JXB Advance Access originally published online on January 31, 2006
Journal of Experimental Botany 2006 57(5):1149-1160; doi:10.1093/jxb/erj068
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
RESEARCH PAPER |
High-affinity potassium and sodium transport systems in plants
1Laboratorio de Microbiología, Departamento de Biotecnología, Escuela Técnica Superíor de Ingenieros Agrónomos, Universidad Politécnica de Madrid, E-28040 Madrid, Spain
2Departamento de Nutrición Vegetal, Centro de Edafología y Biología Aplicada del Segura-CSIC, E-30100 Murcia, Spain
* To whom correspondence should be addressed. E-mail: alonso.rodriguez{at}upm.es
Received 27 May 2005; Accepted 12 September 2005
 |
Abstract |
|---|
 Top Abstract IntroductionK+ transportNa+ uptakeHigh-affinity K+ or Na+...Problems in the functional...OutlookReferences |
|---|
All living cells have an absolute requirement for K+, which must be taken up from the external medium. In contrast to marine organisms, which live in a medium with an inexhaustible supply of K+, terrestrial life evolved in oligotrophic environments where the low supply of K+ limited the growth of colonizing plants. In these limiting conditions Na+ could substitute for K+ in some cellular functions, but in others it is toxic. In the vacuole, Na+ is not toxic and can undertake osmotic functions, reducing the total K+ requirements and improving growth when the lack of K+ is a limiting factor. Because of these physiological requirements, the terrestrial life of plants depends on high-affinity K+ uptake systems and benefits from high-affinity Na+ uptake systems. In plants, both systems have received extensive attention during recent years and a clear insight of their functions is emerging. Some plant HAK transporters mediate high-affinity K+ uptake in yeast, mimicking K+ uptake in roots, while other members of the same family may be K+ transporters in the tonoplast. In parallel with the HAK transporters, some HKT transporters mediate high-affinity Na+ uptake without cotransporting K+. HKT transporters have two functions: (i) to take up Na+ from the soil solution to reduce K+ requirements when K+ is a limiting factor, and (ii) to reduce Na+ accumulation in leaves by both removing Na+ from the xylem sap and loading Na+ into the phloem sap.
Key words: Potassium transport, sodium transport
|
Introduction |
|---|
|
TopAbstractIntroductionK+ transportNa+ uptakeHigh-affinity K+ or Na+...Problems in the functional...OutlookReferences |
|---|
Among all the cations that were present in the sea, where the early evolution of life took place, K+ was utilized by cells as the major cation of their internal environment, with the chief functions of maintaining electroneutrality and osmotic equilibrium. In this cellular K+-rich environment further evolution of some biochemical processes made use of K+ for regulatory purposes while, in others, there evolved protein activities that depended on K+–protein interactions. Because these interactions were not mimicked by Na+ or by any other cation, K+ became absolutely necessary for living cells. This K+ dependence did not confine the evolution of life to the sea, where K+ has always been abundant. Quite the reverse, the emergence of the terrestrial plants in the Cambrian era (Heckman et al., 2001
; Sanderson, 2003) and their evolution from Bryophytes to flowering plants (Qiu and Palmer, 1999; Nickrent et al., 2000) took place in oligotrophic environments where K+ was at much lower concentrations than in sea waters. Despite this K+ shortage terrestrial plants not only kept their K+ dependence but also developed new functions for K+, such as for hydraulic cell movements (Blatt, 2000).
Because, the K+ requirement applies to every cell in multicellular organisms, after entering a plant, K+ has to be transported to distant organs through the xylem. K+ moves from the root symplast to the xylem sap and from this to the apoplastic space outside the bundle sheath, a process that involves many types of cells. Although, in most cells, the cytoplasmic K+ concentrations are quite similar in non-stressing conditions, around 100 mM (Walker et al., 1996a; Cuin et al., 2003), the external K+ concentrations and pH values to which root and internal cells are exposed are considerably variable (Leigh and Wyn Jones, 1984). Consequently, it is not surprising that plant genomes contain a high number of genes encoding K+ transporters and channels (Mäser et al., 2001, 2002b; Véry and Sentenac, 2002, 2003). Some of these transporters have the specific capacity of taking up K+ from very low K+ concentrations and of keeping very high concentration ratios across the plasma membrane. This type of transporter may be important for many plant cells, but are crucial in root epidermal and cortical cells, where they determine the capacity of the plant to thrive in soils with very low K+ concentrations.
The term ‘high-affinity transporter’ does not have a formal definition and it is used here to indicate that the transporter exhibits a Km that is not much higher than that of the high-affinity ‘Mechanism I’ that was described in pioneering papers on K+ transport (Epstein et al., 1963). Although under such low-K+ conditions transport may involve a high energetic demand, the term high-affinity does not imply that the transporter necessarily mediates an active process (Rodríguez-Navarro, 2000). For example, the high-affinity K+ transporter of Neurospora crassa is an active transporter because it mediates the accumulation of K+ when the diffusion potential of K+ is more negative than the membrane potential (Rodríguez-Navarro et al., 1986). By contrast, a channel may exhibit high-affinity for K+ (Sentenac et al., 1992; Brüggemann et al., 1999), but cannot mediate active transport.
Although plants have an absolute requirement for K+, and Na+ is toxic for many biological reactions in the cytoplasm, this does not apply to vacuolar processes and the replacement of K+ by Na+ in the vacuole does not produce toxicity (Flowers and Läuchli, 1983; Subbarao et al., 2003). With an unrestricted supply of K+, a significant proportion is in the vacuole; its replacement by Na+ greatly reduces the total K+ content of the plant and, consequently, its ability to take up Na+ is an evolutionary advantage that plants have used. However, if Na+ is scarce, the aforementioned difficulties for taking up K+ apply to Na+, which also requires a high-affinity transporter.
This paper aims to present an overview of the advances that have taken place in recent years on the functional understanding of high-affinity K+ and Na+ transport systems. There are references to a previous review by Rodríguez-Navarro (2000) for general concepts and this is complemented by more recent reviews on K+ (Schachtman, 2000; Mäser et al., 2001, 2002b; Tester and Leigh, 2001; Shabala, 2003; Véry and Sentenac, 2003; Amtmann et al., 2004) and Na+ (Blumwald et al., 2000; Tester and Davenport, 2003; Horie and Schroeder, 2004) transport, avoiding repetitions. Recent reviews on cation channels (Demidchik et al., 2002; Véry and Sentenac, 2002; Chérel, 2004) are also relevant to this paper.
|
K+ transport |
|---|
|
TopAbstractIntroductionK+ transportNa+ uptakeHigh-affinity K+ or Na+...Problems in the functional...OutlookReferences |
|---|
High-affinity K+ uptake and HAK transporters
High-affinity K+ uptake was firstly described by Epstein et al. (1963)
. It was shown that the roots of barley (Hordeum vulgare L.) seedlings that had been germinated in a diluted CaSO4 solution developed a high-affinity K+ influx with a Km of 10–20 mM K+, which did not discriminate between K+ and Rb+ and was unaffected by micromolar concentrations of Na+. Interestingly, an additional characteristic was its low discrimination against Cs+ (Zhu and Smolders, 2000; and references therein). This system was named high-affinity ‘Mechanism I’ (Epstein et al., 1963). Further studies on the regulation of this K+ uptake system showed that it was rapidly up-regulated when the supply of exogenous K+ was arrested (Glass, 1978; Glass and Dunlop, 1978). Similar research with other species proved that high-affinity K+ uptake was a general capacity of plants and that the barley model applied to many species (Kochian and Lucas, 1988; Rodríguez-Navarro, 2000). During the last decade, several laboratories have been working on the identification of the plant genes that encode this uptake system, a system that shares all the aforementioned characteristics with fungal HAK transporters (Rodríguez-Navarro, 2000). However, the molecular and genetic characterization of transport systems starting from simple kinetic data is not an easy task. Fortunately, the use of yeast mutants, defective in K+ uptake, proved an important tool that allowed rapid progress in the identification of plant cDNAs that encode K+ transporters. A further combination of these findings with the genetic studies on the model plant Arabidopsis thaliana that are described below allowed a comprehensive model of high-affinity K+ uptake in plants to be produced.
