and proved to play an important role in K+ release associated with stomata closure. Ca2+ activation of TPK1 is direct, because it possesses four EF-hands (specific Ca2+ binding domains) at C-termini, which display affinity to Ca2+ in a submicromolar range (Gobert et al. 2007). TPK1s from different species have osmo- and mechano-sensitive properties, so they may be implemented in a general control of cell turgor (Maathuis 2011). In TPK1 loss-of-function mutants ABAinduced stomata closure is retarded but not arrested, which implies the involvement of additional routes for K+ release from vacuoles (Gobert et al. 2007), either K+ -selective or non-selective cation ones. It is still a matter of debates of whether other members of the tandem-pore K+ channels family TPK2, TPK3, and TPK5 that are also expressed at the tonoplast, form functional vacuolar K+ channels in Arabidopsis (Voelker et al. 2010). Although expressed at smaller numbers in cell types other than stomata, VK channels may play an

important role in the vacuolar K+ mobilization during salt stress (Pottosin et al. 2003). The other two channels types are SV (encoded by TPC1 gene) and FV (a product of some unknown gene(s)) channels (Tikhonova et al. 1997, Peiter et al. 2005). Both channels can conduct monovalent cations ¨ with a little preference (Bruggemann et al. 1999a, Pottosin et al. 2001, Bonales-Alatorre et al. 2013) but SV can also conduct divalent cations such as Ca2+ and Mg2+ (Ward and Schroeder 1994, Pottosin et al. 2001), whereas FV channels are inhibited by micromolar Ca2+ ¨ and Mg2+ (Tikhonova et al. 1997, Bruggemann et al. 1999b). SV channels possess four EF-hands at cytosolic linkers between two halves of subunit: two high affinity ones, specific for Ca2+ , and two others, with a low and comparable affinity for Ca2+ and Mg2+ (Schulze et al. 2011). This can explain the channel’s potentiation by the cytosolic Mg2+ and its complex regulation by ¨ the cytosolic Ca2+ (Pottosin and Schonknecht 2007). In addition to direct Ca2+ binding, SV channels are modulated by calmodulin and Ca2+ -dependent protein phosphorylation and dephosphorylation (reviewed by Hedrich and Marten 2011). Overall, with a few exceptions FV channels are more active at resting levels of cytosolic Ca2+ , whereas VK and SV channels require elevated cytosolic Ca2+ levels for their activity. K+ release from the vacuole via FV and SV channels is also strongly reduced by the vacuolar Ca2+ (Tikhonova et al. 1997, Pottosin et al. 2004). Sensitivity of SV channels to vacuolar Ca2+ was reduced in fou1 mutants, displaying increased jasmonate production in a response to wounding. This finding led to a structural characterization of the luminal Ca2+ -binding sites within TPC1 protein, which share similarity with EF-domains (Dadacz-Narloch et al. 2011). Vacuolar Na+ >K+ , Mg2+ , and low pH tend to desensitize SV channel to vacuolar Ca2+ changes within its physiological range of concentrations (Pottosin et al. 2005, P´erez et al. 2008). Control by cations from both membrane sides tends to minimize vacuolar Ca2+ release via SV channels (P´erez et al. 2008, Pottosin et al. 2009). Yet, SV channel conductance for monovalent cations (K+ ) is by an order of magnitude higher than for divalent ones (Pottosin et al. 2001) so these channels could still mediate significant K+ fluxes. FV and SV channels are regulated in a feedback manner by the vacuolar K+ and probably operate like valves, setting upper limit for vacuolar K+ accumulation by regulating K+ release from the lumen (Pottosin et al. 2003, 2005). Though, under salt stress conditions such behavior may interfere with the vacuolar Na+ accumulation, because high vacuolar Na+ tended to increase the activity of SV and FV channels in a similar to K+ fashion, and Na+ can leak via the

