Journal of Experimental Botany

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Journal of Experimental Botany, Vol. 52, No. 357, pp. 839-844, April 15, 2001
© 2001 Oxford University Press

Original Papers

Influx and accumulation of Cs⁺ by the akt1 mutant of Arabidopsis thaliana (L.) Heynh. lacking a dominant K⁺ transport system

Martin R. Broadley^1,3, Abraham J. Escobar-Gutiérrez¹, Helen C. Bowen¹, Neil J. Willey² and Philip J. White¹

¹ Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK
² University of the West of England, Coldharbour Lane, Frenchay, Bristol BS16 1QY, UK

Received 14 June 2000; Accepted 9 November 2000

	Abstract

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An extensive literature reports that Cs⁺, an environmental contaminant, enters plant cells through K⁺ transport systems. Several recently identified plant K⁺ transport systems are permeable to Cs⁺. Permeation models indicate that most Cs⁺ uptake into plant roots under typical soil ionic conditions will be mediated by voltage-insensitive cation (VIC) channels in the plasma membrane and not by the inward rectifying K⁺ (KIR) channels implicated in plant K nutrition. Cation fluxes through KIR channels are blocked by Cs⁺. This paper tests directly the hypothesis that the dominant KIR channel in plant roots (AKT1) does not contribute significantly to Cs⁺ uptake by comparing Cs⁺ uptake into wild-type and the akt1 knockout mutant of Arabidopsis thaliana (L.) Heynh. Wild-type and akt1 plants were grown to comparable size and K⁺ content on agar containing 10 mM K⁺. Both Cs⁺ influx to roots of intact plants and Cs⁺ accumulation in roots and shoots were identical in wild-type and akt1 plants. These data indicate that AKT1 is unlikely to contribute significantly to Cs⁺ uptake by wild-type Arabidopsis from ‘single-salt’ solutions. The influx of Cs⁺ to roots of intact wild-type and akt1 plants was inhibited by 1 mM Ba²⁺, Ca²⁺ and La³⁺, but not by 10 µM Br-cAMP. This pharmacology resembles that of VIC channels and is consistent with the hypothesis that VIC channels mediate most Cs⁺ influx under ‘single-salt’ conditions.

Key words: Caesium (Cs), cation channel, potassium transport, phytoremediation.

	Introduction

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Caesium (Cs) is a Group I alkali metal with chemical properties similar to potassium (K). Concentrations of the naturally-occurring, stable isotope (¹³³Cs) can reach 25 µg g^-1 dry soil, corresponding to low micromolar Cs⁺ concentrations in soil solutions (reviewed by White and Broadley, 2000). There is no known role for Cs in plant nutrition. However, excessive Cs can be toxic to plants and the radioisotopes of Cs (¹³⁴Cs and ¹³⁷Cs) produced in nuclear reactors or during nuclear explosions pose a significant environmental risk due to their rapid incorporation into biological systems, emissions of harmful ß and radiation during decay and their relatively long half-lives. The soil concentrations of Cs radioisotopes are at least six orders of magnitude lower than those of ¹³³Cs.

Early physiological studies demonstrated that K⁺ and Cs⁺ competed for influx to plant roots and suggested that these cations entered root cells by the same molecular mechanism(s) (reviewed by White and Broadley, 2000). The molecular identity and/or electrophysiological signature of many K⁺ transporters expressed in the plasma membrane of root cells have been described (Gaymard et al., 1998; Czempinski et al., 1999; Schachtman and Liu, 1999; White and Broadley, 2000). The KUP/HAK gene family encode ‘high-affinity’ K⁺/H⁺ symporters capable of transporting Cs⁺ (Rubio et al., 2000) and inward-rectifying K⁺ (KIR), outward-rectifying K⁺ (KOR) and voltage-insensitive cation (VIC) channels are all permeable to Cs⁺ (White and Broadley, 2000).