The first transporters that were identified in yeast mutants using cDNA libraries (Anderson et al., 1992; Sentenac et al., 1992) belonged to the class of inward-rectifier K+ channels. From kinetic considerations, the identity of any of these channels with the high-affinity barley transporter was unlikely. The putative high-affinity barley transporter was eventually identified assuming sequence similarity to fungal HAK transporters (Santa-María et al., 1997). Later, BLAST searches and the systematic use of an RT- PCR approach led to the isolation of cDNAs from Arabidopsis (Rubio et al., 2000), rice (Oryza sativa L.) (Bañuelos et al., 2002), and pepper (Capsicum annuum. L) (Martínez-Cordero et al., 2004) that encoded transporters of the same family. Functional expression of these cDNAs (AtHAK5, HvHAK1, OsHAK1, and CaHAK1) in yeast mutants revealed that the encoded transporters exhibited the expected characteristics: a high capacity to deplete external K+ to very low concentrations (<1 µM); very low Kms for K+, Rb+, and Cs+; 
inhibited K+ uptake, but was not transported; and Na+ exhibited low-affinity for the transporters. Taken together, these lines of evidence strongly suggested that the identified plant HAK transporters were those that mediated the high-affinity K+ uptake by roots or, at least, a major component of it. Additional evidence is that transcript expression is enhanced by K+ starvation, paralleling the onset of the high-affinity K+ uptake in roots.
The genetic model in Arabidopsis
The use of the model plant Arabidopsis provided the opportunity to add the use of powerful genetic approaches for the study of K+ transporters. However, the use of this model plant presents some difficulties because uptake tests are difficult to perform and basic kinetic data of K+ uptake (Km and Kis of other alkali cations) are still incomplete. Nevertheless, using BLAST searches, 13 genes encoding proteins with sequence similarities to the above-mentioned HAK transporters have been identified in Arabidopsis (Mäser et al., 2001). This type of transporter has also been named KT and KUP (Quintero and Blatt, 1997; Fu and Luan, 1998; Kim et al., 1998). Out of the 13 putative K+ transporters of this family, one of them, AtHAK5, is in the phylogentic cluster that is defined by the high-affinity HAK transporters of other plant species. As already mentioned, the kinetic characteristics of AtAHK5 expressed in yeast mutants are very similar to those taken as a model of high-affinity K+ uptake in plants (Rubio et al., 2000) and AtAHAK5 is induced in roots upon K+ starvation (Ahn et al., 2004; Armengaud et al., 2004; Shin and Schachtman, 2004; Gierth et al., 2005). Interestingly, reactive oxygen species production is an early response of K+ deficiency and externally added H2O2 was sufficient for the induction of the high-affinity component of Rb+ uptake (Shin and Schachtman, 2004).
The characteristics described above for AtHAK5 suggested that it might be crucial for high-affinity K+ uptake in Arabidopsis. However, the lack of detailed studies on the kinetics of root K+ uptake hampers the establishment of the relevance of AtHAK5 because there are not enough plant kinetic data to which the functional expression in yeast can be compared. Significant progress in this line of research has been made with the recent characterization of two Arabidopsis lines with T-DNA insertions in AtHAK5, which has shed light on the role of this transporter in the plant (Gierth et al., 2005). athak5 plants lack an inducible high-affinity transport system with a Km for Rb+/K+ of approximately 15–24 µM, which agrees with the Km shown by AtHAK5 expressed in yeast (Rubio et al., 2000).
The remaining system mediating K+ uptake in the micromolar range of concentrations in athak5 plants is the inward-rectifier K+ channel AtAKT1. The involvement of AtAKT1 in high-affinity K+ uptake goes against the paradigm proposing that channels mediate low-affinity K+ uptake (Rodríguez-Navarro, 2000), but it is well documented by the characterization of a T-DNA insertion line in AtAKT1, which proved that the AtAKT1 channel mediates K+ uptake from solutions that contained as little as 10 µM K+ (Hirsch et al., 1998). By using membrane potential measurements in root cells, it was found that the AKT1 component of wild-type permeability was between 55% and 63% of total permeability when external K+ was between 10 µM and 1000 µM and was absent. The finding that specifically inhibited the non-AtAKT1 component of K+ uptake (Spalding et al., 1999) is consistent with the notion that this component involves a HAK transporter.
In contrast to the results obtained by membrane potential depolarization measurements, kinetic studies in wild-type and atakt1 plants suggest a small contribution of AtAKT1 to K+ uptake in the micromolar range of concentrations, because the Km of the K+ influx amounted to 0.9 mM K+(Rb+) (Gierth et al., 2005). Although this conclusion might be taken as contradictory with that proposing that AtAKT1 mediated 55–63% of the K+ uptake in the micromolar range of K+ concentrations, both are consistent. The apparent contradictions can be explained by the use of Rb+ as a tracer of K+ in the study with the atakt1 mutant (Gierth et al., 2005). In the case of the HAK component of uptake, the Rb+ data apply directly to K+ because HAK transporters do not discriminate between the two cations, but this is not necessarily true for a channel, which may be less permeable to Rb+ than to K+. Assuming a lower Vmax and a higher Km for Rb+ versus K+ influx when AtAKT1 is involved, the notion that this channel mediates a significant part of the K+ uptake in Arabidopsis in the micromolar range of K+ becomes apparent.
In general terms, the conclusion drawn from the experiments performed with the Arabidopsis mutants probably applies to many plants. However, for more quantitative conclusions two caveats must be considered: that the knockout of a gene may generate pleiotropic effects (see below) and that different growth conditions may change the proportion of the uptake that is mediated by the channel and the transporter. Regarding the growth conditions, in barley (Santa-María et al., 2000) and pepper (Martínez-Cordero et al., 2005) the contribution of the -sensitive (putatively HAK1-type transporters) versus the -insensitive (putatively AKT1-type channels) pathways of high-affinity K+ uptake was lower in -grown plants than in plants grown in the absence of 
Moreover, in pepper, the enhancement of the expression of CaHAK1 transcripts by K+ starvation was decreased by the presence of in the nutrient solution.
All this suggests that, as a general rule for many plants suffering K+ starvation, root high-affinity K+ uptake can be mediated by an AKT1-type channel and an HAK1-type transporter, but that the former may be important only in plants grown in the presence of
K+ transport within the plant
After entry into the root symplast, K+ has to be distributed to the rest of the plant cells, firstly by loading the xylem and later moving to the surrounding cells. In these movements K+ crosses the plasma membranes of several types of cells, depending on plant species. Moreover, fluxes into and out of the vacuole are also involved in cell K+ homeostasis. It is clear that K+ channels mediate many of these fluxes (Véry and Sentenac, 2003), even when K+ is taken up from diluted solutions (Brüggemann et al., 1999), but other transporters are also involved. Kinetic characteristics and thermodynamic reasons (Smith and Epstein, 1964; Osmond and Laties, 1968; Reed and Bonner, 1974; Blatt, 1985; Bellando et al., 1995; see also Rodríguez-Navarro, 2000) strongly suggest that high-affinity HAK K+ transporters are involved in some of these fluxes. Interestingly, at the xylem/bundle sheath interface in maize leaves, the permeability for Rb+ is at least as high as that for K+ (Keunecke et al., 2001), which resembles the most notorious characteristic of HAK transporters. All this suggests that the function of high-affinity HAK K+ uptake transporters is not restricted to K+ uptake from the soil solution in root epidermal and cortical cells. Consistent with this, AtHAK5 is expressed in shoots (Rubio et al., 2000; Ahn et al., 2004) and in stellar root cells (Gierth et al., 2005).
A more complex question about the KT/HAK/KUP transporters is the function (or existence) of the low-affinity members of this family (Senn et al., 2001; Bañuelos et al., 2002; Garciadeblas et al., 2002). In fact, most of the transporters of the KT/HAK/KUP family, 13 in Arabidopsis (Mäser et al., 2001) and 17 in rice (Bañuelos et al., 2002), do not belong to the cluster of the high-affinity transporters (Bañuelos et al., 2002), and in some cases it has been demonstrated that they are low-affinity K+ transporters (Senn et al., 2001; Garciadeblas et al., 2002). A possible hypothesis is that the main characteristics of all the transporters of this family is to be K+-H+ symporters (Rodríguez-Navarro, 2000). At a first glance, it seems unlikely that an active mechanism is associated with a low-affinity K+ transporter in the plasma membrane, because when K+ is at millimolar concentrations in the external medium, the membrane potential as the unique driving force is sufficient to give rise to the observed transmembrane gradient. An alternative possibility is that some of these K+-H+ symporters locate to the tonoplast as shown for OsHAK10 (Bañuelos et al., 2002). Because the electrical potential across the tonoplast is less negative than that across the plasma membrane, active transport of K+ from the vacuole to the cytoplasm may be necessary when the K+ content of the vacuole is low. This occurs in root cells of barley plants under K+-limiting conditions (Walker et al., 1996a). In Na+-grown plants, the same flux is not active in leaves (Cuin et al., 2003), but has to be active in root cortical cells (Carden et al., 2003). What is interesting regarding this possibility is that some HAK transporters of Mesembryanthemum crystallinum L. that belong to group II are induced by high external Na+ concentrations (Su et al., 2002).
