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Inhibition by Ammonium and Stimulation by Sodium
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,,|| Program in Cell and Molecular Biology, Department of Horticulture, and || Biotechnology Center, University of Wisconsin, Madison, Wisconsin 53706
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Key Words: Arabidopsis • plant nutrition • root • transferred-DNA insertion mutant
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). It is their most abundant inorganic constituent, contributing importantly to the osmotic potential and electrolytic character of cytoplasm. The plasma membrane is typically more permeable to K+ than to other ions, so the difference in its concentration across the membrane has a large influence on the membrane potential and, hence, cell physiology. Another reason for its essentiality is that some enzymes require K+ as a cofactor.
The mechanism by which cells concentrate K+ from dilute extracellular sources such as soil has received considerable attention because plant growth depends directly on it. Early kinetic studies by Epstein et al. (1963) gave evidence of two distinct uptake mechanisms: a high affinity system operating over micromolar concentration ranges and a low affinity system that predominates when [K+]ext is in the millimolar range. Recent measurements of K+ electrochemical potential gradients were incorporated into this classical model to create the widely held view that active transport is necessary when [K+]ext is less than 
300 µM, but that a passive mechanism suffices at higher values of [K+]ext (Maathuis and Sanders, 1993, 1994, 1997; Walker et al., 1996a). This important thermodynamic information was readily integrated with ground-breaking molecular advances occurring at about the same time. Genes encoding passive K+ channels and active K+ cotransporters were cloned by complementation of yeast mutants, functionally characterized after heterologous or ectopic expression, and demonstrated to be expressed in roots (reviewed in Smart et al., 1996; de Boer, 1999). These advances collectively gave rise to the dominant view that transporters such as HKT1 (Schachtman and Schroeder, 1994; Rubio et al., 1995; Gassmann et al., 1996; Wang et al., 1998) and the KUP family (Quintero and Blatt, 1997; Santa-Maria et al., 1997; Fu and Luan, 1998; Kim et al., 1998) are responsible for "high affinity" K+ uptake and that inward-rectifying K+ channels such as AKT1 (Sentenac et al., 1992; Basset et al., 1995; Lagarde et al., 1996) mediated uptake when K+ was more concentrated than 300 µM.
This paradigm was shown to require modification when an Arabidopsis mutant lacking detectable AKT1 channel activity (akt1) was found to be defective in K+ uptake and growth on solutions as dilute as 10 µM K+, a concentration previously thought to be well outside the realm of possibilities for channels (Hirsch et al., 1998). However, measurements of membrane potentials more negative than –230 mV in Arabidopsis roots demonstrated that uptake of K+ from 10 µM solutions by channels was indeed energetically feasible, at least in cells near the root apex (Hirsch et al., 1998). Now it seems reasonable to view inward-rectifying K+ channels as passive uptake mechanisms capable of conducting growth-supporting K+ fluxes in the high-affinity concentration range, provided that the K+ electrochemical potential gradient is inward.
The existence of a mutant lacking inward-rectifying K+ channels in the root provides an opportunity to dissect genetically the channel-mediated contribution to K+ uptake from that of other transporters, and to determine the significance of each under various ionic conditions a plant may encounter. A condition meriting close attention in this respect is the presence of NH4+, as Hirsch et al. (1998) found it must be present to observe the akt1 phenotype (poor growth relative to wild type on [K+]ext < 0.1 mM). In the absence of NH4+, mutant and wild type grow similarly. This would be expected if NH4+ inhibited a K+ transport mechanism that operates in parallel with AKT1 and is necessary for growth when AKT1 activity is lacking. There is much support in the literature for this possibility. Inhibitory effects of NH4+ on K+ uptake have been noted (Rufty, et al., 1982; Van Beusichem, 1988) and, in a study of maize roots, Vale et al. (1987) found that K+ uptake was comprised of NH4+-sensitive and NH4+-insensitive components. Smith and Epstein (1964) presented evidence that NH4+ inhibited K+ uptake by competing for a binding site on the transporter in maize leaves. However, the converse (K+ inhibition of NH4+ uptake) does not seem to occur, a result that at least one authority considered "quite surprising" (Marschner, 1995). The present work takes advantage of the akt1 mutation to produce an explanation of this relationship between K+, NH4+, and growth.