Inward rectifying K⁺ channels open upon plasma membrane hyperpolarization and facilitate K⁺ influx to root cells (Schroeder et al., 1994; White, 1997). The major KIR channel expressed in roots of Arabidopsis thaliana appears to be AKT1 (Sentenac et al., 1992; Basset et al., 1995). This channel dominates the nutritional uptake of K⁺ in the presence of ammonium at external K⁺ concentrations ([K⁺]_ext) between 0.01 and 1 mM (Hirsch et al., 1998; Spalding et al., 1999) and its expression is unaffected by tissue or external K⁺ concentration (Bassett et al., 1995). It has been assumed that KIR also dominate Cs⁺ uptake at high external Cs⁺ concentrations ([Cs⁺]_ext), based on competition studies with K⁺ and the complex relationships between [Cs⁺]_ext and Cs⁺ uptake or cell membrane potential (Sacchi et al., 1997; Zhu et al., 2000). However, since [Cs⁺]_ext inhibits KIR (White and Broadley, 2000) this mechanism is unlikely to mediate significant Cs⁺ influx at high [Cs⁺]_ext. Permeation models predict that most of the Cs⁺ uptake into plant roots will be mediated by VIC channels supplemented by KUP-like H⁺/Cs⁺ symporters, rather than by KIR channels (White and Broadley, 2000). Such permeation models also suggest that Cs⁺ influx through VIC channels and KUP-like H⁺/Cs⁺ symporters can produce the characteristic ‘dual-isotherm’ relationship between Cs⁺ influx to excised roots and external Cs⁺ concentrations ([Cs⁺]_ext) below 200 µM demonstrated in classical kinetic studies (cf. Shaw and Bell, 1989).

This paper describes whole-plant experiments designed to evaluate the predictions of these models by testing the hypothesis that the dominant KIR channel in plant roots (AKT1) does not contribute significantly to Cs⁺ uptake from solutions containing only CsCl plus CaCl₂ (henceforth termed ‘single salt’ solutions). It was necessary to include CaCl₂ to maintain membrane integrity. However, this external Ca²⁺ concentration does not block cation influx through root KIR (White, 1997) and, although Ca²⁺ may reduce cation influx through VIC, this blockade is incomplete (White, 1999). Thus, the presence of CaCl₂ does not compromise the testing of the primary hypothesis.

	Materials and methods

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Plant material
Seeds of Arabidopsis thaliana (L.) Heynh., ecotype Wassilewskija (Ws), were washed in 70% (v/v) ethanol/water, rinsed in distilled water and surface-sterilized using NaOCl (1% active chlorine). Seeds were then rinsed in sterile, distilled water, and sown in unvented, polycarbonate culture boxes (Sigma-Aldrich, Dorset, UK). Seedlings were grown on perforated polycarbonate discs placed on 75 ml 0.8% (w/v) agar containing 1% (w/v) sucrose and a basal salt mix formulated according to half-strength Murashige and Skoog (Murashige and Skoog, 1962) medium with the exception that the K concentration ([K⁺]_ext) was varied between 0.001 and 20 mM through a balanced addition of KH₂PO₄ and KNO₃ or Ca²⁺ salts. This was termed half-strength MS agar. Seedlings of the wild type and a mutant lacking the K⁺ channel AKT1 (akt1; Hirsch et al., 1998) were grown on the same disc. Roots grew into the agar, but shoots remained on the opposite side of the disc. Boxes were placed in a growth room set to 24 °C, with 16 h light d^-1. Illumination was provided by a bank of 100 W 84 fluorescent tubes (Philips, Eindhoven, Netherlands) giving an intensity of 45 µmol photons m^-2 s^-1 at plant height. Tissue K content was determined by atomic emission spectroscopy by inductively coupled plasma (Jobin-Yvon JY-24 Atomic Emission Spectrophotometer; ICA, Middlesex, UK) on bulked and weighed material from batches of 10 plants 21 d after sowing. Plant weights and tissue K contents were determined in experiments performed on three separate occasions.

Caesium uptake into intact seedlings
For Cs⁺ uptake experiments, seedlings were grown for 14 d in polycarbonate boxes on perforated polycarbonate discs on half-strength MS agar containing 10 mM K⁺. Seedlings were then transferred, still on polycarbonate discs, to a hydroponic system and grown for a further 3 d over 0.45 l aerated quarter-strength MS solution containing 1 mM K⁺. To assay Cs⁺ uptake, discs holding seedlings were placed over 0.45 l of aerated ‘single salt’ solution containing 0.5 mM CaCl₂ plus CsCl isotopically labelled with approximately 370 kBq ¹³⁴Cs l^-1. Three experiments were conducted: (1) to determine the time-course of Cs accumulation in plants grown for up to 48 h in solutions containing a [Cs⁺]_ext of 4 µM, (2) to determine the concentration dependence of Cs⁺ influx, measured over a 10 min period, across a range of [Cs⁺]_ext from 0.004 to 200 µM and (3) to determine the pharmacology of Cs⁺ influx from solutions, measured over a 20 min period containing a [Cs⁺]_ext of 40 µM. For the pharmacological study, 0.5 mM CaCl₂ was replaced by 1 mM LaCl₃, BaCl₂ or CaCl₂. Bromo-cyclicadenosinemonophosphate (Br-cAMP) was supplied at 10 µM.