same channels (P´erez et al. 2008, Bonales-Alatorre et al. 2013). A downregulation of SV and FV channel activities can be a part of the solution of this problem (BonalesAlatorre et al. 2013). Another plausible mechanism may be an increase in the vacuolar Ca2+ to inhibit release of monovalent cations via SV and FV channels. A steady state level of vacuolar Ca2+ depends on the balance between active Ca2+ import to vacuoles via Ca2+ pumps and CAX-type Ca2+ /H+ antiporters and (mainly SV) channels ´ mediated vacuolar Ca2+ release. Consequently, there is a large difference in the accumulation of Ca2+ between Arabidopsis mesophyll and epidermis, which reflects a 400-lower TPC1 and a 1000 higher CAX1 expression in the epidermis (Gilliham et al. 2011). These authors have also shown that knockouts of TPC1 may accumulate many-fold higher Ca2+ in leaf epidermis. CAX1 is upregulated by CIPK24 under salt stress conditions, and deregulation of CAX1 caused an increase of salt sensitivity (Cheng et al. 2004). Yet, it is not clear whether the upregulation of CAX1 under salt stress caused Ca2+ accumulation in vacuoles, sufficient to be sensed by the vacuolar FV and SV channels. ROS activate multiple non-selective cation conductances in plant plasma membrane, which can also mediate K+ efflux (see the next chapter). Here it is important to mention the Ca2+ -amplifying loop in regulation of the activity of NOX, a principle PM ROS-generating enzyme. ROS-induced conductance mediates Ca2+ influx, which further activates NOX via a direct Ca2+ binding to EFhands of the enzyme (Takeda et al. 2008) and due to the NOX phosphorylation by the CPK (Kimura et al. 2012). Polyamines and ROS ROS and polyamines (PAs) are accumulated in plant tissues during abiotic and biotic stresses. Rather than being sheer collateral consequences of metabolic changes, induced by stress, ROS and PAs can alleviate stress-induced damage and participate as active players in the stress signaling cascades (Shetty et al. 2008, Garg and Manchanda 2009, Alc´azar et al. 2010, Mittler et al. 2011, Tavaldoraki et al. 2012, Gupta et al. 2013). K+ deficiency leads to H2 O2 release, which induces the expression of genes encoding K+ transporters, such as AtHAK5. Increase of H2 O2 is due to an upregulation of PM NOX and peroxidase. No upregulation of AtHAK5 was observed in NOX lack-of-function rhd2 mutants (Shin and Schatmann 2004, Kim et al. 2010a). A massive accumulation of putrescine (up to 10 mM) was observed in K+ -deficient plants without marked changes of higher polyamines levels (Watson and Malmberg 1996), whereas high (10–15 mM) external K+ depresses Physiol. Plant. 2014

putrescine synthesis and stimulates its conversion to higher polyamines (Aurisano et al. 1993). Increase in Put2+ levels under K+ deficiency in Arabidopsis results from the increased ADC2 expression under control of jasmonate (Armengaud et al. 2004). At millimolar concentrations Put2+ causes a strong inhibition of FV and SV ¨ channels (Bruggemann et al. 1998, Dobrovinskaya et al. 1999a, 1999b). Studies on K+ -deprived barley roots showed that cytosolic K+ can be maintained relatively constant until vacuolar K+ drops down to 10% of its level at K+ -replete conditions. At the same time, the tonoplast potential difference is kept constant and close to zero, which implies that K+ release from the vacuole is active at K+ deprivation (Walker et al. 1996). Clearly, under these conditions passive re-uptake of K+ by vacuoles has to be minimized, which probably is achieved via concerted downregulation of vacuolar FV and SV channels by vacuolar K+ and Ca2+ , as well as by putrescine. Drought and salt both cause activation of higher PAs biosynthesis in Arabidopsis (Alc´azar et al. 2010). Vacuolar FV and SV channels have shown much higher sensitivity to higher PAs as compared with Put2+ ¨ (Bruggemann et al. 1998, Dobrovinskaya et al. 1999a). Inhibition of vacuolar non-selective cation channels by PAs, which hardly affected VK channels (Hamamoto et al. 2008) implies an increase of K+ /Na+ selectivity of the tonoplast conductance. Thus, PAs will prevent Na+ leak from the vacuole, allowing at the same time refilling of cytosolic K+ via K+ release by VK channels (ZepedaJazo et al. 2008a). Recently, overexpression of TPK1 in tobacco was shown to enhance salt tolerance, possibly due to increased mobilization of K+ from vacuole to cytosol (Wang et al. 2013). Increase in Spd3+ content under drought inhibit inwardly rectifying KAT1 channels in guard cells, reducing stomata aperture and the overall water loss (Liu et al. 2000). In pea mesophyll, NaClinduced membrane depolarization and K+ loss can be ameliorated via inhibition of the dominant plasma membrane NSCC by PAs (Shabala et al. 2007). Similarly, in barley roots PAs reduced NSCC-mediated NaClinduced K+ efflux (Zhao et al. 2007). Based on these results, Zepeda-Jazo et al. (2008b) proposed a simple model, where a restriction of Na+ influx and Na+ induced depolarization, and a direct block of NSCC and KORC by PAs would allow better K+ retention under salt stress. A direct challenge of this model by Pandolfi et al. (2010), however, revealed that depending on growing conditions and a root zone, as well as on PAs and plant species, PAs can ameliorate or potentiate NaCl-induced K+ efflux. Potentiation of the NaCl-induced K+ efflux by PAs requires implementation of a mechanism, different from the direct channel block or inhibition. Catabolization of PAs in the apoplast, Physiol. Plant. 2014