A related and somewhat controversial topic is the role of Na+ in K+ uptake (Maathuis et al. 1996; Rubio et al., 1996; Walker et al. 1996b). The renewal of interest in Na+–K+ relationships is due to the finding that the HKT1 transporter of barley functions as a Na+-coupled K+ symporter (Rubio et al., 1995; Gassmann et al., 1996), and to genetic advances in understanding the relationship between the ability of a plant to resist Na+ stress and K+ nutritional status (Zhu et al., 1998). The akt1 mutant was used here in studies that shed light on how the uptake mechanisms responsible for growth-sustaining K+ fluxes are importantly influenced by NH4+ and Na+.
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in order to assess the permeability of the membrane to K+. Eq. 1 is a simplified description of the ionic basis of Vm in plant cells:
 | (1) |
GK and EK are the conductance and equilibrium potential for K+, GX and EX represent the conductance and equilibrium potential for all other ions lumped together, and Ipump is the current created by an electrogenic pump (the H+-ATPase in the case of plants). Gtot is the total conductance of the membrane.
Shifts in extracellular KCl concentration ([KCl]ext) were imposed on the root while Vm was recorded continuously. The change in Vm resulting from shifts in [KCl]ext is described by:
 | (2) |
Assuming that an imposed shift in [KCl]ext affects only the K+ and Cl– components, Eq. 2 simplifies to:
 | (3) |
Increasing [KCl]ext caused positive shifts in Vm (see Fig. 1), demonstrating that the membrane was more permeable to K+ than the counterion Cl–, as is typical of plant cells. In the extreme case of a negligible Cl– conductance, Eq. 3 reduces to:
 | (4) |
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Vm resulting from shifts in [KCl]ext is interpreted here as a measure of the relative K+ permeability of the membrane.
The solutions used to bathe the roots were exactly the same solutions used for the growth experiments (below), except agarose was omitted. For experiments that tested the effects of NH4+, Na+, and H+, the mounted seedlings were bathed in the test solution for 2 h before impalement. Rb+ fluxes were also performed exactly as described by Hirsch et al. (1998). Percent inhibition by NH4+ was calculated so that the results of independent trials involving different specific activities could be averaged.
Plant Growth
24 surface-sterilized seeds of either akt1 or the Wassilewskija wild type were sown with equal spacing across square Petri plates containing media (described below) solidified with 0.8% agarose. They were maintained in darkness at 4°C for 48 h before being placed in a growth chamber set to deliver 16 h days and 8 h nights at 21°C. Germination was assayed after 72 h when [K+]ext was 10 or 100 µM (see Fig. 4, A and B), but after only 48 h when [K+]ext was 1,000 µM (Fig. 4 C) because of the faster embryo growth in this condition. A seed was considered to have germinated if emergence of the radicle from the seed coat could be detected with the aid of a 40x dissecting scope. After 4 d of growth, the fresh weight of the group of seedlings was determined to the nearest 0.1 mg, and at 8 d the harvesting/weighing procedure was repeated with a separate plate of seedlings. The difference in mass between the two time points was divided by the number of intervening days to obtain an average growth rate for the group of seedlings between days 4 and 8. Experiments spanning 12 d of growth produced similar results. All data shown are the averages of at least three independent trials.