The [Cs⁺]_ext did not deplete significantly during the course of any experiment (data not shown). Following ¹³⁴Cs⁺ uptake, seedlings were transferred to a fresh solution containing 1 mM CsCl and 0.5 mM CaCl₂ for 2 min to remove Cs⁺ from the cell wall. This was purely precautional as apoplastic binding effects were negligible (data not shown). Roots and shoots of individual plants were separated, blotted on filter paper and fresh weights recorded. Tissue Cs contents were estimated from ¹³⁴Cs activities determined by -emission over 300 s, using a well-type counter (LKB Wallac Compugamma, 1282, Helsinki, Finland). Three or four replicate plants were taken for each Arabidopsis genotype at each sampling point. All three experiments were repeated on three separate occasions. Analyses of variance were performed using Genstat 5 (Genstat 5 Committee, 1997).

	Results

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These experiments were designed to test directly the hypothesis that Cs⁺ does not enter Arabidopsis roots through AKT1 K⁺ channels, the dominant K⁺ uptake system, by comparing Cs⁺ uptake into wild-type and the akt1 knockout mutant. Since plant growth rate and tissue K⁺ content may affect the uptake of monovalent cations (Kochian and Lucas, 1988), it was first necessary to determine growth conditions suitable for producing plants of equivalent morphology and tissue K⁺ content. Wild-type and akt1 plants were grown in half-strength MS agar containing [K⁺]_ext from 0.001 to 20 mM (Fig. 1). Shoot fresh weight and shoot K content differed between genotypes over these [K⁺]_ext. Below 10 mM [K⁺]_ext, shoot fresh weight and K content were lower in akt1 than in wild-type Arabidopsis. This is consistent with previous reports that the akt1 phenotype of reduced growth compared to wild-type Arabidopsis is displayed at [K⁺]_ext below 1 mM (Hirsch et al., 1998). It is noteworthy (i) that the akt1 phenotype appears to require to be present in the extracellular media (Spalding et al., 1999), and here was used as an N source, and (ii) that the expression of AKT1 is not affected by [K⁺]_ext (Basset et al., 1995). When grown at 10 mM [K⁺]_ext there was uniformity between genotypes, including similar shoot weight, tissue K⁺ content (Fig. 1A) and root:shoot biomass allocation (Fig. 2). Thus, growing plants at 10 mM [K⁺]_ext provided suitable comparative material on which to test these hypotheses concerning the molecular mechanism of Cs⁺ uptake by plants.

View larger version (16K): [in this window] [in a new window]   Fig. 1. The effect of K supply on (A) shoot fresh weight and (B) shoot K content in wild-type (•) and akt1 () Arabidopsis thaliana. Least significant difference between wild-type and akt1 is indicated by the bar (d.f.=22; n=3; P=0.05). Plants were grown on 0.8% (w/v) agar containing 1% (w/v) sucrose and a basal salt mix formulated according to half-strength MS medium (Murashige and Skoog, 1962) with the K+ concentrations indicated.

 

View larger version (19K): [in this window] [in a new window]   Fig. 2. (A) Shoot and root fresh weight of wild-type (n=25) and akt1 (n=23) Arabidopsis thaliana grown for 14 d on half-strength MS agar containing 10 mM K+, then grown hydroponically for a further 3 d on quarter-strength MS medium containing 1 mM K+. (B) Time-course of Cs+ accumulation from a ‘single salt’ solution containing 4 µM CsCl plus 0.5 mM CaCl2 in the shoots and roots of wild-type (•) and akt1 () Arabidopsis thaliana. Data are expressed as mean±SEM.

 
The time-course of Cs⁺ accumulation in shoots and roots of plants exposed to solutions containing 0.5 mM CaCl₂ plus 4 µM CsCl was almost identical in wild-type and akt1 Arabidopsis (Fig. 2B). Further, there was no difference in Cs⁺ influx to roots (measured over a 10 min period) of intact wild-type or akt1 Arabidopsis across five orders of magnitude of [Cs⁺]_ext (Fig. 3A). These data indicate that the AKT1 channel is unlikely to contribute to Cs⁺ uptake by wild-type Arabidopsis under these ionic conditions. The influx of Cs⁺ into roots of intact plants showed a non-Michaelian dependence on [Cs⁺]_ext. However, a Hofstee transformation of the combined data from wild-type and akt1 Arabidopsis can be fitted by a double Michaelis-Menten function y=V_max1x/(K_m1+x)+V_max2x/(K_m2+x), where V_max1=16.98 µmol g^-1 f. wt root h^-1, K_m1=2607 µM, V_max2=0.0523µmolg^-1f.wtrooth^-1, K_m2=0.6864 µM (R²=>0.99; P<0.0001; Fig. 3B).