giving a rise to H2 O2 and other ROS, may be one of explanations. Activation of a non-selective cation current by H2 O2 was the first time reported for guard cells (Pei et al. 2000). At the same time, micromolar H2 O2 inhibits inward-rectifying K+ current in guard cells, preventing stomata opening (Zhang et al. 2001a). At millimolar concentration H2 O2 can stimulate SKOR, by oxidation of cysteine in the S3 helix (Garcia-Mata et al. 2010). This cystein is conserved among plant outward rectifying K+ channels, suggesting that H2 O2 may have a similar effect on GORK in guard cells. H2 O2 production and H2 O2 induced Ca2+ influx, leading to K+ and anion efflux, are considered nowadays as important downstream event in ABA-induced stomata closure (Wang and Song 2008). The source of H2 O2 in this case may be the activity of PM NOX and of apoplastic diamine oxidase, which uses putrescine as a substrate (An et al. 2008). Hydroxyl radicals (OH ) can also induce large efflux of K+ . Patchclamp studies revealed that this efflux consists of instantaneous and time-dependent components; the latter is likely attributed to the activity of GORK (Demidchik et al. 2003, 2010). In addition, Arabidopsis annexin1 appears to mediate OH -activated time- and voltage-dependent K+ and Ca2+ -permeable currents across the plasma membrane in roots (Laohavisit et al. 2012). OH -induced instantaneous current displayed a dual permeability for cations and small anions, and was sensitive to variety of cation and anion channel blockers (Zepeda-Jazo et al. 2011). This current was termed ROSIC (for ROS-Induced ion Conductance) and its induction by OH in roots was potentiated by all natural PAs, although the effect was restricted to the mature root zone and was not observed in the distal elongation zone (Pottosin et al. 2012). Notably, when two barley varieties, contrasting in their salt sensitivity, were examined, potentiation of ROSIC and OH -induced K+ efflux by PAs was dramatically higher in a salt-sensitive variety (Velarde-Buend´ıa et al. 2012). This corroborates the view that K+ retention is critical for barley salt tolerance (Chen et al. 2007a) and that ROS (OH )-induced K+ efflux may contribute to salt sensitivity, by PCD-mediated mechanism discussed above (Fig. 1). PAs exodus to apoplast and their oxidation there are an important source of ROS during stress responses and, depending on the magnitude of oxidative burst, defense or PCD scenarios may be implemented (Tavaldoraki et al. 2012). •

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Phytohormones ABA is a universal stress hormone mediating plant signaling to drought and salinity stresses. ABA causes stomata closure, reducing plant water loss (Kim et al.

2010b, Lee and Luan 2012). ABA is sensed by the cytosolic PYR/PYL/PCAR protein receptors, which inactivate (sequester) negative regulators, namely PP2Ctype phosphatases (Hubbard et al. 2010). In their turn, PP2Cs are capable to mute phosphorylation of different target proteins, including SLAC1 (Geiger et al. 2009), inward rectifier K+ channel KAT1 (Sato et al. 2009), and the plasma membrane NOX (Sirichandra et al. 2010). ABA may also regulate membrane potential, in a tissue-specific manner, causing either hyperpolarization (Roberts and Snowman 2000) or depolarization (Brault et al. 2004) of the plasma membrane. In guard cells, such PM depolarization will result in a massive K+ efflux by GORK, enabling water efflux and resulting in a turgor loss and stomatal closure. ABA caused a Ca2+ -dependent suppression of the inward rectifying K+ current, preventing stomata re-opening (Kim et al. 2010b). ABA also induced KAT1 internalization via endocytosis, thus reducing the number of active KAT1 channels in the PM (Sutter et al. 2007). It was also proposed that ABA induces dissociation of 14-33 proteins from outward and inward-rectifying K+ channels and the PM H+ -ATPase, causing reduction of the channel-mediated K+ uptake and increase of the K+ efflux, respectively (van den Wijngaard et al. 2005). Auxin is a growth stimulator and controller of graviand phototropic responses in plants. An early cellular response to auxin is a rapid (within minutes) increase of the H+ -pumping activity, caused by the incorporation of vesicles, containing the pre-synthesized H+ -ATPase into the PM (Hager et al. 1991). This increase produced external medium acidification and membrane hyperpolarization, providing the driving force for K+ uptake, which underlies, for instance, the auxin-induced stomata opening (Lohse and Hedrich 1992). In maize, the auxininduced coleoptile growth and protoplast swelling have shown a remarkably similar dependency on the external K+ . Reversible inhibition of growth by TEA+ suggests the involvement of the inwardly rectifying K+ channels (Christian et al. 2006). Apart from the direct regulation of inward rectifying K+ channels by hyperpolarization, a density of inward rectifying K+ current increased upon the auxin treatment, due to the incorporation of de novo synthesized K+ channels into the PM (Thiel and Weise 1999). In maize roots, the expression of ZMK1, an inward rectifying K+ channel, was rapidly (within 10–15 min) induced by auxin, in a dose-dependent manner (Philippar et al. 1999). In addition, ZMK1 was activated by the external acidification (Bauer et al. 2000). Expression of genes, involved in auxin biosynthesis, are reversibly upregulated by K+ deficiency, suggesting the role of auxin in a response to low K+ (Armengaud et al. 2004). Interestingly, K+ deficiency-induced