Two Arabidopsis mutants that are defective in root hair (attrh1) (Rigas et al., 2001) and hypocotyl (atshy3-1) (Elumalai et al., 2002) growth were found to have mutations in genes of the KT/HAK/KUP family. The attrh1 (TRH1 is equivalent to KT3 and KUP4) mutation reduces auxin efflux in isolated root segments and expression of the atTRH1 cDNA in yeast cells accelerates auxin efflux (Vicente-Agullo et al., 2004). The AtTRH1 protein does not have sequence similarity to auxin transporters (Kramer, 2004, and references therein) and it is unlikely that it transports auxin. A possible explanation of this puzzle is that the attrh1 mutation in plant cells and the expression of the AtTRH1 cDNA in yeast cells affect the cellular pH, which might occur if AtTRH1 is a tonoplast K+-H+ symporter. Auxin is a weak acid (pKa=4.75) and in its undissociated form is lipophilic (the acid but not the anion), and will readily cross the plasma membrane. This implies that the lower the cytoplasmic pH, the higher the passive efflux. This applies to yeast, which does not have auxin transporters, while the case of plant cells is obviously more complex.
|
Na+ uptake |
|---|
|
TopAbstractIntroductionK+ transportNa+ uptakeHigh-affinity K+ or Na+...Problems in the functional...OutlookReferences |
|---|
High-affinity Na+ uptake and HKT transporters
High-affinity Na+ uptake was described many years ago in the roots of K+-starved barley seedlings (Rains and Epstein, 1967a
, b). However, because the addition of low K+ concentrations inhibited Na+ uptake at the same time as it elicited a rapid K+ uptake, it was concluded that the system that so strongly selected K+ over Na+ was the high-affinity ‘Mechanism I’ that transports K+ (Epstein et al., 1963). Despite the interest of these results, high-affinity Na+ uptake in plants received little attention for more than 30 years. Especially important is the repeated observation that Na+ reduces K+ requirements (Rodríguez-Navarro, 2000; Subbarao et al., 2003). It is assumed in explaining this observation that in the absence of external K+, the uptake of some Na+ is better than no monovalent cation at all. In the absence of external K+, the cellular K+ content decreases and, concomitantly, the cellular pH also decreases (Walker et al., 1996a, 1998), injuring the physiology of the cell. By contrast, if Na+ is taken up and substitutes for K+, a decrease of the cellular pH can be avoided (Carden et al., 2003). A low amount of Na+ is unlikely to be toxic in the cytoplasm, and even high amounts of Na+ are not toxic in the vacuole (Flowers and Läuchli, 1983; Blumwald et al., 2000; Subbarao et al., 2003).
Given the potential benefits of Na+ uptake when K+ limits the growth of a plant, it might be expected that high-affinity Na+ uptake played a crucial role in the evolution of terrestrial plants as they conquered an oligotrophic medium in the Cambrian era. This prediction can be extended to fungi, which also colonized terrestrial environments (Blackwell, 2000; Heckman et al., 2001) and thrive in soils together with plant roots. The existence of a high-affinity Na+ uptake in fungi (Benito et al., 2004) confirmed the suspected importance of Na+ and high-affinity Na+-uptake systems for the physiology of organisms thriving in low-K+ environments.
The first plant transporter that was reported to be involved in high-affinity Na+ uptake was the wheat HKT1. Although HKT1 mediates Na+-driven high-affinity K+ uptake and low-affinity Na+ uptake in yeast cells and Xenopus oocytes (Rubio et al., 1995) its involvement in the physiological function of Na+ uptake was not proposed. Later it was found that the Arabidopsis AtHKT1 (Uozumi et al., 2000) and the rice OsHKT1 (Horie et al., 2001) mediated Na+ uptake that was not coupled to K+ uptake. Almost simultaneously, a study with transgenic lines of wheat that showed down-regulation of HKT1 transcripts in certain conditions suggested that the transporter encoded by these transcripts mediated Na+ uptake but not K+ uptake (Laurie et al., 2002). In all these cases the uptake of Na+ as a single ion was demonstrated only in the low-affinity range of concentrations.
After these reports, molecular studies in rice (Garciadeblás et al., 2003) have demonstrated that HKT transporters mediate the high-affinity Na+ uptake that is carried out by K+-starved plants and that this occurs without the cotransport of K+. The basis of the proposal is that these transporters expressed in yeast cells mimic, almost exactly, high-affinity Na+ uptake in the roots of rice, including the effects of several inhibitors. Consistent with the notion that high-affinity Na+ uptake is only supplementary to K+ uptake, it was found that high-affinity Na+ uptake and the expression of the transcripts that encode the HKT1 transporters in barley, wheat (Wang et al., 1998; Haro et al., 2005), and rice (Garciadeblás et al., 2003) are greatly enhanced when plants are K+-starved. Furthermore, Na+ uptake is inhibited by K+ in K+-starved plants of rice, wheat, and barley (Garciadeblás et al., 2003). Based on these studies and those already described for HAK transporters, the pioneering proposal of Epstein should be modified in the sense that the high-affinity ‘Mechanism I’ of barley is made up of two systems, the HAK1 K+ transporter and HKT1 Na+ transporter, which operate in parallel (Fig. 1), when the plants are grown in the absence of
|
An intriguing question that currently cannot be answered is whether all plant species can carry out root high-affinity Na+ uptake. In fungi, in which Na+ uptake has been extensively investigated and many complete genome sequences are available, it has been found that high-affinity Na+ uptake does not exist in species that have adapted to media with high K+ contents (Benito et al., 2004
). The experiments needed to answer the question in plants are very simple because the high-affinity Na+ uptake test is unmistakable. However, thus far, only some cereals and sunflower plants (Helianthus annuus L.) have been tested, and, although the results have been positive in these species (Garciadeblás et al., 2003), the existence of this transport system may not be a general rule. For example, it may be absent in Arabidopsis, because AtHKT1 seems to be a low-affinity Na+ uptake transporter (Uozumi et al., 2000) and there is not another HKT transporter encoded in the Arabidopsis genome that could carry out the high-affinity uptake (Mäser et al., 2001). Moreover, Na+ influx did not differ from the wild type in an athkt1 insertional mutant (Essah et al., 2003). Although this is a convincing result, a definitive conclusion needs further research. The main caveat regarding the experiments with the athkt1 mutant is to know whether, in the conditions of the experiments, AtHKT1 was functional in the wild-type plants and whether its activity is significant versus the activity of the channels that transport Na+ (Tyerman and Skerrett, 1999; Davenport and Tester, 2000; Maathuis and Sanders, 2001; Demidchik et al., 2002; Essah et al., 2003) when tests are performed with the cation at millimolar concentrations.
The properties of HKT transporters explain the controversy regarding their function
The function of HKT transporters as high-affinity Na+ uptake systems conflicts with the description of the wheat HKT1 transporter and this conflict deserves further discussion. The wheat HKT1 transporter was originally characterized as the K+-H+ symporter that mediated the high-affinity K+ uptake system of wheat roots (Schachtman and Schroeder, 1994), but it was later found that it cotransported Na+-K+ when expressed in yeast cells or Xenopus oocytes (Rubio et al., 1995). The latter finding has not completely eliminated the notion that considered HKT1 as a root high-affinity K+ transporter (Horie and Schroeder, 2004). However, Na+-stimulated K+ uptake, resembling a Na+-K+ cotransport function, has never been shown to operate in the roots of any cereal (Maathuis et al., 1996; Walker et al., 1996b; Hayes et al., 2001; Garciadeblás et al., 2003). This negative observation does not rule out that HKT1 functions as a high-affinity K+ transporter (Rubio et al., 1996), but it cannot be Epstein's high-affinity ‘Mechanism I’, which is kinetically different.