View larger version (16K): [in this window] [in a new window]   Fig. 3. (A) Influx of Cs+, measured over 10 min, to roots of intact wild-type (•) and akt1 () Arabidopsis thaliana from ‘single salt’ solutions containing 0.5 mM CaCl2 plus CsCl at the concentrations indicated (n=3; data expressed as mean±SEM). Plants were grown as described in the legend to Fig. 2. (B) Hofstee transformation of combined data for Cs+ influx to roots of intact wild-type and akt1 plants shown in panel A (n=6; data expressed as mean±SEM). The untransformed data from both genotypes were fitted to a double Michaelis-Menten function y=Vmax1x/(Km1+x)+Vmax2x/(Km2+x), where Vmax1=16.98 µmol g-1 f. wt root h-1, Km1=2607 µM, Vmax2=0.0523 µmol g-1 f. wt root h-1, Km2=0.6864 µM (R2=>0.99; P<0.0001). Curve fitting was performed in SigmaPlot for Windows, Version 4 (SPSS Inc.).

 
An indication of the dominant mechanism for Cs⁺ influx to roots is given by a comparison of the pharmacology of Cs⁺ influx to roots of wild-type and akt1 plants. The inorganic cations Ba²⁺, Ca²⁺ and La³⁺ are diagnostic inhibitors of VIC channels at millimolar concentrations (White, 1999; Davenport and Tester, 2000), whilst Br-cAMP modulates the activity of voltage-independent, cyclic nucleotide-gated channels at micromolar concentrations (Davenport and Tester, 2000; White and Broadley, 2000). There were no significant differences in the sensitivity of Cs⁺ influx to roots of wild-type and akt1 plants to inhibition by Ba²⁺, Ca²⁺, La³⁺ or Br-cAMP. The combined data from wild-type and akt1 plants indicated that the presence of 1 mM Ba²⁺ or Ca²⁺ significantly reduced Cs⁺ influx to roots of intact plants (Fig. 4). In addition, although neither 1 mM La³⁺ nor 10 µM Br-cAMP had a significant effect, there was an indication that the presence of 1 mM La³⁺ inhibited Cs⁺ influx to roots of intact plants (Fig. 4). Since this pharmacology is similar to that of VIC channels (White, 1999; Davenport and Tester, 2000), it supports the conclusion from modelling studies that VIC channels mediate the majority of Cs⁺ influx to root cells.

View larger version (38K): [in this window] [in a new window]   Fig. 4. The effect of pharmaceuticals on the influx of Cs+, measured over 20 min., to roots of intact Arabidopsis thaliana from ‘single salt’ solutions containing 40 µM CsCl, or 40 µM CsCl plus 10 µM bromo-cAMP, 1 mM LaCl3, 1 mM BaCl2 or 1 mM CaCl2. Bars represent means of combined data for Cs+ influx to roots of both intact wild-type and akt1 plants. Statistically indistinguishable values are indicated by the same letter (n=18; P=0.05). Plants were grown as described in the legend to Fig. 2.

 

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
The characterization of specific mutants has proved useful in the dissection of many biochemical, physiological and developmental processes. Arabidopsis mutants obtained by reverse genetic approaches (akt1, skor) and through screens of tolerance to caesium (Sheahan et al., 1993; Maathuis and Sanders, 1996) and sodium (Saleki et al., 1993; Werner and Finkelstein, 1995; Zhu et al., 1998) have been used to elucidate the physiological roles of specific transporters and to dissect the processes controlling monovalent cation transport within the plant. Thus, the AKT1 channel has been implicated in nutritional K⁺ uptake (Hirsch et al., 1998) and SKOR in loading K⁺ into the xylem (Gaymard et al., 1998). Here, the akt1 mutant has further been used to investigate the mechanism(s) of Cs⁺ uptake.