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150 µm from the apex of the cap with a microelectrode. After the voltage stabilized at –236 mV, the continuously flowing bathing solution containing 10 µM K+ was switched to one containing 100 µM K+, a treatment referred to as [K+]10–100, and then subsequently to 1,000 µM K+ ([K+]100–1000). The change in steady state Vm that occurred in response to these shifts (Vm) is related to the K+ permeability of the plasma membrane as discussed in MATERIALS AND METHODS. The permeability detected by this method in akt1 mutant roots may be attributed to non-AKT1 activities because of the evidence that the mutant allele is functionally a null, despite the transferred-DNA being inserted in what might appear to be a dispensable cytoplasmic tail (Hirsch et al., 1998). The contribution of AKT1 channel activity to the K+ permeability of wild-type roots may be inferred by subtracting the Vm measured in akt1 roots from the wild-type Vm. Following this reasoning, Fig. 1 B shows that the wild-type K+ permeability, in the absence of NH4+, was 63% due to AKT1 channel activity and 37% due to non-AKT1 activities when the shift was [K+]10–100. When assayed at the higher concentration ([K+]100–1,000 shift), the AKT1 component was a similar 55% of the now larger wild-type K+ permeability (Fig. 1 C). Such accounting of the membrane's K+ permeability permitted an examination of which components were affected by NH4+. Approximately 50% of the wild-type Vm resulting from a [K+]10–100 shift was inhibited by 2 mM NH4+. The NH4+-sensitive component of the wild-type response was very similar in magnitude to the minus-NH4+ akt1 response, which was completely blocked by 2 mM NH4+. Thus, the Vm in wild-type roots, a parameter related to K+ permeability, behaves as the quantitative sum of a NH4+-insensitive AKT1 component and a NH4+-sensitive non-AKT1 component. This simple quantitative relationship did not persist when [K+]ext was increased from 100 to 1,000 µM (Fig. 1 C). Instead, it appeared that 2 mM NH4+ inhibited only 50% of the non-AKT1 component, as opposed to 100% at the lower [K+]ext (compare akt1 responses ± NH4+ in Fig. 1, B and C). The actual steady state value of Vm for each genotype in each condition is shown in Table 1.
The finding that the degree of inhibition by 2 mM NH4+ depended on [K+]ext prompted a more detailed investigation of the K+ and NH4+ concentration interdependence of the phenomenon. Fig. 2 demonstrates that 2 mM NH4+ inhibited 50% of the Vm caused by [K+]100–1,000 in akt1 roots, consistent with the data in Fig. 1 C. Only 0.5 mM NH4+ was needed to inhibit 50% of the smaller response to [K+]10–100 and 2 mM was completely inhibitory, consistent with Fig. 1 B. The large Vm response to shifting [K+]ext from 1 to 10 mM was much less sensitive to this range of [NH4+]ext (Fig. 2). Taken together, the results in Figs. 1 and 2 indicate that AKT1 channel activity accounts for 50–60% of the K+ permeability of the root plasma membrane, with the remainder resulting from one or more NH4+-sensitive transporters. Furthermore, the data in Fig. 2 may be taken as evidence that the non-AKT1 transporter has a K+-binding site to which NH4+ may competitively bind when it is in large excess, preventing K+ transport. The 50% block of the response to [K+]100–1,000 by 2 mM NH4+ may be taken as evidence that the K+-binding site of the non-AKT1 mechanism has a 50% probability of being occupied by NH4+ under those particular conditions. This occupancy by NH4+ increased to 100% when [K+]ext was 10-fold lower, and it decreased to near negligible levels when [K+]ext was in the millimolar range.
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90% of Rb+ uptake into akt1 roots from 10 µM solutions was inhibited by treatment with 4 mM NH4+. This inhibition by NH4+ was [Rb+]ext dependent, being only 20% at 1,000 µM Rb+. Thus, fluxes at the organ level (Fig. 3) and electrical changes at the membrane (Figs. 1 and 2) both indicate that NH4+ competitively inhibits one or more important K+-transport mechanisms detectable in the absence of AKT1 channel activity. The data presented thus far indicate that the wild-type root employs at least two K+-uptake mechanisms operating in parallel, each contributing significantly to the total flux even from 10 µM external solutions. One of these "high affinity" transporters is the passive AKT1 channel and the other is an NH4+-sensitive transporter of unknown molecular identity.