changes appear to be highly species-specific. While in rice many auxin related genes were upregulated, A. thaliana mainly relied on the jasmonate-related enzymes (Ma et al. 2012). Finally, auxin transport and re-distribution per se is depended on the expression of K+ transporters. Transport of auxin from shoots to roots and related root hair development, gravitropic behavior and response to K+ deprivation were strongly depended on the root-tip localized expression of K+ transporter TRH1, member of the KT/KUP/HAK family (VicenteAgullo et al. 2004). ZIFL1, a member of Major Facilitator Superfamily, can indirectly modulate auxin efflux and transport, by regulating plasma membrane abundance of PIN-formed carrier, possibly, via its impact on K+ and H+ transmembrane gradients (Remy et al. 2013). Jasmonate, which plays important roles in signaling upon pathogenesis and wounding, is also involved in response to K+ deficiency, by inducing coherent expression of a high-affinity K+ transporter HAK5 (Armengaud et al. 2004). Genes involved in the jasmonate biosynthesis are regulated by external K+ changes in a tissue-specific manner; it is conceivable that this differential expression assists nutrient recycling under K+ stress (Rubio et al. 2009). Ethylene production is also doubled at K+ deficiency (Shin and Schachtman 2004). Ethylene, acting upstream of the ROS production, stimulates the expression of HAK5 at low K+ , although in ethylene insensitive mutants not all K+ deficiency responses were suppressed (Jung et al. 2009). Finally, cytokinins negatively affect plant responses to K+ deprivation, so that a reduction in the cytokinins levels helped plant’s adaptation by stimulation of ROS production, root hairs development, and HAK5 expression (Nam et al. 2012).

Gasotransmitters (NO, CO and H2 S) Haem-proteins are crucial for generation, sensing and cross-talk between gasotransmitters (NO, CO and H2 S), which, in contrast to ‘physiological’ ligand O2 , are considered to be ‘toxic’ ligands (Kajimura et al. 2010). Gases have relatively long half-life in solution, from seconds (NO) to minutes (CO and H2 S) (Wang 2002) and may permeate through lipid membranes or be channeled by the aquaporins (Boron 2010). Thus, gasotransmitters can readily reach any molecular target within a cell, irrespective to the site of their production. Plants can produce NO via NO synthase or nitrate reductase activities, or by non-enzymatic reactions such as liberation of NO from nitrite reduction in the apoplast under acid conditions (Crawford 2006). NO was shown to stimulate the H+ pumping across the PM (Wang et al. 2009. Zandonadi et al. 2010). Physiol. Plant. 2014