The influx and accumulation of Cs⁺ from ‘single salt’ solutions were identical in wild-type and akt1 Arabidopsis of equivalent size and K⁺ content (Figs 2, 3). The simplest explanation for this observation is that negligible Cs⁺ entered plants through the AKT1 K⁺ channel from ‘single salt’ solutions, although perfect compensatory changes in the complement of Cs⁺ transporters in akt1 cannot be discounted. This result may be attributed to the voltage-dependent blockade of AKT1 by micromolar [Cs⁺]_ext (Bertl et al., 1997). Although it is theoretically possible for some Cs⁺ to enter root cells through KIR channels in plants grown agriculturally, since the inhibition of KIR channels by [Cs⁺ ]_ext can be alleviated by increasing [K⁺]_ext, there would appear to be appreciable inhibition of KIR channels at the prevalent K⁺ and ¹³³Cs⁺ concentrations in many soil solutions (White and Broadley, 2000).

The influx of Cs⁺ to roots of intact Arabidopsis from ‘single salt’ solutions was inhibited by millimolar Ba²⁺, Ca²⁺ and La³⁺, but not by 10 µM Br-cAMP, in the assay solution (Fig. 4). This is consistent with previous studies reporting that Cs⁺ uptake into plant roots is partially inhibited by millimolar concentrations of divalent cations, with an apparent effectiveness of Ba²⁺> Mg²⁺Ca²⁺ (Bange and Overstreet, 1960; Handley and Overstreet, 1961; Sze and Hodges, 1977). This pharmacology also matches that of VIC channels in the plasma membrane of root cells (White, 1999; Davenport and Tester, 2000). Thus, the pharmacological profile for inhibition of Cs⁺ influx to roots of intact plants is consistent with the conclusions from the modelling studies performed earlier (White and Broadley, 2000), namely, that VIC channels will mediate most of the Cs⁺ influx to roots from ‘single salt’ solutions. Indeed, due to only partial inhibition of VIC channels by [Ca²⁺]_ext, it is also likely that VIC channels will catalyse most Cs⁺ influx to roots under typical soil ionic conditions.

The characteristics of Cs⁺ uptake by the roots will influence the potential of plants for phytoextraction or cultivation on land contaminated by radioisotopes of Cs (White and Broadley, 2000). More Cs⁺ might be removed from the soil solution by rendering KIR less sensitive to [Cs⁺]_ext blockade. There are two ways by which this might be achieved. First, since the sensitivity of root KIR channels to inhibition by Cs⁺ is reduced by increasing [K⁺]_ext (Bregante et al., 1997), the application of K⁺ fertilizer might enable plants to take up more Cs⁺ through KIR. However, since [K⁺]_ext will impact on Cs⁺ influx through other Cs⁺ transporters (White and Broadley, 2000) and also on Cs⁺ dynamics in the soil, such a strategy will have complex consequences for Cs⁺ uptake by plants. Second, allelic variation in KIR channel proteins might be sought. Both the sensitivity to inhibition by Cs⁺ and the cation selectivity of plant KIR appear to be encoded by a region of the protein termed the P domain, which forms part of the channel pore. Mutational studies of KAT1, a KIR channel expressed in guard cells, have identified residues that alter its sensitivity to inhibition by Cs⁺ and/or its Cs⁺ permeability (Hoth et al., 1997; Ichida et al., 1999). Thus, molecular biological approaches to modulate KIR-mediated Cs⁺ influx to root cells appear feasible. Since VIC channels could mediate most Cs⁺ influx to root cells under natural conditions, the entry of radioactive Cs⁺ into the food chain might be restricted by down-regulation of VIC channel activities. Alternatively, as has been suggested by White and Broadley (White and Broadley, 2000), down-regulating stelar KOR channels might specifically restrict Cs⁺ movement to the shoot. The latter hypothesis could be tested directly using the skor Arabidopsis knockout mutant.

	Acknowledgments

 
We thank Dr RE Hirsch and Professor MR Sussman for providing the akt1 Arabidopsis mutant, Dr IG Burns (HRI) for comments on the manuscript, Ms J Brown and Ms Jenny Powell (UWE) for radio-analytical support. This work was supported by the UK Biotechnology and Biological Sciences Research Council and the UK Ministry of Agriculture, Fisheries and Food.

	Notes

 
³ To whom correspondence should be addressed. Fax: +44 1789 470552. martin.broadley{at}hri.ac.uk

	Abbreviations

 
Br-cAMP, bromocyclicadenosinemonophosphate; [Cs⁺]_ext, external Cs⁺concentration; [K⁺]_ext, external K⁺concentration; KIR, inward-rectifying K⁺; KOR, outward-rectifying K⁺; MS, Murashige and Skoog; VIC, voltage-insensitive cation..

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