The apparent contradiction between the function of the rice HKT1 transporter, which is taken as a model of high-affinity Na+ uptake, and the wheat HKT1 transporter lies in the complexity of the heterologous expressions of HKT transporters. The same cDNA, either HvHKT1 (barley) or TaHKT1 (wheat), can be expressed as a Na+-K+ symport or Na+ (or K+) uniport in yeast, depending on the construct in which the cDNA is inserted. This can be explained by alternative initiations of translation, which give rise to different proteins with different kinetic properties (Haro et al., 2005). In barley, only the uniport function mimics the kinetics of Na+ uptake in roots, which suggests that the Na+-K+ symport may either be an artefact or a function that is expressed in non-root epidermal and cortical cells. Interestingly, with the rice OsHKT1 transporter the problems show some similarities with those seen with the wheat transporter, because the expression of OsHKT1 in Xenopus oocytes has been reported to be either an Na+ transporter (Horie et al., 2001) or a Na+ or K+ transporter that shows higher currents when Na+ and K+ are added together (Golldack et al., 2002). In yeast (perhaps in a particular construct), OsHKT1 behaves as a high-affinity Na+ uptake system that is strongly inhibited by K+ and to a lesser extent by Ba2+, mimicking, as described above, the high-affinity Na+ uptake exhibited by K+-starved rice roots (Garciadeblás et al., 2003).
Now, the most likely explanation for the diverse results concerning HKT transporters is that, as described for the expression in yeast, some HKT mRNAs have alternative initiations of translations in the plant, which give rise to transporters with different kinetic properties that are adapted to different physiological conditions. If these alternative initiations of translations are not performed in heterologous systems exactly as they are in the plants, the properties of the expressed transporter could be variable and not physiological (Haro et al., 2005).
The versatility of functions of plant HKT transporters, which may be used by the plant in a mode that is not yet known, probably lies in their capacity for transporting two cations simultaneously. These transporters have a structure made up of four MPM (membrane-pore-membrane) motifs that also occurs in bacterial and fungal transporters of the same family (Rodríguez-Navarro, 2000; Kato et al., 2001; Zeng et al., 2004). Plant HKT and fungal TRK transporters are similar, and all the evidence suggests that they have two cation binding sites that must be occupied before the bound ions can cross the membrane (Rodríguez-Navarro, 2000; Haro and Rodríguez-Navarro, 2002, 2003; Garciadeblás et al., 2003). If the same alkali cation, K+ or Na+, can occupy the two sites, the result is a uniport of either K+ or Na+, as in the case of K+ transport in Saccharomyces cerevisiae and Na+ transport by OsHKT1, TaHKT1, HvHKT1, and AtHKT1. In the event that the same ion cannot bind the two sites (or can do so only with very low affinity), but that two different ions can and cross the membrane, the result is a Na+-K+ symport, as occurs with some constructs of TaHKT1 and HvHKT1. Finally, if Na+ can bind the two sites with high affinity and be transported, and K+ can bind one of the two sites with high affinity but cannot cross the membrane, the result is a Na+ uniporter whose function is strongly inhibited in the presence of K+, as described for OsHKT1 (Fig. 2). In other words, this transporter mediates Na+ uptake, but only when K+ is not available. All these descriptions apply when K+ and Na+ are bound at micromolar concentrations (AtHKT1 and OsHKT4 may be exceptions). When the cations are present at millimolar concentrations some of these transporters may uniport Na+, K+, or Rb+, regardless of the function that they exhibit when the cations are at micromolar concentrations (Gassmann et al., 1996; Garciadeblás et al., 2003).
|
It is worth observing that the binding of two Na+, as in OsHKT1 in Fig. 2, does not result in an active process (Rodríguez-Navarro, 2000
). Although specific experiments aimed at thermodynamic calculation have not been reported, typical uptake experiments with plants or yeast cells expressing OsHKT1, in which external Na+ can be depleted down to 1–2 mM (a slightly lower concentration can be reached during K+ starvation of roots and yeast cells if the nutrient medium has an initial low amount of Na+) (Garciadeblás et al., 2003; Haro et al., 2005), do not imply an active uptake. Roots with a membrane potential of –180 mV, which is a reasonable assumption (Spalding et al., 1999, and references therein), could reach a maximum cytoplasmic/external concentration ratio of Na+ of 103, which means that the Na+ concentration in the cytoplasm could not reach a value higher than 1–2 mM. It can be predicted that this value is not exceeded in the described experiments, because the amount of Na+ that is taken up is low and a significant part of the Na+ taken up is probably accumulated into the vacuole (Carden et al., 2003).
Making use of mutants (Diatloff et al., 1998; Rubio et al., 1999; Liu et al., 2000; Mäser et al., 2002c; see also Kato et al., 2001) and by comparing the sequences of the OsHKT1 and OsHKT2 transporters (Horie et al., 2001) the role of several amino acid residues in the Na+/K+ selectivity has been discussed. Although these data suggest functional domains, the fact that small changes in the protein change the function of these transporters (uniport or symport) suggests that more complete kinetic studies are necessary before a clear scheme of the structure–function relationships of these transporters can be made. It is especially important to determine the effect of the mutations on the affinity of the transporter in each one of the two binding sites and on the Vmax. In addition, the kinetic response may be affected more by the aforementioned variability of the expressed protein than by the change of a particular amino acid residue. This applies to the Gly or Ser residue that is located at the end of the first P loop of the transporter. A Gly residue is probably necessary for K+ transport in some species (Horie et al., 2001; Mäser et al., 2002c), but a Ser residue allows K+ transport in others (Fairbairn et al., 2000; Liu et al., 2001; Golldack et al., 2002). Even AtHKT1, which is a model of a Na+ transporter, transports K+ when expressed in bacteria (Uozumi et al., 2000).
In addition to what has been described, high-affinity TRK-HKT transporters have other important characteristics whose physiological roles have not been sufficiently investigated so far. A striking characteristic is that some of them can function as Cl– channels (Baev et al., 2004; Kuroda et al., 2004). Probably unrelated to this function or to that proper to transporting Na+ or K+, the expressions of some HKT transporters in yeast, or at least some constructs with the HKT cDNAs, are quite toxic. This is the case of OsHKT1 (Garciadeblás et al., 2003). In the case of the Arabidopsis transporter AtHKT1, which transports Na+ (Uozumi et al., 2000; Berthomieu et al., 2003), some constructs cannot be studied in yeast because of their extreme toxicity (FJ Quintero and F Rubio, unpublished results).
Na+ transport within the plant
As described for K+, the Na+ taken up by roots from the soil solution moves into the xylem from where it can be taken up by several types of cells in roots and shoots, and eventually returned to roots (Kramer et al., 1977; Johanson et al., 1983; Johanson and Cheeseman, 1983; Jeschke and Pate, 1991; Jeschke et al., 1992; Durand and Lacan, 1994; Lacan and Durand, 1995, 1996). Na+ tolerance and differences in Na+ tolerance in related plants may lie in the different capacities of different plants for carrying out these fluxes (Wolf et al., 1991; Blom-Zandstra et al., 1998; Watson et al., 2001; Davenport et al., 2005). It has already been mentioned that cellular Na+ uptake can be mediated by channels (Tyerman and Skerrett, 1999; Davenport and Tester, 2000; Maathuis and Sanders, 2001; Demidchik et al., 2002; Essah et al., 2003). However, the most likely possibility is that HKT transporters and not channels mediate many of the internal Na+ movements described in the aforementioned references. In the first place, because HKT transporters are the only known transporters that are specific for Na+ and can carry out this uptake in the presence of K+. In the second place, because it has been already shown that AtHKT1 mediates Na+ distribution within the plant in Arabidopsis (Rus et al., 2001, 2004; Mäser et al., 2002a; Berthomieu et al., 2003; Gong et al., 2004). These considerations apply especially to the removal of Na+ from the xylem sap, which may be a key process to limit the ascent of Na+ to leaves.
Even assuming some uncertainty regarding the precision with which heterologous systems reproduce the physiological functions of HKT transporters, it is possible that some HKT transporters expressed within the plant exhibit low affinity for Na+, AtHKT1 (Uozumi et al., 2000), McHKT1 (Su et al., 2003), and OsHKT4 (Garciadeblás et al., 2003). Taking into account the K+ and Na+ concentrations that can be expected in xylem and apoplast (Almeida and Huber, 1999; Grignon and Sentenac, 1991; Watson et al., 2001) the suitability of low-affinity HKT transporters for the function of removing Na+ from the apoplast is clear. Less clear is the suitability of the high-affinity transporters to this function although TaHKT1 (Schachtman and Schroeder, 1994) and OsHKT1 (Garciadeblás et al., 2003) are expressed in shoots. However, as already mentioned, high-affinity HKT transporters may transport Na+ in different modes and a comprehensive understanding of the functions of these transporters needs more extensive research.