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Growth rates of seedlings were also determined under the same conditions. Fig. 5 A demonstrates that in the absence of NH4+, akt1 seedlings grew more slowly than wild type on 10 µM K+, as was the case with the embryo growth responsible for germination (Fig. 4 A). This is evidence that the K+ flux conducted by AKT1 channels contributed significantly to growth even when [K+]ext was 10 µM. Submillimolar NH4+ added to the 10 µM K+ medium inhibited the growth rate of akt1 seedlings, which was too low to measure reliably at concentrations >700 µM. The faster wild-type growth was not inhibited by NH4+ in this concentration range. Embryo growth, assayed as germination rate, behaved similarly with respect to inhibition by NH4+ (Fig. 4 A). When [K+]ext was increased to 100 µM (Fig. 5 B), wild-type and akt1 seedlings grew several times faster than at 10 µM K+, and similar to each other in the absence of NH4+ (as was also the case for embryos). Increasing [NH4+]ext from 0 to 2 mM strongly inhibited the growth rate of akt1 seedlings without affecting the wild-type rate. This inhibition of akt1 growth rate by NH4+ displayed a concentration dependence very similar to the NH4+ inhibition of membrane K+-permeability assayed by [K+]100–1,000 (Fig. 2). This result, along with those in Figs. 2 and 3, supports the idea that NH4+ inhibits growth of akt1 seedlings by inhibiting K+ permeability and fluxes mediated by one or more non-AKT1 transporters. Increasing [K+]ext to 1,000 µM markedly reduced the amount of inhibition caused by NH4+ (Fig. 5 C). Thus, protection against NH4+ inhibition by increasing K+ was observed for seedling growth as it was with K+ permeability, Rb+ fluxes, and embryo growth. This is consistent with the notion that the K+ transport activity supporting growth in the absence of AKT1 channel activity employs at least one substrate (K+) binding site for which NH4+ can compete under physiologically relevant conditions.
Transport Characteristics of the Non-AKT1 Activity
The lack of inward-rectifying channel activity in akt1 roots was exploited in experiments designed to reveal information about what energizes the parallel, NH4+-sensitive, non-AKT1 activity. The approach was to measure Vm in cells of akt1 roots in the absence of NH4+ and administer shifts in [K+]ext. Specifically, the hypothesis to be tested was whether the non-AKT1 K+-transport activity behaved as a coupled transporter, such as a H+-K+ cotransporter (Rodriguez-Navarro et al., 1986; Newman et al., 1987; Maathuis and Sanders, 1994) or a Na+-K+ cotransporter (Schachtman and Schroeder, 1994; Rubio et al., 1995; Gassmann et al., 1996; Wang et al., 1998). Fig. 6 demonstrates that the presence of 2 mM Na+ more than doubled the Vm induced by [K+]10–100 when the pH of the medium was buffered at 5.7. Decreasing the proton concentration to pH 7.7 significantly reduced the magnitude of the Vm (K+ permeability) of akt1 roots, but Na+ stimulation was still observed. Reducing the proton concentration further (pH 8.7) essentially eliminated the response to [K+]10–100 in the absence of Na+, though a measurable Vm could be observed in the presence of Na+. At higher K+ concentrations ([K+]100–1,000), a significant pH dependence of K+ permeability was not detected. The Na+ effect was relatively weaker than observed in the lower K+ conditions, and not significant at the P = 0.05 level. These results are consistent with the non-AKT1 K+ transport occurring by a symport mechanism that is energized by the electrochemical potential gradient of Na+ and H+. Perhaps separate Na+-K+ and H+-K+ symporters function in parallel to actively transport K+. If so, the substrate-binding sites of both must have an affinity for NH4+. Alternatively, a single K+ symporter may be capable of using electrochemical potential gradients of either Na+ or H+ as an energy source. It is also possible that the non-AKT1 transporter has an obligate requirement for both Na+ and H+ to actively transport K+, as our nominally 0 Na+ conditions contain trace amounts (see MATERIALS AND METHODS).