However, NO also specifically inhibited the blue lightinduced stomata opening via ABA-dependent pathway, causing a reduction in the H+ pumping and affecting an inwardly-rectifying K+ current (Zhao et al. 2012). NO effects on the H+ pump and K+ channels may be indirect and mediated by intracellular Ca2+ . Only moderate increase in Ca2+ influx and intracellular Ca2+ concentration was induced by the blue light, whereas NO generation provoked a large increase of the HACC activity, leading to a dramatic increase in intracellular Ca2+ and a strong suppression of the inward rectifying K+ current (Zhao et al. 2013). A soluble guanylate cyclase (sGC) is one of the crucial targets for NO. The binding of NO to its haem leads to a long-lasting modification, characterized by several hundred fold higher enzymatic activity, as compared with 3–4-fold increase, induced by CO binding (Derbyshire and Marletta 2009). NOinduced activation of the slow anion channels and suppression of inward rectifying K+ currents in guard cells were due to Ca2+ release from intracellular stores, sensitive to inhibitors of the cGMP cascade (Garcia-Mata et al. 2003). In plants CO is generated by the haem oxygenase (HO), together with bilirubin and inorganic iron as byproducts (Shekhawat and Verma 2010). Treatment with CO or NO donors improved K+ retention under salt stress, which was associated with an increase in the PM H+ -ATPase activity (Xie et al. 2008, Xu et al. 2006). In agreement with this, HO-overexpressing mutants of A. thaliana showed higher expression of the PM H+ -ATPase and SOS1, as well as a higher rate of H+ pumping and lower K+ efflux in roots in response to acute salt stress (Bose et al. 2013). In contrast, there was a report of a direct activation of a current, ascribed as a K+ outward rectifier, by CO in pollen tubes (Wu et al. 2011a). These authors speculated that, due to anoxic conditions in the ovary, this will tend to inactivate the channel, causing a decrease of K+ efflux, increase of the turgor, and, eventually, a burst of a pollen tube, discharging the sperm. Yet this study raises several doubts on the channel identity as it had relatively low selectivity for K+ over Na+ and anions and, apparently, was activated by cytosolic Ca2+ , the property not demonstrated for GORK or SKOR elsewhere. H2 S is synthetized endogenously by L-cysteine desulphydrase activity, via two enzymes, cystathionine βsynthase and cystathionine γ -lyase (Garcia-Mata and Lamattina 2010). In animals it modulates activity of various ion channels including ATP-sensitive K+ channels. Mechanism of the H2 S action includes direct channel protein sulfhydration and redox modulation, effects mediated by interactions with other gasotransmitters (e.g. CO and NO), and indirect effects such as modulation of Physiol. Plant. 2014

channel-regulating kinases (Peers et al. 2012). The question of whether similar regulation takes place in plant tissues remains to be answered. It was documented that H2 S as a signaling molecule participated in plant stress responses, where it generally tends to lower nitrosylation and oxidation stress components, increasing the glutathione level and activating antioxidant enzymes (reviewed by Lisjak et al. 2013). The most studied experimental model for the H2 S action is stomata, yielding, however, rather controversial results. Whereas Lisjak et al. (2010) found that H2 S causes stomata opening and prevents its closure in the dark, Garc´ıa-Mata and Lamattina (2010) reported the H2 S-induced stomata closure in several plant species. Obviously, net effect of H2 S on stomata aperture is contextually determined. H2 Sinduced stomata closure was impaired by sulfohydryl reagent (glibenclamide, which binds to SUR complex and inhibits KATP channels in animals), implying participation of some ATP-binding cassette (ABC) transporter (Garc´ıa-Mata and Lamattina 2010). When it comes to the H2 S-induced stomata opening, H2 S decreases ABAinduced NO production, either directly interacting with NO, with a formation of nitrosothiol, or by inhibition of the NO biosynthesis (Lisjak et al. 2010). Antagonistic action of NO and H2 S on the stomata aperture is just an example of multiple cross-talks between different gasotransmitters. Response to CO seems to involve the NO signal (Xie et al. 2008, Liu et al. 2010). HO/CO signaling may converge with the NO-signaling pathway on the level of cGMP production and respective increase of intracellular Ca2+ (Xuan et al. 2008). In addition, NO increased HO expression (Noriega et al. 2007) implying that NO and CO signaling cascades interact synergistically. Gasotransmitters also interact with ROS signaling. HO expression is induced by ROS (Yannarelli et al. 2006) and there is an abundant evidence that the HO-activity may efficiently decrease the ROS production by downregulating the NADPH oxidase by CO, ROS-scavenging and stimulation of antioxidant enzymes by CO and bilirubin (Ling et al. 2009, Shekhawat and Verma 2010, Wu et al. 2011b). However, there is also a report, linking NO and CO with increased ROS production in roots (Xuan et al. 2008). Also, NO synthesis in response to ABA and chitosan was dependent on the production of H2 O2 (Neill et al. 2008, Srivastava et al. 2009). There is also circumvented evidence that PAs signaling may be mediated, at least in part, by H2 O2 or amine oxidases, downstream of NO production (Wimalasekera et al. 2011).