HKT transporters across the species
The two plants whose genomes have been sequenced, A. thaliana and rice, are quite different regarding the number of existing HKT genes. In rice, there are eight HKT transporters that can be assigned either to the high-affinity or to the low-affinity groups, and the roots carry out a rapid, high-affinity Na+ uptake (Garciadeblás et al., 2003). By contrast, in the genome of A. thaliana there is only one HKT gene and the encoded transporter exhibits low-affinity for Na+ (Uozumi et al., 2000). Although information is still very limited, the comparison of rice and Arabidopsis suggests the existence of two plant models regarding Na+ transport. In the two models, HKT transporters would be involved in Na+ transport across the plasma membranes of different types of internal cells (xylem parenchyma, bundle sheath, companion, pith) but only in the rice model would high-affinity HKT transporters be expressed and mediate Na+ uptake in root epidermal and cortical cells.
Regarding other plant species, Eucalyptus camaldulensis (Liu et al., 2001) and M. crystallinum (Su et al., 2003, and accession number AY231175) have at least two genes, and the study of EST databases suggests that HKT genes may be present in most vascular plants. In rice, in which many ESTs have been identified, HKT ESTs are not abundant, which suggests that only in plants with a high number of sequenced ESTs the identification of HKT ESTs is probable. In dicotyledonous species most of the ESTs belong to a single gene, but Medicago truncatula L. has at least two HKT genes (EST accession numbers, BF632626 and CX528138).
|
High-affinity K+ or Na+ ATPases |
|---|
|
TopAbstractIntroductionK+ transportNa+ uptakeHigh-affinity K+ or Na+...Problems in the functional...OutlookReferences |
|---|
In some fungi, high-affinity K+ and Na+ uptake is mediated by P-type ATPases. The K+ and Na+ Kms of these ATPases are very low (perhaps less than 1 µM) and can mediate the uptake of these cations down to extremely low concentrations (Benito et al., 2004
). The existence of this type of P-type ATPase has not been reported in plants and no genes encoding them exist in the Arabidopsis or rice genomes. Therefore, there is currently no reason to predict their existence in plants, but neither can their presence be ruled out. It is worth observing that the Na+-ATPase described in Physcomitrella patens mediates Na+ efflux, but not Na+ uptake (Benito and Rodríguez-Navarro, 2003). In any case, the existence of K+ or Na+-uptake ATPases in fungi, which undertake the same function as other systems do in plants, suggests that the capacity to take up K+ and Na+ from the soil solution when these cations are at very low concentrations was of such selective advantage during evolution of terrestrial organisms that different systems evolved to fulfil to the same function. |
Problems in the functional identification of K+ and Na+ transporters |
|---|
|
TopAbstractIntroductionK+ transportNa+ uptakeHigh-affinity K+ or Na+...Problems in the functional...OutlookReferences |
|---|
In the case of K+ and Na+ transporters the power of genomics has been hampered by the difficulties underlying the functional studies of these genes. Unfortunately, the two obvious approaches, gene knockout and expression in heterologous systems, present problems that do not generally occur with other genes. In this review, several examples of these problems have been cited, and especially important are those that may be found in the use of yeast mutants for expressing K+ transporters.
The problem of gene knockout is the pleiotropic effect caused by mutations that affect K+ transporters. In fungi, it is known that the disruption of the TRK (Madrid et al., 1998; Mulet et al., 2004) but not HAK genes (Bañuelos et al., 2000) produces hyperpolarization and a consequent enhancement of K+ uptake through non-K+ transporters (Madrid et al., 1998). In addition, alteration of K+ transport is related to multistability of the fungal growth pattern and can produce incomplete penetrance and variable expressivity of growth defects (Lalucque and Silar, 2004). In the case of transporters that are expressed in internal membranes (this may be the case of some KT-HAK-KUP transporters) and involved in the regulation of cellular pH, the disruption may affect vesicle trafficking (Brett et al., 2005) and also result in multiple responses. As far as is known, these problems have not been reported in plants, but possibly only because they have not been investigated.
The problems that have arisen with the use of heterologous expression systems have been previously described (Dreyer et al., 1999), and very little can be added except for the use of yeast mutants defective in K+ uptake (trk1 trk2 mutants). In addition to the problems that result from their highly hyperpolarized state, these mutants are quite unstable and revert to a condition requiring much less K+ to grow. After cloning a cDNA it is possible to pick up a revertant and reach the conclusion that the cloned cDNA encodes a K+ transporter. Unless the expressed transporter exhibits a very low Km (1–100 µM K+), the plasmid must be cured and afterwards it must be checked that the recipient clone is still K+-dependent. The reason for this behaviour is not clear, but it is known that trk1 trk2 mutants that originally keep a low-affinity K+ transport lose it if additional mutations on the PPZ1 or PPZ2 genes are introduced (Ruiz et al., 2004).
|
Outlook |
|---|
|
TopAbstractIntroductionK+ transportNa+ uptakeHigh-affinity K+ or Na+...Problems in the functional...OutlookReferences |
|---|
Over the last few years, the field of high-affinity K+ uptake in plant roots has experienced significant progress and high-affinity Na+ uptake has emerged as a new process that deserves further study, although its physiological importance is currently unknown. In addition to the models that this progress has originated and their importance for the emergence of new paradigms, the progress is also relevant because it has involved new techniques and approaches, which allow prediction of future rapid progress in the field. Good examples are some of the genes or plant mutants described in this review. The current model that is proposed here (Fig. 3) may not be entirely correct but is testable and a starting point for new working hypotheses. All this is well ahead of the knowledge of low-affinity K+ and Na+ transporters. Arabidopsis (Shin and Schachtman, 2004
) and other plant species (Rodríguez-Navarro, 2000) grown under K+-sufficient conditions exhibit low-affinity kinetics for Rb+ or Na+ influx, but thus far it cannot be said with certainty what protein mediates these influxes. Similarly, the proteins that mediate many of the processes of cellular Na+ uptake that are well described in the references cited above under the heading ‘Na+ transport within the plant’ are also unknown. The authors' proposal that HKT transporters are involved obviously needs further investigation. A technical problem is that the study of these transporters in yeast may be difficult because the yeast mutants that are available for expressing K+ or Na+ transporters have intrinsic low-affinity transporters (Madrid et al., 1998) that exhibit a high Vmax and may dominate the uptake over the activity of the plant transporter (Santa-María et al., 1997; Rubio et al., 2000).
|
|
References |
|---|
|
TopAbstractIntroductionK+ transportNa+ uptakeHigh-affinity K+ or Na+...Problems in the functional...OutlookReferences |
|---|
Ahn SJ, Shin R, Schachtman DP. 2004. Expression of KT/KUP genes in Arabidopsis and the role of root hairs K+ uptake. Plant Physiology 134, 1135–1145.
Almeida DPF, Huber DJ. 1999. Apoplastic pH and inorganic ion levels in tomato fruit: a potential means for regulation of cell wall metabolism during ripening. Physiologia Plantarum 105, 506–512.[CrossRef]
Amtmann A, Armengaud P, Volkov V. 2004. Potassium nutrition and salt stress. In: Blatt MR, ed. Membrane transport in plants. Oxford: Blackwell Publishing 293–339.
Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF. 1992. Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, USA 89, 3736–3740.
Armengaud P, Breitling R, Amtmann A. 2004. The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiology 136, 2556–2576.
Baev D, Rivetta A, Vylkova S, Sun JN, Zeng G-F, Slayman CL, Edgerton M. 2004. The TRK1 potassium transporter is the critical effector for killing of Candida albicans by the cationic protein, Histatin 5. Journal of Biological Chemistry 279, 55060–55072.
Bañuelos MA, Garciadeblas B, Cubero B, Rodríguez-Navarro A. 2002. Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiology 130, 784–795.
Bañuelos MA, Madrid R, Rodríguez-Navarro A. 2000. Individual functions of the HAK and TRK potassium transporters of Schwanniomyces occidentalis. Molecular Microbiology 37, 671–679.[CrossRef][Web of Science][Medline]
Bellando M, Marrè MT, Sacco S, Talaricio A, Venegoni A, Marrè E. 1995. Transmembrane potential-mediated coupling between H+ pump operation and K+ fluxes in Elodea densa leaves hyperpolarized by fusicoccin, light or acid load. Plant, Cell and Environment 18, 963–976.[CrossRef]
Benito B, Garciadeblás B, Schreier P, Rodríguez-Navarro A. 2004. Novel P-type ATPases mediate high-affinity potassium or sodium uptake in fungi. Eukaryotic Cell 3, 359–368.