Stimulation of Growth by Na+
The results in Fig. 6 formed the basis of another test of the hypothesis that the K+ permeability detected electrophysiologically in the absence of AKT1 channels (Figs. 1 and 2) represents the uptake pathway upon which growth of akt1 plants depends. Na+ should stimulate growth of akt1 plants if the K+ required for growth is taken up by this Na+-stimulated, NH4+-sensitive, non-AKT1 activity. Furthermore, the growth rate of wild-type plants should be less Na+ dependent, given that a significant portion (50–60%) of wild-type K+ permeability was attributed to AKT1 channels (Fig. 2). Fig. 7 A demonstrates that both of these predicted results were observed when seedlings were grown on 10 µM K+. The growth rate of akt1 plants increased by 119% as [Na+]ext was increased to 1,000 µM. Wild-type seedlings also benefited from increasing [Na+]ext, though not to the same relative extent. At stressful levels of Na+ (50– 100 mM), the growth rates of wild-type and akt1 plants were relatively equally inhibited (data not shown), indicating that the akt1 phenotype is distinct from that of the salt overly-sensitive mutants (Wu et al., 1996; Zhu et al., 1998). The growth rate of akt1 plants was not stimulated by Na+ when [K+]ext was 100 µM. This is consistent with the relatively weaker stimulatory effect of Na+ on K+ permeability when assayed at this higher [K+]ext (Fig. 6 B) and the evidence that, when >100 µM, [K+] is not limiting growth rate (0 NH4+ points in Fig. 5, B and C are similar).
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). It seems reasonable to suppose that other soil conditions encountered by plants may impair AKT1 function, shifting the bulk of K+-uptake activity to the non-AKT1 mechanism.
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, which were based on studies performed before a null mutant was available to exploit. Both AKT1 and non-AKT1 mechanisms clearly contribute in the absence of NH4+ when [K+]ext is 10 or 100 µM (Fig. 1). This is somewhat surprising, given that the enhancement of K+ permeability by Na+ and H+ at low [K+]ext suggests that the non-AKT1 mechanism is an active symporter with K+ transport coupled to the electrochemical potential gradient of one or both of those ions. It would be surprising, though not a violation of any thermodynamic law, if a cotransport mechanism contributed significantly to fluxes that could be conducted by passive channels. It is possible that the non-AKT1 mechanism is also passive and the enhancement of Vm by Na+ and H+ (Fig. 6) is due to a faster transport cycle, higher open probability, or the recruitment of more transporters into action. Interestingly consistent with this notion is the demonstration that Na+ positively modulates the kinetics of AKT1 without permeating the channel (Bertl et al., 1997). Rigorous voltage-clamp studies and Na+ flux measurements are needed to distinguish whether Na+ affects the kinetics or thermodynamics of the non-AKT1 transport mechanism(s). Such a study may reveal that Na+ affects both because the two possibilities are not mutually exclusive. Regardless of how the non-AKT1 transport activity is energized, its inhibition by NH4+ and stimulation by Na+ were mirrored in most conditions by the effects of these ions on the growth of akt1 and, to a much lesser extent, wild-type plants. These close positive and negative correlations constitute evidence that the K+ permeability detected electrically in akt1 roots is due to an activity that supports growth when the AKT1 mechanism is inoperative. The results also indicate that the relative contributions to plant growth of genetically distinct K+ transport systems depend on ionic variables of the sort and magnitude encountered in soils. This finding may be relevant to the agronomic practice of managing plant nutrients. There is every reason to believe that continuing the combined electrophysiological and reverse-genetic approach will lead to a more complete and useful molecular-level accounting of the K+-transport activities supporting growth.
The reverse-genetic approach to studying the non-AKT1 contributor requires knowing beforehand what gene or genes to eliminate. Therefore, it is now very important to consider what genes may be responsible for the non-AKT1 transport activity characterized physiologically by the present work. The recent impressive isolation and characterization of plant genes encoding proteins that perform K+ transport has produced two strong candidates. The stimulation by Na+ (Fig. 6) brings the HKT1 transporter originally found in wheat to the forefront as a candidate for the non-AKT1 activity. HKT1 is believed to function as a K+-Na+ symporter (Rubio et al., 1995; Gassmann et al., 1996). The earlier report of H+ gradients serving as an energy source for HKT1-mediated K+ transport (Schachtman and Schroeder, 1998) also can be accommodated by the pH dependence of the non-AKT1 activity (Fig. 6). Unfortunately, the present literature on HKT1 does not contain tests of NH4+ as an inhibitor. Ideally, an Arabidopsis mutant with a disruption in an HKT1 homologue will be isolated and provide for a combined genetic and physiological test of the idea that AKT1 and HKT1 together conduct the K+ fluxes needed for growth.