Conclusions and future prospects As shown above, literally every major abiotic and biotic stress leads to a significant disturbance to intracellular K+ homeostasis, resulting in a massive K+ leak. The consequences of this process are many-fold. In the short term, a decrease in the cytosolic K+ pool may be beneficial for shutting down many energy-dependent metabolic processes allowing allocation of the larger portion of the available ATP pool toward defense-related processes. De novo synthesis of compatible solutes is one of such processes. Not only such osmolytes are essential for cytosolic osmotic adjustment under drought and saline conditions but some of them (e.g. proline, mannitol, myo-inositol) may also play a key role in the oxidative stress protection, acting as non-enzymatic antioxidants. K+ efflux is also essential to compensate for the membrane depolarization caused by excessive Na+ uptake under saline conditions. Also, K+ leak from the cortical cells under prolonged hypoxia may be instrumental in aerenchyma formation via PCD mechanism (Shabala 2011), thus enabling plant acclimation to waterlogged conditions. However, the above benefits of a rapid K+ efflux may be overruled by the major damage to cell structures and metabolism in the longer term. The failure of the cell to restore cytosolic K+ pool by either increased K+ uptake from external media, or by redrawing equivalent amounts of K+ from the vacuolar pool will jeopardize cell metabolic competence and may result in the cell elimination. While K+ depletion-triggered PCD mechanism in the root cortex may be essential to the aerenchyma formation, the same process in epidermal tissue has no physiological advantage to plants. The same is true for salinity-induced PCD in plant roots also linked to cytosolic K+ depletion (Demidchik et al. 2010). Moreover, severe depletion of the cytosolic K+ pool is causally related to the increased ROS formation in cell organelles and compartments. The failure to deal with these (and, specifically, with the hydroxyl radical) may cause oxidative damage to the key cellular structures and, ultimately, cell death by necrosis. Thus, cytosolic K+ content may be considered as one of the ‘master switches’ enabling plant transition from the normal metabolism to a ‘hibernated state’ during first hours after the stress exposure and then to a recovery phase. Although multiple physiological and molecular mechanisms contribute to above regulation, several of them warrant a special attention. First, it appears that voltagegated K+ channels are critical to plant adaptive responses to literally every known stress factor. While it remains to be shown to what extent transcriptional changes contribute to their regulation, there is little doubt that post-translational factors play a major role in this process.

Numerous second messengers including ROS, cytosolic Ca2+ , polyamines, hormones and gasotransmitters contribute to the regulation of K+ transport across cellular membranes. Moreover, interaction between these factors may be of a synergistic nature (Zepeda-Jazo et al. 2011). Thus, more attention should be paid to the possible cross-talks between signal transduction pathways and their impact on regulation of cytosolic K+ homeostasis. As commented above, stress-induced cytosolic K+ depletion may be quickly restored on expense of the vacuole (e.g. Shabala et al. 2006 for salinity stress). This implies a tight coupling of plasma membrane and tonoplast K+ transport. While regulation of tonoplast SV, FV and VK channels has been a subject of ¨ thorough investigation for decades (e.g. Bruggemann et al. 1998, 1999a, 1999b), such regulation has never been considered in concert and under conditions matching stress-induced changes in the level of signaling compounds in plant cells. Another aspect that should be put in the spotlight is an orchestrated regulation of K+ and water transport, both at the cellular (e.g. aquaporins) and whole-plant (e.g. a link between xylem K+ and root to shoot water movement) levels. The latter aspect has recently received some attention in the literature. It has been predominantly put in the context of the drought stress (e.g. Trifilio et al. 2011). Meanwhile, oxygen deprivation in waterlogged roots is highest in the root stele (Colmer and Greenway 2011), with a major consequences to the xylem K+ loading. Thus, linking oxygen profiles and transport in plant roots with regulation of specific K+ channels activity in root xylem parenchyma may be critical to understand detrimental effects of waterlogging on plant nutrient and water transport to the shoot. Last but not least, ROS production appears to be a common denominator of literally every abiotic and biotic stress. Revealing the molecular nature of ROS sensors and mechanism of ROS activation of K+ permeable channels may be, therefore, instrumental in improving plant stress tolerance in the MAS-based breeding programs. Acknowledgements – This work was supported by the Australian Research Council and Grain Research Development Corporation grants to Prof S. Shabala and CONACyT grants to Prof I. Pottosin.

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