Benito B, Rodríguez-Navarro A. 2003. Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens. The Plant Journal 36, 382–389.[CrossRef][Web of Science][Medline]
Berthomieu P, Conejero G, Nublat A, et al. 2003. Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO Journal 22, 2004–2014.[CrossRef][Web of Science][Medline]
Blackwell M. 2000. Terrestrial life- fungal from the start? Science 289, 1884–1885.[CrossRef][Web of Science][Medline]
Blatt MR. 1985. Extracellular potassium activity in attached leaves and its relation to stomatal function. Journal of Experimental Botany 36, 240–251.
Blatt MR. 2000. Cellular signaling and volume control in stomatal movements in plants. Annual Review of Cell and Developmental Biology 16, 221–241.[CrossRef][Web of Science][Medline]
Blom-Zandstra M, Vogelzang SA, Veen BW. 1998. Sodium fluxes in sweet peper exposed to varying sodium concentration. Journal of Experimental Botany 49, 1863–1868.
Blumwald E, Aharon GS, Apse MP. 2000. Sodium transport in plant cells. Biochimica et Biophysca Acta 1465, 140–151.
Brett CL, Tukaye DN, Mukherjee S, Rao R. 2005. The yeast endosomal Na+ (K+)/H+ exchanger Nhx1 regulates cellular pH to control vesicle trafficking. Molecular Biology of the Cell 16, 1396–1405.
Brüggemann L, Dietrich P, Becker D, Dreyer I, Palme K, Hedrich R. 1999. Channel-mediated high-affinity K+ uptake into guard cells from Arabidopsis. Proceedings of the National Academy of Sciences, USA 96, 3298–3302.
Carden DE, Walker DJ, Flowers TJ, Miller AJ. 2003. Single-cell measurements of the contribution of cytosolic Na+ and K+ to salt tolerance. Plant Physiology 131, 676–683.
Chérel I. 2004. Regulation of K+ channel activities in plants: from physiological to molecular aspects. Journal of Experimental Botany 55, 337–351.
Cuin TA, Miller AJ, Laurie SA, Leigh RA. 2003. Potassium activities in cell compartments of salt-grown barley leaves. Journal of Experimental Botany 54, 657–661.
Davenport R, James RA, Zakrisson-Plogander A, Tester M, Munns R. 2005. Control of sodium transport in durum wheat. Plant Physiology 137, 807–818.
Davenport RJ, Tester M. 2000. A weakly voltage-dependent, non-selective cation channel mediates toxic sodium influx in wheat. Plant Physiology 122, 823–834.
Demidchik V, Davenport RJ, Tester M. 2002. Non-selective cation channels in plants. Annual Review of Plant Physiology and Plant Molecular Biology 53, 67–107.[CrossRef][Medline]
Diatloff E, Kumar R, Schachtman DP. 1998. Site directed mutagenesis reduces the Na+ affinity of HKT1, a Na+ energized high affinity K+ transporter. FEBS Letters 432, 31–36.[CrossRef][Web of Science][Medline]
Dreyer I, Horeau C, Lemaillet G, Zimmermann S, Bush DR, Rodríguez-Navarro A, Schachtman DP, Spalding EP, Sentenac H, Gaber RF. 1999. Identification and characterization of plant transporters using heterologous expression systems. Journal of Experimental Botany 50, 1073–1078.[Abstract]
Durand M, Lacan D. 1994. Sodium partitioning within the shoot of soybean. Physiologia Plantarum 91, 65–71.
Elumalai RP, Nagpal P, Reed JW. 2002. A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. The Plant Cell 14, 119–131.
Epstein E, Rains DW, Elzam OE. 1963. Resolution of dual mechanisms of potassium absorption by barley roots. Proceedings of the National Academy of Sciences, USA 49, 684–692.
Essah PA, Davenport R, Tester M. 2003. Sodium influx and accumulation in Arabidopsis. Plant Physiology 133, 307–318.
Fairbairn DJ, Liu W, Schachtman DP, Gomez-Gallego S, Day SR, Teasdale RD. 2000. Characterization of two distinct HKT1-like potassium transporters from Eucalyptus camaldulensis. Plant Molecular Biology 43, 515–525.[CrossRef][Web of Science][Medline]
Flowers TJ, Läuchli A. 1983. Sodium versus potassium: substitution and compartmentation. In: Läuchli A, Bieleski RL, eds. Inorganic plant nutrition, Vol. 15B. Berlin: Springer-Verlag, 651–681.
Fu H-H, Luan S. 1998. AtKUP1: a dual affinity K+ transporter from Arabidopsis. The Plant Cell 10, 63–73.
Garciadeblas B, Benito B, Rodríguez-Navarro A. 2002. Molecular cloning and functional expression in bacteria of the potassium transporters CnHAK1 and CnHAK2 of the seagrass Cymodocea nodosa. Plant Molecular Biology 50, 623–633.[CrossRef][Web of Science][Medline]
Garciadeblás B, Senn ME, Bañuelos MA, Rodríguez-Navarro A. 2003. Sodium transport and HKT transporters: the rice model. The Plant Journal 34, 788–801.[CrossRef][Web of Science][Medline]
Gassmann W, Rubio F, Schroeder JI. 1996. Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. The Plant Journal 10, 869–882.[CrossRef][Web of Science][Medline]
Gierth M, Maser P, Schroeder JI. 2005. The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiology 137, 1105–1114.
Glass A. 1978. The regulation of K+ influx into intact roots of barley (Hordeum vulgare (L) cv. Conquest) by internal K+. Canadian Journal of Botany 56, 1759–1764.
Glass ADM, Dunlop J. 1978. The influence of potassium content on the kinetics of potassium influx into excised ryegrass and barley roots. Planta 141, 117–119.[CrossRef]
Golldack D, Su H, Quigley F, Kamasani UR, Muñoz-Garay C, Balderas E, Popova OV, Bennett J, Bohnert HJ, Pantoja O. 2002. Characterization of a HKT-type transporter in rice as a general alkali cation transporter. The Plant Journal 31, 529–542.[CrossRef][Web of Science][Medline]
Gong J-M, Waner DA, Horie T, Li SL, Horie R, Abid KB, Schroeder JI. 2004. Microarray-based rapid cloning of an ion accumulation deletion mutant in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 101, 15404–15409.
Grignon C, Sentenac H. 1991. pH and ionic conditions in the apoplast. Annual Review of Plant Physiology and Plant Molecular Biology 42, 103–128.[CrossRef][Web of Science]
Haro R, Bañuelos MA, Senn ME, Barrero-Gil J, Rodríguez-Navarro A. 2005. HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast. Plant Physiology 139, 1495–1506.
Haro R, Rodríguez-Navarro A. 2002. Molecular analysis of the mechanism of potassium uptake through the TRK1 transporter of Saccharomyces cerevisiae. Biochimica et Biophysica Acta 1564, 114–122.[Medline]
Haro R, Rodríguez-Navarro A. 2003. Functional analysis of the M2D helix of the TRK1 potassium transporter of Saccharomyces cerevisiae. Biochimica et Biophysica Acta 1613, 1–6.[Medline]
Hayes DE, Smith FA, Walker NA. 2001. High-affinity potassium transport into wheat roots involves sodium: a role for HKT1? Australian Journal of Plant Physiology 28, 643–652.
Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129–1133.[CrossRef][Web of Science][Medline]
Hirsch RE, Lewis BD, Spalding EP, Sussman MR. 1998. A role for the AKT1 potassium channel in plant nutrition. Science 280, 918–921.
Horie T, Schroeder JI. 2004. Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiology 136, 2457–2462.
Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A. 2001. Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. The Plant Journal 27, 115–128.[CrossRef][Web of Science][Medline]
Jeschke WD, Pate JS. 1991. Cation and chloride partitioning through xylem and phloem within the whole plant of Ricinus communis L. under conditions of salt stress. Journal of Experimental Botany 42, 1105–1116.
Jeschke WD, Wolf O, Hartung W. 1992. Effect of NaCl salinity on flows and partitioning of C, N, and mineral ions in whole plants of white lupin, Lupinus albus. Journal of Experimental Botany 43, 777–788.
Johanson JG, Cheeseman JM. 1983. Uptake and distribution of sodium and potassium by corn seedlings. I. Role of the mesocotyl in ‘sodium exclusion’. Plant Physiology 73, 153–158.
Johanson JG, Cheeseman JM, Enkoji C. 1983. Uptake and distribution of sodium and potassium by corn seedlings. II. Ion transport within the mesocotyl. Plant Physiology 73, 159–164.