The increase in K+ permeability due to the presence of Na+ was greater when assayed by [K+]10–100 shifts than [K+]100-1,000 shifts (Fig. 6, A vs. B). The same trend was observed in akt1 seedling growth rate: Na+ more than doubled the growth rate at 10 µM K+, but was without effect when [K+]ext was 100 µM (Fig. 7, A vs. B). Perhaps the non-AKT1 mechanism is more Na+ coupled when the electrochemical potential gradient for K+ is great, but less so when the energetics permit a passive mode of operation. Previous work has attributed a passive conductance to HKT1 that is separate from its Na+-K+ symport activity (Gassmann et al., 1996), indicating that cotransporters can display such complexity of mechanism. Also, the growth rate of seedlings was limited by something other than K+ at concentrations above 100 µM (Fig. 5), so Na+ may have stimulated K+ uptake from 100-µM solutions, but limitations in some other factor prevented growth rate from responding.
Another possible contributor to the non-AKT1 transport activity is one or more of the KUP family of K+ transporters recently identified in Arabidopsis and barley. These transporters can complement K+-uptake deficiencies in mutants of Escherichia coli and yeast and can confer enhanced K+ uptake into cultured Arabidopsis cells when overexpressed (Quintero and Blatt, 1997; Santa-Maria et al., 1997; Fu and Luan, 1998; Kim et al., 1998). A member of this family from barley is inhibited by NH4+, similar to the non-AKT1 activity studied here in planta (Santa-Maria et al., 1997). Arabidopsis KUP-mediated K+ transport is also inhibited by NH4+ (E. Kim and J.I. Schroeder, personal communication), though it is not stimulated by Na+ (Fu and Luan, 1998). Thus, the Na+ data (Figs. 6 and 7) currently favor HKT1, while the NH4+ data (Figs. 1–5) favor KUP as the molecule(s) responsible for the non-AKT1 component of the root K+-uptake apparatus. It is also possible that the non-AKT1 activity is due to a combination of KUP and HKT1 activities insofar as both are inhibited by NH4+.
The last point to make is that the competition between NH4+ and K+ for a binding site on the non-AKT1 transporter (Figs. 2–5) explains the previously observed inhibition of K+ transport by NH4+ in corn roots (Vale et al., 1987). The fact that plants have a specific NH4+ transporter that is not blocked by K+ (Ninneman et al., 1994) explains why the converse (block of NH4+ uptake by K+) is typically not observed. Thus, the result that surprised Marschner (1995) receives a molecular-level explanation as a result of the present work.