Kato Y, Sakaguchi M, Mori Y, Saito K, Nakamura T, Bakker EP, Sato Y, Goshima S, Uozumi N. 2001. Evidence in support of a four transmembrane-pore-transmembrane topology model for the Arabidopsis thaliana Na+/K+ translocating AtHKT1 protein, a member of the superfamily of K+ transporters. Proceedings of the National Academy of Sciences, USA 98, 6488–6493.
Keunecke M, Linder B, Seydel U, Schulz A, Hansen UP. 2001. Bundle sheath cells of small veins in maize leaves are the location of uptake from the xylem. Jounal of Experimental Botany 52, 709–714.
Kim EJ, Kwak JM, Uozumi N, Schroeder JI. 1998. AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. The Plant Cell 10, 51–62.
Kochian LV, Lucas WJ. 1988. Potassium transport in roots. Advances in Botanical Research 15, 93–178.
Kramer D, Läuchli A, Yeo AR, Gullasch J. 1977. Transfer cells in roots of Phaseolus coccineus: ultrastructure and possible function in exclusion of sodium from the shoot. Annals of Botany 41, 1031–1040.
Kramer EM. 2004. PIN and AUX/LAX proteins: their role in auxin accumulation. Trends in Plant Science 9, 578–582.[CrossRef][Web of Science][Medline]
Kuroda T, Bihler H, Bashi E, Slayman CL, Rivetta A. 2004. Chloride channel function in the yeast TRK-potassium transporters. Journal of Membrane Biology 198, 177–192.[CrossRef][Web of Science][Medline]
Lacan D, Durand M. 1995. Na+ and K+ transport in excised soybean roots. Physiologia Plantarum 93, 132–138.
Lacan D, Durand M. 1996. Na+-K+ exchange at the xylem/symplast boundary: its significance in the salt sensitivity of soybean. Plant Physiology 110, 705–711.[Abstract]
Lalucque H, Silar P. 2004. Incomplete penetrance and variable expressivity of a growth deffect as a consequence of knocking out two K+ transporers in the euascomycete fungus Podospora anserina. Genetics 166, 125–133.
Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA. 2002. A role for HKT1 in sodium uptake by wheat roots. The Plant Journal 32, 139–149.[CrossRef][Web of Science][Medline]
Leigh RA, Wyn Jones RG. 1984. A hypothesis relating critical potassium concentrations for growth to the distribution and function of this ion in the plant cell. New Phytologist 97, 1–13.[CrossRef][Web of Science]
Liu W, Fairbairn DJ, Reid RJ, Schachtman DP. 2001. Characterization of two HKT1 homologues from Eucalyptus camaldulensis that display intrinsic osmosensing capability. Plant Physiology 127, 283–294.
Liu W, Schachtman DP, Zhang W. 2000. Partial deletion of a loop region in the high affinity K+ transporter HKT1 changes ionic permeability leading to increased salt tolerance. Journal of Biological Chemistry 275, 27924–27932.
Maathuis FJM, Sanders D. 2001. Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiology 127, 1617–1625.
Maathuis FJM, Verlin D, Smith FA, Sanders D, Fernández JA, Walker NA. 1996. The physiological relevance of Na+-coupled K+-transport. Plant Physiology 112, 1609–1616.[Abstract]
Madrid R, Gómez MJ, Ramos J, Rodríguez-Navarro A. 1998. Ectopic potassium uptake in trk1 trk2 mutants of Saccharomyces cerevisiae correlates with a highly hyperpolarized membrane potential. Journal of Biological Chemistry 273, 14838–14844.
Martínez-Cordero MA, Martínez V, Rubio F. 2004. Cloning and functional characterization of the high-affinity K+ transporter HAK1 of pepper. Plant Molecular Biology 56, 413–421.[CrossRef][Web of Science][Medline]
Martínez-Cordero MA, Martínez V, Rubio F. 2005. High-affinity K+ uptake in pepper plants Journal of Experimental Botany 56, 1553–1562.
Mäser P, Eckelmann B, Vaidyanathan R, et al. 2002a. Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Letters 531, 157–161.[CrossRef][Web of Science][Medline]
Mäser P, Gierth M, Schroeder JI. 2002b. Molecular mechanisms of potassium and sodium uptake in plants. Plant and Soil 247, 43–54.[CrossRef][Web of Science]
Mäser P, Hosoo Y, Goshima S, et al. 2002c. Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per subunit HKT transporters from plants. Proceedings of the National Academy of Sciences, USA 99, 6428–6433.
Mäser P, Thomine S, Schroeder JI, et al. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiology 126, 1646–1667.
Mulet JM, Alejandro S, Romero C, Serrano R. 2004. The trehalose pathway and intracellular glucose phosphates as modulators of potassium transport and general cation homeostasis in yeast. Yeast 21, 569–582.[CrossRef][Web of Science][Medline]
Nickrent DL, Parkinson CL, Palmer JD, Duff RJ. 2000. Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Molecular Biology and Evolution 17, 1885–1895.
Osmond CB, Laties GG. 1968. Interpretation of the dual isotherm for ion absorption in beet tissue. Plant Physiology 43, 747–755.
Qiu Y-L, Palmer JD. 1999. Phylogeny of early land plants: insights from genes and genomes. Trends in Plant Science 4, 26–29.[CrossRef][Web of Science][Medline]
Quintero J, Blatt MR. 1997. A new family of K+ transporters from Arabidopsis that are conserved across phyla. FEBS Letters 415, 206–211.[CrossRef][Web of Science][Medline]
Rains DW, Epstein E. 1967a. Sodium absorption by barley roots: role of the dual mechanisms of alkali cation transport. Plant Physiology 42, 314–318.[Medline]
Rains DW, Epstein E. 1967b. Sodium absorption by barley roots: its mediation by mechanism 2 of alkali cation transport. Plant Physiology 42, 319–323.[Medline]
Reed NR, Bonner BA. 1974. The effect of abscisic acid on the uptake of potassium and chloride in Avena coleoptile sections. Planta 116, 173–185.[CrossRef]
Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann KA, Grabov A, Dolan L, Hatzopoulos P. 2001. TRH1 encodes a potassium transporter requiered for tip growth in Arabidopsis root hairs. The Plant Cell 13, 139–151.
Rodríguez-Navarro A. 2000. Potassium transport in fungi and plants. Biochimica et Biophysica Acta 1469, 1–30.[Medline]
Rodríguez-Navarro A, Blatt MR, Slayman CL. 1986. A potassium–proton symport in Neurospora crassa. The Journal of General Physiology 87, 649–674.
Rubio F, Gassmann W, Schroeder JI. 1995. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270, 1660–1663.
Rubio F, Gassmann W, Schroeder JI. 1996. High-affinity potassium uptake in plants. Response. Science 273, 978–979.
Rubio F, Santa-María GE, Rodríguez-Navarro A. 2000. Cloning of Arabidopsis and barley cDNAs encoding HAK potasium transporters in root and shoot cells. Physiologia Plantarum 109, 34–43.[CrossRef]
Rubio F, Schwarz M, Gassmann W, Schroeder JI. 1999. Genetic selection of mutations in the high affinity K+ transporter HKT1 that define functions of a loop site for reduced Na+ permeability and increased Na+ tolerance. Journal of Biological Chemistry 274, 6839–6847.
Ruiz A, Ruiz MC, Sánchez-Garrido MA, Ariño J, Ramos J. 2004. The Ppz protein phosphatases regulate Trk-independent potassium influx in yeast. Yeast 578, 58–62.
Rus A, Lee B, Muñoz-Mayor A, Sharkhuu A, Miura K, Zhu J-K, Bressan RA, Hasegawa PM. 2004. AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiology 136, 2500–2511.
Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee B, Matsumoto TK, Koiwa H, Zhu J-K, Bressan RA, Hasegawa PH. 2001. AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proceedings of the National Academy of Sciences, USA 98, 14150–14155.
Sanderson MJ. 2003. Molecular data from 27 proteins do not support a Precambrian origin of land plants. American Journal of Botany 90, 954–956.
Santa-María GE, Danna CH, Czibener C. 2000. High-affinity potassium transport in barley roots: ammonium-sensitive and -insensitive pathways. Plant Physiology 123, 297–306.
Santa-María GE, Rubio F, Dubcovsky J, Rodríguez-Navarro A. 1997. The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. The Plant Cell 9, 2281–2289.[Abstract]
Schachtman DP. 2000. Molecular insights into the structure and function of plant K+ transport mechanisms. Biochimica et Biophysica Acta 1465, 127–139.[Medline]
Schachtman DP, Schroeder JI. 1994. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370, 655–658.[CrossRef][Medline]
Senn ME, Rubio F, Bañuelos MA, Rodríguez-Navarro A. 2001. Comparative functional features of plant potassium HvHAK1 and HvHAK2 transporters. Journal of Biological Chemistry 276, 44563–44569.
Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon J-M, Gaymard F, Grignon C. 1992. Cloning and expression in yeast of a plant potassium ion transport system. Science 256, 663–665.
Shabala S. 2003. Regulation of potassium transport in leaves: from molecular to tissue level. Annals of Botany 92, 627–634.
Shin R, Schachtman DP. 2004. Hydrogen peroxide mediates plant root cells response to nutrient deprivation. Proceedings of the National Academy of Sciences, USA 101, 8827–8832.
Smith RC, Epstein E. 1964. Ion absorption by shoot tissue: kinetics of potassium and rubidium absorption by corn leaf tissue. Plant Physiology 39, 992–996.
Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR, Lewis BD. 1999. Potassium uptake supporting plant growth in the absence of AKT1 channel activity. Inhibition by ammonium and stimulation by sodium. The Journal of General Physiology 113, 909–918.
Su H, Balderas E, Vera-Estrella R, Golldack D, Quigley F, Zhao C, Pantoja O, Bohnert HJ. 2003. Expression of the cation transporter McHKT1 in a halophyte. Plant Molecular Biology 52, 967–980.[CrossRef][Web of Science][Medline]
Su H, Golldack D, Zhao C, Bohnert HJ. 2002. The expression of HAK-type K+ transporter is regulated in response to salinity stress in common ice plant. Plant Physiology 129, 1482–1493.
Subbarao GV, Ito O, Berry WL, Wheeler RM. 2003. Sodium: a functional plant nutrient. Critical Reviews in Plant Sciences 22, 391–416.
Tester M, Davenport R. 2003. Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
Tester M, Leigh RA. 2001. Partitioning of nutrient transport processes in roots. Journal of Experimental Botany 52, 445–457.
Tyerman SD, Skerrett IM. 1999. Root ion channels and salinity. Scientia Horticulturae 78, 175–235.
Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker EP, Nakamura T, Schroeder JL. 2000. The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiology 122, 1249–1259.
Véry A-A, Sentenac H. 2002. Cation channels in the Arabidopsis plasma membrane. Trends in Plant Science 7, 168–175.[CrossRef][Web of Science][Medline]
Véry A-A, Sentenac H. 2003. Molecular mechanisms and regulation of K+ transport in higher plants. Annual Review of Plant Biology 54, 575–603.[CrossRef][Medline]
Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A. 2004. Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. The Plant Journal 40, 523–535.[CrossRef][Web of Science][Medline]
Walker DJ, Black CR, Miller AJ. 1998. The role of cytosolic potassium and pH in the growth of barley roots. Plant Physiology 118, 957–964.
Walker DJ, Leigh RA, Miller AJ. 1996a. Potassium homeostasis in vacuolate plant cells. Proceedings of the National Academy of Sciences, USA 93, 10510–10514.
Walker NA, Sanders D, Maathuis FJM. 1996b. High-affinity potassium uptake in plants. Science 273, 977–978.[CrossRef][Web of Science][Medline]
Wang T-B, Gassmann W, Rubio F, Schroeder JI, Glass ADM. 1998. Rapid up-regulation of HKT1, a high-affinity potassium transporter gene, in roots of barley and wheat following withdrawal of potassium. Plant Physiology 118, 651–659.
Watson R, Pritchard J, Malone M. 2001. Direct measurement of sodium and potassium in the transpirating stream of salt-excluding and non-excluding varieties of wheat. Journal of Experimental Botany 52, 1873–1881.
Wolf O, Munns R, Tonnet ML, Jeschke WD. 1991. The role of the stem in the partitioning of Na+ and K+ in salt-treated barley. Journal of Experimental Botany 42, 697–704.
Zeng G-F, Pypaert M, Slayman CL. 2004. Epitope tagging of the yeast K+ carrier Trk2p demonstrates folding that is consistent with a channel-like structure. Journal of Biological Chemistry 279, 3003–3013.
Zhu Y-G, Smolders E. 2000. Plant uptake of radiocaesium: a review of mechanisms, regulation and application. Journal of Experimental Botany 51, 1635–1645.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  M. Jabnoune, S. Espeout, D. Mieulet, C. Fizames, J.-L. Verdeil, G. Conejero, A. Rodriguez-Navarro, H. Sentenac, E. Guiderdoni, C. Abdelly, et al. Diversity in Expression Patterns and Functional Properties in the Rice HKT Transporter Family Plant Physiology, August 1, 2009; 150(4): 1955 - 1971. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Malagoli, D. T. Britto, L. M. Schulze, and H. J. Kronzucker Futile Na+ cycling at the root plasma membrane in rice (Oryza sativa L.): kinetics, energetics, and relationship to salinity tolerance J. Exp. Bot., November 1, 2008; 59(15): 4109 - 4117. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Zhao, N.-H. Cheng, C. M. Motes, E. B. Blancaflor, M. Moore, N. Gonzales, S. Padmanaban, H. Sze, J. M. Ward, and K. D. Hirschi AtCHX13 Is a Plasma Membrane K+ Transporter Plant Physiology, October 1, 2008; 148(2): 796 - 807. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. W. Szczerba, D. T. Britto, S. A. Ali, K. D. Balkos, and H. J. Kronzucker NH4+-stimulated and -inhibited components of K+ transport in rice (Oryza sativa L.) J. Exp. Bot., September 1, 2008; 59(12): 3415 - 3423. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. J. Kronzucker, M. W. Szczerba, L. M. Schulze, and D. T. Britto Non-reciprocal interactions between K+ and Na+ ions in barley (Hordeum vulgare L.) J. Exp. Bot., July 1, 2008; 59(10): 2793 - 2801. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. A. Banuelos, R. Haro, A. Fraile-Escanciano, and A. Rodriguez-Navarro Effects of Polylinker uATGs on the Function of Grass HKT1 Transporters Expressed in Yeast Cells Plant Cell Physiol., July 1, 2008; 49(7): 1128 - 1132. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. C. Collins, F. Tardieu, and R. Tuberosa Quantitative Trait Loci and Crop Performance under Abiotic Stress: Where Do We Stand? Plant Physiology, June 1, 2008; 147(2): 469 - 486. [Full Text] [PDF]
|
|
|
|
|
|
S. Huang, W. Spielmeyer, E. S. Lagudah, and R. Munns Comparative mapping of HKT genes in wheat, barley, and rice, key determinants of Na+ transport, and salt tolerance J. Exp. Bot., March 5, 2008; (2008) ern033v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-M. Wang, J.-L. Zhang, and T. J. Flowers Low-Affinity Na+ Uptake in the Halophyte Suaeda maritima Plant Physiology, October 1, 2007; 145(2): 559 - 571. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Prista, J. C. Gonzalez-Hernandez, J. Ramos, and M. C. Loureiro-Dias Cloning and characterization of two K+ transporters of Debaryomyces hansenii Microbiology, September 1, 2007; 153(9): 3034 - 3043. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Lunde, D. P. Drew, A. K. Jacobs, and M. Tester Exclusion of Na+ via Sodium ATPase (PpENA1) Ensures Normal Growth of Physcomitrella patens under Moderate Salt Stress Plant Physiology, August 1, 2007; 144(4): 1786 - 1796. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Grabov Plant KT/KUP/HAK Potassium Transporters: Single Family - Multiple Functions Ann. Bot., June 1, 2007; 99(6): 1035 - 1041. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Byrt, J. D. Platten, W. Spielmeyer, R. A. James, E. S. Lagudah, E. S. Dennis, M. Tester, and R. Munns HKT1;5-Like Cation Transporters Linked to Na+ Exclusion Loci in Wheat, Nax2 and Kna1 Plant Physiology, April 1, 2007; 143(4): 1918 - 1928. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Hirose, N. Makita, M. Kojima, T. Kamada-Nobusada, and H. Sakakibara Overexpression of a Type-A Response Regulator Alters Rice Morphology and Cytokinin Metabolism Plant Cell Physiol., March 1, 2007; 48(3): 523 - 539. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Md. A. Kader, T. Seidel, D. Golldack, and S. Lindberg Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars J. Exp. Bot., December 1, 2006; 57(15): 4257 - 4268. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Huang, W. Spielmeyer, E. S. Lagudah, R. A. James, J. D. Platten, E. S. Dennis, and R. Munns A Sodium Transporter (HKT7) Is a Candidate for Nax1, a Gene for Salt Tolerance in Durum Wheat Plant Physiology, December 1, 2006; 142(4): 1718 - 1727. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||