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Submitted: 20 January 1999
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G. Desbrosses, C. Josefsson, S. Rigas, P. Hatzopoulos, and L. Dolan AKT1 and TRH1 are required during root hair elongation in Arabidopsis J. Exp. Bot., February 1, 2003; 54(383): 781 - 788. [Abstract] [Full Text] [PDF]
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M. A. Banuelos, B. Garciadeblas, B. Cubero, and A. Rodriguez-Navarro Inventory and Functional Characterization of the HAK Potassium Transporters of Rice Plant Physiology, October 1, 2002; 130(2): 784 - 795. [Abstract] [Full Text] [PDF]
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H. Su, D. Golldack, C. Zhao, and H. J. Bohnert The Expression of HAK-Type K+ Transporters Is Regulated in Response to Salinity Stress in Common Ice Plant Plant Physiology, August 1, 2002; 129(4): 1482 - 1493. [Abstract] [Full Text] [PDF]
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R. Pratelli, B. Lacombe, L. Torregrosa, F. Gaymard, C. Romieu, J.-B. Thibaud, and H. Sentenac A Grapevine Gene Encoding a Guard Cell K+ Channel Displays Developmental Regulation in the Grapevine Berry Plant Physiology, February 1, 2002; 128(2): 564 - 577. [Abstract] [Full Text] [PDF]
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K. L. Dennison, W. R. Robertson, B. D. Lewis, R. E. Hirsch, M. R. Sussman, and E. P. Spalding Functions of AKT1 and AKT2 Potassium Channels Determined by Studies of Single and Double Mutants of Arabidopsis Plant Physiology, November 1, 2001; 127(3): 1012 - 1019. [Abstract] [Full Text] [PDF]
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A. Rus, S. Yokoi, A. Sharkhuu, M. Reddy, B.-h. Lee, T. K. Matsumoto, H. Koiwa, J.-K. Zhu, R. A. Bressan, and P. M. Hasegawa AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots PNAS, October 31, 2001; (2001) 241501798. [Abstract] [Full Text] [PDF]
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 N. Uozumi Escherichia coli as an expression system for K+ transport systems from plants Am J Physiol Cell Physiol, September 1, 2001; 281(3): C733 - C739. [Abstract] [Full Text] [PDF]
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 J. C. Cushman Osmoregulation in Plants: Implications for Agriculture Integr. Comp. Biol., August 1, 2001; 41(4): 758 - 769. [Abstract] [Full Text] [PDF]
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M. R. Broadley, A. J. Escobar-Gutierrez, H. C. Bowen, N. J. Willey, and P. J. White Influx and accumulation of Cs+ by the akt1 mutant of Arabidopsis thaliana (L.) Heynh. lacking a dominant K+ transport system J. Exp. Bot., April 15, 2001; 52(357): 839 - 844. [Abstract] [Full Text] [PDF]
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O. Borsani, J. Cuartero, J. A. Fernández, V. Valpuesta, and M. A. Botella Identification of Two Loci in Tomato Reveals Distinct Mechanisms for Salt Tolerance PLANT CELL, April 1, 2001; 13(4): 873 - 888. [Abstract] [Full Text]
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M. Tester and R. A. Leigh Partitioning of nutrient transport processes in roots J. Exp. Bot., March 1, 2001; 52(90001): 445 - 457. [Abstract] [Full Text]
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H. Su, D. Golldack, M. Katsuhara, C. Zhao, and H. J. Bohnert Expression and Stress-Dependent Induction of Potassium Channel Transcripts in the Common Ice Plant Plant Physiology, February 1, 2001; 125(2): 604 - 614. [Abstract] [Full Text]
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K. L. Dennison and E. P. Spalding Glutamate-Gated Calcium Fluxes in Arabidopsis Plant Physiology, December 1, 2000; 124(4): 1511 - 1514. [Full Text]
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N. Uozumi, E. J. Kim, F. Rubio, T. Yamaguchi, S. Muto, A. Tsuboi, E. P. Bakker, T. Nakamura, and J. I. Schroeder The Arabidopsis HKT1 Gene Homolog Mediates Inward Na+ Currents in Xenopus laevis Oocytes and Na+ Uptake in Saccharomyces cerevisiae Plant Physiology, April 1, 2000; 122(4): 1249 - 1260. [Abstract] [Full Text]
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P. H. Buschmann, R. Vaidyanathan, W. Gassmann, and J. I. Schroeder Enhancement of Na+ Uptake Currents, Time-Dependent Inward-Rectifying K+ Channel Currents, and K+ Channel Transcripts by K+ Starvation in Wheat Root Cells Plant Physiology, April 1, 2000; 122(4): 1387 - 1398. [Abstract] [Full Text]
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A. Rus, S. Yokoi, A. Sharkhuu, M. Reddy, B.-h. Lee, T. K. Matsumoto, H. Koiwa, J.-K. Zhu, R. A. Bressan, and P. M. Hasegawa AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots PNAS, November 20, 2001; 98(24): 14150 - 14155. [Abstract] [Full Text] [PDF]
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, wild-type; •, akt1.
